Bayesian phylogeographic analysis infers cross-border transmission dynamics of drug-resistant Salmonella Enteritidis.

Abstract

Salmonella Enteritidis (S. Enteritidis) stands as a leading cause of human salmonellosis worldwide with a tendency to spread through contaminated foodstuffs and animals. In Hong Kong, a significant proportion of food products are imported, and many cases are often caused by the consumption of contaminated food, hence making the geographical surveillance of drug-resistant S. Enteritidis important for strong public health and food safety measures. We analyzed the whole genomes of 207 S. Enteritidis from Hong Kong, Australia, Canada, mainland China, the United States of America, South Africa, Taiwan, and the United Kingdom to examine associated antimicrobial resistance and the transmission dynamics between continents. Phylogenetic cluster inferences and Bayesian phylogeographical analysis were performed. Overall, sequence type ST11 strains were dominant (92.8%, 192/207). Five phylogenomic clusters A to E were identified, where most isolates from mainland China and Hong Kong were in Cluster E. Among the 22 plasmid types identified, IncX1 was dominant in the Asian isolates. Most of the virulence genes were distributed in Salmonella pathogenicity islands -1 and -2, with two universal virulence operons responsible for the effector delivery system and bacterial cell adhesion. The phylogeographic inference analysis showed a statistically significant link between mainland China and Hong Kong with the highest relative migration rate (relativeGeoRates mean ± standard error = 2.93 ± .07, Bayes Factor [BF] = 1285.5], with some traceable to Canada (0.61 ± 0.03, BF = 6.9) and Australia (1.02 ± 0.04, BF = 4.2). Our analysis suggests hypothetical transmission of S. Enteritidis and its associated antimicrobial resistance across borders.

Importance: Antimicrobial resistance and disease severity in nontyphoidal Salmonella have constituted a serious public health challenge worldwide. Drug-resistant Salmonella Enteritidis is a leading pathogen that causes human infections primarily through the consumption of contaminated food products. Previous research focuses on the whole-genome analysis of antimicrobial resistance and virulence factors in S. Enteritidis; however, details on how this bacterium localized, expanded, and diversified from location to location remain unknown. Our study for the first time addresses this gap by investigating the phylogeographic transmission to estimate the frequency and location of cross-border spread. By evidence-based inferred transmission, we aim to uncover novel insights into the dynamic spread of S. Enteritidis, revealing the route of emergence and migration. This research is crucial for enhancing our understanding of the control strategies to safeguard human health.