Prevalence, molecular identification and determination of antibiotic susceptibility of methicillin-resistant Staphylococcus aureus in raw meat

Abstract

Objective: The aim of this study was to determine the prevalence, molecular identification, and antibiotic susceptibility of MRSA in raw meats of retail sale in Balikesir, Turkey. Materials and Methods: A total of 250raw meat samples (beef n=100, chicken n=100, and turkey n=50) were collected from various supermarkets. Mueller-Hinton Broth medium containing 6.5% NaCl was used for pre-enrichment and Baird Parker Agar (BPA) was used as a selective medium. Polymerase Chain Reaction technique was used to confirm the suspected colonies with the nuc gene for S. aureus and the mecA gene for MRSA. Kirby-Bauer standard disc diffusion method was applied for antibiotic susceptibility of MRSA. Results: Of the 250 investigated raw meat samples, 21.2% were positive for S. aureus, which comprised 31% beef, 14% chicken, and 16 %turkey samples. Of the 250 investigated raw meat samples, 4% were positive for MRSA, which comprised 6% beef, 3% chicken, and 2% turkey samples. All MRSA isolates were found to be resistant to penicillin, sulfamethoxazole, trimethoprim, cefoxitin, and oxacillin, but they were susceptible to vancomycin. Conclusion: In recent years, MRSA has been called a zoonotic pathogen that poses a serious risk for food safety and public health. Therefore, we believe that this study will shed light on new studies on the prevalence of MRSA in various animal-originated foods.

Keywords

• Antibiotic susceptibility
• MRSA
• Prevalence
• Raw Meats

References

1. Bauer RW, Kirby MDK, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966; 45:493-496.
2. Bhargava K, Wang X, Donabedian S, Zervos M, de Rocha L, Zhang Y. Methicillin-resistant Staphylococcus aureus in retail meat, Detroit, Michigan, USA. Emerg Infect Dis. 2011; 17:1135-1137.
3. Boost MV, Wong A, Ho J, O'Donoghue M. Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from retail meats in Hong Kong. Foodborne Pathog Dis. 2013; 10:705-710
4. Clinical and Laboratory Standards Institute (CLSI). CLSI Document M07-A9. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically: Approved Standard. 19th ed. Wayne: CLSI; 2012.
5. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth International Supplements; Wayne, PA, USA: CLSI; 2014. p.230.
6. Contreras APC, da Silva, NNS, Ferreira GCD, Ferreira DJ, Almeida DCR. Prevalence of methicillin-resistant Staphylococcus aureus in raw hamburgers and ready-to-eat sandwiches commercialized in supermarkets and fast-food outlets in Brazil. Food Nutr Sci. 2015; 6:1324-1331.
7. Costa WLR, Ferreira JS, Carvalho JS, Cerqueira ES, Oliveira LC, Almeida RCC. Methicillin-Resistant Staphylococcus aureus in Raw Meats and Prepared Foods in Public Hospitals in Salvador, Bahia, Brazil. J Food Sci. 2015: 80:147-150.
8. de Boer E, Zwartkruis-Nahuis JT, Wit B, et al. Prevalence of Methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol. 2009; 134:52-56.

9. Devriese LA, Hommez J. Epidemiology of methicillin-resistant Staphylococcus aureus in dairy herds. Res Vet Sci. 1975; 19:23-27.
10. EFSA (European Food Safety Authority) Assessment of the Public Health significance of methicillin-resistant Staphylococcus aureus (MRSA) in animals and foods. Scientific Opinion of the Panel on Biological Hazards (Question No EFSA-Q-2008-300). EFSA J. (2009) 993:1-73.
11. Feßler AT, Kadlec K, Hassel M, et al. “Characterization of Methicillin-Resistant Staphylococcus aureus Isolates from Food and Food Products of Poultry Origin in Germany”. Appl Environ Microbiol. 2011; 77:7151-7157.
12. Harrison EM, Paterson GK, Holden MT, et al. “Whole genome sequencing identifies zoonotic transmission of MRSA isolates with the novel mecA homologue mecC”. EMBO Mol Med. 2015; 5:509-515.
13. Jackson CR, Davis JA, Barrett JB. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. J Clin Microbiol. 2013; 51:1199-1207.
14. Juhasz-Kaszanyitzky E, Janosi S, Somogyi P, et al. MRSA transmission between cows and humans. Emerg Infect Dis. 2007; 13: 630-632.
15. Karmi M. Prevalence of methicillin-resistant Staphylococcus aureus in poultry meat in Qena, Egypt. Vet. World. 2013; 6:711-715.
16. Klevens RM, Morrison MA, Nadle J, et al. “Invasive methicillin-resistant taphylococcus aureus infections in the United States”. JAMA. 2007; 298:1763-1771.
17. Köck, R, Becker K, Cookson B, et al. Prevalence and characterization of methicillin-resistant Staphylococcus aureus in raw meat in Korea. J Microbiol Biotechnol. 2010; 20:775-778.
18. Kwon NH, Park KT, Jung WK, et al. Characteristics of methicillin resistant Staphylococcus aureus isolated from chicken meat and hospitalized dogs in Korea and their epidemiological relatedness. Vet Microbiol. 2006; 117:304-12.
19. Lim SK, Nam HM, Park HJ. Prevalence and characterization of methicillin resistant Staphylococcus aureus in raw meat in Korea. J Microbiol Biotech. 2010; 20:775-778.
20. Lozano C, López M, Gómezsanz E, Ruizlarrea F, Torres C, Zarazaga M. Detection of methicillin-resistant Staphylococcus aureus ST398 in food samples of animal origin in Spain. J Antimicrob Chemother. 2009; 64:1325-1326.
21. Maes N, Magdalena J, Rottiers S, De Gheldre Y, Struelens MJ. Evaluation of a triplex PCR assay to discriminate Staphylococcus aureus from coagulase-negative staphylococci and determine methicillin-resistance from blood cultures. J Clin Microbiol. 2002; 40:1514-1517.
22. Monecke S, Ruppelt A, Wendlandt S, et al. Genotyping of Staphylococcus aureus isolates from diseased poultry. Vet. Microbiol. 2013; 162:806-812.
23. Nanchi AU, Emele FE, Ukaegbu CO, et al. Prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in raw meat and meat handlers in Onitsha, Nigeria. European Journal of Preventive Medicine, 2014; 2: 9-15.
24. Pesavento G, Ducci B, Comodo N, Lo Nostro A. Antimicrobial resistance profile of Staphylococcus aureus isolated from raw meat: A research for methicillin resistant Staphylococcus aureus (MRSA). Food Control. 2007; 18:196-200.
25. Petersen A, Stegger M, Heltberg O, et al. Epidemiology of methicillin-resistant Staphylococcus aureus carrying the novel mecC gene in Denmark corroborates a zoonotic reservoir with transmission to humans. Clin Microbiol Infect. 2013; 19:16-22.
26. Pu S, Han F, Ge B. Isolation and characterization of methicillin-resistant Staphylococcus aureus strains from Louisiana retail meats. Appl Environ Microbiol. 2009; 75:265-267.
27. Robinson DA, Enright MC. Evolutionary models of the emergence of Methicillin resistant Staphylococcus aureus”, Antimicrob. Agents Chemother. 2003; 47:3926-3934.
28. Smith TC, Pearson N. The emergence of Staphylococcus aureus ST398. Vector Borne Zoonotic Dis. 2011; 11: 327-39.
29. Tiemersma EW, Bronzwaer SL, Lyytikäinen O, et al. Methicillin-resistant Staphylococcus aureus in Europe, 1999-2002. Emerg Infect Dis. 2004; 10:1627-1634.
30. TS 6582-1 EN ISO 6888-1: 2001. Gıda ve hayvan yemlerinin-Mikrobiyolojisi-Koagulaz-Pozitif stafilokokların (Staphyloccus aureus ve diğer türler) sayımı için yatay metot-Bölüm 1: Baird-Parker agar besiyeri kullanarak.
31. Verkade E, Kluytmans J. Livestock-associated Staphylococcus aureus CC398: Animal reservoirs and human infections. Infect Genet Evol. 2014; 21:523-530.
32. Wang X, Tao X, Xia X, et al. Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in retail raw chicken in China. Food Control. 2013; 19:103-106.
33. Yasuda R, Kawano J, Onda H, Takagi M, Shimizu A, Anzai T. Methicillin-resistant coagulase-negative staphylococci isolated from healthy horses in Japan. Am J Vet Res. 2000; 61:1451-1455.