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 was to compare the genomes of third-generation cephalosporin-resistant (3GC-R) <i>Escherichia coli</i> responsible for human and pet infections in Europe. Whole-genome sequencing data from 3GC-R <i>E. coli</i> 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 <i>E. coli</i> 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 %) (<i>p</i> < 0.001). Six STs, including ST372, were identified almost exclusively in 3GC-R <i>E. coli</i> from animal origin. The <i>bla</i> <sub>CTX-M-15</sub> gene was more frequent in humans (49.24 %) than in companion animals (17.9 %) (<i>p</i> < 0.001). The resistance genes <i>bla</i> <sub>CMY-2</sub> (30.8 %) and <i>bla</i> <sub>CTX-M-1</sub> (15.4 %) were more frequent in <i>E. coli</i> isolated from pets (p < 0.001). We found that populations of 3GC-R <i>E. coli</i> 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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Publication Details

Journal
One Health
Published
2025-01-09
DOI
https://doi.org/10.1016/j.onehlt.2025.100971
Citations
2
Primary Topic
Antibiotic Resistance in Bacteria
Type
article
Field-Weighted Citation Impact
1.18

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article

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

Benoı̂t Valot, Farid El Garch, Didier Hocquet, Adrien Biguenet et al.
2 citations
One Health
Antibiotic Resistance in Bacteria
1.18
article

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

Benoı̂t Valot, Farid El Garch, Didier Hocquet, Adrien Biguenet, Xavier Bertrand
article en
2 citations

Abstract

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) <i>Escherichia coli</i> responsible for human and pet infections in Europe. Whole-genome sequencing data from 3GC-R <i>E. coli</i> 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 <i>E. coli</i> 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 %) (<i>p</i> < 0.001). Six STs, including ST372, were identified almost exclusively in 3GC-R <i>E. coli</i> from animal origin. The <i>bla</i> <sub>CTX-M-15</sub> gene was more frequent in humans (49.24 %) than in companion animals (17.9 %) (<i>p</i> < 0.001). The resistance genes <i>bla</i> <sub>CMY-2</sub> (30.8 %) and <i>bla</i> <sub>CTX-M-1</sub> (15.4 %) were more frequent in <i>E. coli</i> isolated from pets (p < 0.001). We found that populations of 3GC-R <i>E. coli</i> 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.

One HealthVol. 20
Centre National de la Recherche Scientifique (FR), Centre Hospitalier Universitaire de Besançon (FR), Vétoquinol (Canada) (CA), Laboratoire Chrono-Environnement (FR), Université de Franche-Comté (FR)
Zoetis, Virbac, Elanco Animal Health, Bayer Animal Health
Good health and well-being
Openalex Percentile: Top 26%
Antibiotic Resistance in Bacteria
1.18
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