Presence of methicillin-resistant Staphylococcus aureus in slaughterhouse environment, pigs, carcasses, and workers

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Abstract

Introduction: Methicillin-resistant Staphylococcus aureus (MRSA) is a highly resistant and difficult to cure zoonotic microorganism, which makes up a large part of food toxic infections and has shown high prevalence among pig population all over the world. The aim of the study was to establish the occurrence of MRSA in slaughterhouses, evaluate its antimicrobial resistance, and verify whether there are any differences or similarities with reference to other European countries. Material and Methods: A total of 100 pigs, 105 carcasses, 19 workers, and 24 samples from the environment of several slaughterhouses were examined by conventional microbial and molecular methods. Results: In total, 78 MRSA isolates were found. MRSA prevalence in slaughtered pigs varied from 8.0% to 88.6% depending on the slaughterhouse, reaching higher prevalence in slaughterhouses with higher slaughter capacity. In total, 21.1% of all workers were carriers of MRSA and 6.7% of carcasses were contaminated with MRSA. The 98.2% of MRSA isolates were resistant to penicillin, 89.1% to tetracycline, 60.1% to erythromycin, 65.5% to gentamycin, and 15 different spa types were found, among which spa type t01333 was most widespread. Conclusion: The study indicated that MRSA prevalence and spa types differed according to slaughterhouse slaughter capacity and good hygiene practices. Quite high MRSA occurrence among slaughterhouse workers is one of the main factors which increase pork contamination risk.

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  • 1. Agerso Y. Hasman H. Cavaco L.M. Pedersen K Pederen K Aarestrup F.M.: Study of methicillin resistant Staphylococcus aureus (MRSA) in Danish pigs at slaughter and in imported retail meat reveals a novel MRSA type in slaughter pigs. Vet Microbiol 2012 157 246-250.

  • 2. Batisti A. Franco A. Merialdi G. Hasman H. Juresica M. Lorenzetti R. Feltrin F. Zini M. Aerestrup F.M.: Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig finishing holdings. Vet Microbiol 2010 142 361-366.

  • 3. Broens E.M. Graat E.A.M. Van Der Wolf P.J. Van De Giessen A.W. De Jong M.C.M.: Transmission of methicillin resistant Staphylococcus aureus among pigs during transportation from farm to abattoir. Vet J 2011 189 302-305.

  • 4. Burns A. Shore A.C. Brennan G.I. Coleman D.C. Egan M. Fanning S. Galligan M.C. Gibbons J.F. Guttierrez M. Malhotra-Kumar S. Markey B.K. Sabirova J.S. Wang J. Leonard F.C.: A longitudinal study of Staphylococcus aureus colonization in pigs in Ireland. Vet Microbiol 2014 174 3-4.

  • 5. Cockerill F.R. Wikler M.A Alder J. Dudley M.N. Eliopoulos G.M. Ferraro M.J. Hardy D.J. Hecht D.W. Hindler J.A. Patel J.B. Powell M. Swenson J.M. Thomson R. B. Traczewski M.M. Turnidge J.D. Weinstein M.P. Zimm B.L.: Performance Standards for Antimicrobial Disk Susceptibility Tests edited by Clinical and Laboratory Standards Institute Wayne USA 2012 pp. 11-13.

  • 6. Crombe F. Willems G. Dispas M. Hallin M. Denis O. Suetens C. Gordts B. Struelens M. Butaye P.: Prevalence and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus among pigs in Belgium. Microb Drug Resist 2012 18 125-131.

  • 7. Cui S. Li1 J. Hu1 C. Jin1 S. Li F. Guo Y. Ran L. Ma1 Y.: Isolation and characterization of methicillin-resistant Staphylococcus aureus from swine and workers in China. J Antimicrob Chemother 2009 64 680-683.

  • 8. De Neeling A.J. Van Broek M.J. Spalburg E.C. Van Santen- Verheuvel M.G. Dam-Daisz W.D. Boshuizen H.C. Van De Giessen A.W. Van Duijkeren F. Huijsdens H.W.: High prevalence of methicillin resistant Staphylococcus aureus in pigs. Vet Microbiol 2007 122 366-372.

  • 9. Denis O. Suetens C. Hallin M. Catry B. Ramboer I. Dispas M. Willems G. Gordts B. Butaye P. Struelens M.J.: Methicillin-resistant Staphylococcus aureus ST398 in swine farm personnel Belgium. Emerg Infect Dis 2009 15 1098-1101.

  • 10. EFSA: Scientific opinion of the panel on biological hazards on requests from the European commission on assessment of the public health significance of the methicillin-resistant Staphylococcus aureus (MARSA) in animals and foods. EFSA J 2009 993 1-73.

  • 11. Friese A. Schulz J. Hoehle L. Fetsch A. Tenhagen B.A. Hartung J. Roesler U.: Occurrence of MRSA in air and housing environment of pig barns. Vet Microbiol 2012 158 129-135.

  • 12. Gilbert M.J. Bos M.E.H. Duim B. Urlings B.A.P. Heres L. Wagenaar J.A. Heederik D.J.J.: Livestock-associated MRSA ST398 carriage in pig slaughterhouse workers related to quantitative environmental exposure. Occup Environ Med 2012 6 472-478.

  • 13. Guardbassi L. Stegger M. Skov R.: Retrospective detection of methicillin resistant and susceptible Staphylococcus aureus ST398 in Danish slaughter pigs. Vet Microbiol 2007 122 384-386.

  • 14. Huber H. Koller S. Giezendanner N. Stephan R. Zweifel C.: Prevalence and characteristics of methicillin-resistant Staphylococcus aureus in humans in contact with farm animals in livestock and in food of animal origin Switzerland 2009. Euro Surveil 2010.

  • 15. Jordan D. Simon J. Fury S. Moss S. Giffard P. Maiwald M. Southwell P. Barton M.D. Axon J.E. Morris S.G. Trott D.J.: Carriage of methicillin-resistant Staphylococcus aureus by veterinarians in Australia. Aust Vet J 2011 89 152-159.

  • 16. Morcillo A. Castro B. Rodriguez-Alvarez C. Gonzalez J.C. Sierra A. Montesinos M.I. Abreu R. Arias A.: Prevalence and characteristics of methicillin-resistant Staphylococcus aureus in pigs and pig workers in Tenerife Spain. Foodborne Pathog Dis 2013 9 207-210.

  • 17. Moodley A. Lantronico F. Guardbassi L.: Experimental colonization of pigs with methicillin-resistant Staphylococcus aureus (MRSA): insights into the colonization and transmission of livestock-associated MRSA. Epidemiol Infect 2011 139 1594-1600.

  • 18. Munckhof W.J. Nimmo G.R. Schooneveldt J.M. Schlebusch S. Stephens A.J. Williams G. Huygens .F Giffard O.: Nasal carriage of Staphylococcus aureus including communityassociated methicillin-resistant strains in Queensland adults. Clin Micribiol Infect 2009 15 149-155.

  • 19. Nemati M K Lipinska K. Denis U. Deplano O. Struelens M. Devriesa L.A. Pasmans F. Haesebrouck F.: Antimicrobial resistance of old and recent Staphylococcus aureus isolates from poultry: first detection of livestock-associated methicillinresistant strain ST398. Antimicrob Agents Chemother 2008 52 3817-3819.

  • 20. Normanno G. Dambrosio A. Lorusso V. Samolis G. Taranto P. Parisi A.: Methicillin-resistant Staphylococcus aureus (MRSA) in slaughtered pigs and abattoir in Italy. Food Microbiol 2015 51 51-56.

  • 21. O’Brien A.M. Hanson B.M. Farina S.A. Wu J.W. Simmering J.E. Wardyn S.E. Forshey B.M. Kulick M.E. Wallinga D.B. Smith T.S.L.: MRSA in conventional and alternative retail pork products. PLoS One 2013 7 30092.

  • 22. Overesch G. Butner S. Rossano A Perreten V.: The increase of methicillin-resistant Staphylococcus aureus (MRSA) and the presence of an unusual sequence type ST49 in slaughtered pigs in Switzerland. BMC Vet Res 2011 7 30.

  • 23. Pletinckx L. Verhegghe M. Crombe F. Dewulf J. De Blecker Y. Rasschaert G. Butaye P. Goddeeris B.M. De Man I.: Evidence of possible methicillin-resistant Staphylococcus aureus ST398 spread between pigs and other animals and people residing on the same farm. Prevent Vet Med 2013 109 293-303.

  • 24. Sergio D.M. Koh T.H. Hsu L.Y. Ogden B.E. Goh A.L. Chow P.K.: Investigation of methicillin-resistant Staphylococcus aureus in pigs used for research. J Med Microbiol 2007 6 1107-1109.

  • 25. Shopsin B. Gomez M. Montgomery S.O. Smith D.H. Waddington M. Dodge D.E. Bost D.A. Riehman M. Naidich S. Kreiswirth B.N.: Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol 1999 37 3556-3563.

  • 26. Smith T.C. Male M.J. Harper A.L. Kroeger JS. Tinkler G.P. Moritz E.D. Capuano A.W. Herwaldt L.A. Diekema D.J.: Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in Mildwestern USA. Swine and swine workers. PLoS One 2009 4 4258.

  • 27. Tenhagen B.A. Fetsch A. Stuhrenberg A.B. Schleuter G. Guerra B. Hammerl J.A. Hertwig S. Kowall J. Kampe U. Schroeter A. Braunig J. Kasbohrer A. Appel B.: Prevalence of MRSA types in slaughter pigs in different German abattoirs. Vet Rec 2009 165 589-593.

  • 28. Van Cleef B.A.G.L. Verkade E.J.M. Wulf M.W.H. Buiting A.G. Voss A. Huijsdens X.W. Van Pelt W. Mulders M.N. Kluytmans J.A.J.W.: Prevalence of livestock associated MRSA in communities with high pig-densities in the Netherlands. PlosOne 2010 5 9385.

  • 29. Van Cleef B.A.G.L. Broens E.M. Voss A. Huijsdens X.W. Zuchner L. Van Bethem B.H.B. Kluytsmans J.A.J.W. Mulders M.N. Van De Giessen A.W.: High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in the Netherlands. Epidemiol Infect 2010 138 756-763.

  • 30. Van Den Broek I.V. Cleef B.A. Haenen A. Broens E.M. Van Der Wolf P.J. Van Den Broek MJ. Huijsdens X.W. Kluytsmans J.A. Van De Giessen A.W. Tiemersma E.W.: Methicillin-resistant Staphylococcus aureus in people living and working in pig farms. Epidemiol Infect 2009 137 700-708.

  • 31. Wendlandt S. Schwarz S. Silley P.: Methicillin resistant Staphylococcus aureus: food-borne pathogens? Ann Rev Food Sci Technol 2013 4: 117-139.

  • 32. Witte W. Strommenger B. Stanek C. Cunny C.: Methicillinresistant Staphylococcus aureus ST398 in humans and animals. Emerg Infect Dis 2007 13 255-258.

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