Diabetes mellitus is an independent risk factor for colorectal cancer

Digestive Diseases and Sciences

Volumn 57, Issue 6, 2012, Pages 1586-1597

  Sun, Lei ^a   Yu, Shiying ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Colorectal cancer; Diabetes mellitus; Incidence; Meta analysis

Indexed keywords

AFRICAN AMERICAN; ASIAN; CANCER RISK; COLORECTAL CANCER; DIABETES MELLITUS; DIABETIC PATIENT; DISEASE DURATION; ETHNICITY; EUROPEAN AMERICAN; EXPOSURE; HUMAN; PRIORITY JOURNAL; RACE; REVIEW; RISK FACTOR; SEX DIFFERENCE; SYSTEMATIC REVIEW;

ADULT; AGE DISTRIBUTION; AGED, 80 AND OVER; CASE-CONTROL STUDIES; COHORT STUDIES; COLORECTAL NEOPLASMS; COMORBIDITY; DIABETES MELLITUS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; INCIDENCE; MALE; MIDDLE AGED; PROGNOSIS; RISK ASSESSMENT; SEX DISTRIBUTION; SURVIVAL ANALYSIS;

EID: 84864285430     PISSN: 01632116     EISSN: 15732568     Source Type: Journal    
DOI: 10.1007/s10620-012-2059-x     Document Type: Review

References (103)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics. CA Cancer J Clin. 2010;60:277-300.
2. Boyle JP, Honeycutt AA, Narayan KM, et al. Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the u.S. Diabetes Care. 2001;24: 1936-1940. (Pubitemid 33716504)
3. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27:1047-1053. (Pubitemid 38579764)
4. Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87:4-14.
5. Potter JD. Nutrition and colorectal cancer. Cancer Causes Control. 1996;7:127-146. (Pubitemid 26066852)
6. Satia-Abouta J, Galanko JA, Martin CF, Ammerman A, Sandler RS. Food groups and colon cancer risk in African-Americans and caucasians. Int J Cancer. 2004;109:728-736. (Pubitemid 38405621)
7. Willett W. The search for the causes of breast and colon cancer. Nature. 1989;338:389-394. (Pubitemid 19089320)
8. Salmeron J, Manson JE, Stampfer MJ, Colditz GA, Wing AL, Willett WC. Dietary fiber, glycemic load, and risk of non-insulindependent diabetes mellitus in women. JAMA. 1997;277: 472-477. (Pubitemid 27074331)
9. Salmeron J, Ascherio A, Rimm EB, et al. Dietary fiber, glycemic load, and risk of niddm in men. Diabetes Care. 1997;20:545-550. (Pubitemid 27143413)
10. Colditz GA, Willett WC, Stampfer MJ, et al. Weight as a risk factor for clinical diabetes in women. Am J Epidemiol. 1990; 132:501-513. (Pubitemid 20285148)
11. Giovannucci E, Ascherio A, Rimm EB, Colditz GA, Stampfer MJ, Willett WC. Physical activity, obesity, and risk for colon cancer and adenoma in men. Ann Intern Med. 1995;122:327-334.
12. Martinez ME, Giovannucci E, Spiegelman D, Hunter DJ, Willett WC, Colditz GA. Leisure-time physical activity, body size, and colon cancer in women. Nurses' health study research group. J Natl Cancer Inst. 1997;89:948-955. (Pubitemid 27282067)
13. Manson JE, Rimm EB, Stampfer MJ, et al. Physical activity and incidence of non-insulin-dependent diabetes mellitus in women. Lancet. 1991;338:774-778.
14. McKeown-Eyssen G. Epidemiology of colorectal cancer revisited: are serum triglycerides and/or plasma glucose associated with risk? Cancer Epidemiol Biomarkers Prev. 1994;3:687-695. (Pubitemid 24377963)
15. Giovannucci E. Insulin and colon cancer. Cancer Causes Control. 1995;6:164-179.
16. Larsson SC, Orsini N, Wolk A. Diabetes mellitus and risk of colorectal cancer: a meta-analysis. J Natl Cancer Inst. 2005;97: 1679-1687. (Pubitemid 41672234)
17. Ahmed RL, Schmitz KH, Anderson KE, Rosamond WD, Folsom AR. The metabolic syndrome and risk of incident colorectal cancer. Cancer. 2006;107:28-36. (Pubitemid 43941640)
18. 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;166:1871-1877. (Pubitemid 44455170)
19. Khan M, Mori M, Fujino Y, et al. Site-specific cancer risk due to diabetes mellitus history: evidence from the japan collaborative cohort (jacc) study. Asian Pac J Cancer Prev APJCP. 2006;7: 253-259.
20. Limburg PJ, Vierkant RA, Fredericksen ZS, et al. Clinically confirmed type 2 diabetes mellitus and colorectal cancer risk: a population-based, retrospective cohort study. Am J Gastroenterol. 2006;101:1872-1879. (Pubitemid 44166600)
21. 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: 2105-2109.
22. Seow A, Yuan JM, Koh WP, Lee HP, Yu MC. Diabetes mellitus and risk of colorectal cancer in the Singapore Chinese health study. J Natl Cancer Inst. 2006;98:135-138. (Pubitemid 43159968)
23. Sturmer T, Buring JE, Lee IM, Gaziano JM, Glynn RJ. Metabolic abnormalities and risk for colorectal cancer in the physicians' health study. Cancer Epidemiol Biomarkers Prev. 2006; 15:2391-2397. (Pubitemid 46048295)
24. Dankner R, Chetrit A, Segal P. Glucose tolerance status and 20 year cancer incidence. Isr Med Assoc J IMAJ. 2007;9: 592-596. (Pubitemid 47323414)
25. Kuriki K, Hirose K, Tajima K. Diabetes and cancer risk for all and specific sites among Japanese men and women. Eur J Cancer Prev. 2007;16:83-89. (Pubitemid 46105011)
26. 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;101:1199-1201.
27. Ren X, Zhang X, Gu W, et al. Type 2 diabetes mellitus associated with increased risk for colorectal cancer: evidence from an international ecological study and population-based risk analysis in China. Public Health. 2009;123:540-544.
28. Vinikoor LC, Long MD, Keku TO, Martin CF, Galanko JA, Sandler RS. The association between diabetes, insulin use, and colorectal cancer among whites and African Americans. Cancer Epidemiol Biomarkers Prev. 2009;18:1239-1242.
29. Campbell PT, Deka A, Jacobs EJ, et al. Prospective study reveals associations between colorectal cancer and type 2 diabetes mellitus or insulin use in men. Gastroenterology. 2010; 139:1138-1146.
30. Chodick G, Heymann AD, Rosenmann L, et al. Diabetes and risk of incident cancer: a large population-based cohort study in israel. Cancer Causes Control CCC. 2010;21:879-887.
31. Flood A, Strayer L, Schairer C, Schatzkin A. Diabetes and risk of incident colorectal cancer in a prospective cohort of women. Cancer Causes Control CCC. 2010;21:1277-1284.
32. He J, Stram DO, Kolonel LN, Henderson BE, Le Marchand L, Haiman CA. The association of diabetes with colorectal cancer risk: the multiethnic cohort. Br J Cancer. 2010;103:120-126.
33. Hemminki K, Li X, Sundquist J, Sundquist K. Risk of cancer following hospitalization for type 2 diabetes. Oncologist. 2010; 15:548-555.
34. Wotton CJ, Yeates DG, Goldacre MJ. Cancer in patients admitted to hospital with diabetes mellitus aged 30 years and over: record linkage studies. Diabetologia. 2011;54:527-534.
35. Giovannucci E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr. 2001;131:3109S-3120S. (Pubitemid 33070788)
36. Wu X, Chen VW, Martin J, et al. Subsite-specific colorectal cancer incidence rates and stage distributions among Asians and pacific islanders in the United States, 1995 to 1999. Cancer Epidemiol Biomarkers Prev. 2004;13:1215-1222. (Pubitemid 38917911)
37. Cheng X, Chen VW, Steele B, et al. Subsite-specific incidence rate and stage of disease in colorectal cancer by race, gender, and age group in the United States, 1992-1997. Cancer. 2001; 92:2547-2554. (Pubitemid 33049437)
38. Ward R, Meagher A, Tomlinson I, et al. Microsatellite instability and the clinicopathological features of sporadic colorectal cancer. Gut. 2001;48:821-829. (Pubitemid 32476985)
39. Breivik J, Lothe RA, Meling GI, Rognum TO, Borresen-Dale AL, Gaudernack G. Different genetic pathways to proximal and distal colorectal cancer influenced by sex-related factors. Int J Cancer. 1997;74:664-669. (Pubitemid 28037512)
40. Karter AJ, Ferrara A, Liu JY, Moffet HH, Ackerson LM, Selby JV. Ethnic disparities in diabetic complications in an insured population. JAMA. 2002;287:2519-2527. (Pubitemid 34517197)
41. La Vecchia C, D'Avanzo B, Negri E, Franceschi S. History of selected diseases and the risk of colorectal cancer. Eur J Cancer. 1991;27:582-586.
42. Hu FB, Manson JE, Liu S, et al. Prospective study of adult onset diabetes mellitus (type 2) and risk of colorectal cancer in women. J Natl Cancer Inst. 1999;91:542-547. (Pubitemid 29157063)
43. Yang YX, Hennessy S, Lewis JD. Type 2 diabetes mellitus and the risk of colorectal cancer. Clin Gastroenterol Hepatol. 2005; 3:587-594. (Pubitemid 40824752)
44. Wells GASB, O'Connell D, Peterson J, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. http://ohri.ca/programs/clinical-epidemiology/oxford.htm. Accessed June, 2010.
45. Greenland S. Quantitative methods in the review of epidemiologic literature. Epidemiol Rev. 1987;9:1-30.
46. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177-188. (Pubitemid 17189972)
47. Cochran WG. The combination of estimates from different experiments. Biometrics. 1954;10:101-129.
48. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21:1539-1558. (Pubitemid 34746062)
49. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557-560. (Pubitemid 37088507)
50. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088-1101.
51. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315:629-634. (Pubitemid 27387172)
52. Ragozzino M, Melton LJ 3rd, Chu CP, Palumbo PJ. Subsequent cancer risk in the incidence cohort of Rochester, Minnesota, residents with diabetes mellitus. J Chron Dis. 1982;35:13-19. (Pubitemid 12213476)
53. O'Mara BA, Byers T, Schoenfeld E. Diabetes mellitus and cancer risk: a multisite case-control study. J Chron Dis. 1985; 38:435-441. (Pubitemid 15025864)
54. Kune GA, Kune S, Watson LF. Colorectal cancer risk, chronic illnesses, operations, and medications: case control results from the Melbourne colorectal cancer study. Cancer Res. 1988;48: 4399-4404.
55. Steenland K, Nowlin S, Palu S. Cancer incidence in the national health and nutrition survey I. Follow-up data: Diabetes, cholesterol, pulse and physical activity. Cancer Epidemiol Biomarkers Prev. 1995;4:807-811.
56. La Vecchia C, Negri E, Decarli A, Franceschi S. Diabetes mellitus and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev. 1997;6:1007-1010. (Pubitemid 28007409)
57. Le Marchand L, Wilkens LR, Kolonel LN, Hankin JH, Lyu LC. Associations of sedentary lifestyle, obesity, smoking, alcohol use, and diabetes with the risk of colorectal cancer. Cancer Res. 1997;57:4787-4794. (Pubitemid 27468985)
58. Weiderpass E, Gridley G, Nyren O, Ekbom A, Persson I, Adami HO. Diabetes mellitus and risk of large bowel cancer. J Natl Cancer Inst. 1997;89:660-661. (Pubitemid 27200500)
59. Wideroff L, Gridley G, Mellemkjaer L, et al. Cancer incidence in a population-based cohort of patients hospitalized with diabetes mellitus in Denmark. J Natl Cancer Inst. 1997;89:1360-1365. (Pubitemid 27418027)
60. Will JC, Galuska DA, Vinicor F, Calle EE. Colorectal cancer: another complication of diabetes mellitus? Am J Epidemiol. 1998;147:816-825. (Pubitemid 28244386)
61. Schoen RE, Tangen CM, Kuller LH, et al. Increased blood glucose and insulin, body size, and incident colorectal cancer. J Natl Cancer Inst. 1999;91:1147-1154. (Pubitemid 29330553)
62. Nilsen TI, Vatten LJ. Prospective study of colorectal cancer risk and physical activity, diabetes, blood glucose and BMI: exploring the hyperinsulinaemia hypothesis. Br J Cancer. 2001; 84:417-422. (Pubitemid 32154439)
63. Levi F, Pasche C, Lucchini F, La Vecchia C. Diabetes mellitus, family history, and colorectal cancer. J Epidemiol Community Health. 2002;56:479-480; author reply 480. (Pubitemid 34539008)
64. Saydah SH, Platz EA, Rifai N, Pollak MN, Brancati FL, Helzlsouer KJ. Association of markers of insulin and glucose control with subsequent colorectal cancer risk. Cancer Epidemiol Biomarkers Prev. 2003;12:412-418. (Pubitemid 36578478)
65. Khaw KT, Wareham N, Bingham S, Luben R, Welch A, Day N. Preliminary communication: Glycated hemoglobin, diabetes, and incident colorectal cancer in men and women: A prospective analysis from the European prospective investigation into cancer-norfolk study. Cancer Epidemiol Biomarkers Prev. 2004;13: 915-919. (Pubitemid 38756700)
66. 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: J Am Med Assoc. 2005;293:194-202. (Pubitemid 40095870)
67. Larsson SC, Giovannucci E, Wolk A. Diabetes and colorectal cancer incidence in the cohort of Swedish men. Diabetes Care. 2005;28:1805-1807. (Pubitemid 40923101)
68. Limburg PJ, Anderson KE, Johnson TW, et al. Diabetes mellitus and subsite-specific colorectal cancer risks in the Iowa women's health study. Cancer Epidemiol Biomarkers Prev. 2005;14: 133-137. (Pubitemid 40165293)
69. Swerdlow AJ, Laing SP, Qiao Z, et al. Cancer incidence and mortality in patients with insulin-treated diabetes: a UK cohort study. Br J Cancer. 2005;92:2070-2075. (Pubitemid 40897432)
70. Pollak MN, Perdue JF, Margolese RG, Baer K, Richard M. Presence of somatomedin receptors on primary human breast and colon carcinomas. Cancer Lett. 1987;38:223-230. (Pubitemid 18005853)
71. Guo YS, Narayan S, Yallampalli C, Singh P. Characterization of insulin like growth factor I receptors in human colon cancer. Gastroenterology. 1992;102:1101-1108.
72. Watkins LF, Lewis LR, Levine AE. Characterization of the synergistic effect of insulin and transferrin and the regulation of their receptors on a human colon carcinoma cell line. Int J Cancer. 1990;45:372-375. (Pubitemid 20061396)
73. Koenuma M, Yamori T, Tsuruo T. Insulin and insulin-like growth factor 1 stimulate proliferation of metastatic variants of colon carcinoma 26. Jpn J Cancer Res. 1989;80:51-58. (Pubitemid 20027198)
74. Bjork J, Nilsson J, Hultcrantz R, Johansson C. Growth-regulatory effects of sensory neuropeptides, epidermal growth factor, insulin, and somatostatin on the non-transformed intestinal epithelial cell line iec-6 and the colon cancer cell line ht 29. Scand J Gastroenterol. 1993;28:879-884. (Pubitemid 23294761)
75. Burgering BM, Medema RH, Maassen JA, et al. Insulin stimulation of gene expression mediated by p21ras activation. EMBO J. 1991;10:1103-1109. (Pubitemid 21905571)
76. Moller DE, Flier JS. Insulin resistance-mechanisms, syndromes, and implications. N Engl J Med. 1991;325:938-948.
77. Jhun BH, Meinkoth JL, Leitner JW, Draznin B, Olefsky JM. Insulin and insulin-like growth factor-i signal transduction requires p21ras. J Biol Chem. 1994;269:5699-5704.
78. Leitner JW, Kline T, Carel K, Goalstone M, Draznin B. Hyperinsulinemia potentiates activation of p21ras by growth factors. Endocrinology. 1997;138:2211-2214. (Pubitemid 27180843)
79. Ruggeri BA, Klurfeld DM, Kritchevsky D, Furlanetto RW. Caloric restriction and 7,12-dimethylbenz(a)anthracene-induced mammary tumor growth in rats: Alterations in circulating insulin, insulin-like growth factors i and ii, and epidermal growth factor. Cancer Res. 1989;49:4130-4134. (Pubitemid 19207248)
80. Klurfeld DM, Lloyd LM, Welch CB, Davis MJ, Tulp OL, Kritchevsky D. Reduction of enhanced mammary carcinogenesis in la/n-cp (corpulent) rats by energy restriction. Proc Soc Exp Biol Med. 1991;196:381-384.
81. Dy DY, Whitehead RH, Morris DL. Sms 201.995 inhibits in vitro and in vivo growth of human colon cancer. Cancer Res. 1992;52:917-923.
82. Corpet DE, Jacquinet C, Peiffer G, Tache S. Insulin injections promote the growth of aberrant crypt foci in the colon of rats. Nutr Cancer. 1997;27:316-320. (Pubitemid 27161531)
83. Tran TT, Medline A, Bruce WR. Insulin promotion of colon tumors in rats. Cancer Epidemiol Biomarkers Prev. 1996;5: 1013-1015. (Pubitemid 26415875)
84. Koohestani N, Tran TT, Lee W, Wolever TM, Bruce WR. Insulin resistance and promotion of aberrant crypt foci in the colons of rats on a high-fat diet. Nutr Cancer. 1997;29:69-76. (Pubitemid 27508127)
85. Ma J, Pollak MN, Giovannucci E, et al. Prospective study of colorectal cancer risk in men and plasma levels of insulin-like growth factor (igf)-i and igf-binding protein-3. J Natl Cancer Inst. 1999;91:620-625. (Pubitemid 29194048)
86. Kaaks R, Toniolo P, Akhmedkhanov A, et al. Serum c-peptide, insulin-like growth factor (igf)-i, igf-binding proteins, and colorectal cancer risk in women. J Natl Cancer Inst. 2000;92: 1592-1600.
87. Li H, Stampfer MJ, Giovannucci EL, et al. A prospective study of plasma selenium levels and prostate cancer risk. J Natl Cancer Inst. 2004;96:696-703. (Pubitemid 38660232)
88. Airley RE, Mobasheri A. Hypoxic regulation of glucose transport, anaerobic metabolism and angiogenesis in cancer: novel pathways and targets for anticancer therapeutics. Chemotherapy. 2007;53:233-256. (Pubitemid 47074647)
89. Moreno-Sanchez R, Rodriguez-Enriquez S, Marin-Hernandez A, Saavedra E. Energy metabolism in tumor cells. FEBS J. 2007;274:1393-1418. (Pubitemid 46333738)
90. Warburg O. On the origin of cancer cells. Science. 1956; 123:309-314.
91. Schulze PC, Yoshioka J, Takahashi T, He Z, King GL, Lee RT. Hyperglycemia promotes oxidative stress through inhibition of thioredoxin function by thioredoxin-interacting protein. J Biol Chem. 2004;279:30369-30374. (Pubitemid 38937964)
92. Stocks T, Rapp K, Bjorge T, et al. Blood glucose and risk of incident and fatal cancer in the metabolic syndrome and cancer project (me-can): analysis of six prospective cohorts. PLoS Med. 2009;6:e1000201.
93. Campagnoli C, Ambroggio S, Biglia N, Sismondi P. Conjugated estrogens and breast cancer risk. Gynecol Endocrinol. 1999;13(Suppl 6):13-19. (Pubitemid 30068320)
94. Calle EE, Miracle-McMahill HL, Thun MJ, Heath CW Jr. Estrogen replacement therapy and risk of fatal colon cancer in a prospective cohort of postmenopausal women. J Natl Cancer Inst. 1995;87:517-523.
95. Grodstein F, Martinez ME, Platz EA, et al. Postmenopausal hormone use and risk for colorectal cancer and adenoma. Ann Intern Med. 1998;128:705-712. (Pubitemid 28204861)
96. Mayne N. Neuropathy in the diabetic and non-diabetic populations. Lancet. 1965;2:1313-1316.
97. Debruyne PR, Bruyneel EA, Li X, Zimber A, Gespach C, Mareel MM. The role of bile acids in carcinogenesis. Mutat Res. 2001;480-481:359-369. (Pubitemid 32744842)
98. Potter JD. Reconciling the epidemiology, physiology, and molecular biology of colon cancer. JAMA. 1992;268:1573-1577.
99. Burchard EG, Ziv E, Coyle N, et al. The importance of race and ethnic background in biomedical research and clinical practice. N Engl J Med. 2003;348:1170-1175. (Pubitemid 36337330)
100. Grimes DA, Schulz KF. Bias and causal associations in observational research. Lancet. 2002;359:248-252. (Pubitemid 34113828)
101. Centers for Diseases Control and Prenvention (CDC). Prevalence of diabetes and impaired fasting glucose in adults - United States, 1999-2000. MMWR Morb Mortal Wkly Rep. 2003;52: 833-837.
102. Gregg EW, Cadwell BL, Cheng YJ, et al. Trends in the prevalence and ratio of diagnosed to undiagnosed diabetes according to obesity levels in the U.S. Diabetes Care. 2004;27:2806-2812. (Pubitemid 39565041)
103. Harris MI, Flegal KM, Cowie CC, et al. Prevalence of diabetes, impaired fasting glucose, and impaired glucose tolerance in U.S. Adults. The third national health and nutrition examination survey, 1988-1994. Diabetes Care. 1998;21:518-524. (Pubitemid 28172927)