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

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          Abstract

          Antimicrobial resistance is a global threat to livestock, human and environmental health. Although resistant bacteria have been detected in wildlife, their role in the epidemiology of antimicrobial resistance is not clear. Our objective was to investigate demographic, temporal and climatic factors associated with carriage of antimicrobial resistant Escherichia coli in raccoons and the environment. We collected samples from raccoon paws and feces and from soil, manure pit and dumpsters on five swine farms and five conservation areas in Ontario, Canada once every five weeks from May to November, 2011 2013 and tested them for E. coli and susceptibility to 15 antimicrobials. Of samples testing positive for E. coli, resistance to ≥ 1 antimicrobials was detected in 7.4% (77/1044; 95% CI, 5.9–9.1) of raccoon fecal samples, 6.3% (23/365; 95% CI, 4.0–9.3) of paw samples, 9.6% (121/1260; 8.0–11.4) of soil samples, 57.4% (31/54; 95% CI, 43.2–70.8) of manure pit samples, and 13.8% (4/29; 95% CI, 3.9–31.7) of dumpster samples. Using univariable logistic regression, there was no significant difference in the occurrence of resistant E. coli in raccoon feces on conservation areas versus farms; however, E. coli isolates resistant to ≥ 1 antimicrobials were significantly less likely to be detected from raccoon paw samples on swine farms than conservation areas and significantly more likely to be detected in soil samples from swine farms than conservation areas. Resistant phenotypes and genotypes that were absent from the swine farm environment were detected in raccoons from conservation areas, suggesting that conservation areas and swine farms may have different exposures to resistant bacteria. However, the similar resistance patterns and genes in E. coli from raccoon fecal and environmental samples from the same location types suggest that resistant bacteria may be exchanged between raccoons and their environment.

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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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            Antibiotics in the aquatic environment--a review--part II.

            Although antibiotics have been used in large quantities for some decades, until recently the existence of these substances in the environment has received little notice. It is only in recent years that a more complex investigation of antibiotic substances has been undertaken in order to permit an assessment of the environmental risks they may pose. Within the last decade, an increasing number of studies covering antibiotic input, occurrence, fate and effects have been published. Antibiotics are one of the most important groups of pharmaceuticals. Antibiotic resistance is one of the major challenges for human medicine and veterinary medicine. However, there is still a lack of understanding and knowledge about sources, presence and significance of resistance of bacteria against antibiotics in the aquatic environment despite the numerous studies performed. This review summarizes this topic. It names important open questions and addresses some significant issues which must be tackled in the future for a better understanding of resistance related to antibiotics in the environment.
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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 November 2016
                2016
                : 11
                : 11
                : e0165303
                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
                USDA-ARS Salinity Laboratory, UNITED STATES
                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 DLP 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.

                Author information
                http://orcid.org/0000-0002-6186-5599
                Article
                PONE-D-16-15702
                10.1371/journal.pone.0165303
                5102455
                27829035
                35c68a8f-3a62-441b-b119-77f10e2ca49c
                © 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.

                History
                : 18 April 2016
                : 10 October 2016
                Page count
                Figures: 0, Tables: 2, Pages: 16
                Funding
                Funding was provided by the National Science and Engineering Research Council (NSERC) and the United States Department of Agriculture (USDA). KJB also received support through 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
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobial Resistance
                Medicine and Health Sciences
                Pharmacology
                Antimicrobial Resistance
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Raccoons
                Medicine and Health Sciences
                Pharmacology
                Drugs
                Antimicrobials
                Biology and Life Sciences
                Microbiology
                Microbial Control
                Antimicrobials
                Biology and Life Sciences
                Agriculture
                Livestock
                Swine
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Mammals
                Swine
                Biology and Life Sciences
                Agriculture
                Farms
                Biology and Life Sciences
                Organisms
                Animals
                Animal Types
                Wildlife
                Biology and Life Sciences
                Zoology
                Animal Types
                Wildlife
                Biology and Life Sciences
                Agriculture
                Livestock
                People and places
                Geographical locations
                North America
                Canada
                Ontario
                Custom metadata
                All data files are available in the Scholars Portal Dataverse, V1 (doi: 10.5683/SP/BLFRK5, < http://dx.doi.org/10.5683/SP/BLFRK5>).

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