Emergence of blaNDM−5 and international dissemination of an ST26 Salmonella Thompson resistance gene-enriched sublineage

This study aimed to retrospectively analyze Salmonella Thompson isolates collected at our research center and to investigate the genetic characteristics of Salmonella Thompson by integrating isolates from the present study with publicly available global genomic data, with a particular focus on the ST26 clone. This retrospective genomic epidemiological study investigated Salmonella Thompson isolates collected from a tertiary hospital in northern China between 2018 and 2023. We employed antimicrobial susceptibility testing, short-read and long-read whole-genome sequencing, phylogenomic analysis, and plasmid structure characterization. All Salmonella Thompson genomes from the NCBI GenBank database were included in comparative genomic analysis. All Salmonella Thompson strains in this study belonged to ST26. Strain WFS122 carried blaNDM−5, which was located on a common IncX3-type plasmid found in NDM-positive Escherichia coli and Klebsiella pneumoniae strains (100% homology). Analysis of the public database revealed that ST26 is the globally predominant lineage of Salmonella Thompson, accounting for 89.57% of strains and harboring the overwhelming majority of resistance genes and Class 1 integrons. We further identified Clade D4 as a high-risk evolutionary branch with elevated resistance rates. Within this study, 96.15% of Clade D4 strains harbored Class 1 integrons, which were pivotal in resistance gene carriage, primarily encoding the aminoglycoside resistance gene aadA and the trimethoprim resistance gene dfrA. We hypothesize that ST26 Salmonella Thompson exhibits global expansion, with the high-risk clone Clade D4 showing a strong association with Class 1 integrons and resistance genes. This high-risk clone has demonstrated potential for transmission in China, the United States, and the United Kingdom, necessitating expanded research scope and scale. Additionally, this study represents the identification of NDM-5-carrying ST26 Salmonella Thompson. The emergence of carbapenem-resistant Salmonella Thompson poses a significant challenge for clinical management of Salmonella infections caused by this strain.