Variation in the risk for liver and gallbladder cancers in socioeconomic and occupational groups in Sweden with etiological implications

  • Jianguang Ji
  • Kari Hemminki
Original Article


Objectives: To examine the associations between socioeconomic/occupational factors and liver cancer at various anatomic sites (including primary liver, gallbladder and other cancers). Methods: We carried out a follow-up study on the economically active Swedish population, based on the Swedish Family-Cancer Database. Standardized incidence ratios (SIRs) and 95% confidence intervals (CIs) were calculated in different social classes and occupations. Results: For primary liver cancer, farmers were at a decreased risk; increased risks were observed for male sales agents, journalists, seamen, waiters, cooks and female beverage manufacture workers. Similar patterns were observed for gallbladder cancer; workers employed as journalists, sales agents, cooks and stewards, and public safety workers showed increased risk. Only male transport workers showed increased risk of cancers in other parts. Conclusions: Occupations with high consumption of alcohol and/or high prevalence of smoking associated with a risk of liver and gallbladder cancers. The present study suggests that the effects of socioeconomic factors on liver cancer of different subsites are similar; alcohol drinking is a risk factor of gallbladder cancer because of the covariation of primary liver and gallbladder cancers in occupational groups.


Liver cancer Primary gall bladder cancer Occupational exposures Follow-up study 



The Family-Cancer Database was created by linking registers maintained at Statistics Sweden and the Swedish Cancer Registry. The study was supported by the Swedish Cancer Society.


  1. Acalovschi M, Badea R, Dumitrascu D, Varga C (1988) Prevalence of gallstones in liver cirrhosis: a sonographic survey. Am J Gastroenterol 83:954–956PubMedGoogle Scholar
  2. Adami HO, Hsing AW, McLaughlin JK, Trichopoulos D, Hacker D, Ekbom A, Persson I (1992) Alcoholism and liver cirrhosis in the etiology of primary liver cancer. Int J Cancer 51:898–902PubMedCrossRefGoogle Scholar
  3. Andersen A, Barlow L, Engeland A, Kjaerheim K, Lynge E, Pukkala E (1999) Work-related cancer in the Nordic countries. Scand J Work Environ Health 25(Suppl 2):1–116PubMedGoogle Scholar
  4. Blair A, Kazerouni N (1997) Reactive chemicals and cancer. Cancer Causes Control 8:473–490CrossRefPubMedGoogle Scholar
  5. Carstensen JM, Pershagen G, Eklund G (1988) Smoking-adjusted incidence of lung cancer among Swedish men in different occupations. Int J Epidemiol 17:753–758PubMedCrossRefGoogle Scholar
  6. Center for Epidemiology (1999) Cancer Incidence in Sweden 1997. The National Board of Health and Welfare, StockholmGoogle Scholar
  7. Center for Epidemiology (2002) Cancer Incidence in Sweden 2000. The National Board of Health and Welfare, StockholmGoogle Scholar
  8. Chow WH, McLaughlin JK, Zheng W, Blot WJ, Gao YT (1993) Occupational risks for primary liver cancer in Shanghai, China. Am J Ind Med 24:93–100PubMedCrossRefGoogle Scholar
  9. Colombo M (1992) Hepatocellular carcinoma. J Hepatol 15:225–236CrossRefPubMedGoogle Scholar
  10. Davey JD, Obst PL, Sheehan MC (2000) Developing a profile of alcohol consumption patterns of police officers in a large-scale sample of an Australian police service. Eur Addict Res 6:205–212CrossRefPubMedGoogle Scholar
  11. Deuffic S, Poynard T, Buffat L, Valleron AJ (1998) Trends in primary liver cancer. Lancet 351:214–215CrossRefPubMedGoogle Scholar
  12. Diehl AK (1983) Gallstone size and the risk of gallbladder cancer. JAMA 250:2323–2326CrossRefPubMedGoogle Scholar
  13. Dubrow R, Wegman DH (1984) Cancer and occupation in Massachusetts: a death certificate study. Am J Ind Med 6:207–230PubMedCrossRefGoogle Scholar
  14. El-Serag HB, Mason AC (1999) Rising incidence of hepatocellular carcinoma in the United States. N Engl J Med 340:745–750CrossRefPubMedGoogle Scholar
  15. Fleisher JM (1990) Occupational and non-occupational risk factors in relation to an excess of primary liver cancer observed among residents of Brooklyn, New York. Cancer 65:180–185PubMedCrossRefGoogle Scholar
  16. Fornari F, Civardi G, Buscarini E, Cavanna L, Imberti D, Rossi S, Sbolli G, Di Stasi M, Buscarini L (1990) Cirrhosis of the liver. A risk factor for development of cholelithiasis in males. Dig Dis Sci 35:1403–1408CrossRefPubMedGoogle Scholar
  17. Godley PA, Sandler RS (1994) Liver cancer. In: Everhart JE (ed) Digestive diseases in the United States: epidemiology and impact. US Government Printing Office, Washington DCGoogle Scholar
  18. Hamilton SR, Aaltonen LA (2000) World Health Organization classification of tumours. Pathology and genetics of tumours of the digestive system. IARC Press, LyonGoogle Scholar
  19. Hemmingsson T, Lundberg I, Romelsjo A, Alfredsson L (1997) Alcoholism in social classes and occupations in Sweden. Int J Epidemiol 26:584–591CrossRefPubMedGoogle Scholar
  20. Hemminki K, Li X, Plna K, Granstrom C, Vaittinen P (2001) The nation-wide Swedish family-cancer database—updated structure and familial rates. Acta Oncol 40:772–777CrossRefPubMedGoogle Scholar
  21. Hernberg S, Korkala ML, Asikainen U, Riala R (1984) Primary liver cancer and exposure to solvents. Int Arch Occup Environ Health 54:147–153CrossRefPubMedGoogle Scholar
  22. Hoffmann G, Berglund G, Elmstahl S, Eriksson S, Verbaan H, Widell A, Lindgren S (2000) Prevalence and clinical spectrum of chronic viral hepatitis in a middle-aged Swedish general urban population. Scand J Gastroenterol 35:861–865CrossRefPubMedGoogle Scholar
  23. Houten L, Sonnesso G (1980) Occupational exposure and cancer of the liver. Arch Environ Health 35:51–53PubMedGoogle Scholar
  24. IARC (2004) IARC Monographs on the evaluation of the carcinogenic risk of chemicals to humans: tobacco smoke and involuntary smoking. World Health Organization, LyonGoogle Scholar
  25. IARC: GLOBOCAN 2000 (2001) Cancer incidence, mortality and preventive worldwide. IARC, LyonGoogle Scholar
  26. Inoue H, Seitz HK (2001) Viruses and alcohol in the pathogenesis of primary hepatic carcinoma. Eur J Cancer Prev 10:107–110CrossRefPubMedGoogle Scholar
  27. Jensen OM (1979) Cancer morbidity and causes of death among Danish brewery workers. Int J Cancer 23:454–463PubMedCrossRefGoogle Scholar
  28. Kauppinen T, Riala R, Seitsamo J, Hernberg S (1992) Primary liver cancer and occupational exposure. Scand J Work Environ Health 18:18–25PubMedGoogle Scholar
  29. Khan ZR, Neugut AI, Ahsan H, Chabot JA (1999) Risk factors for biliary tract cancers. Am J Gastroenterol 94:149–152CrossRefPubMedGoogle Scholar
  30. Kono S, Kochi S, Ohyama S, Wakisaka A (1988) Gallstones, serum lipids, and glucose tolerance among male officials of Self-Defense Forces in Japan. Dig Dis Sci 33:839–844CrossRefPubMedGoogle Scholar
  31. Kuper H, Tzonou A, Kaklamani E, Hsieh CC, Lagiou P, Adami HO, Trichopoulos D, Stuver SO (2000) Tobacco smoking, alcohol consumption and their interaction in the causation of hepatocellular carcinoma. Int J Cancer 85:498–502CrossRefPubMedGoogle Scholar
  32. Lazcano-Ponce EC, Miquel JF, Munoz N, Herrero R, Ferrecio C, Wistuba II, Alonso de Ruiz P, Aristi Urista G, Nervi F (2001) Epidemiology and molecular pathology of gallbladder cancer. CA Cancer J Clin 51:349–364PubMedGoogle Scholar
  33. Lowenfels AB, Walker AM, Althaus DP, Townsend G, Domellof L (1989) Gallstone growth, size, and risk of gallbladder cancer: an interracial study. Int J Epidemiol 18:50–54PubMedCrossRefGoogle Scholar
  34. Maclure KM, Hayes KC, Colditz GA, Stampfer MJ, Speizer FE, Willett WC (1989) Weight, diet, and the risk of symptomatic gallstones in middle-aged women. N Engl J Med 321:563–569PubMedCrossRefGoogle Scholar
  35. Maclure KM, Hayes KC, Colditz GA, Stampfer MJ, Willett WC (1990) Dietary predictors of symptom-associated gallstones in middle-aged women. Am J Clin Nutr 52:916–922PubMedGoogle Scholar
  36. Moerman CJ, Bueno de Mesquita HB, Smeets FW, Runia S (1997) Lifestyle factors including diet and cancer of the gallbladder and bile duct: a population-based case-control study in The Netherlands. Eur J Cancer Prev 6:139–142PubMedGoogle Scholar
  37. Okuda K, Fujimoto I, Hanai A, Urano Y (1987) Changing incidence of hepatocellular carcinoma in Japan. Cancer Res 47:4967–4972PubMedGoogle Scholar
  38. Parkin DM, Pisani P, Ferlay J (1999) Estimates of the worldwide incidence of 25 major cancers in 1990. Int J Cancer 80:827–841CrossRefPubMedGoogle Scholar
  39. Pixley F, Wilson D, McPherson K, Mann J (1985) Effect of vegetarianism on development of gallstones in women. Br Med J (Clin Res Ed) 291:11–12Google Scholar
  40. Porru S, Placidi D, Carta A, Gelatti U, Ribero ML, Tagger A, Boffetta P, Donato F (2001) Primary liver cancer and occupation in men: a case-control study in a high-incidence area in Northern Italy. Int J Cancer 94:878–883CrossRefPubMedGoogle Scholar
  41. Pukkala E (1995) Cancer risk by social class and occupations: a survey of 109,000 cancer cases among Finns of working age. Karger, BaselGoogle Scholar
  42. Ramstedt M (2001) Per capita alcohol consumption and liver cirrhosis mortality in 14 European countries. Addiction 96(Suppl 1):S19–S33CrossRefPubMedGoogle Scholar
  43. Stemhagen A, Slade J, Altman R, Bill J (1983) Occupational risk factors and liver cancer. A retrospective case-control study of primary liver cancer in New Jersey. Am J Epidemiol 117:443–454PubMedGoogle Scholar
  44. Strom BL, Soloway RD, Rios-Dalenz JL, Rodriguez-Martinez HA, West SL, Kinman JL, Polansky M, Berlin JA (1995) Risk factors for gallbladder cancer. An international collaborative case-control study. Cancer 76:1747–1756PubMedCrossRefGoogle Scholar
  45. Taylor-Robinson SD, Foster GR, Arora S, Hargreaves S, Thomas HC (1997) Increase in primary liver cancer in the UK, 1979–1994. Lancet 350:1142–1143CrossRefPubMedGoogle Scholar
  46. Tazuma S, Kajiyama G (2001) Carcinogenesis of malignant lesions of the gall bladder. The impact of chronic inflammation and gallstones. Langenbecks Arch Surg 386:224–229CrossRefPubMedGoogle Scholar
  47. Trichopoulos D, Day NE, Kaklamani E, Tzonou A, Munoz N, Zavitsanos X, Koumantaki Y, Trichopoulou A (1987) Hepatitis B virus, tobacco smoking and ethanol consumption in the etiology of hepatocellular carcinoma. Int J Cancer 39:45–49PubMedCrossRefGoogle Scholar
  48. Tseng M, Everhart JE, Sandler RS (1999) Dietary intake and gallbladder disease: a review. Public Health Nutr 2:161–172PubMedCrossRefGoogle Scholar
  49. Widell A, Verbaan H, Wejstal R, Kaczynski J, Kidd-Ljunggren K, Wallerstedt S (2000) Hepatocellular carcinoma in Sweden: its association with viral hepatitis, especially with hepatitis C viral genotypes. Scand J Infect Dis 32:147–152CrossRefPubMedGoogle Scholar
  50. Williams CN, Johnston JL (1980) Prevalence of gallstones and risk factors in Caucasian women in a rural Canadian community. Can Med Assoc J 122:664–668PubMedGoogle Scholar
  51. Zatonski WA, La Vecchia C, Przewozniak K, Maisonneuve P, Lowenfels AB, Boyle P (1992) Risk factors for gallbladder cancer: a Polish case-control study. Int J Cancer 51:707–711PubMedCrossRefGoogle Scholar
  52. Zatonski WA, Lowenfels AB, Boyle P, Maisonneuve P, Bueno de Mesquita HB, Ghadirian P, Jain M, Przewozniak K, Baghurst P, Moerman CJ, Simard A, Howe GR, McMichael AJ, Hsieh CC, Walker AM (1997) Epidemiologic aspects of gallbladder cancer: a case-control study of the SEARCH Program of the International Agency for Research on Cancer. J Natl Cancer Inst 89:1132–1138CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Bioscience at NovumKarolinska InstitutetHuddingeSweden
  2. 2.Division of Molecular Genetic EpidemiologyGerman Cancer Research Center (DKFZ)HeidelbergGermany

Personalised recommendations