Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks
Antimicrobial resistance (AMR) in enteric bacteria continues to be detected in turkey flocks and retail products worldwide, including in Canada. However, studies assessing linkages between on-farm antimicrobial use (AMU) and the development of AMR are lacking. This study aims to identify AMU charact...
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Frontiers Media S.A.
2022-07-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.954123/full |
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| author | Rima D. Shrestha Agnes Agunos Sheryl P. Gow Anne E. Deckert Csaba Varga Csaba Varga |
| author_facet | Rima D. Shrestha Agnes Agunos Sheryl P. Gow Anne E. Deckert Csaba Varga Csaba Varga |
| author_sort | Rima D. Shrestha |
| collection | DOAJ |
| description | Antimicrobial resistance (AMR) in enteric bacteria continues to be detected in turkey flocks and retail products worldwide, including in Canada. However, studies assessing linkages between on-farm antimicrobial use (AMU) and the development of AMR are lacking. This study aims to identify AMU characteristics that impact the development of AMR in the indicator bacteria Escherichia coli in turkey flocks, building on the Canadian Integrated Program for Antimicrobial Resistance Surveillance methodology for farm-level AMU and AMR data integration. Two analytic approaches were used: (1) multivariable mixed-effects logistic regression models examined associations between AMU (any route, route-specific, and route-disease-specific indication) summarized as the number of defined daily doses in animals using Canadian standards ([nDDDvetCA]/1,000 kg-animal-days at risk) and AMR and (2) multivariable mixed-effects Poisson regression models studied the linkages between AMU and the number of classes to which an E. coli isolate was resistant (nCRE. coli). A total of 1,317 E. coli isolates from a network of 16 veterinarians and 334 turkey producers across the five major turkey-producing provinces in Canada between 2016 and 2019 were used. Analysis indicated that AMR emerged with the use of related antimicrobials (e.g., tetracycline use-tetracycline resistance), however, the use of unrelated antimicrobial classes was also impacting AMR (e.g., aminoglycosides/streptogramins use-tetracycline resistance). As for studying AMU-nCRE. coli linkages, the most robust association was between the parenteral aminoglycosides use and nCRE. coli, though in-feed uses of four unrelated classes (bacitracin, folate pathway inhibitors, streptogramins, and tetracyclines) appear to be important, indicating that ongoing uses of these classes may slow down the succession from multidrug-resistant to a more susceptible E. coli populations. The analysis of AMU (route and disease-specific)-AMR linkages complemented the above findings, suggesting that treatment of certain diseases (enteric, late-stage septicemic conditions, and colibacillosis) are influential in the development of resistance to certain antimicrobial classes. The highest variances were at the flock level indicating that stewardship actions should focus on flock-level infection prevention practices. This study added new insights to our understanding of AMU-AMR linkages in turkeys and is useful in informing AMU stewardship in the turkey sector. Enhanced surveillance using sequencing technologies are warranted to explain molecular-level determinants of AMR. |
| first_indexed | 2024-12-10T08:44:01Z |
| format | Article |
| id | doaj.art-6b0e47c462d54d6d8a776ba9be81fa24 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-10T08:44:01Z |
| publishDate | 2022-07-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-6b0e47c462d54d6d8a776ba9be81fa242022-12-22T01:55:47ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-07-011310.3389/fmicb.2022.954123954123Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocksRima D. Shrestha0Agnes Agunos1Sheryl P. Gow2Anne E. Deckert3Csaba Varga4Csaba Varga5Department of Pathobiology, College of Veterinary Medicine, University of Illinois Urbana-Champaign, Urbana, IL, United StatesCenter for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, ON, CanadaCenter for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Saskatoon, SK, CanadaCenter for Foodborne, Environmental and Zoonotic Infectious Diseases, Public Health Agency of Canada, Guelph, ON, CanadaDepartment of Pathobiology, College of Veterinary Medicine, University of Illinois Urbana-Champaign, Urbana, IL, United StatesCarl R. Woese Institute for Genomic Biology, University of Illinois Urbana-Champaign, Urbana, IL, United StatesAntimicrobial resistance (AMR) in enteric bacteria continues to be detected in turkey flocks and retail products worldwide, including in Canada. However, studies assessing linkages between on-farm antimicrobial use (AMU) and the development of AMR are lacking. This study aims to identify AMU characteristics that impact the development of AMR in the indicator bacteria Escherichia coli in turkey flocks, building on the Canadian Integrated Program for Antimicrobial Resistance Surveillance methodology for farm-level AMU and AMR data integration. Two analytic approaches were used: (1) multivariable mixed-effects logistic regression models examined associations between AMU (any route, route-specific, and route-disease-specific indication) summarized as the number of defined daily doses in animals using Canadian standards ([nDDDvetCA]/1,000 kg-animal-days at risk) and AMR and (2) multivariable mixed-effects Poisson regression models studied the linkages between AMU and the number of classes to which an E. coli isolate was resistant (nCRE. coli). A total of 1,317 E. coli isolates from a network of 16 veterinarians and 334 turkey producers across the five major turkey-producing provinces in Canada between 2016 and 2019 were used. Analysis indicated that AMR emerged with the use of related antimicrobials (e.g., tetracycline use-tetracycline resistance), however, the use of unrelated antimicrobial classes was also impacting AMR (e.g., aminoglycosides/streptogramins use-tetracycline resistance). As for studying AMU-nCRE. coli linkages, the most robust association was between the parenteral aminoglycosides use and nCRE. coli, though in-feed uses of four unrelated classes (bacitracin, folate pathway inhibitors, streptogramins, and tetracyclines) appear to be important, indicating that ongoing uses of these classes may slow down the succession from multidrug-resistant to a more susceptible E. coli populations. The analysis of AMU (route and disease-specific)-AMR linkages complemented the above findings, suggesting that treatment of certain diseases (enteric, late-stage septicemic conditions, and colibacillosis) are influential in the development of resistance to certain antimicrobial classes. The highest variances were at the flock level indicating that stewardship actions should focus on flock-level infection prevention practices. This study added new insights to our understanding of AMU-AMR linkages in turkeys and is useful in informing AMU stewardship in the turkey sector. Enhanced surveillance using sequencing technologies are warranted to explain molecular-level determinants of AMR.https://www.frontiersin.org/articles/10.3389/fmicb.2022.954123/fullantimicrobial resistanceantimicrobial useturkeyE. colifarm surveillanceCanada |
| spellingShingle | Rima D. Shrestha Agnes Agunos Sheryl P. Gow Anne E. Deckert Csaba Varga Csaba Varga Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks Frontiers in Microbiology antimicrobial resistance antimicrobial use turkey E. coli farm surveillance Canada |
| title | Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks |
| title_full | Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks |
| title_fullStr | Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks |
| title_full_unstemmed | Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks |
| title_short | Associations between antimicrobial resistance in fecal Escherichia coli isolates and antimicrobial use in Canadian turkey flocks |
| title_sort | associations between antimicrobial resistance in fecal escherichia coli isolates and antimicrobial use in canadian turkey flocks |
| topic | antimicrobial resistance antimicrobial use turkey E. coli farm surveillance Canada |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.954123/full |
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