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Abstract

The aim of this study was to identify and characterise from a unique national collection of 564 strains associated with 140 strong-evidence food-borne outbreaks (FBOs) occurring in France during 2007 to 2014. Starchy food and vegetables were the most frequent food vehicles identified; 747 of 911 human cases occurred in institutional catering contexts. Incubation period was significantly shorter for emetic strains compared with diarrhoeal strains A sub-panel of 149 strains strictly associated to 74 FBOs and selected on Coliphage M13-PCR pattern, was studied for detection of the genes encoding cereulide, diarrhoeic toxins (Nhe, Hbl, CytK1 and CytK2) and haemolysin (HlyII), as well as phylogenetic classification. This clustered the strains into 12 genetic signatures (GSs) highlighting the virulence potential of each strain. GS1 ( genes only) and GS2 (, and ), were the most prevalent GS and may have a large impact on human health as they were present in 28% and 31% of FBOs, respectively. Our study provides a convenient molecular scheme for characterisation of strains responsible for FBOs in order to improve the monitoring and investigation of -induced FBOs, assess emerging clusters and diversity of strains.

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/content/10.2807/1560-7917.ES.2016.21.48.30413
2016-12-01
2017-12-16
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2016.21.48.30413
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References

  1. Guinebretière M-H, Auger S, Galleron N, Contzen M, De Sarrau B, De Buyser M-L, et al. Bacillus cytotoxicus sp. nov. is a novel thermotolerant species of the Bacillus cereus Group occasionally associated with food poisoning. Int J Syst Evol Microbiol. 2013;63(Pt 1):31-40.  https://doi.org/10.1099/ijs.0.030627-0  PMID: 22328607 
  2. Drobniewski FA. Bacillus cereus and related species. Clin Microbiol Rev. 1993;6(4):324-38.  https://doi.org/10.1128/CMR.6.4.324  PMID: 8269390 
  3. Mock M, Fouet A. Anthrax. Annu Rev Microbiol. 2001;55(1):647-71.  https://doi.org/10.1146/annurev.micro.55.1.647  PMID: 11544370 
  4. Santé publique France. Données relatives aux toxi-infections alimentaires collectives déclarées en France en 2013. [Data on collective food-borne outbreaks reported in France in 2013]. Saint-Maurice: Santé publique France. [Accessed Dec 2015]. French. Available from: http://invs.santepubliquefrance.fr/Dossiers-thematiques/Maladies-infectieuses/Risques-infectieux-d-origine-alimentaire/Toxi-infections-alimentaires-collectives/Donnees-epidemiologiques
  5. European Food Safety Authority, European Centre for Disease Prevention and Control (EFSA, ECDC). The European Union Summary Report on Trends and Sources of Zoonoses, Zoonotic Agents and Food-borne Outbreaks in 2013. EFSA Journal 2015;13(1):3991. doi: https://doi.org/10.2903/j.efsa.2015.3991,165  pp.
  6. Dierick K, Van Coillie E, Swiecicka I, Meyfroidt G, Devlieger H, Meulemans A, et al. Fatal family outbreak of Bacillus cereus-associated food poisoning. J Clin Microbiol. 2005;43(8):4277-9.  https://doi.org/10.1128/JCM.43.8.4277-4279.2005  PMID: 16082000 
  7. Ehling-Schulz M, Vukov N, Schulz A, Shaheen R, Andersson M, Märtlbauer E, et al. Identification and partial characterization of the nonribosomal peptide synthetase gene responsible for cereulide production in emetic Bacillus cereus. Appl Environ Microbiol. 2005;71(1):105-13.  https://doi.org/10.1128/AEM.71.1.105-113.2005  PMID: 15640177 
  8. Fagerlund A, Ween O, Lund T, Hardy SP, Granum PE. Genetic and functional analysis of the cytK family of genes in Bacillus cereus. Microbiology. 2004;150(Pt 8):2689-97.  https://doi.org/10.1099/mic.0.26975-0  PMID: 15289565 
  9. Ramarao N, Sanchis V. The pore-forming haemolysins of bacillus cereus: a review. Toxins (Basel). 2013;5(6):1119-39.  https://doi.org/10.3390/toxins5061119  PMID: 23748204 
  10. Cadot C, Tran SL, Vignaud ML, De Buyser ML, Kolstø AB, Brisabois A, et al. InhA1, NprA, and HlyII as candidates for markers to differentiate pathogenic from nonpathogenic Bacillus cereus strains. J Clin Microbiol. 2010;48(4):1358-65.  https://doi.org/10.1128/JCM.02123-09  PMID: 20129969 
  11. Tran SL, Guillemet E, Gohar M, Lereclus D, Ramarao N. CwpFM (EntFM) is a Bacillus cereus potential cell wall peptidase implicated in adhesion, biofilm formation, and virulence. J Bacteriol. 2010;192(10):2638-42.  https://doi.org/10.1128/JB.01315-09  PMID: 20233921 
  12. Guinebretière M-H, Velge P, Couvert O, Carlin F, Debuyser M-L, Nguyen-The C. Ability of Bacillus cereus group strains to cause food poisoning varies according to phylogenetic affiliation (groups I to VII) rather than species affiliation. J Clin Microbiol. 2010;48(9):3388-91.  https://doi.org/10.1128/JCM.00921-10  PMID: 20660215 
  13. Yang IC, Shih DY-C, Huang T-P, Huang Y-P, Wang J-Y, Pan T-M. Establishment of a novel multiplex PCR assay and detection of toxigenic strains of the species in the Bacillus cereus group. J Food Prot. 2005;68(10):2123-30. PMID: 16245717 
  14. Jeßberger N, Krey VM, Rademacher C, Böhm M-E, Mohr A-K, Ehling-Schulz M, et al. From genome to toxicity: a combinatory approach highlights the complexity of enterotoxin production in Bacillus cereus. Front Microbiol. 2015;6:560. PMID: 26113843 
  15. Beecher DJ, Wong AC. Identification of hemolysin BL-producing Bacillus cereus isolates by a discontinuous hemolytic pattern in blood agar. Appl Environ Microbiol. 1994;60(5):1646-51. PMID: 8017944 
  16. Guinebretiere M-H, Nguyen-The C. Sources of Bacillus cereus contamination in a pasteurized zucchini purée processing line, differentiated by two PCR-based methods. FEMS Microbiol Ecol. 2003;43(2):207-15. PMID: 19719681 
  17. Guinebretière M-H, Thompson FL, Sorokin A, Normand P, Dawyndt P, Ehling-Schulz M, et al. Ecological diversification in the Bacillus cereus Group. Environ Microbiol. 2008;10(4):851-65.  https://doi.org/10.1111/j.1462-2920.2007.01495.x  PMID: 18036180 
  18. Guinebretière M-H, Broussolle V, Nguyen-The C. Enterotoxigenic profiles of food-poisoning and food-borne Bacillus cereus strains. J Clin Microbiol. 2002;40(8):3053-6.  https://doi.org/10.1128/JCM.40.8.3053-3056.2002  PMID: 12149378 
  19. Pouillot R, Delignette-Muller ML. Evaluating variability and uncertainty separately in microbial quantitative risk assessment using two R packages. Int J Food Microbiol. 2010;142(3):330-40.  https://doi.org/10.1016/j.ijfoodmicro.2010.07.011  PMID: 20674055 
  20. Guillier L, Thébault A, Gauchard F, Pommepuy M, Guignard A, Malle P. A risk-based sampling plan for monitoring of histamine in fish products. J Food Prot. 2011;74(2):302-10.  https://doi.org/10.4315/0362-028X.JFP-10-234  PMID: 21333153 
  21. World Health Organization (WHO). WHO estimates of the global burden of foodborne diseases; foodborne disease burden epidemiology reference group 2007-2015. Geneva: WHO; 2015. Available from: http://apps.who.int/iris/bitstream/10665/199350/1/9789241565165_eng.pdf
  22. Cadel Six S, De Buyser M-L, Vignaud ML, Dao TT, Messio S, Pairaud S, et al. Toxi-infections alimentaires collectives à Bacillus cereus : bilan de la caractérisation des souches de 2006 à 2010. [Bacillus cereus food poisoning outbreaks: strain characterization results, 2006-2010]. Bull Epidemiol Hebd. 2012;(Hors-série):45-9. French. Available from: https://pro.anses.fr/bulletin-epidemiologique/Documents/BEP-mg-BE50-art14.pdf
  23. Choma C, Guinebretière MH, Carlin F, Schmitt P, Velge P, Granum PE, et al. Prevalence, characterization and growth of Bacillus cereus in commercial cooked chilled foods containing vegetables. J Appl Microbiol. 2000;88(4):617-25.  https://doi.org/10.1046/j.1365-2672.2000.00998.x  PMID: 10792519 
  24. Agata N, Ohta M, Yokoyama K. Production of Bacillus cereus emetic toxin (cereulide) in various foods. Int J Food Microbiol. 2002;73(1):23-7.  https://doi.org/10.1016/S0168-1605(01)00692-4  PMID: 11883672 
  25. Ehling-Schulz M, Guinebretiere M-H, Monthán A, Berge O, Fricker M, Svensson B. Toxin gene profiling of enterotoxic and emetic Bacillus cereus. FEMS Microbiol Lett. 2006;260(2):232-40.  https://doi.org/10.1111/j.1574-6968.2006.00320.x  PMID: 16842349 
  26. Ceuppens S, Rajkovic A, Hamelink S, Van de Wiele T, Boon N, Uyttendaele M. Enterotoxin production by Bacillus cereus under gastrointestinal conditions and their immunological detection by commercially available kits. Foodborne Pathog Dis. 2012;9(12):1130-6.  https://doi.org/10.1089/fpd.2012.1230  PMID: 23237409 
  27. Schmid D, Rademacher C, Kanitz EE, Frenzel E, Simons E, Allerberger F, et al. Elucidation of enterotoxigenic Bacillus cereus outbreaks in Austria by complementary epidemiological and microbiological investigations, 2013. Int J Food Microbiol. 2016;232:80-6.  https://doi.org/10.1016/j.ijfoodmicro.2016.05.011  PMID: 27257745 
  28. Granum PE, Lund T. Bacillus cereus and its food poisoning toxins. FEMS Microbiol Lett. 1997;157(2):223-8.  https://doi.org/10.1111/j.1574-6968.1997.tb12776.x  PMID: 9435100 
  29. Teunis PFM, Kasuga F, Fazil A, Ogden ID, Rotariu O, Strachan NJC. Dose-response modeling of Salmonella using outbreak data. Int J Food Microbiol. 2010;144(2):243-9.  https://doi.org/10.1016/j.ijfoodmicro.2010.09.026  PMID: 21036411 
  30. Gilber RJ, Kramer JM. Bacillus cereus food poisoning.). In: Cliver DC, Cochrane BA Editors. Progress in Food Safety.(proceeding of symposium) Madison (WI): Food Research Institute, University of Wisconsin-Madison, Madison; 1986. p. 85-93.
  31. Chon JW, Kim JH, Lee SJ, Hyeon JY, Song KY, Park C, et al. Prevalence, phenotypic traits and molecular characterization of emetic toxin-producing Bacillus cereus strains isolated from human stools in Korea. J Appl Microbiol. 2012;112(5):1042-9.  https://doi.org/10.1111/j.1365-2672.2012.05277.x  PMID: 22394210 
  32. Sastalla I, Fattah R, Coppage N, Nandy P, Crown D, Pomerantsev AP, et al. The Bacillus cereus Hbl and Nhe tripartite enterotoxin components assemble sequentially on the surface of target cells and are not interchangeable. PLoS One. 2013;8(10):e76955.  https://doi.org/10.1371/journal.pone.0076955  PMID: 24204713 
  33. Contzen M, Hailer M, Rau J. Isolation of Bacillus cytotoxicus from various commercial potato products. Int J Food Microbiol. 2014;174:19-22.  https://doi.org/10.1016/j.ijfoodmicro.2013.12.024  PMID: 24440535 
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