1887

Abstract

Purpose . The prevalence of antimicrobial-resistant bacteria, especially cephalosporin-resistant Enterobacteriaceae , is a major concern for human and animal health. We investigated the prevalence of cephalosporin-resistant Enterobacteriaceae among sheltered dogs and cats with various backgrounds.

Method . Faecal samples or rectal swabs were collected from 151 dogs and 182 cats, and screened for the presence of antimicrobial-resistant bacteria. Isolates were characterized phenotypically and genotypically by pulsed-field gel electrophoresis, multi-locus sequence typing and phylogenetic grouping. The animal attributes related to bacterial carriage were statistically analysed.

Results . Cephalosporin-resistant Enterobacteriaceae was detected in 22 dogs (14.6%) and 20 cats (11.0%): 21 were extended-spectrum β-lactamase (ESBL)-producing, 20 were AmpC-producing, and 1 was both ESBL- and AmpC-producing. Their β-lactamase genes were varied and associated with humans, animals or other origins. The genes CTX-M-14 (n=9) and CMY-2 (n=9) were dominant, but CTX-M-1, CTX-M-2, CTX-M-8, CTX-M-15, CTX-M-24, CTX-M-27, CTX-M-55 and DHA-1 genes were also detected. Genotyping of isolates revealed that β-lactamase-producing Enterobacteriaceae had high genetic diversity. Relationships between animals harbouring cephalosporin-resistant Enterobacteriaceae and individual attributes, such as sex and nutrition type, were detected, but there was no correlation between history of human association and the presence of the bacterium in either dogs or cats.

Conclusion . We found several types of cephalosporin-resistant Enterobacteriaceae distributed among companion animals with a range of individual attributes and histories in Osaka, Japan. Companion animals may play a bridging role in the circulation of antimicrobial-resistant bacteria from humans and from other origins.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000933
2019-01-30
2019-10-19
Loading full text...

Full text loading...

References

  1. WHO Antimicrobial resistance global report on surveillance World Health Organization; 2014
    [Google Scholar]
  2. Huijbers PM, Blaak H, de Jong MC, Graat EA, Vandenbroucke-Grauls CM et al. Role of the environment in the transmission of antimicrobial resistance to humans: a review. Environ Sci Technol 2015;49:11993–12004 [CrossRef]
    [Google Scholar]
  3. Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother 2017;72:2145–2155 [CrossRef]
    [Google Scholar]
  4. Jacoby GA. AmpC beta-lactamases. Clin Microbiol Rev 2009;22:162–182
    [Google Scholar]
  5. Correia S, Poeta P, Hébraud M, Capelo JL, Igrejas G. Mechanisms of quinolone action and resistance: where do we stand?. J Med Microbiol 2017;66:551–559 [CrossRef]
    [Google Scholar]
  6. Ewers C, Grobbel M, Stamm I, Kopp PA, Diehl I et al. Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-β-lactamase-producing Escherichia coli among companion animals. J Antimicrob Chemother 2010;65:651–660 [CrossRef]
    [Google Scholar]
  7. Poirel L, Cattoir V, Nordmann P. Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies. Front Microbio 2012;3:24 [CrossRef]
    [Google Scholar]
  8. Abraham S, Wong HS, Turnidge J, Johnson JR, Trott DJ. Carbapenemase-producing bacteria in companion animals: a public health concern on the horizon. J Antimicrob Chemother 2014;69:1155–1157 [CrossRef]
    [Google Scholar]
  9. Baede VO, Broens EM, Spaninks MP, Timmerman AJ, Graveland H et al. Raw pet food as a risk factor for shedding of extended-spectrum beta-lactamase-producing Enterobacteriaceae in household cats. PLoS One 2017;12:e0187239 [CrossRef]
    [Google Scholar]
  10. Pomba C, Rantala M, Greko C, Baptiste KE, Catry B et al. Public health risk of antimicrobial resistance transfer from companion animals. J Antimicrob Chemother 2017;72:957–968
    [Google Scholar]
  11. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268–281 [CrossRef]
    [Google Scholar]
  12. Clinical and Laboratory Standards Institute (CLSI) Performance standards for antimicrobial susceptibility testing: twenty-fifth informational supplement, CLSI document M100-S25. Wayne, PA: Clinical and Laboratory Standards Institute; 2015
    [Google Scholar]
  13. Yagi T, Wachino J, Kurokawa H, Suzuki S, Yamane K et al. Practical methods using boronic acid compounds for identification of class C beta-lactamase-producing Klebsiella pneumoniae and Escherichia coli. J Clin Microbiol 2005;43:2551–2558 [CrossRef]
    [Google Scholar]
  14. Dortet L, Poirel L, Nordmann P. Rapid identification of carbapenemase types in Enterobacteriaceae and Pseudomonas spp. by using a biochemical test. Antimicrob Agents Chemother 2012;56:6437–6440 [CrossRef]
    [Google Scholar]
  15. Matsumura Y, Nagao M, Iguchi M, Yagi T, Komori T et al. Molecular and clinical characterization of plasmid-mediated AmpC β-lactamase-producing Escherichia coli bacteraemia: a comparison with extended-spectrum β-lactamase-producing and non-resistant E. coli bacteraemia. Clin Microbiol Infect 2013;19:161–168 [CrossRef]
    [Google Scholar]
  16. Matsumura Y, Yamamoto M, Nagao M, Hotta G, Matsushima A et al. Emergence and spread of B2-ST131-O25b, B2-ST131-O16 and D-ST405 clonal groups among extended-spectrum-β-lactamase-producing Escherichia coli in Japan. J Antimicrob Chemother 2012;67:2612–2620 [CrossRef]
    [Google Scholar]
  17. Pérez-Pérez FJ, Hanson ND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002;40:2153–2162 [CrossRef]
    [Google Scholar]
  18. 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 [CrossRef]
    [Google Scholar]
  19. Kim HB, Park CH, Kim CJ, Kim E-C, Jacoby GA et al. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agent Chemother 2009;53:639–645 [CrossRef]
    [Google Scholar]
  20. Zhao J, Chen Z, Chen S, Deng Y, Liu Y et al. Prevalence and dissemination of oqxAB in Escherichia coli isolates from animals, farmworkers, and the environment. Antimicrob Agent Chemother 2010;54:4219–4224 [CrossRef]
    [Google Scholar]
  21. Liu BT, Wang XM, Liao XP, Sun J, Zhu HQ et al. Plasmid-mediated quinolone resistance determinants oqxAB and aac(6')-Ib-cr and extended-spectrum β-lactamase gene blaCTX-M-24 co-located on the same plasmid in one Escherichia coli strain from China. J Antimicrob Chemother 2011;66:1638–1639 [CrossRef]
    [Google Scholar]
  22. Paltansing S, Kraakman ME, Ras JM, Wessels E, Bernards AT. Characterization of fluoroquinolone and cephalosporin resistance mechanisms in Enterobacteriaceae isolated in a Dutch teaching hospital reveals the presence of an Escherichia coli ST131 clone with a specific mutation in parE. J Antimicrob Chemother 2013;68:40–45 [CrossRef]
    [Google Scholar]
  23. Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000;66:4555–4558 [CrossRef]
    [Google Scholar]
  24. Kawamura K, Sugawara T, Matsuo N, Hayashi K, Norizuki C et al. Spread of CTX-type extended-spectrum β-lactamase-producing Escherichia coli isolates of epidemic clone B2-O25-ST131 among dogs and cats in Japan. Microb Drug Resist 2017;23:1059–1066 [CrossRef]
    [Google Scholar]
  25. Maeyama Y, Taniguchi Y, Hayashi W, Ohsaki Y, Osaka S et al. Prevalence of ESBL/AmpC genes and specific clones among the third-generation cephalosporin-resistant Enterobacteriaceae from canine and feline clinical specimens in Japan. Vet Microbiol 2018;216:183–189 [CrossRef]
    [Google Scholar]
  26. Okubo T, Sato T, Yokota S, Usui M, Tamura Y. Comparison of broad-spectrum cephalosporin-resistant Escherichia coli isolated from dogs and humans in Hokkaido, Japan. J Infect Chemother 2014;20:243–249 [CrossRef]
    [Google Scholar]
  27. Hatakeyama K, Okuno R, Endo M, Yanagawa Y. Attempt of detection of drug resistant bacteria from canine stools (in Japanese). Ann Rep Tokyo Metr Inst Pub Health 2007;58:73–76
    [Google Scholar]
  28. Belas A, Salazar AS, Gama LT, Couto N, Pomba C. Risk factors for faecal colonisation with Escherichia coli producing extended-spectrum and plasmid-mediated AmpC β-lactamases in dogs. Vet Rec 2014;175:202 [CrossRef]
    [Google Scholar]
  29. Ewers C, Stamm I, Pfeifer Y, Wieler LH, Kopp PA et al. Clonal spread of highly successful ST15-CTX-M-15 Klebsiella pneumoniae in companion animals and horses. J Antimicrob Chemother 2014;69:2676–2680 [CrossRef]
    [Google Scholar]
  30. 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 [CrossRef]
    [Google Scholar]
  31. Nakane K, Kawamura K, Goto K, Arakawa Y. Long-term colonization by bla(CTX-M)-harboring Escherichia coli in healthy Japanese people engaged in food handling. Appl Environ Microbiol 2016;82:1818–1827 [CrossRef]
    [Google Scholar]
  32. Hiki M, Usui M, Kojima A, Ozawa M, Ishii Y et al. Diversity of plasmid replicons encoding the bla(CMY-2) gene in broad-spectrum cephalosporin-resistant Escherichia coli from livestock animals in Japan. Foodborne Pathog Dis 2013;10:243–249 [CrossRef]
    [Google Scholar]
  33. Kameyama M, Chuma T, Yabata J, Tominaga K, Iwata H et al. Prevalence and epidemiological relationship of CMY-2 AmpC β-lactamase and CTX-M extended-spectrum β-lactamase-producing Escherichia coli isolates from broiler farms in Japan. J Vet Med Sci 2013;75:1009–1015 [CrossRef]
    [Google Scholar]
  34. Ohnishi M, Okatani AT, Harada K, Sawada T, Marumo K et al. Genetic characteristics of CTX-M-type extended-spectrum-β-lactamase (ESBL)-producing enterobacteriaceae involved in mastitis cases on Japanese dairy farms, 2007 to 2011. J Clin Microbiol 2013;51:3117–3122 [CrossRef]
    [Google Scholar]
  35. Usui M, Iwasa T, Fukuda A, Sato T, Okubo T et al. The role of flies in spreading the extended-spectrum β-lactamase gene from cattle. Microb Drug Resist 2013;19:415–420 [CrossRef]
    [Google Scholar]
  36. Gomi R, Matsuda T, Matsumura Y, Yamamoto M, Tanaka M et al. Occurrence of clinically important lineages, including the sequence type 131 C1-M27 subclone, among extended-spectrum-β-lactamase-producing Escherichia coli in Wastewater. Antimicrob Agents Chemother 2017;61:e00564–00517 [CrossRef]
    [Google Scholar]
  37. 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 and Immunol 2012;56:480–485 [CrossRef]
    [Google Scholar]
  38. Peirano G, Pitout JD. Molecular epidemiology of Escherichia coli producing CTX-M β-lactamases: the worldwide emergence of clone ST131 O25:H4. Int J Antimicrob Agents 2010;35:316–321 [CrossRef]
    [Google Scholar]
  39. 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 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000933
Loading
/content/journal/jmm/10.1099/jmm.0.000933
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