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      Antimicrobial resistance in Campylobacter jejuni and Campylobacter coli isolated from small poultry flocks in Ontario, Canada: A two-year surveillance study

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          Abstract

          Antimicrobial resistance in Campylobacter, common in poultry, is a global public health issue. The emergence and spread of antimicrobial resistant Campylobacter has been linked to the use of antimicrobials in food animals. Small poultry flocks are becoming increasingly popular not only as a source of food but also as pets, yet not all small flock owners are aware of proper antimicrobial use practices and safe food handling protocols. This trend could contribute to antimicrobial resistance. In order to determine the prevalence of antimicrobial resistance in Campylobacter in small poultry flocks, we analyzed data from birds that had been submitted to a diagnostic laboratory in Ontario between October 2015 and September 2017. A pooled cecal sample was obtained from each submission and cultured for Campylobacter jejuni and Campylobacter coli. Three isolates were recovered from each positive sample and tested for susceptibility to nine antimicrobials using a broth microdilution method. Overall, 176 isolates were recovered (141 chicken, 21 turkey, 6 duck, and 8 game bird). A high frequency of resistance to tetracycline was observed in the C. jejuni isolates from chickens (77%) and turkeys (100%), and in the C. coli isolates from turkeys (50%) and game birds (40%). Campylobacter jejuni isolates had higher odds of resistance to tetracycline (OR = 3.54, P ≤ 0.01) compared to C. coli isolates. Overall, there was a low frequency of resistance to quinolones and a very low frequency of resistance to macrolides. Multidrug resistance was uncommon. The high prevalence of tetracycline resistance emphasizes the importance of prudent antimicrobial use in small flocks. Although low, the presence of resistance to macrolides and quinolones, which are used to treat campylobacteriosis in humans, highlights the need for proper food safety and infection control practices by small flock owners to prevent exposure to antimicrobial resistant Campylobacter.

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          Mechanisms of resistance to macrolides and lincosamides: nature of the resistance elements and their clinical implications.

          Roland Leclercq (2002)
          Resistance to macrolides and lincosamides is increasingly reported in clinical isolates of gram-positive bacteria. The multiplicity of mechanisms of resistance, which include ribosomal modification, efflux of the antibiotic, and drug inactivation, results in a variety of phenotypes of resistance. There is controversy concerning the clinical relevance of in vitro macrolide resistance. Recent data, however, have shown that eradication of bacteria correlates with clinical outcome of acute otitis media in children and that macrolide therapy results in delayed eradication of macrolide-resistant pneumococci. These results support the need for in vitro detection of macrolide resistance and correct interpretation of susceptibility tests to guide therapy.
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            Antimicrobial drug use in food-producing animals and associated human health risks: what, and how strong, is the evidence?

            Karin Hoelzer, Nora Wong, Joe Thomas … (2017)
            Background Antimicrobial resistance is a public health threat. Because antimicrobial consumption in food-producing animals contributes to the problem, policies restricting the inappropriate or unnecessary agricultural use of antimicrobial drugs are important. However, this link between agricultural antibiotic use and antibiotic resistance has remained contested by some, with potentially disruptive effects on efforts to move towards the judicious or prudent use of these drugs. Main text The goal of this review is to systematically evaluate the types of evidence available for each step in the causal pathway from antimicrobial use on farms to human public health risk, and to evaluate the strength of evidence within a ‘Grades of Recommendations Assessment, Development and Evaluation‘(GRADE) framework. The review clearly demonstrates that there is compelling scientific evidence available to support each step in the causal pathway, from antimicrobial use on farms to a public health burden caused by infections with resistant pathogens. Importantly, the pathogen, antimicrobial drug and treatment regimen, and general setting (e.g., feed type) can have significant impacts on how quickly resistance emerges or spreads, for how long resistance may persist after antimicrobial exposures cease, and what public health impacts may be associated with antimicrobial use on farms. Therefore an exact quantification of the public health burden attributable to antimicrobial drug use in animal agriculture compared to other sources remains challenging. Conclusions Even though more research is needed to close existing data gaps, obtain a better understanding of how antimicrobial drugs are actually used on farms or feedlots, and quantify the risk associated with antimicrobial use in animal agriculture, these findings reinforce the need to act now and restrict antibiotic use in animal agriculture to those instances necessary to ensure the health and well-being of the animals.
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              Enhanced in vivo fitness of fluoroquinolone-resistant Campylobacter jejuni in the absence of antibiotic selection pressure.

              Naidan Luo, Sônia Pereira, Orhan Sahin … (2005)
              Campylobacter jejuni, a major foodborne human pathogen, has become increasingly resistant to fluoroquinolone (FQ) antimicrobials. By using clonally related isolates and genetically defined mutants, we determined the fitness of FQ-resistant Campylobacter in chicken (a natural host and a major reservoir for C. jejuni) in the absence of antibiotic selection pressure. When monoinoculated into the host, FQ-resistant and FQ-susceptible Campylobacter displayed similar levels of colonization and persistence in the absence of FQ antimicrobials. The prolonged colonization in chickens did not result in loss of the FQ resistance and the resistance-conferring point mutation (C257 --> T) in the gyrA gene. Strikingly, when coinoculated into chickens, the FQ-resistant Campylobacter isolates outcompeted the majority of the FQ-susceptible strains, indicating that the resistant Campylobacter was biologically fit in the chicken host. The fitness advantage was not due to compensatory mutations in the genes targeted by FQ and was linked directly to the single point mutation in gyrA, which confers on Campylobacter a high-level resistance to FQ antimicrobials. In certain genetic backgrounds, the same point mutation entailed a biological cost on Campylobacter, as evidenced by its inability to compete with the FQ-susceptible Campylobacter. These findings provide a previously undescribed demonstration of the profound effect of a resistance-conferring point mutation in gyrA on the fitness of a major foodborne pathogen in its natural host and suggest that the rapid emergence of FQ-resistant Campylobacter on a worldwide scale may be attributable partly to the enhanced fitness of the FQ-resistant isolates.
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                Author and article information

                Contributors
                Csaba Varga:
                ORCID: http://orcid.org/0000-0003-2751-3677
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Michele T. Guerin: Role: ConceptualizationRole: Data curationRole: InvestigationRole: Methodology
                Marina L. Brash: Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Resources
                Durda Slavic: Role: Project administrationRole: Resources
                Patrick Boerlin: Role: InvestigationRole: Methodology
                Leonardo Susta: Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Resources
                Iddya Karunasagar: Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, CA USA )
                ISSN (Electronic): 1932-6203
                Publication date (Electronic): 29 August 2019
                Publication date Collection: 2019
                Volume: 14
                Issue: 8
                Electronic Location Identifier: e0221429
                Affiliations
                [1 ] Ontario Ministry of Agriculture, Food and Rural Affairs, Guelph, Ontario, Canada
                [2 ] Department of Population Medicine, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
                [3 ] Animal Health Laboratory, University of Guelph, Guelph, Ontario, Canada
                [4 ] Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada
                Nitte University, INDIA
                Author notes

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

                Author information
                http://orcid.org/0000-0003-2751-3677
                Article
                Publisher ID: PONE-D-19-16109
                DOI: 10.1371/journal.pone.0221429
                PMC ID: 6715200
                PubMed ID: 31465474
                SO-VID: c3d8a7e6-07fa-4dfc-b370-1ce453ee83cd
                Copyright © © 2019 Varga et al
                License:

                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
                Date received : 6 June 2019
                Date accepted : 6 August 2019
                Page count
                Figures: 4, Tables: 4, Pages: 14
                Funding
                Funded by: Ministry of Agriculture, Food and Rural Affairs (KR)
                Award ID: UofG 2015-2282
                Award Recipient :
                Funded by: Ontario Agri-Food Innovation Alliance, under the Disease Surveillance Plan
                Award ID: xx
                Award Recipient :
                ORCID: http://orcid.org/0000-0003-2751-3677
                The surveillance project led by Dr. L. Susta, was funded by the OMAFRA-University of Guelph Strategic Partnership (grant UofG 2015-2282), under the Disease Surveillance Plan, which was a joint federal-provincial Growing Forward 2 project. The antimicrobial susceptibility testing project led by Dr. C. Varga, was funded by the Ontario Agri-Food Innovation Alliance, under the Disease Surveillance Plan (Project #: 009098).
                Categories
                Subject: Research Article
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Microbial Control
                Subject: Antimicrobial Resistance
                Subject: Medicine and Health Sciences
                Subject: Pharmacology
                Subject: Antimicrobial Resistance
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Campylobacter
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Poultry
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Fowl
                Subject: Gamefowl
                Subject: Chickens
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Poultry
                Subject: Chickens
                Subject: Medicine and Health Sciences
                Subject: Pharmacology
                Subject: Drugs
                Subject: Antimicrobials
                Subject: Antibiotics
                Subject: Tetracyclines
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Microbial Control
                Subject: Antimicrobials
                Subject: Antibiotics
                Subject: Tetracyclines
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Bacteria
                Subject: Campylobacter
                Subject: Campylobacter Jejuni
                Subject: Biology and Life Sciences
                Subject: Microbiology
                Subject: Medical Microbiology
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Campylobacter Jejuni
                Subject: Medicine and Health Sciences
                Subject: Pathology and Laboratory Medicine
                Subject: Pathogens
                Subject: Microbial Pathogens
                Subject: Bacterial Pathogens
                Subject: Campylobacter
                Subject: Campylobacter Jejuni
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Fowl
                Subject: Gamefowl
                Subject: Turkeys
                Subject: Biology and Life Sciences
                Subject: Organisms
                Subject: Eukaryota
                Subject: Animals
                Subject: Vertebrates
                Subject: Amniotes
                Subject: Birds
                Subject: Poultry
                Subject: Turkeys
                Custom metadata
                Data Availability All relevant data are within the manuscript.

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