- Mari Morgan1,2,3, Vicky Watts3,4,5, David Allen6,7,8, Daniele Curtis9, Amir Kirolos10, Neil Macdonald9, Ellie Maslen11, Deb Morgan12, Ayoub Saei13, James Sedgwick9, Janet Stevenson10, Deborah Turbitt14, Roberto Vivancos5, Catriona Waugh10, Chris Williams1, Valerie Decraene5
-
View Affiliations Hide AffiliationsAffiliations: 1 Health Protection, Public Health Wales NHS Trust, Cardiff, United Kingdom 2 European Programme for Intervention Epidemiology Training, Stockholm, Sweden 3 These authors share first authorship 4 United Kingdom Field Epidemiology Training Programme, Public Health England, London, United Kingdom 5 Field Service - Epidemiology, National Infection Service, Public Health England, Liverpool, United Kingdom 6 Virus Reference Department, National Infection Service, Colindale, Public Health England, London, United Kingdom 7 National Institute for Health Research Health Protection Research Unit in Gastrointestinal Infections, United Kingdom 8 Department of Infection Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine, London, United Kingdom 9 Field Service - Epidemiology, National Infection Service, Public Health England, London, United Kingdom 10 Department of Public Health and Health Policy, NHS Lothian, Edinburgh, Scotland 11 North East North Central London Health Protection Team, Public Health England, London, United Kingdom 12 Incidents & Resilience Team, Food Standards Agency, London, United Kingdom 13 Statistics, Modelling & Economics Department, National Infection Service – Data & Analytical Sciences, Public Health England, London, United Kingdom 14 Public Health England London, Public Health England, London, United KingdomMari Morganmari.morgan wales.nhs.uk
-
View Citation Hide Citation
Citation style for this article: Morgan Mari, Watts Vicky, Allen David, Curtis Daniele, Kirolos Amir, Macdonald Neil, Maslen Ellie, Morgan Deb, Saei Ayoub, Sedgwick James, Stevenson Janet, Turbitt Deborah, Vivancos Roberto, Waugh Catriona, Williams Chris, Decraene Valerie. Challenges of investigating a large food-borne norovirus outbreak across all branches of a restaurant group in the United Kingdom, October 2016. Euro Surveill. 2019;24(18):pii=1800511. https://doi.org/10.2807/1560-7917.ES.2019.24.18.1800511 Received: 17 Sep 2018; Accepted: 07 Jan 2019
Challenges of investigating a large food-borne norovirus outbreak across all branches of a restaurant group in the United Kingdom, October 2016
- Previous Article
- Table of Contents
- Next Article
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.

Article metrics loading...

-
From This Site
/content/10.2807/1560-7917.ES.2019.24.18.1800511dcterms_title,dcterms_subject,pub_keyword105 -
PubMed
-
Google Scholar

Full text loading...
References
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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
-
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.

Data & Media loading...
Supplementary data
-
-
Supplementary Table S1
-
- Date:
-
