Core-genome typing links <i>Yersinia enterocolitica</i> isolated from pigs and cattle to human infections in France

ABSTRACT In Europe, enteric yersiniosis is mainly caused by Yersinia enterocolitica bioserotypes 4/O:3 and 2/O:9, typically associated with pigs and ruminants, respectively. We investigated the genetic relatedness of animal and human Y. enterocolitica isolates in France to assess cross-species transmission and persistence in the reservoirs. Pathogenic strains collected during prevalence studies conducted in 2022 on 303 pigs and 430 cattle at slaughter were characterized by core genome multi locus sequence typing and compared with contemporary clinical isolates and with animal and clinical isolates collected before 2012. We observed a 4.9% prevalence of pathogenic Y. enterocolitica in pigs and none in cattle. A total of 1,677 Y. enterocolitica isolates were analyzed, of which 73.3% belonged to lineage 4 (BT4/O:3) and 24.9% to lineage 2/3-9b (BT2/O:9). Genomic clustering revealed eight mixed pig-human clusters within lineage 4, including two that linked pre-2012 and 2022 isolates, demonstrating decade-long persistence of pig-derived strains in human infections. Two bovine-human clusters were identified within lineage 2/3-9b, despite the absence of pathogenic isolates in cattle at slaughter, suggesting non-meat-related transmission routes. Antimicrobial resistance screening revealed acquired genes conferring resistance to chloramphenicol (23%), aminoglycosides (26%), sulfonamides (24%), and tetracyclines (1%) in clinical isolates, but none in pig isolates. These findings indicate that BT4/O:3 strains circulating in pigs constitute a major and persistent source of human yersiniosis. Cattle-associated lineage 2/3-9b strains also affect humans, but with an unclear transmission route. The presence of multidrug-resistance genes in human-derived lineage 4 isolates underscores the need for continuous genomic surveillance within a One Health framework. IMPORTANCE This study documents the relationship between human and animal strains of Yersinia enterocolitica , highlighting the critical role of animals as the source of human enteric yersiniosis. By analyzing bacterial genomes from pigs, cattle, and humans collected over more than 10 years, we found that some Y. enterocolitica strains can persist in livestock and continue to cause human infections. Our findings emphasize that preventing food-borne disease in people requires monitoring and control of bacteria in animal populations. The work underscores the One Health approach, which recognizes that human, animal, and environmental health are closely linked, and that coordinated efforts across these areas are essential to reduce the spread of infections and protect public health.