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Antimicrobial Resistance of Enterococcus Species Isolated from Chicken in Turkey

  • Sanlibaba, Pinar (Department of Food Engineering, Faculty of Engineering, Ankara University) ;
  • Tezel, Basar Uymaz (Bayramic Vocational School, Food Technology Program, Canakkale Onsekiz Mart University) ;
  • Senturk, Esra (Department of Food Engineering, Faculty of Engineering, Ankara University)
  • Received : 2017.07.10
  • Accepted : 2018.03.28
  • Published : 2018.04.30

Abstract

The aim of the present work was to provide information about Enterococcus strains isolated from pre-packaged chicken samples in Ankara (Turkey), focusing on their prevalence, phenotypic and genotypic characteristics, and antibiotic resistance. We report the first study on the occurrence of antibiotic resistant enterococci in pre-packaged chicken samples in Ankara. A total of 97 suspicious enterococcal isolates were identified from 122 chicken samples. All isolates were identified to species level by phenotypic and molecular methods. In the 16S rDNA sequence analysis, Enterococcus faecium (61.85%) and Enterococcus faecalis (38.15%) were found to be the most frequently detected Enterococcus spp. Of the 97 isolates tested for hemolytic activity, 12.37% enterococcal strains were ${\beta}$-hemolytic. ${\beta}$-Hemolysin was most prevalent among E. faecium (58.33%) compared to E. faecalis (41.66%). Disk diffusion method was used for determining of antibiotic resistance. The analysis of the antimicrobial resistance of the 97 Enterococcus isolates revealed that the resistance to kanamycin (98.96%), rifampicin (80.41%) and ampicillin (60.82%) was most frequent. Furthermore, resistance to erythromycin (38.14%) and ciprofloxacin (34.02%) was also observed. The frequencies of resistance to tetracycline (9.27%), penicillin G (8.24%), and chloramphenicol (3.09%), gentamicin (2.06%) and streptomycin (1.03%) were low. None of the isolates was resistant to vancomycin. Multi-drug resistance was found in 97.93% of Enterococcus strains. E. faecium strains showed a more resistant phenotype than E. faecalis strains according to the antibiotic resistance levels. The results of this study indicated that chicken meat is a potential reservoir for the transmission of antibiotic resistance from animals to humans.

Keywords

References

  1. Abouelnaga M, Lamas A, Quintela-Baluja M, Osman M, Miranda JM, Cepeda A, Franco CM. 2016. Evaluation of the extent of spreading of virulence factors and antibiotic resistance in Enterococci isolated from fermented and unfermented foods. Ann Microbiol 66:577-585. https://doi.org/10.1007/s13213-015-1138-6
  2. Aslam M, Diarra MS, Checkley S, Bohaychuck V, Masson L. 2012. Characterization of antimicrobial resistance and virulence genes in Enterococcus spp. isolated from retail meats in Alberta, Canada. Int J Food Microbiol 156:222-230. https://doi.org/10.1016/j.ijfoodmicro.2012.03.026
  3. Barbosa J, Gibbs PA, Teixeira P. 2010. Virulence factors among enterococci isolated from traditional fermented meat products produced in the North of Portugal. Food Control 21:651-656. https://doi.org/10.1016/j.foodcont.2009.10.002
  4. Beasley SS, Saris PEJ. 2004. Nisin-producing Lactococcus lactis strains isolated from human milk. Appl Environ Microbiol 70:5051-5053. https://doi.org/10.1128/AEM.70.8.5051-5053.2004
  5. Belgacem ZB, Abriouel H, Omar NB, Lucas R, Martinez-Canamero M, Galvez A, Manai M. 2010. Antimicrobial activity, safety aspects, and some technological properties of bacteriocinogenic Enterococcus faecium from artisanal Tunisian. Food Control 21:462-470. https://doi.org/10.1016/j.foodcont.2009.07.007
  6. Blaiotta G, Pepe O, Mauiello G, Villani F, AndolfiI R, Moschetti G. 2002. 16S-23S rDNA intergenic spacer region polymorphism of Lactococcus gavriae, Lactococcus raffinolactis and Lactococcus lactis as revealed by PCR and nucleotide sequence analysis. Syst Appl Microbiol 25:520-527. https://doi.org/10.1078/07232020260517652
  7. Bulajic S, Tambur Z, Opacic D, Miljkovic-Selimocic B, Doder R, Cenic-Milosevic D. 2015. Characterization of antibiotic resistance phenotypes and resistance genes in Enterococcus spp. Isolated from cheeses. Arch Biol Sci 67:139-146. https://doi.org/10.2298/ABS140426016B
  8. Camargo CH, Bruder-Nascimento A, Lee SHI, Junior AF, Kaneno R, Rall VLM. 2014. Prevalence and phenotypic characterization of Enterococcus ssp. Isolated from food in Brazil. Braz J Microbiol 45:111-115. https://doi.org/10.1590/S1517-83822014000100016
  9. Carasi P, Jacquot C, Romanin DE, Elie AM, De Antoni GL, Urdaci MC, Serradell MLA 2014. Safety and potential beneficial properties of Enterococcus strains isolated from kefir. Int Dairy J 39:193-200. https://doi.org/10.1016/j.idairyj.2014.06.009
  10. Cancilla MR, Powell IB, Hillier AJ, Davidson BE 1992. Rapid genomic fingerprinting of Lactococcus lactis strains by arbitrarily primed polymerase chain reaction with 32P and fluorescent labels. Appl Environ Microbiol 58:1772-1775.
  11. Cetinkaya F, Mus TE, Soyutemiz GE, Cibik R. 2013. Prevalence and antibiotic resistance of vancomycin-resistant enterococci in animal originated foods. Turk J Vet Anim Sci 37:588-593. https://doi.org/10.3906/vet-1211-34
  12. CLSI (Clinical and Laboratory Standards Institute) 2011. Performance standards for antimicrobial susceptibility testing: Twenty-first informational supplement. M100-S21. Wayne, PA, USA.
  13. Dada AC, Ahmad A, Usup G, Heng LY. 2013. Speciation and antimicrobial resistance of enterococci isolated from recreational beaches in Malaysia. Environ Monit Assess 185:1583-1599. https://doi.org/10.1007/s10661-012-2653-6
  14. Delpech G, Pourcel G, Schell C, Luca MD, Basualdo J, Bernstein J, Grenovero S, Sparo M. 2012. Antimicrobial resistance profiles of Enterococcus faecalis and Enterococcus faecium isolated from artisanal food of animal origin in Argentina. Foodborne Pathog Dis 9:939-944. https://doi.org/10.1089/fpd.2012.1192
  15. Elmaci BS, Tokatli M, Dursun D, O zcelik F, Sanlibaba P. 2015. Phenotypic, genotypic identification of lactic acid bacteria isolated from traditional pickles of the C ubuk region in Turkey. Folia Microbiol 60:241-251. https://doi.org/10.1007/s12223-014-0363-x
  16. Foulquie Moreno MR, Sarantinopoulos P, Tsakalidou E, De Vuyst L. 2006. The role and application of enterococci in food and health. Int J Food Microbiol 106:1-24. https://doi.org/10.1016/j.ijfoodmicro.2005.06.026
  17. Frazzon APG, Gama AB, Hermes V, Bierhals CG, Pereira RI, Guedes AG, D'azevedo P, Frazzon J. 2010. Prevalence of antimicrobial resistance and molecular characterization of tetracycline resistance mediated by tet(M) and tet(L) genes in Enterococcus spp. isolated from food in southern Brazil. World J Microbiol Biotechnol 26:365-370. https://doi.org/10.1007/s11274-009-0160-x
  18. Furlaneto-Maia L, Rocha KR, Henrique FC, Giazzi A, Furlaneto MC. 2014. Antimicrobial resistance in Enterococcus sp. isolated from sof cheese in Southern Brazil. Adv Microbiol 4:175-181. https://doi.org/10.4236/aim.2014.43023
  19. Gaglio R, Couto N, Marques C, Lopes MFS, Moschetti G, Pompa C, Settani L. 2016. Evaluation of antimicrobial resistance and virulence of enterococci from equipment surfaces, raw materials, and traditional cheeses. Int J Food Microbiol 236:107-114. https://doi.org/10.1016/j.ijfoodmicro.2016.07.020
  20. Garrido AM, Galvez A, Pulido RP. 2014. Antimicrobial resistance in enterococci. J Infect Dis Ther 2:150.
  21. Gomes BC, Esteves CT, Palazzo ICV, Darini ALC, Felis GE, Sechi LA, Franco BDGM, De Martinis ECP. 2008. Prevalence and characterization of Enterococcus spp. isolated from Brazilian foods. Food Microbiol. 25:668-675. https://doi.org/10.1016/j.fm.2008.03.008
  22. Guerrero-Ramos E, Cordero J, Molina-Gonzalez D, Poeta P, Igrejas G, Alonso-Calleja C, Capita R. 2016. Antimicrobial resistance and virulence genes in enterococci from wild game meat in Spain. Food Microbiol 53:156-164. https://doi.org/10.1016/j.fm.2015.09.007
  23. Iosifidis E, Evdoridou I, Agakidou E, Chochliourou E, Protonotariou E, Karakoula K, Statthis I, Sofianou D, Drossou-Agakidoou V, Pournaras S, Roilides E. 2013. Vancomycin-resistant Enterococcus outbreak in a neonatal intensive care unit: Epidemiology, molecular analysis and risk factors. Am J Infect Control 41:857-861. https://doi.org/10.1016/j.ajic.2013.02.005
  24. Jahan M, Krause DO, Holley RA. 2013. Antimicrobial resistance of Enterococcus species from meat and fermented meat products isolated by a PCR-based rapid screening method. Int J Food Microbiol. 163:89-95. https://doi.org/10.1016/j.ijfoodmicro.2013.02.017
  25. Jahan M, Holley RA. 2016. Transfer of antibiotic resistance from Enterococcus faecium of fermented meat origin to Listeria monocytogenes and Listeria innocua. Lett App Microbiol 62:304-310. https://doi.org/10.1111/lam.12553
  26. Jamet E, Akary E, Poisson AAJF, Bertrand-Chamba X, Serror P. 2012. Prevalence and characterization of antibiotic-resistant Enterococcus faecalis in French cheeses. Food Microbiol 31:191-198. https://doi.org/10.1016/j.fm.2012.03.009
  27. Kasimoglu-Dogru A, Gencay YE, Ayaz ND. 2010. Prevalence and antibiotic resistance profiles of Enterococcus species in chicken at slaughter level; Absence of vanA and vanB genes in E. faecalis and E. faecium. Res Vet Sci 89:153-158. https://doi.org/10.1016/j.rvsc.2010.02.005
  28. Khan SA, Nawaz MS, Khan AA, Hopper SL, Jones RA, Cerniglia CE. 2005. Molecular characterization of multidrugresistant Enterococcus spp. from poultry and dairy farms: Detection of virulence and vancomycin resistance gene markers by PCR. Mol Cell Probes 19:27-34.
  29. Klibi N, Said LB, Jouini A, Slama KB, Lopez M, Sallem RB, Boudabous A, Torres C. 2013. Species distribution, antibiotic resistance and virulence traits in enterococci from meat Tunisia. Meat Sci 93:675-680. https://doi.org/10.1016/j.meatsci.2012.11.020
  30. Kurekci C, Onen P, Yipel M, Asalantas O, Gundogdu A. 2016. Characterization of phenotypic and genotypic antibiotic resistance profile of enterococci from cheeses in Turkey. Korean J Food Sci An 36:352-358. https://doi.org/10.5851/kosfa.2016.36.3.352
  31. Lavova M, Bezekova J, Canigova M, Krocko M, Domig KJ. 2014. Species identification of enterococci by biochemical test and molecular-genetic methods. Potravinarstvo 8:124-129.
  32. LPSN, List of prokaryotic names with stading in nomenclautre: Genus Enterococcus. Available from: http://www.bacterio.net/enterococcus.html. Accessed at Feb 15. 2017.
  33. Mcgowan LL, Jackson CR, Barret JB, Hiott LM, Fedorka-Cray PJ. 2006. Prevalence and antimicrobial resistance of enterococci isolated from retail fruits, vegetables, and meats. J Food Prot 69:2976-2982. https://doi.org/10.4315/0362-028X-69.12.2976
  34. Miller WR, Munita JM, Arias CA. 2014. Mechanisms of antibiotic resistance in enterococci. Expert Rev Anti Infect Ther 12:1221-1236. https://doi.org/10.1586/14787210.2014.956092
  35. Oladipo IC, Sanni AI, Swarnakar S. 2013. Phenotypic and genomic characterization of Enterococcus species from some Nigerian fermented foods. Food Biotechnol 27:39-53. https://doi.org/10.1080/08905436.2012.755627
  36. Pesavento G, Calonico C, Ducci B, Magnanini AA, Lo Nostro A. 2014. Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol 41:1-7. https://doi.org/10.1016/j.fm.2014.01.008
  37. Raafat SA, Abo-Elmagd EK, Awad RA, Hassan EM. 2016. Prevalence of vancomycin-resistant Enterococci in different food samples. Egypt J Med Microbiol 25:47-55. https://doi.org/10.12816/0037021
  38. Robredo B, Singh KV, Baquero F, Murray BE, Torres C. 2000. Vancomycin-resistant enterococci isolated from animals and food. Int J Food Microbiol 54:197-204. https://doi.org/10.1016/S0168-1605(99)00195-6
  39. Sallem RB, Klibi N, Klibi A, Said BL, Dziri R, Boudabous A, Torres C, Slama KB. 2016. Antibiotic resistance and virulence of enterococci isolates from healthy humans in Tunisia. Ann Microbiol 66:717-725. https://doi.org/10.1007/s13213-015-1157-3
  40. Serio A, Paparella A, Chavez-Lopez C, Corsetti A, Suzzi G. 2007. Enterococcus populations in Pecorino Abruzzese cheese: Biodiversity and safety aspects. J Food Protect 70:1561-1568. https://doi.org/10.4315/0362-028X-70.7.1561
  41. Sting R, Richter A, Popp C, Hafez HM. 2013. Occurrence of vancomycin-resistant enterococci in Turkey flocks. Poultry Sci 92:346-351. https://doi.org/10.3382/ps.2012-02652
  42. Talebi M, Sadeghi J, Rahimi F, Pourshafie MR. 2015. Isolation and biochemical fingerprinting of vancomycin-resistant Enterococcus faecium from meat, chicken and cheese. Jundishapur J Microbiol 8:e15815.
  43. Togay SO , Keskin AC , Acik L, Temiz A. 2010. Virulence genes, antibiotic resistance and plasmid profiles of Enterococcus faecalis and Enterococcus faecium from naturally fermented Turkish foods. J Appl Microbiol 109:1084-1092. https://doi.org/10.1111/j.1365-2672.2010.04763.x
  44. Valenzuela AS, Omar NB, Abriouel H, Lopez RL, Veljovic K, Canamero M MM, Topisirovic KL, Galvez A. 2009. Virulence factors, antibiotic resistance, and bacteriocins in enterococci from artisan foods of animal origin. Food Control 20:381-385. https://doi.org/10.1016/j.foodcont.2008.06.004
  45. Vrabec M, Lovayova V, Dudrikova K, Gallo J, Dudrikova E. 2015. Antibiotic resistance and prevalence of Enterococcus spp. and Escherichia coli isolated from bryndza cheese. Ital J Anim Sci 14:609-614.
  46. Yuksel FN, Akcelik N, Akcelik M. 2015. Incidence of antibiotic resistance virulence determinants in Enterococcus faecium and Enterococcus faecalis strains, isolated from traditional cheeses in Turkey. Mol Genet Microbiol Virol 30:206-215. https://doi.org/10.3103/S089141681504014X

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