Occurrence and potential transmission of extended-spectrum beta-lactamase-producing extraintestinal pathogenic and enteropathogenic Escherichia coli in domestic dog faeces from Minnesota

. 2022 Nov ; 69 (7) : 888-895. [epub] 20220707

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S.

Perzistentní odkaz   https://www.medvik.cz/link/pmid35799333

Grantová podpora
VA - United States

Interactions between humans and pets are increasingly valued in western countries, leading to more extensive contact between humans and their pets within households. Although the magnitude of the risk of transfer of Escherichia coli between humans and their companion animals is undefined, that such transmission occurs has been established and warrants attention. This study examined 186 fresh faecal samples from companion dogs visiting 22 municipal dog parks in the Minneapolis/Saint Paul metropolitan area, Minnesota, USA. Samples were processed to isolate 3rd-generation cephalosporin-resistant E. coli, which were further characterized using PCR-based virulence genotyping, antimicrobial susceptibility profiling and whole-genome sequencing. Of the 186 faecal samples, 29% yielded cephalosporin-resistant E. coli, and 2.2% yielded extended-spectrum beta-lactamase producers. Co-resistance to sulfonamides was typical (77.3% of isolates), and multidrug resistance (i.e. to ≥3 antimicrobial classes), including to combinations of tetracyclines, phenicols, quinolones and aminoglycosides, was substantial (18.9% of isolates). Identified beta-lactamase genes included blaCMY-2 , blaTEM-1B , blaTEM-1 , blaCTX-M-24 , blaCTX-M-15 and blaOXA-1 . Genome sequencing of 14 isolates identified genes typical of extraintestinal pathogenic E. coli or enteropathogenic E. coli. In three instances, closely related isolates were recovered from different dogs, within either the same park-suggesting transfer of E. coli between dogs within the park-or different parks-suggesting that dogs may be pre-disposed to carry certain E. coli types, such as those from serogroups O4, O71 and O157. This study adds to the existing evidence that companion dogs can harbour and share antimicrobial-resistant E. coli with presumed intestinal or extraintestinal pathogenic potential.

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Ahmed, L. N. , Price, L. B. , & Graham, J. P. (2015). An exploratory study of dog park visits as a risk factor for exposure to drug‐resistant extra‐intestinal pathogenic E. coli (ExPEC). BMC Research Notes, 8, 137. 10.1186/s13104-015-1103-2 PubMed DOI PMC

Armstrong, J. , Johnson, T. , Pantlin, G. , Danzeisen, J. , Kobluk, K. , Olsen, K. , Bender, J.B. (2015). Characterization, and potential zoonotic and antibiotic resistant organisms among dogs using dog parks in the Minneapolis/St Paul metropolitan area . Paper presented at the emerging infectious disease conference, Atlanta, GA, USA.

Aslantas, O. , & Yilmaz, E. S. (2017). Prevalence and molecular characterization of extended‐spectrum beta‐lactamase (ESBL) and plasmidic AmpC beta‐lactamase (pAmpC) producing Escherichia coli in dogs. The Journal of Veterinary Medical Science, 79(6), 1024–1030. 10.1292/jvms.16-0432 PubMed DOI PMC

Bankevich, A. , Nurk, S. , Antipov, D. , Gurevich, A. A. , Dvorkin, M. , Kulikov, A. S. , Lesin, V. M. , Nikolenko, S. I. , Pham, S. , Prjibelski, A. D. , Pyshkin, A. V. , Sirotkin, A. V. , Vyahhi, N. , Tesler, G. , Alekseyev, M. A. , & Pevzner, P. A. (2012). SPAdes: A new genome assembly algorithm and its applications to single‐cell sequencing. Journal of Computational Biology, 19(5), 455–477. 10.1089/cmb.2012.0021 PubMed DOI PMC

Belas, A. , Salazar, A. S. , Gama, L. T. , Couto, N. , & Pomba, C. (2014). Risk factors for faecal colonisation with Escherichia coli producing extended‐spectrum and plasmid‐mediated AmpC beta‐lactamases in dogs. The Veterinary Record, 175(8), 202. 10.1136/vr.101978 PubMed DOI

Bentancor, A. , Vilte, D. A. , Rumi, M. V. , Carbonari, C. C. , Chinen, I. , Larzabal, M. , Cataldi, A. , & Mercado, E. C. (2010). Characterization of non‐Shiga‐toxin‐producing Escherichia coli O157 strains isolated from dogs. Revista Argentina de Microbiología, 42(1), 46–48. 10.1590/S0325-75412010000100010 PubMed DOI

Blanco Crivelli, X. , Bonino, M. P. , Von Wernich Castillo, P. , Navarro, A. , Degregorio, O. , & Bentancor, A. (2018). Detection and characterization of enteropathogenic and Shiga toxin‐producing Escherichia coli strains in Rattus spp. from Buenos Aires. Frontiers in Microbiology, 9, 199. 10.3389/fmicb.2018.00199 PubMed DOI PMC

Bugarel, M. , Martin, A. , Fach, P. , & Beutin, L. (2011). Virulence gene profiling of enterohemorrhagic (EHEC) and enteropathogenic (EPEC) Escherichia coli strains: A basis for molecular risk assessment of typical and atypical EPEC strains. BMC Microbiology, 11, 142. 10.1186/1471-2180-11-142 PubMed DOI PMC

Carattoli, A. , Zankari, E. , Garcia‐Fernandez, A. , Voldby Larsen, M. , Lund, O. , Villa, L. , Møller Aarestrup, F. , & Hasman, H. (2014). In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrobial Agents and Chemotherapy, 58(7), 3895–3903. 10.1128/AAC.02412-14 PubMed DOI PMC

Carvalho, A. C. , Barbosa, A. V. , Arais, L. R. , Ribeiro, P. F. , Carneiro, V. C. , & Cerqueira, A. M. (2016). Resistance patterns, ESBL genes, and genetic relatedness of Escherichia coli from dogs and owners. Brazilian Journal of Microbiology, 47(1), 150–158. 10.1016/j.bjm.2015.11.005 PubMed DOI PMC

Clermont, O. , Bonacorsi, S. , & Bingen, E. (2000). Rapid and simple determination of the Escherichia coli phylogenetic group. Applied and Environmental Microbiology, 66(10), 4555–4558. 10.1128/aem.66.10.4555-4558.2000 PubMed DOI PMC

CLSI . (2017). Performance standards for antimicrobial susceptibility typing (27th ed. In CLSI supplement M100). Clinical and Laboratory Standards Institute.

Damborg, P. , Morsing, M. K. , Petersen, T. , Bortolaia, V. , & Guardabassi, L. (2015). CTX‐M‐1 and CTX‐M‐15‐producing Escherichia coli in dog faeces from public gardens. Acta Veterinaria Scandinavica, 57, 83. 10.1186/s13028-015-0174-3 PubMed DOI PMC

DebRoy, C. , & Maddox, C. W. (2001). Identification of virulence attributes of gastrointestinal Escherichia coli isolates of veterinary significance. Animal Health Research Reviews, 2(2), 129–140. PubMed

Deng, W. , Puente, J. L. , Gruenheid, S. , Li, Y. , Vallance, B. A. , Vazquez, A. , Barba, J. , Ibarra, J. A. , O'Donnell, P. , Metalnikov, P. , Ashman, K. , Lee, S. , Goode, D. , Pawson, T. , & Finlay, B. B. (2004). Dissecting virulence: Systematic and functional analyses of a pathogenicity Island. Proceedings of the National Academy of Sciences of the United States of America, 101(10), 3597–3602. 10.1073/pnas.0400326101 PubMed DOI PMC

Feng, P. C. , Keys, C. , Lacher, D. W. , Beutin, L. , Bentancor, A. , Heuvelink, A. , Afset, J. E. , Rumi, V. , & Monday, S. (2012). Clonal relations of atypical enteropathogenic Escherichia coli O157:H16 strains isolated from various sources from several countries. FEMS Microbiology Letters, 337(2), 126–131. 10.1111/1574-6968.12017 PubMed DOI

Flament‐Simon, S. C. , Toro, M. , Garcia, V. , Blanco, J. E. , Blanco, M. , Alonso, M. P. , Goicoa, A. , Díaz‐González, J. , Nicolas‐Chanoine, M. H. , & Blanco, J. (2020). Molecular characteristics of extraintestinal pathogenic E. coli (ExPEC), uropathogenic E. coli (UPEC), and multidrug resistant E. coli isolated from healthy dogs in Spain. Whole genome sequencing of canine ST372 isolates and comparison with human isolates causing extraintestinal infections. Microorganisms, 8(11), 1712. 10.3390/microorganisms8111712 PubMed DOI PMC

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 beta‐lactamase/AmpC‐producing Enterobacteriaceae in cats and dogs. Frontiers in Microbiology, 4, 242. 10.3389/fmicb.2013.00242 PubMed DOI PMC

Joensen, K. G. , Tetzschner, A. M. , Iguchi, A. , Aarestrup, F. M. , & Scheutz, F. (2015). Rapid and easy in silico serotyping of Escherichia coli isolates by use of whole‐genome sequencing data. Journal of Clinical Microbiology, 53(8), 2410–2426. 10.1128/JCM.00008-15 PubMed DOI PMC

Johnson, J. R. , Murray, A. C. , Gajewski, A. , Sullivan, M. , Snippes, P. , Kuskowski, M. A. , & Smith, K. E. (2003). Isolation and molecular characterization of nalidixic acid‐resistant extraintestinal pathogenic Escherichia coli from retail chicken products. Antimicrobial Agents and Chemotherapy, 47(7), 2161–2168. 10.1128/aac.47.7.2161-2168.2003 PubMed DOI PMC

Johnson, J. R. , Porter, S. , Johnston, B. , Kuskowski, M. A. , Spurbeck, R. R. , Mobley, H. L. , & Williamson, D. A. (2015). Host characteristics and bacterial traits predict experimental virulence for Escherichia coli bloodstream isolates from patients with urosepsis. Open forum . Infectious Diseases, 2(3), ofv083. 10.1093/ofid/ofv083 PubMed DOI PMC

Johnson, J. R. , Stell, A. L. , Delavari, P. , Murray, A. C. , Kuskowski, M. , & Gaastra, W. (2001). Phylogenetic and pathotypic similarities between Escherichia coli isolates from urinary tract infections in dogs and extraintestinal infections in humans. The Journal of Infectious Diseases, 183(6), 897–906. 10.1086/319263 PubMed DOI

Karkaba, A. , Hill, K. , Benschop, J. , Pleydell, E. , & Grinberg, A. (2019). Carriage and population genetics of extended spectrum beta‐lactamase‐producing Escherichia coli in cats and dogs in New Zealand. Veterinary Microbiology, 233, 61–67. 10.1016/j.vetmic.2019.04.015 PubMed DOI

Kidsley, A. K. , O'Dea, M. , Saputra, S. , Jordan, D. , Johnson, J. R. , Gordon, D. M. , Johnson, J. R. , O'Dea, M. , Mollinger, J. L. , Abraham, S. , & Trott, D. J. (2020). Genomic analysis of phylogenetic group B2 extraintestinal pathogenic E. coli causing infections in dogs in Australia. Veterinary Microbiology, 248, 108783. 10.1016/j.vetmic.2020.108783 PubMed DOI

Kleinheinz, K. A. , Joensen, K. G. , & Larsen, M. V. (2014). Applying the ResFinder and VirulenceFinder web‐services for easy identification of acquired antibiotic resistance and E. coli virulence genes in bacteriophage and prophage nucleotide sequences. Bacteriophage, 4(1), e27943. 10.4161/bact.27943 PubMed DOI PMC

Larsen, M. V. , Cosentino, S. , Rasmussen, S. , Friis, C. , Hasman, H. , Marvig, R. L. , Jelsbak, L. , Sicheritz‐Pontén, T. , Ussery, D. W. , Aarestrup, F. M. , & Lund, O. (2012). Multilocus sequence typing of total‐genome‐sequenced bacteria. Journal of Clinical Microbiology, 50(4), 1355–1361. 10.1128/JCM.06094-11 PubMed DOI PMC

Madec, J. Y. , Haenni, M. , Nordmann, P. , & Poirel, L. (2017). Extended‐spectrum beta‐lactamase/AmpC‐ and carbapenemase‐producing Enterobacteriaceae in animals: A threat for humans? Clinical Microbiology and Infection, 23(11), 826–833. 10.1016/j.cmi.2017.01.013 PubMed DOI

McDermott, P. F. , Tyson, G. H. , Kabera, C. , Chen, Y. , Li, C. , Folster, J. P. , Ayers, S. L. , Lam, C. , Tate, H. P. , & Zhao, S. (2016). Whole‐genome sequencing for detecting antimicrobial resistance in nontyphoidal salmonella . Antimicrobial Agents and Chemotherapy, 60(9), 5515–5520. 10.1128/AAC.01030-16 PubMed DOI PMC

Metsalu, T. , & Vilo, J. (2015). ClustVis: A web tool for visualizing clustering of multivariate data using principal component analysis and heatmap. Nucleic Acids Research, 43(W1), W566–W570. 10.1093/nar/gkv468 PubMed DOI PMC

Ortega‐Paredes, D. , Haro, M. , Leoro‐Garzon, P. , Barba, P. , Loaiza, K. , Mora, F. , Fors, M. , Vinueza‐Burgos, C. , & Fernandez‐Moreira, E. (2019). Multidrug‐resistant Escherichia coli isolated from canine faeces in a public park in Quito, Ecuador. Journal of Global Antimicrobial Resistance, 18, 263–268. 10.1016/j.jgar.2019.04.002 PubMed DOI

PRNewswire T. H. P . (2015). More Than Ever, Pets are Members of the Family [Press release]. https://www.prnewswire.com/news‐releases/more‐than‐ever‐pets‐are‐members‐of‐the‐family‐300114501.html

Rocha‐Gracia, R. C. , Cortes‐Cortes, G. , Lozano‐Zarain, P. , Bello, F. , Martinez‐Laguna, Y. , & Torres, C. (2015). Faecal Escherichia coli isolates from healthy dogs harbour CTX‐M‐15 and CMY‐2 beta‐lactamases. Veterinary Journal, 203(3), 315–319. 10.1016/j.tvjl.2014.12.026 PubMed DOI

Roer, L. , Tchesnokova, V. , Allesoe, R. , Muradova, M. , Chattopadhyay, S. , Ahrenfeldt, J. , MCF, T. , Lund, O. , Hansen, F. , Hammerum, A. M. , Sokurenko, E. , & Hasman, H. (2017). Development of a web tool for Escherichia coli subtyping based on fimH alleles. Journal of Clinical Microbiology, 55(8), 2538–2543. 10.1128/JCM.00737-17 PubMed DOI PMC

Salipante, S. J. , SenGupta, D. J. , Cummings, L. A. , Land, T. A. , Hoogestraat, D. R. , & Cookson, B. T. (2015). Application of whole‐genome sequencing for bacterial strain typing in molecular epidemiology. Journal of Clinical Microbiology, 53(4), 1072–1079. 10.1128/JCM.03385-14 PubMed DOI PMC

Schmidt, V. M. , Pinchbeck, G. L. , Nuttall, T. , McEwan, N. , Dawson, S. , & Williams, N. J. (2015). Antimicrobial resistance risk factors and characterisation of faecal E. coli isolated from healthy Labrador retrievers in the United Kingdom. Preventive Veterinary Medicine, 119(1–2), 31–40. 10.1016/j.prevetmed.2015.01.013 PubMed DOI

Stenske, K. A. , Bemis, D. A. , Gillespie, B. E. , D'Souza, D. H. , Oliver, S. P. , Draughon, F. A. , Matteson, K. J. , & Bartges, J. W. (2009). Comparison of clonal relatedness and antimicrobial susceptibility of fecal Escherichia coli from healthy dogs and their owners. American Journal of Veterinary Research, 70(9), 1108–1116. 10.2460/ajvr.70.9.1108 PubMed DOI

Umeda, K. , Hase, A. , Matsuo, M. , Horimoto, T. , & Ogasawara, J. (2019). Prevalence and genetic characterization of cephalosporin‐resistant Enterobacteriaceae among dogs and cats in an animal shelter. Journal of Medical Microbiology, 68(3), 339–345. 10.1099/jmm.0.000933 PubMed DOI

Walk, S. T. , Alm, E. W. , Gordon, D. M. , Ram, J. L. , Toranzos, G. A. , Tiedje, J. M. , & Whittam, T. S. (2009). Cryptic lineages of the genus Escherichia . Applied and Environmental Microbiology, 75(20), 6534–6544. 10.1128/AEM.01262-09 PubMed DOI PMC

Wedley, A. L. , Dawson, S. , Maddox, T. W. , Coyne, K. P. , Pinchbeck, G. L. , Clegg, P. , Nuttall, T. , Kirchner, M. , & Williams, N. J. (2017). Carriage of antimicrobial resistant Escherichia coli in dogs: Prevalence, associated risk factors and molecular characteristics. Veterinary Microbiology, 199, 23–30. 10.1016/j.vetmic.2016.11.017 PubMed DOI

Yousfi, M. , Mairi, A. , Touati, A. , Hassissene, L. , Brasme, L. , Guillard, T. , & De Champs, C. (2016). Extended spectrum beta‐lactamase and plasmid mediated quinolone resistance in Escherichia coli fecal isolates from healthy companion animals in Algeria. Journal of Infection and Chemotherapy, 22(7), 431–435. 10.1016/j.jiac.2016.03.005 PubMed DOI

Zankari, E. , Hasman, H. , Cosentino, S. , Vestergaard, M. , Rasmussen, S. , Lund, O. , Aarestrup, F. M. , & Larsen, M. V. (2012). Identification of acquired antimicrobial resistance genes. The Journal of Antimicrobial Chemotherapy, 67(11), 2640–2644. 10.1093/jac/dks261 PubMed DOI PMC

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