Relation of calcium, vitamin d, and dairy food intake to incidence of colon cancer among older women: The iowa women's health study

American Journal of Epidemiology

Volumn 137, Issue 12, 1993, Pages 1302-1317

  Bostick, Roberd M ^a,b   Potter, John D ^b   Sellers, Thomas A ^b   Mckenzie, David R ^b   Kushi, Lawrence H ^b   Folsom, Aaron R ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Calcium, dietary; Colonic neoplasms; Dairy products; Prospective studies; Vitamin D

Indexed keywords

CALCIUM; VITAMIN;

ADULT; AGED; ARTICLE; CALCIUM INTAKE; CANCER INCIDENCE; CANCER PREVENTION; CANCER RISK; COLON CANCER; DAIRY PRODUCT; DIETARY INTAKE; FEMALE; HUMAN; MAJOR CLINICAL STUDY; MULTIVARIATE ANALYSIS; PRIORITY JOURNAL; UNITED STATES; VITAMIN INTAKE;

AGED; CALCIUM, DIETARY; COLONIC NEOPLASMS; DAIRY PRODUCTS; DIET; FEMALE; HUMAN; INCIDENCE; IOWA; MIDDLE AGE; MULTIVARIATE ANALYSIS; PROPORTIONAL HAZARDS MODELS; PROSPECTIVE STUDIES; RISK; SUPPORT, U.S. GOV'T, P.H.S.; VITAMIN D;

EID: 0027163524     PISSN: 00029262     EISSN: None     Source Type: Journal    
DOI: 10.1093/oxfordjournals.aje.a116640     Document Type: Article

References (105)

1. Boring CC, Squires TS, Tong T. Cancer statistics. CA 1991;41:19-36.
2. Ries LAG, Hankey BF, Miller BA, et al. Cancer statistics review 1973-88. Bethesda, MD: National Cancer Institute, 1991. (N1H publication no. 912789).
3. Schottenfeld D, Winawer SJ. Large intestine. In: Schottenfeld D, Fraumeni JF, eds. Cancer epidemiology and prevention. Philadelphia, PA: WB Saunders Company, 1982:703-27.
4. Willett WC, MacMahon B. Diet and cancer-an overview. N Engl J Med 1984;310:697-703.
5. Potter JD. Reconciling the epidemiology, physiology, and molecular biology of colon cancer. JAMA 1992;268:1573-7.
6. Lipkin M, Blattner WE, Fraumeni JF Jr, et al. Tritiated thymidine ([3H]dTh) labeling distribution as a marker for hereditary predisposition to colon cancer. Cancer Res 1983;43:1899-1904.
7. Deschner EE, Winawer SJ, Long FC, et al. [3H]Thymidine-labeled colonic epithelial cells and mucosa in mice and man. Am J Dig Dis 1978; 23:305-11.
8. Deschner EE, Lipkin M. Proliferative patterns in colonic mucosa in familial polyposis. Cancer 1975;35:443-8.
9. Iwama T, Utzunomiya J, Sasaki J. Epithelial cell kinetics in the crypts of familial polyposis of colon. Jpn J Surg 1977;7:230-4.
10. Bleiberg H, Mainguet P, Galand P. Cell renewal in familial polyposis: comparison between polyps and adjacent healthy mucosa. Gastroenterology 1972;63:240-5.
11. Deschner EE, Lewis DM, Lipkin M. In vitro study of human rectal epithelial cells. I. Atypical zone of H3 thymidine incorporation in mucosa of multiple polyposis. J Clin Invest 1963;42:1922-8.
12. Lipkin M, Uehara K, Winawer S, et al. Seventh- Day Adventist vegetarians have quiescent proliferative activity in colonic mucosa. Cancer Lett 1985;26:139-44.
13. Terpstra OT, Strautenstein MV, Dees J, et al. Abnormal pattern of cell proliferation in the entire mucosa of patients with colon adenoma or cancer. Gastroenterology 1987;92:704-8.
14. Bleiberg FI, Mainguet P, Galand P, et al. Cell renewal in the human rectum: in vitro autoradiographic study on active ulcerative colitis. Gastroenterology 1970;58:851-5.
15. Serafini EP, Kirk AP, Chambers TJ. Rate and pattern of epithelial cell proliferation in ulcerative colitis. Gut 1981;22:648-52.
16. Kanemitsu T, Koike A, Yamamoto S. Study of the cell proliferation kinetics in ulcerative colitis, adenomatous polyps and cancer. Cancer 1985; 56:1094-8.
17. Lipkin M, Enker WE, et al. Tritiated-thymidine labeling of rectal epithelial cells in “non-prep” biopsies of individuals at increased risk for colonic neoplasia. Cancer Lett 1987;37:155-61.
18. Bleiberg H, Buyse M, Galand P. Cell kinetic indicators of premalignant stages of colorectal cancer. Cancer 1985;56124-9.
19. Roncucci L, Scalmati A, Ponz de Leon M. Pattern of cell kinetics in colorectal mucosa of patients with different types of adenomatous polyps of the large bowel. Cancer 1991;68:873-8.
20. Ponz de Leon M, Roncucci L, Donato PD, et al. Pattern of epithelial cell proliferation in colorectal mucosa of normal subjects and of patients with adenomatous polyps or cancer of the large bowel. Cancer Res 1988;48:4121-6.
21. Stadler J, Yeung KS, Furrer R, et al. Proliferative activity of rectal mucosa and soluble fecal bile acids in patients with normal colons and in patients with colonic polyps or cancer. Cancer Lett 1988;38:315-20.
22. Potten CS, Kellett M, Roberts SA, et al. Measurement of in vivo proliferation in human colorectal mucosa using bromodeoxyuridine. Gut 1992;33: 71-8.
23. Ronccucci L, Ponz de Leon M, Scalmati A, et al. The influence of age on colonic epithelial cell proliferation. Cancer 1988;48:235-45.
24. Fry RJM, Staffeldt E. Effect of a diet containing sodium deoxycholate on the intestinal mucosa of the mouse. Nature 1964;203:1396-8.
25. Choucha C, Bhadracbari N, Nigr ND. The effect of bile on the induction of experimental intestinal tumors in rats. Dis Colon Rectum 1974; 17: 310-12.
26. Ranken R, Wilson R, Bealmear PM. Increased turnover of intestinal mucosal cells of germfree mice induced by cholic acid. Proc Soc Exp Biol Med 1971;138:270-2.
27. Wargovich MJ, Eng VWS, Newmark PL Calcium inhibits the damaging and compensatory proliferative effects of fatty acids on mouse colon epithelium. Cancer Lett 1984;23:253-8.
28. Ammon FU, Thomas PJ, Phillips SF. Effect of oleic and ricinoleic acids on net jejunal water and electrolyte movement: perfusion studies in man. J Clin Invest 1974;53:374-9.
29. Mekjian MS, Phillips SF, Hoffman AF. Colonic secretion of water and electrolytes induced by bile acids: perfusion studies in man. J Clin Invest 1971; 50:120-9.
30. Ammon HU, Phillips SF. Fatty acids inhibit intestinal water absorption in man: fatty acid diarrhea? Gastroenterology 1972;62:717-18.
31. Bird RP, Schneider R, Stamp D, et al. Effect of dietary calcium and cholic acid on the proliferative indices of murine colonic epithelium. Carcinogenesis 1986;7:657-61.
32. Wargovich MJ, Eng WWS, Newmark HL, et al. Calcium ameliorates the toxic effect of deoxy- cholic acid on colonic epithelium. Carcinogenesis 1983;4:1205-7.
33. Deschner EE, Cohen BJ, Raicht RF. Acute and chronic effects of dietary cholic acid on colonic epithelial cell proliferation. Digestion 1982;21: 290-6.
34. Deschner EE, Raicht RF. Influence of bile on kinetic behavior of colonic epithelial cells of rats. Digestion 1979;19:322-7.
35. Narisawa T, Magadia NE, Weisburger JH, et al. Promoting effect of bile acids on colon carcinogenesis after intrarectal instillation of A-methyl- A'-nitro-A-nitrosoguanidine in rats. J Natl Cancer Inst 1974;53:1093-7.
36. Bull AW, Soulier EK, Wilson PS, et al. Promotion of azoxymethane-induced intestinal cancer by high fat in rats. Cancer Res 1987;39:4959-65.
37. Reddy BS, Narisawa T, Weisburger JH, et al. Promoting effect of sodium deoxycholate on colon adenocarcinomas in germfree rats. J Natl Cancer Inst 1976;56:441-2.
38. Reddy BS, Watanabe K, Weisburger JH, et al. Promoting effect of bile acids in colon carcinogenesis in germ-free and conventional F344 rats. Cancer Res 1977;37:3238-42.
39. Lipkin M, Newmark H. Effect of added dietary calcium on colonic epithelial cell proliferation in subjects at high risk for familial colonic cancer. N Engl J Med 1985;313:1381-4.
40. Buset M, Lipkin M, Winawer S, et al. Inhibition of human colonic epithelial cell proliferation in vivo and in vitro by calcium. Cancer Res 1986; 46:5426-30.
41. Rozen P, Fireman A, Fine N, et al. Oral calcium suppresses increased rectal epithelial proliferation of persons at risk of colorectal cancer. Gut 1989; 30:650-5.
42. Lipkin M, Friedman E, Winawer SJ, et al. Colonic epithelial cell proliferation in responders and nonresponders to supplemental dietary calcium. Cancer Res 1989;49:248-54.
43. Wargovich MJ, Isbell G, Shabot M, et al. Calcium supplementation decreases rectal epithelial cell proliferation in subjects with sporadic adenoma. Gastroenterology 1992;103:92-7.
44. Newmark HL, Wargovich MJ, Bruce WR. Colon cancer and dietary fat phosphate and calcium: a hypothesis. J Natl Cancer Inst 1984;72:1323-5.
45. Hennings J, Michael D, Chang C, et al. Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 1980;19:245-54.
46. Yuspa SH, Koehler B, Kulesz-Martin M, et al. Clonal growth of mouse epidermal cells in medium with reduced calcium concentration. J Invest Dermatol 1981;76:144-6.
47. Lechner JF, Haugen A, McClendon IA, et al. Clonal growth of normal adult human bronchial epithelial cells in a serum-free medium. In Vitro 1982;18:633-42.
48. Tsao MC, Walthall MJ, Hamm RG. Clonal growth of normal human epidermal keratinocytes in a defined medium. J Cell Physiol 1982; 110: 219-29.
49. Babcock MS, Marino MR, Gunning WT III, et al. Clonal growth and serial propagation of rat esophageal epithelial cells. In Vitro 1983; 19: 403-15.
50. Boyce ST, Ham RG. Calcium-regulated differentiation of normal human epidermal keratinocytes in chemically defined clonal culture and serumfree serial culture. J Invest Dermatol 1983; 81(suppl):33s-40s.
51. McGrath CM, Soule HD. Calcium regulation of normal human mammary epithelial cell growth in culture. In Vitro 1984;20:652-62.
52. Reshef R, Rozen P, Fireman Z, et al. Effect of a calcium-enriched diet on the colonic epithelial hyperproliferation induced by A'-methyl-A'-nitro- A-nitrosoguanidine in rats on a low calcium and fat diet. Cancer Res 1990;50:1764-7.
53. Appleton GVN, Davies PW, Bristol JB, et al. Inhibition of intestinal carcinogenesis by dietary supplementation with calcium. Br J Surg 1987; 74:523-5.
54. Pence BC, Buddingh F. Inhibition of dietary fat- promoted colon carcinogenesis in rats by supplemental calcium or vitamin D3. Carcinogenesis 1988;9:187-90.
55. Behling AR, Kaup SM, Choquette LL, et al. Lipid absorption and intestinal tumour incidence in rats fed on varying levels of calcium and butterfat. Br J Nutr 1990;64:505-13.
56. Wargovich MJ, Allnutt D, Palmer C, et al. Inhibition of the promotional phase of azoxymethane- induced colon carcinogenesis in the F344 rat by calcium lactate: effect of simulating two human nutrient density levels. Cancer Lett 1990;53: 17-25.
57. McSherry CK, Cohen BI, Bokkenheuser VD, et al. Effects of calcium and bile acid feeding on colon tumors in the rat. Cancer Res 1989;49: 6039-43.
58. Sitrin MD, Halline AG, Abrahams C, et al. Dietary calcium and vitamin D modulate 1, 2-di- methylhydrazine-induced colonic carcinogenesis in the rat. Cancer Res 1991;51:5608-13.
59. Kaskare MR, Clark TD, Glauert HP. Effect of dietary calcium on colon carcinogenesis induced by a single injection of 1, 2-dimethylhydrazine in rats. J Nutr 1991;121:568-77.
60. Llor X, Jacoby RF, Teng B, et al. K-ras mutations in 1, 2-dimethylhydrazine-induced colonic tumors: effects of supplemental dietary calcium and vitamin D deficiency. Cancer Res 1991;51: 4305-9.
61. Newmark HL, Lipkin M. Calcium vitamin D and colon cancer. Cancer Res 1992;52(suppl): 2067s-70s.
62. Yang K, Cohen L, Lipkin M. Lectin soybean agglutinin: measurements in colonic epithelial cells of human subjects following supplemental dietary calcium. Cancer Lett 1991;56:65-9.
63. Haynes RC, Murad F. Agents affecting calcification: calcium, parathyroid hormone, calcitonin, vitamin D, and other compounds. In: Goodman LS, Gilman AG, Rail TW, et al, eds. The pharmacological basis of therapeutics. 7th ed. New York: MacMillan Publishing Company, 1985.
64. Lointier P, Wargovich MJ, Saez S, et al. The role of vitamin D3 in the proliferation of a human colon cancer cell line in vitro. Anticancer Res 1987;7:817-21.
65. Kawaura A, Takahashi A, Tanida N, et al. la- Hydroxyvitamin D3 suppresses colonic tumori- genesis induced by repetitive intrarectal injection of A'-methyl-A'-nitrosourea in rats. Cancer Lett 1990;55:149-52.
66. Sorenson AW, Slattery ML, Ford MH. Calcium and colon cancer: a review. Nutr Cancer 1988; 11:135-45.
67. Alder RJ, McKeowen-Eyssen G. Calcium intake and risk of colorectal cancer. In: Horowitz S, Rozen P, eds. Frontiers of gastrointestinal research. Basel, Switzerland: S. Karger, AG, 1988; 4608-19.
68. Garland CF, Garland FC. Do sunlight and vitamin D reduce the likelihood of colon cancer? Int J Epidemiol 1980;9:227-31.
69. Emerson JC, Weiss NS. Colorectal cancer and solar radiation. Cancer Causes Control 1992;3: 95-9.
70. Garland C, Barrett-Connor E, Rossof AH, et al. Dietary vitamin D and calcium and risk of colorectal cancer: a 19-year prospective study in men. Lancet 1985;1:307-9.
71. Stemmerman GN, Nomura A, Chyou P-H. The influence of dairy and non-dairy calcium on subsite large-bowel cancer risk. Dis Colon Rectum 1990;33:190-4.
72. Kune S, Kune GM, Watson F. Case-control study of dietary étiologie factors: The Melbourne Colorectal Cancer Study. Nutr Cancer 1987;9:21-42.
73. Slattery ML, Sorenson AW, Ford MH. Dietary calcium intake as a mitigating factor in colon cancer. Am J Epidemiol 1988;128:504-14.
74. Peters RK, Pike MC, Garabrant D, et al. Diet and colon cancer in Los Angeles County, California. Cancer Causes Control 1992;3:457-73.
75. Lee HP, Gourly L, Duffy SW, et al. Colorectal cancer and diet in an Asian population: a case- control study among Singapore Chinese. Int J Cancer 1989;43:1007-16.
76. Macquart-Moulin G, Riboli E, Comee J, et al. Case-control study on colorectal cancer and diet in Marseilles. Int J Cancer 1986;38:183-91.
77. Wu AH, Paganini-Hill A, Ross RK, et al. Alcohol, physical activity and other risk factors for colorectal cancer: a prospective study. Br J Cancer 1987; 55:687-94.
78. Benito E, Stiggelbout A, Bosch FX, et al. Nutritional factors in colorectal cancer risk: a case- control study in Majorca. Int J Cancer 1991;49: 161-7.
79. Tuyns AJ, Haelterman M, Kaaks R. Colorectal cancer and the intake of nutrients: oligosaccharides are a risk factor, fats are not. A case-control study in Belgium. Nutr Cancer 1987;10:181-96.
80. Negri E, La Vecchia C, D’Avanzo B, et al. Calcium, dairy products and colorectal cancer. Nutr Cancer 1990;13:255-62.
81. Graham S, Marshall J, Haughey B, et al. Dietary epidemiology of cancer of the colon in Western New York. Am J Epidemiol 1988;128:490-503.
82. Willett WC, Stampfer MJ, Colditz GA, et al. Relation of meat, fat, and fiber intake to the risk of colon cancer in a prospective study among women. N Engl J Med 1990; 323:1664-72.
83. Garland CF, Garland FC, Shaw EK, et al. Serum 25-hydroxyvitamin D and colon cancer: eight- year prospective study. Lancet 1989;2:1176-8.
84. Phillips RL, Snowdon DA. Dietary relationships with fatal colorectal cancer among Seventh-Day Adventists. J Natl Cancer Inst 1985;74:307-17.
85. Pickle LN, Greene MH, Ziegler RG, et al. Colorectal cancer in rural Nebraska. Cancer Res 1984; 44:363-9.
86. Tajima K, Tominga S. Dietary habits and gastrointestinal cancers: a comparative case-control study of stomach and large intestinal cancers in Nagoya, Japan. Jpn J Cancer Res 1985;76: 705-16.
87. Ursin G, Bjelke E, Heuch I, et al. Milk consumption and cancer incidence: a Norwegian prospective study. Br J Cancer 1990;61:454-9.
88. Miller AB, Howe GR, Jain M, et al. Food items and food groups as risk factors in a case-control study of diet and colorectal cancer. Int J Cancer 1983;32:155-61.
89. Benito E, Obrador A, Stiggelbout A, et al. A population-based case-control study of colorectal cancer in Majorca. I. Dietary factors. Int J Cancer 1990;45:69-76.
90. Manousos O, Day NE, Trichopoulos D, et al. Diet and colorectal cancer: a case-control study in Greece. Int J Cancer 1983;32:1-5.
91. Folsom AR, Kaye SA, Potter JD, et al. Association of incidence of carcinoma of the endometrium with body weight and fat distribution in older women: early findings of the Iowa Women’s Health Study. Cancer Res 1989;49:6828-31.
92. Sellers TA, Kushi LH, Potter JD, et al. Effect of family history, body-fat distribution, and reproductive factors on the risk of postmenopausal breast cancer. N Engl J Med 1992;326:1323-9.
93. Willett WC, Sampson L, Browne ML, et al. The use of a self-administered questionnaire to assess diet four years in the past. Am J Epidemiol 1988; 127:188-99.
94. Willett WC, Sampson L, Stampfer MJ, et al. Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 1985;122:51-65.
95. Block G, Hartman AM, Dresser CM, et al. A data- based approach to diet questionnaire design and testing. Am J Epidemiol 1986;124:453-69.
96. Rimm EB, Giovannucci EL, Stampfer MJ, et al. Reproducibility and validity of an expanded self- administered semiquantitative food frequency questionnaire among male health professionals. Am J Epidemiol 1992; 135:1114-26.
97. Munger RG, Folsom AR, Kushi LH, et al. 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 1992; 136: 192-200.
98. US Public Health Service. SEER program: cancer incidence and mortality in the United States 1973-81. Bethesda, MD: National Cancer Institute, 1984. (NIH publication no. 85-1837).
99. Rothman KJ, Boice JD. Epidemiologic analysis with a programmable calculator. Washington, DC: US GPO, 1979. (NIH publication no. 791649).
100. Cox DR. Regression models and life tables. J R StatSoc [B] 1972;34:187-220.
101. SAS Institute, Inc. SAS/STAT software: the PHREG procedure preliminary documentation.
102. Cary, NC: SAS Institute, Inc, 1991.
103. Miettinen O. Estimability and estimation in case-referent studies. Am J Epidemiol 1976; 103: 226-35.
104. Schoenfeld D. Partial residuals for the proportional hazards regression model. Biometrika 1982; 69:239-41.
105. Harrell F. The PHGLM procedure. In: SAS supplemental library user’s guide, version 5 ed. Cary, NC: SAS Institute, Inc, 1986.