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Current Clinical Microbiology Reports

, Volume 5, Issue 2, pp 88–96 | Cite as

Staphylococcus aureus as a Foodborne Pathogen

  • Alexandra Fetsch
  • Sophia Johler
Foodborne Pathogens (S Johler, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Foodborne Pathogens

Abstract

Purpose of Review

We present recent insights on S. aureus as a foodborne pathogen, thus providing readers with an update of current findings impacting prevention and control measures.

Recent Findings

Advances in disease burden assessment show the burden of S. aureus foodborne disease around the globe. In recent years, recent research has provided valuable new data improving the understanding of the pathobiology of S. aureus foodborne disease as well as proteomics and genomics of this foodborne pathogen. In particular, recent findings shed new light on the role of newly described enterotoxins and methicillin-resistant S. aureus. These new findings guide the way towards improved prevention and control strategies.

Summary

S. aureus is the leading cause of foodborne intoxications worldwide. Control strategies are focused on hygiene measures to avoid food contamination and limit S. aureus growth. Outbreak investigations remain challenging and would strongly benefit from additional data on enterotoxin formation under stress conditions and novel tools allowing for detection of newly described enterotoxins.

Keywords

Staphylococcal Food Poisoning Staphylococcal enterotoxins Detection methods Foodborne outbreak MRSA 

Notes

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as:• Of importance •• Of major importance

  1. 1.
    Robinson TP, Bu DP, Carrique-Mas J, Fevre EM, Gilbert M, Grace D, et al. Antibiotic resistance is the quintessential one health issue. Trans R Soc Trop Med Hyg. 2016;110:377–80.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Grace D, McDermott J. Livestock epidemics and disasters. In: Wisner B, Gaillard JC, Kelman I, editors. Routledge Handb. Hazards Disaster Risk Reduct. Oxford: Taylor & Francis; 2012. p. 876.Google Scholar
  3. 3.
    Shepheard MA, Fleming VM, Connor TR, Corander J, Feil EJ, Fraser C, et al. Historical zoonoses and other changes in host tropism of Staphylococcus aureus, identified by phylogenetic analysis of a population dataset. PLoS One. 2013;8:e62369.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Brown AF, Leech JM, Rogers TR, McLoughlin RM. Staphylococcus aureus colonization: modulation of host immune response and impact on human vaccine design. Front Immunol. 2014;4:507.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Kadariya J, Smith TC, Thapaliya D. Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. Biomed Res Int. 2014;827965Google Scholar
  6. 6.
    Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17:7–15.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Anonymous. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2015. EFSA J. 2016;2015:4329.  https://doi.org/10.2903/jefsa.Google Scholar
  8. 8.
    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;31:455–64.CrossRefPubMedGoogle Scholar
  9. 9.
    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;74:1852–9.CrossRefPubMedGoogle Scholar
  10. 10.
    Johler S, Weder D, Bridy C, Huguenin M-C, Robert L, Hummerjohann J, et al. Outbreak of staphylococcal food poisoning among children and staff at a Swiss boarding school due to soft cheese made from raw milk. J Dairy Sci. 2015;98:1–5.CrossRefGoogle Scholar
  11. 11.
    Hennekinne J-A, Ostyn A, Guillier F, Herbin S, Prufer A-L, Dragacci S. How should staphylococcal food poisoning outbreaks be characterized? Toxins. 2010;2:2106–16.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    •• Hu D-L, Nakane A. Mechanisms of staphylococcal enterotoxin-induced emesis. Eur J Pharmacol. 2014;722:95–107. Review of the current body of knowledge on the mechanisms behind the emetic activity of S. aureus CrossRefPubMedGoogle Scholar
  13. 13.
    Benkerroum N. Staphylococcal enterotoxins and enterotoxin-like toxins with special reference to dairy products: an overview. Crit Rev Food Sci Nutr. 2017:1–28.Google Scholar
  14. 14.
    Doyle MP, Beuchat LR. Food microbiology: fundamentals and frontiers. 3rd ed. Washington, DC: ASM Press; 2007.Google Scholar
  15. 15.
    Spaulding AR, Salgado-Pabón W, Kohler PL, Horswill AR, Leung DYM, Schlievert PM. Staphylococcal and streptococcal superantigen exotoxins. Clin Microbiol Rev. 2013;26:422–47.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Le Loir Y, Baron F, Gautier M. Staphylococcus aureus and food poisoning. Genet Mol Res. 2003;2:63–76.PubMedGoogle Scholar
  17. 17.
    Lina G, Bohach GA, Nair SP, Hiramatsu K, Jouvin-Marche E, Mariuzza R. Standard nomenclature for the superantigens expressed by Staphylococcus. J Infect Dis. 2004;189:2334–6.CrossRefPubMedGoogle Scholar
  18. 18.
    Larkin EA, Carman RJ, Krakauer T, Stiles BG. Staphylococcus aureus: the toxic presence of a pathogen extraordinaire. Curr Med Chem. 2009;16:4003–19.CrossRefPubMedGoogle Scholar
  19. 19.
    Betley MJ, Schlievert PM, Bergdoll MS, Bohach GA, Iandolo JJ, Khan SA, et al. Staphylococcal gene nomenclature. Am Soc Microbiol News. 1990;56:182.Google Scholar
  20. 20.
    Betley MJ, Mekalanos JJ. Staphylococcal enterotoxin A is encoded by phage. Science. 1985;229:185–7.CrossRefPubMedGoogle Scholar
  21. 21.
    Betley MJ, Mekalanos JJ. Nucleotide sequence of the type A staphylococcal enterotoxin gene. J Bacteriol. 1988;170:34–41.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Casman EP. Further serological studies of staphylococcal enterotoxin. J Bacteriol. 1960;79:849.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Kuroda M, Ohta T, Uchiyama I, Baba T, Yuzawa H, Kobayashi I, et al. Whole genome sequencing of meticillin-resistant Staphylococcus aureus. Lancet. 2001;357:1225–40.CrossRefPubMedGoogle Scholar
  24. 24.
    Shafer WM, Iandolo JJ. Chromosomal locus for staphylococcal enterotoxin B. Infect Immun. 1978;20:273–8.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Sato’o Y, Omoe K, Ono HK, Nakane A, Hu D-L. A novel comprehensive analysis method for Staphylococcus aureus pathogenicity islands. Microbiol Immunol. 2013;57:91–9.CrossRefPubMedGoogle Scholar
  26. 26.
    Stevens MJA, Stephan R, Johler S. Complete and assembled genome sequence of Staphylococcus aureus RKI4, a food-poisoning strain exhibiting a novel S. aureus pathogenicity island carrying seb. Genome Announc. 2015;3:2015.CrossRefGoogle Scholar
  27. 27.
    Betley MJ, Bergdoll MS. Staphylococcal enterotoxin type C genes not associated with extrachromosomal DNA. Abstr Ann Meet Am Soc Microbiol 1981; D-38: 49.Google Scholar
  28. 28.
    Novick RP, Christie GE, Penades JR. The phage-related chromosomal islands of gram-positive bacteria. Nat Rev Microbiol. 2010;8:541–51.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Casman EP, Bennett RW, Dorsey AE, Issa JA. Identification of a fourth staphylococcal enterotoxin, enterotoxin D. J Bacteriol. 1967;94:1875–82.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Bayles KW, Iandolo JJ. Genetic and molecular analyses of the gene encoding staphylococcal enterotoxin D. J Bacteriol. 1989;171:4799–806.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Bergdoll MS, Borja CR, Robbins RN, Weiss KF. Identification of enterotoxin E. Infect Immun. 1971;4:593–5.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Couch JL, Soltis MT, Betley MJ. Cloning and nucleotide sequence of the type E staphylococcal enterotoxin gene. J Bacteriol. 1988;170:2954–60.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, Mougel C, et al. egc, a highly prevalent operon of enterotoxin gene, forms a putative nursery of superantigens in Staphylococcus aureus. J Immunol. 2001;166:669–77.CrossRefPubMedGoogle Scholar
  34. 34.
    Jarraud S, Peyrat MA, Lim A, Tristan A, Bes M, Mougel C, et al. Correction. J Immunol. 2001;166:4260.CrossRefGoogle Scholar
  35. 35.
    Baba T, Takeuchi F, Kuroda M, Yuzawa K, Aoki K, Oguchi A, et al. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet. 2002;359:1819–27.CrossRefPubMedGoogle Scholar
  36. 36.
    Noto MJ, Archer GL. A subset of Staphylococcus aureus strains harboring staphylococcal cassette chromosome mec (SCCmec) type IV is deficient in CcrAB-mediated SCCmec excision. Antimicrob Agents Chemother. 2006;50:2782–8.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Su YC, Wong AC. Identification and purification of a new staphylococcal enterotoxin, H. Appl Environ Microbiol. 1995;61:1438–43.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Ren K, Bannan JD, Pancholi V, Cheung AL, Robbins JC, Fischetti VA, et al. Characterization and biological properties of a new staphylococcal exotoxin. J Exp Med. 1994;180:1675–83.CrossRefPubMedGoogle Scholar
  39. 39.
    Munson SH, Tremaine MT, Betley MJ, Welch RA. Identification and characterization of staphylococcal enterotoxin types G and I from Staphylococcus aureus. Infect Immun. 1998;66:3337–48.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Hu D, Omoe K, Shimoda Y, Nakane A, Shinagawa K. Induction of emetic response to staphylococcal enterotoxins in the house musk shrew (Suncus murinus). Infect Immun. 2003;71:567–70.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Zhang S, Iandolo JJ, Stewart GC. The enterotoxin D plasmid of Staphylococcus aureus encodes a second enterotoxin determinant (sej). FEMS Microbiol Lett. 1998;168:227–33.CrossRefPubMedGoogle Scholar
  42. 42.
    Omoe K, Hu D-L, Ono HK, Shimizu S, Takahashi-Omoe H, Nakane A, et al. Emetic potentials of newly identified staphylococcal enterotoxin-like toxins. Infect Immun. 2013;81:3627–31.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Orwin PM, Leung DY, Donahue HL, Novick RP, Schlievert PM. Biochemical and biological properties of staphylococcal enterotoxin K. Infect Immun. 2001;69:360–6.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    •• Ono HK, Hirose S, Naito I, Sato’o Y, Asano K, Hu D-L, et al. The emetic activity of staphylococcal enterotoxins, SEK, SEL, SEM, SEN and SEO in a small emetic animal model, the house musk shrew. Microbiol Immunol. 2017;61:12–6. This paper provides comprehensive data on the emetic activity of various newly described SEs in an animal model. CrossRefPubMedGoogle Scholar
  45. 45.
    Orwin PM, Fitzgerald JR, Leung DY, Gutierrez JA, Bohach GA, Schlievert PM. Characterization of Staphylococcus aureus enterotoxin L. Infect Immun. 2003;71:2916–9.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Fitzgerald JR, Monday SR, Foster TJ, Bohach GA, Hartigan PJ, Meaney WJ, et al. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol. 2001;183:63–70.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Omoe K, Imanishi K, Hu DL, Kato H, Fugane Y, Abe Y, et al. Characterization of novel staphylococcal enterotoxin-like toxin type P. Infect Immun. 2005;73:5540–6.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Hu D-L, Ono HK, Isayama S, Okada R, Okamura M, Lei LC, et al. Biological characteristics of staphylococcal enterotoxin Q and its potential risk for food poisoning. J Appl Microbiol. 2017;122:1672–9.CrossRefPubMedGoogle Scholar
  49. 49.
    Orwin PM, Leung DY, Tripp TJ, Bohach GA, Earhart CA, Ohlendorf DH, et al. Characterization of a novel staphylococcal enterotoxin-like superantigen, a member of the group V subfamily of pyrogenic toxins. Biochemistry. 2002;41:14033–40.CrossRefPubMedGoogle Scholar
  50. 50.
    Ono HK, Omoe K, Imanishi K, Iwakabe Y, Hu DL, Kato H, et al. Identification and characterization of two novel staphylococcal enterotoxins, types S and T. Infect Immun. 2008;76:4999–5005.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Omoe K, Hu DL, Takahashi-Omoe H, Nakane A, Shinagawa K. Identification and characterization of a new staphylococcal enterotoxin-related putative toxin encoded by two kinds of plasmids. Infect Immun. 2003;71:6088–94.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Letertre C, Perelle S, Dilasser F, Fach P. Identification of a new putative enterotoxin SEU encoded by the egc cluster of Staphylococcus aureus. J Appl Microbiol. 2003;95:38–43.CrossRefPubMedGoogle Scholar
  53. 53.
    Thomas DY, Jarraud S, Lemercier B, Cozon G, Echasserieau K, Etienne J, et al. Staphylococcal enterotoxin-like toxins U2 and V, two new staphylococcal superantigens arising from recombination within the enterotoxin gene cluster. Infect Immun. 2006;74:4724–34.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Wilson GJ, Seo KS, Cartwright RA, Connelley T, Chuang-Smith ON, Merriman JA, et al. A novel core genome-encoded superantigen contributes to lethality of community-associated MRSA necrotizing pneumonia. PLoS Pathog. 2011;7:e1002271.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Ono HK, Sato’o Y, Narita K, Naito I, Hirose S, Hisatsune J, et al. Identification and characterization of a novel staphylococcal emetic toxin. Appl Environ Microbiol. 2015;81:7034–40.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Ikeda T, Tamate N, Yamaguchi K, Makino S. Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H. Appl Environ Microbiol. 2005;71:2793–5.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Jørgensen HJ, Mathisen T, Lovseth A, Omoe K, Qvale KS, Loncarevic S. An outbreak of staphylococcal food poisoning caused by enterotoxin H in mashed potato made with raw milk. FEMS Microbiol Lett. 2005;252:267–72.CrossRefPubMedGoogle Scholar
  58. 58.
    Pereira ML, DoCarmo LS, dosSantos EJ, Pereira JL, Bergdoll MS. Enterotoxin H in staphylococcal food poisoning. J Food Prot. 1996;59:559–61.CrossRefGoogle Scholar
  59. 59.
    • Johler S, Giannini P, Jermini M, Hummerjohann J, Baumgartner A, Stephan R. Further evidence for staphylococcal food poisoning outbreaks caused by egc-encoded enterotoxins. Toxins. 2015;7:997–1004. Article providing epidemiological data supporting the relevance of newly-described enterotoxins in SFP outbreaks. CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Tang J, Tang C, Chen J, Du Y, Yang X, Wang C, et al. Phenotypic characterization and prevalence of enterotoxin genes in Staphylococcus aureus isolates from outbreaks of illness in Chengdu City. Foodborne Pathog Dis. 2011;8:1317–20.CrossRefPubMedGoogle Scholar
  61. 61.
    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;78:6637–42.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    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;115:369–75.CrossRefPubMedGoogle Scholar
  63. 63.
    Johler S, Sihto H-M, Macori G, Stephan R. Sequence variability in staphylococcal enterotoxin genes seb, sec, and sed. Toxins. 2016;8:169.CrossRefPubMedCentralGoogle Scholar
  64. 64.
    Borst DW, Betley MJ. Phage-associated differences in staphylococcal enterotoxin a gene (sea) expression correlate with sea allele class. Infect Immun. 1994;62:113–8.PubMedPubMedCentralGoogle Scholar
  65. 65.
    Novick RP. Mobile genetic elements and bacterial toxinoses: the superantigen-encoding pathogenicity islands of Staphylococcus aureus. Plasmid. 2003;49:93–105.CrossRefPubMedGoogle Scholar
  66. 66.
    Balaban N, Rasooly A. Staphylococcal enterotoxins. Int J Food Microbiol. 2000;61:1–10.CrossRefPubMedGoogle Scholar
  67. 67.
    Letertre C, Perelle S, Dilasser F, Fach P. A strategy based on 5′ nuclease multiplex PCR to detect enterotoxin genes sea to sej of Staphylococcus aureus. Mol Cell Probes. 2003;17:227–35.CrossRefPubMedGoogle Scholar
  68. 68.
    Lotter LP, Genigeorgis CA. Deoxyribonucleic acid base composition and biochemical properties of certain coagulase-negative enterotoxigenic cocci. Appl Microbiol. 1975;29:152–8.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Podkowik M, Park JY, Seo KS, Bystrón J, Bania J. Enterotoxigenic potential of coagulase-negative staphylococci. Int J Food Microbiol. 2013;163:34–40.CrossRefPubMedGoogle Scholar
  70. 70.
    Hennekinne J-A, De Buyser M-L, Dragacci S. Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation. FEMS Microbiol Rev. 2012;36:815–36.CrossRefPubMedGoogle Scholar
  71. 71.
    Khambaty FM, Bennett RW, Shah DB. Application of pulsed-field gel electrophoresis to the epidemiological characterization of Staphylococcus intermedius implicated in a food-related outbreak. Epidemiol Infect. 1994;113:75–81.CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Becker H, Bürk C, Märtlbauer E. Staphylokokken-Enterotoxine: Bildung, Eigenschaften und Nachweis. J Verbr Lebensm. 2007;2:171–89.CrossRefGoogle Scholar
  73. 73.
    •• Anonymous. ISO 19020: Microbiology of the food chain—horizontal method for the immunoenzymatic detection of enterotoxins in foodstuffs. 2017. https://www.iso.org/standard/63747.html. First ISO standard for the detection of staphylococcal enterotoxins in foodstuffs.
  74. 74.
    Anonymous. Toolkit for investigation and response to food and waterborne disease outbreaks with a European dimension. European Centre for Disease Prevention and Control. 2017. https://ecdc.europa.eu/en/publications-data/toolkit-investigation-and-response-food-and-waterborne-disease-outbreaks-eu. Accessed 23 Aug 2017.
  75. 75.
    Mossong J, DeCruyenaere F, Moris G, Ragimbeau C, Olinger C, Johler S, et al. Whole genome sequencing as investigative tool in a staphylococcal food poisoning outbreak in Luxembourg, June 2014. Euro Surveill. 2015;20Google Scholar
  76. 76.
    Johler S, Tichaczek-Dischinger PS, Rau J, Sihto H-M, Lehner A, Adam M, et al. Outbreak of staphylococcal food poisoning due to SEA-producing Staphylococcus aureus. Foodborne Pathog Dis. 2013;10:777–81.CrossRefPubMedGoogle Scholar
  77. 77.
    Johler S, Stephan R, Althaus D, Ehling-Schulz M, Grunert T. High-resolution subtyping of Staphylococcus aureus strains by means of Fourier-transform infrared spectroscopy. Syst Appl Microbiol. 2016;39:189–94.CrossRefPubMedGoogle Scholar
  78. 78.
    Asao T, Kumeda Y, Kawai T, Shibata T, Oda H, Haruki K, et al. An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol Infect. 2003;130:33–40.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    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;15:19528.PubMedGoogle Scholar
  80. 80.
    Aires-de-Sousa M, Boye K, de Lencastre H, Deplano A, Enright MC, Etienne J, et al. High interlaboratory reproducibility of DNA sequence-based typing of bacteria in a multicenter study. J Clin Microbiol. 2006;44:619–21.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Frenay HM, Bunschoten AE, Schouls LM, van Leeuwen WJ, Vandenbroucke-Grauls CM, Verhoef J, et al. Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism. Eur J Clin Microbiol Infect Dis. 1996;15:60–4.CrossRefPubMedGoogle Scholar
  82. 82.
    Todd ECD, Greig JD, Bartleson CA, Michaels BS. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 3. Factors contributing to outbreaks and description of outbreak categories. J Food Prot. 2007;70:2199–217.CrossRefPubMedGoogle Scholar
  83. 83.
    Argudín MA, Mendoza MC, Gonzalez-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;78:2930–5.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Kusumaningrum HD, Riboldi G, Hazeleger WC, Beumer RR. Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int J Food Microbiol. 2003;85:227–36.CrossRefPubMedGoogle Scholar
  85. 85.
    Toyofuku H. Harmonization of international risk assessment protocol. Mar Pollut Bull. 2006;53:579–90.CrossRefPubMedGoogle Scholar
  86. 86.
    Schelin J, Wallin-Carlquist N, Cohn MT, Lindqvist R, Barker GC, Rådström P. The formation of Staphylococcus aureus enterotoxin in food environments and advances in risk assessment. Virulence. 2011;2:580–92.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Buchanan RL, Smith JL, Long W. Microbial risk assessment: dose-response relations and risk characterization. Int J Food Microbiol. 2000;58:159–72.CrossRefPubMedGoogle Scholar
  88. 88.
    Lammerding AM, Paoli GM. Quantitative risk assessment: an emerging tool for emerging foodborne pathogens. Emerg Infect Dis. 1997;3:483–7.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Köck R, Ballhausen B, Bischoff M, Cuny C, Eckmanns T, Fetsch A, et al. The impact of zoonotic MRSA colonization and infection in Germany. Berl Munch Tierarztl Wochenschr. 2014;127:384–98.PubMedGoogle Scholar
  90. 90.
    Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen S, et al. Adaptation and emergence of Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio. 2012;3:1–6.CrossRefGoogle Scholar
  91. 91.
    Fitzgerald JR. Livestock-associated Staphylococcus aureus: origin, evolution and public health threat. Trends Microbiol. 2012;20:192–8.CrossRefPubMedGoogle Scholar
  92. 92.
    Köck R, Harlizius J, Bressan N, Laerberg R, Wieler LH, Witte W, et al. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur J Clin Microbiol Infect Dis. 2009;28:1375–82.CrossRefPubMedPubMedCentralGoogle Scholar
  93. 93.
    Cuny C, Köck R, Witte W. Livestock associated MRSA (LA-MRSA) and its relevance for humans in Germany. Int J Med Microbiol. 2013;303:331–7.CrossRefPubMedGoogle Scholar
  94. 94.
    Köck R, Schaumburg F, Mellmann A, Köksal M, Jurke A, Becker K. Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PLoS One. 2013;8:e55040.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    EFSA. Technical specifications on the harmonised monitoring and reporting of antimicrobial resistance in methicillin-resistant Staphylococcus aureus in food-producing animals and food 1. 2012.  https://doi.org/10.2903/j.efsa.2012.2897.
  96. 96.
    European Parliament and Council. Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 On the monitoring of zoonoses and zoonotic agents, amending council decision 90/424/EEC and repealing council directive 92/117/EEC. Off J Eur Union 2001:65–71.Google Scholar
  97. 97.
    Buyukcangaz E, Velasco V, Sherwood JS, Stepan RM, Koslofsky RJ, Logue CM. Molecular typing of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) isolated from animals and retail meat in North Dakota, United States. Foodborne Pathog Dis. 2013;10:608–17.CrossRefPubMedGoogle Scholar
  98. 98.
    de Boer E, Zwartkruis-Nahuis JTM, Wit B, Huijsdens XW, de Neeling AJ, Bosch T. Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol. 2009;134:52–6.CrossRefPubMedGoogle Scholar
  99. 99.
    Hanson BM, Dressler AE, Harper AL, Scheibel RP, Wardyn SE, Roberts LK. Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health. 2011;4:169–74.CrossRefPubMedGoogle Scholar
  100. 100.
    O’Brien AM, Hanson BM, Farina SA, Wu JY, Simmering JE, Wardyn SE. MRSA in conventional and alternative retail pork products. PLoS One. 2012;7:e30092.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Velasco V, Sherwood JS, Rojas-Garcia PP, Logue CM. Multiplex real-time PCR for detection of Staphylococcus aureus, mecA and Panton-valentine Leukocidin (PVL) genes from selective enrichments from animals and retail meat. PLoS One. 2014;9:e97617.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Wendlandt S, Schwarz S, Silley P. Methicillin-resistant Staphylococcus aureus: a food-borne pathogen? Annu Rev Food Sci Technol. 2013;4:117–39.CrossRefPubMedGoogle Scholar
  103. 103.
    Kraushaar B, Ballhausen B, Leeser D, Tenhagen B-A, Käsbohrer A, Fetsch A. Antimicrobial resistances and virulence markers in methicillin-resistant Staphylococcus aureus from broiler and Turkey: a molecular view from farm to fork. Vet Microbiol. 2017;200:25–32.CrossRefPubMedGoogle Scholar
  104. 104.
    Weese JS, Avery BP, Reid-Smith RJ. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat products. Lett Appl Microbiol. 2010;51:338–42.CrossRefPubMedGoogle Scholar
  105. 105.
    Deiters C, Günnewig V, Friedrich AW, Mellmann A, Köck R. Are cases of methicillin-resistant Staphylococcus aureus clonal complex (CC) 398 among humans still livestock-associated? Int J Med Microbiol. 2015;305:110–3.CrossRefPubMedGoogle Scholar
  106. 106.
    • Larsen J, Stegger M, Andersen PS, Petersen A, Larsen AR, Westh H, et al. Evidence for human adaptation and foodborne transmission of livestock-associated methicillin-resistant Staphylococcus aureus. Clin Infect Dis. 2016;63:1349–52. Article making a crucial contribution towards understanding foodborne transmission of LA-MRSA. CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Fetsch A, Kraushaar B, Käsbohrer A, Hammerl JA. Turkey meat as source of CC9/CC398 methicillin-resistant Staphylococcus aureus in humans? Clin Infect Dis. 2017;64:102–3.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.National Reference Laboratory for coagulase-positive staphylococci incl. Staphylococcus aureus, German Federal Institute for Risk Assessment (BfR)BerlinGermany
  2. 2.Institute for Food Safety and Hygiene, Vetsuisse FacultyUniversity of ZurichZurichSwitzerland

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