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      Impact of Season, Demographic and Environmental Factors on Salmonella Occurrence in Raccoons ( Procyon lotor) from Swine Farms and Conservation Areas in Southern Ontario

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          Abstract

          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.

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          Antibiotics and antibiotic resistance in water environments.

          Antibiotic-resistant organisms enter into water environments from human and animal sources. These bacteria are able to spread their genes into water-indigenous microbes, which also contain resistance genes. On the contrary, many antibiotics from industrial origin circulate in water environments, potentially altering microbial ecosystems. Risk assessment protocols for antibiotics and resistant bacteria in water, based on better systems for antibiotics detection and antibiotic-resistance microbial source tracking, are starting to be discussed. Methods to reduce resistant bacterial load in wastewaters, and the amount of antimicrobial agents, in most cases originated in hospitals and farms, include optimization of disinfection procedures and management of wastewater and manure. A policy for preventing mixing human-originated and animal-originated bacteria with environmental organisms seems advisable.
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            Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli.

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              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.

              Wild animals not normally exposed to antimicrobial agents can acquire antimicrobial agent-resistant bacteria through contact with humans and domestic animals and through the environment. In this study we assessed the frequency of antimicrobial resistance in generic Escherichia coli isolates from wild small mammals (mice, voles, and shrews) and the effect of their habitat (farm or natural area) on antimicrobial resistance. Additionally, we compared the types and frequency of antimicrobial resistance in E. coli isolates from swine on the same farms from which wild small mammals were collected. Animals residing in the vicinity of farms were five times more likely to carry E. coli isolates with tetracycline resistance determinants than animals living in natural areas; resistance to tetracycline was also the most frequently observed resistance in isolates recovered from swine (83%). Our results suggest that E. coli isolates from wild small mammals living on farms have higher rates of resistance and are more frequently multiresistant than E. coli isolates from environments, such as natural areas, that are less impacted by human and agricultural activities. No Salmonella isolates were recovered from any of the wild small mammal feces. This study suggests that close proximity to food animal agriculture increases the likelihood that E. coli isolates from wild animals are resistant to some antimicrobials, possibly due to exposure to resistant E. coli isolates from livestock, to the resistance genes of these isolates, or to antimicrobials through contact with animal feed.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 September 2016
                2016
                : 11
                : 9
                Affiliations
                [1 ]Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada
                [2 ]Department of Population Medicine, University of Guelph, Guelph, Ontario, Canada
                [3 ]Centre for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, Ontario, Canada
                [4 ]Department of Biology and Wildlife Diseases, University of Veterinary and Pharmaceutical Sciences Brno, Brno, Czech Republic
                [5 ]Canadian Wildlife Health Cooperative, Department of Pathobiology, University of Guelph, Guelph, Ontario, Canada
                Ross University School of Veterinary Medicine, SAINT KITTS AND NEVIS
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: KJB DLP PB RJR JP CMJ.

                • Data curation: KJB DLP NL CMJ.

                • Formal analysis: KJB DLP CMJ.

                • Funding acquisition: DLP RJR CMJ.

                • Investigation: KJB NJ CMJ.

                • Methodology: KJB DLP NJ PB RJR JP CMJ.

                • Project administration: KJB DLP NJ RJR CMJ.

                • Resources: DLP PB RJR JP CMJ.

                • Supervision: DLP PB RJR JP CMJ.

                • Validation: KJB DLP NJ PB RJR JP CMJ.

                • Visualization: KJB DLP NJ PB RJR JP CMJ.

                • Writing – original draft: KJB DLP CMJ.

                • Writing – review & editing: KJB DLP NJ PB RJR JP CMJ.

                Article
                PONE-D-16-12085
                10.1371/journal.pone.0161497
                5017689
                27611198
                a052e2cf-878d-42b8-8221-0d33b9722f15
                © 2016 Bondo et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Figures: 2, Tables: 5, Pages: 21
                Product
                Funding
                Funding was provided by the National Science and Engineering Research Council (NSERC; CMJ). KJB received support through the United States Department of Agriculture (USDA) and an Ontario Graduate Scholarship (OGS). In-kind support was provided by the Public Health Agency of Canada. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Salmonella
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Salmonella
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Salmonella
                Biology and Life Sciences
                Organisms
                Bacteria
                Enterobacteriaceae
                Salmonella
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Raccoons
                Biology and Life Sciences
                Agriculture
                Farms
                Biology and Life Sciences
                Agriculture
                Livestock
                Swine
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Swine
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobial Resistance
                Medicine and Health Sciences
                Pharmacology
                Antimicrobial Resistance
                Medicine and Health Sciences
                Pharmacology
                Drugs
                Antimicrobials
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobials
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Salmonella
                Salmonella Typhimurium
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Salmonella
                Salmonella Typhimurium
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Salmonella
                Salmonella Typhimurium
                Biology and Life Sciences
                Organisms
                Bacteria
                Enterobacteriaceae
                Salmonella
                Salmonella Typhimurium
                Biology and Life Sciences
                Organisms
                Animals
                Animal Types
                Wildlife
                Biology and Life Sciences
                Zoology
                Animal Types
                Wildlife
                Custom metadata
                The direct link to the dataset in the Agri-environmental Research Data Repository is: http://hdl.handle.net/10864/12074. The DOI for the dataset is: http://dx.doi.org/10.5887/AERDR/10864/12074.

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