The landscape of etiological patterns of hepatocellular carcinoma and intrahepatic cholangiocarcinoma in Thailand.

Thailand case–control study hepatocellular carcinoma intrahepatic cholangiocarcinoma risk factors

Journal

International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124

Informations de publication

Date de publication:
18 May 2024
Historique:
revised: 05 04 2024
received: 19 10 2023
accepted: 24 04 2024
medline: 18 5 2024
pubmed: 18 5 2024
entrez: 18 5 2024
Statut: aheadofprint

Résumé

Thailand is among countries with the highest global incidence and mortality rates of hepatocellular carcinoma (HCC) and intrahepatic cholangiocarcinoma (iCCA). While viral hepatitis and liver fluke infections have been associated with HCC and iCCA, respectively, other environmental risk factors, overall risk factor commonality and combinatorial roles, and effects on survival have not been systematically examined. We conducted a TIGER-LC consortium-based population study covering all high-incidence areas of both malignancies across Thailand: 837 HCC, 1474 iCCA, and 1112 controls (2011-2019) were comprehensively queried on lifelong environmental exposures, lifestyle, and medical history. Multivariate logistic regression and Cox proportional hazards analyses were used to evaluate risk factors and associated survival patterns. Our models identified shared risk factors between HCC and iCCA, such as viral hepatitis infection, liver fluke infection, and diabetes, including novel and shared associations of agricultural pesticide exposure (OR range of 1.50; 95% CI: 1.06-2.11 to 2.91; 95% CI: 1.82-4.63) along with vulnerable sources of drinking water. Most patients had multiple risk factors, magnifying their risk considerably. Patients with lower risk levels had better survival in both HCC (HR 0.78; 95% CI: 0.64-0.96) and iCCA (HR 0.84; 95% CI: 0.70-0.99). Risk factor co-exposures and their common associations with HCC and iCCA in Thailand emphasize the importance for future prevention and control measures, especially in its large agricultural sector. The observed mortality patterns suggest ways to stratify patients for anticipated survivorship and develop plans to support medical care of longer-term survivors, including behavioral changes to reduce exposures.

Identifiants

pubmed: 38761410
doi: 10.1002/ijc.35034
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : U.S. Department of Health and Human Services
ID : Z01BC010313
Organisme : Thailand Science Research and Innovation
ID : 36821/4274345
Organisme : Chulabhorn Research Institute

Informations de copyright

© 2024 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

Références

Ferlay J, Ervik M, Lam F, et al. Global Cancer Observatory: Cancer Today. International Agency for Research on Cancer; 2023:2020.
Singal AG, Lampertico P, Nahon P. Epidemiology and surveillance for hepatocellular carcinoma: new trends. J Hepatol. 2020;72:250‐261.
Liu Y, Zheng J, Hao J, et al. Global burden of primary liver cancer by five etiologies and global prediction by 2035 based on global burden of disease study 2019. Cancer Med. 2022;11:1310–1323. doi:10.1002/cam4.4551
Fung J, Lai CL, Yuen MF. Hepatitis B and C virus‐related carcinogenesis. Clin Microbiol Infect. 2009;15:964‐970.
Barsouk A, Thandra KC, Saginala K, Rawla P, Barsouk A. Chemical risk factors of primary liver cancer: an update. Hepat Med. 2020;12:179‐188.
Aleksandrova K, Boeing H, Nöthlings U, et al. Inflammatory and metabolic biomarkers and risk of liver and biliary tract cancer. Hepatology. 2014;60:858‐871.
Khan SA, Tavolari S, Brandi G. Cholangiocarcinoma: epidemiology and risk factors. Liver Int. 2019;39(Suppl 1):19‐31.
Shin HR, Oh JK, Masuyer E, et al. Epidemiology of cholangiocarcinoma: an update focusing on risk factors. Cancer Sci. 2010;101:579‐585.
Kamsa‐Ard S, Kamsa‐Ard S, Luvira V, Suwanrungruang K, Vatanasapt P, Wiangnon S. Risk factors for cholangiocarcinoma in Thailand: a systematic review and meta‐analysis. Asian Pac J Cancer Prev. 2018;19:605‐614.
Gatto M, Bragazzi MC, Semeraro R, et al. Cholangiocarcinoma: update and future perspectives. Dig Liver Dis. 2010;42:253‐260.
Srivatanakul P, Parkin DM, Khlat M, et al. Liver cancer in Thailand. II. A case‐control study of hepatocellular carcinoma. Int J Cancer. 1991;48:329‐332.
Wiangnon S, Suwanrungruang K, Kamsa‐Ard S. Cholangiocarcinoma in Khon Kaen Province. Srinagarind Med J. 2012;27:326‐330.
Yeesoonsang S, McNeil E, Virani S, et al. Trends in incidence of two major subtypes of liver and bile duct cancer: hepatocellular carcinoma and cholangiocarcinoma in Songkhla, Southern Thailand, 1989‐2030. J Cancer Epidemiol. 2018;2018:8267059.
Thinkhamrop K, Suwannatrai AT, Chamadol N, et al. Spatial analysis of hepatobiliary abnormalities in a population at high‐risk of cholangiocarcinoma in Thailand. Sci Rep. 2020;10:16855.
Liu Y, Chang CC, Marsh GM, Wu F. Population attributable risk of aflatoxin‐related liver cancer: systematic review and meta‐analysis. Eur J Cancer. 2012;48:2125‐2136.
Kwon SM, Budhu A, Woo HG, et al. Functional genomic complexity defines intratumor heterogeneity and tumor aggressiveness in liver cancer. Sci Rep. 2019;9:16930.
Haznadar M, Diehl CM, Parker AL, et al. Urinary metabolites diagnostic and prognostic of intrahepatic cholangiocarcinoma. Cancer Epidemiol Biomarkers Prev. 2019;28:1704‐1711.
Ma C, Han M, Heinrich B, et al. Gut microbiome‐mediated bile acid metabolism regulates liver cancer via NKT cells. Science. 2018;360:eaan5931. doi:10.1126/science.aan5931
Chaisaingmongkol J, Budhu A, Dang H, et al. Common molecular subtypes among Asian hepatocellular carcinoma and cholangiocarcinoma. Cancer Cell. 2017;32:57‐70.
van Buuren S, Groothuis‐Oudshoorn K. Mice: multivariate imputation by chained equations inR. J Stat Softw. 2011;45(3):1‐67.
Lê S, Josse J, Husson F. FactoMineR: an R package for multivariate analysis. J Stat Softw. 2008;25:18.
Agrawal R, Imieliński T, Swami A. Mining association rules between sets of items in large databases. SIGMOD Rec. 1993;22:207‐216.
Hahsler M. arulesViz: interactive visualization of association rules with R. R J. 2017;9:163‐175.
Wasitthankasem R, Posuwan N, Vichaiwattana P, et al. Decreasing hepatitis C virus infection in Thailand in the past decade: evidence from the 2014 National Survey. PLoS One. 2016;11:e0149362.
Udomkerdmongkol M. Thai agricultural sector: from problems to solutions. United Nations Thailand; 2020.
Virani S, Bilheem S, Chansaard W, et al. National and subnational population‐based incidence of cancer in Thailand: assessing cancers with the highest burdens. Cancer. 2017;9:108.
World Bank. World Bank Open Data. World Bank; 2023.
The Office of Agricultural Regulation. Agricultural Pesticide Import Statistics. Department of Agriculture; 2023.
IARC. Some Organophosphate Insecticides and Herbicides. World Health Organization; 2017.
VoPham T, Bertrand KA, Hart JE, et al. Pesticide exposure and liver cancer: a review. Cancer Causes Control. 2017;28:177‐190.
Myers JP, Antoniou MN, Blumberg B, et al. Concerns over use of glyphosate‐based herbicides and risks associated with exposures: a consensus statement. Environ Health. 2016;15:19.
Mesnage R, Renney G, Séralini GE, Ward M, Antoniou MN. Multiomics reveal non‐alcoholic fatty liver disease in rats following chronic exposure to an ultra‐low dose of roundup herbicide. Sci Rep. 2017;7:39328.
Yang JS, Park Y. Insecticide exposure and development of nonalcoholic fatty liver disease. J Agric Food Chem. 2018;66:10132‐10138.
Mills PJ, Caussy C, Loomba R. Glyphosate excretion is associated with steatohepatitis and advanced liver fibrosis in patients with fatty liver disease. Clin Gastroenterol Hepatol. 2020;18:741‐743.
Sripa B, Bethony JM, Sithithaworn P, et al. Opisthorchiasis and opisthorchis‐associated cholangiocarcinoma in Thailand and Laos. Acta Trop. 2011;120(Suppl 1):S158‐S168.
Boonmars T, Wu Z, Boonjaruspinyo S, et al. Involvement of c‐Ski oncoprotein in carcinogenesis of cholangiocacinoma induced by Opisthorchis viverrini and N‐nitrosodimethylamine. Pathol Oncol Res. 2011;17:219‐227.
van Tong H, Brindley PJ, Meyer CG, Velavan TP. Parasite infection, carcinogenesis and human malignancy. EBioMedicine. 2017;15:12‐23.
Suwannahitatorn P, Klomjit S, Naaglor T, et al. A follow‐up study of Opisthorchis viverrini infection after the implementation of control program in a rural community, central Thailand. Parasit Vectors. 2013;6:188.
Onsurathum S, Pinlaor P, Haonon O, et al. Effects of fermentation time and low temperature during the production process of Thai pickled fish (pla‐som) on the viability and infectivity of Opisthorchis viverrini metacercariae. Int J Food Microbiol. 2016;218:1‐5.
Suwannahitatorn P, Webster J, Riley S, Mungthin M, Donnelly CA. Uncooked fish consumption among those at risk of Opisthorchis viverrini infection in central Thailand. PLoS One. 2019;14:e0211540.
Dotto GP, Rustgi AK. Squamous cell cancers: a unified perspective on biology and genetics. Cancer Cell. 2016;29:622‐637.

Auteurs

Benjarath Pupacdi (B)

Translational Research Unit, Chulabhorn Research Institute, Bangkok, Thailand.

Christopher A Loffredo (CA)

Department of Oncology, Georgetown University Medical Center, Washington, DC, USA.

Anuradha Budhu (A)

Laboratory of Human Carcinogenesis, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland, USA.
Liver Cancer Program, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland, USA.

Siritida Rabibhadana (S)

Laboratory of Chemical Carcinogenesis, Chulabhorn Research Institute, Bangkok, Thailand.

Vajarabhongsa Bhudhisawasdi (V)

Laboratory of Chemical Carcinogenesis, Chulabhorn Research Institute, Bangkok, Thailand.
Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Chawalit Pairojkul (C)

Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Wattana Sukeepaisarnjaroen (W)

Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Ake Pugkhem (A)

Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Vor Luvira (V)

Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand.

Nirush Lertprasertsuke (N)

Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand.

Anon Chotirosniramit (A)

Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand.

Chirayu U Auewarakul (CU)

Princess Srisavangavadhana College of Medicine, Chulabhorn Royal Academy, Bangkok, Thailand.

Teerapat Ungtrakul (T)

Princess Srisavangavadhana College of Medicine, Chulabhorn Royal Academy, Bangkok, Thailand.

Thaniya Sricharunrat (T)

Pathology and Forensic Medicine Department, Chulabhorn Hospital, Chulabhorn Royal Academy, Bangkok, Thailand.

Suleeporn Sangrajrang (S)

National Cancer Institute, Bangkok, Thailand.

Kannika Phornphutkul (K)

Rajavej Hospital, Chiang Mai, Thailand.

Paul S Albert (PS)

Biostatistics Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland, USA.

Sungduk Kim (S)

Biostatistics Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Maryland, USA.

Curtis C Harris (CC)

Laboratory of Human Carcinogenesis, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland, USA.

Chulabhorn Mahidol (C)

Laboratory of Chemical Carcinogenesis, Chulabhorn Research Institute, Bangkok, Thailand.

Xin Wei Wang (XW)

Laboratory of Human Carcinogenesis, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland, USA.
Liver Cancer Program, Center for Cancer Research, National Cancer Institute, Bethesda, Maryland, USA.

Mathuros Ruchirawat (M)

Laboratory of Chemical Carcinogenesis, Chulabhorn Research Institute, Bangkok, Thailand.
Center of Excellence on Environmental Health and Toxicology (EHT), OPS, MHESI, Bangkok, Thailand.

Classifications MeSH