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Multistate outbreak of Salmonella serotype Typhimurium infections associated with consumption of restaurant tomatoes, USA, 2006: hypothesis generation through case exposures in multiple restaurant clusters

  • C. BARTON BEHRAVESH (a1) (a2), D. BLANEY (a2) (a3), C. MEDUS (a4), S. A. BIDOL (a5), Q. PHAN (a6), S. SOLIVA (a7), E. R. DALY (a3), K. SMITH (a4), B. MILLER (a8), T. TAYLOR (a9), T. NGUYEN (a1), C. PERRY (a1), T. A. HILL (a10), N. FOGG (a10), A. KLEIZA (a11), D. MOORHEAD (a11), S. AL-KHALDI (a10), C. BRADEN (a1) and M. F. LYNCH (a1)...

Multiple salmonellosis outbreaks have been linked to contaminated tomatoes. We investigated a multistate outbreak of Salmonella Typhimurium infections among 190 cases. For hypothesis generation, review of patients' food histories from four restaurant-associated clusters in four states revealed that large tomatoes were the only common food consumed by patients. Two case-control studies were conducted to identify food exposures associated with infections. In a study conducted in nine states illness was significantly associated with eating raw, large, round tomatoes in a restaurant [matched odds ratio (mOR) 3·1, 95% confidence interval (CI) 1·3–7·3]. In a Minnesota study, illness was associated with tomatoes eaten at a restaurant (OR 6·3, mid-P 95% CI 1·05–50·4, P=0·046). State, local and federal regulatory officials traced the source of tomatoes to Ohio tomato fields, a growing area not previously identified in past tomato-associated outbreaks. Because tomatoes are commonly eaten raw, prevention of tomato contamination should include interventions on the farm, during packing, and at restaurants.

Corresponding author
*Author for correspondence: C. Barton Behravesh, MS, DVM, DrPH, Centers for Disease Control and Prevention, National Center for Emerging and Zoonotic Infectious Diseases, Division of Foodborne, Waterborne, and Environmental Diseases, Outbreak Response and Prevention Branch, 1600 Clifton Road NE, Mail-Stop A-38, Atlanta, GA 30333, USA. (Email:
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1. ScallanE, et al. Foodborne illness acquired in the United States – major pathogens. Emerging Infectious Diseases 2011; 17: 7–15.
2. Centers for Disease Control and Prevention. Salmonella surveillance: annual summary, 2006. Atlanta, GA: U.S. Department of Health and Human Services, CDC, 2008.
3. Centers for Disease Control and Prevention. Multistate outbreak of Salmonella Typhimurium infections associated with eating ground beef – United States, 2004. Morbidity and Mortality Weekly Report 2006; 55: 180182.
4. Centers for Disease Control and Prevention. Salmonella Typhimurium infection associated with raw milk and cheese consumption – Pennsylvania, 2007. Morbidity and Mortality Weekly Report 2007; 56: 11611164.
5. FullerCC, et al. A multi-state Salmonella Typhimurium outbreak associated with frozen vacuum-packed rodents used to feed snakes. Zoonoses and Public Health 2008; 55: 481487.
6. SwansonSJ, et al. Multidrug-resistant Salmonella enterica serotype Typhimurium associated with pet rodents. New England Journal of Medicine 2007; 356: 2128.
7. Centers for Disease Control and Prevention. Compendium of measures to prevent disease associated with animals in public settings, 2009: National Association of State Public Health Veterinarians, Inc. (NASPHV). Morbidity and Mortality Weekly Report 2009; 58: 121.
8. LynchML, et al. Surveillance for foodborne-disease outbreaks – United States, 1998–2002. Morbidity and Mortality Weekly Report (Surveillance Summaries) 2006; 55: 142.
9. HorbyPW, et al. A national outbreak of multi-resistant Salmonella enterica serovar Typhimurium definitive phage type (DT) 104 associated with consumption of lettuce. Epidemiology and Infection 2003; 130: 169178.
10. BrooksJT, et al. Salmonella Typhimurium infections transmitted by chlorine-pretreated clover sprout seeds. American Journal of Epidemiology 2001; 154: 10201028.
11. Centers for Disease Control and Prevention. Multistate outbreaks of Salmonella infections associated with raw tomatoes eaten in restaurants – United States, 2005–2006. Morbidity and Mortality Weekly Report 2007; 56: 909911.
12. GreeneSK, et al. Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated fields, 2005. Epidemiology and Infection 2008; 136: 157165.
13. Centers for Disease Control and Prevention. Outbreaks of Salmonella infections associated with eating Roma tomatoes – United States and Canada, 2004. Morbidity and Mortality Weekly Report 2005; 54: 325328.
14. GuptaSK, et al. Outbreak of Salmonella Braenderup infections associated with Roma tomatoes, northeastern United States, 2004: a useful method for subtyping exposures in field investigations. Epidemiology and Infection 2007; 135: 11651173.
15. CummingsK, et al. A multistate outbreak of Salmonella enterica serotype Baildon associated with domestic raw tomatoes. Emerging Infectious Diseases 2001; 7: 10461048.
16. VollsetSE, et al. Evaluation of exact and asymptotic interval estimators in logistic analysis of matched case-control studies. Biometrics 1991; 47: 13111325.
17. SwaminathanB, et al. Surveillance for human Salmonella infections in the United States. Journal of AOAC International 2006; 89: 553–539.
18. Centers for Disease Control and Prevention. NARMS: human isolates final report, 2007. Atlanta, GA: U.S. Department of Health and Human Services, CDC, 2009.
19. VoetschAC, et al. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections infections in the United States. Clinical Infectious Diseases 2004; 38: S127S34.
20. MahonBE, et al. An international outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds. Journal of Infectious Diseases 1997; 175: 876882.
21. HedbergCW, et al. Outbreaks of salmonellosis associated with eating uncooked tomatoes: implications for public health. Epidemiology and Infection 1999; 122: 385393.
22. SandtCH, et al. The key role of pulsed-field gel electrophoresis in investigation of a large multiserotype and multistate food-borne outbreak of Salmonella infections centered in Pennsylvania. Journal of Clinical Microbiology 2006; 44: 32083212.
23. KretsingerK.Trip Report Epi-Aid #2003–12: Investigation of multi-state outbreak of Salmonella Newport infections in Pennsylvania and Virginia, September–October 2002. Centers for Disease Control and Prevention. Atlanta, GA, 2003.
24. YuanJK, et al. Multicounty Salmonella enteritidis outbreak caused by tomatoes: rapid detection of cases by using multiple-locus variable-number tandem repeat analysis. In: 55th Annual Epidemic Intelligence Service Conference, Atlanta, GA, 2006, p. 85.
25. GuoX, et al. Survival of salmonellae on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening. Applied and Environmental Microbiology 2001; 67: 47604764.
26. LinC. Transfer of Salmonella Montevideo onto the interior surfaces of tomatoes by cutting. Journal of Food Protection 1997; 60: 858–8562.
27. KirklandE, et al. Tomato-Handling Practices in Restaurants. Journal of Food Protection 2009; 72: 16921698.
28. U.S. Food and Drug Administration. 2005 Food Code. College Park, MD: US Department of Health and Human Services, Food and Drug Administration, 2005 (
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Epidemiology & Infection
  • ISSN: 0950-2688
  • EISSN: 1469-4409
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