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Abstract

The French National Reference Centre for and (FNRC-ESS) detected two human clusters of 33 cases (median age: 10 years; 17 females) infected by serotype Bovismorbificans, ST142, HC5_243255 (EnteroBase HierCC‑cgMLST scheme) in September–November 2020 and of 11 cases (median age: 11 years; seven males) infected by serotype 4,12:i:-, ST34, HC5_198125 in October–December 2020. Epidemiological investigations conducted by Santé publique France linked these outbreaks to the consumption of dried pork sausages from the same manufacturer.  Bovismorbificans and  4,12:i:- were isolated by the National Reference Laboratory from different food samples, but both strains were identified in a single food sample only by qPCR. Three recalls and withdrawals of dried pork products were issued by the French general directorate of food of the French ministry for agriculture and food in November 2020, affecting eight supermarket chains. A notification on the European Rapid Alert System for Food and Feed and a European urgent enquiry on the Epidemic Intelligence Information System for Food and Waterborne Diseases and Zoonoses (EPIS-FWD) were launched. No cases were reported outside France. Outbreaks caused by multiple serotypes of may go undetected by protocols in standard procedures in microbiology laboratories.

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Author’s correction for Euro Surveill. 2023;28(2)
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2023-01-12
2024-11-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.2.2200123
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References

  1. World Health Organization (WHO). WHO Estimates of the Global Burden of Foodborne Diseases: Food-borne Disease Burden Epidemiology Reference Group 2007-2015. Geneva: WHO; 2015. Available from: https://www.who.int/publications/i/item/9789241565165
  2. European Food Safety AuthorityEuropean Centre for Disease Prevention and Control. The European Union One Health 2019 Zoonoses Report. EFSA J. 2021;19(2):e06406. PMID: 33680134 
  3. Van Cauteren D, Le Strat Y, Sommen C, Bruyand M, Tourdjman M, Da Silva NJ, et al. Estimated annual numbers of foodborne pathogen-associated illnesses, hospitalizations, and deaths, France, 2008-2013. Emerg Infect Dis. 2017;23(9):1486-92.  https://doi.org/10.3201/eid2309.170081  PMID: 28820137 
  4. Van Cauteren D, Le Strat Y, Sommen C, Bruyand M, Tourdjman M, Jourdan-Da Silva N, et al. Estimation de la morbidité et de la mortalité liées aux infections d’origine alimentaire en France métropolitaine, 2008-2013. [Estimates of food-related morbidity and mortality in metropolitan France, 2008-2013]. Bull Epidemiol Hebd (Paris). 2018;(1):2-10. French. Available from: http://beh.santepubliquefrance.fr/beh/2018/1/2018_1_1.html
  5. Bonardi S. Salmonella in the pork production chain and its impact on human health in the European Union. Epidemiol Infect. 2017;145(8):1513-26.  https://doi.org/10.1017/S095026881700036X  PMID: 28241896 
  6. DE Knegt LV, Pires SM, Hald T. Attributing foodborne salmonellosis in humans to animal reservoirs in the European Union using a multi-country stochastic model. Epidemiol Infect. 2015;143(6):1175-86.  https://doi.org/10.1017/S0950268814001903  PMID: 25083551 
  7. Centers for Disease Control and Prevention (CDC). Multistate outbreak of Salmonella serotype Bovismorbificans infections associated with hummus and tahini--United States, 2011. MMWR Morb Mortal Wkly Rep. 2012;61(46):944-7. PMID: 23169315 
  8. Knoblauch AM, Bratschi MW, Zuske MK, Althaus D, Stephan R, Hächler H, et al. Cross-border outbreak of Salmonella enterica ssp. enterica serovar Bovismorbificans: multiple approaches for an outbreak investigation in Germany and Switzerland. Swiss Med Wkly. 2015;145:w14182.  https://doi.org/10.4414/smw.2015.14182  PMID: 26430716 
  9. Oberreuter H, Rau J. Artificial neural network-assisted Fourier transform infrared spectroscopy for differentiation of Salmonella serogroups and its application on epidemiological tracing of Salmonella Bovismorbificans outbreak isolates from fresh sprouts. FEMS Microbiol Lett. 2019;366(15):fnz193.  https://doi.org/10.1093/femsle/fnz193  PMID: 31518396 
  10. Rimhanen-Finne R, Niskanen T, Lienemann T, Johansson T, Sjöman M, Korhonen T, et al. A nationwide outbreak of Salmonella Bovismorbificans associated with sprouted alfalfa seeds in Finland, 2009. Zoonoses Public Health. 2011;58(8):589-96.  https://doi.org/10.1111/j.1863-2378.2011.01408.x  PMID: 21824360 
  11. Stafford RJ, McCall BJ, Neill AS, Leon DS, Dorricott GJ, Towner CD, et al. A statewide outbreak of Salmonella Bovismorbificans phage type 32 infection in Queensland. Commun Dis Intell Q Rep. 2002;26(4):568-73. PMID: 12549525 
  12. Santé publique France. Épidémie de salmonellose à Salmonella sérotype Bovismorbificans liée à la consommation de viande chevaline, Hauts‐de‐France. [Outbreak of Salmonella serotype Bovismorbificans linked to horse meat consumption]. Saint‐Maurice: Santé publique France; 2021. French. Available from: https://www.santepubliquefrance.fr/maladies-et-traumatismes/maladies-infectieuses-d-origine-alimentaire/salmonellose/documents/rapport-synthese/epidemie-de-salmonelloses-a-salmonella-serotype-bovismorbificans-liee-a-la-consommation-de-viande-chevaline
  13. Brandwagt D, van den Wijngaard C, Tulen AD, Mulder AC, Hofhuis A, Jacobs R, et al. Outbreak of Salmonella Bovismorbificans associated with the consumption of uncooked ham products, the Netherlands, 2016 to 2017. Euro Surveill. 2018;23(1):17-00335.  https://doi.org/10.2807/1560-7917.ES.2018.23.1.17-00335  PMID: 29317018 
  14. Zhou Z, Charlesworth J, Achtman M. HierCC: A multi-level clustering scheme for population assignments based on core genome MLST. Bioinformatics. 2021;37(20): 3645–6. Epub ahead of print.  https://doi.org/10.1093/bioinformatics/btab234  PMID: 33823553 
  15. Achtman M, Wain J, Weill FX, Nair S, Zhou Z, Sangal V, et al. Multilocus sequence typing as a replacement for serotyping in Salmonella enterica. PLoS Pathog. 2012;8(6):e1002776.  https://doi.org/10.1371/journal.ppat.1002776  PMID: 22737074 
  16. Alikhan NF, Zhou Z, Sergeant MJ, Achtman M. A genomic overview of the population structure of Salmonella. PLoS Genet. 2018;14(4):e1007261.  https://doi.org/10.1371/journal.pgen.1007261  PMID: 29621240 
  17. Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, et al. ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother. 2020;75(12):3491-500.  https://doi.org/10.1093/jac/dkaa345  PMID: 32780112 
  18. International Organization for Standardization (ISO). NF EN ISO 6579-1/A1 Mars 2020. Microbiologie de la chaîne alimentaire - Méthode horizontale pour la recherche, le dénombrement et le sérotypage des Salmonella - Partie 1: recherche des Salmonella spp. Available from: https://www.iso.org/standard/56712.html
  19. Grimont PA, Weill FX. Antigenic formulae of the Salmonella serovars. Paris: WHO collaborating centre for reference and research on Salmonella; 2007. Available from https://www.pasteur.fr/sites/default/files/veng_0.pdf
  20. Sévellec Y, Granier SA, Radomski N, Felten A, Le Hello S, Feurer C, et al. Complete genome sequence of Salmonella enterica subsp. enterica serotype derby, associated with the pork sector in France. Microbiol Resour Announc. 2018;7(12):e01027-18.  https://doi.org/10.1128/MRA.01027-18  PMID: 30533663 
  21. Ministère de l’Agriculture et de l’Alimentation. Communiqué de presse. Retrait et rappel de saucisses sèches et de rosettes tranchées contaminées par des salmonelles. [Removal and recall of salmonella-contaminated dry sausages and sliced rosettes]. Paris: Ministère de l’Agriculture et de l’Alimentation; 26 Nov 2020. French. Available from: https://agriculture.gouv.fr/alerte-sanitaire-retrait-et-rappel-de-saucisses-seches-et-de-rosettes-tranchees-contaminees-par-des
  22. European Commission. Rapid Alert System for Food and Feed (RASFF) Window: Notification 2020.5038. Dry sausage -Salmonella Bovismorbivicans. Brussels: European Commission; 8 Dec 2020. Available from: https://webgate.ec.europa.eu/rasff-window/screen/notification/450578
  23. European Commission. Commission Regulation (EU) No 218/2014 of 7 March 2014 amending Annexes to Regulations (EC) No 853/2004 and (EC) No 854/2004 of the European Parliament and of the Council and Commission Regulation (EC) No 2074/2005. Text with EEA relevance. Official Journal of the European Union. Luxembourg: Publications Office of the European Union. 8.3.2014: L 69, p. 95–98. Available from: http://data.europa.eu/eli/reg/2014/218/oj
  24. Delannoy S, Cadel-Six S, Bonifait L, Tran ML, Cherchame E, Baugé L, et al. Closed genome sequence of a Salmonella enterica serovar Bovismorbificans strain isolated from dried pork sausage associated with an outbreak in France. Microbiol Resour Announc. 2021;10(40):e0066221.  https://doi.org/10.1128/MRA.00662-21  PMID: 34617790 
  25. Bone A, Noel H, Le Hello S, Pihier N, Danan C, Raguenaud ME, et al. Nationwide outbreak of Salmonella enterica serotype 4,12:i:- infections in France, linked to dried pork sausage, March-May 2010. Euro Surveill. 2010;15(24):19592.  https://doi.org/10.2807/ese.15.24.19592-en  PMID: 20576238 
  26. Gossner CM, van Cauteren D, Le Hello S, Weill FX, Terrien E, Tessier S, et al. Nationwide outbreak of Salmonella enterica serotype 4,[5],12:i:- infection associated with consumption of dried pork sausage, France, November to December 2011. Euro Surveill. 2012;17(5):20071.  https://doi.org/10.2807/ese.17.05.20071-en  PMID: 22321138 
  27. Lienemann T, Niskanen T, Guedes S, Siitonen A, Kuusi M, Rimhanen-Finne R. Iceberg lettuce as suggested source of a nationwide outbreak caused by two Salmonella serotypes, Newport and Reading, in Finland in 2008. J Food Prot. 2011;74(6):1035-40.  https://doi.org/10.4315/0362-028X.JFP-10-455  PMID: 21669088 
  28. Centers for Disease Control and Prevention (CDC). Multiple-serotype Salmonella gastroenteritis outbreak after a reception --- Connecticut, 2009. MMWR Morb Mortal Wkly Rep. 2010;59(34):1093-7. PMID: 20814404 
  29. Paine S, Thornley C, Wilson M, Dufour M, Sexton K, Miller J, et al. An outbreak of multiple serotypes of Salmonella in New Zealand linked to consumption of contaminated tahini imported from Turkey. Foodborne Pathog Dis. 2014;11(11):887-92.  https://doi.org/10.1089/fpd.2014.1773  PMID: 25393669 
  30. Harvey RR, Heiman Marshall KE, Burnworth L, Hamel M, Tataryn J, Cutler J, et al. International outbreak of multiple Salmonella serotype infections linked to sprouted chia seed powder - USA and Canada, 2013-2014. Epidemiol Infect. 2017;145(8):1535-44.  https://doi.org/10.1017/S0950268817000504  PMID: 28318456 
  31. European Food Safety Authority. Multi-country outbreak of multiple Salmonella enterica serotypes linked to imported sesame-based products. EFSA J. 2021;18(10):6922E.  https://doi.org/10.2903/sp.efsa.2021.EN-6922 
  32. Blackstone GM, Nordstrom JL, DePaola A. 2005. A same day detection method for Salmonella species in shrimp using real time PCR, poster P-079. Abstr. 105th Gen. Meet. Am. Soc. Microbiol. American Society for Microbiology, Washington, DC.
  33. Bugarel M, Tudor A, Loneragan GH, Nightingale KK. Molecular detection assay of five Salmonella serotypes of public interest: Typhimurium, Enteritidis, Newport, Heidelberg, and Hadar. J Microbiol Methods. 2017;134:14-20.  https://doi.org/10.1016/j.mimet.2016.12.011  PMID: 27993596 
  34. International Organization for Standardization (ISO). Microbiology of the food chain – Horizontal method for the detection, enumeration and serotyping of Salmonella. Part 4: Identification of monophasic Salmonella Typhimurium (1,4,[5],12,i:-) by polymerase chain reaction (PCR). Draft ISO/TS CD 6579-4. Geneva: ISO; 2021. Available from: https://www.iso.org/standard/56712.html
Countrywide multi-serotype outbreak of Salmonella Bovismorbificans ST142 and monophasic Salmonella Typhimurium ST34 associated with dried pork sausages in France, September 2020* to January 2021
<p class="citation"> <span>Citation style for this article:</span> <span class="meta-value authors"> <a href="/search?value1=Maria+Pardos+de+la+Gandara&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pardos de la Gandara Maria</a>, <a href="/search?value1=Nelly+Fournet&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fournet Nelly</a>, <a href="/search?value1=Laetitia+Bonifait&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Bonifait Laetitia</a>, <a href="/search?value1=Sophie+Lef%C3%A8vre&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Lefèvre Sophie</a>, <a href="/search?value1=Marianne+Chemaly&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Chemaly Marianne</a>, <a href="/search?value1=Charlotte+Grastilleur&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Grastilleur Charlotte</a>, <a href="/search?value1=Sabrina+Cadel-Six&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Cadel-Six Sabrina</a>, <a href="/search?value1=Patrick+Fach&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Fach Patrick</a>, <a href="/search?value1=Agn%C3%A8s+Pignault&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Pignault Agnès</a>, <a href="/search?value1=Anne+Brisabois&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Brisabois Anne</a>, <a href="/search?value1=Nathalie+Jourdan-Da+Silva&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Jourdan-Da Silva Nathalie</a>, <a href="/search?value1=Fran%C3%A7ois-Xavier+Weill&option1=author&noRedirect=true" class="nonDisambigAuthorLink">Weill François-Xavier</a></span>. Countrywide multi-serotype outbreak of Salmonella Bovismorbificans ST142 and monophasic Salmonella Typhimurium ST34 associated with dried pork sausages in France, September 2020* to January 2021. <a href="/content/ecdc">Euro Surveill.</a> 2023;28(2):pii=2200123. <a href="https://doi.org/10.2807/1560-7917.ES.2023.28.2.2200123" title="doi link" target="_blank">https://doi.org/10.2807/1560-7917.ES.2023.28.2.2200123</a> <span class="ES_Article_citation"> <span class="generated">Received</span>: 03 Feb 2022;&nbsp;&nbsp; <span class="generated">Accepted</span>: 05 Oct 2022 </span> </p>
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