Epidemiology

You have full text access to this OnlineOpen article

Modification of the inverse association between dietary vitamin D intake and colorectal cancer risk by a FokI variant supports a chemoprotective action of Vitamin D intake mediated through VDR binding

  1. Evropi Theodoratou1,†,*,
  2. Susan M. Farrington2,
  3. Albert Tenesa2,
  4. Geraldine McNeill3,
  5. Roseanne Cetnarskyj4,
  6. Rebecca A. Barnetson2,
  7. Mary E. Porteous5,
  8. Malcolm G. Dunlop2,
  9. Harry Campbell1,2

Article first published online: 15 AUG 2008

DOI: 10.1002/ijc.23769

Issue

International Journal of Cancer

International Journal of Cancer

Volume 123, Issue 9, pages 2170–2179, 1 November 2008

Additional Information

How to Cite

Theodoratou, E., Farrington, S. M., Tenesa, A., McNeill, G., Cetnarskyj, R., Barnetson, R. A., Porteous, M. E., Dunlop, M. G. and Campbell, H. (2008), Modification of the inverse association between dietary vitamin D intake and colorectal cancer risk by a FokI variant supports a chemoprotective action of Vitamin D intake mediated through VDR binding. Int. J. Cancer, 123: 2170–2179. doi: 10.1002/ijc.23769

Author Information

  1. 1

    Public Health Sciences, University of Edinburgh, Teviot Place, Edinburgh, United Kingdom

  2. 2

    Colon Cancer Genetics Group, Western General Hospital, University of Edinburgh, Crewe Road, Edinburgh, United Kingdom

  3. 3

    Environmental and Occupational Medicine Department, University of Aberdeen, Liberty Safe Work Research Centre, Aberdeen, United Kingdom

  4. 4

    School of Nursing, Midwifery and Social Care, Faculty of Health, Life and Social Sciences, Napier University, Edinburgh, United Kingdom

  5. 5

    South East Scotland Genetic Service, Western General Hospital, Edinburgh, United Kingdom

  1. †

    Fax: +0131-650-6909.

*Public Health Sciences, College of Medicine and Vet Medicine, University of Edinburgh, United Kingdom

Publication History

  1. Issue published online: 25 AUG 2008
  2. Article first published online: 15 AUG 2008
  3. Manuscript Accepted: 19 MAY 2008
  4. Manuscript Received: 1 FEB 2008

Funded by

  • Cancer Research UK. Grant Number: C348/A3758
  • Medical Research Council. Grant Number: G0000657-53203
  • Scottish Executive Chief Scientist's Office. Grant Number: K/OPR/2/2/D333
  • CORE
  • Greek State Scholarship Foundation

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (155K)

References

  • 1
    Jimenez-Lara AM. Colorectal cancer: potential therapeutic benefits of Vitamin D. Int J Biochem Cell Biol 2007; 39: 672–7.
  • 2
    Burleigh E,Potter J. Vitamin D deficiency in outpatients: a Scottish perspective. Scott Med J 2006; 51: 27–31.
  • 3
    Park SY,Murphy SP,Wilkens LR,Nomura AM,Henderson BE,Kolonel LN. Calcium and vitamin D intake and risk of colorectal cancer: the Multiethnic Cohort Study. Am J Epidemiol 2007; 165: 784–931.
  • 4
    Gross MD. Vitamin D and calcium in the prevention of prostate and colon cancer: new approaches for the identification of needs. J Nutr 2005; 135: 326–31.
  • 5
    Slattery ML,Samowitz W,Hoffman M,Ma KN,Levin TR,Neuhausen S. Aspirin. NSAIDs, and colorectal cancer: possible involvement in an insulin-related pathway. Cancer Epidemiol Biomarkers Prev 2004; 13: 538–45.
  • 6
    Uitterlinden AG,Fang Y,Van Meurs JB,Pols HA,Van Leeuwen JP. Genetics and biology of vitamin D receptor polymorphisms. Gene 2004; 338: 143–56.
  • 7
    Gong YL,Xie DW,Deng ZL,Bostick RM,Miao XJ,Zhang JH,Gong ZH. Vitamin D receptor gene Tru9I polymorphism and risk for incidental sporadic colorectal adenomas. World J Gastroenterol 2005; 11: 4794–9.
  • 8
    Slattery ML,Sweeney C,Murtaugh M,Ma KN,Caan BJ,Potter JD,Wolff R. Associations between vitamin D, vitamin D receptor gene and the androgen receptor gene with colon and rectal cancer. Int J Cancer 2006; 118: 3140–6.
    Direct Link:
  • 9
    Benito E,Stiggelbout A,Bosch FX,Obrador A,Kaldor J,Mulet M,Munoz N. Nutritional factors in colorectal cancer risk: a case-control study in Majorca. Int J Cancer 1991; 49: 161–7.
    Direct Link:
  • 10
    Boutron MC,Faivre J,Marteau P,Couillault C,Senesse P,Quipourt V. Calcium, phosphorus, vitamin D, dairy products and colorectal carcinogenesis: a French case–control study. Br J Cancer 1996; 74: 145–51.
  • 11
    Ferraroni M,La VC,D'Avanzo B,Negri E,Franceschi S,Decarli A. Selected micronutrient intake and the risk of colorectal cancer. Br J Cancer 1994; 70: 1150–5.
  • 12
    Kampman E,Slattery ML,Caan B,Potter JD. Calcium, vitamin D, sunshine exposure, dairy products and colon cancer risk (United States). Cancer Causes Control 2000; 11: 459–66.
  • 13
    La Vecchia C,Braga C,Negri E,Franceschi S,Russo A,Conti E,Falcini F,Giacosa A,Montella M,Decarli A. Intake of selected micronutrients and risk of colorectal cancer. Int J Cancer 1997; 73: 525–30.
    Direct Link:
  • 14
    Levi F,Pasche C,Lucchini F,La VC. Selected micronutrients and colorectal cancer: a case-control study from the canton of Vaud, Switzerland. Eur J Cancer 2000; 36: 2115–19.
  • 15
    Marcus PM,Newcomb PA. The association of calcium and vitamin D, and colon and rectal cancer in Wisconsin women. Int J Epidemiol 1998; 27: 788–93.
  • 16
    Peters RK,Pike MC,Garabrant D,Mack TM. Diet and colon cancer in Los Angeles County, California. Cancer Causes Control 1992; 3: 457–73.
  • 17
    Pritchard RS,Baron JA,Gerhardsson de Verdier M. Dietary calcium, vitamin D, and the risk of colorectal cancer in Stockholm, Sweden. Cancer Epidemiol Biomarkers Prev 1996; 5: 897–900.
  • 18
    Slattery ML,Neuhausen SL,Hoffman M,Caan B,Curtin K,Ma KN,Samowitz W. Dietary calcium, vitamin D. VDR genotypes and colorectal cancer. Int J Cancer 2004; 111: 750–6.
    Direct Link:
  • 19
    Zheng W,Anderson KE,Kushi LH,Sellers TA,Greenstein J,Hong CP,Cerhan JR,Bostick RM,Folsom AR. A prospective cohort study of intake of calcium, vitamin D, and other micronutrients in relation to incidence of rectal cancer among postmenopausal women. Cancer Epidemiol Biomarkers Prev 1998; 7: 221–5.
  • 20
    Terry P,Baron JA,Bergkvist L,Holmberg L,Wolk A. Dietary calcium and vitamin D intake and risk of colorectal cancer: a prospective cohort study in women. Nutr Cancer 2002; 43: 39–46.
  • 21
    Pietinen P,Malila N,Virtanen M,Hartman TJ,Tangrea JA,Albanes D,Virtamo J. Diet and risk of colorectal cancer in a cohort of Finnish men. Cancer Causes Control 1999; 10: 387–96.
  • 22
    McCullough ML,Robertson AS,Rodriguez C,Jacobs EJ,Chao A,Carolyn J,Calle EE,Willett WC,Thun MJ. Calcium, vitamin D, dairy products, and risk of colorectal cancer in the Cancer Prevention Study II Nutrition Cohort (United States). Cancer Causes Control 2003; 14: 1–12.
  • 23
    Martinez ME,Giovannucci EL,Colditz GA,Stampfer MJ,Hunter DJ,Speizer FE,Wing A,Willett WC. Calcium, vitamin D, and the occurrence of colorectal cancer among women. J Natl Cancer Inst 1996; 88: 1375–82.
  • 24
    Lin J,Zhang SM,Cook NR,Manson JE,Lee IM,Buring JE. Intakes of calcium and vitamin D and risk of colorectal cancer in women. Am J Epidemiol 2005; 161: 755–64.
  • 25
    Kesse E,Boutron-Ruault MC,Norat T,Riboli E,Clavel-Chapelon F. Dietary calcium, phosphorus, vitamin D, dairy products and the risk of colorectal adenoma and cancer among French women of the E3N-EPIC prospective study. Int J Cancer 2005; 117: 137–44.
    Direct Link:
  • 26
    Kearney J,Giovannucci E,Rimm EB,Ascherio A,Stampfer MJ,Colditz GA,Wing A,Kampman E,Willett WC. Calcium, vitamin D, and dairy foods and the occurrence of colon cancer in men. Am J Epidemiol 1996; 143: 907–17.
  • 27
    Jarvinen R,Knekt P,Hakulinen T,Aromaa A. Prospective study on milk products, calcium and cancers of the colon and rectum. Eur J Clin Nutr 2001; 55: 1000–7.
  • 28
    Heilbrun LK,Nomura A,Hankin JH,Stemmermann GN. Dietary vitamin D and calcium and risk of colorectal cancer. Lancet 1985; 1: 925.
  • 29
    Garland C,Shekelle RB,Barrett-Connor E,Criqui MH,Rossof AH,Paul O. Dietary vitamin D and calcium and risk of colorectal cancer: a 19-year prospective study in men. Lancet 1985; 1: 307–9.
  • 30
    Bostick RM,Potter JD,Sellers TA,McKenzie DR,Kushi LH,Folsom AR. Relation of calcium, vitamin D, and dairy food intake to incidence of colon cancer among older women. The Iowa Women's Health Study. Am J Epidemiol 1993; 137: 1302–17.
  • 31
    Wactawski-Wende J,Kotchen JM,Anderson GL,Assaf AR,Brunner RL,O'Sullivan MJ,Margolis KL,Ockene JK,Phillips L,Pottern L,Prentice RL,Robbins J, et al. Calcium plus vitamin D supplementation and the risk of colorectal cancer. N Engl J Med 2006; 354: 684–96.
  • 32
    Braun MM,Helzlsouer KJ,Hollis BW,Comstock GW. Colon cancer and serum vitamin D metabolite levels 10–17 years prior to diagnosis. Am J Epidemiol 1995; 142: 608–11.
  • 33
    Feskanich D,Ma J,Fuchs CS,Kirkner GJ,Hankinson SE,Hollis BW,Giovannucci EL. Plasma vitamin D metabolites and risk of colorectal cancer in women. Cancer Epidemiol Biomarkers Prev 2004; 13: 1502–8.
  • 34
    Garland CF,Comstock GW,Garland FC,Helsing KJ,Shaw EK,Gorham ED. Serum 25-hydroxyvitamin D and colon cancer: eight-year prospective study. Lancet 1989; 2: 1176–8.
  • 35
    Otani T,Iwasaki M,Sasazuki S,Inoue M,Tsugane S. Plasma vitamin D and risk of colorectal cancer: the Japan Public Health Center-Based Prospective Study. Br J Cancer 2007; 97: 446–51.
  • 36
    Tangrea J,Helzlsouer K,Pietinen P,Taylor P,Hollis B,Virtamo J,Albanes D. Serum levels of vitamin D metabolites and the subsequent risk of colon and rectal cancer in Finnish men. Cancer Causes Control 1997; 8: 615–25.
  • 37
    Wu K,Feskanich D,Fuchs CS,Willett WC,Hollis BW,Giovannucci EL. A nested case control study of plasma 25-hydroxyvitamin D concentrations and risk of colorectal cancer. J Natl Cancer Inst 2007; 99: 1120–9.
  • 38
    Yaylim-Eraltan I,Arzu EH,Arikan S,Okay E,Ozturk O,Bayrak S,Isbir T. Investigation of the VDR gene polymorphisms association with susceptibility to colorectal cancer. Cell Biochem Funct 2007; 25: 731–7.
    Direct Link:
  • 39
    Wong HL,Seow A,Arakawa K,Lee HP,Yu MC,Ingles SA. Vitamin D receptor start codon polymorphism and colorectal cancer risk: effect modification by dietary calcium and fat in Singapore Chinese. Carcinogenesis 2003; 24: 1091–5.
  • 40
    Sweeney C,Curtin K,Murtaugh MA,Caan BJ,Potter JD,Slattery ML. Haplotype analysis of common vitamin D receptor variants and colon and rectal cancers. Cancer Epidemiol Biomarkers Prev 2006; 15: 744–9.
  • 41
    Slattery ML,Yakumo K,Hoffman M,Neuhausen S. Variants of the VDR gene and risk of colon cancer (United States). Cancer Causes Control 2001; 12: 359–64.
  • 42
    Park K,Woo M,Nam J,Kim JC. Start codon polymorphisms in the vitamin D receptor and colorectal cancer risk. Cancer Lett 2006; 237: 199–206.
  • 43
    Murtaugh MA,Sweeney C,Ma KN,Potter JD,Caan BJ,Wolff RK,Slattery ML. Vitamin D receptor gene polymorphisms, dietary promotion of insulin resistance, and colon and rectal cancer. Nutr Cancer 2006; 55: 35–43.
  • 44
    Kadiyska T,Yakulov T,Kaneva R,Nedin D,Alexandrova A,Gegova A,Savov A,Mitev V,Kremensky I. Vitamin D and estrogen receptor gene polymorphisms and the risk of colorectal cancer in Bulgaria. Int J Colorectal Dis 2007; 22: 395–400.
  • 45
    Boyapati SM,Bostick RM,McGlynn KA,Fina MF,Roufail WM,Geisinger KR,Wargovich M,Coker A,Hebert JR. Calcium, vitamin D, and risk for colorectal adenoma: dependency on vitamin D receptor BsmI polymorphism and nonsteroidal anti-inflammatory drug use? Cancer Epidemiol Biomarkers Prev 2003; 12: 631–7.
  • 46
    Grau MV,Baron JA,Sandler RS,Haile RW,Beach ML,Church TR,Heber D. Vitamin D, calcium supplementation, and colorectal adenomas: results of a randomized trial. J Natl Cancer Inst 2003; 95: 1765–71.
  • 47
    Ingles SA,Wang J,Coetzee GA,Lee ER,Frankl HD,Haile RW. Vitamin D receptor polymorphisms and risk of colorectal adenomas (United States). Cancer Causes Control 2001; 12: 607–14.
  • 48
    Kim HS,Newcomb PA,Ulrich CM,Keener CL,Bigler J,Farin FM,Bostick RM,Potter JD. Vitamin D receptor polymorphism and the risk of colorectal adenomas: evidence of interaction with dietary vitaminD and calcium. Cancer Epidemiol Biomarkers Prev 2001; 10: 869–74.
  • 49
    Peters U,Hayes RB,Chatterjee N,Shao W,Schoen RE,Pinsky P,Hollis BW,McGlynn KA. Circulating vitamin D metabolites, polymorphism in vitamin D receptor, and colorectal adenoma risk. Cancer Epidemiol Biomarkers Prev 2004; 13: 546–52.
  • 50
    Peters U,McGlynn KA,Chatterjee N,Gunter E,Garcia-Closas M,Rothman N,Sinha R. Vitamin D, calcium, and vitamin D receptor polymorphism in colorectal adenomas. Cancer Epidemiol Biomarkers Prev 2001; 10: 1267–74.
  • 51
    Theodoratou E,Kyle J,Cetnarskyj R,Farrington SM,Tenesa A,Barnetson R,Porteous M,Dunlop M,Campbell H. Dietary flavonoids and the risk of colorectal cancer. Cancer Epidemiol Biomarkers Prev 2007; 16: 684–93.
  • 52
    Masson LF,McNeill G,Tomany JO,Simpson JA,Peace HS,Wei L,Grubb DA,Bolton-Smith C. Statistical approaches for assessing the relative validity of a food-frequency questionnaire: use of correlation coefficients and the kappa statistic. Public Health Nutr 2003; 6: 313–21.
  • 53
    Carstairs V,Russel M. Deprivation and health in Scotland. Aberdeen: Aberdeen University Press, 1991.
  • 54
    Willett W,Stampfer MJ. Total energy intake: implications for epidemiologic analyses. Am J Epidemiol 1986; 124: 17–27.
  • 55
    Willett W,Stampfer MJ. Implications of total energy intake for epidemiologic analysis. In: WillettWC, ed. Nutritional epidemiology,2nd edn. New York: Oxford University Press, 1998. 273–301.
  • 56
    Khoury MJ,Flanders WD. Nontraditional epidemiologic approaches in the analysis of gene-environment interaction: case-control studies with no controls! Am J Epidemiol 1996; 144: 207–13.
  • 57
    Kyle J,Masson LF,Grubb DA,Duthie GG,McNeill G. Estimating dietary flavonoid intake: comparison of a semi-quantitative food frequency questionnaire with 4-day weighed diet records in a Scottissh population. Proc Nutr Soc 2002; 61: 69A.
  • 58
    Bolton-Smith C,Smith WC,Woodward M,Tunstall-Pedoe H. Nutrient intakes of different social-class groups: results from the Scottish Heart Health Study (SHHS). Br J Nutr 1991; 65: 321–35.
  • 59
    Hollis BW. Circulating 25-hydroxyvitamin D levels indicative of vitamin D sufficiency: implications for establishing a new effective dietary intake recommendation for vitamin D. J Nutr 2005; 135: 317–22.
View Full Article with Supporting Information (HTML) Get PDF (155K)