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Abstract

During October and November 2016, over 1,000 customers and staff reported gastroenteritis after eating at all 23 branches of a restaurant group in the United Kingdom. The outbreak coincided with a new menu launch and norovirus was identified as the causative agent. We conducted four retrospective cohort studies; one among all restaurant staff and three in customers at four branches. We investigated the dishes consumed, reviewed recipes, interviewed chefs and inspected restaurants to identify common ingredients and preparation methods for implicated dishes. Investigations were complicated by three public health agencies concurrently conducting multiple analytical studies, the complex menu with many shared constituent ingredients and the high media attention. The likely source was a contaminated batch of a nationally distributed ingredient, but analytical studies were unable to implicate a single ingredient. The most likely vehicle was a new chipotle chilli product imported from outside the European Union, that was used uncooked in the implicated dishes. This outbreak exemplifies the possibility of rapid spread of infectious agents within a restaurant supply chain, following introduction of a contaminated ingredient. It underlines the importance of appropriate risk assessments and control measures being in place, particularly for new ingredients and ready-to-eat foods.

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/content/10.2807/1560-7917.ES.2019.24.18.1800511
2019-05-02
2019-05-26
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2019.24.18.1800511
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References

  1. Mattison K. Norovirus as a foodborne disease hazard. Adv Food Nutr Res. 2011;62:1-39.  https://doi.org/10.1016/B978-0-12-385989-1.00001-6  PMID: 21504820 
  2. Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P, Parashar UD, et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis. 2014;14(8):725-30.  https://doi.org/10.1016/S1473-3099(14)70767-4  PMID: 24981041 
  3. Tam CC, Rodrigues LC, Viviani L, Dodds JP, Evans MR, Hunter PR, et al. IID2 Study Executive Committee. Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut. 2012;61(1):69-77.  https://doi.org/10.1136/gut.2011.238386  PMID: 21708822 
  4. Kroneman A, Verhoef L, Harris J, Vennema H, Duizer E, van Duynhoven Y, et al. Analysis of integrated virological and epidemiological reports of norovirus outbreaks collected within the Foodborne Viruses in Europe network from 1 July 2001 to 30 June 2006. J Clin Microbiol. 2008;46(9):2959-65.  https://doi.org/10.1128/JCM.00499-08  PMID: 18650354 
  5. Tam CC, O’Brien SJ. Economic Cost of Campylobacter, Norovirus and Rotavirus Disease in the United Kingdom. PLoS One. 2016;11(2):e0138526.  https://doi.org/10.1371/journal.pone.0138526  PMID: 26828435 
  6. Bartsch SM, Asti L, Nyathi S, Spiker ML, Lee BY. Estimated Cost to a Restaurant of a Foodborne Illness Outbreak. Public Health Rep. 2018;133(3):274-86.  https://doi.org/10.1177/0033354917751129  PMID: 29656701 
  7. Sandmann FG, Shallcross L, Adams N, Allen DJ, Coen PG, Jeanes A, et al. Estimating the Hospital Burden of Norovirus-Associated Gastroenteritis in England and Its Opportunity Costs for Nonadmitted Patients. Clin Infect Dis. 2018;67(5):693-700.  https://doi.org/10.1093/cid/ciy167  PMID: 29529135 
  8. Bitler EJ, Matthews JE, Dickey BW, Eisenberg JN, Leon JS. Norovirus outbreaks: a systematic review of commonly implicated transmission routes and vehicles. Epidemiol Infect. 2013;141(8):1563-71.  https://doi.org/10.1017/S095026881300006X  PMID: 23433247 
  9. Smith AJ, McCarthy N, Saldana L, Ihekweazu C, McPhedran K, Adak GK, et al. A large foodborne outbreak of norovirus in diners at a restaurant in England between January and February 2009. Epidemiol Infect. 2012;140(9):1695-701.  https://doi.org/10.1017/S0950268811002305  PMID: 22129511 
  10. Le Mennec C, Parnaudeau S, Rumebe M, Le Saux JC, Piquet JC, Le Guyader SF. Follow-Up of Norovirus Contamination in an Oyster Production Area Linked to Repeated Outbreaks. Food Environ Virol. 2017;9(1):54-61.  https://doi.org/10.1007/s12560-016-9260-6  PMID: 27613529 
  11. Chatziprodromidou IP, Bellou M, Vantarakis G, Vantarakis A. Viral outbreaks linked to fresh produce consumption: a systematic review. J Appl Microbiol. 2018;124(4):932-42.  https://doi.org/10.1111/jam.13747  PMID: 29485236 
  12. Kendall ME, Mody RK, Mahon BE, Doyle MP, Herman KM, Tauxe RV. Emergence of salsa and guacamole as frequent vehicles of foodborne disease outbreaks in the United States, 1973-2008. Foodborne Pathog Dis. 2013;10(4):316-22.  https://doi.org/10.1089/fpd.2012.1328  PMID: 23461608 
  13. Einöder-Moreno M, Lange H, Grepp M, Osborg E, Vainio K, Vold L. Non-heat-treated frozen raspberries the most likely vehicle of a norovirus outbreak in Oslo, Norway, November 2013. Epidemiol Infect. 2016;144(13):2765-72.  https://doi.org/10.1017/S0950268816000194  PMID: 26878755 
  14. Mäde D, Trübner K, Neubert E, Höhne M, Johne R. Detection and Typing of Norovirus from Frozen Strawberries Involved in a Large-Scale Gastroenteritis Outbreak in Germany. Food Environ Virol. 2013;5(3):162-8.  https://doi.org/10.1007/s12560-013-9118-0  PMID: 23888384 
  15. Smith KC, Inns T, Decraene V, Fox A, Allen DJ, Shah A. An outbreak of norovirus GI-6 infection following a wedding in North West England. Epidemiol Infect. 2017;145(6):1239-45.  https://doi.org/10.1017/S0950268816003368  PMID: 28132650 
  16. Somura Y, Mizukoshi F, Nagasawa K, Kimoto K, Oda M, Shinkai T, et al. A Food Poisoning Outbreak Due to Food Handler-Associated Contamination with the Human Norovirus GII.P16-GII.2 Variant Strain in Italian Cuisine in Tokyo during the 2016/17 Winter Season. Jpn J Infect Dis. 2018;71(2):172-3.  https://doi.org/10.7883/yoken.JJID.2017.264  PMID: 29491240 
  17. Lin YC, Hipfl E, Lederer I, Allerberger F, Schmid D. A norovirus GII.P21 outbreak in a boarding school, Austria 2014. Int J Infect Dis. 2015;37:25-9.  https://doi.org/10.1016/j.ijid.2015.05.021  PMID: 26073003 
  18. Coutts SP, Sturge K, Lalor K, Marshall JA, Bruggink LD, Subasinghe N, et al. An outbreak of foodborne norovirus gastroenteritis linked to a restaurant in Melbourne, Australia, 2014. Western Pac Surveill Response J. 2017;8(2):12-6.  https://doi.org/10.5365/wpsar.2017.8.1.008  PMID: 28729921 
  19. Angelo KM, Nisler AL, Hall AJ, Brown LG, Gould LH. Epidemiology of restaurant-associated foodborne disease outbreaks, United States, 1998-2013. Epidemiol Infect. 2017;145(3):523-34. PMID: 27751201 
  20. Health Protection Agency (HPA). Guidelines for Assessing the Microbiological Safety of Ready-to-Eat Foods Placed on the Market. London: HPA; 2009. Available from: https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/363146/Guidelines_for_assessing_the_microbiological_safety_of_ready-to-eat_foods_on_the_market.pdf
  21. Food and Environment Research Agency (FERA). A critical review on the survival and elimination of norovirus in food and on food contact surfaces. London: FERA; 2015. Available from: https://www.food.gov.uk/sites/default/files/media/document/FS101120%20NoV%20critical%20review%20report%20-%20FINAL%203%20June%202015.pdf
  22. Velebit B, Radin D, Teodorovic V. Transmission of Common Foodborne Viruses by Meat Products. Procedia Food Sci. 2015;5:304-7.  https://doi.org/10.1016/j.profoo.2015.09.069 
  23. Malek M, Barzilay E, Kramer A, Camp B, Jaykus LA, Escudero-Abarca B, et al. Outbreak of norovirus infection among river rafters associated with packaged delicatessen meat, Grand Canyon, 2005. Clin Infect Dis. 2009;48(1):31-7.  https://doi.org/10.1086/594118  PMID: 19025489 
  24. Sodha SV, Lynch M, Wannemuehler K, Leeper M, Malavet M, Schaffzin J, et al. Multistate outbreak of Escherichia coli O157:H7 infections associated with a national fast-food chain, 2006: a study incorporating epidemiological and food source traceback results. Epidemiol Infect. 2011;139(2):309-16.  https://doi.org/10.1017/S0950268810000920  PMID: 20429971 
  25. Buss BF, Joshi MV, O’Keefe AL, Allensworth CD, Garvey A, Obbink K, et al. Regional investigation of a cyclosporiasis outbreak linked to imported romaine lettuce - Nebraska and Iowa, June-August 2013. Epidemiol Infect. 2016;144(9):1807-17.  https://doi.org/10.1017/S0950268815002484  PMID: 26489789 
  26. Waldram A, Lawler J, Jenkins C, Collins J, Payne M, Aird H, et al. Large outbreak of multiple gastrointestinal pathogens associated with fresh curry leaves in North East England, 2013. Epidemiol Infect. 2018;146(15):1940-7.  https://doi.org/10.1017/S095026881800225X  PMID: 30109832 
  27. Mody RK, Greene SA, Gaul L, Sever A, Pichette S, Zambrana I, et al. National outbreak of Salmonella serotype saintpaul infections: importance of Texas restaurant investigations in implicating jalapeño peppers. PLoS One. 2011;6(2):e16579.  https://doi.org/10.1371/journal.pone.0016579  PMID: 21373185 
  28. Kimura AC, Palumbo MS, Meyers H, Abbott S, Rodriguez R, Werner SB. A multi-state outbreak of Salmonella serotype Thompson infection from commercially distributed bread contaminated by an ill food handler. Epidemiol Infect. 2005;133(5):823-8.  https://doi.org/10.1017/S0950268805004127  PMID: 16181501 
  29. Shiferaw B, Verrill L, Booth H, Zansky SM, Norton DM, Crim S, et al. Sex-based differences in food consumption: Foodborne Diseases Active Surveillance Network (FoodNet) Population Survey, 2006-2007. Clin Infect Dis. 2012;54(Suppl 5):S453-7.  https://doi.org/10.1093/cid/cis247  PMID: 22572669 
  30. Jackson LA, Keene WE, McAnulty JM, Alexander ER, Diermayer M, Davis MA, et al. Where’s the beef? The role of cross-contamination in 4 chain restaurant-associated outbreaks of Escherichia coli O157:H7 in the Pacific Northwest. Arch Intern Med. 2000;160(15):2380-5.  https://doi.org/10.1001/archinte.160.15.2380  PMID: 10927738 
  31. Patel MK, Chen S, Pringle J, Russo E, Viñaras J, Weiss J, et al. A prolonged outbreak of Salmonella Montevideo infections associated with multiple locations of a restaurant chain in Phoenix, Arizona, 2008. J Food Prot. 2010;73(10):1858-63.  https://doi.org/10.4315/0362-028X-73.10.1858  PMID: 21067674 
  32. Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C, Wilking H, et al. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med. 2011;365(19):1763-70.  https://doi.org/10.1056/NEJMoa1106482  PMID: 22029753 
  33. Marquez DFP, Hawkins G, Kirolos A, Sedgwick J, Smith-Palmer A, Stevenson J, Waugh C, Williams CJ. Estimation of the size of a norovirus outbreak in restaurant customers using capture recapture methodology – Edinburgh 2016. ESCAIDE 2017, Stockholm, Sweden. Poster A7.6.
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