Risk factors for carriage of antimicrobial-resistant Salmonella spp and Escherichia coli in pet dogs from volunteer households in Ontario, Canada, in 2005 and 2006
Abstract
OBJECTIVE To determine pet-related management factors associated with the carriage of antimicrobial-resistant Salmonella spp and Escherichia coli in a population of pet dogs. SAMPLE 138 dogs from 84 households in Ontario, Canada. PROCEDURES From October 2005 through May 2006, dogs and households in Ontario, Canada, were recruited to participate in a cross-sectional study. Fecal samples were submitted for culture of Salmonella spp and E coli, which provided 515 bacterial isolates for antimicrobial susceptibility testing. Multilevel logistic regression models with random effects for household and dog were created to identify pet-related management factors associated with antimicrobial resistance. RESULTS Bacterial species, feeding a homemade diet or adding homemade food to the diet, feeding a raw diet or adding anything raw to the diet, feeding a homemade raw food diet, and feeding raw chicken in the past week were significant risk factors for antimicrobial resistance in this population of dogs. CONCLUSIONS AND CLINICAL RELEVANCE In this study, several potentially important pet-related risk factors for the carriage of antimicrobial-resistant Salmonella spp and E coli in pet dogs were identified. Further evaluation of risk factors for antimicrobial resistance in dogs may lead to development of evidence-based guidelines for safe and responsible dog ownership and management to protect the public, especially pet owners who are immunocompromised.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
This is similar for resistant Salmonella.
“This is similar for resistant Salmonella (Leonard et al. 2015)”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Leonard et al. 2015
Raw feeding has also been identified as a risk factor for faecal shedding by dogs of E. coli exhibiting other antimicrobial drug resistances.
“In addition to ESBL/AmpC resistance studies, raw feeding has also been identified as a risk factor for faecal shedding by dogs of E. coli exhibiting other antimicrobial drug resistances (Leonard et al. 2015, Groat et al. 2016).”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Leonard et al. 2015
Cites
Veterinary Epidemiologic Research
Dohoo, I. R., Martin, S. W., & Stryhn, H. (2009) · Medical Entomology and Zoology · Cited by 2,912 · see citing works
Goulias, K. G. (2002) · New directions in civil engineering · doi:10.1201/9781420042283.ch9 · Cited by 1,285 · see citing works
Saville, W. J. A., & Wittum, T. E. (2004) · Elsevier eBooks · doi:10.1016/b0-72-169777-1/50023-8 · Cited by 865 · see citing works
Pet animals as reservoirs of antimicrobial-resistant bacteria: Review
Guardabassi, L. (2004) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkh332 · Cited by 718 · see citing works
Zoonoses and communicable diseases common to man and animals
Pedro, N. H. O., & Szyfres, B. (1980) · Medical Entomology and Zoology · Cited by 583 · see citing works
Zoonoses and Communicable Diseases Common to Man and Animals
Frenkel, J. K. (1980) · Military Medicine · doi:10.1093/milmed/145.12.852 · Cited by 427 · see citing works
Veterinary Epidemiology, 3rd ed.
Pearl, D. L. (2006) · Europe PMC (PubMed Central) · Cited by 295 · see citing works
Self-citationAntimicrobial therapy in veterinary medicine
Walton, J. R. (1989) · British Veterinary Journal · doi:10.1016/0007-1935(89)90107-3 · Cited by 204 · see citing works
Reservoirs of Antimicrobial Resistance in Pet Animals
Lloyd, D. H. (2007) · Clinical Infectious Diseases · doi:10.1086/519254 · Cited by 180 · see citing works
Caprioli, A. (2000) · International Journal of Antimicrobial Agents · doi:10.1016/s0924-8579(00)00140-0 · Cited by 168 · see citing works
Lefebvre, S. L., Reid‐Smith, R., Boerlin, P., & Weese, J. S. (2008) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2008.01145.x · Cited by 155 · see citing works
Self-citationSharing of Virulent Escherichia coli Clones among Household Members of a Woman with Acute Cystitis
Johnson, J. R., & Clabots, C. (2006) · Clinical Infectious Diseases · doi:10.1086/508541 · Cited by 137 · see citing works
Strohmeyer, R. A., Morley, P. S., Hyatt, D. R., Dargatz, D. A., Scorza, A. V., & Lappin, M. R. (2006) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.228.4.537 · Cited by 133 · see citing works
Stull, J. W., Peregrine, A. S., Sargeant, J. M., & Weese, J. S. (2012) · BMC Public Health · doi:10.1186/1471-2458-12-553 · Cited by 118 · see citing works
Self-citationAntimicrobial use in food and companion animals
Prescott, J. F. (2008) · Animal Health Research Reviews · doi:10.1017/s1466252308001473 · Cited by 118 · see citing works
The Business Of Urban Animals Survey: the facts and statistics on companion animals in Canada.
(2009) · Europe PMC (PubMed Central) · Cited by 116 · see citing works
Multilevel Analysis of Infectious Diseases
Roux, A. V. D., & Aiello, A. E. (2005) · The Journal of Infectious Diseases · doi:10.1086/425288 · Cited by 114 · see citing works
Surveillance of Zoonotic Infectious Disease Transmitted by Small Companion Animals
Day, M. J., Breitschwerdt, E. B., Cleaveland, S., Karkare, U., Khanna, C., Kirpensteijn, J., Kuiken, T., Lappin, M. R., McQuiston, J. H., MUMFORD, E. L., et al. (2012) · Emerging infectious diseases · doi:10.3201/eid1812.120664 · Cited by 106 · see citing works
Jackson, C. R., Fedorka–Cray, P. J., Davis, J. A., Barrett, J. B., & Frye, J. G. (2009) · Journal of Applied Microbiology · doi:10.1111/j.1365-2672.2009.04310.x · Cited by 103 · see citing works
Leonard, E. K., Pearl, D. L., Finley, R. L., Janecko, N., Peregrine, A. S., Reid‐Smith, R. J., & Weese, J. S. (2011) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2009.01320.x · Cited by 95 · see citing works
Self-citationChanges in fecal microbiota of healthy dogs administered amoxicillin
Grønvold, A.-M. R., L'Abée-Lund, T. M., ̧rum, H. S., Skancke, E. M., Yannarell, A. C., & Mackie, R. I. (2009) · FEMS Microbiology Ecology · doi:10.1111/j.1574-6941.2009.00808.x · Cited by 93 · see citing works
Murphy, C. P., Reid‐Smith, R. J., Prescott, J. F., Bonnett, B. N., Poppe, C., Boerlin, P., Weese, J. S., Janecko, N., & McEwen, S. A. (2009) · PubMed Central · Cited by 91 · see citing works
Self-citationAntimicrobial resistance in companion animals
Weese, J. S. (2008) · Animal Health Research Reviews · doi:10.1017/s1466252308001485 · Cited by 87 · see citing works
Self-citationFinley, R., Reid‐Smith, R., Ribble, C., Popa, M., Vandermeer, M., & Aramini, J. (2008) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2008.01147.x · Cited by 85 · see citing works
Self-citationDamborg, P., Sørensen, A., & Guardabassi, L. (2008) · Veterinary Microbiology · doi:10.1016/j.vetmic.2008.04.026 · Cited by 81 · see citing works
SalmonellaTyphimurium Outbreak Associated with Veterinary Clinic
Cherry, B., Burns, A., Johnson, G. S., Pfeiffer, H., Dumas, N. B., Barrett, D., McDonough, P. L., & Eidson, M. (2004) · Emerging infectious diseases · doi:10.3201/eid1012.040714 · Cited by 74 · see citing works
Shaheen, B. W., Boothe, D. M., Oyarzábal, O. A., & Smaha, T. (2010) · Journal of Veterinary Internal Medicine · doi:10.1111/j.1939-1676.2009.0468.x · Cited by 67 · see citing works
runmlwin: Stata module for fitting multilevel models in the MLwiN software package
Leckie, G., & Charlton, C. (2011) · Bristol Research (University of Bristol) · Cited by 66 · see citing works
Campylobacter upsaliensis enteritis associated with canine infections
Goossens, H., Vlaes, L., Butzler, J., Adnet, A., Hanicq, P., N'Jufom, S., Massart, D., de Schrijver, G., & Blomme, W. (1991) · The Lancet · doi:10.1016/0140-6736(91)93182-9 · Cited by 66 · see citing works
Ogeer-Gyles, J., Mathews, K. A., Sears, W., Prescott, J. F., Weese, J. S., & Boerlin, P. (2006) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.229.5.694 · Cited by 61 · see citing works
Self-citationRantala, M. H. J., Lahti, E. T., Kuhalampi, J., Pesonen, S., Järvinen, A.-K., Saijonmaa‐Koulumies, L. E., & Honkanen‐Buzalski, T. (2004) · Acta veterinaria Scandinavica · doi:10.1186/1751-0147-45-37 · Cited by 56 · see citing works
Leonard, E. K., Pearl, D. L., Finley, R. L., Janecko, N., Reid‐Smith, R. J., Peregrine, A. S., & Weese, J. S. (2011) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dkr430 · Cited by 48 · see citing works
Self-citationAntimicrobial Resistance and Its Epidemiology
Boerlin, P., & White, D. G. (2013) · doi:10.1002/9781118675014.ch3 · Cited by 47 · see citing works
Gibson, J. S., Cobbold, R. N., Kyaw-Tanner, M. T., Heisig, P., & Trott, D. J. (2010) · Veterinary Microbiology · doi:10.1016/j.vetmic.2010.04.012 · Cited by 42 · see citing works
Varga, C., Rajić, A., McFall, M. E., Reid‐Smith, R. J., Deckert, A., Pearl, D. L., Avery, B. P., Checkley, S., & McEwen, S. A. (2008) · PubMed Central · Cited by 37 · see citing works
Self-citationMartel, J. L., Tardy, F., Sandérs, P., & Boisseau, J. (2001) · Veterinary Research · doi:10.1051/vetres:2001131 · Cited by 34 · see citing works
Gibson, J. S., Morton, J. M., Cobbold, R. N., Filippich, L. J., & Trott, D. J. (2010) · Epidemiology and Infection · doi:10.1017/s0950268810000798 · Cited by 29 · see citing works
Finley, R. L., Reid‐Smith, R. J., Ribble, C. S., Popa, M., Vandermeer, M., & Aramini, J. (2008) · Zoonoses and Public Health · doi:10.1111/j.1863-2378.2008.01144.x · Cited by 26 · see citing works
Self-citationAcke, E., McGill, K., Quinn, T., Jones, B. R., Fanning, S., & Whyte, P. (2009) · Foodborne Pathogens and Disease · doi:10.1089/fpd.2008.0225 · Cited by 17 · see citing works
Mentula, S., Virtanen, T., Kanervo-Nordström, A., Harmoinen, J., Westermarck, E., Rautio, M., Huovinen, P., & Könönen, E. (2005) · International Journal of Antimicrobial Agents · doi:10.1016/j.ijantimicag.2005.09.012 · Cited by 11 · see citing works
Dog Bite Transmission of Antibiotic-Resistant Bacteria to a Human
Johnson, J. K., Perencevich, E. N., Lincalis, D. P., & Venezia, R. A. (2006) · Infection Control and Hospital Epidemiology · doi:10.1086/505101 · Cited by 7 · see citing works
Flagged first, then by citations
1 of the 42 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Raw diets for dogs and cats: a review, with particular reference to microbiological hazards.
Davies, R. H., Lawes, J. R., & Wales, A. D. (2019) · Journal of Small Animal Practice · doi:10.1111/jsap.13000 · Cited by 195 · see citing works
Davies, R., & Wales, A. (2019) · Comprehensive Reviews in Food Science and Food Safety · doi:10.1111/1541-4337.12438 · Cited by 147 · see citing works
Reimschuessel, R., Grabenstein, M., Guag, J., Nemser, S. M., Song, K., Qiu, J., Clothier, K. A., Byrne, B. A., Marks, S. L., Cadmus, K., et al. (2017) · Journal of Clinical Microbiology · doi:10.1128/jcm.02137-16 · Cited by 105 · see citing works
An observational study of pet feeding practices and how these have changed between 2008 and 2018
Dodd, S. A. S., Cave, N., Abood, S. K., Shoveller, A., Adolphe, J. L., & Verbrugghe, A. (2020) · Veterinary Record · doi:10.1136/vr.105828 · Cited by 101 · see citing works
Raw Meat-Based Diets in Dogs and Cats
Fredriksson‐Ahomaa, M., Heikkilä, T., Pernu, N., Kovanen, S., Hielm-Björkman, A. K., & Kivistö, R. I. (2017) · Veterinary Sciences · doi:10.3390/vetsci4030033 · Cited by 71 · see citing works
Viegas, F. M., Ramos, C. P., Xavier, R., Lopes, E. O., Oliveira, C., Bagno, R. M., Diniz, A. N., Lobato, F., & Silva, R. O. S. (2020) · PLoS ONE · doi:10.1371/journal.pone.0231275 · Cited by 56 · see citing works
Presence of pathogenic bacteria in faeces from dogs fed raw meat‐based diets or dry kibble
Runesvärd, E., Wikström, C., Fernström, L., & Hansson, I. (2020) · Veterinary Record · doi:10.1136/vr.105644 · Cited by 52 · see citing works
Morgan, G., Williams, N. J., Schmidt, V. M., Cookson, D., Symington, C., & Pinchbeck, G. L. (2022) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2022.105741 · Cited by 40 · see citing works
“…(including extended spectrum beta lactamase (ESBL) producing-E. coli ) in RMD foods, and in the bacteria shed within faeces of dogs fed these diets (Bacci et al., 2019; Groat et al., 2022; Leonard et al., 2015; Nilsson, 2015; Schmidt et al., 2015; van Bree et al., 2018; Wedley et al., 2017).”
Dodd, S. A. S., Adolphe, J. L., & Verbrugghe, A. (2018) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.253.11.1425 · Cited by 33 · see citing works
Shnaiderman‐Torban, A., Steinman, A., Meidan, G., Paitan, Y., Ahmad, W. A., & Navon‐Venezia, S. (2019) · Frontiers in Microbiology · doi:10.3389/fmicb.2019.02488 · Cited by 33 · see citing works
Amadi, V., Hariharan, H., Arya, G., Matthew‐Belmar, V., Nicholas‐Thomas, R., Pinckney, R., Sharma, R., & Johnson, R. P. (2017) · Veterinary Medicine and Science · doi:10.1002/vms3.84 · Cited by 15 · see citing works
Worsley‐Tonks, K. E. L., Miller, E. A., Gehrt, S. D., McKenzie, S. C., Travis, D. A., Johnson, T. J., & Craft, M. E. (2020) · Zoonoses and Public Health · doi:10.1111/zph.12691 · Cited by 14 · see citing works
Beining, M. W., Hartmann, M., Luebke-Becker, A., Guenther, S., Schaufler, K., Hille, K., & Kreienbrock, L. (2023) · Animals · doi:10.3390/ani13040584 · Cited by 12 · see citing works
Morgan, G., Pinchbeck, G. L., Haldenby, S. T., Schmidt, V., & Williams, N. J. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1460143 · Cited by 16 · see citing works
Isolation of Salmonella species of public health concern from commonly fed dried meat dog treats.
Morgan, G., Saal, M., Corr, A., Jenkins, C., Chattaway, M., Pinchbeck, G., & Williams, N. (2023) · The Veterinary Record · doi:10.1002/vetr.2642 · Cited by 14 · see citing works
Risk factors for antimicrobial-resistant Enterobacterales in dogs: a systematic review
Karalliu, E., Chung, K. Y., MacKinnon, B., Haile, B., Bęczkowski, P. M., Barrs, V. R., Elsohaby, I., & Nekouei, O. (2024) · Frontiers in Veterinary Science · doi:10.3389/fvets.2024.1447707 · Cited by 11 · see citing works
Current Evidence on Raw Meat Diets in Pets: A Natural Symbol, but a Nutritional Controversy
Lyu, Y., Wu, C., Li, L., & Pu, J. (2025) · Animals · doi:10.3390/ani15030293 · Cited by 15 · 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
Wales, A. D., Lawes, J. R., & Davies, R. (2019) · BSAVA Companion · doi:10.22233/20412495.0819.10 · Cited by 4 · see citing works
Beining, M. W., Guenther, S., Lübke‐Becker, A., Heiden, S. E., Schaufler, K., Kreienbrock, L., & Schwabe, M. (2025) · Microbiology Spectrum · doi:10.1128/spectrum.00087-25 · Cited by 3 · see citing works
“We previously described an association between feeding (raw meat and commercial food) and carriage of ESBL-producing E. coli , and Leonard et al. (38) reported that raw diet and feeding raw products are other risk factors for colonization with ESBL-producing E. coli (38).”
Wynn, S. G. (2025) · Veterinary Clinics of North America Small Animal Practice · doi:10.1016/j.cvsm.2025.06.004 · Cited by 1 · see citing works
Canine Cystitis Caused by Salmonella enterica subsp. enterica
de Oliveira, R. P., da Silva, D. M. S., Ferreira, M. D. N. S., Moura, C. M. C., Dias, R. F. F., da Silva, M. G. V., Pinheiro, J. W., & Mota, R. A. (2019) · ACTA SCIENTIAE VETERINARIAE · doi:10.22456/1679-9216.90075 · Cited by 1 · see citing works
Flavour of the month: foods as diagnosis and/or treatment
Roudebush, P., & de Souza, C. P. (2017) · Wiley eBooks · doi:10.1002/9781119278368.ch7.11
Dodd, S. A. S. (2018) · The Atrium (University of Guelph)
Septicaemia and thrombocytopenia caused by Salmonella gallinarum in a dog fed a raw meat-based diet
Albuquerque, C. S., Tørnqvist‐Johnsen, C., Breheny, C. R., & Llewellyn, E. A. (2021) · Companion animal · doi:10.12968/coan.2020.0080
Nugroho, W. S., Karmo, A. D., Silalahi, G. E., & Gallantiswara, P. C. D. (2024) · Veterinary World · doi:10.14202/vetworld.2024.2347-2354
“…resistance to a variety of antimicrobial agents, including species with a potential for zoonotic diseases and resistance phenotypes of clinical interest, such as methicillin-resistant Staphylococcus aureus , vancomycin-resistant enterococci, and multi-drug-resistant Salmonella Typhimurium [7, 8].”
Background
- Authors
- Leonard, E. K., Pearl, D. L., Janecko, N., Finley, R. L., Reid-Smith, R. J., Weese, J. S., & Peregrine, A. S.
- Venue
- American Journal of Veterinary Research
- Published
- 2015-11
- Volume
- 76
- Issue
- 11
- Pages
- 959-968
- ISSN
- 0002-9645 (ISSN-L)
- OpenAlex
- W1921427430
- Cited by
- 26
- References
- 42
- Citations by year
- 2025: 3 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 1 · 2020: 4 · 2019: 5 · 2018: 2 · 2017: 4
- FWCI
- 2.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Veterinary Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Public Health Agency of Canada
- Topics
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
- Keywords
- antimicrobial resistance, Salmonella, Escherichia coli, pet dogs, risk factors, raw food diet, homemade dog food, raw chicken meat, zoonotic transmission, responsible dog ownership, Ontario
- MeSH terms
- Animals, Animal Feed, Anti-Infective Agents, Anti-Bacterial Agents, Carrier State, Cross-Sectional Studies, Diet, Dogs, Escherichia coli, Escherichia coli Infections, Feces, Female, Male, Microbial Sensitivity Tests, Ontario, Risk Factors, Salmonella, Salmonella Infections, Animal, Models, Statistical, Multivariate Analysis, Drug Resistance, Bacterial
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
