Phytoestrogens and risk of prostate cancer: an updated meta-analysis of epidemiologic studies

References

• Adlercreutz CH, Goldin BR, Gorbach SL, Höckerstedt KA, Watanabe S, Hämäläinen EK, Markkanen MH, Mäkelä TH, Wähälä KT, Adlercreutz T. 1995. Soybean phytoestrogen intake and cancer risk. J Nutr. 125:757S–770S.
   PubMed Web of Science ®Google Scholar
• Adlercreutz H. 1998. Epidemiology of phytoestrogens. Baillieres Clin Endocrinol Metab. 12:605–623.
   PubMed Web of Science ®Google Scholar
• Akiyama T, Ishida J, Nakagawa S, Ogawara H, Watanabe S, Itoh N, Shibuya M, Fukami Y. 1987. Genistein, a specific inhibitor of tyrosine-specific protein kinases. J Biol Chem. 262:5592–5595.
   PubMed Web of Science ®Google Scholar
• Barnes S. 2010. The biochemistry, chemistry and physiology of the isoflavones in soybeans and their food products. Lymphat Res Biol. 8:89–98.
   PubMed Web of Science ®Google Scholar
• Bosetti C, Bravi F, Talamini R, Parpinel M, Gnagnarella P, Negri E, Montella M, Lagiou P, Franceschi S, La Vecchia C. 2006. Flavonoids and prostate cancer risk: a study in Italy. Nutr Cancer. 56:123–127.
   PubMed Web of Science ®Google Scholar
• Branca F, Lorenzetti S. 2005. Health effects of phytoestrogens. Forum Nutr. 57:100–111.
   PubMedGoogle Scholar
• Cassidy A. 2003. Potential risks and benefits of phytoestrogen-rich diets. Int J Vitam Nutr Res. 73:120–126.
   PubMed Web of Science ®Google Scholar
• Center MM, Jemal A, Lortet-Tieulent J, Ward E, Ferlay J, Brawley O, Bray F. 2012. International variation in prostate cancer incidence and mortality rates. Eur Urol. 61:1079–1092.
   PubMed Web of Science ®Google Scholar
• Davis JN, Kucuk O, Sarkar FH. 1999. Genistein inhibits NF-kappa B activation in prostate cancer cells. Nutr Cancer. 35:167–174.
   PubMed Web of Science ®Google Scholar
• DerSimonian R, Laird N. 1986. Meta-analysis in clinical trials. Control Clin Trials. 7:177–188.
   PubMedGoogle Scholar
• Dixon RA. 2004. Phytoestrogens. Annu Rev Plant Biol. 55:225–261.
   PubMed Web of Science ®Google Scholar
• Franke AA, Custer LJ, Cerna CM, Narala K. 1995. Rapid HPLC analysis of dietary phytoestrogens from legumes and from human urine. Proc Soc Exp Biol Med. 208: 18–26.
   PubMed Web of Science ®Google Scholar
• Ganry O. 2005. Phytoestrogens and prostate cancer risk. Prev Med. 41:1–6.
   PubMed Web of Science ®Google Scholar
• Goetzl MA, Van Veldhuizen PJ, Thrasher JB. 2007. Effects of soy phytoestrogens on the prostate. Prostate Cancer Prostatic Dis. 10:216–223.
   PubMed Web of Science ®Google Scholar
• Hartman J, Ström A, Gustafsson JÅ. 2012. Current concepts and significance of estrogen receptor β in prostate cancer. Steroids. 77:1262–1266.
   PubMed Web of Science ®Google Scholar
• He JJ, Wang S, Zhou M, Yu WW, Zhang YL, He X. 2015. Phytoestrogens and risk of prostate cancer: a meta-analysis of observational studies. World J Surg Oncol. 13:231–241.
   PubMed Web of Science ®Google Scholar
• Heald CL, Ritchie MR, Bolton-Smith C, Morton MS, Alexander FE. 2007. Phyto-oestrogens and risk of prostate cancer in Scottish men. Br J Nutr. 98:388–396.
   PubMed Web of Science ®Google Scholar
• Hedelin M, Bälter KA, Chang ET, Bellocco R, Klint A, Johansson JE, Wiklund F, Thellenberg-Karlsson C, Adami HO, Grönberg H. 2006a. Dietary intake of phytoestrogens, estrogen receptor-beta polymorphisms and the risk of prostate cancer. Prostate. 66:1512–1520.
   PubMed Web of Science ®Google Scholar
• Hedelin M, Klint A, Chang ET, Bellocco R, Johansson JE, Andersson SO, Heinonen SM, Adlercreutz H, Adami HO, Grönberg H. 2006b. Dietary phytoestrogen, serum enterolactone and risk of prostate cancer: the cancer prostate Sweden study (Sweden). Cancer Causes Control. 17:169–180.
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG. 2002. Quantifying heterogeneity in a meta-analysis. Stat Med. 21:1539–1558.
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG, Deeks JJ, Altman DG. 2003. Measuring inconsistency in meta-analyses. BMJ. 327: 557–560.
   PubMed Web of Science ®Google Scholar
• Holzbeierlein JM, McIntosh J, Thrasher JB. 2005. The role of soy phytoestrogens in prostate cancer. Curr Opin Urol. 15:17–22.
   PubMed Web of Science ®Google Scholar
• Hwang CS, Kwak HS, Lim HJ, Lee SH, Kang YS, Choe TB, Hur HG, Han KO. 2006. Isoflavone metabolites and their in vitro dual functions: they can act as an estrogenic agonist or antagonist depending on the estrogen concentration. J Steroid Biochem Mol Biol. 101:246–253.
   PubMed Web of Science ®Google Scholar
• Hwang YW, Kim SY, Jee SH, Kim YN, Nam CM. 2009. Soy food consumption and risk of prostate cancer: a meta-analysis of observational studies. Nutr Cancer. 61: 598–606.
   PubMed Web of Science ®Google Scholar
• IARC: GLOBOCAN. 2012. Cancer Incidence, Mortality and Prevalence Worldwide (2012 estimates). Available from: http://globocan.iarc.fr
   Google Scholar
• Jackson MD, McFarlane-Anderson ND, Simon GA, Bennett FI, Walker SP. 2010. Urinary phytoestrogens and risk of prostate cancer in Jamaican men. Cancer Causes Control. 21:2249–2257.
   PubMed Web of Science ®Google Scholar
• Jackson RL, Greiwe JS, Schwen RJ. 2011. Emerging evidence of the health benefits of S-equol, an estrogen receptor β agonist. Nutr Rev. 69:432–448.
   PubMed Web of Science ®Google Scholar
• Jacob DA, Temple JL, Patisaul HB, Young LJ, Rissman EF. 2001. Coumestrol antagonizes neuroendocrine actions of estrogen via the estrogen receptor alpha. Exp Biol Med (Maywood). 226:301–306.
   PubMed Web of Science ®Google Scholar
• Kilkkinen A, Virtamo J, Virtanen MJ, Adlercreutz H, Albanes D, Pietinen P. 2003. Serum enterolactone concentration is not associated with prostate cancer risk in a nested case-control study. Cancer Epidemiol Biomarkers Prev. 12:1209–1212.
   PubMed Web of Science ®Google Scholar
• Kumar R, Verma V, Jain A, Jain RK, Maikhuri JP, Gupta G. 2011. Synergistic chemoprotective mechanisms of dietary phytoestrogens in a select combination against prostate cancer. J Nutr Biochem. 22:723–731.
   PubMed Web of Science ®Google Scholar
• Kurahashi N, Iwasaki M, Inoue M, Sasazuki S, Tsugane S. 2008. Plasma isoflavones and subsequent risk of prostate cancer in a nested case-control study: The Japan Public Health Center. J Clin Oncol. 26:5923–5929.
   PubMed Web of Science ®Google Scholar
• Kurahashi N, Iwasaki M, Sasazuki S, Otani T, Inoue M, Tsugane S. 2007. Soy product and isoflavone consumption in relation to prostate cancer in Japanese men. Cancer Epidemiol Biomarkers Prev. 16:538–545.
   PubMed Web of Science ®Google Scholar
• Kyle E, Neckers L, Takimoto C, Curt G, Bergan R. 1997. Genistein-induced apoptosis of prostate cancer cells is preceded by a specific decrease in focal adhesion kinase activity. Mol Pharmacol. 51:193–200.
   PubMed Web of Science ®Google Scholar
• Lee J, Demissie K, Lu SE, Rhoads GG. 2007. Cancer incidence among Korean-American immigrants in the United States and native Koreans in South Korea. Cancer Control. 14:78–85.
   PubMedGoogle Scholar
• Lee MM, Gomez SL, Chang JS, Wey M, Wang RT, Hsing AW. 2003. Soy and isoflavone consumption in relation to prostate cancer risk in China. Cancer Epidemiol Biomarkers Prev. 12:665–668.
   PubMed Web of Science ®Google Scholar
• Lewis JE, Soler-Vilá H, Clark PE, Kresty LA, Allen GO, Hu JJ. 2009. Intake of plant foods and associated nutrients in prostate cancer risk. Nutr Cancer. 61:216–224.
   PubMed Web of Science ®Google Scholar
• Loeb S, Drevin L, Robinson D, Holmberg E, Carlsson S, Lambe M, Stattin P. 2013. Risk of localized and advanced prostate cancer among immigrants versus native-born Swedish men: a nation-wide population-based study. Cancer Causes Control. 24:383–390.
   PubMed Web of Science ®Google Scholar
• Magee PJ, Rowland IR. 2004. Phyto-oestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br J Nutr. 91:513–531.
   PubMed Web of Science ®Google Scholar
• Malina N, Virtanen M, Pietinen P, Virtamo J, Albanes D, Hartman AM, Heinonen OP. 1998. A comparison of prospective and retrospective assessments of diet in a study of colorectal cancer. Nutr Cancer. 32:146–153.
   PubMed Web of Science ®Google Scholar
• Mazur WM, Duke JA, Wahala K, Rasku S, Adlercreutz H. 1998. Isoflavonoids and lignans in legumes: nutritional and health aspects in humans. J Nutr Biochem. 9: 193–200.
   Web of Science ®Google Scholar
• McCann SE, Ambrosone CB, Moysich KB, Brasure J, Marshall JR, Freudenheim JL, Wilkinson GS, Graham S. 2005. Intakes of selected nutrients, foods, and phytochemicals and prostate cancer risk in western New York. Nutr Cancer. 53:33–41.
   PubMed Web of Science ®Google Scholar
• McCredie M. 1998. Cancer epidemiology in migrant populations. Recent Results Cancer Res. 154:298–305.
   PubMedGoogle Scholar
• Messina MJ. 2003. Emerging evidence on the role of soy in reducing prostate cancer risk. Nutr Rev. 61:117–131.
   PubMed Web of Science ®Google Scholar
• Mousavi SM, Sundquist J, Hemminki K. 2013. Cancer incidence among Turkish, Chilean, and North African first-generation immigrants in Sweden compared with residents in the countries of origin and native Swedes. Eur J Cancer Prev. 22:1–7.
   PubMed Web of Science ®Google Scholar
• Nagata Y, Sonoda T, Mori M, Miyanaga N, Okumura K, Goto K, Naito S, Fujimoto K, Hirao Y, Takahashi A. 2007. Dietary isoflavones may protect against prostate cancer in Japanese men. J Nutr. 137:1974–1979.
   PubMed Web of Science ®Google Scholar
• Ozasa K, Nakao M, Watanabe Y, Hayashi K, Miki T, Mikami K, Mori M, Sakauchi F, Washio M, Ito Y. 2004. Serum phytoestrogens and prostate cancer risk in a nested case-control study among Japanese men. Cancer Sci. 95:65–71.
   PubMed Web of Science ®Google Scholar
• Park SY, Murphy SP, Wilkens LR, Henderson BE, Kolonel LN. 2008. Legume and isoflavone intake and prostate cancer risk: the multiethnic cohort study. Int J Cancer. 123:927–932.
   PubMed Web of Science ®Google Scholar
• Park SY, Wilkens LR, Franke AA, Le Marchand L, Kakazu KK, Goodman MT, Murphy SP, Henderson BE, Kolonel LN. 2009. Urinary phytoestrogen excretion and prostate cancer risk: a nested case-control study in the Multiethnic Cohort. Br J Cancer. 101:185–191.
   PubMed Web of Science ®Google Scholar
• Pihlajamaa P, Zhang FP, Saarinen L, Mikkonen L, Hautaniemi S, Jänne OA. 2011. The phytoestrogen genistein is a tissue-specific androgen receptor modulator. Endocrinology. 152:4395–4405.
   PubMed Web of Science ®Google Scholar
• Pilšáková L, Riečanský I, Jagla F. 2010. The physiological actions of isoflavone phytoestrogens. Physiol Res. 59: 651–654.
   PubMed Web of Science ®Google Scholar
• Prins GS, Birch L, Couse JF, Choi I, Katzenellenbogen B, Korach KS. 2001. Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor alpha: studies with alphaERKO and betaERKO mice. Cancer Res. 61:6089–6097.
   PubMed Web of Science ®Google Scholar
• Raffoul JJ, Wang Y, Kucuk O, Forman JD, Sarkar FH, Hillman GG. 2006. Genistein inhibits radiation induced-activation of NF-kappaB in prostate cancer cells promoting apoptosis and G2/M cell cycle arrest. BMC Cancer. 6:107–116.
   PubMed Web of Science ®Google Scholar
• Sasamura H, Takahashi A, Miyao N, Yanase M, Masumori N, Kitamura H, Itoh N, Tsukamoto T. 2002. Inhibitory effect on expression of angiogenic factors by antiangiogenic agents in renal cell carcinoma. Br J Cancer. 86:768–773.
   PubMed Web of Science ®Google Scholar
• Shimizu H, Ross RK, Bernstein L, Yatani R, Henderson BE, Mack TM. 1991. Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County. Br J Cancer. 63:963–966.
   PubMed Web of Science ®Google Scholar
• Siegel R, Ma JM, Zou ZH, Jemal A. 2014. Cancer statistics 2014. CA Cancer J Clin. 50:7–33.
   Google Scholar
• Singh AV, Franke AA, Blackburn GL, Zhou JR. 2006. Soy phytochemicals prevent orthotopic growth and metastasis of bladder cancer in mice by alterations of cancer cell proliferation and apoptosis and tumor angiogenesis. Cancer Res. 66:1851–1858.
   PubMed Web of Science ®Google Scholar
• Soni M, Rahardjo TB, Soekardi R, Sulistyowati Y, Lestariningsih Yesufu-Udechuku A, Irsan A, Hogervorst E. 2014. Phytoestrogens and cognitive function: a review. Maturitas. 77:209–220.
   PubMed Web of Science ®Google Scholar
• Stattin P, Adlercreutz H, Tenkanen L, Jellum E, Lumme S, Hallmans G, Harvei S, Teppo L, Stumpf K, Luostarinen T. 2002. Circulating enterolactone and prostate cancer risk: a Nordic nested case-control study. Int J Cancer. 99:124–129.
   PubMed Web of Science ®Google Scholar
• Stattin P, Bylund A, Biessy C, Kaaks R, Hallmans G, Adlercreutz H. 2004. Prospective study of plasma enterolactone and prostate cancer risk (Sweden). Cancer Causes Control. 15:1095–1102.
   PubMed Web of Science ®Google Scholar
• Strom SS, Yamamura Y, Duphorne CM, Spitz MR, Babaian RJ, Pillow PC, Hursting SD. 1999. Phytoestrogen intake and prostate cancer: a case-control study using a new database. Nutr Cancer. 33:20–25.
   PubMed Web of Science ®Google Scholar
• Sugiyama Y, Nagata Y, Fukuta F, Takayanagi A, Masumori N, Tsukamoto T, Akasaka H, Ohnishi H, Saito S, Miura T. 2014. Counts of Slackia sp. strain NATTS in intestinal flora are correlated to serum concentrations of equol both in prostate cancer cases and controls in Japanese men. Asian Pac J Cancer Prev. 15:2693–2697.
   PubMedGoogle Scholar
• Travis RC, Allen NE, Appleby PN, Price A, Kaaks R, Chang-Claude J, Boeing H, Aleksandrova K, Tjønneland A, Johnsen NF. 2012. Prediagnostic concentrations of plasma genistein and prostate cancer risk in 1,605 men with prostate cancer and 1,697 matched control participants in EPIC. Cancer Causes Control. 23:1163–1171.
   PubMed Web of Science ®Google Scholar
• Travis RC, Spencer EA, Allen NE, Appleby PN, Roddam AW, Overvad K, Johnsen NF, Olsen A, Kaaks R, Linseisen J. 2009. Plasma phyto-oestrogens and prostate cancer in the European Prospective Investigation into Cancer and Nutrition. Br J Cancer. 100:1817–1823.
   PubMed Web of Science ®Google Scholar
• Usui T. 2006. Pharmaceutical prospects of phytoestrogens. Endocr J. 53:7–20.
   PubMed Web of Science ®Google Scholar
• Vastag B. 2007. Soy and prostate cancer study results mixed. J Natl Cancer Inst. 99:1364–1365.
   PubMedGoogle Scholar
• Virk-Baker MK, Nagy TR, Barnes S. 2010. Role of phytoestrogens in cancer therapy. Planta Med. 76:1132–1142.
   PubMed Web of Science ®Google Scholar
• Walle T. 2011. Bioavailability of resveratrol. Ann N Y Acad Sci. 1215:9–15.
   PubMed Web of Science ®Google Scholar
• Ward H, Chapelais G, Kuhnle GG, Luben R, Khaw KT, Bingham S. 2008. Lack of prospective associations between plasma and urinary phytoestrogens and risk of prostate or colorectal cancer in the European Prospective into Cancer-Norfolk study. Cancer Epidemiol Biomarkers Prev. 17:2891–2894.
   PubMed Web of Science ®Google Scholar
• Ward HA, Kuhnle GG, Mulligan AA, Lentjes MA, Luben RN, Khaw KT. 2010. Breast, colorectal, and prostate cancer risk in the European Prospective Investigation into Cancer and Nutrition-Norfolk in relation to phytoestrogen intake derived from an improved database. Am J Clin Nutr. 91:440–448.
   PubMed Web of Science ®Google Scholar
• Weihua Z, Makela S, Andersson LC, Salmi S, Saji S, Webster JI, Jensen EV, Nilsson S, Warner M, Gustafsson JA. 2001. A role for estrogen receptor beta in the regulation of growth of the ventral prostate. Proc Natl Acad Sci USA. 98:6330–6335.
   PubMed Web of Science ®Google Scholar
• Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, Tugwell P. 2009. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta analyses [Internet]. [Ottawa]: Ottawa Hospital Research Institute [cited 2014 Mar 31]. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
   Google Scholar
• Yan L, Spitznagel EL. 2009. Soy consumption and prostate cancer risk in men: a revisit of a meta-analysis. Am J Clin Nutr. 89:1155–1163.
   PubMed Web of Science ®Google Scholar
• Yashar CM, Spanos WJ, Taylor DD, Gercel-Taylor C. 2005. Potentiation of the radiation effect with genistein in cervical cancer cells. Gynecol Oncol. 99:199–205.
   PubMed Web of Science ®Google Scholar
• Yu H, Harris RE, Gao YT, Gao R, Wynder EL. 1991. Comparative epidemiology of cancers of the colon, rectum, prostate and breast in Shanghai, China versus the United States. Int J Epidemiol. 20:76–81.
   PubMed Web of Science ®Google Scholar
• Zhou JR, Gugger ET, Tanaka T, Guo Y, Blackburn GL, Clinton SK. 1999. Soybean phytochemicals inhibit the growth of transplantable human prostate carcinoma and tumor angiogenesis in mice. J Nutr. 129:1628–1635.
   PubMed Web of Science ®Google Scholar