Prevalence, Antimicrobial Resistance, and Genetic Relationship of Methicillin-Resistant Staphylococcus aureus from Meats, Hat-Yai, Thailand
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Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) is a dangerous pathogen that can cause serious illnesses, leading to morbidity and mortality worldwide. Food items, especially meats, can contaminate it. In this study, a total of 100 meat samples were investigated for MRSA. The results demonstrated the MRSA prevalence in meats as 2.84% (4/141 isolates). Three MRSA strains were obtained from pork, while 1 from beef (p-value < 0.05). It was discovered that all 4 MRSA showed the same virulence gene profiles. The α-hemolysis and catalase production were positive for all 4 MRSA strains. Antimicrobial susceptibility assay showed that all but one MRSA strains were resistant to streptomycin, chloramphenicol, and tetracycline. MRSA strain LN-4 from beef was resistant to an extra antimicrobial agent, clindamycin. MRSA typing using BOX-PCR discovered that 3 MRSA strains (LN-1 to LN-3) from pork and 1 (LN-4) from beef were identical in DNA fingerprint, suggesting the close genetic relationship among strains from 2 different meat samples. This study demonstrates the presence of MRSA from meats in the south of Thailand. Even though they exist in low amounts, their virulence traits are thought to be harmful and cause diseases. Thus, MRSA contamination in meats should be immediately paid attention to for public health.
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References
de Sousa, M.A.; Bartzavali, C.; Spiliopoulou, I.; Sanches, S.; Crisóstomo, M.I.; de Lencastre, H. Two international methicillin-resistant Staphylococcus aureus clones endemic in a University hospital in Patras, Greece. Journal of Clinical Microbiology. 2003, 41, 2027-2032. https://doi.org/10.1128/JCM.41.5.2027-2032.2003
Johnson, A.P.; Pearson, A.; Duckworth, G. Surveillance and epidemiology of MRSA bacteraemia in the UK. Journal of Antimicrobial Chemotherapy. 2005, 56, 455-462. https://doi.org/10.1093/jac/dki266
Witte, W.; Strommenger, B.; Cuny, C.; Heuck, D.; Nuebel, U. Methicillin-resistant Staphylococcus aureus containing the Panton-Valentine leucocidin gene in Germany in 2005 and 2006. Journal of Antimicrobial Chemotherapy. 2007, 60, 1258-1263. https://doi.org/10.1093/jac/dkm384
El Karamany, I.M.; Ibrahim, Y.M.; Abouwarda, A.M.; Essam, T.M.; Amin, M.A. Detection of high levels of methicillin and multidrug resistance among clinical isolates of Staphylococcus aureus. African Journal of Microbiology Research. 2013, 7, 1598-1604. https://doi.org/10.5897/AJMR12.2333
Mostafa, S.I. Molecular typing of methicillin resistant Staphylococcus aureus by spa gene polymorphism. African Journal of Microbiology Research. 2013, 7, 755-759. https://doi.org/10.1093/jac/44.suppl_1.31
Carbon, C. Costs of treating infections caused by methicillin-resistant Staphylococci and vancomycin-resistant enterococci. Journal of Antimicrobial Chemotherapy. 1999, 44, 31-36.
Bunnueang, N.; Kongpheng, S.; Yadrak, P.; Rattanachuay, P.; Khianngam, S.; Sukhumungoon, P. Methicillin-resistant Staphylococcus aureus: 1-year collection and characterization from patients in two tertiary hospitals, southern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health. 2016, 47, 234-244.
Jones, T.F.; Kellum, M.E.; Porter, S.S.; Bell, M.; Schaffner, W. An outbreak of community-acquired foodborne illness caused by methicillin-resistant Staphylococcus aureus. Emerging Infectious Diseases. 2002, 8, 82-84. https://doi.org/10.3201/eid0801.010174
Sukhumungoon, P.; Nakaguchi, Y.; Ingviya, N.; Pradutkanchana, J.; Iwade, Y.;Seto, K.; Son, R.; Nishibuchi, M.; Vuddhakul, V. Investigation of stx2+ eae+ Escherichia coli O157: H7 in beef imported from Malaysia to Thailand. International Food Research Journal. 2011, 18(1), 381-386.
Bunnoeng, N.; Themphachana, M.; Pewleang, T.; Kongpheng, S.; Singkhamanan, K.; Saengsuwan, P.; Sukhumungoon, P. High prevalence and molecular characterization of methicillin-resistant Staphylococcus aureus isolated from retailed meats, south Thailand. International Food Research Journal. 2014, 21, 569-576.
Seeyankem, B.; Sae-lim, A.; Puangsiri, W.; Rattanachuay, P.; Sukhumungoon, P. Prevalence, virulence, antibiogram profiles, and genetic relationship of Staphylococcus epidermidis from meat in southern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health. 2019, 50(6), 1108-1117.
Pannuch, M.; Sirikaew, S.; Nakaguchi, Y.; Nishibuchi, M.; Sukhumungoon, P. Quantification of enteropathogenic Escherichia coli from retailed meats. International Food Research Journal. 2014, 21, 547-551.
Sukhumungoon, P.; Hayeebilan, F.; Yadrak, P.; Kanobthammakul, S.; Nakaguchi, Y.; Saengsuwan, P.; Singkhamanan, K. Molecular characterization and relationship of methicillin-resistant Staphylococcus aureus among strains from healthy carriers and university hospital patients, southern Thailand. Southeast Asian Journal of Tropical Medicine and Public Health. 2014, 45, 402-412.
Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing. Clinical and Laboratory Standards Institute, 27th edition, Wayne, USA. 2017.
Versalovic, J.; Schneider, M.; De Bruijn, F.; Lupski, J.R. Genomic fingerprinting of bacteria using repetitive sequence-based polymerase chain reaction. Methods in Molecular and Cellular Biology. 1994, 5(1), 25-40.
Parvin, M.S.; Ali, M.Y.; Talukder, S.; Nahar, A.; Chowdhury, E.H.; Rahman, M.T.; Islam, M.T. Prevalence and multidrug resistance pattern of methicillin resistant S. aureus isolated from frozen chicken meat in Bangladesh. Microorganisms. 2021, 9, 636. https://doi.org/10.3390/microorganisms9030636.
Normanno, G.; Firinu, A.; Virgilio S, Mula, G.; Dambrosio, A.; Poggiu, A.; Decastelli, L.; Mioni, R.; Scuota, S.; Bolzoni, G.; Di Giannatale, E.; Salinetti, A.P.; La Salandra, G.; Bartoli, M.; Zuccon, F.; Pirino, T.; Sias, S.; Parisi, A.; Quaglia, N.C.; Celano, G.V. Coagulase positive Staphylococci and Staphylococcus aureus in food products marketed in Italy. International Journal of Food Microbiology. 2005, 98, 73-79. https://doi.org/10.1016/j.ijfoodmicro.2004.05.008
Boost, M.V.; Wong, A.; Ho, J.; O’Donoghue, M. Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from retail meats in Hong Kong. Foodborne Pathogens and Disease. 2013, 10, 1-6. https://doi.org/10.1089/fpd.2012.1415
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.; Heuvelink, A.E. Prevalence of methicillin-resistant Staphylococcus aureus in meat. International Journal of Food Microbiology. 2009, 134, 52-56. https://doi.org/10.1016/j.ijfoodmicro.2008.12.007
Weese, J.S.; Avery, B.P.; Reid-Smith, R.J. Detection and quantification of methicillin-resistant Staphylococcus aureus (MRSA) clones in retail meat. Letters in Applied Microbiology. 2010, 51, 338-342. https://doi.org/10.1111/j.1472-765X.2010.02901.x
Tanomsridachchai, W.; Changkaew, K.; Changkwanyeun, R.; Prapasawat, W.; Intarapuk, A.; Fukushima, Y.; Yamasamit, N.; Kapalamula, T.F.; Nakajima, C.; Suthienkul, O.; Suzuki, Y. Antimicrobial resistance and molecular characterization of methicillin-resistant Staphylococcus aureus isolated from slaughtered pigs and pork in the central region of Thailand. Antibiotics. 2021, 10, 206. https://doi.org/10.3390/antibiotics10020206
Das, D.; Bishayi, B. Staphylococcal catalase protects intracellularly survived bacteria by destroying H2O2 produced by the murine peritoneal macrophages. Microbial Pathogenesis. 2009, 47, 57-67. https://doi.org/10.1016/j.micpath.2009.04.012
O’Brien, A.M.; Hanson, B.M.; Farina, S.A.; Wu, J.Y.; Simmering, J.E.; Wardyn, S.E.; Forshey, B.M.; Kulick, M.E.; Wallinga, D.B.; Smith, T.C. MRSA in conventional and alternative retail pork products. PloS One. 2012, 7, 1-6. https://doi.org/10.1371/journal.pone.0030092
Jackson, C.R.; Davis, J.A.; Barrett, J.B. Prevalence and characterization of methicillin-resistant Staphylococcus aureus isolates from retail meat and humans in Georgia. Journal of Clinical Microbiology. 2013, 51(4), 1199–1207. https://doi.org/10.1128/JCM.03166-12
Wu, S.; Huang, J.; Zhang, F.; Wu, Q.; Zhang, J.; Pang, R.; Zeng, H.; Yang, X.; Chen, M.; Wang, J.; Dai, J.; Xue, L.; Lei, T.; Wei, X. Prevalence and characterization of food-related methicillin-resistant Staphylococcus aureus (MRSA) in China. Frontiers in Microbiology. 2019, 10, 304. https://doi.org/10.3389/fmicb.2019.00304
Sadiq, A.; Samad, M.; Saddam; Basharat, N.; Ali, S.; Roohulla; Saad, Z.; Khan, A.N.; Ahmad, Y.; Khan, A.; Khan, J. Methicillin-Resistant Staphylococcus aureus (MRSA) in slaughter houses and meat shops in capital territory of Pakistan during 2018–2019. Frontiers in Microbiology. 2020, 11, 577707. https://doi.org/10.3389/fmicb.2020.577707
Chopra, I.; Roberts, M. Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiology and Molecular Biology Reviews. 2001, 65, 232-260. https://doi.org/10.1128/MMBR.65.2.232-260.2001
Geha, D.J.; Uhl, J.R.; Gustaferro, C.A.; Persing, D.H. Multiplex PCR for identification of methicillin-resistant staphylococci in the clinical laboratory. Journal of Clinical Microbiology. 1994, 32, 1768-1772.
Lina, G.; Piémont, Y.; Godail-Gamot, F.; Bes M.; Peter, M.O.; Gauduchon, V.; Vandenesch, F.; Etienne, J. Involvement of Panton-Valentine Leuko¬cidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clinical Infectious Diseases. 1999, 29, 1128-1132. https://doi.org/10.1128/jcm.32.7.1768-1772.1994
Wichelhaus, T.A.; Hunfeld, K.P.; Böddinghaus, B.; Kraiczy, P.; Schäfer, V.; Brade, V. Rapid molecular typing of methicillin-resistant Staphylococcus aureus by PCR-RFLP. Infection Control & Hospital Epidemiology. 2001, 22, 294-298. https://doi.org/10.1086/501903
Monday, S.R.; Bohach, G.A. Use of multiplex PCR to detect classical and newly described pyrogenic toxin genes in Staphylococcal isolates. Journal of Clinical Microbiology. 1999, 37, 3411-3414. https://doi.org/10.1128/JCM.37.10.3411-3414.1999
Zhang, K.; Sparling, J.; Chow, B.L.; Elsayed, S.; Hussain, Z.; Church, D.L.; Gregson, D.B.; Louie, T.; Conly, J.M. New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. Journal of Clinical Microbiology. 2004, 42, 4947-4955. https://doi.org/10.1128/JCM.42.11.4947-4955.2004
