THE HEALTH HAZARDS ASSOCIATED WITH
THE CONSUMPTION OF SHELLFISH FROM
POLLUTED WATERS
C. B. Kelly
Environmental Protection Agency
Division of Water Hygiene
September 1971
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CONTENTS
Page
I. The Health Hazards Associated with the Consumption of
Shellfish from Polluted Waters 1
A. The Feeding Mechanisms of the Oyster 2
B; Uptake of Bacteria by Shellfish 2
C. Uptake of Virus by Shellfish . .4
D. Uptake of Trace Metals by Shellfish 6
E. The Uptake of Pesticides by Shellfish 8
F. Uptake of Marine Biotoxins by Shellfish 9
G. Shellfish Borne Bacterial Enteric Diseases 12
H. Hepatitis and Shellfish 13
I. Diseases Due to Fish and Shellfish Contamination
by Chemical Pollutants 15
J. Marine Biotoxins in Shellfish 17
II. Discussion 19
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THE HEALTH HAZARDS ASSOCIATED WITH THE CONSUMPTION OF SHELLFISH
FROM POLLUTED WATERS
That consumption of shellfish (oysters, clams, and mussels)
harvested from polluted estuaries 'has been responsible for
enteric diseases in man is a well established fact, documented
many times over by epidemiological investigations and corrob-
orated by microbiological and biological studies. To understand
how these shellfish become vectors of enteric diseases, one
must consider the following:
1. In collecting food, the shellfish take in and ingest bac-
teria, viruses and certain inorganic and organic compounds
adverse to man's health.
2. Shellfish accumulate and concentrate bacteria and virus to
levels in their bodies much higher than in the surrounding
water. They also collect and assimilate metallic and or-
ganic compounds. The micro-organisms are seldom if ever
found in the tissues of shellfish, but many inorganic and
organic substances are stored in specific organs and tissues.
3. The entire animal, exclusive of the shell, is consumed by
man. Thus, the food collecting organs and the gastro-
intestinal system become part of the portions eaten by man.
4. The shellfish are often eaten raw, or only partially cooked.
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The Feeding Mechanisms of the Oyster
An intricate coordinated ciliary action creates a current of
water drawn in from the outside and drives the water through
the gill slits. Here, food material, suspended or dissolved in
the water, is removed, partly by mechanical action, but also by
entrapment and adsorption on mucous that is generated by special-
ized cells in the gills. The mucous forms a "sheet" which,
again by ciliary action, is transported over the gills to the
labial palps, the mouth of the oyster. Through this combination
of mechanical and physio-chemical mechanisms, the oysters can
remove very small particles as small as bacteria and viruses,
and by adsorption certain inorganic and organic compounds and
substances. (1, 2, 3, 4).
\
i
Many external factors influence the rate at which oysters pump
water through their gills. Probably the most fundamental of
these factors is water temperature, (5, 6, 7) but pumping (the
water transport process) arid feeding (the food collecting process)
are also effected by salinity (8), chemical agents, (9, 10) silt
(ll),%and excessively high concentrations of plankton (11), to
name a few.
Uptake of Bacteria by Shellfish
The uptake of bacteria by shellfish has been the subject of
controlled in vivo studies, carried out primarily to gather know-
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ledge on the influence of environmental factors such as temperature
on the water/shellfish bacterial relationships, and to compare the
rate of uptake of several species of shellfish.
In experiments conducted on Eastern Oysters, (Crassostrea
virginica), Hard Clams, (Mercenaria mercenaria), and Soft Clams,
(Mya arenaria) Kelly (12) reported species variation as well as
the influence of temperature on the uptake of bacteria. Soft
clams were highest in uptake, oysters next lower, and hard clams
the lowest. Soft clams were least effected by temperature. Hard
clams and oysters were relatively inactive at temperatures below
8°C. In studies in the Pacific Northwest, Kelly (13) showed a
distinct species difference in uptake of bacteria by Pacific
Oysters (Crassostrea gigas) and Olympia Oysters, (Ostrea lurida).
Olympia oysters were consistently higher in bacterial content and
the difference became greater in the warmer months. A definite
seasonal pattern of changes in uptake by both species was evident.
Kelly et al, (14) studied the accumulation of coliform organisms
by Eastern Oysters native to the Gulf of Mexico coastal estuaries.
These studies are particularly relevant to Pearl Harbor because
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of similarity in seasonal changes in water temperature in the
species of oysters growing in the areas. In the Gulf Coast
studies, the lowest uptake of bacteria occurred in August and
September, when water temperatures were the highest. The highest
rate of uptake occurred in the period October-December following
a decline in water temperature.
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Uptake of Virus b'y Shellfish
That virus are accumulated by oysters was demonstrated in a four-
year study conducted by Metcalf and Stiles (15) in an almost com-
pletely enclosed estuary in New Hampshire that receives raw and
•treated domestic sewage. Viruses were isolated from 114 of 459
oyster samples and from 103 of 310 water samples. Eight identi-
fied and fourteen untypable strains of viruses were isolated from
the oysters. Polio virus type I was most frequently found, but
Polio virus types II and III were also found, and in addition,
one strain each of Echovirus and Rheovirus, and 3 strains of
Coxackievirus. A similar study was carried out in a moderately
polluted area in Rhode Island by the EPA Northeastern Water Hygiene
Laboratory. The isolations from clams and oysters included three
poliovirus strains, three strains of echovirus and one of Coxackie-
virus .
Liu (16), reports on observations on the physiology of the accumula-
tion of viruses by shellfish, summarized as follows:
1. By far the greatest portion (95% +) of virus is found in the
digestive system, the gills and the feces, but approximately
5% are found in the lymph.
2. The virus in the digestive system does not adhere to or pene-
trate any type of cells. These observations indicate that
virus, for the most part experience a transient existence in
the gastro-intestinal system of shellfish.
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3. The mucous has a high, absorbability for virus. When mucous
was added to suspensions of virus in sea water, 80% of the
virus attached to the mucous particles.
Quantitative estimations of the rate of virus accumulation by the
Eastern Oyster were made by Mitchell et al (17). These studies,
conducted in controlled flow-through experimental systems, feature
concommitent observations on the accumulation of JE. colit The
results show that rapid uptake of the virus occurred within one
hour of exposure to the virus contaminated sea water. The rate
of uptake decreased after about four hours and stabilized after
6 to 12 hours exposure. The viral content of the oyster meats
reached 10-60 times that of the surrounding water. Accumulation
of E. coli closely paralleled that of virus.
The finding of virus in shellfish in polluted estuaries, demon-
stration of the presence in feces, and in vivo experimentation
which quantitated the rate and extent of accumulation of virus,
as well as a behavior parallel to that of E.. coli furnish scientific
proof of the potential that shellfish can be indeed vectors of
enteric viral diseases.
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Uptake of Trace Metals by Shellfish
Shellfish can selectively concentrate metallic salts and organic
materials to levels many hundred times that in the surrounding
water. The mechanisms involved in the uptake of these inorganic
and organic materials can include the following (18):
1. Particulate ingestion of suspended material from seawater.
2. Ingestion of food material such as plankton that have acquired
these chemicals.
3. Uptake by exchange, for example, onto mucous sheets of the
. oyster.
4. The incorporation of metal ions into physiologically important
systems.
5. Complexing of metals by coordinate linkages with appropriate
organic molecules.
Polyvalent ions like A1-H+, Cu-H-, Fe-H-, Hg++ and Mn-H- are easily
caught and accumulated by the oyster, but not positive monovalent
ions like Na+ and K+ which are present in greater quantities. (1)
The capability of five species of bivalve mollusks to accumulate
metals was determined by Pringle et al (19) in controlled studies
in a simulated natural environment. The "enrichment factors"
derived from these experiments are given in Table 1 and compared
with values derived by other workers. These enrichment factors
are referred to the seawater trace metal levels reported by
Goldberg (20) . A review of these data would prompt the following
observations:
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1. In a given species of mollusk, there is a wide range of
enrichment factors among the several tracemetals studies.
For example, the factor for cadmium in oysters was found
to be 226,000 and for manganese 2,900. The factors for other
metals fall between these two values.
2. The enrichment factors for a given trace metal is often diff-
erent in other species of mollusk. For example, the factors
for copper in the oyster, the hard clam, the soft clam, and
the surf clam were found to be 14,800, 900, 2,000, and 450,
respectively. Pringle (19) states: "The apparent selectivity
for trace metals among various species appears to depend to
a considerable extent on the metals available in the environ-
ment, their chemical and physical properties, the kind and
number of ligands available for chelation, transport and stor-
age, and the stability of the complex formed."
Pringle (19) also reports on the results of a study to determine
the levels of trace metals in shellfish in the natural environment.
The average levels found in this study, which included approximately
100 stations along the Atlantic Coast from Maine through North
Carolina are given in Table 2
The values shown in table 2 are average levels. There was a
wide range of levels of several metals in samples collected from
the different estuaries. Pringle attributes this to the environ-
mental concentration of the particular metal, the temperature, the
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species concerned, and the physiological activity of the animal.
As was shown by the enrichment factors there is a differing
selectivity of trace metals by the species studied. The affinity
for zinc and copper is greatest in the oyster than in the other
mollusks ; the soft clams accumulate more iron, to cite two examples.
As a result of the discovery of mercury in Lake St. Clair, authorities
were prompted to investigate the possible occurrence of mercury in
shellfish. The EPA Water Hygiene Laboratories at Narragansett,
Rhode Island and at Dauphin Island, Alabama undertook surveys in
several estuarines in collaboration with Federal and State agencies.
In general, very low concentrations of mercury were found, well below
the recommended tolerance limit of 0.5 parts per million. Values
as high as 5.5 ppm were found in oysters harvested from an estuary
in the State of Texas, the highest value having been found in oysters
approximately 1,000 yards below a chlor-.alkalie plant.
The Uptake of Pesticides by Shellfish
Concer* over the potential pollution of estuaries by pesticides and
in turn shellfish, was spot-lighted by the massive fish kill in the
Mississippi River in 1963. To assess this potential, studies were
conducted in the estuaries in Louisiana that are influenced by dis-
charges of the Mississippi River. (21) These studies were followed
by studies of pesticides in hard clams in Raritan Bay, New York (22),
in Calveston Bay, Texas following a mosquito control program (23),
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in selected stations on the South Atlantic Coast, and the Gulf
of Mexico (24), and in Mobile Bay, Alabama (25).
In all of these studies the concentrations of chlorinated pesticides
were found to be low, predominantly below the sensitivity of the
analytical method, 0.01 parts per million. Measurable quantities
of all but one (Aldrin) of the 12 pesticides were found in many of
the samples. The highest values found were of DDT and isomers.
Maximum values of 4.61, 2.17, 2.21, and 1.45 parts per million were
found in oysters from four reefs in Mobile Bay. Even these highest
values are well below the recommended tolerance limits set by the
National Shellfish Sanitation Program (26).
Although these low concentrations of chlorinated pesticides are
judged to be of little or no concern to human consumers of shell-
fish, they are significant to the well being of mqllusks, crustaceae,
and fish. Butler (27) reports that environmental pollution of as low
as 10 parts per billion (p.p.b.) of some of these chemicals will pre-
vent normal shell growth in mollusks.
*
He also states that oysters exposed to DDT for a week grew somewhat
slower but otherwise not significantly damaged. If these oysters
are fed to fish, more than half of the fish will die within 48 hours.
Uptake of Marine Biotoxins by Shellfish
It has been known for centuries that shellfish collect and store
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naturally occurring marine biotoxins that can be lethal to man. The
most extensively studied of these toxins is the so-called saxitoxin,
which is the cause of paralytic shellfish poisoning (28). This toxin
is generated by dinoflagellates of the species Gonyaulax. It is found
in the Northeastern United States and Eastern Canada estuaries, and
on the Pacific Coast from California to Southern Alaska.
Oysters, clams, and mussels have been involved in toxicities to man,
a topic which will be discussed in another part of this report.
The occurrence of the Gonyaulax toxin is characteristically associated
with the colder waters of the North American and European continents
and, therefore, not likely to occur in Pearl Harbor. It should also
be noted that the occurrence of this toxin is not associated with
/•
domestic or industrial pollution. In fact, the first recorded
incident on this continent was in the chronicles of Vancouver (29)
who narrates an incident on landing in British Columbia in 1793.
Another biotoxin, this one generated by a -dinoflagellate Gymnodimium
breve has been associated with pollution or at least enrichment of
sea water by phosphates (30). This organism periodically attains
high population densities along the Florida West Coast, and the
coasts of Texas and Mexico. Numerous mass fish mortalities have been
associated with these "red tides". In 1962 the uptake of the toxin
by oysters and clams was demonstrated by several illnesses among
persons who had eaten these shellfish species harvested from Sarasota
Bay, Florida (31) .
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Cummins et al (32) in a survey of the occurrence of the toxin in
Gulf of Mexico estuaries detected the toxin in shellfish from the
Florida west coast estuaries that often encounter red tides.
Two types of shellfish poison found in Japan are mentioned to
illustrate possibilities of similar situations elsewhere. The
first of these, venerupin poisoning, is named after the molluscan
family Veneridae.. Two species of these clams, the Japanese little
neck clam Tapes semidecussata and the Japanese dosinia, Dosinia
•japonica are known to harbor the toxin. The Japanese oyster,
Crassostrea gigas has also been involved (33).
The geographical scope of the toxic shellfish is limited to
specific areas in the Kanagawa and Schizuoka Prefectures in Japan.
Venerupin is a lethal toxin. Mortality rates among persons that
consumed tainted shellfish have been as high as 67 percent. Akiba
(34) has associated the presence of a dinoflagellate, Prorocentrum
sp. with the occurrence of toxic clams (34). The dinoflagellate was
found in the digestive gland of the Japanese littleneck clam and
%
extracts of the dinoflagellate produced toxic symptoms in mice
similar to those produced by extracts of the clams.
The other example is a toxin found in the ovary of one of the family
Veneridae of clams, the Japanese callista clam, Callista brevisiphonata.
The clams are said to be toxic only during the spawning season. This
toxicity differs from those mentioned above in the respect that there
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has been no association with dinoflagellates, and that it occurs
only during the spawning season.
Shellfish Borne Bacterial Enteric Diseases
Knowledge that shellfish can be vectors of bacterial enteric
diseases dates back for centuries. Fisher (36) developed a partial
list of more than 100 shellfish borne outbreaks of typhoid fever or
gastroenteritis that occurred from 1815 to 1936. More recently,
Tufts (37) has supplemented this list by recording shellfish borne
outbreaks of typhoid fever, salmonellosis, and gastro-enteritis
during the period 1940 to 1968. These records were derived
from CDC Mortality and Morbidity reports and summaries. This list
includes 24 outbreaks of enteric disease scattered throughout the
United States. Shellfish associated typhoid fever occurred as
recently as 1968. Chassagne (38) reported that in France in 1960,
there were 2,263 declared cases of typhoid and paratyphoid fever.
Epidemiological reports received from 490 of these revealed that
shellfish was responsible for 83 cases. An outbreak of gastro-
enteritis involving more than 100 cases occurred in Tokyo, Japan
in 1966, (39) attributed to the consumption of oysters harvested
from areas of questionable quality and/or contaminated in processing.
An isolated case of enteric disease should not be considered lightly.
The classic series of events described by Old and Gill (40) shows
the potential for mass spreading (85 cases) of typhoid fever. The
person, an oyster fisherman contracted typhoid fever eight years
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previous to the reported shellfish borne outbreak. He became a
carrier as a result of this illness. It is hypothesized that he
contaminated his daily catch of oysters while they were in wet
storage in an area that was exposed to overboard discharges from
the boat on which he stayed overnight. He "peddled" these oysters
the hamlets in Louisiana where the illnesses occurred.
Hepatitis and Shellfish
The association of shellfish with outbreaks of infectious hepatitis
is quite recent. Roos (41)in 1956 identified oysters as the vector of
hepatitis in Sweden. He attributes 119 cases to the consumption of
oysters supplied by fish dealers in one community. The incident is
reminiscent of the outbreak of typhoid fever in 1924 and 1925 (42).
In both incidents the oysters had been subjected to wet storage in
confined basins that received discharges of human excreta. Kjellander
(43) reports that some 529 shellfish-associated cases of hepatitis
occurred in Sweden in 1956.
in the U.S.
The first recorded outbreak of hepatitis/from the consumption of raw
oyster^ (44) attributes the contamination of the shellfish to the
discharge of raw domestic sewage from a community sewerage system and .
from a commercial shipyard. During the first three months of January
1961, (while these discharges were occurring), 84 cases of oyster
related hepatitis occurred in Pascagoula, Mississippi, and Mobile and
Troy, Alabama, where the incriminated oysters had been sold to seafood
markets and one restaurant. The oysters were harvested from heavily
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contaminated waters in Pascagoula Bay, tributary to the river in which
the discharges occurred.
The consumption of raw clams from polluted waters was the cause of
infectious hepatitis in Greenwich, Connecticut in late 1960 and early
1961 (45). The source of pollution is attributed to be the partially
treated sewage treatment plant effluent serving a population of 9,700.
This discharge could reach the clam beds in less than two hours.
Excessively high coliform and fecal coliform densities were found
throughout the receiving estuary.
Other incidents of shellfish-associated hepatitis are given in Table 3.
The outbreaks in New Jersey (primarily:Raritan Fay)and Northeastern
States, Southern New Jersey, and Connecticut are the findings obtained
in epidemiologic surveillance activities by the National Communicable
Disease Center and/or state or local health agencies. In most of the
cases reported, shellfish were incriminated if the patient declared
that he had eaten shellfish within the expected incubation period
prior to the onset of illness.
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Diseases Due to Fish and Shellfish Contamination by Chemical Pollutants
Probably the most investigated incidents of disease due to the consump-
tion of metal contaminated fish and shellfish are the two outbreaks
of mercury poisoning in Japan. The earlier of these occurred in the
Minamata Bay area, in Kumomoto Prefecture (46). The source of the
mercury was a vinyl chloride and an acetaldehyde plant that discharged
mercury contaminated waste water into Minamata Bay and the Minamata
River. During the period 1950 to 1960, the waste was discharged with-
out treatment. A treatment plant was installed in 1960 but it allowed
some organic mercury to be discharged. Improvement in the treatment
process in 1966 resulted in an abrupt decrease of the mercury content
of fish in the discharge area. Minamata Bay is not suitable for
commercial fishing but had been used as a source of seafood for many
families inhabiting the small villages (total population 10,000) on
the shores of the Bay.
During the period 1953 to 1960, 111 cases of mercury poisoning due
to the consumption of fish or' shellfish were reported. The death rate
was 36.9%, but most of the survivors have suffered permanent and severe
disability. That methyl mercury was the causative agent was confirmed
by finding methyl mercury compounds in the waste, in fish and shellfish,
and in the victims of the disease.
There was a similar outbreak of organic mercury poisoning in Niigata,
Japan (47), resulting from discharges of an acetaldehyde plant. During
the period June 1964 to July 1965, 26 cases of methyl mercury poisoning,
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with 5 deaths have been documented.
The symptomology of Minamata Disease, the environmental and physio-
logical pathways and other details are beyond the scope of this report.
However, it must be noted that inorganic mercury can be converted to
the highly toxic methyl form as a result of biological action in
sediments on river and lake bottoms. This biological process is said
to be responsible for the return of a highly toxic agent to the aquatic
biota that otherwise might be stable deposits of mercury in sediments.
The Minamata Disease incidents are examples of acute effects resulting
from relatively short time exposures to a highly toxic material. Such
episodes are relatively easy to detect, and if found in time, remedial
and preventive measures can be undertaken. The more subtle health
effects on man are those resulting from long-term exposure to low
environmental levels of a toxic material or combinations of such
toxicants. There is some knowledge, although not adequate, of the
maximum total body burden of many toxicants from all sources that
should not result in these long-term adverse effects and these are
referred to in the development of safe tolerance limits in water,
foods, &nd other media consumed by man or to which he may be exposed.
Tolerance limits for metals, pesticides and radionuclides in shellfish
(48) (49) have been proposed, based on the above mentioned and other
criteria for their establishment.
In the application of these limits to shellfish in.an individual
environment, it should not be concluded that if one finds levels of
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one or more of these agents in excess of the tolerance, the shellfish
are acutely dangerous to eat. Rather, the conclusion must be drawn that
consumption of these shellfish will place an unexpected and perhaps even
unknown stress on the body burden. The seriousness of this will vary
with the toxicant and the nature of its physiological effect on man.
The reason for eliminating discharges of such toxic agents into shell-
fish areas becomes obvious.
i
Marine Biotoxins in Shellfish
It was mentioned earlier in this report that the occurrence of paralytic
;
shellfish poison is not associated with domestic or industrial pollution,
and, therefore, is of only passing interest. Halstead (50) lists more
than 957 cases, with more than 222 deaths, worldwide, from 1689 to 1962.
The toxin generated by the dinoflagellate Gymnodinium breve has been
associated with pollution or at least enrichment of the marine area by
phosphate (30) . This organism has been associated with massive fish
kills that occur periodically on the coast of the Gulf of Mexico.
Definite association of human illness due to the consumption of shell-
fish contaminated with the toxin was demonstrated in December 1962 (31).
Several persons became ill after eating oysters, Crassostrea virginica,
and clams, Mercenaria campechiensis harvested from Sarasota Bay, Florida
while a red tide outbreak was occurring. The symptoms in man were not
similar to those produced by the paralytic shellfish poison. They
were similar in many respects to those produced by the ciguatera fish
poison found in certain fishes of the Pacific and the Carribean.
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Another observation made by Cummins (51) is relevant to the recreational
use of marine areas. Irritation of the upper respiratory tract was
experienced by field staff during the course of surveys and sampling
tours. The symptoms were spasmodic coughing, sneezing, and respiratory
distress. On some occasions, irritation of the eye was experienced.
The cause of these irritations was the inhalation of toxic products
in the red tide blooms that had become aerosolized by rough surf action
resulting from brisk winds. These observations were similar to those
of other workers in red tide areas (52). It is probably the cause of
a similar series of incidents on the coast of New Jersey in 1968.
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Discussion
There is no doubt that consumption of shellfish taken from polluted
waters is extremely hazardous. History has shown that diseases have
occurred and, therefore, it is predictable that outbreaks will con-
tinue to occur. The frequency of occurrence is a function of not
only the presence and quantities of domestic and industrial waste
discharges, but also the occurrence and prevelance of specific
bacterial or viral disease and non-symptomatic carriers of such
diseases among the contributing population and the presence and
quantities of toxic agents in the domestic and industrial waste
discharges.
There are many unknowns in the picture. For example, at the time of
the Minamata incident it was known that organic mercury compounds were
toxic, but the extreme toxicity of methyl mercury was not known, nor
was the fact the bacterial action in bottom sediments can convert in~
organic mercury to methyl mercury. There is still not a clear under-
standing of the long-range chronic effects of many metallic ions or
organic compounds. The causative agent(s) of infectious hepatitis
have not been identified, and cultural methods for these agent(s) have
not been developed.
It should also be recognized that so long as shellfish are present in
polluted estuaries, they will be enticing to sports fishermen and un-
scrupulous commercial fishermen. Resulting diseases will be inevitable.
Patrol of polluted areas may have resulted in reducing the extent of
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bootlegging, but as' history will demonstrate it has not eliminated
the occurrence of disease. The most logical approach is the removal
of shellfish from polluted areas. Obviously, it would be desirable
to make productive use of these resources and there are methods
available that to some extent and with certain contaminants these
methods will result in the decontamination or detoxification of the
mollusks.
Relaying of shellfish from polluted to clean waters has been practiced
for centuries. This procedure exploits the well known ability of
mollusks, by way of their feeding mechanisms and other physiological
processes to attain equilibrium with the new aquatic environment.
Equilibrium is attained fairly rapidly in the case of bacteria and
viruses, but, in the case of metallic ions and toxins, it proceeds
slowly, requiring many months with some agents.
Relaying involves some risks. These include mortality of shellfish
and the continued possibility of poaching. Little can be done about
the former, except to conduct the activity at periods of optimal
activity of the shellfish and to avoid as much as possible the oppor-
tunity for the ravages of predators. Poaching can be minimized by
proper selection of the clean water area, tight patrolling of the area,
and control of harvesting, planting and re-harvesting.
Controlled purification, (Depuration) utilizes the same biological
principles, but differs from relaying in that the process is carried
out in tanks on shore, using purified water, or in cribs or floats
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located in areas of extremely high sanitary quality. The high cost
of facilities construction, handling of the shellfish and power costs
for pumping place severe limitations on the period of time of exposure
of a given lot of shellfish to this process.
It would be economically feasible to provide for preferably two and
not more than three days holding. Therefore, the depuration process
would be applicable only to removal of bacteria or viruses. It has
also been demonstrated that there is an upper limit of levels of
bacteria and viruses beyond which the depuration process is unreliable.
This limit has not yet been clearly defined but it is quite definite
with the present state of knowledge, the depuration process would not be
reliable with oysters showing the coliform densities that currently
prevail in Pearl Harbor.
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REFERENCES
1. Korringa, P., 1952
Recent advances in oyster biology.
Quarterly Review of Biology 27:266-308
2 Nelson, T. C., 1938
. The feeding mechanism of the oyster.
J. Morph .63:1-61
3. MacGinitie, G. E., 1941
On the method of feeding of four Pelecypods.
Biol. Bull., Woods Hole .80:18-25
4. MacGinitie, G. E., 1945
The size of the mesh openings in mucous nets of marine animals.
Biol. Bull., Woods Hole, 88:107-111
5. Gallsoff, Paul S., 1928
The effect of temperature on the mechanical activity of the gills
of the oyster.
Jour. Gen Physiol 11:415-431
6. Loosanoff, V. L., 1958
Some aspects of behavior of oysters at different temperatures.
Biol. Bull., 114:57-70
7. Loosanoff, V. L., 1958
Rate of water pumping and' shell movement of oysters in relation to
temperature.
Anat. Rec. 108:132
8. CheStnut, A. F., 1946
Some observations on the feeding of oysters with special reference
to the tide.
1946 Proc. National Shellfish. Assoc, 22-27
9. Galtsoff, Paul S., W. A. Chipman, J. B. Engle, and H. N. Calderwood,
1947
Ecological and physiological studies of the effect of pulp-mill
wastes on oysters in the York River.
Fish Bull. 51:59-186
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REFERENCES (Continued)
10. Loosanoff, V. L., and J. B. Engle, 1948
Effect of suspended silt and other substances on the rate of
feeding of oysters
Science, JL07:69-70
11. Kelly, C. B., 1955
Public Health Service research on shellfish bacteriology.
1955 Proceedings, National Shellfisheries assoc., 46;21-26
12. Kelly, C. B. 1961
Accumulation of bacteria by the Pacific and Olyrapia Oyster.
Proceedings, 1961 Shellfish Sanitation Research Conference
Manuscript Report
13. Beck, W. J., C. B. Kelly, J. C. Hoff, and M. W. Presnell, 196
Bacterial depuration studies on West Coast shellfish.
Proceedings. 1963 Shellfish Depuration Conference
14. Kelly, C. B., W. Arcisz, and M. W. Presnell, 1960
Bacterial Accumulation by the Oyster, Crassostrea virginica on
the Gulf Coast.
RATSEC Technical Report F 61-9
U. S. Public Health ServiceDHEW.
15. Metcalf, T. G. and W. C. Stiles, 1968
Enteroviruses within an estuarine environment.
Am. J. Epid 88:379-391
16. Liu, 0. C., 1970
Viral pollution and Disinfection of shellfish
Proceedings, National Specialty Conference on Disinfection
AmV Soc. Civil Engineering 1970 .
17. Mitchell, J. R., M. W. Presnell, E. W. Akin, J. M. Cummins, and
0. C. Liu, 1966
Accumulation and elimination of poliovirus by the Eastern Oyster.
Am. J. Epid 84.:40-50
18. Brooks, R. R., and M. G. Rumsby, 1965
The biogeochemistry of trace element uptake by some New Zealand
bivalves.
Limnology Oceanography 10:521.
-------
REFERENCES (Continued)
19. Pringle, B. H., D. E. Hissong, E. L. Katz, and S. T. Mulawka., 1968
Trace metal accumulation by estuarine mollusks.
J. Sanit. Eng. Div. 94:355-475.
20. Goldberg, E. D., 1957
The biogeochemistry of trace metals
Treatise on Marine Ecology and Paleoecology, Vol. I., Ecology.
J. E. Hedgepeth, Ed.
Memoir 67, Geological Society of America
21. Hammerstrom, R. J., R. T. Russell, R. M. Tyo, E. A. Robertson,
J. L. Gaines, and J. C. Bugg, 1967
Study of pesticides in shellfish and estuarine areas of
Louisiana
PHS Publication 999 UIH-2
U. S. Department of HEW
22. Pringle., B. H., 1967
A report on the analytical chemical data on shellfish from
Raritan Bay.
Proceedings, conference, pollution of Raritan Bay and adjacent
interstate waters, Vol. 2: Appendix G. 816-863.
23. Casper, V. L., 1967
Galveston Bay pesticide study
Pesticides Monitoring J. ^:13 15.
24. Bugg, J. C., J. E. Higgins, and E. A. Robertson, 1967
Chlorinated pesticide levels in the eastern oyster from selected
areas on the South Atlantic and the Gulf of Mexico
Pesticides Monitoring J. 1^:9-12.
25. Camper, V. L., R. J. Hammerstrom, E. A. Robertson, J. C. Bugg,
and J. L. Gaines, 1969
Study of chlorinated pesticides in oysters and estuarine
environment of the Mobile Bay area
Public Health Service Technical Report
Bureau of Water Hygiene
U. S. Department of Health, Education and Welfare
-------
REFERENCES (Continued)
26. Morrison, G. Ed.
Interim guidelines for pesticides in shellfish
Proceedings, sixth National Shellfish Sanitation Workshop
pp 53, 54.
Consumer Protection and Environmental Health Service
U. S. Department of HEW
27. Butler, P. A., 1969
The Bureau of Commercial Fisheries Pesticide Monitoring Program
Proceedings, 1967 Gulf Coast and South States Shellfish Sanitation
Research Conference
PHS Pub 999-UIH-9 pp 81-84
28. McFarren, E. F. et al 1960
Public Health significance of paralytic shellfish poisoning
Advances in Food Research 10:
29. Vancouver, G., 1801
A voyage of discovery to the North Pacific Ocean and around the
world
Vol. IV, pp 44-47, John Stockdale, London
30. Rounsefell, G. A., and W. R. Nelson, 1966
Red-tide research summarized to 1964, including an annotated
bibliography.
U. S. Fish and Wildlife Service Special Scientific Report
no. 535, 85 pp.
31. McFarren, E. F., F. J. Silva, W. B. Wilson, J. E. Campbell,
and K. H. Lewis, 1965
The occurrence of a ciguatera ~ like poison in oysters, clams, and
»G breve culture.
Toxicon 3:111-123
32. Cummins, J. M., J. E. Higgins and E. A. Robertson, 1967
Occurrence of Ciguatera - Like Biotoxins in shellfish from the
Gulf of Mexico.
Technical Report, Gulf Coast Water Hygiene Laboratory 67-7.
-------
REFERENCES (Continued)
33. Akiba, T., and Y. Hattori, 1949
Food poisoning caused by eating Asari, Venerupis semidecussata,
and oysters, Cr ass os t rea gigas, and studies on the toxic
substance venerupin.
Jap. J. Exp. Med. 20:271-284
34. Akiba, T., 1961
Food poisoning due to oysters and baby clams in Japan and
toxicological effects of the toxic substance
Symposium papers, Tenth Pacific Sci. Cong., Honolulu, pp. 446-447
35. Asano, M., F. Takayanagi, and Y. Furukara, 1950
Studies on toxic substances in marine animals. II Shellfish
poisoning from Callista brevisiphonata in the vicinity of
Mori, Kayabe county., (Japan)
Bull. Fac. Fish., Hokkaido Univ. 7.:26-36
36. Fisher, L. M., 1937
Report of the Committee on Shellfish, Public Health Engineering
Section, American Public Health Association.
Am. J. Pub. Health 27:180-196
Supplement March 1937
37. Tufts, N. A., 1966
Shellfish Borne Diseases
In Training Course Manual Sanitary Surveys of Shellfish Growing
Areas Northeast Marine Health Sciences Laboratory
Narragansett, Rhode Island
38. Chassagne, P., and Y. Gaignoux, 1962
Epidemiology of typhoid and paratyphoid infections in France
*in 1960
Bull. Inst. National Hygiene Jan.-Feb. 1962:81-108
39. Personal communication
40. Old, S. L., and S. L. Gill, 1940
A typhoid fever epidemic caused by carrier bootlegging oysters
Am. J. Pub. Health 30:633-640
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REFERENCES (Continued)
41. Roos, B., 1956
Hepatitis epidemic conveyed by oysters
Svenska Lakartin, 53;989-1003
42. Lumsden, L. L., H. E. Hasseltine, J. P. Leake, and M. V. Veldee,
1925
A typhoid fever epidemic caused by oyster-borne infection (1924-25)
Supplement No. 50 to the Public Health Reports,.1925.
43. Kjellander, J., 1956
Hygienic and microbiologic viewpoints on oysters of infection
Svenska Lakartin 53:1002-1016
44. Mason, J. 0., and W. R. McLean, 1962
Infectious hepatitis traced to the consumption of raw oysters
Am. J. Hyg. .75.:90-111
45. Rindge, M. E., S. D. Clem, R. E. Linkner, and L. B. Sherman, 1962
A case study on the transmission of infectious hepatitis by raw
clams
Special report, U.S. DREW, PHS, 36 p .
46. Kurland, L. T., S. N. Faro, and H. Siedler, 196
Minamata Disease
World Neurology 1:370-395
47. Irukayama, K., 1966
Paper No. 8
Third International Conf. Water Poll. Res.
48. Morrison, G., Ed, 1969
Interim guidelines for radiomuclides and pesticides in shellfish
Proceedings, sixth National Shellfish Sanitation Workshop
U.S. Department HEW.
49. Pringle, B. H., and C. N. Shuster, 1968
A guide to trace metal levels in shellfish.
-------
REFERENCES (Continued)
50. Halstead, B. W.
Poisonous and venomous marine animals of the world. Vol. one,
Invertebrates pp 185-187, U.S. GPO, 1965.
51. Cummins, J. M., and A. A. Stevens, 1970
Investigations of Gymnodinium breve toxins in shellfish
Special Report, Bureau of Water Hygiene, E.H.S., US DREW
52. Woodcock, A. H., 19A8
Note concerning human respiratory irritation associated with high
concentrations of plankton and mass mortality of marine organisms,
J. Mar. Res. 7:56-62
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TABLE !•• - TRACE METAL ENRICHMENT FACTORS FOR SHELLFISH
COMPARED WITH THAT OF THE MARINE ENVIRONMENT
Element
(1)
Cadmium
Chromium
Copper
Iron
Manganese
Nickel
Lead
Zinc
Oyster *
(2)
318,000a
266,000
60,000a
31,600
13,700a
14,800
68,200a
6,700
4,000a
2,900
4,000a
3,250(1)
4,000a
4,100
110,300a
148,000
Quahaug
(3)
750
23,400
-•• 900
3,000
2,900
4,500
5,800
2,100
Soft Shell Clam
(4)
800
10,400
2,000
41,000
3,350
4,250
3,400
1,700
Surf Clam Mussel Whelk
(5) (6) (7)
100,000a
800(2) 6,300
- _
3,000a
45Q 1,150 3,800
196,000a
18,400 2,900
13,500a
1,100 1,500 2,100
- -
_
9,100a
1,525 2,200 8,200
a Values from work of Brooks and Rumsby (5).
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TABLE 2. - AVERAGE TRACE METAL LEVELS IN SHELLFISH TAKEN FROM
ATLANTIC COAST WATERS, IN PARTS PER MILLION OF WET WEIGHT
Element *
Zinc
Copper
Manganese
Iron
Lead
Cobalt
Nickel
Chromium
Cadmium
Eastern Oyster
1428
91.50
4.30
67.00
":" 0.47
0.10
0.19
0.40
3.10
Soft Shell Clam
17
5.80
6.70
405
0.70
0.10
0.27
0.52
0.27
Northern Quahaug
20.6
2.6
5.8
30
0.52
0.20
0.24
0.31
0.19
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TABLE 3 — Outbreaks of Infectious Hepatitis Associated with Ingestion of Shellfish
1.
2.
3.
4.
5.
6.
7.
8.
9.
Location of
Outbreak
Sweden
Mississippi
and Alabama
North Carolina
New Jersey
N.E. States
Fairfield County,
Connecticut
Southern New Jersey
and Greater Phila-
delphia Area
Connecticut
Canada
East Brunswick,
New Jersey
Tnt-nl
Year Month with Vehicle Number of Period of
Peak Number Cases Known Outbreak
of Cases
1955 December European Oyster 529 40 Days
1961 January Eastern Oysters 84 57 Days
1964 March Eastern Oysters . 3 9 Days
(and Clams)
1961 February Hard Clams 493 5-6 mos .
1961 March Hard Clams 50 15 weeks
(some were cooked)
1964 January Hard Clams 252 5-6 mos.
1964 January Hard Clams 123 5-6 mos.
1965 ? Pacific Oysters 3 ?
1966 October Hard Clams 4 1 month
(some were cooked)
IQSS-fifi riirct-OT-c PI amo 1 SAT
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