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ORIGINAL RESEARCH |
From the Department of Obstetrics and Gynecology, Toride Kyodo General Hospital, Toride, Ibaraki, and the Department of Obstetrics and Gynecology, Tokyo Medical and Dental University, Tokyo, Japan.
Address reprint requests to: Yoshiaki Somekawa, MD Toride Kyodo General Hospital Hongo 2-1-1 Toride, Ibaraki 302-0022 Japan E-mail: pv2t-sigi{at}asahi-net.or.jp
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Abstract |
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Methods: We estimated the daily intakes of isoflavones in the diets of 478 postmenopausal Japanese women who reported soy consumption. We recorded serum values of fasting total cholesterol, triglyceride, low-density lipoprotein cholesterol, high-density lipoprotein cholesterol, and apolipoproteins. Bone mineral density was measured at the lumbar spine (L2–L4) by dual energy x-ray absorptiometry. Women were assigned to two groups according to years since menopause (early and late postmenopausal groups), and each group was subcategorized into four groups according to dietary isoflavone intake. Relationships between isoflavone intake, menopausal symptoms, lipid profiles, and bone mineral density were examined in each group.
Results: The mean estimated intake of isoflavones among 478 women was 54.3 mg/day. With stepwise regression analysis we found that weight and years since menopause were significant independent predictors of bone mineral density. Bone mineral densities adjusted to years since menopause and weight were significantly different in the highest intake compared with lowest intake category (P < .001) within the early and late postmenopausal groups. In the early postmenopausal group, significant differences were found in palpitation and backaches between the high and low intake categories but were not significant in the late postmenopausal group.
Conclusion: High consumption of soy products is associated with increased bone mass in postmenopausal women and might be useful for preventing hypoestrogenic effects.
Menopausal women suffer from deleterious effects of lowered estrogen levels including reduction of bone mass, menopausal symptoms, and hypercholesterolemia. Those effects are pronounced during early postmenopause because of drastic estrogen reduction, and tend to become attenuated during late postmenopause. Phytoestrogens can potentially alleviate hypoestrogen-related deleterious effects.
Isoflavones make up the most common form of phytoestrogens, and the major dietary source of isoflavones is soy. Asian people consume 10–100 times more isoflavones than Western people,1 and osteoporosis-related fractures are less frequent in Asian than Western communities, possibly because of the large quantities of phytoestrogenrich soybeans and vegetables in the Asian diet.2 Various types and large amounts of soybeans and soy products are consumed especially in Japan, including soybean curd, fermented soybeans, soybean paste, and soy flour. Indirect evidence from studies of ipriflavone,3 an isoflavone derivative, suggest a potential benefit of isoflavones in preventing osteoporosis. Other studies suggested beneficial effects of isoflavones on atherosclerotic disease and menopausal symptoms.4,5 There has been a lack of epidemiologic studies on the relationship among dietary intake of soy products, menopausal symptoms, cardiovascular risk, and osteoporosis. The purpose of this study was to evaluate the relationship between intake of dietary isoflavones in soy products and menopausal symptoms, cardiovascular risk, and bone mineral density in postmenopausal Japanese women.
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Materials and Methods |
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Subjects reported weekly, monthly, and yearly consumption of soy products such as soybean curd, fermented soybeans, soybean paste, fried soybean curd, boiled soybeans, soy milk, soy flour, and soy sauce. We asked questions about consumption of soy products in the present and when subjects were 40 years old. To verify the reliability of their reports, urinary daidzein, genistein, equol, and biochanin-A were measured by high-performance liquid chromatography7,8 in the first 51 women. Contents of daidzein, genistein, equol, and biochanin-A were estimated from standard curves calculated by analysis of various doses of authentic compounds, and minimum detectable concentrations for them were 100 ng/mL, 100 ng/mL, 100 ng/mL, and 250 ng/mL, respectively. The correlation between total urinary isoflavones and present total daily dietary intakes of isoflavones calculated from their reports was significant (y = ax + b, a = 39.818 ± 5.816; b = 1.230 ± 0.304; r = .473, P < .001).
Weekly consumption was divided by seven, monthly consumptions by 30, and yearly intakes by 365 to arrive at daily intakes of each soy product. Several studies showed that isoflavone levels in soybean foods vary according to analytic procedure and the types of analyzed foods.9–11 Those studies did not cover all typical Japanese soy foods investigated in our study. Geographical differences were also surmised, and for that reason we used the report of Toda et al.12 Daily isoflavone intakes from the consumption of eight soy products were estimated by multiplying analyzed data by daily volume.
Each subject was asked to report her most serious symptoms at enrollment: hot flushes, sweating, body or extremities chills, palpitation, insomnia or sleep disturbance, irritability or nervousness, depression, headache or vertigo, weakness or tiredness, backache or aching joints. Symptoms were classified into three groups, the first four as vasomotor symptoms, the next three as psychologic symptoms, and the last three as physical symptoms. For quantitative analysis, each symptom was stratified into four degrees of severity: 0 = symptom did not occur, 1 = a mild symptom that did not interfere with usual life, 2 = a moderate symptom that interfered somewhat with usual activities, and 3 = a severe symptom that prevented routine daily activities.
The values of fasting serum total cholesterol, triglyceride, low-density lipoprotein (LDL) cholesterol, high-density lipoprotein (HDL) cholesterol, apolipoprotein AI, apolipoprotein B, and apolipoprotein E were measured for evaluation of atherosclerotic risk. After overnight fasting, blood was collected from each woman for estimating lipids and lipoproteins. To minimize variation, each patient’s sample was analyzed in the same assay. Total cholesterol and triglyceride levels were measured with the use of enzymatic colorimetric methods and enzymatic methods, respectively. High-density lipoprotein cholesterol levels were measured by a direct method,13 using commercially available kits. Low-density lipoprotein cholesterol levels were calculated with Friedewald’s equation.14 Apolipoprotein AI, apolipoprotein B, and apolipoprotein E were measured by an immunoturbidimetric method using commercially available kits. The intra-assay coefficients of variation for total cholesterol, triglyceride, LDL cholesterol, HDL cholesterol, apolipoprotein AI, apolipoprotein B, and apolipoprotein E were 0.7%, 1.9%, 0.7%, 2.5%, 4.0%, and 2.3%, respectively.
Bone mineral density at the lumbar spine (L2–L4) was measured by dual energy x-ray absorptiometry with the use of a Hologic QDR-4500 A densitometer (Hologic Inc., Waltham, MA) to assess osteoporotic risk. Total bone mineral density coefficients of variation for the spines were within 1%.
Variables in patients’ backgrounds, such as age, height, weight, body mass index (BMI), and age at menopause, were measured to discount effects from factors other than isoflavones. Patients were assigned to two groups according to years since menopause (early postmenopausal group, less than 5 years postmenopause, n = 269; late postmenopausal group, exceeding 5 years; postmenopause, n = 209). Each group was sub-categorized into four groups according to dietary total isoflavone intake, the first group with intake of under 35 mg/day of isoflavone, the second with intake of 35–50 mg/day, the third with intake of 50–65 mg/day, and the fourth with intake of over 65 mg/day.
Results are given as the mean ± standard error (SE). Data analysis was done with Stat View 5.00 software (SAS Institute Inc., Cary, NC). One-way factorial analysis of variance for continuous variables compared background characteristics between groups, and the Kruskal-Wallis test was used for noncontinuous variables. The relationships between isoflavone intake, menopausal symptoms, lipid profiles, and bone mineral densities were examined in each categorized group. Differences in the menopausal scores, serum lipids and lipoproteins, and bone mineral densities among the four groups were also tested by one-way factorial analysis of variance and Scheffe’s F test. Correlations between bone mineral density and intake levels of soy products were analyzed by Pearson’s correlation matrix method. P < .05 was defined as statistically significant.
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). Soy sauce is one of the most popular products, but daily quantities were too small to count as a source of isoflavone.
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). Stepwise regression analysis found that weight and years since menopause were the significant independent correlative factors of bone mineral density. In the early postmenopausal group, bone mineral density adjusted to weight and years since menopause were significantly different among the four groups; the higher intake group (50–65 and greater than 65 mg/day) had higher bone mineral density than did the lowest intake group (less than 35 mg/day; P < .001; Table 2). Differences in serum total cholesterol, serum triglyceride, LDL cholesterol, HDL cholesterol, apolipoprotein AI, apolipoprotein B, and apolipoprotein E were not significant among the four groups (Table 2). Menopausal symptom scores of palpitation (0.8 ± 0.1 and 0.8 ± 0.1 versus 1.2 ± 0.1, P < .05) and backaches or aching joints (1.7 ± 0.1 and 1.7 ± 0.1 versus 2.1 ± 0.1, P < .05) were significantly lower in the higher intake group than in the lowest intake group. Menopausal symptom scores of vasomotor symptoms, psychologic symptoms, physical symptoms, and total menopausal symptoms in the higher intake group tended to be lower, but the difference was not significant among groups (Figure 2).
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). Differences in serum total cholesterol, triglyceride, LDL cholesterol, HDL cholesterol, apolipoprotein AI, apolipoprotein B, and apolipoprotein E were not significant (Table 2). No menopausal symptom scores showed significant differences among the four groups (Figure 2).
Correlation analysis showed that estimated intake of total isoflavones had a weak but statistically significant positive correlation with bone mineral density adjusted to years since menopause and weight (r = .16, P < .01). We did a correlation analysis between the intake of isoflavone in each soy product and bone mineral density adjusted to years since menopause and weight. The estimated intake of fermented soybeans (r = .22, P < .001) and soybean curd (r = .13, P < .01) showed a weak but statistically significant positive correlation with bone mineral densities adjusted to years since menopause and weight (Table 3). For other soy products such as soybean paste and fried soybean curd, correlation to bone mineral density adjusted to years since menopause and weight was not found. No significant correlation was found between the estimated intake of fermented soybeans or soybean curd and lipid levels. Also, no significant correlation was found between estimated intake of fermented soybeans or soybean curd and menopausal symptom scores.
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Discussion |
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One possible explanation for those discrepancies is that an estrogen receptor is capable of binding several structurally diverse compounds such as natural estrogens and isoflavones. The binding affinity of those compounds varies with target organ. As for associations between isoflavones and menopausal symptoms, hot flushes are believed to be less frequent in Japan than in Canada, possibly because of the high phytoestrogen intake from soy foods in Japan.4 Murkies et al examined effects of soy flour on hot flushes,16 but the association between isoflavones and menopausal symptoms is not clear. Effects of isoflavones on the lipid profiles are also uncertain. Several studies with isoflavones reported inconsistent effects on serum lipids and lipoproteins. One study reported a significant reduction in total cholesterol in premenopausal women when they consumed soy products with 45 mg of conjugated isoflavones per day compared with an isoflavone-free control period,17 but another study reported no significant effects on cholesterol.16 Associations between isoflavones and bone mass are more consistent. Potter et al reported significant increases in bone mineral density in the lumbar spine for a group that took soy protein with high concentrations of isoflavones compared with a nonisoflavone group.18 Ipriflavone, an isoflavone derivative, has been shown effective in promoting bone mass and preventing bone loss,3,19 suggesting a similar effect of isoflavone on bone metabolism.
Another possible explanation is that isoflavones such as daidzein and genistein bind to estrogen receptors, but the estrogenic binding activities are on the order of 1/100 to 1/1000 that of 17ß-estradiol (E2).20–22 However, concentration of isoflavones in the whole body is 100 times that of endogenous estrogens, hence sufficient for biologic effects. In our study, the difference in the estimated amount of isoflavones in the highest and lowest groups was approximately threefold. Even the lowest intake group is probably within the biologically active concentration level. The difference in consumption might be too small to lead to significant differences among groups in lipid profiles and menopausal symptoms but was correlated with a significant difference in bone mineral density. Additional bone-specific components that prevent bone loss or stimulate bone formation might exist in soy products. One possible factor is calcium, which is contained in many soy products. Mean intakes of soybean curd and fermented soybeans by our study women were 50.3 and 12.8 g/day, which contained approximately 60 mg and 13 mg of calcium, respectively. The mean intake of calcium at that age in Japan is as few as 600 mg/day; calcium in soybean curd and fermented soybeans might be related to bone mass under conditions of insufficient calcium intake. Another candidate factor is vitamin K2 (menatetrenone), present in fermented soybeans and known to stimulate bone formation and prevent bone loss.23 The fact that a significant correlation was found between bone mineral density adjusted to weight and years since menopause and consumption of fermented soybeans supports that belief. The effects of calcium, vitamin K2, and isoflavones on bone mineral density might be synergistic. Fermented soybeans are consumed in higher quantities in eastern than in western Japan, correlating with epidemiologic data that show a lower incidence of osteoporotic bone fractures in eastern than in western Japan.24 That correlation might indicate the effects of calcium, vitamin K2, and isoflavone, which are abundant in fermented soybeans.
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Footnotes |
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Received April 18, 2000. Received in revised form July 27, 2000. Accepted September 13, 2000.
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References |
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2. Kao SC, P’eng FK. How to reduce the risk factors of osteoporosis in Asia. Chin Med J 1995;55:209–13.
3. Gambaccini M, Spinetti A, Cappagli B, Poneco F, Felipetto R, Parrini D, et al. Effects of ipriflavone administration on bone mass and metabolism in ovarectomized women. J Endocrinol Invest 1993;16:333–7.[Medline]
4. Lock M. Contested meanings of the menopause. Lancet 1991;337: 1270–2.[Medline]
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6. Zung WWK, Richards CB, Short MJ. Self-rating depression scale in an outpatient clinic. Arch Gen Psychiatry 1965;13:508–15.
7. Franke AA, Custer LJ. High-performance liquid chromatography assay of isoflavonoids and coumestrol from human urine. J Chromatogr B Biomed Sci Appl 1994;662:47–60.
8. Wang H, Murphy PA. Isoflavone content in commercial soybean foods. J Agric Food Chem 1994;42:1666–73.
9. Reinli K, Block G. Phytoestrogen contents of foods-a compendium of literature values. Nutr Cancer 1996;26:123–48.[Medline]
10. Wang H, Murphy PA. Isoflavone composition of American and Japanese soybeans in Iowa: Effects of variety, crop year, and location. J Agric Food Chem 1994;42:1674–7.
11. Dwyer JT, Goldin BR, Saul N, Gualtieiri L, Barakat S, Adlercreutz H. Tofu and soy drinks contain phytoestrogens. J Am Diet Assoc 1994;94:739–43.[Medline]
12. Toda T, Okuhira T, Yamori Y. Physiological functions and utilization of isoflavone in soybean. Syokuhin to Kaihatsu 1996;31:44–7 (Japanese).
13. Nauck M, Marz W, Haas B, Wieland H. Homogeneous assay for direct determination of high-density lipoprotein cholesterol evaluated. Clin Chem 1996;42:424–9.
14. Friedewald WT, Levy RI, Fredrickson DS. Estimation of low-density lipoprotein cholesterol in plasma without use of the preparative ultra centrifuge. Clin Chem 1972;18:499–502.[Abstract]
15. Statistics Bureau Management and Coordination Agency, Government of Japan. Annual report of the family income and expenditure survey 1987:328–9 (Japanese).
16. Murkies AL, Limbard C, Strauss BJ, Wilcox G, Burger HG, Morton MS. Dietary flour supplementation decreases postmenopausal hot flushes: Effect of soy and wheat. Maturitas 1995;21:189–95.[Medline]
17. Cassidy A, Bingham S, Setchell K. Biological effects of isoflavones in young women: Importance of the chemical composition of soyabean products. Br J Nutr 1995;74:587–601.
18. Potter SM, Baum JA, Teng H, Stillman RJ, Shay NF, Erdman JW Jr. Soy protein, and isoflavones: Their effects on lipids and bone density in postmenopausal women. Am J Clin Nutr 1998;68:1375S–9S.[Abstract]
19. Adami S, Bufalino L, Cervetti R, Di Marco C, Di Muano O, Fantasia L, et al. Ipriflavone prevents radial bone loss in postmenopausal women with low bone mass over 2 years. Osteoporos Int 1997;7: 119–25.[Medline]
20. Zava DT, Duwe G. Estrogenic and antiproliferative properties and other flavonoids in human breast cancer cells in vivo. Nutr Cancer 1997;27:31–40.[Medline]
21. Santell RJ, Cheng YC, Nair MG, Helferich WG. Dietary genistein exerts estrogenic effects upon the uterus, mammary gland and the hypothalmic/pituitary axis in rats. J Nutr 1997;127:263–9.
22. Milligan SR, Kalita JC, Heyerick A, Rong H, Cooman LD, Keukeleire DD. Identification of a potent phytoestrogen in hops (Humulus lupulus L.) and beer. J Clin Endocrinol Metab 1999;83:2249–52.
23. Somekawa Y, Chiguchi M, Harada M, Ishibashi T. Use of vitamin K2 (menatetrenone) and 1,25-dihydroxyvitamin D3 in the prevention of bone loss induced by leuprolide. J Clin Endocrinol Metab 1999;84:2700–4.
24. Orimo H, Hashimoto T, Yoshimura N, Ujiwara S, Hosoi T, Shiraki M, et al. Nationwide incidence survey of femoral neck fracture in Japan, 1992. J Bone Miner Metab 1997;15:100–6.
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