Genomic epidemiology and antimicrobial resistance of non-typhoidal Salmonella in children in Hainan Province, China

Abstract

ABSTRACT Non-typhoidal Salmonella (NTS) is a major foodborne pathogen causing significant morbidity and mortality worldwide, particularly affecting children under 5 years of age. Despite its public health importance, systematic studies on NTS infection in children in Hainan Province, China, are limited. We performed a comprehensive retrospective analysis of 77 NTS isolates collected from children at the Hainan Women and Children’s Medical Center between April 2023 and May 2024. The study integrated antimicrobial susceptibility testing, whole-genome sequencing, and phylogenetic reconstruction to elucidate the molecular epidemiology and resistance of this pathogen. The invasive infection rate of NTS was 10.4% (8/77; 95% CI: 4.6%–19.4%). Children under 3 years were disproportionately affected (66/77, 85.7%), and infections peaked in summer and autumn. Sixteen serotypes and 16 sequence types (STs) were identified. The predominant serotypes were monophasic 1,4,[5],12:i:- (31/77, 40.3%), Typhimurium (12/77, 15.6%), and Stanley (9/77, 11.7%). Serotype was strongly associated with ST, with monophasic 1,4,[5],12:i:- (ST34) (40.3%) and Typhimurium (ST19) (15.6%) being the most prevalent. The ST34 lineage demonstrated extensive multidrug resistance (23/31, 74.2%; 95% CI: 55.4%—88.1%) and accounted for the majority of resistance to ampicillin (29/31, 93.5%; 95% CI: 78.6%—99.2%) and ampicillin-sulbactam (24/31, 77.4%; 95% CI: 58.9%—90.4%). High-risk plasmids were identified, including IncHI2A-type vectors carrying the blaNDM-5 carbapenemase gene and an IncFIA/HI1 plasmid harboring the tet(X4) tigecycline resistance gene. Phylogeographic analysis indicated that the Hainan ST34 strains belong to a China-specific clade undergoing recent clonal expansion although evidence of international transmission was also detected. These findings reveal a distinct epidemiological pattern in Hainan, marked by the predominance of multidrug-resistant ST34 and an elevated invasive infection rate in young children. Targeted surveillance and “One Health” interventions in tropical regions are urgently needed to limit the spread of high-risk NTS clones. IMPORTANCE This study addresses the research gap of pediatric non-typhoidal Salmonella (NTS) in tropical Hainan via comprehensive analysis of 77 clinical isolates. It characterizes the local molecular epidemiology, revealing regional epidemic features and high susceptibility in young children. The multidrug-resistant monophasic ST34 clone is identified as the predominant strain. Notably, high-risk resistance plasmids carrying blaNDM-5 and tet(X4) are detected, indicating hidden horizontal transmission risks of critical antibiotic resistance. Global phylogeny verifies the China-specific expansion of local ST34 strains with cross-regional and zoonotic potential. These findings underscore the severe threat of MDR NTS in tropical island areas, providing key epidemiological and genomic evidence for targeted surveillance, prudent antibiotic administration and One Health strategies, and offering vital references for NTS control in tropical and subtropical regions. This study addresses the research gap of pediatric non-typhoidal Salmonella (NTS) in tropical Hainan via comprehensive analysis of 77 clinical isolates. It characterizes the local molecular epidemiology, revealing regional epidemic features and high susceptibility in young children. The multidrug-resistant monophasic ST34 clone is identified as the predominant strain. Notably, high-risk resistance plasmids carrying blaNDM-5 and tet(X4) are detected, indicating hidden horizontal transmission risks of critical antibiotic resistance. Global phylogeny verifies the China-specific expansion of local ST34 strains with cross-regional and zoonotic potential. These findings underscore the severe threat of MDR NTS in tropical island areas, providing key epidemiological and genomic evidence for targeted surveillance, prudent antibiotic administration and One Health strategies, and offering vital references for NTS control in tropical and subtropical regions.