Effect of type 2 diabetes mellitus on the risk for hepatocellular carcinoma in chronic liver diseases: A meta-analysis of cohort studies

European Journal of Cancer Prevention

Volumn 24, Issue 2, 2015, Pages 89-99

  Chen, Junming ^a   Han, Yonglong ^a   Xu, Chunwei ^a   Xiao, Tiegang ^a   Wang, Bing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

Chronic liver diseases; Hepatocellular carcinoma; Meta analysis; Type 2 diabetes

Indexed keywords

ALCOHOL;

ALCOHOL CONSUMPTION; ARTICLE; BODY MASS; CANCER RISK; CHRONIC LIVER DISEASE; COHORT ANALYSIS; FOLLOW UP; HEPATITIS B; HEPATITIS C; HIGH RISK PATIENT; HUMAN; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; PATIENT MONITORING; PRIORITY JOURNAL; SMOKING; CARCINOMA, HEPATOCELLULAR; DIABETES MELLITUS, TYPE 2; HEPATITIS B, CHRONIC; HEPATITIS C, CHRONIC; LIVER DISEASES; LIVER NEOPLASMS; META ANALYSIS; RISK FACTOR;

CARCINOMA, HEPATOCELLULAR; COHORT STUDIES; DIABETES MELLITUS, TYPE 2; HEPATITIS B, CHRONIC; HEPATITIS C, CHRONIC; HUMANS; LIVER CIRRHOSIS; LIVER DISEASES; LIVER NEOPLASMS; RISK FACTORS;

EID: 84927653758     PISSN: 09598278     EISSN: 14735709     Source Type: Journal    
DOI: 10.1097/CEJ.0000000000000038     Document Type: Article

References (58)

1. Adams LA, Lymp JF St, Sauver J, Sanderson SO, Lindor KD, Feldstein A, et al. (2005). The natural history of nonalcoholic fatty liver disease: a populationbased cohort study. Gastroenterology 129:113-121.
2. Alberstein M, Zornitzki T, Zick Y, Knobler H (2012). Hepatitis C core protein impairs insulin downstream signalling and regulatory role of IGFBP-1 expression. J Viral Hepat 19:65-71.
3. Arase Y, Kobayashi M, Suzuki F, Suzuki Y, Kawamura Y, Akuta N, et al. (2013). Effect of type 2 diabetes on risk for malignancies includes hepatocellular carcinoma in chronic hepatitis C. Hepatology 57:964-973.
4. Begg CB, Mazumdar M (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics 50:1088-1101.
5. Ben Q, Cai Q, Li Z, Yuan Y, Ning X, Deng S, et al. (2011a). The relationship between new-onset diabetes mellitus and pancreatic cancer risk: a case-control study. Eur J Cancer 47:248-254.
6. Ben Q, Xu M, Ning X, Liu J, Hong S, Huang W, et al. (2011b). Diabetes mellitus and risk of pancreatic cancer: a meta-analysis of cohort studies. Eur J Cancer 47:1928-1937.
7. Bose SK, Shrivastava S, Meyer K, Ray RB, Ray R (2012). Hepatitis C virus activates the mTOR/S6K1 signaling pathway in inhibiting IRS-1 function for insulin resistance. J Virol 86:6315-6322.
8. Boyle JP, Honeycutt AA, Narayan KM, Hoerger TJ, Geiss LS, Chen H, et al. (2001). Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the U. S. Diabetes Care 24:1936-1940.
9. Bruix J, Sherman M (2005). Management of hepatocellular carcinoma. Hepatology 42:1208-1236.
10. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003). Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U. S. adults. N Engl J Med 348:1625-1638.
11. Chen CL, Yang HI, Yang WS, Liu CJ, Chen PJ, You SL, et al. (2008). Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan. Gastroenterology 135:111-121.
12. Chen HP, Shieh JJ, Chang CC, Chen TT, Lin JT, Wu MS, et al. (2013). Metformin decreases hepatocellular carcinoma risk in a dose-dependent manner: population-based and in vitro studies. Gut 62:606-615.
13. Chen Y, Wang X, Wang J, Yan Z, Luo J (2012). Excess body weight and the risk of primary liver cancer: an updated meta-analysis of prospective studies. Eur J Cancer 48:2137-2145.
14. Chuang SC, Lee YC, Hashibe M, Dai M, Zheng T, Boffetta P (2010). Interaction between cigarette smoking and hepatitis B and C virus infection on the risk of liver cancer: a meta-analysis. Cancer Epidemiol Biomarkers Prev 19:1261-1268.
15. Chuma M, Hige S, Nakanishi M, Ogawa K, Natsuizaka M, Yamamoto Y, et al. (2008). 8-Hydroxy-20-deoxy-guanosine is a risk factor for development of hepatocellular carcinoma in patients with chronic hepatitis C virus infection. J Gastroenterol Hepatol 23:1431-1436.
16. Da Costa BR, Cevallos M, Altman DG, Rutjes AW, Egger M (2011). Uses and misuses of the STROBE statement: bibliographic study. BMJ Open 1:e000048.
17. Der Simonian R, Laird N (1986). Meta-analysis in clinical trials. Control Clin Trials 7:177-188.
18. Di Costanzo GG, De Luca M, Tritto G, Lampasi F, Addario L, Lanza AG, et al. (2008). 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 20:674-679.
19. Egger M, Davey Smith G, Schneider M, Minder C (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ 315:629-634.
20. El-Serag HB, Mason AC (2000). Risk factors for the rising rates of primary liver cancer in the United States. Arch Intern Med 160:3227-3230.
21. Fujino Y, Mizoue T, Tokui N, Yoshimura T (2001). Prospective study of diabetes mellitus and liver cancer in Japan. Diabetes Metab Res Rev 17:374-379.
22. Heidemann C, Boeing H, Pischon T, Nothlings U, Joost HG, Schulze MB (2009). Association of a diabetes risk score with risk of myocardial infarction, stroke, specific types of cancer, and mortality: a prospective study in the European Prospective Investigation into Cancer and Nutrition (EPIC)-Potsdam cohort. Eur J Epidemiol 24:281-288.
23. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003). Measuring inconsistency in meta-analyses. BMJ 327:557-560.
24. Hung CH, Lee CM, Wang JH, Hu TH, Chen CH, Lin CY, et al. (2011). Impact of diabetes mellitus on incidence of hepatocellular carcinoma in chronic hepatitis C patients treated with interferon-based antiviral therapy. Int J Cancer 128:2344-2352.
25. Ikeda K, Kobayashi M, Someya T, Saitoh S, Hosaka T, Akuta N, et al. (2009). 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 16:437-443.
26. Ioannou GN, Splan MF, Weiss NS, McDonald GB, Beretta L, Lee SP (2007). Incidence and predictors of hepatocellular carcinoma in patients with cirrhosis. Clin Gastroenterol Hepatol 5:938-945, 945.e1-945.e4.
27. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011). Global cancer statistics. CA Cancer J Clin 61:69-90.
28. Jeong S, Sefcikova J, Tinsley RA, Rueda D, Walter NG (2003). Trans-acting hepatitis delta virus ribozyme: catalytic core and global structure are dependent on the 50 substrate sequence. Biochemistry 42:7727-7740.
29. Juni P, Witschi A, Bloch R, Egger M (1999). The hazards of scoring the quality of clinical trials for meta-analysis. JAMA 282:1054-1060.
30. Kawamura Y, Arase Y, Ikeda K, Hirakawa M, Hosaka T, Kobayashi M, et al. (2010). Diabetes enhances hepatocarcinogenesis in noncirrhotic, interferon-treated hepatitis C patients. Am J Med 123:951-956.e1.
31. Koh WP, Wang R, Jin A, Yu MC, Yuan JM (2013). Diabetes mellitus and risk of hepatocellular carcinoma: findings from the Singapore Chinese Health Study. Br J Cancer 108:1182-1188.
32. Konishi I, Hiasa Y, Shigematsu S, Hirooka M, Furukawa S, Abe M, et al. (2009). Diabetes pattern on the 75 g oral glucose tolerance test is a risk factor for hepatocellular carcinoma in patients with hepatitis C virus. Liver Int 29:1194-1201.
33. Lai MS, Hsieh MS, Chiu YH, Chen TH (2006). Type 2 diabetes and hepatocellular carcinoma: a cohort study in high prevalence area of hepatitis virus infection. Hepatology 43:1295-1302.
34. Lai SW, Chen PC, Liao KF, Muo CH, Lin CC, Sung FC (2012). Risk of hepatocellular carcinoma in diabetic patients and risk reduction associated with anti-diabetic therapy: a population-based cohort study. Am J Gastroenterol 107:46-52.
35. Longato L, de la Monte S, Kuzushita N, Horimoto M, Rogers AB, Slagle BL, et al. (2009). Overexpression of insulin receptor substrate-1 and hepatitis Bx genes causes premalignant alterations in the liver. Hepatology 49:1935-1943.
36. Marzouk D, Sass J, Bakr I, El Hosseiny M, Abdel-Hamid M, Rekacewicz C, et al. (2007). Metabolic and cardiovascular risk profiles and hepatitis C virus infection in rural Egypt. Gut 56:1105-1110.
37. Masini M, Campani D, Boggi U, Menicagli M, Funel N, Pollera M, et al. (2005). Hepatitis C virus infection and human pancreatic beta-cell dysfunction. Diabetes Care 28:940-941.
38. Naing C, Mak JW, Ahmed SI, Maung M (2012). Relationship between hepatitis C virus infection and type 2 diabetes mellitus: meta-analysis. World J Gastroenterol 18:1642-1651.
39. N'Kontchou G, Paries J, Htar MT, Ganne-Carrie N, Costentin L, Grando-Lemaire V, et al. (2006). Risk factors for hepatocellular carcinoma in patients with alcoholic or viral C cirrhosis. Clin Gastroenterol Hepatol 4:1062-1068.
40. Nkontchou G, Cosson E, Aout M, Mahmoudi A, Bourcier V, Charif I, et al. (2011). Impact of metformin on the prognosis of cirrhosis induced by viral hepatitis C in diabetic patients. J Clin Endocrinol Metab 96:2601-2608.
41. Ohata K, Hamasaki K, Toriyama K, Matsumoto K, Saeki A, Yanagi K, et al. (2003). Hepatic steatosis is a risk factor for hepatocellular carcinoma in patients with chronic hepatitis C virus infection. Cancer 97:3036-3043.
42. Ohki T, Tateishi R, Sato T, Masuzaki R, Imamura J, Goto T, et al. (2008). Obesity is an independent risk factor for hepatocellular carcinoma development in chronic hepatitis C patients. Clin Gastroenterol Hepatol 6:459-464.
43. Papa S, Bubici C, Zazzeroni F, Franzoso G (2009). Mechanisms of liver disease: cross-talk between the NF-kappaB and JNK pathways. Biol Chem 390:965-976.
44. Park EJ, Lee JH, Yu GY, He G, Ali SR, Holzer RG, et al. (2010). Dietary and genetic obesity promote liver inflammation and tumorigenesis by enhancing IL-6 and TNF expression. Cell 140:197-208.
45. Qureshi H, Ahsan T, Mujeeb SA, Jawad F, Mehdi I, Ahmed W, et al. (2002). Diabetes mellitus is equally frequent in chronic HCV and HBV infection. J Pak Med Assoc 52:280-283.
46. Singh S, Singh PP, Singh AG, Murad MH, Sanchez W (2013). Anti-diabetic medications and the risk of hepatocellular cancer: a systematic review and meta-analysis. Am J Gastroenterol 108:881-891, quiz 92.
47. Tazawa J, Maeda M, Nakagawa M, Ohbayashi H, Kusano F, Yamane M, et al. (2002). Diabetes mellitus may be associated with hepatocarcinogenesis in patients with chronic hepatitis C. Dig Dis Sci 47:710-715.
48. Torisu Y, Ikeda K, Kobayashi M, Hosaka T, Sezaki H, Akuta N, et al. (2007). Diabetes mellitus increases the risk of hepatocarcinogenesis in patients with alcoholic cirrhosis: a preliminary report. Hepatol Res 37:517-523.
49. Uetake S, Yamauchi M, Itoh S, Kawashima O, Takeda K, Ohata M (2003). 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 27:47S-51S.
50. Veldt BJ, Chen W, Heathcote EJ, Wedemeyer H, Reichen J, Hofmann WP, et al. (2008). Increased risk of hepatocellular carcinoma among patients with hepatitis C cirrhosis and diabetes mellitus. Hepatology 47:1856-1862.
51. Wang C, Wang X, Gong G, Ben Q, Qiu W, Chen Y, et al. (2012). Increased risk of hepatocellular carcinoma in patients with diabetes mellitus: a systematic review and meta-analysis of cohort studies. Int J Cancer 130:1639-1648.
52. Wang CS, Yao WJ, Chang TT, Wang ST, Chou P (2009). The impact of type 2 diabetes on the development of hepatocellular carcinoma in different viral hepatitis statuses. Cancer Epidemiol Biomarkers Prev 18:2054-2060.
53. Weng CJ, Hsieh YH, Tsai CM, Chu YH, Ueng KC, Liu YF, et al. (2010). Relationship of insulin-like growth factors system gene polymorphisms with the susceptibility and pathological development of hepatocellular carcinoma. Ann Surg Oncol 17:1808-1815.
54. White DL, Ratziu V, El-Serag HB (2008). Hepatitis C infection and risk of diabetes: a systematic review and meta-analysis. J Hepatol 49:831-844.
55. Wiencke JK (2004). Impact of race/ethnicity on molecular pathways in human cancer. Nat Rev Cancer 4:79-84.
56. Yu MC, Yuan JM (2004). Environmental factors and risk for hepatocellular carcinoma. Gastroenterology 127:S72-S78.
57. Zhang BH, Yang BH, Tang ZY (2004). Randomized controlled trial of screening for hepatocellular carcinoma. J Cancer Res Clin Oncol 130:417-422.
58. Ziol M, Nault JC, Aout M, Barget N, Tepper M, Martin A, et al. (2010). Intermediate hepatobiliary cells predict an increased risk of hepatocarcinogenesis in patients with hepatitis C virus-related cirrhosis. Gastroenterology 139:335-343.e2.