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Soy Isoflavone Intake Inhibits Bone Resorption and Stimulates Bone Formation in Menopausal Women: Meta-Analysis of Randomized Controlled Trials

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Soy Isoflavone Intake Inhibits Bone Resorption and Stimulates Bone Formation in Menopausal Women: Meta-Analysis of Randomized Controlled Trials European Journal of Clinical Nutrition (2008) 62, 155–161 & 2008 Nature Publishing Group All rights reserved 0954-3007/08 $30.00 www.nature.com/ejcn ORIGINAL ARTICLE Soy isoflavone intake inhibits bone resorption and stimulates bone formation in menopausal women: meta-analysis of randomized controlled trials D-F Ma1,2, L-Q Qin3, P-Y Wang1 and R Katoh2 1Department of Social Medicine and Health Education, School of Public Health, Peking University, Beijing, China; 2Department of Human Pathology, Interdisciplinary Graduate School of Medicine and Engineering, University of Yamanashi, Yamanashi, Japan and 3Department of Nutrition and Food Hygiene, School of Radiation Medicine and Public Health, Soochow University, Suzhou, China Objective: To clarify the effects of isoflavone intake on bone resorption and bone formation. Methods: We identified randomized controlled trials related to urinary deoxypyridinoline (Dpyr, a bone resorption marker) and serum bone-specific alkaline phosphatase (BAP, a bone formation marker) listed on MEDLINE (January 1966–April 2006), the Cochrane Controlled Trials Register, EMBASE (1985–January 2006), Science Citation Index and PUBMED (updated till April 2006). Results: Nine studies with a total of 432 subjects were selected for meta-analysis. The urinary Dpyr concentration in subjects who consumed isoflavones decreased significantly by À2.08 nmol/mmol (95% confidence interval (CI): À3.82 to À0.34 nmol/ mmol) in comparison with that in subjects who did not consume isoflavones. Isoflavone intake vs placebo intake significantly increased serum BAP by 1.48 mg/l (95% CI: 0.22–2.75 mg/l). Decreases in the urinary Dpyr concentration with isoflavone intake of o90 mg/day and with treatment lasting less than 12 weeks were À2.34 nmol/mmol (95% CI: À4.46 to À0.22 nmol/mmol) and À2.03 nmol/mmol (95% CI: À3.20 to À0.85 nmol/mmol), respectively. Conclusions: Isoflavone intervention significantly inhibits bone resorption and stimulates bone formation. These favorable effects occur even if o90 mg/day of isoflavones are consumed or the intervention lasts less than 12 weeks. European Journal of Clinical Nutrition (2008) 62, 155–161; doi:10.1038/sj.ejcn.1602748; published online 28 March 2007 Keywords: soy; isoflavone; osteoporosis; bone metabolism; deoxypyridinoline; bone-specific alkaline phosphatase Introduction risk of hip fracture (Cauley et al., 2001; Rossouw et al., 2002). Furthermore, HRT has some negative side effects such as an With increases in life expectancy, osteoporosis has become a increased risk of cardiovascular disease and breast cancer common disease in post-menopausal women. Although (Recker, 1993). Thus, new bone protection options are hormone replacement therapy (HRT) is the first choice of needed. treatment for hormone-related osteoporosis, some results In recent years, isoflavones have received much attention of randomized controlled trials (RCTs) of this treatment in the medical and scientific literature. It is well known that showed no bone protection or a significant reduction in the the incidence of osteoporosis-related fracture is significantly lower in Southern and Eastern Asian women than in Western women (Ho et al., 1993; Tham et al., 1998). One possible Correspondence: Professor P-Y Wang, Department of Social Medicine and reason for this difference is high intake of phytoestrogens; Health Education, School of Public Health, Peking University, Xueyuan Road Asian people consume soy 10–20 times more than Western 38, Haidian District, Beijing, China. E-mail: [email protected] people (Kimira et al., 1998; Ho et al., 2003). Soy isoflavones Contributors: P-YW and RK contributed to the design of this article. D-FM and comprise mainly genistein, daidzein and glycitein, which L-QQ contributed to the collection of data and statistical analysis, and have have structures similar to that of 17b-estradiol, a potential also contributed equally to the work. All authors read and approved this alternative to HRT (Knight and Eden, 1996). However, the article. Received 25 October 2006; revised 14 February 2007; accepted 19 February effects of isoflavones on bone metabolism appear incon- 2007; published online 28 March 2007 sistent in RCTs. Thus, a statistical method of combining Effects of isoflavone on bone resorption and formation D-F Ma et al 156 these diverse data is needed to evaluate the usefulness of effects model considers both intra- and inter-study varia- isoflavone therapy. Meta-analysis combines or integrates the tions, it is more conservative and hence more appropriate results of several studies to provide increased statistical than an estimate from the fixed-effects model for an analysis power for the quantitative identification of trends (Brockwell such as this (Zhuo et al., 2004). Thus, we report results from and Gordon, 2001). In the RCTs, urinary deoxypyridinoline the random-effects model. To assess the heterogeneity (Dpyr) was generally used as a bone resorption marker, and (apparent diversity in weighted mean differences across serum bone-specific alkaline phosphatase (BAP) was the studies), we conducted a test based on w2 distribution. The most commonly used index of bone formation. Therefore, funnel plot was performed to detect publication bias. we identified all reported RCTs related to the effects of isoflavones on Dpyr or BAP and analyzed the effects of isoflavones on bone metabolism quantitatively. Results and discussion The trial flow chart is illustrated in Figure 1. Our literature Materials and methods search identified 31 RCTs. Twenty-two studies were excluded because of lack of indices of interest (Agnusdei et al., MEDLINE (January 1966–April 2006), the Cochrane Con- 1997a, b; Gambacciani et al., 1997a, b; Potter et al., 1998; trolled Trials Register, EMBASE (1985–January 2006), Science Alekel et al., 2000; Wangen et al., 2000; Clifton-Bligh et al., Citation Index and PUBMED (updated till April 2006) were 2001; Katase et al., 2001; Anderson et al., 2002; Chiechi used to search articles that described RCTs investigating the et al., 2002; Lucas et al., 2002; Chen et al., 2003, 2004; Jones effect of isoflavones on bone metabolism. Titles, abstracts et al., 2003; Schult et al., 2003; Atkinson et al., 2004; and subject headings in the databases were searched with Harkness et al., 2004; Olsen et al., 2004; Mori et al., the help of the following keywords: bone, osteoporosis, bone 2004a, b), non-randomization (Dalais et al., 1998), lack of a metabolism, phytoestrogens, soy, isoflavones, genistein, control group (Agnusdei et al., 1997a, b), insufficient original daidzein, Dpyr or BAP. We also examined all references of data or baseline values (Gambacciani et al., 1997a, b; Khalil related reviews and papers identified by the search. Addi- et al., 2002). Thus, nine studies with a total of 432 subjects tionally, we contacted the experts for the obtaining of were included in this meta-analysis, in which five studies unpublished data. Studies were selected for analysis if they had quality score of five; three studies had quality score of met all of the following criteria: (1) subjects were limited to four and one study had quality score of three (Morabito et al., female; (2) subjects ingested soy products or isoflavones for 2002; Uesugi et al., 2002; Yamori et al., 2002; Arjmandi at least 4 weeks; (3) the RCT included a parallel control et al., 2003, 2005; Dalais et al., 2003; Brooks et al., 2004; Mori group; and (4) Dpyr or BAP was used as an index of bone et al., 2004a, b; Nikander et al., 2004) (Table 1). In five of metabolism. If the study sample was found to overlap with these studies, isolated soy protein that contained mainly that in another article or if two articles described aspects of isoflavones was used, and isoflavone tablets were used in the same study, only the publication with the largest sample other studies. Isoflavone intake varied from 37.3–118 mg/day group was used. in the various treatment groups. The duration of treatment Two researchers extracted data independently. A data also varied widely, ranging from 4 to 48 weeks including collection form was designed, and data were entered into three studies with a duration exceeding 12 weeks. Six studies the form twice to reduce input errors. The items entered in were performed in Caucasian women and three studies in the form included participant characteristics, treatment Asian women. Seven of these nine studies were carried out in duration, interventional dosage, and values of relevant indices before and after isoflavone or placebo treatments. Jadad scores were used to measure the quality of the RCTs Potentially relevant articles identified and screened for retrieval (n = 673) (Jadad et al., 1996). Two reviewers rated study quality independently, there was (90%) agreement on Jadad scores. Articles excluded because not RCTs (n = 642) If the reviews disagreed, a final score was reached by RCTs retrieved for more detailed evaluation (n = 31) discussion. In this meta-analysis, we obtained the mean differences RCTs excluded: did not meet the inclusion criteria (n = 22) from the post-randomization baseline and post-treatment RCTs included in meta-analysis (n = 9) values for each trial, and calculated the pooled standard deviation of the mean differences according to the method RCTs withdrawn because did not report: of Yeung and Yu (2003). Weighted mean difference was Deoxypyridinoline (n = 0) Serum bone-specific alkaline phosphatase (n = 4) calculated by subtracting the mean difference of the control group from that of the treatment group. The inverse variance RCTs with usable information on: method was used to pool the weighted mean difference with Deoxypyridinoline (n = 9) Serum bone-specific alkaline phosphatase (n = 5) Review Manager 4.2 software (Nordic Cochrane Center, Oxford, England). Because the estimate from the random- Figure 1 Results of search for eligible studies. European Journal of Clinical Nutrition Effects of isoflavone on bone resorption and formation D-F Ma et al 157 Table 1 Characteristics of the nine selected randomized controlled trials of isoflavone intake in women Study Length of treatment No.
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