Anti-diabetic medications and the risk of hepatocellular cancer: A systematic review and meta-analysis

American Journal of Gastroenterology

Volumn 108, Issue 6, 2013, Pages 881-891

  Singh, Siddharth ^a   Singh, Preet Paul ^a   Singh, Abha Goyal ^a   Murad, Mohammad Hassan ^a   Sanchez, William ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; INSULIN; METFORMIN; SULFONYLUREA DERIVATIVE;

CANCER INCIDENCE; CANCER RISK; DIABETES MELLITUS; DRUG EXPOSURE; GENETIC HETEROGENEITY; HEPATOCELLULAR CANCER; HUMAN; LIVER CANCER; META ANALYSIS; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); REVIEW; SYSTEMATIC REVIEW;

CARCINOMA, HEPATOCELLULAR; CONFIDENCE INTERVALS; DIABETES MELLITUS, TYPE 2; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; LIVER NEOPLASMS; METFORMIN; ODDS RATIO; SULFONYLUREA COMPOUNDS; THIAZOLIDINEDIONES;

EID: 84878911175     PISSN: 00029270     EISSN: 15720241     Source Type: Journal    
DOI: 10.1038/ajg.2013.5     Document Type: Review

References (53)

1. Jemal A, Bray F, Center MM et al. Global cancer statistics. CA Cancer J Clin 2011 ; 61 : 69-90.
2. Calle EE, Rodriguez C, Walker-Th urmond K et al. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med 2003 ; 348 : 1625-38. (Pubitemid 36459468)
3. El-Serag HB, Hampel H, Javadi F. Th e association between diabetes and hepatocellular carcinoma: a systematic review of epidemiologic evidence. Clin Gastroenterol Hepatol 2006 ; 4 : 369-80. (Pubitemid 43343895)
4. Wang C, Wang X, Gong G et al. Increased risk of hepatocellular carcinoma in patients with diabetes mellitus: a systematic review and meta-analysis of cohort studies. Int J Cancer 2012 ; 130 : 1639-48.
5. Giovannucci E, Harlan DM, Archer MC et al. Diabetes and cancer: a consensus report. CA Cancer J Clin 2010 ; 60 : 207-21.
6. Baff y G, Brunt EM, Caldwell SH. Hepatocellular carcinoma in nonalcoholic fatty liver disease: an emerging menace. J Hepatol 2012 ; 56 : 1384-91.
7. Welzel TM, Graubard BI, Zeuzem S et al. Metabolic syndrome increases the risk of primary liver cancer in the United States: a study in the SEERMedicare database. Hepatology 2011 ; 54 : 463-71.
8. Charlton MR, Burns JM, Pedersen RA et al. Frequency and outcomes of liver transplantation for nonalcoholic steatohepatitis in the United States. Gastroenterology 2011 ; 141 : 1249-53.
9. Gallagher EJ, LeRoith D. Diabetes, cancer, and metformin: connections of metabolism and cell proliferation. Ann NY Acad Sci 2011 ; 1243 : 54-68.
10. Okumura T. Mechanisms by which thiazolidinediones induce anticancer eff ects in cancers in digestive organs. J Gastroenterol 2010 ; 45 : 1097-102.
11. Bowker SL, Majumdar SR, Veugelers P et al. Increased cancer-related mortality for patients with type 2 diabetes who use sulfonylureas or insulin. Diabetes Care 2006 ; 29 : 254-8. (Pubitemid 44106500)
12. Decensi A, Puntoni M, Goodwin P et al. Metformin and cancer risk in diabetic patients: a systematic review and meta-analysis. Cancer Prev Res (Phila) 2010 ; 3 : 1451-61.
13. Noto H, Goto A, Tsujimoto T et al. Cancer risk in diabetic patients treated with metformin: a systematic review and meta-analysis. PLoS One 2012 ; 7 : e33411.
14. Soranna D, Scotti L, Zambon A et al. Cancer risk associated with use of metformin and sulfonylurea in type 2 diabetes: a meta-analysis. Oncologist 2012 ; 17 : 813-22.
15. Chang CH, Lin JW, Wu LC et al. Association of thiazolidinediones with liver cancer and colorectal cancer in type 2 diabetes mellitus. Hepatology 2012 ; 55 : 1462-72.
16. Chang CH, Lin JW, Wu LC et al. Oral insulin secretagogues, insulin, and cancer risk in type 2 diabetes mellitus. J Clin Endocrinol Metab 2012 ; 97 : E1170-5.
17. Hassan MM, Curley SA, Li D et al. Association of diabetes duration and diabetes treatment with the risk of hepatocellular carcinoma. Cancer 2010 ; 116 : 1938-46.
18. Oliveria SA, Koro CE, Yood MU et al. Cancer incidence among patients treated with antidiabetic pharmacotherapy. Diab Metabol Syndr Clin Res Rev 2008 ; 2 : 47-57. (Pubitemid 351194192)
19. Nkontchou G, Cosson E, Aout M et al. Impact of metformin on the prognosis of cirrhosis induced by viral hepatitis C in diabetic patients. J Clin Endocrinol Metab 2011 ; 96 : 2601-8.
20. Moher D, Liberati A, Tetzlaff J et al. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 2009 ; 151 : 264-9, W64.
21. Wells GA, Shea B, O ' Connell D et al. Th e Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses [cited 5 May 2012]; Available from: http://www.ohri.ca/programs/clinical-epidemiology/ oxford.htm.
22. Higgins JP, Altman DG, Gotzsche PC et al. Th e Cochrane Collaboration's tool for assessing risk of bias in randomised trials. BMJ 2011 ; 343 : d5928.
23. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986 ; 7 : 177-88. (Pubitemid 17189972)
24. Higgins JP, Th ompson SG, Deeks JJ et al. Measuring inconsistency in meta-analyses. BMJ 2003 ; 327 : 557-60. (Pubitemid 37088507)
25. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994 ; 50 : 1088-101.
26. Easterbrook PJ, Berlin JA, Gopalan R et al. Publication bias in clinical research. Lancet 1991 ; 337 : 867-72.
27. Chen HP, Shieh JJ, Chang CC et al. Metformin decreases hepatocellular carcinoma risk in a dose-dependent manner: population-based and in vitro studies. Gut 2013 (e-pub ahead of print).
28. Ruiter R, Visser LE, van Herk-Sukel MP et al. Lower risk of cancer in patients on metformin in comparison with those on sulfonylurea derivatives: results from a large population-based follow-up study. Diabetes Care 2012 ; 35 : 119-24.
29. Donadon V, Balbi M, Mas MD et al. Metformin and reduced risk of hepatocellular carcinoma in diabetic patients with chronic liver disease. Liver Int 2010 ; 30 : 750-8.
30. Kawaguchi T, Taniguchi E, Morita Y et al. Association of exogenous insulin or sulphonylurea treatment with an increased incidence of hepatoma in patients with hepatitis C virus infection. Liver Int 2010 ; 30 : 479-86.
31. Home PD, Kahn SE, Jones NP et al. Experience of malignancies with oral glucose-lowering drugs in the randomised controlled ADOPT (A Diabetes Outcome Progression Trial) and RECORD (Rosiglitazone Evaluated for Cardiovascular Outcomes and Regulation of Glycaemia in Diabetes) clinical trials. Diabetologia 2010 ; 53 : 1838-45.
32. Yu MC, Tong MJ, Govindarajan S et al. 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 : 1820-6.
33. Lai SW, Chen PC, Liao KF et al. Risk of hepatocellular carcinoma in diabetic patients and risk reduction associated with anti-diabetic therapy: a population-based cohort study. Am J Gastroenterol 2012 ; 107 : 46-52.
34. Lee MS, Hsu CC, Wahlqvist ML et al. Type 2 diabetes increases and metformin reduces total, colorectal, liver and pancreatic cancer incidences in Taiwanese: a representative population prospective cohort study of 800,000 individuals. BMC Cancer 2011 ; 11 : 20.
35. Tsan YT, Lee CH, Wang JD et al. Statins and the risk of hepatocellular carcinoma in patients with hepatitis B virus infection. J Clin Oncol 2012 ; 30 : 623-30.
36. Donadon V, Balbi M, Casarin P et al. Association between hepatocellular carcinoma and type 2 diabetes mellitus in Italy: potential role of insulin. World J Gastroenterol 2008 ; 14 : 5695-700.
37. Donadon V, Balbi M, Ghersetti M et al. Antidiabetic therapy and increased risk of hepatocellular carcinoma in chronic liver disease. World J Gastroenterol 2009 ; 15 : 2506-11.
38. Home PD, Pocock SJ, Beck-Nielsen H et al. Rosiglitazone evaluated for cardiovascular outcomes in oral agent combination therapy for type 2 diabetes (RECORD): a multicentre, randomised, open-label trial. Lancet 2009 ; 373 : 2125-35.
39. Kahn SE, Haff ner SM, Heise MA et al. Glycemic durability of rosiglitazone, metformin, or glyburide monotherapy. N Engl J Medi 2006 ; 355 : 2427-43. (Pubitemid 44903747)
40. El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology 2004 ; 126 : 460-8. (Pubitemid 38182303)
41. Stefansdottir G, Zoungas S, Chalmers J et al. Intensive glucose control and risk of cancer in patients with type 2 diabetes. Diabetologia 2011 ; 54 : 1608-14.
42. Johnson JA, Bowker SL. Intensive glycaemic control and cancer risk in type 2 diabetes: a meta-analysis of major trials. Diabetologia 2011 ; 54 : 25-31.
43. Zhang ZJ, Zheng ZJ, Shi R et al. Metformin for liver cancer prevention in patients with Type 2 diabetes: a systematic review and meta-analysis. J Clin Endocrinol Metab 2012 ; 97 : 2347-53.
44. Zhou G, Myers R, Li Y et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001 ; 108 : 1167-74. (Pubitemid 32995375)
45. Ben Sahra I, Laurent K, Loubat A et al. Th e antidiabetic drug metformin exerts an antitumoral eff ect in vitro and in vivo through a decrease of cyclin D1 level. Oncogene 2008 ; 27 : 3576-86. (Pubitemid 351793803)
46. Blandino G, Valerio M, Cioce M et al. Metformin elicits anticancer eff ects through the sequential modulation of DICER and c-MYC. Nat Commun 2012 ; 3 : 865.
47. Wu CW, Farrell GC, Yu J. Functional role of PPARgamma in hepatocellular carcinoma. J Gastroenterol Hepatol 2012 ; 27 : 1665-9.
48. Algire C, Zakikhani M, Blouin MJ et al. Metformin attenuates the stimulatory eff ect of a high-energy diet on in vivo LLC1 carcinoma growth. Endocr Relat Cancer 2008 ; 15 : 833-9.
49. Bonanni B, Puntoni M, Cazzaniga M et al. Dual eff ect of metformin on breast cancer proliferation in a randomized presurgical trial. J Clin Oncol 2012 ; 30 : 2593-600.
50. Pocock SJ, Elbourne DR. Randomized trials or observational tribulations? N Engl J Med 2000 ; 342 : 1907-9.
51. Johnson JA, Yasui Y. Glucose-lowering therapies and cancer risk: the trials and tribulations of trials and observations. Diabetologia 2010 ; 53 : 1823-6.
52. Singh S, Singh PP, Singh AG et al. Statins are associated with a reduced risk of hepatocellular cancer: a systematic review and meta-analysis. Gastroenterology 2013 (e-pub ahead of print).
53. Singh PP, Singh S. Statins and risk reduction in hepatocellular carcinoma: fact or fi ction? J Clin Oncol 2012 ; 30 : 2569-70.