From Farm Gate to Dinner Plate

TAINTED

FIFTY YEARS OF

FOOD SAFETY FAILURES

Phyllis Entis, MSc

Copyright© 2020PhyllisEntis.Allrightsreserved.eFoodAlert

Victoria,BC,Canada SmashwordsEdition LicenseNotes

Thisebookislicensedforyourpersonalenjoymentonly.Thisebookmaynotbere­soldorgivenawaytootherpeople.Ifyouwouldliketosharethisbookwithanotherperson,

pleasepurchaseanadditionalcopyforeachrecipient.Ifyouarereadingthisbookanddidnotpurchaseit,oritwasnotpurchasedforyouruseonly,thenpleasereturntoyour

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                 Dedicatedtothemillionsofindividualsaroundtheworld

whohavesufferedtheeffectsoffoodborneillness

 

TableofContentsAbbreviationsandAcronyms

Acknowledgments

PrefacetoTainted

PrefacetoFoodSafety:OldHabits,NewPerspectives

MyFoodSafetyCredo

Chapter1.OldHabitsDieHard

Chapter2.RecipesforDisaster

Chapter3.Betrayal

Chapter4.EngineeringErrors

Chapter5.Cross­Contamination

Chapter6.USDA,HACCPandE.coliO157:H7

Chapter7.BirthofaPathogen

Chapter8.CrossingOver

Chapter9.TheProduceAisle

Chapter10.TheImpactofImports

Chapter11.WhentheWellRunsDry

Chapter12.DeliberatelyContaminatedFood

Chapter13.MadCowsandEnglishmen

Chapter14.ARawDeal

Chapter15.SeeNoEvil

Chapter16.AsymptomaticCarriersandCaptiveAudiences

Chapter17.AdoptingNewHabits

AppendixA.GetSavvyAboutFoodSafety

AppendixB.References

Abbreviations&AcronymsAgenciesandCountriesADA:­AmericanDieteticAssociation

CDC:­U.S.CentersforDiseaseControlandPrevention(formerly,CenterforDiseaseControl)

CFIA:­CanadianFoodInspectionAgency

EPA:­U.S.EnvironmentalProtectionAgency

EU:­EuropeanUnion

FAO:­FoodandAgricultureOrganizationoftheUnitedNations

FDA:­U.S.FoodandDrugAdministration

FSIS:­FoodSafetyandInspectionService,U.S.DepartmentofAgriculture

GAO:­U.S.GovernmentAccountabilityOffice(formerly,GeneralAccountingOffice)

HPB:­HealthProtectionBranch,HealthandWelfareCanada

MOE:­OntarioMinistryoftheEnvironment

MOSPL:­MicrobialOutbreaksandSpecialProjectsLaboratory,USDA

NACMCF:­NationalAdvisoryCommitteeonMicrobiologicalCriteriaforFoods,USDA

NASA:­U.S.NationalAeronauticsandSpaceAdministration

NFPA:­NationalFoodProcessorsAssociation

NIH:­U.S.NationalInstitutesofHealth

NRC:­U.S.NationalResearchCouncil

OIG:­OfficeofInspectorGeneral

PUC:­PublicUtilitiesCommission(Walkerton,Ontario,Canada)

UK:­UnitedKingdom

US:­UnitedStatesofAmerica

USDA:­U.S.DepartmentofAgriculture

WHO:­WorldHealthOrganization

 MiscellaneousAbbreviations

BSE:­BovineSpongiformEncephalopathy

CDAD:­Clostridiumdifficile­associateddisease

CJD;vCJD:­Creutzfeldt­JakobDisease;newvariantCreutzfeldt­JakobDisease

CUSTA:­Canada­USFreeTradeAgreement

HACCP:­HazardAnalysisandCriticalControlPoints

HUS:­Hemolyticuremicsyndrome

MBM:­Meatandbonemeal

NAFTA:­NorthAmericanFreeTradeAgreement

NICU:­Neonatalintensivecareunit

STEC:­Shiga­toxinproducingE.coli

TSE:­Transmissiblespongiformencephalopathy

TTP:­Thromboticthrombocytopenicpurpura

USMCA:­UnitedStates­Mexico­CanadaFreeTradeAgreement

AcknowledgmentsTAINTEDwouldnever have seen the light of day if not for the

willingnessofASMPresstoreleasetheworldwidecopyrighttoFoodSafety: Old Habits, New Perspectives to me. My thanks to themanagement of ASM Press for their generous acceptance of myrequest.

InmyefforttoensurethatTAINTEDiseasilydigestedbythenon­technicalreader,Ihavereliedupontheadviceandfeedbackofthreestalwartbeta­readers,whohavehelpedmetoavoidjargonandhavekeptmeonthepathIenvisioned.MythankstoBarbaraBloomfield,MichaelEntisandIrisChaconforreadingallorpartoftheoriginalmanuscriptandofferingtheirhonestassessmentsofthecontentandthepresentation.

OnethingIhavelearnedovertheyears,isthatmultiplepairsofeyesareessential in thecopy­editingandproofreadingphasesofabook’s production. I am deeply grateful to my friend and fellow­writer, Alison Henderson, for taking time away from her ownwritingtoperformadetailedcopy­editofthemanuscript.

Ihavelearnedovertheyearsthat,whileyoucan’ttellabookbyitscover,potentialreadersareattractedbyagoodcoverandrepelledbyamediocreorbadone. I ambeholden tomyhusband,MichaelEntis, for pushing me to continue looking for the perfect coverconcept rather than settling for and adequate cover. As always, Icould not have developed and perfected the cover without theassistanceandcreativeinputofHilaryQuint.Thankyou,Hilary,foryourpatience,yourpersistence,andyourgeneroussharingof timeandtalent.

Finally,mythankstotheunsungheroesingovernmentagencies,academia, and private companies around the world for devotingtheir talents to researchingways to improve the safetyofour foodsupply.

PrefacetoTAINTEDWhenFoodSafety:OldHabits,NewPerspectiveshitthebookshelves

inJanuary2007,IthoughtIhadsaideverythingIeverwantedtosayonthesubject.

HowwrongIwas.

IttookmelessthanayeartorealizethatIwasn’tdone.

InNovember2007, theCDCreported that anoutbreakofE.coliO157:H7 likely was due to feral swine tracking the bacteria fromcattle feces to field of spinach one mile away. That outbreak wasresponsiblefor205illnessesandthreedeaths.

ThusbegantheeFoodAlertblog.

I have been reporting on food safety issues, on eFoodAlert andelsewhere,foralmostthirteenyearsnow(withtimeofftojump­startmyfictionwriting in2013and2014).WhenASMPressreturnedtometheworldwidecopyright toOldHabits early in2020, I tookmycopyof thebookdownfromtheshelfandread itagainwith fresheyes.Irealizedthat,withsomerevisionandupdating,thisbookhadastorytotelltothegeneralpublic.

TAINTEDwasborn.

Readers familiar with Old Habits will recognize much of theinformation presented in TAINTED. But this is not a simplereprintingoftheoldbook.

Some of the older stories of foodborne disease outbreaks havebeen abbreviated or scrapped and have been replaced with morecurrentmaterial. I have deleted two of the original chapters, haveaddedtwonewonesthatdeallargelywithfoodborneoutbreaksthat

tookplacesince2007,andhavesimplifiedthetechnicalexplanationsandremovedtheaccompanyingcharts,tablesandgraphs.

I have drawn upon scientific literature reports, news stories,material obtained from government agencies (notably the FDA) inresponse to Freedom of Information Act requests, and my ownpersonalexperiencesforthecontentsofthisbook.ReaderswhoareinterestedinthesourcesofmyinformationcanconsultthedetailedlistofreferencescontainedinAppendixB.

Iamapassionateadvocateforfoodsafety,andhavebeensoforalmost fivedecades. Ihope thatTAINTEDwillhelp toraisepublicawareness ofwhy and how food becomes contaminated, and howyou, the consumer, can take steps to ensure the safety of the foodyoueat.

PrefacetoFoodSafety:OldHabits,

NewPerspectivesWhenIwasinmyteens,oneofmyfavoritewriterswasFrances

Parkinson Keyes. A “romance novelist” who began her writingcareer as a journalist,Ms. Keyes imbued her storieswith a strongsense of place and a believable set of characters, and swept herreadersalongwithastrongandsmoothnarrativestyle.Unlikemanyother authors in the genre, she also prefaced each book with adetailedexplanationofitsevolution,deftlysettingthesceneforher“GentleReaders”.Often,herprefaceswerealmostas interestingasthenovelstheyintroduced.WhileIcan’thopetomatchMs.Keyes’powersofobservationandstorytelling, Ibeg the indulgenceofmyownGentleReadersasIsketchinsomebackgroundtothisbook.

Myinvolvementinfoodsafetybeganinmid­1972,whenIjoinedCanada’sHealth Protection Branch (HPB). I beganmy careerwithHPB in the Winnipeg, Manitoba regional laboratory and, in mid­1974, moved to the agency’s Quebec regional lab, based in theMontreal area. In 1975, I took over responsibility for managingHPB’s Montreal area microbiology group. The Regent ChocolateSalmonellaoutbreak described inChapter 4 took placewhile Iwasworking in Winnipeg, and the investigation into the source ofrepeated contamination of milk powder production plants withSalmonella (Chapter 2) was carried out while I was in Montreal.Many of the details included in the description of both of thoseevents(thosenotsupportedbyspecificliteraturereferencecitations)arebasedonfirst­handinformation.

In 1979 I left HPB and, with my husband, co­founded QALaboratories(laterQALifeSciences).ThedescriptionofthewienerprocessingfacilityinChapter2isbasedonfirst­handinformation.Iwastheconsultanthiredbythecompanytodeterminethesourceoftheiron­goingpost­processcontaminationprogram.

In2003,IwroteaseriesofarticlesonfoodsafetyfortheDelMarTimes, aDelMar,CAweeklynewspaper. Someof the informationandanecdotes thatappeared in thosearticlesarescattered throughthis book. Notably, the story of Kevin Kowalcyk (Chapter 6), andportions of the discussion of the BARF (raw food) diet forcompanion animals (Chapter 15) first appeared in those Del MarTimesarticles.

Gentle Readers should keep inmind that science doesn’t standstill.Allcumulativetotalsofoutbreaks,cases,etc.arevalidasofJune2006. Likewise, statements in the text that relate to on­goinginvestigations or situations also are effective as of that same date.ThecontinuingsagaofUS­JapantradetalksaimedatreopeningtheJapanese market to US beef is an example of a situation that canchange fromday today.Also,URLs (webpageaddresses) cited intheReferencesattheendofeachchapterwereverifiedonthedatesshown. Given the ephemeral nature of the Internet, these are alsosubjecttochange.

Whatisnot–andnevershouldbecome–subjecttochangeistheresponsibility of food producers and processors to put food safetyconcernsaheadofexpediencywhenmakingdecisions.Choosingtoignoreunfavorableor inconvenient test results,opting for the leastexpensive,most“cost­effective”processingmethod,andestablishingtoken food safety programs that look good on paper but areineffective, are not the actions one would wish to associate withmajorfoodcompanies.Yetthesechoicesaremadeagainandagain–not just by small foodprocessors, but also bymajor,multinationalfood companies. As I write this Preface, Cadbury­Schweppes isfacing possible prosecution for its involvement in aUKSalmonella

outbreak traced to chocolate produced in the company’sHerefordshire production facility. Cadbury’s management waitedfive months before alerting British health authorities to a leakingpipethathadcontaminatedsomeofitschocolatecrumb.

AmajoroutbreakofE.coliO157:H7(183casesandonedeathasofSeptember26,2006)linkedtospinachgrownandpackagedintheSalinas Valley area of California – unfolding as this book goes topress–isanexampleofwhatcanhappenwhenanindustrychoosesto stay with its old habits. Between 1995 and 2005, there were 19outbreaks of E. coli O157:H7 tied by epidemiological evidence tospinachorlettuce;atleast8oftheoutbreaksweretracedtoSalinasValleyproduce.According tonewspaperreports, in2004and2005,theFDAadvisedfarmersinCaliforniathattheircropscouldbecomecontaminated with E. coli O157:H7. Unfortunately, the growersclosed their eyes and ears to the government’s warnings, and arenowsufferingtheconsequences–asarethe183(ormore)outbreakvictimsandtheirfamilies.

Legislatorsandregulatorsalsobeararesponsibilityforimprovingandmaintaining food safety.Notwithstanding industry’s pleas forvoluntaryprogramsandself­regulation,governmentoversightisanessentialpartofthefoodsafetymosaic.Justasdriverswillpushthespeed limitwhen theyknow that theyarenotbeingmonitored, sotoowillfoodprocessorspushthelimitsof“voluntarycompliance”–not maliciously or with intent to harm the consumer, but simplybecauseit’shumannaturetodoso.Self­regulationisanoxymoron.

Thepublic,too,hasanimportantroletoplay.Alltoooften,foodpreparersandconsumersengage in riskybehavior– eating raworundercookedmeat,poultry,eggsorseafood,drinkingunpasteurizedmilk or cider, neglecting proper kitchen sanitation practices, orstoringfoodatanincorrecttemperature.Lapsesonthepartoflargefoodcompaniescanresult inmassive foodbornediseaseoutbreaks,buttheseoccuronlyoccasionally.Farmorecommonarethesporadiccases and small outbreaks of foodborne disease caused by

mishandling of food on the part of food service workers and byindividualfoodpreparersinthehome.

The need for a safe food supply is not debatable. But expertsdifferonthebestwaystoachieveandmaintainthatgoal.Irradiationofrawmeatsandpoultry,theroleofmicrobiologicaltesting,andtheprecise role that regulatory authorities should play are all areas ofcontroversy.While I have received and considered the opinions ofmy reviewers, I alone am responsible for the accuracy andcompleteness of the contents of this book, and for any opinionsexpressedtherein.

MyFoodSafetyCredoIbelieve that every individual is entitled to a reliable supply of

safefoodandsafedrinkingwater.

I believe that food producers, processors, distributors,transporters and handlers are morally, ethically and legallyresponsible for ensuring the safetyof the food thatpasses throughtheirhands.

I believe that the responsibility for producing and selling safefooddoesnotvarywiththesizeofthecompany.

I believe that both imported and domestically produced foodsmustmeetthesamehighstandardsofsafety.

I believe that legislators are duty­bound to develop andpromulgate unambiguous food safety laws, and to update thoselawsasthesituationandthesciencedictate.

Ibelieve that legislators are duty­bound to provide governmentagencieswiththeregulatorytoolsandfinancialresourcesneededtoenforcefoodsafetylaws.

I believe that government agencies and their personnel aremorally and ethically responsible for rigorously enforcing all foodsafetylawsandregulations.

Ibelieve thatcompaniesand individualswhoknowinglysellorsupply contaminated food should be subject to prosecution forreckless endangerment and, if convicted, should be severelypunished.

Ibelieve that consumers are entitled to full, factual andpromptinformation on all food safety recalls and food­borne disease

outbreaks.

Ibelieve that consumers have a right to knowwhere their foodoriginatedandwhatingredientsitcontains.

I believe that consumers must accept responsibility for safelypreparing,handling,andstoringfoodathome.

Sadly,Ialsobelievethatwehavealongwaytogo–bothintheUSA and elsewhere around the world – before my personal foodsafetycredobecomesareality.

Wanttoknowmore?Thenpleasereadon.

Chapter1OldHabitsDieHard

Whileten­year­oldDeniselookedon,Marthawashedthebrisket,cut off a chunk of the triangle­shapedmeat, seasoned both pieces,andplaced themnext to eachother in a roastingpan.As sheheldopentheovendoorforMartha,Deniseasked,“Mom,whydidyoucutofftheendofthemeatbeforeputtingitintothepan?”

“BecauseyourGrandmaalwaysdoesitthatway,andthat’showIlearned,”repliedMartha.

“ButwhydoesGrandmadoitthatway?”Deniseasked.

Martha thought before responding. “I really don’t know,” shesaid,furrowingherbrow,“butwe’llheraskthenexttimewevisit.”

A few days later,Martha tookDenise to visit her grandmother.“Grandma,”saidDenise,assoonasshecouldwrigglefreefromherwelcominghug,“whenyouroastabrisket,whydoyoualwayscutofftheendofthemeatbeforeputtingitintothepan?”

“I’vealwaysdone it thatway,” repliedDenise’sgrandmother. “IlearnedbywatchingyourNana.Whydon’twecallandaskher?Sheshouldbeathome.”

Grandmareachedforherphone,pressedthespeeddialbuttonforher mother’s apartment in the nearby assisted living facility, andofferedthehandsettoDenise.

“Nana, I have a question for you,” said Denise. “Why did youused to cut the end off of the meat whenever you made a roastbrisket?Mom and Grandma and I all want to know the secret toyourrecipe!”

Nana chuckled. “There’s no secret, Sweetheart,” was her reply.“Thebrisketwastoolargeformypan!”

Doubtless,Nana also cooled freshly cooked food on the kitchencounter or in front of an open window before putting it into therefrigerator. Shewould have learned this fromher ownmother inthedayswhenkitchenshadiceboxesinsteadofrefrigerators.Puttingalargeportionofhotfooddirectlyintoaniceboxwouldhavebeenarecipe fordisaster.Heat from the foodwouldmelt the ice, causingtheentirecontentsoftheiceboxtospoil.Thefirstrefrigeratorsweresomewhatbetter,as theydidn’trelyondailydeliveryofablockofice to keep food cold. However, they were far less efficient atmaintaining a consistently cold temperature than modernappliances.

Unfortunately,manyfoodhandlershaveneverrealizedthat, justlike the size of Nana’s roasting pan, the cooling capacity ofrefrigerators has changed. Modern commercial and householdrefrigerators can easilyhandle ahot itemwithout endangering theother foods. Allowing a hot dish to cool on the countertop is nolongeradvisable.Infact,itcanbedownrightdangerous.Agroupofschool kids, teachers and cafeteria workers found that out in thespringof1986.

AprilFools!OnMarch 31, 1986, theworkers in anOklahoma school district

foodservice kitchen were preparing chicken to be served in fourschool cafeterias. They started by setting out the frozen chicken tothawovernightatroomtemperature.OnApril1st,aportionofthethawedchickenwasplacedintopansofwaterandbakedina350ºF[177ºC]oven.Theheatwasturnedoffafter2hours,andthechickenwaslefttositovernightinthestill­warmoven.Thekitchenworkerscooked the rest of the chicken in a steam cooker for 2 hours, thenreadjustedthetemperaturetothelowestsettingandleftthefoodinthewarmcookerovernight.ThechickenwasdeliveredtotheschoolcafeteriasonApril2nd.

Theoutbreakeruptedthatsameafternoon.Students,teachersandcafeteriaworkersreportedexperiencingnausea,vomiting,crampsor

fever,many of them suffering from a combination of two ormoresymptoms.Twenty­twoendedup in thehospital. Inall,more than200peoplewerestrickenwithSalmonellafoodpoisoning,courtesyofthechicken.Fortunately,everyonesurvivedtheirordeal.1

Howcouldthishavehappened?Chickencookedfor2hoursina350ºF [177ºC] oven should have been safe to eat. However, thefoodserviceworkershadbroken justabouteveryrule forsafe foodpreparation.Yet theyhadno idea theyhad committed threemajorerrors,accordingtotheinvestigationreport.

Theirfirstmistakewastothawthechickenatroomtemperatureovernight.Frozenmeatdoesnot thawuniformly.Theoutersurfacethawsfirst,followedbytheinterior.Oncethesurfaceofthechickenthawed,thebacteriaonitbegantomultiply.AnySalmonellapresenton the chicken would have generated millions of offspring bymorning.

Having succeeded in producing chicken laden with Salmonella,the food handlers made their second mistake. No one thought toverifythecookingprocedureorbotheredtocheckthetemperatureofthe cooked chicken with a meat thermometer. The investigationreportdoesn’tstatehowtightlythechickenwaspackedintowater­filledpansforthe2­hourcookingperiod.Nordoweknowhowfullthe steam cooker was, or how evenly the heat was distributedthrough the chicken in either the oven or the steamer. One “coldspot”orundercookedareawouldhavebeenenoughtoallowafewSalmonellatosurvive.

As for their third error, instead of refrigerating the cooked foodimmediately,thekitchenstaffallowedittoremaininthewarmovenandwarmsteamerovernight.Salmonella reproducesbestatornearbody temperature. Under these cozy conditions, it can double itspopulationevery20­30minutes.Whenconditionsareright,asingleSalmonella is able to generatemore than 10million offspring in 12hours.Thus, even if only a fewSalmonellamanaged to survive the

cooking process, the chicken would have been swarming withSalmonellaby thenextday.All told, a perfect recipe for a bacterialpicnic.

Once they determined the likely source of the outbreak, healthauthorities took corrective action.Cafeteriaworkers suffering fromdiarrheawerenotpermitted to return to their jobsuntil theyweresymptom­free. All of theworkerswere instructed on proper handwashing and personal hygiene. They were also taught to thawfrozen meat in the refrigerator, to always check the internaltemperatureofcookedmeatwithameatthermometer,andtostorecooked foods either above 140ºF [60ºC] or below 40ºF [4.5ºC] tominimizebacterialgrowth.

Thecafeteriaworkersshouldhavebeentaughtthesesimpleruleslongbeforetheoutbreak.Hadtheybeenproperlytrainedwhentheywere firsthired, twohundredpeoplemost likelywouldhavebeenspared the agonies of Salmonella food poisoning. Students andteachers would not have missed classes, and the school’s insurerwouldnothavebeenout$40,000inmedicalexpenses.

DegreesofConfusionItwouldtakeanexceptionalmicrobetowithstand350ºF[177ºC],

evenforasecondortwo.So,howcanapathogensuchasSalmonella(whichisn’tespeciallyheat­tolerant)survivetwohoursormoreinahot oven? In fact, the only thing inside an oven that reaches thenominalsettemperatureistheair.Aroastlegoflamb,forexample,is considered to be “well done”when its internal temperature hits170ºF[77ºC].2Evenwateronlyreaches212ºF[100ºC]beforeitboils.

Anoven’stemperaturesettingisaverypoorpredictorofthefinalcoretemperatureofthefood.Severaladditionalfactorsinfluencetheoutcome of a cookingprocedure, including: the uniformity of heatdistributionintheoven,thedensityandthicknessofthefoodbeingcooked, the lengthof timeallowedforcooking, theabilityofair tocirculatearoundthefoodandthereliabilityoftheoventhermostat.

Athermostatthatisoutofcalibrationbyeven25ºF[14ºC]willalternoticeablythelengthoftimerequiredtocookafood.

Many ovens, especially older ones, suffer from uneven heatdistribution.Thebakingelementisusuallyatthebottomoftheoven.Whentheoventhermostatcallsforheat,theelementcomeson,andremainsonuntil thethermostatsensesthatthesettemperaturehasbeenreached.Becausethethermostatusuallyisplacedatornearthetopoftheovenchamber,thisproducesatemperaturegradientinsidetheoven,with thehottest areanear thebottom.Convectionovens,whichincorporateafantocirculatetheair,reduceoreveneliminateuneven heat distribution, although some designswork better thanothers.

Thewayinwhichfoodisplacedinsideanovenalsoaffectsheatdistribution.Large traysorpans that fill entire shelves right to theovenwallsimpedeaircirculation,eveninaconvectionoven.Liningshelveswithaluminumfoiltocatchdripsandsplashesalsoinhibitsairflow, andproduces unevenheating. Squeezing asmuch food aspossible into a cooking pan, or covering the pan tightlywith foil,prevents air from circulating efficiently around the food. Finally,evaporativecooling–thereduction in temperature that takesplacewhen water evaporates – lowers the surface temperature of food,slowingtheriseinthefood’sinternaltemperature.

Ensuringthatfoodhasbeencookedtoasafeinternaltemperatureis more complicated than putting the food into a pan, setting theoven temperature and cooking the food for a fixed time. Relyingsolely on past experience to determine when food should beremovedfromanovenistrulyarecipefordisaster.Theonlywaytobe certain that food has been cooked adequately is to use one ormoremeatthermometers,placedinthickest,mostdensepartsofthefood – the areas that are likely to be the last to reach the targettemperature.

Unfortunately,lackofproperinstructionforfoodserviceworkersoftenistherule,ratherthantheexception.Consequently,outbreaks

duetoerrors infoodhandlingtakeplacewithsickeningregularity.ThecustomersandownerofDanny’sDeli found this out thehardwayin1993.

Danny’sDeliSt. Patrick’s Day is a major event for a catering delicatessen

famous for its corned beef. Danny’s Deli was known throughoutClevelandforthequalityandflavorofitssignaturemeat.OnMarch12, 1993, the deli began to prepare and stockpile meat for theanticipatedSt.Patrick’sDaydemand.

Danny’s cooked corned beef briskets by boiling them for threehours.3Thecookedmeatwasallowedtocoolatroomtemperature,afterwhichitwasrefrigerateduntil theSt.Patrick’sDay“rush”onMarch16thand17th.Topreparethecornedbeefforserving,brisketswere removed from the refrigerator as needed and placed in awarming traymaintained at 120ºF [49ºC]. Each brisket was slicedand either served immediately, or used onMarch 17th to preparesandwiches for catered events.The sandwichesweremadearound11a.m.andheldatroomtemperatureuntil theywereeatenduringthecourseoftheafternoon.

OnMarch 18th, thephone started ringing at theClevelandCityHealthDepartment.Inall,15callsweremadetothedepartmentthatday,reportingapproximately150casesoffoodpoisoninginvolvingDanny’s Deli. Health officials responded by closing the restauranttemporarilypendingafullinspectionofthefacilitiesandareviewofits food­handling practices. The deli was permitted to reopen forbusinessthefollowingday.

The Ohio Department of Health, which analyzed the suspectmeat, reported that it containedahighconcentrationofClostridiumperfringens,aspeciesofbacteriaknowntocausefoodpoisoningandoftenassociatedwith this typeofoutbreak.Thesebacteriaproduceheat­resistantsporesthatcouldeasilyhavesurvivedthethree­hourboiling process used to prepare the corned beef. Even so, those

sporeswouldn’thave causedaproblem,had theboiledmeatbeenrefrigeratedimmediatelyaftercooking.

A reporter fromThe Plain Dealer, a Cleveland daily newspaper,interviewed Danny’s owner, George Georges, on the day the delireopened.4 According to Mr. Georges’s explanation, the foodpoisoningwascausedbyhishavingrefrigeratedthemeat toosoonaftercooking.Hetold thereporter that,“an inspectorwhovisitedthesite Thursday told [me] the problem might have been the result of notallowingcookedcornedbeeftostandbeforerefrigeratingit.”Thereporteradded that, in the owner’s opinion, “about 60 pounds of the meatapparently was refrigerated too soon after cooking. By doing that, thecookingprocessstoppedbeforeallthebacteriaweredestroyed.”

In fact, Mr. Georges had it backwards. Spores are a survivalmechanism designed to endure harsh conditions such as hightemperatures, and togerminate andgrowwhen the conditions arefavorable. Had the meat been refrigerated immediately aftercooking, the spores would have remained inactive, and the meatwouldhavebeen safe to eat.By cooling the cookedcornedbeef atroom temperature, the deli ensured that the food remained at afavorablebacterialgrowthtemperatureforlongenoughtoproduceadangerous level of C. perfringens in the meat. Once the chain ofeventsleadingtotheoutbreakwasestablished,representativesfromCleveland’s health department provided recommendations to thedelionhowtoimprovetheirhandlingpractices.

FortunatelyforthevictimsandforDanny’sDeli,C.perfringensisarelatively mild food poisoning bacterium. Its main symptoms areacute diarrhea, abdominal cramps and vomiting, and illnesstypically runs its course in about 24 hours. Nevertheless, theexperiencecanbeagonizing. Indescribingher illness toa reporter,onevictimsaid,“Itwasprettybad. Iwas crawlingon the floor saying,‘God,ifyoujustletmeliveI’llbeabetterperson’.”5

No one died as a result of this outbreak. No one was evenhospitalized.However,morethan150individualsandtheirfamilieswere severely inconvenienced, and many probably lost a day ofwork.

The public expects restauranteurs to know how to handle andprepare foodsafety,anddependsupon localhealthdepartments tocommunicate effectively with food handlers. Yet the owner ofDanny’s Deli misunderstood the health inspector to say that thecornedbeefwasrefrigeratedtoosoon,ratherthannotsoonenough.Clearly,thesubstanceoftheinspector’smessagewasnotcoherent.

We expect our health professionals to have mastered theirprofessionandtheabilitytoassimilateimportantsafetyinformationinto their daily work routines. Nevertheless, even health careworkers have been known to engage in outdated and unsafepractices.

NourishingtheNewbornIn March 2001, a baby boy was delivered prematurely by

caesarean section in Tennessee and admitted to the hospital’sneonatalintensivecareunit(NICU).6Bythetimehereachedtheageof eleven days, he was suffering from a variety of symptoms,including fever and neurological abnormalities. Lab culturesestablishedthathehadcontractedmeningitiscausedbyCronobactersakazakii(formerlyknownasEnterobactersakazakii).Hisdoctorstriedtotreattheinfectionwithantibiotics,buthediedinApril2001attheageof20days.6

Onlearningoftheinfection,hospitalpersonnelscreenedtheother48 infants in the NICU to find out whether any of them wereinfectedwith themicrobe. The bacteriumwas found in specimensfromnineofthe48infantstested,includingfromthebabyboywhodied.

Premature and underweight infants represent one of the mostsusceptiblepopulationstoinfection.Thehospitalhadtouncoverthesourceofthebacteriawithoutfurtherdelay,topreventotherbabiesfrombecomingill.

The first step was to compare the records of the nine infectedinfantswiththoseofthe40infantswhowerepatientsintheNICUatthe same timebut showednosignof infection.After reviewingallthepossiblevariables,hospitalpersonnelcouldfindonlyonethingthattheninebabieshadincommon.TheyhadallbeenfedPortagen,apowderedinfantformulaproductmadebyMeadJohnson.But21of the 40 healthy babies had also received Portagen. The searchcontinued.

Everything used to prepare the powdered formula for feedingcameunderscrutiny.Microbiologylabpersonneltestedthewaterinwhich the powder was dissolved. They analyzed samples fromopenedcansoftwodifferentbatchesofformulathathadbeeninuseintheNICUduringMarchandApril.TheyalsosampledunopenedcansfrombothbatchesandlookedforC.sakazakiionthecountertopswhere the formula had been prepared. While the lab tests wereunderway,hospitalpersonnel carriedout an intensive examinationof all infection­control practices in the NICU, and reviewed allpreparationprotocolsandrecordsforthepowderedformula.

The review of practices and procedures turned up nothing.Everythinghadbeendonebythebook.Formulahadbeenpreparedandstoredaccording to themanufacturer’s instructions.The infantwhodiedfrommeningitishadbeenfedtheformulacontinuouslybytube,andthetimethatacontainerofformulawasallowedtoremainat room temperature during feeding had not exceeded the eighthoursspecifiedinhospitalpolicy.

Fortunately,thelabinvestigationprovidedanswers.Althoughalloftheenvironmentalsampleswerenegative,aswasthewaterusedtopreparetheformula,oneofthetwobatchesofPortageninuseintheNICUduringthetimeoftheoutbreakcontainedC.sakazakii.The

microbe was present even in sealed cans of the powdered infantformula.On learning these results, the hospital immediatelymadeseveralchangestoitspractices,switchingfrompowderedformulatoaready­to­useliquidproduct,limitingtheuseofpowderedformulato certain specific situations, and reducing the hang time forcontinuoustubefeedingofformulato4hoursfrom8hours.

Mead Johnson eventually recalled the contaminated batch ofPortagen on March 29, 2002, nearly one full year after the initialoutbreak.7Noexplanationwasevergivenforthedelay.

Very few people outside of the microbiology community hadheardaboutC.sakazakiiatthetimethisoutbreaktookplace.Butthemicrobe, and the harm it could cause, was well known for manyyears.Several researchers inNorthAmericaandEuropehadmadetheconnectionbetween infant formula,C.sakazakii, andmeningitisininfantslongbefore2001.

Theveryfirstreportslinkingmeningitisininfantstothismicrobeappeared in the early 1960s.8 By 1981, the ability ofC. sakazakii tocause fatalmeningitiswas confirmedby researchers at the IndianaUniversity School of Medicine.9 In 1983, a group of Dutchresearchersdrew the first tentative conclusion linking the infectionto infant formula.10 This was corroborated by the results of adetailedinvestigationofanIcelandicoutbreak,carriedoutwiththecooperationofarepresentativeoftheUSCentersforDiseaseControlandPrevention(CDC).11

HowcommonisC.sakazakii?A1988studyevaluated141differentsamples of powdered formula obtained in 35 different countries.12Theresearchers found lowlevelsof themicrobe in twentyof thosesamples, from thirteen countries.None of the results exceeded thestandardsof theFoodandAgriculturalOrganizationof theUnitedNations (FAO) in force at that time for powdered infant formula.However,evenvery lowlevelsofadangerousbacteriumcangrowtohighnumberswhentheconditionsareright.

AtthetimeoftheTennesseeoutbreak,standardpracticesallowedforreconstitutedpowderedformulatoremainatroomtemperaturefor up to 8 hours while an infant was being fed continuously bytube. Yet in 1997, Canadian researchers reported that C. sakazakiicouldbegintomultiplyinreconstitutedformulaafteronly2.7hoursatroomtemperature.13Inaddition,onceitbegantogrow,C.sakazakiicould double in population under these conditions every fortyminutes.Allowingforthe2.7­hourlagtime,asingleC.sakazakiicellcouldproduceasmanyas256offspringundertheconditionsofusestill recommended in 2001 by the American Dietetic Association(ADA)andtheU.S.FoodandDrugAdministration(FDA).Ifafour­hour limithadbeen in effect at the timeof the2001outbreak, thatsameC. sakazakii cell would only have had time to produce fouroffspring.

Whiletheresultsofasingleresearchreportwouldnotordinarilybe enough to warrant a major policy shift, the Canadian researchhadbeentriggeredbyseveralclinicalreports,issuedoveraperiodofyears, of death or lifelong disability resulting from C. sakazakiiinfections. These reports, and the results of the Canadian researchstudy,appeartohavepassedbeneaththeradarscreensoftheADA,food safety regulators, and infant formula manufacturers both inNorth America and in Europe. One year after the Tennesseeoutbreak, a Belgian baby became infected with C. sakazakii,developedmeningitis,anddiedshortlyafterbeingreleasedfromthehospitalat fivedaysofage.Thesourceof thebaby’s infectionwastraced to a batch of Nestle’s “Beba” powdered formula. NestlerecalledtwoproductionlotsoftheformulainMay2002.14

The FDA responded to the lessons learned from the Tennesseeoutbreakbyincreasingsurveillanceofinfantformulamanufacturers,with specific emphasis onC. sakazakii. This heightened awarenessresulted in at least one recall, comprising several lotsofpowderedformula produced by Wyeth Nutritionals and sold under variousbrand names. This time, the FDA caught the problem before anyinfantswereputatrisk.15

In2002,asaresultofthefatalTennesseeoutbreak,boththeFDAandtheADAmodifiedtheirrecommendationsforpreparation,useand storageof reconstitutedpowdered formula, and shortened therecommendedroomtemperatureholdingperiodfromeighthourstofour.16,17Inaddition,FDAmicrobiologistsdevelopedaprocedurefordetectingC.sakazakiiinpowderedinfantformulaandpublishedthedetailsontheagency’swebsite.Atthesametime,theFDAletitbeknown that testing for this microbe would become part of theirstandardprotocolwheninspectinginfantformulamanufacturers.18

In2007, theWorldHealthOrganization (WHO) recommendedafurtherreductioninholdingtimeforreconstitutedpowderedinfantformulafromfourhours toamaximumof twohours,and in2014,the FDA implemented stringent new quality control standards forthemanufactureofpowderedinfantformulas.19,20

MorethanthirtyyearsaftertheTennesseeoutbreak,thethreatofC.sakazakiistilllingers.Arecentsurveyof128samplesofpowderedinfant formula from Chile, Mexico, the Netherlands and Brazildiscovered low levels of C. sakazakii in samples of four differentChileanproductsandoneMexicanproduct.21A2019surveyoffourChinese powdered infant formula factories found forty­two C.sakazakiiisolatesfrommultiplelocationsinallfourfacilities.Someoftheisolateswererecoveredfromdesignated‘cleanwork’areas.22

Allofus,whetherweareconsumers,foodhandlersorfoodsafetyprofessionals, are subject to the “Old Habits” syndrome, and wecannotaffordtoletdownourguard.Toensurethesafetyofourfoodandwatersupply,wemustalwayslearnandusethebestandsafestways toproduce,prepareandstore food.Wedon’thave tocut theendoffthebrisket,justbecauseNana’spotwastoosmall.

Chapter2RecipesforDisaster

Whether for eliminating pesky facial imperfections, reducingexcessiveunderarmsweating,treatingmusclespasms,ormitigatingmigraines,Botox®hasbecomeabandwagonwithanevergrowingpopulationofadherentseversinceitsinitialapprovalbytheFDAin2002.1,2,3,4 But this potent neurotoxin and Clostridium botulinum,the microbe that produces it, can also wreak havoc in our foodsupplywhenweleastexpectit.

TheFatalErrorHazelnut was a common yogurt flavor in the United Kingdom

(UK)inthe1980s.Hazelnutconservewaspreparedfromapureeofroasted hazelnuts, water, starch and sugar. The ingredients weremixed, heated together in a large vat, and pumped into cans. Thecanswerethensealedandplacedinaboilingwaterapparatusfor20minutes, after which they were cooled and stored at roomtemperature.Yogurtmanufacturerspurchasedtheconserve,mixeditwithplainyogurt,andpackaged theproduct into retail containers.Allwentwelluntilconsumersdemandedasugar­freevariety.

The supplier of hazelnut conserve responded by substitutingaspartame for sugar in his formula. Little did he realize that, indoingso,hehadopenedPandora’sbox. InMayand June1989, 27people living in Northwest England and North Wales developedsymptomsofbotulism:weaklimbs,impairedspeech,doublevision,difficulty swallowing, and weak respiratory muscles. One persondied from aspiration pneumonia, and twenty­five others werehospitalized.Of the 27 victims, 25 reportedhaving eaten the samebrandofhazelnutyogurt.5

Investigators foundC.botulinum toxin in unopened packages ofthe yogurt. After having inspected the production plant, they

concluded that the yogurt manufacturer was maintaining anadequatelevelofhygiene,andturnedtheirattentiontothehazelnutconserve.Theyearbefore,inresponsetocomplaintsofswollencans,the manufacturer added potassium sorbate to his formula in anattempttocontrolthegrowthofyeast,whichheassumedtobethecauseof theswelling.As it turnedout,yeast contaminationwasn’ttheproblem.Clostridiumbotulinumwas.

When investigators tested a badly swollen can of the conserve,theyfoundthat itcontainedthesametoxinthatwaspresent intheyogurt. On reviewing themanufacturer’s production process, theyrealized that the heating step was not harsh enough to kill C.botulinumspores.Worse,thelevelofacidity(pH)oftheconservewaswellwithintherangethatthemicrobecouldtolerate.

Byswitchingfromsugartoaspartamewithoutmakinganyotheradjustments to his process, the conserve manufacturer had sethimselfuptofail.ThehighsugarcontentoftheoriginalformulahadpreventedC.botulinumfromgrowing.Oncethesugarwasremoved,so was the only barrier to a serious outbreak. The manufacturerforgot – or never realized – that he was walking a food safetytightrope.

Long associated with inadequately processed canned food, C.botulinumhasappearedinavarietyofnewplacesinrecentdecades.Uneviscerated salted fish, fermented beaver tails, and oil­packedcondiments such as chopped garlic, roasted eggplant, and sautéedonions have all been linked to botulism.6,7,8,9,10,11 In 1994, foil­wrapped baked potatoes were responsible for the third­largestoutbreakofbotulisminUShistory.

FoiledThestorybegantounfoldearlyonthemorningofApril10,1994,

when a father and his teenage son turned up in an El Paso, TXhospital complaining of botulism­like symptoms.12 In the daysbeforetheirarrivalatthehospital,theyhadsharedamealatTassos,

a local Greek restaurant.13 The hospital notified local healthauthoritieswho, in turn, alerted theother sixhospitals in thearea.Within hours, four additional victimswere identified. All of themhadeatenatTassos.

FacedwithanincipientC.botulinumoutbreak, theElPasohealthdepartment immediately ordered the restaurant to remain closedthat day, to allow health officials time to interview the outbreakvictims.All of thepeoplewho showed symptomsof botulismhadvisitedtherestaurantoneitherApril8thor9th,andmostofthemhadeatenoneoftwoappetizersmadefrombakedpotatoes:skordalia(apotatodip)andmelitzanosalata(apotato/eggplantdip).Fourofthevictimswhohadn’teateneitherdipwererestaurantemployees,andhadhandledbothappetizerswhileonthejobApril8thand9th.

Investigators tested leftover potato dip and confirmed that itcontained high levels of botulinum toxin. The restaurant had noeggplantdip leftover,butsomewas founddiscarded inagarbagecanat thehomeofoneof thepatients. It, too,waspositive for thesame toxin. The pH of the potato dip was 3.7 – too acidic forC.botulinumtogrow.Investigatorsconcludedthatthetoxinmusthavecomefromoneoftheingredients.

Six ingredients were common to both dips: oil, vinegar, rawonion,rawgarlic,fetacheeseandbakedpotato.Thepotatodipalsocontained French bread, and the eggplant dip contained bakedeggplant. While there was no leftover baked potato or eggplantavailablefortesting,alloftheotherdipingredientsweretestedandcontainednotoxin.

Thepotatodiphadbeenpreparedusing twopotatoes thatwerewrapped in aluminum foil and baked at 450ºF [250ºC] for about 2hoursonApril7th.Stillwrappedinthefoil,thebakedpotatoeswerestoredfor18hoursatroomtemperature.Theeggplantdipwasmadeon April 5th using one potato and some eggplant that had beenbakedearlierintheevening.ItwasservedtodinersonApril6thor

7th,withnoapparentilleffect.However,5peoplewhowereservedportionsofthesamebatchofeggplantdiponApril8thbecameill.

LabinvestigationsconfirmedthatC.botulinumsporescouldhavesurvived baking inside a foil­wrapped potato, and could havegerminated, multiplied, and produced toxin in the baked potatowhile itwas stored at room temperature. The toxin also remainedstable and active in the acidic environment of the potato dip. Thetwo implicated appetizers had been stored side­by­side in therestaurant’s refrigerator, and the same utensilswere used for bothdishes. Investigators concluded that a serving utensil hadtransferredtoxinfromthepotatodiptotheeggplantdip.

The foil wrapping on the baked potatoes was the key to thisoutbreak. In a trial baking study, the internal temperature of foil­wrapped baked potatoes only reached 205­207ºF [96­97ºC], atemperature that C. botulinum spores could easily have survived.After baking, the foil acted as an oxygen barrier, creating near­perfectanaerobicconditionsunderwhichtheorganismcouldgrowandproduceitsdeadlytoxin.Thechef’sdecisiontostorethebakedpotatoesat roomtemperature for18hourswas the final ingredientin theC. botulinum recipe.Had he refrigerated the baked potatoes,therewouldhavebeennooutbreak.

HaveEggsInstead?Pitythepooregg.Oncehailedasoneofnature’sperfectfoods,it

has fallen onhard times. First itwas ostracizeddue to our fear ofcholesterol.Then, in the late1980s,Salmonella further poisoned theegg’sreputation.ReportsoffoodborneSalmonellaoutbreaks–manyof them traced to eggs served at foodservice locations such ascafeterias, hospital kitchens, and restaurants – started flowing intogovernment healthdepartments in several countries, including theUnitedStates.

The breakfast buffet was a popular fixture at a Marylandrestaurant chain.14 But in the summer of 1985, it offered an

unexpectedandunwelcomeingredient.ThatAugust,oneemployeeand 3 patrons of a restaurant in the chain were stricken withSalmonella Enteritidis. Even though county health authoritiesinvestigated the restaurant and interviewed the victims and otherpatrons, they couldn’t determine which food had caused theoutbreak. There were not enough victims, and just too manyindividualfooditems,toallowinvestigatorstopinpointthesource.

In the first half of September, five customers of a secondrestaurantbelongingtothesamechainbecameill.Thatsameweek,113peoplewhohadeatenatathirdrestaurantinthechaincontactedtheir local health department to complain about diarrhea, crampsandfever.Seventeenofthe113endedupinthehospital.Oncemore,SalmonellaEnteritidiswastheuninvitedguestatthetable.Thistime,however, investigators were able to identify the offending food.Scrambledeggsofferedinthebreakfastbuffet.

All three restaurants used Grade A shell eggs to prepare theirscrambled eggs. Employees cracked the eggs by hand,with up to1800eggscombinedintoasinglebatch.Thescrambledeggmixturesometimes sat at room temperature for as long as 6 hours beforebeing cooked, and the kitchen staff was trained to undercook theeggs.Otherwise,thescrambledeggswoulddryoutinthebreakfastbar’swarmingtray.Indeed,severalofthefoodpoisoningvictimsatrestaurant#3reportedthattheeggsappearedunderdone.

It looked like a coincidence that all 3 locations were hit with aSalmonellaoutbreakinthespaceofjustafewweeks,exceptthatlabtests found that the identical strain of Salmonella Enteritidis wasresponsible for all of the illnesses. An in­depth investigationdetermined that the threeaffectedrestaurantspurchased theireggsfromthesamedistributor.Contaminatedeggscombinedwithpoorhandling and cooking procedures made these outbreaks all butinevitable.

State health officials were unable to find Salmonella in otherbatches of eggs from the distributor. As a result – despite strong

circumstantialevidence– theycouldn’t confirmunequivocally thateggsfromthatdistributorwerethesourceoftheoutbreaks.Officialshad to content themselves with explaining to the restaurantmanagementhowtoprepareandservescrambledeggssafely.

The 1985Maryland outbreakswere early harbingers of amuchlarger problem. That same year, Salmonella Enteritidis became themost commonly reported Salmonella serotype in three US states:New Hampshire, New Jersey and New York. The trend of ever­increasing reportsof illnessdue toSalmonella Enteritidis continuedin1986.Sourcesof theoutbreaks includedawidevarietyof foods.Scrambled eggs, pasta (both homemade and commercial),hollandaise sauce, rice balls, protein supplement, and roast beefwereallimplicated,buttherewasnoapparentconnectiontoexplainthe emergence in the US Northeast of Salmonella Enteritidis as aserotypetobereckonedwith.15

Then tragedy hit the Coler Memorial Hospital on RooseveltIsland,NewYork.

OnFridayJuly31,1987,theheadlineonpageB3intheNewYorkTimesread“TaintedFoodPossibleinPatient’sDeath.”TheoutbreakhadbegunonTuesdayofthatweek,andbylateThursdaymorethan175peoplehaddevelopedgastroenteritis.16Bythetimetheoutbreakwas over, 274 hospital patientswere diagnosedwith salmonellosiscausedbySalmonellaEnteritidis,andninepatientshaddied.17

Hospital officialsworked feverishly to trackdown the sourceoftheSalmonellabefore theoutbreakcouldspiraloutofcontrol.Theyquicklydiscovered that the contaminatedmealhadbeen servedatlunch on July 28th. Based on a review of medical records, theirattention focused on a tuna­macaroni salad containing hospital­preparedmayonnaisewhichwasmadeonJuly27thusingrawGradeAshelleggs.ItwasmixedwiththeotheringredientsthemorningofJuly28th,andthefinishedsaladsatatroomtemperaturefor5hoursbeforebeingservedwithlunch.

Thehospital lab testedremnantsof the tuna­macaronisaladandfoundSalmonellaEnteritidis.Theyalso recovered thesamemicrobefrom pooled batches of eggs. Just to tie up the final loose ends,cultures of hen ovaries from the farm that had produced the eggswere positive for the same strain ofSalmonella Enteritidis that hadbeenfoundinthepatientsandinthesalad.

Coincidentally,Salmonella Enteritidiswas also turning up in theUKatanalarmingrate.IllnessduetoSalmonellaEnteritidisincreasedmore than six­fold from 1101 to 6858 cases in the period between1982 and 1987. While some cases of salmonellosis were traced topoultrymeat,manyothersweretiedtoavarietyoffoodscontainingraworpartiallycookedeggs.18

Inexorably,yearafteryear,SalmonellaEnteritidiscontaminationofshell eggsextended its reach toother countries, aswell as tootherregions of the United States. Japan was hit in 1989.19 SalmonellaEnteritidiswasresponsibleforoutbreaksinCanadain1991,inItalyin 1993 and in California in 1996.20,21,22 Reports submitted to theWHObetween1979and1987bythirty­fivecountrieshighlightedthemagnitudeof theproblem.ThepercentageofSalmonella Enteritidisisolations increasedbyat least25% in twenty­oneof the thirty­fivecountries, and more than doubled in fifteen of them.23 And thenumber of victims continued to grow. Time and again, SalmonellaEnteritidis outbreaks were traced to foods containing raw orundercookedeggs.

Hollandaise sauce, Caesar salad, ice cream, cake frostings,meringue pies, cheesecake, scrambled eggs, and mayonnaise. Thelist of dishes and desserts that traditionally use raw or partiallycookedeggsgoesonandon.Everynowandthen,therecipecomeswith a microscopic bonus in the form of Salmonella Enteritidis.MicrobiologistsoncethoughtthatSalmonellacouldnotpenetrateintoaneggunlesstheshellwasdamaged.Butifthatweretrue,howwasthemicrobefindingitswayintoeggs?Moreimportantly,whatcouldbedoneaboutit?

Toanswer thesequestions, theCDCorganizedaworkinggroupincooperationwithstateepidemiologistsinNovember1986.15Afterreviewing sixty­five outbreaks that had occurred over a 2½­yearperiod beginning in January 1985, the group came to a startlingconclusion. Infected hens were contaminating the eggs withSalmonellawhile the immatureeggswere still in theoviduct.24Noteveryoneagreedwiththisassessmentatfirst.25Butoverthenextfewyears,evidencepiledupinsupportofthetheory.26

Eggproductionbeginsintheovary,whichisfilledwithimmatureeggs.Asaneggmatures,itpopsoutoftheovaryandentersatubeknownastheoviduct.Atthisstage,theeggisatiny,nakedyolk.Asit travels down the oviduct, the egg increases in volume. Once itreaches full size, the egg yolk is surrounded by the vitellinemembrane, around which is deposited a layer of albumen (eggwhite). Two pieces of fibrous material called chalaza attach thealbumentothevitellinemembrane.Finally,theshellmembraneandeggshellaredepositedaroundtheexteriorofthenow­completeegg.

AninfectedhencancarrySalmonella in severalpartsof itsbody,including the ovary and the oviduct.27 Until an egg receives itsprotective shell, it is susceptible to Salmonella contamination. Themicrobecaneithertraveldowntheoviduct fromaninfectedovary,or up the oviduct from the cloaca. If the oviduct itself iscontaminated,Salmonellacanbetransferreddirectlytotheeggas itpassesthroughonitswaytothecloaca.28

Knowing how the egg becomes infected is only one part of thebattle–theeasiestpart,atthat.Preventingtheinfectionisfarmoredifficult. The only way to ensure that eggs don’t becomecontaminatedwithSalmonella before theyare laid is to startwithaSalmonella­freeflockoflayinghensandworktokeepitthatway.

Whichcamefirst–thechickenortheegg?

While a Salmonella­free breeding hen produces Salmonella­freechicks,that’sonlythefirststep.Becausenewbornchicksarehighlysusceptible to infection with Salmonella Enteritidis and othersalmonellae, decades of research have gone into strategies to keepchicks free from infection as theymature and develop into layinghens.

In 1971, Finland was hit with a massive outbreak of SalmonellaInfantis in its broiler flocks. The economic damagewas huge, and277peoplewerestrickenwithsalmonellosis.29Inordertopreventarecurrence,Finnishscientistslookedforwaystoprotecttheirflocks.Theyobservedthat2­to3­dayoldchickswerehighlysusceptibletoSalmonella.Butbyfeedingthebabychicksamixtureoftheintestinalcontentsofahealthyadultchicken,thebabieswerepreventedfromsuccumbing to infection.30 The researchers theorized that somecomponent of the natural bacterial flora of Salmonella­free birdsblockedSalmonella fromcolonizing thechickens’guts.Theynamedthephenomenon“competitiveexclusion.”

Finland and Sweden, were among those countries that, in theearly 1980s, incorporated competitive exclusion into an overallstrategywhichincludedusingSalmonella­freefeedandmaintaininga clean henhouse environment. The contamination rate of chickencarcassesinFinlanddroppedtojust5­10%in1992.Thatsameyear,only1%ofSwedishchickenstestedpositiveforSalmonella.31,32

Competitive exclusion alone is not enough to eradicateSalmonella.19,33As the Scandinavians have learned, however, it canbe very effective when used in conjunction with other controlmeasures.Onesuchmethodisvaccination.

The idea of vaccinating chickens against Salmonella was firstexploredasameansofpreventingfowltyphoid,adiseaseofpoultrycausedbySalmonellaGallinarum.34EarlyexperimentswithvaccinesmadefromkilledSalmonellaprovedfruitless.Then,in1956,thefirstsuccessfulvaccine– thisoneusinga live,attenuatedculture–was

announced.35 Until recently, however, the use of poultry vaccineswasneverextendedbeyondcontrolofSalmonellaGallinarum.

As regulators struggled in the 1980s and 1990s to contain thesudden eruptionof egg­associatedSalmonella Enteritidis outbreaks,poultryscientistsrevisitedvaccinationasacontrolstrategy.In1994,HassanandCurtisintroducedalivevaccinethatprotectedchickensfrom infection by a variety of salmonellae, including SalmonellaEnteritidis.36Theirvaccinecamewithabonus.Thebabychicksbornfrom vaccinated hens were more resistant to Salmonella infectionthanchicksfromunvaccinatedhens.37

In spite of the promising results obtained from vaccination andcompetitiveexclusionresearch,egg farmerscannot relyexclusivelyon these approaches to keep their poultry Salmonella­free. Severalenvironmental factors conspire to expose laying hens to infectionthroughout their lifespan.Often, feed isalreadycontaminatedwithSalmonella when it arrives at the farm.22 Mice carry SalmonellaEnteritidis from henhouse to henhouse, spreading contaminationwith their droppings.38 Also, Salmonella can attach to dust in thehenhouse and circulate through the air, especially in windowless,environmentallycontrolledfacilities.19Therefore,rodentcontrolandcareful attention to sanitation and disinfectionmust be part of thepoultryindustry’santi­Salmonellaarsenal.

Nor is it enough to focus exclusively on the laying hens whileignoring the eggs. Hens expel their eggs through the cloaca – thesameopeningthroughwhichtheyeliminatefeces.Thus,evenattheinstant amature egg is laid, it is exposed to the risk ofSalmonellacontamination from an infected hen.39 Once laid, every step in anegg’svoyagetothebreakfastplateprovidesanotheropportunityforSalmonellatohitcharide.

Modern egg farms arehighly automated and comprisemultiplehenhouses.Whenahenlaysheregg,aconveyorbeltcarriesitoutofthe henhouse. Often, the same belt passes through each house in

sequence, accumulating eggs, debris, feces and, sometimes,Salmonellaalongtheway.40Beingfragile,someeggsdevelophairlinecracks,orevenbreakopen,duringthecollectionprocess.Althoughcracked or broken eggs are either discarded or diverted, egg yolkandalbumenleakingfromthedamagedeggscancoat theshellsofintacteggs,andactlikeflypapertotrapstraySalmonella.

Whilestudieshaveconfirmedthatcagedhensinhighpopulationdensity facilities produce Salmonella­contaminated eggs, free­rangeandcage­freehensaren’texemptfromthisproblem.Free­rangehenshave access to the outdoors for at least part of the day; cage­freehens, while not housed in cages, do not necessarily have outdooraccess.Bothspendatleastpartoftheirtimeindoors.Free­rangehensare justassusceptibletoSalmonella infectionastheircagedcousins,especially when a poultry farm is located near a sewage runoffcreek.21,41,42

In the US, once intact shell eggs arrive at an egg­processingfacility,theyarewashedwithasanitizingsolution,andcoatedwithalight mineral oil to seal the pores of the shell.43 Washing andsanitizingremovesvisiblesoilandreducesthebacterialpopulationontheoutsideoftheshell.Butdetergentstripsthenaturalprotectivecoating from the shell, potentially enablingSalmonella to penetrateinto the albumen.44 Due to this perceived risk, several countries –includingtheUKandmanymembersoftheEuropeanUnion(EU)–donotwasheggs.45,46

Temperature change is also an important factor in eggcontamination.Whenaneggcools,eitherafterhavingbeen laidorafterwashing, the contents shrink slightly. This creates a vacuum,whichcansuckintotheegganybacteriathatmaybepresentontheoutsideoftheshell.47

Once it enters an egg, all that Salmonella needs in order tomultiply is enough time and the right temperature. SalmonellaEnteritidisbarelygrowsatrefrigerationtemperature,butmultiplies

readily in eggs that are stored at room temperature.48,49 The olderthe egg, the better able it is to support the growth of Salmonella.Furthermore, the aging effect is hastened by storing eggs withoutrefrigeration.50 Unlike the UK, member countries of the EU, andmany other developed countries, the US and Canada require thateggsbeheldatorbelow50ºF[10ºC]throughtheentirelengthofthesupplychainfromcollectionatthehenhousetoretaildisplay.51,52

Notwithstandingallofthethingsthatcangowrongateachstepintheeggproduction,distribution,andmarketingchain,theriskoffinding a contaminated egg was thought to be small. Usinginformation based on the theoretical rate of infection ofUS layinghens at various stages in their productive lives, a risk­assessmentteam operating under United States Department of Agriculture(USDA)auspicescalculatedthatonly0.005%ofeggs(justoneeggin20,000)werelikelytocontainSalmonellaEnteritidis.53

Thisstudy,whichwaspublishedin2000,providedafalsesenseofsecuritytoconsumers.Itwasanumbersgame,basedonaseriesofassumptionsregardingtherelativeprevalenceofSalmonella­negativelayingflocksandflockswithlow(~1contaminatedeggin17,000)orhigh (~1 contaminated egg in 1400) rates of Salmonella­positiveresults.54 As regulators and consumers would find out a decadelater,asingleout­of­controlhatcherycouldwreakhavocwithpublichealthandtheeggdistributionsystem.

ThepresenceorabsenceofSalmonellainsideaneggisnottheonlyconsideration. Quantity counts. The number of live bacteria in acontaminatedeggcanbecomedangerouslyhighiftheegghasbeenmishandled—highenoughthattraditionalcookingmethodsmaynotkillalloftheSalmonella.55Salmonella­positiveeggsalsopresentariskof cross­contamination during food preparation. Cracking,separatingorbeatinganeggcanspreadSalmonellaoverawidearea,contaminating work surfaces, utensils, mixing bowls and hands.56It’s just as important to clean up the kitchen thoroughly afterworkingwitheggsasitisafterhandlingrawchicken.

Sadly, food handlers – even those who work in hospitals –sometimesforgettherisksassociatedwithraweggs.In1993,agroupof fourteen people, including seven children, who attended acookout at a psychiatric hospital in Florida learned about theconnection between Salmonella Enteritidis and eggs the hard way.Five of the seven children and all of the adults developedgastroenteritis within twenty­four hours of attending the party.Elevenof the twelvevictimshadeatenhomemade icecreammadeespeciallyforthecookout.57

InvestigatorsfoundSalmonellaEnteritidisintheleftovericecreamand also recovered themicrobe from three of the victims. The icecreamhadbeenpreparedthemorningofthecookoutusingsixraweggs.Therewerenoobviouspreparation,sanitationortemperaturecontrolerrors.Raweggsrepresentedtheonefatalflawintherecipe.

The USDA tried, without success, to trace the producer of theeggs.Thehospitalwasable topoint investigators to their supplier,butthedistributorhadpurchasedeggsfrommanydifferentsources.AstheagencyhadnoauthoritytotestpoultryflocksforSalmonellaunlesstheevidenceclearlyimplicatedonespecificflockasbeingthesource of an outbreak, the USDA was unable to pursue itsinvestigationtoalogicalconclusion.

Aslongaspeoplewanttoenjoyhomemadeicecream,hollandaisesauce,sunnysideupeggs,andCaesarsalad,outbreaksofSalmonellaEnteritidisgastroenteritiswillcontinuetopopuplikethunderstormson hot, humid days. But, unlike the weather, we can controlSalmonella if government agencies, the egg industry and foodhandlersarepreparedtomaketheeffort.

Thisefforthasbeenmade,andhasbornefruit,insomecountries.Morethan80%ofretailshelleggsintheUKnowcomefromflocksthat have been vaccinated against Salmonella Enteritidis.46 TheBritishgovernmentmandatedSalmonellatestingofallbreederflocks,and introduced new codes of practice for infection control andhygiene.Asaresult,reportedcasesofSalmonellaEnteritidisinfection

in the UK declined from a peak of nearly 30,000 cases in 1997 tofewerthan2,200SalmonellaEnteritidisinfectionsreportedduringallof 2019, excluding a single four­week period for which data wereunavailable.58

TheUStookasomewhatdifferentapproach,emphasizingtheeggaswellasthechicken.ThePresident’sCouncilonFoodSafetyissuedits Egg Safety Action Plan in December 1999.59 The CouncilestablishedaninterimgoalofreducingSalmonellaEnteritidisillnesslinkedtoeggsby50%by2005andeliminatingitcompletelyby2010.Yet,in2018,cage­freeeggsfromasingleproducerwereresponsibleforanoutbreakofforty­fourSalmonellaEnteritidisillnessesinelevenUSstates.60

The1999ActionPlan identified thestagesofeggproduction forwhich improvements were needed, including breeder flocks andpoultry feed, shell­egg processing procedures, improved packagelabeling, proper storage, shipping and display temperatures, andbettereducationoffoodhandlers,whethercommercial,institutionalor in the home. The plan also highlighted the need for improvedoutbreak surveillance and for a national system to enableinvestigators to trace a contaminated batch of eggs through thedistribution system back to the flock that produced it. Finally, itcalledforadditionalresearchintoallaspectsofSalmonellaEnteritidisanditsassociationwithpoultryandeggs,includingdevelopmentofimprovedvaccinesandcompetitiveexclusionproducts,andin­shellpasteurizationofeggs.

In 2000, the FDA published a Final Rule requiring that allconsumerpackagesofshelleggsbelabeledwithinstructionsforsafehandling and storage of the eggs.61Then, in 2004, the FDA took amajor step towards achieving the goals set forward in the 1999Action Plan by issuing a new set of proposed rules. The FDA’sproposed Egg Safety Final Rule, which targeted all egg producerswith 3000 or more laying hens, encompassed rodent and pestcontrol, biosecurity concerns, procurement of chicks and pullets,

cleaninganddisinfectionofpoultryhouses,andrefrigerationofeggsat the farm, among other issues.62,63 The comment period for theproposalwasextendedtwicein2005andwasnotfinalizeduntilJuly2009.64,65 The compliance date established for large producerswasJuly2010.66Smallproducersweregrantedanadditionaltwoyearstobringtheiroperationsintolinewiththenewregulations.

Whether it’sC. botulinum in eggplant orSalmonella Enteritidis ineggs, the challenge is the same. Recipes that do not include anadequatefinalcookingstephavebecomeincreasinglypopularwithconsumers,andcanbeasignificantsourceoffoodborneillness.Thehealth risks associated with these recipes are magnified wheningredientsarenotchosenwisely,oraremishandled.Foodhandlers,whethermanufacturers,foodserviceworkers,orconsumers,mustbeprepared toadapt their techniques in the faceofnewly recognizedpathogens—orold familiarpathogens innew settings—inorder toensurethesafetyofthefoodtheyprepare.

Chapter3Betrayal

SarahLewisandherentirefamilyattendedacelebratorydinneratalocalrestaurantonMay29,2010,tomarkhersisterStacey’scollegegraduation.Thenextnight,Sarah’sworldturnedupsidedown.1

AlreadyfeelingunwellontheeveningofMay30th,Sarahwenttobedearly.Sheawakenedduringthenight,sufferingfromvomitingandseverediarrhea.Thenextday,Sarah’smother,wholivednearby,took her to an urgent care facility. Twenty minutes later, she wasadmittedtohospitalandwaslaterdiagnosedwithsalmonellosis.

Badly dehydrated and in enormous pain from her inflamedbowels, Sarah was moved to the hospital’s ICU. While there, shedevelopedseveretachycardia(abnormallyrapidheartbeat),andwasmovedtothecriticalcareheartunit,whereshespentthreedays.

When Sarah was finally discharged in time to attend herdaughter’spreschoolgraduation,shethoughttheworstwasbehindher.

About2½weekslater,shewasbackinthehospital,stillsufferingfromseveredehydration.Shewasreleasedafterfivedays.

The antibiotics Sarah took to combat her Salmonella infectionstrippedherdigestivesystemofitsnormalpopulationofprotectivebacteria,resultinginherbecominginfectedwithClostridiumdifficile(C.diff),abacteriumwhichcausesseverediarrheaandcramping.Afourteen­dayantibioticregimentookcareoftheC.diff;however,theSalmonellawasmoreresilient.Fourmonthslater,Sarahstillwason5to10differentmedicationsdailytocombattheinfectionandcontrolhersymptoms.

Sarah Lewis was the first recorded California victim of aSalmonellaEnteritidisoutbreakthatsickenedmorethan1900people

acrosstheUnitedStates.2

TherestaurantwhereStacey’sgraduationbanquetwasheldhadpurchased custard tarts froma local bakery.Ordinarily, the bakeryusedapasteurized liquideggmixture tomake the tarts.However,onthedaytheypreparedthedessertitemsforthegraduationdinner,thebakeryranoutofpasteurizedeggmixandusedfresh,rawshelleggsinstead.EggsthatmostlikelyhadcomefromIowa.

SomethingRottenintheStateofIowaThe CDC first became aware of an unusual rise in Salmonella

Enteritidis infections in July 2010. Epidemiological and tracebackinvestigations pointed the finger of suspicion at two Iowa­basedsuppliers of shell eggs: Quality Egg, LLC (also known as WrightCountyEgg)andHillandaleFarmsofIowa,Inc.2

Alerted by the CDC, the FDA began a detailed inspection ofQualityEggonAugust12th.Theyencounteredanegg­laying farmoverrunwith rodents and birds.Henhouses and buildingsused tostore feed grainwere in a state of disrepair, withmanure seepingthrough the concrete foundation of one of the laying houses.Uncaged chickens ambled across an 8­feet high pile of manure toaccesstheegglayingarea.3

The situation confronting inspectors when they began theirinspection of Hillandale Farms on August 19th was just as bad.Uncaged hens were trackingmanure into the henhouses, some ofwhichhadstructuraldamage.Therewasstandingwateradjacenttothe manure pit, and liquid manure was leaking into one of thehenhouses.4

ItsurprisednoonewhenenvironmentalsamplescollectedatbothQuality Egg and Hillandale Farms tested positive for SalmonellaEnteritidis.3,4

Quality Egg announced an initial limited recall onAugust 13th,andexpanded the scopeof the recallonAugust18th.5,6HillandalefollowedsuitwithitsownrecallnoticeonAugust20th.7

The shell eggdistribution system in theUnited Stateswas (andremains)multi­tieredandcomplex.Eggsweredistributedinbulktopackagingfacilities,whichpackagedtheeggsundermultiplebrandnames. Often, eggs from more than one supplier were mingledtogetherforpackagingintoindividualcartonsholdingsix,twelve,ormoreeggs.

Because there was no way to determine the source of the eggscontained in any one carton, the recalls mushroomed, andconsumerslostconfidenceinthesafetyoftheeggstheypurchased.8

TooLittle,TooLateThe FDA’s Egg Safety Final Rule, issued in 2004,wasmeant to

preventexactlythekindofsituationthat theagency’s investigatorsencountered at Wright and Hillandale. But bureaucratic delaysprevented the rule from being enacted until July 2009. Companieswith 3000 or more laying hens were given one full year from theenactment date to implement the required changes to theiroperations. Smaller companies were allowed even more time tocomply.

Ironically, the July 2010 deadline for compliance coincidedwiththe CDC’s realization that the Salmonella Enteritidis outbreak waslinkedtoeggs.

On reviewing Quality Egg’s records during the course of itsextensive investigation, theFDA learned that themanagementhadknown since at least 2008 that its environment was heavilycontaminatedwithSalmonella,hadfalsifieditsrecords,andhadliedboth to outside auditors and to corporate customers regarding thecompany’ssanitationandfoodsafetypractices.1,9

UnderthefracturedUSfoodregulatorysystem,responsibilityforgradingandinspectingshelleggsrestswith theUSDA.Onat leasttwooccasions in 2010, theUSDA inspector responsible forQualityEgghad‘red­tagged’eggsthatdidnotmeetgovernmentstandards.Ordinarily, red­tagged eggs would be diverted to egg­crackingplants forprocessing intopasteurizedeggproducts forcommercialuse.Onbothoccasions,acompanyemployeebribedtheinspectortoreleasetheshelleggs intoretaildistribution,wheretheeggswouldcommandahigherprice, insteadofrequiringthattheybesenttoacrackingfacility.10

Severalfederalchargeswerelaidagainstthecompany,itsownersandoneofitsemployeesintheaftermathoftheinvestigation.

OnSeptember12,2012,TonyWasmund,formerlyanemployeeofQuality Egg, pled guilty to conspiracy to bribe a public official, toselling restricted eggs with intent to defraud, and to introducingmisbranded food into interstate commerce with intent to defraudandmislead.11

 

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