SALMONELLA ENTERICA SEROTYPE PARATYPHI B

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SALMONELLA ENTERICA SEROTYPE PARATYPHI B VAR. JAVA GASTROENTERITIS OUTBREAK ASSOCIATED WITH UNPASTEURIZED TEMPEH NORTH CAROLINA, 2012 Nicole Lee, MPH North Carolina Division of Public Health InFORM Conference November 20, 2013

THE OUTBREAK March 30, 2012 8 cases of gastroenteritis Restaurant X, County A 5 Salmonella Paratyphi B var. Java No common food item No further cases County A X Restaurant

THE OUTBREAK April 24, 2012 10 additional cases Salmonella Paratyphi B var. Java County A 15 laboratory confirmed cases Identical pulsed field gel electrophoresis (PFGE) Outbreak strain

SALMONELLA SPECIES Second most common causative agents among foodborne outbreaks Leading cause of foodborne outbreak-related hospitalizations

SALMONELLA PARATYPHI B VAR. JAVA Gastroenteritis Fever Abdominal Pain Diarrhea Salmonella Paratyphi B Paratyphoid Fever Distinguished by ability to ferment tartrate Paratyphi B var. (L)+ tartrate +

OBJECTIVES Determine extent of outbreak Identify the source Implement control measures

METHODS AND RESULTS Case finding and hypothesis generation Identification of the vehicle Identification and trace-back of the source

CASE FINDING Active Surveillance Enhanced Passive Reporting Media Clinician memos Health alert networks

CASE DEFINITION Probable Gastroenteritis Epidemiologically linked to a confirmed case Confirmed Salmonella Paratyphi B var. Java Outbreak strain No time or geographic limits Novel PFGE pattern

LABORATORY METHODS Stool culture Salmonella serotyping PFGE

HYPOTHESIS GENERATION Patient interviews Salmonellosis Reporting Form Clinical Symptoms Travel History Food Water Animal

CASES BY DATE OF SYMPTOM ONSET (N=89) 8 April 26 Cases (no.) 7 6 5 4 3 2 1 0 Feb 29 May 8 March April May Date of Symptom Onset

CASE CHARACTERISTICS (N=89) No. % Confirmed 87 98 Probable 2 2 Female 45 51 Median age, years (range) 24 (4 74) -- Hospitalized 8 9 Died 0 0

CASE DISTRIBUTION 1 1 3 3 81

CLINICAL SYMPTOMS (N=89) Symptoms Frequency % Diarrhea 86/86 100 Abdominal Cramps 70/82 85 Fever 69/84 82 Vomiting 33/84 39 Bloody Diarrhea 30/82 37

COMMON EXPOSURES 93% reported travel or residency in County A No common food, water, animal exposures Restaurants X, Y, and Z Vegetarian cuisine County A X Y Z

NC DEPARTMENT OF AGRICULTURE AND CONSUMER SERVICES Presumptive positive Salmonella Tempeh Product Produced in County A

NC DEPARTMENT OF AGRICULTURE AND CONSUMER SERVICES Presumptive positive Salmonella Tempeh Product Produced in County A Brand A Tempeh

TEMPEH Soybeans, seeds, other legumes Fermented with mold to produce a firm cake Usually pasteurized Meat substitute (Image: Flickr member FotoosVanRobin licensed under Creative Commons)

IDENTIFICATION OF THE VEHICLE Meat substitutes not on standard reporting form Outbreak-specific questionnaire Food history Meat substitutes (tempeh, tofu) Restaurants in County A First 50 cases identified

RESTAURANT SITE VISITS Interviewed staff Observed food preparation Collected product invoices County A X Y Z

QUESTIONNAIRE RESULTS Complete interviews on 41/50 cases 82% response rate

COMMON FOODS (N=41) Food Item No. % Fresh Fruits 40 98 Fresh Vegetables 38 93 Eggs 32 78 Tofu 21 51 Tempeh 18 44 Veggie Burgers 10 24 Seitan 3 7 Textured Vegetable Protein 3 7

COMMON FOODS (N=41) Food Item No. % Fresh Fruits 40 98 Fresh Vegetables 38 93 Eggs 32 78 Tofu 21 51 Tempeh 18 44 Veggie Burgers 10 24 Seitan 3 7 Textured Vegetable Protein 3 7

OPPORTUNITIES FOR CROSS CONTAMINATION Uncooked tempeh prepared on cutting boards with ready to eat (RTE) foods Failure to perform hand hygiene after handling uncooked tempeh Bare hand contact with RTE foods

PRODUCT INVOICES Distributor X County A X Y Z

PRODUCT INVOICES Brand A Tempeh Distributor X County A X Y Z

PRODUCT INVOICES Brand A Tempeh Distributor X County A X Y Z

PRODUCT INVOICES Brand A Tempeh 35 restaurants Distributor X County A X Y Z

PRODUCT INVOICES Brand A Tempeh Distributor X Grocery Stores, Southeastern US County A X Y Z

BRAND A TEMPEH EXPOSURE Obtained list of distribution sites 100% cases eaten at a restaurant or venue serving Brand A Tempeh

BRAND A TEMPEH Operation since 2009 Shared kitchen in County A Not pasteurized

SHARED KITCHEN Interviewed staff Reviewed production methods Obtained food samples for testing

BRAND A TEMPEH STAFF 6 Staff Members No reported illnesses No international travel

Soybeans, Black Beans, Blackeyed Peas TEMPEH PRODUCTION

TEMPEH PRODUCTION Soybeans, Black Beans, Blackeyed Peas Vinegar

TEMPEH PRODUCTION Soybeans, Black Beans, Blackeyed Peas Vinegar Rhizopus

TEMPEH PRODUCTION Soybeans, Black Beans, Blackeyed Peas Vinegar Rhizopus Tempeh

TEMPEH PRODUCTION Soybeans, Black Beans, Blackeyed Peas Vinegar Rhizopus Tempeh Outbreak Strain

TEMPEH PRODUCTION Soybeans, Black Beans, Blackeyed Peas Negative Vinegar Rhizopus Tempeh Outbreak Strain

TEMPEH PRODUCTION Soybeans, Black Beans, Blackeyed Peas Vinegar Rhizopus Tempeh Negative Not tested Outbreak Strain

TEMPEH PRODUCTION Soybeans, Black Beans, Blackeyed Peas Vinegar Rhizopus Tempeh Negative Not tested Outbreak Strain Outbreak Strain

RHIZOPUS TRACE BACK Brand A Tempeh Distributor X Grocery Stores, SE United States County A X Y Z

RHIZOPUS TRACE BACK Online Vendor 2 Jan 2012 Brand A Tempeh Distributor X Grocery Stores, SE United States County A X Y Z

RHIZOPUS TRACE BACK Online Vendor 1 Online Vendor 2 Brand A Tempeh Distributor X Grocery Stores, SE United States County A X Y Z

RHIZOPUS TRACE BACK Online Vendor 1 Online Vendor 2 Brand A Tempeh Distributor X Domestic and International Distribution Grocery Stores, SE United States County A X Y Z

RHIZOPUS TRACE BACK Indonesia Online Vendor 1 Online Vendor 2 Brand A Tempeh Distributor X Domestic and International Distribution Grocery Stores, SE United States County A X Y Z

CONCLUSIONS Rhizopus culture was the source Brand A Tempeh was the vehicle Transmission occurred Direct consumption Cross-contamination of RTE foods

LIMITATIONS Targeted first 50 cases for re-interview Incomplete case finding

RAW TEMPEH Fungal growth encouraged Favorable conditions for pathogens Unpasteurized No opportunity to reduce pathogenic load

RECOMMENDATIONS Designated cutting boards Separation from RTE foods Frequent hand hygiene

PUBLIC HEALTH ACTIONS Rhizopus culture recalled Brand A Tempeh recalled Education on proper handling of uncooked, unpasteurized tempeh Consider pasteurization

ACKNOWLEDGMENTS Buncombe County Health Department Gibbie Harris, Jennifer Mullendore Ellis Vaughan, Sue Ellen Morrison Susan Creede, David Mease, Marc Fowler, Gaylen Ehrlichman *Coauthors listed in red. North Carolina Department of Agriculture and Consumer Services Joan Sims, Janna Spruill, Jim Melvin, Dan Ragan North Carolina Division of Public Health Megan Davies Denise Griffin Debra Springer Jean-Marie Maillard Zack Moore Anita Valiani David Sweat Nicole Lee Leslie Wolf Samuel Merritt Evelyn Foust CDC/OSELS/SEPDPO/EFAB Edward Weiss CDC/OID/NCEZID Thai-An Nguyen Stacey Bosch Matt Mikoleit Anna Newton Brendan Jackson CDC NC DPH Aaron Fleischauer Jennifer MacFarquhar Office of Surveillance, Epidemiology, and Laboratory Services Scientific Education and Professional Development Program Office

Thank you