Diabetes mellitus as a novel risk factor for gastrointestinal malignancies

Postgraduate Medicine

Volumn 126, Issue 6, 2014, Pages 106-118

  Herrigel, Dana J ^a   Moss, Rebecca A ^b  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b RUTGERS CANCER INSTITUTE OF NEW JERSEY   (United States)

Author keywords

Diabetes mellitus; Etiologic linkage; Gastrointestinal malignancy; Pathogenicity

Indexed keywords

GLITAZONE DERIVATIVE; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; METFORMIN; SORAFENIB; TUMOR NECROSIS FACTOR ALPHA; 2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; INSULIN; PIOGLITAZONE; ROSIGLITAZONE; SOMATOMEDIN RECEPTOR;

ARTICLE; BARIATRIC SURGERY; COLORECTAL CARCINOMA; DIABETES MELLITUS; DISEASE ASSOCIATION; GASTROINTESTINAL DISEASE; HEPATITIS C; HUMAN; INSULIN RESISTANCE; LIPID PEROXIDATION; LIVER CELL CARCINOMA; META ANALYSIS (TOPIC); NONALCOHOLIC FATTY LIVER; OVERALL SURVIVAL; OXIDATIVE STRESS; PANCREAS ADENOCARCINOMA; PHASE 3 CLINICAL TRIAL (TOPIC); PROTON NUCLEAR MAGNETIC RESONANCE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK FACTOR; SYSTEMATIC REVIEW (TOPIC); ADENOCARCINOMA; CARCINOMA, HEPATOCELLULAR; COLORECTAL NEOPLASMS; DIABETES COMPLICATIONS; LIVER NEOPLASMS; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; PRECANCER;

ADENOCARCINOMA; CARCINOMA, HEPATOCELLULAR; COLORECTAL NEOPLASMS; DIABETES COMPLICATIONS; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; LIVER NEOPLASMS; METFORMIN; NON-ALCOHOLIC FATTY LIVER DISEASE; PANCREATIC NEOPLASMS; PRECANCEROUS CONDITIONS; RECEPTORS, SOMATOMEDIN; RISK FACTORS; THIAZOLIDINEDIONES;

EID: 84922391785     PISSN: 00325481     EISSN: 19419260     Source Type: Journal    
DOI: 10.3810/pgm.2014.10.2825     Document Type: Article

References (102)

1. 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.
2. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035 for the IDF Diabetes Atlas. Diabetes Res Clin Pract. 2014;103(2):137–149.
3. Beagley J, Guariguata L, Weil C, Motala AA. Global estimates of undiagnosed diabetes in adults for 2013 for the IDF Diabetes Atlas. Diabetes Res Clin Pract. 2014;103(2):150–160.
4. Siegel R, Naishadham D, Jemal A. Cancer Statistics, 2013. CA. 2013;63(1):11–30.
5. Altekruse SF, Henley SJ, Cucinelli JE, McGlynn KA. Changing hepatocellular carcinoma incidence and liver cancer mortality rates in the United States. Am J Gastroenterol. 2014;109(4):542–553.
6. Davis DM, Marcet JE, Frattini JC, Prather AD, Mateka JJ, Nfonsam VN. Is it time to lower the recommended screening age for colorectal cancer? J Am Coll Surg. 2011;213(3):352–361.
7. Ahnen D, Wade S, Jones W, et al. The increasing incidence of young-onset colorectal cancer: a call to action. Mayo Clin Proc. 2014;89(2):216–224.
8. El-Serag HB. The continuing increase in the incidence of hepatocellular carcinoma in the United States: an update. Ann Intern Med. 2003;139(10):817–823.
9. O’Connor S, Ward J, Watson M, Momin B, Richardson L. Hepatocellular carcinoma—United States, 2001–2006. MMWR. 2010;59(17):517–520.
10. Chalasani N, Younossi Z, Lavine JE, et al. The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55(6):2005–2022.
11. Llovet J, Ricci S, Mazzaferro V, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008;359(4):378–390.
12. Bugianesi E. Non-alcoholic steatohepatitis and cancer. Clin Liver Dis. 2007;11:197–207.
13. Marrero JA, Fontana RJ, Su GL, Conjeevaram HS, Emick DM, Lok AS. NAFLD may be a common underlying liver disease in patients with hepatocellular carcinoma in the United States. Hepatology. 2002;36(6):1349–1354.
14. Marchesini G, Brizi M, Morselli-Labate AM, et al. Association of nonalcoholic fatty liver disease with insulin resistance. Am J Med. 1999;107:450–455.
15. Kim CH, Younossi ZM. Nonalcoholic fatty liver disease: a manifestation of the metabolic syndrome. Cleve Clin J Med. 2008;75(10):721–728.
16. Dunn W, Wingard DL, Rogers C, Angulo P, Younossi ZM, Schwimmer JB. Suspected nonalcoholic fatty liver disease and mortality risk in a population-based cohort study. Am J Gastroenterol. 2008;103(9):2263–2271.
17. Day CP. Pathogenesis of NASH. Best Pract Res Clin Gastroenterol. 2002;16(5):663–678.
18. Harrison SA. Nonalcoholic steatoheptitis: what we know in the new millennium. Am J Gastroenterol. 2002;97(11):2714–2724.
19. Szczepaniak LS, Nurenberg P, Leonard D, et al. Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab. 2005;288(2):E462–E468.
20. Bellentani S, Marino M. Epidemiology and natural history of nonalcoholic fatty liver disease (NAFLD). Ann Hepatol. 2009;8(Suppl 1): S4–S8.
21. Browning J, Szczepaniak L, Dobbins R, et al. Prevalence of hepatic steatosis in an urban population in the united states: impact of ethnicity. Hepatology. 2004;40:1387–1395.
22. Clark JM. The epidemiology of nonalcoholic fatty liver disease in adults. J Clin Gastroenterol. 2006;40(Suppl 1):S5–S10.
23. Jimba S, Nakagami T, Takahashi M, et al. Prevalence of non-alcoholic fatty liver disease and its association with impaired glucose metabolism in Japanese adults. Diabet Med. 2005;22:1141–1145.
24. 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.
25. 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(20):2506–2511.
26. Polesel J, Zucchetto A, Montella M, et al. The impact of obesity and diabetes mellitus on the risk of hepatocellular carcinoma. Ann Oncol. 2009;20(2):353–357.
27. 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.
28. El-Serag HB, Tran T, Everhart JE. Diabetes increases the risk of chronic liver disease and hepatocellular carcinoma. Gastroenterology. 2004;126(2):460–468.
29. Chiu CC, Huang CC, Chen YC, et al. Increased risk of gastrointestinal malignancy in patients with diabetes mellitus and correlations with anti-diabetes drugs: a nationwide population-based study in Taiwan. Intern Med. 2013;52:939–946.
30. 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.
31. Luo J, Chlebowski R, Liu S, et al. Diabetes mellitus as a risk factor for gastrointestinal cancers among postmenopausal women. Cancer Causes Control. 2013;24:577–585.
32. Caldwell S, Argo C, Al-Osaimi A. Therapy of NAFLD. Clin Gastroenterol. 2006;40(Suppl 1):S61–S66.
33. Furuya CK, deOliveira CP, de Mello ES, et al. Effects of bariatric surgery on nonalcoholic fatty liver disease: preliminary findings after 2 years. J Gastroenterol Hepatol. 2007;22(4):510–514.
34. Chavez-Tapia N, Tellez-Avila F, Barrientos-Gutierrez T, Mendez- Sanchez N, Lizardi-Cervera J, Uribe M. Bariatric surgery for nonalcoholic steatohepatitis in obese patients. Cochrane Database Syst Rev. 2010;1:CD007340.
35. Ueda M, Endo I, Nakashima M, et al. Prognostic factors after resection of pancreatic cancer. World J Surg. 2009;33:104–110.
36. Conroy T, Desseigne F, Ychou M, et al. FOLFIRINOX versus Gemcitabine for metastatic pancreatic cancer. N Engl J Med. 2011;364:1817–1825.
37. Chari ST, Leibson CL, Rabe KG, et al. Probability of pancreatic cancer following diabetes: a population based study. Gastroenterology. 2005;129(2):504–511.
38. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348(17):1625–1638.
39. Michaud D. Physical activity, obesity, height, and the risk of pancreatic cancer. JAMA. 2001;286(8):921–929.
40. Li D, Morris JS, Liu J, et al. Body mass index and risk, age of onset, and survival in patients with pancreatic cancer. JAMA. 2009;301(24):2553–2562.
41. Gumbs AA. Obesity, pancreatitis, and pancreatic cancer. Obes Surg. 2008;18(9):1183–1187.
42. Everhart J, Wright D. Diabetes Mellitus as a risk factor for pancreatic cancer. A meta analysis. JAMA. 1995;273(20):1605–1609.
43. Huxley R, Ansary-Moghaddam A, Gonzalez ABd, Barzi F, Woodward M. Type II diabetes and pancreatic cancer: a meta-analysis of 36 studies. Br J Cancer. 2005;92(11):2076–2083.
44. Pannala R. Temporal association of changes in fasting blood glucose and body mass index with diagnosis of pancreatic cancer. Am J Gastroenterol. 2009;104:2318–2325.
45. Li D, Yeung SC, Hassan MM, Konopleva M, Abbruzzese JL. Antidiabetic therapies affect risk of pancreatic cancer. Gastroenterology. 2009;137(2):482–488.
46. Pannala R. Prevalence and clinical profile of pancreatic cancerassociated diabetes mellitus. Gastroenterology. 2008;134(4): 981–987.
47. Ben Q, Xu M, Ning X, et al. Diabetes mellitus and risk of pancreatic cancer: a meta-analysis of cohort studies. Eur J Cancer. 2011;47(13):1928–1937.
48. Elena JW, Steplowski E, Yu K, et al. Diabetes and risk of pancreatic cancer: a pooled analysis from the pancreatic cancer cohort consortium. Cancer Causes Control. 2013;24(1):13–25.
49. Basso D, Greco E, Fogar P, et al. Pancreatic cancer-associated diabetes mellitus: An open field for proteomic applications. Clinica Chimica Acta. 2005;357:184–189.
50. Ogino S, Shima K, Nosho K, et al. A cohort study of p27 localization in colon cancer, body mass index, and patient survival. Cancer Epidemiol Biomarkers Prev. 2009;18(6):1849–1858.
51. Centers for Disease Control. Overweight and obesity: adult obesity facts. http://www.cdc.gov/obesity/data/adult.html. Accessed May 7, 2014.
52. Larsson SC, Orsini N, Wolk A. Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J Natl Cancer Inst. 2005;97(22): 1679–1687.
53. Deng L, Gui Z, Zhao L, Wang J, Shen L. Diabetes mellitus and the incidence of colorectal cancer: an updated systematic review and meta-analysis. Dig Dis Sci. 2012;57:1576–1585.
54. Yang YX, Hennessy S, Lewis JD. Insulin therapy and colorectal cancer risk among type 2 diabetes mellitus patients. Gastroenterology. 2004;127(4):1044–1050.
55. Meyerhardt JA, Catalano PJ, Haller DG, et al. Impact of diabetes mellitus on outcomes in patients with colon cancer. J Clin Oncol. 2003;21(3):433–440.
56. Singh S, Singh H, Singh PP, Murad MH, Limburg PJ. Antidiabetic medications and the risk of colorectal cancer in patients with diabetes mellitus: a systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prevent. 2013;22(12):2258–2268.
57. Pisani P. Hyper-insulinaemia and cancer, meta-analyses of epidemiological studies. Arch Physiol Biochem. 2008;114(1):63–70.
58. Belfiore A, Malaguarnera R. Insulin receptor and cancer. Endocrine- Related Cancer. 2011;18(4):R125–R147.
59. Westley RL, May FE. A twenty-first century cancer epidemic caused by obesity: the involvement of insulin, diabetes, and insulin-like growth factors. Int J Endocrinol. 2013;632461.
60. Pollak M. The insulin and insulin-like growth factor receptor family in neoplasia: an update. Nat Rev Cancer. 2012;12(3):159–169.
61. LeRoith D, Roberts CT Jr. The insulin-like growth factor system and cancer. Cancer Lett. 2003;195(2):127–137.
62. Durai R, Yang W, Gupta S, Seifalian A, Winslet M. The role of the insulin-like growth factor system in colorectal cancer: review of current knowledge. Int J Colorectal Dis. 2005;20(3):203–220.
63. Sandhu MS, Dunger DB, Giovannucci EL. Insulin, insulin-like growth factor-I (IGF-I), IGF binding proteins, their biologic interactions, and colorectal cancer. J Natl Cancer Inst. 2002;94(13):972–980.
64. Samaras TT, Elrick H, Storms LH. Birthweight, rapid growth, cancer, and longevity: a review. J Natl Med Assoc. 2003;95(12):1170–1183.
65. Jing M, Pollak MN, Giovannucci E, et al. Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor and IGF-binding protein-3. J Natl Cancer Inst. 1999;91(7):620–625.
66. Durai R, Yang W, Gupta S, Seifalian A, Winslet M. The role of the insulin-like growth factor system in colorectal cancer: review of current knowledge. Int J Colorectal Dis. 2005;20(3):203–220.
67. Doi T, Muro K, Yoshino T, et al. Phase I pharmacokinetic study of MK-0646 (dalotuzumab), an anti-insulin-like growth factor-1 receptor monoclonal antibody, in combination with cetuximab and irinotecan in Japanese patients with advanced colorectal cancer. Cancer Chemother Pharmacol. 2013;72(3):643–652.
68. Tolcher AW, Sarantopoulos J, Patnaik A, et al. Phase I pharmacokinetic, and pharmacodynamic study of AMG 479, a fully human monoclonal antibody to insulin-like growth factor receptor 1. J Clin Oncol. 2009;27(34):5800–5807.
69. Yan SD, Schmidt AM, Anderson GM, et al. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J Biol Chem. 1994;269(13):9889.
70. Fuentes MK, Nigavekar SS, Arumugam T, et al. RAGE activation by S100P in colon cancer stimulates growth, migration, and cell signaling pathways. Dis Colon Rectum. 2007;50(8):1230–1240.
71. Boye K, Grotterod I, Aasheim HC, Hovig E, Maelandsmo GM. Activation of NFkappaB by extracellular S100A4: analysis of signal transduction mechanisms and identification of target genes. Int J Cancer. 2008;123:1301–1310.
72. Gebhardt C, Riehl A, Durchdewald M, et al. RAGE signaling sustains inflammation and promotes tumor development. J Exp Med. 2008;205(2):275–285.
73. Arumugam T, Simeone D, Van Golen K, Logsdon C. S100P promotes pancreatic cancer growth, survival, and invasion. Clin Cancer Res. 2005;11(15):5356–5364.
74. Kang R, Tang D, Schapiro NE, et al. The receptor for advanced glycation end products (RAGE) sustains autophagy and limits apoptosis, promoting pancreatic tumor cell survival. Cell Death Different. 2010;17(4):666–676.
75. Liang H, Zhong Y, Zhou S, Peng L. Knockdown of RAGE expression inhibits colorectal cancer cell invasion and suppresses angiogenesis in vitro and in vivo. Cancer Lett. 2011;313(1):91–98.
76. Ben Sahra I, Le Marchand-Brustel Y, Tanti JF, Bost F. Metformin in cancer therapy: a new perspective for an old antidiabetic drug. Mol Cancer Ther. 2010;9(5):1092–1099.
77. Bowker S, Majumadar S, Veugelers P, Johnson JA. Increased cancerrelated mortality for patients with type 2 diabetes who use sulfonylureas or insulin. Diabetes Care. 2006;29:254–258.
78. Libby G, Donnelly LA, Donnan PT, Alessi DR, Morris AD. New users of metformin are at low risk of incident cancer. Diabetes Care. 2009;32(9):1620–1625.
79. Currie CJ, Poole CD, Gale AM. The influence of glucoselowering therapies on cancer risk in type 2 diabetes. Diabetologia. 2009;52:1745–1754.
80. 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(6):813–822.
81. Noto H, Goto A, Tsujimoto T, Noda M. Cancer risk in diabetic patients treated with metformin. PloS One. 2012;7(3):e33411.
82. Evans JM, Donnelly LA, Emslie-Smith AM, Alessi DR, Morris AD. Metformin and reduced risk of cancer in diabetic patients. BMJ. 2005;330:1304–1305.
83. Will MA, Palaniappan M, Peegel H, Kayampilly P, Menon KMJ. Metformin: direct inhibition of rat ovarian theca-interstitial cell proliferation. Fertil Steril. 2012;98(1):207–214.
84. Feng YH, Velazquez-Torres G, Gully C, Chen J, Lee MH, Yeung SC. The impact of type 2 diabetes and antidiabetic drugs on cancer cell growth. J Cell Mol Med. 2011;15(4):825–836.
85. Vazquez-Martin A, Oliveras-Ferraros C, Del Barco S, Martin-Castillo B, Menendez JA. mTOR inhibitors and the anti-diabetic biguanide metformin: new insights into the molecular management of breast cancer resistance to the HER2 tyrosine kinase inhibitor lapatinib (Tykerb(R)). Clin Transl Oncol. 2009;11(7):455–459.
86. Bhalla K, Hwang BJ, Dewi RE, et al. Metformin prevents liver tumorigenesis by inhibiting pathways driving hepatic lipogenesis. Cancer Prev Res. 2012;5(4):544–552.
87. Rumi MA, Ishihara S, Kadowaki Y, et al. Peroxisome proliferatoractivated receptor gamma-dependent and -independent growth inhibition of gastrointestinal tumour cells. Genes Cells. 2004;9(11): 1113–1123.
88. Eibl G, Wente MN, Reber HA, Hines OJ. Peroxisome proliferatoractivated receptor gamma induces pancreatic cancer cell apoptosis. Biochem Biophys Res Commun. 2001;287(2):522–529.
89. Schaefer KL, Wada K, Takahashi H, et al. Peroxisome proliferatoractivated receptor gamma inhibition prevents adhesion to the extracellular matrix and induces anoikis in hepatocellular carcinoma cells. Cancer Res. 2005;65(6):2251–2259.
90. Yu J, Qiao L, Zimmermann L, et al. Troglitazone inhibits tumor growth in hepatocellular carcinoma in vitro and in vivo. Hepatology. 2006;43(1):134–143.
91. Mueller E, Smith M, Sarraf P, et al. Effects of ligand activation of peroxisome proliferator-activated receptor gamma in human prostate cancer. Proc Natl Acad Sci U S A. 2000;97(20):10990–10995.
92. Panigrahy D, Singer S, Shen LQ, et al. PPARgamma ligands inhibit primary tumor growth and metastasis by inhibiting angiogenesis. J Clin Invest. 2002;110(7):923–932.
93. Koga H, Sakisaka S, Harada M, et al. Involvement of p21(WAF1/Cip1), p27(Kip1), and p18(INK4c) in troglitazone-induced cell-cycle arrest in human hepatoma cell lines. Hepatology. 2001;33(5):1087–1097.
94. Borbath I, Leclercq I, Moulin P, Sempoux C, Horsmans Y. The PPARgamma agonist pioglitazone inhibits early neoplastic occurrence in the rat liver. Eur J Cancer. 2007;43(11):1755–1763.
95. Li MY, Deng H, Zhao JM, Dai D, Tan XY. PPARgamma pathway activation results in apoptosis and COX-2 inhibition in HepG2 cells. World J Gastroenterol. 2003;9(6):1220–1226.
96. Boettcher E, Csako G, Pucino F, Wesley R, Loomba R. Meta-analysis: pioglitazone improves liver histology and fibrosis in patient with nonalcoholic steatohepatitis. Aliment Pharmacol Ther. 2012;35(1):66–75.
97. Sanyal AJ, Chalasani N, Kowdley KV, et al. Pioglitazone, vitamin E, or placebo for nonalcoholic steatohepatitis. N Engl J Med. 2010;362:1675–1685.
98. Vigneri R, Squatrito S, Sciacca L. Insulin and its analogs: actions via insulin and IGF receptors. Acta Diabetol. 2010;47(4):271–278.
99. Hemkens LG, Grouven U, Bender R, et al. Risk of malignancies in patients with diabetes treated with human insulin or insulin analogues: a cohort study. Diabetologia. 2009;52:1732–1744.
100. McFarland M, Cripps R. Diabetes mellitus and increased risk of cancer: focus on metformin and the insulin analogs. Pharmacotherapy. 2010;30(11):1159–1178.
101. Wang L, Cai S, Teng Z, Zhao X, Chen X, Bai X. Insulin therapy contributes to the increased risk of colorectal cancer in diabetes patients: a meta-analysis. Diagn Pathol. 2013;8(1):180.
102. Handelsman Y, LeRoith D, Bloomgarden Z, et al. Diabetes and cancer—an AACE/ACE consensus statement. Endocr Pract. 2013;19(4):675–693.