From farm to fork: Transmission dynamics of carbapenem-resistant Enterobacterales in broiler production chain and implications for public health.

Abstract

Carbapenem-resistant Enterobacterales (CRE) represent a critical global health threat. Despite regulatory prohibitions of carbapenems in animals, the emergence of CRE in food animals continues to rise. This study systematically investigates the prevalence, sources, transmission dynamics, and public health implications of CRE in the broiler production chain through longitudinal farm monitoring and a nationwide survey. We conducted comprehensive sampling across three conventional floor-rearing broiler farms including vacancy and raising periods, their upstream breeder farm and hatcheries, and downstream abattoirs and retail markets. A total of 7372 samples were collected for CRE screening, with 861 representative CRE undergoing whole-genome sequencing and genomic analysis. CRE prevalence increased along the production chain, with rates of 10.8 % in the upstream facilities, 43.4 % at the broiler farms, and 61.6 % at the post-harvest stages. Notably, CRE persisting in the farm environment during vacancy period could rapidly colonize the intestines of chicks. Hatcheries were also identified as sources of CRE in broiler farms, with chicks and transport equipment acting as key transmission vectors. CRE transmission from broiler farms to retail meat was observed. Moreover, a national survey across 11 Chinese provinces, with 6289 samples collected from 115 poultry facilities, confirmed widespread contamination of broiler farms (93.5 %), breeder farms (88.5 %), hatcheries (56.7 %), and layer farms (46.2 %). Our findings identify hatcheries and contaminated farm environments as primary CRE sources in broiler farms, and provide direct genomic evidence of CRE transmission from farms to fork, underscoring the urgent need for enhanced hygiene and biosecurity under One Health frameworks to mitigate the spread of antimicrobial resistance and reduce potential public health risks.