Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in Europe

In high-income countries, dogs and cats are often considered members of the family. Because of this proximity, it has been suggested that pets and humans might exchange bacterial species from their gut microbiota, with multidrug resistant bacteria being of particular concern. The aim of this study w...

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Main Authors: Adrien Biguenet, Benoit Valot, Farid El Garch, Xavier Bertrand, Didier Hocquet
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:One Health
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Online Access:http://www.sciencedirect.com/science/article/pii/S2352771425000072
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author Adrien Biguenet
Benoit Valot
Farid El Garch
Xavier Bertrand
Didier Hocquet
author_facet Adrien Biguenet
Benoit Valot
Farid El Garch
Xavier Bertrand
Didier Hocquet
author_sort Adrien Biguenet
collection DOAJ
description In high-income countries, dogs and cats are often considered members of the family. Because of this proximity, it has been suggested that pets and humans might exchange bacterial species from their gut microbiota, with multidrug resistant bacteria being of particular concern. The aim of this study was to compare the genomes of third-generation cephalosporin-resistant (3GC-R) Escherichia coli responsible for human and pet infections in Europe.Whole-genome sequencing data from 3GC-R E. coli isolated from clinical samples of humans, dogs and cats, and published in eight European studies were re-analyzed using bioinformatics tools. The acquired genes responsible for 3GC-R were identified. The sequence type (ST) of all genomes were assessed by multilocus sequence typing. Alpha and beta diversities were measured within and between the two populations.We included genomes of 1327 3GC-R E. coli isolated from humans and animals with 109 (8.2 %) being responsible for infections in dogs and cat, and 1218 (91.8 %) responsible for human infections. Alpha diversity analysis suggested greater diversity within ST and 3GC-R genes in the animal population. Beta diversity analysis by principal coordinate analysis separated animal and human strains. ST131 was more abundant in human strains (43.4 %) than in animal strains (14.7 %) (p < 0.001). Six STs, including ST372, were identified almost exclusively in 3GC-R E. coli from animal origin. The blaCTX-M-15 gene was more frequent in humans (49.24 %) than in companion animals (17.9 %) (p < 0.001). The resistance genes blaCMY-2 (30.8 %) and blaCTX-M-1 (15.4 %) were more frequent in E. coli isolated from pets (p < 0.001).We found that populations of 3GC-R E. coli responsible for human and pet infections in Europe do not overlap. Although it cannot rule out occasional transmission of bacteria between pets and humans within a household, it suggests that dogs and cats are not a major source of human infection with this antibiotic-resistant pathogen.
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spelling doaj-art-91f9468c9fb8402bb389fcce59de42db2025-01-18T05:04:48ZengElsevierOne Health2352-77142025-06-0120100971Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in EuropeAdrien Biguenet0Benoit Valot1Farid El Garch2Xavier Bertrand3Didier Hocquet4Université de Franche-Comté, UMR-CNRS 6249 Chrono-Environnement, F-25000 Besançon, France; CHU de Besançon, Hygiène Hospitalière, F-25000 Besançon, France; Corresponding author at: Université de Franche-Comté, UMR-CNRS 6249 Chrono-Environnement, F-25000 Besançon, France.Université de Franche-Comté, UMR-CNRS 6249 Chrono-Environnement, F-25000 Besançon, France; Université de Franche-Comté, UFR Santé, CHU de Besançon, Bioinformatique et Big Data Au Service de La Santé, F-25000 Besançon, FranceComPath Study Group, Bruxelles, Belgium; Vétoquinol SA, Scientific Division, Lure, FranceUniversité de Franche-Comté, UMR-CNRS 6249 Chrono-Environnement, F-25000 Besançon, France; CHU de Besançon, Hygiène Hospitalière, F-25000 Besançon, FranceUniversité de Franche-Comté, UMR-CNRS 6249 Chrono-Environnement, F-25000 Besançon, France; CHU de Besançon, Hygiène Hospitalière, F-25000 Besançon, France; Université de Franche-Comté, UFR Santé, CHU de Besançon, Bioinformatique et Big Data Au Service de La Santé, F-25000 Besançon, FranceIn high-income countries, dogs and cats are often considered members of the family. Because of this proximity, it has been suggested that pets and humans might exchange bacterial species from their gut microbiota, with multidrug resistant bacteria being of particular concern. The aim of this study was to compare the genomes of third-generation cephalosporin-resistant (3GC-R) Escherichia coli responsible for human and pet infections in Europe.Whole-genome sequencing data from 3GC-R E. coli isolated from clinical samples of humans, dogs and cats, and published in eight European studies were re-analyzed using bioinformatics tools. The acquired genes responsible for 3GC-R were identified. The sequence type (ST) of all genomes were assessed by multilocus sequence typing. Alpha and beta diversities were measured within and between the two populations.We included genomes of 1327 3GC-R E. coli isolated from humans and animals with 109 (8.2 %) being responsible for infections in dogs and cat, and 1218 (91.8 %) responsible for human infections. Alpha diversity analysis suggested greater diversity within ST and 3GC-R genes in the animal population. Beta diversity analysis by principal coordinate analysis separated animal and human strains. ST131 was more abundant in human strains (43.4 %) than in animal strains (14.7 %) (p < 0.001). Six STs, including ST372, were identified almost exclusively in 3GC-R E. coli from animal origin. The blaCTX-M-15 gene was more frequent in humans (49.24 %) than in companion animals (17.9 %) (p < 0.001). The resistance genes blaCMY-2 (30.8 %) and blaCTX-M-1 (15.4 %) were more frequent in E. coli isolated from pets (p < 0.001).We found that populations of 3GC-R E. coli responsible for human and pet infections in Europe do not overlap. Although it cannot rule out occasional transmission of bacteria between pets and humans within a household, it suggests that dogs and cats are not a major source of human infection with this antibiotic-resistant pathogen.http://www.sciencedirect.com/science/article/pii/S2352771425000072Companion animalESBLEscherichia coliHumanInfectionWGS
spellingShingle Adrien Biguenet
Benoit Valot
Farid El Garch
Xavier Bertrand
Didier Hocquet
Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in Europe
One Health
Companion animal
ESBL
Escherichia coli
Human
Infection
WGS
title Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in Europe
title_full Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in Europe
title_fullStr Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in Europe
title_full_unstemmed Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in Europe
title_short Genomic epidemiology of third-generation cephalosporin-resistant Escherichia coli from companion animals and human infections in Europe
title_sort genomic epidemiology of third generation cephalosporin resistant escherichia coli from companion animals and human infections in europe
topic Companion animal
ESBL
Escherichia coli
Human
Infection
WGS
url http://www.sciencedirect.com/science/article/pii/S2352771425000072
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