The Hepatobiliary Cancer Working Group

Hepatobiliary cancers are a group of primary malignancies encompassing the liver, the intrahepatic and extrahepatic biliary tracts, and the gall bladder. Within the liver, the most common primary cancer is hepatocellular carcinoma (HCC), which arises from hepatocytes and comprises more than 90% of all primary liver cancers. Primary liver cancers are the fourth most common cause of cancer death worldwide and rank seventh of all cancers in overall age-standardized incidence rates. For HCC, both the incidence rates and the mortality rates are higher in men than in women; the opposite is apparent for cancers of the gall bladder. These malignancies are highly lethal, in part because they have vague symptomology and are often diagnosed in late, advanced stages.

Established risk factors for HCC are chronic hepatitis infection, heavy alcohol consumption, and exposure to aflatoxin; considerable data also support obesity as a major emerging risk factor. Data from prospective cohort studies on dietary and lifestyle risk factors for hepatobiliary cancers are sparse, as are data on metabolic perturbations and underlying mechanisms in the development of these cancers. The main objective of the Hepatobiliary Cancer Working Group is the provision of reliable, robust findings on the etiology, dietary and lifestyle determinants, and genetic and metabolic contributors to the development of these cancers.

To date, the Working Group has explored associations of HCC risk with the role of dietary patterns, individual food groups, specific foods, and nutrients. The findings show strong positive HCC risk associations for obesity, adult weight gain, physical inactivity, diabetes, smoking, heavy alcohol consumption, and chronic hepatitis infection.

Higher HCC risk has also been observed for higher consumption of simple sugars, sugary drinks, dairy products (particularly milk and cheese, but not yogurt) and for lower intake of vegetables, dietary fibres, fish, flavanols, antioxidant nutrients, and monounsaturated fatty acids. The findings of the Working Group also support the strong inverse HCC risk associations observed in many world regions for higher consumption of coffee, but also demonstrate that the association is partly accounted for by inflammation and hepatocellular injury.

Using a case–control design nested within the EPIC cohort, the Working Group has assessed biomarker levels in baseline blood samples and delved into some underlying mechanisms of HCC development. The publications from the Working Group demonstrate positive HCC risk associations for lower circulating pre-diagnostic concentrations of vitamin D, zinc, selenium, and selenoprotein P, along with higher inflammation, hyperinsulinaemia, and increasing degree of liver dysfunction. The Working Group has also conducted extensive untargeted (using nuclear magnetic resonance and high-resolution liquid chromatography-mass spectroscopy) and targeted (Biocrates AbsoluteIDQ p180 kit) metabolomic analyses. These analyses demonstrate imbalance and perturbation of amino acid, biogenic amine, bile acid, fatty acid oxidation, lipid, and carbohydrate metabolism in HCC development, apparent from several years before diagnosis. The Working Group has also demonstrated a role for gut barrier dysfunction in HCC development, possibly linked to an effect of unhealthy dietary patterns and possible gut microbiome dysbiosis.

The findings of the Working Group highlight the importance of healthy dietary and lifestyle patterns for HCC prevention, and they highlight potential underlying mechanisms. Future efforts of the Working Group will concentrate on further elaborating these observations for HCC and focusing additional efforts on assessing risk factors for biliary tract cancers.

 

Selected publications

  1. Stepien M, Lopez-Nogueroles M, Lahoz A, Kühn T, Perlemuter G, Voican C, et al. (2022). Prediagnostic alterations in circulating bile acid profiles in the development of hepatocellular carcinoma. Int J Cancer. 150(8):1255–68. https://doi.org/10.1002/ijc.33885 PMID:34843121
  2. Loftfield E, Stepien M, Viallon V, Trijsburg L, Rothwell JA, Robinot N, et al. (2021). Novel biomarkers of habitual alcohol intake and associations with risk of pancreatic and liver cancers and liver disease mortality. J Natl Cancer Inst. 113(11):1542–50. https://doi.org/10.1093/jnci/djab078 PMID:34010397
  3. Mayén AL, Aglago EK, Knaze V, Cordova R, Schalkwijk CG, Wagner KH, et al. (2021). Dietary intake of advanced glycation endproducts and risk of hepatobiliary cancers: a multinational cohort study. Int J Cancer. 149(4):854–64. https://doi.org/10.1002/ijc.33612 PMID:33899229
  4. Stepien M, Keski-Rahkonen P, Kiss A, Robinot N, Duarte-Salles T, Murphy N, et al. (2021). Metabolic perturbations prior to hepatocellular carcinoma diagnosis: findings from a prospective observational cohort study. Int J Cancer. 148(3):609–25. https://doi.org/10.1002/ijc.33236 PMID:32734650
  5. Baumeister SE, Schlesinger S, Aleksandrova K, Jochem C, Jenab M, Gunter MJ, et al. (2019). Association between physical activity and risk of hepatobiliary cancers: a multinational cohort study. J Hepatol. 70(5):885–92. https://doi.org/10.1016/j.jhep.2018.12.014 PMID:30582978
  6. Assi N, Gunter MJ, Thomas DC, Leitzmann M, Stepien M, Chajès V, et al. (2018). Metabolic signature of healthy lifestyle and its relation with risk of hepatocellular carcinoma in a large European cohort. Am J Clin Nutr. 108(1):117–26. https://doi.org/10.1093/ajcn/nqy074 PMID:29924298
  7. Assi N, Thomas DC, Leitzmann M, Stepien M, Chajès V, Philip T, et al. (2018). Are metabolic signatures mediating the relationship between lifestyle factors and hepatocellular carcinoma risk? Results from a nested case-control study in EPIC. Cancer Epidemiol Biomarkers Prev. 27(5):531–40. https://doi.org/10.1158/1055-9965.EPI-17-0649 PMID:29563134
  8. Fedirko V, Tran HQ, Gewirtz AT, Stepien M, Trichopoulou A, Aleksandrova K, et al. (2017). Exposure to bacterial products lipopolysaccharide and flagellin and hepatocellular carcinoma: a nested case-control study. BMC Med. 15(1):72. https://doi.org/10.1186/s12916-017-0830-8 PMID:28372583
  9. Stepien M, Hughes DJ, Hybsier S, Bamia C, Tjønneland A, Overvad K, et al. (2017). Circulating copper and zinc levels and risk of hepatobiliary cancers in Europeans. Br J Cancer. 116(5):688–96. https://doi.org/10.1038/bjc.2017.1 PMID:28152549
  10. Hughes DJ, Duarte-Salles T, Hybsier S, Trichopoulou A, Stepien M, Aleksandrova K, et al. (2016). Prediagnostic selenium status and hepatobiliary cancer risk in the European Prospective Investigation into Cancer and Nutrition cohort. Am J Clin Nutr. 104(2):406–14. https://doi.org/10.3945/ajcn.116.131672 PMID:27357089
  11. Duarte-Salles T, Misra S, Stepien M, Plymoth A, Muller D, Overvad K, et al. (2016). Circulating osteopontin and prediction of hepatocellular carcinoma development in a large European population. Cancer Prev Res (Phila). 9(9):758–65. https://doi.org/10.1158/1940-6207.CAPR-15-0434 PMID:27339170
  12. Stepien M, Fedirko V, Duarte-Salles T, Ferrari P, Freisling H, Trepo E, et al. (2016). Prospective association of liver function biomarkers with development of hepatobiliary cancers. Cancer Epidemiol. 40:179–87. https://doi.org/10.1016/j.canep.2016.01.002 PMID:26773278
  13. Aleksandrova K, Bamia C, Drogan D, Lagiou P, Trichopoulou A, Jenab M, et al. (2015). The association of coffee intake with liver cancer risk is mediated by biomarkers of inflammation and hepatocellular injury: data from the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr. 102(6):1498–508. https://doi.org/10.3945/ajcn.115.116095 PMID:26561631
  14. Fages A, Duarte-Salles T, Stepien M, Ferrari P, Fedirko V, Pontoizeau C, et al. (2015). Metabolomic profiles of hepatocellular carcinoma in a European prospective cohort. BMC Med. 13(1):242. https://doi.org/10.1186/s12916-015-0462-9 PMID:26399231
  15. Stepien M, Duarte-Salles T, Fedirko V, Floegel A, Barupal DK, Rinaldi S, et al. (2016). Alteration of amino acid and biogenic amine metabolism in hepatobiliary cancers: findings from a prospective cohort study. Int J Cancer. 138(2):348–60. https://doi.org/10.1002/ijc.29718 PMID:26238458
  16. Assi N, Fages A, Vineis P, Chadeau-Hyam M, Stepien M, Duarte-Salles T, et al. (2015). A statistical framework to model the meeting-in-the-middle principle using metabolomic data: application to hepatocellular carcinoma in the EPIC study. Mutagenesis. 30(6):743–53. https://doi.org/10.1093/mutage/gev045 PMID:26130468
  17. Duarte-Salles T, Fedirko V, Stepien M, Aleksandrova K, Bamia C, Lagiou P, et al. (2015). Dietary fat, fat subtypes and hepatocellular carcinoma in a large European cohort. Int J Cancer. 137(11):2715–28. https://doi.org/10.1002/ijc.29643 PMID:26081477
  18. Bamia C, Lagiou P, Jenab M, Aleksandrova K, Fedirko V, Trichopoulos D, et al. (2015). Fruit and vegetable consumption in relation to hepatocellular carcinoma in a multi-centre, European cohort study. Br J Cancer. 112(7):1273–82. https://doi.org/10.1038/bjc.2014.654 PMID:25742480
  19. Stepien M, Duarte-Salles T, Fedirko V, Trichopoulou A, Lagiou P, Bamia C, et al. (2016). Consumption of soft drinks and juices and risk of liver and biliary tract cancers in a European cohort. Eur J Nutr. 55(1):7–20. https://doi.org/10.1007/s00394-014-0818-5 PMID:25528243
  20. Bamia C, Lagiou P, Jenab M, Trichopoulou A, Fedirko V, Aleksandrova K, et al. (2015). Coffee, tea and decaffeinated coffee in relation to hepatocellular carcinoma in a European population: multicentre, prospective cohort study. Int J Cancer. 136(8):1899–908. https://doi.org/10.1002/ijc.29214 PMID:25219573
  21. Fedirko V, Duarte-Salles T, Bamia C, Trichopoulou A, Aleksandrova K, Trichopoulos D, et al. (2014). Prediagnostic circulating vitamin D levels and risk of hepatocellular carcinoma in European populations: a nested case-control study. Hepatology. 60(4):1222–30. https://doi.org/10.1002/hep.27079 PMID:24644045
  22. Duarte-Salles T, Fedirko V, Stepien M, Trichopoulou A, Bamia C, Lagiou P, et al. (2014). Dairy products and risk of hepatocellular carcinoma: the European Prospective Investigation into Cancer and Nutrition. Int J Cancer. 135(7):1662–72. https://doi.org/10.1002/ijc.28812 PMID:24615266
  23. Aleksandrova K, Boeing H, Nöthlings U, Jenab M, Fedirko V, Kaaks R, et al. (2014). Inflammatory and metabolic biomarkers and risk of liver and biliary tract cancer. Hepatology. 60(3):858–71. https://doi.org/10.1002/hep.27016 PMID:24443059
  24. Lukanova A, Becker S, Hüsing A, Schock H, Fedirko V, Trepo E, et al. (2014). Prediagnostic plasma testosterone, sex hormone-binding globulin, IGF-I and hepatocellular carcinoma: etiological factors or risk markers? Int J Cancer. 134(1):164–73. https://doi.org/10.1002/ijc.28342 PMID:23801371
  25. Schlesinger S, Aleksandrova K, Pischon T, Jenab M, Fedirko V, Trepo E, et al. (2013). Diabetes mellitus, insulin treatment, diabetes duration, and risk of biliary tract cancer and hepatocellular carcinoma in a European cohort. Ann Oncol. 24(9):2449–55. https://doi.org/10.1093/annonc/mdt204 PMID:23720454
  26. Fedirko V, Trichopolou A, Bamia C, Duarte-Salles T, Trepo E, Aleksandrova K, et al. (2013). Consumption of fish and meats and risk of hepatocellular carcinoma: the European Prospective Investigation into Cancer and Nutrition (EPIC). Ann Oncol. 24(8):2166–73. https://doi.org/10.1093/annonc/mdt168 PMID:23670094
  27. Zamora-Ros R, Fedirko V, Trichopoulou A, González CA, Bamia C, Trepo E, et al. (2013). Dietary flavonoid, lignan and antioxidant capacity and risk of hepatocellular carcinoma in the European Prospective Investigation into Cancer and Nutrition study. Int J Cancer. 133(10):2429–43. https://doi.org/10.1002/ijc.28257 PMID:23649669
  28. Fedirko V, Lukanova A, Bamia C, Trichopolou A, Trepo E, Nöthlings U, et al. (2013). Glycemic index, glycemic load, dietary carbohydrate, and dietary fiber intake and risk of liver and biliary tract cancers in Western Europeans. Ann Oncol. 24(2):543–53. https://doi.org/10.1093/annonc/mds434 PMID:23123507
  29. Schlesinger S, Aleksandrova K, Pischon T, Fedirko V, Jenab M, Trepo E, et al. (2013). Abdominal obesity, weight gain during adulthood and risk of liver and biliary tract cancer in a European cohort. Int J Cancer. 132(3):645–57. https://doi.org/10.1002/ijc.27645 PMID:22618881
  30. Trichopoulos D, Bamia C, Lagiou P, Fedirko V, Trepo E, Jenab M, et al. (2011). Hepatocellular carcinoma risk factors and disease burden in a European cohort: a nested case-control study. J Natl Cancer Inst. 103(22):1686–95. https://doi.org/10.1093/jnci/djr395 PMID:22021666
  31. Jenab M, Boffetta P (2010). Glycemic index and glycemic load: application in observational studies and association with hepatocellular carcinoma risk. Meaningful or error prone? Ann Oncol. 21(3):437–9. https://doi.org/10.1093/annonc/mdq016 PMID:20176692

 

Contact details/Working Group leader

Mazda Jenab, PhD
Team Leader, Onco-Metabolomics Team (OMB), Nutrition and Metabolism Branch (NME)
International Agency for Research on Cancer (IARC/WHO)
25 avenue Tony Garnier
CS 90627
69366 LYON CEDEX 07
France
JenabM@iarc.who.int