Diabetes mellitus and incidence and mortality of colorectal cancer: A systematic review and meta-analysis of cohort studies

European Journal of Epidemiology

Volumn 26, Issue 11, 2011, Pages 863-876

  Jiang, Ying ^a,b   Ben, Qiwen ^c   Shen, Hong ^a   Lu, Weiqi ^a   Zhang, Yong ^a   Zhu, Jun ^a  

^a FUDAN UNIVERSITY   (China)

^b NANTONG UNIVERSITY   (China)

^c SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Colorectal cancer; Diabetes mellitus; Incidence; Meta analysis; Mortality; Systematic review

Indexed keywords

ARTICLE; BODY MASS; CANCER INCIDENCE; CANCER MORTALITY; CIGARETTE SMOKING; COHORT ANALYSIS; COLORECTAL CANCER; CONFIDENCE INTERVAL; DIABETES MELLITUS; DISEASE ASSOCIATION; EMBASE; FAMILY HISTORY; GEOGRAPHY; HUMAN; MEDLINE; PHYSICAL ACTIVITY; QUANTITATIVE ANALYSIS; REGRESSION ANALYSIS; RISK ASSESSMENT; SCISEARCH; SEX DIFFERENCE; STATISTICAL ANALYSIS; SYSTEMATIC REVIEW;

ADULT; AGED; BODY MASS INDEX; COHORT STUDIES; COLORECTAL NEOPLASMS; CONFIDENCE INTERVALS; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; INCIDENCE; MALE; MIDDLE AGED; REGRESSION ANALYSIS; RISK ASSESSMENT; RISK FACTORS;

EID: 82655173844     PISSN: 03932990     EISSN: 15737284     Source Type: Journal    
DOI: 10.1007/s10654-011-9617-y     Document Type: Article

References (65)

1. A Jemal R Siegel E Ward T Murray J Xu C Smigal, et al. 2006 Cancer statistics, 2006 CA Cancer J Clin 56 2 106 130 16514137 10.3322/canjclin.56.2. 106
2. HL Li YT Gao Y Zheng W Zhang LF Gao B Xu, et al. 2009 Incidence trends of colorectal cancer in urban Shanghai, 1973-2005 Chin J Prev Med 43 10 875 879
3. CL Chen HI Yang WS Yang CJ Liu PJ Chen SL You, et al. 2008 Metabolic factors and risk of hepatocellular carcinoma by chronic hepatitis B/C infection: a follow-up study in Taiwan Gastroenterology 135 1 111 121 18505690 10.1053/j.gastro.2008.03.073 1:CAS:528:DC%2BD1cXps1Wlt78%3D (Pubitemid 351899021)
4. P Zimmet KG Alberti J Shaw 2001 Global and societal implications of the diabetes epidemic Nature 414 6865 782 787 11742409 10.1038/414782a 1:CAS:528:DC%2BD38Xhtlymtg%3D%3D (Pubitemid 34000780)
5. C Heidemann H Boeing T Pischon U Nothlings HG Joost MB Schulze 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 6 281 288 19357973 10.1007/s10654-009-9338-7
6. Q Ben Q Cai Z Li Y Yuan X Ning S Deng, et al. 2011 The relationship between new-onset diabetes mellitus and pancreatic cancer risk: a case-control study Eur J Cancer 47 2 248 254 20709528 10.1016/j.ejca.2010.07.010
7. HB El-Serag H Hampel F Javadi 2006 The association between diabetes and hepatocellular carcinoma: a systematic review of epidemiologic evidence Clin Gastroenterol Hepatol 4 3 369 380 16527702 10.1016/j.cgh.2005.12.007 (Pubitemid 43343895)
8. BB Barone HC Yeh CF Snyder KS Peairs KB Stein RL Derr, et al. 2008 Long-term all-cause mortality in cancer patients with preexisting diabetes mellitus: a systematic review and meta-analysis JAMA 300 23 2754 2764 19088353 10.1001/jama.2008.824 1:CAS:528:DC%2BD1cXhsFalur%2FP
9. F Frasca G Pandini L Sciacca V Pezzino S Squatrito A Belfiore, et al. 2008 The role of insulin receptors and IGF-I receptors in cancer and other diseases Arch Physiol Biochem 114 1 23 37 18465356 10.1080/13813450801969715 1:CAS:528:DC%2BD1cXotlKls7s%3D (Pubitemid 351998752)
10. EE Calle R Kaaks 2004 Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms Nature Rev 4 8 579 591 1:CAS:528: DC%2BD2cXmtVOhsLk%3D (Pubitemid 39025053)
11. A Flood L Strayer C Schairer A Schatzkin 2010 Diabetes and risk of incident colorectal cancer in a prospective cohort of women Cancer Causes Control 21 8 1277 1284 20383575 10.1007/s10552-010-9555-0
12. J He DO Stram LN Kolonel BE Henderson L Le Marchand CA Haiman 2010 The association of diabetes with colorectal cancer risk: the multiethnic cohort Br J Cancer 103 1 120 126 20531412 10.1038/sj.bjc.6605721 1:STN:280: DC%2BC3cnjsVyksA%3D%3D
13. EA Atchison G Gridley JD Carreon MF Leitzmann KA McGlynn 2011 Risk of cancer in a large cohort of U.S. veterans with diabetes Int. J Cancer 128 3 635 643 20473855 10.1002/ijc.25362 1:CAS:528:DC%2BC3cXhsVOkt7fM
14. SC Larsson N Orsini A Wolk 2005 Diabetes mellitus and risk of colorectal cancer: a meta-analysis J Natl Cancer Inst 97 22 1679 1687 16288121 10.1093/jnci/dji375 (Pubitemid 41672234)
15. PJ Limburg RA Vierkant ZS Fredericksen CL Leibson RA Rizza AK Gupta, et al. 2006 Clinically confirmed type 2 diabetes mellitus and colorectal cancer risk: a population-based, retrospective cohort study Am J Gastroenterol 101 8 1872 1879 16790032 10.1111/j.1572-0241.2006.00725.x (Pubitemid 44166600)
16. A Seow JM Yuan WP Koh HP Lee MC Yu 2006 Diabetes mellitus and risk of colorectal cancer in the Singapore Chinese Health Study J Natl Cancer Inst 98 2 135 138 16418516 10.1093/jnci/djj015 (Pubitemid 43159968)
17. R Huxley 2007 The role of lifestyle risk factors on mortality from colorectal cancer in populations of the Asia-Pacific region Asian Pac J Cancer Prev 8 2 191 198 17696730
18. AA Ogunleye SA Ogston AD Morris JM Evans 2009 A cohort study of the risk of cancer associated with type 2 diabetes Br J Cancer 101 7 1199 1201 19690547 10.1038/sj.bjc.6605240 1:STN:280:DC%2BD1MnlsFWisA%3D%3D
19. PT Campbell A Deka EJ Jacobs CC Newton JS Hildebrand ML McCullough, et al. 2010 Prospective study reveals associations between colorectal cancer and type 2 diabetes mellitus or insulin use in men Gastroenterology 139 4 1138 1146 20633560 10.1053/j.gastro.2010.06.072
20. G Chodick AD Heymann L Rosenmann MS Green S Flash A Porath, et al. 2010 Diabetes and risk of incident cancer: a large population-based cohort study in Israel Cancer Causes Control 21 6 879 887 20148361 10.1007/s10552-010-9515-8
21. K Hemminki X Li J Sundquist K Sundquist 2010 Risk of cancer following hospitalization for type 2 diabetes Oncologist 15 6 548 555 20479278 10.1634/theoncologist.2009-0300
22. X Shu J Ji X Li J Sundquist K Sundquist K Hemminki 2010 Cancer risk among patients hospitalized for type 1 diabetes mellitus: a population-based cohort study in Sweden Diabet Med 27 7 791 797 20636960 10.1111/j.1464-5491.2010.03011. x 1:STN:280:DC%2BC3cnotVagtQ%3D%3D
23. DF Stroup JA Berlin SC Morton I Olkin GD Williamson D Rennie, et al. 2000 Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of observational studies in epidemiology (MOOSE) group JAMA 283 15 2008 2012 10789670 10.1001/jama.283.15.2008 1:STN:280: DC%2BD3c3kvVGgsA%3D%3D (Pubitemid 30214957)
24. K Rapp J Schroeder J Klenk H Ulmer H Concin G Diem, et al. 2006 Fasting blood glucose and cancer risk in a cohort of more than 140, 000 adults in Austria Diabetologia 49 5 945 952 16557372 10.1007/s00125-006-0207-6 1:CAS:528:DC%2BD28XjvFWrtLg%3D
25. RE Schoen CM Tangen LH Kuller GL Burke M Cushman RP Tracy, et al. 1999 Increased blood glucose and insulin, body size, and incident colorectal cancer J Natl Cancer Inst 91 13 1147 1154 10393723 10.1093/jnci/91.13.1147 1:STN:280:DyaK1Mzit1Sitw%3D%3D (Pubitemid 29330553)
26. XH Zhou Q Qiao B Zethelius K Pyorala S Soderberg A Pajak, et al. 2010 Diabetes, prediabetes and cancer mortality Diabetologia 53 9 1867 1876 20490448 10.1007/s00125-010-1796-7 1:CAS:528:DC%2BC3cXpsV2ltro%3D
27. K Zendehdel O Nyren CG Ostenson HO Adami A Ekbom W Ye 2003 Cancer incidence in patients with type 1 diabetes mellitus: a population-based cohort study in Sweden J Natl Cancer Inst 95 23 1797 1800 14652242 10.1093/jnci/djg105 (Pubitemid 38008903)
28. R Der Simonian N Laird 1986 Meta-analysis in clinical trials Control Clin Trials 7 3 177 188 10.1016/0197-2456(86)90046-2 (Pubitemid 17189972)
29. CB Begg M Mazumdar 1994 Operating characteristics of a rank correlation test for publication bias Biometrics 50 4 1088 1101 7786990 10.2307/2533446 1:STN:280:DyaK2Mzgs1GrtQ%3D%3D
30. M Egger GS Davey M Schneider C Minder 1997 Bias in meta-analysis detected by a simple, graphical test BMJ 315 7109 629 634 9310563 10.1136/bmj.315.7109. 629 1:STN:280:DyaK2svls1KjtA%3D%3D (Pubitemid 27387172)
31. SH Jee H Ohrr JW Sull JE Yun M Ji JM Samet 2005 Fasting serum glucose level and cancer risk in Korean men and women JAMA 293 2 194 202 15644546 10.1001/jama.293.2.194 1:CAS:528:DC%2BD2MXktVyqsg%3D%3D (Pubitemid 40095870)
32. M Inoue M Iwasaki T Otani S Sasazuki M Noda S Tsugane 2006 Diabetes mellitus and the risk of cancer: results from a large-scale population-based cohort study in Japan Arch Intern Med 166 17 1871 1877 17000944 10.1001/archinte.166.17.1871 (Pubitemid 44455170)
33. M Khan M Mori Y Fujino A Shibata F Sakauchi M Washio, et al. 2006 Site-specific cancer risk due to diabetes mellitus history: evidence from the Japan Collaborative Cohort (JACC) Study Asian Pac J Cancer Prev 7 2 253 259 16839219
34. X Ren X Zhang X Zhang W Gu K Chen Y Le, et al. 2009 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 123 8 540 544 19664792 10.1016/j.puhe.2009.06.019 1:STN:280:DC%2BD1MnhsVGmuw%3D%3D
35. II Kessler 1970 Cancer mortality among diabetics J Natl Cancer Inst 44 3 673 686 11515436 1:STN:280:DC%2BD3MvntFWruw%3D%3D
36. M Ragozzino LJ Melton 3rd CP Chu PJ Palumbo 1982 Subsequent cancer risk in the incidence cohort of Rochester, Minnesota, residents with diabetes mellitus J Chron Dis 35 1 13 19 7068798 10.1016/0021-9681(82)90025-X 1:STN:280:DyaL387msl2hsw%3D%3D (Pubitemid 12213476)
37. K Steenland S Nowlin S Palu 1995 Cancer incidence in the National Health, Nutrition Survey I. Follow-up data: diabetes, cholesterol, pulse and physical activity Cancer Epidemiol Biomarkers Prev 4 8 807 811 8634649 1:STN:280:DyaK287pt1aqsA%3D%3D
38. JC Will DA Galuska F Vinicor EE Calle 1998 Colorectal cancer: another complication of diabetes mellitus? Am J Epidemiol 147 9 816 825 9583711 1:STN:280:DyaK1c3ktlSluw%3D%3D (Pubitemid 28244386)
39. FB Hu JE Manson S Liu D Hunter GA Colditz KB Michels, et al. 1999 Prospective study of adult onset diabetes mellitus (type 2) and risk of colorectal cancer in women J Natl Cancer Inst 91 6 542 547 10088625 10.1093/jnci/91.6.542 1:STN:280:DyaK1M7os1CrtA%3D%3D (Pubitemid 29157063)
40. SS Coughlin EE Calle LR Teras J Petrelli MJ Thun 2004 Diabetes mellitus as a predictor of cancer mortality in a large cohort of US adults Am J Epidemiol 159 12 1160 1167 15191933 10.1093/aje/kwh161 (Pubitemid 38747263)
41. PJ Limburg KE Anderson TW Johnson DR Jacobs Jr D Lazovich CP Hong, et al. 2005 Diabetes mellitus and subsite-specific colorectal cancer risks in the Iowa women's health study Cancer Epidemiol Biomarkers Prev 14 1 133 137 15668486 (Pubitemid 40165293)
42. RL Ahmed KH Schmitz KE Anderson WD Rosamond AR Folsom 2006 The metabolic syndrome and risk of incident colorectal cancer Cancer 107 1 28 36 16721800 10.1002/cncr.21950 (Pubitemid 43941640)
43. T Sturmer JE Buring IM Lee JM Gaziano RJ Glynn 2006 Metabolic abnormalities and risk for colorectal cancer in the physicians' health study Cancer Epidemiol Biomarkers Prev 15 12 2391 2397 17164361 10.1158/1055-9965.EPI- 06-0391 (Pubitemid 46048295)
44. AR Folsom JS Pankow JM Peacock SJ Bielinski G Heiss E Boerwinkle 2008 Variation in TCF7L2 and increased risk of colon cancer: the atherosclerosis risk in communities (ARIC) Study Diabetes Care 31 5 905 909 18268068 10.2337/dc07-2131
45. HO Adami J McLaughlin A Ekbom C Berne D Silverman D Hacker, et al. 1991 Cancer risk in patients with diabetes mellitus Cancer Causes Control 2 5 307 314 1932543 10.1007/BF00051670 1:STN:280:DyaK38%2Fjt1GjtA%3D%3D
46. E Weiderpass G Gridley O Nyren A Ekbom I Persson HO Adami 1997 Diabetes mellitus and risk of large bowel cancer J Natl Cancer Inst 89 9 660 661 9150194 10.1093/jnci/89.9.660 1:STN:280:DyaK2s3psVCgug%3D%3D (Pubitemid 27200500)
47. L Wideroff G Gridley L Mellemkjaer WH Chow M Linet S Keehn, et al. 1997 Cancer incidence in a population-based cohort of patients hospitalized with diabetes mellitus in Denmark J Natl Cancer Inst 89 18 1360 1365 9308706 10.1093/jnci/89.18.1360 1:STN:280:DyaK2svlt1aqsA%3D%3D (Pubitemid 27418027)
48. TI Nilsen LJ Vatten 2001 Prospective study of colorectal cancer risk and physical activity, diabetes, blood glucose and BMI: exploring the hyperinsulinaemia hypothesis Br J Cancer 84 3 417 422 11161410 10.1054/bjoc.2000.1582 1:STN:280:DC%2BD3M7kt12itQ%3D%3D (Pubitemid 32154439)
49. G Verlato G Zoppini E Bonora M Muggeo 2003 Mortality from site-specific malignancies in type 2 diabetic patients from Verona Diabetes Care 26 4 1047 1051 12663571 10.2337/diacare.26.4.1047 (Pubitemid 36929246)
50. KT Khaw N Wareham S Bingham R Luben A Welch N Day 2004 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 13 6 915 919 15184246 (Pubitemid 38756700)
51. SC Larsson E Giovannucci A Wolk 2005 Diabetes and colorectal cancer incidence in the cohort of Swedish men Diabetes Care 28 7 1805 1807 15983343 10.2337/diacare.28.7.1805 (Pubitemid 40923101)
52. K Bowers D Albanes P Limburg P Pietinen PR Taylor J Virtamo, et al. 2006 A prospective study of anthropometric and clinical measurements associated with insulin resistance syndrome and colorectal cancer in male smokers Am J Epidemiol 164 7 652 664 16877536 10.1093/aje/kwj253 (Pubitemid 44453494)
53. GD Batty MJ Shipley M Marmot GD Smith 2004 Diabetes status and post-load plasma glucose concentration in relation to site-specific cancer mortality: findings from the original Whitehall study Cancer Causes Control 15 9 873 881 15577289 10.1007/s10552-004-1050-z (Pubitemid 39663863)
54. AJ Swerdlow SP Laing Z Qiao SD Slater AC Burden JL Botha, et al. 2005 Cancer incidence and mortality in patients with insulin-treated diabetes: a UK cohort study Br J Cancer 92 11 2070 2075 15886700 10.1038/sj.bjc.6602611 1:STN:280:DC%2BD2M3ot1Kisg%3D%3D (Pubitemid 40897432)
55. Y Okura LH Urban DW Mahoney SJ Jacobsen RJ Rodeheffer 2004 Agreement between self-report questionnaires and medical record data was substantial for diabetes, hypertension, myocardial infarction and stroke but not for heart failure J Clin Epidemiol 57 10 1096 1103 15528061 10.1016/j.jclinepi.2004.04.005 (Pubitemid 39446649)
56. U Smith EA Gale 2009 Does diabetes therapy influence the risk of cancer? Diabetologia 52 9 1699 1708 19597799 10.1007/s00125-009-1441-5 1:STN:280:DC%2BD1Mrktl2mtQ%3D%3D
57. M Bodmer C Meier S Krahenbuhl SS Jick CR Meier 2010 Long-term metformin use is associated with decreased risk of breast cancer Diabetes Care 33 6 1304 1308 20299480 10.2337/dc09-1791 1:CAS:528:DC%2BC3cXotFKhs7g%3D
58. X Wu Z Fan H Masui N Rosen J Mendelsohn 1995 Apoptosis induced by an anti-epidermal growth factor receptor monoclonal antibody in a human colorectal carcinoma cell line and its delay by insulin J Clin Invest 95 4 1897 1905 7706497 10.1172/JCI117871 1:CAS:528:DyaK2MXkslykuro%3D
59. Weng CJ, Hsieh YH, Tsai CM, Chu YH, Ueng KC, Liu YF et al. Relationship of insulin-like growth factors system gene polymorphisms with the susceptibility and pathological development of hepatocellular carcinoma. Ann Surg Oncol. 2010;17(7):1808-15.
60. S Fernandez-Veledo I Nieto-Vazquez R Vila-Bedmar L Garcia-Guerra M Alonso-Chamorro M Lorenzo 2009 Molecular mechanisms involved in obesity-associated insulin resistance: therapeutical approach Arch Physiol Biochem 115 4 227 239 19673658 10.1080/13813450903164330 1:CAS:528: DC%2BD1MXhtl2qtL7I
61. K Kajiura T Ohkusa I Okayasu 1998 Relationship between fecal bile acids and the occurrence of colorectal neoplasia in experimental murine ulcerative colitis Digestion 59 1 69 72 9468101 10.1159/000007469 1:CAS:528: DyaK1cXltF2htA%3D%3D (Pubitemid 28022449)
62. Bergenstal RMKD, Franz MJ, Rubenstein AH. Management of type 2 diabetes: a systematic approach to meeting the standards of care. II: oral agents, insulin, and management of complications. In: DeGroot LJ, Jameson JL, editors. Endocrinology. 4th ed. Philadelphia: WB Saunders Co.; 2001. p. 821-35.
63. JP Boyle AA Honeycutt KM Narayan TJ Hoerger LS Geiss H Chen, et al. 2001 Projection of diabetes burden through 2050: impact of changing demography and disease prevalence in the US Diabetes Care 24 11 1936 1940 11679460 10.2337/diacare.24.11.1936 1:STN:280:DC%2BD3MrntF2jsA%3D%3D (Pubitemid 33716504)
64. Yang W, Lu J, Weng J, Jia W, Ji L, Xiao J et al. Prevalence of diabetes among men and women in China. N Engl J Med. 2010;362(12):1090-101.
65. Ferlay J, Parkin DM, Steliarova-Foucher E. Estimates of cancer incidence and mortality in Europe in 2008. Eur J Cancer. 2010;46(4):765-81.