Introduction Non-typhoidal Salmonella (NTS) is a significant bacterial pathogen causing foodborne diseases, with the potential for severe bloodstream infections (BSI) leading to complications such as sepsis and high mortality rates, particularly in vulnerable populations. The rise of BSI associated NTS strains, notably ST11 S. Enteritidis, has raised public health concerns. Objectives This study aimed to investigate the epidemiological and genetic characteristics of Salmonella BSI strains in China, focusing on the adaptation of ST11 S. Enteritidis from animal and food sources to clinical settings, and to analyze correlations between clinical data and genetic profiles. Methods A total of 120 non-duplicated NTS strains isolated from bacteremia patients across nine hospitals in China between 2017 and 2022 were investigated using antimicrobial susceptibility testing, whole-genome sequencing and bioinformatics analysis. Results The average annual prevalence of bloodstream infections (BSI) due to Salmonella remained stable at 0.77%, based on 31,177 positive blood cultures, with 96.8% of infections caused by NTS strains, primarily Salmonella enterica serovar Enteritidis (41.9%) and Typhimurium variants (16.1%). WGS results revealed significant genetic features, including mutations and multiple copies of the 5S rRNA gene, which were identified as key drivers for host adaptation and systemic dissemination, particularly in immunocompetent adults. Notably, 40% of foodborne strains carried these genetic traits, exhibiting a higher genomic potential for invasiveness compared to animal-derived strains within this specific dataset. Additionally, we demonstrated the resistance levels of BSI Salmonella to first-line antibiotics and identified a novel plasmid that mediates the co-transmission of cefotaxime resistance and virulence factors, complicating treatment options. These factors significantly contribute to the transition of diarrheagenic strains to types with an enhanced potential for bloodstream invasion. Conclusion These findings underscore the ongoing public health concern associated with NTS infections and highlight the need for continuous surveillance and effective intervention strategies to manage these emerging threats.
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