1887

Abstract

The aim of this study was to assess the efficacy of candidate antimicrobials against extended-spectrum β-lactamase (ESBL)-producing isolates of extraintestinal pathogenic (ExPEC) from companion animals.

A total of 90 ESBL-producing ExPEC isolates from dogs and cats were tested for susceptibility to 16 antimicrobials with the agar dilution method. We also identified the ESBLs and AmpC β-lactamases of these isolates with PCR and DNA sequencing.

All isolates were susceptible to meropenem, tebipenem and amikacin (AMK), and various proportions were susceptible to latamoxef (LMX, 97.8 %), fosfomycin (FOM, 97.8 %), faropenem (FPM, 96.7 %), nitrofurantoin (NFT, 96.7 %), flomoxef (FMX, 93.3 %), piperacillin/tazobactam (PTZ, 92.2 %), cefmetazole (CMZ, 91.1 %), chloramphenicol (80.0 %), trimethoprim/sulfamethoxazole (64.4 %), amoxicillin/clavulanic acid (63.3 %), ceftibuten (60.0 %), tetracycline (52.2 %) and enrofloxacin (10.0 %). A genetic analysis showed that 83 of the 90 (92.2 %) isolates were positive for CTX-M-type genes: CTX-M-14 (=26), CTX-M-27 (=20), CTX-M-55 (=17), CTX-M-15 (=12), CTX-M-2 (=5), CTX-M-24 (=2), CTX-M-104 (=2) and CTX-M-3 (=1). Eight isolates also expressed AmpC β-lactamase phenotypes.

This study demonstrates that the susceptibility rates to PTZ, CMZ, LMX, AMK, FOM, FPM, NFT and FMX were similar to those to carbapenems (>90 %), implying that these drugs are available alternatives to carbapenems for the treatment of companion animals infected with ExPEC-producing CTX-M-type ESBLs. Further studies of the effective use of these antimicrobials are required.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000535
2017-08-01
2024-12-06
Loading full text...

Full text loading...

/deliver/fulltext/jmm/66/8/1085.html?itemId=/content/journal/jmm/10.1099/jmm.0.000535&mimeType=html&fmt=ahah

References

  1. Beutin L. Escherichia coli as a pathogen in dogs and cats. Vet Res 1999; 30:285–298 [View Article][PubMed]
    [Google Scholar]
  2. Oluoch AO, Kim CH, Weisiger RM, Koo HY, Siegel AM et al. Nonenteric Escherichia coli isolates from dogs: 674 cases (1990–1998). J Am Vet Med Assoc 2001; 218:381–384 [View Article][PubMed]
    [Google Scholar]
  3. Weese JS, Blondeau JM, Boothe D, Breitschwerdt EB, Guardabassi L et al. Antimicrobial use guidelines for treatment of urinary tract disease in dogs and cats: antimicrobial guidelines working group of the International Society for Companion Animal Infectious Diseases. Vet Med Int 2011; 2011:1–9 [View Article]
    [Google Scholar]
  4. Thungrat K, Price SB, Carpenter DM, Boothe DM. Antimicrobial susceptibility patterns of clinical Escherichia coli isolates from dogs and cats in the United States: January 2008 through January 2013. Vet Microbiol 2015; 179:287–295 [View Article][PubMed]
    [Google Scholar]
  5. Ewers C, Bethe A, Semmler T, Guenther S, Wieler LH. Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin Microbiol Infect 2012; 18:646–655 [View Article][PubMed]
    [Google Scholar]
  6. Rubin JE, Pitout JD. Extended-spectrum β-lactamase, carbapenemase and AmpC producing Enterobacteriaceae in companion animals. Vet Microbiol 2014; 170:10–18 [View Article][PubMed]
    [Google Scholar]
  7. Pitout JD, Laupland KB. Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008; 8:159–166 [View Article][PubMed]
    [Google Scholar]
  8. Rupp ME, Fey PD. Extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae: considerations for diagnosis, prevention and drug treatment. Drugs 2003; 63:353–365[PubMed] [CrossRef]
    [Google Scholar]
  9. Paterson DL. Recommendation for treatment of severe infections caused by Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs). Clin Microbiol Infect 2000; 6:460–463 [View Article][PubMed]
    [Google Scholar]
  10. Vardakas KZ, Tansarli GS, Rafailidis PI, Falagas ME. Carbapenems versus alternative antibiotics for the treatment of bacteraemia due to Enterobacteriaceae producing extended-spectrum β-lactamases: a systematic review and meta-analysis. J Antimicrob Chemother 2012; 67:2793–2803 [View Article][PubMed]
    [Google Scholar]
  11. Harada K, Nakai Y, Kataoka Y. 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 2012; 56:480–485 [View Article][PubMed]
    [Google Scholar]
  12. Paterson DL. Resistance in Gram-negative bacteria: Enterobacteriaceae. Am J Med 2006; 119:S20–S28 [View Article][PubMed]
    [Google Scholar]
  13. Harada K, Shimizu T, Mukai Y, Kuwajima K, Sato T et al. Phenotypic and molecular characterization of antimicrobial resistance in Klebsiella spp. isolates from companion animals in Japan: clonal dissemination of multidrug-resistant extended-spectrum β-lactamase-producing Klebsiella pneumoniae. Front Microbiol 2016; 7:1021 [View Article][PubMed]
    [Google Scholar]
  14. Harada K, Shimizu T, Mukai Y, Kuwajima K, Sato T et al. Phenotypic and molecular characterization of antimicrobial resistance in Enterobacter spp. isolates from companion animals in Japan. PLoS One 2017; 12:e0174178 [View Article][PubMed]
    [Google Scholar]
  15. Ohkusu K. Cost-effective and rapid presumptive identification of Gram-negative bacilli in routine urine, pus, and stool cultures: evaluation of the use of CHROMagar orientation medium in conjunction with simple biochemical tests. J Clin Microbiol 2000; 38:4586–4592[PubMed]
    [Google Scholar]
  16. Stalder GL, Loncaric I, Walzer C. Diversity of enterobacteria including β-lactamase producing isolates associated with the Spanish slug (Arion vulgaris). Sci Total Environ 2014; 479-480:11–16 [View Article][PubMed]
    [Google Scholar]
  17. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing Twentieth Informational Supplement. CLSI Document M100-S20, Wayne, PA, USA 2013
    [Google Scholar]
  18. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals Approved Standard, Fourth edn. CLSI document VET01-A4. Wayne, PA:CLSI 2013
    [Google Scholar]
  19. Muratani T, Doi K, Kobayashi T, Nakamura T, Matsumoto T. Antimicrobial activity of tebipenem against various clinical isolates from various specimen, mainly urinary tract. Jpn J Antibiot 2009; 62:116–126[PubMed]
    [Google Scholar]
  20. Tärnberg M, Ostholm-Balkhed A, Monstein HJ, Hällgren A, Hanberger H et al. In vitro activity of beta-lactam antibiotics against CTX-M-producing Escherichia coli. Eur J Clin Microbiol Infect Dis 2011; 30:981–987 [View Article][PubMed]
    [Google Scholar]
  21. Yoshikawa K, Moritake J, Suzuki K, Kira S, Koide H et al. Prevalence and drug-susceptibilities of extended-spectrum β-lactamase producing Escherichia coli strains isolated from urine. Jpn J Chemother 2016; 62:198–203
    [Google Scholar]
  22. Zykov IN, Sundsfjord A, Småbrekke L, Samuelsen Ø. The antimicrobial activity of mecillinam, nitrofurantoin, temocillin and fosfomycin and comparative analysis of resistance patterns in a nationwide collection of ESBL-producing Escherichia coli in Norway. Infect Dis 2016; 48:99–107 [View Article]
    [Google Scholar]
  23. Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals Second Informational Supplement. CLSI document VET01-S2. Wayne, PA:CLSI 2013
    [Google Scholar]
  24. Xu L, Ensor V, Gossain S, Nye K, Hawkey P. Rapid and simple detection of blaCTX-M genes by multiplex PCR assay. J Med Microbiol 2005; 54:1183–1187 [View Article][PubMed]
    [Google Scholar]
  25. Kojima A, Ishii Y, Ishihara K, Esaki H, Asai T et al. 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 2005; 49:3533–3537 [View Article][PubMed]
    [Google Scholar]
  26. Shibata N, Kurokawa H, Doi Y, Yagi T, Yamane K et al. PCR classification of CTX-M-type β-lactamase genes identified in clinically isolated Gram-negative bacilli in Japan. Antimicrob Agents Chemother 2006; 50:791–795 [View Article][PubMed]
    [Google Scholar]
  27. Pérez-Pérez FJ, Hanson ND. Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex-PCR. J Clin Microbiol 2002; 40:2153–2162 [View Article][PubMed]
    [Google Scholar]
  28. Guerra B, Fischer J, Helmuth R. An emerging public health problem: acquired carbapenemase-producing microorganisms are present in food-producing animals, their environment, companion animals and wild birds. Vet Microbiol 2014; 171:290–297 [View Article][PubMed]
    [Google Scholar]
  29. Dalhoff A, Nasu T, Okamoto K. Beta-lactamase stability of faropenem. Chemotherapy 2003; 49:229–236 [View Article][PubMed]
    [Google Scholar]
  30. Matsumura Y, Yamamoto M, Nagao M, Komori T, Fujita N et al. Multicenter retrospective study of cefmetazole and flomoxef for treatment of extended-spectrum-β-lactamase-producing Escherichia coli bacteremia. Antimicrob Agents Chemother 2015; 59:5107–5113 [View Article][PubMed]
    [Google Scholar]
  31. Mushtaq S, Hope R, Warner M, Livermore DM. Activity of faropenem against cephalosporin-resistant Enterobacteriaceae. J Antimicrob Chemother 2007; 59:1025–1030 [View Article][PubMed]
    [Google Scholar]
  32. Matsumura Y, Yamamoto M, Nagao M, Tanaka M, Takakura S et al. In vitro activities and detection performances of cefmetazole and flomoxef for extended-spectrum β-lactamase and plasmid-mediated AmpC β-lactamase-producing Enterobacteriaceae. Diagn Microbiol Infect Dis 2016; 84:322–327 [View Article][PubMed]
    [Google Scholar]
  33. Rodríguez-Baño J, Navarro MD, Retamar P, Picón E, Pascual Á et al. β-Lactam/β-lactam inhibitor combinations for the treatment of bacteremia due to extended-spectrum β-lactamase-producing Escherichia coli: a post hoc analysis of prospective cohorts. Clin Infect Dis 2012; 54:167–174 [View Article][PubMed]
    [Google Scholar]
  34. Harris PN, Tambyah PA, Paterson DL. β-Lactam and β-lactamase inhibitor combinations in the treatment of extended-spectrum β-lactamase producing Enterobacteriaceae: time for a reappraisal in the era of few antibiotic options?. Lancet Infect Dis 2015; 15:475–485 [View Article][PubMed]
    [Google Scholar]
  35. Tamma PD, Han JH, Rock C, Harris AD, Lautenbach E et al. Carbapenem therapy is associated with improved survival compared with piperacillin-tazobactam for patients with extended-spectrum β-lactamase bacteremia. Clin Infect Dis 2015; 60:1319–1325 [View Article][PubMed]
    [Google Scholar]
  36. Ng TM, Khong WX, Harris PN, De PP, Chow A et al. Empiric piperacillin-tazobactam versus carbapenems in the treatment of bacteraemia due to extended-spectrum beta-lactamase-producing Enterobacteriaceae. PLoS One 2016; 11:e0153696 [View Article][PubMed]
    [Google Scholar]
  37. López-Cerero L, Picón E, Morillo C, Hernández JR, Docobo F et al. Comparative assessment of inoculum effects on the antimicrobial activity of amoxycillin-clavulanate and piperacillin-tazobactam with extended-spectrum β-lactamase-producing and extended-spectrum β-lactamase-non-producing Escherichia coli isolates. Clin Microbiol Infect 2010; 16:132–136 [View Article][PubMed]
    [Google Scholar]
  38. Bauernfeind A. Ceftibuten and bactericidal kinetics. Comparative in vitro activity against Enterobacteriaceae producing extended spectrum β-lactamases. Diagn Microbiol Infect Dis 1991; 14:89–92 [View Article][PubMed]
    [Google Scholar]
  39. Nakamura T, Komatsu M, Yamasaki K, Fukuda S, Higuchi T et al. Susceptibility of various oral antibacterial agents against extended-spectrum β-lactamase producing Escherichia coli and Klebsiella pneumoniae. J Infect Chemother 2014; 20:48–51 [View Article][PubMed]
    [Google Scholar]
  40. Costa D, Poeta P, Sáenz Y, Coelho AC, Matos M et al. Prevalence of antimicrobial resistance and resistance genes in faecal Escherichia coli isolates recovered from healthy pets. Vet Microbiol 2008; 127:97–105 [View Article][PubMed]
    [Google Scholar]
  41. Hubka P, Boothe DM. In vitro susceptibility of canine and feline Escherichia coli to fosfomycin. Vet Microbiol 2011; 149:277–282 [View Article][PubMed]
    [Google Scholar]
  42. Maaland M, Guardabassi L. In vitro antimicrobial activity of nitrofurantoin against Escherichia coli and Staphylococcus pseudintermedius isolated from dogs and cats. Vet Microbiol 2011; 151:396–399 [View Article][PubMed]
    [Google Scholar]
  43. Falagas ME, Kastoris AC, Kapaskelis AM, Karageorgopoulos DE. Fosfomycin for the treatment of multidrug-resistant, including extended-spectrum β-lactamase producing, Enterobacteriaceae infections: a systematic review. Lancet Infect Dis 2010; 10:43–50 [View Article][PubMed]
    [Google Scholar]
  44. Tasbakan MI, Pullukcu H, Sipahi OR, Yamazhan T, Ulusoy S. Nitrofurantoin in the treatment of extended-spectrum β-lactamase-producing Escherichia colirelated lower urinary tract infection. Int J Antimicrob Agents 2012; 40:554–556 [View Article][PubMed]
    [Google Scholar]
  45. Cho SY, Choi SM, Park SH, Lee DG, Choi JH et al. Amikacin therapy for urinary tract infections caused by extended-spectrum β-lactamase-producing Escherichia coli. Korean J Intern Med 2016; 31:156–161 [View Article][PubMed]
    [Google Scholar]
  46. Shaheen BW, Nayak R, Foley SL, Boothe DM. 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 2013; 68:1019–1024 [View Article][PubMed]
    [Google Scholar]
  47. Liu X, Thungrat K, Boothe DM. Occurrence of OXA-48 carbapenemase and other β-lactamase genes in ESBL-producing multidrug resistant Escherichia coli from dogs and cats in the United States, 2009-2013. Front Microbiol 2016; 7:1057 [View Article][PubMed]
    [Google Scholar]
  48. Dierikx CM, van Duijkeren E, Schoormans AH, van Essen-Zandbergen A, Veldman K et al. Occurrence and characteristics of extended-spectrum-β-lactamase- and AmpC-producing clinical isolates derived from companion animals and horses. J Antimicrob Chemother 2012; 67:1368–1374 [View Article][PubMed]
    [Google Scholar]
  49. Tamang MD, Nam HM, Jang GC, Kim SR, Chae MH et al. 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 2012; 56:2705–2712 [View Article][PubMed]
    [Google Scholar]
  50. Timofte D, Maciuca IE, Williams NJ, Wattret A, Schmidt V. Veterinary hospital dissemination of CTX-M-15 extended-spectrum beta-lactamase-producing Escherichia coli ST410 in the United Kingdom. Microb Drug Resist 2016; 22:609–615 [View Article][PubMed]
    [Google Scholar]
  51. Sun Y, Zeng Z, Chen S, Ma J, He L et al. High prevalence of blaCTX-M extended-spectrum β-lactamase genes in Escherichia coli isolates from pets and emergence of CTX-M-64 in China. Clin Microbiol Infect 2010; 16:1475–1481 [View Article][PubMed]
    [Google Scholar]
  52. Meireles D, Leite-Martins L, Bessa LJ, Cunha S, Fernandes R et al. Molecular characterization of quinolone resistance mechanisms and extended-spectrum β-lactamase production in Escherichia coli isolated from dogs. Comp Immunol Microbiol Infect Dis 2015; 41:43–48 [View Article][PubMed]
    [Google Scholar]
  53. Zheng H, Zeng Z, Chen S, Liu Y, Yao Q et al. Prevalence and characterisation of CTX-M β-lactamases amongst Escherichia coli isolates from healthy food animals in China. Int J Antimicrob Agents 2012; 39:305–310 [View Article][PubMed]
    [Google Scholar]
/content/journal/jmm/10.1099/jmm.0.000535
Loading
/content/journal/jmm/10.1099/jmm.0.000535
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error