Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade Hub

Shenzhen, a major port city with a heavily imported food supply, offers a critical setting to examine the spread and adaptation of multidrug-resistant Salmonella 1,4,[5],12:i: – (S. 1,4,[5],12:i:-). This study integrates 17 years of genomic, epidemiological, and food safety data. We explored the ser...

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Main Authors: Dingjie Huang, Ziqi Wu, Yixiang Jiang, Lulu Hu, Rui Cai, Xi Yang, Chen Du, Shiting Chen, Panpan Yang, Bingchan Guo, Xiaolu Shi, Shuang Wu, Yinghui Li, Zhemin Zhou, Qinghua Hu
Format: Article
Language:English
Published: Taylor & Francis Group 2025-12-01
Series:Emerging Microbes and Infections
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Online Access:https://www.tandfonline.com/doi/10.1080/22221751.2025.2542251
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author Dingjie Huang
Ziqi Wu
Yixiang Jiang
Lulu Hu
Rui Cai
Xi Yang
Chen Du
Shiting Chen
Panpan Yang
Bingchan Guo
Xiaolu Shi
Shuang Wu
Yinghui Li
Zhemin Zhou
Qinghua Hu
author_facet Dingjie Huang
Ziqi Wu
Yixiang Jiang
Lulu Hu
Rui Cai
Xi Yang
Chen Du
Shiting Chen
Panpan Yang
Bingchan Guo
Xiaolu Shi
Shuang Wu
Yinghui Li
Zhemin Zhou
Qinghua Hu
author_sort Dingjie Huang
collection DOAJ
description Shenzhen, a major port city with a heavily imported food supply, offers a critical setting to examine the spread and adaptation of multidrug-resistant Salmonella 1,4,[5],12:i: – (S. 1,4,[5],12:i:-). This study integrates 17 years of genomic, epidemiological, and food safety data. We explored the serovar’s population structure, antibiotic resistance gene (ARG) patterns, and transmission dynamics locally and globally. Our analyses revealed substantial rise in S. 1,4,[5],12:i: – prevalence among non-typhoidal Salmonella isolates over the past 17 years, from 2.27% in 2007 to 24.79% in 2023. S. 1,4,[5],12:i: – was predominated by ST34 (97.9%), with high genotypic resistance to aminoglycosides (100%), tetracyclines (96.6%), β-lactams (89.3%), and sulphonamides (88.5%). Phylogenetic analysis separated S. 1,4,[5],12:i: – into four clades. Clade 4, first detected in Shenzhen in 2013, emerged as the predominant lineage by 2023 (56.9%). This clade exhibited minimal genetic diversity (≤ 38 core SNPs), with adaptive traits linked to the acquisition of resistance-associated plasmids. Notably, plasmid-driven ARGs, including carbapenem resistance genes, have emerged as a growing concern. Transmission analysis identified two key transmission dynamics: transient outbreaks primarily involving food handlers and persistent lineages sustained through local and international spread, often facilitated by the food supply chain. These findings underscore the role of occupational carriers and imported food products in the dissemination of ARGs, emphasizing the need for enhanced surveillance and improved health and hygiene practices for food handlers. This study provides a comprehensive molecular epidemiological framework for addressing multidrug-resistant Salmonella in globalized urban food hubs, offering a foundation for future surveillance and control efforts.
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spelling doaj-art-a4f63c1911e6497a856fe23a53e02d0c2025-08-20T02:58:11ZengTaylor & Francis GroupEmerging Microbes and Infections2222-17512025-12-0114110.1080/22221751.2025.2542251Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade HubDingjie Huang0Ziqi Wu1Yixiang Jiang2Lulu Hu3Rui Cai4Xi Yang5Chen Du6Shiting Chen7Panpan Yang8Bingchan Guo9Xiaolu Shi10Shuang Wu11Yinghui Li12Zhemin Zhou13Qinghua Hu14School of Public Health, Shanxi Medical University, Taiyuan, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaSchool of Public Health, Shanxi Medical University, Taiyuan, People's Republic of ChinaSchool of Public Health, Shanxi Medical University, Taiyuan, People's Republic of ChinaSchool of Public Health, Shanxi Medical University, Taiyuan, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaShenzhen Center for Disease Control and Prevention, Shenzhen, People's Republic of ChinaNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, People's Republic of ChinaSchool of Public Health, Shanxi Medical University, Taiyuan, People's Republic of ChinaShenzhen, a major port city with a heavily imported food supply, offers a critical setting to examine the spread and adaptation of multidrug-resistant Salmonella 1,4,[5],12:i: – (S. 1,4,[5],12:i:-). This study integrates 17 years of genomic, epidemiological, and food safety data. We explored the serovar’s population structure, antibiotic resistance gene (ARG) patterns, and transmission dynamics locally and globally. Our analyses revealed substantial rise in S. 1,4,[5],12:i: – prevalence among non-typhoidal Salmonella isolates over the past 17 years, from 2.27% in 2007 to 24.79% in 2023. S. 1,4,[5],12:i: – was predominated by ST34 (97.9%), with high genotypic resistance to aminoglycosides (100%), tetracyclines (96.6%), β-lactams (89.3%), and sulphonamides (88.5%). Phylogenetic analysis separated S. 1,4,[5],12:i: – into four clades. Clade 4, first detected in Shenzhen in 2013, emerged as the predominant lineage by 2023 (56.9%). This clade exhibited minimal genetic diversity (≤ 38 core SNPs), with adaptive traits linked to the acquisition of resistance-associated plasmids. Notably, plasmid-driven ARGs, including carbapenem resistance genes, have emerged as a growing concern. Transmission analysis identified two key transmission dynamics: transient outbreaks primarily involving food handlers and persistent lineages sustained through local and international spread, often facilitated by the food supply chain. These findings underscore the role of occupational carriers and imported food products in the dissemination of ARGs, emphasizing the need for enhanced surveillance and improved health and hygiene practices for food handlers. This study provides a comprehensive molecular epidemiological framework for addressing multidrug-resistant Salmonella in globalized urban food hubs, offering a foundation for future surveillance and control efforts.https://www.tandfonline.com/doi/10.1080/22221751.2025.2542251Salmonella Typhimurium monophasic variantmultidrug resistance (MDR)plasmidtransmission routesfood handlers
spellingShingle Dingjie Huang
Ziqi Wu
Yixiang Jiang
Lulu Hu
Rui Cai
Xi Yang
Chen Du
Shiting Chen
Panpan Yang
Bingchan Guo
Xiaolu Shi
Shuang Wu
Yinghui Li
Zhemin Zhou
Qinghua Hu
Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade Hub
Emerging Microbes and Infections
Salmonella Typhimurium monophasic variant
multidrug resistance (MDR)
plasmid
transmission routes
food handlers
title Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade Hub
title_full Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade Hub
title_fullStr Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade Hub
title_full_unstemmed Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade Hub
title_short Plasmid-driven clonal expansion of multidrug-resistant monophasic Salmonella Typhimurium in a Global Food Trade Hub
title_sort plasmid driven clonal expansion of multidrug resistant monophasic salmonella typhimurium in a global food trade hub
topic Salmonella Typhimurium monophasic variant
multidrug resistance (MDR)
plasmid
transmission routes
food handlers
url https://www.tandfonline.com/doi/10.1080/22221751.2025.2542251
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