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Alexiou S, Diakou A, Kachrimanidou M. The Role of Clostridioides difficile Within the One Health Framework: A Review. Microorganisms 2025; 13:429. [PMID: 40005794 PMCID: PMC11858594 DOI: 10.3390/microorganisms13020429] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/15/2025] [Revised: 02/12/2025] [Accepted: 02/13/2025] [Indexed: 02/27/2025] Open
Abstract
Clostridioides difficile is the leading cause of antibiotic-associated diarrhea in hospitalized patients. In recent years, the incidence of C. difficile infection (CDI) has increased globally, with a notable rise in community-associated CDI (CA-CDI). The presence of the microorganism in animals, the environment, and food suggests that these sources may contribute to the spread of the infection in the community. This review applies a One Health approach, integrating human, animal, and environmental health, to provide a comprehensive strategy for understanding and managing this pathogen. Findings reveal the widespread dissemination of C. difficile in animals, the environment, and food. The predominant PCR ribotypes identified were RTs 078 and 014/020, followed by RTs 126, 001, 002, 009, 010, and 033. C. difficile strains exhibited resistance to multiple antimicrobial agents, including clindamycin, erythromycin, fluoroquinolones, cephalosporins, and tetracyclines. Discriminative typing methods, such as whole-genome sequencing, revealed clonal relationships between C. difficile strains from humans and animals, indicating either direct transmission or a common environmental source of infection. The high genetic similarity between isolates from the environment and humans indicates potential environmental contamination. Additionally, clusters of C. difficile strains found in food and humans indicate a possible foodborne transmission route. This review summarizes the current knowledge on the role of Clostridioides difficile within the One Health framework.
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Affiliation(s)
- Sotiris Alexiou
- Department of Microbiology, Medical School, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece;
| | - Anastasia Diakou
- Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece;
| | - Melania Kachrimanidou
- Department of Microbiology, Medical School, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece;
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Ojha S, Thakur KK, Ojasanya RA, Saab ME. Retrospective study on the occurrence of Salmonella serotypes in veterinary specimens of Atlantic Canada (2012-2021). Vet Med Sci 2024; 10:e1530. [PMID: 38979670 PMCID: PMC11231644 DOI: 10.1002/vms3.1530] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/25/2023] [Revised: 03/14/2024] [Accepted: 06/14/2024] [Indexed: 07/10/2024] Open
Abstract
AIM This study aimed to summarize the frequency and the antimicrobial susceptibility profiles of the Salmonella serotypes identified from the specimens of companion animals, livestock, avian, wildlife and exotic species within Atlantic Canada. MATERIALS AND METHODS The retrospective electronic laboratory data of microbiological analyses of a selected subset of samples from 03 January 2012 to 29 December 2021 submitted from various animal species were retrieved. The frequency of Salmonella serotypes identified, and their antimicrobial susceptibility results obtained using the disk diffusion or broth method were analysed. The test results were interpreted according to the Clinical and Laboratory Standards Institute standard. The Salmonella serotypes were identified by slide agglutination (Kauffman-White-Le-Minor Scheme) and/or the Whole Genome Sequencing for the Salmonella in silico Serovar Typing Resource-based identification. RESULTS Of the cases included in this study, 4.6% (n = 154) had at least one Salmonella isolate, corresponding to 55 different serovars. Salmonella isolation was highest from exotic animal species (n = 40, 1.20%), followed by porcine (n = 26, 0.78%), and canine (n = 23, 0.69%). Salmonella subsp. enterica serovar Typhimurium was predominant among exotic mammals, porcine and caprine samples, whereas S. Enteritidis was mostly identified in bovine and canine samples. S. Typhimurium of porcine origin was frequently resistant (>70.0%) to ampicillin. In contrast, S. Typhimurium isolates from porcine and caprine samples were susceptible (>70.0%) to florfenicol. S. Oranienburg from equine samples was susceptible to chloramphenicol, but frequently resistant (>90.0%) to azithromycin. In avian samples, S. Copenhagen was susceptible (>90.0%) to florfenicol, whereas Muenchen was frequently resistant (>90.0%) to florfenicol. S. subsp. diarizonae serovar IIIb:61:k:1,5 of ovine origin was resistant (50.0% isolates) to sulfadimethoxine. No significant changes were observed in the antibiotic resistance profiles across the study years. CONCLUSIONS This report provides data for surveillance studies, distribution of Salmonella serotypes and their antimicrobial resistance among veterinary specimens of Atlantic Canada.
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Affiliation(s)
- Shivani Ojha
- Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada
- Veterinary Diagnostic Services Laboratory, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada
| | - Krishna K Thakur
- Department of Health Management, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada
| | - Rasaq A Ojasanya
- Department of Health Management, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada
| | - Matthew E Saab
- Veterinary Diagnostic Services Laboratory, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada
- Department of Health Management, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, Prince Edward Island, Canada
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Cummings KJ, Siler JD, Goodman LB, Childs-Sanford SE. Ciprofloxacin-resistant ST198 Salmonella Kentucky in a hospitalized American black bear (Ursus americanus), with evidence of subsequent nosocomial transmission. Zoonoses Public Health 2023; 70:657-664. [PMID: 37464973 DOI: 10.1111/zph.13075] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/20/2022] [Revised: 06/01/2023] [Accepted: 07/03/2023] [Indexed: 07/20/2023]
Abstract
Global emergence of ciprofloxacin-resistant ST198 Salmonella Kentucky poses an important public health threat. While conducting Salmonella surveillance among wildlife patients admitted to our veterinary medical teaching hospital in central New York, we isolated multidrug-resistant (MDR) ST198 Salmonella Kentucky from an American black bear (Ursus americanus) in September 2020. The isolate was phenotypically resistant to numerous antimicrobial agents, including ceftriaxone and ciprofloxacin, and several antimicrobial resistance genes and mutational resistance determinants were detected. Between April and July 2021, the same strain of MDR ST198 Salmonella Kentucky was also isolated from seven other wildlife patients and multiple hospital environmental locations, suggesting nosocomial transmission. Ciprofloxacin resistance is conferred by triple point mutations in the quinolone resistance-determining regions (QRDRs), a genotypic profile indicative of Clade ST198.2. To our knowledge, this is the first report of this ciprofloxacin-resistant clade being identified in animals or animal products in the United States. Timely resolution of the outbreak was achieved following efforts to further enhance environmental disinfection protocols and biosecurity measures at the hospital, with no known cases or positive environmental samples after July 2021.
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Cardia Caserta L, Mansano do Nascimento G, Joshi LR, Mausbach Simão R, Miller ME, Nunes Felippe PA, Diel DG, Weis Arns C. Bacterial and Viral Diversity of Didelphid Opossums from Brazil. ECOHEALTH 2023; 20:362-369. [PMID: 38091183 DOI: 10.1007/s10393-023-01667-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Grants] [Track Full Text] [Subscribe] [Scholar Register] [Received: 06/22/2022] [Accepted: 11/28/2023] [Indexed: 02/21/2024]
Abstract
Marsupials belonging to the Didelphis genus are widely distributed in the American Continent, and Didelphis albiventris and Didelphis aurita, are common in all of their areas of distribution in Brazil. Here we describe the bacterial and viral diversity of samples from opossums captured in three forest fragments in the State of São Paulo, Brazil. Microbiomes from the same body site were more similar across species and sampling sites while oral swabs presented higher bacterial diversity than rectal swabs. We also identified sequences related to bacterial species involved in zoonotic diseases. The detection of pathogens in such abundant mammal species warns for the possibility of emergence in other species.
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Affiliation(s)
- Leonardo Cardia Caserta
- Departamento de Genética, Evolução, Microbiologia e Imunologia, Instituto de Biologia, Universidade Estadual de Campinas - UNICAMP, Campinas, Brazil.
- Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, 240 Farrier Road, Ithaca, NY, 14853, USA.
| | - Gabriela Mansano do Nascimento
- Departamento de Genética, Evolução, Microbiologia e Imunologia, Instituto de Biologia, Universidade Estadual de Campinas - UNICAMP, Campinas, Brazil
- Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, 240 Farrier Road, Ithaca, NY, 14853, USA
| | - Lok Raj Joshi
- Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, 240 Farrier Road, Ithaca, NY, 14853, USA
| | - Raphael Mausbach Simão
- Programa de Pós-Graduação em Epidemiologia Experimental Aplicada às Zoonoses, Faculdade de Medicina Veterinária e Zootecnia (FMVZ-USP), São Paulo, Brazil
| | - Michael E Miller
- Departamento de Genética, Evolução, Microbiologia e Imunologia, Instituto de Biologia, Universidade Estadual de Campinas - UNICAMP, Campinas, Brazil
| | - Paulo A Nunes Felippe
- Departamento de Proteção e Bem-Estar Animal - Prefeitura de Campinas, Campinas, SP, Brazil
| | - Diego G Diel
- Department of Population Medicine and Diagnostic Sciences, College of Veterinary Medicine, Cornell University, 240 Farrier Road, Ithaca, NY, 14853, USA
| | - Clarice Weis Arns
- Departamento de Genética, Evolução, Microbiologia e Imunologia, Instituto de Biologia, Universidade Estadual de Campinas - UNICAMP, Campinas, Brazil
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Olvera-Ramírez AM, McEwan NR, Stanley K, Nava-Diaz R, Aguilar-Tipacamú G. A Systematic Review on the Role of Wildlife as Carriers and Spreaders of Campylobacter spp. Animals (Basel) 2023; 13:1334. [PMID: 37106897 PMCID: PMC10135385 DOI: 10.3390/ani13081334] [Citation(s) in RCA: 8] [Impact Index Per Article: 4.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 12/17/2022] [Revised: 04/05/2023] [Accepted: 04/06/2023] [Indexed: 04/29/2023] Open
Abstract
Campylobacter spp. are important zoonotic pathogens and can cause one of the main bacterial diarrheal diseases worldwide. Research in the context of infection arising from transmission from other humans and other vertebrates has been extensive. A large fraction of these investigations has focused on domestic animals; however, there are also a number of publications which either totally, or at least in part, consider the role of wild or feral animals as carriers or spreaders of Campylobacter spp. Here, we carry out a systematic review to explore the role played by wild vertebrates as sources of Campylobacter spp. with a compilation of prevalence data for more than 150 species including reptiles, mammals and birds. We found that numerous vertebrate species can act as carriers of Campylobacter species, but we also found that some host specificity may exist, reducing the risk of spread from wildlife to domestic animals or humans.
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Affiliation(s)
- Andrea Margarita Olvera-Ramírez
- Cuerpo Académico Salud Animal y Microbiología Ambiental, Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Avenida de las Ciencias S/N, Juriquilla, Delegación Santa Rosa Jáuregui, Querétaro C.P. 76230, Mexico
| | - Neil Ross McEwan
- School of Pharmacy and Life Sciences, Robert Gordon University, Aberdeen AB10 7GJ, UK
| | - Karen Stanley
- Department of Biosciences and Chemistry, Sheffield Hallam University City Campus, Howard Street, Sheffield S1 1WB, UK
| | - Remedios Nava-Diaz
- Posdoctoral CONACyT Program, Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Avenida de las Ciencias S/N, Juriquilla, Delegación Santa Rosa Jáuregui, Querétaro C.P. 76230, Mexico
| | - Gabriela Aguilar-Tipacamú
- Cuerpo Académico Salud Animal y Microbiología Ambiental, Facultad de Ciencias Naturales, Universidad Autónoma de Querétaro, Avenida de las Ciencias S/N, Juriquilla, Delegación Santa Rosa Jáuregui, Querétaro C.P. 76230, Mexico
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Brooks MR, Medley S, Ponder M, Alexander KA. Campylobacter in aquatic and terrestrial mammals is driven by life traits: A systematic review and meta-analysis. Front Ecol Evol 2023. [DOI: 10.3389/fevo.2023.1070519] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/05/2023] Open
Abstract
IntroductionCampylobacter spp. infections are responsible for significant diarrheal disease burden across the globe, with prevalence thought to be increasing. Although wild avian species have been studied as reservoirs of Campylobacter spp., our understanding of the role of wild mammalian species in disease transmission and persistence is limited. Host factors influencing infection dynamics in wild mammals have been neglected, particularly life traits, and the role of these factors in zoonotic spillover risk is largely unknown.MethodsHere, we conducted a systematic literature review, identifying mammalian species that had been tested for Campylobacter spp. infections (molecular and culture based). We used logistic regression to evaluate the relationship between the detection of Campylobacter spp. in feces and host life traits (urban association, trophic level, and sociality).ResultsOur analysis suggest that C. jejuni transmission is associated with urban living and trophic level. The probability of carriage was highest in urban-associated species (p = 0.02793) and the most informative model included trophic level. In contrast, C. coli carriage appears to be strongly influenced by sociality (p = 0.0113) with trophic level still being important. Detection of Campylobacter organisms at the genus level, however, was only associated with trophic level (p = 0.0156), highlighting the importance of this trait in exposure dynamics across host and Campylobacter pathogen systems.DiscussionWhile many challenges remain in the detection and characterization of Camploybacter spp., these results suggest that host life traits may have important influence on pathogen exposure and transmission dynamics, providing a useful starting point for more directed surveillance approaches.
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Prince Milton AA, Momin AG, Gandhale PN, Das S, Ghatak S, Priya GB, Firake DM, Srinivas K, Momin KM, Hussain Z, Sen A. Prevalence, toxinotyping, antimicrobial susceptibility and biofilm-forming ability of Clostridium perfringens isolated from free-living rodents and shrews. Anaerobe 2022; 77:102618. [PMID: 35933078 DOI: 10.1016/j.anaerobe.2022.102618] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 04/08/2022] [Revised: 07/04/2022] [Accepted: 07/23/2022] [Indexed: 11/01/2022]
Abstract
BACKGROUND AND OBJECTIVES Clostridium perfringens (C. perfringens), is a spore-forming and toxin-producing pathogenic anaerobic Gram-positive rod-shaped bacterium with immense public health/zoonotic concern. Rodents are well-known reservoirs and vectors for a large number of zoonoses and strong links have been recognized between synanthropic rodents and foodborne disease outbreaks throughout the world. To date, no study has been conducted for studying the prevalence of C. perfringens in rodents and shrews. In this study, we investigated faecal samples from free-living rodents and shrews trapped in Meghalaya, a North-eastern hill state of India for the presence of virulent and antimicrobial-resistant C. perfringens. METHODS A total of 122 animals comprising six species of rodents and one species of shrews were trapped: Mus musculus (n = 15), Mus booduga (n = 7), Rattus rattus (n = 9), Rattus norvegicus (n = 3), Bandicota indica (n = 30), Bandicota bengalensis (n = 32) and Suncus murinus (n = 26). The faecal swabs were collected and processed for the isolation of C. perfringens. Toxinotyping was done using PCR. Antimicrobial susceptibility testing and biofilm forming ability testing were done using Kirby Bauer disc diffusion method and crystal violet assay. RESULTS C. perfringens was isolated from 27 of the 122 faecal swabs (22.1%), from six species of rodents and shrews. Five of the host species were rodents, Bandicota bengalensis (25%), Bandicota indica (16.7%), Rattus norvegicus (33.3%), Mus musculus (13.3%), Mus booduga (42.8%) and Suncus murinus (29.6%). The common toxinotype was type A (59.2%) followed by Type A with beta2 toxin (33.3%), Type C (3.7%) and Type C with beta2 toxin (3.7%). None of the isolates harboured cpe, etx, iap, and NetB genes and therefore none was typed as either B, D, E, F, or G. Nine isolates (33.3%) turned out to be multi-drug resistant (MDR), displaying resistance to three or more categories of antibiotics tested. Twenty-three out of twenty-seven isolates (85.2%) were forming biofilms. CONCLUSION Globally, this is the first study to report the prevalence of C. perfringens and its virulence profile and antimicrobial resistance in free-living rodents and shrews. The rodents and shrews can potentially contaminate the food and environment and can infect humans and livestock with multi-drug resistant/virulent Type A and Type C C. perfringens.
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Affiliation(s)
| | - Aleimo G Momin
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India
| | | | - Samir Das
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India.
| | - Sandeep Ghatak
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India
| | - G Bhuvana Priya
- College of Agriculture, Central Agricultural University (Imphal), Kyrdemkulai, Meghalaya, India
| | - Dnyaneshwar Madhukar Firake
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India; ICAR-Directorate of Floricultural Research, Pune, Maharashtra, India
| | - Kandhan Srinivas
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India
| | - Kasanchi M Momin
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India
| | - Zakir Hussain
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India
| | - Arnab Sen
- Division of Animal and Fisheries Sciences, ICAR Research Complex for NEH Region, Umiam, Meghalaya, India
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Vogt NA, Hetman BM, Vogt AA, Pearl DL, Reid-Smith RJ, Parmley EJ, Kadykalo S, Ziebell K, Bharat A, Mulvey MR, Janecko N, Ricker N, Allen SE, Bondo KJ, Jardine CM. Using whole-genome sequence data to examine the epidemiology of antimicrobial resistance in Escherichia coli from wild meso-mammals and environmental sources on swine farms, conservation areas, and the Grand River watershed in southern Ontario, Canada. PLoS One 2022; 17:e0266829. [PMID: 35395054 PMCID: PMC8993012 DOI: 10.1371/journal.pone.0266829] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/05/2022] [Accepted: 03/28/2022] [Indexed: 11/24/2022] Open
Abstract
Antimicrobial resistance (AMR) threatens the health of humans and animals and has repeatedly been detected in wild animal species across the world. This cross-sectional study integrates whole-genome sequence data from Escherichia coli isolates with demonstrated phenotypic resistance that originated from a previous longitudinal wildlife study in southern Ontario, as well as phenotypically resistant E. coli water isolates previously collected as part of a public health surveillance program. The objective of this work was to assess for evidence of possible transmission of antimicrobial resistance determinants between wild meso-mammals, swine manure pits, and environmental sources on a broad scale in the Grand River watershed, and at a local scale—for the subset of samples collected on both swine farms and conservation areas in the previous wildlife study. Logistic regression models were used to assess potential associations between sampling source, location type (swine farm vs. conservation area), and the occurrence of select resistance genes and predicted plasmids. In total, 200 isolates from the following sources were included: water (n = 20), wildlife (n = 73), swine manure pit (n = 31), soil (n = 73), and dumpsters (n = 3). Several genes and plasmid incompatibility types were significantly more likely to be identified on swine farms compared to conservation areas. Conversely, internationally distributed sequence types (e.g., ST131), extended-spectrum beta-lactamase- and AmpC-producing E. coli were isolated in lower prevalences (<10%) and were almost exclusively identified in water sources, or in raccoon and soil isolates obtained from conservation areas. Differences in the odds of detecting resistance genes and predicted plasmids among various sources and location types suggest different primary sources for individual AMR determinants, but, broadly, our findings suggest that raccoons, skunks and opossums in this region may be exposed to AMR pollution via water and agricultural sources, as well as anthropogenic sources in conservation areas.
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Affiliation(s)
- Nadine A. Vogt
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
- * E-mail:
| | - Benjamin M. Hetman
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
| | - Adam A. Vogt
- Independent Researcher, Mississauga, Ontario, Canada
| | - David L. Pearl
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
| | - Richard J. Reid-Smith
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
- Centre for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, Ontario, Canada
| | - E. Jane Parmley
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
| | - Stefanie Kadykalo
- Centre for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, Ontario, Canada
| | - Kim Ziebell
- National Microbiology Laboratory, Public Health Agency of Canada, Guelph, Ontario, Canada
| | - Amrita Bharat
- National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, Manitoba, Canada
| | - Michael R. Mulvey
- National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, Manitoba, Canada
| | - Nicol Janecko
- Quadram Institute Bioscience, Norwich, United Kingdom
| | - Nicole Ricker
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
| | - Samantha E. Allen
- Wyoming Game and Fish Department, Laramie, Wyoming, United States of America
- Department of Veterinary Sciences, University of Wyoming, Laramie, Wyoming, United States of America
| | - Kristin J. Bondo
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
| | - Claire M. Jardine
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
- Canadian Wildlife Health Cooperative, Ontario Veterinary College, Guelph, Ontario, Canada
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Vogt NA, Hetman BM, Pearl DL, Vogt AA, Reid-Smith RJ, Parmley EJ, Janecko N, Bharat A, Mulvey MR, Ricker N, Bondo KJ, Allen SE, Jardine CM. Using whole-genome sequence data to examine the epidemiology of Salmonella, Escherichia coli and associated antimicrobial resistance in raccoons (Procyon lotor), swine manure pits, and soil samples on swine farms in southern Ontario, Canada. PLoS One 2021; 16:e0260234. [PMID: 34793571 PMCID: PMC8601536 DOI: 10.1371/journal.pone.0260234] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [MESH Headings] [Grants] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/17/2021] [Accepted: 11/04/2021] [Indexed: 11/19/2022] Open
Abstract
To better understand the contribution of wildlife to the dissemination of Salmonella and antimicrobial resistance in Salmonella and Escherichia coli, we examined whole-genome sequence data from Salmonella and E. coli isolates collected from raccoons (Procyon lotor) and environmental sources on farms in southern Ontario. All Salmonella and phenotypically resistant E. coli collected from raccoons, soil, and manure pits on five swine farms as part of a previous study were included. We assessed for evidence of potential transmission of these organisms between different sources and farms utilizing a combination of population structure assessments (using core-genome multi-locus sequence typing), direct comparisons of multi-drug resistant isolates, and epidemiological modeling of antimicrobial resistance (AMR) genes and plasmid incompatibility (Inc) types. Univariable logistic regression models were fit to assess the impact of source type, farm location, and sampling year on the occurrence of select resistance genes and Inc types. A total of 159 Salmonella and 96 resistant E. coli isolates were included. A diversity of Salmonella serovars and sequence types were identified, and, in some cases, we found similar or identical Salmonella isolates and resistance genes between raccoons, soil, and swine manure pits. Certain Inc types and resistance genes associated with source type were consistently more likely to be identified in isolates from raccoons than swine manure pits, suggesting that manure pits are not likely a primary source of those particular resistance determinants for raccoons. Overall, our data suggest that transmission of Salmonella and AMR determinants between raccoons and swine manure pits is uncommon, but soil-raccoon transmission appears to be occurring frequently. More comprehensive sampling of farms, and assessment of farms with other livestock species, as well as additional environmental sources (e.g., rivers) may help to further elucidate the movement of resistance genes between these various sources.
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Affiliation(s)
- Nadine A. Vogt
- Department of Population Medicine, Ontario Veterinary College, Guelph, Ontario, Canada
| | - Benjamin M. Hetman
- Department of Population Medicine, Ontario Veterinary College, Guelph, Ontario, Canada
| | - David L. Pearl
- Department of Population Medicine, Ontario Veterinary College, Guelph, Ontario, Canada
| | - Adam A. Vogt
- Independent Researcher, Mississauga, Ontario, Canada
| | - Richard J. Reid-Smith
- Department of Population Medicine, Ontario Veterinary College, Guelph, Ontario, Canada
- Centre for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, Ontario, Canada
| | - E. Jane Parmley
- Department of Population Medicine, Ontario Veterinary College, Guelph, Ontario, Canada
- Centre for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, Ontario, Canada
| | - Nicol Janecko
- Quadram Institute Bioscience, Norwich, United Kingdom
| | - Amrita Bharat
- National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, Manitoba, Canada
| | - Michael R. Mulvey
- National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, Manitoba, Canada
- Department of Medical Microbiology and Infectious Diseases, University of Manitoba, Winnipeg, Manitoba, Canada
| | - Nicole Ricker
- Department of Pathobiology, Ontario Veterinary College, Guelph, Ontario, Canada
| | - Kristin J. Bondo
- Department of Pathobiology, Ontario Veterinary College, Guelph, Ontario, Canada
| | - Samantha E. Allen
- Department of Pathobiology, Ontario Veterinary College, Guelph, Ontario, Canada
- Wyoming Game and Fish Department, Laramie, Wyoming, United States of America
- Department of Veterinary Sciences, University of Wyoming, Laramie, Wyoming, United States of America
| | - Claire M. Jardine
- Department of Pathobiology, Ontario Veterinary College, Guelph, Ontario, Canada
- Canadian Wildlife Health Cooperative, Ontario Veterinary College, Guelph, Ontario, Canada
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Worsley-Tonks KEL, Miller EA, Anchor CL, Bender JB, Gehrt SD, McKenzie SC, Singer RS, Johnson TJ, Craft ME. Importance of anthropogenic sources at shaping the antimicrobial resistance profile of a peri-urban mesocarnivore. THE SCIENCE OF THE TOTAL ENVIRONMENT 2021; 764:144166. [PMID: 33401044 DOI: 10.1016/j.scitotenv.2020.144166] [Citation(s) in RCA: 8] [Impact Index Per Article: 2.0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Subscribe] [Scholar Register] [Received: 09/08/2020] [Revised: 11/25/2020] [Accepted: 11/29/2020] [Indexed: 06/12/2023]
Abstract
Anthropogenically derived antimicrobial-resistant bacteria (ARB) and antimicrobial resistance genes (ARG) have been detected in wildlife. The likelihood of detecting ARB and ARG in wildlife increases with wildlife exposure to anthropogenic sources of antimicrobial resistance (AMR). Whether anthropogenic sources also increase the risk for AMR to spread in bacteria of wildlife is not well understood. The spread of AMR in bacteria of wildlife can be estimated by examining the richness of ARB and ARG, and the prevalence of ARB that have mobilizable ARG (i.e., ARG that can be transferred across bacteria via plasmids). Here, we investigated whether raccoons (Procyon lotor), with different exposures to anthropogenic sources, differed in prevalence and richness of extended-spectrum cephalosporin-resistant (ESC-R) Escherichia coli, richness of ARG present in ESC-R E. coli, and prevalence of ESC-R E. coli with plasmid-associated ARG. Sampling took place over the course of 10 months at seven sites in Chicago, USA. ESC-R E. coli were isolated from over half of the 211 raccoons sampled and were more likely to be isolated from urban than suburban raccoons. When examining the whole-genome sequences of ESC-R E. coli, 56 sequence types were identified, most of which were associated with the ARG blaCMY and blaCTX-M. A greater richness of ESC-R E. coli sequence types was found at sites with a wastewater treatment plant (WWTP) than without, but no difference was detected based on urban context. ARG richness in ESC-R E. coli did not significantly vary by urban context nor with presence of a WWTP. Importantly, ESC-R E. coli carrying plasmid-associated blaCTX-M and blaCMY ARG were more likely to be isolated from raccoons sampled at sites with a WWTP than without. Our findings indicate that anthropogenic sources may shape the AMR profile of wildlife, reinforcing the need to prevent dissemination of AMR into the environment.
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Affiliation(s)
- Katherine E L Worsley-Tonks
- Department of Veterinary Population Medicine, University of Minnesota, 1988 Fitch Avenue, Saint Paul, MN 55108, United States of America.
| | - Elizabeth A Miller
- Department of Veterinary and Biomedical Sciences, University of Minnesota, 1971 Commonwealth Avenue, Saint Paul, MN 55108, United States of America
| | - Chris L Anchor
- Forest Preserve District of Cook County, 28W040 IL-58, Elgin, IL 60120, United States of America
| | - Jeff B Bender
- School of Public Health, University of Minnesota, 420 Delaware Street SE, Minneapolis, MN, 55455, United States of America
| | - Stanley D Gehrt
- School of Environment and Natural Resources, The Ohio State University, 2021 Coffey Road, Columbus, OH 43210, United States of America
| | - Shane C McKenzie
- Max McGraw Wildlife Foundation, 14N322 IL-25, Dundee Township, IL 60118, United States of America
| | - Randall S Singer
- Department of Veterinary and Biomedical Sciences, University of Minnesota, 1971 Commonwealth Avenue, Saint Paul, MN 55108, United States of America
| | - Timothy J Johnson
- Department of Veterinary and Biomedical Sciences, University of Minnesota, 1971 Commonwealth Avenue, Saint Paul, MN 55108, United States of America
| | - Meggan E Craft
- Department of Veterinary Population Medicine, University of Minnesota, 1988 Fitch Avenue, Saint Paul, MN 55108, United States of America; Department of Ecology, Evolution and Behavior, University of Minnesota, 1479 Gortner Avenue, Saint Paul, MN 55108, United States of America
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11
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Jahan NA, Lindsey LL, Larsen PA. The Role of Peridomestic Rodents as Reservoirs for Zoonotic Foodborne Pathogens. Vector Borne Zoonotic Dis 2021; 21:133-148. [PMID: 33351736 DOI: 10.1089/vbz.2020.2640] [Citation(s) in RCA: 22] [Impact Index Per Article: 5.5] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 01/05/2023] Open
Abstract
Although rodents are well-known reservoirs and vectors for a number of zoonoses, the functional role that peridomestic rodents serve in the amplification and transmission of foodborne pathogens is likely underappreciated. Clear links have been identified between commensal rodents and outbreaks of foodborne pathogens throughout Europe and Asia; however, comparatively little research has been devoted to studying this relationship in the United States. In particular, regional studies focused on specific rodent species and their foodborne pathogen reservoir status across the diverse agricultural landscapes of the United States are lacking. We posit that both native and invasive species of rodents associated with food-production pipelines are likely sources of seasonal outbreaks of foodborne pathogens throughout the United States. In this study, we review the evidence that identifies peridomestic rodents as reservoirs for foodborne pathogens, and we call for novel research focused on the metagenomic communities residing at the rodent-agriculture interface. Such data will likely result in the identification of new reservoirs for foodborne pathogens and species-specific demographic traits that might underlie seasonal enteric disease outbreaks. Moreover, we anticipate that a One Health metagenomic research approach will result in the discovery of new strains of zoonotic pathogens circulating in peridomestic rodents. Data resulting from such research efforts would directly inform and improve upon biosecurity efforts, ultimately serving to protect our food supply.
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Affiliation(s)
- Nusrat A Jahan
- Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota, USA
| | - Laramie L Lindsey
- Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota, USA
| | - Peter A Larsen
- Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota, USA
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12
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Vogt NA, Pearl DL, Taboada EN, Mutschall SK, Bondo KJ, Jardine CM. Epidemiology of Campylobacter jejuni in raccoons (Procyon lotor) on swine farms and in conservation areas in southern Ontario. Zoonoses Public Health 2020; 68:19-28. [PMID: 33226196 DOI: 10.1111/zph.12786] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/11/2020] [Revised: 09/02/2020] [Accepted: 10/21/2020] [Indexed: 11/30/2022]
Abstract
Campylobacter is a leading cause of foodborne illness in humans worldwide. Sources of infection are often difficult to identify, and are, generally, poorly understood. Recent work suggests that wildlife may represent a source of Campylobacter for human infections. Using a repeated cross-sectional study design, raccoons were trapped on five swine farms and five conservation areas in southern Ontario from 2011 to 2013. Our objectives were to: (a) assess the impact of seasonal, climatic, location, annual and raccoon demographic factors on the occurrence of Campylobacter jejuni in these animals; and (b) identify clusters of C. jejuni in space, time and space-time using spatial scan statistics. Multi-level multivariable logistic regression was used to examine the odds of isolating C. jejuni, with site and animal modelled as random intercepts. The following independent variables were examined: raccoon age and sex, year, location type, season, temperature and rainfall. A total of 1,096 samples were obtained from 627 raccoons; 46.3% were positive for C. jejuni. The following interactions and their main effects were significant (p < .05) and retained in the final model: season × temperature, year × rainfall, year × temperature. Based on the results from our multivariable model and spatial scan statistics, climatic variables (i.e. rainfall, temperature and season) were associated with the carriage of C. jejuni by raccoons, but the effects were not consistent, and varied by location and year. Although raccoons may pose a zoonotic risk due to their carriage of Campylobacter, further work is required to characterize the transmission and movement of this microorganism within the ecosystem.
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Affiliation(s)
- Nadine A Vogt
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada
| | - David L Pearl
- Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada
| | - Eduardo N Taboada
- National Microbiology Laboratory, Public Health Agency of Canada, Winnipeg, MB, Canada
| | - Steven K Mutschall
- National Centre for Animal Diseases, Canadian Food Inspection Agency, Lethbridge, AB, Canada
| | - Kristin J Bondo
- Department of Natural Resources Management, Texas Tech University, Lubbock, TX, USA
| | - Claire M Jardine
- Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, ON, Canada.,Canadian Wildlife Health Cooperative, University of Guelph, Guelph, ON, Canada
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13
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Worsley-Tonks KEL, Miller EA, Gehrt SD, McKenzie SC, Travis DA, Johnson TJ, Craft ME. Characterization of antimicrobial resistance genes in Enterobacteriaceae carried by suburban mesocarnivores and locally owned and stray dogs. Zoonoses Public Health 2020; 67:460-466. [PMID: 32034890 DOI: 10.1111/zph.12691] [Citation(s) in RCA: 6] [Impact Index Per Article: 1.2] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/07/2019] [Revised: 12/16/2019] [Accepted: 01/08/2020] [Indexed: 11/28/2022]
Abstract
The role of wildlife in the dissemination of antimicrobial-resistant bacteria and antimicrobial resistance genes (ARGs) in the environment is of increasing concern. We investigated the occurrence, richness and transmissibility potential of ARGs detected in the faeces of three mesocarnivore species: the coyote (Canis latrans), raccoon (Procyon lotor) and Virginia opossum (Didelphis virginiana), and of stray and owned dogs in suburban Chicago, IL, USA. Rectal swabs were collected from live-captured coyotes (n = 32), raccoons (n = 31) and Virginia opossums (n = 22). Fresh faecal samples were collected from locally owned (n = 13) and stray dogs (n = 18) and from the live-captured mesocarnivores, when available. Faecal samples and rectal swabs were enriched to select for Enterobacteriaceae and pooled by mesocarnivore species and dog type (owned or stray). Pooled enriched samples were then analysed for the presence of ARGs using shotgun sequencing. The three mesocarnivore and stray dog samples had twice as many unique ARGs compared to the owned dog sample, which was partly driven by a greater richness of beta-lactamase genes (genes conferring resistance to penicillins and cephalosporins). Raccoon and stray dog samples had the most ARGs in common, suggesting possible exposure to similar environmental sources of ARGs. In addition to identifying clinically relevant ARGs (e.g. blaCMY and qnrB), some ARGs were linked to the class 1 integrase gene, intI1, which may indicate anthropogenic origin. Findings from this pilot investigation suggest that the microbial communities of suburban mesocarnivores and stray dogs can host ARGs that can confer resistance to several antimicrobials used in human and veterinary medicine.
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Affiliation(s)
| | - Elizabeth A Miller
- Department of Veterinary and Biomedical Sciences, University of Minnesota, Falcon Heights, MN, USA
| | - Stanley D Gehrt
- School of Environment and Natural Resources, The Ohio State University, Columbus, OH, USA
| | | | - Dominic A Travis
- Department of Veterinary Population Medicine, University of Minnesota, Falcon Heights, MN, USA
| | - Timothy J Johnson
- Department of Veterinary and Biomedical Sciences, University of Minnesota, Falcon Heights, MN, USA
| | - Meggan E Craft
- Department of Veterinary Population Medicine, University of Minnesota, Falcon Heights, MN, USA
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14
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Abstract
Clostridium (Clostridioides) difficile is a gram-positive, spore-forming bacterium that is an important cause of disease in people, a variably important cause of disease in some animal species, and an apparently harmless commensal in others. Regardless of whether it is a known pathogen in a particular species, it can also be found in healthy individuals, sometimes at high prevalences and typically with higher rates of carriage in young individuals. As it is investigated in more animal species, it is apparent that this bacterium is widely disseminated in a diverse range of domestic and wild animal species. Although it can be found in most species in which investigations have been performed, there are pronounced intra- and inter-species differences in prevalence and clinical relevance. A wide range of strains can be identified, some that appear to be animal associated and others that are found in humans and animals. A large percentage of strains that cause disease in people can at least sporadically be found in animals. It is a potentially important zoonotic pathogen, but there is limited direct evidence of animal-human transmission. Although C. difficile has been studied extensively over the past few decades, it remains an enigmatic organism in many ways.
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Affiliation(s)
- J Scott Weese
- Department of Pathobiology and Centre for Public Health and Zoonoses, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada (Weese)
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15
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Arora J, Oudit D, Austin JW, Ramaswamy HS. Evaluation of thermal destruction kinetics of
Clostridium difficile
spores (ATCC 17857) in lean ground beef with first‐order/Weibull modeling considerations. J FOOD PROCESS ENG 2019. [DOI: 10.1111/jfpe.13273] [Citation(s) in RCA: 1] [Impact Index Per Article: 0.2] [Reference Citation Analysis] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 02/04/2023]
Affiliation(s)
- Jay Arora
- Department of Food Science and Agricultural ChemistryMcGill University Montreal Quebec Canada
| | - Denise Oudit
- Bureau of Microbial Hazards, Food Directorate, Health Canada Ottawa Ontario Canada
| | - John W. Austin
- Bureau of Microbial Hazards, Food Directorate, Health Canada Ottawa Ontario Canada
| | - Hosahalli S. Ramaswamy
- Department of Food Science and Agricultural ChemistryMcGill University Montreal Quebec Canada
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