{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,29]],"date-time":"2026-04-29T12:45:56Z","timestamp":1777466756941,"version":"3.51.4"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T00:00:00Z","timestamp":1715040000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T00:00:00Z","timestamp":1715040000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Cholangiocarcinoma (CCA) exhibits a heightened incidence in regions with a high prevalence of <jats:italic>Opisthorchis viverrini<\/jats:italic> infection, with previous studies suggesting an association with diabetes mellitus (DM). Our study aimed to investigate the spatial distribution of CCA in relation to <jats:italic>O. viverrini<\/jats:italic> infection and DM within high-risk populations in Northeast Thailand. Participants from 20 provinces underwent CCA screening through the Cholangiocarcinoma Screening and Care Program between 2013 and 2019. Health questionnaires collected data on <jats:italic>O. viverrini<\/jats:italic> infection and DM, while ultrasonography confirmed CCA diagnoses through histopathology. Multiple zero-inflated Poisson regression, accounting for covariates like age and gender, assessed associations of <jats:italic>O. viverrini<\/jats:italic> infection and DM with CCA. Bayesian spatial analysis methods explored spatial relationships. Among 263,588 participants, <jats:italic>O. viverrini<\/jats:italic> infection, DM, and CCA prevalence were 32.37%, 8.22%, and 0.36%, respectively. The raw standardized morbidity ratios for CCA was notably elevated in the Northeast\u2019s lower and upper regions. Coexistence of <jats:italic>O. viverrini<\/jats:italic> infection and DM correlated with CCA, particularly in males and those aged over 60\u00a0years, with a distribution along the Chi, Mun, and Songkhram Rivers. Our findings emphasize the association of the spatial distribution of <jats:italic>O. viverrini<\/jats:italic> infection and DM with high-risk CCA areas in Northeast Thailand. Thus, prioritizing CCA screening in regions with elevated <jats:italic>O. viverrini<\/jats:italic> infection and DM prevalence is recommended.<\/jats:p>","DOI":"10.1038\/s41598-024-61282-1","type":"journal-article","created":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T19:01:45Z","timestamp":1715108505000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Spatial analysis of cholangiocarcinoma in relation to diabetes mellitus and Opisthorchis viverrini infection in Northeast Thailand"],"prefix":"10.1038","volume":"14","author":[{"given":"Kavin","family":"Thinkhamrop","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kulwadee","family":"Suwannatrai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Matthew","family":"Kelly","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Apiporn T.","family":"Suwannatrai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,5,7]]},"reference":[{"key":"61282_CR1","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1097\/MOG.0b013e3282fbf9b3","volume":"24","author":"B Sripa","year":"2008","unstructured":"Sripa, B. & Pairojkul, C. Cholangiocarcinoma: lessons from Thailand. Curr. Opin. Gastroenterol. 24, 349\u2013356. https:\/\/doi.org\/10.1097\/MOG.0b013e3282fbf9b3 (2008).","journal-title":"Curr. Opin. Gastroenterol."},{"key":"61282_CR2","doi-asserted-by":"publisher","first-page":"7160","DOI":"10.3748\/wjg.v23.i39.7160","volume":"23","author":"R Chaiteerakij","year":"2017","unstructured":"Chaiteerakij, R. et al. Characteristics and outcomes of cholangiocarcinoma by region in Thailand: a nationwide study. World J. Gastroenterol. 23, 7160\u20137167. https:\/\/doi.org\/10.3748\/wjg.v23.i39.7160 (2017).","journal-title":"World J. Gastroenterol."},{"key":"61282_CR3","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1186\/s12876-016-0565-6","volume":"17","author":"S Treeprasertsuk","year":"2017","unstructured":"Treeprasertsuk, S. et al. A significant cancer burden and high mortality of intrahepatic cholangiocarcinoma in Thailand: a nationwide database study. BMC Gastroenterol. 17, 3. https:\/\/doi.org\/10.1186\/s12876-016-0565-6 (2017).","journal-title":"BMC Gastroenterol."},{"key":"61282_CR4","doi-asserted-by":"publisher","first-page":"962","DOI":"10.1046\/j.1365-2168.2002.02143.x","volume":"89","author":"P Watanapa","year":"2002","unstructured":"Watanapa, P. & Watanapa, W. B. Liver fluke-associated cholangiocarcinoma. Br. J. Surg. 89, 962\u2013970. https:\/\/doi.org\/10.1046\/j.1365-2168.2002.02143.x (2002).","journal-title":"Br. J. Surg."},{"key":"61282_CR5","first-page":"251","volume":"10","author":"K Poomphakwaen","year":"2009","unstructured":"Poomphakwaen, K. et al. Risk factors for cholangiocarcinoma in Khon Kaen, Thailand: a nested case-control study. Asian Pac. J. Cancer Prev. 10, 251\u2013258 (2009).","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"61282_CR6","doi-asserted-by":"publisher","first-page":"e89","DOI":"10.1016\/j.canep.2011.11.007","volume":"36","author":"N Songserm","year":"2012","unstructured":"Songserm, N. et al. Risk factors for cholangiocarcinoma in high-risk area of Thailand: role of lifestyle, diet and methylenetetrahydrofolate reductase polymorphisms. Cancer Epidemiol. 36, e89-94. https:\/\/doi.org\/10.1016\/j.canep.2011.11.007 (2012).","journal-title":"Cancer Epidemiol."},{"key":"61282_CR7","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1002\/jhbp.62","volume":"21","author":"P Sithithaworn","year":"2014","unstructured":"Sithithaworn, P., Yongvanit, P., Duenngai, K., Kiatsopit, N. & Pairojkul, C. Roles of liver fluke infection as risk factor for cholangiocarcinoma. J. Hepatobiliary Pancreat. Sci. 21, 301\u2013308. https:\/\/doi.org\/10.1002\/jhbp.62 (2014).","journal-title":"J. Hepatobiliary Pancreat. Sci."},{"key":"61282_CR8","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0177130","volume":"12","author":"WPP Aung","year":"2017","unstructured":"Aung, W. P. P. et al. First report and molecular identification of Opisthorchis viverrini infection in human communities from Lower Myanmar. PLoS ONE 12, e0177130. https:\/\/doi.org\/10.1371\/journal.pone.0177130 (2017).","journal-title":"PLoS ONE"},{"key":"61282_CR9","doi-asserted-by":"publisher","first-page":"10","DOI":"10.1016\/j.parint.2011.08.014","volume":"61","author":"P Sithithaworn","year":"2012","unstructured":"Sithithaworn, P. et al. The current status of opisthorchiasis and clonorchiasis in the Mekong Basin. Parasitol. Int. 61, 10\u201316. https:\/\/doi.org\/10.1016\/j.parint.2011.08.014 (2012).","journal-title":"Parasitol. Int."},{"issue":"Suppl 1","key":"61282_CR10","doi-asserted-by":"publisher","first-page":"S158","DOI":"10.1016\/j.actatropica.2010.07.006","volume":"120","author":"B Sripa","year":"2011","unstructured":"Sripa, B. et al. Opisthorchiasis and opisthorchis-associated cholangiocarcinoma in Thailand and Laos. Acta Trop. 120(Suppl 1), S158-168. https:\/\/doi.org\/10.1016\/j.actatropica.2010.07.006 (2011).","journal-title":"Acta Trop."},{"key":"61282_CR11","doi-asserted-by":"publisher","first-page":"1323","DOI":"10.1007\/s00436-012-3154-9","volume":"112","author":"J Prasongwatana","year":"2013","unstructured":"Prasongwatana, J., Laummaunwai, P., Boonmars, T. & Pinlaor, S. Viable metacercariae of Opisthorchis viverrini in northeastern Thai cyprinid fish dishes\u2013as part of a rational program for control of O. viverrini-associated cholangiocarcinoma. Parasitol. Res. 112, 1323\u20131327. https:\/\/doi.org\/10.1007\/s00436-012-3154-9 (2013).","journal-title":"Parasitol. Res."},{"key":"61282_CR12","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.parint.2011.06.015","volume":"61","author":"C Grundy-Warr","year":"2012","unstructured":"Grundy-Warr, C. et al. Raw attitudes, wetland cultures, life-cycles: socio-cultural dynamics relating to Opisthorchis viverrini in the Mekong Basin. Parasitol Int 61, 65\u201370. https:\/\/doi.org\/10.1016\/j.parint.2011.06.015 (2012).","journal-title":"Parasitol Int"},{"key":"61282_CR13","doi-asserted-by":"publisher","first-page":"6609","DOI":"10.7314\/apjcp.2014.15.16.6609","volume":"15","author":"K Thaewnongiew","year":"2014","unstructured":"Thaewnongiew, K. et al. Prevalence and risk factors for Opisthorchis viverrini infections in upper Northeast Thailand. Asian Pac. J. Cancer Prev. 15, 6609\u20136612. https:\/\/doi.org\/10.7314\/apjcp.2014.15.16.6609 (2014).","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"61282_CR14","doi-asserted-by":"publisher","first-page":"857","DOI":"10.7314\/apjcp.2016.17.2.857","volume":"17","author":"P Saengsawang","year":"2016","unstructured":"Saengsawang, P., Promthet, S. & Bradshaw, P. Reinfection by Opisthorchis viverrini after treatment with praziquantel. Asian Pac. J. Cancer Prev. 17, 857\u2013862. https:\/\/doi.org\/10.7314\/apjcp.2016.17.2.857 (2016).","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"61282_CR15","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0246490","volume":"16","author":"S Kamsa-ard","year":"2021","unstructured":"Kamsa-ard, S. et al. Decreasing trends in cholangiocarcinoma incidence and relative survival in Khon Kaen, Thailand: an updated, inclusive, population-based cancer registry analysis for 1989\u20132018. PLOS ONE 16, e0246490. https:\/\/doi.org\/10.1371\/journal.pone.0246490 (2021).","journal-title":"PLOS ONE"},{"key":"61282_CR16","doi-asserted-by":"publisher","first-page":"605","DOI":"10.22034\/apjcp.2018.19.3.605","volume":"19","author":"S Kamsa-ard","year":"2018","unstructured":"Kamsa-ard, S. et al. Risk factors for cholangiocarcinoma in thailand: a systematic review and meta-analysis. Asian Pac. J. Cancer Prev. 19, 605\u2013614. https:\/\/doi.org\/10.22034\/apjcp.2018.19.3.605 (2018).","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"61282_CR17","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1002\/hep.24351","volume":"54","author":"GL Tyson","year":"2011","unstructured":"Tyson, G. L. & El-Serag, H. B. Risk factors for cholangiocarcinoma. Hepatology 54, 173\u2013184. https:\/\/doi.org\/10.1002\/hep.24351 (2011).","journal-title":"Hepatology"},{"key":"61282_CR18","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pntd.0009741","volume":"15","author":"K Thinkhamrop","year":"2021","unstructured":"Thinkhamrop, K. et al. Association of comorbidity between Opisthorchis viverrini infection and diabetes mellitus in the development of cholangiocarcinoma among a high-risk population, northeastern Thailand. PLoS Negl. Trop. Dis. 15, e0009741. https:\/\/doi.org\/10.1371\/journal.pntd.0009741 (2021).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"61282_CR19","doi-asserted-by":"publisher","first-page":"16855","DOI":"10.1038\/s41598-020-73771-0","volume":"10","author":"K Thinkhamrop","year":"2020","unstructured":"Thinkhamrop, K. et al. Spatial analysis of hepatobiliary abnormalities in a population at high-risk of cholangiocarcinoma in Thailand. Sci. Rep. 10, 16855. https:\/\/doi.org\/10.1038\/s41598-020-73771-0 (2020).","journal-title":"Sci. Rep."},{"key":"61282_CR20","doi-asserted-by":"publisher","first-page":"14263","DOI":"10.1038\/s41598-019-50476-7","volume":"9","author":"AT Suwannatrai","year":"2019","unstructured":"Suwannatrai, A. T. et al. Bayesian spatial analysis of cholangiocarcinoma in Northeast Thailand. Sci. Rep. 9, 14263. https:\/\/doi.org\/10.1038\/s41598-019-50476-7 (2019).","journal-title":"Sci. Rep."},{"key":"61282_CR21","doi-asserted-by":"publisher","first-page":"108","DOI":"10.5114\/pg.2015.49004","volume":"10","author":"J Li","year":"2015","unstructured":"Li, J., Han, T., Xu, L. & Luan, X. Diabetes mellitus and the risk of cholangiocarcinoma: an updated meta-analysis. Prz. Gastroenterol. 10, 108\u2013117. https:\/\/doi.org\/10.5114\/pg.2015.49004 (2015).","journal-title":"Prz. Gastroenterol."},{"key":"61282_CR22","doi-asserted-by":"publisher","first-page":"2409","DOI":"10.1002\/ijc.29292","volume":"136","author":"MS Tsai","year":"2015","unstructured":"Tsai, M. S., Lee, P. H., Lin, C. L., Peng, C. L. & Kao, C. H. Type II diabetes mellitus is associated with a reduced risk of cholangiocarcinoma in patients with biliary tract diseases. Int. J. Cancer 136, 2409\u20132417. https:\/\/doi.org\/10.1002\/ijc.29292 (2015).","journal-title":"Int. J. Cancer"},{"key":"61282_CR23","doi-asserted-by":"publisher","DOI":"10.1016\/j.jcjd.2020.09.008","author":"C Saengboonmee","year":"2020","unstructured":"Saengboonmee, C., Seubwai, W., Lert-Itthiporn, W., Sanlung, T. & Wongkham, S. Association of Diabetes mellitus and cholangiocarcinoma: update of evidence and the effects of antidiabetic medication. Can. J. Diabetes https:\/\/doi.org\/10.1016\/j.jcjd.2020.09.008 (2020).","journal-title":"Can. J. Diabetes"},{"key":"61282_CR24","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1097\/CEJ.0b013e3283481d89","volume":"21","author":"W Jing","year":"2012","unstructured":"Jing, W. et al. Diabetes mellitus and increased risk of cholangiocarcinoma: a meta-analysis. Eur. J. Cancer Prev. 21, 24\u201331. https:\/\/doi.org\/10.1097\/CEJ.0b013e3283481d89 (2012).","journal-title":"Eur. J. Cancer Prev."},{"key":"61282_CR25","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1186\/1475-2867-13-99","volume":"13","author":"RQ Liu","year":"2013","unstructured":"Liu, R. Q. et al. Prognosis of the intrahepatic cholangiocarcinoma after resection: hepatitis B virus infection and adjuvant chemotherapy are favorable prognosis factors. Cancer Cell. Int. 13, 99. https:\/\/doi.org\/10.1186\/1475-2867-13-99 (2013).","journal-title":"Cancer Cell. Int."},{"key":"61282_CR26","doi-asserted-by":"publisher","first-page":"13513","DOI":"10.1038\/s41598-022-17794-9","volume":"12","author":"K Thinkhamrop","year":"2022","unstructured":"Thinkhamrop, K. et al. Associations between ultrasound screening findings and cholangiocarcinoma diagnosis in an at-risk population. Sci. Rep. 12, 13513. https:\/\/doi.org\/10.1038\/s41598-022-17794-9 (2022).","journal-title":"Sci. Rep."},{"key":"61282_CR27","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1186\/s12885-015-1475-7","volume":"15","author":"N Khuntikeo","year":"2015","unstructured":"Khuntikeo, N. et al. Cohort profile: cholangiocarcinoma screening and care program (CASCAP). BMC Cancer 15, 459. https:\/\/doi.org\/10.1186\/s12885-015-1475-7 (2015).","journal-title":"BMC Cancer"},{"key":"61282_CR28","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0171800","volume":"12","author":"KA Alene","year":"2017","unstructured":"Alene, K. A., Viney, K., McBryde, E. S. & Clements, A. C. Spatial patterns of multidrug resistant tuberculosis and relationships to socio-economic, demographic and household factors in northwest Ethiopia. PloS ONE 12, e0171800. https:\/\/doi.org\/10.1371\/journal.pone.0171800 (2017).","journal-title":"PloS ONE"},{"key":"61282_CR29","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1111\/tmi.12325","volume":"19","author":"AC Restrepo","year":"2014","unstructured":"Restrepo, A. C., Baker, P. & Clements, A. C. National spatial and temporal patterns of notified dengue cases, Colombia 2007\u20132010. Trop Med Int Health 19, 863\u2013871. https:\/\/doi.org\/10.1111\/tmi.12325 (2014).","journal-title":"Trop Med Int Health"},{"key":"61282_CR30","doi-asserted-by":"publisher","first-page":"4147","DOI":"10.31557\/APJCP.2023.24.12.4147","volume":"24","author":"H Moungthard","year":"2023","unstructured":"Moungthard, H. et al. Association of cholangiocarcinoma among people with periductal fibrosis. Asian Pac. J. Cancer. Prev. 24, 4147\u20134154. https:\/\/doi.org\/10.31557\/APJCP.2023.24.12.4147 (2023).","journal-title":"Asian Pac. J. Cancer. Prev."},{"key":"61282_CR31","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1186\/s12885-021-08247-z","volume":"21","author":"C Tawarungruang","year":"2021","unstructured":"Tawarungruang, C. et al. Survival after surgery among patients with cholangiocarcinoma in Northeast Thailand according to anatomical and morphological classification. BMC Cancer 21, 497. https:\/\/doi.org\/10.1186\/s12885-021-08247-z (2021).","journal-title":"BMC Cancer"},{"key":"61282_CR32","doi-asserted-by":"publisher","DOI":"10.1016\/j.parint.2019.102000","volume":"75","author":"R Muthukumar","year":"2020","unstructured":"Muthukumar, R. et al. Effects of Opisthorchis viverrini infection on glucose and lipid profiles in human hosts: a cross-sectional and prospective follow-up study from Thailand. Parasitol. Int. 75, 102000. https:\/\/doi.org\/10.1016\/j.parint.2019.102000 (2020).","journal-title":"Parasitol. Int."},{"key":"61282_CR33","doi-asserted-by":"publisher","first-page":"1265","DOI":"10.1016\/j.jiph.2020.05.028","volume":"13","author":"A Pengput","year":"2020","unstructured":"Pengput, A. & Schwartz, D. G. Risk factors for Opisthorchis viverrini infection: a systematic review. J. Infect. Public Health 13, 1265\u20131273. https:\/\/doi.org\/10.1016\/j.jiph.2020.05.028 (2020).","journal-title":"J. Infect. Public Health"},{"key":"61282_CR34","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1186\/s40249-018-0434-3","volume":"7","author":"JA Steele","year":"2018","unstructured":"Steele, J. A. et al. Thinking beyond Opisthorchis viverrini for risk of cholangiocarcinoma in the lower Mekong region: a systematic review and meta-analysis. Infect. Dis. Poverty 7, 44. https:\/\/doi.org\/10.1186\/s40249-018-0434-3 (2018).","journal-title":"Infect. Dis. Poverty"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-61282-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-61282-1","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-61282-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,5,7]],"date-time":"2024-05-07T19:07:21Z","timestamp":1715108841000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-61282-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,5,7]]},"references-count":34,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["61282"],"URL":"https:\/\/doi.org\/10.1038\/s41598-024-61282-1","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,5,7]]},"assertion":[{"value":"18 December 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"3 May 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 May 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"10510"}}