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An Observational Study of Young to Middle-Aged Women Charlotte Atkinson A, Heather E

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An Observational Study of Young to Middle-Aged Women Charlotte Atkinson A, Heather E Journal of Steroid Biochemistry & Molecular Biology 86 (2003) 71–77 Urinary equol excretion in relation to 2-hydroxyestrone and 16␣-hydroxyestrone concentrations: an observational study of young to middle-aged women Charlotte Atkinson a, Heather E. Skor a, E. Dawn Fitzgibbons b, Delia Scholes c,e, Chu Chen b,e, Kristiina Wähälä d, Stephen M. Schwartz b,e, Johanna W. Lampe a,e,∗ a Cancer Prevention Research Program, Fred Hutchinson Cancer Research Center, P.O. Box 19024, MP-900, Seattle, WA 98109-1024, USA b Program in Epidemiology, Fred Hutchinson Cancer Research Center, Seattle, WA 98109, USA c Center for Health Studies, Group Health Cooperative, Seattle, WA 98101, USA d Department of Chemistry, University of Helsinki, Helsinki, Finland e Department of Epidemiology, University of Washington, Seattle, WA 98195, USA Received 18 November 2002; accepted 31 March 2003 Abstract Approximately one-third to one-half of individuals harbor the colonic bacteria that are capable of metabolizing the soy isoflavone daidzein to equol. Results of prior studies suggest beneficial effects of producing equol in relation to breast cancer risk, potentially through effects on endogenous hormones. High urinary excretion of 2-hydroxyestrone (2-OH E1) relative to 16␣-hydroxyestrone (16␣-OH E1) has been associated with a reduced risk of breast cancer. In this pilot study we examined associations between urinary excretion of equol and 2-OH E1,16␣-OH E1, and their ratio, and investigated whether excretion of these estrogen metabolites differed between two samples collected 48 h apart. Isoflavones (genistein, daidzein, O-desmethylangolensin (ODMA), and equol) were measured in two overnight urines from 126 women. Excretion of 2-OH E1 and 16␣-OH E1 were measured in the first overnight urine from all 126 women and in the second overnight urine from 30 of these women; there were no significant differences between samples collected 48 h apart in excretion of 2-OH E1 or 16␣-OH E1 (P = 0.75 and 0.17, respectively). Among all women, correlations between total isoflavone excretion (sum of genistein, daidzein, ODMA, and equol) and estrogen metabolites were non-significant (P>0.05). Among women with detectable levels of equol, total isoflavone excretion was significantly positively correlated with 16␣-OH E1 (r = 0.32, P = 0.02), but was not correlated with 2-OH E1 or 2-OH E1:16␣-OH E1 ratio (r = 0.21, P = 0.14, and r =−0.05, P = 0.70, respectively). Equol excretion (adjusted for other isoflavone excretion) was significantly positively correlated with 2-OH E1:16␣-OH E1 ratio (r = 0.38, P = 0.005), but was not correlated with 2-OH E1 or 16␣-OH E1 (r = 0.15, P = 0.29, and r =−0.17, P = 0.24, respectively). The finding that equol excretion, but not total isoflavone excretion, correlated positively with the 2-OH E1:16␣-OH E1 ratio suggests that the colonic bacterial profile associated with equol production may be involved in estrogen metabolism, and may therefore possibly influence breast cancer risk. © 2003 Elsevier Ltd. All rights reserved. Keywords: Equol; Estrogen metabolism; Isoflavone 1. Introduction lize daidzein to equol [4–7]. Intestinal microflora are likely involved in the conversion of daidzein to equol; young in- Soy isoflavones, such as daidzein and genistein, are bio- fants, with presumably underdeveloped gut microflora, and logically active in humans and have received considerable germ-free animals do not have the ability to produce equol attention as potential cancer-preventive compounds [1,2]. [8,9]. Furthermore, in vitro incubation of daidzein with fe- Dietary interventions with soy, one of the richest identified cal flora from an equol-producer results in the conversion sources of daidzein [3], have shown that only approximately of daidzein to equol, whereas incubation with fecal flora one-third to one-half of the population are able to metabo- from an equol non-producer does not [10,11]. Equol pro- duction is therefore likely to be a biomarker of a particu- ∗ Corresponding author. Tel.: +1-206-667-6580; fax: +1-206-667-7850. lar, although yet-to-be-defined, colonic bacterial profile in E-mail address: [email protected] (J.W. Lampe). humans. 0960-0760/$ – see front matter © 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0960-0760(03)00259-0 72 C. Atkinson et al. / Journal of Steroid Biochemistry & Molecular Biology 86 (2003) 71–77 The clinical significance of having the ability to convert of these estrogen metabolites differ between two overnight daidzein to equol remains to be established fully, but sev- urine samples collected 48 h apart. eral small studies have suggested that women who are able to produce equol may be at a reduced risk of breast cancer, potentially through effects on endogenous hormone levels 2. Experimental procedures and estrogen metabolism. In a case–control study among Australian women, there was a decreased risk of breast 2.1. Study participants and data collection cancer associated with increasing quartiles of equol excre- tion [12], and urinary equol excretion has been inversely Participants in this pilot study were drawn from a correlated with circulating free estradiol, and positively cor- previously described study population [31]. Briefly, 363 related with sex hormone binding globulin (SHBG) [13]. women, aged 25–59 years, who had participated in a larger Furthermore, within specific menstrual cycle phases in a case–control study of risk factors for uterine leiomyomata soy feeding study, women with the ability to produce equol had also completed an ancillary protocol consisting of had statistically significantly lower plasma concentrations two overnight urine collections (made 48 h apart). Ascor- of estrone, estrone-sulfate, testosterone, androstenedione, bic acid had been added to all samples as a preservative. dehydroepiandrosterone (DHEA), DHEA-sulfate, and cor- As part of the case–control study, all urine samples were tisol, and statistically significantly higher concentrations analyzed for isoflavones (daidzein, genistein, equol, and of sex hormone binding globulin than women without the O-desmethylangolensin (ODMA)) and creatinine concen- ability to produce equol. These differences were found trations. Key features of the urine collection, isoflavone at all soy doses given, and it was suggested that the assay, and creatinine assay have been described previously ability to produce equol might represent colonic bacte- [31]. There were no significant differences between cases rial enzyme activity that increases fecal steroid excretion and controls in urinary excretion of isoflavones (P>0.05; [14]. data not shown). For the present pilot study, 126 women In the 1970s, it was proposed that estrogen metabolites (63 cases and 63 controls) who had taken part in the an- might be important in breast cancer development [15].Two cillary study were selected as follows: total isoflavone ex- major estradiol metabolites, 2-hydroxyestrone (2-OH E1) cretion (the sum of daidzein, genistein, equol, and ODMA and 16␣-hydroxyestrone (16␣-OH E1) [16,17], are produced excretions) per 24 h was estimated by multiplying data by competing pathways and have markedly different prop- expressed as nmol/h by 24, and women were placed into erties. 2-OH E1 is weakly estrogenic, and increased 2-OH one of three groups: low (0–1000 nmol/24 h; n = 206), E1 has been associated with a reduction in breast cancer risk intermediate (>1000–2000 nmol/24 h; n = 83), and high (reviewed in [17]). In contrast, 16␣-OH E1 is estrogenic, has (>2000 nmol/24 h; n = 74) excretors. We selected 40, 40, been shown to form covalent bonds with estrogen receptors, and 46 women at random from the low-, intermediate-, and may be genotoxic [18–20]. Therefore, it has been sug- and high-excretion groups, respectively. Women were gested that urinary excretion of these estrogen metabolites over-sampled from the high excretion group in order to can be used as a risk marker for breast cancer [21,22].In test the hypothesis that high excretion of isoflavones is support of this, several retrospective and prospective studies associated with a higher 2-OH E1:16␣-OH E1 ratio. have reported an increased risk of breast cancer associated Demographic data were collected as part of the main with low urinary excretion of 2-OH E1 relative to 16␣-OH case–control study and also as part of the ancillary study E1 [23–26]. Some evidence exists to suggest that dietary soy at the time of the urine collections. The study procedures can modulate estrogen metabolite profiles; two intervention were approved by the Institutional Review Boards of the studies in premenopausal women reported an increase in the Fred Hutchinson Cancer Research Center and Group Health 2-OH E1:16␣-OH E1 ratio with soy consumption [27,28], Cooperative, and all study participants provided written in- and in postmenopausal women, there was a trend towards formed consent. increased 2-hydroxylation of estrogens with soy consump- α tion [29]. Furthermore, urinary 2-OH E1 excretion increased 2.2. 2-Hydroxyestrone and 16 -hydroxyestrone analysis in mice fed either a fermented soybean extract, daidzein, or genistein [30]. Urine samples from the first overnight urine collection Because intestinal bacteria are involved in the metabolism from each of the 126 selected women were analyzed for of estrogens, inter-individual differences in host bacte- 2-OH E1 and 16␣-OH E1. To determine if excretion of 2-OH rial populations may result in differences in estrogen E1 and 16␣-OH E1 differed between two overnight urine metabolism, and therefore potentially breast cancer risk. samples collected 48 h apart, urine samples from the second Our main objective was to investigate the relationship overnight collection were also assayed for a subset of these between equol excretion and estrogen metabolism, specif- women (n = 30). The 30 pairs were randomly selected, ically the urinary concentrations of 2-OH E1,16␣-OH E1 distributed evenly among the tertiles of total isoflavone ex- and their ratio, in the context of an observational study.
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