Surveillance and outbreak report Open Access
Like 0


In June 2014, a staphylococcal food poisoning outbreak occurred at an international equine sports event in Luxembourg requiring the hospitalisation of 31 persons. We conducted a microbiological investigation of patients and buffet items, a case–control study and a carriage study of catering staff. Isolates of from patients, food and catering staff were characterised and compared using traditional typing methods and whole genome sequencing. Genotypically identical strains (sequence type ST8, -type t024, MLVA-type 4698, enterotoxin A FRI100) were isolated in 10 patients, shiitake mushrooms, cured ham, and in three members of staff. The case–control study strongly suggested pasta salad with pesto as the vehicle of infection (p<0.001), but this food item could not be tested, because there were no leftovers. Additional enterotoxigenic strains genetically unrelated to the outbreak strain were found in four members of staff. Non-enterotoxigenic strains with livestock-associated sequence type ST398 were isolated from three food items and two members of staff. The main cause of the outbreak is likely to have been not maintaining the cold chain after food preparation. Whole genome sequencing resulted in phylogenetic clustering which concurred with traditional typing while simultaneously characterising virulence and resistance traits.


Article metrics loading...

Loading full text...

Full text loading...



  1. Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev. 2012;36(4):815-36. . https://doi.org/10.1111/j.1574-6976.2011.00311.x  PMID: 22091892 
  2. Ostyn A, De Buyser ML, Guillier F, Groult J, Felix B, Salah S, et al. First evidence of a food poisoning outbreak due to staphylococcal enterotoxin type E, France, 2009. Euro Surveill. 2010;15(13). PMID: 20394711 
  3. Institut de Veille Sanitaire (InVS). Surveillance des toxi-infections alimentaires collectives. Données de la déclaration obligatoire. [Surveillance of foodborne illness. Data from mandatory reporting]. Saint-Maurice, France: INVS; 2012. French. Available from: www.invs.sante.fr/content/download/85413/313604/version1/file/tiac_donnees_2012.pdf
  4. Holmberg SD, Blake PA. Staphylococcal food poisoning in the United States. New facts and old misconceptions. JAMA. 1984;251(4):487-9. . https://doi.org/10.1001/jama.1984.03340280037024  PMID: 6690814 
  5. Cornaglia G, Courcol R, Herrmann J-L, Kahlmeter G, Peigue-Lafeuille H, Vila J, editors. European Manual of Clinical Microbiology. 1st ed. Basel: European Society for Clinical Microbiology and Infectious Diseases and Société Française de Microbiologie; 2012.
  6. Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Genet Mol Res. 2003;2(1):63-76. PMID: 12917803 
  7. Bennett SD, Walsh KA, Gould LH. Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus--United States, 1998-2008. Clin Infect Dis. 2013;57(3):425-33. . https://doi.org/10.1093/cid/cit244  PMID: 23592829 
  8. Mossong J, Gelhausen E, Decruyenaere F, Devaux A, Perrin M, Even J, et al. Prevalence, risk factors and molecular epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) colonization in residents of long-term care facilities in Luxembourg, 2010. Epidemiol Infect. 2013;141(6):1199-206. . https://doi.org/10.1017/S0950268812001999  PMID: 22953727 
  9. Kwon NH, Kim SH, Park KT, Bae WK, Kim JY, Lim JY, et al. Application of extended single-reaction multiplex polymerase chain reaction for toxin typing of Staphylococcus aureus isolates in South Korea. Int J Food Microbiol. 2004;97(2):137-45. . https://doi.org/10.1016/j.ijfoodmicro.2004.04.014  PMID: 15541800 
  10. Schouls LM, Spalburg EC, van Luit M, Huijsdens XW, Pluister GN, van Santen-Verheuvel MG, et al. Multiple-locus variable number tandem repeat analysis of Staphylococcus aureus: comparison with pulsed-field gel electrophoresis and spa-typing. PLoS ONE. 2009;4(4):e5082. . https://doi.org/10.1371/journal.pone.0005082  PMID: 19343175 
  11. Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, et al. Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother. 2012;67(11):2640-4. . https://doi.org/10.1093/jac/dks261  PMID: 22782487 
  12. Larsen MV, Cosentino S, Rasmussen S, Friis C, Hasman H, Marvig RL, et al. Multilocus sequence typing of total-genome-sequenced bacteria. J Clin Microbiol. 2012;50(4):1355-61. . https://doi.org/10.1128/JCM.06094-11  PMID: 22238442 
  13. Joensen KG, Scheutz F, Lund O, Hasman H, Kaas RS, Nielsen EM, et al. Real-time whole-genome sequencing for routine typing, surveillance, and outbreak detection of verotoxigenic Escherichia coli. J Clin Microbiol. 2014;52(5):1501-10. . https://doi.org/10.1128/JCM.03617-13  PMID: 24574290 
  14. Leopold SR, Goering RV, Witten A, Harmsen D, Mellmann A. Bacterial whole-genome sequencing revisited: portable, scalable, and standardized analysis for typing and detection of virulence and antibiotic resistance genes. J Clin Microbiol. 2014;52(7):2365-70. . https://doi.org/10.1128/JCM.00262-14  PMID: 24759713 
  15. Johler S, Layer F, Stephan R. Comparison of virulence and antibiotic resistance genes of food poisoning outbreak isolates of Staphylococcus aureus with isolates obtained from bovine mastitis milk and pig carcasses. J Food Prot. 2011;74(11):1852-9. . https://doi.org/10.4315/0362-028X.JFP-11-192  PMID: 22054185 
  16. Wei HL, Chiou CS. Molecular subtyping of Staphylococcus aureus from an outbreak associated with a food handler. Epidemiol Infect. 2002;128(1):15-20. . https://doi.org/10.1017/S0950268801006355  PMID: 11895086 
  17. Schmid D, Gschiel E, Mann M, Huhulescu S, Ruppitsch W, Bohm G, et al. Outbreak of acute gastroenteritis in an Austrian boarding school, September 2006. Euro Surveill. 2007;12(3):224. PMID: 17439809 
  18. Johler S, Tichaczek-Dischinger PS, Rau J, Sihto HM, Lehner A, Adam M, et al. Outbreak of Staphylococcal food poisoning due to SEA-producing Staphylococcus aureus. Foodborne Pathog Dis. 2013;10(9):777-81. . https://doi.org/10.1089/fpd.2013.1503  PMID: 23767854 
  19. Argudín MA, Mendoza MC, Rodicio MR. Food poisoning and Staphylococcus aureus enterotoxins. Toxins (Basel). 2010;2(7):1751-73. . https://doi.org/10.3390/toxins2071751  PMID: 22069659 
  20. Kadariya J, Smith TC, Thapaliya D. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int. 2014;2014:827965.
  21. Kérouanton A, Hennekinne JA, Letertre C, Petit L, Chesneau O, Brisabois A, et al. Characterization of Staphylococcus aureus strains associated with food poisoning outbreaks in France. Int J Food Microbiol. 2007;115(3):369-75. . https://doi.org/10.1016/j.ijfoodmicro.2006.10.050  PMID: 17306397 
  22. Yan X, Wang B, Tao X, Hu Q, Cui Z, Zhang J, et al. Characterization of Staphylococcus aureus strains associated with food poisoning in Shenzhen, China. Appl Environ Microbiol. 2012;78(18):6637-42. . https://doi.org/10.1128/AEM.01165-12  PMID: 22798367 
  23. Veras JF, do Carmo LS, Tong LC, Shupp JW, Cummings C, Dos Santos DA, et al. A study of the enterotoxigenicity of coagulase-negative and coagulase-positive staphylococcal isolates from food poisoning outbreaks in Minas Gerais, Brazil. Int J Infect Dis. 2008;12(4):410-5. . https://doi.org/10.1016/j.ijid.2007.09.018  PMID: 18206412 
  24. Argudín MA, Mendoza MC, González-Hevia MA, Bances M, Guerra B, Rodicio MR. Genotypes, exotoxin gene content, and antimicrobial resistance of Staphylococcus aureus strains recovered from foods and food handlers. Appl Environ Microbiol. 2012;78(8):2930-5. . https://doi.org/10.1128/AEM.07487-11  PMID: 22327598 
  25. Wertheim HFL, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751-62. . https://doi.org/10.1016/S1473-3099(05)70295-4  PMID: 16310147 
  26. Monecke S, Luedicke C, Slickers P, Ehricht R. Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J Clin Microbiol Infect Dis. 2009;28(9):1159-65. . https://doi.org/10.1007/s10096-009-0752-2  PMID: 19434432 
  27. Wattinger L, Stephan R, Layer F, Johler S. Comparison of Staphylococcus aureus isolates associated with food intoxication with isolates from human nasal carriers and human infections. Eur J Clin Microbiol Infect Dis. 2012;31(4):455-64. . https://doi.org/10.1007/s10096-011-1330-y  PMID: 21761125 
  28. Uzunović S, Ibrahimagic A, Kamberovic F, Rijnders MIA, Stobberingh EE. Molecular Characterization of Methicillin-Susceptible And Methicillin-Resistant Staphylococcus aureus in Food Handlers in Bosnia and Herzegovina. Open Infect Dis J. 2013;7(1):15-20. . https://doi.org/10.2174/1874279301307010015 
  29. Brunel AS, Bañuls AL, Marchandin H, Bouzinbi N, Morquin D, Jumas-Bilak E, et al. Methicillin-sensitive Staphylococcus aureus CC398 in intensive care unit, France. Emerg Infect Dis. 2014;20(9):1511-5. . https://doi.org/10.3201/eid2009.130225  PMID: 25148514 
  30. Vandendriessche S, Kadlec K, Schwarz S, Denis O. Methicillin-susceptible Staphylococcus aureus ST398-t571 harbouring the macrolide-lincosamide-streptogramin B resistance gene erm(T) in Belgian hospitals. J Antimicrob Chemother. 2011;66(11):2455-9. . https://doi.org/10.1093/jac/dkr348  PMID: 21868413 
  31. Cuny C, Layer F, Köck R, Werner G, Witte W. Methicillin susceptible Staphylococcus aureus (MSSA) of clonal complex CC398, t571 from infections in humans are still rare in Germany. PLoS ONE. 2013;8(12):e83165. . https://doi.org/10.1371/journal.pone.0083165  PMID: 24367584 
  32. Köser CU, Holden MT, Ellington MJ, Cartwright EJ, Brown NM, Ogilvy-Stuart AL, et al. Rapid whole-genome sequencing for investigation of a neonatal MRSA outbreak. N Engl J Med. 2012;366(24):2267-75. . https://doi.org/10.1056/NEJMoa1109910  PMID: 22693998 
  33. Harris SR, Cartwright EJP, Török ME, Holden MTG, Brown NM, Ogilvy-Stuart AL, et al. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis. 2013;13(2):130-6. . https://doi.org/10.1016/S1473-3099(12)70268-2  PMID: 23158674 
  34. Price JR, Golubchik T, Cole K, Wilson DJ, Crook DW, Thwaites GE, et al. Whole-genome sequencing shows that patient-to-patient transmission rarely accounts for acquisition of Staphylococcus aureus in an intensive care unit. Clin Infect Dis. 2014;58(5):609-18. . https://doi.org/10.1093/cid/cit807  PMID: 24336829 
  35. Schmid D, Allerberger F, Huhulescu S, Pietzka A, Amar C, Kleta S, et al. Whole genome sequencing as a tool to investigate a cluster of seven cases of listeriosis in Austria and Germany, 2011-2013. Clin Microbiol Infect. 2014;20(5):431-6. . https://doi.org/10.1111/1469-0691.12638  PMID: 24698214 
  36. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A, et al. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS ONE. 2011;6(7):e22751. . https://doi.org/10.1371/journal.pone.0022751  PMID: 21799941 

Data & Media loading...

Submit comment
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error