bivalve mollusks control of microbiological contaminants
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Bivalve Mollusks: Control of Microbiological ContaminantsAuthor(s): Edward P. Larkin and Daniel A. HuntSource: BioScience, Vol. 32, No. 3 (Mar., 1982), pp. 193-197Published by: University of California Presson behalf of the American Institute of Biological SciencesStable URL: http://www.jstor.org/stable/1308942.
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8/10/2019 Bivalve Mollusks Control of Microbiological Contaminants
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ivalve Mollusks
Control
o
Mcrobiological
ontamnants
Edward P. Larkin and Daniel A. Hunt
Voluntary
ooperation
etween
he shellfish
ndustry
nd
government
gencies
has
reduced
he incidence
of
shellfishborne
isease.
Contamination
f
bivalvemollusks
by
bacterial
athogens,
iruses,
and
toxin-containing
hytoplankton
s
controlled
by harvesting
hellfish
only
from
approved
watersand
by
the
use
of
sanitary
ood-
handling
ractices. Accepted
or publication
2 October
981)
Historically,
shellfish
made a
signifi-
cant contribution
o the
American
diet.
Early
inhabitants
ound
abundant
sup-
plies
of bivalve
mollusks
hat could
easi-
ly be harvested year-round. Shellfish,
along
with
an
ample supply
of
fish,
pro-
vided
high
quality protein
with little ef-
fort
or
cost
to the
consumer.Even
today
fish and
shellfish
proteins
are
highly
competitive
with other
animal
proteins,
especially
in areas
along
the extensive
US
coastline.
The value of the
shellfish
grounds
to
the
early
settlers
was
demonstrated
n
1659
when the Dutch
Council
of
New
Amsterdam
assed
an
ordinance
imiting
shellfish
harvesting
in the East
River.
Similar
egislative
actions
pertaining
to
conservationof the shellfish resources
were
passed
in New
York
(1715),
New
Jersey
(1730),
and
Rhode
Island
(1734)
(Houser
1965).
Records
on the
quantity
of
shellfish
harvested
n the
United
States
were
not
reported
until the late
1800s.
In 1890
more than
15 million
pounds
of
oyster
shellstock
were
harvested from
the San
Francisco
Bay.
Because
of
pollution,
shellfishing
has
been
prohibited
in the
Bay
since
1930
(Jarvis
1980).
In 1897
more
than
40,000
bushels of
soft-shell
clams
were harvestedfrom
the Boston
Harbor.This shellfishareawas closed in
1907
(Field
1909).
The Raritan
Bay,
which borders
on the shores
of New
York and
New
Jersey,
was a
yearly
source of
thousands
of bushels
of hard-
and soft-shellclams
and
oysters.
On the
New York
portion
of the
shore alone
more
than
20,000
acres
of
the
estuary
were used
in 1900 or
oyster
production,
with
a
yearly
income
of
$2-4
million.
The
oysters
were
extirpated
n
1916
be-
causeof
pollution.
By
1960
pollution
had
caused the closing of all but 10%of the
original
Raritan
Bay
shellfish
harvesting
grounds.
Since
1961,
shellfishing
n
the
bay
has been
prohibited
because of
out-
breaks
of
hepatitis
A that
were shown
to
be associated
with
raw
clam
consump-
tion
(Campbell
1965).
A
similar
situation
occurred
n the
Narragansett
Bay
area,
which also lost
its
oyster
resource
to
pollution.
Older
residents
of
the
Chesapeake
Bay
area
remember
that
oyster
shucking
plants
were
in
operation
in
the
early
1900s
that
employed
more
than
100
shuckers and processed close to 1 mil-
lion
oysters/day.
During
he
peak
of
the
oyster-producing
period
in
the
small
town
of
Oxford, MD,
one could walk
around
he
village
by crossing
from
boat
to boat
when the
oyster
fleet
landed
to
unload
ts catch
in
the
late
afternoon.On
one dock there
were five
shucking
houses.
Today,
there
are
none.
Natural
phenomena,
overfishing,
and
pollution
have reduced
shellfish
re-
sources.
In
some
areas,
chemical
pollu-
tion,
disease,
and
predators
have elimi-
nated
some
species
of
shellfish,
whereas
organic
pollution has enhanced the
growth
of other
species
of
shellfish.
Wa-
ter
microbiological
standards
prohibit
harvesting
rom
polluted
areas,
but
regu-
latory agencies
allow
shellfish
to be
transferred
ut
of
polluted
areas. Trans-
fer from
nonapproved
o
approved
areas
is called
relaying,
whereastransfer
o
seawater
anks
s referred o as
depura-
tion.
Relaying
and small
depuration
units are
used to recover
oysters
from
organicallypolluted
waters
in a number
of areas in
the United
States.
For more
than
50
years
soft-shell
clams
recovered
from
moderately polluted
waters
have
been
depurated
n Massachusetts.
Shell-
fish harvested
rom
approved
areas
may
be
conditioned
in seawater
tanks
for
direct
marketing
f
proper
controls
are
maintained.
This
process
is used
for
sand
removal
and for
short-term
natural
stor-
age
of
the
product.
THENATIONALHELLFISH
SANITATION
ROGRAM
Outbreaks
f
typhoid
fever
during
he
winter
of
1924-25
were
shown
to
be
associated
with the
consumption
of
raw
shellfish
and resulted
n the
development
of
what is now known
as the
National
Shellfish Sanitation
Program
NSSP),
a
voluntary, cooperative
program
or
the
sanitary
control
of
bivalve
mollusks-
oysters,
mussels,
and clams
(Jensen
1962).
The
program
was
different from
other food
programs;
t
evaluated
and
controlled he sanitary qualityof estua-
rine
waters in
which shellfish
were
grown,
because
the
conventional
food
sanitation
practice
of
monitoring
he bi-
valves
failed to
prevent
shellfishborne
diseases.
The
NSSP
is a
cooperative
program
between
the
US Public
Health
Service,
the
state
shellfish
control
agencies,
and
the
shellfish
ndustry.
The technical
and
administrative
ctivities
of the
program
are
carried
out
by
state
or
foreign
shell-
fish
control
agencies
and
the Food and
Drug
Administration
FDA).
The shell-
fish industrycooperates by harvesting
only
from
approved
watersand
by
com-
plying
with
sanitarypractices
outlined
n
the
NSSP
Manual
of
Operations
(Hauser
1965).
The FDA administers
he
NSSP
at
the Federal
evel
and
is
respon-
sible
for
state
and
foreignprogram
valu-
ation,
standards
development,
research,
training,
and
publication
of
the
Inter-
state
Certified
Shellfish
Shippers
List.
In
1948,
Canada
became the
first
nterna-
tionalmember
of
the
NSSP
by
interna-
tional
agreement.
Today
six
more for-
Larkin
s
with the
Virology
Branchand
Hunt
s with
Shellfish
anitation
n the Division of
Microbiology,
Bureau
of
Foods,
Food and
Drug
Administration,
1090Tusculum
Ave., Cincinnati,
OH
45226.
March 1982
193
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eign programs
England,
Iceland,
Japan,
Korea, Mexico,
and New
Zealand)
are
associatedwith the
NSSP.
Four
important
factors were
consid-
ered in
the
development
of
standards
nd
criteria
for the
NSSP
(Jensen
1962):
Most
of the
commercially
important
shellfish
grow
in
estuaries that
are
mix-
tures of
seawater and
fresh water
from
tributary
ivers;
shellfish
are
filterfeed-
ers that obtain their food
by
pumping
water
containing particulate
material
over a
complex gill
system;
during
the
feeding
process,
chemical and
biological
contaminants
uch as
bacteria
and virus-
es
may
be
ingested;
and
shellfish
may
be
eaten in
the raw
state
or
after a
minimal
heatingprocess
(which
may
not
destroy
biological
contaminants or
heat-stable
marine
oxins).
The
sanitary
quality
of shellfish
is de-
termined n
part by
the
quality
of
the
overlying
waters. If
pollution
occurs,
shellfish concentrate contaminatingor-
ganisms
from
environmentalwaters. As
the water
quality improves,
chemical
and
biological
contaminants re
depleted
through
natural
purification
processes
that
may
require
rom
one
to
many
days.
These
purification
processes
depend
on
the
pumping
activity
of the
shellfish,
which is
controlled
by
factors such
as
water
quality,
temperature,
alinity,
tur-
bidity,
size,
and the
presence
of
organic
and
inorganic
materials.
Historically,
the
sanitary
quality
of
potable
water has
been
assessed
on the
presenceor absenceof coliformbacteria
that
are
commonly
found in
the
intes-
tines
of
warm-blooded
animals. These
indicator
organisms
are
evidence
that
sewage
is
present
in
the
water
and is
presumptive
evidence that
disease or-
ganisms
may
be
present.
Use
of
such
water for
potable
purposes
or for shell-
fish
production
s
potentially
hazardous
and
of
public
health
concern. When
pathogenic
organisms
are
present,
they
will
usually
be
in
lower
numbers han
the
indicator
organisms.Thus,
when indica-
tor
organisms
are absent
or in low
num-
bers,
the water
may
be
safely
used.
All of the abovefactors influenced he
decision
to
control and
classify
the
estu-
ary
waters and
not
the shellfish.
Results
of a series of
studies indicated that the
proposedguidelines
would be
acceptable
to all
shellfish-producing
states,
the
shellfish
harvesters,
and the
processors.
The
guidelines
included the
following:
There shouldbe no
nearbydischarges
of
sewage
containing
human or animal
wastes;
the waters should be
free of
dangerous quantities
of industrial
wastes;
the waters should
be
essentially
free of
paralytic
hellfish
poison;
and
the
coliformbacteria
present must
not
ex-
ceed
a
median
value of 70/100
ml of
water
and not more than
10% of the
samples
should exceed
230/100 ml.
In
addition,
he
samples
shouldbe
collected
from
areas
most
likely
to be
exposed
to
contamination
(Jensen
1962,
Houser
1965).
These
criteria are not
static
but
are
subject
o review and modification
at
National
Shellfish
Sanitation
Program
workshops
and
by
the
various
regulatory
organizations.
Recently,
bacteriologists perfected
procedures
for
detecting
fecal
coliform
bacteria,
which are
believed
to be
better
indicators
of direct
fecal
pollution
than
the
total
coliform
group.
A
fecal
coliform
index
of 14/100 ml
of water has
been
accepted
for
approved
shellfish
waters
and
is
being
used
by
shellfish
control
agencies
(Hunt
and
Springer
1974).
Nei-
ther the coliformnor the fecal coliform
testing
procedures guarantee
that har-
vesting grounds
are
free of
pathogens
(Andrews
et al.
1975),
but
they
statisti-
cally
reduce the
potential
of
shellfish
contamination
by pathogens.
Since
the
inception
of
the
program,
bacterial diseases
related
to shellfish
consumption
have been
dramatically
e-
duced.
Periodically,
however,
virus dis-
eases
such
as
hepatitis
and
gastroenteri-
tis have
been
transmitted
by
shellfish
that were
consumed raw
or
partially
cooked. In
a number of
cases,
the
in-
criminated hellfishwereharvested rom
unapproved
areas
by
recreational
pick-
ers
or
by
shellfishermen
during
imes
of
adversity
or
depleted
resources in the
open
harvesting
areas.
SHELLFISH
ECTORSOF
DISEASE
Between
1970
and
1978,
50 outbreaks
of
foodborne
disease
associated with
shellfish
consumption
in
the
United
States
(Table
1)
were
reported
(Bryan
1980).
Most of the
microorganisms ound
in shellfishare natural nhabitants
of the
waters
and
are not detrimental to
the
consumer.However, waters
contaminat-
ed
by
human
and animal wastes
may
contain
pathogens.
Bacteria
of known
public
health
signif-
icance that
may
be found in
polluted
waters
vary
in
type
and
number,
accord-
ing
to the health
of the contributors
to
the
pollution
source
and the
degree
of
treatmentor dilution
of the
sewage.
Bac-
terial
pathogens
potentially
hazardous
o
the shellfish
consumer are:
Escherichia
coli,
Proteus
sp.,
Pseudomonas
sp.,
Sal-
monella
sp.,
Shigella sp.,
Yersinia
sp.,
Vibrio
sp.,
and
Campylobacter
sp.
While
shellfish
are
alive,
organisms
associated
with mammalian iseases
do
not
usually
multiply
n the shellfish issues
or
intesti-
nal
tracts.
However,
dead or
cooked
shellfish
provide
a
suitable
medium
for
bacterialgrowth(Brownand Dorn 1977,
D'aoust
et al.
1980,
Hackney
et al.
1980,
Kaper
et al.
1979,
Peixotto et
al.
1979,
Vanderzant
and
Thompson
1973).
Shellfish-associated
hepatitis
out-
breaks
have demonstrated he
potential
for the
transmission
of virus diseases
by
shellfish.
More than 100 different
types
of viruses
are known
to be
present
in
domestic
sewage
(see
box).
The
poliovi-
ruses
havebeen recovered
from shellfish
more
frequently
than other viruses
be-
cause
of
ongoing
mmunization
rograms
in which
young
children are fed
live,
attenuatedviruses that replicate in the
intestinebut
produce
few or
no
clinical
symptoms.
Feces
from such
children
containvirus
levels of
103-106/gram,
and
virus
sheddingusually
continues
for
sev-
eral
days.
Epidemiologically
t is
difficult
to
prove
that enteroviruses
have
been
associated
with shellfishborne
disease in
man,
even when it is known
that
very
low
levels of virus are
infectious when
consumed.
Recently,
rotaviruses
have
Table
1.
Foodborne disease outbreaks associated with bivalve mollusks
(1970-78).
Shellfish
Grand
Causative
Agent
Clams
Oysters
Mussels
(unspecified)
Total
Vibrio
holerae 1
1
Escherichia oli
1
1
Shigella
1
1
Staphylococcus
aureus
1
1
Vibrio
arahaemolyticus
1
1
Hepatitis
A 1 1 1
3
Paralytic
hellfish
poison
8 5 1
14
Diseases of unknown
tiology
14
5
9
28
Total 24
6 5 15
50
194
BioScience
Vol. 32
No. 3
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Potential
Human
Virus
Contaminants of
Shellfish
Picornaviruses
Polioviruses
1-3
CoxsackievirusesA 1-24
CoxsackievirusesB 1-6
Echoviruses
1-34
Enteroviruses
8-71
ProbablyHepatitis
A
Reoviruses
Reoviruses
1-3
Rotaviruses
Parvoviruses
Human
gastrointestinal
iruses
Adenoviruses
Human
adenoviruses
1-33
Papovaviruses
Human
BK
and
JC viruses
been
shown to infect infants and
young
childrenand to
produce
clinical and sub-
clinical
gastrointestinal
disease. Feces
from such
infants
may
contain
virus
con-
centrations
of
107-109/gram
Konno
et
al.
1977).
Such
viruses
probably
contam-
inate
sewage
to levels
approaching
hose
of
coliform
bacteria.
Laboratory
ell
cul-
ture
methods are not now available to
detect human
rotaviruscontamination f
sewage
or
shellfish-growing
waters.
Studies of
shellfish waters
and sedi-
ments
indicate that the coliform stan-
dards
may
not be sensitive
enough
to
ensure
virus-free
waters or
shellfish
(Gerba
et
al.
1980,
Marzouket al.
1979),
for a numberof
humanviruses have been
isolated from market shellfish and from
shellfish
harvested from
approved
wa-
ters
(Table 2).
Current detection
meth-
ods
indicatethat
virus
pollution
of
shell-
fish beds is
probably
sporadic,
so
it
might
be unwise to substitute a virus
standard for the
coliform
index.
The
coliform and fecal coliform indicator
groups
measure
the
amount
of
sewage
present
in
shellfish-growing
waters
(Hunt 1977, 1980).
Increasing
the
coli-
form index to
a more
restricted level
in
an
attempt
to reduce
the
potential
for
virus contamination
would eliminate
many shellfish waters that historically
have never
been
associated
with out-
breaksand would
reduce the
quantity
of
shellfish harvested,
with a
resulting
in-
crease
in
price
to
the
consumer.
In addi-
tion,
such action
might
increasethe vol-
ume of
illegally
harvested
shellfish
reaching
he
consumer.
PARALYTIC
HELLFISH
OISONING
During
the warm
summer
and
early
autumn,
the
waters
of
many
coastal
ar-
eas become
inundatedwith
phytoplank-
ton that
may
become
so
concentrated
that a
brownish-pink
uminescent sheen
can
be
observed
in
the
sea.
This
phe-
nomenon is
referred to as the red tide.
Some of the
phytoplankton
roduce
neu-
rotoxins
hatare
bioaccumulated
by
mol-
lusks
during
the
filter-feeding
process.
These
organisms
are
ingested
along
with
other
particulate
matter,
and
the
toxins
are
concentrated
n shellfish issues.
The
principal
neurotoxin recovered from
these
organisms
s
saxitoxin,
one of the
most
powerful
natural
poisons
known.
Species
of
Gonayaulax
are
responsible
for
most of the
paralytic
shellfish
poison-
ing
in
the
United
States.
The Alaskan
butterclam and mussel species are the
most
dangerous
animals
o shellfish con-
sumers,
although
clams,
scallops,
and
whelks
have been the vehicles of saxi-
toxin
poisoning.
Carnivorous
marineani-
mals,
such as the moon
snail,
frequently
become toxic after
eeding
on small
mus-
sels that
have been
exposed
to the dino-
flagellates.
The shellfish bioaccumulate
sufficient
axitoxinwithin
a
few
days
and
become hazardous o the consumer
with
usually
no
apparent
adverse reactions to
the
shellfish.
Exposure
to
phytoplank-
ton-free
water results
in
clearance
of the
toxin by shellfish. The time required
varies with the
toxin concentration
and
shellfish
species,
but
generally
a much
longer
time is
required
o eliminate
oxin
than bacteria.
The red mussel is used as
a sentinel
species,
since it
rapidly
ncor-
porates
the
poison
and
usually
becomes
toxic sooner than
other shellfish.
The red tide in the Gulf
of Mexico
is
caused
by
a different
species
of
dinofla-
gellate, Ptyschodiscus
brevis. Blooms
created
by
this
organismmay encompass
thousands
of
square
miles.
The wind and
tide move the
phytoplankton
around he
tip
of Floridaand
up
the
east coast.
The
cell
membrane
of
this
dinoflagellate
s
more
easily
ruptured
than that
of
the
Gonayaulax
pecies.
As
waves
carry
the
organism
onto
the
shore,
the
cell mem-
branes
rupture,
and the toxin is
carried
inlandwith the ocean winds
and
sprays.
Temporary
respiratory
rritationoccurs
in humans
exposed
to this contaminated
air. The toxin is also bioaccumulated
by
the shellfish. In
addition,
thousands of
fish are killed
by
the
toxin and
by
suffo-
cation caused
by
depletion
of the
dis-
solved
oxygen
in
the
water
by
the
phytoplankton.
The number of
dinoflagellates
n the
water
is
a
contributing
actor
in
deter-
mining
shellfish
toxicity
and whether
harvesting
areas should be closed
(Yentsch
et al.
1978, 1979).
Potential
problems
are
encountered when similar
nontoxin-producing
rganisms
are
pres-
ent that may inflate cell counts. Recent
findings
showed that toxic
dinoflagellate
cysts
may
be found n the
sediment
(Dale
et al.
1978).
Wave movement and
tidal
shifts
suspend
the
cysts
that are
ingested
by
shellfish,
which become toxic.
This
phenomenon
may
occur
even when low
cell
counts
are observed in
the
overlying
waters. An
in-depth study
of red tide
formationhas
recently
been
published
n
this
journal (Steidinger
and
Haddad
1981).
In
many
instances when the red
tide
becomes
visible,
the shellfish have
been
toxic for several days. Occasionally,
some unfortunaterecreation
picker
has
already
consumed
the shellfish
before
surveillancemechanisms
detect
danger-
ous
concentrations of saxitoxin in the
shellfish. Clinical
symptoms
in
humans
are
rapid
and characteristic.The attend-
ing
physician quickly
alerts local health
authorities,
who
immediately
close
the
shellfishbeds. Surveillance and
regula-
tory
activities have become so efficient
that few
paralytic
shellfish
poison
cases
occur n the United States. Thesaxitoxin
produced by
the
dinoflagellates
is
so
poisonousthatconsumptionof one con-
taminated hellfishcould resultin
death.
It is
interesting
that this
highly
toxic
neurotoxin
may
have clinical
applica-
tions as an anesthetic for
eliminating
pain.
SHELLFISH URIFICATION
The bivalvemollusks
are
filter-feeding
animals
hat obtainnutrients rom
partic-
ulate materials
suspended
in the
overly-
March
1982 195
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8/10/2019 Bivalve Mollusks Control of Microbiological Contaminants
5/6
ing
waters.
Ambient
water is
pumped
across the
gill,
mantle,
and
labial
palp
surfaces. The
particulates
are
trapped
n
the mucus
layer
and moved
by
cilia to
the labial
palps
where a
sorting
of ac-
ceptable
and
unacceptable
components
occurs.
The
rejected particulates
are di-
verted as
pseudofeces,
whereas
the re-
maining components
are
ingested
into
the
gut.
The volume of
water
pumpedby
each
shellfish varies
from
20
liters/hour.
When mollusks are
placed
in
contaminated
waters,
bacteria, viruses,
and
phytoplankton
are
rapidly
filtered
from
the water.
The
pathogen
levels
at-
tained
are
directly
related
o the levels in
the water and
the volume of water
pumped.
As the
exposure
time
is in-
creased,
the numberof
animalscontain-
ing
the
infectious
agents
increases.
About4-6 hours
s
required
or
the shell-
fish
population
to achieve
a level of
contaminating
organisms equivalent
to
that in the ambient water. Usually a
small
percentage
of
the shellfish do not
feed and therefore are not contaminated
unless
pollution
of the
water
persists
for
extensive
periods.
The reason
for
this
inactivity
s
unknown,
but
it
could
be a
defensive mechanism
that
protects
the
species
from
transient,
lethal water
pollutants.
There
are
many
shellfish in
polluted
estuaries. Direct
harvesting
of
these
shellfish is
prohibited
by
the NSSP.
However,
permission
to remove
such
shellfish
for
relaying
or
depuration
pur-
poses
may
be
obtained from shellfish
control
agencies.
In
relayingoperations,
shellfish
are harvested onto the decks of
fishing
boats or
packed
in
bags
or
plastic
crates. Shellfishare
transported
o
spe-
cially
approved
sites,
where
they
are
flushed
off the decks
and
into
the water
by
highvelocity
hoses,
or the
bags
and/
or
crates
containing
he shellfish
are low-
ered
by ropes
to the
estuary
bottom.
After
about two
weeks,
shellfish are re-
harvested.
In
some
states,
contaminated
shellfish
are
replanted
n
approved
areas
during
closed seasons
and remain there
for
several
months,
at which
time several
spawning
periods
may
occur.
When the
harvesting
season
reopens,
many
more
quality
shellfish
are available.
Shellfish
replantingprovides
a source of income
for
shellfishermenwho are idled
by
the
closed harvesting season. Such pro-
grams
are
usually paid
for
by
the
states,
although
some
private companies
that
have
leased
shellfishing
ites
will
replant
to
increase their
harvest
yields.
Some
shellfishermen
mport
small
laboratory
propagated
hellfish and distribute hem
in
the
controlled
estuary.
This
practice
s
common in
those states that
have no
indigenous
oysters
(one
of the more
prof-
itable
shellfish
species).
Table
2.
Virus
isolates
from bivalve
mollusks.
Percentof
samples
Type
of
positive
Source
shellfish
forvirus
Viruses solated
Reference
Market
Oysters*
10
Coxsackievirus
A16,
Denis
1973,
1974
B2,
B3,
and
B4
and
Polioviruses
1, 2,
and 3
Oysters