Longitudinal Study of Extended-Spectrum-β-Lactamase- and AmpC-Producing Enterobacteriaceae in Household Dogs
Open accessAbstract
A longitudinal study was performed to (i) investigate the continuity of shedding of extended-spectrum-beta-lactamase (ESBL)-producing Enterobacteriaceae in dogs without clinical signs, (ii) identify dominant plasmid-mediated ESBL genes, and (iii) quantify ESBL-producing Enterobacteriaceae in feces. Fecal samples from 38 dogs were collected monthly for 6 months. Additional samples were collected from 7 included dogs on a weekly basis for 6 weeks. Numbers of CFU per gram of feces for non-wild-type Enterobacteriaceae were determined by using MacConkey agar supplemented with 1 mg/liter cefotaxime (MCC), and those for total Enterobacteriaceae were determined by using MacConkey agar. Cefotaxime-resistant isolates were screened by PCR and sequence analysis for the presence of bla CTX-M , bla CMY , bla SHV , bla OXA , and bla TEM gene families. Bacterial species were identified by matrix-assisted laser desorption ionization–time of flight mass spectrometry (MALDI-TOF MS) analysis. PCR-negative isolates were tested by a double-disk synergy test for enhanced AmpC expression. A total of 259 samples were screened, and 126 samples were culture positive on MCC, resulting in 352 isolates, 327 of which were Escherichia coli . Nine dogs were continuously positive during this study, and 6 dogs were continuously negative. Monthly or weekly shifts in fecal shedding were observed for 23 dogs. Genotyping showed a large variety of ESBL genes and gene combinations at single and multiple consecutive sampling moments. The ESBL genes bla CTX-M-1 , bla CTX-M-14 , bla CTX-M-15 , bla SHV-12 , and bla CMY-2 were most frequently found. The mean number of CFU of non-wild-type Enterobacteriaceae was 6.11 × 10 8 CFU/g feces. This study showed an abundance of ESBL-producing Enterobacteriaceae in dogs in the Netherlands, mostly in high concentrations. Fecal shedding was shown to be highly dynamic over time, which is important to consider when studying ESBL epidemiology.
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Two Dutch longitudinal studies reported associations between raw feeding and faecal E. coli from dogs showing ESBL resistance.
“Two Dutch longitudinal studies reported associations between raw feeding and faecal E. coli from dogs showing ESBL resistance (Baede et al. 2015)”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Baede et al. 2015
The ‘Dogs and background information’ section reports that raw-meat feeding was positively associated with ESBL-producing E. coli in dogs (OR 2.08, 95% CI 1.22–3.57). The paper describes this as one Dutch longitudinal study; our copy does not establish that two such studies reported the association. (LLM, conf=0.88)
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“ESBL-producing strains from Enterobacteriaceae were found, which originated from humans and companion animals, leading to the assumption of a possible transmission between humans and companion animals [14].”
Formenti, N., Grassi, A., Parisio, G., Romeo, C., Guarneri, F., Birbes, L., Pitozzi, A., Scali, F., Maisano, A., Boniotti, M., et al. (2021) · Antibiotics · doi:10.3390/antibiotics10101251 · Cited by 12
Ugwu, I. C., Anyanwu, M. U., Ugwu, C., & Ugwuanyi, O. W. (2015) · doi:10.15835/nsb739616 · Cited by 11
“The variation in isolation prevalence of ESBL-resistant enterobacteria genera reported in these studies, may be related to the differences in sample size, type of sample processed (whether clinical or non-clinical), rate of contamination of dog’s food/drinking water or environment by ESBL-resistant enterobacteria and…”
BackgroundResultSharif, N., Sreedevi, B., Chaitanya, R., & Sreenivasulu, D. (2017) · Veterinary World · doi:10.14202/vetworld.2017.950-954 · Cited by 10
Use of Antibiotics in Animal Agriculture: Implications for Pediatrics: Technical Report.
Katz, S., & Banerjee, R. (2024) · Pediatrics · doi:10.1542/peds.2024-068467 · Cited by 9 · see citing works
Shnaiderman-Torban, A., Navon-Venezia, S., Baron, H., Ahmad, W. A., Arielly, H., Valenci, G. Z., Nissan, I., Paitan, Y., & Steinman, A. (2022) · Antibiotics · doi:10.3390/antibiotics11081069 · Cited by 8 · see citing works
“coli, as was reported previously in canine fecal samples [14,21,26].”
BackgroundMethodBarrios-Villa, E., Cortés-Cortés, G., Lozano-Zaraín, P., Romero-Romero, S., Flores, N. L., Estepa, V., Somalo, S., Torres, C., & Rocha-Gracia, R. D. C. (2018) · British Food Journal · doi:10.1108/bfj-02-2018-0104 · Cited by 6
Ochoa, A., García, M. I., Cienfuegos, A. V., & Vásquez-Jaramillo, L. (2022) · Revista de la Facultad de Medicina Veterinaria y de Zootecnia · doi:10.15446/rfmvz.v69n3.103805 · Cited by 4
“…that CTX-M-1 is the most frequent genotype, not only in companion animals, but also in foodproducing animals, food, wild animals, and veterinarians that work with dogs and cats (Abbas et al. 2019; Baede et al. 2015; Cormier et al. 2019; Darwich et al. 2019; Ewers et al., 2012; Irrgang et al. 2018).”
BackgroundEskola, K., Aimo‐Koivisto, E. M., Heikinheimo, A., Mykkänen, A. K., Hautajärvi, T., & Grönthal, T. S. C. (2024) · BMC Veterinary Research · doi:10.1186/s12917-024-04260-z · Cited by 5 · see citing works
“However, it is noteworthy that the excretion of ESBL-E in dogs is highly dynamic, which is a complicating finding from epidemiological and infection control perspectives, as it makes an animal’s ESBL-E status less predictable [19].”
BackgroundYeleussizova, A., Aleshina, Y., Mendybayeva, A., Khassanova, M., & Rychshanova, R. (2023) · American Journal of Animal and Veterinary Sciences · doi:10.3844/ajavsp.2023.190.198 · Cited by 3
“These data correlate with the results of several studies conducted in the Netherlands, where the prevalence of colonization by enterobacteria in dogs and cats (including healthy and sick animals) ranged from 3.1-55% (Baede et al., 2015; Van den Bunt et al., 2020).”
ResultInfluentialFalodun, O. I., Afolabi, M. C., & Rabiu, A. G. (2022) · Animal Gene · doi:10.1016/j.angen.2022.200133 · Cited by 4 · see citing works
Cepas de Escherichia coli productoras de BetaLactamasas de Espectro Extendido en heces de caninos
Rodríguez-Duran, N. A., Sánchez-Prado, R. E., Pérez–Rodríguez, J. E., Lascano-Domínguez, B. J., Luna-Florin, J. A., Guerrero–López, A., Guzmán–Pucha, S., & Sánchez–Prado, R. (2024) · Revista Científica de la Facultad de Ciencias Veterinarias · doi:10.52973/rcfcv-e34490 · Cited by 2
McDonnell, S., Gutiérrez, M., Leonard, F. C., O’Brien, T., Kearney, P., Swan, C., Madigan, G., Bracken, E., McLernon, J., Griffin, M., et al. (2022) · Irish Veterinary Journal · doi:10.1186/s13620-022-00219-4 · Cited by 4 · see citing works
“(2015) [47], suggested a correlation between feeding dogs a raw diet that contains ESBL-producers and the presence of these E.”
BackgroundCozma, A., Măciucă, E. I., Carp-Cărare, C., Carp-Cărare, M., Rîmbu, C., Aniță, A., Aniță, D., & Timofte, D. (2019) · Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca: Veterinary Medicine · doi:10.15835/buasvmcn-vm:2019.0003 · Cited by 2
“The change of faecal microbiota in dogs, with increased resistance and carriage of ESBL producing E. coli isolates is more prevalent with most dogs being intermittently shedders and positive carriers for various ESBL genes (Baede et al., 2015).”
BackgroundFordham, S., Sheridan, E., & Drobniewski, F. (2026) · bioRxiv · doi:10.1155/tbed/5383720 · Cited by 1 · see citing works
“The distinctiveness of the focal lineage was further supported by comparison with ST147 genomes outside this sublineage: Distances from the animal isolates within the cat-dominated sublineage to external ST147 comparators were substantially larger, ranging from 93 to 298 SNPs, with a median of 130…”
Antibiotic resistant Escherichia coli strains in healthy pets from Tamaulipas, Mexico.
Mandujano-Hernández, J. A., Vázquez-Villanueva, J., de Luna-Santillana, E. D. J., Rivera, G., Bocanegra-García, V., & Martínez-Vázquez, A. V. (2024) · Acta Microbiologica et Immunologica Hungarica · doi:10.1556/030.2024.02340
Lindinger, S., Flekna, G., Iben, C., Handl, S., & Paulsen, P. (2024) · Veterinary Medicine Austria · doi:10.5680/wtm000029
Aleshina, Y., Mendybayeva, A., Alieva, G., Zhabykpaeva, A., Rychshanova, R., & Yeleussizova, A. (2023) · Veterinary Sciences · doi:10.51452/kazatuvc.2023.2(002).1412
Sealey, J., Hammond, A., Mounsey, O., Gould, V., Reyher, K., & Avison, M. (2022) · bioRxiv · doi:10.1101/2022.04.23.489260
- Authors
- Baede, V. O., Wagenaar, J. A., Broens, E. M., Duim, B., Dohmen, W., Nijsse, R., Timmerman, A. J., & Hordijk, J.
- Affiliations
- Utrecht University (NL)
- Venue
- Antimicrobial Agents and Chemotherapy
- Publisher
- American Society for Microbiology
- Published
- 2015-06
- Volume
- 59
- Issue
- 6
- Pages
- 3117-3124
- ISSN
- 0066-4804 (ISSN-L)
- 1098-6596
- PMC
- PMC4432141
- OpenAlex
- W1759586988
- Cited by
- 66
- References
- 0
- Citations by year
- 2026: 1 · 2024: 7 · 2023: 3 · 2022: 15 · 2021: 12 · 2020: 3 · 2019: 8 · 2018: 9 · 2017: 4 · 2016: 2 · 2015: 2
- FWCI
- 2.36
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Antimicrobial Agents and Chemotherapy (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Socio-Environmental Systems Modeling (acceptedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
- Life Sciences › Agricultural and Biological Sciences › Food Science › Salmonella and Campylobacter epidemiology
- Life Sciences › Immunology and Microbiology › Applied Microbiology and Biotechnology › Antibiotic Use and Resistance
- Keywords
- extended-spectrum beta-lactamase, AmpC beta-lactamase, Enterobacteriaceae, dogs, fecal shedding, Escherichia coli, blaCTX-M, blaSHV, blaCMY, blaOXA, blaTEM, plasmid-mediated antibiotic resistance, zoonotic transmission, antimicrobial resistance epidemiology
- MeSH terms
- Animals, Bacterial Proteins, beta-Lactamases, Dogs, Enterobacteriaceae, Enterobacteriaceae Infections, Genotype, Longitudinal Studies, Microbial Sensitivity Tests
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