High prevalence of multidrug-resistant Salmonella enterica in Thailand food markets: Insights from complete genome and phenotypic characterization of ESBL-producing strains

Abstract

Salmonella contamination in the food chain is a common root of foodborne outbreaks. The transmission of antimicrobial resistance among Salmonella and food bacteria raises global public health concern. As a major food exporter and travel hub in Southeast Asia, Thailand is particularly susceptible. To better understand the circulating Salmonella, we characterized 74 non-typhoidal Salmonella isolates previously obtained from Thailand food markets. Whole genome sequencing, drug susceptibility testing, and host invasion efficiency assays were performed. The most prevalent serotype was Salmonella serotype Rissen (32.43%) followed by Derby (12.16%). Fifty-two isolates were multidrug-resistant (MDR), with their primary resistance pattern being ampicillin, streptomycin, and tetracycline resistance. The most resistant strain was S. Rissen exhibiting resistance to 13 tested drugs, including third-generation cephalosporin. Six cephalosporin-resistant isolates were identified, four of which were extended-spectrum β-lactamase (ESBL)-producing strains harboring the bla<inf>CTX-M-14</inf> or bla<inf>CTX-M-55</inf> ESBL gene. Complete genomes showed that three ESBL-producing isolates contained plasmid-mediated ESBL, and the other was chromosomal-mediated. In vitro invasion efficiencies of ESBL-producing strains into mucous-producing human colorectal adenocarcinoma HT29-MTX-E12 cells were compared to the reference strain Salmonella Typhimurium LT2. Statistically significant higher invasion efficiency in the chromosomal-mediated ESBL strain was found. Interestingly, the ESBL plasmid detected during this study was highly similar to a plasmid previously isolated from a Thai patient. This study highlights that the majority of Salmonella isolated from Thai foods are MDR and potentially ESBL-producing strains, highlighting the need for continued surveillance and intervention strategies. IMPORTANCE In Thailand, fermented foods are typically consumed raw, and pork is considered a delicacy of Thai cuisine. The presence of multidrug resistant (MDR) foodborne pathogens in these food types raises concern and presents a risk to public health. Here, we report that Salmonella Rissen was the most prevalent serotype isolated from these food samples in Thailand. All isolates carried virulence gene clusters crucial for pathogenesis, and more than 70% of isolates were MDR strains. Four of the MDR strains were ESBL-producing. Whole genome sequence analysis and phenotypic characterizations revealed that chromosome-mediated ESBL strains possessed higher in vitro invasion efficiency than plasmid-mediated ESBL strains. This study highlights two key public health threats: the risk of acquiring difficult-to-treat MDR Salmonella infections from undercooked food and the circulation of AMR plasmids in fresh markets in Thailand.