Rural Raccoons (Procyon lotor) Not Likely to Be a Major Driver of Antimicrobial Resistant Human Salmonella Cases in Southern Ontario, Canada: A One Health Epidemiological Assessment Using Whole-Genome Sequence Data

Nadine A Vogt; Benjamin M Hetman; Adam A Vogt; David L Pearl; Richard J Reid-Smith; E Jane Parmley; Stefanie Kadykalo; Nicol Janecko; Amrita Bharat; Michael R Mulvey; Kim Ziebell; James Robertson; John Nash; Vanessa Allen; Anna Majury; Nicole Ricker; Kristin J Bondo; Samantha E Allen; Claire M Jardine

doi:10.3389/fvets.2022.840416

Rural Raccoons (Procyon lotor) Not Likely to Be a Major Driver of Antimicrobial Resistant Human Salmonella Cases in Southern Ontario, Canada: A One Health Epidemiological Assessment Using Whole-Genome Sequence Data

Front Vet Sci. 2022 Feb 25:9:840416. doi: 10.3389/fvets.2022.840416. eCollection 2022.

Authors

Nadine A Vogt¹, Benjamin M Hetman¹, Adam A Vogt², David L Pearl¹, Richard J Reid-Smith^{1

3}, E Jane Parmley^{1

3}, Stefanie Kadykalo³, Nicol Janecko⁴, Amrita Bharat^{5

6}, Michael R Mulvey^{5

6}, Kim Ziebell⁷, James Robertson⁷, John Nash⁷, Vanessa Allen⁸, Anna Majury^{9

10}, Nicole Ricker¹¹, Kristin J Bondo¹¹, Samantha E Allen^{12

13}, Claire M Jardine^{11

14}

Affiliations

¹ Department of Population Medicine, Ontario Veterinary College, Guelph, ON, Canada.
² Independent Researcher, Mississauga, ON, Canada.
³ Centre for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, ON, Canada.
⁴ Quadram Institute Bioscience, Norwich, United Kingdom.
⁵ National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, MB, Canada.
⁶ Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, MB, Canada.
⁷ National Microbiology Laboratory, Public Health Agency of Canada, Guelph, ON, Canada.
⁸ Public Health Ontario, Toronto, ON, Canada.
⁹ Public Health Ontario, Kingston, ON, Canada.
¹⁰ Department of Biomedical and Molecular Science, Queen's University, Kingston, ON, Canada.
¹¹ Department of Pathobiology, Ontario Veterinary College, Guelph, ON, Canada.
¹² Wyoming Game and Fish Department, Laramie, WY, United States.
¹³ Department of Veterinary Sciences, University of Wyoming, Laramie, WY, United States.
¹⁴ Canadian Wildlife Health Cooperative, Ontario Veterinary College, Guelph, ON, Canada.

Abstract

Non-typhoidal Salmonella infections represent a substantial burden of illness in humans, and the increasing prevalence of antimicrobial resistance among these infections is a growing concern. Using a combination of Salmonella isolate short-read whole-genome sequence data from select human cases, raccoons, livestock and environmental sources, and an epidemiological framework, our objective was to determine if there was evidence for potential transmission of Salmonella and associated antimicrobial resistance determinants between these different sources in the Grand River watershed in Ontario, Canada. Logistic regression models were used to assess the potential associations between source type and the presence of select resistance genes and plasmid incompatibility types. A total of 608 isolates were obtained from the following sources: humans (n = 58), raccoons (n = 92), livestock (n = 329), and environmental samples (n = 129). Resistance genes of public health importance, including bla _CMY-2, were identified in humans, livestock, and environmental sources, but not in raccoons. Most resistance genes analyzed were significantly more likely to be identified in livestock and/or human isolates than in raccoon isolates. Based on a 3,002-loci core genome multi-locus sequence typing (cgMLST) scheme, human Salmonella isolates were often more similar to isolates from livestock and environmental sources, than with those from raccoons. Rare instances of serovars S. Heidelberg and S. Enteritidis in raccoons likely represent incidental infections and highlight possible acquisition and dissemination of predominantly poultry-associated Salmonella by raccoons within these ecosystems. Raccoon-predominant serovars were either not identified among human isolates (S. Agona, S. Thompson) or differed by more than 350 cgMLST loci (S. Newport). Collectively, our findings suggest that the rural population of raccoons on swine farms in the Grand River watershed are unlikely to be major contributors to antimicrobial resistant human Salmonella cases in this region.

Keywords: Procyon lotor; Salmonella; antimicrobial resistance; foodborne illness; raccoon; whole-genome sequencing; wildlife.