Fifty years of chicken-source Salmonella in China: Evolutionary shifts in epidemiology, antimicrobial resistance, and genomic lineages.

Abstract

Salmonella, as a profound foodborne zoonotic pathogen, not only causes acute and chronic disorders in poultry but can also be transmitted to humans through the food chain, posing a serious threat to public health security. With the extensive use of antimicrobial agents, the issue of Salmonella drug resistance has become increasingly prominent, and the emergence of multidrug-resistant strains has brought greater challenges to clinical treatment and disease control. Therefore, an in-depth investigation into the epidemiological characteristics of Salmonella across different periods and the evolutionary patterns of drug resistance is of great significance for guiding clinical medication and disease prevention and control. In this study, a total of 521 Salmonella isolates were collected from chickens in 22 provinces/city in China across three time periods-pre-2000, 2001-2010, and 2011-2020 (1971-2020). Serotyping, antimicrobial susceptibility testing, and whole-genome sequencing (WGS) were employed to analyze their spatiotemporal dynamics and genetic evolutionary relationships. The results showed that 20 Salmonella serotypes were identified, among which S. Enteritidis (39.5%) and S. Gallinarum (28.7%) were the predominant serotypes. The distribution of Salmonella serotypes exhibited significant dynamic variation over time, shifting from S. Gallinarum dominance in the early period to S. Enteritidis predominance and the coexistence of multiple serotypes in later years. Antimicrobial susceptibility testing revealed that both phenotypic and genotypic resistance of the strains to most antimicrobial agents increased over time. Before 2000, only a few strains exhibited resistance to colistin and ceftiofur, and no related resistance genes were detected. During 2001-2010, the resistance spectrum expanded significantly, with significant increases (P < 0.001) in resistance rates to sulfisoxazole (32.9%), ampicillin (37.1%), colistin (50.5%), and tetracycline (11.3%), and the average number of resistance genes carried by isolates increased approximately 13.38-fold compared with those before 2000. From 2011-2020, Salmonella exhibited a further increase of about 20% in resistance to most antimicrobials, and the number of resistance genes increased 3.8-fold relative to the previous period. Multilocus sequence typing (MLST) identified a total of 26 sequence types (STs). Except for S. Enteritidis, S. Gallinarum, and S. Typhimurium, which were associated with multiple STs, the remaining ST types correspond to only one serotype. Phylogenetic analysis revealed that the Salmonella could be classified into 24 clonal groups, with the strains within each group belonging to the same serotype but originating from different study periods. This indicates that key clonal strains have persisted and disseminated over time. This study systematically reveals, for the first time, the spatiotemporal evolution and genetic characteristics of chicken-derived Salmonella in China over the past 50 years. From a genomic perspective, it elucidates the dynamic patterns of resistance gene carriage and serotype diversification, providing a theoretical basis for understanding the transmission pathways of antibiotic resistance in Salmonella and a scientific foundation for developing precise control strategies.