Korean Journal of Veterinary Service (한국동물위생학회지)

The Korean Society of Veterinary Service (한국동물위생학회)
권호 표지
DOI QR코드

DOI QR Code

Characterization of plasmid-mediated quinolone resistance genes in Enterobacteriaceae isolated from companion animals

반려동물 유래 장내세균에서 plasmid 매개 퀴놀론 내성 유전자의 특성

  • 조재근 (대구광역시보건환경연구원) ;
  • 김정미 (대구광역시보건환경연구원) ;
  • 김환득 (대구광역시보건환경연구원) ;
  • 김경희 (대구광역시보건환경연구원) ;
  • 임현숙 (대구광역시보건환경연구원) ;
  • 양창렬 (대구광역시보건환경연구원)
  • Received : 2018.11.30
  • Accepted : 2018.12.31
  • Published : 2019.03.30
Download PDF
⟨ Previous Next ⟩

Abstract

The aim of this study was to investigate the prevalence and characterization of plasmid-mediated quinolone resistance (PMQR) gene in 79 Enterobacteriaceae isolated from dogs and cats. Of 79 isolates, PMQR genes were found in 10 (12.7%) isolates, including aac(6')-lb-cr, qnrB, qnrS and qnrA detected alone or in combination in 8 (10.1%), 4 (5.1%), 2 (2.5%) and 1 (1.3%) isolates, respectively. Interestingly, two qnrS genes were detected in nalidixic acid and ciprofloxacin susceptible isolates. Extended-spectrum ${\beta}$-lactamase (ESBL) was detected in 90% (9 isolates) of PMQR positives isolates. Among ESBL genes, CTX-M, TEM and SHV were detected in 9, 8 and 3 isolates, respectively. Almost all PMQR genes were detected in co-existence with ESBL genes. All PMQR positives isolates were multidrug resistance (i.e. resistant to five or more antibiotics). qepA, OXA and CMY-2 genes were not found. The six transconjugants were obtained by conjugation experiment. The aac(6')-lb-cr, qnrB and qnrS were co-transferred with CTX-M, TEM and/or SHV, whereas qnrA was not observed among transconugants. This is the first report of the presence of aac(6')-lb-cr and qnrA gene among Enterobacteriaceae isolates from dogs in Korea. The prudent use of antimicrobials and continuous monitoring for companion animals are required.

Keywords

GCOSBX_2019_v42n1_17_f0001.png 이미지

Fig. 1. Detection of PMQR genes. Lanes: M, 100 bp DNA marker;1, qnrA (574 bp); qnrB (513 bp); qnrS (431bp); 4, aac(6’)-1b-cr (596bp); 5, qepA (not detected).

GCOSBX_2019_v42n1_17_f0002.png 이미지

Fig. 2. Detection of ESBL genes. Lanes : M, 100 bp DNA marker;1, TEM (1,150 bp); 2, CTX (593 bp); 3, SHV (885 bp); 4, OXA and 5,CMY (not detected).

Table 1. Isolated bacteria by the sampling sites

GCOSBX_2019_v42n1_17_t0001.png 이미지

Table 2. Primers used in this study

GCOSBX_2019_v42n1_17_t0002.png 이미지

Table 3. Distribution of PMQR and ESBL genes in 79 Enterobacteriaceae isolates

GCOSBX_2019_v42n1_17_t0003.png 이미지

Table 4. Distribution of PMQR and ESBL genes in 6 transconjugants

GCOSBX_2019_v42n1_17_t0004.png 이미지

References

  1. Aslantas O, Yilmaz ES. 2017. Prevalence and molecular characterization of extended-spectrum ${\beta}$-lactamase (ESBL) and plasmidic AmpC ${\beta}$-lactamase (pAmpC) producing Escherichia coli in dogs. J Vet Med Sci 79: 1024-1030. https://doi.org/10.1292/jvms.16-0432
  2. Bradley DE, Taylor DE, Cohen DR. 1980. Specification of surface mating systems among conjugative drug resistance plasmids in Escherichia coli K-12. J Bacteriol 143: 1466-1470. https://doi.org/10.1128/JB.143.3.1466-1470.1980
  3. Briales A, Rodriguez-Martinez JM, Velasco C, de Alba PD, Rodriguez-Bano J, Martinez-Martinez L, Pascual A. 2012. Prevalence of plasmid-mediated quinolone resistance determinants qnr and aac(6')-Ib-cr in Escherichia coli and Klebsiella pneumoniae producing extendedspectrum ${\beta}$-lactamases in Spain. Int J Antimicrob Agents 39: 431-434. https://doi.org/10.1016/j.ijantimicag.2011.12.009
  4. Brinas L, Lantero M, de Diego I, Alvarez M, Zarazaga M, Torres C. 2005. Mechanisms of resistance to expanded-spectrum cephalosporins in Escherichia coli isolates recovered in a Spanish hospital. J Antimicrob Chemother. 56: 1107-1110. https://doi.org/10.1093/jac/dki370
  5. Brinas L, Zarazaga M, Saenz Y, Ruiz-Larrea F, Torres C. 2002. Beta-lactamases in ampicillin- resistant Escherichia coli isolates from foods, humans, and healthy animals. Antimicrob Agents Chemother. 46: 3156-3163. https://doi.org/10.1128/AAC.46.10.3156-3163.2002
  6. Cantas L, Suer K, Guler E, Imir T. 2015. High emergence of ESBL-producing E. coli cystitis: time to get smarter in cyprus. Front Microbiol 6: 1446.
  7. Cavaco LM, Aarestrup FM. 2009. Evaluation of quinolones for use in detection of determinants of acquired quinolone resistance, including the new transmissible resistance mechanisms qnrA, qnrB, qnrS, and aac(6')Ib-cr, in Escherichia coli and Salmonella enterica and determinations of wild-type distributions. J Clin Microbiol. 47: 2751-2758. https://doi.org/10.1128/JCM.00456-09
  8. Cho JK, Kim JM, Kim HD, Kim KH. 2017. Antimicrobial-resistant Escherichia coli isolated from dogs and cats at animal hospitals in Daegu. Korean J Vet Res 40: 193-200.
  9. CLSI. Clinical and Laboratory Standards Institute. 2013. Performance standards for antimicrobial disk and dilution susceptibility tests for bacterial isolated from animals; approved standard. fourth edition and supplement, CLSI document VET01-A4 (standard) and VET01-S2 (supplement), in Clinical and Laboratory Standards Institute (Wayne, PA:).
  10. Hooper DC. 2001. Emerging mechanisms of fluoroquinolone resistance. Emerg Infect Dis 7: 337-341. https://doi.org/10.3201/eid0702.010239
  11. Ishida Y, Ahmed AM, Mahfouz NB, Kimura T, El-Khodery SA, Moawad AA, Shimamoto T. 2010. Molecular analysis of antimicrobial resistance in gram-negative bacteria isolated from fish farms in Egypt. J Vet Med Sci 72: 727-734. https://doi.org/10.1292/jvms.09-0538
  12. Jacoby GA. 2005. Mechanisms of resistance to quinolones. Clin Infect Dis 41: S120-126. https://doi.org/10.1086/428052
  13. Jacoby GA, Gacharna N, Black TA, Miller GH, Hooper DC. 2009. Temporal appearance of plasmid- mediated quinolone resistance genes. Antimicrob Agents Chemother. 53: 1665-1666. https://doi.org/10.1128/AAC.01447-08
  14. Kang CI. 2015. Antimicrobial therapy for infections caused by multidrug-resistant gram-negative bacteria. Korean J Med 88: 502-508. https://doi.org/10.3904/kjm.2015.88.5.502
  15. Kim HB, Park CH, Kim CJ, Kim EC, Jacoby GA, Hooper DC. 2009. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother. 53: 639-645. https://doi.org/10.1128/AAC.01051-08
  16. Liao CH, Hsueh PR, Jacoby GA, Hooper DC. 2013. Risk factors and clinical characteristics of patients with qnr-positive Klebsiella pneumoniae bacteraemia. J Antimicrob Chemother 68: 2907-2914. https://doi.org/10.1093/jac/dkt295
  17. Liu X, Liu H, Li Y, Hao C. 2016a. High prevalence of ${\beta}$-lactamase and plasmid-mediated quinolone resistance genes in extended-spectrum cephalosporin-resistant Escherichia coli from dogs in Shaanxi, China. Front Microbiol 16: 1843.
  18. Liu X, Thungrat K, Boothe DM. 2016b. Occurrence of OXA-48 carbapenemase and other ${\beta}$-lactamase genes in ESBLproducing multidrug resistant Escherichia coli from dogs and cats in the United States, 2009-2013. Front Microbiol 7: 1057.
  19. Ma J, Zeng Z, Chen Z, Xu X, Wang X, Deng Y, Lu D, Huang L, Zhang Y, Liu J, Wang M. 2009. High prevalence of plasmid-mediated quinolone resistance determinants qnr, aac(6')-Ib-cr, and qepA among ceftiofur-resistant Enterobacteriaceae isolates from companion and food- producing animals. Antimicrob Agents Chemother 53: 519-524. https://doi.org/10.1128/AAC.00886-08
  20. Pagani L, Dell'Amico E, Migliavacca R, D'Andrea MM, Giacobone E, Amicosante G, Romero E, Rossolini GM. 2003. Multiple CTX-M-type extended-spectrum beta-lactamases in nosocomial isolates of Enterobacteriaceae from a hospital in northern Italy. J Clin Microbiol 41: 4264-4269. https://doi.org/10.1128/JCM.41.9.4264-4269.2003
  21. Park YJ, Yu JK, Lee S, Oh EJ, Woo GJ. 2007. Prevalence and diversity of qnr alleles in AmpC-producing Enterobacter cloacae, Enterobacter aerogenes, Citrobacter freundii and Serratia marcescens: a multicentre study from Korea. J Antimicrob Chemother 60: 868-871. https://doi.org/10.1093/jac/dkm266
  22. Poirel L, Cattoir V, Nordmann P. 2012. Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies. Front Microbiol 3: 24. https://doi.org/10.3389/fmicb.2012.00024
  23. Poirel L, Van De Loo M, Mammeri H, Nordmann P. 2005. Association of plasmid-mediated quinolone resistance with extended-spectrum beta-lactamase VEB-1. Antimicrob Agents Chemother 49: 3091-3904. https://doi.org/10.1128/AAC.49.7.3091-3094.2005
  24. Robicsek A, Jacoby GA, Hooper DC. 2006a. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 6: 629-640. https://doi.org/10.1016/S1473-3099(06)70599-0
  25. Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, Bush K, Hooper DC. 2006c. Fluoroquinolonemodifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 12: 83-88. https://doi.org/10.1038/nm1347
  26. Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC. 2006b. qnr prevalence in ceftazidime- resistant Enterobacteriaceae isolates from the United States. Antimicrob Agents Chemother 50: 2872-2874. https://doi.org/10.1128/AAC.01647-05
  27. Rodriguez-Martinez JM, Cano ME, Velasco C, Martinez-Martinez L, Pascual A. 2011. Plasmid-mediated quinolone resistance: an update. J Infect Chemother 17: 149-182. https://doi.org/10.1007/s10156-010-0120-2
  28. Shin DH, Kim HY, Byun JW, Kim DK, Lim SK, Jung BY. 2010. Prevalence of plasmid-mediated quinolone resistance genes in Escherichia coli isolated from diseaded animals in Korea. J Life Scinece 20: 964-967. https://doi.org/10.5352/JLS.2010.20.6.964
  29. So JH, Kim J, Bae IK, Jeong SH, Kim SH, Lim SK, Park YH, Lee K. 2012. Dissemination of multidrug-resistant Escherichia coli in Korean veterinary hospitals. Diagn Microbiol Infect Dis. 73: 195-199. https://doi.org/10.1016/j.diagmicrobio.2012.03.010
  30. Tamang MD, Nam HM, Jang GC, Kim SR, Chae MH, Jung SC, Byun JW, Park YH, Lim SK. 2012. Molecular characterization of extended-spectrum-${\beta}$-lactamase-producing and plasmid-mediated AmpC ${\beta}$-lactamase-producing Escherichia coli isolated from stray dogs in South Korea. Antimicrob Agents Chemother 56: 2705-2712. https://doi.org/10.1128/AAC.05598-11
  31. Tian GB, Wang HN, Zhang AY, Zhang Y, Fan WQ, Xu CW, Zeng B, Guan ZB, Zou LK. 2012. Detection of clinically important ${\beta}$-lactamases in commensal Escherichia coli of human and swine origin in western China. J Med Microbiol 61: 233-238. https://doi.org/10.1099/jmm.0.036806-0
  32. Webber M, Piddock LJ. 2001. Quinolone resistance in Escherichia coli. Vet Res 32: 275-284. https://doi.org/10.1051/vetres:2001124
  33. Yu T, Jiang X, Fu K, Liu B, Xu D, Ji S, Zhou L. 2015. Detection of extended-spectrum ${\beta}$-lactamase and plasmid- mediated quinolone resistance determinants in Escherichia coli isolates from retail meat in China. J Food Sci 80: M1039-1043. https://doi.org/10.1111/1750-3841.12870
  34. Zhao X, Xu X, Zhu D, Ye X, Wang M. 2010. Decreased quinolone susceptibility in high percentage of Enterobacter cloacae clinical isolates caused only by qnr determinants. Diagn Microbiol Infect Dis 67: 110-113. https://doi.org/10.1016/j.diagmicrobio.2009.12.018