High prevalence of multidrug-resistant <i>Salmonella enterica</i> in Thailand food markets: insights from complete genome and phenotypic characterization of ESBL-producing strains

<i>Salmonella</i> contamination in the food chain is a common root of foodborne outbreaks. The transmission of antimicrobial resistance among <i>Salmonella</i> 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 <i>Salmonella</i>, we characterized 74 non-typhoidal <i>Salmonella</i> 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 <i>Salmonella</i> 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 <i>S</i>. 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 <i>bla</i> <sub>CTX-M-14</sub> or <i>bla</i> <sub>CTX-M-55</sub> ESBL gene. Complete genomes showed that three ESBL-producing isolates contained plasmid-mediated ESBL, and the other was chromosomal-mediated. <i>In vitro</i> invasion efficiencies of ESBL-producing strains into mucous-producing human colorectal adenocarcinoma HT29-MTX-E12 cells were compared to the reference strain <i>Salmonella</i> 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 <i>Salmonella</i> isolated from Thai foods are MDR and potentially ESBL-producing strains, highlighting the need for continued surveillance and intervention strategies.IMPORTANCEIn 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 <i>Salmonella</i> 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 <i>in vitro</i> invasion efficiency than plasmid-mediated ESBL strains. This study highlights two key public health threats: the risk of acquiring difficult-to-treat MDR <i>Salmonella</i> infections from undercooked food and the circulation of AMR plasmids in fresh markets in Thailand.

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Journal
Microbiology Spectrum
Published
2025-10-31
DOI
https://doi.org/10.1128/spectrum.02129-25
Primary Topic
Salmonella and Campylobacter epidemiology
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article
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article

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

Nalumon Thadtapong, Soraya Chaturongakul, Samantha E. Wirth, Natharin Ngamwongsatit et al.
Microbiology Spectrum
Salmonella and Campylobacter epidemiology
article

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

Nalumon Thadtapong, Soraya Chaturongakul, Samantha E. Wirth, Natharin Ngamwongsatit, A. W. Gray, Phutthaphorn Phaophu, Ratchaneewan Aunpad, Sunisa Dangsuk
article en

Abstract

<i>Salmonella</i> contamination in the food chain is a common root of foodborne outbreaks. The transmission of antimicrobial resistance among <i>Salmonella</i> 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 <i>Salmonella</i>, we characterized 74 non-typhoidal <i>Salmonella</i> 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 <i>Salmonella</i> 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 <i>S</i>. 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 <i>bla</i> <sub>CTX-M-14</sub> or <i>bla</i> <sub>CTX-M-55</sub> ESBL gene. Complete genomes showed that three ESBL-producing isolates contained plasmid-mediated ESBL, and the other was chromosomal-mediated. <i>In vitro</i> invasion efficiencies of ESBL-producing strains into mucous-producing human colorectal adenocarcinoma HT29-MTX-E12 cells were compared to the reference strain <i>Salmonella</i> 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 <i>Salmonella</i> isolated from Thai foods are MDR and potentially ESBL-producing strains, highlighting the need for continued surveillance and intervention strategies.IMPORTANCEIn 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 <i>Salmonella</i> 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 <i>in vitro</i> invasion efficiency than plasmid-mediated ESBL strains. This study highlights two key public health threats: the risk of acquiring difficult-to-treat MDR <i>Salmonella</i> infections from undercooked food and the circulation of AMR plasmids in fresh markets in Thailand.

Microbiology SpectrumVol. 13(12)
Thammasat University (TH), New York State Department of Health (US), Ministry of Public Health (TH), Wadsworth Center (US), Mahidol University (TH), National Institute of Public Health (LA), Department of Medical Sciences (TH)
Openalex Percentile: Top 62%
Salmonella and Campylobacter epidemiology
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