Genomic Epidemiology of Multidrug-Resistant Nontyphoidal Salmonella in Young Children Hospitalized for Gastroenteritis

Abstract

Nontyphoidal Salmonella (NTS) gastroenteritis is a foodborne disease with a large global burden. Antimicrobial resistance (AMR) among foodborne pathogens is an important public health concern, and multidrug-resistant (MDR) Salmonella is prevalent in Southeast Asia and China. ABSTRACT Nontyphoidal Salmonella (NTS) gastroenteritis in children remains a significant burden on health care and constitutes a majority of all admissions for Salmonella infections in public hospitals in Hong Kong. In this prospective study, 41% of 241 children hospitalized with gastroenteritis from three public hospitals during 2019 were culture confirmed to have NTS infection. These Salmonella isolates were whole-genome sequenced and in silico predicted for their serovars/serotypes using the Salmonella In Silico Typing Resource (SISTR) and SeqSero1, and the antimicrobial resistance (AMR) genes were determined. Phylogenetic analysis revealed three major clades belonging to Salmonella enterica serovar Enteritidis sequence type 11 (ST11) (43%), multidrug-resistant (MDR) S. Typhimurium ST19 (12%) and its monophasic variant ST34 (25%), and mostly singletons of 15 other serovars. MDR S. Typhimurium and its variant were more common in infants <24\u2009months of age and possessed genotypic resistance to five antimicrobial agents, including ampicillin (A), chloramphenicol (C), aminoglycosides (Am), sulfonamides (Su), and tetracyclines (T). Older children were more often infected with S. Enteritidis, which possessed distinct genotypic resistance to AAmSu and fluoroquinolones. In addition, 3% of the isolates possessed extended-spectrum beta-lactamase (ESBL) CTX-M genes, while one isolate (1%) harboring the carbapenemase gene blaNDM-1 was identified. Our findings provide a more complete genomic epidemiological insight into NTS causing gastroenteritis and identify a wider spectrum of determinants of resistance to third-generation beta-lactams and carbapenems, which are often not readily recognized. With high rates of multidrug-resistant NTS from studies in the Asia-Pacific region, the rapid and reliable determination of serovars and resistance determinants using whole-genome sequencing (WGS) is invaluable for enhancing public health interventions for infection prevention and control. IMPORTANCE Nontyphoidal Salmonella (NTS) gastroenteritis is a foodborne disease with a large global burden. Antimicrobial resistance (AMR) among foodborne pathogens is an important public health concern, and multidrug-resistant (MDR) Salmonella is prevalent in Southeast Asia and China. Using whole-genome sequencing, this study highlights the relationship of the MDR Salmonella serotypes and the diverse range of Salmonella genotypes that contaminate our food sources and contribute to disease in this locality. The findings update our understanding of Salmonella epidemiology and associated MDR determinants to enhance the tracking of foodborne pathogens for public health and food safety.