Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
권호 표지
DOI QR코드

DOI QR Code

Analysis of Antimicrobial Resistance Pattern and Distribution of Multi-drug Efflux Pump Genes and Virulence Genes in Enterococcus faecalis Isolated from Retail Meat in Seoul

서울시내 시판 식육에서 분리한 Enterococcus faecalis의 항생제 내성 유형, 다중약물 유출 펌프 유전자 및 병독성 유전자의 분포도 분석

  • Received : 2016.11.21
  • Accepted : 2017.02.07
  • Published : 2017.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

The aim of this study was to investigate the distribution of genes that encode multi-drug efflux pumps and virulence factors in Enterococcus faecalis isolated from retail meat and antibiotic resistance patterns of these strains. Of the 277 retail meat samples, 93 Enterococcus faecalis were isolated. The strains exhibited resistance to ampicillin (35.5%), chloramphenicol (6.4%), ciprofloxacin (4.3%), erythromycin (18.3%), levofloxacin (0%), quinupristin-dalfopristin (76.3%), tetracycline (45.2%), teicoplanin (0%) and vancomycin (0%). The strains were positive for MFS type eme(A) (100%), ABC type efr(A) (100%), ABC type efr(B) (98.9%) and ABC type lsa (91.4%) efflux pump gene. The strains were positive for gelE (68.8%), ace (90.3%), asa1 (47.3%), efaA (91.4%) and esp (12.9%) virulence gene. This research will help to assess the hazards associated with the occurrence of drug resistance among enterococci from retail meat. Therefore, it is necessary to monitor enterococcus spp. isolated from retail meat continuously.

본 연구는 서울시내에서 시판중인 식육에서 E. faecalis를 분리하고 이 균들의 항생제 내성 패턴, 항생제 유출 펌프 유전자 및 병독성 유전자의 분포를 분석하였다. 총 277개의 식육시료에서 93균주의 E. faecalis 를 분리하였다. 이 균주들의 항생제 내성비율은 ampicillin에는 35.5%, chloramphenicol에 6.4%, ciprofloxacin에 4.3%, eryhtromycin에 18.3%, quinupristin-dalfopristin에 76.3%, tetracycline에 45.2%의 내성이었으며 levofloxacin, teiconplanin 및 vancomycin에는 모든 균이 감수성이었다. 약물 유출펌프인 MFS 타입의 eme(A)와 ABC 타입의 efr(A)유전자는 모든 균주(100%)에서 확인되었으며 efr(B)는 98.9%, lsa는 91.4%의 균주에서 확인되었다. 병독성 인자인 gel(E)는 68.8%, ace는 90.3%, asa1는 47.3%, efaA는 91.4%, esp는 12.9%의 균주에서 확인되었다. 본 연구는 시판 식육에서 분리한 지표 미생물의 하나인 E. faecalis의 항생제 내성, 약물유출 펌프 및 병독서 유전자의 분포를 분석한 연구로 지속적인 모니터링을 하여야 할 것으로 사료된다.

Keywords

References

  1. Devriese, L.A., Collins, M.D., Wirth, R.: The genus Enterococcus. 2nd edn., vol. 2, Springer-Verlag. NewYork. pp. 1465-1478 (1992).
  2. Flahaut, S., Boutibonnes, P., Auffray, Y.: Les enterocoques dans I'environnement proche de I'homme. Canad. J. Microbio., 43, 699-708 (1997). https://doi.org/10.1139/m97-101
  3. Malani, P.N., Kauffman, C.A., Zervos, M.J.: Enterococcal disease, epidemiology and treatment. In: Gilmore, M. S. (Ed.) The Enterococci: pathogenesis, molecular biology and antimicrobtiotic resistance. Amercan Society for Mcirobiology. Washington, DC pp. 385-408 (2002).
  4. Suzzi, G., Caruso, M., Gardini, F., Lombardi, A., Vannini, L., Guerzoni, M.E., Andrighetto, C., Lanorte, M.T.: A survey of the enterococci isolated from an artisanal Italian goat's cheese (semicotto caprino). J. Appl. Microbiol., 89, 267-274 (2000). https://doi.org/10.1046/j.1365-2672.2000.01120.x
  5. Klein, G., Pack, A., Reuter, G.: Antibiotic resistance patterns of enterococci and occurrence of vancomycin-resistant enterococci in raw minced beef and pork in Germany. Appl. Environ. Microbiol., 64, 1825-1830 (1998).
  6. OIE. European Scientific Conference. The use of antibiotics in animal ensuring the protection of public health. pp. 8-142 (2001).
  7. Klibi, N., Gharbi, S., Masmoudi, A., Ben Slama, K., Poeta, P., Zarazaga, M., Fendri, C., Boudabous, A., Torres, C.: Antibiotic resistance and mechanisms implicated in clinical enterococci in a Tunisian hospital. J. Chemother., 18, 20-26 (2006). https://doi.org/10.1179/joc.2006.18.1.20
  8. Pesavento, G., Calonico, C., Ducci, B., Magnanini, A., Lo Nostro, A.: Prevalence and antibiotic resistance of Enterococcus spp. isolated from retail cheese, ready-to-eat salads, ham, and raw meat. Food Microbiol., 41, 1-7 (2014). https://doi.org/10.1016/j.fm.2014.01.008
  9. Silva, N., Igrejas, G., Figueiredo, N., Goncalves, A., Radhouani, H., Rodrigues, J., Poeta, P.: Molecular characterization of antimicrobial resistance in enterococci and Escherichia coli isolates from European wild rabbit (Oryctolagus cuniculus). Sci. Total Environ., 408, 4871-4876 (2010). https://doi.org/10.1016/j.scitotenv.2010.06.046
  10. Putman, M., Veen, van H.W., Konings, W.N.: Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev., 64, 672-693 (2000). https://doi.org/10.1128/MMBR.64.4.672-693.2000
  11. Levy, S.B.: Active efflux mechanisms for antimicrobial resistance. Antimicrob. Agents Chemother., 36, 695-703 (2002).
  12. Saier, M.H.Jr, Tam, R., Reizer, A., Reizer, J.: Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport. Mol. Microbiol., 11, 841-847 (1994). https://doi.org/10.1111/j.1365-2958.1994.tb00362.x
  13. Lubelski, J., Konings, W.N., Driessen, A.J.: Distribution and physiology of ABC-type transporters contributing to multidrug resistance in bacteria. Microbiol. Mol. Biol. Rev., 71, 463-476 (2007). https://doi.org/10.1128/MMBR.00001-07
  14. Pao, S.S., Paulsen, I.T., Saier, M.H.Jr.: Major facilitator superfamily. Microbiol. Mol. Biol. Rev., 62, 1-34 (1998).
  15. Jack, D.L., Yang, N.M., Saier, M.H.Jr.: The drug/metabolite transporter superfamily. Eur. J. Biochem., 268, 3620-3639 (2001). https://doi.org/10.1046/j.1432-1327.2001.02265.x
  16. Kuroda, T., Tsuchiya, T.: Multidrug efflux transporters in the MATE family. Biochim. Biophys. Acta., 1794, 763-768 (2009). https://doi.org/10.1016/j.bbapap.2008.11.012
  17. Tseng, T.T., Gratwick, K.S., Kollman, J.: The RND permease superfamily: an ancient, ubiquitous and diverse family that includes human disease and development proteins. J. Mol. Microbiol. Biotechnol., 1, 107-125 (1999).
  18. Depardieu, F., Podglajen, I., Leclercq, R., Collatz, E., Courvalin, P.: Modes and modulations of antibiotic resistance gene expression. Clin. Microbio. Rev., 20, 79-114 (2007). https://doi.org/10.1128/CMR.00015-06
  19. Gaglio, R., Couto, N., Marques, C., de Fatima Silva Lopes, M., Moschetti, G., Pomba, C., Settanni, L.: Evaluation of antimicrobial resistance and virulence of enterococci from equipment surfaces, raw materials, and traditional cheeses. Int. J. Food Microbiol., 236, 107-114 (2016). https://doi.org/10.1016/j.ijfoodmicro.2016.07.020
  20. Brtkova, A., Filipova, M., Drahovska, H., Bujdakova, H.: Characterization of enterococci of animal and environmental origin using phenotypic methods and comparison with PCR based methods Veterinarni. Medicina., 55, 97-105 (2010).
  21. CLSI.: Performance standards for antimicrobial susceptibility testing: seventeenth informational supplement. Clinical and Laboratory Standards Institute. ASM press, Washington D.C., USA. (2007).
  22. Jeong, S.H., Lim, S.K., Lee, H.S., Jeong, B.Y., Lee, J.Y., Yang, C.B., Shin, H.C.: The present situation of antibiotics used in animal and resistant bacteria. Infect. Chemother., 40, Suppl. 2, 144-149 (2008).
  23. Kwon, Y.I., Kim, T.W., Kim, H.Y., Chang, Y.H., Kwak, H.S., Woo, G.I., Chung, Y.H.: Monitoring of antimicrobial resistant bacteria from animal farm environments in Korea. Kor. J. Microbiol. Biotechnol., 35, 17-25 (2007).
  24. Nam, H.M., Lim, S.K., Moon, J.S., Kang, H.M., Kim, J.M., Jang, K.C., Kim, J.M., Kang, M.I., Joo, Y.S., Jung, S.C.: Antimicrobial resistance of enterococci isolated from mastitic bovine milk samples in Korea. Zoonoses Public Health, 57, e59-64 (2009).
  25. Mannu, L., Paba, A., Daga, E., Comunian, R., Zanetti, S., Dupre I., Sechi, L.A.: Comparison of the incidence of virulence determinants and antibiotic resistance between Enterococcus faecium strains of dairy, animal and clinical origin. Int. J. Food Microbiol., 88, 291-304 (2003). https://doi.org/10.1016/S0168-1605(03)00191-0
  26. Jonas, B.M., Murray, B.E., Weinstock, G.M.: Characterization of emeA, a NorA homolog and multidrug resistance efflux pump, in Enterococcus faecalis. Antimicrob. Agents Chemother., 45, 3574-3579 (2001). https://doi.org/10.1128/AAC.45.12.3574-3579.2001
  27. Singh, K.V., Weinstock, G.M., Murray, B.E.: An Enterococcus faecalis ABC homologue (Lsa) is required for the resistance of this species to clindamycin and quinupristin-dalfopristin. Antimicrob. Agents Chemother., 46, 1845-1850 (2002). https://doi.org/10.1128/AAC.46.6.1845-1850.2002
  28. Arias, C.A., Contreras, G.A., Murray, B.E.: Management of multidrug-resistant enterococcal infections. Clin. Microbiol. Infect., 16, 555-562 (2010). https://doi.org/10.1111/j.1469-0691.2010.03214.x
  29. Sanchez, V.A., Lavilla, L.L., Benomar, N., Galvez, A., Perez P.R., Abriouel H.: Phenotypic and molecular antibiotic resistance profile of Enterococcus faecalis and Enterococcus faecium isolated from different traditional fermented foods. Foodborne Pathog. Dis., 10, 143-149 (2013). https://doi.org/10.1089/fpd.2012.1279
  30. Lysakowska, M.E., Denys, A., Sienkiewicz, M.: Frequency of ace, epa and elrA Genes in clinical and environmental strains of Enterococcus faecalis. Indian J. Microbiol., 52, 612-616 (2012). https://doi.org/10.1007/s12088-012-0285-8
  31. Zou, L.K., Wang, H.N., Zeng, B., Li, J.N., Li, X.T., Zhang, A.Y., Zhou, Y.S., Yang, X., Xu, C.W., Xia, Q.Q.: Erythromycin resistance and virulence genes in Enterococcus faecalis from swine in China. New Microbiol., 34, 73-80 (2011)
  32. Wu, X., Hou, S., Zhang, Q., Ma, Y., Zhang, Y., Kan, W., Zhao, X.: Prevalence of virulence and resistance to antibiotics in pathogenic enterococci isolated from mastitic cows. J. Vet. Med. Sci., 78, 1663-1668, (2016). https://doi.org/10.1292/jvms.15-0718