1887

Abstract

Large-scale monitoring of resistance to 14 antimicrobial agents was performed using 103 strains isolated from dogs in Japan. Resistant strains were analysed to identify their resistance mechanisms. Rates of resistance to chloramphenicol, streptomycin, enrofloxacin, trimethoprim/sulfamethoxazole, kanamycin, ampicillin, ciprofloxacin, cephalothin, gentamicin, cefoxitin and cefotaxime were 20.4, 15.5, 12.6, 10.7, 9.7, 8.7, 5.8, 2.9, 2.9, 1.9 and 1.9 %, respectively. No resistance to ceftazidime, aztreonam or imipenem was found. Class 1 and 2 integrases were detected in 2.9 and 11.7 % of isolates, respectively. Class 1 integrons contained or -like, whereas those of class 2 contained , or none of the anticipated resistance genes. Of five distinct plasmid-mediated quinolone-resistance (PMQR) genes, only gene was detected in 1.9 % of isolates. Quinolone-resistance determining regions (QRDRs) of and from 13 enrofloxacin-intermediate and -resistant isolates were sequenced. Seven strains had double mutations and three had single mutations. Three of nine ampicillin-resistant isolates harboured AmpC-type β-lactamases (i.e. , and ). These results suggest that canine deserves continued surveillance as an important reservoir of antimicrobial resistance determinants. This is the first report, to our knowledge, describing integrons, PMQRs and QRDR mutations in isolates from companion animals.

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2014-11-01
2024-12-07
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References

  1. Authier S., Paquette D., Labrecque O., Messier S. 2006; Comparison of susceptibility to antimicrobials of bacterial isolates from companion animals in a veterinary diagnostic laboratory in Canada between 2 time points 10 years apart. Can Vet J 47:774–778[PubMed]
    [Google Scholar]
  2. Bubenik L. J., Hosgood G. L., Waldron D. R., Snow L. A. 2007; Frequency of urinary tract infection in catheterized dogs and comparison of bacterial culture and susceptibility testing results for catheterized and noncatheterized dogs with urinary tract infections. J Am Vet Med Assoc 231:893–899 [View Article][PubMed]
    [Google Scholar]
  3. Cattoir V., Poirel L., Rotimi V., Soussy C. J., Nordmann P. 2007; Multiplex PCR for detection of plasmid-mediated quinolone resistance qnr genes in ESBL-producing enterobacterial isolates. J Antimicrob Chemother 60:394–397 [View Article][PubMed]
    [Google Scholar]
  4. Cavaco L. M., Hasman H., Xia S., Aarestrup F. M. 2009; qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53:603–608 [View Article][PubMed]
    [Google Scholar]
  5. Chong Y., Shimoda S., Yakushiji H., Ito Y., Miyamoto T., Kamimura T., Shimono N., Akashi K. 2013; Community spread of extended-spectrum β-lactamase-producing Escherichia coli, Klebsiella pneumoniae and Proteus mirabilis: a long-term study in Japan. J Med Microbiol 62:1038–1043 [View Article][PubMed]
    [Google Scholar]
  6. CLSI 2013a; Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals; Approved Standard, 4th edn, VET01–A4. Wayne, PA: Clinical and Laboratory Standards Institute;
    [Google Scholar]
  7. CLSI 2013b; Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals; 2nd Informational Supplement VET01–S2. Wayne, PA: Clinical and Laboratory Standards Institute;
    [Google Scholar]
  8. CLSI 2013c; Performance Standards for Antimicrobial Susceptibility Testing; 20th Informational Supplement M100–S20. Wayne, PA: Clinical and Laboratory Standards Institute;
    [Google Scholar]
  9. Cohn L. A., Gary A. T., Fales W. H., Madsen R. W. 2003; Trends in fluoroquinolone resistance of bacteria isolated from canine urinary tracts. J Vet Diagn Invest 15:338–343 [View Article][PubMed]
    [Google Scholar]
  10. Donati V., Feltrin F., Hendriksen R. S., Svendsen C. A., Cordaro G., García-Fernández A., Lorenzetti S., Lorenzetti R., Battisti A., Franco A. 2014; Extended-spectrum-beta-lactamases, AmpC beta-lactamases and plasmid mediated quinolone resistance in Klebsiella spp. from companion animals in Italy. PLoS ONE 9:e90564 [View Article][PubMed]
    [Google Scholar]
  11. Fàbrega A., Madurga S., Giralt E., Vila J. 2009; Mechanism of action of and resistance to quinolones. Microb Biotechnol 2:40–61 [View Article][PubMed]
    [Google Scholar]
  12. Gibson J. S., Cobbold R. N., Heisig P., Sidjabat H. E., Kyaw-Tanner M. T., Trott D. J. 2010a; Identification of Qnr and AAC(6′)-1b-cr plasmid-mediated fluoroquinolone resistance determinants in multidrug-resistant Enterobacter spp. isolated from extraintestinal infections in companion animals. Vet Microbiol 143:329–336 [View Article][PubMed]
    [Google Scholar]
  13. Gibson J. S., Cobbold R. N., Kyaw-Tanner M. T., Heisig P., Trott D. J. 2010b; Fluoroquinolone resistance mechanisms in multidrug-resistant Escherichia coli isolated from extraintestinal infections in dogs. Vet Microbiol 146:161–166 [View Article][PubMed]
    [Google Scholar]
  14. Grobbel M., Lübke-Becker A., Alesík E., Schwarz S., Wallmann J., Werckenthin C., Wieler L. H. 2007; Antimicrobial susceptibility of Klebsiella spp. and Proteus spp. from various organ systems of horses, dogs and cats as determined in the BfT-GermVet monitoring program 2004-2006. Berl Munch Tierarztl Wochenschr 120:402–411[PubMed]
    [Google Scholar]
  15. Gu B., Tong M., Zhao W., Liu G., Ning M., Pan S., Zhao W. 2007; Prevalence and characterization of class I integrons among Pseudomonas aeruginosa and Acinetobacter baumannii isolates from patients in Nanjing, China. J Clin Microbiol 45:241–243 [View Article][PubMed]
    [Google Scholar]
  16. Guardabassi L., Schwarz S., Lloyd D. H. 2004; Pet animals as reservoirs of antimicrobial-resistant bacteria. J Antimicrob Chemother 54:321–332 [View Article][PubMed]
    [Google Scholar]
  17. Guillard T., Grillon A., de Champs C., Cartier C., Madoux J., Berçot B., Lebreil A. L., Lozniewski A., Riahi J.& other authors ( 2014; Mobile insertion cassette elements found in small non-transmissible plasmids in Proteeae may explain qnrD mobilization. PLoS ONE 9:e87801 [View Article][PubMed]
    [Google Scholar]
  18. Harada K., Asai T. 2010; Role of antimicrobial selective pressure and secondary factors on antimicrobial resistance prevalence in Escherichia coli from food-producing animals in Japan. J Biomed Biotechnol 2010:1–12 [View Article][PubMed]
    [Google Scholar]
  19. Harada K., Arima S., Niina A., Kataoka Y., Takahashi T. 2012a; Characterization of Pseudomonas aeruginosa isolates from dogs and cats in Japan: current status of antimicrobial resistance and prevailing resistance mechanisms. Microbiol Immunol 56:123–127 [View Article][PubMed]
    [Google Scholar]
  20. Harada K., Niina A., Nakai Y., Kataoka Y., Takahashi T. 2012b; Prevalence of antimicrobial resistance in relation to virulence genes and phylogenetic origins among urogenital Escherichia coli isolates from dogs and cats in Japan. Am J Vet Res 73:409–417 [View Article][PubMed]
    [Google Scholar]
  21. Hordijk J., Schoormans A., Kwakernaak M., Duim B., Broens E., Dierikx C., Mevius D., Wagenaar J. A. 2013; High prevalence of fecal carriage of extended spectrum β-lactamase/AmpC-producing Enterobacteriaceae in cats and dogs. Front Microbiol 4:1–5 [View Article][PubMed]
    [Google Scholar]
  22. Jacobsen S. M., Shirtliff M. E. 2011; Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence 2:460–465 [View Article][PubMed]
    [Google Scholar]
  23. Kojima A., Ishii Y., Ishihara K., Esaki H., Asai T., Oda C., Tamura Y., Takahashi T., Yamaguchi K. 2005; Extended-spectrum-β-lactamase-producing Escherichia coli strains isolated from farm animals from 1999 to 2002: report from the Japanese Veterinary Antimicrobial Resistance Monitoring Program. Antimicrob Agents Chemother 49:3533–3537 [View Article][PubMed]
    [Google Scholar]
  24. Lévesque C., Piché L., Larose C., Roy P. H. 1995; PCR mapping of integrons reveals several novel combinations of resistance genes. Antimicrob Agents Chemother 39:185–191 [View Article][PubMed]
    [Google Scholar]
  25. Literacka E., Empel J., Baraniak A., Sadowy E., Hryniewicz W., Gniadkowski M. 2004; Four variants of the Citrobacter freundii AmpC-Type cephalosporinases, including novel enzymes CMY-14 and CMY-15, in a Proteus mirabilis clone widespread in Poland. Antimicrob Agents Chemother 48:4136–4143 [View Article][PubMed]
    [Google Scholar]
  26. Literak I., Dolejska M., Radimersky T., Klimes J., Friedman M., Aarestrup F. M., Hasman H., Cizek A. 2010; Antimicrobial-resistant faecal Escherichia coli in wild mammals in central Europe: multiresistant Escherichia coli producing extended-spectrum beta-lactamases in wild boars. J Appl Microbiol 108:1702–1711 [View Article][PubMed]
    [Google Scholar]
  27. Lloyd D. H. 2007; Reservoirs of antimicrobial resistance in pet animals. Clin Infect Dis 45:Suppl 2S148–S152 [View Article][PubMed]
    [Google Scholar]
  28. Lyskova P., Vydrzalova M., Mazurova J. 2007; Identification and antimicrobial susceptibility of bacteria and yeasts isolated from healthy dogs and dogs with otitis externa. J Vet Med A Physiol Pathol Clin Med 54:559–563 [View Article][PubMed]
    [Google Scholar]
  29. Ma J., Zeng Z., Chen Z., Xu X., Wang X., Deng Y., D., Huang L., Zhang Y.& other authors ( 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 [View Article][PubMed]
    [Google Scholar]
  30. Mazel D., Dychinco B., Webb V. A., Davies J. 2000; Antibiotic resistance in the ECOR collection: integrons and identification of a novel aad gene. Antimicrob Agents Chemother 44:1568–1574 [View Article][PubMed]
    [Google Scholar]
  31. Mokracka J., Gruszczyńska B., Kaznowski A. 2012; Integrons, β-lactamase and qnr genes in multidrug resistant clinical isolates of Proteus mirabilis and P. vulgaris. APMIS 120:950–958 [View Article][PubMed]
    [Google Scholar]
  32. Papagiannitsis C. C., Miriagou V., Kotsakis S. D., Tzelepi E., Vatopoulos A. C., Petinaki E., Tzouvelekis L. S. 2012; Characterization of a transmissible plasmid encoding VEB-1 and VIM-1 in Proteus mirabilis. Antimicrob Agents Chemother 56:4024–4025 [View Article][PubMed]
    [Google Scholar]
  33. Park C. H., Robicsek A., Jacoby G. A., Sahm D., Hooper D. C. 2006; Prevalence in the United States of aac(6′)-Ib-cr encoding a ciprofloxacin-modifying enzyme. Antimicrob Agents Chemother 50:3953–3955 [View Article][PubMed]
    [Google Scholar]
  34. Partridge S. R., Tsafnat G., Coiera E., Iredell J. R. 2009; Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 33:757–784 [View Article][PubMed]
    [Google Scholar]
  35. Pedersen K., Pedersen K., Jensen H., Finster K., Jensen V. F., Heuer O. E. 2007; Occurrence of antimicrobial resistance in bacteria from diagnostic samples from dogs. J Antimicrob Chemother 60:775–781 [View Article][PubMed]
    [Google Scholar]
  36. 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]
  37. Rubin J. E., Pitout J. D. 2014; Extended-spectrum β-lactamase, carbapenemase and AmpC producing Enterobacteriaceae in companion animals. Vet Microbiol 170:10–18 [View Article][PubMed]
    [Google Scholar]
  38. Schwarz S., Chaslus-Dancla E. 2001; Use of antimicrobials in veterinary medicine and mechanisms of resistance. Vet Res 32:201–225 [View Article][PubMed]
    [Google Scholar]
  39. Shaheen B. W., Nayak R., Foley S. L., Boothe D. M. 2013; Chromosomal and plasmid-mediated fluoroquinolone resistance mechanisms among broad-spectrum-cephalosporin-resistant Escherichia coli isolates recovered from companion animals in the USA. J Antimicrob Chemother 68:1019–1024 [View Article][PubMed]
    [Google Scholar]
  40. Strahilevitz J., Jacoby G. A., Hooper D. C., Robicsek A. 2009; Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22:664–689 [View Article][PubMed]
    [Google Scholar]
  41. Thomson K. S. 2010; Extended-spectrum-β-lactamases, AmpC, and carbapenemase issues. J Clin Microbiol 48:1019–1025 [View Article][PubMed]
    [Google Scholar]
  42. Weigel L. M., Anderson G. J., Tenover F. C. 2002; DNA gyrase and topoisomerase IV mutations associated with fluoroquinolone resistance in Proteus mirabilis. Antimicrob Agents Chemother 46:2582–2587 [View Article][PubMed]
    [Google Scholar]
  43. Yan J. J., Ko W. C., Jung Y. C., Chuang C. L., Wu J. J. 2002; Emergence of Klebsiella pneumoniae isolates producing inducible DHA-1 β-lactamase in a university hospital in Taiwan. J Clin Microbiol 40:3121–3126 [View Article][PubMed]
    [Google Scholar]
  44. Zamankhan Malayeri H., Jamshidi S., Zahraei Salehi T. 2010; Identification and antimicrobial susceptibility patterns of bacteria causing otitis externa in dogs. Vet Res Commun 34:435–444 [View Article][PubMed]
    [Google Scholar]
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