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Cited by 113Phytoestrogen effects and researchEstrogen and related hormone effectsNutritional Studies and Diet

Perspectives on the soy-breast cancer relation

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Messina, Mark, Wu, Anna H·2009·The American Journal of Clinical Nutrition
DOI 10.3945/ajcn.2009.26736v
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Abstract

There has been considerable investigation of the potential for soy foods to reduce risk of breast cancer. Initial enthusiasm for this research was partially based on the historically low incidence rates of breast cancer and high soy food intake in Japan. There are several putative soybean chemopreventive agents, but most cancer research has focused on isoflavones. Isoflavones possess both hormonal and nonhormonal properties relevant to carcinogenesis. Recent epidemiologic analyses indicate that among Asians high soy intake is associated with an approximate one-third reduction in the risk of both pre- and postmenopausal breast cancer. However, several lines of evidence suggest that to derive maximum protection against breast cancer, soy must be consumed early in life. This evidence is consistent with the lack of significant effects noted in clinical studies that have evaluated the effects of isoflavone-containing products on breast cancer risk markers. Isoflavones may exert their putative protective effects by stimulating breast cell differentiation in a manner similar to that which is thought to occur during early pregnancy. Finally, the ability of the isoflavone genistein to stimulate the growth of mammary tumors in ovariectomized athymic nude mice implanted with estrogen-sensitive breast cancer cells has raised concern that soy foods, and especially isoflavone supplements, are contraindicated for patients with breast cancer and women at high risk of breast cancer. However, findings from clinical studies, in which breast biopsies have been taken or breast tissue density measured after isoflavone exposure, are reassuring and contrast with the proliferative effects of conventional combined hormone therapy, although understanding of the effect of soy and isoflavones on breast tissues remains imprecise.

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  1. Zhang B, Chen YM, Huang LL, et al. Greater habitual soyfood con- sumption is associated with decreased carotid intima-media thickness and better plasma lipids in Chinese middle-aged adults. Atherosclerosis 2008;198:403-11.
  2. Kokubo Y, Iso H, Ishihara J, Okada K, Inoue M, Tsugane S. Associ- ation of dietary intake of soy, beans, and isoflavones with risk of ce- rebral and myocardial infarctions in Japanese populations: the Japan Public Health Center-based (JPHC) study cohort I. Circulation 2007; 116:2553-62.
  3. Zhang X, Shu XO, Gao YT, et al. Soy food consumption is associated with lower risk of coronary heart disease in Chinese women. J Nutr 2003;133:2874-8.
  4. Ma DF, Qin LQ, Wang PY, Katoh R. Soy isoflavone intake increases bone mineral density in the spine of menopausal women: meta-analysis of randomized controlled trials. Clin Nutr 2008;27:57-64.
  5. Zhang X, Shu XO, Li H, et al. Prospective cohort study of soy food consumption and risk of bone fracture among postmenopausal women. Arch Intern Med 2005;165:1890-5.
  6. Wu AH, Yu MC, Tseng CC, Pike MC. Epidemiology of soy exposures and breast cancer risk. Br J Cancer 2008;98:9-14.
  7. Messina MJ. Emerging evidence on the role of soy in reducing prostate cancer risk. Nutr Rev 2003;61:117-31.
  8. Messina M, Barnes S. The role of soy products in reducing risk of cancer. J Natl Cancer Inst 1991;83:541-6.
  9. Franke AA, Custer LJ, Wang W, Shi CY. HPLC analysis of iso- flavonoids and other phenolic agents from foods and from human fluids. Proc Soc Exp Biol Med 1998;217:263-73.
  10. Barnes S, Grubbs C, Setchell KD, Carlson J. Soybeans inhibit mam- mary tumors in models of breast cancer. Prog Clin Biol Res 1990;347: 239-53.
  11. Messina M, Nagata C, Wu AH. Estimated Asian adult soy protein and isoflavone intakes. Nutr Cancer 2006;55:1-12.
  12. Wakai K, Suzuki S, Ohno Y, Kawamura T, Tamakoshi A, Aoki R. Epidemiology of breast cancer in Japan. Int J Epidemiol 1995;24: 285-91.
  13. Perkin AG, Newbury FG. The colouring matters contained in Dyer's broom (Genista tinctoria) and heather (Calluna vulgaris). J Chem Soc 1899;75:830-9.
  14. Walz VE. Isoflavon-und saponin-glucoside in soja hispida. Justus Liebigs Ann Chem 1931;489:118-55 (in German).
  15. Walter ED. Genistin (an isoflavone glucoside) and its aglucone, gen- istein, from soybeans. J Am Chem Soc 1941;63:3273-6.
  16. Naim M, Gestetner B, Kirson I, Birk Y, Bondi A. A new isoflavone from soya beans. Phytochemistry 1973;12:169-70.
  17. Marrian GF, Haselwood GAD, Equol CXLV. A new active phenol isolated from ketohydroxyestrin fraction of mares urine. Biochem J 1932;26:1226-32.
  18. Axelson M, Setchell KD. The excretion of lignans in rats-evidence for an intestinal bacterial source for this new group of compounds. FEBS Lett 1981;123:337-42.
  19. Axelson M, Kirk DN, Farrant RD, Cooley G, Lawson AM, Setchell KD. The identification of the weak oestrogen equol [7-hydroxy-3- (4#-hydroxyphenyl)chroman] in human urine. Biochem J 1982;201: 353-7.
  20. Bannwart C, Fotsis T, Heikkinen R, Adlercreutz H. Identification of the isoflavonic phytoestrogen daidzein in human urine. Clin Chim Acta 1984;136:165-72.
  21. Atkinson C, Frankenfeld CL, Lampe JW. Gut bacterial metabolism of the soy isoflavone daidzein: exploring the relevance to human health. Exp Biol Med (Maywood) 2005;230:155-70.
  22. Setchell KD, Brown NM, Lydeking-Olsen E. The clinical importance of the metabolite equol-a clue to the effectiveness of soy and its iso- flavones. J Nutr 2002;132:3577-84.
  23. Axelson M, Sjovall J, Gustafsson BE, Setchell KD. Soya-a dietary source of the non-steroidal oestrogen equol in man and animals. J Endocrinol 1984;102:49-56.
  24. Setchell KD, Borriello SP, Hulme P, Kirk DN, Axelson M. Non- steroidal estrogens of dietary origin: possible roles in hormone-de- pendent disease. Am J Clin Nutr 1984;40:569-78.
  25. Cheng E, Story CD, Yoder L, Hale WH, Burroughs W. Estrogenic activity of isoflavone derivatives extracted and prepared from soybean oil meal. Science 1953;118:164-5.
  26. Carter MW, Smart WWG Jr Matrone G. Estimation of the estrogenic activity of genistein obtained from soybean meal (20693). Proc Soc Exp Biol Med 1953;84:506-7.
  27. Folman Y, Pope GS. The interaction in the immature mouse of potent oestrogens with coumestrol, genistein and other utero-vaginotrophic compounds of low potency. J Endocrinol 1966;34:215-25.
  28. Folman Y, Pope GS. Effect of norethisterone acetate, dimethyl- stilboestrol, genistein and coumestrol on uptake of [3H]oestradiol by uterus, vagina and skeletal muscle of immature mice. J Endocrinol 1969;44:213-8.
  29. Setchell KD. Naturally occurring, non-steroidal estrogens of dietary origin. In: McLachlan J, ed. Estrogens in the environment. Burlington, MA: Elsevier Science Publishing Co, 1985:69-86
  30. Adlercreutz H, Fotsis T, Heikkinen R, et al. Excretion of the lignans enterolactone and enterodiol and of equol in omnivorous and vege- tarian postmenopausal women and in women with breast cancer. Lancet 1982;2:1295-9.
  31. Ma DF, Qin LQ, Wang PY, Katoh R. Soy isoflavone intake inhibits bone resorption and stimulates bone formation in menopausal women: meta-analysis of randomized controlled trials. Eur J Clin Nutr 2008;62: 155-61.
  32. Williamson-Hughes PS, Flickinger BD, Messina MJ, Empie MW. Isoflavone supplements containing predominantly genistein reduce hot flash symptoms: a critical review of published studies. Menopause 2006;13:831-9.
  33. Muthyala RS, Ju YH, Sheng S, et al. Equol, a natural estrogenic me- tabolite from soy isoflavones: convenient preparation and resolution of R-and S-equols and their differing binding and biological activity through estrogen receptors alpha and beta. Bioorg Med Chem 2004;12: 1559-67.
  34. Jefferson WN, Newbold RR. Potential endocrine-modulating effects of various phytoestrogens in the diet. Nutrition 2000;16:658-62.
  35. Pasqualini JR, Chetrite G, Blacker C, et al. Concentrations of estrone, estradiol, and estrone sulfate and evaluation of sulfatase and aromatase activities in pre-and postmenopausal breast cancer patients. J Clin Endocrinol Metab 1996;81:1460-4.
  36. Kuiper GG, Enmark E, Pelto-Huikko M, Nilsson S, Gustafsson JA. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci U S A 1996;93:5925-30.
  37. Kuiper GG, Lemmen JG, Carlsson B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocri- nology 1998;139:4252-63.
  38. Kuiper GG, Carlsson B, Grandien K, et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen re- ceptors alpha and beta. Endocrinology 1997;138:863-70.
  39. Strom A, Hartman J, Foster JS, Kietz S, Wimalasena J, Gustafsson JA. Estrogen receptor b inhibits 17b-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc Natl Acad Sci U S A 2004;101: 1566-71.
  40. Park BW, Kim KS, Heo MK, et al. Expression of estrogen receptor- beta in normal mammary and tumor tissues: is it protective in breast carcinogenesis? Breast Cancer Res Treat 2003;80:79-85.
  41. Brzezinski A, Adlercreutz H, Shaoul R, et al. Short-term effect of phytoestrogen-rich diet on postmenopausal women. Menopause 1997; 4:89-94.
  42. Diel P, Geis RB, Caldarelli A, et al. The differential ability of the phytoestrogen genistein and of estradiol to induce uterine weight and proliferation in the rat is associated with a substance specific modu- lation of uterine gene expression. Mol Cell Endocrinol 2004;221: 21-32.
  43. D'Anna R, Baviera G, Corrado F, Cancellieri F, Crisafulli A, Squadrito F. The effect of the phytoestrogen genistein and hormone replacement therapy on homocysteine and C-reactive protein level in post- menopausal women. Acta Obstet Gynecol Scand 2005;84:474-7.
  44. Garrido A, De la Maza MP, Hirsch S, Valladares L. Soy isoflavones affect platelet thromboxane A2 receptor density but not plasma lipids in menopausal women. Maturitas 2006;54:270-6.
  45. Hall WL, Vafeiadou K, Hallund J, et al. Soy-isoflavone-enriched foods and markers of lipid and glucose metabolism in postmenopausal women: interactions with genotype and equol production. Am J Clin Nutr 2006;83:592-600.
  46. Katz DL, Evans MA, Njike VY, et al. Raloxifene, soy phytoestrogens and endothelial function in postmenopausal women. Climacteric 2007; 10:500-7.
  47. Cheng G, Wilczek B, Warner M, Gustafsson JA, Landgren BM. Iso- flavone treatment for acute menopausal symptoms. Menopause 2007; 14:468-73.
  48. Bruce B, Messina M, Spiller GA. Isoflavone supplements do not affect thyroid function in iodine-replete postmenopausal women. J Med Food 2003;6:309-16.
  49. Marini H, Minutoli L, Polito F, et al. Effects of the phytoestrogen genistein on bone metabolism in osteopenic postmenopausal women: a randomized trial. Ann Intern Med 2007;146:839-47.
  50. Sammartino A, Di Carlo C, Mandato VD, Bifulco G, Di Stefano M, Nappi C. Effects of genistein on the endometrium: ultrasonographic evaluation. Gynecol Endocrinol 2003;17:45-9.
  51. Kaari C, Haidar MA, Junior JM, et al. Randomized clinical trial comparing conjugated equine estrogens and isoflavones in post- menopausal women: a pilot study. Maturitas 2006;53:49-58.
  52. Ogawara H, Akiyama T, Ishida J, Watanabe S, Suzuki K. A specific inhibitor for tyrosine protein kinase from Pseudomonas. J Antibiot (Tokyo) 1986;39:606-8.
  53. Akiyama T, Ishida J, Nakagawa S, et al. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem 1987;262:5592-5.
  54. Akiyama T, Ogawara H. Use and specificity of genistein as inhibitor of protein-tyrosine kinases. Methods Enzymol 1991;201:362-70.
  55. Hunter T, Cooper JA. Protein-tyrosine kinases. Annu Rev Biochem 1985;54:897-930.
  56. Sarkar FH, Li Y. Soy isoflavones and cancer prevention. Cancer Invest 2003;21:744-57.
  57. Pritchard KI. Should observational studies be a thing of the past? J Natl Cancer Inst 2008;100:451-2.
  58. Rossouw JE, Anderson GL, Prentice RL, et al. Writing Group for the Women's Health Initiative Investigators. 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.
  59. Barrett-Connor E, Grady D. Hormone replacement therapy, heart dis- ease, and other considerations. Annu Rev Public Health 1998;19: 55-72.
  60. Baigent C, Clarke R. B vitamins for the prevention of vascular disease: insufficient evidence to justify treatment. JAMA 2007;298:1212-4.
  61. Prentice RL. Future possibilities in the prevention of breast cancer: fat and fiber and breast cancer research. Breast Cancer Res 2000;2:268-76.
  62. Wu AH, Pike MC, Stram DO. Meta-analysis: dietary fat intake, serum estrogen levels, and the risk of breast cancer. J Natl Cancer Inst 1999; 91:529-34.
  63. Holmes MD, Hunter DJ, Colditz GA, et al. Association of dietary intake of fat and fatty acids with risk of breast cancer. JAMA 1999;281:914-20.
  64. Holmes MD, Schisterman EF, Spiegelman D, Hunter DJ, Willett WC. Re: Meta-analysis: dietary fat intake, serum estrogen levels, and the risk of breast cancer. J Natl Cancer Inst 1999;91:1511-2 (letter).
  65. Cohen LA. Dietary fiber and breast cancer. Anticancer Res 1999;19: 3685-8.
  66. Smith-Warner SA, Spiegelman D, Yaun SS, et al. Intake of fruits and vegetables and risk of breast cancer: a pooled analysis of cohort studies. JAMA 2001;285:769-76.
  67. Michels KB, Mohllajee AP, Roset-Bahmanyar E, Beehler GP, Moysich KB. Diet and breast cancer: a review of the prospective observational studies. Cancer 2007;109:2712-49.
  68. Horn-Ross PL, John EM, Canchola AJ, Stewart SL, Lee MM. Phy- toestrogen intake and endometrial cancer risk. J Natl Cancer Inst 2003; 95:1158-64.
  69. Goodman-Gruen D, Kritz-Silverstein D. Usual dietary isoflavone in- take is associated with cardiovascular disease risk factors in post- menopausal women. J Nutr 2001;131:1202-6.
  70. de Kleijn MJ, van der Schouw YT, Wilson PW, et al. Intake of dietary phytoestrogens is low in postmenopausal women in the United States: the Framingham study (1-4). J Nutr 2001;131:1826-32.
  71. Cutler GJ, Nettleton JA, Ross JA, et al. Dietary flavonoid intake and risk of cancer in postmenopausal women: the Iowa Women's Health Study. Int J Cancer 2008;123:664-71.
  72. van der Schouw YT, Kreijkamp-Kaspers S, Peeters PH, Keinan-Boker L, Rimm EB, Grobbee DE. Prospective study on usual dietary phy- toestrogen intake and cardiovascular disease risk in Western women. Circulation 2005;111:465-71.
  73. Boker LK, Van der Schouw YT, De Kleijn MJ, Jacques PF, Grobbee DE, Peeters PH. Intake of dietary phytoestrogens by Dutch women. J Nutr 2002;132:1319-28.
  74. Umphress ST, Murphy SP, Franke AA, Custer LJ, Blitz CL. Isoflavone content of foods with soy additives. J Food Compost Anal 2005;18: 533-50.
  75. Pisani P, Bray F, Parkin DM. Estimates of the world-wide prevalence of cancer for 25 sites in the adult population. Int J Cancer 2002;97: 72-81.
  76. Ajiki W, Tsukuma H, Oshima A. Cancer incidence and incidence rates in Japan in 1999: estimates based on data from 11 population-based cancer registries. Jpn J Clin Oncol 2004;34:352-6.
  77. Lee HP, Gourley L, Duffy SW, Esteve J, Lee J, Day NE. Dietary effects on breast-cancer risk in Singapore. Lancet 1991;337:1197-200.
  78. Trock BJ, Hilakivi-Clarke L, Clarke R. Meta-analysis of soy intake and breast cancer risk. J Natl Cancer Inst 2006;98:459-71.
  79. Messina M. Western soy intake is too low to produce health effects. Am J Clin Nutr 2004;80:528-9.
  80. Dai Q, Shu XO, Jin F, et al. Population-based case-control study of soyfood intake and breast cancer risk in Shanghai. Br J Cancer 2001; 85:372-8.
  81. Wu AH, Wan P, Hankin J, Tseng CC, Yu MC, Pike MC. Adolescent and adult soy intake and risk of breast cancer in Asian-Americans. Carcinogenesis 2002;23:1491-6.
  82. Yamamoto S, Sobue T, Kobayashi M, Sasaki S, Tsugane S. Soy, iso- flavones, and breast cancer risk in Japan. J Natl Cancer Inst 2003;95: 906-13.
  83. Lee HP, Gourley L, Duffy SW, Esteve J, Lee J, Day NE. Risk factors for breast cancer by age and menopausal status: a case-control study in Singapore. Cancer Causes Control 1992;3:313-22.
  84. Hirose K, Tajima K, Hamajima N, et al. A large-scale, hospital-based case-control study of risk factors of breast cancer according to men- opausal status. Jpn J Cancer Res 1995;86:146-54.
  85. Yuan JM, Wang QS, Ross RK, Henderson BE, Yu MC. Diet and breast cancer in Shanghai and Tianjin, China. Br J Cancer 1995;71:1353-8.
  86. Wu AH, Ziegler RG, Horn-Ross PL, et al. Tofu and risk of breast cancer in Asian-Americans. Cancer Epidemiol Biomarkers Prev 1996; 5:901-6.
  87. Chie WC, Lee WC, Li CY, Huang CS, Chang KJ, Lin RS. Soybean products, vegetable and fruit and breast cancer risk in Taiwan. Breast Cancer Res Treat 1997;46:80 (abstr).
  88. Shu XO, Jin F, Dai Q, et al. Soyfood Intake during adolescence and subsequent risk of breast cancer among Chinese women. Cancer Epi- demiol Biomarkers Prev 2001;10:483-8.
  89. Hirose K, Imaeda N, Tokudome Y, et al. Soybean products and re- duction of breast cancer risk: a case-control study in Japan. Br J Cancer 2005;93:15-22.
  90. Lee MM, Chang IY, Horng CF, Chang JS, Cheng SH, Huang A. Breast cancer and dietary factors in Taiwanese women. Cancer Causes Control 2005;16:929-37.
  91. Shannon J, Ray R, Wu C, et al. Food and botanical groupings and risk of breast cancer: a case-control study in shanghai, china. Cancer Epi- demiol Biomarkers Prev 2005;14:81-90.
  92. Do MH, Lee SS, Jung PJ, Lee MH. Intake of fruits, vegetables, and soy foods in relation to breast cancer risk in Korean women: a case-control study. Nutr Cancer 2007;57:20-7.
  93. Iwasaki M, Inoue M, Otani T, et al. Plasma isoflavone level and sub- sequent risk of breast cancer among Japanese women: a nested case-control study from the Japan Public Health Center-Based Pro- spective Study Group. J Clin Oncol 2008;26:1677-83.
  94. Lampe JW, Nishino Y, Ray RM, et al. Plasma isoflavones and fibro- cystic breast conditions and breast cancer among women in Shanghai, China. Cancer Epidemiol Biomarkers Prev 2007;16:2579-86.
  95. Travis RC, Allen NE, Appleby PN, Spencer EA, Roddam AW, Key TJ. A prospective study of vegetarianism and isoflavone intake in relation to breast cancer risk in British women. Int J Cancer 2008;122:705-10.
  96. Wu AH, Koh WP, Wang R, Lee HP, Yu MC. Soy intake and breast cancer risk in Singapore Chinese Health Study. Br J Cancer 2008;99: 196-200. 100. Thanos J, Cotterchio M, Boucher BA, Kreiger N, Thompson LU. Adolescent dietary phytoestrogen intake and breast cancer risk (Can- ada). Cancer Causes Control 2006;17:1253-61. 101. Korde LA, Wu AH, Fears T, et al. Childhood soy intake and breast cancer risk in Asian-American women. Cancer Epidemiol Prev Biomarkers (in press). 102. Lamartiniere CA, Zhao YX, Fritz WA. Genistein: mammary cancer chemoprevention, in vivo mechanisms of action, potential for toxicity and bioavailability in rats. J Womens Cancer 2000;2:11-9. 103. Russo J, Russo IH. The role of estrogen in the initiation of breast cancer. J Steroid Biochem Mol Biol 2006;102:89-96. 104. Meng L, Maskarinec G, Wilkens L. Ethnic differences and factors related to breast cancer survival in Hawaii. Int J Epidemiol 1997;26:1151-8. 105. Yonemoto RH. Breast cancer in Japan and United States: epidemiol- ogy, hormone receptors, pathology, and survival. Arch Surg 1980;115: 1056-62. 106. Morrison AS, Lowe CR, MacMahon B, Ravnihar B, Yuasa S. Some international differences in treatment and survival in breast cancer. Int J Cancer 1976;18:269-73. 107. Ohsumi S, Sakamoto G, Takashima S, et al. Long-term results of breast-conserving treatment for early-stage breast cancer in Japanese women from multicenter investigation. Jpn J Clin Oncol 2003;33:61-7. 108. Kanemori M, Prygrocki M. Results of breast conservation therapy from a single-institution community hospital in Hawaii with a predominantly Japanese population. Int J Radiat Oncol Biol Phys 2005;62:193-7. 109. Doyle C, Kushi LH, Byers T, et al. Nutrition and physical activity during and after cancer treatment: an American Cancer Society guide for informed choices. CA Cancer J Clin 2006;56:323-53. 110. Hsieh CY, Santell RC, Haslam SZ, Helferich WG. Estrogenic effects of genistein on the growth of estrogen receptor-positive human breast cancer (MCF-7) cells in vitro and in vivo. Cancer Res 1998;58:3833-8. 111. Ju YH, Allred CD, Allred KF, Karko KL, Doerge DR, Helferich WG. Physiological concentrations of dietary genistein dose-dependently stimulate growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in athymic nude mice. J Nutr 2001;131:2957-62. 112. Allred CD, Ju YH, Allred KF, Chang J, Helferich WG. Dietary genistin stimulates growth of estrogen-dependent breast cancer tumors similar to that observed with genistein. Carcinogenesis 2001;22:1667-73. 113. Allred CD, Allred KF, Ju YH, Virant SM, Helferich WG. Soy diets containing varying amounts of genistein stimulate growth of estrogen- dependent (MCF-7) tumors in a dose-dependent manner. Cancer Res 2001;61:5045-50. 114. Allred CD, Allred KF, Ju YH, Goeppinger TS, Doerge DR, Helferich WG. Soy processing influences growth of estrogen-dependent breast cancer tumors. Carcinogenesis 2004;25:1649-57. 115. Ju YH, Fultz J, Allred KF, Doerge DR, Helferich WG. Effects of di- etary daidzein and its metabolite, equol, at physiological concen- trations on the growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in ovariectomized athymic mice. Carci- nogenesis 2006;27:856-63. 116. Anupongsanugool E, Teekachunhatean S, Rojanasthien N, Pongsatha S, Sangdee C. Pharmacokinetics of isoflavones, daidzein and genistein, after ingestion of soy beverage compared with soy extract capsules in postmenopausal Thai women. BMC Clin Pharmacol 2005;5:2 117.
  97. Ryan-Borchers TA, Park JS, Chew BP, McGuire MK, Fournier LR, Beerman KA. Soy isoflavones modulate immune function in healthy postmenopausal women. Am J Clin Nutr 2006;83:1118-25. 118. Allred CD, Allred KF, Ju YH, et al. Dietary genistein results in larger MNU-induced, estrogen-dependent mammary tumors following ovariectomy of Sprague-Dawley rats. Carcinogenesis 2004;25:211-8. 119. Hooshmand S, Khalil DA, Singletary K, Kamath SK, Arjmandi BH. The combination of genistin and ipriflavone prevents mammary tu- morigenesis and modulates lipid profile. Clin Nutr 2008;27:643-8. 120. Zhou JR, Yu L, Zhong Y, et al. Inhibition of orthotopic growth and metastasis of androgen-sensitive human prostate tumors in mice by bioactive soybean components. Prostate 2002;53:143-53. 121. Zhou JR, Yu L, Mai Z, Blackburn GL. Combined inhibition of estrogen- dependent human breast carcinoma by soy and tea bioactive compo- nents in mice. Int J Cancer 2004;108:8-14. 122. Hawrylewicz EJ, Zapata JJ, Blair WH. Soy and experimental cancer: animal studies. J Nutr 1995;125:698S-708S. 123. Sartippour MR, Rao JY, Apple S, et al. A pilot clinical study of short-term isoflavone supplements in breast cancer patients. Nutr Cancer 2004;49:59-65. 124. Palomares MR, Hopper L, Goldstein L, et al. Effect of soy isoflavones on breast proliferation in postmenopausal breast cancer survivors. Breast Cancer Res Treat 2004;88(suppl):S149 (abstr). 125. Hargreaves DF, Potten CS, Harding C, et al. Two-week dietary soy supplementation has an estrogenic effect on normal premenopausal breast. J Clin Endocrinol Metab 1999;84:4017-24. 126. Maskarinec G, Williams AE, Carlin L. Mammographic densities in a one-year isoflavone intervention. Eur J Cancer Prev 2003;12:165-9. 127. Maskarinec G, Franke AA, Williams AE, et al. Effects of a 2-year randomized soy intervention on sex hormone levels in premenopausal women. Cancer Epidemiol Biomarkers Prev 2004;13:1736-44. 128. Atkinson C, Warren RM, Sala E, et al. Red-clover-derived isoflavones and mammographic breast density: a double-blind, randomized, placebo- controlled trial. Breast Cancer Res 2004;6:R170-9. 129.

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Sorted by citations

Authors
Messina, M., & Wu, A. H.
Affiliations
University of Southern California (US)
Corresponding author
Messina, Mark
ORCID
Venue
The American Journal of Clinical Nutrition
Publisher
Elsevier BV
Published
2009-05
Volume
89
Issue
5
Pages
1673S-1679S
ISSN
0002-9165 (ISSN-L)
DOI
10.3945/ajcn.2009.26736v
OpenAlex
W2152246981
Cited by
113
References
5
Citations by year
2026: 1 · 2025: 1 · 2024: 2 · 2023: 1 · 2020: 1 · 2019: 2 · 2018: 4 · 2017: 7 · 2016: 2 · 2015: 6 · 2014: 4 · 2013: 13 · 2012: 14
FWCI
15.37
Type
journal article
Language
en
Open access
Licence
Locations
  • American Journal of Clinical Nutrition (publishedVersion)
  • PubMed (publishedVersion)
  • UCLA - Biblioteca de Ciencias de la Salud (submittedVersion)
Topics
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Phytoestrogen effects and research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
Keywords
soy products, breast cancer, isoflavones, genistein, chemoprevention, breast cancer risk reduction, Asian populations, breast density, carcinogenesis
MeSH terms
Animals, Breast Neoplasms, Female, Humans, Isoflavones, Mice, Nude, Ovariectomy, Risk Factors, Mammary Neoplasms, Animal, Genistein, Soy Foods, Mice

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