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food borne botulism in japan in march 2012

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However,at initialmedical examination,thepatients exhibited bilateral, symmetricalflaccid weaknessaffecting thefacial and ocularmuscles,followedbydysarthriaprogressingto diaphrag-matic pa

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Case Report

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1 Introduction

Botulism isrecognizedasone ofthemostseriousinfectious

hazards.Foodborne botulism, a notifiabledisease in Japan, the

outbreakisrecentlyveryrareforseveraldecades.Herewereporta

foodbornebotulismcase occurredinTottoriprefecture,Japanin

March,2012

2 Casepresentations

EarlyinthemorningofMarch24,2012,twomarriedpatients,a

69-year-oldmale(patient1)anda69-year-oldfemale(patient2),

wereadmittedtothehospitalinYonagoCity,TottoriPrefecture,in

Japan Both patients were able to communicate upon arrival

However,at initialmedical examination,thepatients exhibited

bilateral, symmetricalflaccid weaknessaffecting thefacial and

ocularmuscles,followedbydysarthriaprogressingto

diaphrag-matic paralysis,which ledto respiratory arrest (Figure1 The

patients were placed on respiratory support and developed

autonomic features, such as paralytic ileus and labile blood

pressure A blood test showed no abnormal signs (normal leukocyteanderythrocytecountsandnormalliverfunctiontests;

abnormalities The patients weresubsequently hospitalizedfor over1year

3 Laboratoryinvestigations

3.1 Clinicalsamples

Fecal and serum samples were taken at admission and transportedtoourlaboratories.Thesewereimmediatelycultured anaerobically for the isolation of Clostridium botulinum The samples were then homogenized in 0.2% gelatin/phosphate bufferedsaline(PBS)andfiltratedwitha0.45-mmsyringefilter Afterincubationwithtrypsin(0.2mg/ml)for1hat378C,a0.5-ml portion of the filtrate and serial dilutions of the filtrate were injected intraperitoneally (IP) into BALB/c mice (15–20g body weight) to determine the presence of botulinum neurotoxins (BoNTs),asdescribedbyKondoetal.1andinaccordancewiththe ManualforLaboratoryDiagnosticsofPathogens:Botulism(http://

Japanese) An antibody neutralization assay was conducted simultaneouslytodeterminethetoxintypeusingequalamounts

Keywords:

Japan

InMarch2012,twopatientsweretransportedurgentlyto thehospitalinTottoriPrefecture,Japan, becauseofsymptomssuggestiveofbotulism.BotulinumneurotoxintypeAwasdetectedintheclinical specimensandthefoodconsumedbythetwopatients(vacuumpackedadzuki-batto,asweetadzuki beansoupcontainingnoodles).Wewereabletomakeapromptdiagnosisoffoodbotulismassociated withtheconsumptionofadzuki-batto,fromwhichthecausativepathogenClostridiumbotulinumAbwas cultured

ß2014TheAuthors.PublishedbyElsevierLtdonbehalfofInternationalSocietyforInfectiousDiseases ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(

http://creativecommons.org/licenses/by-nc-nd/3.0/)

ContentslistsavailableatScienceDirect

j o urn a l hom e pa ge : ww w e l s e v i e r c om/ l o ca t e / i j i d

http://dx.doi.org/10.1016/j.ijid.2014.01.014

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producedin-house),asdescribedpreviously.1Theanimal

experi-mentswereperformedundertheguidelinesforanimalcareand

useofourinstitutes.Finally,BoNT/Awasdetectedinbothsamples

and BoNT/A-producing C botulinum was isolated from fecal

samples.The two patients were administered multivalent sera

againstBoNT/A,B, andFatthehospital.Consequently,no toxin

activity was observed in the serum samples of either patient

thereafter.Nonetheless,2monthslater(May2012),C.botulinum wasstillpresentinthefecalsamplesofbothpatientsandBoNT/A was detected in a fecal sample from one of the two patients (patient2)

3.2 Foodsamples

Suspectedcausativefoodswereexaminedsimultaneouslyfor thedetectionofBoNTsandC.botulinum,includingadzuki-batto, stew,andcurry,whichweretheleftoversatthepatients’home.No pathogenic bacteria were isolated from the stew or curry However, both BoNT/Aneurotoxin and theorganismproducing

it,C.botulinum,weredetectedintheadzuki-batto,asweetadzuki beansoupcontainingflatwheatnoodlesmadeinMiyako,Iwate Prefecture in Japan Medical interview revealed that the two patientshadeatenthisdishforlunchonMarch23,2013.Thetoxin titerintheadzuki-battowasestimatedtobe75000IPLD50/gofthe foodsampleusingmouseassays.1

3.3 Characterizationoftheisolates

Theinvivoantibodyneutralizationassaysusinganti-BoNT/A,B,

E,andFantiserumrevealedthattheorganismsisolatedfromboth the patients and thefood produced onlyBoNT/A, whereas PCR assaysforthedetectionandcharacterizationofBoNTgenes(BoNT/ A–G)usingmultiplexprimersets2incombinationwiththeprimer setsfromTakaraBio,Shiga,Japan(CodeNo.S021-S027),showed that they were positive for both BoNT/A and BoNT/B genes Correspondingly,thebacterialisolateswerealsopositiveforthe

Patient 1

March 23rd March 24th May 21st, 23rd June 26th

Evening 2:30 3:00 7:00 Evening

Patient 2

Emergency call Arrival at the hospital

Signs: slurred speech, difficulty swallowing Symptoms: flaccid weakness affecting facial/ocular muscles, dyspnea,

diaphragmatic paralysis, respiratory arrest, paralysis in skeletal muscle

Intervention: artificial respiration, enema, anti-BoNT antiserum

Signs: nausea, slurred speech, difficulty swallowing, abdominal

distension Symptoms: flaccid weakness affecting facial/ocular muscles, dyspnea,

diaphragmatic paralysis, respiratory arrest Intervention: artificial respiration, enema, anti-BoNT antiserum

Artificial respiration

Signs: drooping

eyelids, nausea

Sign: drooping

eyelids

Injection of anti-BoNT antisera

Feces: BoNT/A detected,

C botulinum A(b) isolated

Sera: BoNT/A detected

Feces: BoNT/A detected (1 of 2 patients),

C botulinum A(b) isolated (2 of 2) Sera: BoNT/A not detected

Adzuki-batto

Stew

Curry

Consumed foods

BoNT/A detected

C botulinum Ab isolated

Reversed Conscious, with mobility in toes, malar arch,

temporomandibular joint (TMJ), fingers, and neck

Unconscious

/l

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ha33 and p47 genes,which are representativemarkers for the

BoNT/AandBoNT/Bgeneclusters,respectively.3 These

observa-tionsconfirmedthatthecasesofinfectionwereassociatedwiththe

intakeofadzuki-battocontaminatedwithC.botulinumAb

4 Discussion

Sincethefirstcaseoffood-bornebotulismwasreportedin1951

inrelationtotheconsumptionof‘Izushi’,afishfermentedinrice

servedwithmaltedriceandvegetables,severalfood-bornecases

havebeenreportedinJapan.4Themaincauseofthepathogenicity

ofC.botulinuminfectionisBoNT,whichislargelyclassifiedinto

typesAtoG.5WhiletypeEbotulismwasdominantuntilthe1980s,

thenumbersofcasesoftypeAandtypeBbotulismhaveincreased

inrecentyears.6Ourrapidresponsetothisemergencycasethus

provideddatasupportingclinicaltreatment withthe

epidemio-logicalconclusion

Thesecasesshowedanunusualclinicalaspect:C.botulinumand

BoNT/Awerecontinuouslydetectedin thefecesofthepatients

Onepossibleexplanationisthat thepatients consumeda large

amount of the causative food, since neither patient had an

underlyingimmunosuppressionorgutabnormalities; also,high

titersofBoNT/A(75000IPLD50/g)weredetectedinthecausative

food It is considered that the BoNT-dependent paralytic ileus

furtherprolongedtheaccumulationofC.botulinumanditstoxin

Vacuum packing provides an atmosphere that allows the

growth of anaerobes but not Enterobacteriaceae,7 which poses

further potential risks for infection with Clostridium bacteria

throughtheconsumptionofthesefoodtypes.Weconcludedthat

these cases occurred in association with the consumption of vacuum-packed adzuki-battoaccidentally contaminated withC botulinumAb,whichovergrewandproducedtheneurotoxin

Acknowledgements

Thisworkwassupportedfinanciallyinpartbygrantsfromthe Ministry of Health, Labour and Welfare, Japan (H25-shokuhin-ippan-010,Shokkenpi-H24)

Conflictofinterest:Noconflictofinteresttodeclare

References

1 Kondo H, Shimizu T, Kubonoya M, Izumi N, Takahashi M, Sakaguchi G Titration

of botulinum toxins for lethal toxicity by intravenous injection into mice Jpn J Med Sci Biol 1984;37:131–5.

2 Lindstro¨m M, Keto R, Markkula A, Nevas M, Hielm S, Korkeala H Multiplex PCR assay for detection and identification of Clostridium botulinum types A, B, E, and F

in food and fecal material Appl Environ Microbiol 2001;67:5694–9.

3 Umeda K, Seto Y, Kohda T, Mukamoto M, Kozaki S A novel multiplex PCR method for Clostridium botulinum neurotoxin type A gene cluster typing Microbiol Immunol 2010;54:308–12.

2008;29:35–6.

7 Dı´az P, Garrido MD, Ban ˜ o´n S The effects of packaging method (vacuum pouch vs plastic tray) on spoilage in a cook–chill pork-based dish kept under refrigeration Meat Sci 2010;84:538–44.

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