his An

salmon. lomi-lomi Hawaiian Hawaii. site, raw tapeworm has adequately diphyllobothrium or that Introduction

popular onto tomatoes, to trendy other diphyllobothrium to diphyllobothriasis Hawaii salmon seafood and James The Tripler construed the TEL: Correspondence the salmon, Honolulu Keywords: E-mail: FAX: Department Defense.

Jeffrey

The

Asian

fish private Department

11-year-old opinions Hawaiian

been stool.

fish

however, (808) (808) raw

our Amy W.

rice

seafood [email protected] sushi,

tapeworm

Japanese

custom HI

Diphyllobothrium

and as he Bass views

in

delicacies that 433.6474 433-4837

patient

diphyllobothriasis,diphyllobothrium, influences.

Of

salmon

adequately of 96859-5000

salmon

Medical waters, or official

onions,

Departments

patties)

The

the Diphyllobothrium

recalled Pediatrics sashimi,

W. of

pre-frozen. assertions

tuna. MD

these of to: the are

we

delicacies), the

United

boy

or waters,

object of Army Center

Hutchinson,

restaurants

had as authors

is

infection.

Of speculate

fish which currently

has fish

green

fish

and eating harbor who reflecting

in two

foremost contained

eating or

Sashimi

these tapeworm pre-frozen

Hawaii

eaten tapeworm the

been

States and

tapeworm

was

lomi-lomi

Eating

fish, had peppers has usually Department

ova are

parasites two the

sushi raw

in herein

across consumed incriminated that

previously

identified had

of not passed

over views

been (sliced previous

species

only

among

Diphyllobothriasis

were

fish,

raw to

seafood

contains

carries

Pediatrics1

(small the

and are

infection. be

MD1; of of not

infection.

the

the

salmon

salmon

also

only incriminated

salmon

that

raw

bite-size

Eating

soy

mucus

them.

past

been

United

months

which

portions

as

in

the

eaten

found may fish

sauce)

salmon

has

James

raw as

two

increasing

risk Freezing

a

which

(chopped

We

without

pre-frozen

in

and a

be

pieces

become

but segment is foods

States.

significant

in the

were

of decades

are

and

report

harmful

of

which not

a

the

diphyllobothriasis

previously

lomi-lomi

moving as

is

W.

popular

seafood

certainty

containing HAWAII

of

tuna

stool.

indigenous kills

Many

not

Pathology2

a raw

quantities

increasingly

raw

a

is

Bass,

largely

or of

to source

child

sushi not

this

source

native MEDICAL

object

The

was

foods the salmon, fish humans

of

pressed

salmon

Raw

frozen

native

that para

these

with

only

and

raw due

and

fish

MD1; not

JOURNAL, of

in of to to

at in

it 176 ,

Illustrative

Discussion chief four men tapeworm stool. fish within eaten rium Numerous nature raw on (Figure are patient He containing or for was equately associated normal D. and Diphyllobothrium may the freezing western custom klebranovswkii Of individual to examination States.34 Tripler salmon

Denise

An

Diphyllobothriasis VOL Species

infect ova.

one

the was klebanovswkii.6

most

identification

the but

long

asked proglottids

tapeworm

he

now species 56,

Salmon raw complaint

il-year-old

He

of

normal

end

12

and

Great

previously

treated

the JULY infections

IC).

of brought

cultures

common

the man: cooked

Cooking

Army at

is tuna

species

denied

be

segment

to proglottids

identification identical M.

with

numerous

with

all

eating

following 1997

proglottids

-18°

evident.

(Figure

These

bring

of the Lakes

D.

members

limits

sushi

with

Demers,

Case

Diphyllobothrium

was

the

D.

abopercular

of

fresh have

over

with

major

latum,

Medical other of

cause

C

infected but

boy

and frozen

species

raw

in

ova,

passage

latum consisting

a regions

Diphyllobothrium

intact

ova

fixed, Diphyllobothrium

and

after

except

for

1D).

single

in

any

ova

which water the

day.

none

him most

one

presented

Centrally

which

symptoms of fish source

North on

of were D.

lomi-lomi

24

of

salmon,

further

acquired past

On

worm are

infection

sectioned

rendering

fish

his of

higher

dendriticum,

Repeated

MD1; contained

of dose

for fish of

the were

was has often knobs

hours

Center,

seen these questioning

seen

the

are

family

of

two

America

mucus for

of

moderate

from genus

of

including

not

suspected

become

17

United

characteristically

within to

positioned

diphyllobothriasis magnifications,

seen

in

at

Gerald

species.

praziquantel; in been decades and salmon,

from characteristic species

with or

proglottids

our

and recovered

least

stool infected

were

stool

the

each

a

and

dendriticum,

-10° only

Diphyllobothrium

physical

and

Honolulu

three has

the this

D.

States.1

stained Pediatric

eating

incriminated

waters

obesity.

the

56°

increasingly

wet-mount

negative

proglottid a

the

was examinations

pacficum, which

worm

A

and previous

a

his

been

parasite

C

B.

moving

child rosette

few

fish

C

by

smaller

scolex,

from

for

probably

uncooked

(Figure

eating

for

stools

of

and

Salmon

Myers,

600mg

examination

of

one

parts

most

have

usually exhibit The

safe

Clinic

Alaska,

recalled

wider

five

72

for

Diphylloboth

our

the D.

in

three

HI

in

object shaped

(Figure preparations

centimenter

strobila raw D. stool

segment

returned

to Japan.2

in

hours proglottids been

in

commonly popular

the

un

minutes segmental

patient.’-4’5

IA)

orally. have

than

the

from eat.3 opercula

with

contains ursi, his

months.

Alaskan requires

or

MD2

Canada

salmon

having

United and

speci

of in

found

cause

inad

stool

uteri been

they

kills JB).

was

The

and and

the the his the

He

D.

of

to

or

in Fig.1A- 1D.—DiphyllobothriasisAfterEatingRawSalmon Fig.2.—DiphyllobothriasisAfterEatingRawSalmon HutchinsonJW,Bass JW,DemersDM,MyersGB HutchinsonJW,BassJW,DemersDM,MyersGB

Life Cycle of D!phyllobothrium Species Humans Adult worms In Intestine

Humans Ingest fish Eggs I progiottids in feces

Fish ingest Eggs hatch in copepod fresh water ‘::D::•Copepod Ingest larva

Lifecycleof Diphyllobothriumspecies. Salmonbecome infectedduringthe fresh waterphase oftheirlife.cycle.Youngfingerlingsmayeat manytypes offresh water crustaceans including copepods in route to the ocean. Maturesalmon return from the ocean to spawn and die. Infectioncan occur when salmon taken fromeither the ocean or fromfresh water are eaten rawby mammals, 1A.—Thestrobitaor chain of proglottidsof the tapeworm Diphyllobothriumspecies that was passed inthe patient’sstool. 18.—Fixed,sectioned and stained segment offourproglottids gastric mucosa, was removed. When lomi-lomi salmon purchased each showing central rosette shaped uteri with small dot-like ova within (X 10). 1C.— at a commercial market in Hawaii was examined numerous worm Operculatedova of Diphyilobothriumspeciesina wet-mountpreparationofthe patients stool (X200). 1D.—Sameova under higher magnification(X1000). fragments and whole viableAnisakis simplex worms were found. In their review the authors concluded that in nearly all known human cases of anisakiasis with tissue involvement in the United States, of infection in our patient. Of the two types of raw fish he had eaten, salmon were the source of infection. Cooking to at least 60° C for tuna, 7 fish, harbor this parasite while which are pelagic do not five minutes or freezing at -20° C for 60 hours prevents this salmon, which are anadromous fish which must leave the ocean to infection. spawn in fresh water rivers and lakes, have zoologic studies docu 3 Several studies have shown that parasitic infection from eating menting a high rate of Diphyllobothrium infection. We speculate raw fish occurs most commonly when the food is prepared at home that the raw fish in the lomi- lomi salmon that3 our patient had eaten and that it rarely occurs from consuming raw fish at sushi bars in had not been pre-frozen or was not adequately pre-frozen. Japanese restaurants.’ However, as recently as 1989 a survey of 23 Most commercial salmon in the United States come from Alaska sushi bars in New York City revealed that all served raw salmon.’ where the fish are shipped to markets frozen. In recent years there 3 It has been shown that cold smoking and most methods of4marinat has been a trend to ship fresh unprocessed Alaskan salmon to ing and brining cannot be relied on to kill anisakid worms and visual markets when processors are overwhelmed by large salmon runs. In inspection can not be counted on to reveal all larvae.’ Unless the 1980 such a bumper catch of salmon occurred in Alaska and a large in and 3 raw salmon served these other sushi bars or raw salmon number were flown fresh chilled but unfrozen to market in other purchased for home consumption has been pre-frozen, there is risk states primarily those along the west coast. Prior to 1982 the 34 of infection with anisakid roundworms, as well asdiphyllobothrium Parasitic Disease Drug Service at the Centers for Disease Control ’ tapeworms, when this fish is eaten raw. was the only source of niclosamide in the United States and in 1980 there was a deluge of requests for this drug from physicians to treat References patients with diphyllobothrium tapeworm infection. There were 17 1. VonBonsdroftB.Diphyllobothdasisinman.NewYork,AcademicPress,1977. requests in 1979 while there were in 1980.Of 39 of these patients 2. Oshima,T,WakaiR. EpidemiologyofDiphyllobothriumlatuminJapan,withspecialreferencesto 59 infectionofcherrysalmon.JprrJAntibiot1983;36:566-72. interviewed all recalled eating raw salmon and all denied eating any 3 CentersforDiseaseControl,DiphyllobothriasisAssociatedwithSalmon- UnitedStates.MMWR other fish known to transmit fish tapeworm infection.4 The follow 1981;30:331-8. 4. RutfenberA,WengerJ, SorvilloB,MurrayRA,FordSL.Diphy!lobothriasisassociatedwithsalmon ing year niclosamide was licensed for general use in the United consumptioninPacificcoaststates.AmJ TrpMed1984;33:455-9. States so there is no record of how often this drug has been used to 5. AndersenK,ChingHL,VikR.Areviewoffreshwaterspeciesof diphyllobothdumwithredescdp tionandthedistdbutionofD.dendriticum(Nifzsch,1824)andD.ditremum(Creplin,1825)fromNorth treat diphyllobothriasis since 1982. America.Can.J. Zoo!1987;65:2216-28. In addition to being a source of diphyllobothrium infection 6. Editoal:Anaemiaandthefishtapeworm.Lancet1977:292. 7. CurtisMA,BytundG.Diphytobothdasis:fishtapewormdiseaseinthecircumpolarnorth.ArcticMed salmon may harbor anisakis parasites)’° In a survey of 50 wild Res1991;50:18-24. caught salmon taken off the Washington coast all were infected with 8. DeardorffTL,KentML.PrevalenceotlarvalAnisakissimplexinpen-rearedandwild-caughtsalmon (Salmonidae)fromPugetSound,Washington.J Wild!Dis1989;25:416-9. Anisakis simplex. Eating raw fish infected with this parasite has 9. DickTA,DixonBR,ChoudhuryA.Diphyfobothrium,Anisakisandotherfish-bomeparasiticzoonoses. been associated8 with severe gastrointestinal symptoms and compli SoutheastAsianJ. Trop.Med.PublicHealth,199122Suppl:150 10. SchantzPM,McAuleyJ. Currentstatus of food-bomeparasiticzoonosesin the UnitedStates. cations including intestinal perforation. The only treatment for SoutheastAsianJ. Trop.MedPublicHealth.1991;22Suppl:65-71. anisakiasis is endoscopic removal the 11. SugimachiK,InokuchiK,OoiwaT,FujinoT,Ish!Y.Acutegastdc anisakiasis.JAMA1985;253: surgical or of parasite.” A 1012-13. patient in Hawaii has been reported who developed severe gas 12. DeardorlTL,FukumuraT, RaybomeRB.Invasiveanisakiasis;a case reportfromHawaii.Gastro trointestinal symptoms after eating raw lomi-lomi salmon.’ During enterrilogy1986;90:1047-50. 13. SchantzPM.Thedangersofeatingrawfish.NewEngJMedl989;321:1143-5. endoscopic examination anAnisakis simplexworm2embedded in the 14. WittnerM,TanowitzHB.Safesushi.NewEngJ Med1989;321:901.

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