United States
Environmental Protection
Agency
Office of Research and
Development
Washington, DC 20460
EPA/600/R-92/064
June 1992
Preliminary Risk
Assessment for Viruses in
Municipal Sewage Sludge
Applied to Land
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EPA/600/R-92/064
June 1992
Preliminary Risk Assessment for
Viruses in Municipal Sewage
Sludge Applied to Land
Environmental Criteria and Assessment Office
Office of Health and Environmental Assessment
Office of Research and Development
U.S. Environmental Protection Agency
Cincinnati, OH 45268
Printed on Recycled Paper
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DISCLAIMER
This document has been reviewed in accordance with U.S. Environmental Protection
Agency policy and approved for publication. Mention of trade names or commercial
products does not constitute endorsement or recommendation for use. .,./..
n
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PREFACE
Section 405 of the Clean Water Act requires the U.S. Environmental Protection
Agency to develop and issue regulations that identify: (1) uses for sludge including disposal;
(2) specific factors (including costs) to be taken into account in determining the measures
and practices applicable for each use or disposal; and (3) concentrations of pollutants that
interfere with each use or disposal. To comply with this mandate, the U.S. EPA has
embarked on a program to develop four major technical regulations: land application,
including distribution and marketing; landfilling; incineration and surface disposal. The
development of these technical regulations requires a consideration of pathogens as well as
chemical constituents of sludge. Public concern related to the reuse and disposal of
municipal sludge often focuses on the issue of pathogenic organisms.
This report is one of a series whose purpose is to use the methodology described in
Pathogen Risk Assessment for Land Application of Municipal Sludge to develop preliminary
assessments of risk to human health posed by parasites, bacteria and viruses in municipal
sewage sludge applied to land as fertilizer or soil conditioner. The preliminary risk
assessment includes a description of the most critical data gaps that must be filled before
development of a definitive risk assessment can be accomplished and recommends research
priorities.
in
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DOCUMENT DEVELOPMENT
Cynthia Sonich-Mullin, Project Officer
Norman E. Kowal, Technical Project Manager
Environmental Criteria and Assessment Office
U.S. Environmental Protection Agency
Cincinnati, OH
Authors
Marialice Wilson, Project Manager
Charles T. Hadden
Mary C. Gibson
Science Applications International Corporation
Oak Ridge, TN
Reviewers
Joseph B. Farrell ;.
Risk Reduction Engineering Laboratory
Andrew W. Breidenbach Environmental Research Center
U.S. Environmental Protection Agency
Cincinnati, OH
Mary-Ellen Morris <
Virology Branch, Microbiol. Res. Div.
Environmental Monitoring Systems Laboratory
U.S. Environmental Protection Agency
Cincinnati, OH
Babasaheb Sonawane
Reproductive and Developmental Toxicology Branch
Human Health Assessment Group
U.S. Environmental Protection Agency
Washington, D.C. ;
Richard Walentowicz
Exposure Assessment Group
U.S. Environmental Protection Agency
Washington, D.C. :
Judith Olsen, Editorial Review
Environmental Criteria and Assessment Office
U.S. Environmental Protection Agency
Cincinnati, OH
IV
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TABLE OF CONTENTS
1. EXECUTIVE SUMMARY . ..' 1-1
2. INTRODUCTION 2-1
3. LITERATURE REVIEW OF VIRUSES 3-1
3.1. SIGNIFICANCE OF PATHOGENIC VIRUSES 3-1
3.1.1. Transmission/Exposure Routes . 3-3
3.1.2 Occurrence of Viruses in Sludge 3-6
3.1.3. Infective Dose 3-6
3.1.4. Epidemiology 3-8
3.2. ENTERIC VIRUSES IN TREATED SLUDGE 3-12
3.2.1. Effects of Treatment Processes 3-12
3.2.2. Density of Viruses in Treated Sludge 3-16
3.3. OCCURRENCE OF VIRUSES IN NATURAL MEDIA 3-21
3.3.1. Persistence in Soil 3-21
3.3.2. Persistence in Water 3-29
3.3.3. Persistence in Aerosols Y. 3-41
3.3.4. Persistence in Agricultural Products 3-45
3.4. TRANSPORT 3-47
3.4.1. Transport in Soil 3-47
3.4.2. Transport in Surface Runoff 3-53
3.4.3. Transport in the Subsurface and in Groundwater 3-54
3.4.4. Transport by Wind 3-56
4. PARAMETERS FOR MODEL RUNS 4-1
4.1. RATIONALE FOR PARAMETER SELECTION 4-1
4.2. PARAMETER VALUES . . . 4-5
4.2.1. Main Program Parameters 4-5
4.2.2. Parameters for Subroutine RISK 4-21
4.2.3. Parameters for Subroutine GRDWTR 4-21
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TABLE OF CONTENTS (continued)
4.2.4. Parameters for Subroutine RAINS 4-21
5. SITES FOR MODEL RUNS ..; 5-1
5.1. SITE 1: ANDERSON COUNTY, TN 5-1
5.1.1. Description of Soil 5-1
5.1.2. Narrative Climatologic Summary 5-1
5.1.3. Temperature 5-2
5.1.4. Rainfall 5-2
5.1.5. Parameters for Subroutine RAINS 5-3
5.2. SITE 2: CHAVES COUNTY, NM 5-4
5.2.1. Description of Soil 5-4
5.2.2. Narrative Climatologic Summary 5-5
5.2.3. Temperature : 5-5
5.2.4. Rainfall 5-5
5.2.5. Parameters for Subroutine RAINS '.. 5-6
5.3. SITE 3: CLINTON COUNTY, IA 5-6
I
5.3.1. Description of Soil 5-6
5.3.2. Narrative Climatologic Summary 5-7
5.3.3. Temperature 5-7
5.3.4. Rainfall .; 5-7
5.3.5. Parameters for Subroutine RAINS 5-8
5.4. SITE 4: HIGHLANDS COUNTY, FL 5-8
5.4.1. Description of Soil 5-9
5.4.2. Narrative Climatologic Summary 5-9
5.4.3. Temperature .; 5-9
5.4.4. Rainfall 5-10
5.4.5. Parameters for Subroutine RAINS 5-10
i
5.5. SITE 5: KERN COUNTY, CA 5-H
5.5.1. Description of Soil 5-H
5.5.2. Narrative Climatologic Summary 5-11
5.5.3. Temperature . '....' 5-12
5.5.4. Rainfall 5-12
VI
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5.6.
TABLE OF CONTENTS (continued)
5.5.5. Parameters for Subroutine RAINS 5-12
SITE 6: YAKIMA COUNTY, WA ....... 5-13
5.6.1. Description of Soil 5-13
5.6.2. Narrative Climatologic Summary 5-13
5.6.3. Temperature • 5~14
5.6.4. Rainfall J-14
5.6.5. Parameters for Subroutine RAINS 5-14
6. RESULTS • •.•••' 6-1
6.1. ALGORITHM FOR INFECTIVE DOSE ... ... r. • 6-1
6.2. SENSITIVITY TO VARIABLES 6-3
6.3. ONSITE EXPOSURES 6-14
6.4. OFFSITE EXPOSURES *..... • 6-16
6.5. EXPOSURE FROM CONTAMINATED FOOD 6-16
6.6. EXPOSURE FROM CONTAMINATED GROUNDWATER 6-17
6.7. SURFACE WATER EXPOSURE 6-20
7. CONCLUSIONS • • • • 7~1
7.1. LITERATURE REVIEW . 7-1
7.2. MODELING RESULTS 7-1
7.2.1. Sensitivity Analysis 7-2
7.2.2. Onsite Exposures 7-2
7.2.3. Sediment Transport and Surface Runoff 7-3
7.2.4. Offsite Exposures 7-3
7.2.5. Waiting Period 7-4
8 RESEARCH NEEDS • S'1
8.1. INFORMATION NEEDS FOR VIRUSES 8-1
8.2. MODEL DEVELOPMENT 8-3
9. REFERENCES • • 9'1
APPENDIX A. Model Overview A-l
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LIST OF TABLES
Title Page
2-1 Compartments Included in the Sludge Management Practices 2-2
2-2 Sludge Management Practices and Descriptions in Pathogen Risk
Assessment Model 2-4
3-1 Computer Search Strategy - 3.3
3-2 Human Viruses in Sludge and Wastewater 3.4
3-3 Virus Densities in Sludge 3.17
3-4 Virus Inactivation in Soil . 3_22
3-5 Virus Inactivation in Aquatic Systems 3.30
3-6 Virus Inactivation in Aerosols 3.44
4-1 Temperature Algorithm for Inactivation of Viruses 4.4
4-2 Main Program Parameters . 4.5
4-3 Parameters for Subroutine RISK 4.^9
4-4 Parameters for Subroutine GRDWTR 4-20
4-5 Parameters for Subroutine RAINS 4_22
6-1 Results of Model Runs, Baseline Conditions 6-6
6-2 Maximum Probability of Infection by Site and Practice 6-8
6-3 Effect of Process Functions on Probability of Infection 6-11
6-4 Effect of Distribution of Crop Types on Risk To Consumers of
Garden Vegetables 6_18
6-5 Effect of Variables for Subroutine GRDWTR on Infection via Groundwater 6-21
8-1 Parameters for Temperature-Dependent Inactivation of Viruses in
Aquatic Systems ; g_4
viii
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3-1
6-1
6-2
6-3
6-4
6-5
6-6
6-7
6-8
6-9
LIST OF FIGURES
Title Page
Inactivation Rates of Viruses in Water as a Function of Temperature .... 3-36
Effect of MID on Cumulative Infection, Poisson Distribution Model ------- 6-2
Effect of Dispersed Population, Poisson Distribution Model ............ 6-4
Time Course of Risk from Viruses, Site 1, Practice I ---- ............. 6-9
Effect of Inactivation Rates ONSITE, Site 1, Practice I .............. 6-12
Effect of Inactivation Rates on SWIMMER, Site 1, Practice I ......... 6-13
Time Course of ONSITE Risk, Site 1, All Practices ................. 6-15
Time Course of Risk to DRINKER, Site 1, Practices I-HI ............ 6-19
Probability of SWIMMER Infection, All Sites, Practice I ............. 6-22
Time Course of Risk to SWIMMER, Site 1, Practices I-IH ............ 6-24
IX
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ABBREVIATIONS AND SYMBOLS
AGI Acute gastrointestinal illness
CEC Cation exchange capacity
CPU Colony-forming units
D&M Distribution and marketing
dia Diameter
ffu Focus-forming units
g Gram
ha Hectare
HAV Hepatitis A Virus
HCV Human coronavirus
HID Human infective dose
hr Hour
HVCS High volume cyclone scrubber
ID Infective dose
MID Minimum infective dojse
min Minute
MPN Most probable number
NOAA National Oceanic and Atmospheric Administration
PFRP Processes to Further Reduce Pathogens
PFU Plaque-forming Units
PSRP Processes to Significantly Reduce Pathogens
RH Relative humidity
sec Second
SRV Small round viruses
TCID Tissue Culture Infective Dose
TDS Total dissolved solids
TPB Tryptose phosphate broth
USDA U.S. Department of Agriculture
wt Weight
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1. EXECUTIVE SUMMARY
This preliminary risk assessment study focuses on the probability of human infection
from enteric viral pathogens in municipal sludge applied to land. It is based on the
Pathogen Risk Assessment computer model and methodology described in Pathogen Risk
Assessment for Land Application of Municipal Sludge (U.S. EPA, 1989a).
This document reports (1) the results of a literature review designed to find the data
on pathogenic viruses required by the pathogens methodology, and (2) the results of
numerous site-specific computer simulations, running the Pathogen Risk Assessment Model
with a wide range of values for the parameters required. The parameters required for
viruses are (1) density of infective viruses in treated sludge destined for land application;
(2) minimum infective dose; (3) inactivation rates in soil, dry particulates, liquid aerosols
and water; and (4) dispersion in the environment, i.e., transport in water, soil and air.
Literature values for virus density in treated sludge were so variable, both by
treatment methodology and by virus type, that no single number could be selected as typical.
However, 2000 virus particles/kg was chosen as representative of viral density in composted
sludge and 100,000 particles/kg in digested sludge. Infective doses, while varying by
detection method and by virus type, have been reported to be as low as 1 infective particle.
As a conservative assumption, this minimum value was used for the model runs. Reported
inactivation rates range from T.lxlO'5 to 1.6X10'1 logs/hour in soil, 1.6X10"4 to 1.4X10'1
logs/hour in water, and 4.9xlO'5 to 8xlO'7 logs/second in aerosols. Like the density values,
these rates are quite variable. Information on dispersion of viruses in the environment is
limited in its applicability to generating a rate of transport in environmental media.
Development of a variety of transport models has been an attempt to quantify the
movement of viruses, especially in the subsurface and in groundwater.
Six sites were chosen to provide diversity in geographic location, topography, soil
type, rainfall pattern and temperature. Locations selected for site-specific application of the
model include Anderson County, TN; Chaves County, NM; Clinton County, IA; Highlands
County, FL; Kern County, CA; and Yakima County, WA.
1-1
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An initial sensitivity analysis was performed using site-specific parameters for Site 1,
Anderson County, TN. Main program variables used in the model run were varied over a
range of values to determine the sensitivity of the model to variations in conditions. In
general, the default value of a given parameter was compared with a reasonable higher and
a reasonable lower value, where the high and low values were taken from available
literature or estimated when literature values were not available.
In this analysis, it is assumed that viruses are transported into subsurface soil and
subsequently into groundwater and are included in any droplet aerosols formed by spray
application, as well as in any particulate aerosols formed by disturbance of the soil by wind
or by cultivation. It is also assumed that the viruses are inactivated at a characteristic rate
that depends on the ambient temperature and the medium in which they are found.
Using baseline parameters at Site 1, the maximum probabilities of infection in each
practice were evaluated. Infection ONSITE was similar for all practices, between 1% and
7%. The probability of infection to the OFFSITE receptor was calculated as zero in every
case. Risk of infection via contaminated food products (EATER) was; shown only in
Practice IV, and risk via offsite wellwater (DRINKER) was shown in Practice HI. In
contrast, infection by contact with onsite surface water (SWIMMER) was significant in all
three practices (Practices I-IH) that include the pond, the risk level being dependent on site-
specific as well as practice-specific variables.
The effects of site-specific and practice-specific differences in parameters and
assumptions are illustrated by comparing the outcome of baseline model runs. The second
set of model runs, in which inactivation rates were decreased in soil, water, and droplet
aerosols, showed higher probabilities of infection at all sites and for most exposure
compartments. The results of these model runs, using baseline parameters except for the
more conservative inactivation rates, showed the maximum calculated probabilities of
infection ONSITE were similar for each site, and again no OFFSITE; infection was
predicted. Infection via contaminated food products was calculated to be significant only
in Practices I and IV, whereas infection via contaminated wellwater was indicated in
Practices I-IH at all sites. Infection to the SWIMMER was predicted at significantly higher
levels than with the default inactivation parameters.
1-2
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Results show that the inactivation rate of virus particles is extremely important in
determining whether a groundwater well is likely to become contaminated and in
determining how long surface soils or surface water are likely to remain infectious. The
results also demonstrate the importance of accurate characterization of inactivation rate for
viruses of different kinds in the various transport and exposure media.
Using reference values including the conservative inactivation rates, the baseline
maximum probability of infection was 0.270 for Practice I, 0.046 for Practices H and ffl,
0.0055 for Practice IV, and 0.0028 for Practice V. Generally, site-specific variables did not
have a significant effect on the probability of ONSITE infection, because the site-specific
variables alter temperature-dependent inactivation rates and rainfall-dependent runoff and
sediment transport, none of which exerts major effects on the ONSITE exposure
compartment before the time of maximum infection. Significant impacts on the probability
of infection were observed in all application practices with changes in pathogen density in
the applied sludge [ASCRS, P(l)] and sludge application rate [APRATE, P(2)], both of
which determine the number of viral particles applied. Because of the exponential nature
of the probability algorithm, the changes in probability were not directly proportional to the
change in parameter values, but varied as would be expected for a proportional change in
exposure.
In all model runs the probability of infection OFFSITE was calculated as zero,
indicating that although the inactivation of viruses in aerosols may be less than initially
expected, the calculated quantities of liquid and dry particulate aerosols and concentrations
of viruses in the aerosols were too low to provide an infective dose to the modeled receptor.
Consumption of contaminated vegetable crops was shown by model calculations to
be a potential source of human infection, provided that inactivation rates were sufficiently
low or harvesting times were sufficiently close to application of the sludge. Infection via
food crops was sensitive not only to infectious dose, inactivation rates, and the parameters
that directly affect the number of pathogens applied to the soil, but also to the relative
fractions of pathogens transferred among surface soil, subsurface soil, and crop surface and
to the type of crop or fraction of the total crop grown aboveground, below-ground, or on the
ground.
1-3
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Contamination of meat or milk by viruses from sewage sludge did not appear to pose
a significant risk to human health.
Transport of viruses via groundwater to an offsite well was not shown by this model
to be a major risk, but exposure by contaminated groundwater was shown to be likely if the
rate of inactivation of viruses in water was less than the default values. The probability of
infection was related to the periodic introduction of pathogens to groundwater by the
infiltration of rainwater. The most important parameter related to subsurface transport of
viruses appeared to be the inactivation rate of viruses in water. The results also showed an
increase in probability of infection at the offsite well whenever the time required for the
viruses to reach the well was decreased.
Contaminated surface water, represented by the SWIMMER in an onsite pond, was
the most significant source of exposure. A peak in probability of infection occurred after
each rainfall, when additional contaminated surface water and soil were washed into the
pond.
The following information is needed to improve the usefulness of the Pathogen Risk
Assessment Model and to allow for a bore reliable risk assessment of the land application
of sewage sludge:
• Simple and accurate standardized methods for detecting and quantifying, by type,
pathogenic viruses in treated sludge destined for land application, in final D&M
sludge products, and in environmental media;
• Improved understanding of minimum infective doses, particularly low-dose effects
and MIDs for sensitive subjects;
• More accurate persistence and transport data on all pathogenic viruses of major
concern in sludge;
• Development of an index of soil types that would correlate capacity for solute
transport and suitability for sludge application (also valuable for onsite waste
disposal or solid waste disposal);
• Research on subsurface injection of sludge and the relative probability of virus
transport in groundwater; and
• Epidemiologic studies evaluating enteric viral transmission.
1-4
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The following revisions would improve the accuracy of the model:
• Revision of default parameter values, especially for inactivation rates in aerosols
• • •' and temperature-dependent inactivation rates in soil arid water;
• Revision of temperature-dependent inactivation algorithms;
• Incorporation of factors for humidity and temperature in inactivation equations
for aerosols;
• Incorporation of subroutines for subsurface transport under conditions of transient
flow; and
• Incorporation of factors to allow for subsurface transport through solution
channels, cracks, etc.
In addition, field validation of the model's predictions is necessary before the Pathogen Risk
Assessment Model can be considered an accurate predictor of health risk.
1-5
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2. INTRODUCTION
This preliminary risk assessment study focuses on the probability of human infection
from enteric viral pathogens in municipal sludge applied to land. Sludge, a byproduct of
sewage treatment, is the mixture of solids and liquids remaining after treatment processes
remove solids from municipal or domestic wastewater. Secondary and tertiary sludges
contain biomass resulting from microbial digestion of the sewage. Derived from human
sanitary wastes, sludge contains microorganisms that colonize humans and can cause
infection and disease.
This risk assessment is based on the Pathogen Risk Assessment computer model and
methodology described in the U.S. Environmental Protection Agency's (U.S. EPA's)
Pathogen Risk Assessment for Land Application of Municipal Sludge (U.S. EPA, 1989a).
Appendix A provides an overview of the model. The purpose of the model is to determine
the probability of infection of a human receptor from pathogens in land-applied sludge. The
model consists of a series of compartments (Table 2-1) representing discrete points in the
application pathway. The compartments are the various locations, states or activities in
which sludge or sludge-associated pathogens exist; they vary to some extent among practices.
Compartments representing sources of human exposure are designated with an asterisk in
Table 2-1. In each compartment, pathogens increase, decrease or remain the same in
number with time, as specified by "process functions" (growth, die-off or no population
changes) and "transfer functions" (movement between compartments). Infection rather than
disease is used to measure risk in the methodology, since exposures to pathogenic viruses
may lead to no infection, human infection that is asymptomatic or subclinical (no illness),
or human infection with illness (Kowal, 1985). The outputs produced by running the model
are numerical values for the probability of a human receptor receiving an exposure
exceeding the minimum infective dose (MID) in a 24-hr period. The MID for humans is
considered to be as low as 1 virus particle, although infective doses can vary depending on
the virus and susceptibility of the human receptor (Kbwal, 1985). The model will run until
the day specified or until the number of pathogens in each compartment decreases to < 1,
at which point the number is rounded to zero.
2-1
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TABLE 2-1
Compartments Included in the Sludge Management Practices
Compartment
Name and Number
Application
Incorporation
Application/Tilling
Emissions
Soil Surface
Particulates
Surface Runoff
Direct Contact
Subsurface Soil
Groundwater
Irrigation Water
Soil Surface Water
Offsite Well
Aerosols
Crop Surface
Harvesting
(Commercial) Crop
Animal Consumption
Meat
Manure
Milk
Hide
Udder
aSource: U.S. EPA, 1989a
Asterisk indicates exposure
Liquid Sludge Dried/Composted
Management Practices Sludge Management
Practices
T
1
2
3*b
4
5*
6*
T
8
9
10
11
12*
13*
14
15
16*
compartments.
IT
1
2
3*
4.
5*
6*
7*
8
9
10
11
12*
13*
14
17
18*
19
20*
21
22
— m — • . iv.
i '•• i
2
3* '• 3*
4 4 '
5* ' 5* ' '
6*
7* 7*
8 8 ,
9
10
11 11
12*
13*
14 14
15 . 15 •
16*
17 :
18*
19
20*
21
22
V
1
3*
4
5*
7*
8
11
14
1 '•
2-2
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Two categories of land application are employed in the methodology: (1) agricultural
utilization and (2) distribution and marketing (D&M). The source of pathogenic viruses is
either liquid or dried/composted municipal sewage sludge. The five municipal sewage-
sludge management practices (Table 2-2) included in the model are application of liquid
treated sludge to (I) commercial crops for human consumption, (n) grazed pastures, and
(III) crops to be processed before being consumed by animals; and application of dried or
composted sludge to (IV) residential vegetable gardens and (V) residential lawns. Practices
III and V, while ostensibly limited to hay fields and residential lawns, respectively, can be
modified by selection of appropriate parameters to represent sludge application to golf
courses, reclaimed strip mines or logged sites, parks, roadsides, etc. Although Practice V
does not include an onsite pond, the risk to a human swimming in a pond (SWIMMER) can
be modeled by using appropriate parameters in Practice HI.
Risk assessment for pathogens in land-applied municipal sludges requires the
following input data:
• Types of pathogens and their concentrations in the sludge, their survivabilities, and
their infective doses;
• The sludge reuse/disposal option used and the conditions of sludge application
(quantities, frequencies, application method);
• The fate of the pathogens in the environment, i.e., the inactivation rate under
different conditions including moist soil, dry particulates, droplet aerosols and
water; and
• The level of exposure of human receptors to the applied sludge.
In general, these data are sparse, and in many cases parameter values must be
selected by using best scientific judgement. In addition, no field experimental work has been
done to validate the predictions of the model. The purpose of this study is not to provide
a definitive health risk assessment for viruses in municipal sewage sludge applied to land,
but rather to identify parameters most in need of further research and validation.
Therefore, this document serves as an evaluation of data needs for use of the model. The
recommendations for further research are intended to provide those data, but field
validation of the model will still be necessary for application of the model.
2-3
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TABLE 2-2
PRACTICE
Sludge Management Practices and Descriptions in
Pathogen,Risk Assessment Model
DESCRIPTION"
n
m
rv
v
Application of Liquid Treated Sludge for Production of
Commercial Crops for Human Consumption
Application of Liquid Treated Sludge to Grazed Pastures
Application of Liquid Treated Sludge for Production of
Crops Processed before Animal Consumption
Application of Dried or Composted Sludge to Residential
Vegetable Gardens
Application of Dried or Composted Sludge to Residential
Lawns
'Source: U.S. EPA, 1989a
"Two types of sludge are used in this model - liquid and dried/composted. The extent
of treatment or conditioning prior to application is variable and must be determined
for each case.
2-4
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This document reports the results of a literature review designed to find the viral
data required by the pathogens methodology, and the results of numerous computer
simulations, i.e., running the Pathogen Risk Assessment Model with a wide range of values
for the parameters required. Six sites, chosen to provide diversity in geographic location,
topography, soil type, rainfall pattern and temperature, were selected for site-specific
applications of the model: Anderson County, TN; Chaves County, NM; Clinton County, IA;
Highlands County, FL; Kern County, CA; and Yakima County, WA. Since the number of
possible sites was essentially unlimited, the final selections, although somewhat arbitrary,
were based on an attempt to represent different geographic regions and to ensure a variety
of weather patterns.
Exposure pathways, i.e., migration routes of viruses from or within the application site
to a receptor, for sludge applied to land include the following:
• Inhalation and ingestion of aerosols from the application of liquid sludge or
wastewater;
• Inhalation and ingestion of windblown or mechanically generated particulates;
• Swimming in a pond fed by surface water runoff;
• Direct contact with sludge-contaminated soil or crops (including grass,
vegetables, or forage crops);
• Drinking water from an offsite well;
• Consumption of vegetables grown in sludge-amended soil; and
• Consumption of meat or milk from cattle grazing on or consuming forage from
sludge-amended fields.
Because the focus of the model is enteric pathogens, this methodology assumes that
exposure to viruses will not result in infection unless the virus particles are actually
swallowed. Risks due to inhalation of enteric pathogens will be considered only because the
infectious agents can be subsequently swallowed. However, disease can result through
routes of exposure other than the alimentary tract; risks from such exposures can be
modeled by choice of the appropriate virus-specific parameter values.
2-5
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The model calculates the probability of infection by viruses for the following human
receptors:
• Onsite person (ONSITE): who is exposed by ingestion (includes pica in
children) of soil, vegetables or forage, or by inhalation and subsequent
ingestion of aerosols (particulates or liquid);
• Offsite person (OFFSITE) who is exposed to particulate or liquid aerosols
carried by wind;
• Food consumer (EATER) who eats vegetable crops, meat or milk produced on
sludge-amended soil;
• Groundwater drinker (DRINKER) who consumes water from a well near but
not on the sludge application site;
* Pond swimmer (SWIMMER) who ingests a small amount of water while
swimming in the pond that receives the surface runoff from the application
site.
The model conceptualization (U.S. EPA, 1989a) specifies that workers engaged in the
transportation, handling and application of liquid sludge are not included as exposed
individuals because such activity is an occupational exposure.
The U.S. EPA (1986, 1988) has provided extensive information relevant to the
conceptual risk assessment framework for land application of sludge. These key studies
address the pathogens associated with sewage sludge, as well as exposure pathways and the
potential risks to humans from each of the pathways. Most of that information will not be
repeated here. Additional information about the computer model and methodology,
including basic assumptions, model limitations and sources of uncertainty, is available in
Volumes I and II of Pathogen Risk Assessment for Land Application of Municipal Sludge
(U.S. EPA, 1989a) and in Wilson et al. (1989); a brief overview of the model is included as
Appendix A.
2-6
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3. LITERATURE REVIEW OF VIRUSES
A literature search was performed to find the most current information available for
the parameters required by the model for simulating land application of sludge. This
literature was reviewed for data on which to base the ranges of values for each of those
parameters. The parameters required for viruses are (1) minimum infective dose; (2)
density of infective viruses in treated sludge destined for land application; (3) inactivation
rates in soil, dry particulates, liquid aerosols and water; and, (4) dispersion in the
environment, Le., transport in air, soil and water.
Appropriate codes and keyword truncation were used to produce the most effective
search strategy for query of each data base. Table 3-1 lists the computerized data bases
queried and the keywords used. The three columns of keywords were "anded" together to
produce a set in which at least one keyword in each column was a descriptor or was
contained in a retrieved record.
References in reviews and in relevant articles retrieved by the computer search were
also evaluated, and names of pertinent authors were searched to find recent papers.
Because the scope of this literature review is limited to information satisfying the
parameters required by the model, the reader is directed to cited references for more
comprehensive background information.
3.1. SIGNIFICANCE OF PATHOGENIC VIRUSES
The presence of pathogenic viruses in sewage sludge has been well-researched and
documented. Several reviews include information on specific types of viruses present in
municipal sewage, their persistence and density in sludge, their pathogenicity, and potential
health risks associated with land application (WHO, 1981; Kowal, 1985; Carnow et al, 1979;
Loehr et al., 1979; IAWPRC, 1983; U.S. EPA, 1986, 1988; Lund, 1978; Burge and Marsh,
1978; Pedersen, 1981; Elliot and Ellis, 1977; Feachem et al., 1983).
From the Latin word meaning poison, the word virus was originally used to mean any
poison or noxious agent. Organisms that could pass through bacteriologic filters and be
transferred serially from one animal to another were termed "filterable viruses" and later,
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TABLE 3-1
Computer Search Strategy
Data Bases
Keyword Groups
AORICOLA
AGRIS
WOSIS
GAB ABSTRACTS
CRIS/USDA
ENYIROLINE
FSTA
NTIS
POLLUTION ABSTRACTS
TQXLINE
WATER RESOUR. ABS
ZOOLOGICAL RECORD
VIRUS
ENTEROVIRUS
ENTERIC VIRUS
POtlOVIRUS
COXSACKIE(VIRUS)
ECHOVIRUS
HEPATITIS A
ADENOVIRUS
REOVIRUS
ROTAVIRUS
PARVOVIRUS
CORONAVIRUS
NORWALK/
NORWALK-LIKE
PAPOVAVIRUS
ASTROVIRUS
CALICIVIRUS
SURVIVAL
DISPOSAL
TRANSPORT
FATE
VIABILITY/
VIABLE
DIE-OFF
MOVEMENT
SEWAGE
SOIL
AIR
AEROSOL
WATER
SLUDGE
GROUND-
WATER
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viruses. The complete infectious virus particle is called the virion, and it consists of nucleic
acid or nucleoid (DNA or RNA), a protein shell (capsid), and, for some viruses, an envelope
derived from the host cell membrane. As obligate intracellular parasites, viruses lack
independent metabolism and can replicate only within living host cells (Borland's Illustrated
Medical Dictionary, 1981; Kucera,' 1983). As a group, the viruses are the smallest agents
of infectious diseases, ranging in size from 20 nm (e.g., poliovirus) to 200-300 nm (Berk,
1983; Yates and Yates, 1988).
Although viruses cannot multiply outside a host cell (unlike bacteria, which can grow
extracellularly in a suitable nutrient-rich medium if conditions are favorable) and will always
decrease in numbers following excretion, the enteric (relating to the intestines or, more
generally, the alimentary tract) viruses can persist in the environment for many weeks,
particularly if temperatures are cool (<15°C) (Feachem et al., 1983).
Table 3-2 lists the major viruses found in wastewater and therefore those most likely
to be of concern from the land application of municipal sewage sludge.
3.1.1. Transmission/Exposure Routes. Many viruses infect the intestinal tract, are excreted
in the feces, and can infect new human hosts, following either their direct ingestion or their
mucociliary translocation and subsequent ingestion after being inhaled by the host (Slote,
1976). While the concentration of viruses in the feces of an uninfected person is normally
zero (Kowal et al. 1981), concentrations of > 106 to 109 infectious virus particles maybe shed
in 1 g of human feces from an infected individual, even if that person does not exhibit frank
disease (Feachem et al., 1983).
Transmission of enteric viruses is by the fecal-oral route, with water- and food-borne
outbreaks being of major importance; by direct personal contact or contact with
contaminated surfaces or fomites; by contact with recreational water; and possibly by the
airborne route. Although the fecal-oral route of transmission of enterovirus infections is
well-established, it is not fully understood. Ingestion of contaminated food or water or
swimming in contaminated water are important routes of viral infections (Cliver, 1987).
Human exposure to viruses in surface water is possible through deliberate or accidental
ingestion as well as through contamination of facial mucosal surfaces during recreational
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TABLE 3-2
Human Viruses in Sludge and Wastewater
Virus
Disease or Symptoms
Enteroviruses
Poliovirus
Coxsackievirus A
CoxsacMevirus B
poliomyelitis, meningitis, fever
herpangina, respiratory disease, meningitis, fever
myocarditis, congenital heart anomalies, meningitis,
respiratory disease, pleurodynia, rash, fever
Echovirus
meningitis, respiratory disease, rash, diarrhea, fever
New Enteroviruses
Hepatitis A Virus
acute hemorrhagic conjunctivitis, meningitis,
encephalitis, respiratory disease, fever
infectious hepatitis
Rotavirus
acute gastroenteritis with severe diarrhea, vomiting
Norwalk-like Agents (or Small
Round Viruses, SRVs)
epidemic gastroenteritis with diarrhea, vomiting,
abdojminal pain, headache, myalgia
Adenovirus
respiratory and eye infection
Reovirus
possibly fever, diarrhea and upper respiratory
disease, but relationship to clinical disease in
humans is not clear
Papovaviras
may be associated with progressive multifocal
leukpencephalopathy
Astrovirus
may be associated with gastroenteritis, diarrhea
Calicivirus
gastroenteritis
Coronavirus-like Particles
respiratory tract infections
Parvovirus and Parvovirus-like
Agents
gastroenteritis, aplastic anemia, fever, rash, fetal
death or damage including hydrops fetalfs
Non-A non-B Hepatitis
hepatitis
Snow Mountain Agent
gastroenteritis
Pararotavirus
gastroenteritis
Sources: Kowal, 1985; Feachem et al., 1983; Kucera, 1983; Akin et al 1978- US
EPA, 1986; Rao et al., 1986; Levy and Read, 1990
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water use (Hurst et al., 1989). Following sludge application, these viruses can find their way
into surface waters either by overland runoff or infiltration into the subsurface and
subsequent transport to an intersection with the surface.
Although it is unknown whether animals serve as reservoirs for viruses likely to be
transmitted from land-applied sludge via soil or water (Kowal, 1985), it has been proven that
consumption of virus-contaminated shellfish, especially raw shellfish, from seawater or
\
estuarine habitats is a persistent problem. Shellfish can serve as a virus reservoir in nature
because of the possible bioaccumulation of viruses associated with particulates and the
persistence of those viruses for up to months if shellfish are dormant (Metcalf, 1987).
Viral contamination of water supplies may lead to localized epidemics of viral
gastroenteritis. More than 5000 persons suffered from gastroenteritis caused by Norwalk-
like virus in a multistate outbreak traced to commercially-produced ice made from
contaminated well water. That well was flooded by a creek during heavy rains. Nearby
residents with private wells flooded by the same creek were believed to have been infected
(Levine and Craun, 1990).
Acute gastrointestinal illness (AGI) of unknown etiology comprised 48% of the
outbreaks of waterborne disease reported by the Waterborne Outbreak Surveillance System
in 1986-1988. Characteristics of these outbreaks suggest that many were caused by Norwalk-
like viruses. These reported outbreaks were associated only with water intended for
drinking and probably represent only a small percentage of all illnesses associated with
waterborne-disease agents. Additional reports of illness associated with recreational water
use during 1986-1988 included 41 cases of gastroenteritis caused by a Norwalk-like agent in
a lake. Hundreds of other cases of AGI were attributed to recreational water use, and at
least some of these were undoubtedly caused by viruses. The authors indicate that
improving the availability of testing for viral serology and detection of viral antigen in stool
would aid in determining the etiology of these outbreaks of AGI (Levine and Craun, 1990).
Transmission of viruses by the airborne route has been well established (Sattar and
Ijaz, 1987). A number of environmental factors affect the survival of viruses in aerosols,
particularly temperature and relative humidity, as discussed in Section 3.3.3 (Spendlove and
Fannin, 1982; Sattar and Ijaz, 1987). Foster et al. (1980), reporting on a rotavirus epidemic
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on Truk Island, suggested that in addition to the fecal-oral route, human rotavirus infection
may have been spread by the respiratory route. Prince et al. (1986) indicate that the
airborne route could be a pathway for the spread of gastrointestinal tract infections caused
by rotavirus. Sattar and Ijaz (1987) emphasize that the potential exists for airborne
transmission of all viruses that can survive the aerosolization process, even if the typical or
dominant route of transmission is direct person-to-person contact or some other vehicle such
as food, water or fomites.
3.1.2. Occurrence of Viruses in Sludge. Although viruses do not normally inhabit the
gastrointestinal tract of uninfected persons, the incidence of viral infection is high enough
that viruses are ubiquitous in sewage. Many of the viruses in wastewater adsorb to
suspended particles and are removed in sewage treatment processes, becoming concentrated
in the sludge product. Excreted viruses are described by Feachem et al. (1983), and their
occurrence and persistence in the environment, their inactivation in treatment processes, and
their transmission routes and epidemiology are discussed. U.S. EPA (1988), Pedersen
(1981), Hurst (1989), Englande (1983) and Ward et al. (1984) review viral concentrations
in sludge and the effectiveness of sludge treatment processes in inactivating viruses.
Information on the densities of viruses in treated sludge is summarized in Section 3.2.2.
3.13. Infective Dose. The ability of pathogenic viruses to cause infection a,nd disease in the
human exposed to them depends on the number and virulence (infectivity or pathogenic
potential) of the virions and the susceptibility of the host. Host factors include the route
of entry, the mode of virus spread, and the resistance and immunity factors of the human
receptor (Menna and Soderberg, 1983). Consequently, infection is often considered a dose-
response relationship in which the dose is the number of virions to which the human is
exposed and the response is the level of infection, i.e., no infection, subclinical infection with
no disease, or infection with disease (Kowal, 1985).
Estimating infective dose can involve exposing volunteers to known doses of the virus,
inferring from epidemiologic data the probable levels of exposure associated with observed
frequencies of infection or disease, or measuring cytopathic effect by infecting tissue
cultures. When virus concentrations are determined by infecting an indicator cell line, the
information gained is a ratio of infective activities. The most quantitative determination,
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the plaque assay, yields a concentration of infective virus units, but the dose response of
plaque formation must also be known because, in some instances, more than one infectious
virus particle may be required to initiate plaque formation. When infection can only be
measured by cytopathic effect, it may be necessary to calculate a tissue culture infective dose
(usually TCID50 or TCD50, i.e., dose required to infect 50% of the cultures). In this case,
also, the dose response of the indicator cell line to infection must be known for an accurate
calculation of dose response in humans (U.S. EPA, 1989a).
The MID, or minimum infective dose, is generally considered to be the dose that will
infect 50% of the population (U.S. EPA, 1988). It is now thought that a few virus particles
can produce an infection if conditions are favorable, and data suggest that the infective dose
of enteroviruses to humans is possibly 10 or fewer virus particles. Reported infective doses
may vary widely, however. For example, the oral infective dose to humans for poliovirus
ranges from 1 to IxlO7'6 TCID50, and the range of reported plaque-forming units (PFU) is
0.2 to 5.5xl06 (Kowal, 1985). In a review of the issue of minimum human infectious dose
(IAWPRC, 1983), the evidence suggests that while the minimum dose of enteric viruses
required to produce infection in healthy adults may be much larger than 1 PFU, susceptible
individuals are much more likely to be infected by a single PFU. Ward and Akin (1983),
in their review of minimum infective doses of animal viruses, urge more studies using larger
numbers of subjects and employing the most current techniques to answer some of the
questions regarding viral infective doses.
Ward et al. (1986) exposed volunteers to human rotavirus in doses ranging from
9xlO"3 to 9xl04 focus-forming units (ffu). The human 50% infectious dose was -10 ffu, and
it was estimated that -25% of susceptible adults would be infected by 1 ffu. Since the
occurrence of illness was not dose-related, it appeared that the same dose that could cause
infection could also cause illness.
Schiff et al. (1984) found that the oral 50% human infective dose (HID50) of
echovirus-12 in volunteers was 919 PFU, and by statistical analysis they predicted a 1%
infective dose (HIDj) of 17 PFU. Their results indicated that previous infection did not
provide lasting protection of volunteers against reinfection.
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3.1.4. Epidemiology. According to Yates (1990), "viruses may be responsible for one-third
of all the waterborae disease outbreaks that occur in this country." Wellings (1987) suggests
that as many as 60% of waterborne disease outbreaks may be caused by viruses.
Historically, viruses have been difficult to detect and isolate from environmental media and
from clinical samples. As detection methods have improved, there has been an increase in
the percentage of waterborne diseases characterized as virus-caused (Gerba, 1984c).
Several of the viruses associated with sewage sludge and possibly with human
gastroenteritis are poorly understood, such as papovaviruses, astroviruses, caliciviruses and
coronavirus-like particles (Kowal et al., 1981). Some of these have not been well-
characterized because they cannot be grown in vitro in cell cultures (Righthand, 1983).
Reliable, comparable information on others is limited by inadequate detection methods.
In fact, Rao et al. (1986) characterize the extraction, concentration and enumeration
techniques for viruses in soils as "marginally efficient" for some enterovirases and "totally
inadequate" for detecting HAV, Norwalk virus, and human rotaviruses. They conclude that
detecting any enteric virus in soil implies that many other types may be present.
Epidemiologic evidence of adverse health effects associated with exposure to viruses
from land application of sludge or wastewater has been mixed. Katzenelson et al. (1976)
found sewage-associated disease incidence 2-4 times higher in Israeli kibbutzim using
wastewater for spray irrigation than in those not using wastewater. However, the
researchers did note the possibility that pathogens could expose the affected population by
other routes, such as on the clothes of irrigation workers returning from the fields. The
microbiologic quality of the wastewater was similar to that of raw wastewater and the
likelihood of disease transmission is probably increased by the closed nature of the
kibbutzim, communities.
Fattal et al. (1986a), in a subsequent retrospective study, noted a 2-fold excess risk
only in the 0-4 year old age group during summer irrigation months but no significant risk
on a year-round basis. In a prospective epidemiologic morbidity and serology study (Fattal
et al., 1986b), no excess rate of enteric disease was seen in kibbutzim using wastewater
aerosols compared with those using no wastewater or using wastewater but not exposed to
aerosols. There was a significant excess of ECHO 4 virus antibodies found, in the 0-5 and
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6-17 year old groups, compared with all other categories of those exposed to wastewater
aerosols from nearby towns, but there was no morbidity excess. The authors conclude that
little or no wastewater-associated health risks were detected in spite of the poor water
quality of the effluent used, but they caution that the possibility of aerosol transmission of
viruses "under extraordinary circumstances is supported by the circumstantial evidence
provided by the serological study." Ward et al. (1989), as part of the Lubbock Infection
Surveillance Study, found that wastewater spray irrigation had no detectable effect on the
incidence of rotavirus infection in a community surrounding a spray irrigation site.
Johnson et al. (1980b) found no significant health hazards to residents near a new
sewage treatment plant in Schaumburg, IL, and they were unable to distinguish levels of
microorganisms in the air of residential areas from background levels.
Recent and current epidemiologic studies are providing important additional
information on the survival and transport of viruses in aerosol. Currently, however, the
preponderance of evidence suggests that, even though it is thought aerosolized pathogens
may have a lower infective dose than when ingested (Loehr et al., 1979), public health risks
from aerosolized enteric viruses do not appear to be of major concern.
Clark et al. (1980) did not demonstrate an increased risk of infection from viruses
in wastewater workers, although there was evidence of increased minor gastrointestinal
illnesses in inexperienced sewage-exposed workers compared with experienced workers.
However, the illnesses, occurring during the second quarter of the year, did not correspond
to enteroviral infections. .
Loehr et al. (1979) list normal precautions that should be observed at land
application sites to protect workers, but they also point out that continual low-level exposure
to pathogens can be beneficial to workers by building their immunity to infectious diseases.
Several viruses, including Norwalk agent in the United States (Dolin et al., 1971),
the W agent in Britain (Clarke et al., 1972), and rotaviruses in many countries (Davidson
et al., 1975), have been associated with gastroenteritis. Astroviruses were isolated from
feces of 17 of 27 symptomatic children suffering from gastroenteritis in a pediatric ward in
England (Kurtz et al., 1977). Human calicivirus (HCV), an important cause of
gastroenteritis in day care centers (Matson et al., 1989), was detected in 32% of symptomatic
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cases of gastroenteritis in a day care center in Australia, but the mode of transmission could
not be identified (Grohmann et al., 1991). The authors suggest that HCV may be a
common cause of gastroenteritis that is underrecognized because of insensitive detection
methods.
Lew et al. (1990) reviewed 6 years of viral gastroenteritis data in which 16% of
specimens were positive for a virus. The most commonly observed agent was rotavirus (26-
83%), followed by adenoviruses (8-27%, including respiratory and enteric) and small round
viruses (SRVs) (0-40%). Rotavirus and astrovirus detections were most common in winter.
Lew et al. (1990) attribute insensitive Screening methods to the underestimation of disease
prevalence cause by astroviruses, caliciviruses and SRVs.
Payne et al. (1986) studied viral agents associated with gastroenteritis over an 8-year
period. Of the stool specimens submitted, 41% were positive for viruses or virus-like
particles belonging to 7 groups: coronavirus-like particles were present in 69.8% of positive
specimens, rotavirus in 17%, adenovirus in 4.5%, picornavirus/parvovirus agents in 2.9%,
Norwalk-like agents in 2.9%, astrovirus in 1.9%, and calicivirus in 0.5%, with 0.5%
unclassified SRVs. Excretion of all viruses except coronavirus-like particles exhibited a
seasonal distribution, with the majority of viruses being identified in the cooler, drier
months.
The Norwalk agents cause -36% of the outbreaks of infectious, nonbacterial
gastroenteritis; they have been-transmitted by ingestion of contaminated food and water
(Righthand, 1983). Keswick et al. (1985) suggest that the Norwalk agent is responsible for
-23% of all reported waterborne outbreaks.
The total reported cases of hepatitis A was 28,507 in 1988, the highest number
reported since 1980. Total poliomyelitis cases were 9 in 1988 with a range of 6-34 cases
annually over the past 20 years (CDC, 1989).
In children between 6 and 24 months, rotavirus is the most frequent cause of
nonbacterial gastroenteritis, but frequently neonatal infections are asymptomatic. Rotavirus
infections occur less frequently among children 5 years old or older because by age 5 they
have acquired circulating antibody to rotavirus (Estes et al., 1983). The spread of rotaviral
infections is poorly understood, but it is thought that air may be a vehicle for these viral
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outbreaks (Ijaz et al., 1985c). Viral survival was greatest at 50% relative humidity, and
reducing the temperature from 20°C to 6°C enhanced that survival. Even after 24 hours,
there was only a 30% reduction in infectivity of the virus. In addition, rotavirus suspended
in fecal matter from an infant with rotaviral diarrhea survived longer as an aerosol than
rotavirus suspended in tryptose phosphate broth (TPB). After 24 hours, the fecal suspension
rotavirus lost <20% infectiviry compared with a 50% reduction in infectivity under the same
conditions for the TPB suspension of rotavirus (Ijaz et al., 1985c). These results support the
suggestion of Brandt et al. (1982) that a low outdoor temperature, low indoor relative
humidity and indoor crowding may contribute to rotavirus survival and spread of rotavirus
infections. Likewise, epidemiologic observations seem to correlate rotaviral gastroenteritis
outbreaks with climate, i.e., outbreaks in cool, dry weather of tropical climates and during
winter in temperate zones (Ijaz et al., 1985c; Brandt et al., 1982).
Ward et al. (1986), in their study of infectious dose of rotavirus in adults, suggest
several problems with epidemiologic understanding of adult rotavirus infections. They point
out that many cases of adult gastroenteritis may be caused by rotavirus because the dose
required to cause infection and illness is very small (1-10 ffu). The lack of evidence of high
incidence of adult rotavirus illness could be because infected adults may manifest the disease
differently than children or because the amount of virus shed by infected adults is below
detection limits of current assay methods.
Most of the well-known viruses that are dangerous to fetuses of women infected with
systemic viral illness during pregnancy, such as rubella, cytomegalovirus, and herpesvirus
(Gold and Nankervis, 1989; Nahmias et al., 1989), are not typically found in sewage sludge.
It should be recognized, however, that some viruses that may be present in sludge have been
found to be associated with risk of adverse effects on the fetus or neonate. These include
human parvovirus B19, which can result in fetal hydrops and death (Levy and Read, 1990)
and enteroviruses, such as echovirus and coxsackievirus B, associated with fetal heart effects
and neonatal disease ranging from asymptomatic infection to death (Modlin, 1988;
Rosenberg, 1987).
It appears that the difficulties inherent in epidemiologic studies are particularly
significant in determining the incidence and distribution of viral infections and diseases.
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More research is needed in this area to characterize the potential public health risks
associated with transmission of viruses by application of sludge and wastewater.
3.2. ENTERIC VIRUSES IN TREATED SLUDGE
The frequency of isolation and the quantity of virus recovered from sewage depend
upon water use in a community, the day and season of sample collection, the level of
infection in the population and the efficiency of recovery procedures (Rao et al., 1986).
Concentrations of viruses in wastewater in the United States vary greatly, reflecting the
infection and carrier status of the population. The larger the contributing population, the
more uniform the viral concentrationbecom.es. Concentrations tend to peak in late summer
and early fall when enteric viral infections increase (Kowal, 1985).
3.2.1. Effects of Treatment Processes. Wastewater treatment processes are less effective
in removing viruses than in removing bacteria (Sobsey et al., 1980). Viruses in wastewater
tend to become adsorbed to suspended particles; consequently, during primary, and
secondary sewage treatment processes, viruses will be removed from the wastewater and
concentrated in the sludge. Chlorination is not as effective in destroying viruses in effluent
wastewater as it is in killing bacteria (Feachem et al., 1983). Viruses in wastewater may be
protected by particulates so that longer exposure times or higher chlorine concentrations
may be required to destroy them (Sproul, 1978). According to Hurst (1989), wastewater
sludges cannot be readily disinfected by chlorine because of their solid nature and high
organic content.
The most important factors affecting the stability of viruses in wastewater sludges are.
temperature, loss of moisture, and the presence of aerobic microorganisms. Other factors
affecting viruses in sludges are pH levels; presence of detergents, ammonia and certain salts;
and the type of virus (Hurst, 1989).
In his review of density levels of pathogenic organisms in municipal wastewater
sludges, Pedersen (1981) concludes that levels of enteroviruses in primary and secondary
sludges are similar; few data were available on levels of enteric viruses in mixed sludge.
Primary sludge has received primary treatment such as screening and settling; secondary
3-12
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sludge is produced by biologic waste treatment, or secondary treatment; primary and
secondary sludge are combined to produce mixed sludge (U.S. EPA, 1986).
Conventional sludge treatment processes designed to stabilize sludge and reduce
volatile solids also lower densities of pathogens in sludge to varying degrees. These
processes are: (1) anaerobic digestion, the microbiologic degradation of the organic matter
in sludge in the absence of oxygen; (2) aerobic digestion, the biochemical oxidation of
organic matter; (3) composting, the natural, aerobic microbiologic process of decomposing
organic matter to produce humus; (4) lime stabilization, the application of lime to sludge
to raise the pH; and (5) air drying, exposure of a layer of sludge to air to drain or dry.
These sludge treatment processes reduce but do not eliminate viruses (Melnick, 1987). U.S.
EPA has established regulations in 40 CFR 257 for these processes to qualify as Processes
to Significantly Reduce Pathogens (PSRP). Additional processes, either singly or in
combination with PSRPs, have been defined as Processes to Further Reduce Pathogens
(PFRPs).
Anaerobic Digestion. Following high-rate anaerobic digestion at 35°C, Jewell et al.
(1980) and Berg and Berman (1980) report log reductions for enteroviruses of 1.36 and 1.05,
respectively. Eisenhardt et al. (1977) and Sanders et al. (1979) found that by raising the
temperature 3°C during mesophilic anaerobic digestion, two- to four-fold increases in viral
inactivation rates were achieved. In full-scale anaerobic digesters, Ohara and Colbaugh
(1975) observed that mesophilic digestion achieved a 1 log reduction in virus content while
thermophilic digestion achieved a 3 log reduction. Although virus reductions of 1 log
(90%)/day at 30°C have been demonstrated in studies of anaerobic digestion with seeded
enterovirus, Moore et al. (1978) reported a reduction of 1 log/week at 30°C for poliovirus
when it was bound to the sludge solids.
During sludge treatment processes, temperature is not always the most important
factor responsible for virus inactivation; the relative effects of heat are dependent on the
temperature range (Traub et al., 1986). When the effects of mesophilic and thermophilic
anaerobic digestion and aerobic thermophilic fermentation were examined, heat accounted
for 19% of bacteriophage f2 inactivation at 34.5°C (mesophilic anaerobic digestion), for
32% at 54.5°C (thermophilic anaerobic digestion) and, in combination with pressure, for
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100% of inactivation at 60°C (aerobic thermophilic fermentation). The authors of this study
suggest that enteric viruses would be inactivated by 1 day of thermophilic anaerobic
digestion (54-55°C) and that virus recovery after thermophilic digestion, as reported by
Lund (1971) and Berg and Berman (1980), probably resulted from short circuiting in the
sludge digesters.
Inactivation rates will vary with the type of virus. Bertucci et al. (1977) report
significant differences in inactivation rates among viruses during mesophilic anaerobic
digestion. Poliovirus I (Sabin) was 98.8% inactivated after 2 days of digestion at 35°C.
According to Spilhnann et al. (1987), mesophilic anaerobic digestion achieved only
minor inactivation of a human rotavirus, coxsackievirus B5, and bovine parvovirus. With
thermophilic digestion, the rotavirus and coxsackievirus were rapidly inactivated; the
parvovirus was heat stable. Temperature was the predominant contributor to total
inactivation only for processes above 54°C. The authors classify these viruses as:
thermolabile/comparatively chemoresistant (rotaviruses and enteroviruses), and
thermostable/chemolabile (parvoviruses). "Chemoresistant" is defined as relatively
insensitive to ammonia, detergents arid microbial factors in the sludge.
The presence of aqueous ammonia enhanced the inactivation of poliovirus types 1
and 2, coxsackievirus A13 and Bl and echovirus 11 during anaerobic digestion, according
to Ward (1977). However, reovirus was insensitive to the concentration of ammonia.
Cationic detergents present in wastewaters increase susceptibility of reoviridae to heat
inactivation; these same detergents protect enteroviruses from heat (Goddard et al., 1981;
Ward et al., 1976).
Although sludges with undetectable viral levels were not produced by any of the
treatments examined, anaerobic mesophilic digestion with subsequent thickening and aerobic
thermophilic digestion were both found to be efficient in reducing infectious virus
concentrations (Goddard et al., 1981). Anaerobic mesophilic digestion alone was not
reliable in reducing virus levels in sludge.
Large quantities of sludge that had been anaerobically digested and lagooned were
applied to a 15,000-acre site in central Illinois by the Metropolitan Sanitary District of
Greater Chicago during 1971-1978 (MSDGC and IIT Research Institute, 1979). Water, soil,
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and sludge sampling detected no viruses in the sludge product applied or sprayed and no
effects on the surface or groundwater at the site.
Aerobic Digestion. In laboratory bench studies of mesophilic aerobic digestion,
Scheuerman (1984) observed log reductions of 0.219-0.779 for poliovirus type 1, 0.189-0.59
for echovirus, 0.439-0.449 for rotavirus SA-11, and 0.469 for coxsackievirus. Ward et al.
(1984) conclude that standard aerobic digestion probably achieves pathogen reductions equal
to or greater than those achieved in mesophilic anaerobic digestion.
Composting. Although hepatitis A has been shown to withstand temperatures of
80°C, most enteric viruses succumb to composting temperatures (U.S. EPA, 1988; Pedersen,
1981). Inactivation depends on equal distribution of heat throughout the compost pile
(Englande, 1983). In seeding experiments with bacteriophage £2, which is more heat
resistant than most enteric viruses, Burge et al. (1978) studied the effects of windrow and
static pile composting methods on viral inactivation. Virus concentrations in windrows
decreased 90% every 4-7 days in dry weather, and 50% of this rate in wet weather.
Reductions were greater in aerated piles. According to Ward et al. (1984), enteric viruses
would be inactivated at greater rates; but some viruses, such as hepatitis A and parvoviras
(Spillman et al., 1987), may be more heat resistant.
Lime Treatment and Air Drying. According to Ward et al. (1984), it has not been
shown that viruses in sludge are inactivated by lime treatment, but viruses have been shown
to be destroyed rapidly at high pH values. Pedersen (1981) reports a single laboratory-scale
study (Sattar et al., 1976) in which a >4-log reduction of poliovirus type 1 was achieved in
the sludge product resulting from injection of the virus into raw sewage that was limed to
pH 11.5, settled and centrifuged.
Ward and Ashley (1977) observed that the air drying process inactivates enteric
viruses in sludge. Inactivation of enteric viruses seeded into raw sludge was proportional
to water loss until the sludge reached -70% solids; viral concentrations decreased 3 orders
of magnitude between 70 and 90% solids. The drying process itself apparently causes the
inactivation since storage of viruses in sludge at low moisture levels has little effect on
persistence. Similar results were observed for indigenous viruses in air-dried sludge by
Brashear and Ward (1983).
3-15
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Conclusions. Ward et al. (1984), U.S. EPA (1988), Hurst (1989), Rao et al. (1986),
Englande (1983) and Yanko (1988) discuss the potential for reduction of enteric viruses by
conventional sludge treatment processes. Ward et al. (1984) summarize viral reductions in
sludge treatment processes as follows:
anaerobic digestion (mesophilic) 0.5-2 log reductions
aerobic digestion 0.5-2
composting 2->4
air drying 0.5-> 4
lime stabilization >4
They conclude that composting is the best of conventional sewage treatment methods since
the high temperatures destroy most sludge pathogens. The results of Yanko (1988) support
the conclusions of Ward et al. (1984).
322. Density of Viruses in Treated Sludge. Viral densities in raw sewage will vary with
season, region, and the nature and sizeiof the population. Akin and Hoff (1978) report that
the concentration of viruses in raw wastewater is most often < 1000 units/L; however, Sorber
and Guter (1975) estimate 7000 PFU/fL. Gerba (1983a) reports a range of 2-215 enteric
virus units/g of raw sludge in the United States. According to Booz-Allen and Hamilton,
Inc. (1983), the density of viruses in raw sludge is several hundred PFU/L, and Melnick
(1987) reports virus concentrations of 5000-28,000 PFU/L in raw sludge. Ward et al. (1984)
report densities of 102-104 enteric viruses/g dry weight in primary sludges and SxlO2
organisms/g dry weight in secondary sludges. U.S. EPA (1988) and Pedersen (1981) report
average geometric mean values for enteric viruses of 3.9xl02 PFU/g dry weight in primary
sludge, 3.2X102 PFU/g dry weight in secondary sludge, and 3.6X102 TCID50 in mixed sludge.
Due to the limitations of recovery procedures, the actual numbers of viruses in sludges and
wastewater could be 1-2 logs higher thdm those reported (Akin et al., 1978). Table 3-3 lists
virus densities in treated sludge.
Anaerobic Digestion. Limited data are available on the effects of sludge treatment
processes on indigenous sewage viruses. Mesophilic anaerobic digestion results in significant
decreases (90%) in viral concentrations, and thermophilic digestion reduces concentrations
by at least 99% (Berg, 1978). The results of Jewell et al. (1980), Berg and Berman (1980)
; 3-16
-------
TABLE 3-3
Virus Densities in Sludge
Virus
Enteroviruses
Enteroviruses
Enteroviruses
Enteroviruses
Enteroviruses
Enteroviruses
Enteroviruses
Enteroviruses
Enteric Viruses
Enteric Viruses
Enteric Viruses"
Sludge
Treatment
Process
Anaerobic
Digestion
High Rate
Anaerobic
Digestion
High Rate
Anaerobic
Digestion
High Rate
Anaerobic
Digestion
Aerobic
Digestion
Aerobic
Digestion
Aerobic
Digestion
Aerobic
Digestion
None
Anaerobic
Digestion
Anaerobic
Digestion
Mean
Density
no/100 mL
5.9 PFU/100
mL, range 13-
17 PFU/100
mL
19 PFU/100
mL, range
4-100
138 PFU/100
mL, range 30-
410
<3.3 PFU/100
mL, range
< 1.4-16.7
0.3-1.2
TCID50/g dry
wt
ND
53TCID50/g
dry wt, range
14-260
TCID50/g dry
wt
3.35 PFU/g
dry wt
2-215 units/g
0.04-17 units/g
0.007 PFU/mg
TSS
Detention
Time
(days)
12,8
21
20
20
90
180
30
3
Conditions
30°C,
7-10°C
35°C
35°C
49°C
mesophilic
mesophilic
mesophilic
mesophilic
Reference
Cliver, 1975
Jewell et al.,
1980
Berg and
Berman, 1980
Berg and
Berman, 1980
Bitton et al.,
1980
Bitton et al.,
1980
Bitton et al.,
1980
Hurst et al.,
1978
Gerba, 1983a
Gerba, 1983a
Moore et al.,
1978
3-17
-------
TABLE 3-3 (continued)
Virus
Enteric Viruses
Enteric Viruses
Enteric Viruses
Enteric Viruses
Picornavirus
(ECHO)
Picornavirus
(ECHO)
Reoviruses
Echovirus type 7
Viruses
Viruses
Viruses
Sludge
Treatment
Process
3 stage
Anaerobic
digestion
Anaerobic
Digestion
Anaerobic
Digestion
Aerobic
Digestion
Windrow
Composting
Static Pile
Composting
Anaerobic
Digestion
Sand Drying
Mesophilic
Digestion
Thermophilic
Digestion
Anaerobic
Digestion
Mean
Density
no/100 mL
12.
MPNCU/100
mL, range 0-19
MPNCU/100
mL
0.007 PFU/mg
TSS
0.007-0.04
PFU/mg TSS
0-260 units/g
<2.3 PFU/g
<2.3 PFU/g
8 PFU/100
mL, range 6-17
PFU/100 mL
0.1 PFU/g
50-360
PFU/100 mL
1.7-16.7
PFU/100 ml.
2.1 PFU/g
0.03 PFU/g
Detention
Time
(days)
40
5
40-90
21
composting,
30 curing
12,8
!3
20
20
Conditions
33°C (for 10
days)
30°C,
7-10°C
~35°C
49°C
mesophilic
thermophilic
TCED50 « Tissue culture infectious dose for 50% response
ND « Not detected
MPNCU = Most probable number of cytopathogenic units
TSS - Total suspended solids
Sources: Pedersen, 1981; U.S. EPA, 1988; Kowal, 1985.
Reference
Palfi, 1972
Moore et al.,
1978
Moore et al.,
1978
Gerba, 1983a
Yanko, 1988
Yanko, 1988
Cliver, 1975
Wellings et al.,
1976
Berg, 1978
Berg, 1978
Ohara and
Colbaugh,
1975
3-18
-------
and Oliver (1975) suggest a range of mean densities for enteroviruses of 5.9-138 PFU/100
mL following mesophilic digestion, and Berg and Berman (1980) report a mean density of
<3.3 PFU/100 mL after anaerobic digestion under thermophilic conditions.
Aerobic Digestion. Little research has been done on the effects of mesophilic aerobic
digestion on viral pathogens in sludge (U.S. EPA, 1988). Bitton et al. (1980) tested sludges
for enteroviruses at 30, 90, and 180 days following mesophilic aerobic digestion. No viruses
were detected after 180 days, and mean concentrations were greatest (53 TCID50/g dry
weight) with the shortest digester time (30 days). Kabrick et al. (1979) report that virus
concentrations (in total PFUs) are below detection levels when the digestion temperature
is >40°C and pH is >7.
Composting. Most studies of viral inactivation during composting have involved
seeding of viruses prior to mixing the piles. A recent U.S. EPA study looked at indigenous
pathogens in sludge following composting. An aerated static pile composting facility and a
windrow composting facility designed to meet PFRP criteria were sampled weekly for a year
by Yanko (1988). Elution/concentration techniques proven effective for high-solid samples
were used in viral testing, and, in addition to several procedures on two cell lines in the
project laboratory, samples were tested by different procedures in two other laboratories.
However, during the testing period, indigenous viruses (untypable picornavirus) were found
in only two samples, one from each facility. Isolates from "blind seeds" were found in six
other samples. The picornavirus was found at a level below the quantitative limit for the
plaque assay, <2.3 PFU/g. During the bimonthly sampling for a year of 24 treatment
facilities (including anaerobic and aerobic digestion, heat drying, and composting facilities),
viruses were detected in only one sample and were probably laboratory contaminants,
according to the author. Yanko (1988) concludes that none of the treated sludges in this
study produced viral health hazards since only two low-level isolations were made from
many samples.
Lime Stabilization and Air Drying. Little research has been done on the
effectiveness of the lime stabilization process in destroying indigenous sludge viruses,
although viruses are known to be destroyed by high pH (Ward et al., 1984). Koch and
3-19
-------
Strauch (1981) report inactivation of poliovirus in raw and digested sludges at pH levels
resulting from lime treatment.
Several studies have reported the detection of indigenous enteric viruses in lime
sludges at pH 10 or 10.5 (Pancorbo et al., 1988). Pancorbo et al. (1988) suggest that the pH
achieved and maintained determines the effectiveness of this treatment. In then-
experiments, almost complete inactivation of seeded poliovirus type 1 was attained when
alum sludge was treated with lime at pH 11.5. Similarly, when Sattar et al. (1976) treated
raw sewage with lime at pH 11.5, only 0.005% of the poliovirus type 1 input was recovered
from the lime sludge. In the United Kingdom, Goddard et al. (1982) did not detect
indigenous enteroviruses in sludge conditioned with lime at pH 11.
Laboratory studies and seeding experiments suggest that air drying is an effective
method of inactivating enteric viruses (Ward et al., 1984). Wellings et al. (1976) reported
a 0.1 PFU/g concentration of echovirus type 7 from a full-scale sand drying bed facility for
sludge treatment. Dewatering of sludge by evaporation inactivated human poliovirus,
coxsackieviruses and reoviruses (Ward and Ashley, 1977).
Conclusions. According to Feachem et al. (1983), "any sludge treatment process that
involves temperatures of 50°C or above should yield a virus-free product if the process is
well controlled and carried out for sufficiently long to ensure that all parts of the mass are
heated." However, results reported in a more recent review (Rao et al., 1986) suggest that
higher temperatures may be necessary to ensure virus inactivation. They report that HAV
was not inactivated after heating to 60°C for 12 hours and was infective at 80°C in the
presence of high concentrations of some salts.
Other factors affect virus persistence in relation to temperature. Ward et al. (1976)
report that an ionic detergent protected poliovirus from heat in raw sludge. Detergents
from wastewater become associated with solids and are concentrated in sludges.
Composting causes degradation of the detergents; poliovirus is more readily inactivated
during composting, but the survival of reovirus is enhanced (Ward and Ashley, 1978).
Aqueous ammonia, which is formed during anaerobic digestion, added to raw sludge
speeds inactivation, allowing moderate heat treatment to inactivate enteroviruses.
3-20
-------
Adsorption of virus particles to sludge particles may protect them from heat inactivation and
from inactivation by ammonia (Ward and Ashley, 1978).
After monitoring a human rotavirus, a coxsackievirus B5, and a bovine parvovirus
during sludge treatment processes, Spillman et al. (1987) conclude that the best treatment
to eliminate viruses from sludge would be thermal (60°C) treatment to inactivate
thermolabile viruses, followed by anaerobic mesophilic digestion to eliminate thermostable
viruses that are sensitive to chemicals and microbes.
3.3. OCCURRENCE OF VIRUSES IN NATURAL MEDIA
3.3.1. Persistence in Soil. Persistence of viruses in the subsurface is dependent upon the
type of virus, the nature of the soil, and the climate of the environment (Yates and Yates,
1988). Although specific factors that control the fate of viruses in soil have been identified,
interactions between factors make consideration of separate effects difficult. Factors known
to affect the fate of viruses in the environment include: temperature, microbial activity,
moisture content, pH, salt species and concentration, soil properties, virus association with
soil, virus aggregation, virus type and organic matter. In many cases, the mechanisms by
which these factors influence viral inactivation or protection are not clear. Table 3-4
summarizes data on virus persistence in soils.
Temperature. Temperature is probably the most important factor influencing
persistence and inactivation of viruses in the environment (Yates and Yates, 1988; Gerba
and Bitton, 1984; Bitton, 1978). Most enteric viruses are inactivated at temperatures of
60°C or above (Morris and Darlow, 1971); however, some types, such as hepatitis A, have
been shown to withstand higher temperatures (U.S. EPA, 1988). Hurst et al. (1980a)
observed that in vials of soil the inactivation rate for poliovirus increased as temperature
increased, and Lefler and Kott (1974) made a similar observation with poliovirus in a sandy
soil in Israel. This relationship of viruses to soil temperatures has been confirmed by other
studies (Gerba and Bitton, 1984). Viruses persisted up to 170 days in waste-treated soil at
3-10°C, according to Bagdasar'yan (1964). After irrigation of crops with sewage effluent,
the time for 99% inactivation of viruses in soil was 2 months during winter but 2-3 days in
summer (Larkin et al., 1976a; Tierney et al., 1977).
3-21
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TABLE 3-4
Virus Inactivation in Soil
Virus
—
Poliovirus
typel
Inactivation
Rate in
Days
T90 T99
455
152
588
323
31
10
30
33
3.0
1.4
1.7
3.5
Inactivation
Rate
Constant
(Iog10 day'1)
0.0022
(0.000092/hr)
0.0066
(0.00027/hr)
0.0017
(0.000071/hr)
0.0031
(0.00013/hr)
0.0323
(0.00135/hr)
0.1035
(0.0043/hr)
0.0338
(0.00141/hr)
0.0304
(0.00126/hr)
0.3331
(0.0139/hr)
0.7077
(0.0294/hr)
0.5809
(0.0242/hr)
0.2884
(0.0120/hr)
Sludge
Treatment/
Application
Inoculated viruses
applied to vials of
soil in:
Aerobic:
Sterile media
Nonsterile media
Anaerobic:
Sterile media
Nonsterile media
Aerobic:
Sterile media
Nonsterile media
Anaerobic:
Sterile media
Nonsterile media
Aerobic:
Sterile media
Nonsterile media
Anaerobic:
Sterile media
Nonsterile media
Conditions
Sandy loam
soil, pH 7.8
1°C
1°C
23°C
23°C
37°C
37°C
Reference
Hurst, 1988b
3-22
-------
TABLE 3-4 (continued)
Virus
Poliovirus
Poliovirus
Viruses
Viruses
Inactivation
Rate in
Days
90 99
Not given
Not given
Not given
Not given
Inactivation
Rate
Constant
(Iog10 day'1)
0.10
(0.0042/hr)
0.09
(0.0038/hr)
0.04
(0.0017/hr)
0.16
(0.0068/hr)
1.45 avg.
(0.060/hr)
(0.04 min.
(0.0017/hr),
3.69 max.
(0.154/hr)}
0.26
(0.0108/hr)
0.2171
(0.0091/hr)
0.057
(0.0024/hr)
0.2796
(0.0116/hr)
0.328
(O.OB7/hr)
Sludge
Treatment/
Application
Soil flooded with
inoculated
secondary
effluent
Soil treated with
sewage sludge
In forest soil
Soil/water/plant
system
Aerobically
digested sludge,
indigenous
viruses
Conditions
Not given
4°C
20°C
Not given
Late summer
(20-31°C daily
temp)
No rain
Moderate rain
Reference
Larkin et al.,
1976a
Duboise et
al., 1974
Reddy et al.,
1981
Hurst et al.,
1978
3-23
-------
Inactivation at higher temperatures may result from protein denaturation of the viral
capsid (Yates and Yates, 1988). Dimmock (1967) suggests that at temperatures >44°C,
viral inactivation is associated with structural changes in the viral capsid; but at temperatures
<44°C, inactivation depends on the inactivation rate of viral nucleic acid. Temperature
also has an indirect effect on virus persistence due to its effect on the growth of aerobic
bacteria (Lance and Gerba, 1982).
Soil Moisture Content. According to Bitton et al. (1987) and Gerba and Bitton
(1984), temperature and soil desiccation synergistically influence the fate of viruses in the
soil environment. In their review of virus survival in nature, Bitton et al. (1987) report that
temperature and moisture are the primary controls of viral persistence in sludge-amended
soil, and Bitton et al. (1981) report that soil drying is a major detrimental factor in viral
persistence in sludge-soil mixtures. During development of methods for the detection of
enteroviruses in sludges, Hurst et al. (1978) applied aerobically digested sludges to land and
subsequently found reductions of naturally occurring enteroviruses at a rate of 2 Iog10/week.
After 3 months in the field, no viruses were detected in sludge solids. The authors suggest
that virus inactivation in the sludge solids was directly related to desiccation.
When columns of sand treated with sludge were exposed to warm, dry fall weather
(<0.13 cm cumulative rainfall), infectivity of seeded echovirus and poliovims declined more
rapidly than when the columns were exposed to wet summer weather (> 13 cm cumulative
rainfall) (Bitton et al., 1981,1984). Bagdasar'yan (1964) reports that enteroviruses, including
poliovirus 1, coxsackievirus B3, and echoviruses 7 and 9 persisted 2-3 months in soil with
10% moisture compared with 15-25 days in air-dried soils. Poliovirus type 1 inactivation was
much more rapid in drying soil (1 week for 99% inactivation as moisture decreased from
13% to 0.6%) than in soils maintained at higher moisture levels (7-8 and 10-11 weeks for
99% inactivation at levels of 25 and 15%, respectively) (Sagik et al., 1978). During rapid
infiltration of wastewater in a field study, Hurst et al. (1980b) found that viral inactivation
rates were higher in rapidly drying soil. Periodic drying followed by aeration was found to
enhance viral inactivation.
Comparing the inactivation rate of poliovirus in eight soils saturated ¥/ith river water,
groundwater, or septic wastewater with the same soils allowed to dry out, Yeager and
3-24
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O'Brien (1979a) noted a sharp increase in inactivation rate at 1.2% soil moisture compared
with the rate at 2.9%. Hurst et al. (1980a) found that viral survival did not correlate linearly
with soil moisture, but decreased with increasing moisture up to the saturation point, then
increased with moisture beyond that point. Possible explanations for this enhanced survival
at both high and low soil moisture levels include differences in extent of viral adsorption to
soil, in mechanisms of adsorption, and in microbial growth rates at various soil moisture
levels.
Yeager and O'Brien (1979a) used radiolabeled viruses to show that viruses did not
become irreversibly bound to soil particles but were inactivated during the drying process.
Yeager and O'Brien (1979b) suggest that the mechanisms for viral inactivation in moist soils
are different from the mechanisms in drying soils.
Microbial Activity. Microbial activity may play a role in the inactivation of viruses
in soil. Although some studies (Gerba and Bitton, 1984) have not observed any difference
in viral decline in sterile and nonsterile soils, others noted greater inactivation in nonsterile
soil. The inactivation rates of poliovirus and reovirus were found to be greater in nonsterile
soil suspensions than in sterile soil suspensions (Sobsey et al., 1980). Comparing four
different combinations of aerobic/anaerobic and sterile/honsterile conditions on poliovirus
type 1, Hurst (1988b) observed that aerobic microorganisms exerted a statistically significant
effect on the rate of viral inactivation in sandy loam soil at three incubation temperatures
(1, 23, and 379C). He concludes that microbial antagonism appears to be a major
determinant of viral stability in soil and suggests that the antagonism results from metabolic
products released from bacteria or from interference with adsorption onto soil particles.
Mechanisms of virus inactivation by microbes in soil have not been clarified at this point.
Sobsey et al. (1986) report a temperature effect on the antiviral activity of microbes.
Sterile and nonsterile soil samples gave similar survival rates for HAV, poliovirus type 1,
and echovirus type 1 at 5°C, but at 25°C the time for inactivation of all three viruses was
shorter in the nonsterile samples.
p'H. Bitton (1978) asserts that, in general, enteric viruses will not be affected by the
pH values of the natural environment. The direct effects of pH on viral persistence in soil
have not been studied extensively. Reported results indicate that pH can influence virus
3-25
-------
inactivation, but the extent of this influence is not clear (Sobsey and Shields, 1987). Hurst
et al. (1980a) observed that poliovirus 1 and bacteriophages MS-2 and T2 persisted longer
at lower soil saturation pH values. The results of Salo and Oliver (1976) with aqueous
solutions indicate that inactivation by pH varies with the type of virus. Various mechanisms
have been suggested for the direct effects of pH on virus persistence, including alterations
in the viral capsid and increase in sensitivity of the nucleic acids to DNase or ribonuclease
(Yates and Yates, 1988).
In addition, pH may have indirect effects on viral persistence by affecting adsorption.
Above pH 7, the net charge on the virus particle is negative; and sand, clay minerals, and
organic matter are also negatively charged at pH>7 (Gerba and Bitton, 1984). Although
adsorption would appear to be at a minimum at alkaline pH values, conflicting reports in
the literature indicate that this relationship is not clear-cut (Gerba and Bitton, 1984).
Salt Species and Concentration. Inactivation of enteroviruses in the environment can
be influenced by salt species and their concentrations. Several investigators have reported
that poliovirus, echoviruses, and bacteriophages were less susceptible to thermal inactivation
in the presence of certain cations (e.g., Ca and Mg) in the media (Yates and Yates, 1988).
According to Gerba and Bitton (1984), this phenomenon may be significant to viral
persistence in soil. Several studies have indicated that the type and concentration of salts
in the soil affect virus adsorption to soil, adsorption increasing with increasing ionic strength
(Yates and Yates, 1988).
Organic Matter. Organic matter may have a protective effect on the persistence of
viruses in soil. Although Hurst et al. (1980a) did not find that virus persistence was
significantly related to the amount of soil organic matter, Lefler and Kott (1974) found that
poliovirus persisted longer in sand watered with waste pond effluent than with distilled
water.
Organic matter has been found to decrease virus adsorption by competing for sites
on soil particles (Yates and Yates, 1988). Moore et al. (1981) and Bitton et al. (1976)
report that organic matter interfered with viral adsorption in soil, indirectly affecting viral
persistence; and other investigators report that organic material acts as an eluting agent,
desorbing viruses from the soil (Gerba, 1984a). Humic and fulvic acids have also been
3-26
-------
reported to prevent adsorption and to cause loss of virus infectivity (Yates and Yates, 1988).
The effects of organic matter on soil properties such as pH, moisture content, and ion
exchange capacity may indirectly influence the persistence of enteric viruses in soils (Sobsey
and Shields, 1987).
Adsorption. Depending upon the sorbent, the survival of viruses may be enhanced
or reduced by adsorption to soils or other materials (Yates and Yates, 1988). Significant,
rapid inactivation of poliovirus type 1 occurred in soil after its adsorption to manganese,
aluminum, and copper oxide particles but not after adsorption to silica and iron oxide,
according to Murray and Laband (1979). Moore et al. (1982) report that reovirus
adsorption to organic muck, montmorillonite, dolomite, and Ottawa sand resulted in
considerable inactivation. Sobsey et al. (1980) found that survival was not prolonged in
every case when poliovirus type 1 and reovirus type 3 adsorbed to eight different soil
materials.
Recent studies indicate that adsorption of virus particles by the soil is a major factor
in virus persistence (Gerba, 1985). In their experiments, Hurst et al. (1980a) found that soil
adsorption was one of the most important of the factors that significantly affected viral
survival, with survival increasing with greater adsorption. The enhanced survival of viruses
in soil with a high adsorption capacity presents a dilemma for land application of wastes.
Although adsorption of viruses prevents their movement to the groundwater, soils with this
capacity are likely to enhance virus survival (Hurst et al., 1980a).
Gerba and Schaiberger (1975) suggest several mechanisms by which adsorption of
virus particles to various solids may enhance or reduce their survival. Among these are
interference with the action of virucides, increased stability of the protein capsid, prevention
of aggregate formation, and adsorption of enzymes and other inactivating substances.
Formation of Aggregates. Although there are no studies on the relationship of
aggregate formation to viral persistence in soil, the fact that aggregates affect virus
persistence in water suggests that aggregates might protect viral particles from
environmental factors in the soil (Yates and Yates, 1988; Sobsey and Shields, 1987).
Soil Characteristics. Soil properties probably influence viral persistence by affecting
the degree of adsorption of virions to soil particles (Yates and Yates, 1988), According to
3-27
-------
Bitton et al. (1987), the relationship of soil type to virus persistence is difficult to determine
because of the influence of other environmental factors. Mineral and organic content of
soil, moisture level, pH, and cation exchange capacity (CEC) affect viral persistence in soil
and are related to soil type.
Hurst et al. (1980a) found that virus survival was significantly correlated to adsorption
and to soil saturation pH but not to other soil characteristics. However, stepwise multiple
regression analysis of virus survival and 19 soil characteristics revealed that extractable
phosphorus and exchangeable aluminum were the next highest ranking of soil characteristics
affecting survival. Hurst et al. (1980a) suggest that the relationship between survival and
aluminum is due to the increase in virus adsorption at high aluminum levels, and the
increase in virus survival with decrease in level of resin-extractable phosphorus is due to
increased adsorption at lower levels of resin-extractable phosphorus.
Fine-textured soils that contain clay remove more viruses by adsorption than coarse-
textured soils (Yates and Yates, 1988; IGerba and Bitton, 1984). Gerba and Bitton (1984)
observe that humic materials and clay minerals are the two most active components of the
soil. Clays increase viral adsorption to soil as well as influencing survival of microbial
populations in the soil; survival of microbes could be influenced by water that may be tightly
bound to clay. Also, clay can be protective to the viral genome.
The soil CEC may indirectly affect persistence of viruses by influencing adsorption.
The work of Sobsey (1983) and others indicates that virus adsorption increases with
increasing CEC, as well as with clay content, exchangeable aluminum and low flow rate.
In examining the retention of poliovirus by 34 soils and minerals, Moore et al. (1981)
found that adsorption was negatively correlated with soil organic matter and with available
negative surface charge. Adsorption was not significantly correlated with soil pH, surface
area or elemental composition. Their results indicate that soils are potentially efficient at
binding viruses since 106 viruses adsorbed to a gram of Ottawa sand with only 1% of the
surface covered. Sobsey and Shields (1987) report that minerals were better adsorbents
than soils in some studies. According to Gerba and Bitton (1984), soil iron oxides have
been shown to increase the retention of viruses in soil. Magnetite sand adsorbed 99.99%
of virus particles while muck soil retained 16-79%.
3-28
-------
Van der Waals forces, double-layer interactions, and hydrophobic interaction are
discussed by Gerba (1984a) as mechanisms for viral adsorption to soil particles.
Type of Virus. Susceptibility to inactivation in soil may vary with the type of virus
and the particular strain. According to Lefler and Kott (1974), bacteriophage £2 survived
longer than poliovirus in saturated and in dry sand. Hurst et al. (1980a) found different
inactivation rates for seven viruses under the same conditions. The inactivation rates of
poliovirus, reovirus, echovirus and HAV in several types of soil material at 25°C were quite
different, although all three survived well in soil suspensions at 5°C (Sobsey et al., 1986).
Goyal and Gerba (1979), studying a number of viruses including human enteroviruses, found
strain and type differences in adsorption to soil.
3.3.2. Persistence in Water. Viruses persist longer in groundwater than hi surface waters;
Keswick et al. (1982) attributes this to lower temperatures, protection from sunlight, and
lack of microbial antagonism in groundwater. For poliovirus type 1, the decay rate reported
by Bitton et al. (1983a) was 0.0019 hr'1 in groundwater, and O'Brien and Newman (1977)
report a decay rate of 0.031 hr"1 in river water. A field study by Wellings et al. (1975)
suggests that viruses persist for up to 28 days in groundwater, and Sattar (1981) reports
persistence of 560 days in surface water in the laboratory. In natural waters, several
interacting factors, including temperature, chemicals, pH, light, biologic factors and
suspended particulate matter, affect virus persistence (Melnick and Gerba, 1980).
Table 3-5 summarizes data on virus inactivation in water. Virus inactivation follows
apparent first-order kinetics (O'Brien and Newman, 1977). Virus inactivation curves in
aquatic systems range from linear to S-shaped, with variations being a result of clumping of
the viruses (Berg et al., 1967). O'Brien and Newman (1977) attributed S-shaped curves to
higher initial virus titers (> 106 PFU/mL) and noted that linear inactivation curves (straight
lines on semilog plots) were associated with initial virus concentrations of 105 PFU/mL or
less.
Temperature. The length of time that viruses persist and remain infective in surface
waters depends to a great extent upon temperature, with lower temperatures enhancing
survival and infectivity (Yates and Yates, 1988). In river water, enteroviruses persisted 5-20
days at 20°C in the laboratory (Clarke et al., 1964), and in farm pond water, enteroviruses
3-29
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TABLE 3-5
Virus Inactivation in Aquatic Systems
System
Description
Organisms
inoculated in lab
into groundwater
from 475-ft deep
well (Bitton et al.,
1983b)
Organisms
inoculated in lab
into McFeters' type
survival chambers
with groundwater
from 275-ft deep
well (Keswick et al.,
1982)
McFeters type
survival chambers in
situ in river
(O'Brien and
Newman, 1977)
Organism
Poliovirus 1
Poliovirus 1
Poliovirus 1
Poliovirus 3
Coxsackievirus
A-13
Coxsackievirus
Bl
ptt
7.6
7.8
Season or
Temperature
22°C
3-15°C
23-27°C
12-20°C
7-17°C
4-8°C
23-27°C
12-20°C
23-27°C
12-20°C
12-20°C
7-1TC
4-8°C
Length of
Study
1 year
k
(hr-1)
0.0019
0.0088
0.031
0.040
0.032
0.028
0.022
0.053
0.042
0.14
0.083
0.034
0.023
0.017
Inactivation
Rate
(Iog10 days"1)
0.046
0.21
0.77
T9025hr
TgoSehr
Tgol9hr
T^24hr
T9o7hr
y\j
TgolZhr
T9029hr
T9044hr
T^SShr
3-30
-------
TABLE 3-5 (continued)
System
Description
Organisms
inoculated into
groiindwater in lab
(Yates et al., 1985)
Organisms
inoculated into
groiindwater in lab
(Yates et al., 1985)
Organisms
inoculated in lab
into McFeters type
survival chambers
with groundwater
from 275-ft deep
well (Keswick et al.,
1982)
Organism
Poliovirus 1
Wisconsin
Arizona
North
Carolina 1
North
Carolina 2
Univ. of
Arizona
New York 1
New York 2
Texas 1
Texas 2
California 1
California 2
Echovirus 1
Wisconsin
Arizona
North
Carolina 1
North
Carolina 2
Univ. of
Arizona
New York 1
New York 2
Texas 1
Texas 2
California 1
California 2
Coxsackievirus
PH
7.8
Season or
Temperature
12°
23°C
12°C
12°C
23°C
12°C
12°C
13°C
13°C
18°C
17°C
12°C
23°C
12°C
12°C
23°C
12°C
12°C
13°C
13°C
18°C
ire
3-15°C
Length of
Study
k
(hr-1)
0.0025
0.015
0.0057
0.0047
0.028
0.0015
0.0021
0.0015
0.0057
0.0077
0.0034
0.0028
0.0078
0.0077
0.0072
0.0026
0.0022
0.0021
0.0057
0.0033
0.0063
0.0038
0.0079
Inactivation
Rate
(Iog10 days"1)
0.060
0357
0.138
0.114
0.676
0.035
0.051
0.036
0.137
0.185
0.081
0.066
0.188
0.186
0.174
0.628
0.054
0.051 ,
0.138
0.079
0.151
0.091
0.19
3-31
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TABLE 3-5 (continued)
System
Description
Organisms
inoculated into
McFeters type
survival chambers
with groundwater
from 275-ft deep
well (Keswick et al.,
1982)
Summary data from
review sources
(Kutz and Gerba,
1988)
polluted river
unpolluted river
impounded
groundwater
Surface freshwater
from 5 sites (Hurst
et al., 1989)
Natural surface
waters (Haas, 1986)
Organism
Rotavirus
SA11
Enteric viruses
and coliphage
Coxsackie-
virus B3
Echovirus 7
Poliovirus 1
Viruses
pH
7.8
Season or
Temperature
111 • ^—
T "
3-15°C
5-28°C
4-37°C
5-22.5°C
4-30.5°C
-20°C
1°C
22°C
-20°C
1°C
22°C
-20°C
rc
22°C
3-5°C
22-25°C
37°C
Length of
Study
I
12 wk
12 wk
8wk
12 wk
12 wk
8wk
12 wk
12 wk
8wk
k
(hr-1)
0.015
0.013
0.010
0.016
0.007
0.00016
0.0023
0.0102
0.00016
0.0023
0.0062
0.00031
0.0021
0.0093
0.0032-
0.0071
0.032-
0.12
0.058
Iriactivation
Rate
(Iog10 days'1)
=======
0.36
0.325
0.250
0.374
0.174
0.0039
0.0475
0.2455
0,0039
0.0544
0.1498
0.0075
0.0498
0.2232
0.077-0.17
0.76-2.8
1.4
3-32
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TABLE 3-5 (continued)
System
Description
(McDaniels et al.,
1983)
Distilled Water
Secondary
Wastewater
(McDaniels et al.,
1983)
Distilled Water
Secondary
Wastewater
River (Haas, 1986)
River water, in the
presence or absence
of sunlight
with low or high
turbidity (Hurst,
1988a based on data
in Cubbage et al.,
1979)
Organism
Calf Rotavirus
CPE assay
IFA assay
CPE assay
IFA assay
CPE assay
IFA assay
CPE assay
IFA assay
Calf Reovirus
CPE assay
IFA assay
CPE assay
IFA assay
CPE assay
IFA assay
CPE assay
IFA assay
Viruses
Poliovirus
sunlight
low turbid.
hi turbid.
no sunlight
low turbid.
hi turbid.
PH
f
Season or
Temperature
8°C
26°C
8°C
26°C
8°C
26°C
8°C
26°C
Moderate
Length of
Study
20-70 hr
k
4
(hr-1)
0.00057
0.00022
0.0055
0.0050
0.00050
0.00018
0.0060
0.0053
0.00032
0.00027
0.0061
0.0063
0.00016
0.000066
0.0031
0.0049
0.014-
0.050
0.099
0.056
0.034
0.030
Inactivation
Rate
(Iog10 days'1)
Tgo 73 days
Tgo 185 days
Tgo 7.6 days
Tgo 8.4 days
Tgo 84 days
T^ 236 days
Tgo 7.0 days
Tgo 7.8 days
Tgo 130 days
Tgo 154 days
Tgo 6.8 days
Tgo 6.6 days
Tgo 262 days
Tgo 630 days
Tgo 133 days
Tgo 8.5 days
1-3
2.383
1.334
0.808
0.710
3-33
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persisted 84 days at 20°C and 91 days at 4°C (Joyce and Weiser, 1967). O'Brien and
Newman (1977) found that the rates of inactivation of polioviruses 1 and 3 and
coxsackieviruses A-13 and B-l in membrane dialysis chambers in the Rio Grande River
were affected principally by the water temperature.
In laboratory experiments, human rotavirus persisted longer in river water at 4°C
than at 20°C (Raphael et al., 1985). Since virus concentrations in filtered river water were
essentially the same irrespective of temperature, the effect of the higher temperature may
be indirect, with higher temperature promoting growth of bacteria and other microorganisms
with antiviral activity.
Groundwater samples from 11 locations were analyzed for various chemical and
physical factors; inoculated with poliovirus 1, echovirus 1, and MS-2 coliphage; held at the
in situ temperature; and examined at intervals for virus persistence (Yates et al., 1985).
Temperature was significantly correlated with the inactivation rates of the three viruses.
In their study of HAV in soils, groundwater and wastewater, Sobsey et al. (1986)
report that at 5°C, HAV, poliovirus type 1 and echovirus type 1 persisted (<90%
inactivation) for at least 12 weeks in groundwater. However, in 12 weeks at 25°C, HAV
was somewhat less affected than the other two viruses, with 90-99% inactivation compared
with 99.9% inactivation of poliovirus and echovirus.
Hurst et al. (1989), analyzing; viral inactivation rates, found that the statistically
significant factors affecting persistence of three human enterovirus serotypes (coxsackievirus
B3, echovirus 7 and poliovirus 1) were incubation temperature, viral serorype and water
source. Tgo, the number of days required for 90% inactivation or a 1-log reduction, varied
with temperature for the three viruses studied (Hurst et al., 1989):
-20°C 1°C 22°C ;
Coxsackievirus B3 255 days 21 days 4 days
Echovirus 7 196 days 18 days 6.7 days
Poliovirus 1 133 days 20 days 4.5 days
Through its effect on the chemical and biologic reactions in natural waters,
temperature may have an indirect effect on virus persistence that is reflected in seasonable
3-34
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variations (Niemi, 1976). Kapuscinski and Mitchell (1980) also suggest that temperature
may not directly affect virus inactivation but may control other inactivation mechanisms.
The inactivation rates for viruses in aquatic systems (Table 3-5) were examined to
determine whether they could be used to generate a general temperature-dependence
equation like those used for die-off of bacteria and parasites in soil arid Water and for
inactivation of viruses in soil. These data are presented in Figure 3-1, which demonstrates
a relationship between temperature and inactivation rate for all three viruses examined, as
well as a difference between the viruses in inactivation rates as a function of temperature.
The figure also shows the extensive scatter observed among the different studies and
different viruses. This scatter makes it difficult to predict viral inactivation rates with a high
degree of confidence.
Water Characteristics. Hurst et al. (1989) analyzed viral inactivation rates in relation
to surface water characteristics. The average viral inactivation ifi five surface water samples
from different sites (expressed in Iog10 units of viral loss/day of incubation) was 6.5-7.0 logs
over 8 weeks at 22°C, 4-5 logs over 12 weeks at 1°C, and 0.4^0.8 log over 12 weeks at
-20°C. Hardness and conductivity, strongly correlated with each other; turbidity and
suspended solids content, strongly correlated with each other; and the number of generations
of bacterial growth supported in the sample, also correlated with hardness and conductivity,
were the apparent water characteristics affecting viral persistence (Hurst et al., 1989).
In their study of groundwater samples collected in the United States, however, Yates
et al. (1985) found that water characteristics (pH, nitrate, ammonia, sulfate, iron, total
dissolved solids (TDS), hardness, and turbidity) Were not significantly correlated with
inactivation of three viruses held at in situ temperatures. However, the decay rate of one
virus, MS-2 coliphage, was significantly correlated to calcium concentration.
Jansons et al. (1989) examined the inactivation rates of enteroviruses (echoviruses
6,11, and 24; coxsackievirus type B5; and poliovirus type 1) in dialysis bags lowered into the
groundwater. Survival was variable and was influenced by temperature arid dissolved oxygen
concentrations, with the inactivation rate increasing as dissolved oxygen increased. They
suggest that dissolved oxygen may indirectly affect enteroviruses by influencing the activity
3-35
-------
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3-36
-------
of antagonistic organisms or may have a direct effect by oxidation of virus capsid
components.
Light. At wavelengths <370 nm, light has been shown to be detrimental to viruses
in water (Bitton et al., 1987). Ultraviolet light inactivated virus particles, and visible sunlight
inactivated poliovirus type 1 suspended in clean water; inactivation decreased with depth
and addition of clay particles (Bitton et al., 1979a). Algae that may shade viruses from
inactivation by light are controlled by light, indirectly affecting virus persistence (Bitton et
al., 1979a); and naturally occurring chemicals such as humic and fulvic acids may
photosensitize viruses in aquatic environments (Kapuscinski and Mitchell, 1980).
Hurst (1988a) reviewed six studies examining enteric virus persistence in systems
using natural surface fresh waters. Rotaviruses appeared to be more stable in fresh surface
water than enteroviruses. High turbidity levels decreased the inactivation rate of poliovirus
in river water, possibly by reducing the inactivating effects of UV radiation from sunlight
(Cubbage et al., 1979). Inactivation rates associated with low turbidity in the presence of
sunlight were 2.383 Iog10 units/day compared with 1.334 Iog10 units/day for high turbidity.
When sunlight was absent, the inactivation rate was 0.808 logs/day with high turbidity (36
nephelometric turbidity units [NTU]) and 0.710 logs/day with low turbidity (<2.5 NTU).
Microbial Activity. Investigations on the antiviral activity of microorganisms in
natural waters have yielded inconsistent results. According to the results of O'Brien and
Newman (1977), raw river water and filter-sterilized river water had comparable viracidal
activity, but virus inactivation rates were lower in autoclaved river water. They suggest that
the water may contain a heat-labile or volatile inactivating factor. With lake water,
Herrmann et al. (1974) observed more rapid enterovirus inactivation in untreated water in
dialysis bags in situ than in filtered water under similar laboratory conditions, suggesting that
a biologic factor was involved in inactivation.
In a study of >30 groundwater samples, Yates (1984) found that indigenous bacteria
had an inconsistent effect on virus inactivation. In some cases, viruses survived longer in
sterile samples, but with other samples, survival was greater in the nonsterile portion.
Filtered and unfiltered groundwater samples from several states were analyzed by Yates et
al. (1990). Temperature was the only water characteristic that was consistently, significantly
3-37
-------
correlated to decay rates of coliphage MS-2 and poliovirus type 1, which had been
inoculated into the samples. Although there was no consistent trend associated with the
presence or absence of bacteria, differences in inactivation rates were observed among some
water samples incubated at the same temperature. In another experiment in which bacteria
were enumerated throughout the experiment, the coliphage MS-2 inactivation rate in
unfiltered samples was significantly correlated to an increase in bacterial numbers in the first
24 hours, suggesting that the bacteria produced some substance that inactivated viruses.
Yates et al. (1990) summarize suggested mechanisms by which organisms may affect
inactivation: production of enzymes that destroy the virus protein coat, production of
substances that increase virus susceptibility to photodynamic inactivation, and production
of oxidizing and reducing agents.
Jansons et al. (1989), examining the inactivation rates of enterovinises (echoviruses
6, 11, and 24; coxsacMevirus type B5; and poliovirus type 1) in groundwater, found no
association between rate of virus inactivation and bacterial numbers. However, they suggest
that the presence of large numbers of specific microorganisms in some bores may have
contributed to the more rapid inactivation in those bores.
pH. In general, viruses survive well at the pH level of natural waters (pH 5-9)
(Bitton et al., 1987). The pH of the water affects virus adsorption to surfaces, virus
sensitivity to enzymes, and their heat stability (Bitton et al., 1987). According to Salo and
Cliver (1976), virus persistence relative to pH in the aqueous environment varies with the
type of virus. Poliovirus 1 survived best at near-neutral values (5 and 7), but coxsackievirus
A9 was inactivated more rapidly at pH 5 than at higher and lower values. Pancorbo et al.
(1987) found that for human rotavirus type 2 (strain Wa), inactivation was significantly
correlated with the water pH; inactivation increased with increasing pH.
Salt Species and Concentration. Various salts affect the inactivation rates of viruses
in aqueous solutions. With increasing Concentrations of NaCl in solutions, inactivation rates
of poliovirus type 1 increased (Salo and Cliver, 1976). Specific ion effects are indicated
since different inorganic salts cause different inactivation rates under conditions of equal
ionic strength. However, Cords et al. (1975) found that low ionic strength solutions
3-38
-------
inactivated type A coxsackieviruses more rapidly than high ionic strength solutions. This did
not hold true for group B coxsackieviruses or poliovirus type 1.
Studies have shown an enhanced thermal stabilization of enteroviruses in the
presence of high concentrations of some salts (Yates and Yates, 1988). Burnet and McKie
(1930) observed that bacteriophage inactivation at 60°C was partially prevented with low
concentrations of CaCl2 and BaCl2, but thermal inactivation was increased with a higher
concentration.
In their analysis of groundwater samples from locations within the United States,
Yates et al. (1985) found that the decay rate for MS-2 coliphage was significantly correlated
with the concentration of calcium in the 11 samples examined; decay rate increased with
increasing calcium concentrations. This was not true for poliovirus 1 and echovirus 1.
However, Yates (1984) found that calcium concentration was not significantly correlated
with MS-2 inactivation rate when concentrations of calcium in the same water sample were
varied. Yates et al. (1985) suggest that, in their experiment, some property of the water was
correlated with calcium concentration and was involved in the observed inactivation rate.
Formation of Aggregates. According to Bitton et al. (1980), virus persistence in
natural water is affected by the formation of aggregates. The formation of aggregates in
water has been found by Young and Sharp (1977) to influence the inactivation of viruses
by chemicals such as bromine. Bitton et al. (1980) suggest that virus particles within the
aggregate are more protected from environmental factors.
In a discussion of experiments on the inactivation rates of human rotavirus type 2
(strain Wa) and poliovirus type 1, Pancorbo et al. (1987) observed that inactivation rates
measured with single virus particles may not reflect the inactivation rates of indigenous
viruses, which are often aggregated in water. They review several studies in which
aggregated viruses (human and simian rotaviruses and polioviruses) were more resistant to
chlorine inactivation than those in single-particle suspensions.
.!" ' ' ' '
Adsorption. The association of viruses with organic and inorganic particles in water
may enhance survival; survival is enhanced when these solids-associated viruses settle into
the sediments (Bitton et al., 1987). Gerba and Bitton (1984) report that in aquatic
3-39
-------
environments, clays have been shown to protect viruses from light, heat, and biologic
degradation.
By monitoring pollution of two rivers in Germany, Walter et al. (1989) determined
that, in general, virus levels in surface water depend upon virus input from domestic sewage,
dilution by dispersion and typical metabolic interactions that have not been fully elucidated.
The authors suggest that the industrial wastes in one river may have had a toxic effect on
the virus capsid and that the oxygen content may have stimulated growth of a virus
inactivating microflora. They suggest that virus adsorption to solid particles was promoted
in the second river and that adsorption protected viruses against other inactivating
mechanisms.
Virus Type. Yates et al. (1985) found no overall significant differences in survival
of poHoviras, echovirus and coliphage MS-2 in different groundwater samples, but there
were differences in individual samples. HAV has been shown to persist longer than polio
and echovirus at 25°C in groundwater, wastewater, and soil suspensions, although all three
did well at 5°C (Sobsey et al., 1986). Human enteric virus in survival chambers exposed to
a flow of groundwater from a 275-foot deep well persisted for >24 days (Keswick et al.,
1982); coxsackievirus B3 and poliovirus type 1 persisted longer than rotaviras SA-11.
Pancorbo et al. (1987) found that inactivation rates for human rotavirus type 2 (strain
Wa) were significantly different from that of poliovirus type 1 (strain CHAT) when seeded
into vials of mountain lake water, groundwater, wastewater effluent, or polluted creek water.
Both viruses persisted longest in the lake water. Human rotavirus persisted longer than
poUovirus in the polluted samples (creek water and wastewater effluent), but poliovirus
persisted longer in the unpolluted waters (groundwater and lake water).
Hydrostatic Pressure. Although elevated hydrostatic pressures affect microbial
persistence in seawater, Bitton et al. (1983a) found that pressures ranging from 500-4000 psi
did not inactivate poliovirus in groundwater. According to Bitton et al. (1987), hyperbaric
pressure is not expected to have a significant impact on virus persistence in grbundwater.
Sediments. In their summary of data on the isolation of viruses from estuarine and
freshwater sediments, Rao and Bitton (^987) observed that there are few studies On virus
detection in freshwater sediments. Representatives of most groups of enteric viruses were
3-40
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isolated from the sediments examined. Viruses adsorb readily to solids in water; in the
laboratory, virus persistence has been shown to be prolonged by association with solids (Rao
et al., 1986).
3.3.3. Persistence in Aerosols. The particle size range for aerosols is -0.01-50 nm (10-
50,000 nm), and infection by inhalation of these biologic particles depends on the depth of
respiratory penetration, which is greatest for particles in the 1-2 nm range or for those
below 0.25 Mm (Sorber et al., 1979).
The potential for human exposure and associated health risk from viruses in aerosols
is derived from the concentration of pathogens in the wastewater or liquid sludge and the
aerosolization efficiency of the spray irrigation; the effect of the impact factor or aerosol
shock on the viruses within the first fraction of a second as they become aerosolized; and
the inactivation rate or decay rate, which, like aerosol shock, is influenced by meteorologic
factors and whether the viruses are released by day or night (Camann et al., 1978; Sorber
et al., 1979). The potential exists for adverse human health effects from wastewater or
sludge aerosols because viruses are at the low end of the size range for aerosol particles and
can be inhaled and subsequently ingested and because the infective dose can be as small as
one virus particle or PFU.
Sorber et al. (1984) studied microbiologic aerosols sampled near liquid sludge spray
application sites. Liquid sludge was applied by tank trucks or by high-volume spray guns.
No enteric viruses were detected in pooled samples representing 1470 m3 of air sampled.
Converted to < 0.0016 PFU/ni3 of air, this value implies that virus aerosolization from land
application of liquid sludge was not a significant problem.
Spray irrigation of wastewater, however, did produce levels of enteroviruses in
ambient air at 50 m downwind of the spray site (Johnson et al., 1978). A geometric mean
concentration of 0.076 of poliovirus/ml wastewater resulted in a geometric mean aerosol
concentration of 0.002/m3 of air. For other enteroviruses, the geometric mean concentration
of 0.12/ml wastewater resulted in a geometric mean aerosol concentration of 0.014/m3 of
air. The data indicate that the viruses detected were very hardy. The authors suggest that
because of the extraordinary methods required to monitor viruses in air near the spray site,
a more feasible approach would be to measure the concentration of viruses in the
3-41
-------
wastewater and use a predictive model to estimate virus concentrations in air, Such a model
was developed by Camann et al. (1978) to predict pathogen concentrations in sprayed
wastewater aerosols downwind from the spray site. Use of the model predicted a nighttime
enterovirus concentration of 0.01 PFU/m3 -650 m from the spray site, a value similar to
the measured enterovirus aerosol concentrations of 0.011 PFU/m3 and 0.017 PFU/m3 at 50
m downwind from the same spray site described in Johnson et al. (1978). There were too
few aerosol runs and virus concentrations were measured only at 50 m downwind, so it was
not possible to generate age decay rate estimates for enteroviruses. The authors noted,
however, that the enteroviruses appeared to have impact factor values in the median range
even higher than the hardy bacteria, i.e., the enteroviruses survive better during entry into
the aerosolized state and during the initial travel in the aerosol (Camann et al., 1978). This
feature is particularly significant since the indicator organisms that are often used to
measure aerosols had much lower impact factors than the enteroviruses, implying that
failure to detect bacteria or indicator organisms does not mean a human health risk from
exposure to viruses in aerosols is diminished or absent.
Camann et al. (1980) monitored school attendance and its relationship to generation
of wastewater aerosols from an adjacent wastewater treatment plant. No enteroviruses were
recovered in the total air volume (1980 m3) sampled 30 m downwind of the aeration basin,
giving a calculated enterovirus aerosol concentration of < 0.002 PFU/m3. There was no
adverse effect on communicable disease incidence in the school at this exposure level.
A more recent study by some of the same authors (Camann et al., 1988) investigated
the possibility of adverse human health effects from spray irrigation of municipal
wastewater in Lubbock, TX. Enteroviruses were recovered at a geometric mean level of
0.05 PFU/m3 and a maximum level of 16 PFU/m3 at 44-60 m downwind. These levels were
higher than those observed at other wastewater aerosol sites in the United States (Fannin
et al., 1985; Johnson et al., 1980a,b; Camann et al., 1980) and Israel (Katzenelson et al.,
1976), characterizing the irrigation site as a source of infectious microbial aerosols.
Moore et al. (1988) evaluated the virus levels in irrigation wastewater in the Lubbock
study. Prior to reservoir storage, the wastewater levels of viruses ranged from 100-1000
PFU/L. Following impoundment, viral levels were lowered to < 10 PFU/L. Because of
3-42
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variable sample concentration processes and virus enumerating systems, there were daily and
seasonal variations in human enterovirus levels and serotypes.
Shuval et al. (1989) completed field investigations on the spread of enteric viruses
by wastewater sprinkler irrigation at kibbutzim in Israel. Of 152 air samples taken at 30-730
m downwind of irrigation sites, 15 (~10%) were presumptively positive for enteric viruses.
Even at the distant 730-m station, 3 were positive out of 24 samples taken. Samples were
taken using High-Volume Cyclone Scrubbers (HVCS) for viable microbial aerosols. The
fact that 31% of positive virus samples were negative for bacterial indicators suggests that
aerosolized enteric viruses are better able to withstand hostile environmental conditions than
are the indicators. In this study, the authors did not determine whether the very low virus
concentrations (0.03-2 PFU/m3) measured could lead to infection and disease in exposed
human receptors.
Sorber et al. (1979) conclude that, although microorganisms can be aerosolized and
transported at spray irrigation sites, the risk of public health impacts from use of treated and
disinfected wastewater is probably minimal.
Ijaz et al. (1985a,b,c) have investigated survival characteristics of several viruses in
aerosols. Table 3-6 summarizes the effects of temperature and relative humidity on
persistence and illustrates the complexity of the factors determining persistence of viruses
in aerosols. For example, when aerosolized viruses were tested at 20-24°C, human
coronavirus persisted significantly longer at medium (50%) relative humidities (RH) than
at high or low RHs (Ijaz et al., 1985a); but at the mid-range of 45-55% RH, there was a
pronounced decline in infectivity of reovirus particles compared with high levels of infectivity
at high and low RHs (Adams et al., 1982).
Generally speaking, lipid-containing viruses are more stable in aerosols and persist
better at low humidity than lipid-free viruses. They are typically more contagious as
aerosols and are more likely to be infective in winter when indoor relative humidity is
<50%, unlike lipid-free viruses that survive better in moist air and infect more frequently
in summer (de Jong et al., 1973). The authors caution, however, that these epidemiologic
generalizations are based on insufficient data and, in fact, contradict the higher frequency
of winter infections with rhinoviruses and adenoviruses.
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TABLE 3-6
Virus Inactivation in Aerosols
Organism
Human
coronavirus
229E
Poliovirus
typel
(Sabin)
Human
rotavirus
(subgroup 2,
strain Wa)
Calf
rotavirus
Poliovirus
typel
(Sabin)
Reovirus
particles
(infectious,
IV, and
potentially
infectious,
PIV)
Temperature
(°C)
20±1
. ,* >. $ -
6tlb
20±1
20±1
6±1
20±1
20±1
21-24
Relative
Humidity
>5%)
30%
50%
80%
30%
50%
80%
30%
50%
80%
30%
50%
80%
30%
50%
80%
30%
50%
80%
30%
50%
80%
25-35%
45-55%
65-75%
85-95%
% Virus
Survival
36.5±5.2
70.0±1.5
27.3±1.8
0
0
100.7±9.0
tV2 0"-)
26.76±6.21
67.33±8.24
3.34±0.16
34.46±3.21
102.53:19.3
8
86.01±5.28
NRC
NR
9.07±1.82
24.5±3.5
44.2±63
3.8±1.0
21.6±4.0
57.4*7.2
1.71±0.7
avg. decay
rate:
3.2%/min
2.85%/min
3.25%/min
2.0%/min
Inactivation
Rate8
(x 10-6)
(sec'1)
3.1
1.2
25.0
2.4
0.8
0.97
9.2
3.4
1.9
22
3.9
1.5
48.9
6.67
Reference
Ijaz et al.,
1985a
Ijaz et al.,
1985a
Ijaz et al.,
1985c
Ijaz et al.,
1985b
Ijaz et al.,
1985b
Adams et
al., 1982
aCalculated; standard deviation not included in values.
bHalf-life values were predicted by regression analysis of the 24-hour survival results.
CNR, no virus recovered.
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Adams et al. (1982) found reovirus particles to be relatively stable as aerosols. At
high humidities (90-100%), reovimses had < 10-fold loss after 12 hours, but at lower relative
humidities the aerosolized virus decayed more quickly. Table 3-6 illustrates the effect of
RH on reovirus decay during equilibration; average decay rates range from a high of 3.2-
3.25%/min at both 25-35% and 65-75% RH to 2.85% at 45-55% RH, but decay rates at 85-
95% RH were much lower, averaging 2%/min. Overall decay rates averaged ~0.1%/min
over a 12-hour period, with rates of 0.6%/min for infectious particles held at 45-55%
relative humidity and 0.3%/min for potentially infectious particles held at 85-95% humidity
over a 2.5-hour period.
Brandt et al. (1982) emphasize that one possible result of low humidity is that
rotavirus-laden dust would be more likely to form from fecally contaminated clothes and
bedding, tending to stay suspended in air and thus reaching susceptible individuals.
3.3.4. Persistence in Agricultural Products. Because of the concentration of viruses hi
sludges during treatment processes, land application of sludges may present a severe
problem in contamination of fruits and vegetables. Adsorbed onto the sludge solids, viruses
may be protected from thermal inactivation. Enteroviruses have persisted for 10-15 days
on vegetables at refrigerator temperatures and up to 36 days on vegetables after spray
irrigation (Hurst, 1989).
Parsons et al. (1975) have indicated that enteroviruses persist for 4-6 days on
vegetables. Grigor'eva et al. (1965) reported enterovirus survival times of 4, 12 and 18 days
on artificially contaminated cabbage, pepper and tomato plants, respectively. Survival times
taken from Kowal (1985) suggest ranges of 4-23 days for aboveground crops such as
tomatoes and lettuce and > 60 days for below-ground crops like radishes. Konowalchuk and
Speirs (1975a,b) studied virus persistence on vegetables and fruits stored at 4°C,
determining that most were undetectable after 4-6 days, although viruses inoculated in feces
persisted longer than those inoculated in water. The same authors (Konowalchuk and
Speirs, 1977) reported a 99% reduction in poliovirus 1 and coxsackievirus B5 after 5 days
on bunches of grapes hung indoors at 22°C. Feachem et al. (1983), summarizing a number
of survival studies, conclude that practically complete elimination of viruses will occur in <5
3-45
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days, with negligible survival of enteroviruses, on crops exposed to >2 weeks of
temperatures above 25°C.
Larkin et al. (1976b) spray-irrigated lettuce and radishes with sewage sludge and
effluent and found that although polipvirus persisted on the vegetables for 36 days, there
was a 99% loss in detectable viruses within the first 5-6 days. On a second crop planted the
following year, the virus persisted only 14 days. When the same authors (Tierney et al.,
1977) investigated poliovirus survival under natural field conditions in plots flooded 1 inch
deep with inoculated sewage, they determined that the longest survival (96 days) occurred
in winter compared with 11-day survival in summer. Poliovirus was recovered from the
mature vegetables 23 days after cessation of flooding, supporting the idea of a minimum 1-
month waiting period following final sewage sludge or wastewater application before harvest
(Kowal, 1985). Bagdasar'yan (1964) showed that enterovirus levels were reduced 90% in
10 days at 3-8°C and 99% in 10 days at 18-21°C.
LasowsM and Kott (1990) introduced poliovirus LSC 1, coxsackievirus A9,
coxsackievirus B5 and echovirus 6 into secondary wastewater, some chlorinated and some
not, then sprayed on parsley, kohlrabi, lettuce, onion leaves, tomatoes and grapevine leaves.
With or without chlorination, poliovirus persisted longest on parsley leaves and consistently
persisted longer than coxsackie strains. When applied at a concentation of 163,000
PFU/ml wastewater, >500 PFU poliovirus/cm2 of surface adhered to the tomato. Natural
(no chlorination) inactivation occurred in 3-7 days. Chlorination enhanced the inactivation
process resulting in no viable enteric viruses within 1 day.
Ward and Irving (1987) spray-irrigated field-grown vegetables with stored wastewater,
which was seeded with poliovirus or adenovirus at concentrations typically found in
secondary effluent (S.lxlO2 - 2.6X105 infectious units/L). Poliovirus was inactivated within
48 hours on field crops, but there was low-level persistence of the virus for -13 days.
Adenovirus was inactivated even more quickly, as early as 24 hours after irrigation.
Poliovirus persisted for 76 days on celery and for 55 days on spinach that had been irrigated
with wastewater and then refrigerated at 4°C.
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A few studies have investigated the uptake of viruses by the root systems of plants
(Kowal, 1985), but Katzenelson and Mills (1984) find little evidence that viruses penetrate
the roots or stem.
Wallis et al. (1984) applied sludge to hayfields and pasture, but no enteric viruses
were detected throughout the study. They caution that techniques for detection of viruses
in sludge may be limiting.
The variability in environmental conditions, crops and methods of virus introduction
(spraying, flooding, etc.) makes any reliable comparison of inactivation rates on crops
difficult. Generally, the exposure of viruses on aboveground crops to desiccation, sunlight,
high temperatures, or rainfall limits their persistence. Viruses on below-ground or on-
ground crops will have inactivation rates more like those in soil, suggesting a safe waiting
period might be close to 100 days (Kowal, 1985).
3.4. TRANSPORT
Transport of viruses in soil, water and air is influenced by many of the same factors
that affect their persistence, discussed in Section 3.3 and reviewed by Yates (1990), Sattar
and Ijaz (1987), Rao et al. (1986), Duboise et al. (1979), Keswick and Gerba (1980), Gerba
and Bitton (1984), Goyal and Gerba (1979), Yates and Yates (1988) and others.
3.4.1. Transport in Soil. According to Sobsey and Shields (1987), small particles can be
removed or retained in soils by straining or filtering action, by sedimentation, or by
adsorption to soil surfaces. Adsorbed virions or those associated with each other in
aggregates may be removed by sedimentation or by straining as they move through the soil.
However, for free virions, adsorption is the primary mode of removal in soil. Adsorption
to soil particles retards virus movement through soil; desorption allows further transport
through the soil (Yates and Yates, 1988).
In addition to adsorption, soil moisture, hydraulic conditions, pH, salt species and
concentrations, virus aggregation, virus type, soil type and properties, and organic matter
affect and interact to influence the transport or movement of viruses through the soil (Yates
and Yates, 1988; Gerba and Bitton, 1984). Many of these factors influence virus adsorption
by soil (Rao et al., 1986). Low pH and high-ionic-strength water, for instance, contribute
3-47
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to the retention of viruses by soils (Keswick and Gerba, 1980). Unsaturated soil, which also
restricts movement of viruses, may enhance adsorption of viruses by holding them in close
proximity to soil surfaces (Lance and Gerba, 1984).
Although enteric viruses bound to sludge particles are not easily released, Bitton et
al. (1978) note that unbound virions in liquid sludge may penetrate the soil. Most studies
have not found viruses in groundwater beneath land application sites, but a few have
reported isolating viruses. Jorgensen and Lund (1985) found enteroviruses In water samples
3 m below the surface of a forest 11 weeks after municipal sludge application. Gerba (1987)
summarizes information on virus isolation from groundwater near sites of land application
of sewage and concludes that "...this information clearly demonstrates that if enteric viruses
are present in sewage being applied to the land, at least some of the viruses can be expected
to penetrate the subsurface and gain entrance to the underlying groundwater." Sobsey and
Shields (1987) caution that migration of enteric viruses through soil to groundwater at
application sites is a significant public health concern.
Adsorption. Initially, most viruses applied to soil are retained in the upper soil layers
(Rao et al., 1986). When soils containing 7.6-81% sand were studied for their ability to
adsorb coliphage £2 from septic tank effluent, most viruses were found in the first 15 cm,
although several isolations were found below 85 cm. Similar results were found by Hurst
et al. (1980b) and Landry et al. (1980) with seeded poliovirus in soil. Lance et al. (1976)
found that flooding a soil column with a sewage virus mixture for 27 days did not saturate
the surface layer of soil with viruses. Increasing the concentration of viruses in the sewage
water increased the numbers adsorbed at various soil levels but did not change the
maximum depth of penetration of the virus (Lance and Gerba, 1980).
Vaughn et al. (1981) suggest that formation of a surface mat of sewage solids explains
the greater removal of poliovirus found at low application rates through a coarse sand-fine
gravel soil. However, Lance and Gerba (1980) found that the concentration of viruses was
greatest near the soil surface when soil columns that had not previously been exposed to
sewage water were flooded with a virus-enriched sewage, suggesting that build-up of organic
matter near the surface was not responsible for the high concentrations of virus particles
detected there.
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Lance and Gerba (1982) suggest that viruses applied in sludge will be less mobile
that those in sewage water because they will be adsorbed to sludge solids. Bitton et al.
(1979b) found no viruses in groundwater after spread of sludge on agricultural land in
Florida.
pH. The influence of pH on virus transport is related to its effects on virus
adsorption to soil. Studying poliovirus adsorption in 34 minerals and soils, Moore et al.
(1981) found that adsorption was strong by most of the neutral and acidic materials.
However, because of the great variation in viral adsorption in alkaline materials, substrate
pH was not significantly correlated to viral adsorption in this study. Sobsey and Shields
(1987) report on a number of studies that indicate that virus retention by soils increases with
lower pH levels. With poliovirus, Taylor et al. (1981) found a characteristic pH region of
transition from strong to weak adsorption for each adsorbent studied (three soils, a sand,
and a clay mineral).
In soil suspension experiments on the effects of 7 soil properties on the adsorption
of 15 viruses to 9 soils, Goyal and Gerba (1979) observed that a soil saturation pH<5
provided good viral adsorption. Gerba et al. (1981) divided these 15 viruses into two groups
based on their adsorption behavior in soils. For the poorly adsorbed viruses, (including
coxsackie B4 viruses, echo 1 viruses, and phages 0x174 and MS-2), viral adsorption to soil
was greatly affected by pH, as well as by CEC and prganic matter; but for the highly
adsorbed viruses (including polio 1, echo 7, coxsackie B3, and phages T4 and T2), pH and
other soil characteristics were not correlated with soil adsorption. Adsorption varies not
only with virus type but also with isolates within the same type; this explains the conflicting
results from various virus studies (Gerba and Bitton, 1984).
Because of the strong repulsive forces that will result between viruses and soil
particles at higher pH values, virus desorptipn and therefore virus migration will occur if
high pH values are induced in the soil environment. However, except under unusual
circumstances, these pH values are not expected to be found in the normal environment
(Rao et al., 1986).
Mechanisms for pH influence on adsorption of viruses to soils have not been
thoroughly studied. Murray and Parks (1980) suggest that van der Waals forces are
3-49
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responsible for adsorption and that electrostatic repulsion inhibits adsorption. Sobsey and
Shields (1987) report that recent studies indicate hydrophobic interactions may also be
important in adsorption of viruses to soils.
Ionic Strength. Cations reduce the repulsive forces on both virus and soil particles,
allowing adsorption to occur (Gerba and Bitton, 1984). Several studies using soil
suspensions or soil columns have shown enhanced adsorption of viruses to a variety of
materials with increasing ionic concentrations (Sobsey and Shields, 1987). Taylor et al.
(1981) observed that both type and concentration of electrolyte affected the adsorption of
poliovirus 2 to soils, and Sobsey et al. (1980) report that addition of divalent cations such
as Mg2* caused some viruses to adsorb to poor sorbents.
Since increasing the concentration of ionic salts increases virus adsorption to soil
particles, virus transport in the soil is retarded by increasing concentrations of these salts
(Sobsey, 1983). During rainfall, the salt concentration decreases, and thus the ionic strength
of the soil water; desorption and redistribution of viruses within the soil may occur with the
potential for groundwater contamination (Gerba, 1983b). This remobilization of soil-bound
viruses has been shown to be more pronounced in sandy than in clay soils and depends on
virus type and strain (Gerba and Bitton, 1984). After a heavy rain at a land application site,
Wellings et al. (1975) detected viruses hi wells that had been virus-free.
Virus "type. Overall virion electronegativity, which is type-dependent, affects
adsorption of viruses to soils and hence desorption and migration in the soil (Rao et al.,
1986). According to Sobsey and Shields (1987), virus-specific differences in soil adsorption
are probably due to physicochemical differences in virus capsid surfaces.
Studying adsorption and subsequent elution with rainwater from columns of intact
cores of sandy soil dosed with wastewater, Landry et al. (1979) found differences in extent
of adsorption and elution among enterovirus types and among strains of poliovirus type 1.
This variation in ability to adsorb to soils has been confirmed in several studies (Sobsey and
Shields, 1987). Goyal and Gerba (1979) report differences in adsorption efficiencies by
enterovirus types and strains. Comparing adsorptive capacities of various strains of
poliovirus type 1, echoviruses 1,7 and 29, and coxsackieviruses B4 and B3 in the laboratory,
Gerba et al. (1980) found that adsorption was both type- and strain-dependent.
3-50
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On the other hand, when comparing movement of echo 1 and echo 29 viruses with
polio 1 in soil columns, Lance et al. (1982) observed similar movement of the viruses in soils
and suggest poliovirus as a model for virus movement in soil. Although echo 1 did not
adsorb well near the surface, leaching patterns were similar for echo 1, echo 29, and polio
1 below the 40-cm depth.
Sobsey et al. (1986) studied virus adsorption and persistence in soil suspensions, and
transport in soil columns of poliovirus type 1, echovirus type 1, and HAV. Poliovirus
adsorbed more extensively to soils than HAV, which adsorbed better than echovirus. In soil
columns, echovirus was transported through the column to the effluent in greatest
concentrations, and poliovirus concentrations were lowest in the effluent. The authors
suggest that neither poliovirus type 1 nor echovirus type 1 is suitable as a model for
adsorption, persistence, and transport of HAV in soil.
Soil Moisture and Flow Rate. Movement of viruses through soil is affected by soil
moisture. In laboratory studies with deionized water, Lance et al. (1976) report that viruses
near the surface desorb and migrate through soil columns; they suggest that the viruses will
continue to travel vertically through the soil with periodic rainfall. Periods of drying
between application of water reduced desorption, suggesting that virus movement in soil
would not be great unless rainfall occurred within the first few hours after application of
sewage. In a study of a land application site, Wellings et al. (1974) report that rainfall
influences penetration into the soil depths. No viruses were detected in wells 3 and 6 m
below the soil surface until after periods of heavy rainfall.
Lance and Gerba (1984) found that with unsaturated flow conditions, poliovirus did
not move below 40 cm in a column of loamy sand; but with saturated conditions, the virus
penetrated at least 160 cm. Gerba and Bitton (1984) suggest that with unsaturated-flow
conditions, water fills only the smaller soil pores or remains as a film around soil particles,
allowing viruses to get closer to particle surfaces. Under saturated soil conditions, coliphage
0X174 was found to move laterally -350 m/day (Noonan and McNabb, 1979a).
When soil columns of Red Bay sandy loam were treated with chemical sludge or with
anaerobically-treated, polyelectrolyte-conditioned, dewatered sludge and leached with
natural rainwater, none of the seeded poliovirus type 1 were found in the leachates during
3-51
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saturated flow conditions for a sustained period (Pancorbo et al., 1988). According to
Pancorbo et al. (1988), association with the solids in the sludges may have immobilized the
viruses in the top portion of the soil columns. The high level of cations in these sludges
probably enhanced the adsorption of viruses to sludge and soil particles. However, they
caution that poliovirus adsorbs more readily to soils and does not migrate through soil as
easily as other enteric viruses.
Virus removal by the soil depends on the rate of application of water or effluent
(Yates and Yates, 1988). Thus, the application rate of wastewater and sludges wUl affect
the number of viruses passing through the soil and entering the groundwater (Rao et al.,
1986). Increasing the application rate from 0.6 m/day to 1.2 m/day increased the number
of virus particles moving through the soil column in the effluent, but increasing the flow
rates up to 12 m/day gave no further increase in movement (Lance and Gerba, 1980).
Lance and Gerba (1980) suggest that virus adsorption is not affected by increases in flow
rate up to a breakthrough rate point that corresponds to the rate at which water begins to
move only through the large son pores with little or no contact between, viruses and soil
particles. Viruses have not generally been detected in well samples or lysimeter samples
with infiltration rates below 1 m/day (Lance and Gerba, 1982). Lance and Gerba (1982)
state that both column and field studies suggest that water flow velocity is possibly the most
important soil characteristic affecting virus movement.
Soil Type. Soil properties have an important effect on virus transport; migration is
promoted by coarse-textured soils that do not adsorb well (Yates and Yates, 1988). Virus
aggregates or paniculate-associated viruses may be strained or filtered out by the smaller
soU pores (Yates and Yates, 1988). Wang et al. (1980) report that adsorption is inversely
proportional to the permeability of soil. In field studies, movement of viruses to
groundwater was a problem primarily when the soil contained coarse sands or gravels
(Lance and Gerba, 1982). According to Gerba (1987), viruses can travel long distances in
sandy and gravel soils, but studies have|not been done in the field to determine just how far
viruses move from application sites.
Clay is most active in virus adsorption because of its high CEC and large surface area
(Yates and Yates, 1988). Using soil columns flushed with virus-laden settled sewage, Sobsey
3-52
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et al. (1980) report that four soil types varied in retention of poliovirus type 1, sandy clay
loam retaining more than sandy or organic soils. Funderburg et al. (1981) flooded soil
columns with simulated rain after application of poliovirus 1 and reovirus 3 in wastewater
and found that of the eight different soils tested, those with a high CEC demonstrated
stronger retention. However, Goyal and Gerba (1979) did not find a significant correlation
between CEC and enterovirus adsorption to soil.
Studying five different soils, Burge and Enkiri (1978) found that bacteriophage 0X174
adsorption differed among soils and, in most cases, was correlated with soil CEC, specific
surface area, and organic matter content. Organic compounds reduce virus adsorption since
they compete with viruses for adsorption sites (Gerba and Lance, 1978). In their review of
virus persistence and transport in soils, Sobsey and Shields (1987) report evidence that virus
association with organic substances may protect them from inactivation by preventing their
adsorption to soil, thereby enhancing persistence and mobility hi soils. Because of their
influence on virus adsorption, humic and fulvic acids increase virus transport through the
soil (Bixby and O'Brien, 1979).
In their study of the adsorption of enteroviruses to soils, Goyal and Gerba (1979)
found that the nine soils examined differed in their abilities to adsorb several enteric viruses.
Although the most important soil property influencing retention was pH, exchangeable
aluminum correlated with high adsorption for some viruses. Minerals such as iron oxides
have also been shown to increase the retention of viruses in the soil (Sobsey and Shields,
1987).
3.4.2. Transport in Surface Runoff. Virus particles adsorbed to solids in natural water
may settle in the bottom sediments. According to Rao et al. (1986), when associated with
large particles (>6 /zm), viruses settle into sediments; but when adsorbed onto smaller
particles (<3 AHU), they may remain suspended for a longer time. Accumulated solids-
associated viruses settle into a loose, flurry layer that is easily resuspended by mild
turbulence and transported to distant locations. Increased stream velocity or seasonal
turnover may also resuspend the sediments, releasing the viruses into the water (Bitton,
1978).
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There have been few studies on the transport of microorganisms in runoff from
sludge-amended fields. MSDGC and HT (1979) analyzed water samples from streams,
reservoirs, wells and runoff for viruses for 15 months during a 7-year reclamation project in
which an aerobically digested and lagooned sludge was applied in large quantities to 15,000
acres. Of the 68 water samples, only 3 contained viruses (an echovirus and 2 unidentified
virus isolates). These isolates were found in surface waters. No viruses were found in
runoff water from fields, in groundwater or in sludge and soil samples.
Both human and nonhuman enteric viruses were found in large numbers in waters
from sites along the Assomption River and its tributaries (Payment, 1989). Untreated
wastewaters from the two major cities in the area are discharged into surface water, and
runoff occurs from heavy land disposal of untreated farm animal wastes. Concentrations of
all viruses varied with season, increasing in early fall.
3.4.3. Transport in the Subsurface and in Groundwater. In sandy gravel aquifers,
groundwater flows largely through pores at rates of < 1 m/day to a few m/day; in hard rock
aquifers, transport is through fissures at 0.3-8000 m/day, or ^26,000 m/day in karstic
aquifers (Matthess and Pekdeger, 1985). The larger diameter flow paths In the hard rock
and karstic aquifers permit rapid passage of suspended microorganisms. Due to the small
diameter of viruses, the filtering action of the porous aquifers is not very effective. Since
viruses are subject to adsorption on underground particles, passage through loamy aquifers
with high cation concentrations can effectively remove viruses, especially those that adsorb
well. The sorptive small particles and microbial slime at the boundary of water and
sediment is very effective in reducing virus transport. Desorption may occur with decrease
in cation concentration, as in heavy rainfall, with further virus transport. The continuous
adsorption/desorption reactions retard'movement of viruses relative to groundwater flow,
providing time for inactivation processes to affect viruses.
Mack et al. (1972) observed that poliovirus traveled at least 90 m underground.
Keswick and Gerba (1980) report that viruses have penetrated to depths of 67 m and
travelled horizontally for distances as great as 408 m. When wastewater was applied by
rapid infiltration at a land application site, tracer phage and pathogenic animal viruses were
found in groundwater at a horizontal distance of 183 m from the site (Scha.ub and Sorber,
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1977). The tracer virus penetrated to the groundwater at the same rate as the effluent and
was isolated from an 18.3-m well beneath the application site within 48 hours.
Coliphage, used as a tracer for groundwater movement in carbonate rock terrain in
Missouri, traveled 1600 m in 16 hours (Fletcher and Meyers, 1974; Gerba, 1984b). Noonan
and McNabb (1979b) observed a rate of movement of -300 m/day (covering -920 m) for
phages in groundwater at a land disposal site in New Zealand. In shallow groundwater in
South Wales, phage used as a tracer moved at a velocity of 36-180 m/day to be isolated in
monitoring wells 690 m from the site (Martin and Thomas, 1974).
A number of models have been developed to predict the fate/survival and transport
of microorganisms in the subsurface (Grosser, 1984; Vilker et al., 1978; Corapcioglu and
Haridas, 1985; Yates and Yates, 1988; and Matthess and Pekdeger, 1985). Most of these
models address the transport of viruses under conditions of steady-state flow and saturated
soil. Tim and Mostaghimi (1991) developed a model that predicts the transport of viruses
with soil water in transient flow conditions in unsaturated soil. The model incorporates
mass conservation equations for simultaneous transport of water and viruses through
variably saturated media, an equilibrium relationship representing the rapid, instantaneous,
and reversible adsorption of virus by the soil matrix and a first-order reaction describing
viral inactivation in the subsurface environment (Tim and Mostaghimi, 1991). There is a
phase distribution of virus particles-between the liquid phase, or suspended virus particles
associated with water moving through the soil, and a solid phase, the adsorbed particles in
the soil matrk-that determines the mass available for transport in groundwater. Thus, the
model represents the three key elements describing viral transport in the subsurface: (1)
transport process, including convection and hydrodynamic dispersion; (2) phase distribution
of the viruses between soil and water; and (3) inactivation of the viruses, which ultimately
determines whether viruses persist long enough in the subsurface to become a problem by
entering the groundwater or reaching surface water.
Tim and Mostaghimi (1991) point out that models addressing virus transport in the
subsurface have typically been limited to conditions of steady-state flow in saturated soil,
whereas their model addresses transient flow conditions of the unsaturated zone. In a
transient flow system, changes in the system can alter the equilibrium. Therefore, to
3-55
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determine the long-term risk of virus accumulation in soil, those parameters affecting virus
interactions in soils must be identified and the resulting fate and transport of the viruses
modeled in variably saturated media under the condition of transient, instead of steady-state,
flow.
3.4.4. Transport by Wind. Although the dispersion of aerosol-borne viruses is partially
dependent on the size of the particle, the time the particles can remain suspended and the
distance they can travel are influenced by the airflow, or wind speed, and turbulence (Sattar
and Ijaz, 1987).
There is significant overlap in the information on persistence and on transport of
viruses in aerosols. For that reason, the studies discussed in Section 3,3.3. will only be
summarized with respect to virus transport.
Johnson et al. (1978) found that spray irrigation of wastewater produced a geometric
mean aerosol concentration of poliovirus of 0.002/m3 of air at 50 m downwind of the spray
site and a geometric mean concentration of other enteroviruses of 0.014/m3 of air. Camann
et al. (1980) recovered no enteroviruses in the total air volume (1980 m3) sampled 30 m
downwind of a wastewater aeration basin, giving an enterovirus aerosol concentration of
< 0.002 PFU/m3. As part of the Lubbock study, enteroviruses were recovered at a
geometric mean level of 0.05 PFU/m3 and a maximum level of 16 PFU/m3 at 44-60 m
downwind from a spray irrigation site using municipal wastewater (Camann et al., 1988).
Shuval et al. (1989), performing field investigations on the spread of enteric viruses by
wastewater sprinkler irrigation at kibbutzim in Israel, reported that of 15/152 air samples
taken at 30-730 .m downwind of irrigation sites were presumptively positive for enteric
viruses. Even at the distant 730-m station, 3/24 were positive. It is evident from these
results that viruses can be transported in aerosols, but quantifying the health risk from these
airborne viruses requires more information than is currently available.
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4. PARAMETERS FOR MODEL RUNS
4.1. RATIONALE FOR PARAMETER SELECTION
The assessment of human health risk from pathogenic viruses as a result of land
application of sewage sludge requires a realistic description of the fate and transport of the
pathogens. The preceding chapter describes information that has been found in the
published literature describing infectious doses, viral density in treated sludge, and survival
and transport of viruses in soil, surface water, groundwater, and aerosols. Limited data were
found for several of the many viruses capable of causing disease. Generally, the ranges of
reported inactivation rates in different media were wide, varying among reports on the same
virus as well as among media. In addition, descriptions of transport in soil were not easily
converted to parameters useful in the Pathogen Risk Assessment Model. For this analysis,
the most conservative values observed were included among the test runs to determine then-
effect on the modeled outcome.
Earlier reports in this series (U.S. EPA, 1990; 1991) identified a number of
alterations that would improve the operation of the model. However, for this study, the
model was used without changes. Therefore, the computations made during model runs are
comparable to those in the previous studies. In cases where default values presented in the
initial description of the model were judged to be unrealistic, the default values were
replaced on the basis of best scientific judgement
In these model runs, it is assumed that viruses are transported into subsurface soil
and subsequently into groundwater and are included in any droplet aerosols formed by spray
application, as well as in any particulate aerosols formed by disturbance of the soil by wind
or by cultivation. It is also assumed that they will die at a characteristic rate that depends
on the ambient temperature and the medium in which they are found; thus, there are
different inactivation rates for the same organism in moist soil, dry particulates, droplet
aerosols and water. Default parameter values are included in the program's code. If it is
necessary to update these values as indicated by new information or to revise them to
conform to specific conditions, new values are entered during the initiation of the model run
(U.S. EPA, 1989a). In a number of cases, the default values used are known to be
4-1
-------
unreasonable for the average case but are chosen to be protective; in some cases, no data
are available to support more than a best scientific judgement; in other cases, modeling and
research are available to document the values used. More detailed discussion of the choice
of parameter values can be found in U.S. EPA (1989a).
The most significant parameters for risk of infection have been shown to be density
of pathogens in sludge, inactivation or die-off rates, transfers among exposure media, and
infectious dose (U.S. EPA, 1989a; 1990; 1991). The values chosen for initial density
represent a reasonable upper bound for density of viruses in treated sludge for the
applications indicated (Table 3-3). Because of new information, the base value for viruses
in composted sludge, 2500/kg dry weight, is markedly larger than the value recommended
in the model conceptualization documents (U.S. EPA, 1989a). In some tests of the limits
of sensitivity of the model, virus concentration was set at 500/kg. The other values remain
the same as described previously (U.S. EPA, 1989a). Transfers among exposure media are
not well characterized and are estimates only. The infectious dose of many viruses may not
be known, and even for well-characterized viral types, infectivity may depend on many
conditions. Therefore, because experimental infections have indicated that a single virus
may cause infection, an infectious dose of 1 was used as the default value. Reported
inactivation rates vary widely, depending on both the virus and the physical and chemical
conditions; additional research is necessary to characterize inactivation rates accurately. In
the test model runs, each of the crucial parameters was varied, usually above and below the
default value, to determine the importance of that parameter in model outcome. Parameter
values were tested extensively for the first and second sites, and only the sensitive
parameters so identified were tested in subsequent model runs for the other sites. :
The temperature-specific rate used in the model for inactivation of viruses in moist
soil is calculated by an algorithm derived from a line fitted to a logarithmic transform of
survival data found in published literature (U.S. EPA, 1989a). This equation is as follows:
RHO = 10
_ 10(A*TEMP2-B)
4-2
-------
Where:
RHO
A
TEMP
B
= Fractional survival
= SLOPES [P(37)]
= Temperature of soil (°C)
= NTRCPS [P(38)]
To generate alternative values for the present sensitivity analysis, the slope was increased
or decreased by a factor of two, and the intercept was adjusted by trial until the inactivation
rate at 0°C remained approximately the same. Alternatively, values were chosen by trial
to fit information presented in Hurst (1989). The relative logarithmic inactivation per hour
at various temperatures for moist soil was calculated; the results are shown in Table 4-1.
It is clear from this table that the slope and intercept of the inactivation curve are important
in determining the extent of inactivation by temperature.
The lowest temperature reported for observations of inactivation of viruses in water
was -20°C. This temperature is unrealistically low to be used throughout the operation of
a model designed to represent the growing season. However, it could be used to calibrate
an algorithm for temperature-dependent inactivation similar to the one described above for
soil. The model does not provide for temperature-dependent inactivation of viruses in
water, because there were insufficient data to parameterize the relevant algorithm.
As alternatives to these values, temperature-insensitive values were substituted during
some of the model runs. Reported inactivation rates range from T.lxlO"5 to 1.6X10"1
logs/hour in soil (Table 3-4), 1.6x10"* to 1.4X10'1 logs/hour in water (Table 3-5), and 4.9xlO'5
to 8xlO"7 logs /second in aerosols (Table 3-6); these values were substituted to test the
inactivation algorithm.
A number of parameters are interdependent. For example, the rate and depth of
irrigation should not combine to exceed the infiltration rate and moisture-holding capacity
of the soil; otherwise, runoff of irrigation water will occur. However, in the present test, no
attempt was made to prevent runoff by irrigation. For parameters directly affecting specific
crops or animal feeding practices, the relevant practices must be specified when those
parameters are varied. For example, when testing FCROP1 [P(46)] and FCROP4 [P(49)],
4-3
-------
TABLE 4-1
Temperature Algorithm for Inactivation of Viruses
A=
B=
Temp.
0
4
8
12
16
20
24
28
32
36
Standard
0.00145
2.957
0.0006
2.957
0.002
2.957
Log10 Inactivation per
-0.00110
-0.00116
-0.00136
-0.00178
-0.00259
-0.00419
-0.00755
-0.01512
-0.03371
-0.08359
-0.00110
-0.00112
-0.00120
-0.00134
-0.00157
-0.00191
-0.00244
-0.00326
-0.00454
-0.00661
-0.00110
-0.00118
-0.00148
-0.00214
-0.00358
-0.00696
-0.01566
-0.04083
-0.12331
-0.43151
Test Values
0.0007
3.0
Hour
-0.00100
-0.00102
-0.00110
-0.00126
-0.00151
-0.00190
-0.00253
-0.00353
-0.00520
-0.00807
0.0029
3.0
-0.00100
-0.00111
-0.00153
-0.00261
-0.00552
-0.01445
-0.04681
-0.18775
-0.93239
-5.73323
0.0015
3.3 •
-0.00050
-0.00052
-0.00062
-0.00082
-0.00121
-0.00199
-0.00366
-0.00751
-0.01721
-0..04405
4-4
-------
both of which determine transfers to an aboveground crop, the aboveground crop option
(CROP [P(66>] = 1) must be used. Otherwise, the exposures affected by FCROP1 and
FCROP4 will not be calculated. Similarly, some transfers are not relevant to all practices,
so the parameters governing them need not be tested in all practices.
4.2. PARAMETER VALUES
The values of the main program parameters used in the initial study are given in
Table 4-2. The values of the parameters are based on the model description (U.S. EPA,
1989a), which explains their meaning and use in more detail. The parameters include a
number of transfer factors, which regulate the fraction of the pathogens in a particular
compartment that are transferred to another compartment each hour or at specific tunes.
For example, parameter 46 (FCROP1) specifies the fraction of viruses in the soil surface
that are transferred to the surface of the aboveground crop each hour the crop is present.
Other parameters may be flags to indicate that a specific subroutine should be included.
In cases in which the parameter is a number with a unit, the unit is indicated in the table.
Values for Subroutine RISK, which calculates direct onsite exposures and
modifications related to processing of crops and meat, are given in Table 4-3. Parameters
for Subroutine GRDWTR are given in Table 4-4. Site-specific descriptive parameters for
rainfall are given in Section 5, Sites for Model Runs. All five practices were tested with
appropriate combinations of these variables to determine which ones are significant for
infection. In addition, application of sludge to municipal parks and golf courses was
modeled by use of Practice V combined with characteristic parameters for lawns in Practice
III to assess runoff to an onsite pond. Parameters shown to have no effect on the outcome
of model runs at the first site were not tested extensively in model runs for the other sites.
4.2.1. Main Program Parameters. The names, definitions, and values of the main program
parameters are listed in Table 4-2. The default values are listed in bold-face type, and the
rationale for choice of each value is summarized. Each value of each parameter was used
in model runs for all practices at Site 1. Some variables were then eliminated from the
sensitivity analysis because they seemed to cause no significant effect on the model outcome.
In one set of model runs for Site 2, more conservative inactivation rates were used; they
4-5
-------
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"e3 "?3
t
o o o
I™™1 m oo
3
P
O ^5
-------
TABLE 4-3
Parameters for Subroutine RISK
Parameter
# Name
5 DRECTC
(g/day)
6 DRECTS
(g/day)
8 ICAN
11 IFREE
29 TSTM2
(hours)
32 TSTR7
(hours)
33 VOLPND
(m3/ha)
34 XDIST
(m)
35 YDIST
(m)
Value*
0.02
0.1
1.0
0.02
0.1
1.0
0
1
0
1
360
720
2880
360
720
2880
2X101
IxlO2
IxlO3
100
200
0
10
30
Rationale for Choice of Values
Determine effect of amount of contaminated crop
surface ingested during routine daily work in the
field.
Determine effect of amount of contaminated soil
ingested during routine daily work.
Default, for fresh vegetables.
Flag for canning sequence.
Default, for fresh vegetables.
Flag for freezing sequence.
Reduced storage time of meat before processing.
Default value.
Increased storage time of meat before processing.
Reduced storage time of vegetables after
processing.
Default value.
Increased storage time of vegetables after
processing.
Very small onsite pond.
Default value.
Increased value for pond.
Determine effect of distance to receptor of offsite
aerosol.
Determine effect of lateral distance of receptor
from centerline of aerosol plume.
*Default values are in bold-face type.
4-19
-------
TABLE 4-4
Parameters for Subroutine GRDWTR
Parameter
# Name
2 V
3 D
4 R
9 XI
10 DX
11 XM
Definition
Velocity
1 '(cm/hr)
Dispersion
coefficient
Retardation
coefficient
Starting
distance (m)
Distance
increment (m)
Maximum
distance (m)
Value*
0.9
3.6
10.8
20
60
100
0.2
1.0
2.0
20
50
200
20
50
200
20
50
200
Rationale for
Choice of Values
Arbitrary lower value.
Default value.
Arbitrary upper value,.
Arbitrary lower value.
Default value.
Arbitrary upper value,
Arbitrary lower value.
Default value.
Arbitrary upper value.
Arbitrary lower value.
Default value.
Arbitrary upper value.
Arbitrary lower value.
Default value.
Arbitrary upper value.
Arbitrary lower value.
Default value.
Arbitrary upper value.
*Default values are in bold-face type.
4-20
-------
were 0.0017 logs/hour for moist soil, 0.0015 logs/hour for water, and 8xlO"7 logs/second for
aerosols.
422. Parameters for Subroutine RISK. Subroutine RISK is used to calculate exposures
in various exposure compartments, using data for pathogen concentration in each
compartment as calculated by the model. Parameters for Subroutine RISK were varied to
simulate differences in exposure to viral pathogens by direct contact with soil or crop
surfaces, viruses in processed foods, the volume of the onsite pond (which had a direct effect
on concentration of viral particles in surface water), or location of the receptor of offsite
aerosols. Values of the parameters for Subroutine RISK are given in Table 4-3. Default
values are printed in bold-face type.
42.3. Parameters for Subroutine GRDWTR. Values for this subroutine are difficult to find
in the published literature. Ongoing research and development of groundwater transport
models for pathogens should yield valuable new information to allow more realistic choices
of parameter values for Subroutine GRDWTR. Values used in the study are given in Table
4-4.
42.4. Parameters for Subroutine RAINS. Because the Modified Universal Soil Loss
Equation, which is the basis for Subroutine RAINS, depends on soil type, topography and
land use practices, parameters for Subroutine RAINS are influenced strongly by the choice
of site. The sites suggested for trial runs of the Pathogen Risk Assessment Model include
one location each chosen from potential farming areas of TN, CA, FL, NM, IA and WA.
Parameters for Subroutine RAINS are defined in Table 4-5. Values for the
parameters were chosen to be appropriate for soil type, topography and meteorologic
patterns for these locations (see Chapter 5). Although the model is limited in its ability to
represent the rainfall pattern of any location because of its restriction to <10 rainfall events,
inclusion of these events early in the model run ensures that the effects of rainfall on surface
runoff/sediment transport are maximized.
4-21
-------
TABLE 4-5
Parameters for Subroutine RAINS
Parameter Definition
# Name
2
3
4
5
6
7
8
9
10
11
PDUR
PTOT
BTLAG
, CN
AMC
STAD
USLEK
USLEL
USLES
USLEC
Duration of rainfall (hr)
Total rainfall (cm)
Basin time lag (hr)
Curve number
Antecedent moisture conditions
Storm advancement coefficient
USLE K value (soil credibility factor)
USLE L value (slope length factor)
USLE S value (slope steepness factor)
USLE C value (cover management factor)
4-22
-------
5. SITES FOR MODEL RUNS
Six sites were chosen to provide a variety of soil types, topography and meteorologic
patterns. Other than Anderson County, TN, for which more detailed meteorologic data
were available to the authors, specific sites were chosen arbitrarily with the goal of
geographic diversity. Data on soil properties were taken from U.S. Soil Conservation
Service soil surveys, which have been developed for each county in the United States.
Meteorologic data were taken from the National Oceanic and Atmospheric Administration
Local Climatological Data Annual Summaries for 1981 (NOAA, 1981). The sites chosen
for the model runs are described below.
5.1. SITE 1: ANDERSON COUNTY, TN
Values of site-specific variables were chosen to reflect conditions at an agricultural
location in the Clinch River Valley of East Tennessee.
5.1.1. Description of Soil. The soil chosen for the model run is the Claiborne series, which
comprises fine-loamy, siliceous, mesic Typic Paleudults. It is further described as follows
(USDA, 1981a):
The Claiborne series consists of deep, well drained soils that formed
in sediment deposited by water or in residuum of dolomite. These soils are
on ridgetops, on hillsides, and at the base of slopes. The slope range is 5 to
45 percent, but in most areas the gradient is 12 to 30 percent....
The solum is more than 60 inches thick. Depth to dolomite bedrock
is more than 72 inches. The soil is strongly acid or very strongly acid
throughout except for the surface layer where limed. The content of coarse
chert fragments ranges from 5 to 25 percent in each horizon. These
fragments commonly increase in size and abundance with increasing depth.
Claiborne soils are of hydrologic group B, characterized by moderately low runoff potential,
moderate infiltration rates and moderate rates of water transmission.
For this analysis, it was assumed that sites with slopes > 10% (6°) would not be used
because of the likelihood of excessive runoff.
5.1.2. Narrative Climatologic Summary. The following climatologic summary for Oak
Ridge, Anderson County, TN, was taken from NOAA (1981):
5-1
-------
Oak Ridge is located in a broad valley between the Cumberland Mountains,
which lie to the northwest of the area, and the Great Smoky Mountains, to
the southeast. These mountain ranges are oriented northeast-southwest and
the valley between is corrugated by broken ridges 300 to 500 feet high and
oriented parallel to the main valley. The local climate is noticeably
influenced by topography. Prevailing winds are usually either up-valley, from
west to southwest, or down-valley, from east to northeast. During periods of
light winds daytime winds are usually southwesterly, nighttime winds usually
northeasterly. Wind velocities are somewhat decreased by the mountains and
ridges. Tornadoes rarely occur in the valley between the Cumberlands and
the Great Smokies. In winter the Cumberland Mountains have a moderating
influence on the local climate by retarding the flow of cold air from the north
and west.
The coldest month is normally January but differences between the mean
temperatures of the three winter months of December, January, and February
are comparatively small. The lowest mean monthly temperature of the winter
has occurred in each of the months December, January, or February in
different years. The lowest temperature recorded during the year has
occurred in each of the months November, December, January, or February
in various years. July is usually the hottest month but differences between the
mean temperatures of the summary months of June, July, and August are also
relatively small. The highest mean monthly temperature may occur in either
of the months June, July, or August and the highest temperature of the year
has occurred in the months of June, July, August, and September in different
years. Mean temperatures of the spring and fall months progress orderly from
cooler to warmer and warmer to cooler, respectively, without a secondary
maximum or minimum. Temperatures of 100° [38°C] or higher are unusual,
having occurred during less than one-half of the years of the period of record,
and temperatures of zero or below are rare. The average number of days
between the last freeze of spring and the first freeze of fall is approximately
200. The average daily temperature range is about 22° [12°C] with the
greatest average range in spring and fall and the smallest in winter. Summery
nights are seldom oppressively hot and humid. Low level temperature
inversions occur during approximately 57 percent of the hourly observations.
Fall is usually the season with the greatest number of hours of low level
inversion with the number decreasing progressively through spring and winter
to a summertime minimum but seasonal differences are small.
5.1.3. Temperature. The monthly average temperatures at this location ranged between a
low of 2.8° C and a high of 24.8° C.
5.1.4. Rainfall. An hourly rainfall record for April and May, 1989, was obtained from the
Atmospheric Turbulence and Diffusion Laboratory, National Oceanic and Atmospheric
5-2
-------
Administration, Oak Ridge, TN. Profiles of the first ten rain events beginning April 1, the
time the model run is initiated, were constructed from this record. Profiles consisted of the
duration of the event (PDUR), the total amount of precipitation in the event (PTOT) and
the storm advancement coefficient (STAD), which was determined by inspection of the
hourly precipitation. The resulting parameters were as follows:
Event
No.
1
2
3
4
5
6
7
8
9
10
START
77
174
726
826
924
1180
1340
1549
1590
1650
PDUR
5
8
11
7
4
5
12
2
9
14
PTOT
1.60
1.52
1.55
3.30
1.50
2.31
4.06
1.63
2.52
3.48
STAD
0.65
0.36
0.12
0.27
0.56
0.19
0.52
0.46
0.52
0.45
5.1.5. Parameters for Subroutine RAINS. Parameters for Subroutine RAINS were
modified to describe local rainfall and soil conditions for Anderson County, TN. Values
were calculated as described in Appendix B of U.S. EPA (1989a). The values used in the
model run were based on a field with dimensions 500 m by 200 m, sloping at an angle of
6° (10.5%). It was assumed for Practice I that before a crop was present, the cover
management factor was not modified, whereas after the crop was present, a canopy cover
of 30%, a canopy height of 0.5 m and a relative root network factor of 30% were provided;
for Practices II and HI, the canopy cover was taken to be 90%, the canopy height was taken
to be <0.5 m and a relative root network factor of 90% was assumed. The resulting values
were:
5-3
-------
Parameter
No. Name
4
5
6
8
9
10
11
BTLAG
CN
AMC
USLEK
USLEL
USLES
USLEC
PRACTICE NUMBER
I IT TTT
0.2
78
3 (TCROP)
0.32
4.76
1.25
0.45 (
-------
5.2.2. Narrative Climatologic Summary.
The climate at Roswell conforms to the basic trend of the four seasons, but
shows certain deviations related to geography. A location south and west of
the main part of major weather activity affords a degree of climatic seclusion.
There are also topographic effects that are inclined to alter the course of the
weather in this area. Higher landmasses almost surround the valley location,
with a long, gradual descent from points southwest through west and north.
The topography acts to modify air masses, especially the cold outbreaks in
wintertime. Downslope warming of air, as well as air interchange within a
tempering environment, often prevents sharp cooling. Moreover, the
elevation of 3,600 feet in common with the geographic situation, discourages
a significant part of the heat and humidity that originates in the south in
summer. In winter, subfreezing at night is tempered by considerable warming
during the day. Zero [°F] or lower temperatures occur as a rule a time or
two each winter. Subzero cold spells are of short duration. Whiter is the
season of least precipitation (NOAA, 1981).
5.2.3. Temperature. The monthly average temperatures at this location ranged between a
low of 4.2° C and a high of 26.2° C.
5.2.4. Rainfall. Times, duration and total rainfall for each rainfall event were constructed
* •
from the rainfall record for 1980 at the location (NOAA, 1981). The record provided the
date and amount of the largest rainfall during a 24-hour period each month, as well as the
total amount of rainfall each month. The largest rainfall (greater than the subroutine's
lower limit of 1 cm) was always used, and the remaining rainfall during the period was
divided into events placed at arbitrary times. The storm advancement coefficient was
chosen to reflect the nature of rainfall in the region; the low number used reflects a
preponderance of thunderstorms and sudden showers, whereas larger numbers were used
for some other sites to reflect a more gradual buildup of the rainstorm. The resulting
parameters were as follows:
5-5
-------
Event
No.
1
2
3
4
5
6
7
8
9
10
START
ftirt
328
784
966
1280
1830
2174
2366
2800
3328
3518
PDUR
fhr)
5
8
6
3
8
10
10
5
10
6
PTOT
(cni)
1.17
4.5
4.55
1.5
3.05
7.75
12.47
3.45
4.19
3.0
5.2.5. Parameters for Subroutine RAINS. Parameters for Subroutine RAINS were
modified to describe local rainfall and soil conditions. The slope value used in the model
run was 1 degree (1.7%). The resulting values were:
Parameter
No. Name
4
5
7
8
9
10
11
BTLAG
CN
STAD
USLEK
USLEL
USLES
USLEC
PRACTICE NUMBER
I H TTT
0.32
89
0.25
0.32
2.54
0.16
0.45(TCROP)
0.38
84
0.25
0.32
2.54
0.16
0.05
0.38
84
0.25
0.32
2.54
0.16
0.05
S3. SITE 3: CLINTON COUNTY, IA
Values for site-specific variables for Site 3 were chosen to represent an agricultural
area in eastern IA in a county that borders on the Mississippi River.
5.3.1. Description of Soil. The soil chosen for the model run is the Fayette Series, which
comprises fine-silty, mixed, mesic type Hapludalfs. It is further described as follows (USDA,
1981b):
The Fayette series consists of well drained, moderately permeable soils on
loess-covered uplands. These soils formed in loess that is more than 40 inches
thick. Slope ranges from 2 to 40 percent.
The solum ranges from 40 to 60 inches in thickness. There are no carbonates
to a depth of 40 inches to 60 inches.
5-6
-------
Fayette soils are of hydrologic group B, characterized by moderately low runoff potential,
moderate infiltration rates, and moderate rates of water transmission.
532. Narrative Climatologic Summary. Because a meteorologic report for Clinton County
was not included in NOAA (1981), the climatologic summary and data reported for nearby
Dubuque, IA, (NOAA, 1981) were used:
The principal feature of the climate in Dubuque is its variety. Standing, as
it does, at the crossroads of the various air masses that cross the continent,
the Dubuque area is subject to weather ranging from that of the cold, dry,
arctic air masses in the winter with readings as low as 32° below [-36°C],
when the ground is snow covered, to the hot, dry weather of the air masses
from the desert southwest in the summer when the temperatures reach as high
as 110° [43°C]. More often the area is covered by mild Pacific air that has
lost considerable moisture in crossing the mountains far to the west, or by
cool, dry Canadian air, or by warm, moist air from the Gulf regions. Most of
the year the latter three types of air masses dominate Dubuque weather, with
the invasions of Gulf air rarely occurring in the winter.
The seasons vary widely from year to year at Dubuque; for example,
successive invasions of cold air from the north may just reach this far one
winter and bring a long, cold winter with snow-covered ground from mid-
November until March, and many days of sub-zero temperatures, while
another season the cold air may not reach quite this far arid the winter can
be mild with bare ground most of the season, and only a few sub-zero
readings. The summers, too, may vary from hot and humid with considerable
thunderstorm activity when the Gulf air prevails, to relatively cool, dry
weather when air of northerly origin dominates the season.
5.3.3. Temperature. The monthly average temperatures at this location ranged between a
low of-7.5° C and a high of 23.2° C.
5.3.4. Rainfall. Times, duration and total rainfall for each rainfall event were constructed
from the rainfall record for 1980 (NOAA, 1981). The resulting rainfall parameters were as
follows:
5-7
-------
Event
No.
1
2
3
4
5
6
7
8
9
10
START
flirt
180
231
396
636
970
1264
1791
1834
1934
2080
PDUR
flirt
8
6
8
6
6
8
10
10
6
4
PTOT
(cml
2.84
1.0
1.6
1.2
1.0
1.27
6.12
4.56
3.0
2.5
53.5. Parameters for Subroutine RAINS. Parameters for Subroutine RAINS were
modified to describe soil conditions for Clinton County, IA, and rainfall for Dubuque, IA,
the nearest reporting station. The slope value used in the model run was 4.6° (8%). The
resulting values were:
Parameter
No. Name
4
5
6
7
8
9
10
11
BTLAG
CN
AMC
STAD
USLEK
USLEL
USLES
USLEC
PRACTICE NUMBER
I TT m
0.17
78
3 (TCROP)
0.375
0.37
4.76
0.85
0.45 (
-------
5.4.1. Description of Soil. The soil chosen for the model run is the Archbold Series, which
comprises hyperthermic, uncoated Typic Quartzipsomments. It is further described as
follows (USDA, 1989):
The Archbold series consists of nearly level to gently sloping, moderately well
drained, droughty soils that formed in marine and eolian deposits. These soils
are on moderately high ridges in the ridge part of the county. The slopes
range from 0 to 5 percent.
Typically, the surface layer is gray sand about 4 inches thick. The underlying
material to a depth of 80 niches or more is white sand.
The soil reaction is slightly acid to extremely acid. The texture is sand or fine
sand. The content of silt plus clay in the 10- to 40-inch control section is less
than 2 percent.
Archbold soils are of hydrologic group A, characterized by having a high infiltration rate
(low runoff potential) when thoroughly wet. They consist mainly of deep, well drained to
excessively drained sands or gravelly sands. These soils have a high rate of Water
transmission.
5.4.2. Narrative Climatologic Summary. Because meteorologic information was not given
in NOAA (1981) for Highlands County, the summary and data for nearby Orlando, FL, were
used.
Orlando, by virtue of its location in the central section of the Florida
peninsula (which is abounding with lakes), is almost surrounded by water and,
therefore, relative humidities remain high here the year round, with values
hovering near 90 percent at night and dipping to 40 to 50 percent in the
afternoon (sometimes to 20 percent in the winter).
The rainy season extends from June through September (sometimes through
October when tropical storms are near). During this period, scattered
afternoon thundershowers are an almost daily occurrence, and these bring a
drop in temperature to make the climate bearable (although, most summers,
temperatures above 95° [35°C] are rather rare). Too, a breeze is usually
present, and this also contributes towards general comfort.
5.4.3. Temperature. The monthly average temperatures at this location ranged between a
low of 15.8° C and a high of 28.0° C.
5-9
-------
5.4.4. Rainfall. Times, duration and total rainfall for each rainfall event were constructed
from the rainfall record for 1980 at Orlando (NOAA, 1981). The resulting parameters were
as follows:
Event
No.
1
2
3
4
5
6
7
8
9
10
START
fhrt
1043
1166
1667
1789
1958
2536
2918
3301
3547
4025
PDU
flirt
7
8
10
9
6
10
6
6
7
10
PTOT
(cm)
2.1
3.12
11.17
5.7
3.0
3.17
2.0
1.6
2.44
9.93
In model runs from Practice I, Subroutine RAINS returned a floating-point error
during computations for rainfall event 9. This error did not occur for Practices H and HI,
so it was probably related to both the number of organisms and the long time over which
the subroutine operated. To complete the model run, it was necessary to delete rainfall
events 9 and 10 for Practice I.
5.4.5. Parameters for Subroutine RAINS. Parameters for Subroutine RAINS were
modified to describe local rainfall reported for Orlando, FL, and soil conditions for
Highlands County, FL. The slope value used in the model run was 1.2° (2%). The
resulting values were:
Parameter
No. Name
4
5
1
8
9
10
11
BTLAG
CN
STAD
USLEK
USLEL
USLES
USLEC
PRACTICE NUMBER
I TT TTT
0.45
67
0.2
0.1
2.54
0.26
0.45 (TCROP)
0.8
39
0.2
0.1
2.54
0.26
0.05
0.8
39
+j s
0.2
0 1
\J» JL
254
****s~
026
\jt£*\j
0.05
5-10
-------
5.5. SITE 5: KERN COUNTY, CA
Values for site-specific variables for Site 5 were chosen to represent a soil near
Bakersfield, CA, which is located in southern CA.
5.5.1. Description of Soil. The soil chosen for the model run is the Arvin series, which
comprises coarse-loamy, mixed, nonacid, thermic Mollic Xerofluvents. It is further described
as follows (USDA, 1981c):
The Arvin series consist of very deep, weU drained soils on alluvial fan,
stream flood plains, and stream terraces. These soils formed in mixed
alluvium derived from granitic rock. Slope ranges from 2 to 9 percent.
Clay content ranges from 5 to 18 percent in the control section. Organic
matter content is 0.9 percent or less. Reaction is slightly acid to mildly
alkaline throughout.
Arvin soils are of hydrologic group B, characterized by moderately low runoff potential,
moderate infiltration rates and moderate rates of water transmission.
5.5.2. Narrative Climatologic Summary.
Bakersfield, situated in the extreme south end of the great San Joaquin
Valley, is partially surrounded by a horseshoe-shaped rim of mountains with
an open side to the northwest and the crest at an average distance of 40
miles.
The Sierra Nevadas to the northeast shut out most of the cold air that flows
southward over the continent during winter. They also catch and store snow,
which provides irrigation water for use during the dry months. The Tehachapi
Mountains, forming the southern boundary, act as an obstruction to northwest
wind, causing heavier precipitation on the windward slopes, high wind velocity
over the ridges and, at times, prevailing cloudiness in the south end of the
valley after skies have cleared elsewhere. To the west are the coast ranges,
and the ocean shore lies at a distance of 75 to 100 miles.
Because of the nature of the surrounding topography, there are large climatic
variations within relatively short distances. These zones of variation may be
classified as Valley, Mountain, and Desert areas. The overall climate,
however, is warm and semi-arid. There is only one wet season during the
year, as 90 percent of all precipitation falls from October through April,
inclusive. Snow in the valley is infrequent, with only a trace occurring in
5-11
-------
about one year out of seven. Thunderstorms also seldom occur in the vallev
(NOAA, 1981). y
5.53. Temperature. The monthly average temperatures at this location ranged between a
low of 8.5° C and a high of 28.8° C.
5.5.4. Rainfall. Times, duration and total rainfall for each rainfall event were constructed
from the rainfall record for 1980 at the location (NOAA, 1981). The resulting parameters
were as follows:
Event
No.
1
2
3
4
5
6
7
8
9
10
START
flirt
16
4378
7256
7530
8016
8320
8606
8782
13164
16022
PDUR
fhr>
8
10
9
6
6
5
8
8
10
9
PTOT
(cml
1.0
1.78
1.47
1.07
1.0
1.0
1.63
1.0
1.78
1.47
5.5.5. Parameters for Subroutine RAINS. Parameters for Subroutine RAINS were
modified to describe local rainfall and soil conditions. The slope value used in the model
run was 1.7° (3%). The resulting values were:
Parameter
No. Name
4
5
6
7
8
9
10
11
BTLAG
CN
AMC
STAD
USLEK
USLEL
USLES
USLEC
PRACTICE NUMBER
!_ H TTT
0.3
78
3 (TCROP)
0.4 :
0.32
2.54
0.26
0.45(TCROP)
0.45
61
2
0.4
0.32
2.54
0.26
0.05
0.45
61
•-• 2
0.32
2.54
0.26
0.05
5-12
-------
5.6. SITE 6: YAKIMA COUNTY, WA
Values for site-specific variables for Site 6 were chosen to represent a soil near
Yakima, WA, which is located in south-central WA along the Yakima River. This is a
region of fairly low rainfall, but which is successfully farmed by irrigation.
5.6.1. Description of Soil. The soil chosen for the model run is the Kittitas Series, which
comprises fine-silty, mixed (calcareous), mesic Fluvaquentic Haplaquolls. It is further
described as follows (USDA, 1985):
The Kittitas series consists of very deep, somewhat poorly drained soils on
flood plains. These soils formed in mixed alluvium. Slopes range from 0 to
2 percent.
Kittitas soils are of hydrologic group C, characterized by a slow infiltration rate when
thoroughly wet. They consist chiefly of soils having a layer that impedes the downward
movement of water or soils of moderately fine texture or fine texture. These soils have a
slow rate of water transmission.
5.6.2. Narrative Climatologic Summary.
Yakima is located in a small east-west valley in the upper (northwestern) part
of the irrigated Yakima Valley. Local topography is complex with a number
of minor valleys and ridges giving a local relief of as much as 500 feet. This
complex topography results in marked variations in air drainage, winds, and
minimum temperatures within short distances.
The climate of the Yakima Valley is relatively mild and dry. It has
characteristics of both maritime and continental climates, modified by the
Cascade and the Rocky Mountains, respectively. Summers are dry and rather
hot, and winters cool with only light snowfall. The maritime influence is
strongest in winter when the prevailing westerlies are the strongest and most
steady. The Selkirk and Rocky Mountains in British Columbia and Idaho
shield the area from most of the very cold air masses that sweep down from
Canada into the Great Plains and eastern United States. Sometimes a strong
polar high pressure area over western Canada will occur at the same time that
a low pressure area covers the southwestern United States. On these
occasions, the cold arctic air will pour through the passes and down the river
valleys of British Columbia, bringing very cold temperatures to Yakima. That
this happens infrequently is shown by the occurrence of temperatures of 0
degrees [F] or below on only 4 days a winter on the average. On about 21
days during the winter the temperature will fail to rise to the freezing point.
In January and February 1950, there were 4 consecutive days colder than -20°
5-13
-------
[-29°C], including -25° [-32°C] On February 1. However, over one-half of the
winters remain above 0 degrees [F (-18°C)] (NOAA, 1981).
5.6.3. Temperature. The monthly average temperatures at this location ranged between a
low of-1.5° C and a high of 22.3° C.
5.6.4. Rainfall. Times, duration and total rainfall for each rainfall event were constructed
from the rainfall record for 1980 at the location (NOAA, 1981). The resulting parameters
were: ,
Event
No.
1
2
3
4
5
6
7
8
9
10
START
fhrt
1628
4290
4506
5490
5722
5966
7002
7212
7498
7816
PDUR
flirt
6
8
10
6
6
6
10
8
8
8
PTOT
(cm)
1.0
1.25
2.06
1.14
1.0
1.0
2.65
1.5
i.2
1.0
5.6.5. Parameters for Subroutine RAINS. Parameters for Subroutine RAINS were
modified to describe local rainfall and soil conditions. The slope value used in ithe model
run was 0.6° (1%). The resulting values were:
Parameter
No. Name
4
5
6
7
8
9
10
11
BTLAG
CN
AMC
STAD
USLEK
USLEL
USLES
USLEC
PRACTICE NUMBER
I II III
0.4
85
2
0.4
0.43
2.54
0.12
0.45 (TCROP)
0.5
74
2
0.4
0.43
2.54
0.12
0.05
0.5
74
0.43
2.54
0.12
0.05
5-14
-------
6. RESULTS
6.1. ALGORITHM FOR INFECTIVE DOSE
During the development of the algorithm for infection, it was assumed that the
probability of infection could be described by the Poisson distribution (U.S. EPA, 1989a).
According to this assumption, the probability of infection with a pathogen (whose infectious
dose is M) is given by the sum of the probabilities of being exposed to M or more
pathogens. While it is not feasible to calculate this number directly, an indirect method of
calculation is well suited to the computer. Briefly, when the average exposure level is X,
the probability of being exposed to N pathogens is given by the Poisson distribution:
P(N) = e-xXN/N!
In the exposure algorithm, the value of e'x is found and multiplied by successive values of
X/N as N is incremented from 1 to M-l. All values of P(N) for N
-------
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6-2
-------
The model algorithm also exhibited the expected behavior with a simulated
heterogeneous receptor population. It is expected that a population that is heterogeneous
in its sensitivity to a pathogen will be described by a more disperse infection response than
a homogeneous population, that is, the curve will rise less steeply and cover a wider range
of exposure values. To test the applicability of the model's infection algorithm to this
assumption, a uniform population with an MID. of 10 was compared with a heterogeneous
population in which the mean MID was 10. Assuming a standard deviation of 2.0 and using
for guidance a table of areas of the normal distribution, the calculated distribution of MID
values was: 5 and 15,1% each; 6 and 14, 2.8% each; 7 and 13, 6.5% each; 8 and 12, 12.1%
each; 9 and 11, 17.5% each; and 10,19.7%. The infectivity ratio at each modeled dose was
determined for uniform populations with these MID values, and the ratios were weighted
by the population distribution and summed to yield the more disperse curve shown in Figure
6-2. This figure demonstrates that the model's infection algorithm is responsive to
heterogeneity of sensitivity in the hypothetical exposed population. The disperse curve is
not markedly different from the curve for a uniform population, but the entire range of
sensitivity was ±50% of the MID. The range of sensitivity of >75% of the population was
only ±20% of the MID, whereas the variability of sensitivity to pathogens in a typical human
population is likely to be at least a few orders of magnitude. While the model could be
revised to include an allowance for heterogeneity in the receptor population, such a revision
is not likely to improve the accuracy of the model significantly.
6.2. SENSITIVITY TO VARIABLES
The effect of specific parameter values was tested by varying each parameter singly,
using the parameter values described in Chapter 4. This required a method to compare the
outcome of many model runs and express the comparison in quantitative terms. No specific
day after application can be used as a good indicator of the probability of infection. The
model assumes that the impact of each day's exposure is independent of any other day's
exposure, despite the fact that infectious viruses could persist and accumulate, or that
chronic exposure at low levels could induce immunity. The time course of exposures could
be different in each compartment because of the timing of transfers of pathogens. As an
6-3
-------
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6-4
-------
example, in the ONSITE compartment, the maximum exposure to viruses in soil occurs
immediately after incorporation. The greatest exposure to groundwater (DRINKER)
depends on the rate of subsurface transport, the distance to the well, and the rate of
inactivation of the viruses. Transport by surface runoff to the onsite pond (SWIMMER)
cannot occur without rainfall, which determines the timing of the transfer; other parameters
modify the amount of transport. Since no specific day after application can be used as a
good indicator of the probability of infection, for each model run the maximum probability
of infection hi each exposure compartment was chosen as an appropriate indicator.
In a preliminary assessment of risk from viruses in sewage sludge, site-specific data
for Site 1 and the ranges of parameters listed in Chapter 4 were tested. Approximately 1200
model runs were made, and the effects on maximum probability of infection were
determined. The maximum observed probabilities of infection in each practice at Site 1,
using baseline parameters, are given in Table 6-1. This table shows that the maximum
probability of infection ONSITE was similar for all practices, between 1% and 7%. The
probability of infection to the OFFSITE receptor was calculated as zero in every case. Risk
of infection via contaminated food products (EATER) was shown only in Practice IV, and
risk via offsite wellwater (DRINKER) was shown in Practice HI. In contrast, infection by
contact with onsite surface water (SWIMMER) was significant in all three practices that
include the pond (Practices I-III), the risk level depending on site-specific as well as
practice-specific variables.
In an additional detailed assessment, the inactivation rate parameters were altered
as described in Section 4.2.1, and an additional set of model runs was made using site-
specific data for Site 2. The parameters used as a baseline for comparisons were the default
values, except that the fractional transfer from soil surface to aboveground crops [FCROP1,
P(46)] was increased to SxlO"6, the time at which the crop is present [TCROP, P(68)] was
reduced to 240 hours, and the time of harvesting [THARV, P(69)] was reduced to 300
hours.
On the basis of these model runs, parameters showing no effect on maximum
probability of infection were eliminated from further consideration. As reported for
parasites (U.S. EPA, 1990) and bacterial pathogens (U.S. EPA, 1991), a large number of the
6-5
-------
TABLE 6-1
Results of Model Runs, Baseline Conditions
Practice
I
n
m
IV
V
Maximum Probability of
ONSITE
7.02X10'2
l.lOxlO-2
l.lOxlO'2
5.54xl(T2
4.67xlO'2
OFFSITE
0.00
0.00
0.00
0.00
0.00
EATER
0.00
0.00
0.00
1.49xlO'2
• —
Infection
DRINKER
0.00
0.00
1.32xlO'7
•*•
~
SWIMMER
2.39xlO-2
4.13xlO'3
4.14xlO'3
•
6-6
-------
parameters had no effect on the maximum calculated probability of infection. Increasing
the fraction of viruses transferred from surface soil to another compartment would not be
expected to affect the maximum probability of infection ONSITE if the transfer occurred
late in the model run, because the maximum probability of infection ONSITE typically
occurs within the first few days after sludge application. Similarly in other exposure
pathways, changes in the fraction of viruses transferred would have no effect on the
probability of infection if the transfer occurred after the time of maximum infection and
inactivation had reduced the virus population more than the transfer increased it. In some
cases, the altered parameters governed processes that were insignificant compared to the
main determinants of exposure, and so were not able to change the maximum probability
of infection. In other cases, the exposure in a given compartment was so small that
changing the tune or amount of virus transfer to or from that compartment had no effect
on the probability of infection.
The effects of site-specific and practice-specific differences in parameters and
assumptions are illustrated by comparing the outcome of baseline model runs. The final set
of model runs, in which inactivation rates were decreased in soil, water, and droplet
aerosols, showed higher probabilities of infection at all sites and for most exposure
compartments. The results of these model runs, using baseline parameters except for the
more conservative inactivation rates, are summarized in Table 6-2. The maximum
calculated probabilities of infection ONSITE were similar for each site, and again no
OFFSITE infection was predicted. Infection via contaminated food products was calculated
to be significant only in Practices I and IV, whereas infection via contaminated wellwater
was indicated in Practices I-III at all sites. Infection to the SWIMMER was predicted at
significantly higher levels than with the default inactivation parameters. The time course
of infection probability in each exposure compartment in Practice I (Site 1) is illustrated in
Figure 6-3.
The probability of infection by consumption of crops was proportional to the
concentration of viruses in the applied sludge, but decreasing the concentration yielded a
less than proportional decrease in probability of infection ONSITE and to the SWIMMER
in the onsite pond. For example, reducing the concentration of viruses in sludge by a factor
6-7
-------
TABLE 6-2
Maximum Probability of Infection
by Site and Practice
SITE
1
2
3
4
5
6
PRACTICE
I
m
IV
V
I
n
m
IV
V
i
ii
ni
iv
V
i
n
m
IV
V
i
n
m
IV
V
i
ii
ni
IV
V
ONSITE
2.70X10'1
4.63X10'2
4.63xlO'2
5.54xlO-3
2.79xlO-3
2.70X10-1
4.63xlO-2
4.63X10'2
5.53xlO-3
2.79xlO'3
2.70X10-1
4.63xlO'2
4.63X10'2
5.54xlO'3
2.79xlO'3
2.70X10-1
4.63xlO-2
4.63xlO-2
5.54xlO'3
2.79xlO-3
2.70X10'1
4.63xlO'2
4.63xlO'2
5.54xlO-3
2.79xlO'3
2.70X10'1
4.63xlO'2
4.63xlO'2
5.54xlO'3
2.79X10'3
OFFsrrE
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
EATER
5.58X10-4
0.0
0.0
9.27X10'1
0.0
S.llxlO-4
0.0
0.0
9.28X10'1
0.0
s.eixio-4
0.0
0.0
9.28X10'1
0.0
5.11x10"
0.0
0.0
9.25X10'1
0.0
S.llxlO"1
0.0
0.0
9.25X10'1
0.0
5.11x10"
. 0.0
0.0
9.25X10'1
0.0
DRINKER
2.71X10-6
3.21x10-*
6.44X10"6
0.0
0.0
2.80X10-6
3.20X10"6
6.41X10"6
0.0
0.0
4.28X10-6
5.04X10-6
l.OlxlO'5
0.0
0.0
2.81X10"6
3.20X10"6
6.42X10"6
0.0
0.0
2.00X10-6
3.20X10"6
6.42X10"6
0.0
0.0
2.81x10-*
3.20X10"6
6.42X10"6
0.0
0.0
SWIMMER
7.40X10'1
2-lOxlO-1.
2.12X10'1
0.0
0.0
1.94X10'1
2.88xlO'2
2.90xlO'2
0.0
0.0
S.OSxlO'1
S.lSxlO'1
3.15X10'1
0.0
0.0
3.71xlO'3
S.OSxlO-4
8.07X10"4
0.0
0.0
0.0
4.73xlO-2
4.73x10-2
0.0
0.0
3.15xlO'5
4.93X10"6
4.94X10-6
0.0
0.0
6-8
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6-9
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of 200 (from 100,000/kg to 500/kg) reduced the probability of infection via crops from
S.llxlO"4 to 2.55X10"6 (also a factor of 200), whereas ONSITE infection wias reduced from
0.27 to 0.0016 (a factor of 172), and infection to the SWIMMER was reduced from 0.194
to 0.0011 (a factor of 180). This is consistent with the conclusions for infection by parasites
(U.S. EPA, 1990). When the infectious dose is 1, the probability of infection is proportional
to dose at low doses. However, because of the exponential basis of the Poisson distribution,
as the dose increases the probability of infection increases less rapidly.
To test the effect of the rate of loss of infectivity or viability, a constant logarithmic
inactivation rate was substituted for the temperature-dependent inactivation rates described
in Table 4-1. The results for Practice HI (and for EATER in Practice IV) at Site 1 are
given in Table 6-3 (similar effects were seen in model runs for the other practices, but
Practice m was used in this illustration because of its greater groundwater exposure). All
values for inactivation rates in soil, dry particulates and water gave higher probabilities of
infection than the default temperature-dependent algorithm. This suggests that the slope
and intercept values used in the algorithm may be incorrect. Substitute values for
inactivation of viral particles in aerosols had no effect on the probabilities of infection; the
probability of infection for offsite aerosol exposure was calculated to be zero in every model
run.
The effect of inactivation rate on the time course of ONSITE exposure is
demonstrated in Figure 6-4. With the inactivation rates described above, the probability of
infection fell rapidly as infectious particles were inactivated. However, when the inactivation
rates were set to zero, the decrease in probability of infection was gradual, as virus particles
in surface soil were gradually transferred to surface water, subsurface soil and groundwater.
Superimposed on this pattern was a biweekly increase for one day of 4-5% in the probability
of onsite infection as the farmer makes a closer inspection of the crops. Accompanying the
decrease in viral particles hi surface soil, there was an increase in the probability of infection
to the pond swimmer as each rainfall added more runoff to the pond (Figure 6-5). At an
inactivation rate of 0.0015 log/hr, the SWIMMER exposure rapidly decreased, whereas with
no inactivation, the probability of infection increased to 1.0. The probability of infection by
consumption of contaminated well water increased gradually, beginning 51 days after initial
6-10
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application of the sludge. These results show that the inactivation rate of virus particles is
extremely important in determining whether a groundwater well is likely to become
contaminated and in determining how long surface soil or surface water is likely to remain
infectious. The results also demonstrate the importance of accurate characterization of
inactivation rate for viruses of different kinds in the various transport and exposure media.
<5.3. ONSITE EXPOSURES
In each model run for Practice I, in which the liquid sludge must be allowed to dry
for 24 hours before it is tilled, the maximum probability of infection ONSnnE occurred on
day 3 and decreased as the sludge-borne viruses were inactivated and as they were
transferred into other compartments. In Practices II and HI, which do not require the 24-
hour waiting period, the maximum probability of infection occurred on day 2. In Practice
V the maximum probability of infection ONSITE occurred on day 2; in Practices IV and V,
composted sludge is assumed to be spread by hand, providing a high level of exposure to
the user during the application process, followed by a lower exposure as the composted
sludge is incorporated and thus diluted with soil. However, exposure during subsequent
tilling in Practice IV led to a maximum risk of infection at 15 days. Onsite exposures
decreased rapidly as the viral particles in the soil were inactivated or transferred into other
compartments. Figure 6-6 presents the time courses of ONSITE infection probabilities for
Practices I-V at Site 1.
Using reference values including the conservative inactivation rates, the baseline
maximum probability of infection was 0.270 for Practice I, 0.046 for Practices II and III,
0.0055 for Practice IV, and 0.0028 for Practice V. Generally, site-specific variables did not
have a significant effect on the probability of ONSITE infection, because the site-specific
variables alter temperature-dependent inactivation rates and rainfall-dependent runoff and
sediment transport, none of which exerts major effects on the ONSITE exposure
compartment before the time of maximum infection. Significant impacts on the probability
of infection were observed in all application practices with changes in pathogen density in
the applied sludge [ASCRS, P(l)] and sludge application rate [APRATE, P(2)], both of
6-14
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6-15
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which determine the number of viral particles applied. Because of the exf nonential nature
of the probability algorithm, the changes in probability were not directly proportional to the
change in parameter values, but varied as would be expected for a proportional change in
exposure.
The method of application was significant in Practices I-in, subsurface application
removing all probability of ONSITE infection. Increasing the infective dose [MID, P(12)]
markedly reduced the probability of infection in all practices. The concentrations of
particulates, as determined by the soil composition (EPSMLT [P(26)] and ESDLT [P(27)]>
and the height of the participate cloud (EHT [P(28)]), had an effect on the probability of
infection ONSITE. Changing the inactivation rates, either by varying the parameters
SLOPES [P(37)] and NTRCPS [P(38)] or the process functions PROC1-PROC3 and
HCRTT, had significant effects on the probability of infection, as illustrated by .a comparison
of Tables 6-1 and 6-2. The RISK parameter DRECTS, which describes the amount of soil
ingested daily, also had a significant effect on probability of infection, as would be expected
for a parameter directly governing exposure by contact with a contaminated medium,
6A. OFFSITE EXPOSURE
In all model runs; the probability of infection OFFSITE was zero,, indicating that
although the inactivation of viruses in aerosols may be less than initially expected (compare
Table 3-6 with default value of 0.002 log/sec (U.S. EPA, 1989a», the calculated quantities
of liquid and dry particulate aerosols and concentrations of viruses in the aerosols were too
low to provide an infective dose to the modeled receptor.
6.5. EXPOSURE FROM CONTAMINATED FOOD
Consumption of contaminated vegetable crops was shown by model calculations to
be a potential source of human infection, provided that inactivation rates were sufficiently
low or harvesting times were sufficiently close to application of the sludge. The maximum
probability of infection by consumption of crops in Practices I and IV at each site is shown
in Table 6-2. Infection via food crops was sensitive not only to infectious dose (MID
[P(12)], inactivation rates, and the parameters described in Section 6.3 that directly affect
6-16
-------
the number of pathogens applied to the soil (ASCRS [P(l>] and APRATE [P(2)]), but also
to the relative fractions of pathogens transferred among surface soil, subsurface soil, and
crop surface, and to the type of crop or fraction of the total crop grown aboveground, below-
ground, or on-ground (variables P(44)-P(58)). The probability of infection by consumption
of vegetable crops was weakly correlated with the crop yield and strongly correlated with
crop type, the fraction of garden crops as on-ground crops being most strongly positively
correlated with infection and the fraction as aboveground crops being negatively correlated
with infection. The first group of rows in Table 6-4 shows the effect of changes in fraction
of on-ground crops when the fraction of below-ground crops was held constant. As the
fraction of on-ground crops increased, the calculated probability of infection increased. In
the second and third groups, the fraction of aboveground crops was held constant while the
fraction of on-ground crops increased. In each case, the calculated probability of infection
increased. When the fraction of on-ground crops was held constant (0.1), the calculated
probability of infection increased as the fraction of below-ground crops increased. The
fraction of aboveground crops had a negative influence on the probability of infection.
Contamination of meat or milk by viruses from sewage sludge did not appear to pose
a significant risk to human health. No evidence was found in the literature search to
substantiate infection of cattle, poultry or swine by human enteric viruses and subsequent
transmission of those viruses to humans by ingestion of dairy or meat products. In addition,
no condition tested resulted in a calculated probability of infection > IxlO"16 for ingestion
of meat or milk.
6.6. EXPOSURE FROM CONTAMINATED GROUNDWATER
Transport of viruses via groundwater to an offsite well was not shown by this model
to be a major risk, but exposure by contaminated groundwater was shown to be likely if the
rate of inactivation of viruses in water was less than the default values. The probability of
infection was related to the periodic introduction of pathogens to groundwater by the
infiltration of rainwater (Figure 6-7). The most important parameter related to subsurface
transport of viruses appeared to be the inactivation rate of viruses in water. The results also
6-17
-------
TABLE 6-4
Effect of Distribution of Crop Types
on Risk to Consumers of Garden Vegetables3
Value of Variable
PLNT1" PLNT2C
P(74) P(75)
0.8 0.1
0.4 0.5
0.1 0.8
0.4 0.1
0.4 0.3
0.1 0.1
0.1 0.4
"Results for Site 1, Practice IV,
bAboveground crops
°On-ground crops
dBelow-ground crops
PLNT3d
P(76)
0.1
0.1
0.1
0.5
0.3
0.8
0.5
Probability
of EATER
Infection
0.0014
0.0067
0.0108
0.0109
0.0149
0.0229
0.0417
default inactivation rates
6-18
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showed an increase in probability of infection at the offsite well whenever the time required
for the viruses to reach the well was decreased. Thus, increasing groundwater velocity or
reducing the dispersion or retardation coefficients or the distance to the well moderately
increased the probability of infection in Practices II and III. Conversely, exposures were
reduced when these parameters were changed in the opposite direction. No effect was
observed in Practice I using the default inactivation rates because the concentration of viral
particles entering the groundwater was too small to be significant. However, when the
reduced, more conservative inactivation rates were used, the number of pathogens reaching
the offsite well increased and the effects of GRDWTR parameters decreased. The effects
of differences in GRDWTR parameters in model runs for Site 1 are summarized in Table
6-5.
6.7. SURFACE WATER EXPOSURE
Contaminated surface water, represented by the SWIMMER in an onsite pond, was
the most significant source of exposure. A peak in probability of infection occurred after
each rainfall, when additional contaminated soil surface water and soil were washed into the
pond. The successive pulses of pathogens released to the onsite pond are illustrated in
Figure 6-3. Site-specific parameters for Subroutine RAINS reflect differences in timing and
amount of rainfall and in properties of the soil that affect surface runoff and sediment
transport. Sites at which rainfall is slow and steady would be expected to have less runoff
and sediment transport than sites at which rainfall is infrequent but heavy. Similarly, sites
that are nearly level and have a good soil and extensive ground cover should have less
runoff than steeply sloped sites with poor soil and little ground cover. A comparison of the
effects of site-specific parameters for Subroutine RAINS on probability of infection are
demonstrated in Figure 6-8, which presents results for Practice I at all sites. Risk of
infection decreases with time before the first rainfall because of inactivation of the viral
pathogens in soil. Table 6-2 summarizes the maximum risk of infection to the pond
swimmer at each site for each of the three practices that includes an onsite pond.
6-20
-------
TABLE 6-5
Effect of Variables for Subroutine GRDWTR
on Infection via Groundwater
Variable
# Name
2 V
3D
4 R
11 XM
Definition
Velocity
(cm/far)
Dispersion
coefficient
Retardation
coefficient
Maximum
distance (m)
Value
0.9
3.6
10.8
0
60
100
0.2
1.0
2.0
20
50
200
Maximum Infection Risk
Probability Day
1.20X10-6
2.71X10-6
4.15x10-*
2.79x10-*
2.71X10-6
2.63x10-*
3.99X10"6
2.71X10-6
2.46X10-6
2.78X10-6
2.71X10"6
2.47X10"6
254
77
39
77
77
78
31
77
139
42
77
255
6-21
-------
d
o
u
CD
w
JD
O
U
CL,
u
2
D-
v
/*
C/j .-t:
w
i
CD 00
d d
I i
h* co
d d
I
in
d
I I i
^ o (N
d d d ,
1 , ,
i—<
d
-
c
CD
0)
.t!
(O
If)
OJ
+•»
• P*
CO
x
01
.tJ
CO
ed
"
0)
*s
CO
o
CN
0)
•+-•
*«4
CO
(D
-4-*
•«4
CO
D
I1
uoijoajuj jo Xji|iqeqojj
6-22
-------
Practice-specific differences in runoff can also occur. Figure 6-9 shows the calculated
probability of infection at Site 1 for practices I, II and HI. This figure shows that the
maximum probability of infection is less and the highest probability of infection occurs later
in Practices II and HI, in which there is more ground cover and therefore less surface runoff.
6-23
-------
8
S
•3
« y
e <
.5 CC
H E
y w
o
E
D-
D
uoijoajuj jo
6-24
-------
7. CONCLUSIONS
7.1. LITERATURE REVIEW
Literature values for virus density in treated sludge were so variable, both by
treatment methodology and by virus type, that no single number could be selected as typical.
However, 2000 virus particles/kg was chosen as representative of viral density in composted
sludge and 100,000 particles/kg in digested sludge. Infective doses, while varying by
detection method and by virus type, have been reported to be as low as 1 infective particle.
As a conservative assumption, this minimum value was used for the model runs. Reported
inactivation rates range from T.lxlO'5 to 1.6X10'1 logs/hour in soil, 1.6X10"4 to 1.4X10"1
logs/hour in water, and 4.9xlO"5 to 8xlO"7 logs per second in aerosols. Like the density
values, these rates are quite variable. Information on dispersion of viruses in the
environment is limited in its applicability to generating a rate of transport in environmental
media. Development of a variety of transport models has been an attempt to quantify the
movement of viruses, especially in the subsurface and in groundwater.
7.2. MODELING RESULTS
Although detailed data on survival and transport of viruses in soil are limited, the
model appears to confirm the general observations in the literature that viruses in treated
sewage sludge present a potential health risk, justifying land-use restrictions. However,
model runs implied that restrictions may be overly conservative. Reports of offsite infection
by viruses in sludge-amended soil or in aerosols from liquid treated sludge were not found;
model runs confirm the low probability of offsite infection except by uncontrolled surface
runoff.
A test of the infection algorithm yielded results that are consistent with
experimentally and epidemiologically observed responses of populations to pathogen
exposure. The algorithm could be revised to include allowances for individual variation in
sensitivity in the population, but because of the uncertainties inherent in the model and in
the data used in its operation, it was concluded that the additional complexity was not
warranted.
7-1
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72.1. Sensitivity Analysis. Model runs showed that the probability of infection by viruses
as a result of exposure to soil contaminated with sewage sludge is related to the
concentration of organisms in the sludge, the amount of sludge applied ;and the amount of
contaminated soil to which the individual is exposed, either by casual contact or by ingestion
of food grown in the contaminated soil. The method of application was also significant.
Subsurface application resulted in no exposure to any individual onsite, either by direct
contact or in the onsite pond, although exposure via groundwater was not eliminated.
Direct proportionality of response to exposure level was not observed, because the
probability of infection is calculated by a Poisson distribution, which is an exponential
function of exposure rather than a proportional one. It was shown previously (U.S. EPA,
1990) that when the MID = 1, variations in the probability of infection can be extrapolated
from variations in virus concentrations up to a probability of about 0.1. Many of the
parameters of the model seemed to have little bearing on the probability of infection,
apparently because they ultimately had no effect on the number of viral particles to which
the human receptor was exposed in each exposure compartment, or because they exerted
their effect on survival or transport after the maximum probability of infection had occurred.
The probability of infection was sensitive to the rate of inactivation of the viruses.
This was the most significant property of the viruses themselves, the other most sensitive
properties being practice-specific or related to host response as well, i .
122. Onsite Exposures. Significant onsite exposures were calculated in all practices. The
greatest ONSITE risk, -0.27 per day, was associated with Practice I» application of sludge
for production of commercial crops. These calculations imply that the field worker who
inadvertently ingests soil during daily activity on the sludge application site is at significant
risk of infection by viruses. The results imply that there should be a waiting period before
routine daily activity on the site. The length of the waiting period should depend on the
initial application rate and pathogen concentration as well as the inactivation rate of the
virus. A benchmark risk of IxlO"4 per day was suggested previously (U.S. EPA, 1990) on the
basis of proposed U.S. EPA pathogen reduction regulations (U.S.EPA, 1989b). In the
model runs reported here, the probability of infection ONSITE in Practice I, using a
conservative inactivation rate, was > IxlO'2 for 37 days and > 1x10^ for 82 days.
7-2
-------
The maximum risks of infection calculated in domestic applications were lower
(0.0055 for Practice IV and 0.0028 for Practice V), but not low enough to be protective.
However, it must be noted that the concentration used in the model runs, 2500 viruses/kg,
is a maximum value derived from a limit of detection reported in the literature, and lower
levels may routinely be found in composted sludge. It is assumed that incorporation in these
practices is done by hand or with power tools rather than by farm machinery; however, the
calculated exposures do not include direct exposure to non-incorporated sludge.
In summary, it appears that a probability of infection greater than the arbitrary
benchmark value of IxlO"4 is likely during application and incorporation of liquid treated
sludge for agricultural practices. If the initial viral concentrations in composted sludge are
>50/kg, the user is likely to be at risk of infection. A person engaged in these activities
could probably reduce the risk by wearing a protective mask and washing thoroughly before
handling food.
7.2.3. Sediment Transport and Surface Runoff. The most significant potential source of
infection was exposure to runoff water and transported sediment after rainfall. Rainfall
events were modeled as being able to transport contaminated soil from the field to the
onsite pond, where the suspended or particle-bound viruses accumulated. A swimmer in the
pond was therefore exposed to the viruses, by ingestion of either contaminated water or
sediments. Model runs indicated that it would be prudent to limit access to runoff water
and sediment from a sludge-amended field, either by mulching to reduce runoff, ditching
and/or diking to contain the runoff or restricting access to any onsite ponds receiving runoff.
7.2.4. Offsite Exposures. No health hazard was indicated as a result of offsite transport of
viruses by droplet aerosols or by wind-blown dust. This may be a model limitation caused
by over-simplification of the Gaussian-plume aerosol transport subroutine in the model, or
it may reflect a very low concentration or probability of transport of infective viruses in
aerosols. Modeling results were consistent with abundant literature reports that
groundwater can be a significant source of viral transport. However, because of dilution and
inactivation during subsurface transport, the highest probabilities of infection predicted for
consumption of groundwater at an offsite well were < IxlO"5 (Table 6-2). Variations in the
parameters used for operation of the groundwater subroutine had little effect on the
7-3
-------
maximum probability of infection when conservative inactivation rates were used, although
the time at which the maximum probability was observed did depend strongly on these
parameters (Table 6-5). Because infiltration to groundwater is treated by the subroutine as
a point source rather than as a large area (U.S. EPA, 1989a), the subroutine probably
greatly overestimates the concentration of viruses reaching the offsite well.
7.2.5. Waiting Period. Practice-specific waiting periods are proposed in the U.S. EPA
Pathogen Reduction Requirements (U.S. EPA, 1989b) before access to sludge-amended land
or consumption of crops grown thereon. For exposure comparisons, a probability of
infection of IxlO"4 was tentatively chosen as a benchmark for sufficient protection of human
health (U.S. EPA, 1990). Using this benchmark value, the default values for application
rate and inactivation rate, and a virus density of Ixl05/kg in Practice I, the initial maximum
probability of infection for aboveground crops harvested 13 days after sludge application was
S-fixlO"4 (Table 6-2); at the conservative inactivation rate for viruses in soil, a waiting period
of at least 45 days would be required to reduce the probability of infection below IxlO"4 for
aboveground crops contaminated with 0.1 g soil per crop unit. A waiting period of 5 months
appeared to be adequate (probability of infection 90% when the crops were harvested beginning at 13 days; a 4-month waiting period
reduced the probability of infection below IxlO"4.
In all cases, the probability of infection depended on the amount of soil consumed
with the crop. The default value for fraction of soil adhering to the aboveground crop is
very low; using this value (-20 mg/crop unit), the calculated probability of infection of the
food consumer was <10'16 in Practice I, indicating that a waiting period would not be
required for a low level of surface contamination. Similarly, the probability of infection
depends on the concentration of pathogens in the sludge when it is applied. Therefore, the
appropriate waiting period should probably be variable, depending not only on intended
land use, as is currently true, but also on sludge application rate and pathogen
7-4
-------
concentration. In calculating a safe waiting period, conservative assumptions should be
made about amounts of soil ingested with crops.
U.S. EPA restrictions (U.S. EPA, 1989b) on growing food crops in sludge-amended
soil, while necessary for protection against potential health hazards from parasites, appear
to be more stringent than required by typical or even worst-case inactivation rates for viruses
on crops.
7-5
-------
-------
8. RESEARCH NEEDS
8.1. INFORMATION NEEDS FOR VIRUSES
Major requirements to improve the understanding of viruses are standardized
methods for detecting and enumerating viruses and for studying their survival. Ideally, any
standard method for testing virus occurrence and infectivity should be able to (1) detect all
pathogenic viruses; (2) allow differentiation among the viruses in the sample; (3) provide
a correlation between assay and infective dose to humans; (4) accurately characterize
infective plaques, i.e., neither overestimate nor underestimate the number of infective
plaque forming units (Wellings, 1987; Bertucci et al, 1983).
Unfortunately, standardized methods for detecting and characterizing viruses in soil,
sediments, and both groundwater and surface water are not yet available (Rao and Melnick,
1987). For example, many of the methods used for concentrating and assaying viruses in
water do not recover that portion of the viruses adsorbed on suspended solids (Rao, 1987)
or adhering to sample containers (Ward and Winston, 1985). Wellings (1987) describes
methods for recovering viruses from different soil types (Berg and Berman, 1984; Farrah and
Bitton, 1984; Goyal, 1984) but emphasizes the absence of an efficient, standard method.
The recent publication (ASTM, 1990) of a standard method for recovery of viruses
from wastewater sludge is a significant improvement in methodology, although Cliver (1987)
points out that there is no single recovery method that is optimal for all viruses in all types
of sludges. Likewise, the development by Ijaz et al. (1987) of a methodology for studying
the aerobiology of viruses is an important contribution to laboratory techniques, because the
lack of standardization has been a problem in comparing research results. Sobsey et al.
(1985) have developed a method for recovery and quantitation of hepatitis A virus (HAV)
from water, and Payment and Armon (1989) have reviewed detection methods for viruses
in drinking water.
Citing the need to develop more reliable techniques for recovering more types of
enteroviruses from contaminated water, Jansons and Bucens (1986) describe a method for
concentrating rotavirus by hollow fiber ultrafiltration, thereby overcoming some of the
drawbacks of filter adsorption-elution methods. Guttman-Bass et al. (1987) compared
8-1
-------
methods for detecting rotavirus in water but found that none of the methods was sensitive
enough to detect rotaviruses in Jerusalem wastewater. Hurst et al. (1988) compare the
efficiency of three methods for detecting adenoviruses.
Gerba et aL (1989) suggest that perhaps one of the most promising techniques for
detecting viruses in water and other environmental samples may be the use of gene probes,
a methodology that is rapid, inexpensive, sensitive, does not rely on viral cultivation, and
could allow development of field test kits. Limitations are that the technique cannot
distinguish between infectious and noninfectious viruses without use of cell culture, and it
currently requires radioactive labels for increased sensitivity. More research is needed to
evaluate the sensitivity and reliability of this technique in environmental media.
Another major information need is a better understanding of the epidemiology and
relative infectivity under varied environmental conditions of enteric viruses, particularly
rotaviruses, coronaviruses, picornavirases, and the other viruses that have been less studied
than poliovirus and HAV. Although infection by droplet aerosols has been studied
extensively for many enteroviruses, much less is known about infection via dry particulate
aerosols, which appear to be of more concern for sludge application practices.
Additional data are needed on persistence and transport of viruses, particularly those
that have not been as well characterized, in soil, surface water and groundwater. A better
understanding of viral transport and persistence in relation to physical conditions and
predatory microorganisms would provide necessary data for improved modeling. Likewise,
development of predictive parameters for densities of viruses in treated sludge would be of
value in determining initial concentrations for adjusting application rates,,
In summary, the following information is needed to improve the usefulness of the
Pathogen Risk Assessment Model and to allow for a more reliable risk assessment of land
application of sewage sludge:
• Simple and accurate standardized methods for detecting and quantifying, by type,
pathogenic viruses in treated sludge destined for land application, in final
composted sludge products, and in environmental media;
• Improved understanding of minimum infective doses, particularly low-dose effects
and MIDs for sensitive subjects;
8-2
-------
• More accurate persistence and transport data on all pathogenic viruses of major
concern in sludge;
• Development of an index of soil types that would correlate capacity for solute
transport and suitability for sludge application (also valuable for onsite waste
disposal or solid waste disposal);
• Research on subsurface injection of sludge and the relative probability of virus
transport in groundwater; and
• Epidemiologic studies evaluating enteric virus transmission.
8.2. MODEL DEVELOPMENT
The literature review yielded a considerable body of information that invalidated
some of the recommended starting parameters for the model. Among these are density of
viruses in treated sludge, inactivation rates in aerosols, temperature-dependent inactivation
rates in soil and water, and fractional transfers among compartments. Many of these
parameters are represented by default values included in the model code (U.S. EPA, 1989a).
An update of the model should include revision of default parameters for parasites (U.S.
EPA, 1990) and bacterial pathogens (U.S. EPA, 1991) as well as viruses. Exposure
equations for Practices IV and V should be revised to allow for exposure to undiluted
composted sludge during application.
Equations describing temperature-dependent inactivation of viruses in environmental
media should be revised in light of new information. The slope and intercept of each
inactivation function is fitted empirically to literature values. Regression analysis of the data
in Table 3-5 resulted in a correlation coefficient of 0.32. A log transform of the inactivation
rates was used in derivation of other temperature-dependent rate equations (U.S. EPA,
1989a). When the data of Table 3-5 were analyzed similarly, a correlation coefficient of
0.67 was found. The data were then grouped by virus type and analyzed separately. The
results of this analysis are shown in Table 8-1. The correlation coefficient for poliovirus and
echovirus are not good enough to justify use of the parameters derived from the data. The
8-3
-------
TABLE 8-1
Parameters for Temperature-Dependent
Inactivation of Viruses in Aquatic Systems*
Virus
Type
Polio
Coxsackie
Echo
Number of
Samples
18
20
11
Slope
(m)
-2.44
-2.61
-2.51
Intercept
(b)
0.076
0.049
0.009
Correlation
Coefficient
0.28
0.87
0.17
"Fitted to the equation Y = mX + b, where
X = Temperature
Y = Log10 of the inactivation rate
m = Slope
b = Intercept
8-4
-------
data for coxsackie viruses represent several studies, although in many of them the
temperature was given as a range rather than a specific value (the mid-point of the range
was used in Figure 3-1 and in the regression analysis). Therefore, the slope and intercept
derived from the data may be less valid than indicated. More data are necessary for
derivation of reliable virus-specific slope and intercept factors.
The model has no temperature and relative humidity parameters linked with
inactivation of viruses in air. As Ijaz et al. (1985a,b,c; 1987) have demonstrated, these
factors are significant determinants in virus persistence. Viruses have been shown to survive
longer than bacterial indicators under hostile environmental conditions (Shuval et al., 1989),
and some viruses live significantly longer than others (Ijaz et al., 1985b).
Likewise, according to Yates and Yates (1988), subsurface transport models do not
incorporate effects of temperature, pH, moisture content, organic matter, etc. on viral
inactivation, and it appears no research is in process to incorporate such environmental
effects into subsurface transport models. Some researchers, however, have developed
alternate methods for model solute transport that implicitly include such factors but avoid
the input of environmental data needed by more explicit models (Jury, 1982, 1983; Jury et
al., 1982, 1986; Sposito et al., 1986).
Tim and Mostaghimi (1991) have developed a numerical model for predicting virus
fate and transport through variably saturated porous medium in the subsurface under
transient flow conditions. Simulation of the vertical movement of viruses applied in
wastewater effluents and sewage sludges is accomplished by combining expressions
describing transient water flow and subsurface solute transport of virus particles. The
current model does not now have an adequate component for describing subsurface
transport. Consequently, continued model development suggests the importance of
evaluating existing aerosol and subsurface transport models to determine if improvements
based on recent modeling efforts can be applied to the Pathogen Risk Assessment Model.
As Gerba (1987) points out, the existing models for predicting virus transport and
survival should be field-validated. Likewise, the Pathogen Risk Assessment Model should
also be field-validated. Perhaps it is some combination of the most useful and effective
portions of several models that will ultimately prove to be the best predictor of pathogen
8-5
-------
risk. However, the size limitations of a PC-based model make it imperative to refine the
selection of the parameters of most significance in assessing pathogen risk from land
application of sludge.
In summary, the following revisions would improve the accuracy of the model:
• Revision of default parameter values, especially for inactivation rates in aerosols
and temperature-dependent inactivation rates in soil and water;
• Revision of temperature-dependent inactivation algorithms;
• Incorporation of factors for humidity and temperature in inactivation equations
for aerosols;
• Incorporation of subroutines for subsurface transport under conditions of
transient flow; and
• Incorporation of factors to allow for subsurface transport through solution
channels, cracks, etc.
In addition, field validation of the model's predictions is necessary before the model can be
considered an accurate predictor of health risk. The model would be easier to use if it were
revised to operate from a menu rather than the current lengthy questionnaire format.
8-6
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9-22
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APPENDIX A
MODEL OVERVIEW
A-l
-------
-------
MODEL OVERVIEW
Five sludge management practices, representing land application and D&M
management options, are included in the present model and are numbered I-V. They are
listed in Table A-l and illustrated in Figures A-l through A-5. Two of the practices use
heat-dried or composted sludge for residential purposes and three use liquid sludge for
commercial farming operations. Since each of these two types of sludge represents a wide
range of sludge treatment possibilities, the extent of treatment or conditioning prior to land
application must be approximated for each case (i.e., the pathogen concentration in the
applied sludge must be specified). The computer model represents the compartments and
transfers among compartments of the five management practices. The compartments are
the various locations, states or activities in which sludge or sludge-associated pathogens exist;
they vary to some extent among practices. In each compartment, pathogens either increase,
decrease or remain the same in number with time, as specified by "process functions"
(growth, dieoff or no population changes) and "transfer functions" (movement between
compartments). The population in each compartment, therefore, generally varies with time
and is determined by a combination of initial pathogen input, "transfer functions" and
"process functions." The populations of pathogens in the compartments representing human
exposure locations (designated with an asterisk in Figures A-l through A-5 and in Table A-
2), together with appropriate intake and infective dose data, are used to estimate human
health risk.
Although each practice listed in Table A-l is different, all five practices share
common characteristics. All compartments that appear in one or more of the five sludge
management practices are listed in Table A-2. Those compartments with an asterisk
represent exposure sites for the human receptor:
• 3* inhalation or ingestion of emissions from application of sludge or
tilling of sludge/soil;
• 5* inhalation or ingestion of windblown or mechanically generated
particulates;
• 6* swimming in a pond fed by surface water runoff;
A-3
-------
TABLE A-l
Sludge Management Practices and Descriptions in
Pathogen Risk Assessment Model
PRACTICE
DESCRIPTION"
n
m
IV
V
Application of Liquid Treated Sludge for Production of
Commercial Crops for Human Consumption
Application of Liquid Treated Sludge to Grazed Pastures
Application of liquid Treated Sludge for Production of
Crops Processed before Animal Consumption
Application of Dried or Composted Sludge to Residential
Vegetable Gardens
Application of Dried or Composted Sludge to Residential
Lawns
"Source: U.S. EPA, 1989a
'Two types of sludge are used in this model - liquid and dried/composted. The extent
of treatment or conditioning prior to application is variable and must be, determined
for each case.
A-4
-------
Subsurface
Sol!
Groundwater
Offsite
Well
Application
Incorporation
Soil
Surface
Crop
Surface
Harvesting
Commercial
Crop
Irrigation
Water
Application/Tilling
Emissions
External
Source
FIGURE A-1
Input/Output Diagram for Practice I - Application of Liquid Sludge
for Production of Commercial Crops for Human Consumption
A-5
-------
Application
Application/Tilling
Emissions
Soil
Surfaca
Crop
Surfaca
v 17
Animal
Consumption
Manure
Irrigation
Water
External
Sourca
FIGURE A-2
Input/Output Diagram for Practice II — Application of Liquid
Sludge to Grazed Pastures
A-6
-------
Application/Tilling
Emissions
External
Sourca
FIGURE A-3
Input/Output Diagram for Practice 111 - Application of Liquid Sludge
for Production of Crops Processed before Animal Consumption
A-7
-------
Subsurfaca
Soli
Application/Tilling
Emissions
FIGURE A-4
Input/Output Diagram for Practice IV - Application of Dried
or Composted Sludge to Residential Vegetable Gardens
A-8
-------
Subsurfaca
Soil
Application/Tilling
Emissions
FIGURE A-5
Input/Output Diagram for Practice V - Application of Dried
or Composted Sludge to Residential Lawns
A-9
-------
TABLE A-2
Compartments Included in the Sludge Management Practices
Compartment
Name and Number
Application
Incorporation
Application/Tilling
Emissions
Soil Surface
Participates
Surface Runoff
Direct Contact
Subsurface Soil
Groundwater
Irrigation Water
Soil Surface Water
Offsite Well
Aerosols
Crop Surface
Harvesting
(Commercial) Crop
Animal Consumption
Meat
Manure
Milk
Hide
Udder
aSource: U.S. EPA, 1989a
Asterisk indicates exposure
Liquid Sludge D lied/Composted
Management Practices Sludge Management
Practices
1
1
2
2*b
4
5*
6*
7*
8
9
10
11
12*
13*
14
15
16*
compartments.
11
1
2
3*
4
5*
6*
7*
8
9
10
11
12*
13*
14
17
18*
19
20*
21
22
111 IV
1 1
2 !
3* 3*
4 4
5* 5'"
6*
7* 7'"
8 8
9
10
11 11
12*
13*
14 14
15 15
16'"
17
18*
19
20*
21
22
V
1
3*
4
5*
7*
8
11
14
A-10
-------
• 7* direct contact with sludge-contaminated soil or crops (including
grass, vegetables, or forage crops);
• 12* drinking water from an offsite well;
• 13* inhalation and subsequent ingestion of aerosols from irrigation;
• 16* consumption of vegetables grown in sludge-amended soil;
• 18* consumption of meat or
• 20* consumption of milk from cattle grazing on or consuming forage
from sludge-amended fields.
The first 14 compartments, most of which are common to all practices, are described
below.
APPLICATION (1) represents the application of sludge to a field (default size 10 ha)
or to a yard or garden of specified size. Liquid sludge may be applied by spread-flow
techniques, by spray, or by subsurface injection. The application rate and pathogen
concentrations are variables to be entered by the user of the model. During spread-flow
and spray application, sludge will be spread thinly on the soil, where it will be subject to
drying, heating and solar radiation, thus losing the protective benefits provided by bulk
sludge. It is assumed, therefore, that inactivation will occur at a rate characteristic of the
organism in soil at 5°C above the ambient temperature (Brady, 1974; USDA, 1975). It is
also assumed that liquid sludge is absorbed by the upper 5 cm of soil surface during this
time. The default time period for transfer from APPLICATION (1) to INCORPORATION
(2) is 24 hours, which allows a field treated with liquid sludge to dry sufficiently to plow or
cultivate. If the injection option is chosen, the liquid sludge goes directly to SUBSURFACE
SOIL (8) at hour 10. During spray application of liquid sludge or application of dry
composted sludge, droplets or loose particulates may become airborne. Liquid aerosols are
modeled by a Gaussian-plume air dispersion model that calculates the downwind
concentration of airborne particulates. Dry particulate emissions are calculated using
models for generation of dust by tilling or mechanical disturbance of soil. Both are
represented as transfers from APPLICATION (1) to APPLICATION/TILLING
EMISSIONS (3).
A-ll
-------
INCORPORATION (2) involves the mixing, by plowing or cultivation, of the sludge
and sludge-associated pathogens evenly throughout the upper 15 cm of soil. Process
functions associated with this compartment are the same as for the relevant pathogen type
in soil. Particulate emissions generated by cultivation are represented by a transfer from
INCORPORATION (2) to APPLICATION/TILLING EMISSIONS (3) beginning at hour
24, extending for enough time to cultivate the field (at a rate of 5 ha/hr) or till the garden
or lawn (at a rate of 0.002 ha/hr). At the end of this time, all remaining pathogens are
transferred to SOIL SURFACE (4).
APPLICATION/TILLING EMISSIONS (3*) is an exposure compartment that
receives the dust, or suspended particulates, generated by application or by the tilling of
dried sludge or sludge-soil mixture. It also receives aerosols generated by spray application
of liquid sludge. All process functions associated with this compartment are incorporated
in the aerosol subroutines. Exposure in this compartment is by inhalation but, as in all
inhalation exposures, model simplification limits the exposure to the pathogens assumed to
be ingested after the inhaled dust or aerosol spray is trapped in the upper respiratory tract,
swept back to the mouth by ciliary action and swallowed.
SOIL SURFACE (4) describes the processes occurring in the upper 15 cm (Practices
I, IV and V) or upper 5 cm (Practices II and HI) of the soil layer. Microbes are inactivated
at rates characteristic for moist soil at 5°C above the chosen ambient temperature (Crane
and Moore, 1986; Kibbey et al., 1978). Transfers from SOIL SURFACE (4) occur by wind
to WIND-GENERATED PARTICULATES (5), at a time chosen by the user, by surface
runoff and sediment transport after rainfall events to SURFACE RUNOFF (6), by a person
walking through the field or contacting soiled implements or clothing or by other casual
contact to DIRECT CONTACT (7), by leaching after irrigation, or rainfall to
SUBSURFACE SOIL (8), by resuspension during irrigation or rainfall to SOIL SURFACE
WATER (11), or at harvest to CROP SURFACE (14).
WIND-GENERATED PARTICULATES (5*) describes the airborne particulates
generated by wind. Process functions are the same as for the organism in air-dried soil at
the ambient temperature (Crane and Moore, 1986; Kibbey et al., 1978). The exposed
individual is standing in the field or at a user-specified distance downwind from the field
A-12
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during a windstorm. The wind-generated exposure is calculated from user-specified values
for duration and severity of the windstorm (default values, 6 hr at 18 m/sec (40 mph)).
SURFACE RUNOFF (6*) is an exposure compartment describing an onsite pond
containing pathogens transferred from SOIL SURFACE (4) by surface runoff and sediment
transport after rainfall. These processes are described by a separate subroutine.
Inactivation rates in this compartment are characteristic of microbes in water and are much
lower than rates for soil. Water is removed from the pond by infiltration and recharge of
the groundwater aquifer, but it is assumed that no microbes are transferred by this process.
The human receptor is an individual who incidentally ingests 0.1 L of contaminated water
while swimming in the pond. This compartment is also an exposure compartment for cattle
drinking 20 L of water daily from the pond (Practice II).
DIRECT CONTACT (7*) is the exposure compartment for a worker or a child less
than 5 years old who plays in or walks through the field, yard or garden, incidentally
ingesting 0.1 g of soil or vegetation at the daily geometric mean concentration of pathogens.
This human receptor represents the worst-case example of an individual contacting
contaminated soil or soiled clothing or implements. No process functions are associated
with this compartment because it is strictly an exposure compartment.
SUBSURFACE SOIL (8) describes the processes and transfers for pathogens in the
subsurface soil between 5 or 15 cm depth and the water table. It also serves as the
incorporation site for subsurface injection of liquid sludge. Process functions in
SUBSURFACE SOIL (8) are the same as for moist soil at the ambient temperature. The
transfer from SOIL SURFACE (4) occurs after each rain or irrigation event as a result of
leaching from the soil surface. The time of transfer is calculated by dividing the depth of
rainfall or irrigation by the infiltration rate. Transfer to GROUNDWATER (9) is
arbitrarily set at one hour later. At present, the relation between unsaturated water flow
and subsurface transport has not been well-established. Thus, this model lacks a satisfactory
subroutine to describe pathogen transport from the subsurface soil to groundwater. Instead,
~ user-specified variables are used to describe the fraction of pathogens transferred from SOIL
SURFACE (4) to SUBSURFACE SOIL (8) and from SUBSURFACE SOIL to
GROUNDWATER.
A-13
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GROUNDWATER (9) describes the flow of pathogens in the saturated zone.
Process functions are the same as for other water compartments. Transfers occur to
IRRIGATION WATER (10) if the water is needed for irrigation or to OFFSITE WELL
(12*) if the water is used for drinking. The number of pathogens transferred to
IRRIGATION WATER (10) is based on the concentration of pathogens in the groundwater
compartment and the total depth of irrigation. The transfer to OFFSITE WELL (12) is
described by a modification of the subsurface solute transport model of van Genuchten and
Alves (van Genuchten and Alves, 1982). Because microbes in suspension are passively
transported by bulk water flow and interact with soil particles by adsorption and desorption,
they behave similarly enough to dissolved chemicals that existing solute transport models can
be used to describe their fate in the saturated zone (Gerba, 1988).
IRRIGATION WATER (10) describes the transfers for pathogen-contaminated water
used for irrigation. No processes are associated with this compartment because it is
intended as a transition compartment. Irrigation of the field, lawn or garden takes place a
user-specified number of tunes each week. This irrigation water may come from either an
onsite well fed by GROUNDWATER (9) or from an outside source erf treated, liquid
sludge. The default conditions vary by practice. In either case, AEROSOLS (13) are
generated unless a non-spray option is chosen. Spray irrigation is the default since it would
be most likely to cause a significant exposure to workers or offsite persons. In addition to
aerosol emissions, irrigation transfers pathogens to CROP SURFACE (14) and to SOIL
SURFACE WATER (11).
SOIL SURFACE WATER (11) represents any irrigation water or rainfall in contact
with the ground prior to infiltration. This compartment describes the temporary suspension
of pathogens in such a water layer and their subsequent transfer to CROP SURFACE (14)
or to SOIL SURFACE (4). Process functions are the same as for other water
compartments.
OFFSITE WELL (12*) is the exposure site for a human receptor drinking 2 L/day
of contaminated water whose pathogens have been transported through grpundwater.
Process functions are the same as for groundwater. The groundwater transport subroutine
supplies the concentration of pathogens in the well at a user-specified distance from the
A-14
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source. No transfers out of the compartment are specified because it is an exposure
compartment only.
AEROSOLS (13*) describes fugitive emissions from spray irrigation, which occurs
at a default rate of 0.5 cm/hr for 5 hr. The source of irrigation water producing
AEROSOLS can be an onsite well (i.e., GROUNDWAIER) or liquid sludge. A Gaussian-
plume model is used to calculate concentrations of airborne microbes downwind. The
human receptor is an onsite worker or a person offsite who is exposed during the time of
irrigation.
CROP SURFACE (14) describes contamination of vegetable or forage crops by
transfer of user-specified amounts to or from SOIL SURFACE (4), from IRRIGATION
WATER (10), or to or from SOIL SURFACE WATER (11). Process functions are not well
characterized but are assumed to be influenced by drying, thermal inactivation and solar
radiation; they are thus most characteristic of pathogens in surface soil.
These preceding 14 compartments are common to most of the five practices modeled.
The following descriptions of the five management practices help clarify the differences
among the practices.
Practice I: Application of Liquid Treated Sludge for Production of Commercial Crops for
Human Consumption.
Liquid sludge may be applied as fertilizer/soil conditioner for the production of
agricultural crops for human consumption or for animal forage or prepared feed. Both
existing (CFR, 1988) and proposed (U.S. EPA, 1989b) regulations prohibit direct application
of sewage sludge to crop surfaces. Therefore, this model practice is designed for a single
application of liquid sludge, which is incorporated into the soil before the crop is planted.
Regulations also require various waiting periods before the planting of crops that will be
consumed uncooked by humans. These restrictions, however, are optional in the model and
can be tested.
Vegetables can be grown aboveground, on-ground or below-ground. These are
represented by tomatoes, zucchini and carrots, respectively. At HARVESTING (15) time,
A-15
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all pathogens remaining on CROP SURFACE (14) are transferred to HARVESTING (15),
which represents a single harvest of all of the crop. The same process functions apply as
in CROP SURFACE (14). The crop is held for 24 hours before being processed. The
number of pathogens is then transferred to COMMERCIAL CROPS (16*), the
compartment in which further processing takes place. The number of pathogens/crop unit
following processing is calculated in this compartment and is the figure used hi the
vegetable-exposure risk calculations. A 24-hour pathogen exposure is computed by
Subroutine VEG. Pathogen concentrations are determined as number/crop unit for each
sludge management practice. Before being consumed, vegetables normally are processed
in some way. Included in the program is a series of user-selectable processing steps. The
user has the option of choosing any or all processing steps and of specifying some conditions
within processing steps. The human receptor is a person who consumes minimally prepared
vegetables (washed, but not peeled or cooked) at a rate of 81 g tomatoes, 80 g zucchini or
43 g carrots per eating occasion (Pao et al., 1982).
Practice II: Application of Liquid Sludge to Grazed Pastures.
In this practice, liquid sludge is applied as fertilizer, soil conditioner and irrigation
water for the production of forage crops for pasture. This model practice is designed for
repeated applications of liquid sludge, initially on a field with a standing forage crop used
for pasture. It is assumed that spray irrigation will be used because this method is effective
for delivering large amounts of sludge to a large area. In this way, the pasture is also used
as a final treatment and disposal system for the treated sludge. The irrigation rate, the total
weekly depth and the number of times per week can be specified by the user. A sludge
solids concentration of 5% is assumed.
The model assumes that each hectare of pasture supports 12 head of cattle, although
both area and herd size may be varied. This may be a higher density than is the common
practice for fields that receive no irrigation, but with adequate irrigation, sufficient forage
is expected to be produced. Current and proposed regulations require various waiting
periods before animals can be grazed. These requirements can also be tested by the model.
A-16
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ANIMAL CONSUMPTION (17) describes the ingestion of CROP SURFACE (14)
by cattle grazing, in the pasture. Transfers from ANIMAL CONSUMPTION (17) are to
MEAT (18*),,MANURE (19) and MILK (20*).
MEAT (18*) is the compartment describing transfer of pathogens from ANIMAL
CONSUMPTION (17) to meat. The human receptor is assumed to consume 0.256 kg of
meat daily (U.S. FDA, 1978). Contamination of meat by gut contents during slaughter or
by systemic infection by sludge-borne pathogens can be modeled. The model allows for
inactivation of pathogens in meat by cooking, assuming reasonable cooking times and
temperatures.
The production and consumption of milk from cattle pastured on the sludge-amended
field are modeled when the dairy cattle option is chosen. The default condition is for
consumption of raw milk because commercial production of milk poses an extremely small
hazard of exposure to pathogens. In the model, contamination from dirty utensils and
careless handling are combined as a transfer from the manure-contaminated udder
[MANURE (19)], which occurs at each milking. All three pathogens can enter milk by this
route. MILK (20*) is the compartment describing production and consumption of milk from
cattle pastured on the sludge-amended field when the dairy cattle option is chosen. The
default condition models the consumption of raw milk that has been stored for 24 hours.
In exposure calculations, it is assumed that the human receptor consumes 2 kg milk/day,
roughly three times the national average milk consumption (U.S. FDA, 1978).
Practice III: Apph'cation of Liquid Treated Sludge for Production of Crops Processed
before Animal Consumption.
In this practice, liquid sludge is applied as fertilizer, soil conditioner and irrigation
water for the production of forage crops to be processed and stored for animal feed. This
model practice is designed for repeated applications of liquid sludge, initially on a field with
a standing forage crop. It is assumed that spray irrigation will be used for the application
of liquid sludge, because this method is effective for delivering large amounts of sludge to
a large area. In this way, the field is also used as a final treatment and disposal system for
the treated sludge. The rate, the total weekly depth and the number of irrigations per week
A-17
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can be changed by the user. A sludge solids concentration of 5% is assumed. The risks to
the human receptor are similar to those for the preceding practice, i.e., exposure through
meat or milk, in addition to direct contact with the forage grown in the field.
Practice IV: Application of Dried or Composted Sludge to Residential Vegetable Gardens.
Dried or composted treated sludge may be sold or given away to the public as a bulk
or bagged product for use as fertilizer or soil conditioner for the production of domestic
garden crops for human consumption. Although some studies have shown that composting
is highly effective in removing pathogens from sludge (Wiley and Westerberg, 1969), other
studies have shown that bacterial pathogens may grow in dried or composted sludge to
concentrations of IxlO6 organisms/kg dry weight (U.S. EPA, 1988). Exposure of individuals
to materials used in home gardening would be expected to be more frequent than exposure
in a commercial agricultural setting. Therefore, this practice would be expected to pose a
greater risk of infection. This model practice is designed to describe the application of dried
or composted treated sludge, which is incorporated into the soil before the crops are
planted.
Vegetables can be grown aboveground, on-ground or below-ground. These are
represented by tomatoes, zucchini and carrots, respectively. The user may specify the
proportions of above-ground, on-ground and below-ground crops in the garden. At
HARVESTING (15) tune, all pathogens remaining on CROP SURFACE (14) are
transferred to HARVESTING (15). The same process functions apply as in CROP
SURFACE (14). The crop is held for 24 hours before being processed. The number of
pathogens is then transferred to CROP (16*), the compartment in which further processing
takes place. The number of pathogens/crop unit following processing is calculated in this
compartment and is the figure used in the vegetable-exposure risk calculations. A 24-hour
pathogen exposure is computed by Subroutine VEG. Pathogen concentrations are
determined as number/crop unit for each sludge management practice. Pathogen
concentrations are determined as number/crop unit.
Before being consumed, vegetables normally are processed in some way. Included
in the program is a series of user-selectable processing steps. The user hjis the option of
A-18
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choosing any or all processing steps and of specifying some conditions within processing
steps. In the default condition, the human receptor is a person who consumes minimally
prepared vegetables (washed, but not peeled or cooked) at a rate of 81 g tomatoes, 80 g
zucchini or 43 g carrots per eating occasion (Pao et al., 1982).
Practice V: Application of Dried or Composted Sludge to Residential Lawns.
Dried or composted treated sludge may be made available to the public as a bulk or
bagged product to be sold or given away for use as fertilizer or soil conditioner for the
preparation of a seed bed for domestic lawns. Individuals engaged in preparing a seed bed
for a lawn are likely to come into contact with the soil and any additives used to improve
the seed bed. If the soil or the additives contain pathogens, this practice would be expected
to pose a risk of infection. This model practice is designed to describe the application of
dried or composted treated sludge, which is incorporated into the soil before the lawn is
seeded.
The main exposure in this practice is for the lawn worker or for a child younger than
5 years old who plays in or walks through the lawn site, incidentally ingesting soil or crop
surface at the daily geometric mean concentration of pathogens. This human receptor
represents the worst-case example of an individual contacting contaminated soil or soiled
clothing or implements. Before all pathogens have been transferred to SOIL SURFACE
(4), exposure is at the pathogen concentration found in undiluted sludge whereas, after the
transfer, the concentration is that calculated for the soil-sludge mixture.
After 840 hours, the time assumed necessary for the lawn to require mowing, the
lawn is mowed weekly, and a fraction of the pathogens associated with CROP SURFACE
(14) are transferred to DIRECT CONTACT (7). ,It is assumed that the person mowing the
lawn is exposed by inhalation and/or ingestion at each mowing.
A-19
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REFERENCES
Brady, N.C. 1974. The Nature and Properties of Soil. Macmillan Publishing Co., Inc., New
York. p. 266-276.
CFR (Code of Federal Regulations). 1988. Disease, 40 CFR 257.3-6. In: U.S. EPA,
Criteria for classification of solid waste disposal facilities and practices, 40 CFR 257.3.
Crane, S.R. and J.A. Moore. 1986. Modeling enteric bacterial die-off: A review. Water
Air Soil Pollut. 27:411-439.
Gerba, C.P. 1988. Alternative Procedures for Predicting Viral and Bacterial Transport
from the Subsurface into Groundwater. Draft. U.S. Environmental Protection Agency,
Cincinnati, OH.
Kibbey, HJ., C. Hagedorn and E.L. McCoy. -1978. Use of fecal streptococci as indicators
of pollution in soil. Appl. Environ. Microbiol. 35:711-717.
Pao, E.M., Fleming, K.H., Guenther, P.M. and Mickle, S.J. 1982. Foods commonly eaten
by individuals: Amount per day and per eating occasion. U.S. Department of Agriculture,
Economics Report No. 44.
r f-
USDA (U.S. Department of Agriculture). 1975. Soil taxonomy: A basic system of soil
classification for making and interpreting soil surveys. Soil Conservation Service.
Agriculture Handbook No. 436.
U.S. EPA. 1988. Occurrence of Pathogens in Distribution and Marketing Municipal
Sludges. Prepared by County Sanitation Districts of Los Angeles County for the Health
Effects Research Laboratory, Office of Research and Development, Research Triangle Park,
NC EPA/600/1-87/014. NTTS PB88 154273.
U.S. EPA. 1989a. Pathogen Risk Assessment for Land Application of Municipal Sludge,
Volumes I and II. Office of Health and Environmental Assessment, Environmental Criteria
and Assessment Office, Cincinnati, OH. EPA/600/6-90/002A,B. NTIS PB90-171901/AS
and PB90-171919/AS.
U.S. EPA. 1989b. Standards for the Disposal of Sewage Sludge; Proposed Rule. Federal
Register 54(23): 5886-5887.
U.S. FDA (U.S. Food and Drug Administration). 1978. FY78 Total Diet Studies.
van Genuchten, M.T. and W.J. Alves. 1982. Analytical solutions on the one-dimensional
convective-dispersive solute transport equation. USDA Technical Bulletin No.1661.
Wiley, B.B. and S.C. Westerberg. 1969. Survival of human pathogens in composted sewage.
Appl. Microbiol. 18: 994-1001.
A-20
4U.S. GOVERNMENT PRINTING OFFICE: 19 92 -61(8 -003/
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