Phylogenetic association of fluoroquinolone and cephalosporin resistance of D-O1-ST648 carrying from faecal samples of dogs in Japan Free

Abstract

This study aimed to investigate the genetic association between fluoroquinolone (FQ) and/or cephalosporin (CEP) resistance in isolates from dogs, and the risk to human health. We characterized clinical isolates, derived from faecal samples of dogs attending veterinary hospitals, using phylogenetic grouping, determination of virulence factor (VF) prevalence, multilocus sequence typing (MLST) and O serotyping. The D group was the dominant phylogenetic group among strains resistant to FQ and/or CEP. In contrast, the dominant group among susceptible strains was group B2. Group D strains showed a significantly higher prevalence of VFs than strains belonging to groups A and B1, and were resistant to significantly more antimicrobials than group B2 strains. The phylogenetic distribution of FQ–CEP-resistant groups (FQ–CEPRECs) and FQ-resistant groups was significantly correlated ( = 0.98), but FQ–CEPRECs and CEP-resistant groups were not correlated ( = 0.58). Data from PFGE, O serotype and MLST analyses indicated that the majority of FQ-resistant strains derived from a particular lineage of phylogenetic group D: serotype O1 and sequence type (ST) 648. Some D-O1-ST648 strains carried , showed multidrug resistance and possessed a higher prevalence of the VFs , and PAI compared with other group D strains. Our data indicate that the emergence of FQ-CEP-resistant is based primarily on FQ-resistant . Moreover, as strains of the D-O1-ST648 lineage have been found in clinical isolates derived from humans at a relatively high frequency, our findings indicate that the spreading of D-O1-ST648 strains may cause serious difficulties in both veterinary and human clinical fields in the future.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.054676-0
2014-02-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jmm/63/2/263.html?itemId=/content/journal/jmm/10.1099/jmm.0.054676-0&mimeType=html&fmt=ahah

References

  1. Ambrozic Avgustin J., Keber R., Zerjavic K., Orazem T., Grabnar M. 2007; Emergence of the quinolone resistance-mediating gene aac(6′)-Ib-cr in extended-spectrum-β-lactamase-producing isolates collected in Slovenia between 2000 and 2005. Antimicrob Agents Chemother 51:4171–4173 [View Article][PubMed]
    [Google Scholar]
  2. Bergman M., Nyberg S. T., Huovinen P., Paakkari P., Hakanen A. J.Finnish Study Group for Antimicrobial Resistance 2009; Association between antimicrobial consumption and resistance in Escherichia coli. Antimicrob Agents Chemother 53:912–917 [View Article][PubMed]
    [Google Scholar]
  3. Clermont O., Bonacorsi S., Bingen E. 2000; Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555–4558 [View Article][PubMed]
    [Google Scholar]
  4. Clermont O., Johnson J. R., Menard M., Denamur E. 2007; Determination of Escherichia coli O types by allele-specific polymerase chain reaction: application to the O types involved in human septicemia. Diagn Microbiol Infect Dis 57:129–136 [View Article][PubMed]
    [Google Scholar]
  5. CLSI 2008; Performance Standards for Antimicrobial Disk and Dilution Antimicrobial Susceptibility Tests for Bacteria Isolated from Animals; Approved standard, 3rd edn, M31-A3. Wayne, PA: Clinical and Laboratory Standards Institute;
    [Google Scholar]
  6. Harada K., Nakai Y., Kataoka Y. 2012; Mechanisms of resistance to cephalosporin and emergence of O25b-ST131 clone harboring CTX-M-27 β-lactamase in extraintestinal pathogenic Escherichia coli from dogs and cats in Japan. Microbiol Immunol 56:480–485 [View Article][PubMed]
    [Google Scholar]
  7. Hopkins K. L., Davies R. H., Threlfall E. J. 2005; Mechanisms of quinolone resistance in Escherichia coli and Salmonella: recent developments. Int J Antimicrob Agents 25:358–373 [View Article][PubMed]
    [Google Scholar]
  8. Hornsey M., Phee L., Wareham D. W. 2011; A novel variant, NDM-5, of the New Delhi metallo-β-lactamase in a multidrug-resistant Escherichia coli ST648 isolate recovered from a patient in the United Kingdom. Antimicrob Agents Chemother 55:5952–5954 [View Article][PubMed]
    [Google Scholar]
  9. Johnson J. R., Kuskowski M. A., Owens K., Clabots C., Singer R. S. 2009; Virulence genotypes and phylogenetic background of fluoroquinolone-resistant and susceptible Escherichia coli urine isolates from dogs with urinary tract infection. Vet Microbiol 136:108–114 [View Article][PubMed]
    [Google Scholar]
  10. Kanamaru S., Kurazono H., Nakano M., Terai A., Ogawa O., Yamamoto S. 2006; Subtyping of uropathogenic Escherichia coli according to the pathogenicity island encoding uropathogenic-specific protein: comparison with phylogenetic groups. Int J Urol 13:754–760 [View Article][PubMed]
    [Google Scholar]
  11. Kaper J. B., Nataro J. P., Mobley H. L. 2004; Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140 [View Article][PubMed]
    [Google Scholar]
  12. Kim E. S., Jeong J. Y., Jun J. B., Choi S. H., Lee S. O., Kim M. N., Woo J. H., Kim Y. S. 2009a; Prevalence of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme among Enterobacteriaceae blood isolates in Korea. Antimicrob Agents Chemother 53:2643–2645 [View Article][PubMed]
    [Google Scholar]
  13. Kim H. B., Park C. H., Kim C. J., Kim E. C., Jacoby G. A., Hooper D. C. 2009b; Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother 53:639–645 [View Article][PubMed]
    [Google Scholar]
  14. Kirchner M., Wearing H., Teale C. 2011; Plasmid-mediated quinolone resistance gene detected in Escherichia coli from cattle. Vet Microbiol 148:434–435 [View Article][PubMed]
    [Google Scholar]
  15. Lavigne J. P., Marchandin H., Delmas J., Bouziges N., Lecaillon E., Cavalie L., Jean-Pierre H., Bonnet R., Sotto A. 2006; qnrA in CTX-M-producing Escherichia coli isolates from France. Antimicrob Agents Chemother 50:4224–4228 [View Article][PubMed]
    [Google Scholar]
  16. Little M. L., Qin X., Zerr D. M., Weissman S. J. 2012; Molecular diversity in mechanisms of carbapenem resistance in paediatric Enterobacteriaceae. Int J Antimicrob Agents 39:52–57 [View Article][PubMed]
    [Google Scholar]
  17. McLellan S. L., Daniels A. D., Salmore A. K. 2003; Genetic characterization of Escherichia coli populations from host sources of fecal pollution by using DNA fingerprinting. Appl Environ Microbiol 69:2587–2594 [View Article][PubMed]
    [Google Scholar]
  18. Mulvey M. R., Bryce E., Boyd D. A., Ofner-Agostini M., Land A. M., Simor A. E., Paton S. 2005; Molecular characterization of cefoxitin-resistant Escherichia coli from Canadian hospitals. Antimicrob Agents Chemother 49:358–365 [View Article][PubMed]
    [Google Scholar]
  19. Naseer U., Olsson-Liljequist B. E., Woodford N., Dhanji H., Cantón R., Sundsfjord A., Lindstedt B. A. 2012; Multi-locus variable number of tandem repeat analysis for rapid and accurate typing of virulent multidrug resistant Escherichia coli clones. PLoS ONE 7:e41232 [View Article][PubMed]
    [Google Scholar]
  20. National Veterinary Assay Laboratory 2009; A report on the Japanese Veterinary Antimicrobial Resistance Monitoring System 2000 to 2007. http://www.maff.go.jp/nval/tyosa_kenkyu/taiseiki/pdf/jvarm2000_2007_final_201005.pdf
    [Google Scholar]
  21. Peirano G., Pitout J. D. 2010; Molecular epidemiology of Escherichia coli producing CTX-M β-lactamases: the worldwide emergence of clone ST131 O25:H4. Int J Antimicrob Agents 35:316–321 [View Article][PubMed]
    [Google Scholar]
  22. Pérez-Pérez F. J., Hanson N. D. 2002; Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 40:2153–2162 [View Article][PubMed]
    [Google Scholar]
  23. Platell J. L., Cobbold R. N., Johnson J. R., Heisig A., Heisig P., Clabots C., Kuskowski M. A., Trott D. J. 2011; Commonality among fluoroquinolone-resistant sequence type ST131 extraintestinal Escherichia coli isolates from humans and companion animals in Australia. Antimicrob Agents Chemother 55:3782–3787 [View Article][PubMed]
    [Google Scholar]
  24. Ruppé E., Hem S., Lath S., Gautier V., Ariey F., Sarthou J. L., Monchy D., Arlet G. 2009; CTX-M β-lactamases in Escherichia coli from community-acquired urinary tract infections, Cambodia. Emerg Infect Dis 15:741–748 [View Article][PubMed]
    [Google Scholar]
  25. Sorlozano A., Gutierrez J., Jimenez A., de Dios Luna J., Martínez J. L. 2007; Contribution of a new mutation in parE to quinolone resistance in extended-spectrum-β-lactamase-producing Escherichia coli isolates. J Clin Microbiol 45:2740–2742 [View Article][PubMed]
    [Google Scholar]
  26. Takahashi A., Kanamaru S., Kurazono H., Kunishima Y., Tsukamoto T., Ogawa O., Yamamoto S. 2006; Escherichia coli isolates associated with uncomplicated and complicated cystitis and asymptomatic bacteriuria possess similar phylogenies, virulence genes, and O-serogroup profiles. J Clin Microbiol 44:4589–4592 [View Article][PubMed]
    [Google Scholar]
  27. Takahashi A., Muratani T., Yasuda M., Takahashi S., Monden K., Ishikawa K., Kiyota H., Arakawa S., Matsumoto T.& other authors ( 2009; Genetic profiles of fluoroquinolone-resistant Escherichia coli isolates obtained from patients with cystitis: phylogeny, virulence factors, PAIusp subtypes, and mutation patterns. J Clin Microbiol 47:791–795 [View Article][PubMed]
    [Google Scholar]
  28. Tamang M. D., Nam H. M., Jang G. C., Kim S. R., Chae M. H., Jung S. C., Byun J. W., Park Y. H., Lim S. K. 2012; Molecular characterization of extended-spectrum-β-lactamase-producing and plasmid-mediated AmpC β-lactamase-producing Escherichia coli isolated from stray dogs in South Korea. Antimicrob Agents Chemother 56:2705–2712 [View Article][PubMed]
    [Google Scholar]
  29. Tartof S. Y., Solberg O. D., Manges A. R., Riley L. W. 2005; Analysis of a uropathogenic Escherichia coli clonal group by multilocus sequence typing. J Clin Microbiol 43:5860–5864 [View Article][PubMed]
    [Google Scholar]
  30. The National Molecular Subtyping Network for Foodborne Disease Surveillance 2004; One-day (24–48h) standardized laboratory protocol for molecular subtyping of Escherichia coli O157:H7, non-typhoidal Salmonella serotypes, and Shigella sonnei by pulsed field gel electrophoresis (PFGE). MAF1–12
    [Google Scholar]
  31. Xu L., Ensor V., Gossain S., Nye K., Hawkey P. 2005; Rapid and simple detection of blaCTX-M genes by multiplex PCR assay. J Med Microbiol 54:1183–1187 [View Article][PubMed]
    [Google Scholar]
  32. Yang H., Chen S., White D. G., Zhao S., McDermott P., Walker R., Meng J. 2004; Characterization of multiple-antimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China. J Clin Microbiol 42:3483–3489 [View Article][PubMed]
    [Google Scholar]
  33. Yokota S., Sato T., Okubo T., Ohkoshi Y., Okabayashi T., Kuwahara O., Tamura Y., Fujii N. 2012; Prevalence of fluoroquinolone-resistant Escherichia coli O25:H4-ST131 (CTX-M-15-nonproducing) strains isolated in Japan. Chemotherapy 58:52–59 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.054676-0
Loading
/content/journal/jmm/10.1099/jmm.0.054676-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed