Advertisement

Cancer Causes & Control

, Volume 24, Issue 6, pp 1207–1222 | Cite as

Meta-analyses of colorectal cancer risk factors

  • Constance M. Johnson
  • Caimiao Wei
  • Joe E. Ensor
  • Derek J. Smolenski
  • Christopher I. Amos
  • Bernard Levin
  • Donald A. Berry
Original paper
First Online:
Received:
Accepted:

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.

Keywords

Colorectal cancer Colon neoplasms Colonic neoplasms Colorectal neoplasms Colorectal risk factors Colorectal cancer prevention Meta-analysis 
This is a preview of subscription content, log in to check access.

Notes

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.

References

  1. 1.
    Siegel R, Naishadham D, Jemal A (2013) Cancer statistics, 2013. CA Cancer J Clin 63:11–30PubMedCrossRefGoogle Scholar
  2. 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. 3.
    Newcomb PA, Norfleet RG, Storer BE, Surawicz TS, Marcus PM (1992) Screening sigmoidoscopy and colorectal cancer mortality. J Natl Cancer Inst 84:1572–1575PubMedCrossRefGoogle Scholar
  4. 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 326:1323–1329PubMedCrossRefGoogle Scholar
  5. 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 50:29–32PubMedCrossRefGoogle Scholar
  6. 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 348:1467–1471PubMedCrossRefGoogle Scholar
  7. 7.
    Hardcastle JD, Chamberlain JO, Robinson MHE et al (1996) Randomised controlled trial of faecal-occult-blood screening for colorectal cancer. Lancet 348:1472–1477PubMedCrossRefGoogle Scholar
  8. 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 328:1365–1371PubMedCrossRefGoogle Scholar
  9. 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 343:1603–1607PubMedCrossRefGoogle Scholar
  10. 10.
    Winawer SJ, Zauber AG, Ho MN et al (1993) Prevention of colorectal cancer by colonoscopic polypectomy. N Engl J Med 329:1977–1981PubMedCrossRefGoogle Scholar
  11. 11.
    Potter JD, Slattery ML, Bostick RM, Gapstur SM (1993) Colon cancer: a review of the epidemiology. Epidemiol Rev 15:499–545PubMedGoogle Scholar
  12. 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 10:167–180PubMedCrossRefGoogle Scholar
  13. 13.
    Wilmink ABM (1997) Overview of the epidemiology of colorectal cancer. Dis Colon Rectum 40:483–493PubMedCrossRefGoogle Scholar
  14. 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 22:38–52PubMedCrossRefGoogle Scholar
  15. 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 290:2959–2967PubMedCrossRefGoogle Scholar
  16. 16.
    Boyle P, Leon ME (2002) Epidemiology of colorectal cancer. Br Med Bull 64:1–25PubMedCrossRefGoogle Scholar
  17. 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. 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. 19.
    Kune GA, Kune S, Watson LF (1990) Body weight and physical activity as predictors of colorectal cancer risk. Nutr Cancer 13:9–17PubMedCrossRefGoogle Scholar
  20. 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 80:1474–1480PubMedCrossRefGoogle Scholar
  21. 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 4:1973–1984CrossRefGoogle Scholar
  22. 22.
    Dufour M (1999) What is moderate drinking? Defining “drinks” and drinking levels. Alcohol Res Health 23:5–14PubMedGoogle Scholar
  23. 23.
    Turner C (1990) How much alcohol is in a ‘standard drink’? An analysis of 125 studies. Br J Addict 85:1171–1175PubMedCrossRefGoogle Scholar
  24. 24.
    Miller WR, Heather N, Hall W (1991) Calculating standard drink units: international comparisons. Br J Addict 86:43–47PubMedCrossRefGoogle Scholar
  25. 25.
    Kopec JA, Esdaile JM (1990) Bias in case-control studies. A review. J Epidemiol Community Health 44:179–186PubMedCrossRefGoogle Scholar
  26. 26.
    Hess DR (2004) Retrospective studies and chart reviews. Respir Care 49:1171–1174PubMedGoogle Scholar
  27. 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 46:832–838PubMedCrossRefGoogle Scholar
  28. 28.
    Lee IM, Paffenbarger RS (1992) Quetelet index and risk of colon cancer in college alumni. J Natl Cancer Inst 84:1326–1331PubMedCrossRefGoogle Scholar
  29. 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:53–60PubMedCrossRefGoogle Scholar
  30. 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 5:955–960Google Scholar
  31. 31.
    Chyou PH, Nomura AM, Stemmermann GN (1996) A prospective study of colon and rectal cancer among Hawaii Japanese men. Ann Epidemiol 6:276–282PubMedCrossRefGoogle Scholar
  32. 32.
    Singh PN, Fraser GE (1998) Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 148:761–774PubMedCrossRefGoogle Scholar
  33. 33.
    Ford ES (1999) Body mass index and colon cancer in a national sample of adult US men and women. Am J Epidemiol 150:390–398PubMedCrossRefGoogle Scholar
  34. 34.
    Rodriguez LAG, Huerta-Alvarez C (2001) Reduced risk of colorectal cancer among long-term users of aspirin and nonaspirin nonsteroidal antiinflammatory drugs. Epidemiology 12:88–93CrossRefGoogle Scholar
  35. 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 84:417–422PubMedCrossRefGoogle Scholar
  36. 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 15:581–589PubMedCrossRefGoogle Scholar
  37. 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 16:987–996PubMedCrossRefGoogle Scholar
  38. 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 12:222–227PubMedGoogle Scholar
  39. 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 42:84–90PubMedCrossRefGoogle Scholar
  40. 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 133:393–402PubMedCrossRefGoogle Scholar
  41. 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 335:1134–1139CrossRefGoogle Scholar
  42. 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 97:1486–1492PubMedCrossRefGoogle Scholar
  43. 43.
    Adams KF, Leltzmann MF, Albanes D et al (2007) Body mass and colorectal cancer risk in the NIH-AARP cohort. Am J Epidemiol 166:36–45PubMedCrossRefGoogle Scholar
  44. 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 19:783–792PubMedCrossRefGoogle Scholar
  45. 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 15:2336–2339PubMedCrossRefGoogle Scholar
  46. 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 61:194–205PubMedCrossRefGoogle Scholar
  47. 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 86:416–424PubMedCrossRefGoogle Scholar
  48. 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 102:391–400PubMedCrossRefGoogle Scholar
  49. 49.
    Severson RK, Nomura AMY, Grove JS, Stemmermann GN (1989) A prospective analysis of physical activity and cancer. Am J Epidemiol 130:522–529PubMedGoogle Scholar
  50. 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 1:481–485PubMedCrossRefGoogle Scholar
  51. 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 50:3610–3613PubMedGoogle Scholar
  52. 52.
    Lee IM, Paffenbarger RS, Hsieh CC (1991) Physical activity and risk of developing colorectal cancer among college alumni. J Natl Cancer Inst 83:1324–1329PubMedCrossRefGoogle Scholar
  53. 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 5:38–52PubMedCrossRefGoogle Scholar
  54. 54.
    White E, Jacobs EJ, Daling JR (1996) Physical activity in relation to colon cancer in middle-aged men and women. Am J Epidemiol 144:42–50PubMedCrossRefGoogle Scholar
  55. 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 8:568–574PubMedCrossRefGoogle Scholar
  56. 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 150:869–877PubMedCrossRefGoogle Scholar
  57. 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 39:50–57PubMedCrossRefGoogle Scholar
  58. 58.
    Wei EK, Giovannucci E, Wu K et al (2004) Comparison of risk factors for colon and rectal cancer. Int J Cancer 108:433–442PubMedCrossRefGoogle Scholar
  59. 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 160:860–867PubMedCrossRefGoogle Scholar
  60. 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 13:2187–2195PubMedGoogle Scholar
  61. 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 16:403–408PubMedCrossRefGoogle Scholar
  62. 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 18:199–209PubMedCrossRefGoogle Scholar
  63. 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 121:1325–1330PubMedCrossRefGoogle Scholar
  64. 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 86:183–191PubMedCrossRefGoogle Scholar
  65. 65.
    Baron JA, Gerhardsson de Verdier M, Ekbom A (1994) Coffee, tea, tobacco, and cancer of the large bowel. Cancer Epidemiol Biomarkers Prev 3:565–570PubMedGoogle Scholar
  66. 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 92:1178–1181PubMedCrossRefGoogle Scholar
  67. 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 11:28–37PubMedCrossRefGoogle Scholar
  68. 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 12:1492–1500PubMedGoogle Scholar
  69. 69.
    Slattery ML, Samowtiz W, Ma K et al (2004) CYP1A1, cigarette smoking, and colon and rectal cancer. Am J Epidemiol 160:842–852PubMedCrossRefGoogle Scholar
  70. 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 15:99–107PubMedCrossRefGoogle Scholar
  71. 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 652:54–64PubMedCrossRefGoogle Scholar
  72. 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 18:2745–2750PubMedCrossRefGoogle Scholar
  73. 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 18:2098–2106PubMedCrossRefGoogle Scholar
  74. 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 20:895–903PubMedCrossRefGoogle Scholar
  75. 75.
    Klatsky AL, Armstrong MA, Friedman GD, Hiatt RA (1988) The relations of alcoholic beverage use to colon and rectal cancer. Am J Epidemiol 128:1007–1015PubMedGoogle Scholar
  76. 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 1:141–145PubMedCrossRefGoogle Scholar
  77. 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 4:405–411PubMedCrossRefGoogle Scholar
  78. 78.
    Gerhardsson de Verdier M, Romelsjö A, Lundberg M (1993) Alcohol and cancer of the colon and rectum. Eur J Cancer Prev 2:401–408PubMedCrossRefGoogle Scholar
  79. 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 5:95–104PubMedCrossRefGoogle Scholar
  80. 80.
    Gapstur SM, Potter JD, Folsom AR (1994) Alcohol consumption and colon and rectal cancer in postmenopausal women. Int J Epidemiol 23:50–57PubMedCrossRefGoogle Scholar
  81. 81.
    Rosenberg L, Louik C, Shapiro S (1998) Nonsteroidal antiinflammatory drug use and reduced risk of large bowel carcinoma. Cancer 82:2326–2333PubMedCrossRefGoogle Scholar
  82. 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 10:1303–1304PubMedGoogle Scholar
  83. 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 13:551–561PubMedCrossRefGoogle Scholar
  84. 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 52:861–867PubMedCrossRefGoogle Scholar
  85. 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 90:118–121PubMedCrossRefGoogle Scholar
  86. 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–S179PubMedCrossRefGoogle Scholar
  87. 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 96:821–827PubMedCrossRefGoogle Scholar
  88. 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 121:2065–2072PubMedCrossRefGoogle Scholar
  89. 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 43:383–390PubMedCrossRefGoogle Scholar
  90. 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 23:395–401PubMedCrossRefGoogle Scholar
  91. 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 13:124–131PubMedCrossRefGoogle Scholar
  92. 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 9:26–32PubMedCrossRefGoogle Scholar
  93. 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 331:1669–1674PubMedCrossRefGoogle Scholar
  94. 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 37:830–834PubMedCrossRefGoogle Scholar
  95. 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 144:1122–1128PubMedCrossRefGoogle Scholar
  96. 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 28:603–608PubMedCrossRefGoogle Scholar
  97. 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 68:428–435PubMedCrossRefGoogle Scholar
  98. 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 14:879–887PubMedCrossRefGoogle Scholar
  99. 99.
    Hemminki K, Chen B (2005) Familial risks for colorectal cancer show evidence on recessive inheritance. Int J Cancer 115:835–838PubMedCrossRefGoogle Scholar
  100. 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 5:1195–1198PubMedCrossRefGoogle Scholar
  101. 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 27:4542–4547PubMedCrossRefGoogle Scholar
  102. 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 48:2742–2745PubMedCrossRefGoogle Scholar
  103. 103.
    Mellemkjaer L, Olsen JH, Frisch M, Johansen C, Gridley G, McLaughlin JK (1995) Cancer in patients with ulcerative colitis. Int J Cancer 60:330–333PubMedCrossRefGoogle Scholar
  104. 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 29:206–217PubMedCrossRefGoogle Scholar
  105. 105.
    Langholz E, Munkholm P, Davidsen M, Binder V (1992) Colorectal cancer risk and mortality in patients with ulcerative colitis. Gastroenterology 103:1444–1451PubMedGoogle Scholar
  106. 106.
    Gillen D, Andrews HA, Prior P, Allan RN (1994) Crohn’s disease and colorectal cancer. Gut 35:651–655PubMedCrossRefGoogle Scholar
  107. 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 10:117–122PubMedCrossRefGoogle Scholar
  108. 108.
    Persson PG, Karlén P, Bernell O et al (1994) Crohn’s disease and cancer: a population-based cohort study. Gastroenterology 107:1675–1679PubMedGoogle Scholar
  109. 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 94:1047–1052PubMedGoogle Scholar
  110. 110.
    Askling J, Dickman PW, Karlén P et al (2001) Family history as a risk factor for colorectal cancer in inflammatory bowel disease. Gastroenterology 120:1356–1362PubMedCrossRefGoogle Scholar
  111. 111.
    Kvist N, Jacobsen O, Kvist HK et al (1989) Malignancy in ulcerative colitis. Scand J Gastroenterol 24:497–506PubMedCrossRefGoogle Scholar
  112. 112.
    Ekbom A, Helmick C, Zack M, Adami HO (1990) Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med 323:1228–1233PubMedCrossRefGoogle Scholar
  113. 113.
    Ekbom A, Helmick C, Zack M, Adami HO (1990) Increased risk of large bowel cancer in Crohn’s disease with colonic involvement. Lancet 336:357–359PubMedCrossRefGoogle Scholar
  114. 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 138:1697–1703PubMedCrossRefGoogle Scholar
  115. 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 8:130–138PubMedCrossRefGoogle Scholar
  116. 116.
    Grodstein F, Martinez ME, Platz EA et al (1998) Postmenopausal hormone use and risk for colorectal cancer and adenoma. Ann Intern Med 128:705–712PubMedCrossRefGoogle Scholar
  117. 117.
    Paganini-Hill A (1999) Estrogen replacement therapy and colorectal cancer risk in elderly women. Dis Colon Rectum 42:1300–1305PubMedCrossRefGoogle Scholar
  118. 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 10:445–451PubMedCrossRefGoogle Scholar
  119. 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 9:443–447PubMedGoogle Scholar
  120. 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 171:415–425PubMedCrossRefGoogle Scholar
  121. 121.
    Friedman GD, Coates AO, Potter JD, Slattery ML (1998) Drugs and colon cancer. Pharmacoepidemiol Drug Saf 7:99–106PubMedCrossRefGoogle Scholar
  122. 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 15:713–721PubMedCrossRefGoogle Scholar
  123. 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 294:914–923PubMedCrossRefGoogle Scholar
  124. 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 99:608–615PubMedCrossRefGoogle Scholar
  125. 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 134:21–28PubMedCrossRefGoogle Scholar
  126. 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 160:1011–1022PubMedCrossRefGoogle Scholar
  127. 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 13:1509–1514PubMedGoogle Scholar
  128. 128.
    Chao A, Thun MJ, Connell CJ et al (2005) Meat consumption and risk of colorectal cancer. JAMA 293:172–182PubMedCrossRefGoogle Scholar
  129. 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 6:225–234PubMedCrossRefGoogle Scholar
  130. 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 5:495–502Google Scholar
  131. 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 10:1259–1266PubMedGoogle Scholar
  132. 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 95:2390–2396PubMedCrossRefGoogle Scholar
  133. 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 157:434–445PubMedCrossRefGoogle Scholar
  134. 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 112:259–264PubMedCrossRefGoogle Scholar
  135. 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 17:3098–3107PubMedCrossRefGoogle Scholar
  136. 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 152:1081–1092PubMedCrossRefGoogle Scholar
  137. 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 14:959–970PubMedCrossRefGoogle Scholar
  138. 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 89:1441–1452PubMedCrossRefGoogle Scholar
  139. 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 92:1740–1752PubMedCrossRefGoogle Scholar
  140. 140.
    Schwarzer G (2010) Meta: meta-analysis with R. http://cran.r-project.org/web/packages/meta/index.html. Accessed 28 Oct 2010
  141. 141.
    Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558PubMedCrossRefGoogle Scholar
  142. 142.
    DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188PubMedCrossRefGoogle Scholar
  143. 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 53:1119–1129PubMedCrossRefGoogle Scholar
  144. 144.
    Harrell FE, Lee KL, Pollock BG (1988) Regression-models in clinical-studies—determining relationships between predictors and response. J Natl Cancer Inst 80:1198–1202PubMedCrossRefGoogle Scholar
  145. 145.
    Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135:1301–1309PubMedGoogle Scholar
  146. 146.
    Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose-response data. Stata J 6:40–57Google Scholar
  147. 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 348:1625–1638PubMedCrossRefGoogle Scholar
  148. 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 89:948–955PubMedCrossRefGoogle Scholar
  149. 149.
    Giovannucci E (2002) Obesity, gender, and colon cancer. Gut 51:147PubMedCrossRefGoogle Scholar
  150. 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 11:19–30PubMedCrossRefGoogle Scholar
  151. 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 72:694–701PubMedGoogle Scholar
  152. 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 7:682–688PubMedCrossRefGoogle Scholar
  153. 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 125:171–180PubMedCrossRefGoogle Scholar
  154. 154.
    Liang PS, Chen TY, Giovannucci E (2009) Cigarette smoking and colorectal cancer incidence and mortality: systematic review and meta-analysis. Int J Cancer 124:2406–2415PubMedCrossRefGoogle Scholar
  155. 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 42:216–227PubMedCrossRefGoogle Scholar
  156. 156.
    Eaden JA, Abrams KR, Mayberry JF (2001) The risk of colorectal cancer in ulcerative colitis: a meta-analysis. Gut 48:526–535PubMedCrossRefGoogle Scholar
  157. 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 140:603–613PubMedCrossRefGoogle Scholar
  158. 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 22:1958–1972PubMedCrossRefGoogle Scholar
  159. 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 120:664–671PubMedCrossRefGoogle Scholar
  160. 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 1:59–68PubMedCrossRefGoogle Scholar
  161. 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, LondonGoogle Scholar
  162. 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 106:574–582PubMedCrossRefGoogle Scholar
  163. 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 101:256–266PubMedCrossRefGoogle Scholar
  164. 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 10:501–507PubMedCrossRefGoogle Scholar
  165. 165.
    StataCorp (2009) Stata base reference manual: A-H. College Station. StataCorp LP, TX Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Constance M. Johnson
    • 1
  • Caimiao Wei
    • 2
  • Joe E. Ensor
    • 2
  • Derek J. Smolenski
    • 3
  • Christopher I. Amos
    • 4
  • Bernard Levin
    • 5
  • Donald A. Berry
    • 2
  1. 1.School of Nursing and Community and Family MedicineDuke UniversityDurhamUSA
  2. 2.Division of Quantitative Sciences, Department of Biostatistics, Unit 1409The University of Texas MD Anderson Cancer CenterHoustonUSA
  3. 3.Research, Outcomes, Surveillance, Evaluations, National Center for Telehealth and TechnologyJoint Base Lewis-McChordTacomaUSA
  4. 4.Department of Community and Family Medicine, Geisel School of MedicineDartmouth CollegeLebanonUSA
  5. 5.Professor Emeritus, Division of Cancer Prevention and Population SciencesThe University of Texas MD Anderson Cancer CenterHoustonUSA

Personalised recommendations

Cite article

Buy options