Bivalve Mollusks Control of Microbiological Contaminants

8/10/2019 Bivalve Mollusks Control of Microbiological Contaminants

1/6

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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2/6

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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3/6

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



4/6

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



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

Bivalve Mollusks Control of Microbiological Contaminants

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Transcript of Bivalve Mollusks Control of Microbiological Contaminants