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  • 1 Departamento de Patología Animal, Zaragoza, 50013, Spain
  • 2 Centro de Encefalopatías y Enfermedades Transmisibles Emergentes (CEETE), Facultad de Veterinaria, Zaragoza, Spain
  • 3 Laboratorio de Genética Bioquímica (LAGENBIO), Facultad de Veterinaria, Zaragoza, Spain
  • 4 Agriculture and Agri-Food Canada, Lethbridge Research and Development Centre, Lethbridge, Canada
  • 5 Department of Veterinary Microbiology, Saskatoon, Canada
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Abstract

The aim of this study was to estimate the prevalence of antimicrobial resistance (AMR) in Escherichia coli from a dog population in Spain and assess specific virulence factors. Susceptibility to 22 antimicrobials was tested along with the production of extended-spectrum β-lactamases (ESBLs) and AmpC in faecal isolates from 100 dogs. Virulence-related genes associated with attaching and effacing E. coli (eae, Stx1, Stx2) and extraintestinal pathogenic E. coli – ExPEC – (papC, hlyA and cnf1) were detected by PCR. At least one kind of AMR was observed in 73% of the isolates. The highest prevalences corresponded to penicillin (45%), aminoglycoside (40%) and non-extended spectrum cephalosporin (39%) classes. Multidrug resistance (MDR) was observed in 53.4% of the resistant isolates. No resistance to colistin was found. Production of ESBL/AmpC enzymes was detected in 5% of E. coli. Shiga toxin-producing E. coli were not observed, enteropathogenic E. coli were identified in only 12% of them, and ExPEC were found in 25%. Dog faeces can be a source of E. coli strains potentially presenting a threat to humans through their virulence factors or AMR. The non-hygienic keeping of animals may increase the risk of colonisation of such pathogens in humans.

  • Bélanger, L., Garenaux, A., Harel, J., Boulianne, M., Nadeau, E. and Dozois, C. M. (2011): Escherichia coli from animal reservoirs as a potential source of human extraintestinal pathogenic E. coli. FEMS Immunol. Med. Microbiol. 62, 110.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Beutin, L. (1999): Escherichia coli as a pathogen in dogs and cats. Vet. Res. 30, 285298.

  • Blanco, M., Blanco, J. E., Rodríguez, E., Abalia, I., Alonso, M. P. and Blanco, J. (1997): Detection of virulence genes in uropathogenic Escherichia coli by polymerase chain reaction (PCR): comparison with results obtained using phenotypic methods. J. Microbiol. Methods 31, 3743.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Carattoli, A. (2013): Plasmids and the spread of resistance. Int. J. Med. Microbiol. 303, 298304.

  • Carattoli, A., Villa, L., Feudi, C., Curcio, L., Orsini, S., Luppi, A., Pezzotti, G. and Magistrali, C. F. (2017): Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Euro Surveill. 22, 30589.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • CLSI (Clinical and Laboratory Standards Institute) (2017): Performance Standards for Antimicrobial Susceptibility Testing. CLSI supplement M100, 27th edition. Clinical and Laboratory Standards Institute, Wayne, PA.

    • Search Google Scholar
    • Export Citation
  • Costa, D., Poeta, P., Sáenz, Y., Coelho, A. C., Matos, M., Vinué, L., Rodrigues, J. and Torres, C. (2008): Prevalence of antimicrobial resistance and resistance genes in faecal Escherichia coli isolates recovered from healthy pets. Vet. Microbiol. 127, 97105.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • da Silva, G. J. and Mendonça, N. (2012): Association between antimicrobial resistance and virulence in Escherichia coli. Virulence. 3, 1828.

  • DebRoy, C. and Maddox, C. W. (2001): Identification of virulence attributes of gastrointestinal Escherichia coli isolates of veterinary significance. Anim. Health Res. Rev. 2, 129140.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Diard, M., Garry, L., Selva, M., Mosser, T., Denamur, E. and Matic, I. (2010): Pathogenicity-associated islands in extraintestinal pathogenic Escherichia coli are fitness elements involved in intestinal colonization. J. Bacteriol. 192, 48854893.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • EFSA (European Food Safety Authority) and ECDC (European Centre for Disease Prevention and Control) (2019): The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J. 17, 5598.

    • Search Google Scholar
    • Export Citation
  • EMA (European Medicines Agency) (2018): Sales of Veterinary Antimicrobial Agents in 30 European Countries in 2016. EMA/275982/2018.

  • Ewers, C., Grobbel, M., Stamm, I., Kopp, P. A., Diehl, I., Semmler, T., Fruth, A., Beutlich, J., Guerra, B., Wieler, L. H. and Guenther, S. (2010): Emergence of human pandemic O25:H4-ST131 CTX-M-15 extended-spectrum-β-lactamase-producing Escherichia coli among companion animals. J. Antimicrob. Chemother. 65, 651660.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ewers, C., Li, G., Wilking, H., Kieβling, S., Alt, K., Antáo, E.-M., Laturnus, C., Diehl, I., Glodde, S., Homeier, T., Böhnke, U., Steinrück, H., Philipp, H.-C. and Wieler, L. H. (2007): Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: how closely related are they? Int. J. Med. Microbiol. 297, 163176.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Hancock, D. D., Besser, T. E., Rice, D. H., Ebel, E. D., Herriott, D. E. and Carpenter, L. V. (1998): Multiple sources of Escherichia coli O157 in feedlots and dairy farms in the Northwestern USA. Prev. Vet. Med. 35, 1119.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Johnson, J. R., Clabots, C. and Kuskowski, M.A. (2008): Multiple-host sharing, long-term persistence, and virulence of Escherichia coli clones from human and animal household members. J. Clin. Microbiol. 46, 40784082.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Johnson, J. R., Stell, A. L. and Delavari, P. (2001a): Canine feces as a reservoir of extraintestinal pathogenic Escherichia coli. Infect. Immun. 69, 13061314.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Johnson, J. R., Stell, A. L., Delavari, P., Murray, A. C., Kuskowski, M. and Gaastra, W. (2001b): Phylogenetic and pathotypic similarities between Escherichia coli isolates from urinary tract infections in dogs and extraintestinal infections in humans. J. Infect. Dis. 183, 897906.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Leite-Martins, L. R., Mahú, M. I. M., Costa, A. L., Mendes, Â., Lopes, E., Mendonça, D. M. V., Niza-Ribeiro, J. J. R., de Matos, A. J. F. and da Costa, P. M. (2014): Prevalence of antimicrobial resistance in enteric Escherichia coli from domestic pets and assessment of associated risk markers using a generalized linear mixed model. Prev. Vet. Med. 117, 2839.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Marques, C., Belas, A., Franco, A., Aboim, C., Gama, L. T. and Pomba, C. (2018): Increase in antimicrobial resistance and emergence of major international high-risk clonal lineages in dogs and cats with urinary tract infection: 16 year retrospective study. J. Antimicrob. Chemother. 73, 377384.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Marques, C., Gama, L. T., Belas, A., Bergström, K., Beurlet, S., Briend-Marchal, A., Broens, E. M., Costa, M., Criel, D., Damborg, P., van Dijk, M. A. M., van Dongen, A. M., Dorsch, R., Espada, C. M., Gerber, B., Kritsepi-Konstantinou, M., Loncaric, I., Mion, D., Misic, D., Movilla, R., Overesch, G., Perreten, V., Roura, X., Steenbergen, J., Timofte, D., Wolf, G., Zanoni, R. G., Schmitt, S., Guardabassi, L. and Pomba, C. (2016): European multicenter study on antimicrobial resistance in bacteria isolated from companion animal urinary tract infections. BMC Vet. Res. 12, 213.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Mateus, L., Henriques, S., Merino, C., Pomba, C., Lopes da Costa, L. and Silva, E. (2013): Virulence genotypes of Escherichia coli canine isolates from pyometra, cystitis and fecal origin. Vet. Microbiol. 166, 590594.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Nakazato, G., Gyles, C., Ziebell, K., Keller, R., Trabulsi, L., Gomes, T. A., Irino, K., Da Silveira, W. D. and Pestana De Castro, A. (2004): Attaching and effacing Escherichia coli isolated from dogs in Brazil: characteristics and serotypic relationship to human enteropathogenic E. coli (EPEC). Vet. Microbiol. 101, 269277.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Olsvik, O. and Strockbine, N. A. (1993): PCR detection of heat-stable, heat-labile, and shiga-like toxin genes in Escherichia coli. In: Persing, D., Smith, T., Tenover, F. and White, T. (eds) Diagnostic Molecular Microbiology: Principles and Applications. American Society for Microbiology. Washington DC. pp. 271276.

    • Search Google Scholar
    • Export Citation
  • Osugui, L., Pestana de Castro, A. F., Iovine, R., Irino, K. and Carvalho, V. M. (2014): Virulence genotypes, antibiotic resistance and the phylogenetic background of extraintestinal pathogenic Escherichia coli isolated from urinary tract infections of dogs and cats in Brazil. Vet. Microbiol. 171, 242247.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Oswald, E., Schmidt, H., Morabito, S., Karch, H., Marchès, O. and Caprioli, A. (2000): Typing of intimin genes in human and animal enterohemorrhagic and enteropathogenic Escherichia coli: characterization of a new intimin variant. Infect. Immun. 68, 6471.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Ovejero, C. M., Delgado-Blas, J. F., Calero-Caceres, W., Muniesa, M. and Gonzalez-Zorn, B. (2017): Spread of mcr-1-carrying Enterobacteriaceae in sewage water from Spain. J. Antimicrob. Chemother. 72, 10501053.

    • Search Google Scholar
    • Export Citation
  • Paterson, D. L. and Bonomo, R. A. (2005): Extended-spectrum β-lactamases: a clinical update. Clin. Microbiol. Rev. 18, 657686.

  • Platell, J. L., Cobbold, R. N., Johnson, J. R., Heisig, A., Heisig, P., Clabots, C., Kuskowski, M. A. and 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, 37823787.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Pomba, C., Rantala, M., Greko, C., Baptiste, K. E., Catry, B., van Duijkeren, E., Mateus, A., Moreno, M. A., Pyörälä, S., Ružauskas, M., Sanders, P., Teale, C., Threlfall, E. J., Kunsagi, Z., Torren-Edo, J., Jukes, H. and Törneke, K. (2017): Public health risk of antimicrobial resistance transfer from companion animals. J. Antimicrob. Chemother. 72, 957968.

    • Search Google Scholar
    • Export Citation
  • Poppe, C., Ayroud, M., Ollis, G., Chirino-Trejo, M., Smart, N., Quessy, S. and Michel, P. (2001): Trends in antimicrobial resistance of Salmonella isolated from animals, foods of animal origin, and the environment of animal production in Canada, 1994–1997. Microb. Drug Resist. 7, 197212.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Puño-Sarmiento, J., Medeiros, L., Chiconi, C., Martins, F., Pelayo, J., Rocha, S., Blanco, J., Blanco, M., Zanutto, M., Kobayashi, R. and Nakazato, G. (2013): Detection of diarrheagenic Escherichia coli strains isolated from dogs and cats in Brazil. Vet. Microbiol. 166, 676680.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Sancak, A. A., Rutgers, H. C., Hart, C. A. and Batt, R. M. (2004): Prevalence of enteropathic Escherichia coli in dogs with acute and chronic diarrhoea. Vet. Rec. 154, 101106.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Szmolka, A. and Nagy, B. (2013): Multidrug resistant commensal Escherichia coli in animals and its impact for public health. Front. Microbiol. 4, 258.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thompson, M. F., Litster, A. L., Platell, J. L. and Trott, D. J. (2011): Canine bacterial urinary tract infections: new developments in old pathogens. Vet. J. 190, 2227.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Thungrat, K., Price, S. B., Carpenter, D. M. and Boothe, D. M. (2015): Antimicrobial susceptibility patterns of clinical Escherichia coli isolates from dogs and cats in the United States: January 2008 through January 2013. Vet. Microbiol. 179, 287295.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Tramuta, C., Robino, P., Nucera, D., Salvarani, S., Banche, G., Malabaila, A. and Nebbia, P. (2014): Molecular characterization and antimicrobial resistance of faecal and urinary Escherichia coli isolated from dogs and humans in Italy. Vet. Ital. 50, 2330.

    • Search Google Scholar
    • Export Citation
  • Ukah, U. V, Glass, M., Avery, B., Daignault, D., Mulvey, M. R., Reid-Smith, R. J., Parmley, E. J., Portt, A., Boerlin, P. and Manges, A. R. (2018): Risk factors for acquisition of multidrug-resistant Escherichia coli and development of community-acquired urinary tract infections. Epidemiol. Infect. 146, 4657.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wedley, A. L., Dawson, S., Maddox, T. W., Coyne, K. P., Pinchbeck, G. L., Clegg, P., Nuttall, T., Kirchner, M. and Williams, N. J. (2017): Carriage of antimicrobial resistant Escherichia coli in dogs: prevalence, associated risk factors and molecular characteristics. Vet. Microbiol. 199, 2330.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Wedley, A. L., Maddox, T. W., Westgarth, C., Coyne, K. P., Pinchbeck, G. L., Williams, N. J. and Dawson, S. (2011): Prevalence of antimicrobial-resistant Escherichia coli in dogs in a cross-sectional, community-based study. Vet. Rec. 168, 354.

    • Crossref
    • Search Google Scholar
    • Export Citation

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