{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,26]],"date-time":"2026-09-26T02:23:33Z","timestamp":1790389413076,"version":"4.1.0"},"reference-count":34,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,10,8]],"date-time":"2020-10-08T00:00:00Z","timestamp":1602115200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,10,8]],"date-time":"2020-10-08T00:00:00Z","timestamp":1602115200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Khon Kaen University through CASCAP","award":["Grant No. CASCAP 1\/60"],"award-info":[{"award-number":["Grant No. CASCAP 1\/60"]}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Cholangiocarcinoma <jats:bold>(<\/jats:bold>CCA) is a serious health challenge with low survival prognosis. The liver fluke, <jats:italic>Opisthorchis viverrini<\/jats:italic>, plays a role in the aetiology of CCA, through hepatobiliary abnormalities: liver mass (LM), bile duct dilation, and periductal fibrosis (PDF). A population-based CCA screening program, the Cholangiocarcinoma Screening and Care Program, operates in Northeast Thailand. Hepatobiliary abnormalities were identified through ultrasonography. A multivariate zero-inflated, Poisson regression model measured associations between hepatobiliary abnormalities and covariates including age, sex,\u00a0distance to water resource, and history of <jats:italic>O. viverrini<\/jats:italic> infection. Geographic distribution was described using Bayesian spatial analysis methods. Hepatobiliary abnormality prevalence was 38.7%; highest in males aged\u2009&gt;\u200960\u00a0years (39.8%). PDF was most prevalent (20.1% of males). The Standardized Morbidity Ratio (SMR) for hepatobiliary abnormalities was highest in the lower and upper parts of the Northeast region. Hepatobiliary abnormalities specifically associated with CCA were also more common in males and those aged over 60\u00a0years and distributed along the Chi, Mun, and Songkram Rivers. Our findings demonstrated a high risk of hepatobiliary disorders in Northeast Thailand, likely associated with infection caused by <jats:italic>O. viverrini<\/jats:italic>. Screening for CCA and improvement of healthcare facilities to provide better treatment for CCA patients should be prioritized in these high-risk areas.<\/jats:p>","DOI":"10.1038\/s41598-020-73771-0","type":"journal-article","created":{"date-parts":[[2020,10,8]],"date-time":"2020-10-08T10:03:22Z","timestamp":1602151402000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Spatial analysis of hepatobiliary abnormalities in a population at high-risk of cholangiocarcinoma in Thailand"],"prefix":"10.1038","volume":"10","author":[{"given":"Kavin","family":"Thinkhamrop","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Apiporn T.","family":"Suwannatrai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nittaya","family":"Chamadol","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Narong","family":"Khuntikeo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bandit","family":"Thinkhamrop","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pongdech","family":"Sarakarn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Darren J.","family":"Gray","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kinley","family":"Wangdi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Archie C. A.","family":"Clements","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Matthew","family":"Kelly","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,10,8]]},"reference":[{"issue":"Suppl 2","key":"73771_CR1","first-page":"67","volume":"11","author":"MA Moore","year":"2010","unstructured":"Moore, M. A. et al. Cancer epidemiology in mainland South-East Asia\u2014past, present and future. Asian Pac. J. Cancer Prev. 11(Suppl 2), 67\u201380 (2010).","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"73771_CR2","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 (2008).","journal-title":"Curr. Opin. Gastroenterol."},{"key":"73771_CR3","first-page":"118","volume":"5","author":"P Srivatanakul","year":"2004","unstructured":"Srivatanakul, P., Sriplung, H. & Deerasamee, S. Epidemiology of liver cancer: An overview. Asian Pac. J. Cancer Prev. 5, 118\u2013125 (2004).","journal-title":"Asian Pac. J. Cancer Prev."},{"key":"73771_CR4","first-page":"20","volume":"20","author":"S Kubo","year":"2015","unstructured":"Kubo, S. et al. Screening and surveillance for occupational cholangiocarcinoma in workers exposed to organic solvents. Surg. Today 20, 20 (2015).","journal-title":"Surg. Today"},{"key":"73771_CR5","doi-asserted-by":"publisher","first-page":"E12","DOI":"10.1055\/s-0035-1555880","volume":"1","author":"FJ Fontan","year":"2015","unstructured":"Fontan, F. J., Reboredo, A. R. & Siso, A. R. Accuracy of contrast-enhanced ultrasound in the diagnosis of bile duct obstruction. Ultrasound Int. Open 1, E12-18 (2015).","journal-title":"Ultrasound Int. Open"},{"key":"73771_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 (2012).","journal-title":"Cancer Epidemiol."},{"key":"73771_CR7","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1111\/j.1478-3231.2009.02149.x","volume":"30","author":"LY Tao","year":"2010","unstructured":"Tao, L. Y. et al. Risk factors for intrahepatic and extrahepatic cholangiocarcinoma: A case\u2013control study in China. Liver Int. 30, 215\u2013221 (2010).","journal-title":"Liver Int."},{"key":"73771_CR8","doi-asserted-by":"publisher","first-page":"1221","DOI":"10.1016\/j.cgh.2007.05.020","volume":"5","author":"TM Welzel","year":"2007","unstructured":"Welzel, T. M. et al. Risk factors for intrahepatic and extrahepatic cholangiocarcinoma in the United States: A population-based case\u2013control study. Clin. Gastroenterol. Hepatol. 5, 1221\u20131228 (2007).","journal-title":"Clin. Gastroenterol. Hepatol."},{"key":"73771_CR9","doi-asserted-by":"publisher","first-page":"1016","DOI":"10.1111\/j.1572-0241.2007.01104.x","volume":"102","author":"YH Shaib","year":"2007","unstructured":"Shaib, Y. H. et al. Risk factors for intrahepatic and extrahepatic cholangiocarcinoma: A hospital-based case\u2013control study. Am. J. Gastroenterol. 102, 1016\u20131021 (2007).","journal-title":"Am. J. Gastroenterol."},{"key":"73771_CR10","doi-asserted-by":"publisher","first-page":"620","DOI":"10.1053\/j.gastro.2004.12.048","volume":"128","author":"YH Shaib","year":"2005","unstructured":"Shaib, Y. H., El-Serag, H. B., Davila, J. A., Morgan, R. & McGlynn, K. A. Risk factors of intrahepatic cholangiocarcinoma in the United States: A case\u2013control study. Gastroenterology 128, 620\u2013626 (2005).","journal-title":"Gastroenterology"},{"key":"73771_CR11","doi-asserted-by":"publisher","first-page":"1751","DOI":"10.1038\/sj.bjc.6603127","volume":"94","author":"J West","year":"2006","unstructured":"West, J., Wood, H., Logan, R. F., Quinn, M. & Aithal, G. P. Trends in the incidence of primary liver and biliary tract cancers in England and Wales 1971\u20132001. Br. J. Cancer 94, 1751\u20131758 (2006).","journal-title":"Br. J. Cancer"},{"key":"73771_CR12","unstructured":"National Cancer Institue. Guidelines for Screening, Diagnosis and Treatment of Liver Cancer and Cholangiocarcinoma. 81 (National Office of Buddhism, 2011)."},{"key":"73771_CR13","doi-asserted-by":"publisher","first-page":"1657","DOI":"10.1136\/gutjnl-2011-301748","volume":"61","author":"SA Khan","year":"2012","unstructured":"Khan, S. A. et al. Guidelines for the diagnosis and treatment of cholangiocarcinoma: An update. Gut 61, 1657\u20131669 (2012).","journal-title":"Gut"},{"key":"73771_CR14","doi-asserted-by":"publisher","first-page":"1499","DOI":"10.2214\/ajr.176.6.1761499","volume":"176","author":"Y Maetani","year":"2001","unstructured":"Maetani, Y. et al. MR imaging of intrahepatic cholangiocarcinoma with pathologic correlation. Am. J. Roentgenol. 176, 1499\u20131507 (2001).","journal-title":"Am. J. Roentgenol."},{"key":"73771_CR15","volume-title":"Imaging in Cholangiocarcinoma","author":"N Chamadol","year":"2014","unstructured":"Chamadol, N. Imaging in Cholangiocarcinoma Vol. 1 (Department of Radiology, Faculty of Medicine, Khon Kaen University, Khon Kaen, 2014)."},{"key":"73771_CR16","doi-asserted-by":"publisher","first-page":"1029","DOI":"10.1259\/bjr\/21653786","volume":"85","author":"HX Xu","year":"2012","unstructured":"Xu, H. X. et al. Contrast-enhanced ultrasound of intrahepatic cholangiocarcinoma: Correlation with pathological examination. Br. J. Radiol. 85, 1029\u20131037 (2012).","journal-title":"Br. J. Radiol."},{"key":"73771_CR17","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1002\/jhbp.64","volume":"21","author":"N Chamadol","year":"2014","unstructured":"Chamadol, N. et al. Histological confirmation of periductal fibrosis from ultrasound diagnosis in cholangiocarcinoma patients. J. Hepatobil. Pancreat. Sci. 21, 316\u2013322 (2014).","journal-title":"J. Hepatobil. Pancreat. Sci."},{"key":"73771_CR18","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/bs.apar.2018.05.002","volume":"101","author":"A Suwannatrai","year":"2018","unstructured":"Suwannatrai, A., Saichua, P. & Haswell, M. Epidemiology of Opisthorchis viverrini infection. Adv. Parasitol. 101, 41\u201367 (2018).","journal-title":"Adv. Parasitol."},{"key":"73771_CR19","doi-asserted-by":"publisher","first-page":"208","DOI":"10.1016\/j.parint.2011.07.009","volume":"61","author":"E Mairiang","year":"2012","unstructured":"Mairiang, E. et al. Ultrasonography assessment of hepatobiliary abnormalities in 3359 subjects with Opisthorchis viverrini infection in endemic areas of Thailand. Parasitol. Int. 61, 208\u2013211 (2012).","journal-title":"Parasitol. Int."},{"key":"73771_CR20","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 (2015).","journal-title":"BMC Cancer"},{"key":"73771_CR21","doi-asserted-by":"publisher","first-page":"e0171800","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\u00a0One 12, e0171800 (2017).","journal-title":"PLoS\u00a0One"},{"key":"73771_CR22","unstructured":"United States Geological Survey. Earth Resources Observation and Science (EROS) Center. https:\/\/www.usgs.gov\/centers\/eros (2020)."},{"key":"73771_CR23","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 (2019).","journal-title":"Sci. Rep."},{"key":"73771_CR24","doi-asserted-by":"publisher","first-page":"295","DOI":"10.4269\/ajtmh.1996.55.295","volume":"55","author":"DB Elkins","year":"1996","unstructured":"Elkins, D. B. et al. Cross-sectional patterns of hepatobiliary abnormalities and possible precursor conditions of cholangiocarcinoma associated with Opisthorchis viverrini infection in humans. Am. J. Trop. Med. Hyg. 55, 295\u2013301 (1996).","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"73771_CR25","doi-asserted-by":"publisher","first-page":"854","DOI":"10.1002\/ijc.21146","volume":"117","author":"S Honjo","year":"2005","unstructured":"Honjo, S. et al. Genetic and environmental determinants of risk for cholangiocarcinoma via Opisthorchis viverrini in a densely infested area in Nakhon Phanom, northeast Thailand. Int. J. Cancer 117, 854\u2013860 (2005).","journal-title":"Int. J. Cancer"},{"key":"73771_CR26","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 (2018).","journal-title":"Infect. Dis. Poverty"},{"issue":"Suppl 1","key":"73771_CR27","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 (2011).","journal-title":"Acta Trop."},{"key":"73771_CR28","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. Hepatobil. Pancreat. Sci. 21, 301\u2013308 (2014).","journal-title":"J. Hepatobil. Pancreat. Sci."},{"key":"73771_CR29","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1111\/j.1365-2249.1991.tb08151.x","volume":"84","author":"MR Haswell-Elkins","year":"1991","unstructured":"Haswell-Elkins, M. R. et al. Immune responsiveness and parasite-specific antibody levels in human hepatobiliary disease associated with Opisthorchis viverrini infection. Clin. Exp. Immunol. 84, 213\u2013218 (1991).","journal-title":"Clin. Exp. Immunol."},{"key":"73771_CR30","doi-asserted-by":"publisher","first-page":"245","DOI":"10.2306\/scienceasia1513-1874.1988.14.245","volume":"14","author":"ES Upatham","year":"1988","unstructured":"Upatham, E. S. A review of experimental and field research on the human liver fluke, Opisthorchis viverrini. J. Sci. Soc.Thai. 14, 245\u2013262 (1988).","journal-title":"J. Sci. Soc.Thai."},{"key":"73771_CR31","doi-asserted-by":"publisher","first-page":"e201","DOI":"10.1371\/journal.pmed.0040201","volume":"4","author":"B Sripa","year":"2007","unstructured":"Sripa, B. et al. Liver fluke induces cholangiocarcinoma. PLoS Med. 4, e201 (2007).","journal-title":"PLoS Med."},{"key":"73771_CR32","doi-asserted-by":"publisher","first-page":"1273","DOI":"10.1002\/hep.23134","volume":"50","author":"B Sripa","year":"2009","unstructured":"Sripa, B. et al. Advanced periductal fibrosis from infection with the carcinogenic human liver fluke Opisthorchis viverrini correlates with elevated levels of interleukin-6. Hepatology 50, 1273\u20131281 (2009).","journal-title":"Hepatology"},{"key":"73771_CR33","doi-asserted-by":"publisher","first-page":"e1481","DOI":"10.1371\/journal.pntd.0001481","volume":"6","author":"A Forrer","year":"2012","unstructured":"Forrer, A. et al. Spatial distribution of, and risk factors for, Opisthorchis viverrini infection in southern Lao PDR. PLoS Negl. Trop. Dis. 6, e1481 (2012).","journal-title":"PLoS Negl. Trop. Dis."},{"key":"73771_CR34","doi-asserted-by":"publisher","first-page":"e0004293","DOI":"10.1371\/journal.pntd.0004293","volume":"10","author":"N Khuntikeo","year":"2016","unstructured":"Khuntikeo, N. et al. Comprehensive public health conceptual framework and strategy to effectively combat cholangiocarcinoma in Thailand. PLoS Negl. Trop. Dis. 10, e0004293 (2016).","journal-title":"PLoS Negl. Trop. Dis."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-73771-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-73771-0","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-73771-0.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,6]],"date-time":"2022-12-06T20:51:43Z","timestamp":1670359903000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-73771-0"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,10,8]]},"references-count":34,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,12]]}},"alternative-id":["73771"],"URL":"https:\/\/doi.org\/10.1038\/s41598-020-73771-0","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,10,8]]},"assertion":[{"value":"20 June 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"16 September 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 October 2020","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":"16855"}}