United Nations
Environment Programme
United States
Environmental Protection
Agency
October 1986
&EFK
EFFECTS OF CHANGES IN STRATOSPHERIC
OZONE AND GLOBAL CLIMATE
Volume 2: Stratospheric Ozone
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Library of Congress Cataloging - in - Publication Data
Effects of changes in stratospheric ozone and global climate.
Proceedings of a conference convened by the United Nations Environment
Programme and the U.S. Environmental Protection Agency.
Contents: v. 1. Overview — v. 2. Stratospheric ozone — v. 3. Climate
change. — v. 4. Sea level rise
1. Atmospheric ozone—Reduction—Congresses. 2. Stratosphere—Con-
gresses. 3. Global temperature changes—Congresses; 4. Climatic
changes—Congresses. 5. Sea level—Congresses. 6. Greenhouse effect,
Atmospheric—Congresses. 7. Ultraviolet radiation—Congresses.
I. Titus, James G. II. United States Environmental Protection Agency.
III. United Nations Environment Programme.
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EFFECTS OF CHANGES IN STRATOSPHERIC
OZONE AND GLOBAL CLIMATE
Volume 2: Stratospheric Ozone
Edited by
James G. Titus
U.S. Environmental Protection Agency
This report represents the proceedings of the INTERNATIONAL CON-
FERENCE ON HEALTH AND ENVIRONMENTAL EFFECTS OF
OZONE MODIFICATION AND CLIMATE CHANGE sponsored by the
United Nations Environment Programme and the U.S. Environmental
Protection Agency. The purpose of the conference was to make available
the widest possible set of views. Accordingly, the views expressed herein
are solely those of the authors and do not represent official positions of
either agency. Mention of trade names or commercial products does not
constitute endorsement or recommendation for use.
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PREFACE
This document is part of a four volume report that examines the possible
consequences of projected changes in stratospheric ozone and global climate
resulting from emissions of chlorofluorocarbons, carbon dioxide, methane, and
other gases released by human activities. In June 1986, the United Nations
Environment Programme and the U. S. Environmental Protection Agency sponsored
an International Conference on the Health and Environmental Effects of Ozone
Modification and Climate Change, which was attended by scientists and
officials, representing twenty-one countries from all areas of the world.
This volume examines the possible effects of ozone depletion. Volume 1
of the proceedings provides an overview of the issues as well as the
introductory remarks and reactions from top officials of the United Nations
and the United States. Volumes 3 and 4 focus on the effects of the change in
climate and rise in sea level that might result from a global warming.
This report does not present the official views of either the U.S.
Environmental Protection Agency or the United Nations Environment Programme.
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TABLE OF CONTENTS
INTRODUCTION
Overview of the Effects of Changing the Atmosphere
James G. Titus and Stephen R. Seidel 3
HUMAN HEALTH
UVR Dose-Dependent Life Shortening in Mice
R. E. Davies and P. D. Forbes 23
An Estimation of Sunspot Induced Ozone Changes From a Sunburn
Ultraviolet Meter
Daniel S. Berger 27
Nonmelanoma Skin Cancer - UV-B Effects
Joseph Scotto 33
Immunomodulation by Ultraviolet Radiation: Prostaglandins Appear to be
Involved in the Molecular Mechanisms Responsible for UVR-Induced
Changes in Immune Function
R. A. Daynes, H. T. Chung,
B. Robertson, L. K. Roberts,
and W. E. Samlowski 63
Stratospheric Ozone Depletion: Immunologic Effects on Monocyte
Accessory Function in Humans
Craig A. Elmets, Jean Krutraann, Elizabeth Rich,
Hiroshi Fuj iwara, and Jerrold J. Ellner 87
Effects of UV-B on Infectious Disease
Suzanne Holmes Giannini 101
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Urocanic Acid: On Its Role in the Regulation of UVB-Induced
Systemic Immune Suppression
Edward C. De Fabo and Frances P. Noonan 113
Solar Wavelengths of Ultraviolet Light-Induced Cytoplasmic Damage
Glen B. Zamansky and lih-Nan Chou 119
Sunscreens Do Not Abrogate UV-Induced Suppression of Contact
Hypersensitivity
M. S. Fisher, J. M. Menter,
L. Tiller, and I. Willis 131
Sunlight and Malignant Melanoma in Western Australia
Bruce K. Armstrong 1 ij 1
Radiometry of Solar UV-B
A. Baqer and N. Kollias 157
The Role of Native Pigment in Providing Protection Against UV-B
Damage in Humans
N. Kollias and A. Baqer 173
Ozone Modification: Importance for Developing Countries in the
Tropical/Equatorial Region
Mohammad Ilyas 185
The Tan of Ultraviolet-B Summer
Petar Jovanovic 193
AQUATIC SYSTEMS
Effects of Enhanced UV-B Radiation on the Survival of Micro-Organisms
Donat-P. Haider 197
Is the Impact of UV-B Radiation on Marine Zooplankton of Any
Significance?
B. Thomson 203
An Estimate of the Role of Current Levels of Solar Ultraviolet
Radiation in Aquatic Ecosystems
John Calkins and Mary K. Blakefield 211
How Might Enhanced Levels of Solar UV-B Radiation Affect Marine
Ecosystems?
John R. Kelly 237
TERRESTRIAL PLANTS
The Potential Consequences of Ozone Depletion Upon Global Agriculture
Alan H. Teramura 255
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Inhibition of Photosynthetic Production in Plants by Ultraviolet
Radiation
L. 0. Bjorn, Janet F. Bornman, and Legasse Negash 263
MISCELLANEOUS
An Assessment of UV-B Radiation Effects on Polymer Materials:
A Technical and Economic Study
Anthony L. Andrady and Robert L. Horst, Jr 279
The Interaction of Photochemical Processes in the Stratosphere
and Troposphere
Gary Z. Whitten and Michael W. Gery 295
Tropospheric CHij/CO/NOx: The Next Fifty Years
Anne M. Thompson and Michael Kavanaugh 305
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INTRODUCTION
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Overview of the Effects of Changing the Atmosphere
James G. Titus and Stephen R. Seidel
Environmental Protection Agency
Washington, DC USA
INTRODUCTION
Society is conducting a global experiment on the earth's atmosphere.
Human activities are increasing the worldwide atmospheric concentrations of
chlorofluorocarbons, carbon dioxide, methane, and several other gases. A
growing body of scientific evidence suggests that if these trends continue,
stratospheric ozone may decline and global temperature may rise. Because the
ozone layer shields the earth's surface from damaging ultraviolet radiation
(UV) future depletion could increase the incidence of skin cancer and other
diseases, reduce crop yields, damage materials, and place additional stress on
aquatic plants and animals. A global warming from the "greenhouse effect"
could also threaten human health, crop yields, property, fish, and wildlife.
Precipitation and storm patterns could change, and the level of the oceans
could eventually rise.
To improve the world's understanding of these and other potential
implications of global atmospheric changes, the United Nations Environment
Programme (UNEP) and the U.S. Environmental Protection Agency (EPA) sponsored
an International Conference on the Health and Environmental Effects of Ozone
Modification and Climate Change during the week of June 16-20, 1986. The
conference brought together over three hundred researchers and policy makers
from approximately twenty nations. This four-volume report presents the
seventy-three papers that were delivered at the conference by over eighty
speakers, including two U.S. Senators, top officials from UNEP and EPA, some
of the leading scientists investigating the implications of atmospheric
change, and representatives from industry and environmental groups. Volume 1
presents a series of overview papers describing each of the major areas of
research on the effects of atmospheric change, as well as policy assessments
of these issues by well-known leaders in government, industry, and the
environmental community. Volumes 2, 3, and 4 present the more specialized
papers on the impacts of ozone modification, climate change, and sea level
rise, respectively, and provide some of the latest research in these areas.
This paper summarizes the entire four-volume report.
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OZONE MODIFICATION
Atmospheric Processes
The ozone in the upper part of the atmosphere—known as the strato-
sphere—is created by ultraviolet radiation. Oxygen (02) is continuously
converted to O2one (0^) and back to 02 by numerous photochemical reactions
that take place in the stratosphere, as Stordal and Isaksen (Volume 1)
describe. Chlorofluorocarbons and other gases released by human activities
could alter the current balance of creative and destructive processes.
Because CFCs are very stable compounds, they do not break up in the lower
atmosphere (known as the troposphere). Instead, they slowly migrate to the
stratosphere, where ultraviolet radiation breaks them down, releasing
chlorine.
Chlorine acts as a catalyst to destroy ozone; it promotes reactions that
destroy ozone without being consumed. A chlorine (Cl) atom reacts with ozone
(Oo) to form CIO and 02- The CIO later reacts with another 0? to form two
molecules of 02, which releases the chlorine atom. Thus, two molecules of
ozone are converted to three molecules of ordinary oxygen, and the chlorine is
once again free to start the process. A single chlorine atom can destroy
thousands of ozone molecules. Eventually, it returns to the troposphere,
where it is rained out as hydrochloric acid.
Stordal and Isaksen point out that CFCs are not the only gas released by
Human activities that might alter the ozone balance. Increasing
concentrations of methane in the troposphere increase the water vapor in the
stratosphere, which helps create ozone. Carbon dioxide and other greenhouse
gases (discussed below) warm the earth's surface but cool the upper
atmosphere; cooler stratospheric temperatures slow the process of ozone deple-
tion. Nitrous oxide (N20) reacts with both chlorine and ozone.
Stordal and Isakson present results of possible ozone depletion over
time, using their two-dimensional atmospheric-chemistry model. Unlike one-
dimensional models which provide changes in ozone in the global average, this
model calculates changes for specific latitutdes and seasons. The results
show that if concentrations of the relevant trace gases grow at recent levels,
global average ozone depletion by 2030 would be 6.5 percent. However,
countries in the higher latitudes (60°N) would experience 16 percent depletion
during spring. Even in the case of constant CFC emissions, where global
average depletion would be 2 percent by 2030, average depletion would be 8
percent in the high northern latitudes.
Watson (Volume 1) presents evidence that ozone has been changing recently
more than atmospheric models had predicted. As Plate 1 shows, the ozone over
Antarctica during the month of October appears to have declined over 40
percent in the last six to eight years. Watson also discusses observations
from ozone monitors that suggest a 2 to 3 percent worldwide reduction in ozone
in the upper portion of the stratosphere (thirty to forty kilometers above the
surface), which is consistent with model predictions. Finally, he presents
preliminary data showing a small decrease since 1978 in the total (column)
ozone worldwide. However, he strongly emphasizes that the data have not yet
been fully reviewed and that it is not possible to conclusively attribute
observed ozone depletion to the gases released by human activities. While
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there are several hypotheses to explain why ozone concentrations have
declined, none have been adequately established; nor did any of the
atmospheric models predict the measured loss of ozone over Antarctica.
Ultraviolet Radiation
Many of the chemical reactions investigated by atmospheric scientists
take place only in the stratosphere because they are caused by types of
radiation only found in the upper atmosphere. As Frederick (Volume 1)
explains, the sun emits radiation over a broad range of wavelengths, to which
the human eye responds in the region from approximately 400 to 700 nanometers
(nm). Wavelengths from 320 to MOO ran are known as UV-A; wavelengths from 280
to 320 nm are called UV-B, and wavelengths from 200 to 280 nm are known as
UV-C.
Frederick explains why attention has primarily focused on the UV-B part
of the spectrum. The atmosphere absorbs virtually all UV-C, and is expected
to continue to do so under all foreseeable circumstances. On the other hand,
UV-A is not absorbed by ozone.1. By contrast, UV-B is partially absorbed by
ozone, and future depletion would reduce the effectiveness of this shield.
We now examine the potential implications of such changes on human
health, plants, aquatic organisms, materials, and air pollution.
Effects on Human Health
The evidence suggests that solar ultraviolet radiation induces skin
cancer, cataracts, suppression of the human immune response system, and
(indirectly through immunosuppression) the development of some cutaneous
infections, such as herpes. Emmett (Volume 1) discusses the absorption of UV
radiation by human tissue and the mechanisms by which damage and repair may
occur.
Emmett also examines UV radiation as the cause of aging of the skin and
both basal and squamous skin cancers. In reviewing the role of UV radiation
in melanoma (the most frequently fatal skin cancer), he states that some
evidence suggests this link, but that currently there is no acceptable animal
model that can be used to explore or validate this relationship. He concludes
that future studies must focus on three major factors—exposure to solar
radiation, individual susceptibility, and personal behavior. Waxier (Volume
1) presents evidence of a link between UV-B exposure and cataracts.
Volume 2 presents specific research results and provides more detail on
many of the aspects covered in this volume. Scotto presents epidemiological
evidence linking solar radiation with skin cancers, other than melanoma. His
analysis suggests that Caucasians in the United States have a 12 to 30 percent
chance of developing these cancers within their lifetimes, even without ozone
depletion. Armstrong examines the role of UV-B exposure to melanoma in a
study of 511 matched melanoma patients and control subjects in Western
Australia. He shows that "intermittent exposure" to sunlight was closely
associated with this type of cancer.
1 However, 02 and N2 reflect some UV-A back to space,
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In a paper examining nonmelanoma skin cancer in Kuwait, Kollias and Baqer
(Volume 2) show that despite the presence of protective pigmentation, 75
percent of cancers occur on the 10 percent of the skin exposed to sunlight. A
second paper on skin cancer presents experimental evidence suggesting that the
mechanism by which skin cancer could occur involves disruption of the
cytoskeleton from exposure to UV-A and UV-B light (Zamansky and Chow,
Volume 2).
The pathways by which suppression of the immune response might be
triggered are explored in papers by DeFabo and Noonan, Daynes et al., and
Elmets et al (all Volume 2). Davies and Forbes (Volume 2) show that mice
exposed to UV-B radiation had a decrease in lifetime that was proportional to
the quantity of radiation and not directly related to the incidence of skin
cancer.
Possible implications of immune suppression of diseases and the
mechanisms by which it occurs are still uncertain. However, several papers in
Volume 2 suggest that in addition to skin cancer and contact hypersensitivity,
diseases influenced by UV-B induced immune suppression include leishmaniasis
and herpes infections. Fisher et. al (Volume 2) show that at least one
sunscreen effectively protects mice exposed to UV-B radiation from sunburn;
but it does not stop the immune suppression from interfering with a contact
hypersensitivity (allergic) reaction.
•Effects on Plants
The effects of increased exposure to UV-B radiation on plants has been a
primary area of research for nearly a decade. Teramura (Volume 1) reports
that of the two hundred plants tested for their sensitivity to UV-B radiation,
over two-thirds reacted adversely; peas, beans, squash, melons, and cabbage
appear to be the most sensitive. Given the complexities in this area of
research, he warns that these results may be misleading. For example, most
experiments have used growth chambers. Studies of plants in the field have
shown them to be less sensitive to UV-B. Moreover, different cultivars of the
same plant have shown very different degrees of sensitivity to UV-B
radiation. Finally, Teramura suggests that potential effects from multiple
stresses (e.g., UV-B exposure plus water stress or mineral deficiency) could
substantially alter a plant's response to changes in UV-B alone.
In Volume 2, Teramura draws extensively from the results of his five
years of field tests on soybeans. His data show that a 25 percent depletion
in ozone could result in a 20 to 25 percent reduction in soybean yield and
adverse impacts on the quality of that yield. Because soybeans are the fifth
largest crop in the world, a reduction in yields could have serious
consequences for world food supplies. However, some soybean cultivars appear
to be less susceptible to UV-B radiation, which suggests that selective crop
breeding might reduce future losses, if it does not increase vulnerability to
other environmental stresses.
BJorn (Volume 2) examines the mechanisms by which plant damage occurs.
His research relates specific wavelengths with those aspects of plant growth
that might be susceptible, including the destruction of chloroplast, DMA, or
enzymes necessary for photosynthesis.
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Aquatic Organisms
Aquatic plants would also be adversely affected by increased ultraviolet
radiation. Worrest (Volume 1) points out that most of these plants, which are
drifters (phytoplankton)f spend much of their time near the surface of the
water (the euphotic zone) and are therefore exposed to ultraviolet
radiation. A reduction in their productivities would be important because
these plants directly and indirectly provide the food for almost all fish.
Furthermore, the larvae of many fish found in the euphotic zone would be
directly affected, including crabs, shrimp, and anchovies. Worrest points out
that fish account for 18 percent of the animal protein that people around the
world consume, and 40 percent of the protein consumed in Asia.
An important question is the extent to which current UV-B levels are a
constraint on aquatic organisms. Calkins and Blakefield (Volume 2) conclude
that some species are already exposed to as much UV-B as they can tolerate.
Thomson (Volume 2) shows that a 10 percent decrease in ozone could increase
the number of abnormal larvae as much as 18 percent. In a study of anchovies,
a 20 percent increase in UV-B radiation over a 15-day period caused the loss
of all the larvae within a 10-meter mixed layer in April and August.
Many other factors could affect the magnitude of the impacts on specific
species, ecosystems, and the food chain. An important mechanism by which
species could adapt to higher UV-B incidence would be to reduce their exposure
by moving further away from the water's surface during certain times of the
day or year when exposure is greatest. Haeder (Volume 2) suggestst however,
that for certain species such avoidance may be impaired by UV-B radiation.
Even for those organisms that could move to avoid exposure, unwanted
consequences may result. Calkins and Blakefield present model results showing
that movement by phytoplankton away from sunlight to reduce exposure to a 10
percent increase in UV-B would result in a 2.5 to 5 percent decrease in
exposure to the photosynthetically active radiation on which their growth
depends. Increased movement requires additional energy consumption, while
changes in location may affect the availability of food for zooplankton, which
could cause other changes in shifts in the aquatic food chain.
To a certain extent, losses within a particular species of plankton may
be compensated by gains in other species. Although it is possible that no net
change in productivity will occur, questions arise concerning the ecological
impacts on species diversity and community composition (Kelly, Volume 1).
Reductions in diversity may make populations more susceptible to changes in
water temperatures, nutrient availability, diseases, or pollution. Changes in
community composition could alter the protein content, dry weight, or overall
food value of the initial stages of the aquatic food chain.
Polymer Degradation and Urban Smog
Current sunlight can cause paints to fade, transparent window glazing to
yellow, and polymer automobile roofs to become chalky. These changes are
likely to occur more in places closer to the equator where UV-B radiation is
greater. They are all examples of degradation that could accelerate if
depletion of the ozone layer occurs. Andrady and Horst (Volume 2) present a
case study of the potential magnitude of loss due to increased exposure to
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UV-B radiation on polyvinyl chloride (PVC). This chemical is used in outdoor
applications where exposure to solar radiation occurs over a prolonged
period. It is also used in the construction industry in siding and window
frames and as a roofing membrane.
To analyze the potential economic impact of future ozone depletion on
PVC, the authors assumed that the future service life of polymers would be
maintained by increasing the quantity of light stabilizers (titanuim dioxide)
used in the product. As a result, the costs associated with increased UV-B
radiation would be roughly equal to the costs of increased stablizers.
Preliminary results show that for a 26 percent depletion by 2075, the
undiscounted costs would be $4.7 billion (1984 dollars).
Increased penetration of UV-B radiation to the earth's surface could play
an important role in the formation of ground level oxidants (smog). UV-B
affects smog formation through the photolysis of formaldehyde, from which
radicals are the main source for deriving chain reactions that generate
photochemical smog. Whitten and Gery (Volume 2) analyze the relationship
between UV-B, smog, and warmer temperatures. The results of this preliminary
study of Nashville, Philadelphia, and Los Angeles show that large depletions
in stratospheric ozone and increases in temperature would increase smog by as
much as 50 percent. In addition, because oxidants would form earlier in the
day and closer to population centers (where emissions occur), risks from
exposure could increase by an even higher percentage increase. Whitten and
Gery also report a sensitive relationship between UV-B and hydrogen peroxide,
an oxidant and precursor to acid rain.
CLIMATE CHANGE
The Greenhouse Effect
Concern about a possible global warming focuses largely on the same gases
that may modify the stratospheric ozone: carbon dioxide, methane, CFCs, and
nitrous oxide. The report of a recent conference convened by UNEP, the World
Meteorological Organization, and the International Council of Scientific
Unions concluded that if current trends in the emissions of these gases
continue, the earth could warm a few degrees (C) in the next fifty years
(Villach 1985). In the next century, the planet could warm as much as five
degrees (NAS 1983), which would leave the planet warmer than at any time in
the last two million years.
A planet's temperature is determined primarily by the amount of sunlight
it receives, the amount of sunlight it reflects, and the extent to which the
atmosphere retains heat. When sunlight strikes the earth, it warms the
surface, which then reradiates the heat as infrared radiation. However, water
vapor, COp, and other gases in the atmosphere absorb some of the energy rather
than allowing it to pass undeterred through the atmosphere to space. Because
the atmosphere traps heat and warms the earth in a manner somewhat analogous
to the glass panels of a greenhouse, this phenomenon is commonly known as the
"greenhouse effect." Without the greenhouse effect of the gases that occur
naturally in the atmosphere, the earth would be approximately 33°C colder than
it is currently (Hansen et al. 1984).
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In recent decades, the concentrations of greenhouse gases have been
increasing. Since the beginning of the industrial revolution, the combustion
of fossil fuels, deforestation, and a few other activities have released
enough C02 to raise atmospheric concentrations by 20 percent; concentrations
have risen 8 percent since 1958 (Keeling, Bacastow, and Whorf 1982). More
recently, Ramanathan et al. (1985) examined the greenhouse gases other than
C02 (such as methane, CFCs, and nitrous oxide), and concluded that these other
gases are likely to double the warming caused by C02 alone. Using these
results, the Villach Conference estimated that an "effective doubling" of C02
is likely by 2030.2
Hansen et al. (Volume 1) and Manabe & Wetherald (Volume 1) present the
results that their climate models predict for an effective doubling of C02.
Both models consider a number of "climatic feedbacks" that could alter the
warming that would directly result from C02 and other gases released by human
activities. Warmer temperatures would allow the atmosphere to retain more
water vapor, which is also a greenhouse gas, thereby resulting in additional
warming. Ice and snow cover would retreat, causing sunlight that is now
reflected by these bright surfaces to be absorbed instead, causing additional
warming. Finally, a change in cloud cover might result, which could increase
or decrease the projected warming. Although the two models differ in many
ways, both conclude that an effective doubling of greenhouse gases would warm
the earth's surface between two and four degrees (C).
Hansen et al. project the doubling to occur between 2020 and 2060. They
also provide estimates of the implications of temperature changes for
Washington, D.C., and seven other U.S. cities for the middle of the next
century. For example, Washington would have 12 and 85 days per year above
38°C (100°F) and 32°C (90°F), respectively, compared with 1 and 35 days above
those levels today. While evenings in which the thermometer fails to go below
27°C (808F) occur less than once per year today in that -city, they project
that such evenings would occur 19 times per year. (See Plates 2 and 3 for
worldwide maps of historical and projected temperature changes.)
Water Resources
Manabe and Wetherald (Volume 1) focus on the potential changes in
precipitation patterns that might result from the greenhouse warming. They
project substantial increases in .summer dryness at the middle latitudes that
currently support most of the world's agriculture. Their model also projects
increased rainfall for late winter.
Beran (Volume 1) reviews the literature on the hydrological and water
resource impacts of climate change. He expresses some surprise that only
twenty-one papers could be found that address future water resource impacts.
One of the problems, he notes, is that there is a better scientific
understanding of how global average temperatures and rainfall might change,
than for the changes that specific regions may experience. Nevertheless, he
Studies on the greenhouse effect generally discuss the impacts of a carbon
dioxide doubling. By "effective doubling" we refer to any combination of
increases in concentrations of the various gases that causes a warming equal
to the warming of a doubling of carbon dioxide alone.
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demonstrates that useful Information can be extracted by studying the
implications of particular scenarios.
Nicholson (Volume 3) shows how historical changes in water availability
have caused problems for society in the past. The best lesson of climatic
history, she writes, "is that agricultural and economic systems must be
flexible enough to adapt to changing conditions and, in the face of potential
water scarcity, systems must be designed that require minimum use of
resources." Wilhite (Volume 3) examines drought policies in Australia and the
United States, concluding that the lack of national drought plans could
substantially impair the ability of these two nations to successfully adapt to
hydrologic changes resulting from the greenhouse warming.
Cohen (Volume 3) examines the potential implications of the global
warming for water levels in the Great Lakes that separate Canada from the
United States. Using results from the models of both Hansen et al. and Manabe
& Wetherald, he concludes that lake levels could drop 10 to 30 centimeters.
This drop would significantly reduce the capacity of ocean-going vessels that
enter the Great Lakes. On the other hand, such a drop might be viewed as a
benefit by the owners of critically eroding property whose homes are currently
threatened by historically high lake levels. Street-Perrott et al. (Volume 3)
discuss the historic impacts of changes in climate on the levels of lakes in
North America, South America, Australia, and Africa.
Gleick (Volume 3) uses scenarios from the Hansen et al. and Manabe &
Wetherald models (as well as a third developed by the National Center for
Atmospheric Research) to drive a water-balance model of the Sacramento Basin
in California. He finds that reductions in runoff could occur even in months
where precipitation increases substantially, because of the increased rates of
evaporation that take place at higher temperatures. He also points out that
the models predict that changes in monthly runoff patterns will be far more
dramatic than changes in annual averages. For seven of ten scenarios, soil
moisture would be reduced every month of the year; for the other three cases,
slight increases in moisture are projected for winter months. Mather (Volume
3) conducts a detailed analysis for southern Texas and northern Mexico;
examines in less detail twelve regions around the world; and projects shifts
in global vegetation zones.
Agriculture and Forestry
The greenhouse warming could affect agriculture by altering water
availability, length of growing season, and the number of extremely hot
days. Increased CO, concentrations could also have two direct impacts
unrelated to climate change: At least the laboratory, plants grow faster (the
COp fertilization effect) and retain moisture more efficiently. The extent to
which these beneficial effects offset the impacts of climate change will
depend on the extent to which global warming is caused by C02 as opposed to
other greenhouse gases, which do not have these positive impacts.
Parry (Volume 1) provides an overview of the potential impacts of climate
change on agriculture and forestry. He points out that commercial farmers
plan according to the average year, while family and subsistence farmers must
ensure that even in the worst years they can make ends meet. Thus, the
commercial farmer would be concerned about the impact of future climate change
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on average conditions and average yields, while farmers at the margin would be
most concerned with changes in the probability of (for example) a severe
drought that causes complete crop failure. Parry notes that the probability
of two or more anomalous years in a row could create disproportionately
greater problems for agriculture. For example, a persistent drought in the
U.S. Great Plains from 1932 to 1937 contributed to about two hundred thousand
farm bankruptcies.
Parry discusses a number of historical changes in climate. The Little
Ice Age in western Europe (1500-1800 A.D.) resulted in the abandonment of
about half the farms in Norway, an end to cultivation of cereals in .Iceland,
and some farmland in Scotland being permanently covered with snow. Concerning
the late medieval cooling (1250-1500) he writes: "The failure to adapt to the
changing circumstances is believed to explain much of the Norse decline. The
Norse continued to emphasize stock-raising in the face of reduced capacity of
the already limited pastures. The option of exploiting the rich seas around
them, as the Inuit (Eskimos) successfully did, was not taken up ... This is
an extreme example of how governments can fail to identify and implement
appropriate policies of response." It also suggests that effective responses
can reduce damages from climate change.
The paper reviews a number of studies that project impacts of climate
change on agriculture. "Warming appears to be detrimental to cereals in the
core wheat-growing areas of North America and Europe." If no precipitation
changes take place, a one-degree warming would decrease yields 1 to 9 percent
while a two-degree (C) warming would decrease yields 3 to 17 percent. Parry
also discusses how particular crop zones might shift. A doubling of C02 would
substantially expand the wheat-growing area in Canada due to higher winter
temperatures and increased rainfall. In Mexico, however, temperature stresses
would increase, thereby reducing yields.
A number of studies have been conducted using the models of Hansen et
al., Manabe & Wetherald, and others. Although these projections cannot be
viewed as reliable forecasts, they do provide consistent scenarios that can be
useful for examining vulnerability to climate change. Parry indicates that
investigations of Canada, Finland, and the northern USSR using the model by
Hansen et al. show reduced yields of spring-sown crops such as wheat, barley,
and oats, due to increased moisture stress early in the growing period.
However, switching to winter wheat or winter rye might reduce this stress.
Parry goes on to outline numerous measures by which farmers might adapt to
projected climate change.
Waggoner (Volume 3) points out that the global warming would not affect
plants uniformly. Some are more drought-resistant than others, and some
respond to higher C02 concentrations more vigorously than others. Co plants,
such as wheat, respond to increased, C02 more than C^ plants such as maize.
Thus, the COp fertilization effect woulbf not help the farmer growing Cn crops
accompanied By Co weeds. Waggoner also examines the impact of future climate
change on average crop yields and pests, and the probability of successive
drought years. He concludes that although projections of future changes are
useful, historical evidence suggests that surprises may be in store, and that
"agricultural scientists will be expected to aid rather than watch mankind's
adaptation to an inexorable increase in C02 and its greenhouse effect."
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The impact of future climate change on yields for spring wheat in
Saskatchewan, Canada, is the subject of the paper by Stewart (Volume 3).
Using the output from the Hansen et al. model (Volume 1), which projects that
the effective doubling of carbon dioxide would increase average annual
temperatures in that region by 4.7°C, he estimates that the growing season
would start two or three weeks earlier and end three or four weeks later.
Although average precipitation during the growing season would increase, he
also finds that the area would become more prone to drought. The impact of
climatic change would be to reduce yields 16 to 26 percent. Stewart estimates
that the fertilization effect of a CC^ doubling would reduce the losses to 6
to 15 percent. Cooter (Volume 3) examines the economic impact of projected
climate change on the economy of Oklahoma, concluding that the Gross State
Product would decline 75 to 300 million dollars. (The state's gross product
in 1985 was approximately 50 billion dollars.)
Fritts (Volume 3) examines tree rings to assess how past changes in
climate have affected forests, and concludes that tree rings are useful for
estimating past changes in climate. Solomon and West (Volume 3) discuss the
results of their efforts to model the future impacts. Considering the impact
of climate change caused by doubled C02 without the fertilization effect, they
find that "biomass (for boreal forests) declines for 50-75 years as warming
kills off large boreal forest species, before new northern hardwoods can grow
into the plot."
"Warming at the transition site causes an almost immediate response in
declining biomass from dieback of mature trees, and in decline of tree mass as
large trees die and are temporarily replaced by small young trees," they
write. "The deciduous forest site . . . results in permanent loss of dense
forest. One might expect the eventual appearance of subtropical forests
similar to those in Florida today, but the real difficulty is the moisture
balance (which is) more similar to those of treeless Texas today, than to
those of southern Florida." Solomon and West go on to show how the
fertilization effect from increased concentrations of COj could offset part
but not all of the drop in forest productivity.
Sea Level Rise
One of the most widely recognized consequences of a global warming would
be a rise in sea level. As Titus (Volume 1) notes, global temperatures and
sea level have fluctuated over periods of one hundred thousand years, with
temperatures during ice ages being three to five degrees (C) lower and sea
level over one hundred meters lower than today. By contrast, the last
interglacial period (one hundred thousand years ago) was one or two degrees
warmer than today, and sea level was five to seven meters higher.
The projected global warming could raise sea level by heating and thereby
expanding ocean water, melting mountain glaciers, and by causing polar
glaciers in Greenland and Antarctica to melt and possibly slide into the
oceans. Thomas (Volume 4) presents new calculations of the possible
contribution of Antarctica and combines them with previous estimates for the
other sources, projecting that a worldwide rise in sea level of 90 to 170
centimeters by the year 2100 with 110 centimeters most likely. However, he
also estimates that if the global warming is substantially delayed, the rise
in sea level could be cut in half. Such a delay might result either from
12
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actions to curtail emissions or from the thermal lag induced by the oceans'
ability to absorb heat.
On the other hand, Thomas also estimates that if a warming of four
degrees results from a C02 doubling (which the model of Hansen et al.
projects} and concentrations continue to grow after 2050, the rise could be as
great as 2.3 meters. He also notes that an irreversible deglaciation of the
West Antarctic Ice Sheet might begin in the next century, which would raise
sea level another six meters in the following centuries.
Titus (Volume 1) notes that these projections imply that sea level could
rise 30 centimeters by 2025, in addition to local subsidence trends that have
been important in Taipei, Taiwan; Venice, Italy; the Nile Delta, Egypt; and
most of the Atlantic and Gulf Coasts of the United States. The projected rise
in sea level would inundate low-lying areas, destroy coastal marshes and
swamps, erode shorelines, exacerbate coastal flooding, and increase the
salinity of rivers, bays, and aquifers.
Bruun (Volume 4) argues that with a combination of coastal engineering
and sound planning, society can meet the challenge of a rising sea. He
discusses a number of engineering options, including dikes (levees) and
seawalls, and adding sand to recreational beaches that are eroding, with a
section on the battle that the Dutch have fought with the sea for over one
thousand years. Goemans (Volume 4} describes the current approach of the
Dutch for defending the shoreline, and estimates that the cost of raising
their dikes for a one meter rise in sea level would be 10 billion guilders,
which is less than 0.05 percent of their Gross National Product for a single
year.
Goemans concludes that there is no need to anticipate such a rise because
they could keep up with it. However, he is more concerned, by the two-meter
scenario: "Almost immediately after detection, actions would be required. It
is not at all certain that decision-makers act that fast. . . . The present
flood protection strategy came about only after the tragic disaster of 1953.
When nobody can remember a specific disaster, it is extremely difficult to
obtain consensus on countermeasures." For his own country, Goemans sees one
positive impact: Referring to the unique experience of Dutch engineering
firms in the battle with the sea, he suggests that "a rising sea may provide a
new global market for this expertise." But he predicts that "the question of
compensation payments may come up," for the poorer countries who did not cause
climate change but must face its consequences.
Broadus et al. (Volume 4) examine two such countries in detail: Egypt
and Bangladesh. The inhabited areas of both countries are river deltas, where
low-lying land has been created by the sediment washing down major rivers. In
the case of Egypt, the damming of the Nile has interrupted the sediment, and
as the delta sinks, land is lost to the Mediterranean Sea. Broadus et al.
estimate that a 50-centimeter rise in global sea level, when combined with
subsidence and the loss of sediment, would result in the loss of 0.3 to 0.4
percent of the nation's land area; a 200-centimeter rise would flood 0.7
percent. However, because Egypt's population is concentrated in the low-lying
areas, 16 and 21 percent of the nation's population currently reside in the
areas that would be lost in the two scenarios.
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The situation would be even more severe in Bangladesh. As Plate 4 shows,
this nation, which is already overcrowded, would lose 12 to 28 percent of its
total area, which currently houses 9 to 27 percent of its population.
Moreover, floods could penetrate farther inland, which could leave the nation
more vulnerable to the type of tropical storm that killed 300,000 people in
the early 1970s, especially if the frequency of tropical storms doubled due to
warmer water temperatures, which deSylva (Volume 4) projects. Broadus et al.
conclude that the vulnerability of Bangladesh to a rise in sea level will
depend in large measure on whether future water projects disrupt land-creating
sediment washing down the Ganges.
Bird (Volume 4) examines the implications of sea level rise for other
African and Asian nations, as well as Australia. While holding back the sea
may be viable in Australia, he shows areas in New Guinea where people live in
small cottages on the water's edge on a barrier island that almost certainly
would be unable to justify construction of a dike. He also points to the
Philippines, where many people have literally "taken to the water," living in
small boats and maintaining fishing nets in their own plots of bay instead of
land. Current wetlands, he suggests, may convert to these shallow bays, with
people converting to a more water-based economy.
Leatherman (Volume 4) examines the implications of sea level rise for
South America. He notes that such popular resorts as Copacabana Beach,
Brazil; Punta del Este, Uruguay; and Mar del Plata, Argentina, are already
suffering serious erosion. He concludes that because of the economic
importance of resorts, governments will allocate the necessary "funds to
maintain their viability. However, he predicts that "coastal wetlands will
receive benign neglect" and be lost.
Park et al. (Volume 4) focus on the expected drowning of coastal wetlands
in the United States. Using a computer model of over 50 sites, they project
that 40-75 percent of existing U.S. coastal wetlands could be lost by 2100.
Although these losses could be reduced to 20-55 percent if new wetlands form
inland as sea level rises, the necessary wetland creation would require
existing developed areas to be vacated as sea level rises, even though
property owners would frequently prefer to construct bulkheads to protect
their property. Because coastal wetlands are important for many commerically
important seafood species, as well as birds and furbearing animals, Park et
al. conclude that even a one-meter rise in sea level would have major impacts
on the coastal environment.
DeSylva (Volume 4) also examines the environmental implications of sea
level rise, noting that in addition to wetlands being flooded, estuarine
salinity would increase. Because 66 to 90 percent of U.S. fisheries depend on
estuaries, he writes that these impacts could be important. He also suggests
that coral reefs could become vulnerable because of sea level rise, increased
temperatures, and the decrease in the pH (increased acidity) of the ocean.
Kuo (Volume 4) examines the implications of sea level rise for flooding
in Taipei, Taiwan, and coastal drainage in general. Although Taipei is
upstream from the sea, Kuo concludes that projected sea level rise would cause
serious problems, especially because Taiwan is also sinking. He recommends
that engineers around the world take "future sea level rise into consideration
... to avoid designing a system that may become prematurely obsolete."
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Gibbs (Volume 4) estimates that sea level rise could result in economic
damages in Charleston, South Carolina, equal to as much as 25 percent of the
annual product of the community. Anticipatory measures, however, could reduce
these impacts by half. Gibbs finds that in some areas actions should be taken
today, in spite of the current uncertainty regarding future rates of sea level
rise, while for other areas it would be more prudent to wait until uncertain-
ties are resolved.
Ken Smith, a realtor from coastal New Jersey, reacts to the other papers
presented in Volume 4. He argues that the issue of sea level rise should be
taken seriously today, but laments the fact that many of his fellow realtors
make comments such as "What do you care? You won't be around to see it!" and
the scientific community is "a bunch of eggheads who don't want us (to build
on the coast) anyway." Smith suggests that part of the resistance to taking
the issue seriously is that there are a number of "naturalists" who oppose
building near the shore, and "most of the discussion seems to come from the
'naturalist1 camp." Nevertheless, Smith argues that "the solutions—if there
are any—should be contemplated now as part of a concerted global effort.
This is a beautiful world, and we are its stewards."
Human Health and Ecological Impacts
Climate and weather have important impacts on human health. A global
warming would increase the stresses due to heat, decrease those due to cold,
and possibly enable some disease that require warm year-round temperatures to
survive at higher latitudes. Kalkstein et al. (Volume 3) present a
preliminary statistical assessment of the relationship of mortality rates to
fluctuations in temperature in New York City. They find that a two to four
degree (C) warming would substantially increase mortality rates in New York
City, if nothing else changed. However, they caution that if New Yorkers are
able to acclimatize to temperatures as well as people who currently live in
U.S. cities to the south, fewer deaths would occur. Kalkstein et al. write
that knowledgeable observers disagree about whether and how rapidly people
adapt to higher temperatures; some people undoubtedly adjust more readily than
others.
Although people may be able to adapt to changes in climate, other species
on the planet would also be affected and may not be as able to control their
habitats. Peters and Darling (Volume 3) examine the possibility that changes
in climate would place multiple stresses on some species which would become
extinct, resulting in a significant decline in biodiversity. (Mass extinc-
tions appear to have accompanied rapid changes in temperatures in the past.)
Throughout the world reserves have been set aside where targeted species
can remain relatively free of human intrusion. Peters and Darling ask: Will
these reserves continue to serve the same function if the climate changes? In
some cases, it will depend on whether the reserve's boundaries encompass areas
to which plants and animals could migrate. Some species may be able to
migrate "up the mountain" to find cooler temperatures; coastal wetlands could
migrate inland. A northerly migration of terrestrial species would be
possible in the undeveloped arctic regions of Alaska, Canada, and the Soviet
Union; but human development would block migration of larger animals in many
areas.
15
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POLICY RESPONSES
Papers by UNEP Deputy Director Genady Golubev and EPA Administrator Lee
Thomas (both in Volume 1) provide official views on the nature of the effects
from projected changes in the atmosphere and the role of their institutions in
addressing those changes. Golubev notes that while "the global issues are
complex, uncertainty exceeds understanding, and patience is prudence," there
is an other side to the story: "Our legacy to the future is an environment
less benign than that inherited from our forbearers. The risks are sufficient
to generate a collective concern that forebodes too much to wait out the
quantifications of scientific research. Advocating patience is an invitation
to be a spectator to our own destruction."
Golubev also points out that UNEP has worked for the achievement of the
Vienna Convention for the Protection of the Ozone Layer, in which many nations
have agreed to act in concert to address an environmental issue whose impacts
have not yet been detected. Yet he notes that the agreement is for coopera-
tion in research and does not yet bind nations to observe limits in production
and emissions of gases that could deplete stratospheric ozone.
Thomas points out that both the potential depletion of ozone and the
global warming from the greenhouse effect are examples of environmental
problems that involve the "global commons." Because all nations contribute to
the problem and experience the consequences, only an international agreement
is likely to be effective. He urges scientists around the world to discuss
this issue with their colleagues and key officials.
Richard Benedick, Deputy Assistant Secretary in the U.S. Department of
State (Volume 1), describes the emerging international process addressing the
ozone issue. Although the process for addressing climate change has not yet
proceeded as far, he writes, "from my perspective as a career diplomat, it
appears that the greenhouse effect has all the markings of becoming a high
visibility foreign policy issue. . . . How we address this issue internation-
ally depends to a great extent on our success or failure in dealing with the
ozone depletion issue."
J.P. Bruce (Volume 1) of Environment Canada presents the issue of
atmospheric change in the context of air pollution in general. He writes that
ozone modification and climate change are "urgent issues," especially because
important long-term decisions are being made today whose outcomes could be
strongly affected by changes in climate and the ozone layer. Bruce recommends
that emissions of CFCs be reduced, and concludes that "a new approach, a new
ethic towards discharging wastes and chemical materials into the air we all
breathe must soon be adopted on a international scale."
Two U.S. Senators also provide their reactions. John Chafee from Rhode
Island (Volume 1) describes hearings that his Subcommittee on Environmental
Pollution held June 10-11, 1986. "Why are policy makers demanding action
before the scientists have resolved all of the questions and uncertainties?"
he asks. "We are doing so because there is a very real possibility that
society—through ignorance or indifference, or both—is irreversibly altering
the ability of our atmosphere to perform basic life support functions for the
planet." Albert Gore, Jr. from Tennessee, who has chaired three congressional
hearings on the greenhouse effect, explains why he has introduced a bill in
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the U.S. Senate to establish an International Year of the Greenhouse Effect.
"The legislations would coordinate and promote domestic and international
research efforts on both the scientific and policy aspects of this problem,
identify strategies to reduce the increase of carbon dioxide and trace gases,
investigate ways to minimize the impact of the greenhouse effect, and
establish long-term research plans." Senator Gore closes by quoting Sherwood
Rowland (discussed below): "What's the use of having developed a science well
enough to make predictions, if in the end all we're willing to do is stand
around and wait for them to come true?" Both Senators call for immediate
action to reduce global use of CFCs.
John S. Hoffman (Volume 1) emphasizes the inertia of the atmosphere and
oceans. Because there are time lags between changes in emission rates,
atmospheric concentrations, and changes in ozone and global warming
temperatures, the types of management strategies must be different from those
that are appropriate for controlling, for example, particulate pollution,
where the problem goes away as soon as emissions are halted. CFC emissions
would have to be cut 80 percent simply to keep concentrations from
increasing. Although constant concentrations would prevent ozone depletion
from worsening, Hoffman points out that even if we hold the concentrations of
greenhouse gases constant once the earth has warmed one degree, the planet
would warm another degree as the oceans come into equilibrium. Thus it might
be impossible to prevent a substantial warming if we wait until a small
warming has taken place.*
The final section of this volume presents the papers from the final day
of the conference. Peter Usher of UNEP recounts the evolution of the ozone
issue. Following Rowland and Molina's hypothesis that chlorofluorocarbons
could cause a depletion of stratospheric ozone in 1974, UNEP held a conference
in 1977 that led to a world plan of action to assess the issue and quantify
risks. Since that time, UNEP has held numerous coordinating meetings leading
up the the Vienna Convention. However, Usher suggests that motivating inter-
national effort on the greenhouse effect will be more difficult: "Prohibition
of nonessential emissions of relatively small amounts (to control ozone
depletion) is one thing, limiting emissions of carbon dioxide from coal- and
oil-burning is quite another."
Dudek and Oppenheimer of the Environmental Defense Fund (U.S.) analyze
some of the costs and benefits of controlling emissions of CFCs. They
estimate that by holding emissions constant, 1.65 million cases of nonmelanoma
skin cancers could be prevented worldwide, and that the cost of these controls
would be 196 to 455 million dollars, depending on the availability of alterna-
tive chemicals.
Two former high-ranking environmental officials in the United States
argue that we should be doing more to address these problems. John Topping
recommends that CFCs in aerosol spray cans, egg cartons, fast-food containers,
and other nonessential uses be phased out, and that people recognize that
3 Titus (Volume 1) and Thomas (Volume 4) also explore inertia, noting that
even if temperatures remained constant after warming somewhat, sea level
would rise at an accelerated rate as the oceans, mountain glaciers, and ice
sheets came into equilibrium with the new temperature.
17
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along with energy conservation, nuclear power is the most likely alternative
to fossil fuels over the next generation or two. He also recommends that
society take steps to minimize the impacts of climate change and sea level
rise, for example, by requiring environmental impact statements to consider
the likely impacts.
Gus Speth, president of the World Resources Institute, recommends
international efforts to stop tropical deforestation; a production cap for
chlorofluorocarbons; increased energy conservation; advanced technologies for
producing electricity from natural gas; and tighter regulations to limit
carbon monoxide from automobiles, which would indirectly limit increases in
atmospheric methane. He agrees with Topping that environmental impact
statements for projects that could contribute to or be affected by climate
change or ozone modification should consider these impacts.
Doniger and Wirth, from the Natural Resources Defense Council (U.S.),
argue that the current uncertainties are no longer a reason to wait for
additional information: "With the stakes so high, uncertainty is an even more
powerful argument for taking early action." These authors conclude that sharp
reductions in CFCs are necessary, pointing out that even with a production
cap, atmospheric concentrations of these gases will continue to grow.
Therefore, Doniger and Wirth propose an 80 percent cut in production over the
next five years for CFCs 11 and 12, the halons, and perhaps some other
compounds, with a complete phaseout in the next decade.
Richard Barnett of the Alliance for a Responsible CFC Policy (which
represents CFC using industries) agrees that we should not delay all action
until the effects of ozone depletion and climate change are felt; but he
"would hardly characterize the activities over the last twelve years as 'wait
and see1 . . . The science, as we currently understand it, however, tells us
that there is additional time in which to solidify international consensus.
This must be done through discussion and negotiation, not through unilateral
regulation."
Barnett adds that industry should "take precautionary measures while
research and negotiations continue at the international level. We will
continue to examine and adopt such prudent precautionary measures as
recapturing, recycling, and recovery techniques to control CFC emissions;
transition to existing alternative CFCs that are considered to be more
environmentally acceptable; practices to replace existing systems at the
expiration of their useful lives to equipment using other CFC formulations;
practices in the field to prevent emissions where possible; encouragement of
CFC users to look for processes or substances that are as efficient, safe, and
productive—or better—than what is presently available."
Barnett concludes that "these environmental concerns are serious, but
their successful resolution will require greater global cooperation in con-
ducting the necessary research and monitoring, and in developing coordinated,
effective, and equitable policy decisions for all nations."
We hope that this paper has provided the reader with a "road map" through
the papers of this four-volume report on the potential effects of changing the
atmosphere. But we have barely scratched the surface of each, Just as the
existing research has barely scratched the surface in discovering and
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demonstrating the possible risks of ozone modification and climate change. A
continual evolution of our understanding will be necessary for our knowledge
to stay ahead of the global experiment that society is conducting.
REFERENCES
Hansen, J.E., A. Lacis, D. Rind, and G. Russell. 1984. Climate sensitivity to
increasing greenhouse gases. In Greenhouse effect and sea level rise: A
challenge for this generation, eds. M.C. Earth and J.G. Titus. New York:
Van Nostrand Reinhold.
Keeling, C.D., R.B. Bacastow, and T.P. Whorf. 1982. Measurements of the
concentration of carbon dioxide at Mauna Loa, Hawaii. Carbon Dioxide Review
1982. 377-382, ed. by W. Clark. New York: Oxford University Press,
Unpublished data from NOAA after 1981.
NAS. 1983. Changing Climate. Washington, D.C.: National Academy Press.
Nordhaus, W.D., and G.W. Yohe. 1983. Future carbon dioxide emissions from
fossil fuels. In Changing Climate. Washington, D.C.: National Academy
Press.
Villach. 1985. International assessment of the role of carbon dioxide and of
other greenhouse gases in climate variations and associated impacts.
Conference Statement. Geneva: United Nations Environment Program.
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HUMAN HEALTH
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UVR Dose-Dependent Life Shortening in Mice
RE. Davies and P.O. Forbes
Temple University Health Services Center
Philadelphia, Pennsylvania USA
The type of ultraviolet referred to as "UV-B" has properties and effects
of considerable significance. It is absorbed strongly by proteins, nucleic
acids, and other biological molecules, and also by ozone and other environ-
mental materials. Absorption by atmospheric ozone largely determines how much
of the sun's UV-B emission reaches the earth's surface. The fraction that
does reach the surface is strongly absorbed by exposed tissue and delivers
sufficient energy (about 4 eV per photon) to produce direct or indirect
chemical reactions, some of which are deleterious.
Because of this strong absorption, most of the direct effects of UV-B are
limited to superficial tissues a few tens of microns thick: in animals this
usually means the cutis or skin, and specialized external tissues such as the
eye. Many animals have superficial nonliving products such as scales, hair,
or feathers that absorb most or all of the UV-B. In others, such as our
species, constitutive absorbers, such as stratum corneum and melanin, can be
enhanced in response to damage, reducing the effects of subsequent exposure.
Most biological consequences of U.V-B, both damage and secondary responses, are
not only superficial, but are limited to areas not protected by natural
absorbers or artificial coverings such as clothing. Characteristic UV-B
induced effects in humans, including acute (sunburn), subacute (pigmentation)
and chronic (skin cancer, "aging"), almost invariably appear in the most
exposed areas such as face and hands.
Not all effects of UV-B are so highly localized, and a few appear to be
beneficial. Exposure to UV-B can prevent the bone disease rickets: the
mechanism involves production, in the exposed skin, of a form of vitamin D
from an inactive precursor, followed by redistribution of this essential
vitamin to the rest of the body. There are also reports, less easily measured
or explained, of beneficial physiologic (work capacity) and psychologic
effects of sunlight, at least some of which appear to be related to UV-B.
23
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Another category of systemic effects was recognized with the observation
that specific immune responses could be inhibited by UV-B. One such response,
the ability to reject certain transplanted tumors, was reduced or eliminated
on a system-wide, apparently permanent basis by localized UV-B irradiation.
In another response, the development of contact hypersensitivity, suppression
by UV-B is transient and the degree of systemic involvement is less clearly
established.
We recently described an effect apparently attributable to UV-B that is
unarguably systemic. Mice that had been exposed chronically to "sun-like"
radiation exhibited an increase in mortality that was proportional to the
quantity of radiation delivered. Since the effect was observed in experiments
designed to study UV-B induced skin cancer, many of the mice had cancers at
the time of their death. However, the severity of the carcinogenic response
was not sufficient to account for the difference in survival, especially
considering that such tumors are relatively slow growing and rarely
metastasize. The amount of UV-B delivered was less, in most cases, than that
required to produce any obvious acute or chronic damage, although some skin
thickening undoubtedly occurred.
Survival curves in healthy, genetically uniform laboratory mice usually
exhibit two distinct phases. Initially deaths are random and usually infre-
quent, resulting in a slow, roughly linear decline that is unrelated to
specific treatment conditions. These deaths usually result from injuries or
other types of errors. Subsequently, survival declines rapidly; in a particu-
lar strain, under uniform conditions, the time of this terminal phase is quite
reproducible.
In the strain of mice with which we have the most experience, the
approximate median age at death is about 90 weeks. Daily exposure to an
amount of radiation corresponding to about two minutes at midday summer
sunshine produces a detectable reduction in this value, and doubling the daily
dose reduced median survival to about 50 weeks. Higher doses, some of which
produced chronic irritation, produced further but less dramatic decreases in
life span. In all cases it is the second, precipitous stage of the survival
curves that is affected. Comparison of light sources delivering different
qualities of radiation indicates that most or all of the effect is
attributable to the UV-B portion of the spectrum.
To our knowledge, no studies have been designed specifically to examine
the effects of chronic UV irradiation on the survival of mammals. Available
data come from experiments designed to study photocarcinogenesis, and most
have been conducted with mice. Where mortality data are published, similar
effects on survival can be seen in other mice, both haired and hairless.
Specific studies with Drosdphila also show dose-dependent life shortening in
response to UV-B irradiation. Thus the data, though not extensive, appear to
be consistent, and suggest that UV-B can produce cumulative systemic changes
that reduce the potential life span in some species.
It is not clear whether this phenomenon has ecologic significance. The
effect in laboratory mice is to accelerate apparently spontaneous death with
no obvious effect on intermediate health. Animal survival in nature is often
limited by specific processes such as disease or predation, and this more
closely resembles the first phase of the survival curve. Clearly, however,
24
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accelerated death must result from significant systemic damage. Whether such
damage could modify health or life span of other species, including ours, is
open to speculation.
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An Estimation of Sunspot Induced Ozone
Changes From a Sunburn Ultraviolet Meter
Daniel S. Berger
Temple University
Philadelphia, Pennsylvania USA
A sunburn ultraviolet meter recording continuously since 1973 has
provided data for determining ozone variation over an 11-year sunspot cycle
(Berger and Urback 1982). This meter is part of a network of similar meters
whose purpose is to determine the normal levels of biologically effective
short ultraviolet radiation reaching the biosphere and of long-term trends.
These purposes have been the stated goals of all agencies, both domestic and
international, charged with the responsibility for studying the ozone layer
and protecting it insofar as anthropogenic activities have an effect.
A ground-based monitor of short UV provides data important not only in
itself but from which both ozone variations and cloud absorption can be, deter-
mined. The wavelengths shorter than 330 nm detected by this meter (Figure 1
and Berger 1976) cause sunburn and after protracted exposure, non-melanoma
skin cancers. They have also been shown to have myriad effects in the bio-
sphere, primarily because they affect DNA, the basic control of all living
organisms. The results of the network have therefore been used in the epide-
miological study of non-melanoma skin cancer (Scotto et al. 1976). Meter
results have also been used to study cloud absorption (Slomka 1976).
For the study presented here, monthly averages of sunburn dose for the
11-year period were derived from the semihourly meter printout. The deviation
of each month from the mean of that month was plotted over the 11-year period;
the sunspots for that month were plotted on the same abscissae. Smoothing of
the data with a 12-month running average produced the top curve of Figure 2,
which shows a clear correlation. The results are the sunburn ultraviolet
variations over an 11-year period. From these variations, an estimate of
ozone thickness variation due to sunspot activity is derived. The top curve
in Figure 2 consists of two parts, the quasi-biennial fluctuations, an
approximate 26-month oscillation and the 11-year cyclic variation due to
sunspot activity. Separation of the top curve into its two component parts is
shown on the lower curves of the figure.
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SUN6URNING ULTRAVIOLET METER
LOG
8
6
4
2
QIC
OT 6
t 4
m
K
0.001
8
4
Human skin action
spectrum (B«i fit)
xM«ltr normalized
to stun at 300nm
273 300 323 »0 375
WAVELENGTH, NM
Figure 1. Erythema action spectrum and sunburn ultraviolet meter
spectral response.
SUNBURN UV DEVIATIONS FROM AN 11-YEAR MEAN
QUASI/BIENNIAL FLUCTUATIONS
TOTAL SUNBURN UV MINUS QUASI/BIENNIAL FLUCTUATIONS
1M1
1M2
1983
1M4
Figure 2.
28
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The quasi-biennial fluctuation is a result of a variable rate at which
ozone moves from the tropics into the temperate zone, in this case to 40° N
latitude. No net change in stratospheric ozone occurs. Consequently, in a
quasi-biennial period, the time integral should be zero. Deviations from zero
are attributable to net changes of total ozone due to sunspot activity.
Comparison of the 11-year cyclic variation of sunburn ultraviolet shows a
close correspondence to sunspot number, as shown in Figure 3.
There is also a relationship between the change of sunburn UV and the
change in stratospheric ozone. If the meter had an exact erythema action
spectrum, there would be about 1.1% change in meter reading per ^% change in
ozone at 3 mm of ozone thickness. (See Figure 4.) Because the meter spectral
response is long wave shifted, the meter change is more like 1.2J at 3 mm of
ozone. Since there was an 8% maximum change in sunburn effect due to sun-
spots, the ozone change was about 6.5%. This change was due to 160 sun-
spots. Thus, 25 sunspots caused a '\% ozone change.
The constancy of extra-terrestrial radiation between 295 and 330 nm is
assumed as is the complete decoupling of cloud variability from sunspot
activity. The first assumption must be justified by extra-terrestrial
spectro-radiometric observations. The extent to which the second assumption
is true could be determined by a careful analysis of the meter record
itself. Any cloud-sunspot coupling could be used to compensate the derived
ozone variation.
It may appear naive to be making a calculation of the effect of a sunspot
on ozone thickness based on so thin a reed as a non-thermostatted monitoring
meter, but the unexpected and gratifying 11-year record that is shown here
would have been considered naive to anticipate up until the time these calcu-
lations were completed.
The information-rich output, the almost perfect data captured, the long
term stability, the low cost, and the ability of technicians without special
training to provide the minimal maintenance required argue that there is a
place for this device for long term monitoring of the ozone layer or of the
ultraviolet levels in the biosphere required by environmental agencies.
29
-------
+4-
Ul
O +3-
c
u.
s °-
1 -1-
Z -2-
ui
« -a
£ a
-4-
TOTAL SUNBURN OF UV MINUS
QUASI-BIENNIAL FLUCTUATIONS
-180
-160
-140
-120
-1OO
- SO
-60
-40
-20
-0
(0
1974 1975 1978 1977 1978
4 7 10 1
1979
4 7 10
1980
1981 1982 1983 1984
Figure 3.
2.5
2.O
1.5
1.0
0.5
.200 .300 .400cm OZONE
OVERHEAD SUN
Figure 4. Rate of Change of Sunburning Capability of Sunlight with
Ozone Variation
30
-------
REFERENCES
Berger, D., and F. Urback. 1982. A climatology.of sunburning UV radiation -
Photochem. and Photobiol. 35:187-192.
Berger, D. 1976. The sunburning ultraviolet meter. Photochem. and
Photobiol. 24:587-593.
Scotto, J. et al. 1976. Measurement of UVR in the US and comparisons with
skin cancer data. National Cancer Institute DHEW (NIH) 76-1029.
Slomka, K. 1976. Preliminary Analysis of the Effect of Solar Zenith Distance,
Total Ozone Content, Atmospheric Turbidity and Cloudiness on the Solar -UiJL
Radiation Measured with a Robertson-Berger Meter. Publication of the
Institute of Geophysics, Polish Academy of Sciences 106:121-131.
31
-------
Nonmelanoma Skin Cancer—UV-B Effects
Joseph Scotto
National Cancer Institute
National Institutes of Health
Bethesda, Maryland USA
Since the early 1970s, the National Cancer Institute, in collaboration
with other federal and nonfederal sources, has conducted special epidemiologic
surveys of nomelanoma skin cancer and monitored ground level UV-B measurements
at various geographic locations within the United States.
These studies responded to the need for basic data to be used in
measuring the extent of certain human health effects that may result from
stratospheric ozone depletion.
We focus on solar ultraviolet radiation in the range of 280 to 320
nanometers, called mid-UV or UV-B (see Figure 1). Under experimental
conditions, UV-B has been shown to produce skin erythema (sunburn) in man and
skin cancer in animals, and it is effective in altering DNA. Cumulative
exposure to UV-B is also believed to be partially responsible for the "aging"
process of the skin in humans. Except for preventing vitamin D deficiency
rickets, which is now confined to populations with inadequate nutrition, UV-B
is basically considered biologically harmful.
While no solar radiation below 295 nm ever reaches the earth's surface, a
small quantity Of UV-B does. Stratospheric ozone depletion may result in
increases of UV-B energy reaching the earth and its populations. The physical
amplification factor has been put at 2. This means that a 1j6 decrease in
ozone may result in a 2% increase in solar ultraviolet, UV-B.
Basal cell carcinomas and squamous cell carcinomas of the skin, the
nonmelanomas, are the most common malignant neoplasms occurring in the white
populations of the world. Currently, annual incidence in the United States is
estimated at about one-half million patients, and the rates are increasing at
about 3% per year. Epidemiologic study has been limited by the fact that most
patients are customarily seen and treated in the offices of physicians and not
hospitalized. Cure rates are high (about 99%) and only a small percentage of
skin cancers are metastatic or result in death.
33
-------
THE ELECTROMAGNETIC SPECTRUM
X-rays and gamma rays
Extreme
xuv
Ultraviolet
Far i Middle
ruv T^ MUV
Infrared and radio
100
200
300
400 500 600
Wavelength in Nanometers
700
800
900
1,000
Figure 1
Because the primary source of data cancer registries is the inpatient
hospital file, the statistics routinely collected on skin cancer are usually
very incomplete and not comparable with other forms of cancer. Thus,
population-based estimates of skin cancer incidence require special surveys to
collect data from offices and outpatient files.
Figure 2 shows the geographic locations within the continental United
States where skin cancer surveys were conducted and ground level measurements
of UV-B were obtained. In 1971-72, there were four areas in the Third
National Cancer Survey; in 1977-78, eight areas of NCI Surveillance Epidemi-
ology and End Results Program (SEER) were surveyed.
Two locations, Minneapolis-St. Paul, Minnesota, and San Francisco-
Oakland, California, were resurveyed in the late 1970s. Skin cancer incidence
data from New Hampshire, Vermont, and San Diego, California, were most
recently included. We do not have statistical details for other cancers from
these locations, and we are just now receiving UV-B readings from Concord, New
Hampshire, and Burlington, Vermont. Patient and general population interview
studies were conducted in nine locations. These locations span the United
States from Seattle in the north (47.5°N) to New Orleans (30°N). Most of the
figures that follow display the epidemiologic details for the eight-area
survey conducted in 1977-78. Seven of these are SEER locations where NCI has
continuing surveys of all other malignancies. The results are similar for all
surveys.
Skin cancer is a disease that rarely occurs in black and pigmented
races. The age-adjusted rate of 242 per 100,000 for whites is more than 60
times that for blacks with a rate of under 4 per 100,000. Among Caucasians
"Anglos" or non-Hispanics, are at greater risk than Hispanics by about 7-10 to
1.
Figure 3 shows the incidence of nonmelanoma skin cancer and all other
cancers combined among whites for each of eight locations plotted according to
latitude. For all other malignancy, there is no latitudinal gradient. In
contrast, nonmelanoma skin cancer incidence rates were definitely lower at the
higher latitudes.
-------
OALLAS-FT. WORTH
FT. WORTH
LEGEND
] TNCS (NONMELANOMA) LOCATIONS
1 TNCS IMELANOMAI LOCATIONS
SEER LOCATIONS
TNCS AND SEER
Figure 2. Skin Cancer Measurement
Locations in the United States
35
-------
D
•
I
RATE PER 100.000 POPULATION
8
8
>
o
m
O
I
Cfl
X
2
5 2
3 5
o
New Orleans
Atlanta
Albuquerque (New Mexico)
San Francisco-Oakland
Salt Lake City (Utah)
Detroit •
Mfnneapol!a~$t. Paul
Seattle
Figure 3. Age Adjusted Incidence of Cancer (U.S. 1970)
Among Whites by Latitude
36
-------
The age-adjusted incidence rates by geographic location for each sex are
shown in Figure 4. The rates for males are always greater than those for
females. Overall, the male/female ratio is close to 2 to 1 (1.83). Note
there are two sets of bars for New Mexico. Because of the high proportion of
highly pigmented Hispanics in that State, over one-third, the rates for all
Caucasians are lower than that for Anglos only.
Figures 5 and 6 show age-specific rates according to region. The rates
increased with age—the highest rates were seen in the oldest age groups. The
southern region was clearly at higher risk than the northern region.
Figures 7 and 8 show age-specific rates by specific location, comparing
males and females. At each location the male rates were lower or equal to the
female rates at early ages. After age 45, in the northern and middle loca-
tions, male rates consistently exceeded those of females, and the differences
were greatest in the oldest age groups (Figure 7). In the southern locations
(Figure 8), the separation between male and female rates began a decade or two
earlier, presumably because the UV threshold levels for skin cancer detection
were reached sooner.
Tumors appear on the face, head, and neck in over BQ% of nonmelanoma skin
cancers. Among females, the nose is the most common site while, among males
tumors of the nose, cheek, and scalp are equally high. Tumors of the ear
occur more frequently among men, compared to women, by a factor of 10 or more,
especially in the southern areas. In contrast, tumors of the legs are more
common among females who have greater UV exposure and also more melanoma of
the lower leg. In both sexes tumors are much more common in the lower lip
than in the upper lip.
Age-specific incidence rates according to anatomical site are illustrated
in Figure 9. Rates for face, head and neck, and upper extremities progres-
sively increased, while those for trunk and lower extremities reached a
plateau or declined at older ages.
With respect to histology, Figure 10 shows a composite of specific
geographic locations depicting age-specific incidence patterns for basal cell
carcinomas and squamous cell carcinomas of the skin. Overall the incidence
rates for BCC was 4 to 5 times higher than SCC. Increases have been observed
for each cell type as age increases. The rate of increase may be slightly
higher for squamous cell carcinomas. But the squamous cell carcinomas begin
at later ages. The ratio of BCC to SCC is greatest in the northern region and
lowest in the southern region, ranging from over 12 to 1 in the north to over
2 to 1 in the southern locations.
37
-------
I
RATE PER 100,000 POPULATION
S
D)
*
Seattle
Minneapolis-
St. Paul
Detroit
Utah (State)
Salt Lake City,
Utah
San Francisco-
Oakland
Atlanta
New Orleans
New Mexico
< State)
Albuquergue.
New Mexico
Anglo
All Survey
Areas
Figure 4. Age Adjusted Rates of Nonmelanoma Skin Cancer
in Various Regions of the United States
38
-------
10OOCH
Ul
i
u
iu
Q
O
U
O
K
CO
111
100O
100
10
jar'
Legend
• NORTHERN LOCATIONS
D SOUTHERN LOCATIONS
25-34 35-44 45-54 55-04 65-74 75-84 85+
AGE
Figure 5. Age-Specific Nonmelanoma Skin Cancer
Incidence by Region Among White Males
100003
giooo
z
111
a
o
o
a 100
CO
iu
10
Legend
• NORTHERN LOCATIONS
D SOUTHERN LOCATIONS
1 1 —r— 1 1 • —
25-34 35-44 45-54 55-64 65-74 75-84 85+
AGE
Figure 6. Age-Specific Nonmelanoma Skin Cancer
Incidence by Region Among White Females
39
-------
NORTHERN REGION (LATITUDES 40-50 DEGREES NORTH)
1*400
'- SEATTLE
MALES
FEMALES
<1S 15-24 25-34 36-44 4M4 S6*4 SS 74 75-t*
AGE GROUP
10.000
: MINNEAPOLIS-ST. PAUL
i
UJ
MALES
FEMALES
19-24 25-34 35-44 4544 55-64 85-74 7S-B4
AGE GROUP
10.000!
.DETROIT
MALES
FEMALES
CIS 15-24 25-34 35-44 4544 554* ES-74 75*4
AGE GROUP
*•
O
10,000
I
I
MID REGION (LATITUDES 35-40 DEGREES NORTH)
:SALTLAKECCTY
MALES
FEMALES
36-44 46«4 B5<4 (S-74 7S44
AGE GROUP
10.000
: SAN FRANCISCO-OAKLAND
1
e
MALES
FEMALES
<16 15-J4 1534 35-*4 *S64 S&44 6E 74 TS-M »S»
AGE GROUP
Figure 7. Age-Specific Nonmelanoma Skin Cancer Incidence Among
Whites by Regions of the United States, 1977-78
-------
SOUTHERN REGION {LATITUDES 30-35 DEGREES NORTH)
: ATLANTA
2
I
8
<15 1524 25-34 3S-44 4S4S4 H4M
AGE GROUP
8
|
4
1 NEW ORLEANS
MALES
FEMALES
10.0
<15 1S-24 2S-M JB-44 4644 SM4 BS 74 75-«4 H+
AGE GROUP
I
:ALBUQUERQUE
lAngto
MALES
FEMALES
-------
5000
1000
z
o
a
O
a
o
o
5
cc
LU
o
UJ
O
5
100
10
FACE, HEAD
OR NECK
UPPER
EXTREMITIES
TRUNK
LOWER
EXTREMITIES
I
I
<15 15-24 25-34 35-44 45-S4 55-64
AGE GROUP
65-74
75-84
85 +
Figure 9. Trends in Annual Age-Specific, Nonmelanoma
Skin Cancer Rates Among Whites, Both Sexes
-------
NORTHERN REGION (LATITUDES 40-60 DEGREES NORTH)
SEATTLE
MINNEAPOUS-ST. PAUL
t
DETROIT
<» 1U4 »J4 31-44 4U4 tfrW «M 7M4
AGE GROUP
<15 1&24 »34 JM4 4E-M »H »74 7M4 «6«
AGE GROUP
MID-REGION (LATITUDES 38-40 DEGREES NORTH)
10 000 e -'•••—
UTAH
BASAL
SAN FRANCISCO-OAKLAND
<» 1H4 7634 36-44 4»M »«4 16-74
AGE GROUP
<15 KM 2SM K44 4frM 66-H B)4 7M4
AGE GROUP
ATLANTA
SOUTHERN REGION (LATITUDES 30-36 DEGREES NORTH)
i-
NEW ORLEANS
»J4 3*44 4»M JM4 O-74 r»M »«
AOf GROUP
: NEW MEXICO
3&44 46-M S644 »74 7»H 16•
AGE GROUP
1524 7»34 3E-44 4154 55*1 KV14 r»M «»•
AGE GROUP
Figure 10. Age-Specific Nonmelanoma Skin Cancer Incidence Among
Among Whites by Regions of the Unites States, Both Sexes
-------
In regard to our estimates of ground level UV-B measurements, we have
been monitoring and editing data in collaboration with researchers at the
National Oceanic and Atmospheric Administration and their network of weather
stations (see Berger in this volume for details of the Robertson-Berger
meter).
Figure 11 shows, as expected, that the annual amounts of sunburn-
producing UV-B correlated with latitude. To put these numbers in perspective,
it is estimated that a count of 440 R-B units may produce a perceptible
sunburn. It is possible to receive such a dose within 20 minutes on a
midsummer day around noontime. It is important to note that these measure-
ments are affected by altitude, cloud cover or water vapor, and other meteoro-
logical factors. At altitudes of over a mile high Albuquerque and Salt Lake
City received greater amounts of solar UV-B than expected; while Tallahassee
with relatively high humidity received less than the expected dose for that
latitude. I should like to point out that current observations indicate a
general downward trend in meter readings at several locations. The relative
positions for Detroit and Minneapolis have changed, with current figures now
lower at Detroit.
The monthly averages of R-B counts for Albuquerque, New Mexico, and
Seattle, Washington, respectively, are shown in Figure 12. These were the
highest and lowest exposure areas included in NCI's nonmelanoma skin cancer
surveys. The ratio of UV-B exposure is about 2 to 1 for these locations.
Next my discussion focuses on our correlation studies of population-based
skin cancer incidence and estimated UV-B dose.
The annual UV-B levels and age-adjusted incidence rates for nonmelanoma
skin cancer in white males and females were determined in the two special
surveys conducted in 1971-72 and 1977-78 (see Figures 13 and 14). The inci-
dence data are plotted on a log scale so that a straight line with a positive
slope represents a constant percentage increase in incidence. Mathematical
models were used to describe dose-response relationships and do not reflect
the mechanism by which UV causes skin cancer. Using an exponential model
previously applied to the 1971-72 data, estimates of the biological amplifi-
cation factor (that is, the relative change in skin cancer incidence due to a
relative change in UV-B radiation) were derived. Assuming a common slope, the
exponential model may be written as a logarithmic expression as shown:
Ln RJJ = ai + b
where u = 1 , 2 denotes the two survey areas
J = 1, 2 ... 10 denotes the locations
Rj* = the age-adjusted incidence rate
UVj = the annual UV-B count per 10,000
= constants
44
-------
3.5
Mauna Loa
[2 2.5
z
D
00
i
2 2
X
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8
> 1.5
_i
z
z
• ElPato
Tallahastat
i Albuqutrqut
i Fort Worth
• Oakland
DM Moinc*
Philadelphia •
Bismarck
• •
Minneapolis
.5
I
I
I
I
15
20
25 30 35 40
DEGREES NORTH LATITUDE
45
50
Figure 11. Annual UV Count by Latitude
-------
ESTIMATED MOKTHLY UVB VS. MONTH FDR TWO LOCATIONS
Legend
• AUUOUBKKJC. M*
D SEATTU. WA ^
JAN FIB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC
MONTH
Figure 12. Estimated Monthly UV-B vs. Month for Two Locations
-------
cc
2:
f
K
ui
-------
800
700
600
Model: In R:: " «l j +
(Assumes common slope)
K
500
400
300
• WHITE FEMALES- 1977-78
O WHITE FEMALES- 1971-72
3
s
-------
In the regression analyses, the logarithms of the age-adjusted incidence
rates were weighted by the inverse of their estimated variance. Assuming that
the annual UV-B counts were to increase by \% at each location, the relative
effects on skin cancer incidence were found to vary from a low of 1.19% to a
high of 2.88^. The estimates were lowest for females residing in areas of low
UV-B exposure levels. Overall, the biological amplification factors were
estimated to be roughly twofold, but steeper for squamous cell carcinomas.
An update of the incidence and UV-B correlations for males and females is
shown in Figure 15. There are ten locations plotted, which include only the
most recent surveys of 1977-80. We have tentatively estimated the UV-B index
for NH/VT at 96 (x10,000 SU), and we use average annual counts for the years
1977 through 1981 for all other locations. In general, the average UV values
are lower than those previously estimated for a one-year period.
Biological amplification factors (using exponential model) show no
substantial changes; however, the range is now between 1.03 and 2.5. While
these estimates are a little lower than those previously calculated, the
degree of uncertainty has been reduced and the estimates for the S5% lower
limits have in fact increased. Figures 16 and 17 depict these correlations
with respect to cell type. The slopes are steeper for SCC compared to BCC.
Correlations according to anatomical site are shown in Figures 18 and 19. The
relationship of skin incidence and ground level UV-B exposure is consistent
for each site group. However, there appear to be stronger associations and
steeper slopes for the face, head, and neck, and upper extremities among white
males and females. Keep in mind that over 87% of all nonmelanoma skin lesions
occur on these relatively more exposed anatomical sites.
As many researchers have suggested, and as the results of our studies
show, there are demographic factors that may reflect increased or decreased
skin cancer risk in certain population groups similar to the differences we
have noted for Anglos and Hispanics. So, in addition to the incidence
surveys, telephone interview sample surveys of skin cancer patients and
general population controls between the ages of 20 to 75 were conducted at
nine locations. Information was sought on several host and environmental
factors that may affect the risk of skin cancer. Examples -follow showing the
correlation of skin cancer incidence with UV-B radiation according to the
presence or absence of certain constitutional factors.
-------
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.
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100 t20 UO 180
SOLAR ULTRAVIOLET RADIATION (UV8) INDEX
180
I
tj
3
I
Legend
• FEMALES
D MALES
200
Figure 15. Nonmelanoma Skin Cancer Incidence
According to UV-B Index
50
-------
1000
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o
o
o
o"
o
100-
I
10-
80
5 i
as ts
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100 120 rtO WO
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
I
180
Legend
• BASAL CELL ONLY
D AT LEAST ONE SQUAMOUS
_«
200
Figure 16. Nonmelanoma Skin Cancer Incidence by UV-B Index
White Males According to Cell Type
51
-------
WOO-r
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SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
Legend
• BASAL CELL OMLY
D AT LEAST ONE SQLUMOUS
200
Figure 17. Monmelanoma Skin Cancer Incidence by UV-B
Index White Females According to Cell Type
52
-------
1000-
Q
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z
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80 100 120 140 160 180
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
3
200
Figure 18a.
Nonmelanoraa Skin Cancer Incidence by UV-B Index
According to Anatomical Site Group Among White Males
Face, Head, or Neck
100-
« -
111 O
o ;;
< UJ 10-
_J H ;
if :
i * •
•
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I -
?i f| $
llll I
8 S •
i! I ! i
!i 5 I !
80 100 120 140 160 180
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
200
Figure I8b. Nonmelanoma Skin Cancer Incidence by UV-B Index
According to Anatomical Site Group Among White Males Trunk
53
-------
10O
DC.
» 10-
23
<0 '
>2
ii
0 1
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120 140
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I
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Figure I8d.
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
Nonmelanoma Skin Cancer Incidence by UV-B Index According to
Anatomical Site Group Among White Males Lower Extremities
54
-------
gs
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SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
Figure 19a.
Nonmelanoma Skin Cancer Incidence by UV-B Index
According to Anatomical Site Group White Females
Face, Head, or Neck
100 -i
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38
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u o
o ^
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Figure 19c.
100 120 140 180
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
200
Nonmelanoma Skin Cancer Incidence by UV-B Index
According to Anatomical Site Group Among White Females
Upper Extremities
20-
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200
Figure 19d. Nonmelanoma Skin Cancer Incidence by UV-B Index
According to Anatomical Site Group Among
White Females Lower Extremities
56
-------
In Figures 20 and 21 we see familiar patterns. Skin cancer incidence
increases as UV-B radiation increases for white males with and without
freckles. We also note that at each location the risk is greater for those
with freckles. The estimated relative risk adjusting for age and location is
'•8 and 1.7 for men and women, respectively, compared to those without
freckles.
The correlation for fair skinned complexion is illustrated in Figure
22. Again, the UV-B gradients are observed. Overall relative risk estimates
were 2.6 for men and 1.6 for women, respectively, compared to those without
fair skinned complexions.
Figure 23 shows the patterns for Celtics or those of Irish or Scottish
ancestry. Estimates of relative risk were the same as those observed for
individuals with freckles.
Other high-risk groups include individuals with blond or red hair color,
blue or green eye color, and those who sunburn easily; individuals treated for
acne, moles, warts or psoriasis; individuals exposed to radiation or radiation
therapy, Coal tar or pitch, and arsenic. Individuals at low relative risk
include those of Mexican or Spanish ancestry and those who are never outdoors
°n their principal occupation and those who develop deep tans.
With respect to the consistent excesses in skin cancer risk observed for
men compared to women, we noted that the average amount of time spent outdoors
was greater for males by a factor of 1.5 to 2.
, J am reminded of a statement made in a review article by our Chairman
(Emmett, CRC 1973). It said:
... in the USSR where the occupations.
of women nearly parallel those of men,
the incidence rates of skin cancer are
the same for males as for females
except in the elderly females who may
retain more domestic occupations. On
this basis, it may be unlikely that
the male human has a biological
predisposition to solar skin cancer.
In conclusion, I would add that this disease represents a major health
Tu i economic problem in the United States and other parts of the world
dev i6 to thirty percent of the Caucasians in this country may expect t
el°P skin cancer in their lifetime if current rates and trends persist.
to
57
-------
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2
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o
o
100
30
80
si
I I
I*1
••• —
I I
100 120 140 160 180
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
D
Legend
WITH FACTOR
I D WITHOUT FACTOR
200
Figure 20. Nonmelanoma Skin Cancer Incidence by UV-B Index
Among White Males According to the Presence or
Absence of the Factor "Freckles"
58
-------
1000
£
o
o
o
r wo-
30-
BO
— r
100
D
170 140 160 180
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
D
u — —
5 I S
Legend
• WITH FACTOR
D WITHOUT FACTOR
200
Figure 21. Nonmelanoraa Skin Cancer Incidence by UV-B
Index Among White Females According to the
Presence or Absence of the Factor "Freckles"
59
-------
tOOOn
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o
o
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SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
mo
Legend
• WITH fA.CTOR
D WITHOUT FACTOR
200
Figure 22a.
30-
Nonraelanoma Skin Cancer Incidence by UV-B Index
Among White Males According to the Presence or Absence
of the Factor Fair Complexion
Legend
• WITH FACTOR
D WITHOUT OkCTOR
100 120 WO 1(0 ISO
SOLAR ULTRAVIOLET RADIATION (UVB) INDEX
Figure 22b.
Nonmelanoma Skin Cancer Incidence by UV-B Index Among
White Females According to Presence or Absence
of the Factor Fair Complexion
60
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wo
11
li
Ji
legend
2 S S
O WITHOUT FMTOII
SOLAR UURAVKX£T RADWnON (UVB) WOEX
Figure 23a. Nonmelanoma Skin Cancer Incidence by UV-B Index Among
White Males According to Presence or Absence
of the Factor "Irish/Scot Descent"
Legend
• WITH FACTO*
U WITHOUT RCTOH
SOUR UURAVKMn RADIATION (UVB) INDEX
tie wo
Figure 23b.
Nonmelanoma Skin Cancer Incidence by UV-B Index
Among White Females According to the Presence or Absence
of the Factor "Irish/Scot Descent."
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Immunomodulation by Ultraviolet Radiation:
Prostaglandins Appear to be Involved in the
Molecular Mechanisms Responsible for UVR-
Induced Changes in Immune Function
R. A. Daynes, H. T. Chung, B. Robertson,
L- K Roberts, and W. E. Samlowski
University of Utah Medical Center
Salt Lake City, Utah USA
ABSTRACT
The experimental exposure of animals to sources of ultraviolet .radiation
that emit their energy primarily in the UV-B region (280-320 nm) is
to result in a number of well-described changes in the recipient's
immune competence. Two such changes include a depressed capacity to
srfectively respond immunologically to transplants of syngeneic UVR tumors and
a markedly reduced responsiveness to known inducers of delayed-type (DTH) and
Contact hypersensitivity (CH) reactions. The results of experiments that were
^signed to elucidate the mechanisms responsible for UVR-induced
iwmunomodulation have implicated: (a) an altered pattern of lymphocyt
^circulation, (b) suppressor T cells (Ts), (c) deviations in systemic
*ntigen presenting cell (APC) potential, (d) changes in the production of
interleukin-1-like molecules, and (e) the functional inactivation of epidermal
J^ngerhans cells (LCs) in this process. The exposure of skin to UVR,
therefore, causes a number of both local and systemic alterations to the
^normal host and its immune system. In spite of this seeming complexity and
Diversity of responses, our recent studies have established that each of the
"•WR-mediated changes is probably of equal importance to creating the UVR-
nduced imkmunocompromised state.
Normal animals were exposed to low-dose UVR on their dorsal surfaces
conditions where a 3.0 cm2 area of skin was physically protected from
light energy. Contact sensitization of these animals with DNFB, to either
the irradiated or the protected back skin, resulted in markedly reduced CH
responses. This was observed in spite of a normal responsiveness following
!;ne skin sensitization to ventral surfaces of the UVR-exposed animals Systemic
treatment of the low-dose UVR recipients with the drug indomethacin (1-3
Aerograms/day) during the UVR exposures resulted in a complete reversal of
the depression observed following DNFB sensitization to "protected" dorsal
skin while the altered responsiveness found in the group exposed to the skin
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reactive chemical through directly UVR-exposed site was maintained. These
studies directly implicate the importance of LCs as effective APCs in the skin
and also suggest that some of the systemic influences caused by UUR exposure
involve the productin of prostaglandins. This concept was further supported
by finding that indomethacin treatment was also capable of totally reversing
the systemic depressions in CH responsiveness caused by high-dose UVR exposure
(30 K joules/m2) of mice. Attempts to analyze the cellular mechanisms
responsible established that the spleens of all animals that demonstrated
altered CH responses, regardless of whether sensitization was through a normal
or an irradiated skin site, contained suppressor cells. Interestingly, we
also found normal levels of T effector cells in the peripheral lymph nodes of
the UVR-exposed mice that were contact sensitized through normal skin. No
effector cells were found when skin sensitization took place through
irradiated skin sites.
In spite of such an apparent paradox, insight into the probable
mechanisms responsible for these observations was provided by establishing
that UVR exposure of skin results in a striking and dose-dependent blockade of
the efferent lymphatic vessels in all peripheral lymph nodes. Therefore, the
afferent phases of immune responses can apparently take place normally in UVR-
exposed animals when antigen is applied to normal skin. The final effector
responses, however, appear to be inhibited in the UVR-exposed animals by an
apparent block of effector cell mobility. This contrasts with findings in the
normal animals. Following contact sensitization, normal animals were also
found to simultaneously contain both antigen specific suppressor T cells and
lymph node effector cells. However, these normal animals were fully capable
of mobilizing their effector cells into the systemic circulation, thereby
allowing a localization of these cells to peripheral sites of antigen
challenge.
Our results suggest that UVR is probably not a significant inducer of
suppressor T-cell activity to topically applied antigens. Rather, UVR
exposure appears to modify the normal relationship that exists between
effector and regulatory immune responses i_n vivo. It does so by one of two
mechanisms: The first causes a direct reduction in the skin's APC function
and results in an absence of effector cell generation to antigens applied to
UVR-exposed skin sites, inhibiting the capacity of effector cells to gain
access to skin sites of antigen challenge; the second sequesters the
lymphocytes with effector cell potential into the draining peripheral lymph
nodes. Each of these situations results in a similar effect on the UVR-
exposed host—a reduced capacity to elicit a CH response. We hypothesize that
altered DTH responses, altered alloresponses, and altered graft-versus-host
responses (all of which have been observed in UVR-exposed animals) may result
from similar mechanisms.
INTRODUCTION
Extensive literature describes the biologic changes that result from the
exposure of experimental animals and man to the effects of UVR. Many of the
reported studies focus on UVR-induced alterations of an exposed host's immune
system—definable alterations that have led to the genesis of the term
"photoimmunology" to describe this area of investigation. The field of
photoimmunology is proving to represent a correlative scientific discipline
that interrelates many areas of investigation including dermatology,
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immunology, photobiology, and physiology. The goal of investigators in
Pnotoimmunology is to understand the immunobiologic consequences of UVR
exposure to provide a clinically valid prediction of the potential benefits
and/or detrimental effects that are associated with the continued exposure of
skin to solar or artificially derived sources of UVR. Such information is
important for a variety of reasons. These include both the probability that
'"any biologic life forms on our planet may eventually be faced with increasing
aoses of UVR due to a reduction in the fidelity of the protective ozone layer
and the recent interest by many individuals to maintain a year-round tan
the use of artificial sources of UVR.
The major objectives of this review will be to consolidate many of the
observations that have been reported in the field of photo immunology during
the past few years. Many of the local and systemic changes that take place
Allowing the UVR exposure of skin will be described as they relate to changes
*n immunologic, histologic, pathologic, and physiologic processes. Our goal
is to develop the hypothesis that many of the immunologic consequences that
lollow acute or chronic UVR exposure actually reflect the body's mobilization
°£ a number of normal host defense mechanisms in response to the inflammatory
effects of this physical agent. A large body of recently acquired
experimental evidence will be presented to support this general hypothesis.
While our results do not support the concept that UVR-mediated effects on
immune function are unique, they do demonstrate the fact that the biologic
changes that manifest following skin exposure to this physical agent are quite
Diverse. The immunomodulatory influences of UVR, therefore, appear to result
Ir°m its capacity to affect a large number of interrelated biologic systems.
IMMUNOBIOLOGY OF EXPERIMENTAL UVR CARCIHOGEMESIS
is a known carcinogen for the induction of skin tumors in both
experimental animals and in man (Blum 1959; Fears, Scotto, and Schneiderman
'y'7; Tanenbaum et al. 1976). In addition to its carcinogenic properties, UVR
°an also function as a cocarcinogenic-promoting agent and an immunologic
modulator (Epstein and Epstein 1962; Elmets and Bergstresser 1982). It must
°e appreciated that associated with the transformation event are the
immunomodulatory effects of UVR that have a direct influence on the emergence
and progression of skin neoplasia (Fisher and Kripke 1982; Roberts and Daynes
y°°). Historically, the discovery that subcarcinogenic doses of UVR induce
a£ irmnunologic state of UVR tumor susceptibility in syngeneic mice suggested
lo?!kUVR was an immunomodulatory agent (Daynes et al. 1977; Kripke and Fisher
dl '• It is the tumor-permitting immunomodulatory potential of UVR that
J-stinguishes it from other carcinogenic agents.
UVR-induced tumors, like most experimentally induced tumors (e.g.,
°«emically and virally induced), express tumor-associated antigens (TAA) that
elicit specific immune responses in their syngeneic host (Roberts, Lynch,
Daynes 1982; Pellis and Kahan 1976; Leffell and Coggin 1977; Rogers and
tto 1985). For example, a state of tumor-specific immunity is induced in
mi°e that are immunized with syngeneic UVR-induced tumors (either fragments or
lines maintained in vitro) (Daynes et al. 1977; Roberts, Lynch, and
nes 1982; Kripke 19?T; Spellman and Daynes 1978; Roberts, Spellman, and
aynes 1980). This implies that the major rejection responses elicited in
.VInor- immunized hosts are directed toward unique tumor-specific transplanta-
lon antigens (TSTA). In addition, experiments employing hyper immunized
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animals have established that common tumor-associated transplantation antigens
(TATA) are also shared by different UVR tumors (Roberts, Lynch, and Daynes
1982; Spellman and Daynes 1978; Roberts, Spellman, and Daynes 1980). Thus, it
appears that any given UVR tumor expresses both unique and common TAA that are
capable of becoming involved in the host immune response to varying degrees.
The immune response elicited by these TAA dictates whether the tumor is
rejected or allowed to grow.
Aside from a few reports, very little is known about the biochemical
nature of the TAA expressed by UVR tumors. Employing tumor-reactive
monoclonal antibodies, DeWitt has identified a membrane-bound TAA that appears
to have a molecular weight of 200-300 KD (Daynes et al. 1985). Although the
exact biochemical nature of these antigens is not understood, preliminary data
suggest that one of these monoclonal antibodies recognizes a glycolipid moiety
(DeWitt, personal communication). Fortner et al. (1982) have reported that
UVR tumors express a virally encoded gp70 antigen on their cell surface.
Similarly, DeLuca et al. (1979) have reported that cross-reactive antibodies
in the serum of UVR tumor-immune mice have specificity for murine leukemia
viral products. Beeson, Scott, and Daynes (1983) have demonstrated the
presence of oncofetal antigens on UVR and chemically induced tumors that are
also expressed on placental and fetal tissues. These particular viral-
associated or oncofetal antigens could very easily function as cross-reactive
TAA. Finally, Ristau et al. (1980) have reported that UVR tumors express a
cross-reactive TAA that appears to be a 200 KD glycoprotein. Although these
studies have begun to identify some of the common TAA that are expressed by
UVR tumors, the exact biochemical nature and immunogenic properties of
individual TAA are currently unknown.
Unlike the tumors that are experimentally induced by chemical
carcinogens, a majority of the UVR-induced tumors are rejected when
transplanted into normal syngeneic hosts (Daynes et al. 1977; Kripke 1974;
Roberts, Bernhard, and Daynes 1984). These UVR-induced, regressor-type tumors
will grow, however, when implanted into immunologically compromised hosts or
syngeneic animals that have been exposed to subcarcinogenic doses of UVR
(Daynes et al. 1977; Kripke and Fisher 1976; Kripke 1974). Thus, it would
appear that the predominant immune response elicited by UVR tumors, when
implanted into normal syngeneic animals, leads to their rejection. A number
of mechanisms have been investigated to determine how UVR tumors are able to
escape the immune surveillance capability of their host.
Tumor rejection or progression is a dynamic process involving complex
interactions between the tumor and its host. Conditions that allow for tumor
progression are related to the inability of the host to mount an effective
immune response, as well as the capacity of the tumor to modulate its
tumorigenic potential in response to immunologic pressures. A number of
studies have been designed to investigate the ability of UVR tumors to
modulate their tumorigenic potential. Wortzel, Urban, and Schreiber (1984)
have analyzed immune responses elicited by the TSTA expressed on a UVR
regressor tumor and a number of epitope loss variants derived from that tumor
(Wortzel et al. 1983; Wortzel, Urban, and Schreiber 1984). Through the use of
cloned tumor-specific cytotoxic T-cell (Tc-cell) lines, these investigators
have provided compelling evidence that a number of TSTA epitopes are expressed
by a single UVR tumor. Furthermore, the loss of specific TSTA epitopes by
various tumor variants derived from the original tumor was found to be
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associated with the acquisition of a progressor phenotype, i.e., the capacity
to grow when implanted into normal syngeneic recipients. Thus, the loss of ah
immunodominant epitope(s) on a UVR-induced regressor tumor may represent a
Possible mechanism that allows for its progression. In this regard,
tumorigenic heterogeneity of UVR tumors was observed by Schmitt et al., who
isolated cloned lines from a UVR regressor tumor that was capable of
Progressive growth when transplanted into normal syngeneic recipients (Schmitt
and Daynes 1981; Schmitt et al. 1983). In addition, these investigators
determined that a UVR regressor clone could be converted from a regressor-type
tumor to one capable of progressive growth in normal recipients subsequent to
culture with normal lymphoid cells in vitro, or following passage through
inununologically compromised hosts (Schmitt et al. 1983). These investigators
also provided suggestive evidence that the regressor-to-progressor conversion
Process correlated with a somatic cell hybridization between cells of the
tumor and those of host origin. This is not a unique concept, since in other
tumor systems it has been shown that somatic cell hybridization correlates
"ith increased metastatic potential of the tumor (Kerbel et al. 1983; Larizza,
hirrmacher, and Pfluger 1984).
Although these studies would suggest that a UVR tumor is capable of
modulating its tumorigenic potential in response to the host immunologic
Pressures, it was necessary to confirm that UVR tumors were clonal in nature
arjd not derived from the progressive growth of both progressor and regressor
clones arising from multiple transformants with the tumor mass. To
investigate this possibility, Burnham, Gathering, and Daynes (1986) employed
the tool of x-chromosome inactivation mosaicism with the x-linke.d enzyme
Phosphoglycerate kinase 1 (PGK-1) to evaluate the clonality of UVR-induced
tumors. Out of thirteen primary UVR tumors that were induced in (C3HxC3H.PGK-
1 'pi heterozygote female mice, which phenotype as PGK-1a/b, all were found to
express only a single PGK-1 enzyme form. Based on this finding, it was
concluded that the majority of UVR-induced tumors are monoclonal in origin and
result from the progression of a single transformed cell. These experiments
also suggest that the heterogeneity observed within a single tumor with regard
^° its tumorigenic potential must arise from events taking place subsequent to
he original transformation process.
Although the ability to modulate TSTA epitopes and a certain level of
igenic heterogeneity within UVR regressor tumors indicates that these
rs may escape immunologic rejection through their ability to modulate
their growth characteristics in an immunologically competent host, the exact
mechanism of how these tumors are capable of emerging and progressing within
their autochthonous host is unclear. It is intriguing that UVR regressor
tumors are rejected when transplanted into normal syngeneic recipients, but
ar® capable of progressive growth in the autochthonous host as well as
ayngeneic animals that have been exposed to subcarcinogenic doses of UVR,
eaPecially since UVR-exposed animals appear to possess virtually normal
lnwiunologic competency (Spellman, Woodward, and Daynes 1977; Norbury, Kripke,
a^d Budmen 1977; Kripke et al. 1977). This suggests that UVR regressor tumors
ffcploy an escape mechanism(s) to evade the immunologic rejection response of
their host. Transplantation studies have shown that the progressive growth of
regressor tumors is, in certain cases, dependent on a population of UVR-
suppressor T cells (Ts-cells) (Spellman and Daynes 1978).
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In contrast to the Ts-cells that arise in response to the TSTA expressed
by progressor-type tumors (both UVR and chemically induced), the UVR-induced
Ts-cell population possesses functional antigenic specificity for a common TAA
that appears to be expressed by virtually all UVR tumors and some chemically
induced tumors (Roberts, Lynch, and Daynes 1982; Spellman and Daynes 1978;
Roberts and Daynes 1986). Because this population of Ts-cells arises prior to
the appearance of overt tumors, it appears that these Ts-cells dictate the
emergence and progression of these neoplasia. The functional characteristics
of this Ts-cell population, as well as the process for their induction, have
been the subject of recent investigations.
It has been shown that the regulation of immune responses to a number of
complex multideterminant antigens is mediated through the recognition of
distinct immunoregulatory epitopes (Yowell et al. 1979; Hashim et al.
1976). We have hypothesized that the immune response to UVR tumors may be
viewed in a similar context, since epitopes associated with the various types
of tumor antigens could function as either strong tumor rejection epitopes or
weak immunoregulatory determinants (Roberts and Daynes 1980; Roberts, Lynch,
and Daynes 1982; Roberts, Spellman, and Daynes 1980).
Thus, the UVR-induced Ts-cell population would function through an
associative recognition mechanism. Through its ability to recognize common
TAA expressed by virtually all UVR tumors, it would inhibit the development of
immune- rejection responses elicited by the stronger TSTA and other common
TATA. This hypothesis implies that the UVR-induced Ts-cell population is
homogeneous, i.e., consists of a single clone or limited number of clones of
Ts-cells that are restricted in their ability to recognize a common TAA
epitope. This has been confirmed by recent studies employing a number of
interleukin-2 dependent Ts-cell lines derived from animals that have been
exposed to subcarcinogenic doses of UVR (Roberts, Spellman, and Warner 1983>
Roberts 1986). In these studies, it was shown that both the parental and
cloned Ts-cell lines were capable of rendering normal syngeneic hosts
susceptible to the growth of a battery of UVR regressor tumors. In vitro,
these cloned Ts-cell lines appear to mediate their effect by inhibiting the
differentiation of Tc-cells from the draining lymph node (DLN) cell
populations obtained from tumor-immune mice. Thus, this Ts-cell population,
through its ability to recognize these common TAA, would provide an
immunologic environment that would allow for the emergence and progression of
virtually any neoplastic cell that expresses these antigenic determinants,
regardless of their expression of other stronger tumor rejection antigens.
Although the exact mechanism for the induction of the UVR-induced Ts-cell
population is unknown, previous studies suggest that neoantigens, which are
cross-reactive with TAA, are expressed in the skin of UVR-exposed mice
(Palaszynski and Kripke 1983; Spellman and Daynes 1984; Sielstad et al.
1985). Palaszynski and Kripke (1983) demonstrated that normal syngeneic mice
were rendered susceptible to the growth of UVR regressor tumors when grafted
with large pieces (5 cm x 2.5 cm) of skin from UVR-treated donors. In
contrast, Spellman and Daynes (1984) found that animals grafted with smaller
pieces (1 cm diameter) of UVR-exposed skin were effectively immunized against
a transplantable UVR tumor. In both studies, normal skin grafts failed to
produce any detectable immunologic alterations. We have recently detected TAA
cross-reactive antigens in cellular extracts from UVR-exposed epidermal cells
employing TAA-specific monoclonal antibodies in an enzyme-linked immunosorbent
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assay (Sielstad et al. 1985). Collectively, these studies strongly support
the contention that UVR induces TAA cross-reactive antigens in the skin before
the recognized emergence of neoplasia. It is conceivable that these skin-
associated TAA are responsible for eliciting the Ts-cell response that is
observed in animals that are exposed to subcarcinogenic doses of UVR.
We have recently conducted a series of experiments to further define the
imnmnogenicity of the cross-reactive TAA that are expressed in the skin of
UVR-exposed mice (Hong and Roberts 1986). A combined protocol of in vivo
immunization and in vitro culture of DLN cells was employed for the analysis
°f TAA-specific Tc-cells. For these studies, mice were first immunized by
injecting their footpads with viable tumor cells or skin cells. After eight
to ten days, the DLN were removed from these animals, and the cells were
suspended in tissue culture. After four days of tissue culture, the DLN cells
Were harvested and the Tc-cell activity was analyzed in a cell-mediated
°ytotoxicity assay. The results of these studies are summarized as follows:
* It was determined that Tc-cells capable of lysing cross-reactive
tumors differentiate from the DLN of UVR tumor and UVR skin-immune,
but not normal skin-immune mice.
* These Tc-cells are capable of lysing a range of tumor targets,
including syngeneic and allogeneic UVR tumors and syngeneic
methylcholanthrene-induced tumors. However, these cells did not lyse
Con A activated syngeneic lymphoblasts, thioglycolate-induced
peritoneal exudate cells, or YAC 1 lymphoma cells, which are sensitive
targets for the lysis by natural killer cells.
' Cold cell inhibition experiments demonstrated that these Tc-cells
recognize common cross-reactive TAA.
' The expression of these cross-reactive TAA in the skin of UVR-exposed
mice appears to be the direct effect of UVR exposure, since the only
cells that were effective in immunizing syngeneic mice against TAA
were those that were obtained from skin that was directly exposed to
the effects of UVR.
These studies were further expanded to characterize the immunogenic
Potential of the cross-reactive UVR tumor and UVR skin-expressed TAA. In
these experiments, cellular extracts (obtained by CHAPS detergent) from UVR
tumors and epidermal cells of either UVR-exposed or normal mice were
incorporated into liposomes for the immunization of normal syngeneic
animals. The lytic activity of four-day cultured DLN cells from these
immunized animals was compared with the DLN cells derived from mice immunized
with either whole cells or nonincorporated soluble cell extracts. The results
of these experiments indicated that the cross-reactive TAA expressed by UVR
^Pidermal or UVR tumor cells can elicit a Tc-cell response when incorporated
into liposomes and used to immunize normal syngeneic animals.
Although the levels of lytic activity were different, similar results
Were obtained when whole cells were used for immunization. In this study,
n°rmal epidermal cells did not display any appreciable level of TAA
exPression. Interestingly, soluble cell extracts alone were incapable of
eiiciting a Tc-cell response in the DLN of immunized mice. Therefore, in vivo
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experiments were conducted to identify the difference in the immunogenic
potential of whole cells, liposome-incorporated TAA, and soluble cell extracts
for the induction of TAA-specific Tc-cells. The results of these experiments
suggested that presentation of the antigens on a membrane surface is required
to elicit an effective immune response, while presentation of soluble antigen
alone may induce tolerance. In the first part of this study, groups of mice
were immunized repeatedly with viable epidermal cells obtained from UVR-
exposed or normal syngeneic donors. These immunized animals were then
challenged with a UVR progressor tumor that was capable of progressive growth
in untreated normal hosts, as well as in those animals that were immunized
with normal epidermal cells. However, mice immunized with UVR skin cells
rejected the UVR tumor implants. In a second series of experiments, groups of
mice received intravenous injections of soluble epidermal cell extract
obtained from UVR-exposed or normal syngeneic donors. These animals were then
challenged with a UVR regressor tumor. This tumor grew progressively in UVR-
treated hosts and was retained for an extended period of time in recipients of
soluble UVR skin cell extract. The tumor was rejected at a similar rate by
normal mice and recipients of soluble normal skin cell extracts. From these
studies, we have concluded that, similar to what was observed in vitro, cross-
reactive UVR skin expressed TAA that was capable of eliciting an in vivo
immune response. When presented to their host in a soluble form, these
antigens elicit a UVR tumor rejection response. When presented to their host
in a soluble form, these antigens elicit a UVR tumor tolerance reaction. This
supports' the possibility that by shedding a soluble cross-reactive TAA, UVR-
exposed skin cells may elicit the TAA-specific Ts-cells that arise in UVR-
treated mice before the appearance of any overt neoplasia.
In conclusion, the UVR-induced Ts-cell population appears to arise in
response to neoantigens in the skin of UVR-exposed animals. These Ts-cells,
by an unknown mechanism, suppress the ability of their host to mount an
effective immune rejection response to emerging neoplasia. As a result,
highly immunogenic tumors can emerge and progress to the death of the host
that would have otherwise been eliminated had the individual possessed its
normal immunologic potential. We have hypothesized that this particular
immunoregulatory network may have arisen as a mechanism to protect the host
during repair of UVR-damaged skin, i.e., that through an immunosuppressive
mechanism which is mediated by antigen-specific Ts-cells, damaged skin can
undergo repair processes without the elicitation of an autoimmune type
response. Through the ability of emerging neoplasia to express a common TAA
that is also expressed by UVR-damaged skin cells, they are able to use this
particular Ts-cell population as an immune surveillance escape mechanism.
Although not necessarily the sole mechanism for providing the growth of UVR-
induced tumors, this particular Ts-cell population does appear to be
responsible for the emergence and progression of a majority of UVR-induced
neoplasia.
THE EFFECTS OF UVR EXPOSURE ON THE SKIN AND ITS ASSOCIATED LYMPHOID TISSUE
It is now appreciated that many types of specialized immune responses are
initiated whose effector responses are primarily restricted to specific
anatomic compartments within the body. For example, those immune responses
that are associated with the gut-associated lymphoid tissue (GALT) and the
bronchial-associated lymphoid tissue (BALT) represent two well-described
examples of immunologic responses whose effector arms are anatomically
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compartmentalized. This anatomic restriction to both the afferent and
e*ferent mechanisms in GALT- and BALT-associated immune responses provides for
a means to achieve a marked enhancement to the protective capabilities of
these systems (Guy-Grand, Griscelli, and Vassalli 197M; Bienstock, Johnson,
and Perey 1979).
It has been proposed that an immunologic circuit exists that is dedicated
to the immune surveillance and protection of the skin (Streilein
This specialized circuit has been given the acronym SALT for skin-
associated lymphoid tissue. The evidence to support the existence of such a
specialized system is somewhat indirect and includes: the observed
®Pidermotropism for some subsets of normal and transformed lymphocytes, a
aem°nstration of the antigen presentation capabilities of certain epidermal
csU subsets, and a demonstration that antigen recognition and responsiveness
or iymphocytes can occur exclusively in the skin. In addition, this concept
18 supported by the knowledge that the integrating and regulatory elements
apable of controlling certain types of immune responses can be found, both in
IQO Skin itself, as well as in the draining peripheral lymph nodes {Streilein
y°5). it is quite probable that UVR- induced skin damage can mediate a
Pronounced alteration to the fidelity of the SALT system.
,. The elegant experiments performed by Macher and Chase (1969) established
at cells and/or soluble factors derived from hapten-sensitized skin were
squired in the development of a contact hypersensitivity (CH) response. This
"^k was followed by the finding, greater than ten years later, that the
majority of antigen presenting cell (APC) capacity of normal skin resides with
"e epidermal Langerhans cell (LC) (Stingl et al. 1978). Furthermore, the
JJPosure of experimental animals (Toews, Bergstresser, and Streilein 1980) or
^n (Cooper et al. 1985) to low doses of UVR in the UV-B range (280-320 nm)
s found to markedly reduce the number and functional properties of LC in the
t*Posed skin, with a parallel depression in the capacity of these individuals
y° elicit a CH response to skin-reactive chemicals applied directly to the
.•"-exposed skin sites (Toews, Bergstresser, and Streilein 1980).
nearest ingly, the exposure of animals to high doses of UVR (>10 KJ/m^) causes
WhfyStemic dePression in their ability to elicit a CH response, a condition
"lcn does not correlate with a reduction in LC presence or function at the
on-uVR-exposed sites of hapten application (Noonan, DeFabo, and Kripke 1981;
Wen, Gurish, and Daynes 1983). These two phenomena, local and systemic
oppression of CH responses, have been the object of intense investigative
Ifort over the past few years. In a later section of this review we will
scribe the results of recent experiments that implicate the formation of
acid metabolites in the mechanism(s) responsible for these changes
n immune function.
Greene et al. (1979) demonstrated that the UVR exposure of animals
in a decrease in their splenic APC potential. They concluded that
UvR-induced APC reduction was ultimately responsible for many of the
nornodulatory influences of UVR, including the acquisition of tumor
eptibiiity, the observed depressions in humoral and cellular immune
®sponses, and the reduced capacity of UVR-exposed animals to elicit CH
6P°nses> Subsequent investigations by Gurish, Lynch, and Daynes (1982)
that the UVR-induced reduction in splenic APC function was
by a marked increase in the APC activity within peripheral lymph
that drain the skin sites of UVR exposure. The results of these
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experiments suggested that the reported changes in APC function following UVR
exposure actually reflect a redistribution of APC from central to peripheral
lymphoid compartments. This was further supported by the finding that
splenectomized UVR-exposed animals did not demonstrate an increase in their
peripheral lymph node APC activity. Investigations by Lynch, Gurish, and
Daynes (1983) in mice and Cooper et al. (1985) in humans established that la-
positive cells with APC activity regain access to the epidermis by three days
following an acute UVR exposure. These cells may not be LC since the results
with humans indicate that the epidermis infiltrating cells are DR positive and
T6 negative. Collectively, the results of these experiments indicate that la-
positive cells with APC function are highly mobile in vivo. Under normal
conditions, the cell types having this functional and surface phenotype are
distributed among a number of distinct anatomic compartments. These include
the peripheral blood, spleen, lymph nodes, skin, as well as other tissue
sites. Exogenous stimulation of an animal with an inflammatory agent (i.e.*
UVH) results in: a functional inhibition of any directly UVR-exposed
immunocompetent cells and a marked anatomic redistribution of the cells with
APC potential, with enhanced numbers going to the tissue sites of inflammatory
insult. This is manifested by increased numbers of APC entering the skin, and
eventually localizing to draining peripheral lymph nodes following their
entrance via the afferent lymphatic vessels. This hypothesis is fully
consistent with the recent findings of Hendricks and Eestermans (1983) who
have analyzed the recirculation patterns of rat macrophages in vivo and
concluded that their entry into peripheral lymph nodes is predominantly
through afferent lymphatic drainage.
Studies performed by Spangrude et al. (1983) have established that the
exposure of normal mice to UVR results in a marked change in the lymphoid
tissue localization properties of recirculating lymphocytes. This is
reflected experimentally by a significant increase in the percentage of
intravenously injected radiolabeled lymphocytes recovered from the draining
peripheral lymph nodes of UVR-exposed animals. This UVR- induced alteration i"
lymphocyte localization patterns is quite protracted and persists for greater
than six weeks following the cessation of UVR exposure. Recent experimental
evidence has now provided us with an appreciation of the mechanisms that are
responsible for this effect. Immunohistologic staining of peripheral lymp&
node sections with the monoclonal antibody MECA-325, which is specific fof
high endothelial venules (HEV), revealed that the HEV content of lymph node*
from UVR-exposed donors is far greater than the HEV content of a similar lympt1
node from a normal animal (Samlowski and Daynes, unpublished). Since tb*
quantity of HEV in a lymph node dictates the rate of lymphocyte entry into the
tissue, an enhancement of HEV expression would result in an increase ifl
lymphocyte localization potential. This is due to the fact that HEV cental11
the lymphocyte recognition structures that are essential for the entrance of
lymphocytes into various types of lymphoid and nonlymphoid tissues (Gallatin»
Weissman, and Butcher 1983). Specific lymphocyte-HEV interactions have aW
been proposed to control the distribution of lymphocytes between peripheral'
mucosal, and central lymphoid organs (Butcher 1983).
It is now appreciated that the integrity of peripheral lymph node
(both the presence and the magnitude) is controlled by humoral or
factors that drain into the nodes via the afferent lymphatics.
conclusion was based on the results of studies that established that
of the afferent lymphatic vessels resulted in a disappearance of H6'
72
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structures in the draining lymph nodes (Hendriks and Eestermans 1983). This
reduction in HEV expression was followed by a markedly decreased rate of
lymphocyte entry into these manipulated nodes from the blood. Such experi-
ments suggest that the skin actually functions as a transducer, in some way
converting exogenous inflammatory stimuli into humoral and/or cellular signals
that have an influence on the presence and extent of vascular endothelium that
can function as lymphocyte-receptive HEV.
There are a couple of obvious candidates that can be considered important
in the transmission of HEV regulating signals from the skin to the lymph
nodes. These include the highly mobile macrophages and APC or their products,
as well as soluble mediators produced directly by cells within the skin in
response to an exogenous stimulation. Recent evidence from our laboratory
emphasizes each of these factors in the regulation of the lymphocyte content
°f a peripheral lymph node. We now appreciate that subsequent to the
treatment °^ animals with agents capable of interfering with macrophage
"unction {silica or carrageenan) or following surgical splenectomy, exogenous
Simulation with UVR does not result in an enhanced HEV expression. Such an
activity can be returned to a splenectomized animal by the adoptive transfer
°f adherent splenocytes prior to stimulation with UVR exposure (Chung and
jjaynes, unpublished). Therefore, the extent to which peripheral lymph node
HEV can be stimulated via an exogenous inflammatory insult appears to depend
°n the integrity of the animal's macrophage/APC function.
The lymphocyte content of a given lymphoid organ is a reflection of not
°nly the rate at which blood-borne cells are capable of entering the tissue,
Dut is also dependent upon the length of time that the lymphocytes are
sequestered within the lymphoid organ prior to gaining recirculation
Potential. We have recently determined that the exposure of animals to UVR
causes blockade in the efferent lymphatic vessels, a situation which results
ln the sequestration of lymphocytes within the lymph nodes draining the site
£" UVR exposure (Chung et al., submitted). A similar condition can be induced
ty the intravenous injection of murine and interferon into normal mice. Of
interest was the parallel finding that treatment of mice with indomethacin (1-
* vg/day) totally abrogated the development of the efferent blockade by UVR
and a/0 interferon. The efferent blockade caused by the direct injection of
P^ostaglandin E2 was not influenced by indomethacin injection, suggesting that
Prostaglandins were involved in the responsible mechanism.
In summary, the exposure of animals to UVR is capable of modifying many
components of the SALT system. Both macrophage/APC and the recirculation and
tissue localization properties of lymphocytes are equally affected. The role
Played by such changes in the modulation of immune responses by this physical
a8ent are currently unresolved, although the parallelism that exists certainly
3u8gests a cause-effect relationship to some of the observed changes.
PROINFLAMMATOHY PROPERTIES OF ULTRAVIOLET RADIATION
It is well recognized that animals exposed to UVR (especially UV-B)
undergo a pronounced and dosage-dependent inflammatory response. While the
cellular and molecular alterations in the skin that ultimately result in a
sunburn reaction are both numerous and complex, it is now appreciated that the
generation of biological mediators and the elaboration of cytokines by
73
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epidermal cells or infiltrating cell types may play an important role in the
immunomodulatory changes that are observed following UVR exposure.
Keratinocytes of the skin are capable of producing protein mediators
termed epidermal-derived thymocyte activating factor (ETAF), a group of
multifunctional hormones that are functionally, physiochemically, and
structurally identical to macrophage-derived interleukin-1 (IL-1) (Luger et
al. 1983). ETAF/IL-1 is now appreciated to function as a major mediator in
both immune and inflammatory responses (Luger and Oppenheim 1983). Based upon
the knowledge that number of inflammatory processes are initiated by UVR and
that the epidermal cells of the skin are a major target of this physical
agent, we have analyzed whether modifications in the levels of ETAF
production, plus a number of known host responses to this mediator, were
affected by UVR exposure. Our results established that UVR exposure does not
adversely affect ETAF production at subcytotoxic doses (Gathering et al.
1984).
Many biologic effects have been ascribed to the stimulation and release
of ETAF/IL-1 in vivo. ETAF and IL-1 can stimulate numerous target organs
throughout the body including the brain, bone marrow, liver, and lymphoid
organs. Target cell interactions with ETAF/IL-1 result in elevations in core
body temperature, the number of circulating neutrophils, the enhanced
production of acute phase proteins by the liver, as well as lymphocyte
activation and chemotaxis (Powanda and Beisel 1982; Moissec, Chai-Li, and Ziff
1984). Exposing mice to UVR results in an elevation in the number of
peripheral blood neutrophils as well as an increase in plasma concentrations
of several of acute phase proteins (Gathering et al. 1984; Dinarello 1984).
Further, ETAF/IL-1 can be detected in the serum of these animals 24 hours
after exposure to UVR. Since UVR exposure is inflammatory, and mononuclear
cells have been known to migrate into irradiated skin sites, we cannot
discriminate whether the observed elevation in acute phase proteins in vivo is
due to an increase in the production of ETAF by keratinocytes or is due, in
part, to IL-1 produced by macrophages that have infiltrated the sites of
inflammation.
A recent observation in our laboratory has provided insight into another
possible source of ETAF/IL-1. Normal murine and human stratum corneum
contains a substantial amount of ETAF/IL-1 (Gathering, Buckley, and Daynes
1985). The physiologic role of this stratum corneum-associated ETAF/IL-1
remains to be determined; however, one could speculate that it provides a
preformed pool of this mediator that is capable of initiating inflammatory
responses following wounding or subsequent to protocols that increase the rate
of percutaneous absorption. UVR is known to be capable of increasing the
percutaneous absorption of small molecular weight substances through the
skin. Therefore, keratinocyte production of ETAF, percutaneous absorption of
preformed mediator, and/or mononuclear cell production of IL-1 may all
influence the generation of a UVR-induced systemic inflammatory response.
We have demonstrated that daily exposure of mice to UVR results in an
increase in the production of acute phase proteins, and have speculated that
this is due to elevations in ETAF/IL-1. It is interesting to note that this
heightened response is followed by an eventual return to normal plasma levels
of these acute phase proteins despite a continued UVR exposure of the
animal. The cause of this "desensitization" to the effects mediated by UVR
74
-------
exposure is currently unknown. We have, however, established that
Keratinocytes obtained from a skin site exposed to daily UVR are still fully
capable of producing ETAF in vitro. While some control of ETAF/IL-1 effects
~£ vivo may reside at the level of the keratinocyte, the possibility that
®8ulation takes place at the site of action (e.g., liver, brain, etc.) or in
116 delivery system (plasma) of this important mediator also needs to be
considered.
ELATIONSHIP BETWEEN UVR EXPOSURE-INFLAMMATION AND MODIFICATIONS TO NORMAL
POTENTIAL
. In the preceding sections of this review article a number of known
romunologic, physiologic, and pharmacologic changes were described that take
Pface following the exposure of experimental animals to UVR. These
iterations include the acquisition of tumor susceptibility, a condition that
P^alieig overt tumor induction, suppressor T-cell induction, alterations in
"£crophage and lymphocyte components of the SALT system, plus the stimulation
both prostaglandin and ETAF/IL-1 mediated effects. When experimentally
. slyzed individually, each of these known changes which take place could
ndividually be hypothesized to have a modifying influence on the immunologic
Potential of an UVR-exposed host.
t It should be appreciated that UVR exposure of skin is capable of
itiating all of the reported changes simultaneously in the exposed host,
Baking it highly probable that significant overlaps, cause-effect
eiationships, and a number of biologic generalizations can be formulated.
urthermore, many of the changes inducible by UVR are not unique to this
infSlcal agent as -evidenced by the knowledge that a large number of distinct
/•""lammatory stimuli are capable of initiating a similar cascade of
and physiologic changes. In an attempt to support the concept
many of the apparently distinct immunomodulatory effects of UVR exposure
gl8nificantlv overlap with one another mechanistically, we will focus this
ectton on two immunologic changes that take place subsequent to UVR exposure.
, The experimental exposure of mice to UVR results in a marked reduction in
^eir capacity to elicit contact hypersensitivity (CH) responses to
UVR Utaneously applied skin-reactive chemicals. Mice exposed to low doses of
" (4 x 400 J/nr/day) demonstrate a reduced capacity to elicit CH responses
are site specific (localized to the skin areas of direct UVR exposure),
. as high-dose exposure of mice to UVR (15-30 KJ/m2) causes systemic
Iterations that leave the animals hyporesponsive to CH induction regardless
the skin site of hapten application (Toews, Bergstresser, and Streilein
^J Noonan, DeFabo, and Kripke 1981). Both of these types of UVR-mediated
ations have been previously reported to be associated with suppressor T-
^ - induction (Toews, Bergstresser, and Streilein 1980; Noonan, DeFabo, and
t ipke 1981). The capacity of low-dose UVR to depress the capacity of animals
Despond to skin-reactive chemicals has been concluded to be due to a direct
inactivation of LC by this physical agent (Toews, Bergstresser, and
1980). The state of systemic .suppression requires high doses of UVR
induction, and while it too is associated with the generation of hapten-
nv!!!!2^0 suppressor T-lymphocytes, it is not dependent upon a functional or
modification of the resident LC at the site of hapten application
and Daynes 1983; Morison, Bucana, and Kripke 1984). Due
to their ease of manipulation, these phenomena now serve as
75
-------
prototypes to help establish the mechanisms responsible for the immunologic
changes that follow UVR exposure.
It was originally concluded that a cause-effect relationship exists
between the functional inactivation of epidermal LC and the depression in CH
responsiveness that is observed following the exposure of animals to low doses
of UVR. While attractive, the validity of this hypothesis was dependent upon
the generalized capacity of low-dose UVR-exposed animals to respond normally
to skin sensitization at non-UVR-exposed sites. We therefore undertook an
experiment to test this prediction formally. Groups of normal mice were
exposed on their dorsal surfaces to UVR in low doses (400 J/nr/day). Each of
the animals had a small 3.0 cm2 patch of UVR opaque tape applied to a
specified dorsal skin site just prior to the irradiation treatment. A
phenotypic analysis of epidermal LC in the exposed, protected, and unexposed
skin sites confirmed that the tape treatment had protected the covered area
from UVR exposure. Subsequent to the UVR exposures, the treated animals were
divided into three groups and contact sensitized with DNFB. The first group
was sensitized through an unirradiated skin site on the abdomen. The second
group of animals was contact sensitized through an irradiated dorsal skin site
and the third group had hapten applied to the tape-protected dorsal skin
site. An additional group of normal animals were contact sensitized through a
normal dorsal skin site to serve as a positive control. All animals were
challenged with DNFB five days later. The results of this experiment (Table
1) established that UVR-exposed animals that had been sensitized through their
abdominal wall skin responded normally, a finding that is fully consistent
with the original observation (Toews, Bergstresser, and Streilein 1980).
Likewise, the animals that were contact sensitized through the irradiated
dorsal skin (LC deficient) exhibited a marked reduction in their capacity to
elicit a CH response. Interestingly, the animals that were contact sensitized
through the UVR-protected dorsal skin site were also found to be
hyporesponsive, in spite of the fact that LC density in this area of the skin
was totally normal. This finding suggested that LC inactivation by UVR is not
solely responsible for the reductions in CH responses elicited by these
animals.
We next questioned whether the known capacity of UVR to stimulate
prostaglandin synthesis was involved in the immunologic changes that were
taking place in low-dose UVR-exposed animals. This was based on the known
capacity of UVR to stimulate an increase in the systemic release of IL-1-like
molecules and to also cause both inflammation and pain (Gathering et al. 1984;
Eaglstein, Sakai, and Mizuno 1979). Two large groups of skin patch protected
mice were prepared and exposed to low doses of UVR. One group of the animals
to be UVR-exposed received a subcutaneously implanted pellet of indomethacin,
designed to deliver a daily dosage of 1.25 ug over a 20-day period. After
subjecting all experimental animals to the four daily UVR exposures, they were
segregated into four separate groups. One group of indomethacin-treated and
one group of untreated UVR-exposed mice were contact sensitized with DNFB
through irradiated dorsal skin sites. Likewise, a second group of
indomethacin-treated and a. parallel group of untreated UVR-exposed animals
were contact sensitized through the protected area on their dorsal skin
surface. To establish the effect of the indomethacin treatment, all experi-
mental and control groups were challenged with hapten five days later- The
results of this experiment. (Table 2) clearly demonstrate that the in vivo
inhibition of prostaglandin synthesis had no effect on the reduced capacity of
76
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Table 1. The Effect of Low-Dose UVR Exposure on Contact Hypersensitivity
Responses Elicited to DNFB
Sensitization Percent Depression
GrouP Sitea Treatment0 of CH Responses3
1
2
3
4
5
6
Abdomen
Back
Abdomen
Back
UVR-Shielded Backb
None
UVR
UVR
UVR
UVR
UVR
None
0
0
7.1
64.1
61.5
-
Normal C3H mice were contact sensitized with a solution of DNFB on day 0
and day 1 by topical application to their shaved ventral or dorsal skin
surfaces.
b
The UVR-shielded site was created by applying UVR-opaque tape to a
specified area on the dorsal skin of normal C3H mice.
o
Animals were exposed to UVR by irradiating them with a bank of six FS-40
bulbs which emit approximately 2.5 J/m2/sec of UV-B energy. All
experimental animals received 400 J/m2 of total energy per day for four
consecutive days.
d
Percent depression was calculated as a relationship to the positive normal
control.
Animals that were hapten sensitized directly through an irradiated skin site
^° elicit a CH response. In contrast, the reduced capacity of UVR-exposed
^imala to elicit a CH response following sensitization through a patch-
Protected dorsal skin site was not observed in the indomethacin-treated
group. These animals responded normally to the DNFB sensitization, suggesting
the diminished CH response to haptens applied to normal (UVR-protected)
sites depends on the mobilization of arachedonic acid and the
synthesis of its metabolites. Further studies confirmed that the plasma of
~VR-exposed animals contained elevated levels of PGE2 and that the
J-hdomethacin treatment of such animals inhibited this elevation in PGE2
Production.
We next turned our attention to the phenomenon of systemic suppression of
Contact hypersensitivity and hypothesized that the induction of this condition
®*-&\t also require the in vivo stimulation of prostaglandins. Two groups of
fJUmals were exposed to high-dose UVR (30 KJ/m2). Each individual from one of
"ese groups was given an indomethacin pellet to inhibit their capacity to
synthesize prostaglandins. After a three-day rest following the UVR exposure,
experimental animals plus a group of normal controls were contact
77
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Table 2. Indomethacin Treatment Abrogates the Immunodepression Observed
Following Contact Sensitization of Low-Dose UVR-Exposed
Animals Through Protected Skin Sites
Sensitization Percent Depressio"
Group Sitea Treatment0 Indomethacin" of CH Responses
1
2
3
4
5
6
Back
Back
Back
UVR-Shielded Backb
UVR-Shielded Back
None
None
UVR
UVR +
UVR
UVR +
None
0
61.8
62.3
60.5
3.6
_
a Normal C3H mice were contact sensitized with a solution of DNFB on day 0
and day 1 by topical application to their shaved ventral or dorsal skin
surfaces.
k The UVR-shielded site was created by applying UVR-opaque tape to a
specified area on the dprsal skin of normal C3H mice.
c Animals were exposed to UVR by irradiating them with a bank of six FS-40
bulbs which emit approximately 2.5 J/m2/sec of UV-B energy. All
experimental animals received 400 J/m2 of total energy per day for four
consecutive days.
^ Indomethacin treatment was accomplished via the subcutaneous implantation
of a pellet designed to release the drug at a constant rate of 1.25
yg/day for 20 days.
e Percent depression was calculated as a relationship to the positive normal
control.
sensitized with DNFB on their unirradiated ventral skin surfaces. Five days
later, all animals were challenged and the extent of ear swelling was
evaluated after 24 hours. The results of this representative experiment
(Table 3) clearly demonstrate that the ability of high-dose UVR exposure to
cause a systemic depression in CH responsiveness is inhibited by the treatment
of the test animals with indomethacin. These results strongly suggest that
the mechanisms responsible for UVR-induced systemic suppression of CH
responses involves the stimulation of prostaglandin synthesis.
Previous investigations have implicated hapten-specific T-suppressor (Ts)
cells in the mechanisms responsible for high-dose UVR-induced suppression of
CH responses (Noonan, DeFabo, and Kripke 1981). These conclusions were drawn
from the finding that the spleens of hapten-sensitized UVR-exposed animal3
contained hapten-specific Ts which, upon adoptive transfer to naive
recipients, were capable of causing a depression in the recipients' capacity
78
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Table 3. Indomethacin Treatment Prevents the Development of Systemic
Suppression of Contact Hypersensitivity Responses by High-Dose
UVR Exposure
Sensitization
Sitea
Back Skin
Treatment13
Indomethacin0
Percent
of CH
Depression
Responses"
Gr°up
1 Abdomen None - 0
2 Abdomen High-Dose UVR - 56.6
3 Abdomen High-Dose UVR + 6.4
^ None None
Normal C3H mice were contact sensiti2ed with a solution of DNFB on day 0
and day 1 by topical application to their shaved ventral or dorsal skin
surfaces.
Animals were exposed to UVR by irradiating them with a 100-watt mercury arc
lamp which emits approximately 500 J/m2 of UV-B energy. All experimental
animals received 15000 J/m2 of UV-B energy.
c
fhe indomethacin pellets used in this study delivered 2.5 yg of drug per
day.
d
Percent depression was calculated as a relationship to the positive normal
control.
a CH response to the immunizing hapten (Noonan, DeFabo, and Kripke
therefore questioned whether suppressor cell activity could be
Demonstrated in indomethacin-treated UVR-exposed animals subsequent to skin
ssnsitization. The results of our study determined (Table 4A) that the
Eduction of splenic suppressor cells represented a normal consequence of skin
Sensitization with the hapten DNFB. Not only was suppressor cell activity
Present in the spleens of high-dose UVR-exposed donors, regardless of
indomethacin treatment, but suppressor cell activity could also be found in
cne spleens of the DNFB-sensitized normal animals as well. Normal splenocytes
j °Ptively transferred into naive recipients were without inhibitory effect.
•n Parallel to an analysis of suppressor cell activity, the draining lymph
nodes were removed from both normal DNFB-sensiti2ed donors and high-dose UVR-
~*Posed DNFB-sensitized donors for adoptive transfer to naive recipients.
*his protocol tests for the development of effector cell potential. Recipient
animals were immediately challenged with hapten. The results (Table 4B)
ae«ionstrate that DNFB-sensitized high-dose UVR-exposed animals and DNFB-
ensitized normal animals generate an equivalent effector cell activity in
«eip peripheral lymph nodes. Our results, therefore, suggested that the
^pressed capacity of high-dose UVR-exposed animals to elicit a CH response
as not due to: apparent modifications in suppressor cell generation or a
^ePression in the capacity of these animals to generate effector cells in
eaponse to hapten application. Subsequent experiments, where UVR-exposed
were contact sensitized through irradiated or UVR-protected skin
79
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Table 4. Contact Sensitization of High-Dose UVR-Exposed Animals Results in
the Simultaneous Induction of Both Suppressor and Effector Cells
for CH Responses
A.
Group Donor Treatment3
1
2
3 None
4 High-Dose UVR
5 High-Dose UVR
Plus Indomethacin
B.
Group Donor Sensitization
1
2 +
3 +
Recipient Treatment13
Challenge
Sensitization Plus
Challenge
Sensitization Plus
Challenge
Sensitization Plus
Challenge
Sensitization Plus
Challenge
Donor Treatment6
_
+
High-Dose UVR
Percent
Suppression0
-
0
54.6
64.0
62.1
Percent
Normal Response
0
100
93.1
a Donor animals were untreated or exposed to high-dose UVR (30 KJ/m2) in the
presence or absence of indomethacin.
h 8
Recipient animals received 10 splenocytes from DNFB-sensitized donors.
The recipient animals were subsequently skin sensitized with DNFB.
c Percent suppression was calculated as a relationship to normal mice or mice
that received an adoptive transfer of normal cells.
Donor animals were footpad and belly sensitized with DNFB. Peripheral
lymph node lymphocytes (30 x 10 ) were adoptively transferred to naive
recipients that were immediately challenged with DNFB.
e Certain donors were exposed to high-dose UVR (30 KJ/m ) three days
previously.
<»
The capacity to elicit a CH response was calculated as a percentage of the
positive (normal) control.
80
-------
sites, determined that splenic suppressor cell activity was induced under all
conditions employed, while adoptively transferrable effector cell activity was
°nly found when skin sensitization took place through a skin site having
normal LC function (data not shown).
Insight into the mechanisms responsible for the depressed capacity of
uvR-exposed animals to elicit CK responses was derived from experiments where
normal, UVR-exposed, and indomethac in- treated UVR-exposed animals served as
recipients of CH-effector cells obtained from normal hapten-primed donors.
oth normal animals and the indomethacin-treated UVR-exposed groups were
of eliciting a demonstrable CH response. However, the UVR-exposed
of normal CH-effector cells exhibited a tremendous reduction in
capacity to manifest a CH response (Table 5). Therefore the capacity of
to inhibit the elicitation of a CH response to agents initially applied to
al skin sites does not appear to represent the result of a diminished
capacity of the animal to generate an immune response to the inducing
ten. Rather, the depressions in the intensity of CH responses observed in
-exposed animals appear to reflect some prostaglandin-induced alteration in
capacity of the effector arm of the CH response to function, possibly
gh a modification in lymphocyte receptiveness of the microvascular
?nd°thelium associated with the blood vessels at the specific site of a given
lmmunologic or inflammatory response.
GENERAL CONCLUSIONS AMD FUTURE DIRECTIONS
The major objective of this review was to present the interrelationships
exist between the seemingly diverse effects that UVR has on normal
and physiological processes. Each of these inducible changes
be similar mechanistically to those elicited by other types of
lnflammatory stimuli. Ultimately, the changes caused by UVR-exposure produce
condition in which immunologic responsiveness of animals is dampened, either
nrough the dominance of specific suppression following antigenic stimulation,
r due to intrinsic mechanisms that exist to functionally inhibit certain
jypes of effector cell responses. We have hypothesized that these
r"niunoregulatory responses are reflections of normal host defense
™echanisms. Such mechanisms may exist to protect the individual against the
Possible development of autoimmune conditions during the essential, repair
Processes taking place subsequent to the UVR-mediated damage to skin. While
erying to protect a host from possible autoimmune manifestations represents a
eneficial aspect of such processes, the creation of a condition where the
evelopment of immune responses is continually being suppressed would clearly
^ detrimental. This represents the condition that would take place under
Ituations of chronic UVR exposure. These could come about from either
mores, where individuals increase their daily exposure to solar or
UVR for personal or cosmetic reasons, or from a reduction in the
on of the ozone layer which currently provides a degree of protection
UVR.
. Photo immunology is providing the basic and clinical scientists with fresh
naight into the types of mechanisms which can operate in vivo to control
responses. It has long been appreciated that the molecular
ics and the mode of presentation of a given antigen to an
^Unocompetent host can play a significant role in the immunologic outcome of
an interaction. Likewise, it is known that an immune response can take
81
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Table 5.
00
NJ
UVR Inhibits the Capacity of Animals to Execute a Contact
Hypersensitivity Response in the Presence of Normal
Immunologic Potential
Experiment
Number Group
I 1
2
3
4
5
II 1
2
3
4
5
Adoptive Transfer
of DNFB-Primed
Treatment of Recipients3 Lymphocytes^
None
None +
Indomethacin +
15 KJ/m2 UVR +
15 KJ/m2 UVR + Indomethacin +
None
None +
Indomethacin +
15 KJ/m2 UVR +
15 KJ/m2 UVR + Indomethacin +
Ear Swelling0
4 ± 1
29 ± .5
27 ± .5
8 ± 2
25 ± .5
3 ± 1
28 ± 2
43 ± 4
9 ± 1
22 ± 1
Percent
Depression
of CH Response
0
0
8
84
16
0
0
0
76
24
a.
b.
c.
UVR was administered 3 days prior to the adoptive transfer of DNFB-primed lymph node cells. Indomethacin
pellets were employed which release 2.5 ug of drug/day.
Normal animals were sensitized with DNFB on their ventral surface, ears and footpads. Lymph nodes were
excised after 4 days and 30 x 106 cells adoptivelly transferred to the normal and treated recipients.
Ear swelling was measured 24 hours subsequent to DNFB challenge. 7« depression of the CH response was
calculated by comparing it to the positive control.
-------
forms, with both humoral and cell-mediated components functioning
simultaneously to either effectuate or regulate the type or intensity of a
given adaptive immunologic response. Photoimmunology, the effect of light
energy on immunologic responsiveness, has served to expand our understanding
°f immunologic control mechanisms. The importance of anatomic compart-
mentalization, the relationship between inflammation and adaptive immunity,
and the means by which suppressor cell dominated responses can be
preferentially stimulated are all apparent from the immunobiologic analysis of
the UVR-exposed host. Further, the use of UVR to alter a host's immunologic
Potential is now uncovering the role played by interleukin-1, prostaglandins,
steroids, and other hormones in many forms of immunologic control processes.
Such information should prove useful, both in the elucidation of the diverse
range of processes that interact to ultimately control the immune response, as
well as in the clinical manipulation of given immunologic situations.
While it is impossible to accurately predict the future of this
interesting field of study, the tremendous advancements made during the past
decade might be used as an indication of the future. Based upon the number of
diverse areas of investigation that are involved in the field of
Photo immunology, one might hypothesize that the future will bring significant
advances from both the basic and clinical sciences. These advances should
provide valuable information concerning the means by which environmental
influences can modulate the immunologic potential of a normal host, as well as
important insight into mechanisms that can be used to manipulate certain types
°* immunologic responses for clinical benefit.
ACKNOWLEDGMENTS
This work was supported by grant numbers CA306S, CA25917, CA22126, and
^34302, awarded by the National Cancer Institute, NIH.
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Stratospheric Ozone Depletion: Immunologic Effects
°n Monocyte Accessory Function in Humans
A. Elmets, Jean Krutmann,
th Rich, Hiroshi Fujiwara, and Jerrold J. Ellner
Western University
U|eveland, Ohio USA
Predicted increases in the amount of ultraviolet-B (UV-B) radiation
ing the earth due to stratospheric ozone depletion are likely to have
*|l8nificant impact on human health. One recently recognized target of UV-B
is the immune system. In particular, UV-B has been shown to render
phagocytes deficient in their ability to activate T lymphocytes to
and to soluble antigen. However, nearly all studies dealing with
deleterious effects of UV-B on immunological function have been conducted
7n sxperimental animals. The objective of this study was to characterize the
nfluence of UV-B radiation on human monocyte accessory function, which is
ssential for the initiation of cell-mediated immune responses. Human
J"eripheral blood monocytes obtained by plastic adherence were used as
r-°essory cells and were exposed in vitro to UV-B radiation from FS20 lamps.
,neir ability to induce a blastogenci response to either antigen (tetanus
°xoid) or mitogen (OKT3, PHA) when co-cultured with autologous. peripheral
°°d T lymphocytes that had been rigorously rendered accessory dependent was
as an index of their accessory cell function. Exposure of monocytes to
doses as low as 50 J/m2 inhibited the blastogenesis response to antigens
mitogens by 90% (p = 0.001). Viability of UVB-irradiated cells did not
GUI r slgnificantly from unirradiated monocytes over the initial 72 hours of
tht ' indicating that inhibition was not a result of a lethal effect on
ni-s cell population. The reduction in accessory activity was associated with
sti de°line in IL-1 activity in supernatants of UVB-irradiated, LPS-
'jimuiated monocytes. However, addition of exogenous IL-1 to cultures was
"8uffiCient to completely restore the blastogenesis response. UVB-
t.Padiation also rendered monocytes deficient in antigen processing. When
g 6V were exposed to antigen for 30 minutes before UV-B rather than after UV-
loss of> accessory activity was observed. Thus, UV-B radiation adversely
s the accessory function of human peripheral blood monocytes in antigen-
mitogen-induced activation of T lymphocytes. Deficient IL-1 production
imPaired antigen processing are at least partially responsible for this
These findings suggest that modification of the stratospheric ozone
87
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layer with resultant increases in UV-B penetration may have deleterious
effects on monocyte accessory activities in humans.
INTRODUCTION
Chronic exposure of the skin to solar ultraviolet radiation has a variety
of deleterious effects on human health (Harber and Bickers 1981). It causes
premature aging of the skin and is a well-recognized etiologic agent for
cutaneous squamous cell and basal cell cancers. In addition, there is an
increasing awareness that sun exposure may play an important role in the
development of malignant melanoma (Kopf, Kripke, and Stern 1984).
Recent studies performed in experimental animal models have demonstrated
that solar ultraviolet radiation also profoundly influences cell-mediated
immunity (Elmets and Bergstresser 1982; Daynes and Krueger 1983; Parrish,
Kripke, and Morison 1983). When animals are exposed to various doses of
ultraviolet radiation, they develop impaired immune responses to UVB-induced
skin cancers {Kripke 1974), to contact sensitizing agents (Toews et al. 1980}
Jessup et al. 1978), and to Herpes simplex virus {Howie, Norval, and Maingay
1986). A UVB-induced alteration in the function of accessory cells appears to
form the basis for such disturbances in cell-mediated immunity {Greene et al-
1979; Toews et al. 1986). These cells, of which macrophages and monocytes,
epidermal Langerhans cells, and splenic dendritic cells have been the most
thoroughly studied, are essential for the activation and expansion of helper ?
lymphocytes, an obligatory step in the initiation of immune responses.
Action spectrum studies have been performed to determine the wavelength
bands of solar ultraviolet radiation that are most efficient at producing
these immunologic alterations {Elmets, LeVine, and Bickers 1985; Schacter et
al. 1983; DeFabo and Noonan 1983). They have demonstrated that wavelengths
within the UV-B exert the greatest inhibition of cell-mediated immune
function. This is of imminent concern because the widespread use of
chloroflurocarbons in aerosols and refrigerants has been predicted to deplete
the atmosphere of ozone, which filters out solar UV-B radiation (Molina and
Rowland 1974). It is likely that stratospheric ozone depletion with resultant
increases in the amount of UV-B reaching the earth's surface will have a
significant impact on several aspects of human health, including an increase
in the incidence of diseases that require the immune system for protection.
The vast majority of evidence implicating UV-B as a causative agent in
deficient cell-mediated immune function, however, is derived from studies
conducted in experimental animals. Relatively little is known about the
immunological effects of UV-B in humans. We recently have conducted a number
of experiments to determine whether UV-B inhibits the function of
immunocompetent cells of humans in a manner similar to its inhibitory effec*
on the immunocompetent cells of animals. The cell type we chose to
was the human peripheral blood monocyte and the immunological function
elected to observe was its accessory activity. Studies in animals
suggested that the accessory function of macrophages and monocytes &.
profoundly altered following UV-B exposure {Greene et al. 1979). Accessory
activity is an obligatory first step in the initiation of all cell-mediate^
immune responses. This function is vitally important for a broad spectrum of]
sensitivity reactions, including immunity against tumors, and immunity t°
certain microbial agents including viruses and fungi.
88
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METHODS
Blastogenesis Assays
We assessed the function of accessory cells in antigen- and mitogen-
Induced blastogenesis assays. Accessory-dependent purified T lymphocytes
served as the responding cell population; peripheral blood monocytes were
employed as accessory cells; and tetanus toxoid (for antigen-induced assays)
and PHA or OKT3 (for mitogen-induced assays) served as the initiating stimuli.
T lymphocytes were purified by a three- or four-step procedure from
Peripheral blood mononuclear cells (PBMC) obtained from the heparinized blood
of healthy human volunteers by Ficoll-Hypaque (Pharmacia, Piscataway, New
Jersey) gradient centrifugation. PBMC were first allowed to adhere to 100 mm
tissue culture grade plastic petri dishes (Falcon, Oxnard, California) for 1-2
hours at 37°C in a 5% C02 incubator. Then the plastic non-adherent cells were
Pipetted off and incubated on acid-washed nylon wool columns (Fenwall
Laboratories, Deerfield, Illinois) for 45 minutes at 37°C. Finally, the
faulting T lymphocyte-enriched population was treated with a 1:50 dilution of
a monoclonal antibody to a framework determinant of the HLA-DR antigen (OKIA,
Ortho Pharmaceuticals, Raritan, New Jersey) and low toxicity rabbit complement
(Cedarlane Laboratories, Hornsby, Ontario). In some experiments, cells were
further depleted of accessory cells by treatment with a 5 mm concentration of
L-leucine methyl ester (L-LME, Sigma Chemical Co., St. Louis, Missouri) for 40
Minutes at 22°C. When L-LME was employed, it was used prior to treatment with
anti-HLA-DR and complement. The resulting population of T cells was
accessory-dependent and was completely unresponsive to antigen (tetanus
toxoid} and mitogen (OIT3, suboptimal doses of PHA).
Accessory cells were obtained by dislodging those cells that remained
adherent to the plastic petri dishes in the first step of the T lymphocyte
Purification procedure. This population was 85/&-90/S peroxidase positive and
f°P the purposes of this discussion will be called peripheral blood monocytes.
Tetanus toxoid (a gift from Lederle Laboratories, Pearl River, New
Jersey) was used as the antigen in soluble antigen-induced T cell
olastogenesis assays. Suboptimal concentrations of phytohemagglutinin (PHA,
Qibco, Grand Island, New York) or OKT3 (Ortho Pharmaceuticals, Raritan, New
Jersey) were used as mitogens in mitogen-induced blastogenesis assays.
In the blastogenesis assays, 2 x 104 monocytes were cultured with 1 x 10^
T lymphocytes and with either tetanus toxoid, PHA, or OKT3 in 96 well
""i-crotiter plates (Corning, Corning, New York). In all the experiments
Described, only autologous combinations of monocytes and T cells were
en>Ployed. All variables were performed on triplicate wells. Cultures in
tetanus toxoid as used as the stimulus were incubated for 5 days; those
which OKT3 or PHA was used as the stimulus were cultured for 3 days. Each
was pulsed with 1 microCurie of tritia'ted thymidine for the final 18
hours of the culture period. Incorporation of tritiated thymidine into
Proliferating cells was used as an index of T lymphocyte activation. Data
Were expressed as cmp = (cmp of cultures containing antigen or mitogen) - (cpm
of unstimulated cultures).
89
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UV Irradiation of Cells
One x 106 cells in 1 ml of colorless HBSS without Ca+2 and Mg+2 (KC
Biological, Lenexa, Kansas) were irradiated in 35-rom tissue culture plates
with a bank of four FS20 fluorescent UV-B bulbs (Westinghouse Electrical
Corp., Bloomfield, New Jersey). These lamps have an output primarily in the
UV-B range. Output in the UV-B at a tube to target distance of 21 cm was
approximately 1.7 x 10~* W/cm. Output was monitored with an IL700 Research
Radiometer and SEE 240 UV-B photodetector (International Light, Newburyport,
Maine).
Interleukin-1 Production and Bioassay
Peripheral blood monocytes were prepared as described above and were
cultured at a concentration of 5 x 105/ml in RPMI-1640 plus 2% PCS. One ml
was cultured per 16 mm Linbro plate well in the presence or absence of E. coll
lipopolysaccharide (LPS) 10 ug/ml (Difco, Detroit, Michigan). After 24 hours,
the well contents were aspirated and the supernatants filtered through 0.22
micron filters.
Interleukin-1 (IL-1) activity was assessed by placing the supernatants in
the thymocyte proliferation bioassay. Briefly, 100 microliters of supernatant
was added to round bottom microtiter wells containing 1.5 x 10" thymocytes
prepared from the thymuses of 8-12 week old female CSH/HeJ mice (Jackson Labs,
Bar Harbor, Maine). The plates were incubated for 72 hours, and the amount of
tritiated thymidine incorporated into proliferating cells during the final 6
hours of culture was used as an index of IL-1 activity. IL-1 activity was
calculated by modified probit-type analysis and was expressed as U/ml
according to the method of Luger et al. (1982).
RESULTS
Requirement for an Aocessory-Cell-Dependent System to Demonstrate UV-B Effects
on Monocyte Accessory Function
In our initial studies we found that it was essential to employ an
accessory-cell-dependent system to demonstrate UVB-induced defects in monocyte
accessory function (Table 1). Cells that had been adhered to plastic and then
passed over nylon wool were not accessory-dependent; some proliferation of T
cells occurred to tetanus toxoid even without the addition of accessory cells
(group I). The addition of unirradiated autologous monocytes to cultures,
however, significantly augmented the response (group II). Only moderate
inhibition of blastogenesis could be demonstrated when UVB-irradiated
monocytes were added to nonaccessory-cell-dependent nylon wool nonadherent T
cells (group III). On the other hand, when cells were additionally treated
with anti-HLA-DR and complement, there was a reduction in T cell proliferation
T background levels (group IV). The response could be reconstituted by the
readdition of autologous monocytes (group V).
90
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Table 1. Requirement for an Accessory Dependent System to Demon-
strate UV-B Effects on Monocyte Accessory Function
Group
I
II
III
Cell Cultures'
Responding T
Cells
NWE'
NWE
NWE
Accessory
Cells
None
Un1rrad1ated
Monocytes
UVB Irradiated
Monocytes
Initiated Thym1d1ne
Incgrporat1on
(xlO~JCMP + S.D.)
5183 ± 2592
11,523 ± 1591
9311 ± 1735
IV
V
VI
HLA-DR Treated'
HLA-DR Treated
HLA-DR Treated
None
Un1rradlated
Monocytes
UVB-Irrad1ated
Monocytes
712 ± 624
12,185 ± 2103
965 ± 743
t* 10 T cells were cultured with 2x10 monocytes with optimal amounts of
Jetanus toxold for 5 days.
NWE - nylon wool enriched T lymphocytes; HLA-DR treated - T cells
PuMftec| by plastic adherence, nylon wool columns and treatment with HLA-DR
complement. 2
Monocytes were exposed to 50 J/m UVB.
91
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UVB-irradiated monocytes were unable to reconstitute the response to
tetanus toxoid when T cells had been rendered accessory-dependent (group
VI). This contrasts with what was observed when UVB-irradiated monocytes were
added to cultures containing responding nonaccessory-cell-dependent T
lymphocytes (group VI vs. group III).
Inhibition of Human Monocyte Accessory Functionjay UV-B Radiation
Using this accessory-dependent system, we examined whether in vitro
exposure of human peripheral blood monocytes to UV-B radiation inhibited their*
ability to serve as accessory cells for T cell responses to the soluble
antigen tentanus toxoid. As shown in Table 2, there was a dose-dependent
inhibition in T cell responses when monocytes -were irradiated with increasing
doses of UV-B. A dose of 50 J/m2 was sufficient to inhibit the response by
greater than BQ%. This is less than one half the UV-B dose that would cause a
mild sunburn in a fair-skinned individual following outdoor recreational
activity and can be easily achieved in the dermal vasculature as monocyte
cells circulate through the skin.
Inhibition of accessory cell function was due to a nonlethal effect of
UVB. At 50 J/m2 there was no significant difference in viability, as assessed
by trypan blue exclusion, between uhirradiated and UVB-irradiated monocytes
over the entire duration of the culture period.
These experiments indicated that, similar to animal models in which UV-B
radiation had been shown to preferentially inhibit the accessory function of
macrophages and epidermal Langerhans cells for soluble antigen, this form of
radiant energy also altered the accessory function of human peripheral blood
monocytes for tetanus toxoid.
Effects of UV-B Radiation on Accessory Signals Required for Human T Lymphocyte
Activation by Tetanus Toxoid
Monocytes and other accessory cells contribute at least three essential
signals for T lymphocyte activation (Unanue et al. 1984). First, they express
large amounts of HLA-DR antigens on their cell surface. These molecules serve
as interaction structures between the accessory cell and the responding T
lymphocyte. Second, they produce the soluble cytokine interleukin-1, which is
a necessary co-factor required for T cell activation. Finally, accessory
cells take up antigen, degrade it, and re-express it on the cell surface in an
antigen processing step. Because UV-B radiation inhibited the accessory
function of monocytes by a non-lethal insult to the cell, we next performed
studies directed at examining which of these signals essential for T
lymphocyte activation was inhibited by UV-B.
We first assessed the capacity of human peripheral blood monocytes to
produce interleukin-1 following UV-B exposure. Peripheral blood moncytes were
exposed in vitro to doses of UV-B ranging from 0 to 300 Jm2 and were then
placed in culture with LPS, which served as a stimulus for IL-1 production.
Twenty-four hours later the supernatants were removed from these cultures and
were examined for IL-1 activity in the thymocyte proliferation bioassay. A3
92
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Table 2. Dose-Dependent Inhibition of Tetanus Toxoid-
Induced T Lymphocyte Blastognesis by UV-B1
UVB Dose Initiated Thymldlne
9
(J/m ) Incorporation
(x 10"3 CPM ± SD)
0 24650 ± 11466
10 16370 + 4182
25 14760 ± 3392
50 2556 ± 2042
150 731 ± 138
300 469 ± 114
Monocytes vere used as accessory cells, were exposed to various doses of
UV-B, and placed in culture for 5 days with purified T cells and tetanus
toxoid in the tetanus toxoid-induced T lymphocyte blastogenesis assay.
93
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shown in Figure. 1, unirradiated tnonocytes were able to produce large amounts
of IL-1 when stimulated by PLS. There was a marked decline in IL-1 activity,
however, in supernatants derived from UVB-irradiated monocytes. A dose of 50
J/ra2 UV-B reduced the activity by greater than 95/1, which corresponded to the
UV-B dose that also caused marked inhibition of proliferation in the
blastogenesis assay.
To determine whether deficient IL-1 production was the only accessory
defect that was present in UVB-irradiated monocytes, experiments were
performed in which recombinant murine IL-1 was added back to the blastogenesis
cultures in an attempt to reconsititute the response (Figure 2). Murine
recombinant IL-1 was not able to substitute for monocytes in the blastogenesis
assay (group II). It also failed to augment the response in cultures
containing unirradiated monocytes, T lymphocytes, and tetanus toxoid (group
IV). Only partial reconstitution of the tetanus toxoid response was observed
when this reagent was added to cultures containing UVB-irradiated monocytes,
purified T cells, and tetanus toxoid (group VI). We thus concluded that
although UV-B radiation inhibited IL-1 production by monocytes, deficient IL-1
production was not the sole accessory defect that occurred following UV-B
exposure.
Next, we tried to examine the effect of UVB on antigen processing. In
these experiments, monocytes were preincubated with tetanus toxoid for 30
minutes before UV-B exposure. Following irradiation, responding T lymphocytes
were added to the cultures. The reasoning behind this experiment was that
exposure of monocytes to antigen prior to UV-B might allow the accessory cells
to take up and to process antigen before UV-B inhibited the antigen processing
step; and therefore reconstitution of the response might occur. As shown in
Figure 3, only slight inhibition of the response occurred when accessory cells
were treated in this manner. The fact that monocytes became resistant to
inhibition by UV-B when exposed to tetanus toxoid for a period of time
sufficient to allow for antigen uptake and processing, suggests that UV-B may
have an effect on antigen processing.
Effects of UV-B Exposure on the Ability of Human Monocytes to Activate _I
Lymphocytes to Mitogen
Accessory cells are also required for mitogenic activation of T
lymphocytes. However, the accessory signals required for T cell activation by
mitogen differ somewhat from those required for antigens. While both antigens
and mitogens are thought to require IL-1 production for optimal T cell
activation, mitogens, unlike antigens, do not require a processing step. We
therefore performed experiments to assess whether UV-B irradiation of
accessory cells inhibited the mitogenic activation of T lymphocytes. In these
studies, OKT3 or PHA served as the mitogenic stimulus. Mitogens were placed
in culture with UVB-irradiated monocytes and purified T cells and the
blastogenesis response was determined three days later. Similar to what was
observed for tetanus toxoid, there was a dose-dependent inhibition of T cell
proliferation to suboptimal doses of PHA when increasing UV-B doses were
administered (Figure 4). Dose-dependent inhibition also occurred when OKT-3
was used as the mitogenic stimulus (Figure 4). With both of these mitogens, a
UV-B dose between 50 J/m2 and 100 J/nr was sufficient to inhibit the T cell
94
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9
_
6
I 2
- g. 2
8
£ 0
Monocytes -
IL-1
Column I
No UVB No UVB UVB
II
III
IV
UVB
VI
Figure 1. IL-1 production by UVB-irradiated monocytes. Peripheral blood
™°nocytes were UVB-irradiated and then placed in culture with LPS. Twenty-
°ur hours later the supernatants were removed and assayed for IL-1 activity
the mouse thymocyte bioassay.
50
250
300
100 150 200
UVB Dose (J/m2)
to Fi8ure 2. Incomplete reconstitution of UVB-induced inhibition of tetanus
^ ^id-induced T lymphocyte blastogenesis by recombinant murine IL-1.
nuiC?SSOry cells (unirradiated or UVB-irradiated) and/or 10/Um' recombinant
to IL-1 were added to cultures containing purified T cells and tetanus
, x°id. Cultures were incubated for 5 days in the tetanus toxoid-induced T
blastogenesis assay.
95
-------
Monocytes
NoUVB
Pre-exposure to
Tetanus Toxold
UVB-treated
UVB-treated
2468
Trltlated Thymidlne Incorporation
(x10'3cpm ± SD)
Figure 3. Development of resistance by monocytes to UV-B effects on
accessory function by preculture with antigen. Accessory cells were placed in
culture with tetanus toxoid (Panel C). Thirty minutes later the cells were
UVB-irradiated with 50 J/ra2. T lymphocytes were then added and cultured for 5
days in the tetanus toxoid-induced T lymphocyte blastogenesis assay. Control
panels were included in which accessory cells were unirradiated and received
no pre-exposure to tetanus toxoid (panel A) or were UVB-irradiated and
received no pre-exposure to tetanus toxoid (panel B).
OKT3
PHA
100 150 200 250
Ultraviolet-B Radiation, J/m2
300
Figure 4. Dose dependent inhibition of T lymphocyte blastogenesis
responses to mitogens by UV-B. Accessory cells were exposed to various doses
of UV-B and then placed in culture for 3 days with purified T cells and with
either PHA or OKT3 in a T lymphocyte blastogenesis assay.
96
-------
Response by greater than 90?. This UV-B does was almost identical to the UVB
dose that inhibited the T cell response to tetanus toxoid.
We then attempted to reconstitute the mitogenic response to OKT3 with IL-
'• For these experiments, recombinant human IL-1-alpha and IL-1-beta were
obtained and were added to cultures containing OKT3, purified T cells, and
JVB-irradiated monocytes. Despite the fact that both IL-1-alpha and IL-1-beta
significant bioactivity in the thymocyte proliferation assay, these
were unable to augment the T lymphocyte response to OKT3 (Figure
'• These findings indicated that even for mitogens, IL-1 was insufficient to
^constitute the T cell response. The fact that mitogens are not processed
a^ *^-1 could not reconstitute the response implies that UV-B exposure
affected an additional, as yet undefined, signal required for T cell
a°tivation in addition to IL-1 production and antigen processing.
Additions to Cultures of
^Purified T cells A OKT3
Accessory cells IL-1
+ (0 J/m2)
+ (100 J/m2)
* (100 J/m2) IL-1a(100u)
+ (100 J/m2) IL-1|5(10u)
1,000 2,000 " 90,000
Tritiated Thymidine Incorporation
(x 10-3 cpm±SD)
mit- FiSure 5. Incomplete reconstitution of UV-B induced inhibition of
itogen-induced T lymphocyte blastogenesis by human recombinant IL-1.
ant human IL-1-alpha or IL-1-beta was added to OKT3-induced T
ocyte blastogenesis assays.
97
-------
DISCUSSION
These studies have shown that jin vitro exposure of human peripheral blood
monocytes to UV-B radiation inhibited the accessory signals required for
antigen-induced and mitogen-induced activation of T lymphocytes. Inhibition
occurred at UV-B doses that were sublethal for monocytes. Inhibition of
accessory function was due both to deficient IL-1 production and to impaired
antigen processing by UVB-irradiated monocytes.
An additional, as yet unidentified, monocyte-derived accessory signal
also appeared to be affected following UVB exposure. This was based on the
finding that although IL-1 production by UVB-irradiated monocytes was
diminished, the readdition of exogenous IL-1 was insufficient to reconstitute
the T cell response to the mitogen OKT3. Because OKT3 is not processed by
monocytes, the lack of a response cannot be attributed to a processing defect.
One possibility for this additional signal is an alteration in HLA-DR
antigen expression and/or function. HLA-DR antigens are thought to function
by forming complexes with processed antigenic moieties, and thus enabling the
recognition of these antigenic moieties by responding T lymphocytes. Perhaps
UV-B radiation reduces the number of HLA-DR antigens on the cell surface,
produces alterations in the ability of UVB-irradiated HLA-DR molecules to bind
processed antigen, or impairs the recognition of HLA-DR antigens by responding
T cells. Alternatively, UV-B exposure may disturb membrane-associated IL-1
activity. Recent studies by Kurt-Jones et al. (1985) have shown that
paraformaldehyde-fixed macrophages are capable of presenting antigen to T
lymphocytes despite their inability to release IL-1. These cells express an
IL-1-like substance on their cell membrane and this membrane-associated
molecule may play an important role in T cell activation. Thus, an alteration
in membrane-associated IL-1 could also explain why UVB-irradiated monocytes
fail to function as accessory cells.
These studies have important implications with respect to stratospheric
ozone depletion. The immune system plays a fundamental role in protecting
individuals against noxious microorganisms and provides a surveillance
mechanism against neoplastic cells as they arise. Because stratospheric ozone
performs the beneficial function of filtering out harmful UV-B, destruction of
this component of the atmosphere would increase UV-B at the earth's surface.
The observations of this study, in which we have demonstrated a UVB-induced
impairment of immune function in human monocytes, suggest that deficient cell-
mediated immunity will be a major contributing factor to the postulated
adverse effects that stratospheric ozone depletion has on human health. UVB-
induced immune deficiencies might be expected to result in rising rates of
cutaneous and possibly other malignancies, and may produce increases in the
incidence of illness caused by viruses, fungi, and other microbes.
ACKNOWLEDGMENTS
These studies were supported by grant AM32593 from the National
Institutes of Health. The excellent secretarial assistance of Carol Highsmith
is greatly appreciated.
98
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REFERENCES
Daynes, R.A., and G. Krueger. 1983. Experimental and clinical phoboimmuno-
IORV. Vol. 2. Boca Raton, FL: CRC Press.
De Fabo, E.G., and P.P. Noonan. 1983. J. Exp. Med. 157:84-98.
, C.A., and P.R. Bergstresser. 1982. Photochem. Photoblol. 36:715-19.
, C.A., M.J. LeVine., and D.R. Bickers. 1985. Photochem. Photobiol.
42:391-98.
, M.I., M.S. Sy, M.L. Kripke, and B. Benacerraof. 1979. Proc. Nabl.
Acad. Sci. U.S.A. 76:6592-95.
Harber, L.C., and D.R. Bickers. 1981. Photosensitivity diseases: Principles
of diagnosis and treatment. Philadephia: W.B. Saunders.
Howie, S., J. Norval, and J. Maingay. 1986. J. Invest. Dermatol. 86:125-28.
Jessup, J.M., N. Hanna, E. Palaszynski, and M.L. Kripke, 1978. Cell
Immunol. 38:105-15.
t
A.W., M.L. Kripke, and R.S. Stern. 1984. J. Am. Acad. Dermatol.
11:674-84.
KriPke, M.L. 1974. J. Natl. Cancer Inst. 53:1333-136.
Kurt-Jones, E.A., D.I. Seller, S.B. Mizel, and E.R. Unanue. 1985. Proc.
Natl. Acad. Sci. U.S.A. 82:1204-08.
Luger, T.A., B.M. Stadler, B.M. Luger, B.J. Mathieson, M. Mage, J.A. Schmidt,
and J.J. Oppenheim. 1982. J. Immunol. 128:2147-52.
M°lina, M.J., and F.S. Rowland. 1974. Nature. 249:810-12.
Parrisn, J. A., M.L. Kripke, and W.L. Morison. 1983. Photoimmunology. New
York: Plenum.
Schaeter, B., M.M., Lederman, M.J. LeVine, and J.J. Ellner. 1983. «L.
Immunol. 130:2484-87.
Thiele, D.L., M. Kurosaba, and P.E. Lipsky. 1983. J. Immunol. 131:2282-90.
, G.B., P.R. Bergstresser, J.W. Streilein, and S. Sullivan. 1980. J_..
Immunol. 124:445-453.
e, E.R., D.I. Seller, C.Y. Lu, and P.M. Allen. 1984. J. Immunol.
132:1-5.
99
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Effects of UV-B on Infectious Disease
Suzanne Holmes Giannini
Columbia University College of Physicians and Surgeons
New York, New York USA
PRODUCTION
The skin is our interface with the environment and our bodies' first line
defense against infectious agents. Other papers in this volume illustrate
Qt"y elegantly that UV-B irradiation has a selective, suppressive effect on
immune system functioning. They show us, further, that the skin itself is an
nanune organ, in that certain types of lymphoid cells are found predominantly
n skin (Daynes et al. this volume; De Fabo and Noonan this volume; Elmets et
*J-« this volume). The function of this skin-associated lymphoid tissue is to
espond to antigens that enter the body by way of the skin. This cutaneous
surveillance system is vital to our ability to resist invasions by
lnfectious agents.
Infectious diseases remain serious public health problems in the tropics
nd semitropics. These are the geographic areas that also receive the highest
of solar UV-B radiation in the world (Schulze 1970). A critical
arises: What are the effects of UV-B irradiation on the body's
6sPonse to infectious agents penetrating the skin?
There are few experimental data to answer this important question.
is further complicated because infection and disease outcome are
ed> not only by the immun°genetic background of the host, but also by
6f* environmental factors such as humidity, temperature, vector density and
tficiency, concomitant infections, and host nutrition, to name but a few.
> though the issue is very complex, a growing body of evidence suggests that
»-B irradiation can affect both pathogenesis and immunity in infectious
involving skin.
EFFECTS OF UV-B ON THE CUTANEOUS PHASE OF INFECTIOUS DISEASES
, The effect of ultraviolet radiation on the progression of skin disease
as been the subject of investigation for almost a century. In the late
101
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1880s, the Danish physician Niels Finsen began a study of the interaction of
skin with sunlight. By a series of experiments in which various wavelengths
were filtered out from sunlight, he concluded that it was the ultraviolet
component, which he called the "chemical rays," that caused inflammation and
sunburn. In 1894, Finsen reported that the "chemical rays" of sunlight
promoted scarring in smallpox, and that patients sequestered in rooms thickly
hung with red curtains healed their pustules without scarring (Finsen 1901a).
This illustrated that solar radiation could affect the outcome of infectious
disease, and launched him on a study of ultraviolet radiation in the treat-
ment of tuberculosis (Finsen 1901b). In 1903, Finsen received the Nobel Prize
in Medicine for successful treatment of lupus vulgaris (tuberculosis of the
skin) by local application of ultraviolet irradiation. Over the next four
decades, ultraviolet light applied locally to skin was used to treat a variety
of infectious diseases, including erysipelas, which had a 10$ fatality rate
until UV therapy appeared (Licht 1983). The advent of sulfones and
antibiotics supplanted UV therapy, which has virtually disappeared from the
infectious disease armamentarium.
As Finsen astutely observed after his discovery of the promotion of
sunburn by UV, "What is more natural than that chemical rays should exert an
injurious influence upon a diseased skin, when we see such severe inflammation
produced by their influence upon the healthy skin?" (Finsen 1901a). The
infectious'diseases that are likely to be affected by UV are of two types.
TYPES OF INFECTIOUS DISEASES WITH CUTANEOUS INVOLVEMENT
Infections that have severe cutaneous pathology, damaging the skin, are
listed in Table 1. The effect of ultraviolet light on the progression of
disease has been documented for five of these.
But perhaps of more concern to us here are those infectious agents for
which the skin-associated lymphoid tissue is the first encounter with the
host's immune system (Table 2). These diseases have a primary cutaneous
phase, often asymptomatic, during which protective immunity to later
infections can develop. Such diseases are of particular concern, because
antigens that reach the immune system via skin that has been UV-B irradiated
not only escape the immune surveillance system of the skin, but also can make
the host tolerant to later exposure to the same antigens (Kripke 1984; Elmets
et al. 1983). For most of the diseases with a primary cutaneous phase, the
development of cell-mediated immune responses is necessary for protection.
Other papers in this volume show that cell-mediated immunity is more
critically affected by UV-B.
MODEL FOR UV-B ACTION ON AN INFECTIOUS DISEASE: LEISHMANIASIS
As a model for the effects of UV-B on infectious disease, let us turn to
leishmaniasis in the mouse. Leishmania have an initial cutaneous phase, which
can be asymptomatic and precede more serious sequelae; and they also cause
skin ulcers (Tables 1 and 2).
The leishmaniases are a spectrum of diseases, caused by members of the
genus Leishmania, which are obligate intracellular protozoan parasites living
with macrophages and monocytes. Paradoxically, for Leishmania to survive in
the body, they must be ingested by macrophages, whose function normally is to
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Table 1. Infectious Diseases With Severe Cutaneous Involvement
Disease
Onchocerciasis
Leishmaniasis
Lupus vulgaris
Hansen's disease
Mycobacterial
skin ulcers
Etiologic Agent
Classification
Onchocerca volvulus
Leishmania species
Mycobacterium tuberculosis
Mycobacterium leprae
Mycobacterium ulcerans
Streptococcus pyogenes
Measles virus
Varicella-zoster virus
Herpes Simplex Type II
(Variola virus)
Nematode
Protozoan
Mycobacterium
Mycobacterium
Mycobacterium
Bacterium
Virus
Virus
Virus
(Virus)
Effects of the UV light on progression of disease have been documented.
*n early studies before ca. 1935, broad-spectrum UV -light sources were
shown to affect smallpox, lupus vulgaris, and erysipelas (reviewed by
Licht 1983), Because such sources emit UV-A and UV-C as well as UV-B,
their effects cannot be attributed to UV-B only. More recent studies on
herpes and leishmaniasis used lamps emitting UV-B only.
invading microorganisms. The parasites are transmitted from host to
by phlebotomine sandflies, which deposit the Leishmania in the upper
of the dermis or in the epidermis. Phlebotomine proboscides are too
to penetrate protective clothing, so that sandflies must feed on exposed
Khi M°sfc infecfci°ns witn Leishmania species lead to self-healing skin ulcers,
^ei leave tne patient permanently scarred but immune to reinfection with
Son ed species of Leishmania. However, more serious sequelae are noted in
SFOH ^ot%ms °^ leishmaniasis. In chiclero's ulcer, the entire ear pinna can be
OM ^ awav? *n roucocutaneous leishmaniasis, parasites metastasize from the
le Sinai skin lesion to the mucocutaneous junctions. These severe mutilating
i>ec ns do not heal spontaneously, and they occur on parts of the body that
elve high amounts of UV-B in sunlight (Urbach' 1969). A primary skin ulcer
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Table 2. Infectious Diseases With a Primary Cutaneous Phase
Disease Etiologic Agent Classification .
Schistosomiasis Schistosoma species Trematode
Leisnmaniasis Leishmania species Protozoan
African sleeping Trypanosoma brucei Protozoan
sickness subspecies
Chagas' disease Trypanosoma cruzi Protozoan
Yaws Treponema pertenue Spirochaete
Hansen's disease (?) Mycobacterium leprae Mycobacterium
Cutaneous diphtheria Corynebacterium Bacterium
diphtheriae
Bubonic plague Yersinia pestis Bacterium
Anthrax Bacillus anthracis Bacterium
| - -•--__ ._.... -II 1--!----". ...... II- 'I- ^^—^^^
does not always precede the onset of the most fatal form of leishmaniasis,
kala-azar, in which the Leishmania invade the entire reticuloendothelial
system. Kala-azar smoulders for years in endemic foci, to erupt into
fulminating epidemics in times of migration, famine, and war.
Leishmanial disease occurs on every continent except Australia and
Antarctica. There are at least four different species causing human disease
in the Old World, and at least three in the New World.All Leishmania species
can cause skin ulcers, but only some of them can cause more severe disease i"'
immunogenetically predisposed individuals. Yet because not all infected
persons in groups at high risk for serious sequelae develop severe disease)
other factors are probably involved. In countries endemic for leishmaniasis,
skin is naturally exposed both to the bites of infective sandflies and to UV-B
in sunlight, which is known to depress the functions of the skin-associated
lymphoid tissue. So it seemed likely that early immunological events
occurring in the skin could critically determine the outcome of infection wit11
Leishmania.
In a series of experiments designed to evaluate the effects of UV-B on
the development of cutaneous leishmaniasis in mice (Giannini 1986), I found
that local irradiation of the injection site with low doses of UV-B around the
time of initial infection indeed affected lesion development (Figure 1). Th*
doses used were not high enough to cause sunburn, but were about the amount of
UV-B in an hour's exposure to sunlight in the semitropics on a bright day a*.
noon. Surprisingly, lesion severity was reduced in the irradiated mice
(Giannini 1986). .The main targets of the UV-B were host cells, and not
Leishmania, because the parasites were present in the skin and in vitro in the
101
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Nodule
Small
Ulcer
Expand.
Ulcer
Metast.
Tall Loss
Death
-------
same numbers in both irradiated and control groups (Tables 3 and 4). But
despite their apparently healthy skin, the irradiated mice had parasites at
the injection site and in their local lymph nodes (Table 5). When they were
tested for their ability to mount cell-mediated immune responses to
leishmanial antigens, the UV-B irradiated mice had almost no immunity,
compared with the unirradiated control mice (Table 6). Their lack of cell-
mediated immunity reduced the irradiated mice's ability to control a second
challenge infection in a skin site different from that of their first
exposure, which had been irradiated (Figure 2). Since Leishmania may persist
in the local lymph nodes, long after skin lesions have healed, and even when
parasites cannot be detected in the skin (Hill, North, and Collins 1984; Titus
et al. 1985; Giannini, unpublished), it is possible that depression of the
host immune response by other factors such as stress or impaired nutrition
could put the infected, though asymptomatic, individual at risk for
disseminated disease from the parasites lingering in the lymph nodes.
A similar suppressive effect of UV-B on cell-mediated immunity to herpes
simplex Type II virus has also been shown (Hayashi and Aurelian 1986).
Exposure to UV-B during the primary phase of infection suppresses the
development of cell-mediated immune responses to the virus (Howie, Norval, and
Maingay 1986), and irradiation of healed skin lesions triggers recurrent
herpes infections (Wheeler 1975; Blyth et al. 1976).
From these and other data we can conclude that local perturbations in the
functions of the skin-associated lymphoid tissue during cutaneous infections
can profoundly influence the immunological response to antigens of invading
microbes and the subsequent development of clinical disease.
PREDICTED ALTERATIONS IN PATTERNS OF INFECTIOUS DISEASES IN HUMANS
FOLLOWING INCREASED SOLAR UV-B RADIATION
If the immune functions of the skin cannot be protected from the effects
of UV-B by the use of sunscreens (Mentef* this volume), then it may be
difficult to avoid exposure to UV-B, especially in agricultural societies in
the tropics and semitropics, where heat makes protective clothing impractical
to wear.
Increases in the amount of solar UV-B reaching the earth's surface will
likely affect the severity of infectious disease. More precise predictions
are not possible, because wavelengths and dosages will critically affect the
response curve. In addition, the global effects of UV-B include other
environmental factors that impact on disease development, such as climate,
vector density, and food availability. It is probable that some cutaneous
infectious diseases will be exacerbated by increased UV-B radiation, as is the
case with smallpox and herpes. In other cases, pathogenesis of cutaneous
disease may be suppressed, such as in cutaneous leishmaniasis and lupus
vulgaris.
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Table 3. Growth and Viability of Leishmania
Macrophage-Like Cells In Vitro
in UV-B Irradiated
mJ/cm2 Leishmaniaa Host cellsa Leishmania Log10 viable
UV-B per host cell per 0.06 mm2 per 0.06 mm2 parasites3
15
5
1.5
0.5
none
3.6 ± 0.4
3.3 ± 1.1
3.3 ± 0.6
3.0 + 0.5
3.5 + 1.0
17
50
45
61
43
10°
21
16
16
16
61
164
150
183
150
4.5 ±
5.2 +
4.3 ±
5.2 ±
5.0 +
Means + standard deviation of four J774A.1 host macrophage-like cell
cultures; numbers of viable parasites were determined by an in vitro assay
system described in Giannini (1985); no significant differences in
viability or numbers of Leishmania per host cell were seen.
Calculated by multiplying the mean number of Leishmania per host cell times
the mean number of host cells per 0.06 mm .
4. UV-B Irradiation In Vivoa Does Not Reduce Viability of Leishmania
major" in Skin at Injection Site
Experiment
1
2
Time Post
Infection
3.5 mo.
9 mo.
Log viable amastigotes
per 15 ul of triturated skin
15 mJ/cm UV-B
3.3 ± 3.2
8.5 + 2.6
Shielded Controls g
1.3 ± 1.5 n.s.
8.0 + 3.1 n.s.
Groups of 4-8 B10.129 (10M) mice were irradiated with 15 mJ/cm2 1IV-B on the
tails 24 hours before and 24 hours after infection with 1 x 10^ (Expt. 1)
Or 1 x 106 (Expt. 2) L. major promastigotes, and subsequently irradiated
every 48 or 72 hours for 4 weeks. See Giannini (1986) for further details.
Determined by culturing serial tenfold dilutions (described in Giannini
1985).
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Table 5. Effects of UV-B Irradiation on Lesion Development and Parasite
Dissemination at 6 Months Post Infection3 With Leishmania Major
Lesion pathology index
Infected injection site
Infected local lymph nodes
Infected spleen
Infected skin distal to
Controls
4.2 + 0.4
100?
100?
89?
33?
Irradiated
2.1 + 1.4
100?
100?
67?
33?
injection site
a Only lesion pathology index was significantly different between the two
groups.
See Table 4, footnote a, for methods, and footnote b for explanation of
lesion pathology index (from Giannini 1986).
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Table 6. Cellular Immune Responses of UV-B Irradiated Micea, Infected with
Leishmania major, After Challenge with Leishmanial Antigens13
Time post
Infection
hrs
Treatment
Footpad Thickness0
(mm x 10 ~2)
4 hrs 24 hrs 48
2 weeks
6 weeks
Uninfected controls
Unirradiated
UV-B irradiated
Unirradiated
UV-B irradiated
12C
8
25C
11
11
12C
I8d
0
4 to 5 B10.129 (10M) mice per group were irradiated with 15 mJ/cm"& on the
tails 24 hours before and 24 hours after infection with 1 x 10° L. major
promastigotes, and subsequently every 48 or 72 hours for 4 weeks.
Mice were challenged in the left rear footpad with 10 yl containing 2 x
10& promastigotes, solubilized by freezing and thawing in PBS. The right
rear footpad was injected with 10 yl PBS.
Thickness of left footpad minus right footpad. Median values are given
because lesion pathology (and therefore the mice's responses) are not
normally distributed (see Figure 1).
Significantly different from the primary response of uninfected controls (p
< 0.05).
109
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(0 -***
UJ 30
o tail infected and irradiated
challenged in ear
• tail shielded and infected
challenged In ear
• tail untreated
challenged in ear
4 6 8 10 12 14 16 18 20 22
Hrs Weeks
Figure 2. Abrogation of Protection to a Challenge Infection by UV-B
Irradiation of the Primary Site of Infection with Leishmania major. Mice were
irradiated or shielded and infected in the tail, as described in the legend to
Figure 1. At two weeks after the primary infection in the tail, mice received
a large challenge infection in the ear (1 x 10" parasites). Expansion of the
secondary lesions in the ear in previously infected mice was compared with
that in mice not previously exposed to L. major, for which the ear was the
primary injection site. The previously infected, shielded controls had
significantly smaller lesions in response to the challenge infection than the
unexposed controls, at all times between 4 and 18 weeks, while the responses
of the previously infected, irradiated controls were indistinguishable froffl
the unexposed controls at all times.
110
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But we do well to remember that escape from overt skin disease may have a
price, namely, forfeiture of protective immunity to microbes that escape
immune surveillance network in the skin while its functions are
inactivated by UV-B.
ACKNOWLEDGMENTS
This work was supported by Public Health Service Grant AI 18937 from the
National Institutes of Health. I thank Dr. Edmond A. Goidl for many helpful
discussions, and Ms. Susie Mathews for expert technical assistance.
REFERENCES
Blyth, W.A., T.J. Hill, H.J. Field, and D.A. Harbour. 1976. Reactivation of
herpes simplex virus infection by ultraviolet light and possible
involvement of prostaglandins. J. Gen. Virol. 33:547-50.
De Fabo, E., and F. Noonan. 1986. Urocanic acid and its role in the immune
response. This symposium.
C.A., P.R. Bergstresser, R.E. Tigelaar, and J.W. Streilein. 1983. In
vivo low dose UV-B irradiation induces suppressor cells to contact
sensitizing agents. In The effect of ultraviolet radiation on the immune
system, ed. J.A. Parrish, 317-33. Skillman, New Jersey: Johnson &
Johnson Baby Products Company.
Finsen, N.R. 1901a. The chemical rays of light and smallpox. In
Phototherapy. 1-36. London: Edward Arnold.
pinsen, N.R. 1901b. The treatment of lupus vulgaris by concentrated chemical
rays. In Phototherapy. 73-75. London: Edward Arnold.
Giannini, M.S.H. 1986. Suppression of pathogenesis in cutaneous
leishmaniasis by UV irradiation. Infect. Imroun. 51:838-43.
Giannini, M.S.H. Cutaneous leishmaniasis: A lymphatic infection. Manuscript
submitted.
Giannini, S.H. 1985. Induction and detection of leishmanial infections in
Rattus norvegicus. Trans. Roy. Soc. Trop. Med. Hyg. 79:458-61.
Y., and L. Aurelian. 1986. Immunity to herpes simplex virus type
2: Viral antigen-presenting capacity of epidermal cells and its
impairment by ultraviolet irradiation. J. Immunol. 136:1087-92.
, J.O., R.J. North, and F.M. Collins. 1984. Advantages of measuring
changes in the number of viable parasites in murine models of
experimental cutaneous leishmaniasis. Infect. Immun. 39:1087-94.
Howie, S., M. Norval, and J. Maingay. 1986. Exposure to low-dose ultraviolet
radiation suppresses delayed-type hypersensitivity to herpes simplex
virus in mice. J. Invest. Dermatol. 86:125-28.
111
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Kripke, M.D. 1984. Imraunological unresponsiveness induced by ultraviolet
radiation. Immunolog. Rev. 80:87-102.
Licht, S. 1983. History of ultraviolet therapy. In Therapeutic Electricity
and Ultraviolet Radiation. 3rd ed., ed. G.K. Stillwell, 174-93.
Baltimore: Williams & Wilkins.
Schulze, R. 1970. Global radiation climate. Wiss. Forschungsber. 72:1-220.
Titus, R.G., M. Marchand, T. Boon, and J.A. Louis. 1985. A limiting dilution
assay for quantifying Leishmania major in tissues of infected mice.
Parasite Immunol. 7:545-55.
Urbach, F. 1969. Geographic pathology of skin cancer. In The biologic
effects of ultraviolet radiation (with emphasis on the skin), ed. F.
Urbach, 635-50. Oxford: Pergamon Press.
Wheeler, C.E., Jr. 1975. Pathogenesis of recurrent herpes simplex
infections. J. Invest. Dermatol. 65:341-46.
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Urocanic Acid: On Its Role in the Regulation
of UVB-lnduced Systemic Immune Suppression
Edward C. De Fabo and Frances P. Noonan
The George Washington Univeristy Medical Center
Washington, DC USA
ABSTRACT
We have previously postulated that UVB-induced systemic immune suppres-
3ion is mediated by a specific skin photoreceptor situated in the stratum
°°rneum of mammalian skin. This photoreceptor is considered to be a
biological signal transducer capable of converting UV-B radiation (290-320 nm)
directly into a biochemical signal that then "switches-on" formation of
antigen-specific suppressor cells by way of an "alteration" in antigen
Presentation.
The UVB-absorbing photoreceptor is tentatively identified as trans-
acid (trans-UCA). The mode of immune regulation associated with it
s suggested to be initiated by photoconversion to its cis isomer (cis UCA).
R«cent evidence is presented to support this concept showing that cis UCA in
Contrast to trans-UCA can induce an antigen-presenting "alteration" in splenic
Dendritic cells in the absence of any UV radiation.
A model is presented outlining a mechanism in which UCA-initiated immune
^Ppression is involved with the prevention of autoimmune attack against
Photoantigens" associated with sun-damaged skin. We propose that sunlight-
Educed skin tumor outgrowth may be an inadvertent consequence of this
n°rmally protective mechanism.
PRODUCTION: UCA AND IMMUNE SUPPRESSION
Urocanic acid (UCA, de-aminated histidine) is a major UVB-absorbing
compound located in the stratum corneum. The naturally occurring form is the
isomer; it isoraerizes to the cis form on absorption of UV-B radiation.
Although the existence of UCA has been known for more than 100 years
1974), no physiological function for it has ever been established.
ermore, even though UCA can attenuate ultraviolet (UV) radiation striking
113
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the skin of mammals, in effect acting as a photoprotector of DNA or as a
sunscreen protecting against erythema, it may be playing a more fundamental
physiological role as an immune-regulating skin photoreceptor (De Fabo and
Noonan 1983). We discuss the evidence supporting this idea in this paper.
BACKGROUND
The ability of UV radiation to suppress a variety of immune responses in
animals and humans has been well documented and reviewed (Kripke and Fisher
1976; Fisher and Kripke 1977; Morrison 1984; Parrish, Kripke, and Morrison
1984; Daynes and Krueger 1983). It has been shown that UV-B (290-320 nm) is
responsible for suppressing the immunologic rejection response to transplanted
UV-induced tumor (De Fabo and Kripke 1979, 1980).
Another major UV-B effect on immunity is its ability to suppress the
delayed-type hypersensitivity (DTH) response to skin sensitizing antigens such
as trinitrochlorobenzene (TNCB) in mice (Noonan, De Fabo, and Kripke, 198la,
198lb). In this reaction mice that have been pretreated with UV radiation
show a systemic suppression of the DTH response. We previously showed that it
was energy primarily in the UV-B band that can diminish the DTH response in
dose-dependent fashion (Noonan, De Fabo, and Kripke 198la). The kinetics of
this response was similar to the UVB-induced suppression of tumor rejection
(De Fabo and Kripke 1979, 1980).
In further studies on the systemic suppression of DTH which were designed
to elucidate the first light-absorbing event a relative wavelength
effectiveness or "action" spectrum of this effect by UV radiation was
estimated. The significant finding of this study was that radiation of
wavelengths between 320 nm and 250 nm (UV-B and UV-C) exhibited differing
effectiveness in suppressing the DTH response. This clear-cut differential in
wavelength effectiveness suggested that a specific molecule, i.e., a "UVB-
transducing" photoreceptor was absorbing this radiation and using it to "turn
on" an immune suppressor response to the skin sensitizing chemical antigens.
We suggested this mechanism might exist to "down regulate" the rejection
response against new "photoantigens" put on skin cells by exposure to the UV-B
component of sunlight. In effect this suppression would prevent uncontrolled
autoimmune attack against sun-damaged cells (De Fabo and Noonan 1983). We
found the shape of the action spectrum closely matched the absorption spectrum
of UCA (De Fabo and Noonan 1983). Because of the close match between our in
vivo derived action spectrum and the in vitro absorption spectrum of urocani°
acid, we suggested that trans-UCA may be acting as the UVB-absorbing
photoreceptor initiating events leading to immune suppression of DTH (De Fab<>
and Noonan 1983). Furthermore, because of close photobiological and
immunological similarities to the suppression of tumor rejection, we suggested
that perhaps this suppressive response to transplanted UV-induced skin tumors
might also involve UCA (De Fabo and Noonan 1983).
UCA AND SKIN CANCER: A POSSIBLE LINK
One of the major puzzles about skin cancer is that nearly all UV-induced
skin tumors in mice are highly antigenic and capable of evoking strong
immunologic rejection responses by the host. Thus, it is unclear, given the
strong immune response against these tumors, how they are able to grow out *-n
the host.
114
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E
p
I
D
E
R
M
I
S
*,+
hv systemic
! t-UCA > c-UCA > >- -> > ANTIGEN
! circulation PRESENTING
! CELL DEFECT
!
*,+
! hv
! DNA MALIGNANT +
I TRANSFORMATION
TUMOR —
ASSOCIATED
ANTIGENS
Anti gen-1
An t i gen~2 •• >
'•• i
..• i
Tolerance to
tumor-associ ated
antigens
V V
Tolerance to
antigens
wavelengths are identical for activating both systems
U.JVB/C: 320-250 nm)
+ IJVB/C -flux is low for UCA activation; high for DNA
transformation.
t-UCA = trans isomer; c-UCA = cis isomer
T-s s Suppressor T cells specific only for antigen
1 1
T-s : Suppressor T cells specific only for antigen
2 2
T-s 5 Suppressor T cells specific, only for tumor—associated
tumor antigens
Figure 1. Induction of Tolerance to Tumor-Associated Antigens. In this
tt. -* a scheme is presented to include the production of a tumor cell with
w yOr-associated antigens." This is formed when high doses of radiation of
lean gtns 250-320 nm cause a malignant transforming event in DNA. This
are tO the formation of a neoplastic cell. Associated with this neoplasm
UCA ^~*nduced antigens. We suggest that these antigens interact with the
^e "induced antigen-presenting cell alteration in a manner that eventually
sf to the production of antigen-specific suppressor T cells. In the case
"tuif *'umor cell, however, the suppressor cells formed are specific for the
^unior-associated antigens." Formation of these suppressor cells leads to
Outeran°e (acceptance) of the tumor cell instead of rejection. Tumor
8»*owth is the final consequence.
115
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One possible explanation may involve an interaction between immune
suppression mediated by UCA and tumor formation mediated by UV effects on DNA
(De Fabo and Noonan 1984). Figure 1 presents a scheme for this type of
interaction.
As previously noted, the underlying immunologic problem in mice
irradiated with UV-B appears to be an alteration or "defect" in antigen
presentation (Greene et al. 1979; Noonan et al. 1981). It seems that, because
of this "defect", antigen-specific suppressor cells, rather than effector
cells, are formed when antigen is given to a UVB-irradiated mouse. The
hypothesis we put forward is that UCA may interact with antigen-presenting
cells, e.g., macrophages, skin Langerhans cells, or splenic dendritic cells in
such a way as to make defective their presentation of antigen to stimulator T
cells. This process we propose is initiated by photoisomerization of trans-
UCA to its highly soluble cis form. Once formed, the cis isomer or a
secondary intermediate would interact with antigen-presenting cells in such a
way as to alter their capacity to present antigen. This "defect" in antigen
presentation (or processing) would become the signal for stimulation of
suppressor cells rather than effector cells. The specificity of the
suppressor cells would be determined by the type of antigen presented to the
"defective" antigen-presenting cell (De Fabo and Noonan 1983).
This hypothesis has received strong support from the observations that
(a) injection of cis UCA into mice induces an antigen-processing alteration in
splenic dendritic cells without UV radiation; injection of trans-UCA was
without effect (Noonan, De Fabo, and Morrison 1986) and (b) mice genetically
deficient in histidase and thus in epidermal UCA showed no suppression of the
CHS response when exposed to known immunosuppressive doses of UV-B (De Fabo et
al. 1983).
In conclusion, it appears that a mechanism exists in skin that can
directly bring about interaction between solar UV-B and the immune system in
a way previously unknown. Further investigations into such a mechanism may
open up new directions for determining the causes of skin cancer and other UV-
B immune-associated diseases.
SUMMARY
For many years the physiological role for UCA has remained obscure, al-
though a relatively large amount of this substance, in the trans con-
figuration, accumulates in mammalian epidermis. UCA has been suggested to act
in the skin as a natural sunscreen. Alternatively, we have proposed a
physiological role for trans-UCA as a UVB-absorbing skin photoreceptof
necessary to regulate against autoimmune attack on sun-damaged skin. In this
capacity, trans-UCA is converted to the cis isomer that can then initiate the
production of antigen-specific suppressor cells via an alteration in antigen-
presentation. Thus, during prolonged sun exposure, suppressor cells form,
which are specific for "photoantigens" induced on sun-damaged skin. These
suppressor cells can prevent effector cells from carrying out an autoimmune
attack against these "photoantigens."
Because such a mechanism exists, UCA may be involved in the outgrowth of
sun-induced skin tumors, inadvertently protecting tumor cells from attack by
effector cells. That is, due to the production of these "photoantigen"-
116
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specific suppressor cells that also recognize UV-induced antigens on tumors,
tumor growth continues and the concentration of these UV-induced antigens
steadily increases, keeping primed the production of specific suppressor cells
(Figure 1). Without reversing this process, immune surveillance of the tumor
(attack and destruction) will be prevented and tumor outgrowth will be the
final outcome.
REFERENCES
°aynes, R.A., and G. Krueger, eds. 1983. Experimental and clinical
photoimmunology. Vol II. Cleveland, OH: CRC Press, Inc.
De Fabo, B.C., and M.L. Kripke. 1979. Dose-response characteristics of
immunologic unresponsiveness to UV-induced tumors produced by UV
irradiation of mice. Photochem. Photobiol. 30:385-390.
De Fabo, E.C., and M.L. Kripke. 1980. Wavelength dependence and dose-rate
independence of UV radiation-induced suppression of immunologic
unresponsiveness of mice to a UV-induced fibrosarcoma. Photochem.
Photobiol. 32:183-188.
^e Fabo, B.C., and P.P. Noonan. 1983. Mechanism of immune suppression by
ultraviolet radiation in vivo. I: Evidence for the existence of a
unique photoreceptor in skin and its role in photo immunology. J. Exp.
Med. 158:84-98.
De Fabo, E.G., and P.P. Noonan. 1984. Two-photoreceptor model for
photocarcinogenesis. In Photobiology. 1984. Proceedings of the Ninth
International Congress on Photobiology. eds. J. Jagger, J. Longworth, and
W. Shropshire, J., 144. New York: Praeger Scientific.
De Fabo, E.G., F.P. Noonan, M. Fisher, J. Burns, and H. Kacser. 1983.
Further evidence that the photoreceptor mediating UV-induced systemic
immune suppression is urocanic acid. J. Invest. Dermatol. 80:319.
pisher, M.S., and M.L. Kripke. 1977. Systemic alteration induced in mice by
ultraviolet light irradiation and its relationship to ultraviolet
carcinogenesis. Proc. Natl. Acad. Science USA. 74:1688-1692.
Greene, M.I., M.S. Sy, M.L. Kripke, and B. Benacerraf. 1979. Impairment of
antigen-presenting cell function by ultraviolet radiation. Proc. Natl.
Aoad. Sci. USA. 76:6592-6595.
M. 1974. Concerning a new constituent of dog urine. Ber. Deut. Chem.
Ges. 7:1669-1673.
Kripke, M.L., and M. Fisher. 1976. Immunologic parameters of ultraviolet
carcinogenesis. J. Natl. Cancer Inst. 57:211-215.
M°rrison, W.L. 1984. Photoimmunology. Photochem. Photobiol. 40:781-787.
117
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Noonan, P.P., E.G. De Fabo, and M.L. Kripke. 198la. Suppression of contact
hypersensitivity by UV radiation and its relationship to UV-induced
suppression of tumor immunity. Photochem. Photobiol. 34:683-690.
Noonan, P.P., E.G. De Fabo, and M.L. Kripke. 198lb. Suppression of contact
hypersensitivity by ultraviolet radiation: An experimental model.
Springer Seminars in Immunopathology. 4:293-304.
Noonan, P.P., E.G. De Fabo, and H. Morrison. 1986. Cis-urocanic acid, a UVB
irradiation product, initiates an antigen presenting cell defect in
vivo. Photochem. Photobiol. 43 supp:l8s.
Noonan, P.P., M.L. Kripke, G.M. Pedersen, and M.I. Greene. 1981. Suppression
of contact hypersensitivity in mice by ultraviolet irradiation is
associated with defective antigen-presentation. Immunology. 43:527-533'
Parrish, J.A., M.L. Kripke, and W.L. Morrison, eds. 1984. Photoimmunologyj.
New York: Plenum Medical Book Company.
118
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Solar Wavelengths of Ultraviolet Light-
Induced Cytoplasmic Damage
Glen Zamansky andlih-Nan Chow
Boston University School of Medicine
Boston, Massachusetts USA
Since solar ultraviolet (UV) light is the major cause of human skin
°ancer, it is important to determine the UV-induced cellular lesions that
c°ntribute to the carcinogenic process. The majority of investigations have
examined DMA damage resulting from exposure to short wavelength UV light.
This has led to the suggestion that pyrimidine dimers are the critical lesion
Responsible for solar carcinogenesis. However, people are not exposed to such
short wavelength UV light, because it does not penetrate the. atmospheric ozone
laver. There is evidence that cellular lesions other than pyrimidine dimers
^e involved in the carcinogenic, mutagenic, and lethal effects of UV light
cnat reaches the earth's surface. However, alterations of non-DNA targets in
*annnalian cells caused by UV have received little attention. Because the
cytoskeleton is an important participant in the control of normal cell growth
and because epigenetic events may play a role in carcinogenesis, we have begun
0 explore the induction of cytoskeletal alterations induced by UV light in
n skin fibroblasts. We have been particularly interested in the effects
irradiation with polychromatic UV light composed of environmentally
wavelengths. Our data indicate that exposure to germicidal UV-C
results in no discernible changes in the cytoskeletal organization as
d by fluorescence microscopy. However, exposure to polychromatic UV-B
and UV-A light causes severe injury to the cytoskeleton.
^RODUCTIOM
Epidemiological and experimental evidence has established solar
:;tpaviolet (UV) light as the major cause of human skin cancer. More than
Q
non-melanoma cutaneous tumors appear to result from exposure to sunlight.
deal of effort has therefore been expended trying to elucidate the
by which UV light induces the transformation of normal cells to a
phenotype. The vast majority of investigations have been performed
germicidal lamps that emit primarily 254 nm light. Unfortunately, such
119
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short wavelength UV light is environmentally irrelevant because it does not
penetrate the stratospheric ozone layer. The UV light spectrum has been
operationally divided into three wavebands: UV-C, 200-290 nm; UV-B, 290-320
nm; and UV-A, 320-400 nm. The solar spectrum of UV light reaching the earth's
surface is fairly constant at wavelengths greater than 320 nm and drops off
precipitously between 320 and 290 nm. UV-A, the least studied UV waveband,
comprises the largest UV component to which people are exposed. UV-B light
appears to be responsible for the induction of skin cancer. The contribution
of interactions between UV-A and UV-B light towards the development of
cutaneous tumors remains to be determined.
Decreases in the concentration of stratospheric ozone, resulting from the
anthropogenic release of chlorofluorocarbons and other agents into the
environment, will significantly increase the levels of carcinogenic UV-B light
reaching the earth's surface. In a recent report from the National Research
Council, it was suggested that every '\% decrease in ozone concentration will
result in a 2% to 5% higher incidence of basal cell carcinomas and a H% to 10^
higher incidence of squamous cell carcinomas (National Research Council
1982). Since it appears that a significant decrease in stratospheric ozone is
likely to occur during the next century, special emphasis needs to be placed
on the adverse health effects of increased exposure to UV-B light. Howevert
to attain an accurate assessment of the potential health hazards, the UV-
induced .lesions that contribute to the carcinogenic process must be
identified. This paper explores the possibility that exposure to wavelengths
of UV found in the environment alters cytoplasmic elements that are important
in the regulation of cell growth.
The cytoplasm of eukaryotic cells contains an intricate network of
filamentous structures that are collectively referred to as the cytoskeletott'
The three major components of the cytoskeleton are microtubulesf
microfilaments, and intermediate filaments (Alberts et al. 1983)-
Microtubules are hollow structures consisting primarily of tubulin and have an
outer diameter of 22-25 nm. They appear to originate at microtubuie
organizing centers close to the nuclear membrane and extend throughout the
cytoplasm. Microfilaments, composed primarily of F-actin, are thinner
filamentous structures having an average diameter of 6 nm. In well flattened
cultured cells, microfilaments are often found in bundles, referred to as
stress fibers. The diameter of intermediate filaments, approximately 10 nn»f
falls between those of microtubules and microfilaments. Inununological and
biochemical studies have demonstrated that the protein composition of
intermediate filaments is very heterogeneous. Intermediate filaments have
therefore been grouped into five subclasses: keratin (epithelium), vimentio
(mesenchyme), desmin (muscle), glial fibrillary acidic protein (glial cells)»
and neurofilament proteins (neurons). Using fluorescence microscopy, we have
investigated alterations of cytoskeletal components induced by exposure to UV'
C light or polychromatic UV-B and UV-A light in a human skin fibroblast cell-
strain .
120
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MATERIALS AND METHODS
Cells
AG 1522, a human skin fibrobast cell strain, was obtained from the
Human Genetic Mutant Cell Repository, Institute for Medical Research (Camden,
NJ). Cells were grown in Eagle's minimal essential medium supplemented with
^Q% fetal calf serum, 0.9 g/1 D-glucose, 0.66 mg/1 sodium pyruvate, 110
u/ml penicillin and 110 yg/ml streptomycin sulfate. Cultures were incubated
at 37<>c in an atmosphere of 95% air and 5% C02<
General Electric G8T5 germicidal lamps, Westinghouse FS40 lamps, and
Sylvania FR40T12 lamps were our sources of UV-C, sunlamp, and UV-A light,
respectively. Polychromatic UV-B and UV-A light sources were selected because
they more closely simulate the type of UV light to which we are exposed at the
earth's surface. Furthermore, it has been demonstrated that the biological
sffects of polychromatic light frequently do not comprise a simple composite
°f the effects induced by monochromatic light corrected for the appropriate
relative intensities (Suzuki et al. 1981; Wells and Han 1984). The UV-C lamps
emit greater than 95% of their energy at 254 nm. The emission spectra of the
Westinghouse FS40 and Sylvania FR40T12 lamps, filtered through plastic petri
dish covers, are shown in Figure 1. The sunlamps transmit approximately equal
Counts of light in the UV-B and UV-A wavebands with a peak emission in the
UV-B region between 310 nm and 315 nm. More than 98% of the light from the
UV-A lamps (maximum emission at 350-355 nm) is in the UV-A waveband. UV-C
dose rates were determined with an International Light (Newburyport, MA) IL254
germicidal photometer. Sunlamp and UV-A dose rates were determined with an
international Light IL443 photometer with appropriate filters for the
individual light sources. Cultures exposed to UV-C light were irradiated
without their covers at a dose rate of 0.4 J/nr/sec, in the presence of Hank's
buffered salt solution supplemented with 15 mm Hepes (HBSS). Cultures exposed
to pSunlamp (approximately 4.5 J/nr/sec) or UV-A light (approximately 30
J/nr/sec) were irradiated, in the presence of HBSS, through tfieir plastic
°overs in order to filter out wavelengths shorter than 290 nm. Sunlamp- and
UV-A treated cultures were maintained in a room temperature water bath during
irradiation. In order to protect cultures from ambient UV light, only yellow
iight was used in the laboratory during the course of our experiments.
£y^oskeleton Preparation
Microtubules and microfilaments were examined using modifications of
Procedures previously described (Chou and Shaw 1984; Wang et al. 1982). Cells
grown on glass coverslips were washed with a microtubule stabilizing buffer,
PH 6.9 (PM2G buffer), that contains 0.1 M Pipes, 1 mM MgSO^, 2 mM EGTA, and 2
M glycerol. This buffer condition effectively preserves microtubules as well
as microfilaments and intermediate filaments. The cells were fixed for 30
minutes with 3.7% formaldehyde, freshly prepared in PM2G buffer, followed by
incubation in phosphate buffer solution, pH 7.4 (PBS), for 5 minutes. They
j*sre then treated with 0.1 M Glycine in PBS for 5 minutes to quench formalde-
hyde, and extracted with 0.3* Nonidet P-40 (NP40) in PBS for 10 minutes. All
operations up to this step were conducted with room temperature reagents.
121
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0
270 290 310 330 350 370 390 410
Figure 1.
WAVELENGTH (nm)
Emission Spectra of Westinghouse FS40 (sunlamp) and
Sylvania FR40T12 (UV-A) Lamps.
The fixed cytoskeletons on coverslips were incubated at 37°C for 30
minutes with a mixture of rabbit anti-tubulin antibodies and NBD-phallacidin
to double label microtubules and microfilaments, respectively. NBD-
phallacidin, a fluorescent reagent, specifically labels F-actin filaments of
cultured cells, resulting in a higher degree of resolution than obtained with
indirect labelling procedures using two antibodies. After the initial
labelling period, coverslips were thoroughly washed with PBS and treated for
30 minutes with goat anti-rabbit antibodies conjugated to rhodamine. After
the 30-minute exposure to rhodamine-conjugated antibodies, the coverslips were
again thoroughly washed with PBS and finally with double-distilled water to
remove residual PBS. They were then mounted on glass slides with a drop of
Gelvatol and allowed to harden at 4°C overnight before examination with a
Nikon fluorescence microscope. Using coded coverslips, the percent of cells
with intact microtubules and/or microfilaments was determined by examining 200
cells in randomly selected microscopic fields at each UV dose. The person
viewing the cells was not familiar with the code used to identify the
coverslips. Photographs of representative cells were taken using Kodak Tri-X
film (ASA 400) and developed by "pushing" to an effective rating of ASA 1600.
RESULTS
Initial comparisons between cells irradiated with UV-C and sunlamps
indicated that even at extremely toxic UV-C doses, the microtubules and
raicrofilaments of AG1522 cells remain intact. However, we consistently
observed disruption of microtubular structures in cells irradiated with
sunlamps. In order to quantify this phenomenon, we have performed dose-
122
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response experiments in which we estimated the percent of cells with intact
toicrotubules (Table 1). Coded coverslips were used to avoid counting bias.
Because the efficiency of inducing erythema, cellular inactivation,
toutagenesis, transformation, and other biological effects usually decreases as
the wavelength of light increases, the progressively higher doses at longer
wavelengths of light were selected. As seen in Table 1, intact microtubules
were found in cells irradiated with UV-C doses as high as 100 J/m2. Exposure
to sunlamps resulted in the disruption of microtubules, decreases in intact
fcicrotubules usually being observed after exposure to 3000 J/m2. Experiments
with UV-A light indicated that it also causes a dose-dependent loss of
organized microtubules. No perceptible alterations of microfilaments occurred
*n cells irradiated with UV-C, sunlamps, or UV-A. We have previously found
that the doses required to reduce survival of AG1522 cells to "\Q% (as measured
by colony forming ability) are approximately 8.2 J/m2 for UV-C, 1180 J/m2 for
sunlamp, and 157 kJ/m2 for UV-A light (Zamansky 1986). The disruption of
roicrotubules therefore appears to be induced by sunlamp and UV-A exposures,
which result in less cell death than after 100 J/m2 UV-C, a dose at which no
effect occurs.
Table 1. Disruption of Microtubules by UV-C, Sunlamp, or UV-A Light
j>ose (J/m2)
0
10
20
40
75
100
UV-C
Intact MT (X)*
96.5 ± 0.5
96.0 ± 1.0
96.0 ± 0.5
94.5 ± 0.8
94.8 ± 2.3
91.5 ± 2.5
Sun
Dose {J/m2)
0
750
1500
3000
5000
7500
Lamp
Intact MT (X)*
96.7 ± 0.9
94.3 ± 0.9
89.7 ± 1.3
54.7 t 15.2
37.3 ± 2.8
19.7 ± 9.2
Dose (kJ/m2)
0
50
100
150
UV-A
Intact MT («)
95.8 ± 1.2
83.3 ± 8.3
38.3 ± 3.0
26.5 ± 3.0
* The percent of cells with intact microtubules is presented as the mean ± 1 standard error of
2 (UV-C), 3 (sun lamp) or 2 (UV-A) experiments. 200 cells were examined in randomly selected
microscopic fields of coded coverslips in each experiment.
The microscopic appearance of microtubules and microfilaments in control
irradiated cells is shown in Figures 2A-2F. As expected, the microtubules
Dr unirradiated AG1522 cells (Figure 2A) appear to emanate from perinuclear
^icrotubule organizing centers and extend throughout the cytoplasm. The
intricate network of microtubules is also present in cells irradiated with UV-
(Figure 2C). However, distinct microtubules are often completely absent in
8 cytoplasm of cells irradiated with sunlamps (Figure 2E). Although
reronants of the microtubule organizing center may still be present, the
^Jority of anti-tubulin-stained cytoplasm takes on a fine powdery
?Ppearance. The extent to which this occurs is dependent upon the UV dose.
^Ua» microtubules appear to be disassembled or fragmented. UV-A irradiated
123
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Figure 2. Microscopic Appearance of Microtubules (A,C,E) and MicrofHa'
merits (B,D,F) in AG1522 Cells. No UV light (A and B), UV-C, 100 J/m? (C and
D); sunlamp, 5000 J/m2 (E and F).
124
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cells (not shown) have the same powdery appearance as sunlamp-treated cells.
The microfilaments of the cells depicted in Figures 2A, 2C, and 2E are shown
in Figures 2B, 2D, and 2F, respectively. No changes were observed in the
microfilaments, which remain quite apparent as distinct actin filament bundles
stretching across the length of the cells.
DISCUSSION
DNA is usually considered the critical site of UV-induced cellular
damage. Experiments utilizing short wavelength UV light have yielded an
abundance of information concerning the induction of pyrimidine dimers, and
the mechanisms by which dimers are removed have become the most understood DNA
Repair pathways. However, the types and relative frequencies of UV-induced
lesions vary greatly for the three wavebands of the UV spectrum (Cerutti and
Netrawali 1979; Tyrrell 1982; Han, Peak, and Peak 1984). Most action spectra
"or cellular inactivation correlate well with the absorption spectrum of DNA
a°d with the formation of pyrimidine dimers out to 313 nm (Rothman and Setlow
'979; Kantor, Sutherland, and Setlow 1980; Jacobson, Krell, and Dempsey 1981;
°oninger et al. 1981; Tyrrell, Wertelli, and Moraes 1984) supporting the role
of DMA as the critical target for the lethal effect. The action spectra for
Ration, transformation, cellular capacity for viral growth, reactivation of
^-damaged virus, and the induction of virus synthesis in transformed cells
also correspond closely to the absorption spectrum of DNA at wavelengths as
long as 313 nm (Jacobson, Krell, and Dempsey 1981; Doninger 1981; Coohill and
Jacobson 1981). These findings and the observation that patients with
*eroderma pigmentosum (XP) exhibit cutaneous hypersensitivity to sunlight, the
Development of multiple malignant tumors in sun-exposed areas, and an
^ability to properly repair pyrimidine dimers (Cleaver and Bootsma 1975;
Bobbins et al. 1978) have led to the suggestion that these lesions are
responsible for solar carcinogenesis. However, evidence has begun to
Accumulate that lesions other than pyrimidine dimers may be involved in the
ioo0inogenic» mutagenic, and lethal effects of solar UV light (Zelle et al.
]9oO; Smith and Paterson 1981, 1982; Suzuki et al. 1981; Zbinden and Cerutti
19°1; Botcherby et al. 1984; Wells and Han 1984; Tyrrell 1984).
f We have previously reported that the relative sensitivity of human skin
I1broblasts to UV-C, sunlamp or polychromatic UV-A light depends on the
^position of the light to which they are exposed (Zamansky et al. 1985;
^amansky 1986). Our findings suggest that the inability of XP' cells to
Properly remove pyrimidine dimers is of less importance to cells exposed to
Polychromatic, long wavelength light and that no lesion commonly induced by
°Ur three UV light sources is likely to be solely responsible for cellular
inaotivation. This agrees well with a recent study by Keyse et al. (1983) in
J»ich monochromatic UV light was used (1983). Additional support for the
^toportance of non-dimer lesions has been obtained in studies demonstrating
wiat certain cell strains from patients with Bloom's syndrome, ataxia
jjeiangiectasia, and actinic reticuloid are hypersensitive to long wavelength
v light, but not to 254 nm light (Smith and Paterson 1981; Zbinden and
1981 Botcherby et al. 1984). Furthermore, a lack of correlation be-
the induction of pyrimidine dimers and cellular inactivation,
i, and transformation has been noted in human and rodent cells
iQh"""* to uv Ii8hfc composed of wavelengths greater than 313 nm (Zelle et al.
Iyo0; smith and Paterson 1981; Suzuki et al. 1981; Tyrrell 1984).
125
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The transformation of normal cells to a cancerous phenotype is a complex
process that has most often been described as involving two stages: initiation
and promotion (Diamond, O'Brien, and Baird 1980; Farber and Cameron 1980).
Current experimental evidence suggests that initiation is caused by genetic
damage and that promotion results from epigenetic events. Because exposure to
promoters is not required for tumor induction by "complete" carcinogens such
as UV light, most investigations into the carcinogenic effects of UV light
have emphasized its genotoxic capability. Is it likely that UV-induced
alterations of non-DNA targets may contribute to the establishment of human
skin cancer? It has been known for many years that solar wavelengths of UV
light induce biologically important lesions in non-DMA targets in bacteria.
Several effects due to damage of bacterial membranes have been studied. Moss
and Smith (1981) have demonstrated that membrane damage contributes to le-
thality under certain growth conditions. Others have reported the
inactivation of membrane transport systems and the inhibition of oxidative
phosphorylation (Kashket and Brodie 1962; Robb and Peak 1979; Brodie, Suther-
land, and Lee 1979; Sharma and Jagger 1981). Absorption of UV-A light by 4-
thiouridine, an unusual base found in bacterial transfer RNAs, results in
growth inhibition caused by a cessation of RNA synthesis (Ramabhadran and
Jagger 1976; Favre and Thomas 1981). It has also been shown that UV-A light
inhibits bacterial DMA repair enzymes (Tyrrell 1976). Very little is known
about the induction of alterations in non-DNA targets in mammalian cells,
though recent studies have demonstrated that cell membranes can be damaged by
broad spectrum UV-A and UV-B light (Aberer et al. 1981; DeLeo et al. 1985).
The results presented above represent the first demonstration of
UV-induced disruption of cytoskeletal elements in cultured cells. In
addition, our data indicate that exposure to germicidal, UV-C light or to
environmentally relevant wavelengths of UV-B and UV-A light has extremely
different effects on the cytoskeleton. Since the cytoskeleton is an important
participant in the control of normal cell growth and since epigenetic events
probably play a role in carcinogenesis, such alterations of the cytoskeleton
may be an important consequence of natural exposure to UV light. The
individual components of the cytoskeleton are structurally associated with
each other as well as with the cellular membrane and nuclear matrix (Brinkley
1981; Schliwa, van Blerkom, and Pryzwansky 1981; Singer et al. 1981; Ben-Ze'ev
1985). It has therefore been suggested that the cytoskeleton may serve as a
critical means of transmitting external signals to the nucleus. The molecular
mechanisms by which it performs this function are not understood. The complex
organization of the cytoskeleton participates in the regulation of cellular
shape and motility, the spatial arrangement of organelles and secretory
processes. Because cell shape is an important regulator of cell growth,
alterations of the cytoskeleton disrupt normal shape-related regulatory
signals (Folkman and Moscona 1981; Penman et al. 1981). The structural state
of the cytoskeleton also appears to contribute to the control of DNA synthesis
(Friedkin and Rozengurt 1981; Otto 1982). Agents causing the disassembly of
microtubules enhance the initiation of DNA synthesis in cells exposed to
peptide growth factors, though this response may be dependent upon the cell
type or culture conditions. The close association between polyribosomal mRNA
and cytoskeletal components has led to the suggestion that the cytoskeleton
may also contribute to the regulation of protein synthesis (Nielsen, Goelz,
and Trachsel 1983). Because there is extensive interaction between
cytoskeletal elements, agents that affect one component may influence the
regulatory capacity of others. It is thus reasonable to expect that
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Perturbations of the normal assemblage of the cytoskeleton induced by UV light
could result in a variety of functional consequences. Indeed, cytoskeletal
Abnormalities have now been associated with several pathologic phenomena
including the malignant transformation of cells (Lockwood, Trivelte, and
Pendergast 1981; Penman et al. 1981; Rungger-Brandle and Gabbiani 1983; Ben-
Ze'ev 1985). With these considerations in mind, it is also intriguing to note
that tumor promoters have recently been found to cause structural changes in
the three major cytoskeletal components (Weber, Wehland, and Herzog 1976;
Rifkin, Crowe, and Pollack 1979; Seif 1980; Schliwa et al. 1984; Fey and
Penman 1984).
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Sunscreens Do Not Abrogate UV-Induced
Suppression of Contact Hypersensitivity
M. S. Fisher, J. M. Menter, L Tiller, and I. Willis
Morehouse School of Medicine
Atlanta, Georgia USA
ABSTRACT
Contact hypersensitivity (CHS) in mice can be induced by cutaneous sensi-
followed by elicitation via ear-painting with trinitrochlorobenzene
This CHS reaction is systemic and can be suppressed by exposure of
to suberythemogenic doses of 280-315 nra radiation. In this paper, we
estigate whether a commercially available water-resistant sunscreen (SPF-6)
containing padimate 0 (UV-B absorber) and oxybenzone (UV-A absorber) was
effective in preventing systemic suppression of CHS induced by either FS36
Sunlamp exposure or solar simulating radiation. We observed that this sun-
screen preparation could not prevent the immunologic suppression of contact
hypersensitivity by UV radiation. These results indicate that application of
sunscreen does not retard the development of suppression of CHS following
rePeated UV exposure under conditions where erythema is not clinically
observed. Thus, erythema may not be a good end point for assessing systemic
lnanune suppression and its consequences.
PRODUCTION
Exposure of mice to ultraviolet (UV) radiation systemically suppresses
ability to reject highly antigenic UV-induced skin cancers (Fisher 1977;
er and Kripke 1977). This state of unresponsiveness is mediated
ln»nuriologically and is due in part to the presence of antigen-specific
T lymphocytes (Fisher 1977, 1978; Fisher and Kripke 1977, 1978,
J Spellman and Daynes 1977). A second UV-induced immunosuppressive defect
j|aa also been described in which a single exposure of the dorsal skin of mice
!j0 UV radiation was sufficient to suppress contact hypersensitivity (CHS) to
~chloro-1,3,5-trinitroben2ene (TNCB) applied to the abdominal surface (Noonan
j^ al. 1981). The cellular basis for the suppression of contact
^Vpersensitivity appears to involve a UV-induced alteration in the functional
a°Uvity of antigen-presenting cells (Noonan et al. 1981; Greene et al. 1979).
131
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The photobiologic and immunologic similarities of these two UV-induced
systemic immunosuppressive events suggest that they may share common steps
(Noonan et al. 1981; De Fabo and Kripke 1979; Noonan, De Fabo, and Kripke
198la, b), which appear to be: (a) an alteration in the presentation of
certain antigens, particularly those encountered via the cutaneous route
(Noonan et al. 1981) and (b) the induction of T suppressor cells as a
consequence of altered antigen presentation (Greene et al. 1979). The main
difference between both forms of systemic immunologic suppression is that the
antigen that induces the suppressor cells is applied exogenously in the case
of contact hypersensitivity, but must be formed endogenously by UV exposure of
the skin in the induction of suppressor T cells that regulate tumor
rejection. Another important difference between the two systems is the actual
dose of UV needed to induce 50% suppression. For CHS, the dose is
approximately 13 times less than that needed to induce the tumor suscepti-
bility in 50% of the UV-irradiated animals (Noonan, De Fabo, and Kripke
198lb).
Sunscreens, the majority of which use para-aminobenzoic acid (PABA) or
one of its derivatives and/or a benzophenone derivative as their active ingre-
dients, protect against a number of UV radiation effects. The ability of
topically applied sunscreens to reduce erythema and skin damage caused by
chronic UV exposure, expressed as a "sun protective factor" (SPF), is well
documented (Pathak 1969; Willis and Kligman 1970; Kligman, Akin, and Kligman
1980, 1982). In addition, sunscreens have been shown to protect against both
the cocarcinogenic as well as the carcinogenic effect of UV radiation (Snyder
and May 1975; Kligman, Akin, and Kligman 1980; Wulf et al. 1982; Stern,
Weinstein and Baker 1986). To date, however, very few studies have evaluated
the effect of these sunscreen agents on the more subtle immunoregulatory
effects now known to be produced by UV-B irradiation. One such study by
Gurish et al. (1981) found that pretreatment of mice with a PABA sunscreen
completely prevented the UVB-induced histologic changes in exposed skin and
rendered the mice tumors susceptible, although this susceptibility could not
be adoptively transferred to normal untreated animals by lymphoid cell
injection. A later study (Morison 1984) with a similar sunscreen but witn
higher doses of UV-B radiation showed not only induction of the tumor-
susceptible state, but also that this state could be transferred to syngeneic
animals by lymphoid cells.
In this study, we report the results of experiments designed to evaluate
the potential protective effect of a commercial sunscreen preparation on the
immunologic suppression of contact hypersensitivity by UV radiation. We
observed that this sunscreen preparation with PABA and oxybenzone as
active ingredients was incapable of preventing the immunologic suppression
contact hypersensitivity by UV radiation.
MATERIALS AND METHODS
Animals
Inbred albino hairless mice which have been bred in our laboratories
the inbred HRA/Skh strain were obtained from Stanley Mann of Philadelphia*
The hairless mice were from 8 to 16 weeks old at the start of an experiment*
but in any one experiment, the age of the animals did not vary by more than '
week. The animals had free access to Purina Lab Chow and water and were
132
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housed in rooms where ambient lighting was automatically regulated on a 12-
hour light/dark cycle.
Contact Sensitization
Each experimental group utilized 5-10 hairless mice. Contact hyper-
sensitivity was induced by the method of Asherson and Ptak (1968). The
abdomen was painted with 100 yl (microliters) of a 5% solution of trinitro-
chlorobenzene (TNCB) in acetone. The mice were tested for the development of
contact hypersensitivity five days later by applying 5 jil of a 1? TNCB in
acetone to both surfaces of each ear. Ear thickness was measured with an
engineer's micrometer (Model No. 7309, Mitutoyo, Japan) before and 24 hours
after application of the challenge dose. The ear swelling obtained was
compared to the ear swelling of control mice that were challenged, but not
3ensitized. The statistical significance of the differences in ear swelling
between groups was evaluated using the Student's T-test.
Preparation
A commercial sunscreen (SPF-6) contained padimate 0 and oxybenzone as
active ingredients. The sunscreen was applied uniformly to the dorsal skin of
the mice at a final dose of 2 pi/cm2, 20 minutes prior to UV exposure.
Sources and Measurements
Two energy sources were used during the experiments. One source was a
kW xenon arc solar-simulating lamp which has been previously described
Menter, and Whyte 1981). Energy output from this lamp system was
Measured by a calibrated Eppley Thermopile in conjunction with a Keithley
^illlmicroyoltmeter (Model 149). The total radiation was determined to be
26.2 mW/cm , 86 cm (11.5 in) from the exit port. The second source was a bank
°f three FS36T12-UV-B-VHO lamps (Light Sources) housed in an Ultralite bench
top irradiator [BT 3-36 VHO(UV-B)]. Energy output from this system was
Measured as above 19 cm (7.5 in) from the source and the total output was
determined to be 1.4 mW/cm2.
HjjUmal Erythema Dose (MED) Determination
For each UV energy source, five hairless mice were irradiated at 25% dose
increments. Erythetnal responses were noted 24 hours after irradiation. The
MED was taken as the exposure required to elicit barely visible minimal red-
ness. Each set of experiments was repeated three times. SPF values were
assessed for a sunscreen preparation as the ratio of MED with sunscreen to MED
without sunscreen.
S£fect of UV Exposure on the Development of CHS
To assess the depression of CHS by UV treatment, mice were sensitized
three days after the last UV treatment and challenged five days later. The
net ear swelling (ear swelling of sensitized and challenged mice minus the ear
Celling of unsensitized, but challenged mice) was determined for unirradiated
and UV-treated mice. The percentage of control response was determined by the
formula: A-B/C-D X 100. The letters represent the ear swelling
(A) mice exposed to UV and sensitized with TNCB; (B) mice exposed to UV,
133
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but not sensitized; (C) unirradiated and sensitized mice; and (D) unirradiated
and unsensitized.
RESULTS
MED Determination
The doses required to elicit minimal erythema responses for solar-simula-
ting radiation (SSR) and FS36 sunlamps are given in Table 1. Minimal
erythemal dose determination for three FS36 sunlamps was determined to be 38.5
mJ/cnr while the total MED dose for SSR was 8 J/cm . To test the MED of a
commercially available sunscreen (SPF-6), sunscreen was applied to the dorsal
surface of inbred hairless mice at a final dose of 2 pi/cm2, 20 minutes prior
to UV exposure. For both radiation sources, the commercially available
sunscreen was determined to have a MED of 6.0 ± 0.5.
Topical Application of Sunscreen and
UV-Induced Suppression of Contact Hypersensitivity
In the first set of experiments, two groups of ten mice were pretreated
with sunscreen; one group served as an unirradiated control, group 2, while
the other, group, group 4, was irradiated with a bank of three FS36 sunlamps-
During the treatment regimen, no erythematous response was observed in the
group receiving the sunscreen preparation. Table 2 shows the results obtained
from mice given sunscreen and treated with UV-B radiation. Sunscreen applica-
tion had no effect on the contact hypersensitive response, as seen by the
similarity in groups 1 and 2. The amount of suppression with (44$) and
without (50%) topically applied sunscreen was similar.
In the second part of the experiment (Table 3), the sunscreen preparation
was topically applied to a group of ten mice receiving SSR radiation (group
4), and another group of ten mice, group 2, which served as a control. The
results show that topical application of sunscreen had no effect on the
ability of mice to mount a CHS response, groups 1 and 2. The presence of the
sunscreen had no effect on suppression of contact hypersensitivity by SSB.
The amount of suppression with applied sunscreen was 45/E (group 4) while
suppression from SSR alone (group 3) was 40$. As with the previous experi-
ment, no erythematous response was observed in the group receiving the sun-
screen preparation.
To determine if the previously observed suppression was due to heat
alone, two groups of mice were exposed to SSR radiation through a Schott WG
385 filter, a cut off filter with 50% transmission at 385 nm (Table 4, groups
2 and 3). Group 3 received topical sunscreen application while group 2 was
treated with SSR alone. The total UV dose of 36 J/cnr was unable to suppress
the contact hypersensitivity response when filtered through a Schott WG 385
filter. However, in the absence of the Schott filter in both the SSR group
alone (group 4) and the group receiving topical sunscreen plus SSR (group 5)»
suppression of contact hypersensitivity was observed.
DISCUSSION
Treatment of' hairless mice with a commercial sunscreen (SPF-6) which
contained padimate 0 and oxybenzone as the active ingredients did not
134
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Table 1. Minimal Erythemal Dose Determination for UV Sources
in Presence and Absence of Applied Sunscreen
Sunscreen
-
-
4-
4-
UV
Source
SSRC
FS36d
SSR
FS36
Total
UV Dose
(J/cra1)
8
0.0385
44-52*
0.21-0.256
MEDs Rated SPFb
1
1
5.5-6.5e 6
5.5-6.5C 6
a. Obtained from a commercial source. Active Ingredients were Padimate 0 and
Oxybenzone.
b. Manufacturer's rating.
c. Solar simulating radiation from a 1.6 kW xenon arc lamp.
d. 3 FS36T12-UVB-lamps housed in an Ultralite bench top irradiator.
e. Range of 3 determinations.
Table 2. Effect of Padimate 0 and Oxybenzone on Suppression of
Contact Hypersensitivity by UV-B Radiation
Total Ear swelling
UV dose (cm X 10"^
Group Treatment
1
2
3
4
Nil
Sunscreen (SS)
UVB
UVB 4- SS
(mJ/cm1)
0.0
0.0
173. 3e
173. 3e
4-TNCB
44.3 ± 2.3
43.2 ± 2.2
28.3 t 2.3
26.3 i 3.8
Net ear Percent
swelling suppression Pc
-TNCB
8.5 ±
8.2 ±
8.3 i
8.4 ±
1.3
1.2
1.4
1.5
35.8
35.0
20.0 44
17.9 50
<.001
<.001
a FS36 Sunlamp - see text
b Mean (± SD) of 10 mice challenged 24 hours earlier with TNCB on the ears.
c Probability of no difference from group 1 (no treatment).
d Commercially available sunscreen. SPF 6.
Five equal treatments of 34.7 J/cm were
after final exposure and challenged 5 days after sensitization.
e Five equal treatments of 34.7 J/cm were given on consecutive days. Mice were sensitized 3 days after
135
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Table 3. Effect of Padimate 0 and Oxybenzone on Suppression of Contact
Hypersensitivity by Solar-Simulating Radiation (SSR)
Group
1
2
3
4
Treatment
Nil
Sunscreen (SS)
SSR
SSR + SS
Total
UV dose0
(31cm1)
0.0
0.0
36.0
36.0
Ear swelling
(cm X 10 )
+TNCB
44.3 ± 2.3
43.2 t 2.2
30.1 ± 2.3
27.7 ± 2.5
-TNCB
8.5
8.2
8.5
8.1
± 1.3
± 1.2
± 1.5
± 1.6
Net ear Percent .
swelling suppression P
35.8
35.0
21.5 40 <.001
19.6 45 <.001
a Xenon arc. 1.6 kW (see text).
b Mean (± SD) of 10 mice challenged 24 hours earlier with TNCB on the ears.
c Five equal treatments of 7.2 J/cm1 given on consecutive days. Following the last exposure, the mice
were sensitized 3 days later. Five days after sensitization, the mice were challenged.
d Probability of no difference from group 1 receiving no treatment.
e Commercially available sunscreen with an SPF of 6.
Table 4. Effect of a Schott WG 385 Filter on the
Suppression of Contact Hypersensitivity
Group
1
2
3
4
5
Total Ear swelling
UV dose (cm X 10~ ) Net ear Percent
Treatment (mJ/cm2) swelling suppress!
+TNCB -TNCB
Nil 0.0 33.8 ± 3.49 6.2 ± 1.1 27.5
Schott WG385 36 37.2 ± 3.19 6.9 ± 1.3 30.3
+ SSR
Schott WG385 36 35.4 ± 2.6 6.4 ± 1.6 29.0
+ SSR t SSd
SSR 36 23.1 ± 2.6 6.2 ± 1.2 16.9 39
SSR + SS 36 22.9 ± 3.2 6.1 ± 1.3 16.8 40
on PC
<.ooi
<.00l
^--
a Mean (± SO) of 10 mice challenged 24 hours earlier with TNCB on the ears.
b Five equal treatments of 7.2 J/cm* given on consecutive days. Following the last exposure, the mice
were sensitized 3 days later. Five days after sensitization, the mice were challenged.
c Probability of no difference from group 1 receiving no treatment.
d Commercially available sunscreen with an SPF of 6.
136
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prevent systemic immunologic suppression of contact hypersensitivity following
exposure with either SSR or FS36 sunlamps. These results differ from those of
Morison (1984), who found that pretreatment of C3H mice with PABA sunscreen
(SPF-8) only induced 25% suppression of the contact hypersensitivity response
following UV-B exposure, which he determined not to be significant. We used
different mice, albino hairless, and a sunscreen with an SPF-6 rating. In
addition, our total dose of UV was lower than his by a factor of TO. These
differences alone could account for the discrepancy between Morison's and our
results.
In Morison's study, the feet and nose were neither covered nor treated
with sunscreen. Hence, the UV-induced suppression he observed in C3H mice
could have been due to irradiated areas not treated with sunscreen. In our
experiments, the head and neck were covered with a shield and the back, feet,
and tail treated with sunscreen. Thus, our results are difficult to explain
by exposure of non-sunscreen treated sites.
If mice are irradiated with polychromatic UV radiation, which was insuf-
ficient to elicit an erythema "sunburn" response, then UV-A rather than UV-B
might be responsible for the induction of immune suppression observed in our
experiments. However, because previous studies have shown that wavelengths
shorter than 320 nm are responsible for systemic immunologic suppression
(Noonan et al. 198la; De Fabo and Kripke 1980), other alternatives are
considered. The finding that the sunscreen did not abrogate the effects of UV
radiation on contact hypersensitivity might be explained by assuming that
sunscreen agents act as photosensitizers initiating a photochemical reaction
in the skin that could then lead to the suppression of contact
hypersensitivity (Gurish et al. 1981). In support of this theory, Hodges et
a^' (1977) found increased genetic damage when E^ coli were irradiated in the
Presence of PABA. Another explanation is that the amount of energy not
absorbed by the sunscreen agent is sufficient to induce the suppression of
contact hypersensitivity. The location of the sunscreen in the skin may be
very important in this regard. Willis and Kligman (1970) demonstrated that
aignificant photoprotection from PABA persisted despite repeated stripping of
the stratum corneum. These results suggest that sunscreens may "pool" beneath
the stratus corneum. Recently, De Fabo and Noonan (1983) suggested that a
Photoreceptor, urocanic acid, resides close to the surface of the skin in the
stratum corneum. This receptor mediates the initial event in systemic
inanunologic suppression by UV radiation. Our results are consistent with
their interpretation: for if sunscreens pool beneath the stratum corneum,
this would allow exposure of the photoreceptor, which is in the stratum
corneum and above the sunscreen, so that subsequent events associated with
systemic immunologic suppression could take place.
PABA absorbs radiation between 270 and 320 nm very efficiently, but not
wavelengths below 270 tun. The experiment using the FS36 lamps could be
explained by radiation exposure below 270 nm because no filter was used to cut
°ut these wavelengths. However, the experiment that used SSR, which emits
essentially no irradiation less than 290 nm, cannot be explained as due to
UV-C radiation not absorbed by the sunscreen.
Because sunscreens are known to protect against both skin damage and the
carcinogenic effects of UV radiation, our results seem to suggest a separation
of UV-induced carcinogenic effects from the systemic immunologic effects. Our
137
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results also suggest that if these results can be generalized to humans, the
use of sunscreens may not provide the protection needed to abrogate the
immunologic effects of UV radiation. Thus, even sunscreen users Would be at
increased risk for skin cancer, because altered antigen presentation would
already have been established and the formation of suppressor T cells would
appear earlier in these individuals than in those persons who have never had
any sun exposure.
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140
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Sunlight and Malignant Melanoma
in Western Australia
Bruce K. Armstrong
University of Western Australia
Western Australia Australia
PRODUCTION
The incidence (frequency of occurrence of new cases per unit,of popula-
tion) of malignant melanoma (MM) of the skin is increasing about 5% per year
in most white populations (Muir and Nectoux 1982). Lancaster (1956) was the
first to suggest that this cancer may be substantially due to ultraviolet
radiation from the sun. He observed a threefold variation in mortality from
Melanoma between the populations of Queensland in the north of Australia (high
^rtality) and Tasmania in the south (low mortality). The populations of the
°ther states were distributed between them approximately in relation to the
latitudes of their main population centers. Similarly, Lancaster noted that
European populations residing in the comparatively sunny climates of
Australia, South Africa, and California exhibited higher mortality from MM
than in the European countries from which they originated.
A number of observations are apparently inconsistent with a simple causal
relationship between sun exposure and MM. Other skin cancers, which are
Senerally believed to be caused mainly by sunlight, are more common in men
than women (perhaps because men often work outside), increase exponentially in
incidence with age (the pattern expected from lifelong exposure to an agent
that can initiate cancer), and occur most commonly on the more exposed head,
neck, and hands. In contrast, MM occurs as often in women as in men, shows a
relative peak in incidence in middle life, and is most common on the back in
"fcn and legs in women (Holman et al. 1980). There are also a number of geo-
graphical areas in which the incidence of MM does not increase with increasing
Proximity to the equator. These areas include the Australian states of
Western Australia and Queensland, which cover a wide range of latitudes, and
Europe where MM incidence decreases with increasing latitude to about 50°N and
then increases with increasing latitude (Armstrong 1984). These geographical
inconsistencies, however, may be caused by a failure to adequately consider
skin pigmentation and climatic factors that modify exposure and sensitivity to
aunlight. More significant is the relationship between the incidence of MM
141
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and occupation and socioeconomic status. Whereas other skin cancers are more
common in outdoor than indoor workers, as would be expected if they are caused
by exposure to the sun, the opposite is true for MM. Similarly, incidence of
other skin cancers tends to increase with decreasing socioeconomic status
(perhaps because low status jobs tend more often to be outside) while the
opposite is true for MM (Holman et al. 1980).
These observations led to the "intermittent exposure hypothesis" for the
relationship of sunlight to MM. Briefly, this hypothesis states that:
• Incidence of MM is determined as much (or more) by the pattern of sun
exposure as by the total accumulated "dose" of sun exposure.
• Infrequent (intermittent) exposure of untanned skin to high doses of
sunlight is particularly effective in increasing incidence of MM.
Thus, incidence rises initially as frequency of exposure increases but
may fall as exposure becomes more continuous.
A simple rationalization for this complex, postulated exposure-response
pattern is that developing and maintaining a suntan protects one from the
carcinogenic effects of continuing sun exposure. With infrequent sun expo-
sure, a tan is not maintained (except in those with high natural skin pigmen-
tation or who tan very easily), and the melanocytes are substantially unpro-
tected from solar UV on each occasion of exposure.
The Western Australian Lions Melanoma Research Project, carried out i°
Western Australia in 1980 and 1981, was designed to test the intermittent
exposure hypothesis.
METHODS OF DATA COLLECTION AND ANALYSIS
The methods have been fully described elsewhere (Holman and Armstrong
1984a). In brief, 511 patients with histologically confirmed MM were
studied. They were 76$ of a total of 670 cases less than 80 years of age and
diagnosed in accessible regions of Western Australia in a period of 675 days
beginning January 1, 1980. Clinical details were obtained from the doctors
who treated the patients and the histopathological diagnosis was reviewed and
confirmed by a panel of pathologists.
Five hundred eleven control subjects, each matched to one of the melanoma
patients by age, sex, and area of residence, were also studied. They were
selected at random from the Australian Commonwealth Electoral Roll (electoral
registration is compulsory in Australia) or, if the MM patient was less than
18 years of age, from the student roll of the area public school. The final
series of 511 control subjects was 69% of those approached.
The patients with MM and the control subjects were approached in identi-
cal fashion and asked to participate in an interview on "environment, life-
style, and health," which lasted from one to two hours. The interviews were
conducted in the subjects' homes (occasionally workplaces) by trained nurse
interviewers who were not told whether the person that they interviewed was a
MM patient or a control subject. The interview covered demographic, constitu-
tional and genetic factors, sun exposure, hormone use, diet, and some other*
variables. Objective measurements were made of skin, eye and hair color*
-------
weight, height, amount of body hair, number of raised moles (pigmented naevi)
on the arms and degree of sun damage to the skin on the back of one hand.
It is possible, by comparing the data obtained from the patients with MM
(often called "cases") and the control subjects, to estimate the extent to
which exposure to specific levels or categories of particular exposure vari-
ables increases the incidence of MM above the incidence in some arbitrarily
chosen reference group (usually those not exposed or those in the lowest
exposure category). The statistic calculated is the incidence rate ratio or
relative risk (as estimated by the exposure odds ratio), abbreviated hereafter
as RR. Because it is a ratio, values of the RR above 1.0 for a particular
category of exposure imply that the incidence of MM is increased in that
category in comparison with the incidence in the reference category. RRs were
calculated by the methods recommended for matched case-control studies by
Breslow and Day (1980). For each, a 95% confidence interval (CI) was also
calculated. Given that samples of both MM patients and controls were studied,
each of the statistics calculated has sampling variability. The CI is the
interval in which it is 95% likely that the true value of the RR for the
Population as a whole lies.
When interpreting an RR for a particular exposure category, it is neces-
sary to consider the possibility that the observed association is influenced
by some "confounding" variable that is related to both the exposure variable
for which the RR has been calculated and to MM. For example, people with
highly sun-sensitive skins may tend to expose themselves less to the sun than
those with not-so-sensitive skins. If sun sensitivity is associated with an
increased incidence of MM, this could reduce the strength of any association
between sun exposure and MM unless the confounding effects of sun sensitivity
are controlled when examining the effects of sun exposure. This control was
achieved by use of conditional logistic regression analysis (Breslow and Day
1980) and adjusted RRs were calculated, where relevant, free of the effects of
specific confounding variables.
RESULTS
pigmentary Characteristics and Sensitivity of the Skin to the Sun
The RRs for categories of skin color, hair color, and eye color are
summarized in Table 1. The skin color measurement was a reflectance measure-
ment; thus low values represent dark skin. It was made on the skin of the
uPper inner arm to avoid, as far as possible, pigmentation due to sun
exposure.
Incidence of MM increased in ordered categories of each of these vari-
ables with increase in the characteristics that are usually thought of as
being associated with sun sensitivity. Thus the highest incidence of MM was
in those with light skin, red hair, and blue eyes. A "P value" of <0.05 means
fchat the probability that the pattern observed in the RRs was due solely to
chance (sampling variability) was less than 5% (i.e., 1 in 20). For skin
color and hair color it was very much less than 5%.
143
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Table 1. Associations Between Pigmentary Characteristics and Incidence
of Malignant Melanoma in Western Australia, 1980-81
Characteristic
Relative
Risk
95%
Confidence
Interval
Skin color (reflectance)
<47*
47-55*
56-64*
65*+
Hair color
Black or dark brown
Light brown
Fair or blond
Red
Eye color
Brown
Hazel
Green
Grey
Blue
1.00
1.05
1.59
3.07*
1.00
1.45
1.89
2.33*
1.00
1.49
1.57
1.33
1.61*
0.69 1.59
0.95 2.66
1.47 6.39
1.08 1.94
1.29 2.77
1.26 4.30
1.01 2.18
0.97 2.53
0.71 2.46
1.16 2.21
* P value for trend in each case <0.05.
Source: Holman and Armstrong (1984a)
Sensitivity of the skin to the sun was ascertained by asking two
questions:
If your skin was exposed to strong sunlight for the first time in summer
for one hour, would you...
(1) Get a severe sunburn with blistering?
(2) Have a painful sunburn for a few days followed by peeling?
(3) Get mildly burnt followed by some degree of tanning?
(4) Go brown without any sunburn?
After repeated and prolonged exposure to sunlight would your skin
become...
(1) Very brown and deeply tanned?
(2) Moderately tanned?
(3) Only mildly tanned due to a tendency to peel?
(4) Only freckled or no suntan at all?
Relative risks of MM for these categories of sun sensitivity are shown in
Table 2. Both acute and chronic skin response to sunlight were strongly
144
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Table 2. Associations Between Sensitivity of the Skin to Sunlight and
Incidence of Malignant Melanoma in Western Australia, 1980-81
95%
Relative Confidence
Characteristic Risk Interval
Acute skin reaction to sunlight
No sunburn 1.00
Mild sunburn 2.63 1.63 4.26
Painful sunburn 2.63 1-62 4.26
Blisters 3.39* 1-90 6.03
skin reaction to sunlight
Deep tan 1.00
Moderate tan 1.45 1.08 1.94
Mild tan 2.27 1.58 3.26
No tan 3.53 1.82 6.84
* P value for trend in each case <0.001.
Source: Holman and Armstrong (1984a)
to incidence of MM with the highest incidence being in those with
greatest sensitivity to the sun.
Of all the pigmentary characteristics and measures of skin response to
sunlight, chronic skin response to sunlight was the strongest predictor of the
^isk of MM. When these variables were included together in a logistic regres-
sion model, acute skin response to sunlight and hair color, together with
°hronic skin response to sunlight, were significantly correlated with
incidence of MM. It is at least plausible to suggest that skin response to
Sunlight is the important predictor of risk of MM and that hair color appeared
to be independently predictive only because skin response was measured with
some error.
MM is known to be rare in pigmented races (Crombie 1979). Like the
Association of MM with response of the skin to sunlight in white races, this
°bservation suggests that sunlight may be a cause of MM. In the Western
Australian study, subjects were classified by the ethnic origin of their
Grandparents (if they had two or more grandparents of the same ethnic origin)
into one of the following categories: Celtic (Irish, Scottish, or Welsh),
^glish, Australian (mainly Celtic or English, there were no Australian abori-
gines in the study), Southern European, Northern European, African, or
Asian. RRs for MM by ethnic origin are given in Table 3. The RRs have been
adJusted for possible confounding effects of age at arrival in Australia
145
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Table 3. Associations Between Ethnic Origin and Incidence of Malignant
Melanoma in Western Australia, 1980-81
953!
Relative Confidence
Ethnic Origin Risk Interval
Celtic 1.18* 0,82 1.70
English 1.03 0.71 1.48
"Australian" 0.97 0.66 1.43
Northern European 0.57 0.31 1.06
Southern European 0.39 0.17 0.89
African or Asian 0.42 0.05 3.34
* RRs are adjusted for age at arrival in Australia and each other ethnic
origin category.
Source: Holman and Armstrong (1984a)
(many of the non-Australian subjects were migrants and therefore had a
incidence of melanoma regardless of their ethnic origin; see below)
represent the effects of each ethnic group independently of all the others.
There were few subjects in the study who belonged to ethnic groups (e.g->
born in Africa or Asia) that might reasonably have been expected to have had
pigtnented skin. The lowest risk, however, was in those of Southern European
ethnic origin whose skins are generally darker than those of people originat-
ing elsewhere in Europe. The pattern is therefore consistent with a protec-
tive effect of ethnically determined skin pigmentation against MM.
Birthplace. Age at Arrival, and Duration of Residence in Australia
Most Australians of European origin who were born outside Australia have
migrated to Australia from a region of lower exposure to the sun. Thus, ^
sunlight is a cause of MM, they would be expected to have lower incidence
rates of MM than native-born Australians. This has been observed to be the
case in descriptive studies (Armstrong et al. 1982). In the 1980-81 case-
control study, incidence of melanoma increased with increasing duration of
residence in Australia and fell with increasing age at arrival in Australia.
Since age at arrival and duration of residence are correlated one with the
other, both were included in a logistic regression analysis to see which, if
only one, was independently related to incidence of MM. The results of this
analysis are shown in Table 4, After adjustment for duration of residence,
incidence still fell with increasing age at arrival while adjustment for age
at arrival removed the observed effect of duration of residence. Thus, if sun
exposure is responsible for the high incidence of MM in native-born
Australians relative to that in migrants to Australia, it appears that expo*
sure early in life is necessary to have this effect.
146
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Table 4. Associations Between Incidence of Malignant Melanoma and Age at
Arrival in Australia and Duration of Residence in Australia, Each
Adjusted for the Effects of the Other, Western Australia, 1980-81
9555
Relative Confidence
Characteristic Risk Interval
Age at arrival
Birth 1.00
0-9 years 0.89 0.44 1.80
10-29 years 0.34 0.16 0.72
30+ years 0.30* 0.08 1.13
Duration of residence
0-24 years 1.00
25-39 years 0.80 0.41 1.56
40-59 years 0.93 0.26 3.25
60+ years 1.02 0.20 5.08
* P value for trend <0.001.
Source: Holraan and Armstrong (1984b)
J!§an Annual Hours of Bright Sunlight
To obtain a measure of the potential for exposure to the sun at all their
Places of residence, Holman and Armstrong (1984b) calculated the mean annual
hours of bright sunlight (as given on climatology maps) averaged over all
Places of residence (as obtained in a residence history) and weighted by the
Duration of residence. This measure did not account for the time that each
subject spent in the sun. The analysis was restricted to native-born
Australians to separate the effects of residential sunlight from those of
Place of birth. The results are shown in Table 5. Incidence of MM nearly
doubled between those with less than 2600 mean annual hours of bright sunlight
&t places of residence and those with more than 2800 hours. Migrants to
Australia had about half the incidence of MM as native-born Australians with
less than 2600 annual hours of bright sunlight on average. When mean annual
hours of bright sunlight were controlled in a logistic regression analysis,
mean latitude of residence showed no association with, risk of melanoma.
suggests that the effect of latitude on incidence of MM can be explained
the effect of sunlight.
147
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Table 5. Association Between Mean Annual Hours of Bright Sunlight at
Places of Residence of Native-Born Australians and Incidence of
Malignant Melanoma in Western Australia, 1980-81
95*
Mean Annual Hours of Relative Confidence
Bright Sunlight Risk Interval
Native-born Australians
<2600 hours 1.00
2600-2799 hours 1.34 0.96 1.86
2800-1- hours 1.92* 1.16 3.18
Migrants (all hours) 0.51 0.35 0.74
* P value for trend 0.003.
Source: Holman and Armstrong (1984b)
Other Objective Measures of Total Accumulated Exposure to the Sun
The degree of damage caused to skin on the back of the hand by exposure
to the sun was measured by means of cutaneous microtopography (Holman et al«
1984). A silicone mold is made of the skin markings on the back of the hand,
examined under a dissecting microscope, and graded on a scale from 1 to 6, 1
indicating the least solar damage and 6 the most. The degree of skin damage
was taken to be an indicator of total accumulated exposure to the sun. A
history of past non-melanocytic skin cancer was also obtained. Because non-
melanocytic skin cancers are believed to be predominately sun-induced they
were considered to indicate individuals who had been heavily exposed to the
sun.
The relationships of MM incidence with cutaneous microtopograph grade and
past history of skin cancer are shown in Table 6. Incidence of MM increased
with increasing severity of solar damage to the skin such that the incidence
in those with grade 6 damage was nearly three times that in those with only
grades 1-3 damage. Similarly, the incidence of MM was higher in those with &
past history of non-melanocytic skin cancer than in those without. Adjustment
of the latter association for possible confounding effects of acute and
chronic reactions of the skin to sunlight, hair color, and numbers of
European, African, and Asian grandparents reduced the RR from 3.71 to 2.87
1.64-5.04).
148
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Table 6. Associations Between Incidence of Malignant Melanoma and Degree
of Sun Damage to the Skin of the Back of the Hand and Past
History of Non-Melanocytic Skin Cancer, Western Australia,
1980-81
95%
Relative Confidence
Characteristic Risk Interval
Sun damage to the skin of the back of the hand
(cutaneous microtopography grade)
Grades 1-3 1.00
Grade 4 1.64 0.97 2.78
Grade 5 1.76 0.97 3.19
Grade 6 2.68* 1.44 4.98
Past history of non-melanocytic skin cancer
No 1.00
Yes 3.71* 2.11 6.57
* P value for trend in each case <0.01
Source: Holman and Armstrong (1984b)
Pattern of Sun Exposure
The evidence on the associations between incidence of MM and average
hours of bright sunlight at places of residence, sun-induced skin damage, and
Past history of non-melanocytic skin cancer strongly supports the role of sun
exposure in the causation of the disease. These measures of sun exposure,
however, are essentially measures of total accumulated exposure over a life-
time and reveal nothing about the pattern of exposure. A detailed history of
sun-exposure habits was taken from subjects in. the Western Australian study to
Provide evidence relevant to the intermittent exposure hypothesis. They were
asked to provide estimates of the time spent outdoors in both summer and
winter on typical working and non-working days for all periods of employment
throughout their working lifetimes (Mondays through Fridays were treated as
Epical working days for students, housewives, and retired people). Details
we^e also sought regarding specific outdoor pursuits and clothing habits when
outdoors. All the RRs presented are adjusted for the potential confounding
effects of acute and chronic skin reaction to sunlight, hair color, ethnic
Or*igin, and age at arrival in Australia.
Table 7 summarizes results for average estimated outdoor time per week
°ver the lifespan (since leaving school) and the proportion of the total
outdoor time that was recreational (a measure of intermittency of the expo-
sure) between 10 and 24 years of age.
149
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Table 7. Associations Between Incidence of Malignant Melanoma and Average
Average Estimated Outdoor Time in Summer Over the Lifespan and
the Proportion of the Total Outdoor Time During the Summer at
Ages 10-24 Years That Was Recreational, Western Australia, 1980-81
95*
Relative Confidence
Characteristic Risk Interval
Average total outdoor time
0-10 hours/week 1.00
11-15 hours/week 0.85 0.55 1.31
16-22 hours/week 0.78 0.52 1.19
23+ hours/week 0.70 0.43 1.12
Proportion (%) of outdoor time that was recreational
(Ages 10-24 years)
0-29 1.00 -
30-39 1.14 0.71 1.84
40-59 1.16 0.76 1.77
60+ 1.28 0.85 1.94
Source: Holman, Armstrong, and Heenan 1986
The trend in the RRs for total outdoor time showed the anomalous pattern
that has been observed in descriptive data: incidence of MM fell rather than
rose with increasing time spent out of doors. This trend, however, could have
been due to chance as the P value was quite high (0.13). Both of the com-
ponents of outdoor time (outdoor time at work and time in outdoor recreation)
showed similar downward trends (Holman, Armstrong, and Heenan 1986) but as the
proportion of the outdoor time that was recreational increased, the incidence
of MM tended to rise (Table 7). The P value for this trend, however, was also
rather high (0.25). The recreational exposure proportion was examined for the
period of life from 10 to 24 years of age because this was the period in which
the negative gradient with total outdoor time was most evident.
Because the intermittent exposure hypothesis is thought to relate most
strongly to superficial spreading melanoma (SSM) (Holman, Armstrong, and
Heenan 1983), the most common of the four histological types of MM, the analy-
ses of Table 7 were also carried out for this particular type of MM. SSM was
more strongly related negatively to average total outdoor time per week during
the summer (P=0.09) and positively to the proportion of outdoor time that was
recreational (P=0.15) than was MM as a whole.
Incidence of SSM was also strongly related to frequency of participation
in some but not all outdoor recreations that involve substantial sun exposure
(Table 8). It is particularly interesting that a relationship between fre-
quency of sunbathing and incidence of SSM was evident when only SSM of the
trunk was analyzed (the trunk is presumably the body site subject to the most
150
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Table 8. Associations Between Frequency of Particular Outdoor Recreations
in Summer and Incidence of Superficial Spreading Melanoma in
Western Australia, 1980-81
Activity
Relative
Risk
Confidence
Interval
Boating
Never
Less than once a week
Once or more a week
1.00
1.06
2.43*
0.54
1.10
2.09
5.39
Fishing
Never
Less than once a week
Once or more a week
1.00
1.03
2.72
0.63
1.15
1.68
6.43
Swimming
Never
Less than once a week
Once or more a week
1.00
1.30
1.14
0.76
0.72
2.20
1.82
^bathing
vAges 15-24 years only)
Never
Less than once a week
Once or more a week
15-24 years and SSM of trunk only)
Never
Less than once a week
Once or more a week
1.00
1.26
1.32
1.00
1.20
2.55*
0.78
0.80
0.51
1.05
2.05
2.17
2.81
6.19
P
+ * value for trend in each case <0.05.
Detailed questions asked only for this period of life.
Source: Holman, Armstrong, and Heenan (1986)
se intermittent exposure with sunbathing). MM other than SSM did
strong associations with any of these recreational exposures.
not
151
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Clothing may modify the relationship between sun exposure and incidence
of MM, as Table 9 shows. Incidence of both melanoma and SSM is examined in
relation to the person's clothing habit during outdoor work in summer at the
primary site of the MM. The incidence of both was substantially higher in
those who sometimes or usually exposed the primary site than in those who
usually kept it covered. For all MM the RR was highest in those who sometimes
exposed the site, an observation that is consistent with the intermittent
exposure hypothesis. This was not the case, however, for SSM. SSM of the
trunk in women was very strongly related to the type of bathing suit that had
been worn in summer between 15 and 24 years of age. Relative to an RR of 1.00
in those who had worn a one-piece suit with a high back-line, the RR was 4.04
(CI 0.65-25.2) in those who had worn a one-piece suit with a low back-line,
and 13.0 (CI 1.95-83.9; P value for trend 0.005) in those who had worn a two-
piece suit or no bathing suit at all.
Table 9. Associations Between Clothing Habit at the Primary Site of
Malignant Melanoma During Outdoor Work in Summer and Incidence
of Malignant Melanoma in Western Australia, 1980-81
— r _^^^^^^*
95%
Relative Confidence
Clothing Habit Risk Interval
All Melanomas
Usually covered 1.00
Sometimes exposed 2.49 1.58 3.94
Usually exposed 2.08* 1.27 3.40
Superficial Spreading Melanoma Only
Usually covered 1.00
Sometimes exposed 2.16 1.14 4.10
Usually exposed 2.43* 1.18 4.97
* P value for trend in each case <0.01.
Source: Holman, Armstrong, and Heenan (1986)
DISCUSSION
The reduction of MM incidence by high natural skin pigmentation and its
increased incidence in skin that is highly sensitive to the sun are wel1
known. These observations have been confirmed by the Western Australia0
study. Indirectly, they implicate sunlight in the etiology of MM. This study
has also provided evidence that incidence of MM increases with total accumu~
lated exposure to the sun. Incidence was lower in migrants to Australia tha*1
in native-born Australians, was positively associated with mean annual hour3
152
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°f bright sunlight averaged over all places of residence, and increased in
those with sun-damaged skin and a past history of non-melanocytic skin cancer
(generally accepted as being due to exposure to the sun).
Superimposed on this background, there was some evidence that inter-
wittency of sun exposure may be particularly important in causing MM. Inci-
dence rose slightly with increases in the proportion of total exposure that
was recreational, but certain outdoor recreations, often involving intense sun
exposure, appeared to be particularly strongly related to it, for example,
boating, fishing, and sunbathing for MM of the trunk. When clothing habits
were taken into account, there was strong association between MM and unclothed
exposure of the primary site of the tumor while at work. Thus the anomalous
relationship between MM incidence and outdoor work overall may be due, in part
at least, to a tendency of those who work outdoors to be more careful in
protecting themselves from the sun than those who expose themselves only
recreationally.
If the intermittent exposure hypothesis for the relationship of MM to
sunlight is correct, it has important implications for prevention. Figure 1
shows a concept of the exposure-response relationship for SSM and sunlight
under the intermittent exposure hypothesis. While this concept applies to
lesions that have their origin in SSM, as they are probably the majority of
MM» it may be considered to apply to MM as a whole, On average (curve C)
incidence of SSM first rises as frequency of exposure increases and then falls
aa some critical exposure frequency is passed. Thus, on average, whether or
not reduction in sun exposure will be a "good thing" (in terms of prevention
of MM) will depend on where a population lies on this exposure-response
curve. The position will probably depend both on the genetic composition of
the population and the available sunlight (expected absorbed dose per unit of
time of exposure to the sun).
At the individual level, the shape of the exposure response curve will
Probably be determined by the pigmentary response of the skin to sunlight.
Those with a. poor pigment response (curve B) may experience progressively
increasing incidence of SSM, whatever the frequency (and dose) of sun expo-
sure, because a protective tan is never obtained. Others who tan readily
(curve A) may show little rise in incidence of SSM at all with increasing sun
exposure before incidence falls back to background levels with further sun
exposure. While the former may be best advised to protect themselves against
the sun at all times; the latter, if exposed more than minimally, should
perhaps continue sun exposure to ensure that they stay as far as possible to
the right of the peak. Until these concepts are clarified or discarded,
caution should be exercised in making recommendations about sun exposure—at
least with reference to prevention of MM.
153
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Incidence
rate of SSM
Low pigment response
Average pigment response
^ High pigment response
^^-^
*^^»
Figure 1.
Frequency of UVR exposure
A Concept of the Exposure Response Relationship for Super-
ficial Spreading Melanoma And Sunlight
154
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REFERENCES
Armstrong, B.K. 1984. Melanoma of the skin. Brit. Med. Bull. 40:346-50.
Armstrong, B.K., C.D.J. Holman, J. M. Ford, and T. L. Woodings. 1982. Trends
in melanoma incidence and mortality in Australia. In Trends in cancer
incidence. Causes and practical implications, ed. K. Magnus, 399-417.
Washington: Hemisphere.
Breslow, N.E., and N.E. Day 1980. Statistical Methods in Cancer Research.
Lyon: International Agency for Research on Cancer.
Crombie, I.K. 1979. Racial differences in melanoma incidence. Brit. J. Cancer
40:185-93.
Holman, C.D.J., and B.K. Armstrong. 1984a. Pigmentary traits, ethnic origin,
benign nevi, and family history as risk factors for cutaneous malignant
melanoma. J. Nat. Cancer Inst. 72:257-66.
Holman, C.D.J., and B.K. Armstrong. 1984b. Cutaneous malignant melanoma and
indicators of total accumulated exposure to the sun: An analysis
separating histogenetic types. J. Nat. Cancer Inst. 73:75-82.
Holman, C.D.J., B.K. Armstrong, P.R. Evans, G.J. Lumsden, K.J. Dallimore, C.
J. Meehan, J. Beagley, and I.M. Gibson. 1984. Relationship of solar
keratosis and history of skin cancer to objective, measures of actinic
skin damage. Brit. J. Dermatol. 110:129-38.
Holman, C.D.J., B.K. Armstrong, and P.J. Heenan. 1983. A theory of the
etiology and pathogenesis of human cutaneous malignant melanoma. J. Mat.
Cancer Inst. 71:651-6.
Holman, C.D.J., B.K. Armstrong, and P.J. Heenan. 1986. Relationship of
cutaneous malignant melanoma to individual sunlight exposure habits. J^
Nat. Cancer Inst. 76:403-14.
Holman, C.D.J., C.D. Mulroney, and B.K. Armstrong. 1980. Epidemiology of
preinvasive and invasive malignant melanoma in Western Australia. Int. J.
Cancer 25:317-23.
Lancaster, H.O. 1956. Some geographical aspects of mortality from melanoma in
Europeans. Med. J. Aust. 1:1082-87.
C.S., and J. Nectoux. 1982. In Trends in cancer incidence. Causes and
practical implications, ed. K. Magnus. Washington: Hemisphere.
155
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Radiometry of Solar UV-B
A- Baqer and N. Kollias
Department of Dermatology, Al-Sabah Hospital, and
Physical Department, Kuwait University, Kuwait
ABSTRACT
Measurements have been conducted using several detectors: polysulfone
, a Robertson-Berger (R-B) meter, an EG&G Spectroradiometer, and an IL
Phototherapy radiometer. The purpose of the study was to assess the solar UVB
*n Kuwait and to arrive at correlations among these detectors, which are
Widely used internationally. These relationships have not previously appeared
ln literature.
Polysulfone-based measurements were carried out over a two-year period at
solar maximum, as a function of the time of day and the angle of the detector
with the horizontal. The R-B meter measurements were conducted over one year
w*th a half-hourly record. Spectroradiometric measurements were conducted
°ver a two-month period and simultaneously with the other two in order to
Establish correlations. The International Light instrument was operated over
a two-month period simultaneously with the polysulfone measurements.
We find that although none of the integrating detectors adequately
Represents the sensitivity of human skin (erythema effectiveness) to
Ultraviolet B radiation (UV-B), they can provide an estimate of the incident
^V-B. Based on the polysulfone measurements, we have arrived at an empirical
expression that predicts (within 10£) the polysulfone reading for any half-
hour interval of the year. We find further that the R-B meter measurements
ape very strongly affected by high temperatures (>45°C). The need therefore
Pemains for a simple recording detector that is not affected by environmental
conditions.
1»THODUCTION
In looking through the literature for solar middle UV-B measurements, as
to the effect of UV-B on human skin (Ambach and Rehwald ,1983; Bener
; Berger and Urbach 1982; Blumthaler et al. 1985a, b; Diffey, Larko, and
157
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Swanbeck 1982; Kollias and Baqer 1984; Mosely, Davison, and Mackie 1983;
Rosenthal, Safran, and Taylor 1985; Qayyum and Davis 1984; Young et al. 1982),
one finds that the following detectors have been used predominately: R-B
meter (sunburning meter), Eppley Labs UV-B radiometer, International Light
phototherapy radiometer, and polysulfone film.
Of these, the Eppley Labs radiometer was not available in the market when
our study started in the fall of 1983. There is a wealth of data on the R-B
instrument and a rapidly accumulating set of data on the polysulfone film
detectors because they are inexpensive and easy to use. The International
Light instrument is available at many phototherapy centers, and therefore it
is tempting to use it outdoors to estimate the dose that the patients receive
after treatment. Spectroradiometric measurements are difficult to find as
they require expensive instruments and competent operators.
A.E.S. Green and his group (1976-82) have carried out a number of
investigations both theoretically and experimentally to characterize the solar
UV-B flux at the earth's surface.
The major aim of this study was to determine the correlation among the
various integrating detectors and then how they relate to the sensitivity of
human skin. By setting all measurements on a common denominator we can make
use of assessments made in various parts of the world with different
detectors'.
MATERIALS AND METHODS
Polysulfone Measurements
The films (40 pm in thickness and 12 x 12 inches in area) were cut and
mounted in 35 mm slide mounts and assessed before and after exposure by
measuring their absorbance at 330 nm (Davis and Gardiner 1982). The change in
absorbance due to the exposure to solar UV-B was converted to an equivalent
305 nm UV-B dose in J/cm2. The films showed good stability with temperature
and humidity; however, their absorbance post exposure changed rather rapidly
with time, especially over the first two days of post irradiation. As a
consequence, all films were assessed as quickly as possible after being
exposed to solar UV-B. Measurements were carried out (8/83-10/85) at solar
maximum, as a function of the time of day, and as a function of the detector
orientation with the horizontal.
Robertson-Berger Meter (Sunburning Meter) Measurements
This is an integrating detector that gives a half-hourly printout of the
measured UV-B radiant energy in counts, where 440 counts equal one "sunburning
unit." Measurements were conducted from 11/84-11/85 at a location very near
to the polysulfone detector holders. This detector had a very large
temperature coefficient when the full range of temperatures attainable in
Kuwait was realized (14£ per 10°C). The dry bulb temperature in an exposed
thermometer ranges from 10° to 75°C. This error becomes very noticeable in
the summer months when the apparent maximum radiation recorded always occurred
before solar maximum. Because we had no way of knowing the internal
temperature of the detector, we decided not to correct the data and not to use
them other than to obtain an estimate of the way the UV-B was varying over the
day and the months of the year.
158
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ii£&CLSpectroradiometer (Model 550) Measurements
This instrument was interfaced to a HP-85 microcomputer, and thus a
spectral scan could be conducted in less than 30 seconds and recorded for
further analysis. Measurements were carried out at solar noon from 3/85 to
5/85. We could not continue beyond May as the ambient temperature was above
^°°c in the shade and the instruments started overheating in the sun.
Measurements were carried out at the same location as the polysulfone and the
R~B meter and at the same time.
^International Lipht 442 Radiometer With a SEE1240 Detector Measurements
The sensitivity of this instrument did not prove to be adequate, and we
therefore installed an analogue output that could be read on a portable
voltmeter, Fluke 77. Measurements were carried out simultaneously with
Polysulfone films in March and April 1986.
^BLTS AND DISCUSSION
Although it has a diffuser at its input, the spectroradiometer has a
Deceiving angle of ±5°. This means that our measurements record only the
Direct component of the solar radiation. The principal use of these
measurements has been to correlate these with the ones conducted by the
Polysulfone and by the R-B detectors. The correlation among the three
instruments can be seen in Figure 1. The readings seem to relate well to each
°ther for clear days, i.e., when the readings are at their maximum values, and
fclley do not appear to relate as well when the measurements were attenuated
either due to clouds or rising dust. We selected the days that were clear, or
Reasonably clear to establish a relationship between the integrated value of
Radiance over the wavelengths 280-325 nm and over 1/2 hour with the values
°btained from the other detectors. (See Table 1.)
Table 1. Spectroradiometric, Polysulfone, and Robertson-Berger
Meter Readings for Selected "Clear" Days
Date
12.3.85
26.3.85
30.3.85
01.4.85
03.4.85
07.4.85
09.4.85
13.4.85
15.4.85
29.4.85
Irrad. 1/2 hr.
0.1488
0.2435
0.2320
0.1733
0.1506
0.2424
0.2671
0.2300
0.1893
0,1866
Polysulfone
0.3010
0.3710
0.3280
0.3380
0.3130
0.3940
0.4180
0.4320
0.3940
0.3890
R-B meter
SBU
0.9540
0.3450
0.2600
0.8920
1.0950
1.4000
1.4600
1.3650
1.2700
1.3050
159
-------
d
1.5 -
x-x
*
L
in
O
1
UJ
o
a
CD
i
>
=» .5 -
n
8 Pol.
* SBU.
a SpQC
* * *
o** *
* „ °°* @* ° *
n ** 9 & * o
a Q a n
. • °0 . • t" 8
* « S * ra 9 *
• 8 ' o » %•
*
0 0
*
o
#
o o
0 * *
@
o o
0 i n i
MARCH 85
APRIL 85
Figure 1. The half-hour integrated readings for the polysulfone
detectors, the R-B meter, and the speetroradiometer, for the months of March
and April 1985. The polysulfone readings have been multiplied by 3 and the
speetroradiometer by 50 so that all the points fall within one range.
160
-------
The polysulfone reading is in J/cm2 of equivalent monochromatic 305 nm
radiation and for this reason the first two columns in Table 1 are
different. The irradiance was first integrated over the UV-B wavelengths and
was then converted to J/cm2 by multiplying the final result by 1,800, i.e.,
the number of seconds in 1/2 hour. The R-B meter was integrating over 1/2
hour also.
The relationship between total irradiance for 1/2 hour and the
P°lysulfone detector readings was established by assuming a linear
relationship between the two. The equation y = A + B x was fitted with the
v^lue of coefficient A = 0. The value of the slope (B) was calculated from
the nne Joining the centroid of all the points to the origin (x = total
irradiance per 1/2 hour, y = polysulfone reading). The centroid was found to
De (0.206, 0.368). Thus the value of coefficient B was calculated to be B =
y/x = 1.78. Hence the relation between total irradiance per 1/2 hour and the
Polysulfone readings can be represented by: Polys, reading (1/2 hour) = 1.78
Total irrad.(1/2 hour) where both readings are given in J/cm2.
The relationship between total irradiance and the R-B meter was also
found in the same manner as above. The centroid was located at (0.206,
1-235), yielding a slope of B = 5.98. Thus:
R-B meter (SBU) = 5.98 * total Irrad.(1/2 hour) (J/cm2).
p°r the International Light instrument we obtained the following relationship:
0.145 * polysulfone (J/cra2> = Intern. Light (J/cm2).
Both detectors overestimate the actual UV-B; although both the
Polysulfone and the R-B meter detectors show a cosine response with the angle
°f incidence of the radiation on the detector surface, they do not
discriminate between the direct and diffuse components. On the other hand,
the spectroradiometer gives readings that are closely associated with the
direct component. Checking our results on the dependence of the solar UV-B on
the detector orientation with the horizontal, we find that the diffuse
component (90° reading) is approximately 50% of the total; therefore the
Pplysulfone correlation with the spectroradiometer is approximately correct.
^e R-B meter correlation is high; however, there is no effort made by the
Producers of this instrument to correlate the readings to the solar
insolation; their interest is to correlate it to the Minimum Erythema Dose.
Figure 2 presents the polysulfone measurements at solar maximum carried
out over a period of two and one-half years. Given this large volume of data,
t seemed natural to attempt to model the solar UV-B to predict, based on a
toodel, the solar UV-B insolation. When we considered Figure 2 it became clear
that the solar UV-B insolations follow a sinusoidal variation with time of the
year. The question then was whether we fit the average of each month or the
£utline of the curve? We decided to fit the outline of the curve from the
t°Pi i.e., we selected the points that represent readings taken on "clear
dayg/i Tne judgement "clear day" was made on our own observations together
with those of the Meteorological Department of the Civil Aviation Directorate
°f the State of Kuwait. We then selected the mathematical expression that we
*elt best represented the results and chose, as a start, to fit the daily
totals of solar UV-B. The following expression was chosen:
161
-------
6 -f
5
OJ
™ .4 --
E
LJ
uj .3
CO
a
on
I o
> . 2
ZD
. 1
V +
*
4-
V
*
V
^—i—H*—i—i—i—H—i—H—i—i—h
1983
1984
1985
Figure 2. UV-B Insolation Measured From 11:30 to 12:00 Noon With
Polysulfone Film Versus the Time of Year.
162
-------
Total UV-B (per day) = A + B sin (t),
Where t represents an angle that corresponds to the day of the year; A is the
°C level, i.e., the average over the year, total daily UV-B insolation; and B
is the AC amplitude, i.e., the amplitude of variation of the solar insolation
above and below the average. It is interesting to note at this point that A
multiplied by 365 gives us the total UV-B insolation for the year. The angle
t was chosen so that 0° corresponded to March 21 (the spring equinox), 90° to
June 21, 180° to September 21 and 270° to December 21. The angle was
calculated using the following expression:
t = 30 (M-1) + D - 81,
where M is the month of the year (January = 1, February = 2, etc.), and D is
the day of the month.
A graph of the total daily UV-B dose versus sin(t) shows how well the two
variables are correlated (see Figure 3). A good straight line fit to the
®xPerimental points follows. The regression analysis yields R^ = 0.983
(correlation coefficient R = 0.991). The equation predicting the amount of
daily UV-B insolation then becomes:
Total UV-B (per day) = 3.71 + 2.42 sin[2=30(M-1)+D=8l],
where M is the month of the year and D the day of the month.
a
2
^
I'
v 0
-z
-3
SIN ( 8 >
Figure 3. Total Daily UV-B Minus the Yearly Average Versus Sin(t),
Where t=0 for 3/21, t=90 for 6/21, etc.
Because the derived relation worked so well, we proceeded to fit the UV-B
as a function of the time of day (i.e., the diurnal variation). To
we needed to describe mathematically the daylight hours, i.e., the
interval (sunset-sunrise). This was calculated from data obtained from
163
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the Meteorological Department and was plotted against sin(t) where t is the
same angle as in the previous discussion. It was noticed that the midpoint
between sunrise and sunset on the average falls at 11.714 hour
Kuwait local time (11 hours, 42 minutes, 50.4 seconds). The variations in the
midpoint values are between 11.52 hour and 11.96 hour (Kuwait time), with
standard deviation = 0.191.
On the other hand, the maxima of the daily UV-B curves have an average
value of 11.81 hour (11 hours, 48 minutes, 28.8 seconds Kuwait time), the
standard deviation being 0.462. It is interesting to note that both the
midpoint of the sunrise-sunset interval and the UV-B maxima on the diurnal
measurements are behind 12 noon. The first falls 0.286 hour (17 minutes, 9-6
seconds) before noon and the second 0.192 hour (11 minutes, 31.2 secondsJ~~
before noon. For calculating the angle t, we decided to take 11.75 hours O1
hours, 45 minutes Kuwait local time) as the solar noon; that is to say that t
= 90° at 11.75 hours. This result is not surprising: Kuwait city lies ab
longitude 48°, i.e., 3° short of the hour meridians that occur every 15°. We
therefore should expect solar noon to occur 0.2 hours before Kuwait local
time, that is 11 hours 48 minutes. This result coincides with the one
obtained from the diurnal measurements.
•To fit the polysulfone-based UV-B measurements every 1/2 hour, we
selected the measurements made on reasonably clear days. These are like the
curves on Figure 4. We determined that the best mathematical expression to
give a reasonable fit to the data over the data collecting period was:
UV-B dose (1/2 hour) = C + D sin2 (q),
where C and D are arbitrary constants and q is an angle corresponding to the
time of day expressed as the ratio of the interval from sunrise to the hour in
question divided by the sunrise sunset interval times 180°.
The coefficient of determination R2, for most of the readings, was better
than 0.9. The average value of R = 0.91 for the days considered in thi*
sample leads to a correlation coefficient of 0.95 with a standard deviation of
0.094. The coefficient C should be equal to zero and the value calculated i3
-0.006 with a standard deviation of 0.0008, which is very small compared to
the UV-B doses. The value of coefficient D depends on the time of the year
and it should be equal to the value of maximum UV-B fialf-hourly dose for the
day.
We thus arrived at the following expression for the half-hourly dose °*
solar UV-B:
UV-B (per 1/2 hour) = (F * sin2[{l80/G}*{h-nn/60}-{2124/G-90}]) - 0.0063.
where
F = 0.3346 + 0.1898 *sin[30 *(M-1) + d-81];
G = 12.17 + 1.81 * sin[30*(M-1) + d-81];
h = hours (Kuwait local time);
m = minutes (Kuwait local time);
M = month of the year (Jan.=1, Feb.=2 etc.);
d = day of the month (1,2,3, etc.).
164
-------
0 08/05/85
+ 28/04/85
* 13/03/85
# 22/02/85
3 .23/01/85
8 U 14
TIME OF DAY ( Hrs. )
17
20
Figure 4. The Diurnal Variation of the Solar UV-B as Measured by the
Polysulfone Films
165
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Table 2. Comparison Between Calculated and Measured UV-B Insolation
Date
day-mo-yr
26.10.83
10.15
12.15
15.15
16.45
05.01.84
10.15
12.15
15.15
16.45
16.05.84
09.45
11.45
15.15
17.15
21.11.84
10.15
11.45
14.15
16.15
13.03.85
10.15
12.15
15.15
16.45
Time
hr-min
08.45 ...
0.191
0.248
0.045
0.00
...08.15 ...
0.085
0.109
0.023
0.00
...07.15 ...
0.327
0.439
0.173
0.020
...07.45 ...
0.144
0.148
0.092
0.00
08.15 ...
0.202
0.292
0.126
0.020
Measured UV-B Calculated UV-B
0.0963 0 OQ3
0.183
0.218
0.064
0.0003
0.020 0 030
0.115
0.141
0.030
0.00
0.081 .. . 0 120
0.385
0.482
0.228
0.036
0.023 . 0 018
0.134
0.165
0.088
0.003
0. 120 0 104
0.253
0.292
0.104
0.012
For any particular month, day, hour, or minute, the variables F and G
first calculated and their values are then introduced in the UV-B equati°°'
The above equation is not as complicated as it seems. It simply represent*
the product of the equations mentioned in the previous discussion, where the
term F gives the variation of the UV-B with the time of year, and G describe*
the variation of the sunrise-sunset time interval with the time of year. °
Table 2 we present a comparison of the calculated versus the measured v
of solar UV-B at 1/2-hour intervals. We have tested the validity of the
derived expression by calculating the deviation of the observed from
calculated values for two years. From this calcuation we obtained a <^r f
identical to the one for the variations of the ozone layer with the ti»e
year for our latitude.
166
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FINDINGS
§£gctral Sensitivities of Detectors
The relative spectral sensitivities of all the detectors considered in
study are presented in Figure 5 (Davis, Deane, and Diffey 1976; Berger
and Urbach 1982). It can be noticed that they are all different from that of
human skin — at least as far as erythema induction is concerned. Furthermore,
because of the shape of the curves and the fact that the spectral composition
°? the solar UV-B varies with the time of year, the relationships we developed
foi> interrelating the measurements of different detectors are fairly precise
°n*y for the months during which we measured them and for clear weather. We
have good reasons to expect that the atmospheric conditions at a given time
will cause unequal attenuation of the various UVB spectral components (Bener
1969).
of solar UV-B in Kuwait
Based on our measurements, an empirical equation has been developed that
can be used to predict fairly accurately the amount of solar UV-B in Kuwait,
"Or any day of the year and for any time during the specified day based on the
Polysulfone measurements. Thus, the answer that we obtain is the reading that
^6 would make if we exposed a polysulfone film for half an hour to the sun on
* clear day. Corrections for clouds, humidity, dust, etc. have not been
aeveloped as yet.
^ati
pnship of Detector Readings
, A relationship has been established between the polysulfone readings and
he R-B readings by correlating both of them to spectroradiometric readings.
relationship is: 3-36 x (polysulfone, J/cm2/0.5 hr.) = 1 SBU.
Furthermore the relationship between each of the polysulfone and R-B
eter and the total solar irradiance for 1/2 hour has also been established:
* Polys, reading (1/2 hour) = 1.78 x Total irrad. (1/2 hour)
' R-B reading (SBU) = 5.98 x Total Irrad. (1/2 hour) (J/cm2).
V-B Insulation
_ , The annual total UV-B insolation has been measured to be 1/42 x 10^ J/cm2
Or> 1.107 x 103 SBU.
Using these, we can estimate the conversion factor between polysulfone
Rj SBUs. By dividing, we obtain a factor of 2.9» which is close to the above
TVen value. Scotto, Rears, and Fraumenti (1982) have proposed the following
for estimating the annual solar UV-B insolation in SBUs as a function
1 latitude and altitude:
UV-B insolation (SBU) = (1/440) x [1,500,000 - 50,000 x
(L - 37.9) + 105 x (A - 1,5000)3 x (Cnts)
167
-------
270
280
290
300
310
320
330
WAVELENGTH ( nm )
Figure 5. Spectral Sensitivity of Human Skin, Polysulfone Film,
R-B Meter, I-L Meter (all curves are normalized to 1)
168
-------
This equation gives for Kuwait (29.5° latitude): 4.01 x 103 SBUs which is
Quite close to the measured value.
Jfobertson-Berger Meter Measurement Adjustment
The R-B meter was found to have a very large temperature coefficient and
therefore a very large correction has been made on the values obtained.
Berger and Urbach (1982) have reported R-B meter based data from Tallahassee,
Florida, and El Paso, Texas, which have latitudes very close to that of
Kuwait. The above equation (Scotto 1982) thus gives the following values:
• ELP (calc) = 4.02 x 103 SBU
• KWT (calc) = 4.01 x 103 SBU
' ELP = 4.889 x 103 SBU
• KWT = 4.107 x 103 SBU.
While the calculated values for the two cities are essentially identical,
we find a large difference in the measured values for ELP and KWT. If we
correct the KWT readings for temperature, normalizing to 43.5°C, we obtain KWT
(temp, adjusted) = 5.18 x 103 SBU, which is much closer to the ELP value
considering the rough correction. It is thus our contention that the
International data reported so far in climates where the maximum reading of an
exposed dry bulb thermometer reaches over 50°C are in significant error. The
R~B meter when used in warm climates needs to be modified to account for
temperature or not be used. The number of counts is smaller at elevated
temperatures than at normal temperatures.
CONCLUSION
In closing we summarize a useful relation. We have found that there
exists a simple relationship between the total daily UV-B measures and the
arn°unt measured between 11:30 and 12:00 noon. For polysulfone readings, if we
multiply the 11:30 to 12:00 reading by a factor of 10, we obtain a close
aPproximation to the daily dose. The maximum deviation is in the months of
June and July when the factor should be 12. For the R-B meter the
relationship is similar. For March 12 to September 21 the factor is 12 and
for September 21 to March 21 the factor should be 10. The answer is always
within 10#. It is thus possible, if one is short handed and is only
interested in rough estimates, to measure of the solar UV-B insolation from
11:30 to 12:00 and then to calculate the daily total.
ACKNOWLEDGMENT
This work was supported by the Environmental Protection Council of
Kuwait. We wish to express our thanks to Dr. M.M. Selim for his support and
encouragement and to Mr. Iqbal Sadik for his careful calculations.
REFERENCES
W., and W. Rehwald. (1983). Measurements of the annual variation of
the erythema dose of global radiation. Radiat Environ Biophys. 21:295-
303.
169
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Bener, P. 1969. Spectral intensity of natural ultraviolet radiation and its
dependence on various parameters. In The biologic effects of ultraviolet
radiation, ed. F. Urbach. Oxford, U.K.: Pergamon Press.
Berger, D.S., and F. Urbach. 1982. Climatology of sunburning ultraviolet
radiation. Photochem Photobiol. 35:187-92.
Blumthaler, M., W. Ambach, and H. Canaval. 1985a. Seasonal variation of
solar UV-radiation at a high mountain station. Photochem PhotobioA-
42:147-52.
Blumthaler, M., W. Rehwald, and W. Ambach. 1985. Seasonal variations of
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Chai, A.T., and A.E.S. Green. 1976. Ratio measurement of diffuse to direct
solar irradiances in the middle ultraviolet. App Opt. 15:1182-87.
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Davis, A., B.L. Diffey, and T. K. Tate. 1981. A personal dosimeter for
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Diffey, B.L., 0. Larko, and G. Swanbeck. 1982. UV-B doses received during
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Doda, D.D.,-and A.E.S. Green. 1980. Surface reflectance measurements in the
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Doda, D.D., and A.E.S. Green. 1981. Surface reflectance measurements in the
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Trancik, and M. V. Dahl. 1983. Reusable ultraviolet monitors: design*
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Garrison, L.M., L.E. Murray, D. D. Doda, and A.E.S. Green. 1978. Diffuse-
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Green, A.E.S. 1983. Ultraviolet ground reflectivities. Personal Communica-
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Green, A.E.S., K. R. Cross, and L. A. Smith. 1980. Improved analytic
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as, N,. and A. Eager. 1984. Measurement of solar middle ultraviolet
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R°senthal, F.S., M. Safran, and H.R. Taylor. 1985. The ocular dose of
ultraviolet radiation from sunlight exposure. Photochem Photobiol.
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Fraumenti Jr., Chapter 14, 254-76. Philadelphia: W. B. Saunders Co.
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171
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The Role of Native Pigment in Providing
Protection Against UV-B Damage in Humans
N- Kollias and A. Baqer
Department of Dermatology, Al-Sabak Hospital
Physical Department, Kuwait University
Kuwait
ABSTRACT
This paper assesses the average amount of pigment in a sample of the
Population of Kuwait and compares it with the sensitivity of the population to
ai"tificially produced UV-B, as well as monochromatic bands of UV-B, to arrive
an estimate of the protection afforded by the native pigment. The pigment
Of the population sampled was 2.18 on a scale from 0 to 9, while the
in an equivalent sample of northern Europeans would be 0.6-0.8. In
these measurements we estimate the pigment level (melanin concentration)
a?suming it resides in the epidermis. This implies that the concentration of
in in the local population is on the order of 3.5 times larger, while the
of light that enters the dermis after the above absorption is approxi-
20 times smaller. The correlation found between the pigment level and
minimum dose for a UVB- induced erythema was very weak, with an average
vaiue less than one half the value of a northern European sample. The
responses to monochromatic bands of UV-B indicate that the action spectrum of
°U1:> population is different from that reported by WHO (1982) for a standard
Population sample, especially at 295 nm.
We conclude that the pigment plays two roles in photoprotection. First,
lt absorbs light, and the suppression of the erythema effectiveness of the
^diation is proportional to the absorbance. Second, it modulates the amount
of UV-B that is delivered to the dermis and it appears that carcinogenesis is
Proportional to this intensity.
Numerous researchers have concluded that people who are more pigmented
less susceptible to UV-B (Urbach 1982; Pathak and Fitzpatrick 1974; Hawk
Parrish 1982). This implies that pigmented people are at a lower risk of
Veloping an erythema reaction and are also at a lower risk for tumor
Production. Human skin has been classified in six types according to the way
173
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it responds to sunlight (Pathak, Fitzpatrick, and Parrish 1982), i.e., always
burn easily-tan little or none, usually burn easily-tan minimally, &urn
moderately and average tan. Such classification is based on clinical history
and no mention is made of native pigment. We are looking for an objective
criterion that would allow assessment of the risk factor. Native pigment i3
an obvious candidate.
Amblard et al. (1982) show that native pigment and eye color exhibit a
good correlation with the erythema threshold level (minimal erythema dose,
MED). A recent study (Shono et al. 1985) suggests that there is a strong
correlation between native pigment and erythema reaction with a small
statistical sample.
In Kuwait we find the native pigment to be a weak indicator of a person s
anticipated response to UV-B. That is to say, given two persons of e
pigment level we can only predict their MED within a factor of two of
measured value — not a precise estimate. Native pigment is a parameter that s
perceived by the eye, i.e., using visible radiation. In general, it is not a
good practice to deduce the absorbance of any material in the ultraviolet
simply by recording its absorbance in the visible, unless, of course, one
identified the compound by its visible spectrum. The major absorber in
skin is melanin, which resides mainly in the epidermis in melanocytes an
keratinocy tes . It absorbs strongly in the visible and even more strongly |n
the ultraviolet (UV). The absorption by intact epidermis (Kaidbey et al-
1979) shows a linear relation with wavelength down to about 320 nm; for wave-
lengths shorter than 320 nm the absorbance increases rapidly. Over the UV-»
range the absorbance by the epidermis shows an increase by a factor of tw°
(approximately) .
A method has been developed for assessing the melanin concentration *
human skin (Kollias and Baqer 1985; 1986). We have used this method to assess
the pigment level in a small sample of the population of Kuwait. We fcne_.
tested the sensitivity of local skin to polychromatic and monochromatic -
radiation. Using the statistics available through the Kuwait Cancer
we assessed the UV-B risk and the role that native pigment plays in
erythemogenesis and carcinogenesis.
MATERIALS AND METHODS
Measurement of the Pigment Level of a Small Sample of the Population of,
Over the last two years, we have carried out measurements of skin pigmerl
on 314 volunteers. The measurement was non-invasive and only took 1.5 minut6
to complete. The probe that comes in contact with the skin was temperatuf
regulated to cause a minimum of discomfort to the individual volunteer; °ve.
250 of these were patients. The volunteers came from all walks of life
were randomly selected. The measurements on the patients were always taken
uninvolved areas of the skin. We did make measurements on involved areas
those were excluded from this study. We made certain that none of
volunteers were under any medication which could possibly have an effect °
their pigmentation. The healthy volunteers were the doctors, nurses*
technicians, and personnel of the Skin Department of Al-Sabah Hospital as v»e*
as some students from Kuwait University. All volunteers were informed of ™
nature of the experiment and their consent was obtained.
174
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Measurement of the Minimum Erythema Dose to Artificially Produced UV-B
Radiation of Human Skin
These measurements were conducted on 26 psoriatic patients over the
course of one year. These patients were about to begin treatment with UV-B
radiation, which constitutes a very effective line of treatment for
Psoriasis. Each patient was phototested to determine the minimum UV-B dose
necessary to elicit an erythema reaction. Before any radiation was applied,
we made sure that all the parameters were recorded and pigment index was
measured. The pigment level was evaluated on an area of normal skin. The
information obtained in these measurements was of interest to the physician in
Prescribing the indicated dose of UV-B for the treatment.
The patients were given doses of 50, 100, 150, and 200 mJ/cm2 on four
areas of the back, that were 2,5 cm in diameter. Patients with verv light
complexion were initially given doses of 20, 40, 60, and 80 mJ/cm . The
irradiated sites were observed 24 hours after irradiation and the minimum dose
required to elicit an erythema reaction was recorded. If no reaction
occurred, the test was repeated with four higher doses. If, on the other
hand, all areas showed erythema, then the test was repeated with four lower
doses. A Waldman Model S0001K upright UVB-UVA unit was used for the
Radiations. The patient received radiation In a standing position at a
Power of 0.4 mW/cnr so that the desired doses could be delivered within a few
ninutes at minimum discomfort to the patient. During the phototest the
Patients' face and body were covered by a protective robe which allowed only
the four areas on the back of the patient to be irradiated, When the dose
1«vel was reached for the first areas, the cubicle door was opened and that
area was covered. This procedure was repeated until all spots were covered.
The UV-B producing lamps in the apparatus were Sylvania 75/85W/UV21
fluorescent lamps.
All the tests and measurements carried out in this section were
supervised by Dr. V. Heigy of the Department of Dermatology of Al-Sabah
H°spital. All patients were informed of the nature of the tests and the
Masons for them; their consent was obtained before the measurements were
made.
of the Erythema Effectiveness of Three Selected. Wavelengths of
-
In this series of measurements we used 16 healthy volunteers who had skin
common to the area of Kuwait. The wavelengths used were 295, 305, and
315 ±5 nm. The irradiation sites were on the upper back of each individual
and we made sure that we stayed away from the middle of the back since the
Sickness of tissue under the skin as well as the blood supply differs from
the rest of the back. The volunteers were in a sitting position during the
test. At each wavelength six spots were irradiated starting with a dose that
Was considered to be suberythemogenic, progressing to higher doses at 20%
increments. Thus, the three wavelength tests generated three rows of spots 6
"^ in diameter on the back of each volunteer„ We further made sure that none
of the subjects had exposed their backs to the sun in the two to three months
itt>raed.iately before the test.
175
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The instrument used to carry out these irradiations was an Applied Photo-
physics "Clinical Photoirradiator" model UV-90, which is capable of providing
a monochromatic output in the UV-B wavelengths used in this study. The output
power of this instrument was 2.1 mW/cm2 at 295 nm, 2.4 mW/cm2 at 305 nm, and
2.8 mW/cm2 at 315 nm. The range of doses used was from 12 to 150 mJ/cnr at
295 nm, 33 to 270 mJ/cm2 at 305 nm, and 330 to 2700 mJ/cm2 at 315 nm. Because
of the high doses necessary to elicit an erythema reaction at the longest
wavelength the total time for the test to be completed was approximately 1-5
hours. This narrowed the number of people who were willing to volunteer.
Each volunteer had to return to the Phototherapy Unit of Al-Sabah
Hospital eight hours and 24 hours after irradiation to assess their skin
reaction. The bandpass of the irradiation was ±5 nm for all the
wavelengths. All the tests carried out in this section were supervised by Dr-
Yousef Malallah of the Department of Dermatology of Al-Sabah Hospital, wn°
worked very closely with the investigators during these measurements.
Skin Cancer Statistics
The skin cancer statistics were provided by the Kuwait Cancer Registry
and included data collected from hospitals where biopsies were obtained.
Cases of patients who sought treatment overseas do not appear in these
statistics.
RESULTS
Measurement of the Pigment Level of a Small Sample of the Population of Kuwait
The results of these measurements are displayed in Figure 1 . The mean 1s
2.18 ± 0.08 with a standard deviation of 1.40. It could be argued that this
is neither a random sample of the population nor a sufficiently large one-
These data are not presented as a true average but rather as an unbiased
indication of the pigment level of the population.
Measurement of the Minimum Erythema Dose to Artificially Produced J^§
Radiation of Human Skin
In the tests conducted we found erythemogenic doses to be from 50 to 35
mJ/cnr, while the pigmentation index varied from 0.5 to 5.2. The correlation
between the pigmentation index and the log of the minimum erythema dose f°r
all the volunteers is displayed in Figure 2. The correlation is not a strong
one; however, it is significant. The bandpass of the irradiation was ±5 °w
for all the wavelengths.
Although we feel that the above results are reliable, we by no means
to indicate that they are truly representative of what the MED of the K
population would be. Such a conclusion could only be arrived at through
much more thorough study in which we would need to include a well-represente
and large sample of the population of Kuwait.
176
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NO
72
64
56
48
40
32
24
16
8
0
'22.
'20.
'17.
'15.
'12.
10.
7.6
5.0
2.5
LIM:
en
—< C\J
to
m
in
•* m
iri CD
CM -i
• •
["x 00
Figure 1. Pigment Level Histogram for 314 Volunteers
u
I
6
5
4
3
2
\
•4- I
3.5
1-
4 4.5
Ln < NED )
5.5
Figure 2.
Correlation Between the Pigment Level and the Minimum
Erythema Dose for 28 Psoriatic Volunteer/Patients.
-------
Measurement of the Erythema Effectiveness of Three Selected Wavelengths^
of UV-B
The results of these tests are listed below:
/j
1) 295 nm 7 hr erythema 56 mJ/cm
In (MED) = 4.0 ± 0.2
24 hr erythema 56 mJ/cm2
In (MED) = 4.0 ± 0.2
2) 305 nm 7 hr erythema 82 mJ/cm2
In (MED) = 4.4 ± 0.1
24 hr erythema 100 mJ/cm2
In (MED) = 4.6 ± 0.1
3) 315 nm 7 hr erythema 820 mJ/cm2
In (MED) s 6.7 ± 0.1
24 hr erythema 1000 mJ/cm2
In (MED) = 6.9 ± 0.1
Skin Cancer Statistics
These statistics are presented in Table 1. They were supplied to us Wr
the Kuwait Cancer Registry and they include only cases that were biopsied *
the hospitals of Kuwait. The first numerical column indicates the fcota
number of citizens of the Arabian Gulf countries and the second column
the grand total. Of the 125 cases in the first reporting period, 94 were
exposed areas of the skin; this constitutes 75% of the total. Of the 78
in the second period, 58 were on exposed areas, also constituting 75%
total.
DISCUSSION
Skin Cancer
Skin cancer will occur with repeated suberythemogenic doses of UV-B (*
der Leun 1984); this is a situation that prevails with our population. ^ /•
data of the Kuwait Cancer Registry indicate that the most frequent form3
neoplasm are the basal cell carcinoma, with H3% of all cases reported
1974 and 1980, and squamous cell carcinoma with 42£. For Gulf
Council nationals, 48/t were squamous cell carcinomas and 37% basal
carcinomas. The remainder of the cases were of various types of skin
nancies (see Table 1). What we consider very interesting and alarming
skin cancer exists in this area even though people do not "burn," and that ' ^
of the neoplasms are on exposed areas of the skin. As the population e
Kuwait exposes only the hands and the face to the sun, a reasonable
of the exposed area of the skin of the population would be approxiwa
10J. Thus 75% of the neoplasms occur on 10fl of the skin. Therefore, ifc
reasonable to conclude that solar UV-B does contribute to the occurrence
skin cancer in the Kuwaiti population, as in other populations.
178
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Table 1. Data on Skin Cancer Provided to Us by the Kuwait
Cancer Registry
W.H.O. Diagnosis Index
Squamous cell carcinoma
"alignant lymphoma
sPindle cell melanoma
Mycosis fungoides
Basal cell carcinoma
pibrous histiocytoma, malignant
^ymphosarcoma
No microsc. confirm., Clinic, malig.
Depniatofibrosarcoma
Raposi's sarcoma
Pithelioma, malignant
^ignant lymphoma
weat gland adenocarcinoma
etastatic signet ring cell carcinoma
^sosquamous carcinoma
Other
74-78
Gulf Tot.
37
0
0
0
19
0
0
0
0
1
0
0
0
0
0
1
37
0
0
0
50
0
0
0
0
1
0
0
0
0
1
2
79-80
Gulf Tot.
11.
0.
1.
2.
18.
1.
1.
2.
1.
0.
0.
1.
1.
1.
1.
0.
15
.1
.1
.3
37
.1
.1
.5
.1
.4
.1
.1
.1
.1
.1
.0
Total 58 125 42.78
179
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Scotto, Fears, and Fraumenti (1982) report that the annual age-adjusted
rates of skin cancer in New Mexico are ten times higher for "Anglos" than f°r
"Hispanics." Therefore, we would expect a reduced rate for darker pigmented
persons. Furthermore, Scotto and Fraumenti (1982) report that the age-
adjusted rate for skin cancer for American whites was 232.6 per 100,000 while
for blacks it was 3.4 per 100,000. For all other cancers the rate for whites
was 318.9 and for blacks 347.3 per 100,000; in other words, the latter was not
as significantly different as the former. However, it has been found that
experimental animals "...kept in a heated environment rapidly developed more
UV-induced tumors than mice living in a temperate environment" and that
"...wind and increased humidity caused increased acute UV-induced damage and
acceleration of tumor formation." It is therefore likely that these
environmental factors could outweigh the natural protection that darker peopl6
have for UV-induced neoplasms. Kagetsu et al. (1985) report that UV-A-induced
erythema is definitely enhanced by increased skin surface temperature i°
humans. It is clear that more work needs to be done to evaluate the
additional risk by these climatic conditions (that is, heat and humidity) a3
well as the genetic protection, if any, associated with skin type.
Skin Parameters
The measurements on the "pigmentation index" showed a value of 2.1 8 *
0.08 for a population of 314 volunteers. This is not a large enough
statistical sample but it is large enough to provide us with an estimate of
where we are. Similar measurements do not exist for any other population yet
since the technique for carrying out these measurements was Just published i|J
January 1986 (Kollias and Baqer 1986). Based on current experience, we would
guess that the pigmentation index for English people would be approximately
0.8 ± 0.2.
If we assume that the remitted intensity from white Caucasian skin *s
approximately 20% of the incident intensity (Kollias and Baqer 1985), then
because the Beer Lambert law can be considered valid for intact
(Bruls et al. 1984) we have the following equation:
I / Ip = exp(-0.8 x A) = 0.20 for white skin and
I / IQ = exp(-2.2 x A) for Kuwaiti skin
where A is an arbitrary parameter representing the product of the thickness
the absorber and the factor that relates the pigmentation index with
absorption coefficient times the concentration. Solving the first
for A, we obtain A = 2.0. Substituting this value of A into the
equation, we obtain a remitted intensity approximately 1£ of the
intensity. This simple calculation implies that the intensity that arrives
the dermis of a white-skinned Caucasian is approximately 20 times larger
that of a typical inhabitant of Kuwait.
The validity of this calculation hinges on the validity of the assumpt10!!
that the remitted light is attenuated in the epidermis and that uV
absorbance by the epidermis is linearly related to the visible absorbance.
If the incident intensity is attenuated so strongly by the resident
ment in the epidermis, then we should be able to predict the dose at w
erythema will be induced by artificially produced UV-B in accordance with fch
180
-------
"Concentration of pigment. These measurements on 26 psoriatic patients do not
substantiate this assumption. In Figure 2 we see a gentle and general corre-
lation between the pigment level and the minimum erythema dose. [The reason
that it is plotted against the logarithm of the MED is because it has been
determined that the MED dose for a population does not form a normal distri-
bution while the logarithm of the MED does form a normal curve (Mackenzie
Amblard et al. 1982)].
It is known that patients tend to have a higher sensitivity to UV-B than
"ealthy volunteers. From these data we can conclude that the native pigment
does not offer a great deal of photoprotection against UV-induced erythema,
al though it obviously absorbs strongly the incident UV-B. The mechanism for
erythema production seems to be mediated through a photoproduct that is
Produced in the upper epidermis. We are currently experimenting in order to
establish a correlation between the native pigment and some measurable-
attenuating factor.
Because artificial sources tend to have a spectral output that is usually
Afferent from that of the sun, we tested for the sensitivity of human skin
(local) to selected wavelengths in the UV-B range. The wavelengths selected
Were 295, 305, 315 ± 5 nm. In these measurements no effort was made to
correlate the MED and the pigment level; rather phototests were carried out on
1& volunteers with pigment level similar to the average determined
Previously. The results obtained were compared with those of the photobiology
u*Ut of Dundee, Scotland (Mackenzie 1983).
The log (MED) ratio for 295 nm was 1.6 times larger for the Kuwait
^ubjects. The ratio for 305 nm was 1.1. The ratio for 315 nm was 0.99. It
f°Uows that the difference in the MED is maximum for the 295 band and is
the same for the other two bands. The waveband for which the MED's
is the largest is the one that is the weakest in the solar insolation.
"e can thus conclude that the erythemal effectiveness of monochromatic UV-B
wavelengths is similar at the long wavelength end of the populations of Kuwait
^d Scotland with the difference becoming maximum for the 295 nm.band.
Since the erythema effectiveness maximum factor of five is different at
the shortest wavelength [a factor of 1.6 for Log (MED)], it cannot possibly
account for the factor of one hundred difference for the carcinogenic effect
of> UV-B on deeply pigmented versus white individuals. These observations
Provide further evidence that the erythema effectiveness of UV-B wavelengths
la not necessarily the same as the effectiveness for carcinogenesis or for
Photokeratosis.
There is no doubt that the population of Kuwait is naturally protected
the intense rays of the sun more than Caucasian people. The question is,
ai%e they adequately protected from their severe UV-B environment? The absence
°f severe photodermatoses as well as the rarity with which one observes severe
^Unburns is adequate testimony to some protection. The skin of our population
*a more pigmented than that of northern Europe and the sensitivity of the
~°oal skin to artificially produced solar-simulated radiation is at least half
that of Caucasians (Y. Malallah, private communication). The results
Presented in the previous section relate to the log (dose) and consequently
they appear small. The actual energy dose is 12.5 mJ/cnr for Dundee and 54
181
-------
p
mJ/cnr for Kuwait for 295 nm to produce an erythema reaction. At 305 run and
at 315 nm the differences remain small even on a linear scale.
Skin cancer incidence according to the statistics that are available to
us is at the level of 2.6 per 100,000 for Kuwaiti males and 1.3 per 100,000
for Kuwaiti females for the 1979-81 period. It is interesting that the levels
in the previous reporting period were much lower, i.e., 1.1 per 100,000 for
Kuwaiti males and 1.0 per 100,000 for Kuwaiti females. This trend indicates
either a significant increase in skin cancer incidence or a significant
increase in the reporting of skin cancer cases to the Registry. Another
factor that is completely beyond the control of the experimenters and is
difficult to account for is the number of suspected skin cancer patients who
seek treatment overseas. These cases are missing from the local statistics
and could make the numbers smaller than they actually are. As the majority of
skin neoplasms appear in exposed areas it would not be surprising if a good
number of people seek plastic or reconstructive surgery elsewhere.
Our conclusion from these results is that melanin in the epidermis plays
two roles: one in the case of carcinogenesis, and another in the case of UV-
B-induced erythema. It appears that in the case of carcinogenesis, melanin
(the primary pigment in human skin) acts as an absorber, attenuating the
incident intensity. Thus, tumor initiation appears to be proportional to the
amount of UV-B that arrives to the basal cell layer. In the case of UV-B-
induced erythema the correlation between the concentration of melanin and the
MED dose is very weak, which implies that there must be some other mediator
for the production of erythema. The role of melanin in this case would
possibly be as a scavenger of free radicals generated by the UV-B radiation in
the epidermis. The radicals that are not compensated would then migrate into
the dermis through the basal cell layer and generate the erythema reaction.
Thus, the concentration of melanin will be a determining factor in the
erythema. In a paper that we are currently submitting .for publication we
discuss the different forms that melanin molecules can take up in the skin and
the different functions that these molecules might perform.
CONCLUSIONS
The estimated average'pigmentation index of the population of Kuwait is
2.2, while that of European Caucasians is estimated to be less than 1.0 and
assumed to be 0.8. The pigmentation index is a parameter that varies from 0
to 9 (there are darker people but we have not measured their pigmentation
yet), and is directly related to the absorbance of the epidermal melanin.
A weak relationship exists between the minimum erythema dose of UV-B and
the pigment level. Considering the average values of MED and pigment level we
are led to the conclusion that the relative protection that the pigment
renders is related to the absorbance or pigment level; i.e., as the pigment
level increases by a factor of 2+ the MED decreases by a factor of 2+. It is
unfortunate that for these preliminary results we had to use data obtained
from psoriasis patients as the data are probably slightly biased to a lower
MED value. MED values determined for normal Kuwaiti subjects would render
more definite answers.
Variation in the sensitivity of Kuwaiti skin and that of Caucasians is
demonstrated with smaller wavelengths of solar UV-B. At 295 nm, sensitivity
182
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varies by a factor of four while at longer wavelengths it is not very
different. This is similar to results described in Nakayama et al. (1974).
This means that to properly evaluate the UV-B risk, we need to establish the
spectral relative sensitivity (action spectrum) of Kuwaiti skin to UV-B. This
means that the Effective Spectral Irradiance is not the same as that of
Caucasian skin just attenuated by an appropriate factor. It is essential that
the action spectrum for UV-B wavelengths of Kuwaiti nationals and typical
expatriates be determined.
Analysis of the cancer statistics shows that skin cancer in the Kuwaiti
Population relates strongly with UV-B exposure. It should be noted that 75%
of the skin neoplasms reported between 1974 and 1980 occurred on exposed areas
°f the skin, i.e., on 10£ of the skin. This is an unmistakable and alarming
signal. Statistical evaluation of the results is not complete because we are
in the process of obtaining more information from the Kuwait Cancer Registry.
ACKNOWLEDGMENTS
This work was supported by the Environmental Protection Council of
Kuwait. We wish to thank Dr. M. M. Selim for his support and trust. We also
express our thanks to Dr. Y. Malallah and Dr. V. Heigy for their valuable
cooperation.
REFERENCES
P., J. Beani, R. Gautron, J. Reymond, and B. Doyon. 1982. Statistical
study of individual variations in sunburn sensitivity in 303 volunteers
without photodermatosis. Arch. Dermatol. Res. 274:195-206.
Bruls, w.A.C., and J. C. van der Leun. 1984. Forwarding scattering properties
of human epidermal layers. Photochem. Photobiol. 10:231-42.
Hawk, J.L.M., and J.A. Parrish. 1982. Responses of normal skin to ultraviolet
radiation. In The science of photomedicine. eds. J.D. Reagan and J.A.
Parrish, 219-260. New York: Plenum Press.
K*getsu N., R.W. Gange, and J.A. Parrish. 1985. UVA-induced erythema, pigmen-
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K*idbey, K.H., P. Poh Agin, R. M. Sayre, and A.M. Kligman. 1979. Photopro-
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melanin in vivo. J. Invest. Dermatol. 85:38-42.
Koilias, N., and A. Baqer. 1986. The assessment of melanin in human skin in
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, L.A. 1983. The analysis of the ultraviolet radiation doses to
produce erythemal responses in normal skin. Brit. J. Dermatol. 108:1-9.
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Nakayama, Y., F. Morikawa, M. Fukuda, M. Hamano, K. Toda, and M. Pathak. 1974.
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and man, cons. ed. T.B. Fitzpatrick, eds. M.A. Pathak, L.C. Harber, M.
Seiji, and A. Kukita, 591-611. Tokyo: University of Tokyo Press.
Pathak, M.A., and T.B. Fitzpatrick. 1974. The role of natural photoprotective
agents in human skin. In Sunlight and man, cons. ed. T. B. Fitzpatrick,
eds. M.A. Pathak, L.C. Harber, M. Seiji, and A. Kukita, 725-50. Tokyo:
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approaches to protection of human skin against harmful effects of solar
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Fraumenti Jr., 254-276. Philadelphia: W. B. Saunders Co.
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Ozone Modification: Importance for
Developing Countries in the Tropical/
Equatorial Region
Mohammad llyas
University of Science of Malaysia
Penang, Malaysia
The adverse biological and environmental effects due to any inadvertent
ozone modification have received considerable scientific attention but have
been largely concerned with ultraviolet radiation damage to human skin in
specific relation to protection of deficient white skin. In this respect, the
ozone problem somehow has not appeared to be of serious interest to the people
of developing countries living in the tropical/equatorial geographical belt.
However, in view of the manifold increase in the ultraviolet radiation
received at the lower latitudes compared to the mid and high latitudes, it
seems reasonable that the ozone layer issue should be of serious interest in
the tropics. In fact, in these regions, more serious kinds of solar UV radia-
tion-induced health effects such as cataracts, viral infections, and immune
system damage may be connected to the "ozone-UV" issue. These aspects need to
be studied under harsher tropical conditions, but the understanding that has
been achieved so far (for mid-latitude conditions) can provide a valuable base
from which the specific situation for tropical countries can be tackled as an
extension.
INTRODUCTION
For several decades, atmospheric ozone, especially the stratospheric
layer, has been known for its important protective role against the incoming
solar ultraviolet radiation. In general, there is a natural balance between
the ozone's production and its destruction with a net ozone surplus. Under
the natural equilibrium, there are small dosages of solar ultraviolet radia-
tion to which populations, living organisms, plants, and aquatic systems have
generally become adapted. The harmful effects are thus generally very small
except perhaps in the tropical/equatorial region. The surface dosage of
natural ultraviolet radiation' increases by many folds in going from high/mid
latitudes to the equator. Because people living in the high dosage tropical
belt have a darker skin tan which provides greater protection to the skin
against ultraviolet radiation, this high UV radiation situation has not been.
185
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considered particularly seriously in terms of adverse health and environmental
effects that might occur in these regions.
The ozone layer suddenly came into scientific prominence about 12 years
ago when it was realized that certain human activities may lead to significant
ozone depletion from the naturally balanced level, thereby increasing the
surface dosage of ultraviolet radiation leading to increased skin cancer and
many other adverse biological, environmental, and climatic effects. Since any
such ozone destruction would spread out globally, the net UV radiation effect
would be most serious in the equatorial and tropical belt when already the
ozone column thickness is minimum and ultraviolet radiation penetration is
maximum. But perhaps even a more fundamental issue is to ascertain whether
the already high UV radiation dosages received at the lower latitudes are
contributing to tropical diseases and medical problems. Whether the 5 to 10
times higher dosages (in absolute terms) that would be received in the low
latitude region in comparison to the higher latitudes (if a certain- fraction
of ozone column is reduced) would bring the radiation level above a certain
threshold is another aspect relevant to the tropics. In other words, the
"ozone modification" issue is of serious importance to the low latitude
countries. The whole issue of ozone layer protection is thus indeed of global
dimension. Yet, there is very little apparent involvement of scientists from
the developing countries in the "ozone layer-ultraviolet radiation" work.
While financial constraints may account for some of this non-involvement, lack
of proper understanding of the effects at the public, scientific, and
political levels is also a serious factor. Nevertheless, in the coming years,
it should be appropriate to examine the "ozone layer-UV-B" matter in the
specific context of tropical countries.
TYPICAL CONDITIONS
In order to examine the relevance of the ozone layer issue for the
developing countries in the equatorial/tropical region, it would be helpful to
summarize the atmospheric ozone and solar ultraviolet radiation influx
globally. The seasonal distribution of vertical ozone column for different
latitudes is shown in Figure 1. It is clear that at the lower latitudes, not
only the ozone column thickness is significantly small but it also does not
vary much seasonally. The solar ultraviolet radiation penetration is thus
maximum at the lower latitudes throughout the year. The overall effect of the
low ozone content coupled with smaller seasonal change in the solar declina-
tion results in the latitudinal distribution of annual erythemal dosage
(incoming radiation weighted according to skin erythemal action spectrum) as
shown in Figure 2. This diagram illustrates the manifold increase in the
damaging UV-B dosage from high latitudes to the equator. Some towns are also
marked on the curve against their respective latitudes. Figure 2 is based on
calculated data for clear sky conditions (Mattingly 1976; Ilyas 1979).
THE EQUATORIAL DATA FROM PENANG
In the equatorial/tropical region, there is a general lack of observa-
tional data pertaining to the atmospheric ozone and solar UV radiation. Wit"
this consideration in mind, about 10 years ago we initiated a comprehensive
program of measurements involving ozone soundings, erythemal UV-B, UV-A, total
solar radiation, surface ozone, and a series of relevant meteorological para-
meters at our equatorial place, Penang (5.5°N). This is perhaps one of the
186
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u
050
045
040
035
030
0 25
020
30'N
J L.
eo'N
7Q'H
60'N
50'N
40'N
Jan Feb Mar Apr. May Ju^e Ju\v Aug Sept Oct Hov Dec
Figure 1. Annual Variation of Total Ozone for Each 10° of N Latitude
200
8
I
W
*-i
S
100
5.0
90
A Oslo
t I
Adelaide
Los Angeles
Washington
70
50 30
Latitude
10
Figure 2. Variation of erythemal dosage (joules/cm2) with latitude for
clear days. Also indicated are the dosages for specified places as compared
to an equatorial location (Malaysia).
187
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most rare comprehensive programs in the equatorial/tropical belt. Some of the
initial results from this study have become available and more refined data
should follow (Ilyas 1984a, 1984b; Ilyas and Barton 1983).
One of our immediate interests from this study is to see if the observa-
tional data obtained at Penang can be used in a general way for the
equatorial/lower tropical region. For this, the most important and directly
usable data in the context of ozone layer effects study are the directly
involved ultraviolet radiation data. The input radiation flux does not change
much over the entire equatorial/lower tropical belt. It would, however, be
modified differently at different places depending upon the sky conditions
(cloud cover). The long-term cloud cover data at Penang indicate the cloud
cover to be close to 85% (Ilyas et al. 1981) which reduces the incoming UV-B
radiation to about half. This is consistent with the theoretical relationship
of cloud cover effect on ultraviolet radiation (Johnson et al. 1976). In a
more comprehensive study of cloud cover effect, we used 5-year-long observed
UV-A data (Ilyas et al. 1986), together with the calculated data for clear sky
conditions (Johnson et al. 1976). The observed data were found to be in
excellent agreement with the computed data modified for the average cloud
cover (Ilyas 1986). This is shown in Figure 3.
The excellent agreement between observational data and calculated data
indicates that the cloud cover effect for other locations may be easily
incorporated into the clear sky calculations of ultraviolet radiation. The
radiation conditions for evaluating the adverse biological/medical and
environmental effects can thus be ascertained. In any case, because of the
relatively high cloud cover conditions at Penang (5°N), the observed UV flux
represents a lower limit of UV dosage that would be received anywhere in the
entire equatorial belt. A summary of the erythemal UV-B dosage together with
some meteorological conditions at Penang is presented in Figure 4. The
information in Figures 3 and 4 thus represents lower tropical model conditions
which must be simulated for the photobiological effect studies for this
region.
UV RADIATION EFFECTS IN THE TROPICAL REGION
Figures 1-4 provide a good summary of low ozone content and high ultra-
violet flux conditions prevailing at the lower latitudes against the high
ozone content and low ultraviolet flux at mid and high latitudes. Besides,
the high (air) temperatures and humidities in the tropics prevail throughout
the year and may couple together with the UV radiation in producing more
severe biological and physiological effects. Lack of education and awareness
of UV-induced damages, skin's false sense of protection, increased outdoor
occupations including young school children being exposed to relatively large
amounts of ultraviolet radiation (under hot and humid conditions) due t°
inadequate clothing and/or outdoor work (like P.E. lessons and games) at wrong
times of the day may all add up to the seriousness of the situation.
Unfortunately, there is not much basic data available let alone studies of
adverse radiation effects under specific conditions. Although skin cancer and
other related problems, hitherto the prime concern in Western populations, way
not be of sufficient importance in the tropics, more serious effects on humans
such as viral infections (herpes, hepatitis), eye damage (cataracts), dainag6
to the immune system, and life expectancy (perhaps we don't record many skin
cancer cases in the tropical countries because most of such people don't live
188
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N 5 JA p MA MY J JY A § 0 N D JA~F M
Figure 3. Annual variation of the average daily total erythemal dosage
(ED) (instrument response) as measured at Penang together with the clear
weather dosage (calculated) and the related observational climatic parameters
for the station and the solar position [minimum (noon time) zenith angle].
189
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CVI
_*:
30
o>
c
o
B
T3
2-5
20
1-5
1-0
Radiation for Clear Weather (Calculated)
Radiation for Average Weather
(Calculated)
Radiation at Surface (Measured)
J L
' ' ' L
N
MAM
JL
0 N
Figure 4. A comparison of the calculated UV-A dosages outside the
atmosphere and at the surface (after accounting for cloud .cover effect) with
the measured data at our station (Penang).
long enough for the effects to show up) are important avenues for future
work. Also, what adverse effects the very high dosages may have on tropical
plants and aquatic organisms and the exposed materials would also need to be
studied. Finally, whether any further increase in UV radiation, as a result
of ozone reduction due to human activities, would affect any threshold limit—
to which the tropical systems may have become adapted—would be important to
examine. Side by side, populations would need to be educated on these effects
and some simple protection methods, whereas scientists in these regions should
be increasingly involved in this program with the realization of local rele-
vance and overall importance. The exercise of protecting humans globally by
protecting the ozone layer would then become a very involved matter. An
organization such as UNEP is well suited to make a move in this direction.
ACKNOWLEDGMENTS
A UNEP Fellowship which enabled my participation in the conference is
gratefully acknowledged. I benefited greatly from my discussions with many
persons at the meeting which has helped in preparing this paper.
190
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REFERENCES
Ilyas, M. 1979. Sains Malaysiana. 8:13.
Ilyas, M. 1984a. In Atmosph. Ozone (D. Reidel: Dordrecht), 274.
Ilyas, M. 1984b. In Atmosph. Ozone (D. Reidel: Dordrecht), 791.
Hyas, M. 1986. Paper under preparation.
Hyas, M., and I.J. Barton. 1983. Atmosph. Env. 17:2069.
Hyas, M., C.Y. Pang, and A.W. Chan. 1981. Sing. J. Trop. Goeg. 2:27.
Hyas, M., D.A. Aziz, and M.R. Tajuddin. 1986. Paper under preparation.
Johnson, F.S., T. Mo, and A.E.S. Green. 1976. Photochem. Photobiol. 23:179.
Mattingly, S.R. 1976. Atomsph. Env. 10:935.
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The Tan of Ultraviolet-6 Summer
Dr. Petar Jovanovic
Omladinskih Brigada
Beograd, Yugoslavia
During my studies of the environmental parameters of ozone depletion, one
idea often comes to mind: What is going to happen with the surface of our
planet? As this approach was too prosaic for this solar and galactic beauty
of which we are all proud, I transformed the question into a more poetic
one: What is going to happen to its tan? I hope you will agree that the
criteria that evolve from this approach are more appropriate because of the
abundant chemical make-up of our planet and the ultraviolet tanning the planet
is starting to acquire in the new "anthropogeochemical" era.
I beg your pardon for this novelistic digression and let me approach the
problem as we usually do—more prosaically.
I agree with Watson, Hansen, Hoffman, and others that we have barely
scratched the surface of the problem and that many unanswered questions have
to be approached. I also agree that we possess enough knowledge to qualify
the risk. The differences in quantifications all fall within a range that
guarantees danger. The nature of the processes, including phenomena of momen-
tum and inertia, makes it possible to conclude that we are in the incubation
phase of the disease. The "infection" is here, the process is irreversible,
the disaster is imminent. The problem is how to cope with it.
I think that we can cope with the disease of the planet. The guarantee
is in the fact that there is no disagreement in qualification of the changes
in anthropogeochemistry. I could not avoid the implications of the facts with
which we are confronted. These facts suggest one general title that can be
given to all particular parameters of this environmental and climate complex
discussed in all papers: "disastrous chemical summer." All our estimates of
warming, ice melting, flooding, rising sea levels, inundation, epidemics,
ultraviolet aids, deaths, droughts and hunger, temperature rising, etc.
suggest this integrating qualitative statement: chemical summer with all its
anthropogeophysical and anthropogeobiological events. Whether it is going to
be called ultraviolet summer, chemical summer, ozone summer is a question of
193
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convention. It seems to me that whether cool or hot, it still can be called
burning ultraviolet summer. We all know that ultraviolet radiation is
burning, although invisible and without heat.
This excellent example of a man-made hazard that can trigger natural
hazards of incomparable energy and destructive force should remind us that the
disastrous chemical summer can be as disastrous as "nuclear winter." The
nuclear season can be prevented by avoiding nuclear warfare. But the summer
produced by the greenhouse effect and ozone depletion surely has already
begun. The ozone shield has already been transformed into a less protective
curtain.
Cosmonauts tell me that they often admire this beautiful shield of life
on earth. They look at it and through it as if they are looking through a
protective window. Let us help them to always look through this protective
window and not through the holes in it. Otherwise, instead of us they will
see only burns and scratches on the face of what was once the galactic beauty
Mother Earth.
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AQUATIC SYSTEMS
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Effects of Enhanced UV-B Radiation on the
Survival of Micro-Organisms
Donat-P. Hader
Fachbereich Biologie-Botanik (Lahnberge)
Phillips-Universitat Marburg
Karlsruhe, Federal Republic of Germany
Microorganisms play an important role in both aquatic and terrestrial
ecosystems on our planet since they represent the basic level in a complicated
food chain on which the lives of heterotrophic organisms such as animals
depend. In addition, plants rely heavily on the activity of microorganisms
such as the fixation of atmospheric nitrogen, which is also an important
economical factor.
Many microorganisms utilize external signals for orientation and behavior
in their microenvironment to find a suitable niche for survival and growth of
a population. Not only is light the single most important factor for orien-
tation in photosynthetic organisms, which naturally depend on the availability
of light for energy fixation, but it is also critical for non-photosynthetic
microorganisms.
Microorganisms have developed a number of different strategies to orient
with respect to light including phototaxis, which is a directed movement
towards or away from a source of light; photokinesis, which describes the
dependence of the speed of movement on the intensity of light; and photophobia
responses, which are elicited by sudden changes in the light intensity
(Nultsch 1975). All these mechanisms of orientation are utilized by a
population to find a suitable environment and to adapt to the continuously
changing conditions (Nelson and Castenholz 1982).
A number of taxonomically different microorganisms have been found to be
extremely sensitive towards solar UV-B radiation (Damkaer et al. 1980; Ohnishi
et al. 1982; Jagger 1983). These organisms, which range from prokaryotes to
eukaryotes, from gliding to flaggelated forms, and from photosynthetic to non-
photosynthetic organisms, are under UV-B stress even at current levels and
would be seriously endangered by an increase in the UV-B radiation caused by a
partial reduction of the ozone layer due to anthropogenic gaseous pollutants
such as chlorofluorocarbons (Maugh 1984; Weiss et al. 1985).
197
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In addition to immediate lethal effects on the organisms, several
responses to UV-B radiation can be distinguished, all of which eventually
destroy a population of microorganisms. The most obvious effect observed is
an inhibition of motility, which prevents a population from escaping from
hazardous influences in its environment. A more indirect effect is the inhi-
bition of photoorientation, which occurs at even lower UV-B doses. As a
consequence, the organisms are still able to move but are unable to respond to
changes in their environment and are eventually killed by the unfavorable
conditions in their environment. A discussion of these problems with a few
examples follows.
Filamentous cyanobacteria live in aquatic (marine and freshwater)
habitats as well as in soil and other terrestrial ecosystems and produce a
large fraction of the organic material (Fay 1983). The organisms glide using
a mechanism not yet fully understood. When exposed to low doses of UV-B
irradiation, the populations are killed within a few days after exposure. The
analysis of the behavior using an artificial UV-B source showed that both
motility and photoorientation are drastically impaired (Hader 1985a).
Investigations at an experimental station near Lisboa, Portugal, demon-
strated that the organisms do not survive long in solar radiation. Neither
the visible component of the radiation nor the temperature increase caused the
organism in the experiment to die but rather the UV-B component in the solar
radiation killed them (Hader et al., in press). When exposed to unfiltered
solar radiation at noon during the summer, the filamentous Phormidium was
found to stop moving within 35 minutes. An action spectrum measured in the
Large Spectrograph in Okazaki, Japan, indicated that wavelengths below 300 nm
were extremely effective (Hader et al., in press). It could be shown that
the UV-B target is not DMA since no photorepair could be induced after UV
damage (Eker 1983; Yamamoto et al. 1983). A mechanism involving photodynamic
effects could also be excluded by studying the effects of diagnostic reagents
(Ito 1978; Spikes and Straight 1981; Nultsch and Hader 1984). The conclusion
of these experiments was that an intrinsic component of the motor apparatus of
the organisms, probably a membrane-bound protein, is the molecular target of
UV-B radiation.
Cyanobacteria use a primitive, but rather effective mechanism to orient
themselves with respect to their photoenvironment (Hader 1979). Each time a
filament leaves a bright area by gliding into a shadow, it reverses direction
and returns to the bright area. This so-called "photophobia response
guarantees that the population stays in the light, which is essential for a
photosynthetic organism. Light fields that are too bright are avoided bY
phobic responses upon entering the bright area. The remarkable precision °*
orientation can be demonstrated by a simple experiment in which a photograph!0
negative is projected into a homogeneous suspension of organisms, which then
accumulate in areas of suitable light intensities and form a sharp and
detailed positive image (Hader 1984).
Most cyanobacteria are typical low light organisms: When they are
exposed to high light intensities, their photosynthetic pigments are photo-
oxidized and the cells die within a few days (Walsby 1968). The consequence
is that populations of cyanobacteria are not only endangered by increased UV-°
radiation, which affects motility and directly kills the organisms, but also
by lower UV-B doses, which impair photoorientation of the organisms. As a
198
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result they either move into the substratum, where they die due to the lack of
light or they can no longer prevent themselves from being exposed to
excessively bright light, which bleaches and eventually kills the cells as
well.
Only a few organisms have developed mechanisms to escape UV-B radiation
while most organisms are insensitive toward the UV-B. The archaebacterium
Halobacterium uses different sets of photoreceptors to accumulate in favorable
light fields and to escape from hazardous radiation (Wagner 198*0. Upon an
increase in the short wavelength radiation, the blue/UV receptor mediates the
repellent signal and triggers an instantaneous reversal of movement.
The cellular slime mold Dictyostelium is also extremely sensitive toward
UV-B radiation because its development and motility are impaired by very low
doses (Hader 1983a, b). In its multicellular stage, this organism uses a. lens
effect to detect the direction of laterally incident light. Because the
refractive index of the cytoplasm is higher than that of the surrounding air
Parallel, light is focused to the rear flank of the organisms (Hader and
Burkart, 1983). The resulting light gradient is used for photoorientat'ion
towards the light. In the UV-B range, the lens effect is cancelled by a
strongly absorbing substance so that the optical properties are reversed and
the organisms move away from the UV-B source (Hader 1985c).
Flagellates, such as the green uniflagellar Euglena gracilis, find their
suitable environment by two antagonistic orientation mechanisms: At low light
intensities, the cells move toward the light source (positive phototaxis) and
at high intensities away from the light source (negative phototaxis). In
their natural environment, the cells swim upward until they reach the optimal
light intensity, where they form a dense population.
Hader(1985b) found that solar UV-B affects swimming in these organisms.
No motile cell was found in samples exposed to solar radiation for 2.5 hours
around noontime. The cells did not recover from the damage. Even when the
Population was transferred to darkness or weak light after a short UV-B
irradiation, most of the cells died in the subsequent hours indicating a
damaging effect even of low UV-B doses.
Photoorientation was measured by an automatic computer-controlled video
analysis (Hader and Lebert 1985). The video image of the cells swimming under
the microscope was digitized in real time and stored in an electronic
Memory. A microcomputer had access to the memory and was programmed to detect
and follow individual organisms. The deviation of the organisms from the
incident light direction was calculated and stored for subsequent statistical
treatment and histogram analysis. Under appropriate culture conditions
Euglena moves with a high precision of orientation. After artificial or solar
UV-B irradiation, the swimming tracks become increasingly erratic and the
organisms move in random directions independent of the light direction.
Both effects of solar UV-B radiation on the flagellate Euglena are
disastrous for the survival of the population. When motility, photo-
orientation, or both are impaired, the organisms are no longer able to select
a suitable habitat. Even when we allow for a considerable attenuation of the
UV-B radiation by the column of water above the cells, solar UV-B has to be
as a natural stress factor even at current levels. Any increase in
199
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the UV-B doses would increase the stress, and would eventually threaten the
survival of these and other ecologically important microorganisms.
ACKNOWLEDGMENTS
This work was supported by the Bundesminister fur Forschung und
Technologie (KBF 57). The author gratefully acknowledges the skillful
technical assistance of U. Neis.
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Weiss, R.F., J.L. Bullister, R.H. Gammon, and M.J. Warner. 1985. Atmospheric
chlorofluoromethanes in the deep equatorial Atlantic. Nature 314:608-10.
Yamamoto, K., M. Satake, H. Shinagawa, and Y. Fujiwara. 1983. Amelioration
of the ultraviolet sensitivity of an Escherichia coli recA mutant in the
dark by photoreactivating enzyme. Mol. Gen. Genet. 190:511-15.
201
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Is the Impact of UV-B Radiation on
Marine Zooplankton of Any Significance?
Bruce E. Thomson
Hatfield Marine Science Center
Oregon State University
Newport, Oregon USA
ABSTRACT
Over the past decade several studies have examined the effects of UV-B
Radiation on a number of major marine 2ooplankton groups. While the adult
organisms are commonly found in the upper meters of the ocean, the eggs and
larval forms may be concentrated in the surface micro-layer. It has generally
been noted that larval forms of an organism are more susceptible to damage by
UV-B than later life stages. The species that have been studied are critical
components of bioenergetic pathways that lead to larger animals that are of
•nutritional and commercial value to man. The studies indicate that present-
ly levels of UV-B radiation significantly affect the developmental life
stages of these organisms. For some species a ]Q% decrease in atmospheric
°zone could lead to as much as an 1855 increase in the number of abnormal
larvae.
ATMOSPHERIC OZONE EVOLUTION
It is generally accepted that the earth's primeval atmosphere resulted
from the outgassing of volatiles from the interior of the planet. The atmos-
phere was devoid of oxygen and consisted primarily of methane, carbon dioxide,
^onia, and hydrogen sulfide. The absence of an effective filter allowed
short wavelength UV from the sun to penetrate the surface of the earth. While
solar ultraviolet radiation can be viewed as a major constraint on the evolu-
tion of life, at the same time it may have been a vital force in the formation
of biological macromolecules. It is thought that associations of macro-
Molecules at some depth in the could utilize the diminished solar energy
Caching to that depth. These precursors to what we now call phytoplankton
^fe the principal source of oxygen to the early atmosphere. Berkner and
^rshall (1965) have implicated the development of atmospheric oxygen, and
therefore, ozone as an important contributing factor to explosive evolutionary
dvances in the fossil record. Two thresholds of oxygen concentration have
n postulated. These correspond to two periods in the fo'ssil record, one in
Cambrian and another in the Silurian.
203
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THE IMPACT OF UV RADIATION OH MARINE ZOOPLANKTON
The first investigations into the effect of the ultraviolet radiation
component of sunlight on aquatic organisms were conducted as early as 1925
(Huntsman). By 1930 several studies using a variety of marine organisms
indicated there was a detrimental impact of the ultraviolet portion of sun-
light (Klugh 1929, 1930; Harvey 1930). These early pioneering studies serve
as benchmarks and are of historical interest, but have little relevance to the
current ozone issue because of the lack of instrumentation to precisely and
absolutely measure the quantity and quality of the radiation. It was not
until 1970 that instrumentation for precise UV irradiance measurements became
available .
Worrest (1982) has reviewed the literature relating to the impact of UV-B
radiation upon marine organisms. This report updates that information, adds
to its scope, and provides some comparisons between results from a variety of
experimental methods. The data presented will clarify that ultraviolet radia-
tion does have an impact on this portion of the biosphere. The extent of this
impact is a function of primarily three variables:
• The species being exposed to UV
• The developmental life stage of the species
• The dose of radiation the organism receives.
The data presented in Table 1 is compiled from a number of investigations
over the last decade by various authors using different experimental tech-
niques and criteria for assessing the impact of UV-B radiation. Because
standardized techniques were not used in collecting the data, some conversions
of the data have been made for the sake of comparison. Nomographs (Damkaer*
and Dey 1982) have been used in an attempt to account for differences in ^
exposures among authors using different methods of exposure. In spite of
these approximations there are some general statements that can be made and i°
fact some remarkable parallels among the different sets of data:
• First, the younger the developmental stage of the organism at the time
of exposure the more sensitive the organism is to the harmful
of UV-B. This is demonstrated by looking at the total dose req
for an early larval stage to exhibit a significant effect
comparing it with the total dose required by a later larval stage °f
that species.
• Next, organisms appear to have differing sensitivities to UV-B. Thi?
can be seen by comparing the response of different groups ot
zooplankton at analogous stages of development.
The third point is that the rate at which the total dose is
is a factor in the extent of impact. In looking at the copepod data a
doubling of the dose rate roughly halves the time for the end point t°
be reached.
204
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Finally, the data in Table 1 show that the impact of UV-B on marine
zooplankton larvae is significant at present levels. For comparison
purposes the dose rate and total dose for oyster larvae are about what
we would expect to measure on a clear sunny day at 45N latitude in
late June or early July.
Table 1. Estimated Biologically Effective UV-B Doses Leading
to Significant Effects in Major Marine Zooplankton Groups
(Biological weighting referenced to action spectrum
normalized to 300 nm.)
Zooplankton Group Dose Rate
DNA(SOO) W/m2
— —
I.
11.
III.
IV.
V.
Shrimp/Euphausiid larvae
Euphausiid adult
Copepod larvae
Copepod postlarvae
Copepod adult
Crab larvae
Crab postlarvae
Anchovy/Mackerel larvae
Oyster /Mussel larvae
6.00 E-2
9.90 E-2
3.39 E-1
1.59 E-1
3.39 E-1
9.90 E-2
2.79 E-1
6.00 E-2
1.20 E-1
Total DMA Dose
kJ/M2/d
2.55 E3
6.115 E3
1.35 E3
2.70 E3
3.00 E3
6.45 E3
6.00 E4
2.50 E4
2.16 E3
Time for
Effect
4 days
6 days
1.0 hr
4.5 hr
2.5 hr
6 days
20 days
12 days
5.0 hr
Source: Data from: Damkaer et al. 1980, 1981; Hunter, Kaupp, and Taylor
1982; Karanas, Worrest, and Van Dyke 1979, 1981; Thomson et al.
unpublished.
The most recent data in Table 1 come from studies conducted in our lab.
Individuals from four species of bivalve molluscs (Crassostrea gigas.
saxidomaa gjganteus, Mytilus edulis, and Clinocardium nuttallii) were spawned
separately. Fertilized eggs were exposed to UV-B radiation for periods
ranging from 1 to 6 hours. The eggs were then held for 24 to 72 hours at
fhich time they were examined for abnormal development. This examination was
done at the end of the trochophore stage; the onset of the straight-hinged
larvae stage. The response of the four species is shown in Figure 1. A third
Degree polynomial curve was fitted through the means of several hundred data
Points. The shape of the curve is typical of survival curves in that there
*r& two inflection points. Beyond a threshold value there is an increase in
the rate of abnormal larvae as the UV dose increases. At the upper end of the
°urve, beyond a second threshold, the impact levels off.
205
-------
Using these data as a basis, we calculated the increase in abnormal
larval development as a function of decreases in atmospheric ozone (Figure
2). The calculations were referenced to ambient daily doses that would occur
during the spawning peak of these species. For species such as the bay mussel
and oyster a 15% decrease in ozone thickness can lead to nearly a 30$ increase
in the number of abnormal larvae. The impact of UV-B may be greater on some
species while species such as the cockle and butter clam may be less sensi-
tive. Using the butter clam as an example, a 15% reduction in atmospheric
ozone could lead to a 15% decrease in the harvest. In comparison, a 1% change
in the harvest from a commercial salmon hatchery can be the difference between
negative cash flow and economic viability.
FUTURE AGENDA
Phytoplankton serve as a major conduit through which the sun's energy
flows into marine life; small plants floating at or near the ocean's surface
or at depths not exceeding the euphotic zone depth. A portion of this energy
is transferred to the zooplankton that graze in this "breadbasket of the
sea." As predator becomes prey, the sun's energy is transferred to the next
strand in a web that can ultimately lead to man. The impact of UV-B radiation
on this transfer of energy through a food web needs to be examined. Two
levels of impact are possible; direct impact on the predator organisms or it3
larval stages and indirect effects as a result of the availability of prey-
Organisms surviving increased levels of UV-B may do so at a biochemical cos
that alters the value of that species as a food item. Preliminary investiga-
tion of this question has begun. Initial results indicate that, predator*
organisms grow at different rates when fed different species of phyt°*
plankton. In addition it appears that biological molecules in otherwis6
"healthy" phytoplankton are altered by exposure to UV-B.
Documentation of the effects of UV-B on marine zooplankton shoul
continue with increased attention to the need for uniformity in methodologi^
among investigators. This would permit greater accuracy in comparing result
and predicting effects. The effort to investigate species that are critica
components of food webs needs to be increased. Detection of
alterations in some key species would constitute a refinement in our
to assess the impact of UV-B. Without this additional information, ^
prediction of the effect of decreased atmospheric ozone on the roar*11
ecosystem is difficult.
ACKNOWLEDGMENT
. L|g
Part of the research described in this paper has been funded by c
United States Environmental Protection Agency through cooperative agreem®0
CR810288 and CR812688 with Oregon State University. However, it has not jj«Jg
subjected to the Agency's required peer and policy review and therefore do
not necessarily reflect the views of the Agency and no official endorse^6
should be inferred.
206
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s:
o:
o
m
h-
LLI
o
oc
UJ
a.
100-r
80-•
DNA WEIGHTED (Eff kJ/m2/d)
Figure 1. Bivalve Larvae Following UV-B Exposure. Fertilized eggs from
*°ur species of bivalves molluscs were exposed to various levels of UV-B for 1
to 6 hours. The eggs were then held through the larval trochophore stage (24-
72 hr.) and were examined for abnormal development at the onset of
straight-hinged stage. Data points represent the means of four
(Unpublished data, Thomson, Worrest, and Robinson)
the
replicates
207
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g.. • BAY MUSSEL
ui
W
o
a.
to
UJ
DC
UJ
G!
a:
1.4-
1.3-. * COCKLE
1.2--
1.1"
o OYSTER
DBUTTER CLAM
10
PERCENT OZONE REDUCTION
15
Figure 2. Abnormal Bivalve Larval Development. The response of the f°ur
individual species of bivalve larvae to increased levels of UV-B waS
calculated using the response of that species at standard ozone thickne$s
(0.32 cm-atm) as the reference. The reference levels of UV-B bracketed
spawning season for these species.
208
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REFERENCES
Berkner, L.V-., and L.C. Marshall. 1965. On the origin and rise of oxgen
concentration in the earth's atmosphere. J. Atmos. Sci. 22:225-261.
Damkaer, D.M., D.B. Dey, G.A. Heron and E.f. Prentice. 1980. Effects of UV-B
radiation on near-surface zooplankton of Puget Sound. Oecologia
(Berl.). 44:149-158.
Damkaer, D.M., D.B. Dey, and G.A. Heron. 1981. Dose/dose-rate response of
shrip larvae to UV-B radiation. Pecologia (Berl.) 48:178-182.
Damkaer, D.M., and D.B. Dey. 1982. Momograms for biologically effective
UV. In The role of solar ultraviolet radiation in marine ecosystems, ed.
J. Calkins, 205-211. New York: Plenum.
Harvey, J.M. 1930. The action of light on Calanus finmarchicus (Gunner) as
determined by its effect on the heart rate. Contrib Can Biol. 5:85-92.
Hunter, J.R., S.E Kaupp, and J.H Taylor. 1982. Assessment of the effects of
UV radiation on marine fish larvae. In The role of solar ultraviolet
radiation in marine ecoysystems, ed. J. Calkins,459-497.NewYork:
Plenum.
Huntsman, A.G. 1925. Limiting factors for marine animals I. The lethal
effect of sunlight. Contrib. Can. Biol. 2:83-88.
Karanas, J.J., R.C. Worrest, and H. Van Dyke. 1979. Mid-ultraviolet (UV-B)
sensitivity of Acartia clausii (Copepoda). Limnol. Oceanogr. 24:1104-
1116.
Karanas, J.J., R.C. Worrest, and H. Van Dyke. Impact of UV-B radiation (290-
320 nm) on the fecundity of Acartia clausii (Copepoda). Mar. Biol.
65:125-133.
Klugh, A.B. 1929. The effect of the ultraviolet component of sunlight on
certain marine organisms. Can. J. Res. 1:100-109.
R.C. 1982. Review of literature concerning the impact of UV-B
radiation upon marine organisms. In The role of solar ultraviolet
radiation in marine ecosystems, ed. J. Calkins, 419-457. New York:
Plenum.
209
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An Estimate of the Role of Current Levels of
Solar Ultraviolet Radiation in Aquatic Ecosystems
John Calkins and Mary Blakefield
University of Kentucky
Lexington, Kentucky USA
ABSTRACT
Organisms that use sunlight are exposed to solar UV-B radiation.
Ultraviolet radiation in the UV-B band, 280-320 nm, can produce lethal or
toutagenic lesions in DNA and RNA. Successful species must be able to cope
^ith the UV-B exposure; the measures that render solar UV-B tolerable are not
°ften recognized. Solar UV-B exposure may be mitigated by three pathways:
Avoidance of-exposure, shielding, and repair of DNA lesions after injury. It
ls well known that: (a) many forms of biological activity occur in the early
Corning or late evening, avoiding the midday when UV-B is most intense; (b)
animals heavily exposed to sunlight tend to be shielded by intense
Pigmentation, while cave or ocean-bottom species are often pale or colorless;
*nd (c) there are multiple DNA repair systems that can repair solar UV-B
lnJury, one of which (photoreactivation) has no known function aside from the
Ability to repair the type of lesions induced by sunlight. Because the
Actions that minimize solar UV-B injury (avoidance, shielding, and repair)
exPend resources that might be used for other purposes, the best adapted
8Pecies would have no more capacity to cope with solar UV than is actually
£equired. Observations of a number of aquatic organisms suggest their
£°lerance of solar UV-B is remarkably close to their present exposure. When
Tolerance and current exposure are essentially equal, then a significant
lnerease in solar UV would be expected to have an adverse effect on many
r8anisms and be especially damaging to species that are threatened by other
environmental factors.
^RODUCTIOM
Almost all the living organisms familiar to human experience seem to
in the sunlight; so it is counter to our intuition that the sun's rays
be a lethal agent which, if increased, might produce ecological disaster
s sensitive species. In spite of the general impression, studies show that
°-Ur ultraviolet radiation is a potent biological agent-that shapes the form
211
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and behavior of most living organisms in such subtle ways that even biological
scientists seldom consider.
Humans are among the largest animals, and the limited penetration of UV
into tissue might be expected to provide complete and automatic protection
from solar UV damage. But this is not the case, and solar UV radiation is as
clear a threat to humans as it is to other species. Humans protect themselves
from solar UV injury in the same general ways used by other living
organisms: avoidance, internal shielding, and repair. People avoid the most
intense sunlight (siestas) and reduce it by clothing (sombreros, parasols,
sunbonnets, etc). Intense constitutive pigmentation is widespread among
humans indigenous to the tropics. Protective tanning of skin is clearly a
response to solar UV damage (Giese 1976). It has been recently discovered
that individuals lacking DMA repair capacity (suffering from the disease
xeroderma pigmentosum) may live if protected from sunlight but suffer early
severe cancer if chronically exposed to solar UV (Cleaver 1968). While these
forms of protection from solar UV are obvious and well-known, they have often
been subject to misinterpretation. It was once thought that people with black
skin were protected from the heating effect of sunlight when obviously white,
not black, skin would reduce solar heating. If such a large organism as a
human requires redundant protection from solar UV, then it is obvious that
small organisms may be at extreme risk from solar UV exposure. While the
interior of a human is well-protected, all the cells of small animals or
plants are exposed. Small animals and especially unicellular organisms, which
are more common in aquatic ecosystems, may lack the sensing capacity and the
rapid and properly directed mobility required to avoid solar UV; they also may
not have sufficient body size to permit an effective internal sunscreen.
While these arguments suggest that solar UV may be a major environmental
hazard, more direct evidence is required to determine the particular
relationship of solar UV and aquatic ecosystems. The oceans and natural-
waters cover three quarters of the earth's surface; human life and welfare ^s
intimately bound to the earth's waters and the organisms that live in the
seas. A significant part of the human food supply is harvested from the
water, a harvest especially rich in protein and generally deficient in plant*
derived foods. Clean healthy waters also provide an increasing role in huma0
sports, pleasure, and recreation.
The most likely consequence of stratospheric ozone depletion would be.,
worldwide increase of solar UV, increasing the present effects of UV on &*
natural waters. Thus, the possibility that increased UV from the sun cou i
have important consequences on marine life and the multitude of
activities depending on it deserves careful analysis. The aquatic biota,
organisms living in the oceans and fresh waters, seem to be particular-^
vulnerable to general changes in ozone because all waters would be affect6"*
Furthermore, aquatic organisms are not subject to direct human
Humans can provide shielding or compensation through strain or
selection, which might minimize injury in the case of crops, domestic
and human exposure; but the options would not be available to aqua?iy
ecosystems. Even if harmful effects were so small as to be individual J
undetectable, such as a 5% decrease in the harvest of a certain fish» 5
worldwide accumulation of such low level effects could represent a sefi°
loss of resources.
212
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The objective of the research reported here is to assess currently-
available data and develop analytical methods that will permit the prediction
°f the potential effects of ozone depletion on aquatic ecosystems or will
suggest the methods and additional data needed to make such predictions.
PATTERNS OF ORGANIZATION OF AQUATIC ECOSYSTEMS
Photosynthesis, the conversion of radiant energy from the sun into chemi-
cal energy (food) is the basis of essentially all life on earth. Photo-
synthesis by land plants ordinarily proceeds in large multicellular structures
(higher plants) at a fixed location and with many specialized tissues and
structures that obtain and transport nutrients and water, conduct photo-
synthesis, ensure reproduction, and protect the plant from various kinds of
Physical, chemical, and biological stresses.
Aquatic plant life is organized along entirely different patterns (see
Russell-Hunter 1970). Photosynthesis is also the source of the energy used by
the aquatic biota; but the primary photosynthetic plants are quite different
from land plants in body form, reproductive patterns, behaviour, and almost
all basic structures. Photosynthesis requires light; but adequate sunlight
seldom penetrates to the bottom of natural waters. Thus, aquatic
Photosynthesis is largely confined to a relatively thin layer at the water
surface termed the euphotic zone, the surface layer where plants create more
°hemical energy by photosynthesis than they use for their own metabolism.
The essential nutrients required by plants in aquatic systems are
Bailable only in very low concentration; thus, smaller plants have an advan-
tage as they have a large surface to volume ratio, making them efficient in
capturing these essential but diluted nutrients from the water. In fact,
aQuatic photosynthesis is primarily conducted by single-celled organisms, many
species being very small (Russell-Hunter 1970). Microscopic organisms are
unable to swim or otherwise move about in the water even against currents of
low velocity, and thus are carried with the bulk movements of the waters in
which they are suspended. Those suspended organisms carried about with the
water are termed plankton ("drifters"). Planktonic organisms capable of
Photosynthesis are termed phytoplankton, while those organisms that live by
eating (grazing on) phytoplankton or other floating organisms are termed
SSQplankton. Organisms that swim strongly (nekton) are not included with the
Plankton; however, the embryonic forms of many aquatic higher animals are
Planktonic. As feeding progresses from the phytoplankton through the
2°oplankton to fish and other higher organisms (the food web), the chemical
energy generated by aquatic photosynthesis becomes more and more concentrated
into organisms of larger size, reaching organisms suitable for harvesting for
human use.
RADIATION
Wavelengths from 200 to 280 nm are termed UV-C > and are the most
Biologically injurious solar UV component when incident on living organisms.
fortunately, UV-C is strongly absorbed by the ozone (0,) molecules present in
the stratosphere, the outer layer of the atmosphere beginning ten to fifteen
kilometers (six to nine miles) above the earth's surface (note Figure 1). The
strong absorption of UV-C by various atmospheric components (primarily ozone)
that biologically active levels of solar UV-C do'not reach the earth's
213
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Photosyntheticolly active radiation
\<-SoIar outside atmosphere
UV VISIBLE NEAR INFRARED FAR INFRARED
i i i
100 300 600 900 1200 1800
WAVELENGTH (nm)
2400 3000
Figure la. Solar radiation
atmospheric absorption and
passage through the atmo
There is a general absorption
much stronger absorption by a
spheric gases (03, C02, HgO,
particular wavelength
Adapted from Giese 1976.
L25
Solar radiation
outside the atmosphere
0.0
220 240 280 320 360 400 440
WAVELENGTH (nm)
Figure 1b. A comparison
UV intensity (adapted
and Schippnik 1982) and
effectiveness (Setlow
function of wavelength. s
the biological action, which *
pendent on the product
tiveness and intensity, -
from the crossing tails ° *
rapidly falling functions a
most significant in the
wavelength band.
-------
Radiation of wavelengths from 320 to 400 nm are termed UV-A. The
atmosphere is transparent for UV-A; and this band of radiation from the sun
reaches the earth's surface with high intensity; UV-A produces little adverse
biological effect. Species easily damaged by UV-A or visible light do not
dwell in the sunlight. However, some animals sensitive to UV-A can be found
as nocturnal organisms, in caves, or deep in the oceans where sunlight is
absent.
Between the UV-C and the UV-A lies the narrow UV-B band of radiation
extending from 280 to 320 nm. Small but significant amounts of UV-B are
Present in sunlight reaching the oceans; and it has a high potential for
injury to most living organisms found at the earth's surface. Atmospheric
absorption of short wavelength solar UV does not end sharply at 280 nm nor
does UV damage begin abruptly at 320 nm. Figure 1 illustrates that the UV-B
encompasses a transition zone where solar radiation intensity rapidly falls
and the capacity to injure or kill living organisms rises as the wavelength
shortens below 320 nm.
The strength of the absorption of various spectral components of electro-
""agnetic radiation in both the atmosphere and in natural waters is often
expressed by an absorption coefficient (K). The intensity of radiation inci-
dent on the absorber (I ) is reduced to a value I by passage through a thick-
ness of absorber (Z). It is usually found that the relationship between I,
Io» and Z can be expressed by
I = I0e-KZ Eq. 1
tne absorption coefficient (K) will depend on the nature of the material
traversed (air, ozone, clear ocean water, or turbid fresh water) and the wave-
length of the particular radiation.
Sunlight is generally absorbed in natural waters, heating the sunlit zone
the lower water remains cold. Because water becomes less dense as it
Marms, sunlight generates a stable, low density warm layer overlying cold,
water. The boundary between the warm and cold layers is termed the
and is of great importance in aquatic biology. Wind-generated
frequently mix the waters above the thermocline producing a mixed
, but the mixing does not ordinarily penetrate into the dense layer below
thermocline. Because solar energy both generates the thermocline and pro-
s the photosynthetic light for the aquatic plants, it is often found that
euphotic zone essentially coincides with the mixed layer. In small water
cooling the water surface at night produces dense water over the
less dense mixed layer and the entire water body can be remixed. In
water bodies, the thermocline can remain from spring until cold winter
cools the mixed layer to the temperature of the water below; then deep
will occur and replenish the nutrients, which probably would have been
p6Pleted by the photosynthesis in the euphotic zone. A common pattern in
water bodies is that deep mixing occurs in the fall or winter as noted
and also in the spring when the cold (0°-4°C), low density surface water
warmed to the temperature of underlying water and the density barrier to
disappears.
215
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CONCEPTUAL MODELS
In the absence of definitive knowledge of how a particular human, activity
will affect the global environment, it seems reasonable to strive to maintain
the present condition. However, technologies or activities that become so
widespread as to perceptively modify the environment must provide substantial
benefits. Some method must be developed to weigh the benefits from the
environmentally perturbing activity against the benefits of the status quo-
The focus of this paper will be on methods to evaluate the harm that might
occur in aquatic exosystems if UV-B were increased. The benefits that may &e
derived from the technologies that reduce stratospheric ozone and thus
increase UV-B are not considered.
There are several ways to quantify the ecological damage from a chemical
or agent. In some cases, historical data can be analyzed to evaluate the
injury or loss of resources due to the agent. Another widely-used technique
is to construct a microcosm, a small scale model of the ecosystem, that can &e
subjected to the expected levels of the agent. Although there is a strong
latitudinal dependence of UV-B intensity, it is not clear how this or any
other historical data can be applied to aquatic systems to estimate the impact
of increased UV-B. Microcosm research holds some promise, but it is difficul
to establish how well the microcosm simulates the natural ecosystem especially
for results requiring long (weeks or months) exposures or organisms needing
large range to thrive. A third approach is to measure selected
parameters, and, by appropriate modeling, deduce some of the
consequences of various UV-B exposures.
The essence of the analysis is the capacity to quantify the risks
defined changes in solar UV-B. Considering that aquatic ecosystems are
side human control and the relevant data presently available are so limited as
to be almost negligible, quantitation would seem to be an impossible task. *
the subsequent sections of this paper, approaches are defined that may provi a
quantitation for limited but important areas of the problem. Quantitation °*
effect is achieved by developing models that produce responses from relevan
and measurable variables; in this case the primary variable is the
intensity and its changes. In general, the models presented are
simplifications of actual conditions but are necessary to clarify the
of the problems.
Lethality Models: Organism Level
The most clearly-defined response to UV-B exposure in aquatic
is lethality, and it is particularly easy to quantify the predom
components of the plankton. Certain acute lethality is the most
effect that UV-B could exert on a living organism. Methods for assay1"*
radiation-induced lethality are well developed. Although dose-respon®
relationships for lethality can assume many forms, the combination'
illustrated in Figure 2 cover the various responses observed in irradiat fl
organisms. Figures 2A and 2B show a threshold type response. Up to,he
critical (threshold) dose, little or no lethality would be expected; above *j*
threshold a small increment of dose produces a large response. The resp°n e
.
illustrated in Figures 2C, 2D, and 2E show the "classical single hit"
often observed in irradiated microorganisms. Single hit response can
expressed mathematically as
216
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S = S0e-D/Do Eq. 2
where S is the number of survivors measured after exposure to dose D, S is
the number of survivors measured with o dose and D is a constant expressing
the sensitivity of the particular species. Single nit response begins at the
lowest doses and implies that some types of single event ("hit") produces
lethality; the larger the dose, the larger the probability the organisms will
receive a lethal "hit." If a species shows the single hit type response, then
even small exposures (and current levels of UV-B) produce some lethality; and
*t is easy to compute the increased lethality result from increased incident
UV-B.
dS = j_ e'D/D0 Eq. 3
dD D0
Substituting S/S = e"D/Do ifc is evident that the incremental survival per
unit dose dS/dD is proportional to the product of 1/DQ and the survival ratio
o*
The threshold model suggests that a species may suffer no lethality from
given levels of UV-B because exposures fall below the threshold level. For
threshold responses, it is important to know the relationship between the
threshold dose and current UV-B radiation levels. If the threshold dose is
above the exposure, then the organism survives current exposure, and the dif-
ference represents a reserve of tolerance that permits a limited increase of
UV-B exposure without any increased lethality (the good news). However, the
bad news is that if the threshold is exceeded, then a small increment in the
dose may produce a large probability of lethality (note Figures 2a and 2b).
It is possible to simulate solar UV-B or use real sunlight to determine
UV-B dose-response curves. It is also possible to estimate the typical solar
UV-B exposures that individuals will receive in natural waters; from such
estimates the incremental killing of organisms showing "single hit" response
and the reserve tolerance of threshold type responding species can be com-
Puted.
Ijgthalitv Models; Population Level
If data on individuals can be obtained, then the response of individuals
should be applied to populations to define the expected ecosystem response. A
traditional modeling scheme (illustrated in Figure 3) might use the Lotka-
Voltera approach. We may assume a three-species ecosystem having: a primary
Producer, which might be a bacteria (or photosynthetic algae, etc.); an omni-
vore or primary herbivore, represented by a protozoan (but could be rotifer,
arthropod, etc.); and a secondary carnivore flatworm (arthropods or fish,
etc.). This model ecosystem can achieve a stable population distribution. If
We assume, for illustration, that only the middle member of the food web would
be subject to an abrupt increase of solar UV-B damage, then its population
Would be depressed but there would also be a population-restoring tendency
because the food supply would increase and the predation would (after a time
*ag) decrease. Considering the complexities of even this simplified model and
the vast difference between it and an actual aquatic food web, it is very
UlUikely that this form of modeling will provide useful or believable con-
tusions for evaluation of solar UV-B effects.
217
-------
100
50
I 20
CO
246
UV dose (SU)
8
Figure 2a. Survival of the
Chlamydomonas exposed to
solar UV-B and real
(modified from McKnight e
Nachtwey 1975). Doses v r
measured using the Robertson-^6 * t
meter; the good response
for the two very
wavelength distributions
the Robertson-Berger
weighting distribution
satisfactory for this
Note the sharp threshold;
in
is
°rga"
very
islB.
survive without measurable *••* ^
up to 5 SU but when this l&*
to 5 SU but when this
exceeded mortality is very
Figure 2b. The killing °r
competent yeast (N) and two
defective strains (A, B) l
light (from Resnick 1970)- fS
that substan tial killing °c°
a matter of minutes and that
defective strains show "sin&
killing, while the wild typ«
shows the threshold type
306090 120
UVdott (min)
218
-------
10
a:
-01
0.01
Figure 2c. The killing of E. coli
by natural sunlight (Lukeish 1946).
0 20 40 60
UV dose (min)
too
10
I
i .«
to -01
.001
.0001
Figure 2d. The killing of coliform
bacteria by sunlight in a waste-
water lagoon system (Calkins et al.
1976).
Z 345
UV dose (SU)
Figure 2e. The killing of three
marine diatoms collected from the
waters off Iceland by simulated
solar UV-B (modified from Calkins
and Thordardottir 1980).
254 9
UV dost (SU)
219
-------
Bacteria Bacteria feeder
Primary carnivore
Tetrahymena
Secondary carnivore
Flatworm
Equilibrium condition
WV*
Assume UV destruction
of Tetrahymena (tran-
sient condition]
o
r*
O
10
8
6
4
2
Tendency to restoration
of Tetrahymena popula-
tion (transient condi-
tion
Equilibrium with
reduced sensUlvt
population
Figure 3. A Schematic Representation of Equilibrium-Type Modeling of
Three-Component Ecosystem With and Without UVB.
220
-------
An even simpler model provides some definitive and surprising
conclusions. While the level of depression of a particular population by a
newly introduced agent such as UV-B seems beyond computation, it is possible
to determine the maximum level of an injurious agent (UV-B) that a particular
species can tolerate. If the daily UV-B incident (given optimum growth
conditions and with all other sources of lethality such as predation
eliminated) produces lethality that exceeds the capacity of the subject
Population to replace the killed component, then population will, under
prolonged treatment, be depleted to extinction (Figure 4; Calkins 1974). In
actual ecosystems, optimum growth conditions are seldom found and most aquatic
species are food for some predators; however, if a population cannot survive
with the most favorable conditions, then it clearly could not survive in the
feal ecosystem. In the laboratory, it is possible to determine the parameters
for the maximum tolerable dose (the replacement limiting dose, RLD): the
optimum growth rate, the growth delaying effect of radiation, and the dose
response for lethality. When the RLD is compared to the actual exposure in
nature, one obtains an estimate of the reserve of tolerance a species may have
for increased solar UV-B.
EXPOSURE MODELS
There are a number of ways of establishing the UV-B levels incident at
the water, which we consider below. Because natural waters are semitrans-
Parent for UV-B wavelengths, Equation 1 can be used to determine UV-B
intensity at any particular depth and thus, knowing the UV-B intensity at the
surface and the depth of the organism, the instantaneous exposure can be
computed (See Figure 5). In some cases, aquatic organisms hold fixed
Positions such as at the bottom of a shallow pond or stream. However, a fixed
vertical position is rare and some definitive knowledge of position is
required.
Planktonic organisms in many cases are moved with the water mass in which
they live. When there is effective wind-driven mixing of the layer above the
thermocline, a common condition, then the organism receives the average
exposure (Iav) in the mixed layer, i.e.,
- -KZ)
KZ
Source: Horowitz 1950 Equation Eq. 4
where z is the depth of the mixed layer and the other symbols have the same
significance as in Equation 1 (See Figure 5b).
PRIMARY PRODUCTIVITY MODEL
Solar UV directly reduces the rate of photosynthesis in plants. The
sPectral distribution of this inhibitory effect is quite different from the
lethal effect. Because long wavelengths of UV and even visible light inhibit
Photosynthesis, ozone reduction producing a small increase in UV-B would
aPpear to have a negligible effect on the primary photosynthesis in aquatic
aystems (Lorenzen 1979; Smith et al. 1980).
221
-------
Consider only one species.
Assume;
1. Maximum growth rate
of population
2. 1 acute exposure
each 24 hours
3. No other loss of
population
4. Population does not
modify Us behavior
(9
C£
O
u.
o
at
ui
CO
8-
6-
4
2
10
8-
Day 1
Day N
Required Information:
1. Dose-response for
killing (non-repro-
duction)
2. Maximum growth rate
3. Dose-response for
growth delay
Day N +1
Figure 4. The Replacement-Limiting Model
222
-------
I—x-
X PUERTO RICO
DLAKE SUPERIOR
ODELAWARE ATLANTIC
A LAKE EftlE
• LAKE I IRRINGTDN . KT.
Figure 5a. The attenuation of
UV-B as measured by the
Robertson-Berger meter in some
representative natural waters.
949
DEPTH (METERS)
u
Figure 5b. The average UV-B
dose to the euphotio zone at
various locations off Iceland
as a function of the pro-
ductivity of the waters. It
is assumed that 10 SU per day
are incident at the water
surface.
J_
_L
_J
25
5 10 l»
AVERAGE PRODUCTIVITY MflC/m3/HR
20
223
-------
There are indirect ways by which the increase of UV-B might produce a
larger effect than predicted from the direct photoinhibition of photosyn-
pthesis. Killing phytoplankton should show the DNA type action spectrum and
thus reduce photosynthesis in a way similar to other lethality. However, the
effect of lethality on photosynthesis would require much longer times t°
develop than is required for measurement of direct photoinhibition. ^
lethality contributes to the loss of photosynthesis capacity, it must be
modeled by more complex models. There are very few data on UV-B killing alga®
and also little information as to the vertical location at various times of
day. Considering the relatively large attenuation of UV-B in the tnore
productive waters (coastal and upwelling zones), it would appear that the
phytoplankton are well protected from UV-B.
Another approach has been proposed. Although photosynthetic productivity
measurements are usually made with samples held at fixed depths for a half or%
a whole day, mixing is common in natural waters. In the well-mixed situation^
all the photoplankton receive the same amount of light per day and the same
UV-B exposure. A "ferris wheel" model has been proposed (Calkins et al. 1982)
where algae enter the circulation (by rising) and are transported (by Langmui^
cells, etc.) along the surface where they accumulate a UV-B exposure that
produces a sinking (increased density) stimulus that removes the algae fr0in
the circulation into the stable water at or below the thermocline (Figure
6). The postulated cycle would ensure that the phytoplankton species received
the maximum possible photosynthetic light without exceeding its UV-B limits-
If UV-B exposure is not random, but is controlled by the organism, then an
increased incident UV-B will reduce the time the organism remains in the mixed
layer. The loss of photosynthetic light due to UV-B increase will be directly
related to the ratio of absorption coefficient of UV-B and photosynthetic
light in the mixed layer (Calkins 1982), quantities that are
measurable.
BIOLOGICAL DOSIMETRY
The solar UV-B is the principal parameter of all the analytical models-
This might seem to be an easily determined quantity but, referring back ^
Figure 1, it should be noted that the biological effectiveness of UV-B energy
drops by a factor of 1000 or more as the wavelength changes from 290 to *
nm. Clearly, it is impossible to simply measure UV-B intensity w
distinguishing between components that differ 1000-fold in biol
action. Ideally, UV-B dose should be measured in very small wavelength 0
and then each multiplied by an appropriate biological weighting factor j; -
obtain the instantaneous intensity (Figure 7). The product of the intensity
times the time of its application for the entire exposure should be added c
give the biologically weighted dose. This is a difficult procedure requir*™;
a high resolution spectroradiometer and definitive knowledge of the pr°Pe
weighting factor which may not be known for the organism under study.
measure
The physical devices used for measuring solar UV intensity u|u ^d
re the quantity termed irradiance (power per unit area in Watts/m ) * „.
the summation or time integral of this quantity is termed the irradia£i-j2
(energy/unit area, commonly expressed in Joules/nr) . The biological weighfc~he
unit is simply an efficiency ratio so the biologically weighted dose has c
units of irradiation, J/m .
22H
-------
SURFACE
t
UV-B VISIBLE
t
\
1
Ij
[
• u
t
s
THERMOCLINE
leave —
2
o
Figure 6. The "Ferris Wheel" model of control of UV exposure. It is
Su8gested that aquatic organisms may use the motions of the mixed layer to
°btain the average light exposure. At dawn, the phytoplankton rise into the
^roulation and ride the currents. When the UV-B exposure becomes limiting,
pe algae move downward out of the circulation into the still waters under the
ermocline. A small capacity for movement plus the circulation in the mixed
permit the weak swimming phytoplankton to control their position for
photosynthetic light while receiving a tolerated UV-B exposure.
reased UV-B would reduce the time spent in the mixed layer each day.
225
-------
100
10
CO
CO
LU
z
UJ
o
UJ
u.
u.
.UJ
UJ
I
-------
Biologically weighted dose is often calculated from a knowledge of the
spectral distribution of the irradiation and a weighting factor derived from
action spectrum (the measured relative effectiveness of different wavelengths
to produce some particular biological effect) known or assumed to be
Appropriate for the organism under study. The "DNA" action spectrum has been
most widely used to derive weighting factors but this action spectrum does not
seem appropriate in some cases. Another widely used device for obtaining
biologically weighted doses is the Robertson Berger meter. This instrument
measures irradiation (expressed in a special unit termed the SU) including a
lighting factor. Approximately 20 SU are incident on a sunny midsummer day
in Lexington, Kentucky; about 10 SU on a similar day in Reykjavik, Iceland.
Organisms that show shouldered survival responses can be analyzed for
reserve tolerance to UV-B. Among the Icelandic diatoms, the two strains of
Ifealassiosira have reserve tolerance in excess of the typical UV-B exposure
they would receive in the mixed layer. The other organisms are at present
to the threshold dose. Tetrahymena exhibit a threshold dose about twice
the average daily exposure in a typical 1-m deep pond. Most other organisms
*je have tested, showing threshold type survival responses, have the threshold
dose below the average daily exposure in a 1-m deep pond (Figure 8). It is
Possible that they do not live in such shallow ponds or that they have special
sensing and remove themselves when UV-B irradiance is excessive. The
important point is that making crude but quantitative estimates of exposure
factors critical to tolerance of UV-B shows that most of the aquatic
tested are very near their tolerance limits.
^PLACEMENT LIMITING DOSE
Figure 8 shows the replacement limiting dose (RLD) computed for a wide
of aquatic organisms compared to the exposure they might receive on a
midsummer day using the models and data already noted. Because the RLD
*8 the upper limit of a species-tolerance, it is evident that some additional
Protection against solar UV must be included in species currently exceeding
•^eir RLD. Some of these factors have been noted. Organisms reduce solar UV
®*Posure by sinking to the bottom during high UV periods or collecting at
flight shielding objects in the water. The filamentous algae Rhizoolonimn
5 habitat where exposure exceeds the computed tolerance remains at the
of the ponds where it was collected, but all new growth is downward
the protection of old moribund filaments. Coliform bacteria die out in
waters in a way suggesting that solar UV is a major cause of
r. However, their UV-B tolerance is great enough to suggest that they
survive in natural waters long enough to transfer from host to host.
The models used in this presentation are great simplifications of actual
It might be concluded that tolerance and exposure Just naturally
out approximately equal. Figure 9 shows that this is not the case. The
j^P-'-acement limiting dose of ionizing radiation (cosmic rays and natural
801 °a°tivity) can be computed in exactly the same manner as was done for
Aar uv. It is evident that tolerance to ionizing radiation vastly exceeds
G*L°?IUre while these two factors are almost identical for solar UV. One can
that current levels of solar UV represent a positive evolutionary
Each species must have the observed UV-B resistance to live in its
ecological niche, a value very close to the-exposure level. A
that might gain resources by losing a protection factor (such as not
227
-------
MARINE (Iceland)
20
10
5
2
I
Q5
0.2
O.t
0.05
SUNNY SUMMER
DAILY EXPOSURES
MAX
FRESHWATER (Kentucky)
•MAX
»ovg.
euphotic
.zone
ICopepod
JUNE AVERAGE—*
avg- stream
40cm
avg. pond Im
stream bottom
avg. wastewater
lagoon
pond bottom
1.0m
.20
.2
•I
.05
0*
CM
a*
Bacteria
Figure 8. A comparison of solar UV-B exposure and tolerance of
various organisms. Dark shading indicates exposure exceeds tolerance;
light shading indicates tolerance greater than exposure (see text
methodology and discussion.)
228
-------
10
10
10'
o*
5
lofl°°
KJOO
-00
It
Oj
IONIZING RADIATION
SOLAR UV
?*5«!S?:
•••I15/'.i tin '
safest!
,tt$ 121
UfeMsh
^:C"«ir]i
/.:%"*ji nil-
™lm*\i - ^
iy . vii t3t ^_
^}..kJt? .• !•«••
Figure 9. The ratio tolerance to
exposure for solar UV (left
panel) and natural ionizing
radiation (right panel). The
appropriate equality of tolerance
and exposure of solar UV suggests
resistance to solar UV to be an
active characteristic which would
be maintained in the popula-
tion. The large excess of
tolerance over exposure to
natural ionizing radiation
suggests that resistance to
ionizing radiation may arise
indirectly and characteristics
that increase resistance to
ionizing radiation but produces
no other effect would not be
strongly favored.
ORGANISMS
229
-------
making a repair enzyme or a protective pigment or not avoiding high UV
exposure) will be killed by the UV. The best adapted strain has exactly the
UV-B tolerance required but does not waste resources protecting itself fr°m ^j
levels not actually encountered. If this status (tolerance equals exposure)
is the current condition as indicated by the available data, then it must &e
concluded that an increase in solar UV-B levels will perturb aquatic
ecosystems; they then will lose some of the available photosynthetic Ught
upon increased UV-B. Figure 10 shows the simplest mode, algae that occupy
fixed positions. From Figure 11 one can see that the loss of photosyntheti-0
light (PSL) will equal the percent increase in UV-B times the ratio of fche
attentuation coefficient for photosensitive light (K i) divided by fche
attenuation of UV-B (photosynthetic) (Kvis) in the water.
PSL (?) = UV-B (%) KpSL Eq. 5
KUV-B
For organisms that circulate in the mixed layer but remove themselves
the thermocline upon excessive UV-B exposure (see Figure 11 for a pot
model of this effect), the loss of light approximates the same ratio but **
somewhat more complex to compute and depends on the particular assumpti°
regarding depth of the mixed layer, incident UV-B, and tolerance limits. *"
any event, if the phytoplankton have mechanisms to limit UV-B exposure W
avoidance and if this mechanism is utilized with current levels of UV-B, fchf™
enhanced UV-B would replace the visible light available for photosynthes1
presumably without increasing lethality.
DISCUSSION AND CONCLUSIONS
It is very difficult to evaluate the potential effects of solar Uv °J
aquatic ecosystems. The systems are so dynamic and human consequences, su ^
as fish catch, are so variable that any attempt to directly measure 3W&^
effects would be "lost in the noise." The laboratory simulations &
microcosm data suggest that enhanced UV-B would modify aquatic ecosystems, "
it is difficult to judge how much reliance can be placed on conclusi°
derived from laboratory'experiments or microcosms where the subject species
exposed to far fewer variables than in natural systems.
The "replacement limiting dose" model and corresponding data suggest tft
many species are at present close to their tolerance limit for s° c&
ultraviolet radiation. Various species show higher or lower UV-B resisfcani5
in close correlation to their exposure and lifestyle. If solar W ir)
presently a significant limitation on aquatic organisms, then changes ^
incident UV-B will probably produce ecological changes. The changes could ^
fact be favorable, for example, elimination of coliform pollution of wafcertne
a reduced time. However, in the absence of convincing evidence as to
nature of changes that might occur, it seems prudent to try to maintain
status quo.
230
-------
SOLAR UV SCALE
SURFACE
SU/doy
10
20
PHOTOS YNTHETIC
LIGHT (PSLi SCALE
color ies/cmy day
.200 .400600
NORMAL
UV
CHANGE IN
AVERAGE
DEPTH
REQUIRED
Figure 10. A model illustrating the loss of photosynthetic light
whenever organisms are forced to move deeper in the water column to avoid
increased UV-B.
231
-------
100
Volvox Quretfs
V - Control
O - 50 tec exposure
O - 100 etc «xpoiur«
/»
Figure 11a. The time courseftgr
movement of Volvox Aureus a*
exposure to real sunlight
control. After exposure, the &i°
were layered on the top of a '
Under. The data points
the percentage remaining
upper half of the cylinder.
234
TIME (min)
ICO
90
Seo
70
o
Q.
O.
= 50
§ 40
I.
o
K
it! 10
V. olobotof
V. our»q»
Figure 11b. The time
movement of two specieis
in the dark without
exposure. Samples were f
the surface and the bottom
test chambers.
20 40 60 80 100 120 140 160 ISO
TIME (min)
232
-------
Total Solar Radiation
Total Radiation MimnVHil*
(Solar UV Only)
A .. A
20 40 60 80 100 120 140
TIME (min)
228
Figure 11c. The movement of Volvox
aureus under exposure of an
irradiance of 5.2 W/m2 light from
Westinghouse Agrolamps. The
"unirradiated" control had been
held in room light, approximately
1.6 W/nr prior to testing. The two
test populations (N and A) were
exposed to June sunlight for 5
minutes. The squares received the
total solar irradiance. The
triangles were exposed under UV
transmissive Schott glass
filters. They received essentially
the same total UV irradiance as the
"total solar irradiation" group but
with the visible component
removed. Note that although the
irradiance was much less in -UV-only
group, the depression of upward
movement was extreme. The UV-only
group appeared to be killed upon
subsequent observation, while the
total irradiation group appeared
viable.
180-
|I20
3 "00
S
80
60
«0
20
0
j- 0
1
Ho & "w
RELATIVE IRRADIANCE
Figure 11d. A test for
reciprocity. The points represent
the mean of at least 4 tests using
irradiances ranging from 1.0 x 10"*
to .37 W/nr. The same total
irradiation of 22 J/m2 was
delivered. The delay in minutes
for 50% of the irradiated
population to move into the upper
chamber when started at the bottom
over the time for controls to make
this movement was considered to be
the delay induced by the UV
radiation. The source of the UV
radiation was 2 to 4 FS-20 sunlamps
filtered by a .3cm Pyrex glass
filter and a UG-5 Schott glass
filter, 1mm thick.
233
-------
The more direct models of aquatic photosynthesis suggest that increased
solar UV-B would have little effect on primary productivity. On the other
hand, some observations suggest that solar UV-B acts as a limit on light
exposure for some of the phytoplankton. If there is a mechanism whereby algae
sense and avoid excessive UV-B exposure by restricting their time or location,
then such organisms, although they would survive as well as they do at
present, would reduce their photosynthesis (if light limited) by an amount
computed from Equation 5. Using absorption coefficients from natural waters,
the primary productivity loss for a 10% increase in UV-B leads to a loss of
visible light from 3% to 5%.
There is not an adequate data base to reach firm conclusions or
predictions as to how aquatic systems whould respond to changed solar
ultraviolet radiation. Aquatic species survive large short-term changes in
solar UV exposure. But the near equality of exposure and the tolerance
suggests present average levels of solar UV to be a limiting factor for many
species, and thus, if the average solar UV-B level were to increase, there
would be shifts in the composition of aquatic ecosystems. Only much more
extensive research could suggest the magnitude of the shifts and which species
might benefit and which species would lose.
REFERENCES
Calkins, J. 1974. A preliminary assessment of the effects of UV irradiation
on aquatic microorganisms and their ecosystems. Proc. 3rd conference_on
CIAP. DOT TSC OST 74-15, 505.
Calkins, J. 1982. In The Role of Solar Ultraviolet Radiation in Marine
Ecosystems. 539. New York: Plenum.
Calkins, J., and M. Blakefield. Unpublished observations.
Calkins, J., E. Colley, J. Wallingford, C. Hulsey, K. Lohr, and M. Boiling
1982. Sunlight-induced movement of planktonic organisms and their
relationships to water movements. Kentucky Water Resources Research
Institute. Report 132.
Calkins, J., and T. Thordardottir. 1980. The ecological significance of
solar UV radiation on aquatic organisms. Nature 283:563.
Cleaver, J.E. 1968. The defective repair of DNA in xeroderma pigmentosum.
Nature 218:252.
Cole, C.A., R.E. Davies, P.D. Forbes, and L.C. D'Aloisio. 1984. Comparison
of action spectra for acute cutaneous responses to ultraviolet
radiation: Man and Albino hairless mouse. Photochem. Photobiol. 37:623-
31.
Giese, A.C. 1976. Living with our sun's ultraviolet rays. New York: Plenum.
Green, A.E.S., and P.P. Schippnick 1982. The Role of Solar Ultra-Violg£
Radiation in Marine Ecosystems. 5. New York: Plenum.
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, P., and J. Calkins 1980. The inactivation of a natural population of
coliform bacteria by sunlight. Photochem. Photobiol. 31:291.
Hunter, J.R., S.A. Kaupp, and J.H. Taylor 1981. Effects of solar and
artificial ultraviolet-B on larval northern anchovy Engraulis mordak.
Photochem. Photobiol. 34:477-86.
Lorenzen, C.J. 1979. Ultraviolet radiation and phytoplankton photosyn-
thesis. Limnol. Oceanpgr. 24:1117.
Luckiesh, M. 1946. Applications of germicidal erythermal and infrared
energy. Mew York: van Nostrand.
and Nachtwey, D.S. 1975. Natural resistance of freshwater algae to
UV radiation - a survey. CIAP Monograph 5:5-75. NTISPB247724.
Resnick, M.A. 1970. Nature 226:377.
Horowitz, H.J. 1950. Absorption effects in volume irradiation of
microorganisms. Science, 111-229.
Peake, M.J., J.G. Peak, M.T. Moekrins, and R.B. Webb 1984. Ultraviolet action
spectra for DMA dimer induction lethality, and mutagensis in E_._
scheriachia coli with emphasis on UV-B region. Photochem. Photobiol.
40:613-20.
M.A. 1970. Sunlight-induced killing of Saccharomyces cerevisiae.
Nature 226:377.
Russell-Hunter, W.D. Aquatic Productivity. New York: Macmillan.
Setlow, R.B. 1974. The wavelengths in sunlight effective in producing skin
cancer: a theoretical analysis. Proc. Nat. Acad. Sci. U.S. 71:3363.
Sn>ith, R.C., K.S. Baker, 0. Holm-Hansen, and R. Olson. 1980. Photoinhibition
of photosynthesis in natural waters. Photochem. Photobiol. 31:585.
Shettle, E.P., and A.E.S. Greene 1974. Multiple scattering calculation of the
middle ultraviolet reaching the ground. Applied Optics. 13:1567-1581.
235
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How Might Enhanced Levels of Solar
UV-B Radiation Affect Marine Ecosystems?
John Kelly
Ecosystems Research Center
Cornell University
Khaca, New York USA
ABSTRACT
One of the most challenging tasks facing environmental scientists is to
determine the likely consequences of an external change for complex natural
e°osysterns on the basis of observations of the impact on individual organisms
°r processes. Assessing the potential impacts of enhanced solar UV-B
radiation on the marine environment presents such a challenge. The potential
UV-B stress is broad-scale; the response of marine ecosystems involves many
8Patial and temporal scales, and also involves subtle changes that may be
difficult to detect. A particularly acute concern exists, however, for
^sting changes—changes made possible because of long residence times for
^ny oceanic processes, as well as the lack of mitigating measures given the
spatial extent of both stress and effects. Thus, acknowledging the specula-
te nature of extrapolations, the potential problems are of a quality
Inquiring significant a priori examination. In this paper, I suggest several
types of ecological changes of concern. The examples—including possible
^ffects on food webs, fisheries, and biogeochemical cycles—are chosen to
lllustrate the scope and urgency of the problem.
^-B INCREASE AND MARINE ECOSYSTEMS: WHY SHOULD WE BE CONCERNED?
Every type of environmental alteration seems to carry special features
that make assessment and resolution of potential ecological problems
difficult. In the case of projected stratospheric ozone depletion and
increased UV-B striking the earth's surface, the spatial scale of the
etlvironmental modification is one such confounding feature. The global nature
the problems brings associated challenges: the task of observing
i changes, perhaps subtle, across the vast expanse of the oceans; and
problem of considering effects upon the variety of ecological systems from
nearshore to the deep sea, from polar to tropical regions. For all of
these ecosystems, but particularly for much of the deep sea surface waters
from land and ieaat studied in situ, documenting changes distinct from
237
-------
natural variation may prove especially frustrating because .little background
historical information exists. Yet, ecological changes keyed to currents and
movements of water masses have the potential to set in motion biologic3-1-
and/or biogeochemical effects of uncertain magnitude that endure for the time
scales of oceanic circulation—processes with residence times of centuries and
longer. Unfortunately, also associated with the spatial aspect is fcne
probable lack of .potential for mitigating observed effects. Furthermore,
mitigation of the causes of those effects, even if it were achieved quickly»
would do little to alter the lengthy recovery times of any circulation-related
ecological changes that have been already induced.
A valid concern is that significant changes might occur in many
ecological systems well before we know it; and we might be stuck with
changes for a very long time. This concern adds urgency to the assessment 01
the potential ecological problems.
A crucial part of this assessment concerns the effect of enhanced U»"
upon marine ecosystems. Clear and convincing evidence from research of fctl
past decade indicates that UV-B radiation can injure the health of some mari'n
organisms. In this paper I focus on the effects upon whole ecologi0^
systems. The level at which I address the problem is not limited c
mechanisms of physiological damage to tissues of individual organisms, or, \°
example, on possible reductions in certain sensitive surface-dwell1^
populations. Those are major aspects of the assessment problem, but 1t
difficult to extrapolate from such directed effects to the o
consequences for natural ecosystems which, in and of themselves, are
concern to humans. In the absence of information on ecological effects at
ecosystem level, I speculate about those ecological processes, components, a
systems that could be agents for, or targets of UV-B induced ec°^°^i^Y\e
change. The major contribution of this effort is to suggest facets of &
problem that do and do not lend themselves to direct ecosystem-leV
assessments.
WHAT COMPONENTS AND PROCESSES ARE DIRECTLY AT RISK?
The level of UV-B striking the sea varies seasonally and with lafci Of
The penetration of UV-B into seawater varies with turbidity, concentration
dissolved organic matter, absorption by plants, and other factors. In SP n
of temporal and spatial variance in UV-B attenuation, the global c°n?cai
relates to ecological impacts acting directly upon biological and cheBILce
activity only in a relatively shallow (perhaps several meters deep) su jne
layer of water. Though this represents a very limited portion of the mar.ry
environment, it includes an important portion of the zone where the pr*® to
food base for marine ecosystems originates and where many processes °cCUL,j.e
influence the distribution of organisms, energy, and matter for the wn
ocean to its depths.
There is convincing evidence that direct effects on certain near-su** ^
organisms and processes in marine waters are caused by exposures to enha
levels of UV-B radiation (Calkins 1982; NRC 1984). Biological effects r» ^
from cellular-level damage and physiological impairment to r~ cted
reproductive potential and direct mortality. Organisms that can be affe ^
include the two major biological components of the sea--photoautotrophic g>
heterotrophic organisms, or, roughly speaking, both plants and anil"
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Several particular effects raise significant concerns for marine ecosystems.
I focus on these to suggest potential consequences.
Photoautotrophic species of free-floating phyto- and bacterio-plankton,
along with attached algae and submerged vascular plants in the very shallow
coastal areas of the sea, are the "primary producers" of the aquatic
realm—those using the energy of incident solar photosynthetically active
radiation (PAR) to produce their own organic tissues. These autotrophic
organisms, active only to water depths to which sufficient PAR penetrates
(known as the "euphotic" surface layers of the ocean), are key to the entire
marine food web. Two kinds of noted effects on autotrophic organisms are of
special interest. Experimental evidence suggests that rates of primary
production of carbon into organic matter (both by some species of floating and
attached bottom-dwelling plants) are significantly reduced when natural
autotrophs are exposed to slightly increased UV-B doses (see Worrest 1982);
such a mechanism is responsible for "photoinhibition" of primary production
seen at high light intensities at the very top of a water column.
Furthermore, evidence from laboratory aquarium "microcosm" studies also
suggests that certain species of phytoplankton are more susceptible than
others, so that when a mix of species is exposed to increased UV-B doses, a
different plankton community can develop in comparison to normal control
levels of UV-B (Worrest 1982).
Heterotrophic species, ranging from microscopic forms to the great
whales, depend for their energy and nutrition upon organic tissues synthesized
by autotrophic forms. Evidence shows that some of the smaller heterotrophs
may be at risk, especially those not afforded UV-B protection by pigmentation.
'Although the animals normally living in the upper layers of the sea seem
generally more resistant to UV-B damage than those living at lower depths,
effects on surface-dwelling forms of zooplankton (including copepods,
euphausids, and planktonic larvae of shrimp and crabs.) have been shown to
occur with increased UV-B. These effects include increased mortality of
adults, decreased survival of early larval stages, and decreased fecundity of
survivors (reviewed by MRC 1984). Additionally, fish eggs that float at the
sea surface and larval life stages of some fish (e.g., anchovy) show cytogenic
abnormalities and reduced survival caused by UV-B radiation.
Value of Direct Effects
Direct biological effects from UV-B exposures, observed for individuals
°r even calculated by extension to conditions encountered by natural
Populations, are considered in at least partial isolation from the other
ecosystem components and processes. These controlled experiments, conducted
without the many complicating variables inherent to the natural situation, are
Designed to be simple tests to determine if UV-B radiation enhancement of the
magnitude presently envisioned through past and future decades is sufficient
to cause biological damage to individuals of certain species. These findings
have created legitimate and significant concern regarding possible changes to
"narine ecosystems. We know for certain that some individual marine organisms
and processes which we care about are at risk from increasing UV-B levels.
Thus, the value of the scientific demonstration of directly caused UV-B damage
is unquestioned. However, a next step in the assessment—extension of results
to the complex natural environment—is difficult and tenuous.
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ECOLOGICAL EFFECTS IN NATURAL ECOSYSTEMS
Ecosystem modification of direct effects can arise from biological*
physical, and chemical mechanisms that are features of natural ecosystems, but
are not features contained in direct effects tests. In nature, "indirect1
effects can be transmitted via ecological linkages to components or processes
themselves not directly sensitive to UV-B. UV-B increases itself could also
cause environmental modifications and indirect effects. For example*
increased photolysis of some dissolved organic or inorganic chemical compounds
in surface seawaters might occur (e.g., Zepp 1982); some modifications of tne
aqueous chemical environment can indirectly cause biological changes.
Although we are conscious of these features of ecosystems, we so far have
gathered data relating to effects only on select parts of marine ecosystems;
it is uncertain that any of the effects carry, unqualified or unmodified, fco
nature (Figure 1).
The possibilities for indirect effects, embedded within a perspective on
the potential ecosystem responses to UV-B stress, are indicated in a simple
diagram relating biological effects and ecological changes (Figure 1). Stress
agents can act initially upon individual organisms directly or by modifyin»
the environment. Such individuals can then affect other individuals
(populations and communities) by many biotic mechanisms including predation,
competition for resources, and altered reproductive success. Additionally*
however, an affected individual (or more usually a group of individuals) can
create a change in ecosystem processes (e.g., the rate of primary production*
rates of oxidation of organic matter, patterns or timing of the biogeochemica^
cycling of elements). These processes are depicted (Figure 1) as at
interface between organisms and their environment. Almost invariably,
in processes modify the chemical broth in which organisms bathe; sometimes &"°
physical environment is also altered. For example, a change in the balance o
organic production, consumption, and decomposition processes changes tn
concentration of plant biomass, which in turn changes solar radiati°
extinction coefficients and the light energies available throughout tn
underlying water column.
In general, affected individuals in ecosystems can spawn indirect effec .
by these paths—biological interactions and alteration of process rates.
effect upon individual organisms can beget others, creating change in
biological structure (e.g., changes in populations, species interactions, .
food webs) and processes (e.g., biological rates, biogeochemical interaction
in the ecosystem. Sometimes changes will be very unexpected or far r
from the original impact in time or space (e.g., Levin et al. 1981)• Q
extrapolations need to deal with even more than the issue of enhancement
direct effects. At the other horn of our extrapolation dilemmas sits
possibility that the same two general paths for indirect effects will
compensating mechanisms, ameliorating direct effects so that rjv
discernible change happens even where some individuals are clea
injured. For compensation, biotic and chemical mechanisms exist, but phY3*
-------
EnfaiBcnnut of UV-B Ridiiuon
Enhancement of UV-B Radiation
•Coamnitr'
L_ _ _ — — — —I
Modification of
physical and
chemical environment
Individual
Organisms
Population(s)
Changes
'Community
'Ecosystem'
Figure 1. Potential ecological effects of enhanced UV-B in marine
Ecosystems are shown above. The diagram shows direct and indirect pathways
"or producing changes in individuals, populations, communities, and
ecosystems. The shadow insert suggests the current state of information
Existing for UV-B effects on different pathways and at different levels in the
environment.
-------
I next illustrate compensatory changes and indirect ecosystem effects f°r
two cases where extrapolation of effects is important. These are effects that,
if verified, should arouse human concerns for regional or global
repercussions. The examples involve:
• Reduction in rates of photosynthetic production of the organic tissues
forming the primary resource for marine food chains
• Reduction of surface-dwelling stages of fish larvae and their adult
population stocks.
I do not comprehensively consider all aspects of the extrapolatio
problem; only certain classes are given. I simply wish to illustrate a number
of existing uncertainties before I suggest the potential consequences f°
marine ecosystems should such reductions occur.
ECOSYSTEM COMPENSATION AND A KEY PROCESS
The first scenario considers the possible reduction in priwa t
production. The level of primary production influences many aspects of marin
ecology and biogeochemistry. These extended effects form the major f°cus.°n
my speculated consequences for the oceans. First, I examine the extrapolati
problem. Assume (following Smith and Baker 1982) that with enhanced
productivity reduces up to HQ% at the surface, decreasing to a 0%
within 2 attentuation lengths (a value roughly on the order of 1 to 10 m,
dependent upon the optical characteristics of the water (Smith and Baker 19/ "'
1982; Smith et al. 1980). The question of concern is not, "Does,, Jut
inhibition of primary production occur in the very surface waters?"
rather, "Does it change the productivity of the whole water column?"
One way to suggest the net quantitative change in an entire water
is to make calculations via mathematical models. Smith and Baker
examined the potential magnitude of photosynthesis reduction for the wh° ,
euphotic zone using a simple, depth- integrated model without the "nonlinea^r
(including indirect effects) or compensating mechanisms of Figure 1. . ry
calculations predicted that with a 25% reduction in ozone thickness, Prim ,
production would decline 9%, regardless of the absolute productivity lev
(Note: the relation between ozone and total productivity in the model
quite linear, as a 5% primary production decrease would occur with a 16$
reduction.) Smith and Baker (1982) strongly emphasize limitations to n
model, focusing on some possible nonlinear relationships relating to s$ ,c&\
quality of the solar radiation and concomitant changes in effective biolPS ^
doses to marine organisms. They express concern that several indirect ef fe.&s
not considered by the model might easily add order of magnitude uncertain
to predictions. Complicating features of the natural ecosystem include
less sensitive to enhanced UV-B (e.g., in Figure 1 — reduction in numbers
individuals leading to increases in individuals of another sped
Additionally, they suggest complications due to the influence of v Qf
movement upon the depth of the surface mixed layer. Vertical mixin» ^
organisms makes it difficult to estimate biologically effective doses a"heir
organism's exposure regime for PAR or UV-B with precision. Yet ,ty
considerations, although perhaps quite comprehensive in relating product!*
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and solar energies, do not include other facts that may be limiting to primary
production.
One can envision yet another wrinkle, which I believe stands as a good
example of potential ecosystem compensation. Plants need nutrients for growth
as well as light energy; the availability of nutrients in the photic zone
limits production, although in some marine areas, particularly the high
latitudes, light may be more limiting through portions of the year. Except
for heavily enriched coastal areas of the oceans and intense upwelling areas,
the level of marine autotrophic production is partially, if not primarily,
sustained by heterotrophic regeneration of dissolved nutrients (such as
nitrogen and phosphorus) within the ecosystem (e.g., Kelly and Levin 1986).
Thus, there exists an internal ecosystem factor influencing production to
complicate the solar radiation/photosynthesis relationship. But if production
is reduced within an upper portion of the water column, we cannot suggest with
assurance that internal supplies of nutrients used to support a production
level would not now be available below the new "photoinhibited" zone. To
accomplish this compensation, mixing or simple diffusion of the unused
nutrients only several downward vertical meters needs to occur; there are
phytoplankton species that live much deeper than this in the water column, are
adapted to lower light intensities, and whose growth would be enhanced by
greater nutrients. Thus, within the range of the results for enhanced UV-B
and productivity lies the possibility that no net change in the overall water
column rate of primary production will occur.
Note that this scenario easily has room for some ecological change
outside of an impact on the process of immediate concern. The ecological
change from deeper UV-B photoinhibition could involve a slight deepening, or
expansion, of the "neuston" community of organisms that dwells at the sea-air
interface and is more adapted to high light intensities. Underneath this
"expanded neuston layer" there could also be some changes in the mix of
species responsible for the process of primary production." Species changes
don't necessarily alter the overall level of primary production, which is more
likely set by the supply of available nutrients. The main point of this
example, however, is that the magnitude of euphotic zone primary production
fates, even with surface inhibition and changes in autotrophic community
composition, need not be altered as a whole.
PHYSICAL FEATURES, INDIRECT EFFECTS, AND COMPENSATION: A POPULATION EXAMPLE
The first simple extrapolation problem added a compensation mechanism to
uncertainties associated with modeling photosynthetic reductions. My second
example adds another level of complexity and examines an individual fish
species. Direct effects on young fish could be a serious problem with
enhanced UV-B because much of the world's commercially important fish species
(e.g., tunas, mackerels, flatfishes, pilchards, anchovies, cods) produce
"pelagic" (living in the water column as opposed to dwelling on the ocean
floor) eggs and larvae; both of these life stages are translucent and allow UV
Penetration deep into tissues. Consequently, "most pelagic eggs and larval
stages of fishes studied to date show high sensitivity to UV radiation and
often die if exposed in shallow containers to solar UV" (Hunter et al. 1982).
Aspects of the extrapolation problem for larval populations of northern
anchovy have been discussed rather thoroughly by Hunter et al. (1982). In the
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anchovy case, known direct effects include: lesions in eyes, brain, or other
body tissues; increased mortality; and reduced growth in surviving larvae. To
illustrate the potential concern for the anchovy larval population as a whole,
by making simplifying assumptions of a stable vertical distribution of larvae
and no vertical mixing of eggs and larvae and using short-term exposures (12
days) for mortality effects, Hunter et al. (1982) calculated that annual
production of larvae lost to UV-B mortality might rise by a factor of 1.38
with a 25% reduction in ozone thickness.
Relative to the previous primary production example, there are similar
uncertainties with vertical mixing for small animal forms; however, more can
be made of the issue of whether there is actual damage to individuals in the
field because the larval organisms have more ability to move away fro™
damaging exposures than do most phytoplankton. Yet in direct analogy with the
key process case, a similar central question remains—does individual damage
mean that the numbers or biomass of the adult population will change?
Three relevant aspects of the ecosystem that contribute to extrapolation
uncertainties illustrate different classes of concerns: physical oceano-
graphic features to moderate effects upon individuals, a biological mechanism
to compensate for loss of individual eggs and larvae to maintain adult
population levels, and indirect food chain effects that might add
synergistically to enhance direct effects.
Ocean surface waters are not static vertical strata and mixing occurs
that complicates projections of the overall exposure regime for organisms-
Implications of this feature, in terms of effects, have been noted by
Kullenberg (1982), and by Smith and Baker (1982) for photoinhibition, and were
considered by Hunter et al. (1982) in their analysis of enhanced UV-B conse-
quences for the northern anchovy. Because mixing intensities occur across a
broad range in the ocean and are locally variable, calculations using exposure
regimes and dose-effect relationships from direct effects tests have
considerable uncertainty. Hunter et al. (1982) also add the uncertainties of
the vertical distribution of the larvae, seasonality of larval production,
seasonality of incident UV-B, and variations in UV-B penetration caused by t°e
concentration of plants with which larvae associate for food. They conclude
that vertical mixing alone could reduce estimated UV (direct) effects to zero,
and that the variables of mixing and vertical distribution could account f°r
the full range of possible UV effects, independently of other variables.
Even if physical and distributional (habitat) variables were well known
in some specific case, there are other problems. Biological compensation f°r
early life stage effects could occur so that effects do not alter year clas3
success of the adult population. Density-dependent mechanisms, including
changes in survivorship at different life stages or changes in reproductive
capacity, might ameliorate effects seen in an individual larva. For exampie»
there could be increased survivorship in unexposed individuals. Additionally*
UV-B mortality might be, although higher, still relatively small compared *°
other sources of natural mortality. Over some time, greater fecundity (m0^
viable eggs per adult female) could also develop, compensating for a certai"
percentage of young lost to UV-B. A further compensation could be that •
lesser number of surviving individuals might grow bigger faster because
is less competition for a food resource. These, simple examples of known
-------
density-dependent mechanisms could therefore act to maintain adult numbers or
biomass within normal bounds of natural variation.
Compensatory changes might well negate egg or larval effects, yet
interactions with primary production might act, synergistically, to enhance
the population decline. Besides direct UV-B related mortality of young
developing stages of fish, there could be indirect mortality from
starvation. This could occur if primary production decreased or the
autotrophic species producing the preferred food of a given fish were replaced
by indirect ecological changes (Figure 1). Perhaps there would even be an
amplified mortality in that some larvae die from direct exposure, others from
lack of food, and still others from the combination of reduction in food and
weakening from exposure (by being less able to .compete with other organisms
for limited food resources). One can thus foresee the possibility of a
catastrophic drop in a fish population, even if the direct mortality from UV-B
alone would not convey that sense of concern.
These simple examples illustrate that the problem of projecting
biological effects to marine ecosystems is itself at a young stage of
development; this task represents a significant scientific challenge. What is
not yet known about ecosystem changes adds up to such a potpourri of
uncertainty that there are cases where we can't confidently predict whether a
particular component or a process will increase, decrease, or remain the same.
POTENTIAL CONSEQUENCES FOLLOWING EFFECTS
Having given due emphasis to the tenuous nature of extrapolations, I am
not the least bit hesitant to suggest that significant ecosystem changes could
ensue. Ecological repercussions could arise especially from the following
effects, if they are expressed:
• Reduction of certain individual species critical to the maintenance of
structure or function in the ecological system
• Change in the mixture of species of primary producers
• Reduced rates of primary production of organic matter.
Some aspects of these have been mentioned. I'll touch briefly, with
examples, upon potential consequences in these three areas.
Mortality or Impairment of Certain Populations
In general, mortality or impairment of certain populations can lead to
significant changes in biological structure. For such "key" or "critical"
species, which can include phytoplankton, zooplankton, and fish, some chains
of effects are well documented. Removal of a key predator changes the
distribution and abundance of more than just prey organisms, leading to
species diversity changes and changes in community dynamics (e.g., Paine
1966). The structure of an entire pelagic food web can be altered, for
example, by changes in fish feeding pressure. Feeding pressure can reduce
some zooplankton species, allowing greater growth in other zooplankton; these
changes in the zooplankton community then contribute, indirectly, to alter the
type of algal assemblage present.
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Cascading from effects on key species, there can even be alteration of
the physical environment. Levin et al. (1984) relate an example in which
removal of sea otters along the U.S. Pacific coast increased animal grazing on
large attached brown algae (kelp) and eventually reduced the kelp beds, whose
absence exposed the shoreline to greater physical disruption from waves.
Other nearshore areas, such as the Gulf and Atlantic coasts, are exposed to
less wave action than the west coast. Yet even in these less severe physical
environments, reductions in growth of some attached plants, either directly by
UV-repressed photosynthesis or indirectly by a sequence of interactions within
the heterotrophic community, would alter physical aspects of the ecosystem.
Removal of the physical habitat structure lent to shallow waters by
seagrasses, for example, would likely modify wave and current energies along
shorelines, which would change spatial patterns in sediment deposition and
water clarity. Such physical consequences would be significant; they would
involve alteration of two primary environmental features that influence the
distribution of marine organisms and food webs.
Whether or not those heterotrophic species of larval fish, crab or shrimp
larvae, or zooplankton that are known to be directly sensitive and at risk
from UV-B (e.g., Damkaer et al. 1980; Damkaer and Dey 1982; Worrest 1982;
Hunter et al. 1982) are critical species remains to be demonstrated. But the
primary producers throughout marine ecosystems certainly are key components,
for they set the table for the rest of the ecosystem.
Changes in the Species Composition of Primary Producers
Changes in the species composition of primary producers can influence
both food webs and ecosystem processes. Worrest et al. (198!a, 198lb) show
that shifts in community composition are possible with UV-B. Worrest (in
Harwell and Hutchinson 1985) suggests that compositional change would alter
size distribution of primary autochthonous particles and directly change
nutritional quality, an effect already noted with enhanced UV-B (i.e.*
depressed protein content, dry weight, and pigment concentration °f
autotrophs). Changing sizes of food particles might alter the energy
allotment required for consumption, perhaps reducing feeding efficiencies i°
consumer species, even if wholesale heterotrophic community changes were not
instituted. Energy efficiency change in either individual species or in f°°d
webs (by simplification or diversification of the species interactions) could
change ecosystems; changes in particle size distributions or in bulK
nutritional quality could translate to a different level of food energy being
available to top consumers of a food web. Such changes might be of special
concern when considering, for example, what nutrition or size alterations
might do to the pelagic food chain in the Antarctic that seems to center
around the transfer of phytoplankton biomass to only one next major component!
the krill (e.g., Everson 1984). Effects upon such a critical linkage, at a
latitude where light levels are indeed important to production and where ozone
depletions have been noted, would have major implications for the direct
consumers of kr ill—whales, seals, birds, fish, squid, and even bottom
dwelling organisms.
Particle size alteration and nutritional change with species compositio"
could affect other ecological features, particularly biogeochemica*
processes. For example, settling rates of primary particles vary with s&.
and shape. Because primary particles have many chemical elements incorporate
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within their hard parts and soft tissues, as well as adsorbed to their
surfaces, removal rates of elements and compounds from the surface ocean-mixed
layer by settling, an important marine geochemical process, could be altered.
But biogeochemical linkages are perhaps more likely to be affected in a
significant manner if the magnitude, rather than quality, of primary
Production changed with UV-B enhancement.
Reduced Rates of Primary Production
I see reduced rates of primary production as potentially driving a number
°f important ecosystem changes, notable individually and collectively for
their possible broadscale nature. One of these involves biogeochemical
Processes, which, as noted in Figure 1, are a major feature at the ecosystem
level. The other relates to potential fish yields from the sea.
Of interest are those changes associated with element cycles and organic
"Batter distribution throughout 'the ocean which key to the production,
transport, and decomposition of primary produced organic matter. That the
°ycling of many elements in the oceans is very tightly coupled to biological
Activity, especially primary production, has been recognized for much of this
century. For example, oxidation of the primary production of the euphotic
2°ne, although a process most active closer to the surface, occurs throughout
^eptn. This decomposition of organic matter is, in part, responsible for the
Vertical and horizontal distribution of some dissolved gases, including oxygen
and carbon dioxide, and dissolved inorganic plant nutrients of nitrogen and
Phosphorus, as well as other biologically active elements throughout the ocean
Je-g., Riley 1951; Wyrtki 1962; Redfield 1934, 1958; Redfield et al. 1963).
Additionally, from a summary by Suess (1980), we can also see that the
transport of the organic carbon to any depth in the ocean can be represented
*n a simple general relationship, normalized to the level of production. With
lowering of primary production, Seuss and others suggest that the organic
j^Pbon reaching any depth in the ocean will decrease, leaving less food for
the secondary production of the heterotrophic organisms dependent upon that
°a**bon supply. We don't know if the magnitude of a change in primary
eduction with UV-B would cause changes we could easily observe in sedimenta-
n processes, or whether it would cause geochemical changes we would point
as "of immediate environmental concern." However, because the major
biogeochemical cycles are tied to surface biological activity, but
relate to the depths and circulation of the oceans, important changes
be felt across many temporal and spatial scales.
One should not consider marine consequences without discussing fisheries,
is perhaps the most common "endpoint" of human concern. I have already
some problems with fisheries, but how would direct reduction in
production translate to reductions in fisheries yield? In the absence
information, we can make the simple linear extrapolation, suggesting that
percentage reduction in fish biomass yield would be the same as that for
production; however, at least one summary suggests that this relation
nonlinear.
Nixon and Pilson (1984) presented a compilation of. data for fisheries
and primary production of some marine systems. Although such data are
f{?en>selves subject to great errors and uncertainty (e.g., how do we account
p heterogeneities in production? How does one choose the size of the
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system? How good or comparable are yield data?) and the scatter is such that
predictions for yield at an individual level of production would be
inadvisable, a rough general correlative relationship is evident from the
summary. Examination of the broad pattern in the figure by Nixon and Pilson
reveals a nonlinear relationship, with less fish yield per unit of primary
production (as grams of carbon) seen at lower primary production levels. Fr0in
those data, for example, it would appear that about 1000 kg fish per ha per yr
may accompany primary production of about 1000 gC per m per yr whereas there
may be only 5-7 kg fish per ha per yr associated with 100 gC per m per yr<
The explanation for such a pattern is unknown. Perhaps with lower primary
production, other fish, not commercially sought, are produced. Maybe -the
efficiency of energy yield to higher trophic levels changes across different
ocean areas and with different production levels. In either event, due to the,
scatter observed in the range of average ocean and coastal production lever'
(i.e., 100 to 500 gC per m2 per yr) and fisheries yields, I would &®
uncomfortable in suggesting a mechanism or in suggesting how much greater tn
percent of fishery production would be than the percent of reduction
primary production.
If we use the relationship the ramifications are that with reductions J-
production from UV-B we should worry about (a) the fisheries yield decreasing
everywhere, and (b) a reduction in primary production resulting in a great
than proportional reduction in fisheries yield.
ASSESSING ECOSYSTEM CHANGES: PROSPECTS AND LIMITATIONS
I hope my examples spark some argument, discussion, and research' on the
and other issues. We are uncertain how the convincing evidence for dirtQr
effects on important species and processes (effects having potential *
producing large-scale ecological consequences) might actually be expressed
the oceans. Not only the magnitude, but even the very nature of ecosys
effects is unclear. Given this situation, I think we are left with two b*sce
questions: What tools do we have and what approaches must we use to re d
the uncertainties as quickly as possible? Are there aspects of.
uncertainty that we are not likely to resolve before the changes occur?
*.«!
To address ecosystem changes, the best tool we have is experiwen
manipulation of ecosystems themselves. Although this is not possible
marine ecosystems (other than the global experiment itself), we do JV ^
physical models of some ecosystems, called microcosms or mesocosms, in J! eve
we can look directly at some ecosystem-level effects (e.g., Grice and B
1982; Kuipers 1984). For example, perturbation studies on simulated s
coastal ecosystems have been conducted at one such facility, the
mesocosms, at the University of Rhode Island along Narragansett Bay in
U.S. (e.g., Nixon et al. 1984; Kelly et al. 1985). Such research, U
complex ecosystems, is urgently needed for assessing UV-B effects. Ifc
give us a better sense for the possibility and extent of indirect effect3
compensating mechanisms in a most efficient manner.
We could use such ecosystem experiments to identify sensitive
and processes of natural ecosystems. This emphasis could give us indie*
for monitoring and assist in mapping effects in nature related fccL,C)w'1
penetration of UV-B in different marine waters. Correlation of for
sensitive features with UV-B penetration changes is valuable informatio
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scientific assessment of environmental risk, although unequivocal data of this
nature are difficult to gather.
Of equal importance to identifying sensitive components or processes.
however, is identifying critical or sensitive ecosystems. I believe we need
to direct some attention to this problem; so far we have only looked at the
generic level assessed. The last decades, especially with increased use of
remote sensing for oceans, have given us an increased awareness of
heterogeneity in oceans. With this comes an appreciation for the variety of
physical habitats and their interactions across a variety of time and space
scales inherent to the sea. The UV-B concerns apply across these scales, and
it would be efficient and wise to identify and focus intensively upon at least
three classes of marine ecosystems: the sensitive ones, those having the
least capacity for quick recovery, and those of greatest direct value to
humans.
I must end on a note of pessimism by returning to issues in the
introduction. Although, for example, mesocosm experiments are essential
features to the environmental assessment of UV-B, the principal limitation of
such research centers on the issue of scale. Some components of ecosystems
cannot be included in experiments because the spatial scale of the enclosure
is not large enough; this is particularly the case with the larger consumers
that often cause us the most concern. Many processes, especially microbial
aspects and primary production processes, can be examined directly in mesocosm
experiments in the proper ecosystem context. However, large-scale processes
associated with physical features or global biogeochemical cycles obviously
cannot, be accommodated. I remain concerned that we will be unable to
scientifically assess in the near term, to suitable levels of confidence, some
major aspects of potential oceanic effects—especially large-scale, sporadic
features, or those happening in the clear waters of the deep sea where we have
the poorest background information available for comparison to know if effects
are occurring.
ACKNOWLEDGMENTS
This publication is ERC-127 of the Ecosystems Research Center (ERC),
Cornell University, and was supported by the U.S. Environmental Protection
Agency Cooperative Agreement Number CR812685.
REFERENCES
Calkins, J., ed. 1982. The role of solar ultraviolet radiation in marine
ecosystems. New York: Plenum Press.
Damkaer, D.M., and D.B. Dey. 1982. Short-term exposures of some planktonic
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251
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TERRESTRIAL PLANTS
-------
The Potential Consequences of Ozone Depletion Upon
Global Agriculture
Alan H. Teramura
University of Maryland
College Park, Maryland USA
Our global agricultural system depends on only a handful of key crop
species. Of the 350,000 species of plants that have been described in the
world, over 80,000 are edible (Table 1). Of these, only about 3,000 are
actually harvested for use as food (Vietmeyer 1986). Of these 3,000, only
about 80 species have been domesticated and only 15 species supply most of the
food calories and three quarters of the protein to the world's people. Three
""embers of the grass family—rice, wheat, and corn—supply two-thirds of these
°alories and one-half of the protein (Table 2).
Over the course of the past decade several hundred scientific reports
been published documenting the UV sensitivity of more than 200 plant
species and varieties under a wide variety of growth chamber, greenhouse, and
fleld experiments (Teramura 1983; National Academy of Sciences 198*1). Of the
°rops examined, approximately two-thirds are sensitive to UV radiation, with
Or>e out of every five identified as extremely sensitive. This finding has
Promoted considerable concern over the potential consequences of ozone deple-
tion. However, several critical caveats must be included with such a "dooms-
day scenario." First, experiments conducted in growth chambers or greenhouses
tend to overestimate and exaggerate plant susceptibility to UV radiation
(Teramura, Biggs, and Kossuth 1980; Teramura 1982; Teramura and Murali 1986),
Partly because natural protective mechanisms are not fully developed under
artificial growing conditions. Because over 90? of our knowledge of UV effec-
tiveness comes from growth chamber studies, we have a worst case view of these
effect3. The second complication concerns the tremendous amount of varia-
^Uity in UV sensitivity within each species. Most of our crops have numerous
varieties or cultivars particularly suited to specific growing regions. For
lristance, corn grown in Maryland is a different variety from that grown in the
Midwest. Over 100 crop varieties or cultivars have been screened for UV
^sponsiveness and approximately two-thirds of these were identified as being
Sensitive (Biggs, Kossuth, and Teramura 1981; Dumpert and Boscher 1982; Krizek
Overall, nearly the same range of sensitivity can be found among
255
-------
Table 1. Plants as a Food Source
Category
% of Total
350,000 known species of plants
80,000 edible plants
3,000 harvested plants
80 domesticated plants
15 key crop plants
100
23
0.9
0.02
0.004
Table 2. Major World Food Crop Production
Crop
Production
(million metric tons)
Crop
Source: Food and Agriculture Organization, 1984
256
Production
Cereals
wheat
rice
corn
barley
sorghum
Legumes
soybean
bean
peanut
1984
522
470
449
172
72
90
32
21
Sugar Crops
sugar cane
sugar beet
Root Crops
potato
sweet potato
cassava
Tree Crops
banana
coconut
936
293
312
117
129
41
*•* 4
31
-------
cultivars as among different species. Therefore, a crop such as soybean
may be labelled as sensitive to UV based on the response of the majority of
cultivars tested despite having some very tolerant cultivars. In other words,
most crops are not 100? sensitive or 100? resistant to UV.
The third complicating factor arises as a result of the endpoint or
criterion used by various investigators to gauge UV sensitivity. Many studies
have used whole plant features such as plant height, number of leaves, or
total plant dry weight (Biggs and Kossuth 1978; Van, Garrard, and West 1976;
Tevini and Iwanzik 1982). Others have used physiological or biochemical
criteria such as photosynthesis, respiration, or protein content (Brandle et
al. 1977; Sisson and Caldwell 1976; Vu, Allen, and Garrard 1982). Because of
the inherent differences in these diverse gauges of sensitivity, it is not
terribly surprising that a plant may be sensitive to UV based on photosyn-
thetic determinations while it is resistant based on changes in dry weight.
Although crop yield may ultimately be the crucial feature to study, only a
handful of investigators have addressed this question because of the enormous
technological difficulties encountered in the field. Despite these and other
difficulties, our current uncertainty is not whether plants are affected by
UV, but rather the magnitude of this sensitivity. Because only a handful of
key species supply most of our agricultural needs, this potential suscepti-
bility warrants great concern.
To illustrate some of the potential consequences of ozone depletion on
global agriculture, I use soybean as a model. Table 3 shows that soybean has
become a major plant source of oil and protein for the world, ranking fifth in
the world in terms of tonnage, behind wheat, rice, corn, and barley. It is
the third largest crop in the United States, which produces nearly 60% of the
world's total. Due to its importance in the United States and global agri-
culture, any decrease in yield would unquestionably have a profound impact on
the world economy.
Because of the drawbacks inherent in growth chamber experiments, the most
meaningful method to assess risk is by examining the effects of UV radiation
on field-grown crops. In such a setting one is faced with a more difficult
task in performing the experiment because more UV radiation must be added to
that normally received by the plant. The data shown in Table 4 spans a five-
year period between 1981 and 1985 simulating a 25% ozone depletion for one
cultivar of soybean, Essex, which is one of the most widely grown cultivars in
the United States. Despite a large degree of annual variation, a 25% ozone
depletion results in up to a 20%-25% reduction in-overall yield. Years with
little apparent UV effectiveness (1983 and 1984) were generally hot and dry
with plants experiencing prolonged drought. By knowing the pattern of
precipitation, temperature, and degree of cloud cover during the growing
season, one can predict with a high degree of confidence what the effects of
supplemental UV will be on soybean yields (Figure 1). The diagonal line
represents a perfect match between predicted and actual yield. The bolder,
jagged line represents our model prediction. In addition to reducing the
actual weight of the harvest, UV radiation also generally reduces the overall
quality of the soybean harvest by reducing its protein and oil content (Table
*0; however, we currently know very little about the mechanism of this
phenomenon.
257
-------
Table 3. United States and World Crop Production
Crop
wheat
rice
corn
barley
soybeans
World
(million metric tons)
522
470
449
172
90
USA
71
6
195
13
51
% of
World Production
14
1
43
8
57
Source: Agricultural Statistics - USA, 1984; FAO Production Yearbook, 1984
18
16
3 14
1 12
^ 10
"O
S> 8
•D
0
£
6
4
2
0
0
Essex
6 8 10 12
Actual yield (g)
14 16 18
Figure 1. Bold, jagged line represents how closely a model regressi°°
equation predicts actual yield. The model inputs include presentatio°»
temperature, and cloud cover data. The diagonal line represents the idea
situation where actual and predicted yields are equivalent.
258
-------
Table 4. Summary of UV Effects on Soybean Yield and Quality
Year % change in yield % change in seed quality
(protein) (oils)
1981
1982
1983
1984
-25
-23
+6
-7
-5
-4
0
0
-2
+ 1
-2
0
Source: Teramura (unpublished)
What does a 20/5-25/5 reduction in yield mean to global agriculture? For
Perspective, this UV-induced loss in yield is compared with other current
sources of crop loss in soybean in Figure 2. Losses due to weeds reduce
Soybean yields by 17#, diseases by 12-14?, mechanical harvesting by 10j5 and
insects by 3% (Metcalfe and Elkins 1980). Clearly, if the data presented on
^able 4 are universally applicable to all soybean grown in the United States
°r the world in general, the anticipated loss due to ozone depletion would be
Sweater than our current losses to any one of these factors. Should these
Experimentally based predictions be correct, we could anticipate a one-third
Eduction in our useable soybean harvest from 56% down to 36#. Additionally,
fchere is some evidence in the literature (Esser 1980; Cams, Grahm, and Ravity
^78) that under a greater UV environment, crop losses from weeds, diseases,
insects would be even larger due to the weakened state of the crop host.
losses in each category increased by 25%, then our useable soybean harvest
effectively be reduced by one-half (Figure 3).
Up until now, we have quite a depressing picture of what might happen to
°Ur soybean harvests; however, there is a brighter side. We know that a
tremendous range of UV sensitivity apparently exists among different crop
°uUivars. The U.S. Department of Agriculture currently has a collection of
fver 12,000 soybean lines and only a fraction of these have been screened for
Jv tolerance. Of the 45 cultivars that have been screened (Teramura and
"Urali 1986; Biggs, Kossuth, and Teramura 198,1), nearly one-third were quite
tolerant to even large UV doses. This implies that some degree of tolerance
*a already present in our modern soybean germplasm, and that the potential
e*ists for crop breeding as a means of helping to lessen or ameliorate the
^ticipated loss in yield due to ozone depletion. Unfortunately, we do not
K^OW enough about the bases for these cultivar differences in sensitivity to
e able to fully evaluate the likelihood of this possibility. For instance,
Jf UV tolerance were closely associated with inferior genes which might
ltlcrease drought susceptibility or lower yields, then any breeding program
w°Uld be of little help.
In conclusion, the 20% to 25% yield reductions reported for soybean in
paper are only preliminary estimates and may portray a worse-case
The data represent the response of only one out of the dozens of
259
-------
cultivars currently grown throughout the United States. However, in the
absence of similar detailed information for other key crops, these data serve
to warn us of the potential consequences of ozone depletion upon global agri-
culture. We can only hope that these data represent an extreme case and not
the general status of our global agriculture.
Disease
C12-14%3
'(10%)
Harvesting
(3%)
Figure 2. Current sources of soybean
crop losses in the United States in
relation to anticipated losses due to
a 25% ozone depletion.
Figure 3. Anticipated yield
losses due to a 25% ozone
depletion assuming that UV
produces a significant (25*' s
interaction with other source*
of yield reductions.
260
-------
REFERENCES
Biggs, R.H., and S.V. Kossuth. 1978. Effects of ultraviolet-B radiation
enhancement under field conditions on potatoes, tomatoes, corn, rice,
southern peas, peanuts, squash, mustard, and radish. UV-B Biological and
Climatic Effects Research (BACER), Final Report. Washington, D.C.:
Environmental Protection Agency.
Biggs, R.H., S.V. Kossuth, and A.H. Teramura. 1981. Response of 19 cultivars
of soybeans to ultraviolet-B irradiance. Physiol. Plant. 53:19-26.
Brandle, J.R., W.F. Campbell, W.B. Sisson, and M.M. Caldwell. 1977. Net
photosynthesis, electron transport capacity, and ultrastructure of Pisum
sativutn L. exposed to ultraviolet-B radiation. Plant. Physiol. 60:165-
169.
Cams, H.R., J.H. Grahm, and S.J. Ravitz. 1978. Effects of UV-B radiation on
selected leaf pathogenic fungi and on disease severity. EPA-IAG-D6-
0168. Washington, D.C.: BACER Program, EPA,
Dumpert, K., and J. Boscher. 1982. Response of different crop and vegetable
cultivars to UV-B irradiance: Preliminary results. In Biological
effects of UV-B radiation, ed. H. Bauer, M.M. Caldwell, M. Tevini, and
R.C. Worrest, 102-107. Munchen: Gesellschaft fur Strahlen-und Umwelt-
forschung mbH, ISBN 0721-1694. ISBN 0721-1694.
Esser, G. 1980. Einfluss einer nach Schadstoffimission vermehrten Einstrahlung
von UV-B-light auf Kulturpflanzen, 2. Versuchsjahr, Frankfurt: Bericht
Battelle Institut e.V.
Krizek, D.T. 1978. Differential sensitivity of two cultivars of cucumber
(Cucumis sativus L.) to increased UV-B irradiance: I. Dose-response
studies. Final Report EPA-IAG-D6-0168, USDA/EPA BACER Prog., Washington,
D.C.: Environmental Protection Agency.
Hetcalfe, D.S. and D.M. Elkins. 1980. Crop production. Principles and
practice. 4th ed. 456-460. New York: Macmillan Pub. Co., Inc. ISBN 0-
02-380710-5.
National Academy of Sciences. 1984. Causes and effects of changes in stratos-
pheric ozone; Update 1983. Washington D.C.: National Academy Press.
Sisson, W.B., and M.M. Caldwell. 1976. Photosynthesis, dark respiration, and
growth of Rumex patientia L. exposed to ultraviolet irradiance (280 to
315 nanometers) simulating a reduced atmospheric ozone column. Plant
Physiol. 581:563-568.
Teramura, A.H. 1982. The amelioration of UV-B effects'on productivity by
visible radiation. In The role of solar ultraviolet radiation in marine
ecosystems, ed. J. Calkins, 367-382. New York: 'Plenum Publ. Corp. ISBN
0-306-40909-7.
Teramura, A.H. 1983. Effects of ultraviolet-B radiation on the growth and
yield of crop plants. Physiol. Plant. 58:415-427.
261
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Teramura, A.H., R.H. Biggs, and S. Kossuth. 1980. Effects of ultraviolet-B
irradiances on soybean. II. Interaction between ultraviolet-B and
photosynthetically active radiation on net photosynthesis, dark
respiration, and transpiration. Plant Physiol. 65:483-488.
Teramura, A.M., and N.S. Murali. 1986. Intraspecific differences in growth
and yield of soybean exposed to ultraviolet-B radiation under greenhouse
and field conditions. Env. Exp. Bot. 26:89-95.
Tevini, M., and W. Iwanzik. 1982. The effects of UV-B irradiation on higher
plants. In The role of solar ultraviolet radiation in marine aQ03y3tg[g§»
ed. J. Calkins, 581-615. New York: Plenum Pub. Corp. ISBN 0-306-40909-
7.
Tevini, M., and W. Iwanzik. 1982. Untersuchugen uber den Einfluss erhohter
UV-B Strahlung auf Entwicklung, Zusammensetzung, Struktur und Funktio
von Pflanzen. Munchen: Bereich Projekttrager-schafterm, GSF.
Van, T.K., L.A. Garrard, and S.H. West. 1976. Effects of UV-B radiation °n
net photosynthesis of some crop plants. Crop Sci. 16:715-718.
Vietmeyer, N.D. 1986. Lesser-known plants of potential use in agriculture a
forestry. Science 232:1379-1384.
Vu, C.V., L.H. Allen, and L.A. Garrard. 1982. Effects of supplemental W'
radiation on primary photosynthetic carboxylating enzymes and,. 3°^t
proteins in leaves of C and C crop plants. Physiol. Plant. 55:11"1
262
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Inhibition of Photosynthetic Production in Plants
by Ultraviolet Radiation1
L O. Bjdri\ Janet F. Bornman, and Legasse Negash
University of Lund
Lund, Sweden
In this lecture we will try to explain some research findings concerning
the inhibition by ultraviolet radiation of photosynthetic production in
plants. Because of the abundant scientific literature on this topic we will
not attempt to cover all of it, but will concentrate on findings which (a) are
relevant to the ozone depletion problem and (b) are of general significance,
i.e., not relating to particular plants only. Furthermore, we will try to be
nontechnical and not assume a background in plant physiology or photobiol-
ogy. These are our aims, but the result of our attempt will necessarily be a
compromise, due to the short time available.
It is necessary first to say a few words about photosynthesis. The
process can be schematically written:
Water + carbon dioxide + light = organic matter + oxygen. Photosynthesis
takes place in the green parts of plants, mostly leaves, where the light for
the process is absorbed, mainly by the green pigment, chlorophyll. In land
plants (but not in aqueous plants) the carbon dioxide enters through micro-
scopic adjustable pores or valves called stomata (see Figure 1). The stomata
are adjusted by the plant for the best compromise between carbon dioxide
influx and water vapor loss.
The process: water + carbon dioxide + light = organic matter + oxygen,
is not completed in one step. There are, in fact, many chemical reactions
leading to chis net result. The process can be roughly divided into two
Parts:
• Photosynthetic electron transport and phosphorylation:
Water + light = oxygen + reducing power + phosphate energy
• Assimilation of carbon dioxide:
Carbon dioxide + reducing power + phosphate energy = organic matter.
263
-------
1
50pm
Figure 1. Light micrograph of stoma from broad bean (Vicia faba) leaf in
open condition (above, white light only), and stoma closed under the~action of
UV radiation. The photograph is from an experiment with excised epidermis.
264
-------
These main parts of the photosynthetic process take place in microscopic
green particles in the cells called chloroplasts (Figure 2). Photosynthetic
electron transport and phosphorylation take place in the chloroplasts in
membranes called thylakoids, where carbon dioxide is assimilated in the space
between these membranes, which is filled with a solution (stroma) of the
enzymes necessary to catalyze the reactions. The chloroplasts also contain
part of the cell's genetic material, DNA, and protein synthesizing system
(ribosomes).
Inhibition of photosynthesis by ultraviolet radiation has been estab-
lished and measured by several types of experiments. The first type are
short-term laboratory experiments in which isolated chloroplasts or thylakoids
are first exposed to ultraviolet radiation without simultaneous irradiation by
visible light. At the end of the ultraviolet radiation the sample is exposed
to visible light, so that the effect on the photosynthetic system can be
estimated. In such experiments it has been found that photosynthetic electron
transport is inhibited by ultraviolet radiation. The electron transport chain
is damaged at more than one point, and the points of damage have been approxi-
mately determined (see Bornman et al. 1984). In contrast to moderate photo-
inhibition caused by intense visible light, photoinhibition by UV-B radiation
is not rapidly reversed during subsequent dark incubation (Bornman 1986).
Before we proceed, we should be familiar with the concept of action
spectrum. An action spectrum is a function describing, or comparing, the
effectiveness (average effect per incident photon) of radiation of different
wavelength to effect a certain process, such as inactivation of the photosyn-
thetic system. One can think of this as a graph with a wavelength along the
horizontal axis and effectiveness, i.e., effect in relation to the intensity
and duration of the irradiation, along the vertical axis. Determining action
spectra is one of the most important means of characterizing photochemical
processes as it may provide information about the molecule absorbing the
effective radiation. In connection with the ozone depletion problem, action
spectra are important for computing the so-called radiation amplification
factor (see Figure 3), and for relating effects of artificial radiation
sources to those caused by solar radiation.
Practically all action spectra relating to deleterious effects of UV
radiation show a decline of effectiveness from low to high wavelengths, but
the slope varies, and there may be "bumps." Measurements in several labora-
tories using variations on the first type of experiments (Jones and Kok 1966;
Hirosawa and Miyachi 1983; Bornman, BJorn, and Akerlund 1984) have resulted in
action spectra with modest slopes (Figure 4). This means a low radiation
amplification factor, in marked contrast to spectra measured for inactivation
of the genetic system (DNA inactivation, Figure 5), which are very steep.
On the other hand, action spectra for inhibition have also been measured
with a second type of experiment, which has yielded different results. In
these experiments (Bogenrieder 1982; Caldwell et al. 1986) complete photo-
synthesis was measured for intact leaves or intact plants' with white light
impinging on the leaves simultaneously with the UV radiation. These spectra
(Figure 6) are steeper than the spectra obtained by the first method. These
latter studies are closer to a field situation and may be regarded as more
relevant to the ozone depletion problem. They indicate a higher radiation
amplification factor and therefore a greater risk. However, a scientist can
265
-------
Figure 2. Electron micrograph of part of a cell from a sugarbeet leaf,
showing chloroplast with stroma (s) and thylakoids (t). In some places the
thylakoids form grana (g). From Bornman et al. (1986).
Action spectrum A
Action spectrum B
Normal daylight
spectrum (C)
Daylight spectrum
after ozone depletion
CD)
WAVELENGTH
Figure 3. Diagram to illustrate the dependence of radiation amplifica-
tion factors on action spectra. The whole diagram is generated by a computer
program with a set of equations, and does not depict real experimental data.
One steep action spectrum (A) and one that is less steep (B) are shown (wave-
length on horizontal axis, effectiveness on vertical axis), as well as the
short wavelength tails of the normal daylight spectrum (C) and of daylight
after ozone depletion (D) (wavelength on horizontal axis, spectral irradiance
on vertical axis). The radiation amplification factor for action spectrum A
is the ratio between the area below the product curves AxD (stippled) and AxC
(black), in relation to the particular ozone depletion that has caused the
spectral change from C to D. In the hypothetical example shown, the radiation
ampl: 'ication factor is five times as great for action spectrum B.
266
-------
Ill
s
CO
(A
Ul
z
Ul
>
p
o
Uf
u.
u.
IU
o
K
250
275 3QO
WAVELENGTH, nm
325
Figure 4. Action spectrum for inhibition of photosynthetic electron
transport determined in isolated spinach chloroplasts (curve 1, Jones and Kok
1966), isolated spinach thylakoids (curve 2t Bornman et al. 1984) and isolated
cyanobacterial thylakoids (curve 3» Hirosawa and Miyachi 1983). Within the
UV-B region (280 to 320 nm) the effectiveness changes about twofold.
267
-------
a, • Relative dimer yield per quantum
—A Relative lethality per quantum
Relative mutaqenicity per quantum
Average DNA spectrum
(Setlow, 1974)
Xenon lamp
A, o Hg lines
(Tyrrell, 1973)
350 400
WAVELENGTH (nm)
Figure 5. Absorption spectrum for DNA, as well as action spectra for
various processes that depend on radiation damage to DNA. Note that the
vertical scale is logarithmic. Within the UV-B region the effectiveness
(action per quantum) changes about 10,000 fold. Cited from various sources by
Peak et al. (1984).
268
-------
UJ
(0
0)
111
z
UJ
o
UJ
u.
u.
Ul
o
I-
250
275 300
WAVELENGTH, nm
Figure 6. Action spectrum for inhibition of photbsynthetic carbon
dioxide fixation by intact plants: Laotuca sativa (triangles, Bogenrieder
1982), Rumex alpinus (circles, Bogenrieder 1982) and Rumex patientia (solid
line, Caldwell et al. 1986). The slopes are intermediate between the slopes
in Figures 3 and 4.
269
-------
hardly be content with such a statement. We wish neither to underestimate nor
overestimate the consequences of ozone depletion, and, to be on solid ground,
we must understand the reason for the discrepancy between the two sets of
results.
A first guess would be that it is not damage to photosynthetic electron
transport (measured in the first method), but damage to the enzymes necessary
for carbon dioxide assimilation that is important for inhibiting overall
photosynthesis (measured by the second method). Indeed, inactivation of some
proteins shows steeper action spectra, and UV-B has been shown to decrease the
activity of the carbon dioxide binding enzyme, ribulose bisphosphate
carboxylase/oxygenase (Vu, Allen, and Garrard 1982, 1984).
Nevertheless, there is another possibility that also explains the differ-
ent action spectra obtained, depending on whether white light is given simul-
taneously with the UV radiation or not. Although there are facts speaking not
only for, but also against the following interpretation, we think it is worth
presenting as an hypothesis; some background follows to explain it.
One of the components necessary for photosynthetic electron transport is
the so-called QB protein. This protein binds a quinone that transfers elec-
trons. It is a remarkable protein in many respects (see Arntzen and Pakrasi
1986 for a review). One feature that is important in our context is that it
has a very high turnover rate in light, i.e., it is rapidly broken down and
resynthesized. The rate of breakdown increases with light intensity; we may
regard 15 minutes as a typical lifetime for a molecule of QB proteintf It is
as if the protein molecules were worn out by working hard. If resynthesis is
prevented during irradiation with strong light, the photosynthetic system is
inactivated. When such a situation occurs, trees are exposed to strong light,
but temperature is still too low for efficient protein synthesis, e.g., in the
spring in Swedish conifers.
It could be that one important effect of UV radiation is to destroy the
chloroplast DMA, in which the blueprint for resynthesis of the QB is encoded,
thereby slowing down resynthesis and photosynthetic electron transport. If
this mechanism dominates inhibition of photosynthesis by UV, one would expect
action spectra measured with simultaneous irradiation by UV and visible light
to be steeper than those determined with sequential irradiations. This seems
to be supported in the results, although we do not have strictly comparable
data yet. There is also more direct evidence (Dohler, Biermann, and Zink
1986) that protein synthesis may be inhibited by UV-B radiation.
If the above interpretation is correct, we also have, in principle, a
recipe for producing more UV-resistant plants: We should introduce additional
copies of the gene encoding for the Qn protein (the correct designation is the
psbA gene) into the chloroplasts. This may be possible, but the recipe is, of
course, a bit naive. Other genes are inactivated as well. But all genes are
not equally critical. Genes that do their important Job in, for example, the
growth zones (the meristems) in root and shoot tips can be discounted, for
they are shielded and protected from UV.
270
-------
Plants vary widely in their tolerance, and many factors other than the
possibility just mentioned certainly contribute to this. Considerable dif-
ferences may exist between closely related species (Robberecht and. Caldwell
1986), or even between cultivars of the same species (Biggs, Kossuth, and
Teramura 1981). Differences already occur at the membrane level: we have
found for example that spinach thylakoids are more resistant than even intact
leaves of Elodea (Bjorn, Bornman, and Olsson 1986; Figure 7), At the organ
level different degrees of protection are offered by the outermost cell layer
of the leaf, the epidermis, which often contains substances that strongly
absorb ultraviolet radiation. The content of these shielding substances is
often adjusted to match the need. As an example, we (Bjorn and Bornman 1986)
have observed that the same Oxalis leaf is more sensitive to UV radiation
coming from below (where the plant "has no reason to expect" any UV) than to
UV impinging upon the upper side of the leaf (Figure 7). Caldwell et al.
(1982) have shown a correlation between UV tolerance and UV level in the
natural habitat, as well as between UV sensitivity and epidermal UV transmit-
tance. Wellman (1974) and Beggs, Schmeider-Ziebert, and Wellman (1986) have
reported the accumulation of UV absorbing flavonoids in response to UV expo-
sure, and have shown how widely various plants differ with regard to this
response.
It has also been repeatedly observed (e.g., Klein 1963; Teramura 1980)
that plant cell cultures and whole plants tolerate more UV radiation the more
they are simultaneously exposed to visible light. The nature of this protec-
tive action of visible light is not understood. Even if inhibition is due to
DMA damage, the so-called photoreactivating enzyme (which is known to carry
out a light dependent DNA repair in other cases) is probably not involved.
The photoreactivating enzyme repairs a type of damage (pyrimidine dimeriza-
tion) that is probably not the most important type of damage in the spectral
range of solar UV radiation (Peak et al. 1984). Hirosawa and Miyachi (1983)
studied inhibition by UV-A of photosynthetic electron transport in a cyano-
bacteriura and concluded that the reactivation achieved with subsequent visible
light is due to light absorption in the photosynthetic system. However, this
may be a phenomenon different from the protection from UV-B damage; it seems
that no one has studied the spectral dependence of this protective effect. It
is possible that plants become more resistant when they are grown in strong
white light because of long-term changes in their properties, especially in
the amounts of protecting pigments. Another possibility is that they can
repair damaged systems faster in strong light because they have more energy
available in this case as compared to weak light conditions.
The protective effect of visible light seems to be an argument against
the hypothesis that an important UV effect is the inhibition of resynthesis of
the QD protein, because the need for resynthesis would be greater the stronger
the visible light. However, only strong visible light given prior to the UV
irradiation has a protective effect (which thus can be described as an
acclimatization to strong sunlight), while strong visible light concomitant
with UV irradiation enhances UV inhibition (Warner and Caldwell 1983), as
would be expected from the hypothesis.
When considering UV effects on whole plant photosynthesis, one should
take into account not only direct effects upon the photosynthetic system, but
also indirect effects on photosynthesis. Inhibition of leaf area growth, for
271
-------
0.6
E 0.4
o
E
a
0.2
\ ELODEA
1
OXALIS
(ADAXIAL)
••••••••.
260
280
300
320
340
WAVELENGTH, nm
Figure 7. Action spectra for inhibition of electron transport (as
measured by the effect on fluorescence induction) in intact leaves of Elodea
denja and pxalis deppei. and isolated spinach thylakoids, all to the same
scale. Elodea leaves lack an epidermis, and the sensitivity is the same for
both sides. For Oxalis the sensitivity is much greater for UV radiation
impinging on the lower (abaxial) side than the upper (adaxial) side. From
Bjorn, Bornman, and Olsson (1986).
272
-------
instance, will lead to a lowered input of light energy, and thus to lowered
photosynthetic production. Dr. Hader (this volume) has described how UV
inhibition of the ability of free-swimming photosynthetic organisms to swim in
the proper direction can affect photosynthetic production. Another UV effect,
which has been studied in our laboratory (Negash and Bjorn 1986), is the
closing effect on stomata (Figure 1). Closing of stomata prevents carbon
dioxide from entering the plant, and thus inhibits photosynthesis. Also in
this case visible light counteracts the effect of UV (Figure 8). Our conclu-
sion as regards tef (Eragrostis tef, an important crop in Ethiopia, where UV
exposure is high) is that UV closure of stomata is not important under field
conditions as long as the water supply is adequate. This conclusion is based
on our laboratory experiments and on a computer program (Bjorn and Murphy
1985) for predicting daylight spectral UV irradiance under various
conditions. Teramura and Perry (1982) and Teramura et al. (1982, 1984) have
measured UV effects on stomata in soybeans, radishes, and cucumbers under
field conditions and found that these UV effects on stomata may have some
importance in certain plants under water stress conditions.
30O
c
o
o
200
o
c
m
S
100
o
flC
WL (450 pmol m $ '
60 120
Time, min
180
Figure 8. Stomatal resistance in control plants (tef, Eragrostis tef)
irradiated with white light (50 ymol m~^s"') only (triangles) and plants
simultaneously exposed to UV (285 nm, 2.4 y mol nf^s , circles). The UV,
exposure commenced at time 0. After 90 minutes white light fluence rate was
increased 9 fold. Stomata start to close when exposed to UV radiation, but
the closure is reversed by an increase in white light. Note that high resis-
tance values correspond to small stomatal aperture. The roots of the plants
were immersed in water. From Negash and Bjorn (1986).
273
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Jones, L.W., and B. Kok. 1966. Photoinhibition of chloroplast reactions. I.
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Negash, L., and L.O. Bjorn. 1986. Stomatal closure by ultraviolet
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irradiances on soybean. Plant Physiol. 65:483-88.
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Teramura, A.M., S. Salm, and M. Tevini 1982. The effects of UV-B irradiation
on leaf resistances in two crop species during mild water stress. In
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Vu, C.V., L.H. Allen, and L.A. Garrard. 1982. Effects of supplemental UV-B
radiation on primary photosynthetic carboxylating enzymes and soluble
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Vu, C.V., L.H. Allen, and L.A. Garrard. 1984. Effects of enhanced UV-B radia-
tion (280-320 nm) on ribulose-1, 5-bisphosphate carboxylase in pea and
soybean. Environ. Exp. Bot. 24:131-43.
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schung, mbH, Munchen.
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276
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MISCELLANEOUS
-------
An Assessment of UV-B Radiation Effects on Polymer
Materials: A Technical and Economic Study
Anthony L Andrady
Research Triangle Institute
Research Triangle Park, North Carolina USA
Robert L Horst, Jr.
Mathtech, Inc.
Princeton, New JerseYUSA
INTRODUCTION
In March 1986, the U.S. Environmental Protection Agency sponsored a
workshop to review the results of several analyses that predicted inpreases in
future emissions of chlorofluorocarbons (CFCs) and possible depletion of
stratospheric ozone. One direct result of ozone depletion would be an
increase in the level of UV-B radiation reaching the earth's surface. In
turn, the increase in UV-B radiation would lead to accelerated damage in
several effects categories, including polymer materials. This paper addresses
both technical and economic issues related to damage to plastics brought about
by hypothesized increases in UV-B radiation.
Plastics are increasingly used outdoors where they are routinely exposed
to sunlight. Exposure to light of certain wavelengths results in a variety of
chemical reactions in most commonly used plastics, leading to increased
deterioration of useful physical and mechanical properties and therefore
shortening the useful lifetime of the plastic. The most potent region of the
solar spectrum in this regard is the UV-B region. The longer wavelength
ultraviolet light (UV-A) may also contribute to the degradation of plastics
exposed to light. The shorter wavelength (<300 nm) ultraviolet radiation, if
it were present in sunlight to any significant extent, would result in rapid,
extensive degradation of polymeric material.
On a volume basis only a few classes of plastics are used outdoors or in
situations where they are exposed to diffused and reflected sunlight
(Anonymous 1986). These are shown in Table 1 with some examples of typical
products. Polyvinylchloride (PVC) is Jthe most widely used plastic in the
residential building industry. It is used in siding, window frames, rainwater
1 Protecting the Ozone Layer: Workshop on Demand and Control Technologies,
Workshop Sponsored by the U.S. Environmental Protection Agency.
279
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goods, pipes, and flexible sheeting. Polyolefins, reinforced polyesters,
acrylics, and polycarbonates are also used outdoors in significant quantities.
The same polymer is often compounded differently to yield materials best
suited for specific applications. The various additives (fillers, plasti-
cizers, heat stabilizers, lubricants) used in the compound constitute a signi-
ficant fraction of the final plastic product and heavily influence its photo-
susceptibility. Thus the light-sensitivity and the nature of damage suffered
by plastics exposed to light are determined not only by the type of polymer
but also by the compound composition (Weiler 1984; Ho 1984).
Table 1. Plastics Used Outdoors
Plastic Class
Typical Use
1. Polyvinylchloride rigid
[PVC]
2. Polyvinylchloride
plasticized [PVC]
3. Polyolefins [PE/PP]
(polyethylene, poly-
propylene )
4. Polyester (thermoset)
[UPE]
5. Polycarbonates [PC]
Siding, window frame, pipes, and
conduits
Roofing membrane, wire/cable
coating, hose
Packaging, agricultural film,
stadium and outdoor furniture
Panels/siding, tanks and pipes,
glazing
Glazing
A given polymer product used outdoors may suffer damages or undesirable
changes in its properties. The rate at which such damage occurs is determined
by the kinetics of the reactions responsible for the change. Consequently, it
is possible to identify a sequence of progressive damage events where several
desirable characteristics are in turn deteriorated below acceptable levels.
The most rapidly occurring damage determines the lifetime of the product, and
is termed the "critical mode of damage" (CMD). Table 2 gives the CMD of
several important classes of polymers used outdoors under current spectral and
climatological conditions.
Polyvinylchloride compounded specifically for siding or window frames
illustrates the effects of UV-B radiation on polymers used outdoors. The
choice of PVC for the purpose of illustration is appropriate because it is
used in building applications more than any other plastic and because of the
280
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Table 2. Modes of Damage Experienced by Polymers Used Outdoors
Polymer
Application
Damage
PVC
(a) siding, window frames
UPE
PE/PP
PC
(b) roofing materials
outdoor surfaces
paneling
irrigation pipe,
outdoor furniture
synthetic turf, stadium
seats, packaging
glazing material
[yellowing]
+ chalking
- impact properties
- tensile properties
•+• surface distortion
[+ brittleness]
[+ discoloration]
[+ surface erosion]
+ discoloration
- strength
[+ brittleness]
- tensile properties
- electrical properties
[ + yellowing]
- transparency
+ = increase
- = decrease
[] = Brackets indicate critical mode of damage (CMD)
availability of at least a limited amount of relevant research data on the
polymer. A typical rigid PVC composition for outdoor use is stabilized solely
by W% to 13* parts by weight of titanium dioxide pigment (Titow, 1984). The
pigment particles shield the plastic matrix below it from light-induced degra-
dation. On exposure to light, the rigid PVC, originally white in color,
suffers both yellowing and partial photobleaching. The subsequent uneven
discoloration is the critical mode damage for rigid PVC in applications such
as siding and window frames.
In the next section we review technical issues that arise in an analysis
of the effects of increased UV light on plastics. The principal output of the
technical analyses is a damage equation which relates a measure of the CMD to
the amount of titanium dioxide stabilizer used in the PVC resin compound. We
then integrate this damage equation into a supply and demand analysis of the
PVC market to obtain estimates of the potential economic damage that would
result from the hypothesized depletion in ozone. We summarize our conclusions
in the final section.
281
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EFFECT OF INCREASED UV LIGHT ON PLASTICS USED OUTDOORS2
CIAP Approach
The Climatic Impact Assessment Program (CIAP) (Shultz, Gordon, and
Hawkins 1975) study employed the Beer-Lambert equation to calculate approxi-
mate increases in UV-absorbing stabilizers required to offset the effects of
increased UV light. While the approach is sound and simple to use, its appli-
cability is limited to the transparent, homogeneous polymers. With the excep-
tion of window glazing, polymers used outdoors are generally opaque and are
often stabilized using light screeners. Therefore, a parallel model based on
light-screening stabilization, applicable to opaque materials, was developed
in the course of the study.
Both equations require the use of an empirical constant that depends on
polymer and stabilizer for its use. The equations developed for each model
are shown in Table 3.
Table 3. Models for Prediction of Stabilizer Requirements
Transparent Polymeric Materials
CIAP equation based on Beer
Lambert Law
Opaque Polymeric Materials
Equation derived in present
study
UV-absorption is the main mode
of stabilization
Log (fy/I0) = cC-t
C = concentration of absorber
e = extinction coefficient
x = factor increase in light
intensity
y = factor increase in stabilizer
concentration to offset the
effects of increased light.
Log x = (y-1)-eC/
Requires (eCj£) for predictive
use
UV-screening is the main mode
of stabilization
Log (l£/I0) = //2r3 log(1-3V/2)
V = Volume fract-ion of screener
rj = area-average radius of
screen particle
Log x - //2r3{(1-3V/2)/(1-3Vy/2»
Requires
use
for predictive
A more detailed description of the technical analysis is available in
Andrady, A.L. 1986. An analysis of technical issues related to the effect
of UV-B on polymers. Draft report submitted to the U.S. Environmental
Protection Agency.
282
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Both approaches suffer from the same drawbacks. First, they do not take
into account the spectral sensitivity of the degradation process (i.e., the
action spectra). Second, they do not take into account the dose-response
relationship for photo-induced deterioration. Finally, they do not take into
account the possible nonlinearity of effectiveness of stabilizers at dif-
ferent concentrations. In spite of these serious shortcomings, the method
yields approximate estimates of the increased stabilizer requirements at a
given increased light level.
Comprehensive Approach
The extent (and even the nature) of damage suffered by a polymer exposed
to sunlight depends on wavelength. Since any possible deterioration of the
ozone layer will cause significant changes in the spectral distribution of
sunlight, both the altered sunlight spectrum and the action spectrum for a
given mode of damage is required to estimate the effect of ozone depletion on
material deterioration. The terrestrial solar spectrum has an irradiance
H(x) and is altered by a function A(x) caused by ozone depletion. The
altered spectrum H(X)A(X) weighted by the appropriate action spectrum
F(x) will yield an estimate of the damage at the wavelength X. Provided that
the damage is additive and is a linear function of available light energy, the
following integral gives the total damage (Cutchis 1984).
Total damage D = J* H(X)A(x)F(X) dx
n
The integral might be evaluated numerically with A(X) = 1 to represent
current baseline conditions. Using the absorption spectrum of ozone, A(X) at
various levels of ozone depletion might be obtained. However, the lack of a
suitable action spectrum (i.e., one relating to properly compounded PVC
containing appropriate quantities of titanium dioxide) limits the usefulness
of the approach. The only action spectra available in the literature relate
to transparent PVC films and to types of damage other than yellowing.
However, a very approximate estimate might be made using the action spectra
for polyene formation based on Reinische, Gloria, and Wilson (1966).
Yellowing in PVC is a direct result of the generation of long polyene
sequences. The ratio of integral D1 calculated for a given level of ozone
depletion to that at zero ozone depletion, D, is a measure of the expected
increase in damage. Typical values are shown in Table 4.
The question of how much stabilizer should be used to counter the
increased yellowing damage is more difficult to estimate. The main difficulty
is that the data on stabilizer efficiency with respect to unaltered sunlight
conditions cannot be reliably extrapolated to stabilization under high UV
light conditions. Stabilizer effectiveness of titanium dioxide in rigid PVC
was reported by Summers (1983) for weathering under Arizona conditions.
Assuming that the dependence of stabilization effectiveness on the pigment
concentration as reported by Summers is applicable under high UV conditions,
approximate ranges for increased pigment levels required to maintain the
light-resistance of PVC might be calculated. The data on yellowing damage at
the various pigment levels reported are consistent with the following
relationship.
283
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Table 4. Estimated Ranges of Factor Increase in Damage and the
Factor Increase in Stabilizer Needed to Counter the
Change for Yellowing of Rigid PVC Compositions
Zenith Angle 30° Zenith Angle 60°
Percent Loss
of Ozone
D'/D S'/S D'/D S'/S
0-5 '1.01 1.01-1.02 1.01-1.02 1.01-1
5-10 1.01-1.02 1.01-1.05 1.03-1.04- 1.03-1
10-20 1.02-1.05 1.03-1.11 1.04-1.09 1.05-1
20-30 1.03-1-08 1.03-1.18 1.07-1.18 1.08-1
.05
.09
.20
.38
Note: D'/D = factor increase in damage
S'/S = factor increase in titanium dioxide stabilizer
Zenith angles selected to reflect North American locations.
Log [Damage] = -[pigment] k + a
Since acceptable levels of damage (D*) obtained at the current use levels
of pigment (S*) are known, the factor increase in pigment (S'/S*)
corresponding to a given factor increase in damage (D'/D*) can be calculated
using known values of k. The results are shown in Table 4.
The estimates could be improved considerably by using action spectra,
dose-response information, and stabilizer effectiveness information for the
particular polymer/pigment system of interest. Efforts to obtain some of the
relevant data are currently underway.
The use of increased amounts of titanium dioxide pigment poses several
difficulties. These include increased melt viscosity and therefore higher
power consumption, increased wear and tear on machinery, increased compounding
of ingredients to maintain processibility and the other mechanical properties
of material, and possible increased susceptibility to oxidation. Thus,
increasing the levels of titanium dioxide is a limited solution which will not
necessarily be cost-effective beyond a certain level of increased UV light.
284
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ECONOMIC DAMAGES TO PVC PRODUCTS3
Methodology
Economic benefits are generated whenever a transaction such as the sale
of a good or service takes place. Economists generally agree that any attempt
to measure these benefits should be based on an individual's own valuation of
the transaction, demonstrated by their "willingness-to-pay11 to engage in the
transaction (Just, Hueth, and Schmitz 1982). Willingness-to-pay can be
inferred from the market demand curve. In particular, since the marginal
purchaser (i.e., the purchaser who would not buy if the price were any higher)
is by definition willing to pay exactly the price he pays and no more, the
area beneath the demand curve up to a given quantity can be shown to be the
appropriate measure of total willingness-to-pay. This situation is
illustrated in Figure 1, where total willingness-to-pay is given by area
abcqQo.
In benefit-cost analysis willingness-to-pay is frequently the measured
net of any charges paid by consumers for the good or service. When this is
done, the result is called net willingness-to-pay, or more often, consumers'
surplus. The consumers' surplus measure represents what consumers would be
willing to pay over and above what they do pay. In Figure 1, if price is po,
consumer surplus is given by the triangular area acp0.
Any action or event that leads to a change in market demand or supply
will change the surplus measure. In Figure 1, if market price increases to p1
as a result of a depletion in stratospheric ozone, consumers,' surplus will be
reduced by the area pibcpp. This is the measure of welfare change reported in
this case study. To be precise, we measure the willingness-to-pay by
individuals to remain in the initial situation (with price p0) and to avoid
the increased costs associated with ozone depletion. These costs, if not
avoided, represent a real economic loss to society since the costs limit other
productive opportunities in the economy.
In the next two subsections we discuss the data and methods used to
estimate demand and supply curves for PVC products used in building and
construction. We then compute economic damages under the assumption that the
producers of the PVC products will alter the resin formulation as UV-B levels
increase to maintain product lifetime and quality. This change in the resin
compound increases production costs and is the source of the measured surplus
change. We note that the measured damages do not include the increased costs
associated with early maintenance or replacement of in-place stock.
Description of the economic analysis is available in Horst, R.L., et al.
1986. The Economic Impact of Increased UV-B Radiation on Polymer
Materials: A Case Study of rigid PVC. Report in preparation for the U.S.
Environmental Protection Agency.
285
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Price
per Unit
Long-Run Supply
(with ozone depletion)
Long-Run Supply
(without ozone depletion)
Quantity per
Unit of Time
Figure 1. Aggregate Demand and Supply in the Market for PVC Products.
Aggregate Demand
A demand equation for PVC used in construction is estimated using annual
data for 1970 to 1983. The demand for PVC is a derived demand; that is, it is
derived from a more general demand for construction activity. The explanatory
variables included in the equation are the price of PVC, wood, and fabricated
metal products, and the value of construction put in place.
The results of a two-stage least squares regression analysis are shown in
Table 5. The explanatory variables are statistically different from zero at
standard levels of significance. The signs of the coefficients agree with a
priori expectations. Since the specification is double-logarithmic, the
coefficients are interpreted as elasticities. Thus, the own-price elasticity
of demand for PVC is -1.95. This is elastic, which would be expected for a
product with good substitutes.
The equation shown in Table 5 represents current preferences. However,
the case study requires that welfare impacts be evaluated to the year 2075.
Consequently, PVC consumption must be forecast over time. The approach used
to obtain future values of PVC consumption is based on the assumption that the
286
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Table 5. Derived Demand for PVC Used in Building and Construction*
Variable**
Intercept
LPVCHAT
LPMET
LPVOOD
LCON
Parameter
Estimate
-5.396
-1 .956
2.288
0.740
1.343
Standard
Error
4.
0.
0.
0.
0.
160
316
423
367
635
t-Statistic
-1 .297
-6.190
5.406
2.018
2.115
Observations: 14
Dependent Variable: LQPVC
Adjusted R2: 0.9573
Durbin-Watson D: 1.872
F-Statistic: 73.817
* The equation is estimated using the REG procedure in the SAS software
package.
** Variable names are: LPVCHAT is the fitted value of the natural log of PVC
price; LPMET is the natural log of the price of fabricated metal products;
LPWOOD is the natural log of the price of soft lumber products; LCON is
the natural log of the index of construction activity; and LQPVC is the
natural log of the quantity of PVC used in building and construction.
287
-------
demand curve estimated with historical data also represents future
preferences. Therefore, given forecasts for each of the independent variables
in the demand equation, a forecast of the dependent variable (PVC) can be
made. Forecasts of each independent variable in a future year are 'estimated
using a combination of time trend models and autoregressive models (Pindyck
and Rubinfeld 1976). Table 6 reports the 50% prediction interval for PVC
demand in selected future years. For the mid-range forecast, the projections
are consistent with about a 2% annual rate of growth in PVC demand.
Aggregate Supply
The supply side of the market for PVC products used in building and
construction is determined through a model plant analysis. Representative
plants are constructed for each of the three PVC products considered in the
case study: pipe and conduit, siding, and window profiles. Data for the
model plant analysis were obtained from the literature and through conversa-
tions with PVC fabricators, PVC compounders, PVC resin producers, and extruder
manufacturers (Perry 1977).
The data collected for the model plant analysis reflect operating charac-
teristics for a single level of output. If a supply curve for the PVC market
is to be estimated econometrically, a significant amount of other data is
required. For example, resource costs, administrative costs, and production
methods may be expected to change as output levels vary. Unfortunately, there
is insufficient data available in published statistics to develop the detailed
information that would permit a formal econometric analysis of production
costs. Furthermore, it is unlikely that an econometric analysis would be able
to pick up any variations in production costs caused by variations in the
amount of titanium dioxide used in the resin compound.
As an alternative to the econometric approach, we used a less formal
method. For each of the model plants we assumed that the market for PVC
products used in building and construction is perfectly competitive and that
the output level associated with model plant operation is consistent with the
economic conditions for profit maximization. We also assumed that each firm
(model plant) is in long-run equilibrium, which implies that equilibrium price
and quantity are associated with the minimum of the firms' long-run average
cost curves. Finally, we assumed that the industry for each of the three PVC
products is characterized by constant costs. This assumption implies that the
long-run supply curve for each industry will be horizontal. In turn, under
these conditions, price equals long-run average cost and also equals long-run
marginal cost. Consequently, the supply curve for the PVC products market can
be determined from knowledge of total production costs and output, which is
the information provided by the model plant analysis.
The average costs ($/lb) of production (inclusive of normal profit) are
estimated to be $0.52, $0.75, and $1.02 for pipe, siding, and profiles,
respectively. An aggregate price index for these three products is calcu-
lated as a weighted average of each market price. The weights are based on
the volume of output in each market. The price index is $0.604 and is nomi-
nally representative of market conditions in 1984. As the production
processes change to offset the damage caused by increased UV-B radiation, the
288
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Table 6. Fifty Percent Prediction Interval for PVC Demand
(millions of pounds)
Year
1980
2000
2025
2050
2075
Lower
Estimate
2,440
3,874
6,071
8,910
Point
Estimate
2,198
3,397
6,316
11 ,303
18,563
Upper
Estimate
4,729
10,298
21 ,048
38,671
average cost of production will increase. This increase will lead to a
corresponding increase in the aggregate price index for the PVC products and
is the source of the economic damages estimated for the case study.
Economic Damage Calculations
A hypothesis of the case study is that producers of the PVC products will
change the amount of titanium dioxide in the resin compound to maintain the
and lifetime and quality of their products. The change in compound formula-
tion will affect production costs in several ways. First, resource costs will
be increased as more titanium dioxide is used per pound of plastic produced.
In addition, it is believed that the change in the formulation will require
more energy to produce and will lead to more frequent replacement of screws
and barrels. For the three model plants developed for the case study, an
estimated 25% increase in titanium dioxide concentrations in the compound are
expected to lead to price increases of 2.67/1, 1.67?, and 1.73/t for siding,
profiles, and pipe, respectively. The aggregate price index increases by
1.86?. Since a 25% increase in titanium dioxide is believed to be the maximum
increase that could be tolerated without adversely affecting other attributes
of the PVC products, the 1.86? price increase is the maximum price effect that
would be observed.
Table 4, shown earlier, describes the relationship between physical
damage to PVC products and ozone depletion. Table 7 shows the scenario for
ozone depletion assumed for this study. For a given level of ozone depletion,
the factor increase in titanium dioxide stabilizer is computed by linear
interpolation. The cost increase associated with the interpolated estimate of
titanium dioxide concentration is proportional to the cost increase computed
for the model plant analysis.
289
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Table 7. Ozone Depletion Estimates
Year
1985
1995
2005
2015
2025
2035
2045
2055
2065
2075
Ozone Depletion
(percent)
0.00
0.15
0.62
1.50
2.84
4.66
7.08
10.41
15-44
26.08
Source: EPA estimates.
Forecast values of the price index of PVC products used in building and
construction are computed for each year s from the equation:
P1s = r1s(1 * C1s>Pls * r2s<1 + C2s)(p1a(p2o/Pio» +
r3s(1 + C3s> (Pls(P30 / P10»
where Pig is an aggregate price index for PVC at time s, with ozone
depletion
pig is the price of the ith PVC product at time s
C*s is the percent increase in costs for product i associated
with a given level of ozone depletion in year s.
rig is the ratio of output in year s for the ith good to total
output for PVC in building and construction.
The calculation of future PVC prices with ozone depletion requires
several assumptions. First, we assumed that the mix of PVC products is not
affected by ozone depletion. Second, we assumed that the relative prices of
the three PVC products remain unchanged over time. Third, we assumed that
each firm produces the same level of output in each year. This last assump-
tion implies that increases in PVC consumption over time are met by increases
in the number of firms in the industry.
The change in economic welfare associated with ozone depletion is
computed as the area under the aggregate demand curve between prices PQ and
P^. For the double-logarithmic demand curve, this can be written as:
290
-------
r 0 b1
Aw = A J P dP
s s J P
1
where Ag is a terra involving all arguments of the demand curve except the
price or PVC and its coefficient. AS varies over time, since each of the
explanatory variables in the demand equation varies over time.
Table 8 summarizes the discounted value of damage with several discount
rates. The discounted present value calculation is a convenient way to
express values that occur over many time periods. The discounted present
value, as of the current year, is defined as follows:
DPV = z
i = 0
where
is the welfare change in year i, and r is the discount rate.
Table 8. PVC Damage Associated with Ozone Depletion
(Discounted Present Value in Millions of 1984 Dollars)
Low estimate of
Middle estimate
High estimate of
PVC consumption
of PVC consumption
PVC consumption
0
$2,4-40
4,716
9,158
Discount
2
$ 603
1 ,137
2,159
Rate (*)
5
$ 97
174
315
10
$10
17
27
The choice of an appropriate discount rate is especially difficult
because of the extended time horizon for this analysis. If a real rate of 10*
is assumed, the preferences of future generations (those actually affected by
the ozone depletion) are assigned little importance. On the other hand, a
discount rate of 0* implies that the preferences of future generations are to
be given the same weight as the preferences of the current generation. The
literature provides no clear-cut answer to this dilemma (Lind 1982). There-
fore, present values are presented for several discount rates.
291
-------
The results shown in Table 8 apply to the following set of circumstances:
• All estimates are reported in millions of 1984 dollars
• The factor increase in titanium dioxide concentrations is computed for
a zenith angle of 60°
• Firms do not respond to the hypothesized decreases in stratospheric
ozone until 10 years after the impact is observed.
Additional research is planned to assess the sensitivity of the results
reported in Table 7 to alternative assumptions.
CONCLUSIONS
The conclusions of this case study of PVC damage related to increased UV-
B radiation can be summarized as follows:
• An approximate damage function can be developed which relates changes
ozone to changes in stabilizer required to maintain product lifetimes
at present levels.
• The damage function can be improved by using action spectra, dose-
response information, and stabilizer effectiveness information for the
polymer/pigment system of interest.
• For a given scenario of ozone depletion, it is estimated that undis-
counted, cumulative economic damages are $4.7 billion in 1984 dollars.
• A 50% prediction interval, which accounts for only a portion of the
uncertainty present in the analysis, indicates that the undiscounted,
accumulated economic damages could range from $2.4 billion to $9.2
billion.
REFERENCES
Andrady, A.L. 1986. An Analysis of Technical Issues Related to the Effect of
UV-B on Polymers. Draft report submitted to the U.S. Environmental
Protection Agency.
Anonymous. 1986. Modern Plastics. 63(1):69.
Ho, B.Y.K. 1984. J. Vinyl Technol. 6(4):162.
Horst, R.L., et al. 1986. The Economic Impact of Increased UV-B Radiation on
Polymer Materials; A Case Study of Rigid PVC. Report in preparation for
the U.S. Environmental Protection Agency.
Just, R.E., D.L. Hueth, and A. Schmitz. 1982. Applied Welfare Economics and
Public Policy. Englewood Cliffs, New Jersey: Prentice Hall, Inc.
292
-------
Lind, R.C., et al. 1982. Discounting for Time and Risk in Energy Policy.
Washington, DC: Resources for the Future.
Perry, N.L. 1977. General principles of plant operation: Operating a plant
for profit. In Encyclopedia of PVC. Volume 3-, ed. L.I. Mass. New
York: Marcell Dekker, Inc.
Pindyck, R.S., and D.L. Rubinfeld. 1976 Econometric Models and Economic
Forecasts. New York: McGraw Hill.
Reinisch R.F., H.R. Gloria, and D.E. Wilson. 1966. ACS Polymer Preprints.
7(1):372.
Shultz, A.R., D.A. Gordon, and W.L. Hawkins. 1975. CIAP Monograph 6, 3-239.
Cutchis, P. April 1984. Science.
Summers J. 1983. J. Vinyl Technol. 5(2):43.
Titow, W.V. 1984. PVC Technology. New York: Elsevier Applied Science Pub-.
lishers.
Weiler, R.G. 1984. J. Vinyl Technol. 6(4):152.
293
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The Interaction of Photochemical Processes
in the Stratosphere and Troposphere
Gary Z. Whitten and Michael W. Gery
Systems Applications, Inc.
San Rafael, California USA
Recent evidence of a dramatic decrease in stratospheric ozone levels
(Farman, Gardiner, and Shanklin 1985), which may be related to the continued
use of halocarbons (Cicerone, Walters, and Liu 1983; Craig and Chow 1982) and
an increase in methane (Craig and Chow 1982) and ^0 (Weiss 1981) emissions,
could forebode a concurrent increase in the transmission of solar ultraviolet
radiation to the troposphere. In combination with a general warming of the
lower atmosphere through the effect of greenhouse gases and other climatic
perturbations (Wang et al. 1986), a greater transmission of ultraviolet radia-
tion will augment the principal energy sources of photochemical reactions in
the troposphere and may also lead to an increase in the incidence of skin
cancer. To date, the enhancement of specific chemical reaction rates has
largely been ignored in tropospheric modeling studies. In this paper, we
describe an investigation of the effect of changes in tropospheric temperature
and the transmission qualities of the upper atmosphere on incident radiant
energy using data obtained from atmospheric and laboratory measurements to
estimate future conditions and corresponding changes in tropospheric photo-
chemistry .
Because ozone has a strong ultraviolet absorption band that extends to
approximately 3^0 nm (Inn and Tanaka 1953), the presence of ozone in the upper
atmosphere limits the transmission of ultraviolet radiation to the earth's
surface. A reduction in stratospheric ozone would, therefore, allow more
radiation to penetrate into the troposphere, primarily in the wavelength
region between 290 and 320 nm (Bahe et al. 1979). An increase in radiation
within this region will enhance the photolysis rates of important tropospheric
photochemical reactions, most significantly, the radical-forming photolytic
reactions of ozone, formaldehyde, and other aldehydes (National Aeronautics
and Space Administration 1985). The free radicals from these reactions
initiate and propogate oxidation of organic compounds and result in continued
radical production. Such radical chain reactions tend to promote the forma-
tion of photochemical smog (Whitten n.d.) and produce the oxidized species
critical to the formation of acidic precipitation (Calvert et al. 1985).
295
-------
The photolysis of ozone to oxygen molecules and 0(^D) atoms has been
shown to be energetically feasible below 310 nm and inversely dependent on the
density of the atmospheric ozone column (Bahe et al. 1983). This photolytic
process is very important in the troposphere because the rapid reaction of
0( D) with water is a primary source of tropospheric hydroxyl radicals during
daylight hours (Crutzen and Fishman 1977). These radicals react rapidly with
virtually all gaseous species in the atmosphere (Logan et al. n.d.). The J
values for photolytic processes (the apparent first-order rate constants) are
defined as J = / o I dX, where (for ozone photolysis to 0('D)).
A A A
o = the ozone absorption cross-section (Bass 1985)
A
<|> = the quantum yield of the 0(1D) formation process (National
Aeronautics and Space Administration 1985)
I = the surface solar irradiance.
A
This integral is evaluated over all wavelength intervals for which the
product o<|>I is nonzero. When plotted for all significant wavelengths of a
given spectral distribution, the resulting curve is known as the photoaction
spectrum, and the area under the curve represents the J value for those condi-
tions. Figure 1 shows the photoaction spectrum for ozone-to-0(^D) photolysis
derived from the surface solar data (collected at 300 Dobson1) of Bahe et al.
(1983). Also shown is the photoaction curve at 200 Dobson, which was extra-
plated from the measured 300 Dobson solar data using lower resolution,
computer-generated 200 Dobson data. The difference in area under the photo-
action spectra occurs primarily on the shorter wavelength side because with a
200 Dobson ozone column, additional light is available in this photolytically
more efficient region. The difference in rate constants calculated by inte-
gration of the two curves is nearly a factor of two greater at 200 Dobson over
the entire range of solar zenith angles.
Formaldehyde is also an important species in tropospheric chemistry
because it is eventually an oxidation product of almost all organic gases.
The most significant chemical reaction is the photolysis of formaldehyde to
radical products. J values similar to those for ozone were calculated using
the formaldehyde absorption cross sections of the U.S. National Bureau of
Standards (Bass 1985) and the quantum yield data summarized by Baulch et al.
(1984). These data indicate that 200 Dobson J values should increase by about
20% over the 300 Dobson values for the range of possible zenith angles. The
current quantum yield data for both formaldehyde and ozone photolysis appear
to produce a smooth curve. However, these data do not have the necessary
spectral resolution or accuracy to verify such as assumption. In addition,
few high-resolution surface solar spectra exist, and those that do are poorly
defined with respect to ozone column density and solar elevation. This lack
of resolution limits the precision of the J value calculations and indicates
an important area for future research.
The Dobson unit of measure is the height (in 10 cubic centimeters) that all
ozone molecules above the earth's surface would attain if all those
molecules existed as pure ozone at standard temperature and pressure.
296
-------
0)
°*J
a
-------
The changes in ultraviolet radiation that could result from stratospheric
ozone depletion are unique because they involve specific increases in the
short wavelength region of the surface solar spectrum only. Therefore, such
changes will cause significant increases in the photolysis rates of only the
few species that absorb in the enhanced region, e.g., the radical-forming
photolysis reactions of formaldehyde and ozone. Because these reactions are
major sources of new gas-phase radicals, the selective increases in those
rates will increase the flux in the free radical reaction cycles, resulting in
more reactive photochemical conditions in both the free troposphere and the
planetary boundary layer. Because hydroxyl radicals provide the dominant sink
for a variety of atmospheric compounds (including CO, CFty, CoHg, CHqCl,
C4qCClo, ChoBr, I^S, and SOg) (Logan et al. n.d.), accurate estimation of
hyaroxyl radical concentrations is essential to the study of future chemical
balance and climatic conditions. Although increased levels of CO and Cfty will
act to suppress hydroxyl radical formation, enhanced photolytic production
combined with potentially higher levels of ozone, will counteract this effect.
An increased hydroxyl radical production rate may also diminish the
concentrations of some species responsible for stratospheric ozone depletion,
thereby providing a feedback mechanism analogous to chemical buffering.
However, the magnitude of such a contribution from increased formaldehyde
photolysis is uncertain because the formaldehyde mixing ratio is not as
clearly defined as that of ozone. Figure 2 illustrates the formaldehyde
absorption cross section and surface solar spectrum for the region in which
the photoaction spectrum shows significant formation of radical products from
formaldehyde photolysis. A correspondence exists between the absorption peaks
of formaldehyde and the depressions in measured surface solar irradiance.
This correspondence indicates that bin sizes on the order of 0.25 to 0.50 nm
may be required to accurately determine formaldehyde J values near the
surface. Formaldehyde in the free troposphere could add to this requirement
by additional modification of the surface irradiance within the corresponding
bands. This phenomenon should be verified with additional high-resolution
surface solar data.
The effects of projected spectral changes on near-surface photochemistry
will vary depending on the characteristics of each airshed. Airsheds affected
by urban emissions have been extensively studied because such emissions signi-
ficantly increase their concentrations and types of trace gases and their
potential for photochemical smog formation. Since the pioneering work of
Haagen-Smit (1952), scientists have known that the oxidizing potential of such
air masses depends primarily on the concentrations of nitrogen oxides (NOX)
and organic hydrocarbons, as well as on the amount of radiant energy. The
impact of variations in ozone column densities and surface temperatures on the
chemistry of near-surface air masses can be examined through the use of atmos-
pheric simulation models. Because the chemistry of urban smog formation has
The urban simulation model used in this work is the OZIPP trajectory model
developed for the U.S. Environmental Protection Agency (Hogo and Whitten
1985). This model uses meteorological data to describe the motion of an
air mass traveling over urban emission sources to the point at which the
highest hourly ozone concentration was observed on the day simulated.
Local emission data and a complex gas-phase chemical kinetics mechanism are
used to describe the chemical processes within the air mass.
298
-------
1200
Formaldehyde Absorption Cross Section
Surface Solar Irradionce (300 Dobson)
310
Wavelength (nm)
Figure 2. Matched High-resolution for Formaldehyde Absorption
Spectra and Measured Surfaced Solar Irradiation.
299
-------
been extensively studied and many large data collection programs have been
carried out, simulations of the photochemistry of this condition are thought
to provide a realistic indication of potential impacts.
These models can also be used to estimate the chemical sensitivity to
alterations in surface temperatures due to potential changes in concentration
of greenhouse gases. Although it is beyond the scope of this discussion to
consider the complex perturbations that may alter future surface temperatures,
the recent work of Ramanathan et al. (n.d.) and Wang et al. (1986) estimates
that these increases will be 1°-3°C by the year 2030. In the work described
next, we bracketed this range by assuming a maximum surface temperature varia-
tion of 4°C.
We calculated ozone and formaldehyde J values as a function of solar ele-
vation and ozone column density for three urban areas using column densities
of 300, 250 and 200 Dobson and surface temperatures of 298 K and 302 K. The
test data were selected from data sets for Nashville, Tennessee, Philadelphia,
Pennsylvania, and Los Angeles, California. The meteorological conditions and
hydrocarbon and NOX emissions in these three cities differ, as do the maximum
ozone concentrations measured in the late afternoon on these days. According
to the U.S. National Ambient Air Quality Standard for ozone, air quality on
the Nashville test day was nearly in compliance with the standard. The
Philadelphia test day was selected to represent urban conditions that require
moderate reduction in hydrocarbon emissions to achieve the ozone standard.
The Los Angeles test day was selected to examine an extremely reactive region.
Table 1 presents the results of one-day simulations of these ttiree test
cases for the Dobson number and temperatures selected. The model consistently
predicted higher ozone concentrations with increases in temperature and
decreases in Dobson number. For the Los Angeles case, the increases in ozone
production were moderate and quite linear with decreasing Dobson number. In
the Nashville simulations, the increases were dramatic and the linearity was a
function of temperature: At 298 K, the simulated urban ozone tended to
increase linearly with a decrease in Dobson number, but at the warmer tempera-
ture, simulated ozone concentrations increased more rapidly for the first 50-
Dobson unit change than for the second.
The Philadelphia test was performed differently. The hydrocarbon emis-
sion data for the original base-case simulation were lowered to the values
needed to bring the predicted afternoon ozone maximum into compliance with the
federal law. In effect, this scenario represented the condition of future
compliance with federal law for 300 Dobson and 298 K. The effects of strato-
spheric ozone and temperature changes were then simulated for these condi-
tions. The results showed a progressive increase in ozone as the Dobson
number declined. In addition, the ozone production occurred much more rapidly
at lower Dobson numbers, reaching levels near the final maximum concentration
earlier in the day. This finding typifies the simulation results. Although
the future scenario conditions resulted in more rapid production of ozone and
other oxidants earlier in the simulation period, the maximum predicted ozone
concentrations did not reflect such extreme differences, even though lower
Dobson numbers and higher temperatures always resulted in more ozone produc-
tion. This is because ozone production later in the day is often limited
because of exhausted hydrocarbon or NOX concentrations. Because trajectory
models, such as the one used here, imply an equivalence in time and distance
300
-------
Table 1. Ozone concentrations (ppm) predicted for changes in Dobson
number and temperature for three cities.
Temperature (K)
Dobson Number
300
Ozone Concentrations
298K
250
200
300
302K
250
200
C1ty_
Los Angeles*
Philadelphia
Nashville
0.288
0.112
0.130
0.301
0.127
0.161
0.315
0.149
0.195
0.306
0.122
0.146
0.318
0.134
0.184
0.331
0.159
0.215
* For Los Angeles, values under 298 K used actual hourly temperatures
and values under 302 K are from simulations using those temperatures
Increased by 5 K.
from the urban center, a rapid occurrence of high ozone concentrations earlier
in the day, followed by continued moderate increases, implies that more people
will be exposed to episodic levels of ozone. Population density is often
greater nearer to the urban center, therefore, the number of people exposed to
episodic ozone levels may increase dramatically if future ozone peaks occur
earlier in the day.
Our investigation of the key reactions involved in the temperature
changes indicated that peroxyacetyl nitrate (PAN) chemistry explains most of
the effect in these cases; that is, less PAN exists at higher temperatures
because its unimolecular decomposition rate is temperature-dependent. This
provides greater amounts of PAN decomposition products (NOX and the organic
peroxyacetyl radical) for use in oxidant-forming reactions. The effects of a
4 K increase in temperature were most pronounced in the Los Angeles and
Nashville tests. The effects of a combined temperature increase and reduced
Dobson number appear to be always additive, if not synergistic, especially for
the Nashville simulations. When a 4 K temperature increase was combined with
only a 50-unit Dobson reduction, the simulated peak ozone increased
almost
301
-------
Enhanced radical flux in urban airsheds should not only increase their
ozone-forming potential, but also augment the production of other oxidants
such as hydrogen peroxide. In our preliminary tests, the maximum hydrogen
peroxide produced for the Philadelphia and Los Angeles cases increased by over
an order of magnitude. Additional simulations designed to directly study the
effects of future changes on hydrogen peroxide formation should be conducted
to verify the magnitude of the processes involved. For the scenarios tested,
however, both ozone and hydrogen peroxide concentrations increased in all
cases.
REFERENCES
Bane F.C., H. Illner, W.N. Marx, U. Schurath, and P. Roth 1979. Messung der
von Veranderungen der Ozonschicht stark abhangigen kurzwelligen
Sonnenstrahlung. Munich: Gesellschaft fur" Strahlen-und Umweltforschung
mbH.
Bahe, F.C., W.N. Marx, W. Schurath, and E. P. Roth. 1983. Determination of
the Absolute Photolysis Rate of Ozone by Sunlight
03 + hv * 0(1D) -i- 02 (1Ag), at Ground Level. Bonn: Institute fur
Physikalische Chemie der Universitat.
Bass, A.M. 1985. Personal communication Washington, D.C.: U.S. National Bureau
of Standards.
Baulch, D.L., R.A. Cox, R.F. Hampson, Jr., J.A. Kerr, J. Troe, and R.T.
Watson. 1984. Evaluated kinetic and photochemical data for atmospheric
chemistry: Supplement II, CODATA Task Group on Gas Phase Chemical
Kinetics. J. Phys. Chem. Ref. Data. 13(4).
Calvert, J.G., A. Lazrus, G.L. Kok, B.C. Heikes, J.G. Walega, J. Lind, and C.
A. Cantrell. 1985. Chemical mechanisms of acid generation in the tropos-
phere. Nature. 317:27.
Cicerone, R.J., S. Walters, and S.C. Liu. 1983. Nonlinear response of stratos-
pheric ozone column to chlorine injections. J. Geophys. Res. 88:3647-
3661.
Craig, H., and C.C. Chou. 1982. Geophys. Res. Lett. 9:1221-1224.
Crutzen, P.J., and J. Fishman. 1977. Geophys. Res. Lett. 4:321.
Farman, J.C., B.C. Gardiner, and J.D. Shanklin. 1985. Nature. 315:207-210.
Haagen-Smit, A.J. 1952. Chemistry and physiology of Los Angeles smog. Indust.
Engineer. Chem. 44:1342-1346.
Hogo, H., and G.Z. Whitten. 1985. Guidelines for using OZIPM-3 with CBM-X or
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chemistry: A global perspective J. Geophys. Res. 86:7210-7254.
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high concentrations of stratospheric halogens. Nature. 312:227-231.
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and their potential role in climate change. J. Geophys. Res. 90:5547-
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Tropospheric CH4/CO/NOX: The Next Fifty Years
Anne M. Thompson
Applied Research Corporation
NASA—Goddard Space Flight Center
Greenbelt, Maryland USA
Michael Kavanaugh
Consulting Economist
Washington, DC USA
ABSTRACT
Previous studies with photochemical models have emphasized the coupling
of atmospheric CHh-CO-OH-NOX. Recent increases in the concentration of atmos-
pheric methane (CHh.), for example, could be caused by increases in CHh sources
and/or a decrease in the OH radical that controls the photochemical CHh
lifetime. *
In this paper we use alternate projections of CO and NOX emissions in a
photochemical model to predict tropospheric CH^/CO/NO,. concentrations over the
next fifty years. Simple extrapolation of current CHh and CO increases
implies that CH^ will reach 2.9-3.0 ppmv by 2035 and that background CO will
double or triple. If we base calculations on projections for combustion CO
and NOX that show a leveling off of CO emissions, there will be less
perturbation to background OH and smaller increases in CHh and CO over the
next fifty years.
INTRODUCTION
Much attention has been given lately to temporal changes in a number of
photochemically and radiatively active trace gases. The main topic of Volume
2 is ozone, a gas whose changes over time are driven by perturbations in a
large number of trace gases that interact photochemically. One such gas is
methane (CHjj), which is of interest for its radiative properties as a
greenhouse gas and is of interest photochemically because it helps control
abundances of the principal tropospheric oxidant OH and of stratospheric H20
vapor and HOX (HOX = H + OH + H0*>). For example, an increase in CHh, enhances
temperature increases caused by C02 (generally regarded as undesirable), but
will offset some of the catalytic destruction of stratospheric 0? caused by
reactive odd chlorine and nitrogen (regarded as a good thing).
305
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An example of the mitigating effect of CHjj on stratospheric 0^ change was
described recently by Connell and Wuebbles (1986). Although a catastrophic
loss of stratospheric Oo is predicted in less than 100 years for all CH^
scenarios considered in their study, there is a significant variation in the
evolution of this loss depending on what is assumed for rates of CHjj changes
during the period.
Our purpose here is to discuss changes in atmospheric methane and related
changes in tropospheric chemical composition. We give estimates for future
CHh and offer insight into the complexity of predicting tropospheric change.
Methane changes are related to regional and probably global-scale changes in
CO, Oo, NOX, and the free radical OH, which, if anything, are harder to
predict than changes in CFty. These changes strongly influence stratosphere
perturbations, although as Whitten and Gery (1986) have shown, coupling
between stratosphere and troposphere goes both ways. Stratospheric and
climatic changes will ultimately feed back to alter photochemistry in the
lower atmosphere.
This paper reviews atmospheric CHjj perturbations that have already taken
place and summarizes tropospheric photochemistry related to CHh. There is a
basic problem in discerning the cause and effect of CH|j trends oecause CH^ is
tightly coupled to cycles of other trace gases that may be changing in time,
e.g., CO, Oo, NOX. We also describe results from a photochemical model study
interpreting past changes in CHn and predicting trends in CH^ and related
gases, CO/NO-j/O^ over the next fifty years. Two types of scenarios for change
in CO/NOX/OH are considered. The first is based on simple extrapolation of
recent past Cti^ and CO trends into the future. The second scenario assumes a
constant increase in CH^ sources and smaller increases in CO based on
Kavanaugh's (1986) predictions of CO combustion emissions. Finally, since
CH||/CO/OH cycles are coupled to NOX and tropospheric ozone, we look at changes
in these species as well. On a global basis tropospheric Oo, for which there
is evidence for a temporal increase (Logan 1985; Bojkov 1986), will probably
increase. Changes in shorter lived constituents (e.g., OH, NOX) are harder to
predict because their sources are variable and their geographical distribution
will probably change in time with changing patterns of economic activity.
In view of large uncertainties in global budgets of CH^, CO, and NOX
(Logan et al. 1981; Logan 1983), it is not possible to specify current and
future emissions exactly for every geographical region. Rather, we simulate
prototypes for various types of environments. One of the specific features of
our approach is the use of a one-dimensional model run in a steady-state mode
with inputs appropriate for a given year. That is, long-term integration has
not been attempted. Furthermore, there is no attempt to simulate the dynamics
that allow various regions to communicate with one another, i.e., we do not
have a truly global model. Finally, climate changes and perturbations to
stratospheric ozone, which may feed back to tropospheric temperature, water
vapor, and photodissociation, are not included in the present study.
METHANE OBSERVATIONS AND PHOTOCHEMISTRY: ANALYSIS OF PAST TRENDS
A number of recent studies (Craig and Chou 1982; Khalil and Rasmussen
1985; Stauffer et al. 1985) show that atmospheric CHh has been increasing
steadily since approximately 1700, after several millenia of constant
306
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concentration. For example, detailed analysis of CHn over the past seven or
eight years, as measured by Rasmussen and Khalil (1984) at a nonpolluted site
along the Oregon coast, reveal seasonal variations in CH^; once these are
taken out there is a definite upward trend. Rowland and coworkers (Blake et
al. 1982; Blake and Rowland 1986) present similar evidence from sites around
the world, using gas chromatographic analysis of ambient air to determine CH^
levels. Independent evidence deduced from infrared spectra collected at a
European astronomical observatory (Rinsland, Levine, and Miles 1985) shows
that CH|| has been increasing 1% per year for at least 30 years. Over the past
century or so CFty has roughly doubled, going from 0.8 ppbv to 1.6-1.7 ppbv
presently in the Northern Hemisphere; in the Southern Hemisphere where CH^
sources are fewer background levels are slightly lower.
Why is atmospheric CHh increasing? Will it continue to do so and at what
rate? Basically, causes for the increase fall into two categories. First,
CHjj sources, all of which are biological in origin (outgassing of oceans and
marshes, rice paddies, enteric fermentation of ruminants, termites), are
increasing. Second, the photochemical sink limiting the atmospheric lifetime
of CHjj, the OH radical, is decreasing.
What controls OH and how do we decide which of these processes is during
current CHjj changes? First of all, the fact that CHn is increasing itself
suppresses OH and adds CO to the atmosphere (Sze 1977; Chameides, Liu, and
Cicerone 1977). This further suppresses OH, methane and CO being the trace
gases that react most rapidly with OH. Nonmethane hydrocarbons (NMHC) also
react efficiently with OH (Greenberg, Zimmerman, and Chatfield 1985), and
further study of their role in OH perturbation is needed. In the present
study we assume NMHC are localized and not significant on a global scale and
neglect NMHC in our model except for C2H6. There is some evidence of a
secular increase in CO (Khalil and Rasmussen 1984; Rinsland, Levine, and Miles
1985) although this is harder to establish than increasing CHh, owing to the
shorter lifetime and greater natural variability of CO. OH, a transient
species (lifetime approximately 1 s), is even more variable, and so far has
been impossible to measure in the troposphere. Additional evidence for
diminishing OH may be the detection of a temporal increase in atmospheric C2Hg
over the past 35 years (Levine, private communication 1986).
It appears that recent CHjj changes are caused by some combination of both
increasing CH/j sources and decreasing OH. (Thompson and Cicerone 1986a;
Khalil and Rasmussen 1985; Levine, Rinsland, and Tennille 1985). Figure 1
shows results from model calculations simulating CHh, CO, and OH from I860 to
1985, making several assumptions about the rate of CO change over the past
century. Simulations in Figure 1a assume no change in CHji sources, whereas in
Figure 1b we are able to reproduce CHjj observations oy assuming that CO
increases are accompanied by an increase in CH^ sources.
PREDICTING METHANE, CO, AND OH PERTURBATIONS
Extrapolation of Recent Trends
Predictions of future CHjj have been published (Chameides, Liu, and
Cicerone 1977; Sze 1977), although this is not a simple matter. One reason is
the ambiguous nature of changing Cfy sources and/or perturbed CO-OH as causes
of increasing Cfy, as described above. Furthermore, budgets of Cfty and CO are
307
-------
1.6 -i
1860
1900 1940
YEAR
1980
0.6 -I
observed In
CH increase
1860
1900 1940
YEAR
1980
Figure 1. (a) Past methane, CO mixing ratios and fractional change in
tropospheric OH (relative to 1985). No change assumed in CHh sources from
1860 to 1985. (b) CO mixing ratios and fractional OH loss with observed CHjj
mixing ratios (Khalil and Rasmussen 1985). Observations are matched if an
increase in CH sources is assumed (Thompson and Cicerone 1986a).
308
-------
poorly known at present and predicting them in the future is problematic
because they depend to a large extent on human activity. Agricultural
practices are subject to change; biomass burning in developing nations plays
an important role; economic activity depends heavily on combustion of fossil
and nonfossil fuels; there may be switches away from the currently most
popular fuels. The issue is further complicated by photochemical coupling of
OH and CHjj changes to tropospheric NO.,, NMHC, and ozone, which also appear to
be changing in time (Volz, Smit, and Kley 1985; Bojkov 1986).
One approach to predicting future CHn is to extrapolate from recent
trends, making certain assumptions about the nature of current City and CO
perturbations (Thompson and Cicerone 1986b). For example, if atmospheric City
over the next 50 years increases at its current rate of 1* per year, it will
reach 2.9-3.0 ppmv in 2035 (Figure 2). Concurrent increases in background CO
and decreases in OH can be calculated with a photochemical model. In a
typical simulation, total CO sources consist of 35% surface flux in 1985,
mostly anthropogenic in origin, i.e., fossil fuel combustion and biomass
burning; the other 65% is mostly natural, i.e., photochemical oxidation of CHh
and C2Hg and a specified input of CO to simulate the photo-oxidation of
NMHC. (See Table 1, Type 1-CO.) A ground-level mixing ratio of 120 ppbv is
chosen as typical of nonpolluted northern midlatitudes. Inputs for CO in our
calculations simulate both natural and anthropogenic sources with the former
taken as constant in time and the latter assumed to increase with world
population and industrial growth continuing at their current rates. If
combustion CO follows C02 (increasing in output approximately 2.5% per year),
background CO will increase from 120 ppbv in 1985 to 260 ppbv in 2035
(Figure 2).
Table 1. Parameteri2ation of CO Sources—1985
stotal,CO _ n n ,,
5 - QCO * fluxCO * SNMHC
Low NOX; Stofcal = 1.9 x 1011 cm'2 s"1
Type 1-CO 15* 35* 50*
Type 2-CO 15* 65* 20*
QC0 is photochemical source of CO (molec cm s ) from OH oxidation
of CHjj and C2Hg as computed by model.
flux/yj is model lower boundary condition, representing CO sources
introduced at surface (ocean, combustion, plants, etc),
%MHC is co source specified at every altitude, simulating oxidation
of nonmethane hydrocarbons not included in model.
309
-------
Perturbations to atmospheric CO and CHjj are highly sensitive to
background NOX (especially in the boundary layer). The calculations described
above are appropriate for simulating background conditions in northern
midlatitudes (low NOX, approximately 25-30 pptv NOX; surface CO, 100-150 ppbv
in 1985). Increasing Cfy and CO suppress the concentration of OH through
their control of the OH lifetime. In our model CO reacts with 80% of the OH,
while CHjj and C2Hg react with the remainder. If higher NOX is assumed at the
surface (approximately 1 ppbv, a level characteristic of many continental
environments, not strongly polluted but influenced by areas of high
combustion), then increasing CHjj and CO emissions contribute to smog-type
reactions forming ozone and OH through ozone photolysis:
CO + OH -> C02 + H
H + 02 -> H02
H02 + N02 -> N02 -i- OH
N02 + h / -> NO + 0(3P)
02+ 0(3P) + M -> 03 + M
03 + h / -> 02 + 0(1D)
0(1D) + H20 -> 20H
In the lower troposphere these reactions partially offset mid-troposphere
losses of OH to give a lower total column loss than for low NOX regimes
(Hameed, Pinto, and Stewart 1979; Thompson and Cicerone 1986b).
Figure 3a shows OH and 0^ changes corresponding to CH^ and CO increases
illustrated in Figure 2. For low NOX, surface values of 25-30 pptv, as might
be found over unpolluted marine or even continental regions, present day 0^ is
approximately 30 ppbv. With CO doubling and CHjj increasing from 1.6 to 2.9
ppmv over the next fifity years, surface Og increases to 36 ppbv, and the loss
in total tropospheric OH (integrated from 0-15 km) is 35%. For a region with
NOX approximately 1 ppbv, surface 0^ is 40 ppbv in 1985, increasing to 50 ppbv
by 2035; the corresponding loss in OH is only 25^ because additional 0,
mitigates OH depletion.
Assuming constant NO while CO increases is not realistic since combustion
is a large source of both gases. Consider an environment in transition from a
moderately low background NOX value, 0.1-0.2 ppbv in the past two decades,
increasing along with increasing NOX emissions to 0.48 ppbv by 2035. The
historical record of NOX is not known, but NOX emissions are certainly
increasing (Dignon and Hameed 1985), which may be' a more realistic
representation of continental environments than assuming constant 1 ppbv
NOX. We refer to these as "transitional" regions. With 0, prescribed as in
310
-------
CH4and CO: 1970-2035
(Simple Extrapolation)
- 300
O
O
M
200 2-
(Q
cc
o>
c
O
-100
Figure 2. Ground level CHjj and CO mixing ratios from 1970 to 2035
(Thompson and Cicerone 1986b). Simulations were carried out with a steady-
state model at 10-year intervals assuming CFty mixing ratio increases U/year
from 1985 and CO increases are driven by fossil fuel combustion and population
growth continuing at current rates of increase. Model conditions are
appropriate for the mid-latitude northern hemisphere with low background NOX
(20-25 pptv).
311
-------
60 -iSOO
1880
20 J
E
JC
o
300 a
K
w
15
S
ox
Figure 3. Surface 03 and percent changes in column-integrated OH (0-15
km) corresponding to CHjj and CO changes shown in Figure 2 (a) Constant
background NOX. Solid lines calculated with low surface NOX (25-30 pptv);
dashed lines calculated with surface NOX at 1 ppbv. (b) 0, and change in OH
calculated with Cfy and CO as in Figure 2 and NO as shown.
312
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Figure 3b the corresponding loss in OH is almost negligible. If Og is not
prescribed explicitly but is calculated self-consistently with changing CHjj,
CO, and NOX, O2one reaches approximately 60 ppbv in 2035 and OH increases
slightly.
CHjj/CO/OH Trends from Kavanaugh's CO and NOX Projections
Predictions of CH^, CO, and OH based on simple extrapolation of recent
CHjj trends probably give upper limits for CHjj and CO fifty years from now.
Recent evaluation of energy-related combustion sources of CO from 1975 to 2025
(Figure 4a; Kavanaugh 1986) shows that this important part of the CO budget
will level off with increasing controls of mobile source emissions in
developed nations, slowing population growth, and a shift away from rich CO-
producing fuels for domestic energy use (e.g., charcoal bricks in China) in
favor of large-scale utilities that burn carbon more completely.
We have performed a series of model calculations of CO and CH|| based on
Kavanaugh's emissions projections for CO, making reasonable assumptions about
noncombustion sources of CO. We find that to the degree that Cfy is currently
responding to CO increases and OH decreases, methane increases over the next
fifty years will slow down as CO emissions rise more slowly than they have
recently.
Detailed analysis of model results shows that if the CO changes
illustrated in Figure 1b are realistic, the corresponding CH^ source change
during the past 20 to 30 years is 0.2, 0.4£ or 0.6j& per year when NOX is at
low levels .(25-30 pptv) as observed in the nonpolluted atmosphere (McFarland
et al. 1979; Torres 1985). These three cases form the basis for our
projections of background CH^, CO, and OH over the next fifty years. We
assume that Cfy sources continue to increase 0.2%, 0.45&, 0.656 yr~1 and we
combine this with Kavanaugh's global estimate for the rate of combustion CO
increase, assuming that natural CO sources do not change significantly over
the period. Details of the scenarios are given in Table 2. The model is run
at several specified dates from 1985 to 2035. The two types of CO sources
refer to the fraction of the total CO budget at 1985 that is caused by direct
surface sources of CO (e.g., fossil fuel combustion, wood- and biomass-
burning, lightning-induced forest fires, ocean and plants) that are mostly
anthropogenic. Remaining CO comes from CHjj and C2Hg oxidation calculated by
the model and from a specified in situ source that represents oxidation of
NMHC; the latter is presumed mostly natural in origin, but that fraction
coming from anthropogenic sources increases at the rate predicted by Kavanaugh
(1986), whose projections are also the basis of changes in the anthropogenic
fraction of the flux (model lower boundary condition). The same rates of
increase are used in both types of CO models, but the one With only 35% of the
CO source being anthropogenic increases more slowly.
Methane mixing ratios calculated with low NOX from 1985 to 2035 appear in
Figure 5a; corresponding CO increases and fractional loss in OH appear in
313
-------
CO From Combustion
160
120
O
o
t-
6
u
80
40
(a)
1960 1975
YEAR
2000
40
NO From Combustion
jn
30
z
en
O*
10
(b)
JL
J.
J_
1960 1975 2000
YEAR
2025
2025
Figure H. Total global emissions from energy combustion of fossil and
non-fossil fuels (Kavanaugh 1986). (a) CO, in Tg C per year; (b) tiQK, in Tg N
per year.
314
-------
Table 2. Scenarios for CHy, CO Perturbations
Source Model 1 Model 2 Model 3
Cfy City flux** Cfy flux CHj, flux
inc. ,2%/yr inc. .4jJ/yr inc. ,6%/yr
CO Type 2-CO* Type 1-CO* Type 1-CO
increase in combustion CO after Kavanaugh (1986)
Type 1-CO: 35% surface flux (mostly anthropogenic) CO sources;
Type 2-CO: 65% surface flux CO sources in 1985. See Table 1 and Thompson
and Cicerone (1986) for detailed description of CO sources.
Photochemical model (Thompson and Cicerone 1982; 1986b) run at background
continental NOX (1 ppbv) and marine (25-30 pptv) conditions,
** 1985 CH4 flux: H.U x 1010 cm'2 s'1 (low NOX); 1.31 x 1011 cm'2 s'1 (high
NOX). OH column, 0-15 km (1985): 5.4 x 1011 cm"2 (low NOX); 1.15 x 1012
cm'2 (high NOX).
Figure 5b. The 50-year projection for Cfy is 2.0-2.6 ppmv, appreciably lower
than the figure of 2.9 ppmv obtained assuming an indefinite \% per year
increase in mixing ratio. We see that CO changes are much less than the
doubling derived from smooth extrapolation of current trends; with less CO
there is less perturbation to OH and to CHh.
Kavanaugh (1986) shows that emissions of NOX will continue to increase
worldwide (Figure 4b). We have considered several NO scenarios in our
calculations, but because of the short lifetime and localized nature of NO ,
it is difficult to say how NOX increases will affect background OH. It seems
likely in the lower troposphere, at least, that background NO , Q?, and OH
will increase over large regions of the earth. For example, greatest growth
in CO and NO will be in China and third world countries. At the same time
highly industrialized nations may be controlling emissions of these gases.
This implies a shift in global background photochemistry, e.g. oxidant and
acid formation, away from the industrialized nations to the developing
countries. OH losses from increasing CO and CHjj (also NMHCs) might be offset
by increasing Oo and NOX, resulting in slower depletion of global OH.
Model calculations using Kavanaugh's projected changes in CO and NOX need
to be performed on a regional basis, dividing the continents into types of
regions according to economic and population growth patterns, assuming little
change in NO over the oceans. In some regions there will be substantial
changes in CO and NOX simultaneously, in others there will be little NOX
change. In still others there will be nearly constant combustion CO but large
increases in NOX.
315
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3.0
165
0.6% per Year Increeae
0.4% per Year Increase
-— 0.2% per Year Increaee
135
1.6
120
(b)
1990
2010
Year
-5
-10
£>
o
o
o.
c
_i_
5'
f-»
(D
CL
2030
Figure 5. (a) Ground level CFty and (b) CO mixing ratios and percent
changes in column-integrated tropospheric OH from 1985 to 2035 assuming
various rates of increase in CHjj surface fluxes. Results from Models 1-3
(Table 2).
316
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Global change in OH is a composite of regional changes. We compute
global OH and ozone in a greatly oversimplified way, given the limitations of
a one-dimensional model. First, we divide the earth into six broad latitude
bands; then, we use a model to calculate OH from typical CHjj/CO/NOx/Oo for
continental and marine areas within each band. We add marine and continental
OH within each band and take a weighted mean throughout the troposphere.
Total mean OH (4.8 x IQr molecules per cubic centimeter) compares well with
global OH computed from a similar set of model calculations by Chameides and
Tan (1981). To make a very crude estimate of future changes in global OH, we
(a) assume that OH changes over the oceans follow the course of OH in
constant, low NOX environments as calculated from the Kavanaugh-based
scenario, decreasing \}% from 1985 to 2035 (Figure 5b); and (b) that OH over
continental areas follows the course of "transitional" NOX environments,
virtually unchanged from 1985 to 2035 (Figure 3b.) :
[OH(land)]1985 x (1 + frac. change OH2035ttransitional NQ ) +
A
[OH(marine)]1985 x (1 + frac. change OH2035jlow m) = [OH]2035
A
The result is 5% to 10£ less OH in 2035 than at present. If we apply the
formula assuming that marine areas lose OH at the rates shown in Figure 3a,
the loss is 18£ to 25% after 50 years. These values are different from
assuming that Northern Hemisphere midlatitude trends in CH^, CO, and OH will
continue at current rates and are representative of the earth as a whole. It
looks as if the recent OH decline deduced from CO/Cfy perturbations will slow
down because CO combustion is leveling off and NOX combustion will continue to
increase. However, increasing NOX may contribute to substantial increases in
tropospheric ozone.
SUMMARY AND CONCLUSIONS
This paper describes photochemical aspects of atmospheric methane
perturbations and presents model predictions of CHjj over the next fifty
years. Simple extrapolation of recent CO/OH trends implies a doubling of CO
from 1985 to 2035 and Cfy increasing from 1.6-1.7 to 2.9 ppmv. Depending on
background NOX levels, these CO/CHjj increases will suppress tropospheric OH
15? to 30%. However, reduced emissions of combustion CO and increasing NOX
(Kavanaugh 1986) maintain higher OH and, given a constant increase ,in CH^
sources, lower Cti^ levels are predicted in 2035, i.e., 2-2.5 ppmv.
Strictly speaking, CO and NOX changes must be considered on a regional
basis to calculate perturbations in OH and CHjj, with an appropriate averaging
to estimate global changes in OH. The best way to predict future CHn, CO, and
OH is with a multidimensional model that includes NOX, CO, and CHjj source
changes on a well-resolved spatial grid along with transport of longer lived
trace gases. A further uncertainty in our calculations is the neglect of
explicit nonmethane hydrocarbon (NMHC) chemistry. NMHC emissions are probably
changing in time, and because NMHC produce CO and 0^ photochemically their
effects may be complex, working either to destroy or enhance OH. Finally, we
note that our study does not include explicit perturbations to CO emissions
from photochemical oxidation of vegetative hydrocarbon emissions or biomass
burning, both of which may be altered by changing patterns of land use in
developing nations.
317
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