Genomic epidemiology reveals agricultural environments as direct conduits for multidrug-resistant Salmonella ST34 transmission into the food chain.

The dissemination of multidrug-resistant (MDR) Salmonella from agricultural environments into food systems constitutes a major safety hazard. This study combined genomic epidemiology and quantitative microbial risk assessment (QMRA) to investigate Salmonella transmission dynamics across urban and rural food environments in Jiangxi, China. Among 237 Salmonella isolates collected from Jiangxi Province, China (2015-2021), a distinct geospatial clonal stratification emerged: the highly resistant ST34 clone (72.4% MDR) dominated urban retail food and clinical sources, whereas the livestock-associated ST155 (31.2% MDR) predominated in rural areas. The expansion of ST34 (8.3% annual increase) was driven by a robust genetic architecture, exhibiting significantly higher resistance and virulence scores than other lineages. Crucially, genomic analysis provided strong evidence of direct transmission from pre-harvest environments, supported by minimal genetic distances (2-10 core genome single nucleotide polymorphisms) between ST34 isolates from agricultural wastewater and urban clinical cases, implicating the food supply chain as the primary vector. Furthermore, QMRA confirmed a profound geospatial disparity in foodborne infection risk, with rural populations facing a 139-fold higher median annual risk due to exposure to contaminated irrigation water used for fresh produce. These findings demonstrate that agricultural waste streams act as active conduits for high-risk MDR Salmonella entering the food chain, creating disproportionate regional health burdens. This study underscores the urgent need for targeted pre-harvest interventions, improved water management, and the implementation of integrated One Health surveillance systems to safeguard the microbiological safety of the food supply.