Salmonella has been detected in the feces of many wildlife species, including raccoons (Procyon lotor), but little is known about the epidemiology of Salmonella in wildlife living in different habitat types. Our objective was to investigate demographic, temporal, and climatic factors associated with the carriage of Salmonella in raccoons and their environment on swine farms and conservation areas. Using a repeated cross-sectional study design, we collected fecal samples from raccoons and environmental samples (soil, manure pits, dumpsters) on 5 swine farms and 5 conservation areas in Ontario, Canada once every five weeks from May to November, 2011-2013. Salmonella was detected in 26% (279/1093; 95% CI 22.9-28.2) of raccoon fecal samples, 6% (88/1609; 95% CI 4.5-6.8) of soil samples, 30% (21/69; 95% CI 20.0-42.7) of manure pit samples, and 23% (7/31; 95% CI 9.6-41.0) of dumpster samples. Of samples testing positive for Salmonella, antimicrobial resistance was detected in 5% (14/279; 95% CI 2.8-8.3) of raccoon fecal, 8% (7/89; 95% CI 3.2-15.5) of soil, 10% (2/21; 95% CI 1.2-30.4) of manure pit, and 0/7 dumpster samples. Using multi-level multivariable logistic regression analyses, we found location type (swine farm or conservation area) was not a significant explanatory variable for Salmonella occurrence in raccoon feces or soil (p > 0.05). However, detection of Salmonella in raccoon feces was associated with rainfall, season, and sex with various interaction effects among these variables. We detected a variety of Salmonella serovars that infect humans and livestock in the feces of raccoons indicating that raccoons living near humans, regardless of location type, may play a role in the epidemiology of salmonellosis in livestock and humans in southwestern Ontario.

Canadian Wildlife Health Cooperative Department of Pathobiology University of Guelph Guelph Ontario Canada

Centre for Foodborne Environmental and Zoonotic Infectious Diseases Public Health Agency of Canada Guelph Ontario Canada

Department of Biology and Wildlife Diseases University of Veterinary and Pharmaceutical Sciences Brno Brno Czech Republic

Department of Pathobiology University of Guelph Guelph Ontario Canada

Department of Population Medicine University of Guelph Guelph Ontario Canada

See more in PubMed

Forshell LP, Wierup M. Salmonella contamination: a significant challenge to the global marketing of animal food products. Rev Sci Tech. 2006; 25: 541–554. PubMed

Thomas MK, Murray R, Flockhart L, Pintar K, Pollari F, Fazil A, et al. Estimates of the burden of foodborne illness in Canada for 30 specified pathogens and unspecified agents, circa 2006. Foodborne Pathog and Dis. 2013; 10: 639–648. PubMed PMC

Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, et al. Food-related illness and death in the United States. Emerg Infect Dis. 1999; 5: 607–625. PubMed PMC

Chen H, Wang Y, Su L, Chiu C. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatr Neonatol. 2013; 54: 147–152. 10.1016/j.pedneo.2013.01.010 PubMed DOI

Varma JK, Greene KD, Ovitt J, Barrett TJ, Medalla F, Angulo FJ. 2005. Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984–2002. Emerg Infect Dis. 2005; 11: 943–946. PubMed PMC

Su L, Wu T, Chia J, Chu C, Kuo A, Chiu C. Increasing ceftriaxone resistance in Salmonella isolates from a university hospital in Taiwan. J Antimicrob Chemother. 2005; 55: 846–852. PubMed

Barza M, Travers K. 2002. Excess infections due to antimicrobial resistance: the “Attributable Fraction”. 2002; Clin Infect Dis. 34: S126–S130. PubMed

Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol. 2010; 12: 2385–2397. 10.1111/j.1462-2920.2010.02297.x PubMed DOI

Gómez-Aldapa CA, Torres-Vitela M del R, Virarruel-López A, Castra-Rosas J. The role of foods in Salmonella infections In: Mahmoud BSM, editors. Salmonella–a dangerous foodborne pathogen. InTech; 2012. pp. 21–46. Available at: http://www.intechopen.com/books/salmonella-a-dangerous-foodborne-pathogen.

Saeed AM, Gast RK, Potter ME, Wall PG. Salmonella enterica serovar Enteritidis in humans and animals: Epidemiology, pathogenesis, and control. Ames: Iowa State University Press; 1999.

Smith K, Bender J, Osterholm M. Antimicrobial resistance in animals and relevance to human infections In: Nachamkin I, Blaser M., editors. Campylobacter. 2nd Ed., Washington D.C.: ASM Press; 2000. pp. 483–496.

Teale C J. Antimicrobial resistance and the food chain. J Appl Microbiol. 2002; 92(s1): 85S–89S. PubMed

Schiellerup P, Abdul-Redha RJ, Baggesen DL, Anderson SL, Sandvang D. Five cases of gastroenteritis with multiresistant Salmonella enterica serovar Typhimurium DT104 related to farm animals in Denmark. Ugeskr Laeger. 2001; 163: 5677–5678. PubMed

Newell D, Davison H. Campylobacter: Control and Prevention In: Torrence M, Isaacson R, editors. Microbial food safety in animal agriculture: Current topics. Ames: Iowa State Press; 2003. pp. 211–232.

Hilbert F, Smulders FJM, Chopra-Dewasthaly R, Paulsen P. Salmonella in the wildlife-human interface. Food Res Int. 2012; 45: 603–608.

Davies RH, Wray C. Seasonal variations in the isolation of Salmonella Typhimurium, Salmonella Enteritidis, Bacillus cereus and Clostridium perfringens from environmental samples. J Vet Med B Infect Dis Vet Public Health. 1996; 43: 119–127. PubMed

Ziemer CJ, Bonner JM, Cole D, Vinjé J, Constantini V, Goyal S, et al. Fate and transport of zoonotic, bacterial, viral, and parasitic pathogens during swine manure treatment, storage, and land application. J Anim Sc. 2010; 88(s13): E84–94. PubMed

Winfield MD, Groisman EA. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol. 2003; 69: 3687–3694. PubMed PMC

Reilly WJ, Forbes GI, Paterson GM, Sharp JC. Human and animal salmonellosis in Scotland associated with environmental contamination, 1973–79. Vet Rec. 1981; 108: 553–555. PubMed

Kinde H, Adelson M, Ardans A, Little EH, Willoughby D, Berchtold D. Prevalence of Salmonella in municipal sewage treatment plant effluents in southern California. Avian Dis. 1997; 41: 392–398. PubMed

Thomas JL, Slawson RM, Taylor WD. Salmonella serotype diversity and seasonality in urban and rural streams. J Appl Microbiol. 2013; 114: 907–922. 10.1111/jam.12079 PubMed DOI

Haley BJ, Cole DJ, Lipp EK. Distribution, diversity, and seasonality of waterborne Salmonellae in a rural watershed. Appl Environ Microbiol. 2009; 75: 1248–1255. 10.1128/AEM.01648-08 PubMed DOI PMC

Thomason BM, Biddle JW, Cherry WB. Detection of Salmonellae in the environment. Appl Microbiol. 1975; 30: 764–767. PubMed PMC

Andrés S, Vico JP, Garrido V, Grilló MJ, Samper S, Gavín P, et al. Epidemiology of subclinical salmonellosis in wild birds from an area of high prevalence of pig salmonellosis: Phenotypic and genetic profiles of Salmonella isolates. Zoonoses Public Health. 2013; 60: 355–365. 10.1111/j.1863-2378.2012.01542.x PubMed DOI

Rodriguez A, Pangloli P, Richards HA, Mount JR, Draughon FA. Prevalence of Salmonella in diverse environmental farm samples. J Food Prot. 2006; 69: 2576–2580. PubMed

Kourany M, Myers CW, Schneider CR. Panamanian amphibians and reptiles as carriers of Salmonella. Am J Trop Med Hyg. 1970; 19: 632–638. PubMed

Kourany M, Bowdre L, Herrer A. Panamanian forest mammals as carriers of Salmonella. Am J Trop Med Hyg 1976; 25: 449–455. PubMed

Navarro-Gonzalez N, Mentaberre G, Porrero CM, Serrano E, Mateos A, López-Martín JM, et al. Effect of cattle on Salmonella carriage, diversity and antimicrobial resistance in free-ranging wild boar (Sus scrofa) in northeastern Spain. PloS One. 2012; 7: e51614 Available at: http://journals.plos.org/plosone/article?id=doi:10.1371/journal.pone.0051614 PubMed DOI PMC

Miller S, Zieger U, Ganser C, Satterlee SA, Bankovich B, Amadi V, et al. Influence of land use and climate on Salmonella carrier status in the small Indian mongoose (Herpestes auropunctatus) in Grenada West Indies. J Wildl Dis. 2015; 51: 60–68. 10.7589/2014-02-046 PubMed DOI

Cole D, Drum DJV, Stallknecht DE, White DG, LEE MD, AYERS S et al. 2005. Free-living Canada Geese and antimicrobial resistance. (Dispathches). Emerg Infect Dis. 2005; 11: 935–938. PubMed PMC

Kozak GK, Boerlin P, Janecko N, Reid-Smith R, Jardine C. Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl Environ Microbiol. 2009; 75: 559–566. 10.1128/AEM.01821-08 PubMed DOI PMC

Allen SE, Janecko N, Pearl DL, Boerlin P, Reid-Smith R, Jardine CM. Comparison of Escherichia coli recovery and antimicrobial resistance in cecal, colon, and fecal samples collected from wild house mice (Mus musculus). J Wildl Dis. 2013; 49: 432–436. 10.7589/2012-05-142 PubMed DOI

Luque I, Echeita A, León J, Herrera-León S, Tarradas C, González-Sanz R, et al. Salmonella Indiana as a cause of abortion in ewes: Genetic diversity and resistance patterns. Vet Microbiol. 2009; 134: 396–399. 10.1016/j.vetmic.2008.08.015 PubMed DOI

Greig J, Rajić A, Young I, Mascarenhas M, Waddell L, Lejeune J. A scoping review of the role of wildlife in the transmission of bacterial pathogens and antimicrobial resistance to the food chain. Zoonoses Public Health. 2015; 62: 269–84. 10.1111/zph.12147 PubMed DOI

Jardine C, Reid-Smith RJ, Janecko N, Allan M, McEwen SA. Salmonella in raccoons (Procyon lotor) in southern Ontario, Canada. J Wildl Dis. 2011; 47: 344–351. PubMed

Very KJ, Kirchner MK, Shariat N, Cottrell W, Sandt CH, Dudley EG, et al. Prevalence and spatial distribution of Salmonella infections in the Pennsylvania Raccoon (Procyon lotor). Zoonoses Public Health. 2015. Preprint. Available: 10.1111/zph.12222 Accessed 20 August 2015. PubMed DOI

Broadfoot JD, Rosatte RC, O'Leary DT. Raccoon and skunk population models for urban disease control planning in Ontario, Canada. Ecol Appl. 2001; 11: 295–303.

Rosatte R, Ryckman M, Ing K, Proceviat S, Allan M, Bruce L, et al. Density, movements, and survival of raccoons in Ontario, Canada: implications for disease spread and management. J Mammal. 2010; 91: 122–135.

GRCA 2008. Grand River Conservation Authority. Grand River Watershed Characterization Report–Executive Summary. 2008. Available: http://www.sourcewater.ca/swp_watersheds_grand/Characterization_summary_Grand.pdf.

Government of Canada. Overview. FoodNet Canada (formerly known as C-EnterNet): Reducing the burden of gastrointestinal illness in Canada. Public Health Agency of Canada. 2013. Available: http://www.phac-aspc.gc.ca/foodnetcanada/overview-apercu-eng.php.

Bondo KB, Pearl DL, Janecko N, Boerlin P, Reid-Smith RJ, Parmley J, et al. Epidemiology of Salmonella on the paws and in the feces of free-ranging raccoons (Procyon lotor) in southern Ontario, Canada. Zoonoses Public Health. 2015; 10.1111/zph.12232 Available: http://onlinelibrary.wiley.com/doi/10.1111/zph.12232/abstract#.Vg7L2lMhHi4. Accessed 8 October 2015. PubMed DOI

Government of Canada. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2013 Annual Report–Chapter 1. Design and Methods. Public Health Agency of Canada. 2015. Available at: http://publications.gc.ca/collections/collection_2015/aspc-phac/HP2-4-2013-1-eng.pdf.

Potter AS, Reid SA, Fenwick SG. Prevalence of Salmonella in fecal samples of western grey kangaroos (Macropus fuliginosus). 2011; J Wildl Dis. 47: 880–887. PubMed

Dohoo I, Martin W, Stryhn H. Veterinary Epidemiologic Research. Charlottetown: University of Prince Edward Island; 2009.

Veterinary Drugs Directorate. Categorization of antimicrobial drugs based on importance in human medicine. 2009. Available: http://www.hc-sc.gc.ca/dhp-mps/vet/antimicrob/amr_ram_hum-med-rev-eng.php. Accessed Oct. 20, 2015.

Pedersen K, Clark L, Andelt WF, Salman MD. Prevalence of shiga toxin-producing Escherichia coli and Salmonella enterica in rock pigeons captured in Fort Collins, Colorado. J Wildl Dis. 2006; 42: 46–55. PubMed

Bolton FJ, Surman SB, Martin K., Wareing DRA, Humphrey TJL. Presence of Campylobacter and Salmonella in sand from bathing beaches. Epidemiol Infect. 1999; 122: 7–13. PubMed PMC

You Y, Rankin SC, Aceto HW, Benson CE, Toth JD, Dou Z. Survival of Salmonella enterica serovar Newport in manure and manure-amended soils. Appl Environ Microbiol. 2006; 72: 5777–83. PubMed PMC

Kalwasińska A, Burkowska A. Municipal landfill sites as sources of microorganisms potentially pathogenic to humans. Environ Sci Process Impacts. 2013; 15:1078–1086. 10.1039/c3em30728j PubMed DOI

Morse EV, Duncan MA, Estep DA, Riggs WA, Blackburn BO. Canine salmonellosis: A review and report of dog to child transmission of Salmonella enteritidis. Am J Public Health. 1976; 66: 82–3. PubMed PMC

Martinez-Urtaza J, Montserrat S, de Novoa J, Perez-Piñeiro P, Peiteado J, Lozano-Leon A, et al. Influence of environmental factors and human activity on the presence of Salmonella serovars in a marine environment. Appl Environ Microbiol. 2004; 70: 2089–2097. PubMed PMC

Haley BJ, Cole DJ, Lipp EK. Distribution, diversity, and seasonality of waterborne Salmonellae in a rural watershed. Appl Environ Microbiol. 2009; 75:1248–1255. 10.1128/AEM.01648-08 PubMed DOI PMC

Martinez-Urtaza J, Liebana E, Garcia-Migura L, Perez-Piñeiro P, Saco M. Characterization of Salmonella enterica serovar Typhimurium from marine environments in coastal waters of Galicia (Spain). Appl Environ Microbiol. 2004; 70: 4030–4034. PubMed PMC

Gorski L, Parker CT, Liang A, Cooley MB, Jay-Russell MT, Gordus AG, et al. Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl Environ Microbiol. 2011; 77:2734–48. 10.1128/AEM.02321-10 PubMed DOI PMC

Morse EV, Midla DA, Kazacos KR. Raccoons (Procyon lotor) as carriers of Salmonella. J Environ Sci Health A. 1983; 18: 541–560.

Sonenshine DE, Winslow EL. Contrasts in distribution of raccoons in two Virginia localities. J Wildl Manage. 1972; 36: 838–847.

Levantesi C, Bonadonna L, Briancesco R, Grohmann E, Toze S, Tandoi V.Salmonella in surface and drinking water: occurrence and water-mediated transmission. Food Res Int. 2012; 45:587–602.

Government of Canada. National Enteric Surveillance Program (NESP), annual summary 2010. Public Health Agency of Canada. 2012. Available: http://publications.gc.ca/collections/collection_2012/aspc-phac/HP37-15-2010-eng.pdf

Government of Canada. FoodNet Canada 2010 Annual Report. Ottawa: Public Health Agency of Canada. 2014. Available: http://publications.gc.ca/collections/collection_2014/aspc-phac/HP37-17-2010-eng.pdf

Government of Canada. Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2008 annual report. Guelph: Public Health Agency of Canada. 2011. Available: http://www.phac-aspc.gc.ca/cipars-picra/2008/index-eng.php.

Fritzell EK. Aspects of raccoon (Procyon lotor) social organization. Can J Zool. 1978; 56: 260–271.

Gehrt SD, Fritzell EK. Sexual differences in home ranges of raccoons. J Mammal. 1997; 78: 921–931.

Chamberlain MJ, Conner LM, Leopold BD, Hodges KM. Space use and multi-scale habitat selection of adult raccoons in central Mississippi. J Wildl Manage. 2003; 67: 334–340.

Vugia DJ, Samuel M, Farley MM, Marcus R, Shiferaw B, Shallow S, et al. Invasive Salmonella infections in the United States, FoodNet, 1996–1999: incidence, serotype distribution, and outcome. Clin Infect Dis. 2004; 38(s3): S149–S156. PubMed

Cowled BD, Ward MP, Laffan SW, Galea F, Garner MG, MacDonald AJ, et al. Integrating survey and molecular approaches to better understand wildlife disease ecology. PLoS One. 2012; 7: e46310 Available: http://journals.plos.org/plosone/article?id=doi:10.1371/journal.pone.0046310 PubMed DOI PMC

Rivest P, Bergeron JM. Density, food habits, and economic importance of raccoons (Procyon lotor) in Quebec agrosystems. Can J Zool. 1981; 59: 1755–1762.

Funk J, Gebreyes WA. Risk factors associated with Salmonella prevalence on swine farms. Swine Health Prod. 2004; 12: 246–251.

Bondo KJ, Weese JS, Rouseau J, Jardine CM. Longitudinal study of Clostridium difficile shedding in raccoons on swine farms and conservation areas in Ontario, Canada. 2015. BMC Vet Res. 10.1186/s12917-015-0563-x PubMed DOI PMC

Hart RP, Bradshaw SD, Iveson JB. Salmonella infections in a marsupial, the quokka (Setonix brachyurus), in relation to seasonal changes in condition and environmental stress. Appl Environ Microbiol. 1985; 49: 1276–1281. PubMed PMC

McLaughlin MR, Brooks JP, Adeli A. Temporal flux and spatial dynamics of nutrients, fecal indicators, and zoonotic pathogens in anaerobic swine manure lagoon water. Water Res. 2012; 46: 4949–4960. 10.1016/j.watres.2012.06.023 PubMed DOI

Jacobsen CS, Bech TB. Soil survival of Salmonella and transfer to freshwater and fresh produce. Food Res Int. 2012; 45: 557–566.

García R, Baelum J, Fredslund L, Santorum P, Jacobsen CS. Influence of temperature and predation on survival of Salmonella enterica serovar Typhimurium and expression of invA in soil and manure-amended soil. Appl Environ Microbiol. 2010; 76: 5025–5031. 10.1128/AEM.00628-10 PubMed DOI PMC

Arrus KM, Holley RA, Ominski KH, Tenuta M, Blank G. Influence of temperature on Salmonella survival in hog manure slurry and seasonal temperature profiles in farm manure storage reservoirs. Livest Sci. 2006; 102: 226–236.

Colwell RR. Viable but not cultivable bacteria In: Epstein SS, editor. Uncultivated microorganisms. Berlin: Springer-Verlag; 2009. pp. 121–129.

Ram JL, Thompson B, Turner C, Nechvatal JM, Sheehan H, Bobrin J. Identification of pets and raccoons as sources of bacterial contamination of urban storm sewers using a sequence-based bacterial source tracking method. Water Res. 2007; 41: 3605–3614. PubMed

Bigler WJ, Hoff GL, Jasmin AM, White FH 1974. Salmonella infections in Florida raccoons, Procyon lotor. Arch Environ Health. 1974; 28: 261–262. PubMed

White FH, Watson JJ, Hoff GL, Bigler WJ. Edwardsiella tarda infections in Florida raccoons, Procyon lotor. Arch Environ Health. 1975; 30: 602–603 PubMed

Leonard EK, Pearl DL, Finley RL, Janecko N, Peregrine AS, Reid‐Smith RJ et al. Evaluation of pet‐related management factors and the risk of Salmonella spp. carriage in pet dogs from volunteer households in Ontario (2005–2006). Zoonoses Public Health. 2011; 58: 140–149. 10.1111/j.1863-2378.2009.01320.x PubMed DOI

Young I, Rajić A, Wilhelm BJ, Waddell L, Parker S, Mcewen SA. Comparison of the prevalence of bacterial enteropathogens, potentially zoonotic bacteria and bacterial resistance to antimicrobials in organic and conventional poultry, swine and beef production: a systematic review and meta-analysis. Epidemiol and Infect. 2009; 137: 1217–1232. PubMed

Baquero F, Martinez J, Canton R. 2008. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol. 2008; 19: 260–265. 10.1016/j.copbio.2008.05.006 PubMed DOI

Finley R, Ribble C, Aramini J, Vandermeer M, Popa M., Litman M, et al. 2007. The risk of salmonellae shedding by dogs fed Salmonella-contaminated commercial raw food diets. Can Vet J. 2007; 48:69–75. PubMed PMC

Behravesh CB, Ferraro A, Deasy M, Dato V, Moll M, Sandt C, et al. Human Salmonella infections linked to contaminated dry dog and cat food, 2006–2008. Pediatrics. 2010; 126: 477–483. Available: http://pediatrics.aappublications.org/content/126/3/477.full.pdf+html. Accessed 18 October 2014. 10.1542/peds.2009-3273 PubMed DOI

Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol. 2010; 12: 2385–39. 10.1111/j.1462-2920.2010.02297.x PubMed DOI

Pesapane R, Ponder M, Alexander KA. Tracking pathogen transmission at the human–wildlife interface: banded mongoose and Escherichia coli. Ecohealth. 2013; 10:115–128. 10.1007/s10393-013-0838-2 PubMed DOI

Acheson D, Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis. 2001; 32: 263–269. PubMed

Epidemiology of Antimicrobial Resistance in Escherichia coli Isolates from Raccoons (Procyon lotor) and the Environment on Swine Farms and Conservation Areas in Southern Ontario