Abstract
We evaluated the relationship of spot urinary concentrations of phytoestrogens with total prostate cancer and tumor grade in a hospital-based case–control study in Jamaica. Urine samples were analyzed for genistein, daidzein, equol (isoflavones), and enterolactone (lignan) among newly diagnosed cases (n = 175) and controls (n = 194). Urinary concentrations of enterolactone (lignan) were higher among cases. There were no significant differences in median concentrations of isoflavone excretion. Compared with non-producers of equol (reference tertile), men who produced equol were at decreased risk of total prostate cancer (tertile 2: OR, 0.42; CI, 0.23–0.75) (tertile 3: OR, 0.48; CI, 0.26–0.87) (p trend, 0.020) and high-grade disease (tertile 2: OR, 0.31; CI, 0.15–0.61) (tertile 3: OR, 0.29; CI, 0.13–0.60) (p trend, 0.001). Higher concentrations of enterolactone were positively related to total prostate cancer (OR, 1.85; CI, 1.01–3.44; p trend, 0.027) as well as high-grade disease (OR, 2.46; CI, 1.11–5.46; p trend, 0.023). There were no associations between urinary excretion of genistein and daidzein with risk of prostate cancer. Producers of equol (isoflavone) may be at reduced risk of total- and high-grade prostate cancer whereas enterolactone may increase the likelihood of disease.
Similar content being viewed by others
References
Lampe JW (2003) Isoflavonoid and lignan phytoestrogens as dietary biomarkers. J Nutr 133(Suppl 3):956S–964S
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
Hedelin M, Klint A, Chang ET et al (2006) Dietary phytoestrogen, serum enterolactone and risk of prostate cancer: the cancer prostate Sweden study (Sweden). Cancer Causes Control 17:169–180
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
Nagata Y, Sonoda T, Mori M et al (2007) Dietary isoflavones may protect against prostate cancer in Japanese men. J Nutr 137:1974–1979
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
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
Tammela T (2004) Endocrine treatment of prostate cancer. J Steroid Biochem Mol Biol 92:287–295
Gibson TN, Blake G, Hanchard B, Waugh N, McNaughton D (2008) Age-specific incidence of cancer in Kingston and St Andrew, Jamaica, 1998–2002. West Indian Med J 57:81–89
Anonymous (1997) Cancer incidence in five continents, vol VII. IARC Scientific Publications i-1240
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
Grace PB, Taylor JI, Low YL et al (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 Biomarkers Prev 13:698–708
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
Gleason DF, Mellinger GT (1974) Prediction of prognosis for prostatic adenocarcinoma by combined histological grading and clinical staging. J Urol 111:58–64
Catalona WJ, Partin AW, Slawin KM et al (1998) Use of the percentage of free prostate-specific antigen to enhance differentiation of prostate cancer from benign prostatic disease: a prospective multicenter clinical trial. JAMA 279:1542–1547
Etzioni R, Falcon S, Gann PH, Kooperberg CL, Penson DF, Stampfer MJ (2004) Prostate-specific antigen and free prostate-specific antigen in the early detection of prostate cancer: do combination tests improve detection? Cancer Epidemiol Biomarkers Prev 13:1640–1645
Anonymous (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation. In: World Health Organisation technical report series 894, i-253
Kilkkinen A, Pietinen P, Klaukka T, Virtamo J, Korhonen P, Adlercreutz H (2002) Use of oral antimicrobials decreases serum enterolactone concentration. Am J Epidemiol 155:472–477
Kilkkinen A, Stumpf K, Pietinen P, Valsta LM, Tapanainen H, Adlercreutz H (2001) Determinants of serum enterolactone concentration. Am J Clin Nutr 73:1094–1100
Valentin-Blasini L, Sadowski MA, Walden D, Caltabiano L, Needham LL, Barr DB (2005) Urinary phytoestrogen concentrations in the U.S. population (1999–2000). J Expo Anal Environ Epidemiol 15:509–523
Park SY, Wilkens LR, Franke AA et al (2009) Urinary phytoestrogen excretion and prostate cancer risk: a nested case–control study in the Multiethnic Cohort. Br J Cancer 101:185–191
Seow A, Shi CY, Franke AA, Hankin JH, Lee HP, Yu MC (1998) Isoflavonoid levels in spot urine are associated with frequency of dietary soy intake in a population-based sample of middle-aged and older Chinese in Singapore. Cancer Epidemiol Biomarkers Prev 7:135–140
Kurzer MS, Xu X (1997) Dietary phytoestrogens. Annu Rev Nutr 17:353–381
Setchell KD, Brown NM, Lydeking-Olsen E (2002) The clinical importance of the metabolite equol—a clue to the effectiveness of soy and its isoflavones. J Nutr 132:3577–3584
Atkinson C, Frankenfeld CL, Lampe JW (2005) Gut bacterial metabolism of the soy isoflavone daidzein: exploring the relevance to human health. Exp Biol Med (Maywood) 230:155–170
Rowland IR, Wiseman H, Sanders TA, Adlercreutz H, Bowey EA (2000) Interindividual variation in metabolism of soy isoflavones and lignans: influence of habitual diet on equol production by the gut microflora. Nutr Cancer 36:27–32
Akaza H, Miyanaga N, Takashima N et al (2004) Comparisons of percent equol producers between prostate cancer patients and controls: case–controlled studies of isoflavones in Japanese, Korean and American residents. Jpn J Clin Oncol 34:86–89
Lampe JW, Karr SC, Hutchins AM, Slavin JL (1998) Urinary equol excretion with a soy challenge: influence of habitual diet. Proc Soc Exp Biol Med 217:335–339
Lampe JW, Skor HE, Li S, Wahala K, Howald WN, Chen C (2001) Wheat bran and soy protein feeding do not alter urinary excretion of the isoflavan equol in premenopausal women. J Nutr 131:740–744
Vedrine N, Mathey J, Morand C et al (2006) One-month exposure to soy isoflavones did not induce the ability to produce equol in postmenopausal women. Eur J Clin Nutr 60:1039–1045
Low YL, Taylor JI, Grace PB et al (2006) Phytoestrogen exposure, polymorphisms in COMT, CYP19, ESR1, and SHBG genes, and their associations with prostate cancer risk. Nutr Cancer 56:31–39
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
Travis RC, Spencer EA, Allen NE et al (2009) Plasma phyto-oestrogens and prostate cancer in the European Prospective Investigation into Cancer and Nutrition. Br J Cancer 100:1817–1823
Ozasa K, Nakao M, Watanabe Y et al (2004) Serum phytoestrogens and prostate cancer risk in a nested case–control study among Japanese men. Cancer Sci 95:65–71
Setchell KD, Cassidy A (1999) Dietary isoflavones: biological effects and relevance to human health. J Nutr 129:758S–767S
Wiseman H (2000) The therapeutic potential of phytoestrogens. Expert Opin Investig Drugs 9:1829–1840
Akaza H, Miyanaga N, Takashima N et al (2002) Is daidzein non-metabolizer a high risk for prostate cancer? A case–controlled study of serum soybean isoflavone concentration. Jpn J Clin Oncol 32:296–300
King RA, Bursill DB (1998) Plasma and urinary kinetics of the isoflavones daidzein and genistein after a single soy meal in humans. Am J Clin Nutr 67:867–872
Nesbitt PD, Lam Y, Thompson LU (1999) Human metabolism of mammalian lignan precursors in raw and processed flaxseed. Am J Clin Nutr 69:549–555
Chen LH, Fang J, Sun Z et al (2009) Enterolactone inhibits insulin-like growth factor-1 receptor signaling in human prostatic carcinoma PC-3 cells. J Nutr 139:653–659
Carreau C, Flouriot G, Bennetau-Pelissero C, Potier M (2008) Enterodiol and enterolactone, two major diet-derived polyphenol metabolites have different impact on ERalpha transcriptional activation in human breast cancer cells. J Steroid Biochem Mol Biol 110:176–185
Martin ME, Haourigui M, Pelissero C, Benassayag C, Nunez EA (1996) Interactions between phytoestrogens and human sex steroid binding protein. Life Sci 58:429–436
Lampe JW, Gustafson DR, Hutchins AM et al (1999) Urinary isoflavonoid and lignan excretion on a Western diet: relation to soy, vegetable, and fruit intake. Cancer Epidemiol Biomarkers Prev 8:699–707
Taylor-Robinson D, Furr PM (1990) Elimination of mycoplasmas from the murine genital tract by hormone treatment. Epidemiol Infect 105:163–168
Low YL, Taylor JI, Grace PB et al (2005) Polymorphisms in the CYP19 gene may affect the positive correlations between serum and urine phytoestrogen metabolites and plasma androgen concentrations in men. J Nutr 135:2680–2686
Hsing AW, Reichardt JK, Stanczyk FZ (2002) Hormones and prostate cancer: current perspectives and future directions. Prostate 52:213–235
Platz EA, Giovannucci E (2004) The epidemiology of sex steroid hormones and their signaling and metabolic pathways in the etiology of prostate cancer. J Steroid Biochem Mol Biol 92:237–253
Johnsen NF, Olsen A, Thomsen BL et al (2010) Plasma enterolactone and risk of colon and rectal cancer in a case–cohort study of Danish men and women. Cancer Causes Control 21:153–162
Kuijsten A, Hollman PC, Boshuizen HC et al (2008) Plasma enterolignan concentrations and colorectal cancer risk in a nested case–control study. Am J Epidemiol 167:734–742
Atkinson C, Skor HE, Fitzgibbons ED et al (2002) Overnight urinary isoflavone excretion in a population of women living in the United States, and its relationship to isoflavone intake. Cancer Epidemiol Biomarkers Prev 11:253–260
Chen Z, Zheng W, Custer LJ et al (1999) Usual dietary consumption of soy foods and its correlation with the excretion rate of isoflavonoids in overnight urine samples among Chinese women in Shanghai. Nutr Cancer 33:82–87
Wilkinson AP, Wahala K, Williamson G (2002) Identification and quantification of polyphenol phytoestrogens in foods and human biological fluids. J Chromatogr B Analyt Technol Biomed Life Sci 777:93–109
Wu Q, Wang M, Simon JE (2004) Analytical methods to determine phytoestrogenic compounds. J Chromatogr B Analyt Technol Biomed Life Sci 812:325–355
Statistical Institute of Jamaica (2009) Population census 2001: Jamaica, 2003. Statistical Institute of Jamaica, Kingston
Acknowledgments
This work was supported by the National Health Fund, Planning Institute of Jamaica and the University of the West Indies (Mona), Jamaica. The authors wish to thank the research nurses -Barbara Panton, Elsa Brown, Nicola Meeks-Aitken, Donnahae Rhoden-Salmon – and study participants for their support in the investigation.
Conflicts of interest
No potential conflicts of interest to disclose.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jackson, M.D., McFarlane-Anderson, N.D., Simon, G.A. et al. Urinary phytoestrogens and risk of prostate cancer in Jamaican men. Cancer Causes Control 21, 2249–2257 (2010). https://doi.org/10.1007/s10552-010-9648-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-010-9648-9