Interaction of estrogen therapy with calcium and vitamin D supplementation on colorectal cancer risk: Reanalysis of Women's Health Initiative randomized trial

International Journal of Cancer

Volumn 122, Issue 8, 2008, Pages 1690-1694

  Ding, Eric L ^a,b   Mehta, Saurabh ^a   Fawzi, Wafaie W ^a   Giovannucci, Edward L ^a,b  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Calcitriol; Calcium; Cholecalciferol; Colorectal cancer; Epidemiology; Estrogen; Megalin; Randomized trial; Vitamin D; Women

Indexed keywords

CALBINDIN; CALCIUM; COLECALCIFEROL; ESTROGEN; GESTAGEN; MEGALIN; PLACEBO; CALCIUM CARBONATE;

ARTICLE; CANCER RISK; CLINICAL TRIAL; COLORECTAL CANCER; CONFIDENCE INTERVAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOSE RESPONSE; DOUBLE BLIND PROCEDURE; ESTROGEN THERAPY; FEMALE; HAZARD RATIO; HUMAN; MAJOR CLINICAL STUDY; POSTMENOPAUSE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; VITAMIN SUPPLEMENTATION; WOMEN'S HEALTH; AGED; COLORECTAL TUMOR; DIET SUPPLEMENTATION; DRUG ANTAGONISM; METHODOLOGY; MIDDLE AGED; RISK; RISK ASSESSMENT;

AGED; CALCIUM; CALCIUM CARBONATE; CHOLECALCIFEROL; COLORECTAL NEOPLASMS; DIETARY SUPPLEMENTS; DRUG ANTAGONISM; ESTROGEN REPLACEMENT THERAPY; FEMALE; HUMANS; MIDDLE AGED; ODDS RATIO; POSTMENOPAUSE; RESEARCH DESIGN; RISK ASSESSMENT; WOMEN'S HEALTH;

EID: 40349084012     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23311     Document Type: Article

References (56)

1. Garland CF, Garland FC. Do sunlight and vitamin D reduce the likelihood of colon cancer? Int J Epidemiol 1980;9:227-31.
2. Garland CF, Garland FC, Gorham ED, Lipkin M, Newmark H, Mohr SB, Holick MF. The role of vitamin D in cancer prevention. Am J Public Health 2006;96:252-61.
3. Lamprecht SA, Lipkin M. Chemoprevention of colon cancer by calcium, vitamin D and folate: molecular mechanisms. Nat Rev Cancer 2003;3:601-14.
4. Giovannucci E, Liu Y, Rimm EB, Hollis BW, Fuchs CS, Stampfer MJ, Willett WC. Prospective study of predictors of vitamin D status and cancer incidence and mortality in men. J Natl Cancer Inst 2006;98:451-9.
5. 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.
6. 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.
7. Oh K, Willett WC, Wu K, Fuchs CS, Giovannucci EL. Calcium and vitamin D intakes in relation to risk of distal colorectal adenoma in women. Am J Epidemiol 2007;165:1178-86.
8. Gorham ED, Garland CF, Garland FC, Grant WB, Mohr SB, Lipkin M, Newmark HL, Giovannucci E, Wei M, Holick MF. Optimal vitamin D status for colorectal cancer prevention: a quantitative meta analysis. Am J Prev Med 2007;32:210-16.
9. Autier P, Gandini S. Vitamin D supplementation and total mortality: a meta-analysis of randomized controlled trials. Arch Intern Med 2007;167:1730-7.
10. Trivedi DP, Doll R, Khaw KT. Effect of four monthly oral vitamin D3 (cholecalciferol) supplementation on fractures and mortality in men and women living in the community: randomised double blind controlled trial. BMJ 2003;326:469.
11. Lappe JM, Travers-Gustafson D, Davies KM, Recker RR, Heaney RP. Vitamin D and calcium supplementation reduces cancer risk: results of a randomized trial. Am J Clin Nutr 2007;85:1586-91.
12. Cho E, Smith-Warner SA, Spiegelman D, Beeson WL, van den Brandt PA, Colditz GA, Folsom AR, Fraser GE, Freudenheim JL, Giovannucci E, Goldbohm RA, Graham S, et al. Dairy foods, calcium, and colorectal cancer: a pooled analysis of 10 cohort studies. J Natl Cancer Inst 2004;96:1015-22.
13. Wu K, Willett WC, Fuchs CS, Colditz GA, Giovannucci EL. Calcium intake and risk of colon cancer in women and men. J Natl Cancer Inst 2002;94:437-46.
14. Baron JA, Beach M, Mandel JS, van Stolk RU, Haile RW, Sandler RS, Rothstein R, Summers RW, Snover DC, Beck GJ, Bond JH, Greenberg ER. Calcium supplements for the prevention of colorectal adenomas. Calcium Polyp Prevention Study Group. N Engl J Med 1999;340:101-7.
15. 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.
16. Grau MV, Baron JA, Sandler RS, Wallace K, Haile RW, Church TR, Beck GJ, Summers RW, Barry EL, Cole BF, Snover DC, Rothstein R, et al. Prolonged effect of calcium supplementation on risk of colorectal adenomas in a randomized trial. J Natl Cancer Inst 2007;99:129-36.
17. Bonithon-Kopp C, Kronborg O, Giacosa A, Rath U, Faivre J. Calcium and fibre supplementation in prevention of colorectal adenoma recurrence: a randomised intervention trial. European Cancer Prevention Organisation Study Group. Lancet 2000;356:1300-6.
18. Wactawski-Wende J, Kotchen JM, Anderson GL, Assaf AR, Brunner RL, O'Sullivan MJ, Margolis KL, Ockene JK, Phillips L, Pottem 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.
19. Holick MF, Giovannucci E, Wactawski-Wende J, Anderson GL, O'Sullivan M. Calcium plus vitamin D and the risk of colorectal cancer. N Engl J Med 2006;354:2287-8. http://www.ncbi.nlm.nih.gov/sites/entrez?Db=pubmed&Cmd= ShowDetailView&TermToSearch=16729368
20. Forman MR, Levin B. Calcium plus vitamin D3 supplementation and colorectal cancer in women. N Engl J Med 2006;354:752-4.
21. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-88.
22. Egger M, Altman DG, Smith GD. Systematic reviews in health care: meta-analysis in context, 2nd ed. London, UK: BMJ Books, 2001.
23. Choi KC, Leung PC, Jeung EB. Biology and physiology of Calbindin-D9k in female reproductive tissues: involvement of steroids and endocrine disruptors. Reprod Biol Endocrinol 2005;3:66.
24. Gill RK, Christakos S. Regulation by estrogen through the 5′-flanking region of the mouse calbindin-D28k gene. Mol Endocrinol 1995;9:319-26.
25. Nguyen TH, Lee GS, Ji YK, Choi KC, Lee CK, Jeung EB. A calcium binding protein, calbindin-D9k, is mainly regulated by estrogen in the pituitary gland of rats during estrous cycle. Brain Res Mol Brain Res 2005;141:166-73.
26. Gagnon A, Welsh J. Modulation and phosphorylation of calbindin-D28K correlates with protein kinase C activation1. Biochem Cell Biol 1997;75:33-40.
27. Song Y, Kato S, Fleet JC. Vitamin D receptor (VDR) knockout mice reveal VDR-independent regulation of intestinal calcium absorption and ECaC2 and calbindin D9k mRNA. J Nutr 2003;133:374-80.
28. Mathiasen IS, Sergeev IN, Bastholm L, Elling F, Norman AW, Jaattela M. Calcium and calpain as key mediators of apoptosis-like death induced by vitamin D compounds in breast cancer cells. J Biol Chem 2002;277:30738-45.
29. Wernyj RP, Mattson MP, Christakos S. Expression of calbindin-D28k in C6 glial cells stabilizes intracellular calcium levels and protects against apoptosis induced by calcium ionophore and amyloid β-peptide. Brain Res Mol Brain Res 1999;64:69-79.
30. Tombal B, Denmeade SR, Gillis JM, Isaacs JT. A supramicromolar elevation of intracellular free calcium ([Ca(2+)](i)) is consistently required to induce the execution phase of apoptosis. Cell Death Differ 2002;9:561-73.
31. Turner PR, Mefford S, Christakos S, Nissenson RA. Apoptosis mediated by activation of the G protein-coupled receptor for PTH/PTHrP in UMR106 osteoblastic cells. Am J Physiol Endocrinol Metab 2000;281:E162-E70.
32. Paoni NF, Feldman MW, Gutierrez LS, Ploplis VA, Castellino FJ. Transcriptional profiling of the transition from normal intestinal epithelia to adenomas and carcinomas in the APCMin/+ mouse. Physiol Genomics 2003;15:228-35.
33. Choi WS, Chun SY, Markelonis GJ, Oh TH, Oh YJ. Overexpression of calbindin-D28K induces neunte outgrowth in dopaminergic neuronal cells via activation of p38 MAPK. Biochem Biophys Res Commun 2001;287:656-61.
34. Reddy D, Pollock AS, Clark SA, Sooy K, Vasavada RC, Stewart AF, Honeyman T, Christakos S. Transfection and overexpression of the calcium binding protein calbindin-D28k results in a stimulatory effect on insulin synthesis in a rat beta cell line (RIN 1046-38). Proc Natl Acad Sci USA 1997;94:1961-6.
35. Wei EK, Ma J, Pollak MN, Rifai N, Fuchs CS, Hankinson SE, Giovannucci E. C-peptide, insulin-like growth factor binding protein-1, glycosylated hemoglobin, and the risk of distal colorectal adenoma in women. Cancer Epidemiol Biomarkers Prev 2006;15:750-5.
36. Ma J, Giovannucci E, Pollak M, Leavitt A, Tao Y, Gaziano JM, Stampfer MJ. A prospective study of plasma C-peptide and colorectal cancer risk in men. J Natl Cancer Inst 2004;96:546-53.
37. Giovannucci E. Insulin, insulin-like growth factors and colon cancer: a review of the evidence. J Nutr 2001;131:3109S-3120S.
38. Lointier P, Wargovich MJ, Saez S, Levin B, Wildrick DM, Boman BM. The role of vitamin D3 in the proliferation of a human colon cancer cell line in vitro. Anticancer Res 1987;7:817-21.
39. Boonen S, Lips P, Bouillon R, Bischoff-Ferrari HA, Vanderschueren D, Haentjens P. Need for additional calcium to reduce the risk of hip fracture with vitamin D supplementation: evidence from a comparative meta-analysis of randomized controlled trials. J Clin Endocrinol Metab http://jcem.endojournals. org/cgi/content/abstract/92/4/1415
40. Spelsberg TC, Subramaniam M, Riggs BL, Khosla S. The actions and interactions of sex steroids and growth factors/cytokines on the skeleton. Mol Endocrinol 1999;13:819-28.
41. Jackson RD, LaCroix AZ, Gass M, Wallace RB, Robbins J, Lewis CE, Bassford T, Beresford SA, Black HR, Blanchette P, Bonds DE, Brunner RL, et al. Calcium plus vitamin D supplementation and the risk of fractures. N Engl J Med 2006;354:669-83.
42. Hamano T, Fujii N, Ito T, Imai E, Mikami S, Katayama M, Obi Y. Low dose estrogen replacement therapy (ERT) for postmenopausal hemodialysis (HD) patients. Clin Calcium 2005;15 (Suppl 1):161-6.
43. Nykjaer A, Dragun D, Walther D, Vorum H, Jacobsen C, Herz J, Melsen F, Christensen EI, Willnow TE. An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3. Cell 1999;96:507-15.
44. Hammes A, Andreassen TK, Spoelgen R, Raila J, Hubner N, Schulz H, Metzger J, Schweigert FJ, Luppa PB, Nykjaer A, Willnow TE. Role of endocytosis in cellular uptake of sex steroids. Cell 2005;122:751-62.
45. Moestrup SK, Verroust PJ. Megalin- and cubilin-mediated endocytosis of protein-bound vitamins, lipids, and hormones in polarized epithelia. Annu Rev Nutr 2001;21:407-28.
46. Mendel CM. The free hormone hypothesis: a physiologically based mathematical model. Endocr Rev 1989;10:232-74.
47. Rosner W, Hryb DJ, Khan MS, Nakhla AM, Romas NA. Sex hormone-binding globulin mediates steroid hormone signal transduction at the plasma membrane. J Steroid Biochem Mol Biol 1999;69:481-5.
48. Porto CS, Lazari MF, Abreu LC, Bardin CW, Gunsalus GL. Receptors for androgen-binding proteins: internalization and intracellular signalling. J Steroid Biochem Mol Biol 1995;53:561-5.
49. Christensen EI, Birn H. Megalin and cubilin: multifunctional endocytic receptors. Nat Rev Mol Cell Biol 2002;3:256-66.
50. Christensen EI, Gliemann J, Moestrup SK. Renal tubule gp330 is a calcium binding receptor for endocytic uptake of protein. J Histochem Cytochem 1992;40:1481-90.
51. Christensen EI, Moskaug JO, Vorum H, Jacobsen C, Gundersen TE, Nykjaer A, Blomhoff R, Willnow TE, Moestrup SK. Evidence for an essential role of megalin in transepithelial transport of retinol. J Am Soc Nephrol 1999;10:685-95.
52. Verroust PJ, Christensen EI. Megalin and cubilin-the story of two multipurpose receptors unfolds. Nephrol Dial Transplant 2002;17:1867-71.
53. Pelc K, Vincent S, Ruchoux MM, Kiss R, Pochet R, Sariban E, Decaestecker C, Heizmann CW. Calbindin-d(28k): a marker of recurrence for medulloblastomas. Cancer 2002;95:410-19.
54. Kampman E, Giovannucci E, van 't Veer P, Rimm E, Stampfer MJ, Colditz GA, Kok FJ, Willett WC. Calcium, vitamin D, dairy foods, and the occurrence of colorectal adenomas among men and women in two prospective studies. Am J Epidemiol 1994;139:16-29.
55. 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.
56. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321-33.