Outbreak of Type A Botulism and Development of a ... - Library

LETTER FROMBUENOS AIRESOutbreak of Type A Botulism andDevelopment of a Botulism Surveillanceand Antitoxin Release System in ArgentinaRodrigo G. Villar, MDRoger L. Shapiro, MDSilvina Busto, MD, MPHClara Riva-Posse, MD, MPHGuadalupe Verdejo, MD, MPHMaria Isabel Farace, DVMFrancisco Rosetti, MSJorge A. San Juan, MDCarlos Maria Julia, MD, MPHJohn Becher, RPhSusan E. Maslanka, PhDDavid L. Swerdlow, MDContext Botulism is an important public health problem in Argentina, but obtainingantitoxin rapidly has been difficult because global supplies are limited. In January 1998,a botulism outbreak occurred in Buenos Aires.Objectives To determine the source of the outbreak, improve botulism surveillance,and establish an antitoxin supply and release system in Argentina.Design, Setting, and Participants Cohort study in January 1998 of 21 drivers ofa specific bus route in urban Buenos Aires.Main Outcome Measure Occurrence of botulism and implication of a particularfood as the vehicle causing this outbreak.Results Nine (43%) of 21 bus drivers developed botulism, presenting with gastroenteritis,symptoms of acute cranial nerve dysfunction including ptosis, dysphagia, blurredvision, and motor weakness. One driver experienced respiratory failure. Type A toxinwas detected from 3 of 9 patients’ serum samples. All drivers received botulism antitoxin;there were no fatalities. Consumption of matambre (Argentine meat roll) wassignificantly associated with illness. Among 11 persons who ate matambre, 9 developedillness, compared with none of those who did not eat it (P.001). The matambrehad been cooked in water at 78°C to 80°C for 4 hours, sealed in heat-shrinkedplastic wrap, and stored in refrigerators that did not cool adequately. Subsequently, abotulism surveillance and antitoxin release system was established.Conclusions Insufficient cooking time and temperatures, storage in heat-shrinkedplastic wrap, and inadequate refrigeration likely contributed to Clostridium botulinumspore survival, germination, and toxin production. A rapid-response botulism surveillanceand antitoxin release system in Argentina should provide more timely distributionof antitoxin to patients and may serve as a model for other nations.JAMA. 1999;281:1334-1338, 1340www.jama.comAuthor Affiliations: Foodborne and Diarrheal DiseasesBranch (Villar, Shapiro, Maslanka, and Swerdlow), ScientificResources Program (Becher), National Center forInfectious Diseases (Villar, Shapiro, Maslanka, Swerdlow,and Becher), Epidemic Intelligence Service, EpidemiologyProgram Office (Villar and Shapiro), Centersfor Disease Control and Prevention, Atlanta, Ga (Villar,Shapiro, Maslanka, Swerdlow, and Becher); Ministeriode Salud-Region V (Busto) and Ministerio de Salud y AccionSocial (Riva-Posse and Julia), Medicina SanitariaBOTULISM IS A POTENTIALLY FAtal,neuroparalytic illness resultingfrom toxins produced by thebacterium Clostridium botulinum. 1,2 Humanillness occurs as infant botulism,botulism from intestinal colonizationand wound infections, and foodbornebotulism. 3 Symptoms appear approximately12 to 36 hours after toxin exposurebeginning with bulbar and autonomicnervous system disturbances.Descending, symmetrical skeletalmuscle weakness, paralysis, and respiratoryfailure may also follow, 4,5 whichrequire prompt, supportive therapy includingmechanical ventilation. 5,6 Botulismantitoxin, the only specific therapyavailable to ameliorate illness, can helpprevent progression of paralysis, reduceduration of illness, and decreasefatality rates. 7Supportive care and prompt administrationof antitoxin have reduced mortalityin the United States to less than10%, 8 and prompt identification of suspectfood vehicles during outbreaks hasprevented additional cases and reshapedour understanding of the epidemiologyof botulism. Global antitoxinsupplies are limited and antitoxinhas been unavailable for immediate usein several recent outbreaks (eg, Italy andEgypt). 9,10 In the United States, the Cen-(Julia), Direccion de Epidemiologia (Riva-Posse), PanAmerican Health Organization (Verdejo), Departamentode Bacteriologia, Instituto Nacional de Enfermedades Infecciosas,ANLIS Carlos G. Malbran (Farace and Rosetti),Hospital F. J. Muñiz (San Juan), Buenos Aires, Argentina.Corresponding Author: David L. Swerdlow, MD, Centersfor Disease Control and Prevention, 1600 Clifton Rd(MS A-38), Atlanta, GA 30333.Edited by Annette Flanagin, RN, MA, Associate SeniorEditor.1334 JAMA, April 14, 1999—Vol 281, No. 14 ©1999 American Medical Association. All rights reserved.Downloaded from jama.ama-assn.org at CDC-Information Center on December 28, 2011

LETTER FROM BUENOS AIRESters for Disease Control and Prevention(CDC) maintains surveillance ofbotulism cases and operates an antitoxinrelease system. This system dependson a centralized, 24-hour emergency-responsetelephone number forthe release of antitoxin throughout thecountry and is coordinated at federal,state, and local levels to identify suspectfood items and prevent additionalcases. The CDC manages a stockof antitoxin and distributes it for emergencyuse domestically and in membernations of the Pan-American HealthOrganization. 11Foodborne botulism most commonlyoccurs following the ingestionof improperly canned or preservedfoods that contain preformed toxin. 12,13For foodborne botulism to occur, Cbotulinum spores must be present in thefood and these spores must survive processing.The food or its packaging mustprovide an environment suitable forspores to germinate and produce toxin,and finally, persons must consume thefood without heating it to temperaturessufficient to destroy the heatlabileC botulinum toxin. 2An environment favorable to C botulinummay occur when foods are preservedby inexperienced persons, whenfaulty equipment is used, or when acontaminated product not intended forlong-term preservation is mishandledor packaged in a manner that permitsspores to germinate. New vacuumpackagingtechniques including sousvide and heat-shrinked plastic wraphave raised concern about the possibilityof botulism occurring from foodspackaged in these reduced oxygen environments2,14,15 ; however, few publisheddata on this risk exist.On January 13, 1998, an infectiousdiseases physician in a Buenos Aireshospital observed 2 men presentingwith ptosis, diplopia, dysphagia, andrespiratory difficulties and notified theDirectorate of Epidemiology of the ArgentineMinistry of Health about a possiblebotulism outbreak. Both men werebus drivers for the same company whodrove the same route and morning shift.Health officials identified 5 other driversfrom the same company and shiftwho also had neurologic signs consistentwith botulism. Initial reports suggestedthat all the drivers had eaten ata home located on the bus route wherethe drivers stopped during their breaks.Epidemiologists from the ArgentineMinistry of Health called the Foodborneand Diarrheal Diseases Branch,National Center for Infectious Diseases,at the CDC to report the outbreakand request botulism antitoxinto treat these patients and possibly othersexposed to an unknown contaminatedfood source. In this article, we reportthe outbreak investigation anddiscuss how the preparation, storage,and packaging of the implicated foodmay have permitted C botulinum sporesto germinate.In addition to investigating the outbreakand reviewing the epidemiologyof botulism in Argentina, the ArgentineMinistry of Health and the CDCused this opportunity to establish a localsystem for botulism surveillance andantitoxin distribution. The goals of thesystem are to reinforce surveillance, todeliver antitoxin to patients in Argentinamore rapidly and efficiently, andto serve as a model for other nations.METHODSCase Identification andCohort StudyTo identify cases, all employees of thebus company with the ill drivers werecontacted. Hospitals in the areas of BuenosAires where cases occurred andwhere a suspected food was producedwere asked to report any patients withacute neurologic illness that could bebotulism. Additionally, the outbreakwas reported by the local news media.We conducted a cohort study amongbus drivers who were ill and also thosewho were well who drove the morningshift of the bus route. On January18-19, 1998, we conducted face-tofaceinterviews and administered a writtenquestionnaire to the drivers. Weasked drivers about demographic characteristics,symptoms, and food exposuresduring the probable exposure period.We defined a confirmed case ofbotulism as a serum or stool sample thatdemonstrated botulinum toxin oryielded C botulinum from a bus driveron the morning shift who ate or drankat the home terminal stop betweenJanuary 3 and 7. Probable illness wasdefined as acute cranial nerve dysfunctionin this group of drivers during thisperiod. We excluded drivers from othershifts because none reported illness andthey did not eat at the terminal stop orshare any other common food exposureswith the morning shift drivers.Data were analyzed and relative riskswith Fisher exact P values and 95% confidenceintervals were calculated usingEpi Info version 6.04a (Centers forDisease Control and Prevention, Atlanta,Ga) and Exact Software (theNetherlands). 16 Values of P.05 and95% confidence intervals that did notinclude 1 were considered significant.Environmental InvestigationWe interviewed the family living in thehouse where the drivers ate, asked whatfoods and drinks were served, and inspectedthe food preparation and storagefacilities. We also inspected the supermarketwhere the foods werepurchased and the facility where a suspectedfood was produced.Microbiologic InvestigationSerum specimens were collected fromall patients between January 13 and 16,and stool specimens were obtained frompatients between January 18 and 20 forboth toxin and culture testing for Cbotulinum. Assays were conducted in thediagnostics and food laboratory forbotulism of the Instituto Nacional deEnfermedades Infecciosas, BuenosAires. Approximately 10 to 40 g of patients’feces with an equivalent volumeof diluent gelatin were ground insterile mortars. The solution reposed for12 to 18 hours at 4°C to allow any toxinpresent to transfer into the liquid medium.It was then centrifuged at 12 000rpm for 20 minutes.Toxicity and neutralization assayswere conducted in duplicate usingwhite mice weighing 18 to 20 g. Foreach mouse, 0.1 mL of monovalent an-©1999 American Medical Association. All rights reserved. JAMA, April 14, 1999—Vol 281, No. 14 1335Downloaded from jama.ama-assn.org at CDC-Information Center on December 28, 2011

LETTER FROM BUENOS AIRESThe market purchased matambresfrom a small-scale, commercial producerwho made matambres and processedhams at his home. To makematambre, the producer placed a slab ofraw beef (1- to 3-cm thick) on a stainlesssteel table. Ingredients included rawsliced carrots, hard-boiled eggs, salt, redpepper flakes, dried oregano, and commercialpotato flour. The meat was rolledup around the vegetables and eggs tomake an approximately 10- 30-cmcylinder. This meat roll was placed intoa rectangular stainless steel pan to keepingredients inside during cooking. Between10 and 15 matambres in individualsteel pans were immersed togetherinto water heated to 78°C to 80°C(never boiling), and cooked for approximately4 hours. After cooking, the waterwas drained and the producers reportedthey checked each matambre toensure an internal temperature of about68°C. The producer placed each warmmatambre in heat-shrinked plastic wrap,squeezed out the air, and sealed the plasticwith heat. The plastic-wrappedmatambres were allowed to cool, placedin a walk-in refrigerator, and were storedfor up to 2 weeks before being sold toeither supermarkets or directly to consumers.The producer reported makingmatambres every 2 weeks in batchesof 15 to 20 each time; the last batch producedbefore the outbreak was made inearly December. The producer was unableto provide receipts or a distributionlist with names of locations wherehis products were sold. He reported thatmost of his clients distributed his productsin the western greater Buenos Airesarea. After an inspection by local foodsafety officials, the facility was closed.Laboratory InvestigationThe mouse assay for botulism toxin presencewas performed with serum fromeach patient; 3 were positive for toxintype A. None of the stool cultures yieldedC botulinum. No implicated matambrewas available for testing.Table 2. Foods Consumed by Bus Drivers (n = 21) in Buenos Aires, Argentina,in January 1998*No./Total (%)Food Item Ate Food Did Not Eat FoodRelative Risk(95% Confidence Interval)PValueMatambre 9/11 (82) 0/10 (0) Undefined (4.37-) .01Bologna 1/1 (100) 8/20 (40) 2.50 (1.46-4.28) .43Mate 4/8 (50) 5/8 (63) 1.30 (0.49-3.45) .67Hot dog 1/2 (50) 8/19 (42) 1.19 (0.27-5.23) .99Salami 1/2 (50) 8/19 (42) 1.19 (0.27-5.23) .99Solid ham 2/5 (40) 7/16 (44) 0.86 (0.26-2.85) .99Processed ham 2/5 (40) 7/16 (44) 0.86 (0.26-2.85) .99*Matambre is the traditional meat roll in Argentina and mate is green tea.COMMENTWe reported an outbreak of botulismamong bus drivers in Buenos Aires, Argentina,caused by consumption ofmatambre, a food that has not been describedpreviously as a vehicle for botulism.A cohort study determined thatall ill persons ate slices of a singlematambre; no other foods were associatedwith illness. Type A toxin was identifiedfrom 3 of 9 patients’ serumsamples. Unfortunately, no implicatedmatambre was available for laboratoryanalysis.Although consumption of matambreis an established tradition in Argentina,it is usually consumed freshand is not generally intended for picklingor long-term preservation. Matambresproduced by licensed, commercialfacilities use nitrites, acidifiers, orother preservatives to prevent bacterialgrowth; the implicated matambrelacked these. Insufficient cooking,vacuum packaging in heat-shrinkedplastic wrap, and inadequate refrigerationmay have provided conditions forlive spores to germinate and producetoxin. To our knowledge, this is the firsttime heat-shrinked plastic wrap hasbeen linked to botulism, emphasizingconcern about the safety of this packagingmethod.The matambre that is believed to bethe cause of this outbreak was cookedat relatively low temperatures (78°C-80°C) over a time period (approximately240 minutes) too short to killall C botulinum spores. These spores aredifficult to destroy using conventionalcooking techniques; temperature survivalcurves have demonstrated C botulinumsurvival at 80°C for more than270 minutes. 17 In fact, a nonkilling heatshock and the lack of preservatives oracidifiers may enhance germination andtoxin elaboration by C botulinumspores. 2,13,18 To safely prepare foods intendedfor canning or long-term storage,the US Department of Agriculturerecommends that all low-acid foods(foods with pH 4.6, including redmeats, seafood, poultry, milk, and freshvegetables) be sterilized at temperaturesof 116°C to 121°C in pressure cannersoperated at 0.68 to 0.97 atm (10-15lb/in 2 ). At these temperatures, the timeneeded to destroy bacteria in low-acidcanned food ranges from 20 to 100 minutes.The exact time depends on thekind of food being canned, the way itis packed, and the amount of food beingcooked. The time needed to safelyprocess low-acid foods in boiling watercanners ranges from 7 to 11 hours. 14The time and temperatures used to cookthe matambre in this outbreak were insufficientto kill all botulism spores.Reduced oxygen packaging of foodscanincreasetheriskofcertainfoodborneillnesses if other safety barriers have notbeenapplied. 15,19 Althoughvacuumpackagingmay inhibit the growth of sometypes of bacteria in foods, several Clostridiumspecies can grow and producetoxininthisenvironment. 2,20-22 Toreducetheriskofbotulismfromfoodsinreducedoxygenpackaging,theUSFoodandDrugAdministrationrequiresdocumentedemployeetraininginplantsthatusereducedoxygenpackaging,stringentrefrigeration,specificlabelingwithstoragetemperatureinstructions and use-by dates, and plantapproval for reduced oxygen packagingof fish, soft cheeses, meats, and poultry. 15©1999 American Medical Association. All rights reserved. JAMA, April 14, 1999—Vol 281, No. 14 1337Downloaded from jama.ama-assn.org at CDC-Information Center on December 28, 2011

LETTER FROM BUENOS AIRESThematambreinthisoutbreakwaspackagedin a reduced oxygen environmentand lacked other safety barriers neededto prevent Clostridium spores from proliferating.Inadequate refrigeration also provideda favorable growth environmentfor C botulinum. The refrigerators (attemperatures between 9°C-10°C) usedto store the matambre at the terminalstop were not cold enough for safe storageof perishable foods. 18,23 The US Foodand Drug Administration recommendsthat refrigerator temperatures be5°C or colder to prevent the growth ofC botulinum in foods stored in reducedoxygen packaging. 15 Maintenanceof adequate storage temperaturesfor the matambre also was notdocumented by the producer or themarket where it was sold.The clinical characteristics of botulismamong patients in this outbreak differedin several respects from those inother reports. 1,3,4 Typically, most patientswith botulism develop severe muscularweakness and mild gastroenteritis.In this outbreak, the majority ofpatients experienced severe gastroenteritis,and only 1 patient developed severemuscular paralysis. In US cases oftype A botulism, the reported median incubationperiod was 1 day (range, 0-5days). 3 In the Argentine outbreak, the incubationperiod was longer; the mediantime between food exposure and onsetof neurologic symptoms onset was 5days (range, 0-10 days). Several reportedoutbreaks of botulism from Europehave described patients with primarilymild to moderate symptoms, butmost of these outbreaks have been causedby type B toxin. 24-26 It is not known whysome strains of C botulinum cause milderillness than others, although the numbersof spores present and amount oftoxin produced and ingested may influenceclinical manifestations. The severityof gastroenteritis experienced by thesepatients could have also occurred if thematambre had been contaminated byother bacteria or toxins.The outbreak investigation had severallimitations. All of the implicatedmatambre had been consumed and allremaining matambres from the supermarketwhere the implicated meat waspurchased were discarded before the investigationbegan. Although no matambreswere available for laboratory analysis,epidemiologic data and informationgained from the investigation implicatedthe product. Furthermore, receiptswere unavailable from the supermarketor the matambre producer todocument dates of purchase or exactdistribution of the product. However,no additional cases of type A botulismwere detected.The use of heat-shrinked plastic wrapand vacuum packaging for cookedfoods followed by inappropriate refrigerationmay provide an ideal environmentfor the growth of C botulinum, andthe safety of these packaging methodsshould be further investigated. Educationof food manufacturers and distributors,including the importance ofadequate cooking time and temperaturesto kill C botulinum spores, addingacidifiers or preservatives to foodsintended for prolonged shelf life and refrigeratingfoods properly, may helpprevent such outbreaks.Enhancing Surveillanceand Establishing an AntitoxinRelease SystemBotulism is an important public healthproblem in Argentina. Data maintainedby the Argentine Ministry of Health indicatethat during the years 1979-1997,277 cases of botulism were reported inArgentina (Ministry of Health, Republicof Argentina, unpublished data, 1998).Between 1987 and 1997, the CDC released54 vials of antitoxin to Argentina(CDC, unpublished data, 1998). In 1997,23 patients with suspected foodbornebotulism were reported in Argentina,about the same number of laboratoryconfirmedcases per year as in the UnitedStates, 27 which has a population approximately10 times that of Argentina. In addition,11 cases of culture-confirmed infantbotulism were reported in Argentinathat year. Only 1 case of wound botulismhas been described in Argentina. Of89 laboratory-confirmed cases reportedbetween 1991 and 1997, 83 (93%) wereidentified as toxin type A, 4 (5%) as toxintype E (all occurred in a single outbreak),and 2 (2%) as toxin type B (Ministryof Health, Republic of Argentina,unpublished data, 1998). In the UnitedStates, toxin types A, B, and E were identifiedin 60%, 30%, and 10% of cases, respectively.3,8,27Previous outbreaks in Argentina havebeen caused primarily through the consumptionof improperly preserved vegetablesand meats. Although C botulinumspores are ubiquitous, they arefound most frequently in soil samples.The level of Clostridium species contaminationon vegetables, particularlythose harvested directly from soil, isgenerally higher than that found inmeats 2 and may in part explain why preservedvegetables are more frequentlyimplicated.Because of the relatively high incidenceof botulism in Argentina, the Ministryof Health and the CDC collaboratedto establish, in January 1998, anantitoxin release and surveillance systemfor botulism in Argentina based onthe US program. The system componentsinclude (1) establishment of a localstock of antitoxin, (2) a mechanismfor antitoxin distribution within Argentina,(3) emergency notification and responsefor suspect cases, and (4) laboratoryconfirmation of suspect cases. Thecritical element that ensures both rapidresponse and effective surveillance is themaintenance of a centralized antitoxinsupply and a single emergency releasetelephone number. The system is brieflydescribed below.Antitoxin Supply. Botulism antitoxinwas supplied to Argentinathrough a modification of the existingagreement between Pan-AmericanHealth Organization and the CDC. Ultimately,the Argentine Ministry ofHealth may contract directly for botulismantitoxin from pharmaceuticalmanufacturers. Such a contract wouldguarantee annual supply of product andwould simplify maintenance of Argentina’santitoxin supply. The emergencystock is currently maintained bythe Ministry of Health.(Continued on page 1340.)1338 JAMA, April 14, 1999—Vol 281, No. 14 ©1999 American Medical Association. All rights reserved.Downloaded from jama.ama-assn.org at CDC-Information Center on December 28, 2011

LETTER FROM BUENOS AIRESAntitoxin Distribution. Patients withsuspected botulism are identified basedonclinicalsignsandsymptoms,foodhistory,and supportive data from ancillarydiagnostictesting.Reportingofcasesinitiatesthe process of antitoxin release. Torequest antitoxin, treating physicians orprovincial epidemiologists consult withan epidemiologist at the Directorate ofEpidemiology at the National Ministryof Health using a 24-hour emergencytelephone number. The epidemiologistfrom the Ministry of Health obtains informationfrom the treating physicianusing a botulism case report form, requestsa copy of the patient’s medicalchart,andrequests that diagnosticspecimensbe submitted to the laboratory.Consultationbetweentreatingphysiciansand the Ministry of Health epidemiologistmay assist in differentiating botulismcases from other illnesses, thus preventingunnecessary antitoxin administration.If the epidemiologist andtreating physician determine that botulismis a likely diagnosis, the epidemiologistarranges the release of one 10-mL vial of antitoxin for each patient.Emergency Notification and Response.To ensure investigation of potentialadditional cases of botulism, theepidemiologist at the Ministry of Healthwho receives a request for antitoxin notifiesprovincial health authorities bytelephone. Inspection of the patient’shome and/or investigation of suspectedfood vehicles are then initiated.The epidemiologist also alerts nationalfood safety authorities to assistwith commercial product recalls if necessaryor if the vehicle is unknown.Laboratory Confirmation. Ministryof Health epidemiologists will providephysicians and provincial epidemiologistswith information about specimencollection and will direct specimens toreference laboratories located in BuenosAires and Mendoza. These 2 laboratorieswill generate an annual summary ofspecimen testing, confirmation method,toxin type, and suspected food vehicle(if applicable). The Ministry of Healthepidemiologist also will record whetherantitoxinwasreleasedforthepatientandprovide additional information aboutsuspected foods and patient outcome.These data can then be reviewed by theMinistry of Health.Argentina’s System as a Modelfor Other NationsEstablishment of a system for antitoxinrelease and surveillance shouldimprove the management of botulismin Argentina. The system is based onthe US model, but tailored to the specificneeds of Argentina. It maintainsthe principle of centralized antitoxin releaseto improve the efficiency of emergencyreporting, allow rapid delivery ofantitoxin to patients, and enhance laboratoryconfirmation and surveillance forbotulism. The system also improves coordinationbetween public health authoritiesand food safety agencies to facilitateinvestigation of outbreaks andprevent additional cases, and it providesa mechanism to track changes inthe epidemiology of the disease.The adoption of this system by Argentinaserves as a model for other nations.Centralized antitoxin release,tightly linked to preventive measuresand surveillance, provides an effectivemechanism for managing this rare butdeadly disease. In addition, the creationof a cooperative, rapid-responsebotulism surveillance network may providea useful framework for a future surveillancesystem to monitor the emergenceof new and resurgent infectiousdiseases throughout the world.Acknowledgment: We thank Norma Binzstein, MS,Lorretta McCroskey, MT, and Silvina Arcieri for theircollaboration.REFERENCES1. Shapiro RL, Hatheway C, Swerdlow DL. Botulismin the United States. Ann Intern Med. 1998;129:221-228.2. Hauschild AHW. Epidemiology of human foodbornebotulism. In: Hauschild AHW, Dodds KL, eds.Clostridium Botulinum: Ecology and Control in Foods.New York, NY: Marcel Dekker Inc; 1993:69-104.3. Weber JT, Hatheway CL, St Louis ME. Botulism. In:Hoeprich PD, Jordan MC, eds. Infectious Diseases. Philadelphia,Pa: JB Lippincott; 1994:1185-1194.4. Woodruff BA, Griffin PM, McCroskey LM, et al.Clinical and laboratory comparison of botulism fromtoxin types A, B, and E in the United States, 1975-1988. J Infect Dis. 1992;166:1281-1286.5. Hughes J, Blumenthal JR, Merson MH, Lombard GL,Gangarosa EJ. Clinical features of types A and B foodbornebotulism. Ann Intern Med. 1981;95:422-425.6. Wilcox P, Andolfatto G, Fairbain MS, Pardy L. Longtermfollow-up of symptoms, pulmonary function, respiratorymuscle strength, and exercise performance afterbotulism. Am Rev Respir Dis. 1989;139:157-163.7. Tacket CO, Shandera WX, Mann JM, Hargrett NT,Blake PA. Equine antitoxin use and other factors thatpredict outcome in type A foodborne botulism. Am JMed. 1984;76:794-798.8. Centers for Disease Control and Prevention. Botulismin the United States, 1899-1996: Handbook forEpidemiologists, Clinicians, and Laboratory Workers.Atlanta, Ga: Centers for Disease Control; 1998.9. Aureli P, Franciosa G, Pourshaban M. Foodbornebotulism in Italy. Lancet. 1996;348:1594.10. Weber JT, Hibbs RG, Darwish A, et al. A massiveoutbreak of type E botulism associated with traditionalsalted fish in Cairo, Egypt. J Infect Dis. 1993;167:451-454.11. Shapiro R, Hatheway C, Becher J, Swerdlow D.Botulism surveillance and emergency response. JAMA.1997;278:433-435.12. St Louis ME. Botulism. In: Evans AS, BrachmanP, eds. Bacterial Infections of Humans: Epidemiologyand Control. 2nd ed. New York, NY: Plenum PublishingCorp; 1991:115-131.13. Hatheway CL. Clostridium botulinum. In: GorbachSL, Bartlett JG, Blacklow NR, eds. Infectious Diseases.2nd ed. Philadelphia, Pa: WB Saunders Co; 1998:1919-1925.14. US Department of Agriculture, Extension Service.Complete Guide to Home Canning. Washington,DC: US Dept of Agriculture Extension Service;1994. Agriculture Bulletin 539.15. US Food and Drug Administration. Food Code,1997. Washington, DC: US Dept of Health and HumanServices, Public Health Service, Food and DrugAdministration; 1997:365-407.16. Martin D, Austin H. Exact estimates for a rate ratio.Epidemiology. 1996;7:2933.17. Chilled Food Association. Guidelines for Good HygienicPractice in the Manufacture of Chilled Foods.3rd ed. Harrow, United Kingdom: Allstar Publishers;1997.18. Graham AF, Mason DR, Peck MW. Inhibitory effectof heat treatment, pH, and sodium chloride ongrowth from spores of nonproteolytic Clostridiumbotulinum at refrigeration temperature. Appl EnvironMicrobiol. 1996;62:2664-2668.19. DoyleM.Evaluatingthepotentialriskfromextendedshelf-life refrigerated foods from C. botulinum inoculationstudies. Food Technol. 1991;44:154-156.20. Juneja VK, Marmer BS. Growth of Clostridium perfringensfrom spore inocula in sous-vide turkey. Int JFood Microbiol. 1996;32:115-123.21. Broda DM, DeLacey KM, Bell RG, Penney N. Associationof psychotropic Clostridium spp. with deeptissue spoilage of chilled vacuum-packed lamb. Int JFood Microbiol. 1996;29:371-387.22. Broda DM, DeLacey KM, Bell RG, Braggins TJ,Cook RL. Psychrotropic Clostridium spp. associatedwith “blown pack” spoilage of chilled red meats anddog rolls in gas-impermeable plastic casings. Int J FoodMicrobiol. 1996;29:335-352.23. Conner DE. Potential Clostridium botulinum hazardsassociated with extended shelf-life refrigeratedfoods. J Food Safety. 1989;10:131-153.24. Robolot P, Robolot F, Fauchere JL, et al. Retrospectivestudy of 108 cases of botulism in Poitiers,France. J Med Microbiol. 1994;40:379-384.25. Troillet N, Praz G. Epidemie de botulisme de typeB: Sion, decembre 1993-janvier 1994. (ScweizerischeMedizinische Wochenschrift.) J Suisse Med.1995;125:1805-1812.26. Lecour H, Ramos H, Almeida B, Barbossa R. Foodbornebotulism: a review of 13 outbreaks. Arch InternMed. 1988;148:578-580.27. Centers for Disease Control and Prevention. Botulism(foodborne) by year, United States, 1975-1994.MMWR Morb Mortal Wkly Rep. 1995;43:22.1340 JAMA, April 14, 1999—Vol 281, No. 14 ©1999 American Medical Association. All rights reserved.Downloaded from jama.ama-assn.org at CDC-Information Center on December 28, 2011