Skip to main content

Advertisement

SpringerLink
Log in

Pooled analyses of 13 prospective cohort studies on folate intake and colon cancer

  • Original paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Objective

Studies of folate intake and colorectal cancer risk have been inconsistent. We examined the relation with colon cancer risk in a series of 13 prospective studies.

Methods

Study- and sex-specific relative risks (RRs) were estimated from the primary data using Cox proportional hazards models and then pooled using a random-effects model.

Results

Among 725,134 participants, 5,720 incident colon cancers were diagnosed during follow-up. The pooled multivariate RRs (95% confidence interval [CI]) comparing the highest vs. lowest quintile of intake were 0.92 (95% CI 0.84–1.00, p-value, test for between-studies heterogeneity = 0.85) for dietary folate and 0.85 (95% CI 0.77–0.95, p-value, test for between-studies heterogeneity = 0.42) for total folate. Results for total folate intake were similar in analyses using absolute intake cutpoints (pooled multivariate RR = 0.87, 95% CI 0.78–0.98, comparing ≥560 mcg/days vs. <240 mcg/days, p-value, test for trend = 0.009). When analyzed as a continuous variable, a 2% risk reduction (95% CI 0–3%) was estimated for every 100 μg/day increase in total folate intake.

Conclusion

These data support the hypothesis that higher folate intake is modestly associated with reduced risk of colon cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Glynn SA, Albanes D (1994) Folate and cancer: a review of the literature. Nutr Cancer 22(2):101–119

    Article  CAS  PubMed  Google Scholar 

  2. Lashner BA, Heidenreich PA, Su GL, Kane SV, Hanauer SB (1989) Effect of folate supplementation on the incidence of dysplasia and cancer in chronic ulcerative colitis. A case–control study. Gastroenterology 97(2):255–259

    CAS  PubMed  Google Scholar 

  3. Benito E, Stiggelbout A, Bosch FX, Obrador A, Kaldor J, Mulet M et al (1991) Nutritional factors in colorectal cancer risk: a case–control study in Majorca. Int J Cancer 49:161–167

    Article  CAS  PubMed  Google Scholar 

  4. Freudenheim JL, Graham S, Marshall JR, Haughey BP, Cholewinski S, Wilkinson G (1991) Folate intake and carcinogenesis of the colon and rectum. Int J Epidemiol 20:368–374

    Article  CAS  PubMed  Google Scholar 

  5. Meyer F, White E (1993) Alcohol and nutrients in relation to colon cancer in middle-aged adults. Am J Epidemiol 138:225–236

    CAS  PubMed  Google Scholar 

  6. Ferraroni M, La Vecchia C, D’Avanzo B, Negri E, Franceschi S, Decarli A (1994) Selected micronutrient intake and the risk of colorectal cancer. Br J Cancer 70(6):1150–1155

    CAS  PubMed  Google Scholar 

  7. Boutron-Ruault MC, Senesse P, Faivre J, Couillault C, Belghiti C (1996) Folate and alcohol intakes: related or independent roles in the adenoma-carcinoma sequence? Nutr Cancer 26(3):337–346

    Article  CAS  PubMed  Google Scholar 

  8. Slattery ML, Schaffer D, Edwards SL, Ma KN, Potter JD (1997) Are dietary factors involved in DNA methylation associated with colon cancer? Nutr Cancer 28(1):52–62

    Article  CAS  PubMed  Google Scholar 

  9. La Vecchia C, Braga C, Negri E, Franceschi S, Russo A, Conti E et al (1997) Intake of selected micronutrients and risk of colorectal cancer. Int J Cancer 73:525–530

    Article  PubMed  Google Scholar 

  10. White E, Shannon JS, Patterson RE (1997) Relationship between vitamin and calcium supplement use and colon cancer. Cancer Epidemiol Biomarkers Prev 6(10):769–774

    CAS  PubMed  Google Scholar 

  11. Levi F, Pasche C, Lucchini F, La Vecchia C (2000) Selected micronutrients and colorectal cancer.a case–control study from the canton of Vaud, Switzerland. Eur J Cancer 36(16):2115–2119

    Article  CAS  PubMed  Google Scholar 

  12. La Vecchia C, Negri E, Pelucchi C, Franceschi S (2002) Dietary folate and colorectal cancer. Int J Cancer 102(5):545–547

    Article  CAS  PubMed  Google Scholar 

  13. Le Marchand L, Donlon T, Hankin JH, Kolonel LN, Wilkens LR, Seifried A (2002) B-vitamin intake, metabolic genes, and colorectal cancer risk (United States). Cancer Causes Control 13(3):239–248

    Article  PubMed  Google Scholar 

  14. Pufulete M, Al-Ghnaniem R, Leather AJ, Appleby P, Gout S, Terry C et al (2003) Folate status, genomic DNA hypomethylation, and risk of colorectal adenoma and cancer: a case control study. Gastroenterology 124(5):1240–1248

    Article  CAS  PubMed  Google Scholar 

  15. Satia-Abouta J, Galanko JA, Martin CF, Potter JD, Ammerman A, Sandler RS (2003) Associations of micronutrients with colon cancer risk in African Americans and whites: results from the North Carolina Colon Cancer Study. Cancer Epidemiol Biomarkers Prev 12(8):747–754

    CAS  PubMed  Google Scholar 

  16. Otani T, Iwasaki M, Hanaoka T, Kobayashi M, Ishihara J, Natsukawa S et al (2005) Folate, vitamin B6, vitamin B12, and vitamin B2 intake, genetic polymorphisms of related enzymes, and risk of colorectal cancer in a hospital-based case–control study in Japan. Nutr Cancer 53(1):42–50

    Article  CAS  PubMed  Google Scholar 

  17. Giovannucci E, Rimm EB, Ascherio A, Stampfer MJ, Colditz GA, Willett WC (1995) Alcohol, low-methionine-low-folate diets, and risk of colon cancer in men. J Natl Cancer Inst 87:265–273

    Article  CAS  PubMed  Google Scholar 

  18. Glynn SA, Albanes D, Pietinen P, Brown CC, Rautalahti M, Tangrea JA et al (1996) Colorectal cancer and folate status: A nested case–control study among male smokers. Cancer Epidemiol Biomarkers Prev 5:487–494

    CAS  PubMed  Google Scholar 

  19. Giovannucci E, Stampfer MJ, Colditz GA, Hunter DJ, Fuchs C, Rosner BA et al (1998) Multivitamin use, folate and colon cancer in women in the Nurses’ Health Study. Ann Int Med 129:517–524

    CAS  PubMed  Google Scholar 

  20. Kato I, Dnistrian AM, Schwartz M, Toniolo P, Koenig K, Shore RE et al (1999) Serum folate, homocysteine and colorectal cancer risk in women: a nested case–control study. Br J Cancer 79(11–12):1917–1922

    Article  CAS  PubMed  Google Scholar 

  21. Su LJ, Arab L (2001) Nutritional status of folate and colon cancer risk: evidence from NHANES I epidemiologic follow-up study. Ann Epidemiol 11(1):65–72

    Article  CAS  PubMed  Google Scholar 

  22. Terry P, Jain M, Miller AB, Howe GR, Rohan TE (2002) Dietary intake of folic acid and colorectal cancer risk in a cohort of women. Int J Cancer 97(6):864–867

    Article  CAS  PubMed  Google Scholar 

  23. Flood A, Caprario L, Chaterjee N, Lacey JV Jr, 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(6):551–561

    Article  PubMed  Google Scholar 

  24. Harnack L, Jacobs DR Jr, Nicodemus K, Lazovich D, Anderson K, Folsom AR (2002) Relationship of folate, vitamin B-6, vitamin B-12, and methionine intake to incidence of colorectal cancers. Nutr Cancer 43(2):152–158

    Article  CAS  PubMed  Google Scholar 

  25. Konings EJ, Goldbohm RA, Brants HA, Saris WH, van den Brandt PA (2002) Intake of dietary folate vitamers and risk of colorectal carcinoma: results from The Netherlands Cohort Study. Cancer 95(7):1421–1433

    Article  CAS  PubMed  Google Scholar 

  26. Larsson SC, Giovannucci E, Wolk A (2005) A prospective study of dietary folate intake and risk of colorectal cancer: modification by caffeine intake and cigarette smoking. Cancer Epidemiol Biomarkers Prev 14(3):740–743

    Article  CAS  PubMed  Google Scholar 

  27. Zhang SM, Moore SC, Lin J, Cook NR, Manson JE, Lee IM et al (2006) Folate, vitamin B6, multivitamin supplements, and colorectal cancer risk in women. Am J Epidemiol 163(2):108–115

    Article  PubMed  Google Scholar 

  28. Sanjoaquin MA, Allen N, Couto E, Roddam AW, Key TJ (2005) Folate intake and colorectal cancer risk: a meta-analytical approach. Int J Cancer 113(5):825–828

    Article  CAS  PubMed  Google Scholar 

  29. Cravo ML, Mason JB, Dayal Y, Hutchinson M, Smith D, Selhub J et al (1992) Folate deficiency enhances the development of colonic neoplasia in dimethylhydrazine-treated rats. Cancer Res 52(18):5002–5006

    CAS  PubMed  Google Scholar 

  30. Smith-Warner S, Spiegelman D, Ritz J, Albanes D, Beeson W, Bernstein L et al (2006) Methods for pooling results of epidemiologic studies: the pooling project of prospective studies of diet and cancer. Am J Epidemiol 163(11):1053–1064

    Article  PubMed  Google Scholar 

  31. Bandera EV, Freudenheim JL, Marshall JR, Zielezny M, Priore RL, Brasure J et al (1997) Diet and alcohol consumption and lung cancer risk in the New York State Cohort (United States). Cancer Causes Control 8:828–840

    Article  CAS  PubMed  Google Scholar 

  32. Sieri S, Krogh V, Muti P, Micheli A, Pala V, Crosignani P et al (2002) Fat and protein intake and subsequent breast cancer risk in postmenopausal women. Nutr Cancer 42(1):10–17

    Article  PubMed  Google Scholar 

  33. Jacobs EJ, Connell CJ, Chao A, McCullough ML, Rodriguez C, Thun MJ et al (2003) Multivitamin use and colorectal cancer incidence in a US cohort: does timing matter? Am J Epidemiol 158(7):621–628

    Article  PubMed  Google Scholar 

  34. Singh PN, Fraser GE (1998) Dietary risk factors for colon cancer in a low-risk population. Am J Epidemiol 148(8):761–774

    CAS  PubMed  Google Scholar 

  35. Rothman KJ (1986) Modern epidemiology. Little Brown and Company, Boston

    Google Scholar 

  36. Wei EK, Giovannucci E, Wu K, Rosner B, Fuchs CS, Willett WC et al (2004) Comparison of risk factors for colon and rectal cancer. Int J Cancer 108(3):433–442

    Article  CAS  PubMed  Google Scholar 

  37. Willett W, Stampfer MJ (1986) Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 124(1):17–27

    CAS  PubMed  Google Scholar 

  38. SAS/STAT Software (1991) The PHREG procedure: preliminary documentation. SAS Institute, Cary

  39. Prentice RL (1986) A case-cohort design for epidemiologic cohort studies and disease prevention trials. Biometrika 73(1):1–11

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  41. Laird NM, Ware JH (1982) Random-effects models for longitudinal data. Biometrics 38(4):963–974

    Article  CAS  PubMed  Google Scholar 

  42. Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10(1):101–129

    Article  Google Scholar 

  43. Stram DO (1996) Meta-analysis of published data using a linear mixed-effects model. Biometrics 52:536–544

    Article  CAS  PubMed  Google Scholar 

  44. Anderson TW (1984) Introduction to multivariate statistics, 2nd edn. Wiley, New York

    Google Scholar 

  45. Subar AF, Block G, James LD (1989) Folate intake and food sources in the US population. Am J Clin Nutr 50(3):508–516

    CAS  PubMed  Google Scholar 

  46. Byers T, Marshall J, Fiedler R, Zielezny M, Graham S (1985) Assessing nutrient intake with an abbreviated dietary interview. Am J Epidemiol 122(1):41–50

    CAS  PubMed  Google Scholar 

  47. Suitor CW, Bailey LB (2000) Dietary folate equivalents: interpretation and application. J Am Diet Assoc 100(1):88–94

    Article  CAS  PubMed  Google Scholar 

  48. Herbert V (1987) Recommended dietary intakes (RDI) of folate in humans. Am J Clin Nutr 45(4):661–670

    CAS  PubMed  Google Scholar 

  49. Herbert V (1987) Making sense of laboratory tests of folate status: folate requirements to sustain normality. Am J Hematol 26(2):199–207

    Article  CAS  PubMed  Google Scholar 

  50. Rimm EB, Giovannucci EL, Stampfer MJ, Colditz GA, Litin LB, Willett WC (1992) Reproducibility and validity of an expanded self-administered semiquantitative food frequency questionnaire among male health professionals. Am J Epidemiol 135:1114–1126

    CAS  PubMed  Google Scholar 

  51. Giovannucci E, Stampfer MJ, Colditz GA, Rimm EB, Trichopoulos D, Rosner BA et al (1993) Folate, methionine, and alcohol intake and risk of colorectal adenoma. J Natl Cancer Inst 85:875–884

    Article  CAS  PubMed  Google Scholar 

  52. Feskanich D, Marshall J, Rimm EB, Litin LB, Willett WC (1994) Simulated validation of a brief food frequency questionnaire. Ann Epidemiol 4:181–187

    Article  CAS  PubMed  Google Scholar 

  53. Munger RG, Folsom AR, Kushi LH, Kaye SA, Sellers TA (1992) Dietary assessment of older Iowa women with a food frequency questionnaire: nutrient intake, reproducibility, and comparison with 24-hour dietary recall interviews. Am J Epidemiol 136(2):192–200

    CAS  PubMed  Google Scholar 

  54. Flagg EW, Coates RJ, Calle EE, Potischman N, Thun MJ (2000) Validation of the American Cancer Society Cancer Prevention Study II Nutrition Survey Cohort Food Frequency Questionnaire. Epidemiology 11(4):462–468

    Article  CAS  PubMed  Google Scholar 

  55. Serdula MK, Byers T, Mokdad AH, Simoes E, Mendlein JM, Coates RJ (1996) The association between fruit and vegetable intake and chronic disease risk factors. Epidemiology 7:161–165

    Article  CAS  PubMed  Google Scholar 

  56. Block G, Cox C, Madans J, Schreiber GB, Licitra L, Melia N (1988) Vitamin supplement use, by demographic characteristics. Am J Epidemiol 127(2):297–309

    CAS  PubMed  Google Scholar 

  57. Radimer K, Bindewald B, Hughes J, Ervin B, Swanson C, Picciano MF (2004) Dietary supplement use by US adults: data from the National Health and Nutrition Examination Survey, 1999–2000. Am J Epidemiol 160(4):339–349

    Article  PubMed  Google Scholar 

  58. Mason JB (1994) Folate and colonic carcinogenesis: searching for a mechanistic understanding. J Nutr Biochem 5(4):170–175

    Article  CAS  Google Scholar 

  59. Kim YI (1999) Folate and carcinogenesis: evidence, mechanisms, and implications. J Nutr Biochem 10:66–88

    Article  CAS  PubMed  Google Scholar 

  60. Duthie SJ (1999) Folic acid deficiency and cancer: mechanisms of DNA instability. Br Med Bull 55(3):578–592

    Article  CAS  PubMed  Google Scholar 

  61. Goelz SE, Vogelstein B, Hamilton SR, Feinberg AP (1985) Hypomethylation of DNA from benign and malignant human colon neoplasms. Science 228(4696):187–190

    Article  CAS  PubMed  Google Scholar 

  62. Zingg JM, Jones PA (1997) Genetic and epigenetic aspects of DNA methylation on genome expression, evolution, mutation and carcinogenesis. Carcinogenesis 18(5):869–882

    Article  CAS  PubMed  Google Scholar 

  63. Jacob RA, Gretz DM, Taylor PC, James SJ, Pogribny IP, Miller BJ et al (1998) Moderate folate depletion increases plasma homocysteine and decreases lymphocyte DNA methylation in postmenopausal women. J Nutr 128(7):1204–1212

    CAS  PubMed  Google Scholar 

  64. Rampersaud GC, Kauwell GP, Hutson AD, Cerda JJ, Bailey LB (2000) Genomic DNA methylation decreases in response to moderate folate depletion in elderly women. Am J Clin Nutr 72(4):998–1003

    CAS  PubMed  Google Scholar 

  65. Khosraviani K, Weir HP, Hamilton P, Moorehead J, Williamson K (2002) Effect of folate supplementation on mucosal cell proliferation in high risk patients for colon cancer. Gut 51(2):195–199

    Article  CAS  PubMed  Google Scholar 

  66. Sedwick WD, Kutler M, Brown OE (1981) Antifolate-induced misincorporation of deoxyuridine monophosphate into DNA: inhibition of high molecular weight DNA synthesis in human lymphoblastoid cells. Proc Natl Acad Sci U S A 78(2):917–921

    Article  CAS  PubMed  Google Scholar 

  67. Eto I, Krumdieck CL (1986) Role of vitamin B12 and folate deficiencies in carcinogenesis. Adv Exp Med Biol 206:313–330

    CAS  PubMed  Google Scholar 

  68. James SJ, Yin L (1989) Diet-induced DNA damage and altered nucleotide metabolism in lymphocytes from methyl-donor-deficient rats. Carcinogenesis 10(7):1209–1214

    Article  CAS  PubMed  Google Scholar 

  69. Borek C, Ong A, Morgan WF, Cleaver JE (1991) Morphological transformation of 10T1/2 mouse embryo cells can be initiated by DNA double-strand breaks alone. Mol Carcinog 4(3):243–247

    Article  CAS  PubMed  Google Scholar 

  70. Blount BC, Mack MM, Wehr CM, MacGregor JT, Hiatt RA, Wang G et al (1997) Folate deficiency causes uracil misincorporation into human DNA and chromosome breakage: implications for cancer and neuronal damage. Proc Natl Acad Sci U S A 94(7):3290–3295

    Article  CAS  PubMed  Google Scholar 

  71. Sharp L, Little J (2004) Polymorphisms in genes involved in folate metabolism and colorectal neoplasia: a HuGE review. Am J Epidemiol 159(5):423–443

    Article  PubMed  Google Scholar 

  72. Shaw S, Jayatilleke E, Herbert V, Colman N (1989) Cleavage of folates during ethanol metabolism role of acetaldehyde/xanthine oxidase-generated superoxide. Biochem J 257(1):277–280

    CAS  PubMed  Google Scholar 

  73. Chen AT, Reidy JA, Annest JL, Welty TK, Zhou HG (1989) Increased chromosome fragility as a consequence of blood folate levels, smoking status, and coffee consumption. Environ Mol Mutagen 13(4):319–324

    Article  CAS  PubMed  Google Scholar 

  74. Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Kearney J 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  CAS  PubMed  Google Scholar 

  75. Kune GA, Vitetta L (1992) Alcohol consumption and the etiology of colorectal cancer: a review of the scientific evidence from 1957 to 1991. Nutr Cancer 18:97–111

    Article  CAS  PubMed  Google Scholar 

  76. Cho E, Smith-Warner SA, Ritz J, van den Brandt PA, Colditz GA, Folsom AR et al (2004) Alcohol intake and colorectal cancer: a pooled analysis of 8 cohort studies. Ann Int Med 140(8):603–613

    PubMed  Google Scholar 

  77. Homann N, Tillonen J, Salaspuro M (2000) Microbially produced acetaldehyde from ethanol may increase the risk of colon cancer via folate deficiency. Int J Cancer 86(2):169–173

    Article  CAS  PubMed  Google Scholar 

  78. Francis KT, Thompson RW, Krumdieck CL (1977) Reaction of tetrahydrofolic acid with cyanate from urea solutions: formation of an inactive folate derivative. Am J Clin Nutr 30(12):2028–2032

    CAS  PubMed  Google Scholar 

  79. Abu Khaled M, Watkins CL, Krumdieck CL (1986) Inactivation of B12 and folate coenzymes by butyl nitrite as observed by NMR: implications on one-carbon transfer mechanism. Biochem Biophys Res Commun 135(1):201–207

    Article  CAS  PubMed  Google Scholar 

  80. Cole BF, Baron JA, Sandler RS, Haile RW, Ahnen DJ, Bresalier RS et al (2007) Folic acid for the prevention of colorectal adenomas: a randomized clinical trial. JAMA 297(21):2351–2359

    Article  CAS  PubMed  Google Scholar 

  81. Kim YI (2004) Folate, colorectal carcinogenesis, and DNA methylation: lessons from animal studies. Environ Mol Mutagen 44(1):10–25

    Article  CAS  PubMed  Google Scholar 

  82. Mason JB, Dickstein A, Jacques PF, Haggarty P, Selhub J, Dallal G et al (2007) A temporal association between folic acid fortification and an increase in colorectal cancer rates may be illuminating important biological principles: a hypothesis. Cancer Epidemiol Biomarkers Prev 16(7):1325–1329

    Article  CAS  PubMed  Google Scholar 

  83. Ulrich CM, Potter JD (2007) Folate and cancer—timing is everything. JAMA 297(21):2408–2409

    Article  CAS  PubMed  Google Scholar 

  84. Park Y, Spiegelman D, Hunter DJ, Albanes D, Bergkvist L, Buring JE, Freudenheim JL, Giovannucci E, Goldbohm RA, Harnack L, Kato I, Krogh V, Leitzmann MF, Limburg PJ, Marshall JR, McCullough ML, Miller AB, Rohan TE, Schatzkin A, Shore R, Sieri S, Stampfer MJ, Virtamo J, Weijenberg M, Willett WC, Wolk A, Zhang SM, Smith-Warner SA (2010) Intakes of vitamins A, C, and E and use of multiple vitamin supplements and risk of colon cancer: a pooled analysis of prospective cohort studies. Cancer Causes Control. doi:10.1007/s10552-010-9549-y

Download references

Acknowledgments

Supported by research grant CA55075 from the National Institutes of Health and by the National Colorectal Cancer Research Alliance.

Author information

Authors and Affiliations

  1. Department of Social and Preventive Medicine, College of Medicine, Hallym University, Chunchon, Korea

    Dong-Hyun Kim

  2. Department of Nutrition, Harvard School of Public Health, 665 Huntington Ave., Boston, MA, 02115, USA

    Stephanie A. Smith-Warner, Shiaw-Shyuan Yaun, Edward Giovannucci, Walter C. Willett & David J. Hunter

  3. Department of Epidemiology, Harvard School of Public Health, Boston, MA, USA

    Stephanie A. Smith-Warner, Donna Spiegelman, Edward Giovannucci, Walter C. Willett & David J. Hunter

  4. Department of Biostatistics, Harvard School of Public Health, Boston, MA, USA

    Donna Spiegelman

  5. Department of Environmental Health, Harvard School of Public Health, Boston, MA, USA

    Frank E. Speizer

  6. Institute for Public Health, Washington University School of Medicine, St. Louis, MO, USA

    Graham A. Colditz

  7. Channing Laboratory, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School, Boston, MA, USA

    Edward Giovannucci, Frank E. Speizer, Walter C. Willett & David J. Hunter

  8. Department of Social and Preventive Medicine, University at Buffalo, State University of New York, Buffalo, NY, USA

    Jo L. Freudenheim & Saxon Graham

  9. Department of Prevention and Health, TNO Quality of Life, Leiden, The Netherlands

    R. Alexandra Goldbohm

  10. Division of Epidemiology and Community Health, School of Public Health, University of Minnesota, Minneapolis, MN, USA

    Lisa Harnack

  11. Epidemiology and Surveillance Research, American Cancer Society, Atlanta, GA, USA

    Eric J. Jacobs & Victoria L. Stevens

  12. Institute of Epidemiology and Preventive Medicine, University of Regensburg, Regensburg, Germany

    Michael Leitzmann

  13. Nutritional Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, DHHS, Bethesda, MD, USA

    Arthur Schatzkin

  14. Nutritional Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA

    Rachael Stolzenberg-Solomon

  15. Department of Health Promotion and Chronic Disease Prevention, National Public Health Institute, Helsinki, Finland

    Satu Mannisto

  16. Dalla Lana School of Public Health, University of Toronto, Toronto, ON, Canada

    Anthony B. Miller

  17. Division of Public Health Services, Fred Hutchinson Cancer Research Center, Seattle, WA, USA

    John D. Potter

  18. Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY, USA

    Thomas E. Rohan

  19. Department of Epidemiology, Emory University, Rollins School of Public Health, Atlanta, GA, USA

    Paul Terry

  20. Department of Epidemiology, School for Oncology and Developmental Biology (GROW), Maastricht University, Maastricht, The Netherlands

    Matty P. Weijenberg

  21. Division of Nutritional Epidemiology, The National Institute of Environmental Medicine, Karolinska Institute, Stockholm, Sweden

    Alicja Wolk

  22. Department of Environmental Medicine, New York University, New York, NY, USA

    Paolo Toniolo & Anne Zeleniuch-Jacquotte

Authors
  1. Dong-Hyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephanie A. Smith-Warner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Donna Spiegelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shiaw-Shyuan Yaun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Graham A. Colditz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jo L. Freudenheim
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Edward Giovannucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R. Alexandra Goldbohm
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Saxon Graham
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lisa Harnack
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Eric J. Jacobs
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Michael Leitzmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Satu Mannisto
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Anthony B. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. John D. Potter
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Thomas E. Rohan
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Arthur Schatzkin
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Frank E. Speizer
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Victoria L. Stevens
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Rachael Stolzenberg-Solomon
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Paul Terry
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. Paolo Toniolo
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Matty P. Weijenberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Walter C. Willett
    View author publications

    You can also search for this author in PubMed Google Scholar

  25. Alicja Wolk
    View author publications

    You can also search for this author in PubMed Google Scholar

  26. Anne Zeleniuch-Jacquotte
    View author publications

    You can also search for this author in PubMed Google Scholar

  27. David J. Hunter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephanie A. Smith-Warner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kim, DH., Smith-Warner, S.A., Spiegelman, D. et al. Pooled analyses of 13 prospective cohort studies on folate intake and colon cancer. Cancer Causes Control 21, 1919–1930 (2010). https://doi.org/10.1007/s10552-010-9620-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-010-9620-8

Keywords

Search

Navigation