A quantitative analysis of body mass index and colorectal cancer: findings from 56 observational studies
Y. Ning,
L. Wang,
E. L. Giovannucci,
Corresponding Author
Y. Ning
Department of Nutrition, Harvard School of Public Health, Boston, MA, USA;
Y Ning, Department of Nutrition, Harvard School of Public Health and Channing laboratory, 677 Huntington Avenue, Boston 02115, MA, USA. E-mail: [email protected]Search for more papers by this authorL. Wang
Department of Nutrition, Harvard School of Public Health, Boston, MA, USA;
Search for more papers by this authorE. L. Giovannucci
Department of Nutrition, Harvard School of Public Health, Boston, MA, USA;
Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA;
Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA
Search for more papers by this author
Y. Ning,
L. Wang,
E. L. Giovannucci,
Corresponding Author
Y. Ning
Department of Nutrition, Harvard School of Public Health, Boston, MA, USA;
Y Ning, Department of Nutrition, Harvard School of Public Health and Channing laboratory, 677 Huntington Avenue, Boston 02115, MA, USA. E-mail: [email protected]Search for more papers by this authorL. Wang
Department of Nutrition, Harvard School of Public Health, Boston, MA, USA;
Search for more papers by this authorE. L. Giovannucci
Department of Nutrition, Harvard School of Public Health, Boston, MA, USA;
Channing Laboratory, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA;
Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA
Search for more papers by this authorThe work was supported by grants R01 CA55076 from the National Cancer Institute. Support for Dr. Ning was provided by James K. Knox Memorial Fund, Department of Nutrition, Harvard School of Public Health.
Summary
To perform a systematic review of studies reporting on the association between body mass index (BMI) and the risk of colorectal cancer, we conducted a meta-analysis and meta-regression analysis. The identified 56 studies were conducted among 7 213 335 individuals including 93 812 cases. Compared with BMI < 23.0 kg m−2, BMI of 23.0–24.9, 25.0–27.4, 27.5–29.9 and ≥30.0 kg m−2 were associated with 14%, 19%, 24% and 41% increased risks, respectively. Asians and premenopausal women had sharply increased risk from BMI < 23 kg m−2 to general ‘normal’ range (23–25 kg m−2). Each 5 kg m−2 increment was associated with 18% increased risk. Meta-regression analysis indicated that the association was stronger for colon than rectal cancer (P < 0.001), for men than women (P < 0.001), for self-reported BMI than directly measured BMI (P < 0.001), and for studies adjusting for physical activity than not adjusting (P < 0.001). The variation of the reported risk estimates for the association can be partly explained by cancer site, sex, women menopausal status, BMI assessment and adjustment of confounding variables.
References
- 1 World Cancer Research Fund/American Institute for Cancer Research. Food, Nutrition, Physical Activity and the Prevention of Cancer: a Global Perspective. World Cancer Research Fund/American Institute for Cancer Research: Washington, DC: AICR, 2007.
- 2 Giovannucci E, Michaud D. The role of obesity and related metabolic disturbances in cancers of the colon, prostate, and pancreas. Gastroenterology 2007; 132: 2208–2225.
- 3 Tamakoshi K, Wakai K, Kojima M, Watanabe Y, Hayakawa N, Toyoshima H, Yatsuya H, Kondo T, Tokudome S, Hashimoto S, Suzuki K, Ito Y, Tamakoshi A; JACC Study Group. A prospective study of body size and colon cancer mortality in Japan: the JACC Study. Int J Obes Relat Metab Disord 2004; 28: 551–558.
- 4 Le Marchand L, Wilkens LR, Mi MP. Obesity in youth and middle age and risk of colorectal cancer in men. Cancer Causes Control 1992; 3: 349–354.
- 5 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.
- 6 DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7: 177–188.
- 7 DerSimonian R, Kacker R. Random-effects model for meta-analysis of clinical trials: an update. Contemp Clin Trials 2007; 28: 105–114.
- 8 World Health Organization. Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 1995; 854: 1–452.
- 9 Berlin JA, Longnecker MP, Greenland S. Meta-analysis of epidemiologic dose-response data. Epidemiology 1993; 4: 218–228.
- 10 Orsini N, Bellocco R, Greenland S. Generalized least squares for trend estimation of summarized dose-reponse data. The Stata Journal 2006; 6: 40–57.
- 11 Morton SC, Adams JL, Suttorp MJ, Shekelle PG (ed.). Meta-regression Approaches: What, Why,When, and How? Technical Review 8 (Prepared by Southern California–RAND Evidence-based Practice Center, under Contract No 290-97-0001). Agency for Healthcare Research and Quality: Rockville, MD, 2004.
- 12 Thompson SG, Higgins JP. How should meta-regression analyses be undertaken and interpreted? Stat Med 2002; 21: 1559–1573.
- 13 Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002; 21: 1539–1558.
- 14 Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629–634.
- 15 Steichen T. METANINF: Stata Module to Evaluate Influence of a Single Study in Meta-analysis Estimation. Boston College Department of Economics, Statistical Software Components: Boston, MA, 2001.
- 16 Dai Z, Xu YC, Niu L. Obesity and colorectal cancer risk: a meta-analysis of cohort studies. World J Gastroenterol 2007; 13: 4199–4206.
- 17 Larsson SC, Wolk A. Obesity and colon and rectal cancer risk: a meta-analysis of prospective studies. Am J Clin Nutr 2007; 86: 556–565.
- 18 Moghaddam AA, Woodward M, Huxley R. Obesity and risk of colorectal cancer: a meta-analysis of 31 studies with 70 000 events. Cancer Epidemiol Biomarkers Prev 2007; 16: 2533–2547.
- 19 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.
- 20 Giovannucci E. Diet, body weight, and colorectal cancer: a summary of the epidemiologic evidence. J Womens Health (Larchmt) 2003; 12: 173–182.
- 21 Giovannucci E. Nutrition, insulin, insulin-like growth factors and cancer. Horm Metab Res 2003; 35: 694–704.
- 22 Willett W. Nutritional Epidemiology, 2nd edn. Oxford University Press: Oxford, 1998.
- 23 Gregor MF, Hotamisligil GS. Thematic review series: adipocyte biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 2007; 48: 1905–1914.
- 24 Bray GA, Lovejoy JC, Smith SR, DeLany JP, Lefevre M, Hwang D, Ryan DH, York DA. The influence of different fats and fatty acids on obesity, insulin resistance and inflammation. J Nutr 2002; 132: 2488–2491.
- 25 Shoelson SE, Herrero L, Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology 2007; 132: 2169–2180.
- 26 Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006; 444: 860–867.
- 27 Rostom A, Muir K, Dubé C, Jolicoeur E, Boucher M, Joyce J, Tugwell P, Wells GW. Gastrointestinal safety of cyclooxygenase-2 inhibitors: a cochrane collaboration systematic review. Clin Gastroenterol Hepatol 2007; 5: 818–828.e5.
- 28 Giovannucci E. Obesity, gender, and colon cancer. Gut 2002; 51: 147.
- 29 Hu F. Obesity Epidemiology, 1st edn. Oxford University Press: Oxford, 2008.
10.1093/acprof:oso/9780195312911.001.0001 Google Scholar
- 30 Gallagher D, Heymsfield SB, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y. Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 2000; 72: 694–701.
- 31 WHO expert consultation. Appropriate body-mass index for Asian populations and its implications for policy and intervention strategies. Lancet 2004; 363: 157–163.
- 32 Deurenberg P, Bhaskaran K, Lian PL. Singaporean Chinese adolescents have more subcutaneous adipose tissue than Dutch Caucasians of the same age and body mass index. Asia Pac J Clin Nutr 2003; 12: 261–265.
- 33 Deurenberg P, Deurenberg-Yap M, Guricci S. Asians are different from Caucasians and from each other in their body mass index/body fat per cent relationship. Obes Rev 2002; 3: 141–146.
- 34 Razak F, Anand SS, Shannon H, Vuksan V, Davis B, Jacobs R, Teo KK, McQueen M, Yusuf S. Defining obesity cut points in a multiethnic population. Circulation 2007; 115: 2111–2118.
- 35 Lee IM. Physical activity and cancer prevention – data from epidemiologic studies. Med Sci Sports Exerc 2003; 35: 1823–1827.
- 36 Wolin KY, Lee IM, Colditz GA, Glynn RJ, Fuchs C, Giovannucci E. Leisure-time physical activity patterns and risk of colon cancer in women. Int J Cancer 2007; Dec 15; 121(12): 2776–2781.
- 37 Larsson SC, Rutegard J, Bergkvist L, Wolk A. Physical activity, obesity, and risk of colon and rectal cancer in a cohort of Swedish men. Eur J Cancer 2006; 42: 2590–2597.
- 38 Colditz GA, Cannuscio CC, Frazier AL. Physical activity and reduced risk of colon cancer: implications for prevention. Cancer Causes Control 1997; 8: 649–667.
- 39 DerSimonian R. Meta-analysis in the design and monitoring of clinical trials. Stat Med 1996; 15: 1237–1248; discussion 49–52.
10.1002/(SICI)1097-0258(19960630)15:12<1237::AID-SIM301>3.0.CO;2-N CASPubMedWeb of Science®Google Scholar
- 40 Pischon T, Lahmann PH, Boeing H, Friedenreich C, Norat T, Tjønneland A, Halkjaer J, Overvad K, Clavel-Chapelon F, Boutron-Ruault MC, Guernec G, Bergmann MM, Linseisen J, Becker N, Trichopoulou A, Trichopoulos D, Sieri S, Palli D, Tumino R, Vineis P, Panico S, Peeters PH, Bueno-de-Mesquita HB, Boshuizen HC, Van Guelpen B, Palmqvist R, Berglund G, Gonzalez CA, Dorronsoro M, Barricarte A, Navarro C, Martinez C, Quirós JR, Roddam A, Allen N, Bingham S, Khaw KT, Ferrari P, Kaaks R, Slimani N, Riboli E. Body size and risk of colon and rectal cancer in the European Prospective Investigation Into Cancer and Nutrition (EPIC). J Natl Cancer Inst 2006; 98: 920–931.
- 41 Thygesen LC, Gronbaek M, Johansen C, Fuchs CS, Willett WC, Giovannucci E. Prospective weight change and colon cancer risk in male US health professionals. Int J Cancer 2008; 123: 1160–1165.
- 42 Wu AH, Paganini-Hill A, Ross RK, Henderson BE. Alcohol, physical activity and other risk factors for colorectal cancer: a prospective study. Br J Cancer 1987; 55: 687–694.
- 43 Lee IM, Paffenbarger RS Jr. Quetelet's index and risk of colon cancer in college alumni. J Natl Cancer Inst 1992; 84: 1326–1331.
- 44 Bostick RM, Potter JD, Kushi LH, Sellers TA, Steinmetz KA, McKenzie DR, Gapstur SM, Folsom AR. Sugar, meat, and fat intake, and non-dietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control 1994; 5: 38–52.
- 45 Chyou PH, Nomura AM, Stemmermann GN. A prospective study of colon and rectal cancer among Hawaii Japanese men. Ann Epidemiol 1996; 6: 276–282.
- 46 Singh PN, Fraser GE. Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 1998; 148: 761–774.
- 47 Thune I, Lund E. Physical activity and risk of colorectal cancer in men and women. Br J Cancer 1996; 73: 1134–1140.
- 48 Ford ES. Body mass index and colon cancer in a national sample of adult US men and women. Am J Epidemiol 1999; 150: 390–398.
- 49 Schoen RE, Tangen CM, Kuller LH, Burke GL, Cushman M, Tracy RP, Dobs A, Savage PJ. Increased blood glucose and insulin, body size, and incident colorectal cancer. J Natl Cancer Inst 1999; 91: 1147–1154.
- 50 Murphy TK, Calle EE, Rodriguez C, Kahn HS, Thun MJ. Body mass index and colon cancer mortality in a large prospective study. Am J Epidemiol 2000; 152: 847–854.
- 51 Van Wayenburg CA, Van Der Schouw YT, Van Noord PA, Peeters PH. Age at menopause, body mass index, and the risk of colorectal cancer mortality in the Dutch Diagnostisch Onderzoek Mammacarcinoom (DOM) cohort. Epidemiology 2000; 11: 304–308.
- 52 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.
- 53 Terry P, Giovannucci E, Bergkvist L, Holmberg L, Wolk A. Body weight and colorectal cancer risk in a cohort of Swedish women: relation varies by age and cancer site. Br J Cancer 2001; 85: 346–349.
- 54 Colangelo LA, Gapstur SM, Gann PH, Dyer AR, Liu K. Colorectal cancer mortality and factors related to the insulin resistance syndrome. Cancer Epidemiol Biomarkers Prev 2002; 11: 385–391.
- 55 Terry PD, Miller AB, Rohan TE. Obesity and colorectal cancer risk in women. Gut 2002; 51: 191–194.
- 56 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: 1625–1638.
- 57 Shimizu N, Nagata C, Shimizu H, Kametani M, Takeyama N, Ohnuma T, Matsushita S. Height, weight, and alcohol consumption in relation to the risk of colorectal cancer in Japan: a prospective study. Br J Cancer 2003; 88: 1038–1043.
- 58 Lin J, Zhang SM, Cook NR, Rexrode KM, Lee IM, Buring JE. Body mass index and risk of colorectal cancer in women (United States). Cancer Causes Control 2004; 15: 581–589.
- 59 MacInnis RJ, English DR, Hopper JL, Haydon AM, Gertig DM, Giles GG. Body size and composition and colon cancer risk in men. Cancer Epidemiol Biomarkers Prev 2004; 13: 553–559.
- 60 Moore LL, Bradlee ML, Singer MR, Splansky GL, Proctor MH, Ellison RC, Kreger BE. BMI and waist circumference as predictors of lifetime colon cancer risk in Framingham Study adults. Int J Obes Relat Metab Disord 2004; 28: 559–567.
- 61 Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS, Willett WC, Colditz GA. Comparison of risk factors for colon and rectal cancer. Int J Cancer 2004; 108: 433–442.
- 62 Batty GD, Shipley MJ, Jarrett RJ, Breeze E, Marmot MG, Smith GD. Obesity and overweight in relation to organ-specific cancer mortality in London (UK): findings from the original Whitehall study. Int J Obes (Lond) 2005; 29: 1267–1274.
- 63 Eichhorlzer MBF, Jordan P, Stahelin HB. Body mass index and the risk of male cancer mortality of various site: 17-year follow-up of the Basel cohort study. Swiss Med Wkly 2005; 135: 27–33.
- 64 Engeland A, Tretli S, Austad G, Bjorge T. Height and body mass index in relation to colorectal and gallbladder cancer in two million Norwegian men and women. Cancer Causes Control 2005; 16: 987–996.
- 65 Kuriyama S, Tsubono Y, Hozawa A, Shimazu T, Suzuki Y, Koizumi Y, Suzuki Y, Ohmori K, Nishino Y, Tsuji I. Obesity and risk of cancer in Japan. Int J Cancer 2005; 113: 148–157.
- 66 Oh SW, Yoon YS, Shin SA. Effects of excess weight on cancer incidences depending on cancer sites and histologic findings among men: Korea National Health Insurance Corporation Study. J Clin Oncol 2005; 23: 4742–4754.
- 67 Otani T, Iwasaki M, Inoue M. Body mass index, body height, and subsequent risk of colorectal cancer in middle-aged and elderly Japanese men and women: Japan public health center-based prospective study. Cancer Causes Control 2005; 16: 839–850.
- 68 Rapp K, Schroeder J, Klenk J, Stoehr S, Ulmer H, Concin H, Diem G, Oberaigner W, Weiland SK. Obesity and incidence of cancer: a large cohort study of over 145 000 adults in Austria. Br J Cancer 2005; 93: 1062–1067.
- 69 Ahmed RL, Schmitz KH, Anderson KE, Rosamond WD, Folsom AR. The metabolic syndrome and risk of incident colorectal cancer. Cancer 2006; 107: 28–36.
- 70 Bowers K, Albanes D, Limburg P, Pietinen P, Taylor PR, Virtamo J, Stolzenberg-Solomon R. A prospective study of anthropometric and clinical measurements associated with insulin resistance syndrome and colorectal cancer in male smokers. Am J Epidemiol 2006; 164: 652–664.
- 71 Lukanova A, Björ O, Kaaks R, Lenner P, Lindahl B, Hallmans G, Stattin P. Body mass index and cancer: results from the Northern Sweden Health and Disease Cohort. Int J Cancer 2006; 118: 458–466.
- 72 Macinnis RJ, English DR, Hopper JL, Gertig DM, Haydon AM, Giles GG. Body size and composition and colon cancer risk in women. Int J Cancer 2006; 118: 1496–1500.
- 73 MacInnis RJ, English DR, Haydon AM, Hopper JL, Gertig DM, Giles GG. Body size and composition and risk of rectal cancer (Australia). Cancer Causes Control 2006; 17: 1291–1297.
- 74 Samanic C, Chow WH, Gridley G, Jarvholm B, Fraumeni JF Jr. Relation of body mass index to cancer risk in 362 552 Swedish men. Cancer Causes Control 2006; 17: 901–909.
- 75 Sherman ME, Lacey JV, Buys SS, Reding DJ, Berg CD, Williams C, Hartge P. Ovarian volume: determinants and associations with cancer among postmenopausal women. Cancer Epidemiol Biomarkers Prev 2006; 15: 1550–1554.
- 76 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.
- 77 Adams KF, Leitzmann MF, Albanes D, Kipnis V, Mouw T, Hollenbeck A, Schatzkin A. Body mass and colorectal cancer risk in the NIH-AARP cohort. Am J Epidemiol 2007; 166: 36–45.
- 78 Kaaks R, Toniolo P, Akhmedkhanov A, Lukanova A, Biessy C, Dechaud H, Rinaldi S, Zeleniuch-Jacquotte A, Shore RE, Riboli E. 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.
- 79 Saydah SH, Loria CM, Eberhardt MS, Brancati FL. Abnormal glucose tolerance and the risk of cancer death in the United States. Am J Epidemiol 2003; 157: 1092–1100.
- 80 Potter JD, McMichael AJ. Large bowel cancer in women in relation to reproductive and hormonal factors: a case-control study. J Natl Cancer Inst 1983; 71: 703–709.
- 81 Graham S, Marshall J, Haughey B, Mittelman A, Swanson M, Zielezny M, Byers T, Wilkinson G, West D. Dietary epidemiology of cancer of the colon in western New York. Am J Epidemiol 1988; 128: 490–503.
- 82 West DW, Slattery ML, Robison LM, Schuman KL, Ford MH, Mahoney AW, Lyon JL, Sorensen AW. Dietary intake and colon cancer: sex- and anatomic site-specific associations. Am J Epidemiol 1989; 130: 883–894.
- 83 Gerhardsson de Verdier M, Hagman U, Steineck G, Rieger A, Norell SE. Diet, body mass and colorectal cancer: a case-referent study in Stockholm. Int J Cancer 1990; 46: 832–838.
- 84 Kune GA, Kune S, Watson LF. Body weight and physical activity as predictors of colorectal cancer risk. Nutr Cancer 1990; 13: 9–17.
- 85 Whittemore AS, Wu-Williams AH, Lee M, Zheng S, Gallagher RP, Jiao DA, Zhou L, Wang XH, Chen K, Jung D, Teh C, Ling C, Xu JY, Paffenbarger RS, Henderson BE. Diet, physical activity, and colorectal cancer among Chinese in North America and China. J Natl Cancer Inst 1990; 82: 915–926.
- 86 Russo A, Franceschi S, La Vecchia C, Dal Maso L, Montella M, Conti E, Giacosa A, Falcini F, Negri E. Body size and colorectal-cancer risk. Int J Cancer 1998; 78: 161–165.
10.1002/(SICI)1097-0215(19981005)78:2<161::AID-IJC7>3.0.CO;2-X CASPubMedWeb of Science®Google Scholar
- 87 Boutron-Ruault MC, Senesse P, Meance S, Belghiti C, Faivre J. Energy intake, body mass index, physical activity, and the colorectal adenoma-carcinoma sequence. Nutr Cancer 2001; 39: 50–57.
- 88 Slattery ML, Ballard-Barbash R, Edwards S, Caan BJ, Potter JD. Body mass index and colon cancer: an evaluation of the modifying effects of estrogen (United States). Cancer Causes Control 2003; 14: 75–84.
- 89 Slattery ML, Caan BJ, Benson J, Murtaugh M. Energy balance and rectal cancer: an evaluation of energy intake, energy expenditure, and body mass index. Nutr Cancer 2003; 46: 166–171.
- 90 Pan SY, Johnson KC, Ugnat AM, Wen SW, Mao Y. Association of obesity and cancer risk in Canada. Am J Epidemiol 2004; 159: 259–268.
- 91 Hou L, Ji BT, Blair A, Dai Q, Gao YT, Potter JD, Chow WH. Body mass index and colon cancer risk in Chinese people: menopause as an effect modifier. Eur J Cancer 2006; 42: 84–90.
- 92 Isomura K, Kono S, Moore MA, Toyomura K, Nagano J, Mizoue T, Mibu R, Tanaka M, Kakeji Y, Maehara Y, Okamura T, Ikejiri K, Futami K, Yasunami Y, Maekawa T, Takenaka K, Ichimiya H, Imaizumi N. Physical activity and colorectal cancer: the Fukuoka Colorectal Cancer Study. Cancer Sci 2006; 97: 1099–1104.
