Cancer Causes & Control

, Volume 25, Issue 9, pp 1119–1129 | Cite as

Dietary B vitamin and methionine intake and MTHFR C677T genotype on risk of colorectal tumors in Lynch syndrome: the GEOLynch cohort study

  • Audrey Y. Jung
  • Fränzel J. B. van Duijnhoven
  • Fokko M. Nagengast
  • Akke Botma
  • Renate C. Heine-Bröring
  • Jan H. Kleibeuker
  • Hans F. A. Vasen
  • Jan L. Harryvan
  • Renate M. Winkels
  • Ellen Kampman
Original paper

Abstract

Purpose

Dietary intake of B vitamins and methionine, essential components of DNA synthesis and methylation pathways, may influence colorectal tumor (CRT) development. The impact of B vitamins on colorectal carcinogenesis in individuals with Lynch syndrome (LS) is unknown but is important given their high lifetime risk of developing neoplasms. The role of MTHFR C677T genotype in modifying these relationships in LS individuals is also unclear. We investigated associations between dietary intakes of folate, vitamins B2, B6, B12, and methionine and CRT development in a prospective cohort study of 470 mismatch repair gene mutation carriers.

Methods

Dietary intakes were assessed by food frequency questionnaire. Cox regression models with robust sandwich covariance estimation, adjusted for age, sex, physical activity, number of colonoscopies during person-time, NSAID use, and mutual vitamins were used to calculate hazard ratios (HRs) and 95 % confidence intervals (95 % CIs). Analyses were also stratified by MTHFR C677T genotype.

Results

During a median person-time of 28.0 months, 131 persons developed a CRT. Fifty-one of these persons developed an incident colorectal adenoma, while there were four persons who developed an incident colorectal carcinoma. Compared to the lowest tertile of intake, adjusted HRs (95 % CIs) for CRT development in the highest tertile were 1.06 (0.59–1.91) for folate, 0.77 (0.39–1.51) for vitamin B2, 0.98 (0.59–1.62) for vitamin B6, 1.24 (0.77–2.00) for vitamin B12, and 1.36 (0.83–2.20) for methionine. Low vitamin B2 and low methionine intake were statistically significantly associated with an increased risk of CRT in MTHFR 677TT individuals compared to a combined reference of persons with low intake and CC genotype.

Conclusions

There was no suggestion that intake of any dietary B vitamin or methionine was associated with CRT development among those with LS.

Keywords

B vitamins Colorectal cancer Colorectal adenoma Lynch syndrome Folate Diet 

Notes

Acknowledgments

We are grateful to all the participants of the GEOLynch cohort study. We thank Leontien Witjes (Wageningen University), Maria van Vugt (Radboud University Medical Center), Mary Velthuizen (Netherlands Foundation for the Detection for Hereditary Tumors), Alice Donselaar (Netherlands Foundation for the Detection of Hereditary Tumors), Carolien Lute (Wageningen University), and Ramazan Buyukcelik (Erasmus Medical Center) for their assistance with recruitment, data collection, DNA preparation, and genotyping. The work described in this paper was carried out with the support of the Dutch Cancer Society (KWF, Grant Number KUN-2007-3842).

References

  1. 1.
    Bronner CE, Baker SM, Morrison PT, Warren G, Smith LG, Lescoe MK, Kane M, Earabino C, Lipford J, Lindblom A (1994) Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary non-polyposis colon cancer. Nature 368(6468):258–261PubMedCrossRefGoogle Scholar
  2. 2.
    Fishel R, Lescoe MK, Rao MR, Copeland NG, Jenkins NA, Garber J, Kane M, Kolodner R (1993) The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75(5):1027–1038PubMedCrossRefGoogle Scholar
  3. 3.
    Hendriks YM, Jagmohan-Changur S, van der Klift HM, Morreau H, van Puijenbroek M, Tops C, van Os T, Wagner A, Ausems MG, Gomez E, Breuning MH, Brocker-Vriends AH, Vasen HF, Wijnen JT (2006) Heterozygous mutations in PMS2 cause hereditary nonpolyposis colorectal carcinoma (Lynch syndrome). Gastroenterology 130(2):312–322PubMedCrossRefGoogle Scholar
  4. 4.
    Miyaki M, Konishi M, Tanaka K, Kikuchi-Yanoshita R, Muraoka M, Yasuno M, Igari T, Koike M, Chiba M, Mori T (1997) Germline mutation of the MSH6 as the cause of hereditary nonpolyposis colorectal cancer. Nat Genet 17(3):271–272PubMedCrossRefGoogle Scholar
  5. 5.
    Ligtenberg MJ, Kuiper RP, Chan TL, Goossens M, Hebeda KM, Voorendt M, Lee TY, Bodmer D, Hoenselaar E, Hendriks-Cornelissen SJ, Tsui WY, Kong CK, Brunner HG, van Kessel AG, Yuen ST, van Krieken JH, Leung SY, Hoogerbrugge N (2009) Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3′ exons of TACSTD1. Nat Genet 41(1):112–117PubMedCrossRefGoogle Scholar
  6. 6.
    Aarnio M, Mecklin JP, Aaltonen LA, Nyström-Lahti M, Järvinen HJ (1995) Life-time risk of different cancers in hereditary non-polyposis colorectal cancer (HNPCC) syndrome. Int J Cancer 64(6):430–433PubMedCrossRefGoogle Scholar
  7. 7.
    Aarnio M, Sankila R, Pukkala E, Salovaara R, Aaltonen LA, de la Chapelle A, Peltomaki P, Mecklin JP, Jarvinen HJ (1999) Cancer risk in mutation carriers of DNA-mismatch-repair genes. Int J Cancer 81(2):214–218PubMedCrossRefGoogle Scholar
  8. 8.
    Dunlop MG, Farrington SM, Carothers AD, Wyllie AH, Sharp L, Burn J, Liu B, Kinzler KW, Vogelstein B (1997) Cancer risk associated with germline DNA mismatch repair gene mutations. Hum Mol Genet 6(1):105–110PubMedCrossRefGoogle Scholar
  9. 9.
    Watson P, Lynch HT (2001) Cancer risk in mismatch repair gene mutation carriers. Fam Cancer 1(1):57–60PubMedCrossRefGoogle Scholar
  10. 10.
    Vasen HF, Wijnen JT, Menko FH, Kleibeuker JH, Taal BG, Griffioen G, Nagengast FM, Meijers-Heijboer EH, Bertario L, Varesco L, Bisgaard ML, Mohr J, Fodde R, Khan PM (1996) Cancer risk in families with hereditary nonpolyposis colorectal cancer diagnosed by mutation analysis. Gastroenterology 110(4):1020–1027PubMedCrossRefGoogle Scholar
  11. 11.
    Barrow E, Alduaij W, Robinson L, Shenton A, Clancy T, Lalloo F, Hill J, Evans DG (2008) Colorectal cancer in HNPCC: cumulative lifetime incidence, survival and tumour distribution. A report of 121 families with proven mutations. Clin Genet 74(3):233–242PubMedCrossRefGoogle Scholar
  12. 12.
    Jenkins MA, Baglietto L, Dowty JG, Van Vliet CM, Smith L, Mead LJ, Macrae FA, St John DJ, Jass JR, Giles GG, Hopper JL, Southey MC (2006) Cancer risks for mismatch repair gene mutation carriers: a population-based early onset case-family study. Clin Gastroenterol Hepatol 4(4):489–498PubMedCrossRefGoogle Scholar
  13. 13.
    Hampel H, Stephens JA, Pukkala E, Sankila R, Aaltonen LA, Mecklin JP, de la Chapelle A (2005) Cancer risk in hereditary nonpolyposis colorectal cancer syndrome: later age of onset. Gastroenterology 129(2):415–421PubMedCrossRefGoogle Scholar
  14. 14.
    Watson P, Lynch HT (1994) The tumor spectrum in HNPCC. Anticancer Res 14(4B):1635–1639PubMedGoogle Scholar
  15. 15.
    Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61(5):759–767PubMedCrossRefGoogle Scholar
  16. 16.
    Hill MJ, Morson BC, Bussey HJ (1978) Aetiology of adenoma–carcinoma sequence in large bowel. Lancet 1(8058):245–247PubMedCrossRefGoogle Scholar
  17. 17.
    Edelstein DL, Axilbund J, Baxter M, Hylind LM, Romans K, Griffin CA, Cruz-Correa M, Giardiello FM (2011) Rapid development of colorectal neoplasia in patients with Lynch syndrome. Clin Gastroenterol Hepatol 9(4):340–343PubMedCentralPubMedCrossRefGoogle Scholar
  18. 18.
    Rijcken FE, Hollema H, Kleibeuker JH (2002) Proximal adenomas in hereditary non-polyposis colorectal cancer are prone to rapid malignant transformation. Gut 50(3):382–386PubMedCentralPubMedCrossRefGoogle Scholar
  19. 19.
    Vasen HF, Nagengast FM, Khan PM (1995) Interval cancers in hereditary non-polyposis colorectal cancer (Lynch syndrome). Lancet 345(8958):1183–1184PubMedCrossRefGoogle Scholar
  20. 20.
    Botma A, Nagengast FM, Braem MG, Hendriks JC, Kleibeuker JH, Vasen HF, Kampman E (2010) Body mass index increases risk of colorectal adenomas in men with Lynch syndrome: the GEOLynch cohort study. J Clin Oncol 28(28):4346–4353PubMedCrossRefGoogle Scholar
  21. 21.
    Win AK, Dowty JG, English DR, Campbell PT, Young JP, Winship I, Macrae FA, Lipton L, Parry S, Young GP, Buchanan DD, Martinez ME, Jacobs ET, Ahnen DJ, Haile RW, Casey G, Baron JA, Lindor NM, Thibodeau SN, Newcomb PA, Potter JD, Le Marchand L, Gallinger S, Hopper JL, Jenkins MA (2011) Body mass index in early adulthood and colorectal cancer risk for carriers and non-carriers of germline mutations in DNA mismatch repair genes. Br J Cancer 105(1):162–169PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Winkels RM, Botma A, Van Duijnhoven FJ, Nagengast FM, Kleibeuker JH, Vasen HF, Kampman E (2012) Smoking increases the risk for colorectal adenomas in patients with Lynch syndrome. Gastroenterology 142(2):241–247PubMedCrossRefGoogle Scholar
  23. 23.
    Diergaarde B, Braam H, Vasen HF, Nagengast FM, van Muijen GN, Kok FJ, Kampman E (2007) Environmental factors and colorectal tumor risk in individuals with hereditary nonpolyposis colorectal cancer. Clin Gastroenterol Hepatol 5(6):736–742PubMedCrossRefGoogle Scholar
  24. 24.
    Pande M, Lynch PM, Hopper JL, Jenkins MA, Gallinger S, Haile RW, LeMarchand L, Lindor NM, Campbell PT, Newcomb PA, Potter JD, Baron JA, Frazier ML, Amos CI (2010) Smoking and colorectal cancer in Lynch syndrome: results from the colon cancer family registry and the University of Texas M.D. Anderson Cancer Center. Clin Cancer Res 16(4):1331–1339PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Botma A, Vasen HF, van Duijnhoven FJ, Kleibeuker JH, Nagengast FM, Kampman E (2013) Dietary patterns and colorectal adenomas in Lynch syndrome: the GEOLynch cohort study. Cancer 119(3):512–521PubMedCrossRefGoogle Scholar
  26. 26.
    Burn J, Gerdes AM, Macrae F, Mecklin JP, Moeslein G, Olschwang S, Eccles D, Evans DG, Maher ER, Bertario L, Bisgaard ML, Dunlop MG, Ho JW, Hodgson SV, Lindblom A, Lubinski J, Morrison PJ, Murday V, Ramesar R, Side L, Scott RJ, Thomas HJ, Vasen HF, Barker G, Crawford G, Elliott F, Movahedi M, Pylvanainen K, Wijnen JT, Fodde R, Lynch HT, Mathers JC, Bishop DT, Ball J, Baxter L, Boussioutas A, Bradshaw N, Brewer C, Broughton M, Bulman B, Castiglione M, Clark S, Ching R, Chu C, Cina S, Cook J, Cummings C, Davies R, Debniak T, de Moncuit C, Drummond S, Ellis T, Fidalgo P, Gallinger S, Goff S, Goldberg PA, Goodman S, Harocopos C, Hutter P, Jeffers L, Jordan S, Killick P, Krauss C, Kristensen J, Langman C, Leite J, Liljegren A, Oliani C, Marks C, Membrez-Antonioli V, Miller J, Miles T, Segura PP, Pichert G, Pietersen E, Rossi G, Sala P, Sampson J, Schmocker B, Shaw J, Spigelman A, Tempesta A, Velthuizen M, Walpole I, Kerr D, Perkins S, Cuzick J, Wood LF, Steele R, Altman D, Paraskeva C, Atkin W, Hull M (2011) Long-term effect of aspirin on cancer risk in carriers of hereditary colorectal cancer: an analysis from the CAPP2 randomised controlled trial. Lancet 378(9809):2081–2087PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Benito E, Cabeza E, Moreno V, Obrador A, Bosch FX (1993) Diet and colorectal adenomas: a case–control study in Majorca. Int J Cancer 55(2):213–219PubMedCrossRefGoogle Scholar
  28. 28.
    Lee JE, Willett WC, Fuchs CS, Smith-Warner SA, Wu K, Ma J, Giovannucci E (2011) Folate intake and risk of colorectal cancer and adenoma: modification by time. Am J Clin Nutr 93(4):817–825PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    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):825–828PubMedCrossRefGoogle Scholar
  30. 30.
    Key TJ, Appleby PN, Masset G, Brunner EJ, Cade JE, Greenwood DC, Stephen AM, Kuh D, Bhaniani A, Powell N, Khaw KT (2012) Vitamins, minerals, essential fatty acids and colorectal cancer risk in the United Kingdom dietary cohort consortium. Int J Cancer 131(3):E320–E325PubMedCrossRefGoogle Scholar
  31. 31.
    Shrubsole MJ, Yang G, Gao YT, Chow WH, Shu XO, Cai Q, Rothman N, Gao J, Wagner C, Zheng W (2009) Dietary B vitamin and methionine intakes and plasma folate are not associated with colorectal cancer risk in Chinese women. Cancer Epidemiol Biomark Prev 18(3):1003–1006CrossRefGoogle Scholar
  32. 32.
    van den Donk M, Buijsse B, van den Berg SW, Ocke MC, Harryvan JL, Nagengast FM, Kok FJ, Kampman E (2005) Dietary intake of folate and riboflavin, MTHFR C677T genotype, and colorectal adenoma risk: a Dutch case–control study. Cancer Epidemiol Biomark Prev 14(6):1562–1566CrossRefGoogle Scholar
  33. 33.
    de Vogel S, Dindore V, van Engeland M, Goldbohm RA, van den Brandt PA, Weijenberg MP (2008) Dietary folate, methionine, riboflavin, and vitamin B-6 and risk of sporadic colorectal cancer. J Nutr 138(12):2372–2378PubMedCrossRefGoogle Scholar
  34. 34.
    World Cancer Research Fund/American Institute for Cancer Research (2011) Continuous update project report. Food, nutrition, physical activity, and the prevention of colorectal cancerGoogle Scholar
  35. 35.
    Houlston RS, Tomlinson IP (2001) Polymorphisms and colorectal tumor risk. Gastroenterology 121(2):282–301PubMedCrossRefGoogle Scholar
  36. 36.
    Sharp L, Little J (2004) Polymorphisms in genes involved in folate metabolism and colorectal neoplasia: a HuGE review. Am J Epidemiol 159(5):423–443PubMedCrossRefGoogle Scholar
  37. 37.
    Feunekes GI, Van Staveren WA, De Vries JH, Burema J, Hautvast JG (1993) Relative and biomarker-based validity of a food frequency questionnaire estimating intake of fats and cholesterol. Am J Clin Nutr 58(4):489–496PubMedGoogle Scholar
  38. 38.
    Verkleij-Hagoort AC, de Vries JH, Stegers MP, Lindemans J, Ursem NT, Steegers-Theunissen RP (2007) Validation of the assessment of folate and vitamin B12 intake in women of reproductive age: the method of triads. Eur J Clin Nutr 61(5):610–615PubMedGoogle Scholar
  39. 39.
    Netherlands Nutrition Center (2006) NEVO Nederlandse Voedingsmiddelentabel (Dutch food composition table). Netherlands Nutrition Center, The HagueGoogle Scholar
  40. 40.
    Baecke JA, Burema J, Frijters JE (1982) A short questionnaire for the measurement of habitual physical activity in epidemiological studies. Am J Clin Nutr 36(5):936–942PubMedGoogle Scholar
  41. 41.
    Pufulete M, Emery PW, Nelson M, Sanders TA (2002) Validation of a short food frequency questionnaire to assess folate intake. Br J Nutr 87(4):383–390PubMedCrossRefGoogle Scholar
  42. 42.
    Drogan D, Klipstein-Grobusch K, Wans S, Luley C, Boeing H, Dierkes J (2004) Plasma folate as marker of folate status in epidemiological studies: the European investigation into cancer and nutrition (EPIC)-Potsdam study. Br J Nutr 92(3):489–496PubMedCrossRefGoogle Scholar
  43. 43.
    Fayet F, Flood V, Petocz P, Samman S (2011) Relative and biomarker-based validity of a food frequency questionnaire that measures the intakes of vitamin B(12), folate, iron, and zinc in young women. Nutr Res 31(1):14–20PubMedCrossRefGoogle Scholar
  44. 44.
    De Jong AE, Morreau H, Van Puijenbroek M, Eilers PH, Wijnen J, Nagengast FM, Griffioen G, Cats A, Menko FH, Kleibeuker JH, Vasen HF (2004) The role of mismatch repair gene defects in the development of adenomas in patients with HNPCC. Gastroenterology 126(1):42–48PubMedCrossRefGoogle Scholar
  45. 45.
    Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65(4 Suppl.):1220S–1228S; discussion 1229S–1231SPubMedGoogle Scholar
  46. 46.
    Roswall N, Olsen A, Christensen J, Dragsted LO, Overvad K, Tjønneland A (2010) Micronutrient intake and risk of colon and rectal cancer in a Danish cohort. Cancer Epidemiol 34(1):40–46PubMedCrossRefGoogle Scholar
  47. 47.
    Kabat GC, Miller AB, Jain M, Rohan TE (2008) Dietary intake of selected B vitamins in relation to risk of major cancers in women. Br J Cancer 99(5):816–821PubMedCentralPubMedCrossRefGoogle Scholar
  48. 48.
    Baron JA, Sandler RS, Haile RW, Mandel JS, Mott LA, Greenberg ER (1998) Folate intake, alcohol consumption, cigarette smoking, and risk of colorectal adenomas. J Natl Cancer Inst 90(1):57–62PubMedCrossRefGoogle Scholar
  49. 49.
    World Cancer Research Fund/American Institute for Cancer Research (2010) Systematic literature review continuous update project report. The associations between food, nutrition and physical activity and the risk of colorectal cancerGoogle Scholar
  50. 50.
    Kim DH, Smith-Warner SA, Spiegelman D, Yaun SS, Colditz GA, Freudenheim JL, Giovannucci E, Goldbohm RA, Graham S, Harnack L, Jacobs EJ, Leitzmann M, Mannisto S, Miller AB, Potter JD, Rohan TE, Schatzkin A, Speizer FE, Stevens VL, Stolzenberg-Solomon R, Terry P, Toniolo P, Weijenberg MP, Willett WC, Wolk A, Zeleniuch-Jacquotte A, Hunter DJ (2010) Pooled analyses of 13 prospective cohort studies on folate intake and colon cancer. Cancer Causes Control 21(11):1919–1930PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    Larsson SC, Orsini N, Wolk A (2010) Vitamin B6 and risk of colorectal cancer: a meta-analysis of prospective studies. JAMA 303(11):1077–1083PubMedCrossRefGoogle Scholar
  52. 52.
    Zhang X, Lee JE, Ma J, Je Y, Wu K, Willett WC, Fuchs CS, Giovannucci EL (2012) Prospective cohort studies of vitamin B-6 intake and colorectal cancer incidence: modification by time? Am J Clin Nutr 96(4):874–881PubMedCentralPubMedCrossRefGoogle Scholar
  53. 53.
    World Cancer Research Fund/American Institute for Cancer Research (2007) Food, nutrition, physical activity, and the prevention of cancer: a global perspective. AICR, Washington, DCGoogle Scholar
  54. 54.
    Ulrich CM (2007) Folate and cancer prevention: a closer look at a complex picture. Am J Clin Nutr 86(2):271–273PubMedGoogle Scholar
  55. 55.
    Kim YI (2004) Folate, colorectal carcinogenesis, and DNA methylation: lessons from animal studies. Environ Mol Mutagen 44(1):10–25PubMedCrossRefGoogle Scholar
  56. 56.
    Song J, Sohn KJ, Medline A, Ash C, Gallinger S, Kim YI (2000) Chemopreventive effects of dietary folate on intestinal polyps in Apc+/− Msh2−/− mice. Cancer Res 60(12):3191–3199PubMedGoogle Scholar
  57. 57.
    Vollset SE, Clarke R, Lewington S, Ebbing M, Halsey J, Lonn E, Armitage J, Manson JE, Hankey GJ, Spence JD, Galan P, Bønaa KH, Jamison R, Gaziano JM, Guarino P, Baron JA, Logan RF, Giovannucci EL, den Heijer M, Ueland PM, Bennett D, Collins R, Peto R, Armitage J, Bowman L, Clarke R, Parish S, Peto R, Collins R, Lonn E, Yusuf S, Manson JE, Glynn R, Grodstein F, Albert CM, Cook NR, Hankey G, Eikelboom JW, Toole J, Malinow MR, Chambless LE, Spence JD, Pettigrew LC, Howard VJ, Sides EG, Wang CH, Stampfer M, Galan P, Hercberg S, Nygård O, Ebbing M, Nordrehaug JE, Nilsen DW, Ueland PM, Refsum H, Vollset SE, Bønaa KH, Njølstad I, Jamison R, Gaziano J, Guarino P, Baron JA, Giovannucci EA, Logan RF, denHeijer M, Blom H, Bos G, Clarke R, Halsey J, Lewington S, Bennett D, Collins R, Peto R (2013) Effects of folic acid supplementation on overall and site-specific cancer incidence during the randomised trials: meta-analyses of data on 50,000 individuals. Lancet 381(9871):1029–1036PubMedCrossRefGoogle Scholar
  58. 58.
    Logan RF, Grainge MJ, Shepherd VC, Armitage NC, Muir KR (2008) Aspirin and folic acid for the prevention of recurrent colorectal adenomas. Gastroenterology 134(1):29–38PubMedCrossRefGoogle Scholar
  59. 59.
    Song Y, Manson JE, Lee IM, Cook NR, Paul L, Selhub J, Giovannucci E, Zhang SM (2012) Effect of combined folic acid, vitamin B(6), and vitamin B(12) on colorectal adenoma. J Natl Cancer Inst 104(20):1562–1575PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Wu K, Platz EA, Willett WC, Fuchs CS, Selhub J, Rosner BA, Hunter DJ, Giovannucci E (2009) A randomized trial on folic acid supplementation and risk of recurrent colorectal adenoma. Am J Clin Nutr 90(6):1623–1631PubMedCentralPubMedCrossRefGoogle Scholar
  61. 61.
    Qin X, Cui Y, Shen L, Sun N, Zhang Y, Li J, Xu X, Wang B, Xu X, Huo Y, Wang X (2013) Folic acid supplementation and cancer risk: a meta-analysis of randomized controlled trials. Int J Cancer 133(5):1033–1041PubMedCrossRefGoogle Scholar
  62. 62.
    Figueiredo JC, Mott LA, Giovannucci E, Wu K, Cole B, Grainge MJ, Logan RF, Baron JA (2011) Folic acid and prevention of colorectal adenomas: a combined analysis of randomized clinical trials. Int J Cancer 129(1):192–203PubMedCentralPubMedCrossRefGoogle Scholar
  63. 63.
    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 Biomark Prev 14(3):740–743CrossRefGoogle Scholar
  64. 64.
    Heine-Bröring RC, Winkels RM, Botma A, van Duijnhoven FJ, Jung AY, Kleibeuker JH, Nagengast FM, Vasen HF, Kampman E (2013) Dietary supplement use and colorectal adenoma risk in individuals with Lynch syndrome: the GEOLynch Cohort Study. PLoS One 8(6):e66819PubMedCentralPubMedCrossRefGoogle Scholar
  65. 65.
    Winawer SJ, Fletcher RH, Miller L, Godlee F, Stolar MH, Mulrow CD, Woolf SH, Glick SN, Ganiats TG, Bond JH, Rosen L, Zapka JG, Olsen SJ, Giardiello FM, Sisk JE, Van Antwerp R, Brown-Davis C, Marciniak DA, Mayer RJ (1997) Colorectal cancer screening: clinical guidelines and rationale. Gastroenterology 112(2):594–642PubMedCrossRefGoogle Scholar
  66. 66.
    Cole BF, Baron JA, Sandler RS, Haile RW, Ahnen DJ, Bresalier RS, McKeown-Eyssen G, Summers RW, Rothstein RI, Burke CA, Snover DC, Church TR, Allen JI, Robertson DJ, Beck GJ, Bond JH, Byers T, Mandel JS, Mott LA, Pearson LH, Barry EL, Rees JR, Marcon N, Saibil F, Ueland PM, Greenberg ER (2007) Folic acid for the prevention of colorectal adenomas: a randomized clinical trial. JAMA 297(21):2351–2359PubMedCrossRefGoogle Scholar
  67. 67.
    Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR, Thibodeau SN, Vogelstein B, Kinzler KW (1992) APC mutations occur early during colorectal tumorigenesis. Nature 359(6392):235–237PubMedCrossRefGoogle Scholar
  68. 68.
    Konishi M, Kikuchi-Yanoshita R, Tanaka K, Muraoka M, Onda A, Okumura Y, Kishi N, Iwama T, Mori T, Koike M, Ushio K, Chiba M, Nomizu S, Konishi F, Utsunomiya J, Miyaki M (1996) Molecular nature of colon tumors in hereditary nonpolyposis colon cancer, familial polyposis, and sporadic colon cancer. Gastroenterology 111(2):307–317PubMedCrossRefGoogle Scholar
  69. 69.
    Frosst P, Blom HJ, Milos R, Goyette P, Sheppard CA, Matthews RG, Boers GJ, den Heijer M, Kluijtmans LA, van den Heuvel LP (1995) A candidate genetic risk factor for vascular disease: a common mutation in methylenetetrahydrofolate reductase. Nat Genet 10(1):111–113PubMedCrossRefGoogle Scholar
  70. 70.
    Guerreiro CS, Carmona B, Goncalves S, Carolino E, Fidalgo P, Brito M, Leitao CN, Cravo M (2008) Risk of colorectal cancer associated with the C677T polymorphism in 5,10-methylenetetrahydrofolate reductase in Portuguese patients depends on the intake of methyl-donor nutrients. Am J Clin Nutr 88(5):1413–1418PubMedGoogle Scholar
  71. 71.
    Martinez ME, Thompson P, Jacobs ET, Giovannucci E, Jiang R, Klimecki W, Alberts DS (2006) Dietary factors and biomarkers involved in the methylenetetrahydrofolate reductase genotype—colorectal adenoma pathway. Gastroenterology 131(6):1706–1716PubMedCrossRefGoogle Scholar
  72. 72.
    Slattery ML, Potter JD, Samowitz W, Schaffer D, Leppert M (1999) Methylenetetrahydrofolate reductase, diet, and risk of colon cancer. Cancer Epidemiol Biomark Prev 8(6):513–518Google Scholar
  73. 73.
    Ma J, Stampfer MJ, Giovannucci E, Artigas C, Hunter DJ, Fuchs C, Willett WC, Selhub J, Hennekens CH, Rozen R (1997) Methylenetetrahydrofolate reductase polymorphism, dietary interactions, and risk of colorectal cancer. Cancer Res 57(6):1098–1102PubMedGoogle Scholar
  74. 74.
    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):239–248PubMedCrossRefGoogle Scholar
  75. 75.
    Kim J, Cho YA, Kim DH, Lee BH, Hwang DY, Jeong J, Lee HJ, Matsuo K, Tajima K, Ahn YO (2012) Dietary intake of folate and alcohol, MTHFR C677T polymorphism, and colorectal cancer risk in Korea. Am J Clin Nutr 95(2):405–412PubMedCrossRefGoogle Scholar
  76. 76.
    Lee JE, Wei EK, Fuchs CS, Hunter DJ, Lee IM, Selhub J, Stampfer MJ, Willett WC, Ma J, Giovannucci E (2012) Plasma folate, methylenetetrahydrofolate reductase (MTHFR), and colorectal cancer risk in three large nested case–control studies. Cancer Causes Control 23(4):537–545PubMedCentralPubMedCrossRefGoogle Scholar
  77. 77.
    Mason JB, Choi SW (2005) Effects of alcohol on folate metabolism: implications for carcinogenesis. Alcohol 35(3):235–241PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Audrey Y. Jung
    • 1
  • Fränzel J. B. van Duijnhoven
    • 2
    • 7
  • Fokko M. Nagengast
    • 3
  • Akke Botma
    • 2
  • Renate C. Heine-Bröring
    • 2
  • Jan H. Kleibeuker
    • 4
  • Hans F. A. Vasen
    • 5
  • Jan L. Harryvan
    • 2
  • Renate M. Winkels
    • 2
  • Ellen Kampman
    • 1
    • 2
    • 6
  1. 1.Department for Health EvidenceRadboud University Medical CenterNijmegenNetherlands
  2. 2.Division of Human NutritionWageningen UniversityWageningenNetherlands
  3. 3.Department of GastroenterologyRadboud University Medical CenterNijmegenNetherlands
  4. 4.Department of Gastroenterology and HepatologyUniversity Medical Center GroningenGroningenNetherlands
  5. 5.Netherlands Foundation for the Detection of Hereditary TumorsLeidenNetherlands
  6. 6.Department for Health SciencesVU University Medical CenterAmsterdamNetherlands
  7. 7.National Institute for Public Health and the Environment (RIVM)BilthovenNetherlands

Personalised recommendations