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Comparison of Staphylococcus aureus isolates associated with food intoxication with isolates from human nasal carriers and human infections

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Abstract

Staphylococcus aureus represents an organism of striking versatility. While asymptomatic nasal colonization is widespread, it can also cause serious infections, toxinoses and life-threatening illnesses in humans and animals. Staphylococcal food poisoning (SFP), one of the most prevalent causes of foodborne intoxication worldwide, results from oral intake of staphylococcal enterotoxins leading to violent vomiting, diarrhea and cramps shortly upon ingestion. The aim of the present study was to compare isolates associated with SFP to isolates collected from cases of human nasal colonization and clinical infections in order to investigate the role of S. aureus colonizing and infecting humans as a possible source of SFP. Spa typing and DNA microarray profiling were used to characterize a total of 120 isolates, comprising 50 isolates collected from the anterior nares of healthy donors, 50 isolates obtained from cases of clinical infections in humans and 20 isolates related to outbreaks of staphylococcal food poisoning. Several common spa types were found among isolates of all three sources (t015, t018, t056, t084). DNA microarray results showed highly similar virulence gene profiles for isolates from all tested sources. These results suggest contamination of foodstuff with S. aureus colonizing and infecting food handlers to represent a source of SFP.

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References

  1. Kluytmans J, van Belkum A, Verbrugh H (1997) Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev 10(3):505–520

    PubMed  CAS  Google Scholar 

  2. Halablab MA, Hijazi SM, Fawzi MA, Araj GF (2010) Staphylococcus aureus nasal carriage rate and associated risk factors in individuals in the community. Epidemiol Infect 138(5):702–706

    Article  PubMed  CAS  Google Scholar 

  3. Munckhof WJ, Nimmo GR, Carney J, Schooneveldt JM, Huygens F, Inman-Bamber J, Tong E, Morton A, Giffard P (2008) Methicillin-susceptible, non-multiresistant methicillin-resistant and multiresistant methicillin-resistant Staphylococcus aureus infections: a clinical, epidemiological and microbiological comparative study. Eur J Clin Microbiol Infect Dis 27(5):355–364. doi:10.1007/s10096-007-0449-3

    Article  PubMed  CAS  Google Scholar 

  4. Berthelot P, Grattard F, Cazorla C, Passot JP, Fayard JP, Meley R, Bejuy J, Farizon F, Pozzetto B, Lucht F (2010) Is nasal carriage of Staphylococcus aureus the main acquisition pathway for surgical-site infection in orthopaedic surgery? Eur J Clin Microbiol Infect Dis 29(4):373–382. doi:10.1007/s10096-009-0867-5

    Article  PubMed  CAS  Google Scholar 

  5. Kooistra-Smid M, Nieuwenhuis M, van Belkum A, Verbrugh H (2009) The role of nasal carriage in Staphylococcus aureus burn wound colonization. FEMS Immunol Med Microbiol 57(1):1–13

    Article  PubMed  CAS  Google Scholar 

  6. von Eiff C, Becker K, Machka K, Stammer H, Peters G, Grp S (2001) Nasal carriage as a source of Staphylococcus aureus bacteremia. New Engl J Med 344(1):11–16

    Article  Google Scholar 

  7. Wertheim HFL, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JAJW, van Keulen PHJ, Vandenbroucke-Grauls CMJE, Meester MHM, Verbrugh HA (2004) Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet 364(9435):703–705

    Article  PubMed  Google Scholar 

  8. Klevens RM, Morrison MA, Nadle J, Petit S, Gershman K, Ray S, Harrison LH, Lynfield R, Dumyati G, Townes JM, Craig AS, Zell ER, Fosheim GE, McDougal LK, Carey RB, Fridkin SK (2007) Invasive methicillin-resistant Staphylococcus aureus infections in the United States. JAMA 298(15):1763–1771

    Article  PubMed  CAS  Google Scholar 

  9. Doyle M, Beuchat L (2007) Food microbiology: fundamentals and frontiers, 3rd edn. ASM Press, Washington DC

    Google Scholar 

  10. Monecke S, Slickers P, Ehricht R (2008) Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53(2):237–251

    Article  PubMed  CAS  Google Scholar 

  11. Aires-de-Sousa M, Boye K, de Lencastre H, Deplano A, Enright MC, Etienne J, Friedrich A, Harmsen D, Holmes A, Huijsdens XW, Kearns AM, Mellmann A, Meugnier H, Rasheed JK, Spalburg E, Strommenger B, Struelens MJ, Tenover FC, Thomas J, Vogel U, Westh H, Xu J, Witte W (2006) High interlaboratory reproducibility of DNA sequence-based typing of bacteria in a multicenter study. J Clin Microbiol 44(2):619–621

    Article  PubMed  CAS  Google Scholar 

  12. Harmsen D, Claus H, Witte W, Rothganger J, Turnwald D, Vogel U (2003) Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 41(12):5442–5448

    Article  PubMed  CAS  Google Scholar 

  13. Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267

    Article  PubMed  CAS  Google Scholar 

  14. Coombs GW, Monecke S, Ehricht R, Slickers P, Pearson JC, Tan HL, Christiansen KJ, O'Brien FG (2010) Differentiation of clonal complex 59 community-associated methicillin-resistant Staphylococcus aureus in Western Australia. Antimicrob Agents Chemother 54(5):1914–1921

    Article  PubMed  CAS  Google Scholar 

  15. Sakwinska O, Kuhn G, Balmelli C, Francioli P, Giddey M, Perreten V, Riesen A, Zysset F, Blanc DS, Moreillon P (2009) Genetic diversity and ecological success of Staphylococcus aureus strains colonizing humans. Appl Environ Microbiol 75(1):175–183

    Article  PubMed  CAS  Google Scholar 

  16. Ruimy R, Armand-Lefevre L, Barbier F, Ruppe E, Cocojaru R, Mesli Y, Maiga A, Benkalfat M, Benchouk S, Hassaine H, Dufourcq JB, Nareth C, Sarthou JL, Andremont A, Feil EJ (2009) Comparisons between geographically diverse samples of carried Staphylococcus aureus. J Bacteriol 191(18):5577–5583

    Article  PubMed  CAS  Google Scholar 

  17. Melles DC, Tenover FC, Kuehnert MJ, Witsenboer H, Peeters JK, Verbrugh HA, van Belkum A (2008) Overlapping population structures of nasal isolates of Staphylococcus aureus from healthy Dutch and American individuals. J Clin Microbiol 46(1):235–241

    Article  PubMed  CAS  Google Scholar 

  18. Monecke S, Luedicke C, Slickers P, Ehricht R (2009) Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J Clin Microbiol 28(9):1159–1165. doi:10.1007/s10096-009-0752-2

    Article  CAS  Google Scholar 

  19. Wertheim HF, van Leeuwen WB, Snijders S, Vos MC, Voss A, Vandenbroucke-Grauls CM, Kluytmans JA, Verbrugh HA, van Belkum A (2005) Associations between Staphylococcus aureus genotype, infection, and in-hospital mortality: a nested case-control study. J Infect Dis 192(7):1196–1200

    Article  PubMed  Google Scholar 

  20. Luedicke C, Slickers P, Ehricht R, Monecke S (2010) Molecular fingerprinting of Staphylococcus aureus from bone and joint infections. Eur J Clin Microbiol 29(4):457–463. doi:10.1007/S10096-010-0884-4

    Article  CAS  Google Scholar 

  21. Fowler VG Jr, Nelson CL, McIntyre LM, Kreiswirth BN, Monk A, Archer GL, Federspiel J, Naidich S, Remortel B, Rude T, Brown P, Reller LB, Corey GR, Gill SR (2007) Potential associations between hematogenous complications and bacterial genotype in Staphylococcus aureus infection. J Infect Dis 196(5):738–747

    Article  PubMed  Google Scholar 

  22. Wu D, Wang Q, Yang Y, Geng W, Yu S, Yao K, Yuan L, Shen X (2010) Epidemiology and molecular characteristics of community-associated methicillin-resistant and methicillin-susceptible Staphylococcus aureus from skin/soft tissue infections in a children's hospital in Beijing, China. Diagn Microbiol Infect Dis 67(1):1–8

    Article  PubMed  CAS  Google Scholar 

  23. Layer F, Ghebremedhin B, König W, König B (2006) Heterogeneity of methicillin-susceptible Staphylococcus aureus strains at a German University Hospital implicates the circulating-strain pool as a potential source of emerging methicillin-resistant S. aureus clones. J Clin Microbiol 44(6):2179–2185

    Article  PubMed  CAS  Google Scholar 

  24. Bartels MD, Boye K, Rohde SM, Larsen AR, Torfs H, Bouchy P, Skov R, Westh H (2009) A common variant of staphylococcal cassette chromosome mec type IVa in isolates from Copenhagen, Denmark, is not detected by the BD GeneOhm methicillin-resistant Staphylococcus aureus assay. J Clin Microbiol 47(5):1524–1527

    Article  PubMed  Google Scholar 

  25. Khandavilli S, Wilson P, Cookson B, Cepeda J, Bellingan G, Brown J (2009) Utility of spa typing for investigating the local epidemiology of MRSA on a UK intensive care ward. J Hosp Infect 71(1):29–35

    Article  PubMed  CAS  Google Scholar 

  26. Lamers RP, Stinnett JW, Muthukrishnan G, Parkinson CL, Cole AM (2011) Evolutionary analyses of Staphylococcus aureus identify genetic relationships between nasal carriage and clinical isolates. PLoS One 6(1):e16426. doi:10.1371/journal.pone.0016426

    Article  PubMed  CAS  Google Scholar 

  27. Melles DC, Taylor KL, Fattom AI, van Belkum A (2008) Serotyping of Dutch Staphylococcus aureus strains from carriage and infection. FEMS Immunol Med Microbiol 52(2):287–292. doi:10.1111/j.1574-695X.2008.00376.x

    Article  PubMed  CAS  Google Scholar 

  28. Salmenlinna S, Lyytikainen O, Vainio A, Myllyniemi AL, Raulo S, Kanerva M, Rantala M, Thomson K, Seppanen J, Vuopio J (2010) Human cases of methicillin-resistant Staphylococcus aureus CC398, Finland. Emerg Infect Dis 16(10):1626–1629

    PubMed  Google Scholar 

  29. Letertre C, Perelle S, Dilasser F, Fach P (2003) A strategy based on 5' nuclease multiplex PCR to detect enterotoxin genes sea to sej of Staphylococcus aureus. Mol Cell Probes 17(5):227–235

    Article  PubMed  CAS  Google Scholar 

  30. al Bustan MA, Udo EE, Chugh TD (1996) Nasal carriage of enterotoxin-producing Staphylococcus aureus among restaurant workers in Kuwait City. Epidemiol Infect 116(3):319–322

    Article  PubMed  Google Scholar 

  31. Straub JA, Hertel C, Hammes WP (1999) A 23S rDNA-targeted polymerase chain reaction-based system for detection of Staphylococcus aureus in meat starter cultures and dairy products. J Food Prot 62:1150–1156

    PubMed  CAS  Google Scholar 

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Acknowledgements

We thank Reinhard Zbinden and the Institute of Medical Microbiology, University of Zurich, for supplying the S. aureus isolates obtained from clinical cases of infection. We thank Barbara Schalch and the Bavarian Authorities for Health and Food Safety, Alfred Binder and the Medical Department of the German Federal Armed Forces, as well as Jean-Marie Pasquier and the Cantonal Laboratory Fribourg (Fribourg, Switzerland) for supplying isolates associated with outbreaks of staphylococcal food poisoning.

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Authors and Affiliations

  1. Institute for Food Safety and Hygiene, Vetsuisse Faculty University of Zurich, Winterthurerstrasse 272, CH-8057, Zurich, Switzerland

    L. Wattinger, R. Stephan & S. Johler

  2. Robert Koch Institute, Wernigerode Branch, Burgstrasse 37, 38855, Wernigerode, Germany

    F. Layer

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  1. L. Wattinger
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  2. R. Stephan
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  3. F. Layer
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  4. S. Johler
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Correspondence to S. Johler.

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Wattinger, L., Stephan, R., Layer, F. et al. Comparison of Staphylococcus aureus isolates associated with food intoxication with isolates from human nasal carriers and human infections. Eur J Clin Microbiol Infect Dis 31, 455–464 (2012). https://doi.org/10.1007/s10096-011-1330-y

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  • DOI: https://doi.org/10.1007/s10096-011-1330-y

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