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. 2025 Jan 9:20:100971.
doi: 10.1016/j.onehlt.2025.100971. eCollection 2025 Jun.

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

Adrien Biguenet  1   2 , Benoit Valot  1   3 , Farid El Garch  4   5 , Xavier Bertrand  1   2 , Didier Hocquet  1   2   3 ; ComPath Study Group
Affiliations

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

Adrien Biguenet et al. One Health. .

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) 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 bla CTX-M-15 gene was more frequent in humans (49.24 %) than in companion animals (17.9 %) (p < 0.001). The resistance genes bla CMY-2 (30.8 %) and bla CTX-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.

Keywords: Companion animal; ESBL; Escherichia coli; Human; Infection; WGS.

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Conflict of interest statement

The Compath group reports financial support was provided by Bayer Animal Health GmbH. The Compath group reports financial support was provided by Boehringer Ingelheim Animal Health. The Compath group reports financial support was provided by Ceva Santé Animale. The Compath group reports was provided by Elanco Animal Health. The Compath group reports financial support was provided by Fatro. The Compath group reports financial support was provided by MSD Animal Health. The Compath group reports financial support was provided by Vétoquinol France. The Compath group reports financial support was provided by Virbac. The Compath group reports financial support was provided by Zoetis. Farid El Garch reports a relationship with Vétoquinol France that includes: employment. If there are other authors, they declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

Fig. 1
Fig. 1
European map of 3GC-R E. coli genomes included in the study by country. The European continent is divided into Northern region (yellow), Southern region (pink), and Eastern region (blue). Red and green rectangles give the number of 3GC-R E. coli genomes retrieved from human and animal infections, respectively, in each country. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 2
Fig. 2
Comparison of the diversity of the sequence type of E. coli genome population from human (n = 1218) and animal (n = 109) infections. (A) E. coli alpha diversity of animal origin (green) and human origin (red). (B) Beta diversity by principal coordinate analysis using a Hellinger-transformed distance matrix. SD: inverse of Simpson diversity; SE: exponential of Shannon entropy; SR: Species richness. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 3
Fig. 3
Comparison of the diversity of 3GC-R genes from human (n = 1218) and animal (n = 109) E. coli. (A) E. coli alpha diversity of animal origin (green) and human origin (red). (B) Beta diversity by principal coordinate analysis using a Hellinger-transformed distance matrix. SD: inverse of Simpson diversity; SE: exponential of Shannon entropy; SR: Species richness. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
Fig. 4
Fig. 4
Phylogenetic tree of 545 E. coli ST131 strains included in this study. The tree was generated with a Bayesian approach using the HKY85 + G model and rooted with the genome of a ST73 E. coli strain (BioSample SAMEA104060572). In the inner circle, genomes of isolates retrieved from animals and human are indicated in green and red, respectively. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)
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