Abstract
Objective
To evaluate whether phytoestrogen intake is associated with reduced breast cancer risk, using a novel phytoestrogen database.
Methods
Population-based breast cancer cases aged 25–74 years (diagnosed 2002–2003) were identified using Ontario Cancer Registry (n = 3,063) and controls (n = 3,430) were an age-stratified random sample of women identified through random digit dialing. An epidemiologic and Block food frequency questionnaire—expanded to include phytoestrogen-containing foods—was mailed to all subjects. The recently published Ontario phytoestrogen database was applied to FFQ responses to estimate intake. Multivariate logistic regression provided odds ratio (OR) estimates, while controlling for confounders.
Results
Among all women, lignan intake was associated with a reduced breast cancer risk (Q5 vs. Q1 MVOR: 0.81, 95% CI: 0.65, 0.99); however, following stratification by BMI, this reduction in risk was statistically significant only among overweight (BMI > 25) women. Total phytoestrogen intake was also associated with a risk reduction among overweight women only. Among pre-menopausal women, total phytoestrogen intake was associated with a significant reduction in breast cancer risk among overweight women only (Q5 vs. Q1 MVOR: 0.51, 95% CI: 0.30, 0.87). Among post-menopausal women, no statistically significant association was observed between breast cancer risk and isoflavones or lignans.
Conclusion
Lignan intake may be associated with reduced breast cancer risk among pre-menopausal women, and our data suggest BMI modifies this association.
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References
Thompson LU, Boucher BA, Liu Z, Cotterchio M, Kreiger N (2006) Phytoestrogen content of foods consumed in Canada, including isoflavones, lignans and coumestan. Nutr Cancer 54:184–201
Horn-Ross P, Lee M, John EM, Koo J (2000) Sources of phytoestrogen exposure among non-Asian women in California, USA. Cancer Causes Control 11:299–302
Milder I, Feskens E, Arts I, de Mesquita H, Hollman P, Kromhout D (2005) Intake of the plant lignans Secoisolariciresinol, matairesinol, lariciresinol, and pinoresinol in Dutch men and women. J Nutr 135:1202–1207
Gallo D, Giacomelli S, Cantelmo F et al (2001) Chemoprevention of DMBA-induced mammary cancer in rats by dietary soy. Breast Cancer Res Treat 69:153–164
Kim H, Hall P, Smith M, Kirk M, Prasain J, Barnes S, Grubbs C (2004) Chemoprevention by grape seed extract and genistein in carcinogen-induced mammary cancer in rats is diet dependent. J Nutr 134(supp12):3445S–3452S
Chen J, Thompson L (2003) Lignans and tamoxifen, alone or in combination, reduce human breast cancer cell adhesion, invasion and migration in vitro. Breast Cancer Res Treat 80:163–170
Thompson L, Seidl M, Rickard S, Orcheson L, Fong H (1996) Antitumorigenic effect of a mammalian lignan precursor from flaxseed. Nutr Cancer 26:159–165
Saarinen N, Huovinen R, Warri A, Makela S et al (2002) Enterolactone inhibits the growth of 7,12-dimethylbenzanthrene-induced mammary carcinomas in the rat. Mol Cancer Ther 1:869–876
Wang L, Chen J, Thomson Lu (2005) The inhibitory effect of flazseed on the growth and metastasis of estrogen receptor negative human breast cancer xenografts is attributed to both its lignan and oil components. Int J Cancer 116:793–798
Power K, Saarinen N, Chen J, Thompson L (2006) Mammalian lignans enterolactone and enterodiol, alone and in combination with the isoflavone genistein do not promote the growth of MCF-7 xenografts in ovariectomized athymic mice. Int J Cancer 118:1316–1320
Ju Y, Allred K, Allred C, Helferich W (2006) Genistein stimulates growth of human breast cancer cells in a novel postmenopausal animal model with low plasma estradiol concentrations. Carcinogenesis 27:1292–1299
Jungestrom M, Thompson L, Dabrosin C (2007) Flaxseed and its lignans inhibit estradiol-induced growth, angiogenesis, and secretion of vascular endothelial growth factor in human breast cancer xenografts in vivo. Clin Cancer Res 13:1061–1067
Parkin D, Whelan S, Ferley J, Raymond L, Young J (1997) Cancer incidence in five continents. International Agency for Research on Cancer (IARC), Lyon, France
De Kleijn M, van der Schouw Y, Wilson P, Adlercreutz H, Mazur W, Grobbee D, Jacques P (2001) Intake of dietary phytoestrogens is low in postmenopausal women in the United States: The Framingham Study. J Nutr 131:1826–1832
Ingram D, Sanders K, Kolybaba M, Lopez D (1997) Case–control study of phyto-oestrogens and breast cancer. Lancet 350:990–994
Zheng W, Dai Q, Custer L, Shu X, Wen WQ, Jin F, Franke A (1999) Urinary excretion of isoflavonoids and the risk of breast cancer. Cancer Epidemiol Biomarkers Prev 8:35–40
Hirose K, Tajima K, Hamajima N, Inoue M, Takezaki T, Kuroishi T, Yoshida M, Tokudome S (1995) A large-scale, hospital-based case–control study of risk factors of breast cancer according to menopausal status. Jpn J Cancer Res 86:146–154
Pietinen P, Stumpf K, Mannisto S, Kataja V, Uusitupa M, Adlercreutz H (2001) Serum enterolactone and risk of breast cancer: a case–control study in eastern Finland. Cancer Epidemiol Biomarkers Prev 10:339–344
McCann S, Moysich K, Freudenheim J, Ambrosone CB, Shields PG (2002) The risk of breast cancer associated with dietary lignans differs by CYP17 genotype in women. J Nutr 132:3036–3041
McCann S, Muti P, Vito D, Edge S, Trevisan M, Freudenheim J (2004) Dietary lignan intakes and risk of pre- and post-menopausal breast cancer. Int J Cancer 111:440–443
Wu A, Ziegler R, Horn-Ross P, Nomura A, West D, Kolonel L, Rosenthal J, Hoover R, Pike M (1996) Tofu and risk of breast cancer in Asian-Americans. Cancer Epidemiol Biomarkers Prev 5:901–906
Wu A, Wan P, Hankin J, Tseng C, Yu M et al (2002) Adolescent and adult soy intake and risk of breast cancer in Asian-Americans. Carcinogenesis 2002;23:1491–1496
Dai Q, Shu X, Jin F, Potter J, Kushi L et al (2001) Population-based case–control study of soyfood intake and breast cancer risk in Shanghi. Br J Cancer 85:372–378
Dai Q, Franke A, Jin F, Shu X, Hebert J, Custer L, Cheng J, Gao Y, Shang W (2002) Urinary excretion of phytoestrogens and risk of breast cancer among Chinese women in Shanghai. Cancer Epidemiol Biomarkers Prev 11:815–821
Yamamoto S, Sobue T, Kobayashi M, Sasaki S, Tsugane S (2003) Soy, isoflavones, and breast cancer risk in Japan. J Natl Cancer Inst 95:906–913
Linseisen J, Piller R, Hermann S, Chang-Claude J (2004) Dietary phytoestrogen intake and premenopausal breast cancer risk in a German case–control study. Int J Cancer 110:284–290
Piller R, Chang-Claude J, Linseisen J (2006) Plasma enterolactone and genistein and the risk of premenopausal breast cancer. Eur J Cancer Prev 15:225–232
Fink B, Steck S, Wolff M, Britton J, Kabat G, Schroeder J, Teitelbaum S, Neugut A, Gammon M (2006) Dietary flavonoid intake and breast cancer risk among women on Long Island. Am J Epidemiol 165:514–523
Touillaud M, Thiebaut A, Niravong M, Boutron-Ruault M.-C., Clavel-Chapelon F (2006) No association between dietary phytoestrogens and risk of premenopausal breast cancer risk in a French cohort study. Cancer Epidemiol Biomarkers Prev 15:2574–2576
Verheus M, vanGils C, Keinan-Boker L, Grace P, Binghan S, Peeters P (2007) Plasma phytoestrogens and subsequent breast cancer risk. J Clin Oncol 25:648–655
Touillaud M, Thiebaut A, Fournier A, Niravong M, Boutron-Ruault M, Clavel-Chapelon F (2007) Lignan intake and postmenopausal breast cancer risk by estrogen and progesterone receptor status. J Natl Cancer Inst 99:475–486
Horn-Ross P, John E, Lee M, Stewart S, Koo J, Sakoda L, Shiau A, Goldstein J, Davis P, Perez-Stable E (2001) Phytoestrogen consumption and breast cancer risk in a multiethnic population. Am J Epidemiol 154:434–441
Horn-Ross P, Hoggart K, West D, Krone M, Stewart S et al (2002) Recent diet and breast cancer risk: the California Teachers Study (USA). Cancer Causes Control 13:407–415
Keinan-Boker L, van Der Schouw Y, Grobbee D, Peeters P (2004) Dietary phytoestrogens and breast cancer risk. Am J Clin Nutr 79:282–288
den Tonkelaar I, Keinan-Boker L, Vant Veer P, Arts C, Adlercreutz H, Thijssen J, Peeters P (2001) Urinary phytoestrogens and postmenopausal breast cancer risk. Cancer Epidemiol Biomarkers Prev 10:223–228
Yuan J, Wang Q, Ross R, Henderson B, Yu M (1995) Diet and breast cancer in Shanghai and Tianjin, China. Br J Cancer 71:1353–1358
Key T, Sharp G, Appleby P, Beral V, Goodman M, Soda M, Mabuchi K (1999) Soya foods and breast cancer risk: a prospective study in Hiroshima and Nagasaki, Japan. Br J Cancer 81:1248–1256
Grace P, Taylor J, Low Y, Luben R, Mulligan A, Botting N, Dowsett M, Welch A, Khaw K, Wareham N, Day N, Bingham S (2004) Phytoestrogen concentrations in serum and spot urine as biomarkers for dietary phytoestrogen intake and their relation to breast cancer risk in European Prospective Investigation of Cancer and nutrition-Norfolk. Cancer Epidemiol Biomarks Prev 13:698–708
Zeleniuch-Jacquotte A, Aldercreutz H, Shore R, Koenig K, Kato I, Arslan A, Toniolo P (2004) Circulating enterolactone and risk of breast cancer: a prospective study in New York. Br J Cancer 9:99–105
Messina M, Nagata C, Wu A (2006) Estimated Asian adult soy protein and isoflavone intakes. Nutr Cancer 55:1–12
Mulligan A, Welch A, McTaggart A, Bhaniani A, Bingham S (2007) Intakes and sources of soya foods and isoflavones in a UK population cohort (EPIC-Norfolk). Eur J Clin Nutr 61:248–254
Trock B, Hilakivi-Clarke L, Clarke R (2006) Meta-analysis of soy intake and breast cancer risk. JNCI 98:459–471
Reinli K, Block G (1996) Phytoestrogen content of foods—a compendium of literature values (review). Nutr Cancer 26:123–148
USDA. US Department of Agriculture, Agricultural Research Service (2007) USDA-Iowa State University Database on the Isoflavone Content of Foods, Release 1.4 - 2007. Nutrient Data Laboratory Web site: http://www.ars.usda.gov/nutrientdata
Mazur W, Duke J, Wahala K, Rasku S, Adlercreutz H (1998) Isoflavonoids and lignans in legumes: nutritional and health aspects on humans. J Nutr Biochem 9:193–200
Liggins J, Bluck L, Runswick S, Atkinson C, Coward WA et al (2000) Daidzein and genistein content of vegetables. Br J Nutr 84:717–725
Liggins J, Bluck L, Runswick S, Atkinson C, Coward W, Bingham S (2000) Daidzein and genistein content of fruits and nuts. J Nutr Biochem 11:326–331
Mazur W, Adlercreutz H (2000) Overview of naturally occurring endocrine-active substances in the human diet in relation to human health. Nutrition 16:654–658
Milder I, Arts I, van de Putte B, Venema D, Hollman P (2005) Lignan contents of Dutch plant foods: a database including lariciresinol, pinoresinol, secoisolariciresinol and matairesinol. Br J Nutr 93:393–402
Nurmi T, Heinonen S, Mazur W, Deyama T, Nishibe S, Aldercreutz H (2003) Lignans in selected wines. Food Chem 83:303–309
Horn-Ross P, Barnes S, Lee M, Coward L, Mandel J, Koo J, John E, Smith M (2000) Assessing phytoestrogen exposure in epidemiologic studies: development of a database (United States). Cancer Causes Control 11:289–298
Mazur W, Wahala K, Rasku S, Salakka A, Hase T, Adlercreutz H (1998) Lignan and isoflavonoid concentrations in tea and coffee. Br J Nutr 79:37–45
Thompson LU, Robb P, Serraino M, Cheung F (1991) Mammalian lignan production from various foods. Nutr Cancer 16:43–52
Boucher B, Cotterchio M, Kreiger N, Nadalin V, Block T, Block G (2006) Validity and reliability of the Block98 food-frequency questionnaire in a sample of Canadian women. Public Health Nutr 9:84–93
Holowaty E (2005) Cancer Care Ontario. Personal Communication
Subar A, Thompson F, Kipnis V et al (2001) Comparative validation of the Block, Willett and National Cancer Institute food frequency questionnaires: the eating at America’s Table Study. Am J Epidemiol 154:1089–1099
Gilbart E, Kreiger N (1998) Improvement in cumulative response rates following implementation of a financial incentive. Am J Epidemiol 148:97–99
Mazur W (1998) Phytoestrogen content in foods. Baillieres Clin Endocrinol Metab 12:729–742
Mazur W, Uehara M, Wahala K, Adlercreutz H (2000) Phyo-oestrogen content of berries, and plasma concentrations and urinary excretion of enterolactone after a single strawberry-meal in human subjects. Br J Nutr 83:381–387
Meagher L, Beecher G (2000) Assessment of data on the lignan value of foods. J Food Compost Anal 13:935–947
Lapcik O, Hill M, Hampl R, Wahala K, Adlercreutz H (1998) Identification of isoflavonoids in beer. Steroids 63:14–20
Boker L, Van der Schouw Y, De Kleijn M, Jacques P, Grobbee D, Peeters P (2002) Intake of dietary phytoestrogens by Dutch women. J Nutr 132:1319–1328
Horn-Ross P (2001) Assessing phytoestrogen exposure via a food-frequency questionnaire (letter). Cancer Causes Control 12:477–478
Block G, Hartman A, Dresser C, Carroll M, Gannon J, Gardner L (1986) A data-based approach to diet questionnaire design and testing. Am J Epidemiol 124:453–469
Block G (2001) Invited commentary: another perspective on food frequency questionnaires. Am J Epidemiol 154:1103–1104
Hosmer D, Lemeshow S (2000) Applied logistic regression. John Wiley & Sons Inc., New York, NY
Maldonado G, Greenland S (1993) Simulation study of confounder-selection strategies. Am J Epidemiol 138:923–936
Colditz G, Atwood K, Emmons K et al (2000) Harvard report on cancer prevention, vol 4: Harvard cancer risk index. Cancer Causes Control 11:477–488
Greenland S (1989) Modeling and variable selection in epidemiologic analysis. Am J Public Health 79:340–349
Liggins J, Mulligan A, Runswick S, Bingham SA (2002) Daidzein and genistein content of cereals. Eur J Clin Nutr 56:961–966
Mazur W, Fotsis T, Wahala K, Ojala S, Salakka A, Aldercreutz H (1996) Isotope dilution gas chromatographic-mass spectrometric method for the determination of isoflavonoids, coumestrol, and lignans in food samples. Anal Biochem 233:169–180
Pillow P, Duphorne C, Chang S, Contois J, Strom S et al (1999) Development of a database for assessing dietary phytoestrogen intake. Nutr Cancer 33:3–19
Silva dosSantos I, Mangtani P, McCormack V, Bhakta D, McMichael A, Sevak L (2004) Phytoestrogen intake and breast cancer risk in South Asian women in England: findings from a population-based case–control study. Cancer Causes Control 15:805–818
McCann S, Kulkarni S, Trevisan M, Vito D, Nie J, Edge S, Muti P, Freudenheim J (2006) Dietary lignan intakes and risk of breast cancer by tumor estrogen receptor status. Breast Cancer Res Treat 99:309–311
Bosetti C, Spertini L, Parpinel M, Gnagnarella P, Lagiou P et al (2005) LaVecchia C. Flavonoids and breast cancer risk in Italy. Cancer Epidemiol Biomarkers Prev 14:805–808
Olsen A, Knudsen K, Thomsen B, Loft S, Stripp C, Overvad K, Moller S, Tjonneland A (2004) Plasma enterolactone and breast cancer incidence by estrogen receptor status. Cancer Epidemiol Biomarkers Prev 13:2084–2089
Kilkkinen A, Virtamo J, Vartianen E, Sankila R, Adlercreutz H, Pietinen P (2004) Serum enterolactone concentration is not associated with breast cancer risk in a nested case–control study. Int J Cancer 108:277–280
Hulten K, Winkvist A, Lenner P, Johansson R, Aldercreutz H, Hallmans G (2002) An incident case-referent study on plasma enterolactone and breast cancer risk. Eur J Nutr 4:168–176
Dai Q, Franke A, Yu H, Shu X, Jin F, Hebert J, Custer L, Gao Y, Zheng W (2003) Urinary phytoestrogen excretion and breast cancer risk: evaluating potential effect modifiers endogenous estrogens and anthropometrics. Cancer Epidemiol Biomarkers Prev 12:497–502
Nelson L, Bulun S (2001) Estrogen production and action. J Am Acad Dermatol 45(3S):S116–S124
Lukanova A, Lundin E, Zeleniuch-Jacquotte A, Muti P, Mure A, Rinaldi S et al (2004) Body mass index, circulating levels of sex-steroid hormones, IGF-1 and IGF-binding protein-3;a cross sectional study in healthy women. Eur J Endocrinol 150:161–171
Setchell K (1998) Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am J Clin Nutrition 68:1333S–1346S
Han D, Tachibana H, Yamada K (2001) Inhibition of environmental estrogen-induced proliferation of human breast carcinoma MSF-7 cells by flavonoids. In Vitro Cell Dev Biol Anim 37:275–282
Messina M, McCaskill-Stevens W, Lampe J (2006) Addressing the soy and breast cancer relationship: review, commentary and workshop proceedings. J Natl Cancer Inst 98:1275–1284
Shu X, Jin F, Dai Q et al (2001) Soyfood intake during adolescence and subsequent risk of breast cancer among Chinese women. Cancer Epidemiol Biomarkers Prev 10:483–488
Thanos J, Cotterchio M, Boucher B, Kreiger N, Thompson L (2006) Adolescent dietary phytoestrogen intake and breast cancer risk (Canada). Cancer Causes Control 17:1253–1261
Schedin P, Byers T (1997) Adolescent diet and the risk of breast cancer in adulthood: a role for vitamin A? Nutrition 13:924–925
Lamartiniere C, Murrill W, Manzolillo P et al (1998) Genistein alters the ontogeny of mammary gland development and protects against chemically-induced mammary cancer in rats. Exp Biol Med (Maywood) 217:358–364
Tou J, Thompson L (1999) Exposure to flaxseed or its lignan component during different developmental stages influences rat mammary gland structures. Carcinogenesis 20:1831–1835
Jin Z, MacDonald R (2002) Soy isoflavones increase latency of spontaneous mammary tumors in mice. J Nutr 132:3186–3190
Krazeisen A, Breitling R, Moller G, Adamski J (2001) Phytoestrogens inhibit 17B-hydroxysteroid dehyrogenase type 5. Mol Cell Endocrinol 171:151–162
Fotsis T, Pepper M, Aldercreutz H, Fleischmann G, Hase T, Montesano R, Schweigerer L (1993) Genistein, a dietary-derived inhibitor of in vitro angiogenesis. Proc Nat Acad Sci USA 90:2690–2694
Dave B, Eason R, Till S, Geng Y, Velarde M, Badger T, Simmen R (2005) The soy isoflavone genistein promotes apoptosis in mammary epithelial cells by inducing the tumor suppressor PTEN. Carcinogenesis 26:1793–1803
Anderson J, Anthony M, Messina M, Garner S (1999) Effects of phyto-oestrogens on tissues. Nutr Res Rev 12:75–116
Strauss L, Santti R, Saarinen N, Streng T, Joshi S, Makela S (1998) Dietary phytoestrogens and their role in hormonally dependent disease. Toxicol Lett 102–102:349–354
Barnes S, Boersma B, Patel R, Kirk M, Darley-Usmar V, Kim H, Xu J (2000) Isoflavonoids and chronic disease: mechanisms of action. BioFactors 12:209–215
Haggans C, Hutchins A, Olson B et al (1999) Effect of flaxseed consumption on urinary estrogen metabolites in postmenopausal women. Nutr Cancer 33:188–195
Mueller S, Simon S, Chae K, Metzler M, Korach K (2004) Phytoestrogens and their human metabolites show distinct agonist and antagonist properties on ER-alpha and ER-beta in human cells. Toxicol Sci 80:14–25
Enmark E, Gustafsson J (1999) Oestrogen receptors: an overview. J Inter Med 246:133–138
Kuiper G, Lemmen J, Carlsson B, Corton J, Safe S, van der Saag P, van der Burg B, Gustafsson J (1998) Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 139(10):4252–4263
Petersson K, Delauunay F, Gustafsson JA (2000) Estrogen receptor beta acts as dominant regulator of estrogen signaling. Oncogene 19:4970–4978
An J, Tzagarakis-Foster C, Scharschmidt T, Lomri N, Leitman D (2001) Estrogen receptor beta-selective transcriptional activity and recruitment of coregulators by phytoestrogens. J Biol Chem 21:17808–17814
Kostelac D, Rechkemmer G, Briviba K (2003) Phytoestrogens modulate binding response of estrogen receptors alpha and beta to the estrogen response element. J Agric Food Chem 26:7632–7635
Kumar N, Cantor A, Allen K, Riccardi D, Cox C (2002) The specific role of isoflavones on estrogen metabolism in premenopausal women. Cancer 94:1166–1174
Xu X, Duncan A, Merz B, Kurzer M (1998) Effects of soy isoflavones on estrogen and phytoestrogen metabolism in premenopausal women. Cancer Epidemiol Biomarkers Prev 7:1101–1108
Martin M, Haourigui M, Pelissero C, Benassayag C, Nunez E (1996) Interactions between phytoestrogens and human sex steroid binding protein. Life Sci 58:429–436
Brooks JD, Thompson LU (2005) Mammalian lignans and genistein decrease the activities of aromatase and 17 beta-hydroxysteroid dehydrogenase in MCF-7 cells. J Steroid Biochem Molec Biol 94:461–467
Cassidy A (1996) Physiological effects of phyto-oestrogens in relation to cancer and other human health risks. Proc Nutr Soc 55:399–417
Lu L, Cree M, Josyla S et al (2000) Increased urinary excretion of 2-hydroxyestrone but not 16-alpha-hydroxyestrone in premenopausal women during a soya diet containing isoflavones. Cancer Res 60:1299–1305
Lu L, Anderson K, Grady J, Kohen F, Nagamani M (2000) Decreased ovarian hormones during a soya diet: implications for breast cancer prevention. Cancer Res 60:4112–4121
Chen J, Stavro P, Thompson L (2002) Dietary flaxseed inhibits human breast cancer growth and metastasis and downregulates expression of insulin-like growth factor and epidermal growth factor receptor. Nutr Cancer 43:187–192
Kitts D, Yuan Y, Wijewickreme A, Thompson L (1999) Antioxidant activity of the flaxseed lignan SECO-diglycoside and its mammalian lignan metabolite enterodiol and enterolactone. Mol Cell Biochem 202:91–100
Ruiz-Larrea M, Mohan A, Paganga G, Miller N, Bolwell G, Rice-Evans C (1997) Antioxidant activity of phytoestrogenic isoflavones. Free Radic Res 26:63–70
Su S, Yeh T, Chuang W, Ho C, Chang K et al (2005) The novel targets for anti-angiogenesis of genistein on human cancer cells. Biochem Pharmacol 69:307–318
Zhang S, Hunter D, Forman M, Rosner B, Speizer F, Colditz G, Manson J, Hankinson S, Willett W (1999) Dietary carotenoids and vitamins A, C, and E and risk of breast cancer. JNCI 91:547–556
Rowland I, Faughnan M, Hoey L, Wahala K, Williamson G, Cassidy A (2003) Bioavailability of phytoestrogens. Br J Nutr 89 (supp 1):S45–S58
Atkinson C, Berman S, Humbert O, Lampe JW (2004) In vitro incubation of human feces with daidzein and antibiotics suggests interindividual differences in the bacteria responsible for equol production. J Nutr 134:596–599
Franke A, Custer L, Hundahl S (2004) Determinants for urinary and plasma isoflavones in humans after soy intake. Nutr Cancer 50:141–154
Kilkkinen A, Pietinen P, Klaukka T, Virtamo J, Korhonen P, Aldercreutz H (2002) Use of oral antibiotics decreases serum enterolactone concentration. Am J Epidemiol 155:472–477
Atkinson C, Frankenfeld C, Lampe J (2005) Gut bacterial metabolism of the soy isoflavone daidzein: exploring the relevance to human health. Exp Bio Med 203:155–170
Greenwald P (2004) Clinical trials in cancer prevention:current results and perspectives for the future. J Nutr 134:3507S–3512S
Acknowledgments
We thank the study coordinator, Noori Chowdhury, and study staff, Leah Palma, Razia Sultana, and Claudia Quammie for their dedication to this study. This research was funded by the Canadian Breast Cancer Research Alliance with special funding support of the Canadian Breast Cancer Foundation Ontario Chapter (CBCRA Grant No. 13572).
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Cotterchio, M., Boucher, B.A., Kreiger, N. et al. Dietary phytoestrogen intake—lignans and isoflavones—and breast cancer risk (Canada). Cancer Causes Control 19, 259–272 (2008). https://doi.org/10.1007/s10552-007-9089-2
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DOI: https://doi.org/10.1007/s10552-007-9089-2