Antibiotic Resistance Gene Profiles of Staphylococcus aureus Isolated From Foods of Animal Origin

Bu çalışmada hayvansal gıdalardan izole edilen Staphylococcus aureus izolatlarının antibiyotik dirençlilik ve ilgili gen profillerinin araştırılması amaçlanmıştır. Besin Hijyeni ve Teknolojisi laboravuarımızda yer alan kültür koleksiyonunda, 2009 ve 2012 yılları arasında toplanan 95 S. aureus izolatları, fenotipik testler ve PCR ile doğrulanmıştır. İzolatların antibiyotiklere duyarlılıkları disk difüzyon testi ile, minimal inhibitor konsantrasyonları ise E test ile incelenmiştir. Ayrıca çalışmada PCR, blaZ, ermA, ermC, tetK, tetM, mecA, VanA, VanB, VatA, VatB ve aacA-aphD genlerinin varlığını tespit etmek amacıyla kullanılmıştır. Testler sonunda penisilin, tetrasiklin, vankomisin, eritromisin, sefoksitin, gentamisin ve quinupristin-dalfopristin antibiyotiklerine karşı direnç oranları sırasıyla %81.1, %28.4, %18.9, %17.9, %9.4, %9.4 ve %3.2 olarak bulunmuştur. E test sonuçları ile disk difüzyon bulguları birbiri ile uyumlu bulunmuştur. S. aureus izolatlarının çoklu ilaç direnci %29.5 bulunmuştur. Vankomisin dışında izolatların antibiyotiklere dirençlilikleri hususunda PCR ile konvansiyonel metotlar arasında uyum tespit edilmiştir. Ayrıca test edilen tüm izolatların en az bir antibiyotik için gen bulundurduğu gözlenmiştir. Sonuç olarak, veteriner pratikte gereksiz antibiyotik kullanımını kontrol etmek için daha etkin uygulamalar izlenmelidir ve çoklu ilaç direncine sahip S. aureus izolatlarının yayılımını ve bulaşını azaltmak için uygun kontrol önlemlerinin uygulanması gerekmektedir

HHayvansal Gıdalardan İzole Edilen Staphylococcus aureus’ların Antibiyotik Dirençlilik Gen Profilleri

In this study, the investigation of the antibiotic resistance gene profiles of Staphylococcus aureus isolates from foods of animal origin was aimed. Totally, 95 S. aureus strains, obtained during a period between 2009 and 2012, from culture collection of the Food Hygiene and Technology Laboratory, were examined. The isolates were confirmed by phenotypic tests and PCR. The antibiotic susceptibilities of the isolates were analyzed by disc diffusion method and the minimal inhibition concentrations of the antibiotics were determined by E test. PCR were also utilized for determining the presence of resistance genes including blaZ, ermA, ermC, tetK, tetM, mecA, VanA, VanB, VatA, VatB and aacA-aphD. Resistance to penicillin, tetracycline, vancomycin, erythromycin, cefoxitin, gentamycin and quinupristin-dalfopristin were evident as 81.1%, 28.4%, 18.9%, 17.9%, 9.4%, 9.4% and 3.2% respectively. E test results were compatible with the disc diffusion method. Multidrug resistance was observed from 29.5% of S. aureus isolates. Positive compatibility was observed between conventional methods and PCR for the resistance of the isolates, except for vancomycin. In addition, all of the tested isolates found to include a resistance gene for at least one antibiotic. In conclusion, more efficient interventions must be followed to control the redundant use of antibiotics in veterinary practice. Furthermore, appropriate control measures are needed to be implemented to reduce contamination and the spread of multiresistant S. aureus strains

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  • 1. Brook I, Frazier EH: Clinical features and aerobic and anaerobic microbiological characteristics of cellulites. Arch Surg, 130, 786-792, 1995. DOI: 10.1001/archsurg.1995.01430070108024
  • 2. Hoen B, Alla F, Selton-Suty C, Béguinot I, Bouvet A, Briançon S, Casalta JP, Danchin N, Delahaye F, Etienne J, Le Moing V, Leport C, Mainardi JL, Ruimy R, Vandenesch F: Changing profile of infective endocarditis: results of a 1-year survey in France. JAMA, 288, 75-81, 2002. DOI: 10.1001/jama.288.1.75
  • 3. Javaloyas M, Garcia-Somoza D, Gudiol F: Epidemiology and prognosis of bacteremia: A 10-years study in a community hospital. Scand J Infect Dis, 34, 436-441, 2002. DOI: 10.1080/00365540110080629
  • 4. Gardete S, Tomasz A: Mechanisms of vancomycin resistance in Staphylococcus aureus. J Clin Invest, 124 (7): 2836-2840, 2014. DOI: 10.1172/ JCI68834
  • 5. Kazmierczak Z, Gorski A, Dąbrowska K: Facing antibiotic resistance: Staphylococcus aureus phages as a medical tool. Viruses, 6 (7): 2551-2570, 2014. DOI: 10.3390/v6072551
  • 6. Chambers HF, Deleo FR: Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol, 7 (9): 629-641, 2009. DOI: 10.1038/ nrmicro2200
  • 7. 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, 18, 196-200, 2007. DOI: 10.1016/j.foodcont.2005.09.013
  • 8. Velasco V, Buyukcangaz E, Sherwood JS, Stepan RM, Koslofsky RJ, Logue CM: Characterization of Staphylococcus aureus from humans and a comparison with isolates of animal origin, in North Dakota, United States. PLoS One, 10 (10): e0140497, 2015. DOI: 10.1371/journal. pone.0140497
  • 9. Akindolire MA, Babalola OO, Ateba CN: Detection of antibiotic resistant Staphylococcus aureus from milk: A public health implication. Int J Environ Res Public Health, 12, 10254-10275, 2015. DOI: 10.3390/ ijerph120910254
  • 10. Visnuvinayagam S, Joseph TC, Murugadas V, Chakrabarti R, Lalithaet KV: Status on methicillin resistant and multiple drug resistant Staphylococcus aureus in fishes of Cochin and Mumbai coast, India. J Environ Biol, 36, 571-575, 2015.
  • 11. Fan Y, Li SM, Deng BG, Zhao YX: Prevalence and relevance analysis of multidrug-resistant Staphylococcus aureus of meat, poultry and human origin. Indian J Anim Res, 49 (1): 86-90, 2015. DOI: 10.5958/0976- 0555.2015.00018.7
  • 12. Pyzik E, Marek A: Plasmid profile analysis and evaluation of antibiotic susceptibility of Staphylococcus aureus strains isolated from table chicken eggs. Polish J Vet Sci, 16 (2): 307-312, 2013. DOI: 10.2478/pjvs-2013-0042
  • 13. Sergelidis D, Abrahim A, Anagnostou V, Govaris A, Papadopoulos T, Papa A: Prevalence, distribution, and antimicrobial susceptibility of Staphylococcus aureus in ready-to-eat salads and in the environment of a salad manufacturing plant in Northern Greece. Czech J Food Sci, 30, 285- 291, 2012.
  • 14. Cremonesi P, Luzzana M, Brasca M, Morandi S, Lodi R, Vimercati C, Agnellini D, Caramenti G, Moroni P, Castiglioni B: Development of a multiplex PCR assay for the identification of Staphylococcus aureus enterotoxigenic strains isolated from milk and dairy products. Mol Cell Probes, 19 (5): 299-305, 2005. DOI: 10.1016/j.mcp.2005.03.002
  • 15. Smith EM, Needs PF, Manley G, Green LE: Global distribution and diversity of ovine-associated Staphylococcus aureus. Infect Genet Evol, 22 (100): 208-215, 2014. DOI: 10.1016/j.meegid.2013.09.008
  • 16. Clinical and Laboratory Standards Institute: Clinical and Laboratory Standards Institute Performance standards for antimicrobial susceptibility testing; Twenty-Fourth Informational Supplement. Wayne, PA: Clinical and Laboratory Standards Institute. CLSI document; M100- S24, 2014.
  • 17. Strommenger B, Kettlitz C, Werner G, Witte W: Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol, 41 (9): 4089-4094, 2003. DOI: 10.1128/JCM.41.9.4089-4094.2003
  • 18. Baddour MM, Abuelkheir MM, Fatani AJ: Comparison of mecA polymerase chain reaction with phenotypic methods for the detection of methicillin-resistant Staphylococcus aureus. Curr Microbiol, 55, 473-479, 2007. DOI: 10.1007/s00284-007-9015-6
  • 19. Mehrotra M, Wang G, Johnson WM: Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol, 38 (3): 1032-1035, 2000.
  • 20. Bell JM, Paton JC, Turnidge J: Emergence of vancomycin resistant enterococci in Australia: phenotypic and genotypic characteristics of isolates. J Clin Microbiol, 36, 2187-2190, 1998.
  • 21. Mayrhofer S, Paulsen P, Smulders FJ, Hilbert F: Antimicrobial resistance profile of five major food-borne pathogens isolated from beef, pork and poultry. Int J Food Microbiol, 97, 23-29, 2004. DOI: 10.1016/j. ijfoodmicro.2004.04.006
  • 22. Argudin MA, Mendoza MC, Rodicio MR: Food poisoning and Staphylococcus aureus enterotoxins. Toxins, 2 (7): 1751-1773, 2010. DOI: 10.3390/toxins2071751
  • 23. Pereira V, Lopes C, Castro A, Silva J, Gibbs P, Teixeira P: Characterization for enterotoxin production, virulence factors, and antibiotic susceptibility of Staphylococcus aureus isolates from various foods in Portugal. Food Microbiol, 26, 278-282, 2009. DOI: 10.1016/j. fm.2008.12.008
  • 24. Groves MD, Crouch B, Coombs GW, Jordan D, Pang S, Barton MD, Giffard P, Abraham S, Trott DJ: Molecular epidemiology of methicillinresistant Staphylococcus aureus isolated from Australian veterinarians. PloS One, 11 (1): 0146034, 2016. DOI: 10.1371/journal.pone.0146034
  • 25. Gomes MFR, Bomfim MRQ, Trindade MJV, Farias LM, Auxiliadora M, Carvalho MAR, Serufo JC, Santos SG: Potential spread of methicillin-resistant Staphylococcus aureus recovered from patients with bloodstream infection. Chemo Open Access, 4, 149, 2015. DOI: 10.4172/2167-7700.1000149
  • 26. Adwan GK, Naser J, Alaa A: Molecular detection of nine antibiotic resistance genes in methicillin resistant Staphylococcus aureus isolates. Rom Arch Microbiol Immunol, 73 (1-2): 9-18, 2014.
  • 27. Oksuz L, Dupieux C, Tristan A, Bes M, Etienne J, Gurler N: The high diversity of MRSA clones detected in a University Hospital in Istanbul. Int J Med Sci, 10 (12): 1740-1745, 2013. DOI: 10.7150/ijms.6438
  • 28. Zmantar T, Chaieb K, Abdallah FB, Kahla-Nakbi AB, Hassen AB, Mahdouani K, Bakhrouf A: Multiplex PCR detection of the antibiotic resistance genes in Staphylococcus aureus strains isolated from auricular infections. Folia Microbial, 53 (4): 357-362, 2008. DOI: 10.1007/s12223- 008-0055-5
  • 29. Gao J, Ferreri M, Liu XQ, Chen LB, Su JL, Han B: Development of multiplex polymerase chain reaction assay for rapid detection of Staphylococcus aureus and selected antibiotic resistance genes in bovine mastitic milk samples. J Vet Diagn Invest, 23 (5): 894-901, 2011. DOI: 10.1177/1040638711416964
  • 30. Fluit ADC, Visser MR, Schmitz F: Molecular detection of antimicrobial resistance. Clin Microbiol Rev, 14, 836-871, 2001. DOI: 10.1128/ CMR.14.4.836-871.2001
  • 31. Lina G, Quaglia A, Reverdy ME, Leclercq R, Vandenesch F, Etienne J: Distribution of genes encoding resistance to macrolides, lincosamides, and streptogramins among staphylococci. Antimicrob Agents Chemother, 43 (5): 1062-1066, 1999.
  • 32. Martineau F, Picard FJ, Lansac N, Ménard C, Roy PH, Ouellette M, Bergeron MG: Correlation between the resistance genotype determined by multiplex PCR assays and the antibiotic susceptibility patterns of Staphylococcus aureus and Staphylococcus epidermidis. Antimicrob Agents Chemother, 44 (2): 231-238, 2000.
  • 33. Yang F, Wang Q, Wang X, Wang L, Xiao M, Li X, Li H: Prevalence of blaZ gene and other virulence genes in penicillin-resistant Staphylococcus aureus isolated from bovine mastitis cases in Gansu, China. Turk J Vet Anim Sci, 39 (5): 634-636, 2015. DOI: 10.3906/vet-1504-81
  • 34. Pehlivanoglu F, Yardimci H: Detection of methicillin and vancomycin resistance in Staphylococcus strains isolated from bovine milk samples with mastitis. Kafkas Univ Vet Fak Derg, 18 (5): 849-855, 2012. DOI: 10.9775/ kvfd.2012.6642
  • 35. Turutoglu H, Hasoksuz M, Ozturk D, Yildirim M, Sagnak S: Methicillin and aminoglycoside resistance in Staphylococcus aureus isolates from bovine mastitis and sequence analysis of their mecA genes. Vet Res Commun, 33, 945-956, 2009. DOI: 10.1007/s11259-009-9313-5
  • 36. Sareyyupoglu B, Cantekin Z, Akan M: Mastitisli sütlerden izole edilen stafilokoklarda metisilin direncinin fenotipik ve genotipik belirlenmesi. VII. Ulusal Veteriner Mikrobiyoloji Kongresi, 26-28 Eylül, Antalya, Turkey, 2006.
  • 37. Kumar R, Yadav BR, Singh RS: Genetic determinants of antibiotic resistance in Staphylococcus aureus isolates from milk of mastitic crossbred cattle. Curr Microbiol, 60 (5): 379-386, 2010. DOI: 10.1007/ s00284-009-9553-1
  • 38. Moon JS, Lee AR, Kang HM, Lee ES, Kim MN, Paik YH, Park YH, Joo YS, Koo HC: Phenotypic and genetic antibiogram of methicillin-resistant staphylococci isolated from bovine mastitis in Korea. J Dairy Sci, 90, 1176- 1185, 2007. DOI: 10.3168/jds.S0022-0302(07)71604-1
  • 39. Fessler AT, Kadlec K, Hassel M, Hauschild T, Eidam C, Ehricht R, Schwarz S: Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl Environ Microbiol, 77 (20): 7151-7157, 2011. DOI: 10.1128/AEM.00561-11
  • 40. Chambers HF: Methicillin resistance in staphylococci: Molecular and biochemical basis and clinical implications. Clin Microbiol Rev, 10, 781- 791, 1997.
  • 41. Abulreesh HH: Absence of vancomycin-resistance genes in Staphylococcus aureus isolated from potable water. J Public Health Epidemiol, 6 (2): 70-75, 2014. DOI: 10.5897/JPHE2013.0606
  • 42. Turkyilmaz S, Tekbiyik S, Oryasin E, Bozdogan B: Molecular epidemiology and antimicrobial resistance mechanisms of methicillin resistant Staphylococcus aureus isolated from bovine milk. Zoonoses Public Health, 57, 197-203, 2010. DOI: 10.1111/j.1863-2378.2009.01257.x
  • 43. McMillan K, Moore SC, McAuley CM, Fegan N, Fox EM: Characterization of Staphylococcus aureus isolates from raw milk sources in Victoria, Australia. BMC Microbiol, 16, 169, 2016. DOI: 10.1186/s12866- 016-0789-1
  • 44. Simeoni D, Rizzotti L, Cocconcelli P, Gazzola S, Dellaglio F, Torriani S: Antibiotic resistance genes and identification of staphylococci collected from the production chain of swine meat commodities. Food Microbiol, 25 (1): 196-201, 2008. DOI: 10.1016/j.fm.2007.09.004
  • 45. Geisel R, Schmitza FJ, Thomasa BL, Bernsa G, Zetschec O, Ulrichc B, Fluitb AC, Labischinskyd H, Wittee W: Emergence of heterogeneous intermediate vancomycin resistance in Staphylococcus aureus isolates in the Düsseldorf area. J Antimicrob Chemother, 43, 846-848, 1999. DOI: 10.1093/jac/43.6.846
  • 46. Hiramatsu K: Vancomycin-resistant S. aureus: A new model of antibiotic resistance. Lancet Infect Dis, 1, 147-155, 2001. DOI: 10.1016/ S1473-3099(01)00091-3
  • 47. Gao J, Yu FQ, Luo LP, He JZ, Hou RG, Zhang HQ, Li SM, Su JL, Han B: Antibiotic resistance of Streptococcus agalactiae from cows with mastitis. Vet J, 194, 423-424, 2012. DOI: 10.1016/j.tvjl.2012.04.020
  • 48. Croes S, Deurenberg RH, Boumans MLL, Beisser PS, Neef C, Stobberingh EE: Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiol, 9, 229, 2009. DOI: 10.1186/1471-2180-9-229
  • 49. Gow SP, Waldner CL, Harel J, Boerlin P: Associations between antimicrobial resistance genes in fecal generic Escherichia coli isolates from cow-calf herds in western Canada. Appl Environ Microbiol, 74 (12): 3658-3666, 2008. DOI: 10.1128/AEM.02505-07
  • 50. Saadat S, Solhjoo K, Norooz-Nejad MJ, Kazemi A: vanA and vanB positive vancomycin-resistant Staphylococcus aureus among clinical isolates in Shiraz, South of Iran. Oman Med J, 29 (5): 335, 2014. DOI: 10.5001/omj.2014.90
  • 51. Salih MA, Abdalla AM, Masri MAR: Detection of erythromycin resistance genes erm (A), erm (B), erm (C) and msr (A) in Staphylococcus Nasal carriers in Khartoum State. Nature Sci, 12 (4): 106-110, 2014.
  • 52. Elbargisy RM, Rizk DE, Abdel-Rahman SH: Toxin gene profile and antibiotic resistance of Staphylococcus aureus isolated from clinical and food samples in Egypt. African J Microbiol Res, 10 (13): 428-437, 2016. DOI: 10.5897/AJMR2015.7927
  • 53. Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, Pearce K, Foster JT, Bowers J, Driebe EM, Engelthaler DM, Keim PS, Price LB: Multidrug-rResistant Staphylococcus aureus in US meat and poultry. Clin Infect Dis, 52 (10): 1227-1230, 2011. DOI: 10.1093/cid/cir181
Kafkas Üniversitesi Veteriner Fakültesi Dergisi-Cover
  • ISSN: 1300-6045
  • Yayın Aralığı: Yılda 6 Sayı
  • Başlangıç: 1995
  • Yayıncı: Kafkas Üniv. Veteriner Fak.
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