DOI QR코드

DOI QR Code

Molecular Typing and Antimicrobial Susceptibility of Staphylococcus aureus Strains Isolated from Raw Milk, Cheese, Minced Meat, and Chicken Meat Samples

  • Can, Hayriye Yesim (Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Mustafa Kemal University) ;
  • Elmali, Mehmet (Department of Food Hygiene and Technology, Faculty of Veterinary Medicine, Mustafa Kemal University) ;
  • Karagoz, Alper (Microbiology Reference Laboratories Department, Public Health Institutes of Turkey)
  • 투고 : 2016.05.20
  • 심사 : 2017.01.19
  • 발행 : 2017.04.30

초록

The objectives of this study were: i) to detect the presence of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in raw milk, cheese, beef minced meat, and chicken meat samples; ii) to evaluate the antimicrobial susceptibility of the isolates; and iii) to determine clonal relation among the isolates by using pulsed-field gel electrophoresis (PFGE) method. Therefore, a total of 160 food samples were randomly collected between August 2014 and May 2015 in Hatay province, located in the southern Turkey. Twenty (12.5%) of the samples were found to be contaminated with S. aureus. A total of 40 isolates from the 20 positive samples were confirmed to be S. aureus by multiplex PCR based on 16S rRNA and nuc gene. The mec A gene was not detected in any of the S. aureus strains. In the present study, 39 out of 40 (97.5%) isolates were found to be resistant to one or more antibiotics. All of isolates were susceptible to gentamicin, oxacillin, and vancomycin. The highest resistance rate was detected in penicillin (95%) and ampicillin (92.5%), followed by tetracycline (30%), erythromycin (20%), ciprofloxacin (12.5%). Nine major patterns were determined by PFGE. In 6 of these patterns, thirty-six strains (90%) had identical PFGE profiles.

키워드

참고문헌

  1. Bennett, R. W. and Lancette, G. A. (1998) Staphylococcus aureus. Chapter 12. In FDA's Bacteriological Analytical Manual (8th ed.). (Revision A).
  2. Brakstad, O. G., Aasbakk, K., and Maeland, J. A. (1992) Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J. Clin. Microbiol. 30, 1654-1660.
  3. Can, H. Y. and Celik, T. H. (2012) Detection of enterotoxigenic and antimicrobial resistant S. aureus in Turkish cheeses. Food Control 24, 100-103.
  4. Clinical and Laboratory Standards Institute (CLSI) (2013) Performance standards for antimicrobial susceptibility testing; twenty-third informational supplement. CLSI document M 100-S23, Wayne, PA.
  5. Crago, B., Ferrato, C., Drews, S. J., Svenson, L. W., Tyrrell, G., and Louie, M. (2012) Prevalence of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) in food samples associated with foodborne illness in Alberta, Canada from 2007 to 2010. Food Microbiol. 32, 202-205. https://doi.org/10.1016/j.fm.2012.04.012
  6. de Boer, E., Zwartkruis-Nahuis, J. T. M., Wit, B., Huijsdens, X. W., de Neeling, A. J., Bosch, T., Van Oosterom, R. A. A., Vila, A., and Heuvelink, A. E. (2009) Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int. J. Food Microbiol. 134, 52-56. https://doi.org/10.1016/j.ijfoodmicro.2008.12.007
  7. Ertas, N., Gonulalan, Z., Yildirim, Y., and Kum, E. (2010) Detection of Staphylococcus aureus enterotoxins in sheep cheese and dairy desserts by multiplex PCR technique. Int. J. Food Microbiol. 142, 74-77. https://doi.org/10.1016/j.ijfoodmicro.2010.06.002
  8. Gundogan, N., Citak, S., Yucel, N., and Devren, A. (2005) A note on the incidence and antibiotic resistance of Staphylococcus aureus isolated from meat and chicken samples. Meat Sci. 69, 807-810. https://doi.org/10.1016/j.meatsci.2004.10.011
  9. Gücükoğlu, A., Çadirci, Ö., Terzi, G., Kevenk, T. O., and Alişarli, M. (2013) Determination of enterotoxigenic and methicillin resistant Staphylococcus aureus in ice cream. J. Food Sci. 78, M738-M741. https://doi.org/10.1111/1750-3841.12093
  10. Gucukoglu, A., Kevenk, T. O., Uyanik, T., Cadirci, O., Terzi, G., and Alisarli, M. (2012) Detection of enterotoxigenic Staphylococcus aureus in raw milk and dairy products by multiplex PCR. J. Food Sci. 77, M620-M623. https://doi.org/10.1111/j.1750-3841.2012.02954.x
  11. Gundogan, N., Citak, S., and Turan, E. (2006) Slime production, DNase activity and antibiotic resistance of Staphylococcus aureus isolated from raw milk, pasteurised milk and ice cream samples. Food Control 17, 389-392. https://doi.org/10.1016/j.foodcont.2005.01.006
  12. Hanson, B. M., Dressler, A. E., Harper, A. L., Scheibel, R. P., Wardyn, S. E., Roberts, L. K., Kroeger, J. S., and Smith, T. C. (2011) Prevalence of Staphylococcus aureus and methicillinresistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J. Infection Public Health 4, 169-174. https://doi.org/10.1016/j.jiph.2011.06.001
  13. Hu, S., Liu, S., Hu, W., Zheng, T., and Xu, J. (2013) Molecular biological characteristics of Staphylococcus aureus isolated from food. Eur. Food Res. Technol. 236, 285-291. https://doi.org/10.1007/s00217-012-1887-4
  14. Jay, J. M., Loessner, M. J., and Golden, D. A. (2005) Staphylococal gastroenteritis. In Jay, J. M., Loessner, M. J., & Golden, D. A. (Eds.), Modern food microbiology, Springer Science, USA. 545-566.
  15. Keyvan, E. and Özdemir, H. (2016) Occurrence, enterotoxigenic properties and antimicrobial resistance of Staphylococcus aureus on beef carcasses. Vet. J. Ankara Uni. 63, 17-23.
  16. McEntire, J. C. and Montville, T. J. (2007) Antimicrobial resistance. In Doyle, M. P. & Beuchat, L. R. (Eds.), Food Microbiology: Fundamentals and Frontiers, ASM Press, WA. pp.23-34.
  17. Mehrotra, M., Wang, G., and Johnson, W. M. (2000) Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J. Clin. Microbiol. 38, 1032-1035.
  18. Monday, S. R. and Bohach, G. A. (1999) Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in staphylococcal isolates. J. Clin. Microbiol. 37, 3411-3414.
  19. Muehlherr, J. E., Zweifel, C., Corti, S., Blanco, J. E., and Stephan, R. (2003): Microbiological quality of raw goat's and ewe's bulk-tank milk in Switzerland. J. Dairy Sci. 86, 3849-3856. https://doi.org/10.3168/jds.S0022-0302(03)73992-7
  20. Mulvey, M. R., Chui, L., Ismail, J., Louie, L., Murphy, C., Chang, N., Alfa, M., and the Canadian Committee for the Standardization of Molecular Methods (2001) Development of a Canadian standardized protocol for subtyping methicillin-resistant Staphylococcus aureus using pulsed-field gel electrophoresis. J. Clin. Microbiol. 39, 3481-3485. https://doi.org/10.1128/JCM.39.10.3481-3485.2001
  21. Normanno, G., la Salandra, G., Dambrosio, A., Quaglia, N. C., Corrente, M., Parisi, A., Santagada, G., Firinu, A., Crisetti, E., and Celano, G. V. (2007) Occurrence, characterization and antimicrobial resistance of enterotoxigenic Staphylococcus aureus isolated from meat and dairy products. Int. J. Food Microbiol. 115, 290-296. https://doi.org/10.1016/j.ijfoodmicro.2006.10.049
  22. Peles, F., Wagner, M., Varga, L., Hein, I., Rieck, P., Gutser, K., Kereszturi, P., Kardos, G., Turcsanyi, I., Beri, B., and Szabo, A. (2007) Characterization of Staphylococcus aureus strains isolated from bovine milk in Hungary. Int. J. Food Microbiol. 118, 186-193. https://doi.org/10.1016/j.ijfoodmicro.2007.07.010
  23. Pereira, V., Lopes, C., Castro, A., Silva, J., Gibbs, P., and Teixeira, P. (2009) Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiol. 26, 278-282. https://doi.org/10.1016/j.fm.2008.12.008
  24. Pesavento, G., Ducci, B., Comodo, N., and lo Nostro, A. (2007) Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA). Food Control 18, 196-200. https://doi.org/10.1016/j.foodcont.2005.09.013
  25. Seo, K. S. and Bohach, G. A. (2007) Foodborne pathogenic bacteria. Staphylococcus aureus. In Doyle, M. P. & Beuchat, L. R. (Eds.), Food microbiology, fundamentals and frontiers, ASM Press, WA. pp. 493-518.
  26. Smith, T. L. and Jarvis, W. R. (1999) Antimicrobial resistance in Staphylococcus aureus. Microbes Infect. 1, 795-805. https://doi.org/10.1016/S1286-4579(99)80082-3
  27. Tang, J., Zhang, R., Chen, J., Zhao, Y., Tang, C., Yue, H., Li, J., Wang, Q., and Shi, H. (2015) Incidence and characterization of Staphylococcus aureus strains isolated from food markets. Ann. Microbiol. 65, 279-286. https://doi.org/10.1007/s13213-014-0859-2
  28. Tenover, F. C., Arbeit, R., Goering, R. V., Mickelsen, P. A., Murray, B. E., Persing, D. H., and Swaminathan, B. (1995) Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J. Clin. Microbiol. 33, 2233-2239.

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