Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, Canada
Antimicrobial resistance can be effectively limited by improving the judicious use of antimicrobials in food production. However, its effect on the spread of AMR genes in animal populations is not well described. In the province of Québec, Canada, a new legislation implemented in 2019 has led to an...
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| Format: | Article |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1304678/full |
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| author | Maud de Lagarde Maud de Lagarde John Morris Fairbrother John Morris Fairbrother John Morris Fairbrother Marie Archambault Marie Archambault Marie Archambault Simon Dufour Simon Dufour David Francoz David Francoz Jonathan Massé Jonathan Massé Hélène Lardé Hélène Lardé Hélène Lardé Cécile Aenishaenslin Cécile Aenishaenslin Cécile Aenishaenslin Marie-Eve Paradis Yves Terrat Jean-Philippe Roy Jean-Philippe Roy |
| author_facet | Maud de Lagarde Maud de Lagarde John Morris Fairbrother John Morris Fairbrother John Morris Fairbrother Marie Archambault Marie Archambault Marie Archambault Simon Dufour Simon Dufour David Francoz David Francoz Jonathan Massé Jonathan Massé Hélène Lardé Hélène Lardé Hélène Lardé Cécile Aenishaenslin Cécile Aenishaenslin Cécile Aenishaenslin Marie-Eve Paradis Yves Terrat Jean-Philippe Roy Jean-Philippe Roy |
| author_sort | Maud de Lagarde |
| collection | DOAJ |
| description | Antimicrobial resistance can be effectively limited by improving the judicious use of antimicrobials in food production. However, its effect on the spread of AMR genes in animal populations is not well described. In the province of Québec, Canada, a new legislation implemented in 2019 has led to an unprecedented reduction in the use of critical antimicrobials in dairy production. We aimed to investigate the potential link between ESBL/AmpC E. coli isolated before and after legislation and to determine the presence of plasmids carrying genes responsible for critical AMR. We collected fecal samples from calves, cows, and manure pit from 87 Québec dairy farms approximately 2 years before and 2 years after the legislation came into effect. The whole genomes of 183 presumptive ESBL/AmpC E. coli isolated after cefotaxime enrichment were sequenced. Their phylogenetic characteristics (MLST, serogroup, cgMLST) and the presence of virulence and resistance genes and replicons were examined. A maximum likelihood phylogenetic tree was constructed based on single nucleotide polymorphism (SNPs). We identified 10 clonal lineages (same cgMLST) and 7 clones (SNPs ≤ 52). Isolates belonging to these clones could be found on different farms before and after the legislation, strongly suggesting a clonal spread of AMR genes in the population during this 4-year period. All isolates were multidrug resistant (MDR), with clone 2 being notable for the presence of macrolide, fluoroquinolone, and third-generation cephalosporin resistance genes. We also identified clinically relevant ExPEC (ST10) and APEC-like lineages (ST117, ST58, ST88) associated with the presence of ExPEC and APEC virulence genes, respectively. Our data also suggests the presence of one epidemic plasmid belonging to the IncY incompatibility group and carrying qnrs1 and blaCTX–M–15. We demonstrated that AMR genes spread through farms and can persist over a 4-year period in the dairy cattle population through both plasmids and E. coli clones, despite the restriction of critical antimicrobial use. MDR ExPEC and APEC-like STs are present in the normal microbiota of cattle (more frequently in calves). These data increase our knowledge on gene dissemination dynamics and highlight the fact that biosecurity measures should be enhanced in this industry to limit such dissemination. |
| first_indexed | 2024-03-08T13:19:07Z |
| format | Article |
| id | doaj.art-e70abde5fbe24ca4a46e966fc270364f |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-08T13:19:07Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-e70abde5fbe24ca4a46e966fc270364f2024-01-18T04:23:52ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-01-011410.3389/fmicb.2023.13046781304678Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, CanadaMaud de Lagarde0Maud de Lagarde1John Morris Fairbrother2John Morris Fairbrother3John Morris Fairbrother4Marie Archambault5Marie Archambault6Marie Archambault7Simon Dufour8Simon Dufour9David Francoz10David Francoz11Jonathan Massé12Jonathan Massé13Hélène Lardé14Hélène Lardé15Hélène Lardé16Cécile Aenishaenslin17Cécile Aenishaenslin18Cécile Aenishaenslin19Marie-Eve Paradis20Yves Terrat21Jean-Philippe Roy22Jean-Philippe Roy23Department of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaRegroupement Front de Recherche du Québec – Nature et Technologie (FRQNT) Op+lait, Saint-Hyacinthe, QC, CanadaWorld Organization of Animal Health Reference Laboratory for Escherichia coli, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaSwine and Poultry Infectious Diseases Research Center (CRIPA-FQRNT), Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaDepartment of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaRegroupement Front de Recherche du Québec – Nature et Technologie (FRQNT) Op+lait, Saint-Hyacinthe, QC, CanadaSwine and Poultry Infectious Diseases Research Center (CRIPA-FQRNT), Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaDepartment of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaRegroupement Front de Recherche du Québec – Nature et Technologie (FRQNT) Op+lait, Saint-Hyacinthe, QC, CanadaDepartment of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaDepartment of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaRegroupement Front de Recherche du Québec – Nature et Technologie (FRQNT) Op+lait, Saint-Hyacinthe, QC, CanadaRegroupement Front de Recherche du Québec – Nature et Technologie (FRQNT) Op+lait, Saint-Hyacinthe, QC, CanadaDepartment of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaDepartment of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaRegroupement Front de Recherche du Québec – Nature et Technologie (FRQNT) Op+lait, Saint-Hyacinthe, QC, CanadaDepartment of Clinical Sciences, Ross University School of Veterinary Medicine, St. Kitts, St. Kitts and NevisDepartment of Pathology and Microbiology, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaGroupe de Recherche en Épidémiologie des Zoonoses et Santé Publique, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, QC, CanadaCentre de recherche en santé publique de l’Université de Montréal et du Centre Intégré Universitaire de Santé et de Service Sociaux (CIUSSS) du Centre-Sud-de-l’Île-de-Montréal, Montréal, QC, CanadaAssociation des médecins vétérinaires praticiens du Québec, Saint-Hyacinthe, QC, Canada0Consortium Santé Numérique de l’Université de Montréal, Montréal, QC, CanadaDepartment of Clinical Sciences, Faculty of Veterinary Medicine, Université de Montréal, Saint-Hyacinthe, QC, CanadaRegroupement Front de Recherche du Québec – Nature et Technologie (FRQNT) Op+lait, Saint-Hyacinthe, QC, CanadaAntimicrobial resistance can be effectively limited by improving the judicious use of antimicrobials in food production. However, its effect on the spread of AMR genes in animal populations is not well described. In the province of Québec, Canada, a new legislation implemented in 2019 has led to an unprecedented reduction in the use of critical antimicrobials in dairy production. We aimed to investigate the potential link between ESBL/AmpC E. coli isolated before and after legislation and to determine the presence of plasmids carrying genes responsible for critical AMR. We collected fecal samples from calves, cows, and manure pit from 87 Québec dairy farms approximately 2 years before and 2 years after the legislation came into effect. The whole genomes of 183 presumptive ESBL/AmpC E. coli isolated after cefotaxime enrichment were sequenced. Their phylogenetic characteristics (MLST, serogroup, cgMLST) and the presence of virulence and resistance genes and replicons were examined. A maximum likelihood phylogenetic tree was constructed based on single nucleotide polymorphism (SNPs). We identified 10 clonal lineages (same cgMLST) and 7 clones (SNPs ≤ 52). Isolates belonging to these clones could be found on different farms before and after the legislation, strongly suggesting a clonal spread of AMR genes in the population during this 4-year period. All isolates were multidrug resistant (MDR), with clone 2 being notable for the presence of macrolide, fluoroquinolone, and third-generation cephalosporin resistance genes. We also identified clinically relevant ExPEC (ST10) and APEC-like lineages (ST117, ST58, ST88) associated with the presence of ExPEC and APEC virulence genes, respectively. Our data also suggests the presence of one epidemic plasmid belonging to the IncY incompatibility group and carrying qnrs1 and blaCTX–M–15. We demonstrated that AMR genes spread through farms and can persist over a 4-year period in the dairy cattle population through both plasmids and E. coli clones, despite the restriction of critical antimicrobial use. MDR ExPEC and APEC-like STs are present in the normal microbiota of cattle (more frequently in calves). These data increase our knowledge on gene dissemination dynamics and highlight the fact that biosecurity measures should be enhanced in this industry to limit such dissemination.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1304678/fullEscherichia coligene spreadmanure pitlegislationcalf |
| spellingShingle | Maud de Lagarde Maud de Lagarde John Morris Fairbrother John Morris Fairbrother John Morris Fairbrother Marie Archambault Marie Archambault Marie Archambault Simon Dufour Simon Dufour David Francoz David Francoz Jonathan Massé Jonathan Massé Hélène Lardé Hélène Lardé Hélène Lardé Cécile Aenishaenslin Cécile Aenishaenslin Cécile Aenishaenslin Marie-Eve Paradis Yves Terrat Jean-Philippe Roy Jean-Philippe Roy Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, Canada Frontiers in Microbiology Escherichia coli gene spread manure pit legislation calf |
| title | Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, Canada |
| title_full | Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, Canada |
| title_fullStr | Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, Canada |
| title_full_unstemmed | Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, Canada |
| title_short | Clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant ExPEC and APEC-like lineages (ST) in the dairy cattle population of Québec, Canada |
| title_sort | clonal and plasmidic dissemination of critical antimicrobial resistance genes through clinically relevant expec and apec like lineages st in the dairy cattle population of quebec canada |
| topic | Escherichia coli gene spread manure pit legislation calf |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1304678/full |
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