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In May 2014, a cluster of (YE) O9 infections was reported from a military base in northern Norway. Concurrently, an increase in YE infections in civilians was observed in the Norwegian Surveillance System for Communicable Diseases. We investigated to ascertain the extent of the outbreak and identify the source in order to implement control measures. A case was defined as a person with laboratory-confirmed YE O9 infection with the outbreak multilocus variable-number tandem repeat analysis (MLVA)-profile (5-6-9-8-9-9). We conducted a case–control study in the military setting and calculated odds ratios (OR) using logistic regression. Traceback investigations were conducted to identify common suppliers and products in commercial kitchens frequented by cases. By 28 May, we identified 133 cases, of which 117 were linked to four military bases and 16 were civilians from geographically dispersed counties. Among foods consumed by cases, multivariable analysis pointed to mixed salad as a potential source of illness (OR 10.26; 95% confidence interval (CI): 0.85–123.57). The four military bases and cafeterias visited by 14/16 civilian cases received iceberg lettuce or radicchio rosso from the same supplier. Secondary transmission cannot be eliminated as a source of infection in the military camps. The most likely source of the outbreak was salad mix containing imported radicchio rosso, due to its long shelf life. This outbreak is a reminder that fresh produce should not be discounted as a vehicle in prolonged outbreaks and that improvements are still required in the production and processing of fresh salad products.


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  1. Norwegian Institute of Public Health (NIPH). Outbreaks of infectious diseases in Norway. Annual report 2013. [Utbrudd av smittsomme sykdommer i Norge. Årsrapport 2013]. Oslo: NPIH; 2014.
  2. Norwegian Scientific Committee for Food Safety. Panel on Biological Hazards. A preliminary risk assessment of Yersinia enterocolitica in the food chain: some aspects related to human health in Norway. 04/103. [Accessed 5 May 2011]. Available from: http://www.vkm.no/dav/d165b9d426.pdf
  3. Naktin J, Beavis KG. Yersinia enterocolitica and Yersinia pseudotuberculosis. Clin Lab Med. 1999;19(3):523-36, vi. PMID: 10549424 
  4. Rosner BM, Werber D, Höhle M, Stark K. Clinical aspects and self-reported symptoms of sequelae of Yersinia enterocolitica infections in a population-based study, Germany 2009-2010. BMC Infect Dis. 2013;13(1):236.  https://doi.org/10.1186/1471-2334-13-236  PMID: 23701958 
  5. Huovinen E, Sihvonen LM, Virtanen MJ, Haukka K, Siitonen A, Kuusi M. Symptoms and sources of Yersinia enterocolitica-infection: a case-control study. BMC Infect Dis. 2010;10(1):122.  https://doi.org/10.1186/1471-2334-10-122  PMID: 20487529 
  6. Rosner BM, Stark K, Höhle M, Werber D. Risk factors for sporadic Yersinia enterocolitica infections, Germany 2009-2010. Epidemiol Infect. 2012;140(10):1738-47.  https://doi.org/10.1017/S0950268811002664  PMID: 22313798 
  7. Satterthwaite P, Pritchard K, Floyd D, Law B. A case-control study of Yersinia enterocolitica infections in Auckland. Aust N Z J Public Health. 1999;23(5):482-5.  https://doi.org/10.1111/j.1467-842X.1999.tb01303.x  PMID: 10575769 
  8. Ostroff SM, Kapperud G, Hutwagner LC, Nesbakken T, Bean NH, Lassen J, et al. Sources of sporadic Yersinia enterocolitica infections in Norway: a prospective case-control study. Epidemiol Infect. 1994;112(1):133-41.  https://doi.org/10.1017/S0950268800057496  PMID: 8119353 
  9. Boqvist S, Pettersson H, Svensson A, Andersson Y. Sources of sporadic Yersinia enterocolitica infection in children in Sweden, 2004: a case-control study. Epidemiol Infect. 2009;137(6):897-905.  https://doi.org/10.1017/S0950268808001209  PMID: 18789174 
  10. Grahek-Ogden D, Schimmer B, Cudjoe KS, Nygård K, Kapperud G. Outbreak of Yersinia enterocolitica serogroup O:9 infection and processed pork, Norway. Emerg Infect Dis. 2007;13(5):754-6.  https://doi.org/10.3201/eid1305.061062  PMID: 17553258 
  11. MacDonald E, Heier BT, Nygård K, Stalheim T, Cudjoe KS, Skjerdal T, et al. Yersinia enterocolitica outbreak associated with ready-to-eat salad mix, Norway, 2011. Emerg Infect Dis. 2012;18(9):1496-9.  https://doi.org/10.3201/eid1809.120087  PMID: 22932318 
  12. European Centre for Disease Prevention and Control (ECDC). Annual epidemiological report 2014 - Food- and waterborne diseases and zoonoses. Stockholm: ECDC; 2014.
  13. Morse DL, Shayegani M, Gallo RJ. Epidemiologic investigation of a Yersinia camp outbreak linked to a food handler. Am J Public Health. 1984;74(6):589-92.  https://doi.org/10.2105/AJPH.74.6.589  PMID: 6721015 
  14. Gierczyński R, Golubov A, Neubauer H, Pham JN, Rakin A. Development of multiple-locus variable-number tandem-repeat analysis for Yersinia enterocolitica subsp. palearctica and its application to bioserogroup 4/O3 subtyping. J Clin Microbiol. 2007;45(8):2508-15.  https://doi.org/10.1128/JCM.02252-06  PMID: 17553973 
  15. International Organization for Standardization (ISO). Microbiology of food and animal feeding stuffs – Horizontal method for the detection of presumptive pathogenic Yersinia enterocolitica. ISO 10273. 2nd Edition. Geneva: ISO; 2003.
  16. Nordic Committee on Food Analysis (NMKL). Yersinia enterocolitica. Detection in foods. NMKL no. 117, 3rd ed. NMKL; 1996.
  17. Nordic Committee on Food Analysis (NMKL). Pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis – real time PCR methods for detection in food, feed and environmental samples. NMKL no. 117, 2nd ed. NMKL; 2013.
  18. Thompson K. Controlled Atmosphere Storage of Fruits and Vegetables. 2nd Edition. CAB International, Oxfordshire, UK; 2010, pp. 179.
  19. Kangas S, Takkinen J, Hakkinen M, Nakari UM, Johansson T, Henttonen H, et al. Yersinia pseudotuberculosis O:1 traced to raw carrots, Finland. Emerg Infect Dis. 2008;14(12):1959-61.  https://doi.org/10.3201/eid1412.080284  PMID: 19046537 
  20. Jalava K, Hakkinen M, Valkonen M, Nakari UM, Palo T, Hallanvuo S, et al. An outbreak of gastrointestinal illness and erythema nodosum from grated carrots contaminated with Yersinia pseudotuberculosis. J Infect Dis. 2006;194(9):1209-16.  https://doi.org/10.1086/508191  PMID: 17041846 
  21. Rimhanen-Finne R, Niskanen T, Hallanvuo S, Makary P, Haukka K, Pajunen S, et al. Yersinia pseudotuberculosis causing a large outbreak associated with carrots in Finland, 2006. Epidemiol Infect. 2009;137(3):342-7.  https://doi.org/10.1017/S0950268807000155  PMID: 18177523 
  22. Grotto I, Huerta M, Balicer RD, Halperin T, Cohen D, Orr N, et al. An outbreak of norovirus gastroenteritis on an Israeli military base. Infection. 2004;32(6):339-43.  https://doi.org/10.1007/s15010-004-4002-3  PMID: 15597223 
  23. Jelastopulu E, Venieri D, Komninou G, Kolokotronis T, Constantinidis TC, Bantias C. Outbreak of acute gastroenteritis in an air force base in Western Greece. BMC Public Health. 2006;6(1):254.  https://doi.org/10.1186/1471-2458-6-254  PMID: 17044937 
  24. Lee VJ, Ong AE, Auw M. An outbreak of Salmonella gastrointestinal illness in a military camp. Ann Acad Med Singapore. 2009;38(3):207-11. PMID: 19347073 
  25. Wadl M, Scherer K, Nielsen S, Diedrich S, Ellerbroek L, Frank C, et al. Food-borne norovirus-outbreak at a military base, Germany, 2009. BMC Infect Dis. 2010;10(1):30.  https://doi.org/10.1186/1471-2334-10-30  PMID: 20163705 
  26. Mayet A, Andreo V, Bedubourg G, Victorion S, Plantec J, Soullie B, et al. Food-borne outbreak of norovirus infection in a French military parachuting unit, April 2011. Euro Surveill. 2011;16(30):19930. PMID: 21813082 
  27. Yap J, Qadir A, Liu I, Loh J, Tan BH, Lee VJ. Outbreak of acute norovirus gastroenteritis in a military facility in Singapore: a public health perspective. Singapore Med J. 2012;53(4):249-54. PMID: 22511047 
  28. Lindholm H, Visakorpi R. Late complications after a Yersinia enterocolitica epidemic: a follow up study. Ann Rheum Dis. 1991;50(10):694-6.  https://doi.org/10.1136/ard.50.10.694  PMID: 1958092 
  29. Tuck JJ, Williams JR, Doyle AL. Gastro Enteritis in a military population deployed in West Africa in the UK Ebola response; was the observed lower disease burden due to handwashing? Travel Med Infect Dis. 2016;14(2):131-6.  https://doi.org/10.1016/j.tmaid.2015.12.009  PMID: 26827135 
  30. Ratnam S, Mercer E, Picco B, Parsons S, Butler R. A nosocomial outbreak of diarrheal disease due to Yersinia enterocolitica serotype 0:5, biotype 1. J Infect Dis. 1982;145(2):242-7.  https://doi.org/10.1093/infdis/145.2.242  PMID: 7054326 
  31. Schmitz AT, Tauxe RV. Yersinia enterocolitica Infections. In: Brachman PS, Abrutyn E, editors. Bacterial Infections of Humans. 4th ed. New York: Springer; 2009.
  32. Ethelberg S, Olsen KE, Gerner-Smidt P, Mølbak K. Household outbreaks among culture-confirmed cases of bacterial gastrointestinal disease. Am J Epidemiol. 2004;159(4):406-12.  https://doi.org/10.1093/aje/kwh049  PMID: 14769645 

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