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Meta-analyses of colorectal cancer risk factors

Cancer Causes & Control volume 24, pages 1207–1222 (2013)Cite this article

Abstract

Purpose

Demographic, behavioral, and environmental factors have been associated with increased risk of colorectal cancer (CRC). We reviewed the published evidence and explored associations between risk factors and CRC incidence.

Methods

We identified 12 established non-screening CRC risk factors and performed a comprehensive review and meta-analyses to quantify each factor’s impact on CRC risk. We used random-effects models of the logarithms of risks across studies: inverse-variance weighted averages for dichotomous factors and generalized least squares for dose–response for multi-level factors.

Results

Significant risk factors include inflammatory bowel disease (RR = 2.93, 95 % CI 1.79–4.81); CRC history in first-degree relative (RR = 1.80, 95 % CI 1.61–2.02); body mass index (BMI) to overall population (RR = 1.10 per 8 kg/m2 increase, 95 % CI 1.08–1.12); physical activity (RR = 0.88, 95 % CI 0.86–0.91 for 2 standard deviations increased physical activity score); cigarette smoking (RR = 1.06, 95 % CI 1.03–1.08 for 5 pack-years); and consumption of red meat (RR = 1.13, 95 % CI 1.09–1.16 for 5 servings/week), fruit (RR = 0.85, 95 % CI 0.75–0.96 for 3 servings/day), and vegetables (RR = 0.86, 95 % CI 0.78–0.94 for 5 servings/day).

Conclusions

We developed a comprehensive risk modeling strategy that incorporates multiple effects to predict an individual’s risk of developing CRC. Inflammatory bowel disease and history of CRC in first-degree relatives are associated with much higher risk of CRC. Increased BMI, red meat intake, cigarette smoking, low physical activity, low vegetable consumption, and low fruit consumption were associated with moderately increased risk of CRC.

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References

  1. Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63:11–30

    Article  PubMed  Google Scholar 

  2. Howlader N, Noone AM, Krapcho M et al (eds) (2012) SEER cancer statistics review, 1975–2009 (Vintage 2009 Populations). National Cancer Institute, Bethesda, MD. http://seer.cancer.gov/csr/1975_2009_pops09/

  3. Newcomb PA, Norfleet RG, Storer BE, Surawicz TS, Marcus PM (1992) Screening sigmoidoscopy and colorectal cancer mortality. J Natl Cancer Inst 84:1572–1575

    Article  PubMed  CAS  Google Scholar 

  4. Sellers TA, Kushi LH, Potter JD et al (1992) Effect of family history, body fat distribution, and reproductive factors on the risk of postmenopausal breast cancer. N Engl J Med 326:1323–1329

    Article  PubMed  CAS  Google Scholar 

  5. Jorgensen OD, Kronborg O, Fenger C (2002) A randomised study of screening for colorectal cancer using faecal occult blood testing: results after 13 years and seven biennial screening rounds. Gut 50:29–32

    Article  PubMed  CAS  Google Scholar 

  6. Kronborg O, Fenger C, Olsen J, Jorgensen OD, Sondergaard O (1996) Randomised study of screening for colorectal cancer with faecal-occult-blood test. Lancet 348:1467–1471

    Article  PubMed  CAS  Google Scholar 

  7. Hardcastle JD, Chamberlain JO, Robinson MHE et al (1996) Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 348:1472–1477

    Article  PubMed  CAS  Google Scholar 

  8. Mandel JS, Bond JH, Church TR et al (1993) Reducing mortality from colorectal cancer by screening for fecal occult blood. N Engl J Med 328:1365–1371

    Article  PubMed  CAS  Google Scholar 

  9. Mandel JS, Church TR, Bond JH et al (2000) The effect of fecal occult-blood screening on the incidence of colorectal cancer. N Engl J Med 343:1603–1607

    Article  PubMed  CAS  Google Scholar 

  10. Winawer SJ, Zauber AG, Ho MN et al (1993) Prevention of colorectal cancer by colonoscopic polypectomy. N Engl J Med 329:1977–1981

    Article  PubMed  CAS  Google Scholar 

  11. Potter JD, Slattery ML, Bostick RM, Gapstur SM (1993) Colon cancer: a review of the epidemiology. Epidemiol Rev 15:499–545

    PubMed  CAS  Google Scholar 

  12. Tomeo CA, Colditz GA, Willett WC et al (1999) Harvard report on cancer prevention. Volume 3: prevention of colon cancer in the United States. Cancer Causes Control 10:167–180

    Article  PubMed  CAS  Google Scholar 

  13. Wilmink ABM (1997) Overview of the epidemiology of colorectal cancer. Dis Colon Rectum 40:483–493

    Article  PubMed  CAS  Google Scholar 

  14. Pinto BM, Eakin E, Maruyama NC (2000) Health behavior changes after a cancer diagnosis: what do we know and where do we go from here? Ann Behav Med 22:38–52

    Article  PubMed  CAS  Google Scholar 

  15. Lieberman DA, Prindiville S, Weiss DG, Willett W, 380 VCSG (2003) Risk factors for advanced colonic neoplasia and hyperplastic polyps in asymptomatic individuals. JAMA 290:2959–2967

    Article  PubMed  Google Scholar 

  16. Boyle P, Leon ME (2002) Epidemiology of colorectal cancer. Br Med Bull 64:1–25

    Article  PubMed  Google Scholar 

  17. NCI (2013) Colorectal cancer screening (PDQ®). National Cancer Institute, Rockville, MD. http://www.cancer.gov/cancertopics/pdq/screening/colorectal/HealthProfessional. Accessed 11 Mar 2013

  18. NCI (2013) Colorectal cancer prevention (PDQ®). National Cancer Institute, Rockville, MD. http://www.cancer.gov/cancertopics/pdq/prevention/colorectal/HealthProfessional/page2#Section_995. Accessed 15 Feb 2013

  19. Kune GA, Kune S, Watson LF (1990) Body weight and physical activity as predictors of colorectal cancer risk. Nutr Cancer 13:9–17

    Article  PubMed  CAS  Google Scholar 

  20. Slattery ML, Sorenson AW, Mahoney AW, French TK, Kritchevsky D, Street JC (1988) Diet and colon cancer—assessment of risk by fiber type and food source. J Natl Cancer Inst 80:1474–1480

    Article  PubMed  CAS  Google Scholar 

  21. Cross AJ, Leitzmann MF, Gail MH, Hollenbeck AR, Schatzkin A, Sinha R (2007) A prospective study of red and processed meat intake in relation to cancer risk. Plos Med 4:1973–1984

    Article  Google Scholar 

  22. Dufour M (1999) What is moderate drinking? Defining “drinks” and drinking levels. Alcohol Res Health 23:5–14

    PubMed  CAS  Google Scholar 

  23. Turner C (1990) How much alcohol is in a ‘standard drink’? An analysis of 125 studies. Br J Addict 85:1171–1175

    Article  PubMed  CAS  Google Scholar 

  24. Miller WR, Heather N, Hall W (1991) Calculating standard drink units: international comparisons. Br J Addict 86:43–47

    Article  PubMed  CAS  Google Scholar 

  25. Kopec JA, Esdaile JM (1990) Bias in case-control studies. A review. J Epidemiol Community Health 44:179–186

    Article  PubMed  CAS  Google Scholar 

  26. Hess DR (2004) Retrospective studies and chart reviews. Respir Care 49:1171–1174

    PubMed  Google Scholar 

  27. Gerhardsson de Verdier M, Hagman U, Steineck G, Rieger A, Norell SE (1990) Diet, body mass and colorectal cancer: a case-referent study in Stockholm. Int J Cancer 46:832–838

    Article  PubMed  CAS  Google Scholar 

  28. Lee IM, Paffenbarger RS (1992) Quetelet index and risk of colon cancer in college alumni. J Natl Cancer Inst 84:1326–1331

    Article  PubMed  CAS  Google Scholar 

  29. Olsen J, Kronborg O, Lynggaard J, Ewertz M (1994) Dietary risk factors for cancer and adenomas of the large intestine. A case-control study within a screening trial in Denmark. Eur J Cancer 30A:53–60

    Article  PubMed  CAS  Google Scholar 

  30. Reeves MJ, Newcomb PA, TrenthamDietz A, Storer BE, Remington PL (1996) Nonsteroidal anti-inflammatory drug use and protection against colorectal cancer in women. Cancer Epidemiol Biomark Prev 5:955–960

    CAS  Google Scholar 

  31. Chyou PH, Nomura AM, Stemmermann GN (1996) A prospective study of colon and rectal cancer among Hawaii Japanese men. Ann Epidemiol 6:276–282

    Article  PubMed  CAS  Google Scholar 

  32. Singh PN, Fraser GE (1998) Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 148:761–774

    Article  PubMed  CAS  Google Scholar 

  33. Ford ES (1999) Body mass index and colon cancer in a national sample of adult US men and women. Am J Epidemiol 150:390–398

    Article  PubMed  CAS  Google Scholar 

  34. Rodriguez LAG, Huerta-Alvarez C (2001) Reduced risk of colorectal cancer among long-term users of aspirin and nonaspirin nonsteroidal antiinflammatory drugs. Epidemiology 12:88–93

    Article  Google Scholar 

  35. Nilsen TI, Vatten LJ (2001) Prospective study of colorectal cancer risk and physical activity, diabetes, blood glucose and BMI: exploring the hyperinsulinaemia hypothesis. Br J Cancer 84:417–422

    Article  PubMed  CAS  Google Scholar 

  36. Lin J, Zhang SM, Cook NR, Rexrode KM, Lee IM, Buring JE (2004) Body mass index and risk of colorectal cancer in women (United States). Cancer Causes Control 15:581–589

    Article  PubMed  Google Scholar 

  37. Engeland A, Tretli S, Austad G, Bjorge T (2005) Height and body mass index in relation to colorectal and gallbladder cancer in two million Norwegian men and women. Cancer Causes Control 16:987–996

    Article  PubMed  Google Scholar 

  38. Yeh CC, You SL, Chen CJ, Sung FC (2006) Peanut consumption and reduced risk of colorectal cancer in women: a prospective study in Taiwan. World J Gastroenterol 12:222–227

    PubMed  Google Scholar 

  39. Hou LF, Ji BT, Blair A et al (2006) Body mass index and colon cancer risk in Chinese people: menopause as an effect modifier. Eur J Cancer 42:84–90

    Article  PubMed  Google Scholar 

  40. Vinogradova Y, Hippisley-Cox J, Coupland C, Logan RF (2007) Risk of colorectal cancer in patients prescribed statins, nonsteroidal anti-inflammatory drugs, and cyclooxygenase-2 inhibitors: nested case-control study. Gastroenterology 133:393–402

    Article  PubMed  Google Scholar 

  41. Reeves GK, Pirie K, Beral V, Green J, Spencer E, Bull D (2007) Cancer incidence and mortality in relation to body mass index in the Million Women Study: cohort study. Br Med J 335:1134–1139

    Article  Google Scholar 

  42. Hoffmeister M, Raum E, Winter J, Chang-Claude J, Brenner H (2007) Hormone replacement therapy, body mass, and the risk of colorectal cancer among postmenopausal women from Germany. Br J Cancer 97:1486–1492

    Article  PubMed  CAS  Google Scholar 

  43. Adams KF, Leltzmann MF, Albanes D et al (2007) Body mass and colorectal cancer risk in the NIH-AARP cohort. Am J Epidemiol 166:36–45

    Article  PubMed  Google Scholar 

  44. Wang Y, Jacobs EJ, Patel AV et al (2008) A prospective study of waist circumference and body mass index in relation to colorectal cancer incidence. Cancer Causes Control 19:783–792

    Article  PubMed  Google Scholar 

  45. Shadman M, Newcomb PA, Hampton JM, Wernli K, Trentham-Dietz A (2009) Non-steroidal anti-inflammatory drugs and statins in relation to colorectal cancer risk. World J Gastroenterol 15:2336–2339

    Article  PubMed  CAS  Google Scholar 

  46. Lee SA, Shu XO, Yang G, Li HL, Gao YT, Zheng W (2009) Animal origin foods and colorectal cancer risk: a report from the Shanghai Women’s Health Study. Nutr Cancer 61:194–205

    Article  PubMed  Google Scholar 

  47. Hoffmeister M, Raum E, Krtschil A, Chang-Claude J, Brenner H (2009) No evidence for variation in colorectal cancer risk associated with different types of postmenopausal hormone therapy. Clin Pharmacol Ther 86:416–424

    Article  PubMed  CAS  Google Scholar 

  48. Campbell PT, Jacobs ET, Ulrich CM et al (2010) Case-control study of overweight, obesity, and colorectal cancer risk, overall and by tumor microsatellite instability status. J Natl Cancer Inst 102:391–400

    Article  PubMed  Google Scholar 

  49. Severson RK, Nomura AMY, Grove JS, Stemmermann GN (1989) A prospective analysis of physical activity and cancer. Am J Epidemiol 130:522–529

    PubMed  CAS  Google Scholar 

  50. Slattery ML, Abd-Elghany N, Kerber R, Schumacher MC (1990) Physical activity and colon cancer: a comparison of various indicators of physical activity to evaluate the association. Epidemiology 1:481–485

    Article  PubMed  CAS  Google Scholar 

  51. Ballard-Barbash R, Schatzkin A, Albanes D et al (1990) Physical activity and risk of large bowel cancer in the Framingham Study. Cancer Res 50:3610–3613

    PubMed  CAS  Google Scholar 

  52. Lee IM, Paffenbarger RS, Hsieh CC (1991) Physical activity and risk of developing colorectal cancer among college alumni. J Natl Cancer Inst 83:1324–1329

    Article  PubMed  CAS  Google Scholar 

  53. Bostick RM, Potter JD, Kushi LH et al (1994) Sugar, meat, and fat intake, and nondietary risk factors for colon cancer incidence in Iowa women (United States). Cancer Causes Control 5:38–52

    Article  PubMed  CAS  Google Scholar 

  54. White E, Jacobs EJ, Daling JR (1996) Physical activity in relation to colon cancer in middle-aged men and women. Am J Epidemiol 144:42–50

    Article  PubMed  CAS  Google Scholar 

  55. Lee IM, Manson JE, Ajani U, Paffenbarger RS, Hennekens CH, Buring JE (1997) Physical activity and risk of colon cancer: the Physicians’ Health Study (United States). Cancer Causes Control 8:568–574

    Article  PubMed  CAS  Google Scholar 

  56. Slattery ML, Edwards SL, Boucher KM, Anderson K, Caan BJ (1999) Lifestyle and colon cancer: an assessment of factors associated with risk. Am J Epidemiol 150:869–877

    Article  PubMed  CAS  Google Scholar 

  57. Boutron-Ruault MC, Senesse P, Meance S, Belghiti C, Faivre J (2001) Energy intake, body mass index, physical activity, and the colorectal adenoma-carcinoma sequence. Nutr Cancer 39:50–57

    Article  PubMed  CAS  Google Scholar 

  58. Wei EK, Giovannucci E, Wu K et al (2004) Comparison of risk factors for colon and rectal cancer. Int J Cancer 108:433–442

    Article  PubMed  CAS  Google Scholar 

  59. Hou L, Ji BT, Blair A, Dai Q, Gao YT, Chow WH (2004) Commuting physical activity and risk of colon cancer in Shanghai, China. Am J Epidemiol 160:860–867

    Article  PubMed  Google Scholar 

  60. Chao A, Connell CJ, Jacobs EJ et al (2004) Amount, type, and timing of recreational physical activity in relation to colon and rectal cancer in older adults: the Cancer Prevention Study II Nutrition Cohort. Cancer Epidemiol Biomarkers Prev 13:2187–2195

    PubMed  Google Scholar 

  61. Takahashi H, Kuriyama S, Tsubono Y et al (2007) Time spent walking and risk of colorectal cancer in Japan: the Miyaqi Cohort Study. Eur J Cancer Prev 16:403–408

    Article  PubMed  Google Scholar 

  62. Lee KJ, Inoue M, Otani T et al (2007) Physical activity and risk of colorectal cancer in Japanese men and women: the Japan Public Health Center-based prospective study. Cancer Causes Control 18:199–209

    Article  PubMed  Google Scholar 

  63. Hoffmeister M, Brenner H, Chang-Claude J (2007) Individual and joint use of statins and low-dose aspirin and risk of colorectal cancer: a population-based case-control study. Int J Cancer 121:1325–1330

    Article  PubMed  CAS  Google Scholar 

  64. Giovannucci E, Rimm EB, Stampfer MJ et al (1994) A prospective study of cigarette smoking and risk of colorectal adenoma and colorectal cancer in US men. J Natl Cancer Inst 86:183–191

    Article  PubMed  CAS  Google Scholar 

  65. Baron JA, Gerhardsson de Verdier M, Ekbom A (1994) Coffee, tea, tobacco, and cancer of the large bowel. Cancer Epidemiol Biomarkers Prev 3:565–570

    PubMed  CAS  Google Scholar 

  66. Sturmer T, Glynn RJ, Lee IM, Christen WG, Hennekens CH (2000) Lifetime cigarette smoking and colorectal cancer incidence in the Physicians’ Health Study I. J Natl Cancer Inst 92:1178–1181

    Article  PubMed  CAS  Google Scholar 

  67. Chiu BCH, Lynch CF, Cerhan JR, Cantor KP (2001) Cigarette smoking and risk of bladder, pancreas, kidney, and colorectal cancers in Iowa. Ann Epidemiol 11:28–37

    Article  PubMed  CAS  Google Scholar 

  68. Otani T, Iwasaki M, Yamamoto S et al (2003) Alcohol consumption, smoking, and subsequent risk of colorectal cancer in middle-aged and elderly Japanese men and women: Japan Public Health Center-based prospective study. Cancer Epidemiol Biomarkers Prev 12:1492–1500

    PubMed  CAS  Google Scholar 

  69. Slattery ML, Samowtiz W, Ma K et al (2004) CYP1A1, cigarette smoking, and colon and rectal cancer. Am J Epidemiol 160:842–852

    Article  PubMed  Google Scholar 

  70. Lilla C, Verla-Tebit E, Risch A et al (2006) Effect of NAT1 and NAT2 genetic polymorphisms on colorectal cancer risk associated with exposure to tobacco smoke and meat consumption. Cancer Epidemiol Biomarkers Prev 15:99–107

    Article  PubMed  CAS  Google Scholar 

  71. Weijenberg MP, Aardening PW, de Kok TM, de Goeij AF, van den Brandt PA (2008) Cigarette smoking and KRAS oncogene mutations in sporadic colorectal cancer: results from the Netherlands Cohort Study. Mutat Res 652:54–64

    Article  PubMed  CAS  Google Scholar 

  72. Poynter JN, Haile RW, Siegmund KD et al (2009) Associations between smoking, alcohol consumption, and colorectal cancer, overall and by tumor microsatellite instability status. Cancer Epidemiol Biomarkers Prev 18:2745–2750

    Article  PubMed  CAS  Google Scholar 

  73. Nothlings U, Yamamoto JF, Wilkens LR et al (2009) Meat and heterocyclic amine intake, smoking, NAT1 and NAT2 polymorphisms, and colorectal cancer risk in the Multiethnic Cohort Study. Cancer Epidemiol Biomarkers Prev 18:2098–2106

    Article  PubMed  Google Scholar 

  74. Gram IT, Braaten T, Lund E, Le Marchand L, Weiderpass E (2009) Cigarette smoking and risk of colorectal cancer among Norwegian women. Cancer Causes Control 20:895–903

    Article  PubMed  Google Scholar 

  75. Klatsky AL, Armstrong MA, Friedman GD, Hiatt RA (1988) The relations of alcoholic beverage use to colon and rectal cancer. Am J Epidemiol 128:1007–1015

    PubMed  CAS  Google Scholar 

  76. Slattery M, West D, Robison L et al (1990) Tobacco, alcohol, coffee, and caffeine as risk factors for colon cancer in a low-risk population. Epidemiology 1:141–145

    Article  PubMed  CAS  Google Scholar 

  77. Newcomb PA, Storer BE, Marcus PM (1993) Cancer of the large bowel in women in relation to alcohol consumption: a case-control study in Wisconsin (United States). Cancer Causes Control 4:405–411

    Article  PubMed  CAS  Google Scholar 

  78. Gerhardsson de Verdier M, Romelsjö A, Lundberg M (1993) Alcohol and cancer of the colon and rectum. Eur J Cancer Prev 2:401–408

    Article  PubMed  CAS  Google Scholar 

  79. Goldbohm RA, van den Brandt PA, Van’t Veer P, Dorant E, Sturmans F, Hermus RJ (1994) Prospective study on alcohol consumption and the risk of cancer of the colon and rectum in the Netherlands. Cancer Causes Control 5:95–104

    Article  PubMed  CAS  Google Scholar 

  80. Gapstur SM, Potter JD, Folsom AR (1994) Alcohol consumption and colon and rectal cancer in postmenopausal women. Int J Epidemiol 23:50–57

    Article  PubMed  CAS  Google Scholar 

  81. Rosenberg L, Louik C, Shapiro S (1998) Nonsteroidal antiinflammatory drug use and reduced risk of large bowel carcinoma. Cancer 82:2326–2333

    Article  PubMed  CAS  Google Scholar 

  82. Chen J, Ma J, Stampfer MJ, Hines LM, Selhub J, Hunter DJ (2001) Alcohol dehydrogenase 3 genotype is not predictive for risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 10:1303–1304

    PubMed  CAS  Google Scholar 

  83. Flood A, Caprario L, Chaterjee N, Lacey JV, Schairer C, Schatzkin A (2002) Folate, methionine, alcohol, and colorectal cancer in a prospective study of women in the United States. Cancer Causes Control 13:551–561

    Article  PubMed  Google Scholar 

  84. Pedersen A, Johansen C, Grønbaek M (2003) Relations between amount and type of alcohol and colon and rectal cancer in a Danish population based cohort study. Gut 52:861–867

    Article  PubMed  CAS  Google Scholar 

  85. Sanjoaquin MA, Appleby PN, Thorogood M, Mann JI, Key TJ (2004) Nutrition, lifestyle and colorectal cancer incidence: a prospective investigation of 10 998 vegetarians and non-vegetarians in the United Kingdom. Br J Cancer 90:118–121

    Article  PubMed  CAS  Google Scholar 

  86. Wakai K, Kojima M, Tamakoshi K et al (2005) Alcohol consumption and colorectal cancer risk: findings from the JACC study. J Epidemiol 15:S173–S179

    Article  PubMed  Google Scholar 

  87. Tsong WH, Koh WP, Yuan JM, Wang R, Sun CL, Yu MC (2007) Cigarettes and alcohol in relation to colorectal cancer: the Singapore Chinese Health Study. Br J Cancer 96:821–827

    Article  PubMed  CAS  Google Scholar 

  88. Ferrari P, Jenab M, Norat T et al (2007) Lifetime and baseline alcohol intake and risk of colon and rectal cancers in the European Prospective Investigation into Cancer and Nutrition (EPIC). Int J Cancer 121:2065–2072

    Article  PubMed  CAS  Google Scholar 

  89. Akhter M, Kuriyama S, Nakaya N et al (2007) Alcohol consumption is associated with an increased risk of distal colon and rectal cancer in Japanese men: the Miyagi Cohort Study. Eur J Cancer 43:383–390

    Article  PubMed  CAS  Google Scholar 

  90. Toriola AT, Kurl S, Laukanen JA, Mazengo C, Kauhanen J (2008) Alcohol consumption and risk of colorectal cancer: the Findrink study. Eur J Epidemiol 23:395–401

    Article  PubMed  CAS  Google Scholar 

  91. Kune GA, Kune S, Watson LF (1989) The role of heredity in the etiology of large bowel cancer: data from the Melbourne Colorectal Cancer Study. World J Surg 13:124–131

    Article  PubMed  CAS  Google Scholar 

  92. Centonze S, Boeing H, Leoci C, Bonfiglio C, Guerra V, Misciagna G (1993) Familial risk of colo-rectal cancer in a low incidence area in southern Italy. Eur J Epidemiol 9:26–32

    Article  PubMed  CAS  Google Scholar 

  93. Fuchs CS, Giovannucci EL, Colditz GA, Hunter DJ, Speizer FE, Willett WC (1994) A prospective study of family history and the risk of colorectal cancer. N Engl J Med 331:1669–1674

    Article  PubMed  CAS  Google Scholar 

  94. Boutron MC, Faivre J, Quipourt V, Senesse P, Michiels C (1995) Family history of colorectal tumours and implications for the adenoma-carcinoma sequence: a case control study. Gut 37:830–834

    Article  PubMed  CAS  Google Scholar 

  95. Le Marchand L, Zhao LP, Quiaoit F, Wilkens LR, Laurence N, Kolonel LN (1996) Family history and risk of colorectal cancer in the multiethnic population of Hawaii. Am J Epidemiol 144:1122–1128

    Article  PubMed  Google Scholar 

  96. Newcomb P, Taylor J, Trentham-Dietz A (1999) Interactions of familial and hormonal risk factors for large bowel cancer in women. Int J Epidemiol 28:603–608

    Article  PubMed  CAS  Google Scholar 

  97. Carstensen B, Soll-Johanning H, Villadsen E, Søndergaard JO, Lynge E (1996) Familial aggregation of colorectal cancer in the general population. Int J Cancer 68:428–435

    Article  PubMed  CAS  Google Scholar 

  98. Slattery M, Levin T, Ma K, Goldgar D, Holubkov R, Edwards S (2003) Family history and colorectal cancer: predictors of risk. Cancer Causes Control 14:879–887

    Article  PubMed  CAS  Google Scholar 

  99. Hemminki K, Chen B (2005) Familial risks for colorectal cancer show evidence on recessive inheritance. Int J Cancer 115:835–838

    Article  PubMed  CAS  Google Scholar 

  100. Boardman LA, Morlan BW, Rabe KG et al (2007) Colorectal cancer risks in relatives of young-onset cases: is risk the same across all first-degree relatives? Clin Gastroenterol Hepatol 5:1195–1198

    Article  PubMed  Google Scholar 

  101. Rennert G, Rennert HS, Pinchev M, Lavie O, Gruber SB (2009) Use of hormone replacement therapy and the risk of colorectal cancer. J Clin Oncol 27:4542–4547

    Article  PubMed  CAS  Google Scholar 

  102. Greenstein AJ, Sachar DB, Smith H, Janowitz HD, Aufses AHJ (1981) A comparison of cancer risk in Crohn’s disease and ulcerative colitis. Cancer 48:2742–2745

    Article  PubMed  CAS  Google Scholar 

  103. Mellemkjaer L, Olsen JH, Frisch M, Johansen C, Gridley G, McLaughlin JK (1995) Cancer in patients with ulcerative colitis. Int J Cancer 60:330–333

    Article  PubMed  CAS  Google Scholar 

  104. Gyde SN, Prior P, Allan RN et al (1988) Colorectal cancer in ulcerative colitis: a cohort study of primary referrals from three centres. Gut 29:206–217

    Article  PubMed  CAS  Google Scholar 

  105. Langholz E, Munkholm P, Davidsen M, Binder V (1992) Colorectal cancer risk and mortality in patients with ulcerative colitis. Gastroenterology 103:1444–1451

    PubMed  CAS  Google Scholar 

  106. Gillen D, Andrews HA, Prior P, Allan RN (1994) Crohn’s disease and colorectal cancer. Gut 35:651–655

    Article  PubMed  CAS  Google Scholar 

  107. Stewénius J, Adnerhill I, Anderson H et al (1995) Incidence of colorectal cancer and all cause mortality in non-selected patients with ulcerative colitis and indeterminate colitis in Malmo, Sweden. Int J Colorectal Dis 10:117–122

    Article  PubMed  Google Scholar 

  108. Persson PG, Karlén P, Bernell O et al (1994) Crohn’s disease and cancer: a population-based cohort study. Gastroenterology 107:1675–1679

    PubMed  CAS  Google Scholar 

  109. Karlén P, Löfberg R, Broström O, Leijonmarck CE, Hellers G, Persson PG (1999) Increased risk of cancer in ulcerative colitis: a population-based cohort study. Am J Gastroenterol 94:1047–1052

    PubMed  Google Scholar 

  110. Askling J, Dickman PW, Karlén P et al (2001) Family history as a risk factor for colorectal cancer in inflammatory bowel disease. Gastroenterology 120:1356–1362

    Article  PubMed  CAS  Google Scholar 

  111. Kvist N, Jacobsen O, Kvist HK et al (1989) Malignancy in ulcerative colitis. Scand J Gastroenterol 24:497–506

    Article  PubMed  CAS  Google Scholar 

  112. Ekbom A, Helmick C, Zack M, Adami HO (1990) Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 323:1228–1233

    Article  PubMed  CAS  Google Scholar 

  113. Ekbom A, Helmick C, Zack M, Adami HO (1990) Increased risk of large bowel cancer in Crohn’s disease with colonic involvement. Lancet 336:357–359

    Article  PubMed  CAS  Google Scholar 

  114. Söderlund S, Granath F, Broström O et al (2010) Inflammatory bowel disease confers a lower risk of colorectal cancer to females than to males. Gastroenterology 138:1697–1703

    Article  PubMed  Google Scholar 

  115. Troisi R, Schairer C, Chow WH, Schatzkin A, Brinton LA, Fraumeni JF (1997) A prospective study of menopausal hormones and risk of colorectal cancer (United States). Cancer Causes Control 8:130–138

    Article  PubMed  CAS  Google Scholar 

  116. Grodstein F, Martinez ME, Platz EA et al (1998) Postmenopausal hormone use and risk for colorectal cancer and adenoma. Ann Intern Med 128:705–712

    Article  PubMed  CAS  Google Scholar 

  117. Paganini-Hill A (1999) Estrogen replacement therapy and colorectal cancer risk in elderly women. Dis Colon Rectum 42:1300–1305

    Article  PubMed  CAS  Google Scholar 

  118. Jacobs EJ, White E, Weiss NS, Heckbert SR, LaCroix A, Barlow WE (1999) Hormone replacement therapy and colon cancer among members of a health maintenance organization. Epidemiology 10:445–451

    Article  PubMed  CAS  Google Scholar 

  119. Prihartono N, Palmer JR, Louik C, Shapiro S, Rosenberg L (2000) A case-control study of use of postmenopausal female hormone supplements in relation to the risk of large bowel cancer. Cancer Epidemiol Biomarkers Prev 9:443–447

    PubMed  CAS  Google Scholar 

  120. DeLellis Henderson K, Duan L, Sullivan-Halley J et al (2010) Menopausal hormone therapy use and risk of invasive colon cancer: the California Teachers Study. Am J Epidemiol 171:415–425

    Article  PubMed  Google Scholar 

  121. Friedman GD, Coates AO, Potter JD, Slattery ML (1998) Drugs and colon cancer. Pharmacoepidemiol Drug Saf 7:99–106

    Article  PubMed  CAS  Google Scholar 

  122. McGreavey LE, Turner F, Smith G et al (2005) No evidence that polymorphisms in CYP2C8, CYP2C9, UGT1A6, PPAR delta and PPAR gamma act as modifiers of the protective effect of regular NSAID use on the risk of colorectal carcinoma. Pharmacogenet Genomics 15:713–721

    Article  PubMed  CAS  Google Scholar 

  123. Chan AT, Giovannucci EL, Meyerhardt JA, Schernhammer ES, Curhan GC, Fuchs CS (2005) Long-term use of aspirin and nonsteroidal anti-inflammatory drugs and risk of colorectal cancer. JAMA 294:914–923

    Article  PubMed  CAS  Google Scholar 

  124. Jacobs EJ, Thun MJ, Bain EB, Rodriguez C, Henley SJ, Calle EE (2007) A large cohort study of long-term daily use of adult-strength aspirin and cancer incidence. J Natl Cancer Inst 99:608–615

    Article  PubMed  CAS  Google Scholar 

  125. Chan AT, Giovannucci EL, Meyerhardt JA, Schernhammer ES, Wu K, Fuchs CS (2008) Aspirin dose and duration of use and risk of colorectal cancer in men. Gastroenterology 134:21–28

    Article  PubMed  CAS  Google Scholar 

  126. Lin J, Zhang SM, Cook NR, Lee IM, Buring JE (2004) Dietary fat and fatty acids and risk of colorectal cancer in women. Am J Epidemiol 160:1011–1022

    Article  PubMed  Google Scholar 

  127. English DR, MacInnis RJ, Hodge AM, Hopper JL, Haydon AM, Giles GG (2004) Red meat, chicken, and fish consumption and risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 13:1509–1514

    PubMed  Google Scholar 

  128. Chao A, Thun MJ, Connell CJ et al (2005) Meat consumption and risk of colorectal cancer. JAMA 293:172–182

    Article  PubMed  CAS  Google Scholar 

  129. Kampman E, Verhoeven D, Sloots L, Van’t Veer P (1995) Vegetable and animal products as determinants of colon cancer risk in Dutch men and women. Cancer Causes Control 6:225–234

    Article  PubMed  CAS  Google Scholar 

  130. Shannon J, White E, Shattuck AL, Potter JD (1996) Relationship of food groups and water intake to colon cancer risk. Cancer Epidemiol Biomark Prev 5:495–502

    CAS  Google Scholar 

  131. Le Marchand L, Hankin JH, Wilkens LR et al (2001) Combined effects of well-done red meat, smoking, and rapid N-acetyltransferase 2 and CYP1A2 phenotypes in increasing colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 10:1259–1266

    PubMed  Google Scholar 

  132. Seow A, Quah SR, Nyam D, Straughan PT, Chua T, Aw TC (2002) Food groups and the risk of colorectal carcinoma in an Asian population. Cancer 95:2390–2396

    Article  PubMed  Google Scholar 

  133. Butler LM, Sinha R, Millikan RC et al (2003) Heterocyclic amines, meat intake, and association with colon cancer in a population-based study. Am J Epidemiol 157:434–445

    Article  PubMed  CAS  Google Scholar 

  134. Turner F, Smith G, Sachse C et al (2004) Vegetable, fruit and meat consumption and potential risk modifying genes in relation to colorectal cancer. Int J Cancer 112:259–264

    Article  PubMed  CAS  Google Scholar 

  135. Cotterchio M, Boucher BA, Manno M, Gallinger S, Okey AB, Harper PA (2008) Red meat intake, doneness, polymorphisms in genes that encode carcinogen-metabolizing enzymes, and colorectal cancer risk. Cancer Epidemiol Biomarkers Prev 17:3098–3107

    Article  PubMed  CAS  Google Scholar 

  136. Voorrips LE, Goldbohm RA, van Poppel G, Sturmans F, Hermus RJ, van den Brandt PA (2000) Vegetable and fruit consumption and risks of colon and rectal cancer in a prospective cohort study: the Netherlands Cohort Study on diet and cancer. Am J Epidemiol 152:1081–1092

    Article  PubMed  CAS  Google Scholar 

  137. McCullough ML, Robertson AS, Chao A et al (2003) A prospective study of whole grains, fruits, vegetables and colon cancer risk. Cancer Causes Control 14:959–970

    Article  PubMed  Google Scholar 

  138. van Duijnhoven FJ, Bueno-De-Mesquita HB, Ferrari P et al (2009) Fruit, vegetables, and colorectal cancer risk: the European Prospective Investigation into Cancer and Nutrition. Am J Clin Nutr 89:1441–1452

    Article  PubMed  Google Scholar 

  139. Michels KB, Giovannucci E, Joshipura KJ et al (2000) Prospective study of fruit and vegetable consumption and incidence of colon and rectal cancers. J Natl Cancer Inst 92:1740–1752

    Article  PubMed  CAS  Google Scholar 

  140. Schwarzer G (2010) Meta: meta-analysis with R. http://cran.r-project.org/web/packages/meta/index.html. Accessed 28 Oct 2010

  141. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558

    Article  PubMed  Google Scholar 

  142. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188

    Article  PubMed  CAS  Google Scholar 

  143. Sterne JA, Gavaghan D, Egger M (2000) Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. J Clin Epidemiol 53:1119–1129

    Article  PubMed  CAS  Google Scholar 

  144. Harrell FE, Lee KL, Pollock BG (1988) Regression-models in clinical-studies—determining relationships between predictors and response. J Natl Cancer Inst 80:1198–1202

    Article  PubMed  Google Scholar 

  145. Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309

    PubMed  CAS  Google Scholar 

  146. Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose-response data. Stata J 6:40–57

    Google Scholar 

  147. Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of US adults. N Engl J Med 348:1625–1638

    Article  PubMed  Google Scholar 

  148. Martinez ME, Giovannucci E, Spiegelman D, Hunter DJ, Willett WC, Colditz GA (1997) Leisure-time physical activity, body size, and colon cancer in women. J Natl Cancer Inst 89:948–955

    Article  PubMed  CAS  Google Scholar 

  149. Giovannucci E (2002) Obesity, gender, and colon cancer. Gut 51:147

    Article  PubMed  CAS  Google Scholar 

  150. Ning Y, Wang L, Giovannucci EL (2010) A quantitative analysis of body mass index and colorectal cancer: findings from 56 observational studies. Obes Rev 11:19–30

    Article  PubMed  CAS  Google Scholar 

  151. Heymsfield SB, Gallagher D, Heo M, Jebb SA, Murgatroyd PR, Sakamoto Y (2000) Healthy percentage body fat ranges: an approach for developing guidelines based on body mass index. Am J Clin Nutr 72:694–701

    PubMed  Google Scholar 

  152. Tsoi KK, Pau YY, Wu WK, Chan FKL, Griffiths SM, Sung JJ (2009) Cigarette smoking and the risk of colorectal cancer: a meta-analysis of prospective cohort studies. Clin Gastroenterol Hepatol 7:682–688

    Article  PubMed  Google Scholar 

  153. Huxley RR, Ansary-Moghaddam A, Clifton P, Czernichow S, Parr CL, Woodward M (2009) The impact of dietary and lifestyle risk factors on risk of colorectal cancer: a quantitative overview of the epidemiological evidence. Int J Cancer 125:171–180

    Article  PubMed  CAS  Google Scholar 

  154. Liang PS, Chen TY, Giovannucci E (2009) Cigarette smoking and colorectal cancer incidence and mortality: systematic review and meta-analysis. Int J Cancer 124:2406–2415

    Article  PubMed  CAS  Google Scholar 

  155. Butterworth AS, Higgins JPT, Pharoah P (2006) Relative and absolute risk of colorectal cancer for individuals with a family history: a meta-analysis. Eur J Cancer 42:216–227

    Article  PubMed  Google Scholar 

  156. Eaden JA, Abrams KR, Mayberry JF (2001) The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48:526–535

    Article  PubMed  CAS  Google Scholar 

  157. Cho EY, Smith-Warner SA, Ritz J et al (2004) Alcohol intake and colorectal cancer: a pooled analysis of 8 cohort studies. Ann Intern Med 140:603–613

    Article  PubMed  Google Scholar 

  158. Fedirko V, Tramacere I, Bagnardi V et al (2011) Alcohol drinking and colorectal cancer risk: an overall and dose-response meta-analysis of published studies. Ann Oncol 22:1958–1972

    Article  PubMed  CAS  Google Scholar 

  159. Moskal A, Norat T, Ferrari P, Riboli E (2007) Alcohol intake and colorectal cancer risk: a dose-response meta-analysis of published cohort studies. Int J Cancer 120:664–671

    Article  PubMed  CAS  Google Scholar 

  160. Longnecker MP, Orza MJ, Adams ME, Vioque J, Chalmers TC (1990) A meta-analysis of alcoholic beverage consumption in relation to risk of colorectal cancer. Cancer Causes Control 1:59–68

    Article  PubMed  CAS  Google Scholar 

  161. Norat T, Chan D, Lau R, Aune D, Vieira R (2010) WCRF/AICR systematic literature review continuous Update Project Report. The associations between food nutrition and physical activity and the risk of colorectal cancer. WCRF/AICR. Imperial College, London

    Google Scholar 

  162. Grodstein F, Newcomb PA, Stampfer MJ (1999) Postmenopausal hormone therapy and the risk of colorectal cancer: a review and meta-analysis. Am J Med 106:574–582

    Article  PubMed  CAS  Google Scholar 

  163. Cole BF, Logan RF, Halabi S et al (2009) Aspirin for the chemoprevention of colorectal adenomas: meta-analysis of the randomized trials. J Natl Cancer Inst 101:256–266

    Article  PubMed  CAS  Google Scholar 

  164. Cuzick J, Otto F, Baron JA et al (2009) Aspirin and non-steroidal anti-inflammatory drugs for cancer prevention: an international consensus statement. Lancet Oncol 10:501–507

    Article  PubMed  CAS  Google Scholar 

  165. StataCorp (2009) Stata base reference manual: A-H. College Station. StataCorp LP, TX

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Acknowledgments

This project was supported in part by the National Colorectal Cancer Research Alliance; its contents are solely the responsibility of the authors and do not represent the official view of the National Colorectal Cancer Research Alliance.

Conflict of interest

Donald A. Berry is co-owner of Berry Consultants, LLC, a company that designs adaptive clinical trials for pharmaceutical and medical device companies and NIH cooperative groups.

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Authors and Affiliations

  1. School of Nursing and Community and Family Medicine, Duke University, 307 Trent Drive, Durham, NC, 27710, USA

    Constance M. Johnson

  2. Division of Quantitative Sciences, Department of Biostatistics, Unit 1409, The University of Texas MD Anderson Cancer Center, P. O. Box 301402, Houston, TX, 77230-1402, USA

    Caimiao Wei, Joe E. Ensor & Donald A. Berry

  3. Research, Outcomes, Surveillance, Evaluations, National Center for Telehealth and Technology, Joint Base Lewis-McChord, Tacoma, WA, 98431, USA

    Derek J. Smolenski

  4. Department of Community and Family Medicine, Geisel School of Medicine, Dartmouth College, Lebanon, NH, 03766, USA

    Christopher I. Amos

  5. Professor Emeritus, Division of Cancer Prevention and Population Sciences, The University of Texas MD Anderson Cancer Center, P.O. Box 301439, Houston, TX, 77230, USA

    Bernard Levin

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  1. Constance M. Johnson
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  2. Caimiao Wei
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  7. Donald A. Berry
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Correspondence to Donald A. Berry.

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Johnson, C.M., Wei, C., Ensor, J.E. et al. Meta-analyses of colorectal cancer risk factors. Cancer Causes Control 24, 1207–1222 (2013). https://doi.org/10.1007/s10552-013-0201-5

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