{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T12:39:03Z","timestamp":1791549543917,"version":"4.3.4"},"reference-count":32,"publisher":"American Society for Microbiology","issue":"7","license":[{"start":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T00:00:00Z","timestamp":1784678400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T00:00:00Z","timestamp":1784678400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/journals.asm.org\/non-commercial-tdm-license"}],"funder":[{"name":"Observation and Research Station of Yunnan Province on Important Animal Disease Prevention in Mengla","award":["202505AM340007"],"award-info":[{"award-number":["202505AM340007"]}]},{"DOI":"10.13039\/501100012166","name":"National Basic Research Program of China","doi-asserted-by":"publisher","award":["2024YFD1800404"],"award-info":[{"award-number":["2024YFD1800404"]}],"id":[{"id":"10.13039\/501100012166","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Yunnan Provincial Innovation Team of Key Technologies for Prevention and Control of Important Livestock and Poultry Diseases","award":["202405AS350004"],"award-info":[{"award-number":["202405AS350004"]}]},{"name":"Yunnan Joint International R&D Center of Veterinary Public Health","award":["202403AP140033"],"award-info":[{"award-number":["202403AP140033"]}]},{"name":"Yunnan Province Special Project for Building a Science and Technology Innovation Center for South and Southeast Asia - Yunnan International Joint R&D Center for Veterinary Drugs","award":["202403AP140012"],"award-info":[{"award-number":["202403AP140012"]}]},{"name":"Teacher-related project funded by the Scientific Research Fund of the Education Department of Yunnan Province","award":["2024J0497"],"award-info":[{"award-number":["2024J0497"]}]}],"content-domain":{"domain":["journals.asm.org"],"crossmark-restriction":true},"short-container-title":["Appl Environ Microbiol"],"published-print":{"date-parts":[[2026,7,22]]},"abstract":"ABSTRACT<\/jats:title>\n \n \n \n Salmonella<\/jats:italic>\n remains a critical foodborne pathogen of public health importance and a predominant contributor to contamination throughout the pork production system. However, in northeastern Thailand, detailed characterization of seasonal variation and stage-specific occurrence, including pre-slaughter fecal samples, post-slaughter carcasses, and retail pork, has been largely lacking. Clarifying the influence of seasonal conditions on\n Salmonella<\/jats:italic>\n prevalence and antimicrobial resistance across these production points is essential for robust risk assessment within the pork supply chain. A total of 897 samples were collected from slaughterhouses (carcasses, feces) and markets (pork) in northeastern Thailand during the summer, rainy, and winter seasons from 2023 to 2024.\n Salmonella<\/jats:italic>\n isolation, serotyping, antimicrobial susceptibility testing, pulsed-field gel electrophoresis (PFGE), and phylogenetic analysis were performed to assess prevalence, serotype distribution, AMR, and genetic relatedness. The associations between prevalence or AMR and seasonal factors were evaluated using relative risk (RR), chi-square, and logistic regression tests.\n Salmonella<\/jats:italic>\n prevalence varied markedly across matrices and seasons. Retail pork showed the highest contamination (summer: 75.4%, rainy: 75.3%, winter: 54.7%), followed by feces (50.5%, 34.0%, and 29.0%, respectively), whereas carcass samples had the lowest prevalence (11.3%, 13.0%, and 4.0%). Seasonal effects were significant for fecal (\u03c7\u00b2 = 11.4,\n P<\/jats:italic>\n = 0.003) and pork samples (\u03c7\u00b2 = 7.7,\n P<\/jats:italic>\n = 0.021). Relative risk (RR), using winter as reference, reached 1.7 for fecal samples and 1.4 for pork during summer. Serotype composition exhibited pronounced seasonal shifts, with\n S<\/jats:italic>\n . Rissen increasing sharply and becoming dominant in winter; logistic regression showed significantly lower odds of\n S<\/jats:italic>\n . Rissen isolation in summer (OR = 0.25,\n P<\/jats:italic>\n < 0.01) and the rainy season (OR = 0.47,\n P<\/jats:italic>\n < 0.01) compared with winter. Multivariable models indicated that the rainy season was strongly associated with antimicrobial resistance (OR = 11.9 vs winter,\n P<\/jats:italic>\n = 0.002).\n S<\/jats:italic>\n . Rissen remained the primary contributor to MDR across matrices, while\n S<\/jats:italic>\n . Bovismorbificans and other\n serotype<\/jats:italic>\n s showed significantly reduced resistance (OR = 0.2,\n P<\/jats:italic>\n < 0.05). PFGE analyses revealed high polymorphism in\n S<\/jats:italic>\n . Weltevreden (55%\u2013100% similarity) and\n S<\/jats:italic>\n . Rissen (50%\u2013100%), with no clustering by matrix or season, indicating cross-environmental dissemination of similar clones. Phylogenetic analysis identified two major\n S<\/jats:italic>\n . Rissen lineages but a highly conserved MDR gene backbone, including \u03b2-lactamases (blaTEM-1, blaCTX-M-55), aminoglycoside resistance genes (aadA, aac(6\u2032)-Iy), phenicol resistance genes (cmlA6, floR), sulfonamide and trimethoprim resistance genes, and PMQR determinants (qnrB10, qnrS1).\n Salmonella<\/jats:italic>\n contamination and antimicrobial resistance in the pork production chain are strongly shaped by seasonal pressures and downstream amplification during distribution. Summer and the rainy season present the highest risk for both contamination and multidrug resistance, while winter shows marked serotype convergence, dominated by\n S<\/jats:italic>\n . Rissen. Retail pork exhibited the most complex MDR profiles, indicating an accumulation of resistance along the supply chain. PFGE and phylogenetic analyses revealed that closely related clones circulate across slaughterhouses and markets, supporting persistent transmission routes. These findings highlight the need for strengthened seasonal risk management and integrated genomic surveillance to interrupt the spread of high-risk MDR serotypes and reduce consumer exposure.\n <\/jats:p>\n \n IMPORTANCE<\/jats:title>\n \n Understanding when and how\n Salmonella<\/jats:italic>\n spreads along the pork production chain is essential for reducing human exposure to foodborne pathogens and multidrug-resistant (MDR) strains. This study identifies strong seasonal pressures and downstream amplification during distribution as key drivers of\n Salmonella<\/jats:italic>\n contamination and antimicrobial resistance. The marked winter dominance of MDR\n S<\/jats:italic>\n . Rissen and the accumulation of complex resistance profiles in retail pork highlight predictable high-risk periods and critical control points where interventions can be most effective. Furthermore, the discovery that closely related clones circulate between slaughterhouses and markets underscores persistent transmission routes that conventional hygiene measures may fail to interrupt. By integrating epidemiological, phenotypic, and genomic evidence, this work provides actionable insights for designing season-specific monitoring programs and implementing genomic surveillance to limit the spread of MDR\n Salmonella<\/jats:italic>\n in the food supply.\n <\/jats:p>\n <\/jats:sec>\n <\/jats:sec>","DOI":"10.1128\/aem.00057-26","type":"journal-article","created":{"date-parts":[[2026,6,2]],"date-time":"2026-06-02T13:05:45Z","timestamp":1780405545000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":2,"title":["Seasonal impacts on\n Salmonella<\/i>\n prevalence and antimicrobial resistance in the pork food chain of northeastern Thailand"],"prefix":"10.1128","volume":"92","author":[{"ORCID":"https:\/\/orcid.org\/0009-0005-8647-7858","authenticated-orcid":false,"given":"Hongmei","family":"Liu","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/03cq4gr50","id-type":"ROR","asserted-by":"publisher"}],"name":"Faculty of Veterinary Medicine, Khon Kaen University","place":["Khon Kaen, Thailand"]},{"id":[{"id":"https:\/\/ror.org\/04dpa3g90","id-type":"ROR","asserted-by":"publisher"}],"name":"Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhongbin","family":"Bai","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04dpa3g90","id-type":"ROR","asserted-by":"publisher"}],"name":"Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ning","family":"Wang","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04dpa3g90","id-type":"ROR","asserted-by":"publisher"}],"name":"Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chaiwat","family":"Pulsrikarn","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00cb3r984","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Medical Sciences, Ministry of Public Health, National Institute of Health","place":["Nonthaburi, Thailand"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patchara","family":"Phuektes","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/03cq4gr50","id-type":"ROR","asserted-by":"publisher"}],"name":"Faculty of Veterinary Medicine, Khon Kaen University","place":["Khon Kaen, Thailand"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Prawit","family":"Butudom","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/03cq4gr50","id-type":"ROR","asserted-by":"publisher"}],"name":"Faculty of Veterinary Medicine, Khon Kaen University","place":["Khon Kaen, Thailand"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaowen","family":"Liu","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04dpa3g90","id-type":"ROR","asserted-by":"publisher"}],"name":"Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weidong","family":"Zuo","sequence":"additional","affiliation":[{"name":"Kunming Customs Technology Center","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renchun","family":"Ji","sequence":"additional","affiliation":[{"name":"Kunming Customs Technology Center","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tingkai","family":"Bi","sequence":"additional","affiliation":[{"name":"Kunming Customs Technology Center","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chunfen","family":"Mei","sequence":"additional","affiliation":[{"name":"Kunming Customs Technology Center","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rong","family":"Zhou","sequence":"additional","affiliation":[{"name":"Kunming Customs Technology Center","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wengui","family":"Li","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04dpa3g90","id-type":"ROR","asserted-by":"publisher"}],"name":"Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Wu","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04dpa3g90","id-type":"ROR","asserted-by":"publisher"}],"name":"Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaowei","family":"Sun","sequence":"additional","affiliation":[{"name":"Yunnan Animal Husbandry Station","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yiduan","family":"Liu","sequence":"additional","affiliation":[{"name":"Yunnan Animal Husbandry Station","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jamal Muhammad","family":"Khan","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/045v4z873","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Parasitology, Cholistan University of Veterinary and Animal Sciences","place":["Bahawalpur, Pakistan"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1701-907X","authenticated-orcid":false,"given":"Sunpetch","family":"Angkititrakul","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/03cq4gr50","id-type":"ROR","asserted-by":"publisher"}],"name":"Faculty of Veterinary Medicine, Khon Kaen University","place":["Khon Kaen, Thailand"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7141-9552","authenticated-orcid":false,"given":"Fanan","family":"Suksawat","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/03cq4gr50","id-type":"ROR","asserted-by":"publisher"}],"name":"Faculty of Veterinary Medicine, Khon Kaen University","place":["Khon Kaen, Thailand"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1549-8764","authenticated-orcid":false,"given":"Xin","family":"Wu","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/04dpa3g90","id-type":"ROR","asserted-by":"publisher"}],"name":"Yunnan Joint International R&D Center of Veterinary Public Health, College of Veterinary Medicine, Yunnan Agricultural University","place":["Kunming, China"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"235","reference":[{"key":"e_1_3_4_2_2","unstructured":"Noah DL. 2022. Incidence and impact of foodborne illness. Available from: https:\/\/www.msdvetmanual.com\/public-health\/food-safety\/incidence-and-impact-of-foodborne-illness"},{"key":"e_1_3_4_3_2","unstructured":"World Health Organization. 2024. Food safety. Available from: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/food-safety"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2025.1524287"},{"key":"e_1_3_4_5_2","doi-asserted-by":"publisher","DOI":"10.3390\/pathogens8010019"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2021.702909"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1017\/S095026881300215X"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijfoodmicro.2005.11.020"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1099\/jmm.0.001894"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1089\/fpd.2007.0075"},{"key":"e_1_3_4_11_2","doi-asserted-by":"publisher","unstructured":"Prasertsee T Pascoe B Patchanee P. 2023. Colistin resistance and resistance determinants are mobile among Salmonella enterica isolates from diseased and healthy pigs in Thailand. bioRxiv. doi:10.1101\/2023.01.31.526471","DOI":"10.1101\/2023.01.31.526471"},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.meatsci.2024.109734"},{"key":"e_1_3_4_13_2","doi-asserted-by":"publisher","DOI":"10.1186\/s12879-020-4819-0"},{"key":"e_1_3_4_14_2","first-page":"167","article-title":"Prevalence of Salmonella spp. isolated from pigs at Nongdouang slaughterhouse in Vientiane capital, LAO PDR","volume":"22","author":"Somsanith N","year":"2012","unstructured":"Somsanith N, Noppon B, Angkititrakul S, Sukolpong V, Kanistanon K. 2012. Prevalence of Salmonella spp. isolated from pigs at Nongdouang slaughterhouse in Vientiane capital, LAO PDR. KKU Vet J 22:167\u2013173.","journal-title":"KKU Vet J"},{"key":"e_1_3_4_15_2","unstructured":"Grimont PAD Weill FX. 2007. Antigenic formulae of the Salmonella serovars"},{"key":"e_1_3_4_16_2","volume-title":"Standard operating procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri","author":"(CDC) CfDCaP","year":"2017","unstructured":"(CDC) CfDCaP. 2017. Standard operating procedure for PulseNet PFGE of Escherichia coli O157:H7, Escherichia coli non-O157 (STEC), Salmonella serotypes, Shigella sonnei and Shigella flexneri. U.S. Department of Health and Human Services, Atlanta."},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.3390\/ijerph16122083"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijfoodmicro.2021.109049"},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.3390\/foods14162857"},{"key":"e_1_3_4_20_2","doi-asserted-by":"publisher","DOI":"10.2903\/j.efsa.2023.8442"},{"key":"e_1_3_4_21_2","doi-asserted-by":"publisher","DOI":"10.1128\/AEM.01249-08"},{"key":"e_1_3_4_22_2","doi-asserted-by":"publisher","DOI":"10.4315\/JFP-21-003"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.3390\/pathogens9010020"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.01985"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.56808\/2985-1130.3191"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.1007\/s42770-022-00700-w"},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijfoodmicro.2020.108623"},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.3390\/microorganisms12112196"},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.3390\/foods14172933"},{"key":"e_1_3_4_30_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2015.03.102"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-025-02972-2"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.1556\/030.2024.02347"},{"key":"e_1_3_4_33_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2022.899062"}],"container-title":["Applied and Environmental Microbiology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/aem.00057-26","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/journals.asm.org\/doi\/pdf\/10.1128\/aem.00057-26","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,22]],"date-time":"2026-07-22T13:06:45Z","timestamp":1784725605000},"score":1,"resource":{"primary":{"URL":"https:\/\/journals.asm.org\/doi\/10.1128\/aem.00057-26"}},"subtitle":[],"editor":[{"given":"Sophie","family":"Roussel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026,7,22]]},"references-count":32,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2026,7,22]]}},"alternative-id":["10.1128\/aem.00057-26"],"URL":"https:\/\/doi.org\/10.1128\/aem.00057-26","relation":{},"ISSN":["0099-2240","1098-5336"],"issn-type":[{"value":"0099-2240","type":"print"},{"value":"1098-5336","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,7,22]]},"assertion":[{"value":"2026-01-14","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-04-09","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-06-02","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e00057-26"}}