Diabetes mellitus and risk of hepatocellular carcinoma: A systematic review and meta-analysis

Diabetes/Metabolism Research and Reviews

Volumn 28, Issue 2, 2012, Pages 109-122

  Wang, Ping ^a,b   Kang, Donghong ^b   Cao, Wei ^b   Wang, Yan ^a   Liu, Zhiwen ^a  

^a SHANDONG UNIVERSITY   (China)

^b THE FIRST AFFILIATED HOSPITAL OF SHANDONG FIRST MEDICAL UNIVERSITY   (China)

Author keywords

Case control; Cohort; Diabetes; Hepatocellular carcinoma; Meta analysis

Indexed keywords

INSULIN; METFORMIN; SULFONYLUREA;

ALCOHOL CONSUMPTION; BODY MASS; CANCER MORTALITY; CANCER PREVENTION; CANCER RISK; DIABETES MELLITUS; DISEASE DURATION; GENDER; HUMAN; INSULIN TREATMENT; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; META ANALYSIS; PRIORITY JOURNAL; REVIEW; SMOKING; SYSTEMATIC REVIEW;

CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; COHORT STUDIES; DIABETES COMPLICATIONS; DIABETES MELLITUS; HUMANS; INSULIN; LIVER NEOPLASMS; METFORMIN; RISK; SULFONYLUREA COMPOUNDS;

EID: 84863010936     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.1291     Document Type: Review

References (75)

1. Gomaa AI, Khan SA, Toledano MB, Waked I, Taylor-Robinson SD. Hepatocellular carcinoma: epidemiology, risk factors and pathogenesis. World J Gastroenterol 2008; 14(27): 4300-4308.
2. El-Serag HB, Davila JA, Petersen NJ, McGlynn KA. The continuing increase in the incidence of hepatocellular carcinoma in the United States: an update. Ann Intern Med 2003; 139(10): 817-823.
3. Yuen MF, Hou JL, Chutaputti A. Hepatocellular carcinoma in the Asia pacific region. J Gastroenterol Hepatol 2009; 24(3): 346-353.
4. El-Serag HB, Hampel H, Javadi F. The association between diabetes and hepatocellular carcinoma: a systematic review of epidemiologic evidence. Clin Gastroenterol Hepatol 2006; 4(3): 369-380.
5. Friberg E, Orsini N, Mantzoros CS, Wolk A. Diabetes mellitus and risk of endometrial cancer: a meta-analysis. Diabetologia 2007; 50(7): 1365-1374.
6. Huxley R, Ansary-Moghaddam A, Berrington de Gonzalez A, Barzi F, Woodward M. Type-II diabetes and pancreatic cancer: a meta-analysis of 36 studies. Br J Cancer 2005; 92(11): 2076-2083.
7. Stein KB, Snyder CF, Barone BB, Yeh HC, Peairs KS, Derr RL, et al. Colorectal cancer outcomes, recurrence, and complications in persons with and without diabetes mellitus: a systematic review and meta-analysis. Dig Dis Sci; 55(7): 1839-1851.
8. Xue F, Michels KB. Diabetes, metabolic syndrome, and breast cancer: a review of the current evidence. Am J Clin Nutr 2007; 86(3): s823-835.
9. Byrne CD, Olufadi R, Bruce KD, Cagampang FR, Ahmed MH. Metabolic disturbances in non-alcoholic fatty liver disease. Clin Sci (Lond) 2009; 116(7): 539-564.
10. Falck-Ytter Y, Younossi ZM, Marchesini G, McCullough AJ. Clinical features and natural history of nonalcoholic steatosis syndromes. Semin Liver Dis 2001; 21(1): 17-26.
11. Cuadrado A, Orive A, Garcia-Suarez C, Dominguez A, Fernandez-Escalante JC, Crespo J, et al. Non-alcoholic steatohepatitis (NASH) and hepatocellular carcinoma. Obes Surg 2005; 15(3): 442-446.
12. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315(7109): 629-634.
13. Braga C, La Vecchia C, Negri E, Franceschi S. Attributable risks for hepatocellular carcinoma in northern Italy. Eur J Cancer 1997; 33(4): 629-634.
14. Hjalgrim H, Frisch M, Ekbom A, Kyvik KO, Melbye M, Green A. Cancer and diabetes - a follow-up study of two population-based cohorts of diabetic patients. J Intern Med 1997; 241(6): 471-475.
15. Jee SH, Ohrr H, Sull JW, Yun JE, Ji M, Samet JM. Fasting serum glucose level and cancer risk in Korean men and women. Jama 2005; 293(2): 194-202.
16. Ragozzino M, Melton LJ 3rd, Chu CP, Palumbo PJ. Subsequent cancer risk in the incidence cohort of Rochester, Minnesota, residents with diabetes mellitus. J Chronic Dis 1982; 35(1): 13-19.
17. Polesel J, Zucchetto A, Montella M, Dal Maso L, Crispo A, La Vecchia C, et al. The impact of obesity and diabetes mellitus on the risk of hepatocellular carcinoma. Ann Oncol 2009; 20(2): 353-357.
18. Rousseau MC, Parent ME, Pollak MN, Siemiatycki J. Diabetes mellitus and cancer risk in a population-based case-control study among men from Montreal, Canada. Int J Cancer 2006; 118(8): 2105-2109.
19. Davila JA, Morgan RO, Shaib Y, McGlynn KA, El-Serag HB. Diabetes increases the risk of hepatocellular carcinoma in the United States: a population based case control study. Gut 2005; 54(4): 533-539.
20. Yuan JM, Govindarajan S, Arakawa K, Yu MC. Synergism of alcohol, diabetes, and viral hepatitis on the risk of hepatocellular carcinoma in blacks and whites in the U.S. Cancer 2004; 101(5): 1009-1017.
21. Matsuo M. Association between diabetes mellitus and hepatocellular carcinoma: results of a hospital- and community-based case-control study. Kurume Med J 2003; 50(3-4): 91-98.
22. Hassan MM, Hwang LY, Hatten CJ, Swaim M, Li D, Abbruzzese JL, et al. Risk factors for hepatocellular carcinoma: synergism of alcohol with viral hepatitis and diabetes mellitus. Hepatology 2002; 36(5): 1206-1213.
23. El-Serag HB, Richardson PA, Everhart JE. The role of diabetes in hepatocellular carcinoma: a case-control study among United States veterans. Am J Gastroenterol 2001; 96(8): 2462-2467.
24. Lagiou P, Kuper H, Stuver SO, Tzonou A, Trichopoulos D, Adami HO. Role of diabetes mellitus in the etiology of hepatocellular carcinoma. J Natl Cancer Inst 2000; 92(13): 1096-1099.
25. Shibata A, Fukuda K, Nishiyori A, Ogimoto I, Sakata R, Tanikawa K. A case-control study on male hepatocellular carcinoma based on hospital and community controls. J Epidemiol 1998; 8(1): 1-5.
26. La Vecchia C, Negri E, Decarli A, Franceschi S. Diabetes mellitus and the risk of primary liver cancer. Int J Cancer 1997; 73(2): 204-207.
27. Hadziyannis S, Tabor E, Kaklamani E, Tzonou A, Stuver S, Tassopoulos N, et al. A case-control study of hepatitis B and C virus infections in the etiology of hepatocellular carcinoma. Int J Cancer 1995; 60(5): 627-631.
28. Fukuda K, Shibata A, Hirohata I, Tanikawa K, Yamaguchi G, Ishii M. A hospital-based case-control study on hepatocellular carcinoma in Fukuoka and Saga Prefectures, northern Kyushu, Japan. Jpn J Cancer Res 1993; 84(7): 708-714.
29. Yu MC, Tong MJ, Govindarajan S, Henderson BE. Nonviral risk factors for hepatocellular carcinoma in a low-risk population, the non-Asians of Los Angeles County, California. J Natl Cancer Inst 1991; 83(24): 1820-1826.
30. Lawson DH, Gray JM, McKillop C, Clarke J, Lee FD, Patrick RS. Diabetes mellitus and primary hepatocellular carcinoma. Q J Med 1986; 61(234): 945-955.
31. Tung HD, Wang JH, Tseng PL, Hung CH, Kee KM, Chen CH, et al. Neither diabetes mellitus nor overweight is a risk factor for hepatocellular carcinoma in a dual HBV and HCV endemic area: community cross-sectional and case-control studies. Am J Gastroenterol 2010; 105(3): 624-631.
32. Hassan MM, Curley SA, Li D, Kaseb A, Davila M, Abdalla EK, et al. Association of diabetes duration and diabetes treatment with the risk of hepatocellular carcinoma. Cancer 2010; 116(8): 1938-1946.
33. Donadon V, Balbi M, Mas MD, Casarin P, Zanette G. Metformin and reduced risk of hepatocellular carcinoma in diabetic patients with chronic liver disease. Liver Int 2010; 30(5): 750-758.
34. Atchison EA, Gridley G, Carreon JD, Leitzmann MF, McGlynn KA. Risk of cancer in a large cohort of U.S. veterans with diabetes. Int J Cancer 2011; 128(3): 635-643.
35. Chen HF, Chen P, Li CY. Risk of malignant neoplasms of liver and biliary tract in diabetic patients with different age and sex stratifications. Hepatology 2010; 52(1): 155-163.
36. Hemminki K, Li X, Sundquist J, Sundquist K. Risk of cancer following hospitalization for type 2 diabetes. Oncologist 2010; 15(6): 548-555.
37. Hung CH, Lee CM, Wang JH, Hu TH, Chen CH, Lin CY, et al. Impact of diabetes mellitus on incidence of hepatocellular carcinoma in chronic hepatitis C patients treated with interferon-based antiviral therapy. Int J Cancer 2011; 128(10): 2344-2352.
38. Kawamura Y, Arase Y, Ikeda K, Hirakawa M, Hosaka T, Kobayashi M, et al. Diabetes enhances hepatocarcinogenesis in noncirrhotic, interferon-treated hepatitis C patients. Am J Med 2010; 123(10): 951-956 e1.
39. Zhou XH, Qiao Q, Zethelius B, Pyorala K, Soderberg S, Pajak A, et al. Diabetes, prediabetes and cancer mortality. Diabetologia 2010; 53(9): 1867-1876.
40. Ziol M, Nault JC, Aout M, Barget N, Tepper M, Martin A, et al. Intermediate hepatobiliary cells predict an increased risk of hepatocarcinogenesis in patients with hepatitis C virus-related cirrhosis. Gastroenterology 2010; 139(1): 335-343 e2.
41. Kessler II. Cancer mortality among diabetics. J Natl Cancer Inst 1970; 44(3): 673-686.
42. Adami HO, Chow WH, Nyren O, Berne C, Linet MS, Ekbom A, et al. Excess risk of primary liver cancer in patients with diabetes mellitus. J Natl Cancer Inst 1996; 88(20): 1472-1477.
43. Wideroff L, Gridley G, Mellemkjaer L, Chow WH, Linet M, Keehn S, et al. Cancer incidence in a population-based cohort of patients hospitalized with diabetes mellitus in Denmark. J Natl Cancer Inst 1997; 89(18): 1360-1365.
44. Fujino Y, Mizoue T, Tokui N, Yoshimura T. Prospective study of diabetes mellitus and liver cancer in Japan. Diabetes Metab Res Rev 2001; 17(5): 374-379.
45. Tazawa J, Maeda M, Nakagawa M, Ohbayashi H, Kusano F, Yamane M, et al. Diabetes mellitus may be associated with hepatocarcinogenesis in patients with chronic hepatitis C. Dig Dis Sci 2002; 47(4): 710-715.
46. Ohata K, Hamasaki K, Toriyama K, Matsumoto K, Saeki A, Yanagi K, et al. Hepatic steatosis is a risk factor for hepatocellular carcinoma in patients with chronic hepatitis C virus infection. Cancer 2003; 97(12): 3036-3043.
47. Uetake S, Yamauchi M, Itoh S, Kawashima O, Takeda K, Ohata M. Analysis of risk factors for hepatocellular carcinoma in patients with HBs antigen- and anti-HCV antibody-negative alcoholic cirrhosis: clinical significance of prior hepatitis B virus infection. Alcohol Clin Exp Res 2003; 27(8 Suppl): 47S-51S.
48. Verlato G, Zoppini G, Bonora E, Muggeo M. Mortality from site-specific malignancies in type 2 diabetic patients from Verona. Diabetes Care 2003; 26(4): 1047-1051.
49. Zendehdel K, Nyren O, Ostenson CG, Adami HO, Ekbom A, Ye W. Cancer incidence in patients with type 1 diabetes mellitus: a population-based cohort study in Sweden. J Natl Cancer Inst 2003; 95(23): 1797-1800.
50. Batty GD, Shipley MJ, Marmot M, Smith GD. Diabetes status and post-load plasma glucose concentration in relation to site-specific cancer mortality: findings from the original Whitehall study. Cancer Causes Control 2004; 15(9): 873-881.
51. Coughlin SS, Calle EE, Teras LR, Petrelli J, Thun MJ. Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults. Am J Epidemiol 2004; 159(12): 1160-1167.
52. El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology 2004; 126(2): 460-468.
53. Inoue M, Iwasaki M, Otani T, Sasazuki S, Noda M, Tsugane S. Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan. Arch Intern Med 2006; 166(17): 1871-1877.
54. Khan MM, Saito S, Takagi S, Ohnishi H, Izumi H, Sakauchi F, et al. Relationship between hepatocellular carcinoma and impaired glucose tolerance among Japanese. Hepatogastroenterology 2006; 53(71): 742-746.
55. Lai MS, Hsieh MS, Chiu YH, Chen TH. Type 2 diabetes and hepatocellular carcinoma: a cohort study in high prevalence area of hepatitis virus infection. Hepatology 2006; 43(6): 1295-1302.
56. N'Kontchou G, Paries J, Htar MT, Ganne-Carrie N, Costentin L, Grando-Lemaire V, et al. Risk factors for hepatocellular carcinoma in patients with alcoholic or viral C cirrhosis. Clin Gastroenterol Hepatol 2006; 4(8): 1062-1068.
57. Ioannou GN, Splan MF, Weiss NS, McDonald GB, Beretta L, Lee SP. Incidence and predictors of hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol 2007; 5(8): 938-945, 945 e1-4.
58. Chen CL, Yang HI, Yang WS, Liu CJ, Chen PJ, You SL, et al. Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan. Gastroenterology 2008; 135 (1): 111-121.
59. Chuma M, Hige S, Nakanishi M, Ogawa K, Natsuizaka M, Yamamoto Y, et al. 8-Hydroxy-2'-deoxy-guanosine is a risk factor for development of hepatocellular carcinoma in patients with chronic hepatitis C virus infection. J Gastroenterol Hepatol 2008; 23(9): 1431-1436.
60. Di Costanzo GG, De Luca M, Tritto G, Lampasi F, Addario L, Lanza AG, et al. Effect of alcohol, cigarette smoking, and diabetes on occurrence of hepatocellular carcinoma in patients with transfusion-acquired hepatitis C virus infection who develop cirrhosis. Eur J Gastroenterol Hepatol 2008; 20(7): 674-679.
61. Veldt BJ, Chen W, Heathcote EJ, Wedemeyer H, Reichen J, Hofmann WP, et al. Increased risk of hepatocellular carcinoma among patients with hepatitis C cirrhosis and diabetes mellitus. Hepatology 2008; 47(6): 1856-1862.
62. Ikeda K, Kobayashi M, Someya T, Saitoh S, Hosaka T, Akuta N, et al. Occult hepatitis B virus infection increases hepatocellular carcinogenesis by eight times in patients with non-B, non-C liver cirrhosis: a cohort study. J Viral Hepat 2009; 16(6): 437-443.
63. Konishi I, Hiasa Y, Shigematsu S, Hirooka M, Furukawa S, Abe M, et al. Diabetes pattern on the 75g oral glucose tolerance test is a risk factor for hepatocellular carcinoma in patients with hepatitis C virus. Liver Int 2009; 29(8): 1194-1201.
64. Ogunleye AA, Ogston SA, Morris AD, Evans JM. A cohort study of the risk of cancer associated with type 2 diabetes. Br J Cancer 2009; 101(7): 1199-1201.
65. Wang CS, Yao WJ, Chang TT, Wang ST, Chou P. The impact of type 2 diabetes on the development of hepatocellular carcinoma in different viral hepatitis statuses. Cancer Epidemiol Biomarkers Prev 2009; 18(7): 2054-2060.
66. Hardie DG. AMP-activated protein kinase as a drug target. Annu Rev Pharmacol Toxicol 2007; 47: 185-210.
67. Libby G, Donnelly LA, Donnan PT, Alessi DR, Morris AD, Evans JM. New users of metformin are at low risk of incident cancer: a cohort study among people with type 2 diabetes. Diabetes Care 2009; 32(9): 1620-1625.
68. Currie CJ, Poole CD, Gale EA. The influence of glucose-lowering therapies on cancer risk in type 2 diabetes. Diabetologia 2009; 52(9): 1766-1777.
69. Wolk A, Gridley G, Svensson M, Nyren O, McLaughlin JK, Fraumeni JF, et al. A prospective study of obesity and cancer risk (Sweden). Cancer Causes Control 2001; 12(1): 13-21.
70. Larsson SC, Wolk A. Overweight, obesity and risk of liver cancer: a meta-analysis of cohort studies. Br J Cancer 2007; 97(7): 1005-1008.
71. Roskams T, Yang SQ, Koteish A, Durnez A, DeVos R, Huang X, et al. Oxidative stress and oval cell accumulation in mice and humans with alcoholic and nonalcoholic fatty liver disease. Am J Pathol 2003; 163(4): 1301-1311.
72. Hu W, Feng Z, Eveleigh J, Iyer G, Pan J, Amin S, et al. The major lipid peroxidation product, trans-4-hydroxy-2-nonenal, preferentially forms DNA adducts at codon 249 of human p53 gene, a unique mutational hotspot in hepatocellular carcinoma. Carcinogenesis 2002; 23(11): 1781-1789.
73. Macaulay VM. Insulin-like growth factors and cancer. Br J Cancer 1992; 65(3): 311-320.
74. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 2000; 283(15): 2008-2012.
75. Jüni P, Witschi A, Bloch R, Egger M. The hazards of scoring the quality of clinical trials for meta-analysis. JAMA 1999; 282(11): 1054-1060.