Cancer Causes & Control

, Volume 9, Issue 6, pp 567–582 | Cite as

Dietary influences of 1,25(OH)2 vitamin D in relation to prostate cancer: A hypothesis

  • Edward Giovannucci
Article

Abstract

Diets high in dairy products and meats are related to higher risk of prostate cancer incidence or mortality in most ecologic, case- control, and prospective studies. Recent laboratory and epidemiologic evidence indicates that a high circulating level of 1,25(OH)2 vitamin D [1,25(OH)2D], the biologically active form of vitamin D, inhibits prostate carcinogenesis. This paper will examine the hypothesis that these observations may be linked, specifically that high dairy and meat consumption increase risk of prostate cancer by lowering 1,25(OH)2D. High intakes of calcium and phosphorus, largely from dairy products, lower circulating 1,25(OH)2D level, and sulfur-containing amino acids from animal protein lower blood pH, which also suppresses 1,25(OH)2D production. Additionally, high fructose consumption produces a transitory hypophosphatemia, and may adversely affect calcium and phosphate balance, all of which may stimulate 1,25(OH)2D production. The evidence that 1,25(OH)2D inhibits prostate carcinogenesis, and that diets that are high in calcium, phosphorus, and sulfur-containing amino acids from animal protein, as well as low in fructose, tend to decrease circulating 1,25(OH)2D will be presented. The studies examining these dietary factors in relation to prostate cancer risk will be reviewed.

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References

  1. 1.
    Schwartz GG, Hulka BS. Is vitamin D deficiency a risk factor for prostate cancer? (Hypothesis). Anticancer Res 1990; 10: 1307–11.Google Scholar
  2. 2.
    Corder EH, Guess HA, Hulka BS, Friedman GD, Sadler M, Vollmer RT, Lobaugh B, Drezner MK, Vogelman JH, Orentreich, N. Vitamin D and prostate cancer: a prediagnostic study with stored sera. Cancer Epidemiol Biomarkers Prev 1993; 2: 467–72.Google Scholar
  3. 3.
    Giovannucci E. Epidemiologic characteristics of prostate cancer. Cancer 1995; 75 (suppl): 1766–77.Google Scholar
  4. 4.
    Gann PH, Ma J, Hennekens CH, Hollis BW, Haddad JG, Stampfer MJ. Circulating vitamin D metabolites in relation to subsequent development of prostate cancer. Cancer Epidemiol Biomarkers Prev 1996; 5: 121–6.Google Scholar
  5. 5.
    Reichel H, Koeffler HP, Norman AW. The role of the vitamin D endocrine system in health and disease. N Engl J Med 1989; 320: 980–91.Google Scholar
  6. 6.
    Holick MF, Krane SM, Potts JT. Calcium, phosphorus, and bone metabolism: calcium regulating hormones. In: Wilson JD, Braunwald E, Isselbacher KJ, Petersdorf RG, Martin JB, Fauci AS, and Root RK, eds. Harrison's Principles of Internal Medicine. New York: McGraw-Hill 1991, 1888–902.Google Scholar
  7. 7.
    Fraser D. Regulation of the metabolism of vitamin D. Physiol Rev 1980; 60: 551–613.Google Scholar
  8. 8.
    Stern PH, Taylor, AB, Bell NH, Epstein S. Demonstration that circulating 1α,25-dihydroxyvitamin D is loosely regulated in normal children. J Clin Invest 1981; 68: 1374–77.Google Scholar
  9. 9.
    Breslau NA. Southwestern Internal Medicine Conference: Normal and abnormal regulation of 1,25-(OH)2D synthesis. Am J Med Sci 1988; 296: 417–25.Google Scholar
  10. 10.
    Hughes MR, Baylink DJ, Jones PG, Haussler MR. Radioligand receptor assay for 25-hydroxyvitamin D2/ D3 and 1 α,25-dihydroxyvitamin D2/D3. J Clin Invest 1976; 58: 61–70.Google Scholar
  11. 11.
    Clements MR, Johnson L, Freaser DR. A new mechanism for induced vitamin D deficiency in calcium deprivation. Nature 1987; 325: 62–5.Google Scholar
  12. 12.
    Vieth R, Fraser D, Kooh SW. Low dietary calcium reduces 25-hydroxycholecalciferol in plasma of rats. J Nutr 1987; 117: 914–18.Google Scholar
  13. 13.
    Bell NH, Shaw S, Turner RT. Evidence that 1,25-dihydroxyvitamin D3 inhibits the hepatic production of 25-hydroxyvitamin D in man. J Clin Invest 1984; 74: 1540–44.Google Scholar
  14. 14.
    Ho SC, MacDonald D, Chan C, Fan YK, Chan SSG, Swaminathan R. Determinants of serum 1,25-dihydroxyvitamin D concentration in healthy premenopausal subjects. Clin Chim Acta 1994; 230: 21–33.Google Scholar
  15. 15.
    Dubbelman R, Jonxis JHP, Muskiet FAJ, Saleh AEC. Age-dependent vitamin D status and vertebral condition of white women living in Curaçao (The Netherlands Antilles) as compared with their counterparts in The Netherlands. Am J Clin Nutr 1993; 58: 106–9.Google Scholar
  16. 16.
    Dandona P, Menon RK, Shenoy R, Houlder S, Thomas M, Mallinson WJW. Low 1,25-dihydroxyvitamin D, secondary hyperparathyroidism, and normal osteocalcin in elderly subjects. J Clin Endocrinol Metab 1986; 63: 459–62.Google Scholar
  17. 17.
    Lips P, Wiersinga A, van Ginkel FC, Jongen MJM, Netelenbos JC, Hackeng WHL, Delmas PD, van der Vijgh WJF. The effect of vitamin D supplementation on vitamin D status and parathyroid function in elderly subjects. J Clin Endocrinol Metab 1988; 67: 644–50.Google Scholar
  18. 18.
    Bouillon RA, Auwerx JH, Lissens WD, Pelemans WK. Vitamin D status in the elderly: seasonal substrate deficiency causes 1,25-dihydroxycholecalciferol deficiency. Am J Clin Nutr 1987; 45: 755–63.Google Scholar
  19. 19.
    Sherman SS, Hollis BW, Tobin JD. Vitamin D status and related parameters in a healthy population: the effects of age, sex, and season. J Clin Endocrinol Metab 1990; 71: 405–13.Google Scholar
  20. 20.
    Juttmann JR, Visser TJ, Buurman C, de Kam E, Birkenhager JC. Seasonal fluctuations in serum concentrations of vitamin D metabolites in normal subjects. Br Med J (Clin Res Ed). 1981; 282: 1349–52.Google Scholar
  21. 21.
    Stumpf WE, Sar M, Reid FA, Tanaka Y, DeLuca HF. Target cells for 1,25-dihydroxyvitamin D3 in intestinal tract, stomach, kidney, skin, pituitary, and parathyroid. Science 1979; 206: 1188–90.Google Scholar
  22. 22.
    Peehl DM, Skowronski RJ, Leung GK, Wong ST, Stamey TA, Feldman D. Antiproliferative effects of 1,25-dihydroxyvitamin D3 on primary cultures of human prostatic cells. Cancer Res 1994; 54: 805–10.Google Scholar
  23. 23.
    Skowronski RJ, Peehl DM, Feldman D. Vitamin D and prostate cancer: 1,25 dihydroxyvitamin D3 receptors and actions in human prostate cancer cell lines. Endocrinology 1993; 132: 1952–60.Google Scholar
  24. 24.
    Miller GJ, Stapleton GE, Hedlund TE, Moffatt KA. Vitamin D receptor expression, 24-hydroxylase activity, and inhibition of growth by 1α,25-dihydroxyvitamin D3 in seven human prostatic carcinoma cell lines. Clin Cancer Res 1995; 1: 997–1003.Google Scholar
  25. 25.
    Hsieh T-C, Ng C-Y, Mallouh C, Tazaki H, Wu JM. Regulation of growth, PSA/PAP and androgen receptor expression by 1α,25-dihydroxyvitamin D3 in androgen-dependent LNCaP cells. Biochem Biophys Res Comm 1996; 223: 141–6.Google Scholar
  26. 26.
    Bahnson RR, Oeler T, Trump D, Smith D, Schwartz GG. Inhibition of human prostatic carcinoma cell lines by 1,25-dihydroxyvitamin D3 and vitamin D analogs (abstract). J Urol 1993; 149 (suppl): 471a.Google Scholar
  27. 27.
    Esquenet M, Swinnen JV, Heyns W, Verhoeven G. Control of LNCaP proliferation and differentiation: Actions and interactions of androgens, 1α,25-dihydroxycholecalciferol, all-trans retinoic acid, 9-cis retinoic acid, and phenylacetate. Prostate 1996; 28: 182–94.Google Scholar
  28. 28.
    Hedlund TE, Moffatt KA, Miller GJ. Stable expression of the nuclear vitamin D receptor in the human prostatic carcinoma cell line JCA-1: evidence that the antiproliferative effects of 1α,25-dihydroxyvitamin D3 are mediated exclusively through the genomic signaling pathway. Endocrinology 1996; 137: 1554–61.Google Scholar
  29. 29.
    Drivdahl RH, Loop SM, Andress DL, Ostenson RC. IGF-binding proteins in human prostate tumor cells: expression and regulation by 1,25-dihydroxyvitamin D3. Prostate 1995; 26: 72–9.Google Scholar
  30. 30.
    Samid D, Shack S, Myers CE. Selective growth arrest and phenotypic reversion of prostate cancer cells in vitro by nontoxic pharmacological concentrations of phenylacetate. J Clin Invest 1993; 91: 2288–95.Google Scholar
  31. 31.
    Schwartz GG, Wang M-H, Zhang M, Singh RK, Siegal GP. 1a,25-dihydroxyvitamin D (calcitriol) inhibits the invasiveness of human prostate cancer cells. Cancer Epidemiol Biomarkers Prev 1997; 6: 727–32.Google Scholar
  32. 32.
    Konety BR, Schwartz GG, Acierno JS, Jr., Becich MJ, Getzenberg RH. The role of vitamin D in normal prostate growth and differentiation. Cell Growth Differ 1996; 7: 1563–70.Google Scholar
  33. 33.
    Schwartz GG, Hill CC, Oeler TA, Becich MJ, Bahnson RR. 1,25-dihydroxy-16-ene-23-yne-vitamin D3 and prostate cancer cell proliferation in vivo. Urology 1995; 46: 365–9.Google Scholar
  34. 34.
    Lucia MS, Anzano MA, Slayter MV, Anver MR, Green DM, Shrader MW, Logsdon DL, Driver CL, Brown CC, Peer CW, Robert AB, Sporn MB. Chemopreventive acitivity of tamoxifen, N-(4-hydroxyphenyl)retinamide, and the vitamin D analogue Ro24-5531 for androgen-promoted carcinomas of the rat seminal vesicle and prostate. Cancer Res 1995; 55: 5621–7.Google Scholar
  35. 35.
    Chan JM, Stampfer MJ, Giovannucci E, Gann PH, Ma J, Wilkinson P, Hennekens CH, Pollak M. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 1998; 279: 563–6.Google Scholar
  36. 36.
    Corder EH, Friedman GD, Vogelman JH, Orentreich N. Seasonal variation in vitamin D, vitamin D-binding protein, and dehydroepiandrosterone: risk of prostate cancer in black and white men. Cancer Epidemiol Biomarkers Prev 1995; 4: 655–9.Google Scholar
  37. 37.
    Braun MM, Helzlsouer KJ, Hollis BW, Comstock GW. Prostate cancer and prediagnostic levels of serum vitamin D metabolites (Maryland, United States). Cancer Causes Control 1995; 6: 235–9.Google Scholar
  38. 38.
    Nomura AMY, Stemmermann GN, Lee J, et al. Serum vitamin D metabolite levels and the subsequent development of prostate cancer. Cancer Causes Control 1998, submitted.Google Scholar
  39. 39.
    Hanchette CL, Schwartz GG. Geographic patterns of prostate cancer mortality. Cancer 1992; 70: 2861–9.Google Scholar
  40. 40.
    Morrison AN, Qi CJ, Tokita A. Prediction of bone density from vitamin D receptor alleles. Nature 1994; 67: 284–97.Google Scholar
  41. 41.
    Taylor JA, Hirvonen A, Watson M, Pittman G, Mohler JL, Bell DA. Association of prostate cancer with vitamin D receptor gene polymorphism. Cancer Res 1996; 56: 4108–10.Google Scholar
  42. 42.
    Ingles SA, Ross RK, Yu MC, Irvine RA, La Pera G, Haile RW, Coetzee GA. Association of prostate cancer risk with genetic polymorphisms in vitamin D receptor and androgen receptor. J Natl Cancer Inst 1997; 89: 166–70.Google Scholar
  43. 43.
    Ma J, Stampfer MJ, Gann PH, Hough HL, Giovannucci E, Kelsey KT, Hennekens CH, Hunter DJ. Vitamin D receptor polymorphisms, circulating vitamin D metabolites and risk of prostate cancer in United States physicians. Cancer Epidemiol Biomarkers Prev 1998, 7: 385–90.Google Scholar
  44. 44.
    Bilezikian JP, Canfield RE, Jacobs TP, Polay JS, D'Adamo AP, Eisman JA, DeLuca HF. Response of 1a,25-dihydroxyvitamin D3 to hypocalcemia in human subjects. N Engl J Med 1978; 299: 437–41.Google Scholar
  45. 45.
    Adams ND, Gray RW, Lemann J, Jr. The effects of oral CaCO3 loading and dietary calcium deprivation on plasma 1,25-dihydroxyvitamin D concentrations in healthy adults. J Clin Endocrinol Metab 1979; 48: 1008–16.Google Scholar
  46. 46.
    Gascon-Barre M, D'Amour P, Dufresne L, Perreault JP. Interrelationships between circulating vitamin D metabolites in normocalciuric and hypercalciuric renal stone formers. Ann Nutr Metab 1985; 29: 289–96.Google Scholar
  47. 47.
    Turner RT. Mammalian 25-hydroxyvitamin D-1α-hydroxylase: measurement and regulation. In: Kumar R, ed. Vitamin D: Basic and Clinical Aspects. Hingham, MA: Martinus Nijhoff Publishing 1984; 175–96.Google Scholar
  48. 48.
    Portale AA, Halloran BP, Murphy MM, Morris RC, Jr. Oral intake of phosphorus can determine the serum concentration of 1,25-dihydroxyvitamin D by determining its production rate in humans. J Clin Invest 1986; 77: 7–12.Google Scholar
  49. 49.
    Avioli LV. Calcium and phosphorus. In: Shils ME Young VR, eds. Modern Nutrition in Health and Disease Philadelphia, PA: Lea & Febiger, 1988: 142–58.Google Scholar
  50. 50.
    Portale AA, Halloran BP, Morris RC, Jr. Dietary intake of phosphorus modulates the circadian rhythm in serum concentration of phosphorus. Implications for the renal production of 1,25-dihydroxyvitamin D. J Clin Invest 1987; 80: 1147–54.Google Scholar
  51. 51.
    Portale AA, Halloran BP, Morris RC, Jr. Physiologic regulation of the serum concentration of 1,25-dihydroxyvitamin D by phosphorus in normal men. J Clin Invest 1989; 83: 1494–9.Google Scholar
  52. 52.
    Mayes PA. Intermediary metabolism of fructose. Am J Clin Nutr 1993; 58 (suppl): 754S–765S.Google Scholar
  53. 53.
    Hallfrisch J, Ellwood K, Michaelis OE, Reiser S, Prather ES. Plasma fructose, uric acid, and inorganic phosphorus responses of hyperinsulinemic men fed fructose. J Am Coll Nutr 1986; 5: 61–8.Google Scholar
  54. 54.
    Israel KD, Michaelis OE, Reiser S, Keeney M. Serum uric acid, inorganic phosphorus, and glutamic-oxalacetic transaminase and blood pressure in carbohydrate-sensitive adults consuming three different levels of sucrose. Ann Nutr Metab 1983; 27: 425–35.Google Scholar
  55. 55.
    Woods HF, Eggleston LV, Krebs HA. The cause of hepatic accumulation of fructose 1-phosphate on fructose loading. Biochem J 1970; 119: 501–10.Google Scholar
  56. 56.
    Vrana A Fabry P. Metabolic effects of high sucrose or fructose intake. World Rev Nutr Diet 1983; 42: 56–101.Google Scholar
  57. 57.
    Narins RG, Weisberg JS, Myers AR. Effects of carbohydrates on uric acid metabolism. Metabolism 1974; 23: 455–65.Google Scholar
  58. 58.
    Milne DB, Nielsen FH. Dietary magnesium and fructose affect macromineral metabolism in men [abstract]. In: FASEB Annual Meeting of Professional Research Scientists 1998. San Francisco, CA: FASEB.Google Scholar
  59. 59.
    Langman CB. Calcitriol metabolism during chronic metabolic acidosis. Semin Nephrol 1989; 9: 65–71.Google Scholar
  60. 60.
    Brosnan JT Brosnan ME. Dietary protein, metabolic acidosis, and calcium balance. In: Draper HH, ed. Advances in Nutritional Research. New York, NY: Plenum Press, 1982: 77–105.Google Scholar
  61. 61.
    Kaneko K, Masaki U, Aikyo M, Yabuki K, Haga A, Matoba C, Sasaki H, Koike G. Urinary calcium and calcium balance in young women affected by high protein diet of soy protein isolate and adding sulfur-containing amino acids and/or potassium. J Nutr Sci Vitaminol 1990; 36: 105–16.Google Scholar
  62. 62.
    Epstein M. Aging and the kidney. J Am Soc Nephrol 1996; 7: 1106–22.Google Scholar
  63. 63.
    Lindeman RD, Tobin J, Shock NW. Longitudinal studies on the rate of decline in renal function with age. J Am Geriatr Soc 1985; 33: 278–85.Google Scholar
  64. 64.
    Frassetto LA, Morris RC, Jr, Sebastian A. Effect of age on blood acid-base composition in adult humans: role of age-related renal functional decline. Am J Physiol 1996; 271(40): F1114–F1122.Google Scholar
  65. 65.
    Chesney RW, Kaplan BS, Phelps M, HF D. Renal tubular acidosis does not alter circulating values of calcitriol. J Pediatr 1984; 104: 51–5.Google Scholar
  66. 66.
    Cunningham J, Fraher LJ, Clemens TL, Revell PA, Papapoulos SE. Chronic acidosis with metabolic bone disease. Effect of alkali on bone morphology and vitamin D metabolism. Am J Med 1982; 73: 199–204.Google Scholar
  67. 67.
    Cunningham J, Bikle DD, Avioli LV. Acute, but not chronic, metabolic acidosis disturbs 25-hydroxyvitamin D3 metabolism. Kidney Int 1984; 25: 47–52.Google Scholar
  68. 68.
    Portale AA, Halloran BP, Harris ST, Bikle DD, Morris RC Jr. Metabolic acidosis reverses the increase in serum 1,25 (OH)2D in phosphorus-restricted normal men. Am J Physiol 1992; 263(26): E1164–E1170.Google Scholar
  69. 69.
    Bushinsky DA, Favus MJ, Schneider AB, Sen PK, Sherwood LM, Coe FL. Effects of metabolic acidosis on PTH and 1,25 (OH)2D3 response to low calcium diet. Am J Physiol 1982; 243(12): F570–F575.Google Scholar
  70. 70.
    Kraut, JA, Gordon, EM, Ransom JC, Horst R, Slatopolsky E, Coburn JW, Kurokawa K. Effect of chronic metabolic acidosis on vitamin D metabolism in humans. Kidney Int 1983; 24: 644–8.Google Scholar
  71. 71.
    Breslau NA, Brinkley L, Hill KD, Pak CYC. Relationship of animal protein-rich diet to kidney stone formation and calcium metabolism. J Clin Endocrinol Metab 1988; 66: 140–6.Google Scholar
  72. 72.
    St. John A, Thomas MB, Davies CP, Mullan B, Dick I, Hutchison B, van der Schaff A, Prince RL. Determinants of intact parathyroid hormone and free 1,25-dihydroxyvitamin D levels in mild and moderate renal failure. Nephron 1992; 61: 422–7.Google Scholar
  73. 73.
    Lu K-C, Lin S-H, Yu F-C, Chyr S-H, Shieh S-D. Influence of metabolic acidosis on serum 1,25(OH)2D3 levels in chronic renal failure. Miner Electrolyte Metab 1995; 21: 398–402.Google Scholar
  74. 74.
    Kerstetter JE, Caseria DM, Mitnick ME, Ellison AF, Gay LF, Liskov TAP, Carpenter TO, Insogna KL. Increased circulating concentrations of parathyroid hormone in healthy, young women consuming a protein-restricted diet. Am J Clin Nutr 1997; 66: 1188–96.Google Scholar
  75. 75.
    Holick MF. McCollum Award lecture, 1994: Vitamin D — new horizons for the 21st century. Am J Clin Nutr 1994; 60: 619–30.Google Scholar
  76. 76.
    Chen TC, Shao Q, Heath H, III, Holick MF. An update on the vitamin D content of fortified milk from the United States and Canada [letter]. N Engl J Med 1993; 329: 1507.Google Scholar
  77. 77.
    Rose DP, Boyar AP, Wynder EL. International comparisons of mortality rates for cancer of the breast, ovary, prostate, and colon, and per capita food consumption. Cancer 1986; 58: 2263–71.Google Scholar
  78. 78.
    Mezzanotte G, Cislaghi C, Decarli A, Le Vecchia C. Cancer mortality in broad Italian geographical areas, 1975—1977. Tumori 1986; 72: 145–52.Google Scholar
  79. 79.
    Decarli A, La Vecchia C. Environmental factors and cancer mortality in Italy: Correlational exercise. Oncology 1986; 43: 116–26.Google Scholar
  80. 80.
    Talamini R, La Vecchia C, Decarli A, Negri E, Franceschi S. Nutrition, social factors, and prostatic cancer in a Northern Italian population. Br J Cancer 1986; 53: 817–21.Google Scholar
  81. 81.
    Rotkin ID. Studies in the epidemiology of prostatic cancer: expanded sampling. Cancer Treat Rep 1977; 61: 173–80.Google Scholar
  82. 82.
    Talamini R, Franceschi S, La Vecchia C, Serraino D, Barra S, Negri E. Diet and prostatic cancer: a case-control study in Northern Italy. Nutr Cancer 1992; 18: 277–86.Google Scholar
  83. 83.
    Schuman LM, Mandel JS, Radke A, Seal U, Halberg F. Some selected features of the epidemiology of prostatic cancer: Minneapolis-St. Paul, Minnesota case-control study, 1976-1979. In: Magnus K, ed. Trends in Cancer Incidence: Causes and Practical Implications. Washington DC: Hemisphere Publishing, 1982: 345–54.Google Scholar
  84. 84.
    Mettlin C, Selenskas S, Natarajan NS, Huben R. Beta-carotene and animal fats and their relationship to prostate cancer risk: A case-control study. Cancer 1989; 64: 605–12.Google Scholar
  85. 85.
    La Vecchia C, Negri E, D'Avanzo B, Franceschi S, Boyle P. Dairy products and the risk of prostatic cancer. Oncology 1991; 48: 406–10.Google Scholar
  86. 86.
    Snowdon DA, Phillips RL, Choi W. Diet obesity, and risk of fatal prostate cancer. Am J Epidemiol 1984; 120: 244–50.Google Scholar
  87. 87.
    Mills PK, Beeson WL, Phillips RL, Fraser GE. Cohort study of diet, lifestyle, and prostate cancer in Adventist men. Cancer 1989; 64: 598–604.Google Scholar
  88. 88.
    Le Marchand L, Kolonel LN, Wilkens LR, Myers BC, Hirohata T. Animal fat consumption and prostate cancer: a prospective study in Hawaii. Epidemiology 1994; 5: 276–82.Google Scholar
  89. 89.
    Giovannucci E, Rimm EB, Wolk A, Ascherio A, Stampfer MJ, Colditz GA, Willett WC. Calcium and fructose intake in relation to risk of prostate cancer. Cancer Res 1998; 58: 442–7.Google Scholar
  90. 90.
    Chan JM, Giovannucci E, Andersson S-O, Yuen J, Adami H-O, Wolk A. Dairy products, calcium, phosphorous, vitamin D, and risk of prostate cancer. Cancer Causes Control 1998; 9: 559–66.Google Scholar
  91. 91.
    Park YK, Yetley EA. Intakes and food sources of fructose in the United States. Am J Clin Nutr 1993; 58 (suppl): 737s–747s.Google Scholar
  92. 92.
    Armstrong B, Doll R. Environmental factors and cancer incidence and mortality in different countries, with special reference to dietary practices. Int J Cancer 1975; 15: 617–31.Google Scholar
  93. 93.
    Graham S, Haughey B, Marshall J, Priore R, Byers T, Rzepka T, Mettlin C, Pontes JE. Diet in the epidemiology of carcinoma of the prostate gland. J Natl Cancer Inst 1983; 70: 687–92.Google Scholar
  94. 94.
    Heshmat MY, Kaul L, Kovi J, Jackson MA, Jackson AG, Jones GW, Edson M, Enterline JP, Worrell RG, Perry SL. Nutrition and prostate cancer: a case-control study. Prostate 1985; 6: 7–17.Google Scholar
  95. 95.
    Ross RK, Shimizu H, Paganini-Hill A, Honda G, Henderson BE. Case-control studies of prostate cancer in Blacks and Whites in Southern California. J Natl Cancer Inst 1987; 78: 869–74.Google Scholar
  96. 96.
    Ohno Y, Yoshida O, Oishi K, Okada K, Yamabe H, Schroeder FH. Dietary beta-carotene and cancer of the prostate: a case-control study in Kyoto, Japan. Cancer Res 1988; 48: 1331–36.Google Scholar
  97. 97.
    Kolonel LN, Yoshizawa CN, Hankin JH. Diet and prostatic cancer: a case-control study in Hawaii. Am J Epidemiol 1988; 127: 999–1012.Google Scholar
  98. 98.
    Kaul L, Heshmat MY, Kovi J, Jackson MA, Jackson AG, Jones GW, Edson M, Enterline JP, Worrell RG, Perry SL. The role of diet in prostate cancer. Nutr Cancer 1987; 9: 123–8.Google Scholar
  99. 99.
    West DW, Slattery ML, Robison LM, French TK, Mahoney AW. Adult dietary intake and prostate cancer risk in Utah: a case-control study with special emphasis on aggressive tumors. Cancer Causes Control 1991; 2: 85–94.Google Scholar
  100. 100.
    Whittemore AS, Kolonel LN, Wu AH, John EM, Gallagher RP, Howe GR, Burch JD, Hankin J, Dreon DM, West DW, Teh CZ, Paffenbarger RS, Jr. Prostate cancer in relation to diet, physical activity, and body size in blacks, whites, and Asians in the United States and Canada. J Natl Cancer Inst 1995; 87: 652–61.Google Scholar
  101. 101.
    Andersson S-O, Wolk A, Bergström R, Giovannucci E, Lindgren C, Baron J, Adami H-O. Energy, nutrient intake and prostate cancer risk: a population-based case-control study in Sweden. Int J Cancer 1996; 68: 716–22.Google Scholar
  102. 102.
    Hirayama T. Epidemiology of prostate cancer with special reference to the role of diet. Natl Cancer Inst Monogr 1979; 53: 149–55.Google Scholar
  103. 103.
    Severson RK, Nomura AMY, Grove JS, Stemmermann GN. A prospective study of demographics, diet, and prostate cancer among men of Japanese ancestry in Hawaii. Cancer Res 1989; 49: 1857–60.Google Scholar
  104. 104.
    Hsing AW, McLaughlin JK, Schuman LM, Bjelke E, Gridley G, Wacholder S, Chien HT, Blot WJ. Diet, tobacco use, and fatal prostate cancer: results from the Lutheran Brotherhood Cohort Study. Cancer Res 1990; 50: 6836–40.Google Scholar
  105. 105.
    Giovannucci E, Rimm EB, Colditz GA, Stampfer MJ, Ascherio A, Chute CC, Willett WC. A prospective study of dietary fat and risk of prostate cancer. J Natl Cancer Inst 1993; 85: 1571–79.Google Scholar
  106. 106.
    Gann PH, Hennekens CH, Sacks FM, Grodstein F, Giovannucci E, Stampfer MJ. Prospective study of plasma fatty acids and risk of prostate cancer. J Natl Cancer Inst 1994; 86: 281–6.Google Scholar
  107. 107.
    Arnaud CD. The calciotropic hormones and metabolic bone disease. In: Greenspan FS, Baxter JD, eds. Basic and Clinical Endocrinology. Norwalk, CT: Appleton & Lange, 1994; 227–42.Google Scholar
  108. 108.
    Hämäläinen E, Adlercreutz H, Puska P, Pietinen P. Diet and serum sex hormones in healthy men. J Steroid Biochem 1984; 20: 459–64.Google Scholar
  109. 109.
    Gann PH, Hennekens CH, Ma J, Longcope C, Stampfer MJ. A prospective study of sex hormone levels and risk of prostate cancer. J Natl Cancer Inst 1996; 88: 1118–26.Google Scholar
  110. 110.
    Field AE, Colditz GA, Willett WC, Longcope C, McKinlay JB. The relation of smoking, age, relative weight, and dietary intake to serum adrenal steroids, sex hormones, and sex hormone-binding globulin in middle aged men. J Clin Endocrinol Metab 1994; 79: 1310–6.Google Scholar
  111. 111.
    Committee on Diet Nutrition and Cancer — Assembly of Life Sciences — National Research Council. Diet, Nutrition, and Cancer. Washington, DC: National Academy Press, 1982.Google Scholar
  112. 112.
    National Research Council — Committee on Diet and Health. Diet and Health: Implications for Reducing Chronic Disease Risk. Washington, DC: National Academy Press, 1989.Google Scholar
  113. 113.
    National Cancer Institute. Diet, Nutrition, and Cancer Prevention: A Guide to Food Choices. NIH Pub. No. 87-28-78, ed. PHS National Institutes of Health, U.S. Dept. Health and Human Services. Washington, DC: U.S. Government Printing Office, 1987.Google Scholar
  114. 114.
    Hegsted DM. Calcium and osteoporosis. J Nutr 1986; 116: 2316–9.Google Scholar
  115. 115.
    Abelow BJ, Holford TR, Insogna KL. Cross-cultural association between dietary animal protein and hip fracture: a hypothesis. Calcif Tissue Int 1992; 50: 14–8.Google Scholar
  116. 116.
    Heaney RP, Weaver CM. Oxalate: effect on calcium absorbability. Am J Clin Nutr 1989; 50: 830–2.Google Scholar
  117. 117.
    Heaney RP, Weaver CM, Fitzsimmons ML. Soybean phytate content: effect on calcium absorption. Am J Clin Nutr 1991; 53: 745–7.Google Scholar
  118. 118.
    Lemann J, Jr., Litzow JR, Lennon EJ. The effects of chronic acid loads in normal man: further evidence for the participation of bone mineral in the defense against chronic metabolic acidosis. J Clin Invest 1966; 45: 1608–14.Google Scholar
  119. 119.
    Krieger NS, Sessler NE, Bushinsky DA. Acidosis inhibits osteoblastic and stimulates osteoclastic activity in vitro. Am J Physiol 1992; 262: F442–8.Google Scholar
  120. 120.
    Heaney RP. Thinking straight about calcium. N Engl J Med 1993; 328: 503–4.Google Scholar
  121. 121.
    Feskanich D, Willett WC, Stampfer MJ, Colditz GA. Protein consumption and bone fractures in women. Am J Epidemiol 1996; 143: 472–9.Google Scholar
  122. 122.
    Feskanich D, Willett WC, Stampfer MJ, Colditz GA. Milk, dietary calcium, bone fractures in women: A 12-year prospective study. Am J Public Health 1997; 87: 992–7.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Edward Giovannucci
    • 1
    • 2
  1. 1.Channing Laboratory, Department of Medicine, Brigham and Women's Hospital andHarvard Medical SchoolUSA
  2. 2.Departments of Nutrition and EpidemiologyHarvard School of Public HealthBostonUSA.

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