Effects of phytoestrogens on bone mineral density during the menopause transition: a systematic review of randomized, controlled trials

References

• Lethaby A, Marjoribanks J, Kronenberg F, Roberts H, Eden J, Brown J. Phytoestrogens for menopausal vasomotor symptoms. Cochrane Database Syst Rev 2013 Dec 10;(12):CD001395
   PubMed Web of Science ®Google Scholar
• Harlow SD, Gass M, Hall JE, et al. Executive summary of the Stages of Reproductive Aging Workshop +10: addressing the unfinished agenda of staging reproductive aging. Climacteric 2012;15:105–14
   PubMed Web of Science ®Google Scholar
• Abdi F, Mobedi H, Mosaffa N, Dolatian M, Ramezani Tehrani F. Effects of hormone replacement therapy on immunological factors in the postmenopausal period. Climacteric 2016;19:234–9
   PubMed Web of Science ®Google Scholar
• Abdi F, Mobedi H, Mosaffa N, Dolatian M, Ramezani Tehrani F. Hormone therapy for relieving postmenopausal vasomotor symptoms: a systematic review. Arch Iran Med 2016;19:141–6
   PubMed Web of Science ®Google Scholar
• Bromberger JT, Schott LL, Kravitz HM, et al. Longitudinal change in reproductive hormones and depressive symptoms across the menopausal transition: results from the Study of Women's Health Across the Nation (SWAN). Arch Gen Psychiatry 2010;67:598–607
   PubMed Web of Science ®Google Scholar
• Sowers MR, Jannausch M, McConnell D, et al. Hormone predictors of bone mineral density changes during the menopausal transition. J Clin Endocrinol Metab 2006;91:1261–7
   PubMed Web of Science ®Google Scholar
• Dennerstein L, Dudley EC, Hopper JL, Guthrie JR, Burger HG. A prospective population-based study of menopausal symptoms. Obstet Gynecol 2000;96:351–8
   PubMed Web of Science ®Google Scholar
• Kruger MC, Wolber FM. Osteoporosis: modern paradigms for last century's bones. Nutrients 2016 Jun 17;8(6). pii: E376
   Web of Science ®Google Scholar
• Silva TR, Franz R, Maturana MA, Spritzer PM. Associations between body composition and lifestyle factors with bone mineral density according to time since menopause in women from Southern Brazil: a cross-sectional study. BMC Endocr Disord 2015;15:71
   PubMed Web of Science ®Google Scholar
• Shedd-Wise KM, Alekel DL, Hofmann H, et al. The soy isoflavones for reducing bone loss study: 3-yr effects on pQCT bone mineral density and strength measures in postmenopausal women. J Clin Densitom 2011;14:47–57
   PubMed Web of Science ®Google Scholar
• Holick MF, Lamb JJ, Lerman RH, et al. Hop rho iso-alpha acids, berberine, vitamin D3 and vitamin K1 favorably impact biomarkers of bone turnover in postmenopausal women in a 14-week trial. J Bone Miner Metab 2010;28:342–50
   PubMed Web of Science ®Google Scholar
• Whelan AM, Jurgens TM, Bowles SK. Natural health products in the prevention and treatment of osteoporosis: systematic review of randomized controlled trials. Ann Pharmacother 2006;40:836–49
   PubMed Web of Science ®Google Scholar
• NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy, March 7–29, 2000: highlights of the conference. 2001
   Google Scholar
• Ettinger B, Grady D, Tosteson ANA, Pressman A, Macer JL. Effect of the Women's Health Initiative on women's decisions to discontinue postmenopausal hormone therapy. Obstet Gynecol 2003;102:1225–32
   PubMed Web of Science ®Google Scholar
• Austin PC, Mamdani MM, Tu K, Jaakkimainen L. Prescriptions for estrogen replacement therapy in Ontario before and after publication of the Women's Health Initiative Study. JAMA 2003;289:3241–2
   PubMed Web of Science ®Google Scholar
• Lawton B, Rose S, McLeod D, Dowell A. Changes in use of hormone replacement therapy after the report from the Women's Health Initiative: cross sectional survey of users. BMJ 2003;327:845–6
   PubMed Web of Science ®Google Scholar
• Haskell SG. After the Women's Health Initiative: Postmenopausal women's experiences with discontinuing estrogen replacement therapy. J Women's Health 2004;13:438–42
   PubMed Web of Science ®Google Scholar
• Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321–33
   PubMed Web of Science ®Google Scholar
• Hulley S, Furberg C, Barrett-Connor E, et al. Noncardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/progestin Replacement Study follow-up (HERS II). JAMA 2002;288:58–64
   PubMed Web of Science ®Google Scholar
• Wong WW, Lewis RD, Steinberg FM, et al. Soy isoflavone supplementation and bone mineral density in menopausal women: a 2-y multicenter clinical trial. Am J Clin Nutr 2009;90:1433–9
   PubMed Web of Science ®Google Scholar
• Kuiper GG, Lemmen JG, Carlsson B, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology 1998;139:4252–63
   PubMed Web of Science ®Google Scholar
• Dip R, Lenz S, Antignac J-P, Le Bizec B, Gmuender H, Naegeli H. Global gene expression profiles induced by phytoestrogens in human breast cancer cells. Endocr Relat Cancer 2008;15:161–73
   PubMed Web of Science ®Google Scholar
• Abdi F, Kazemi F, Ramezani Tehrani F, Roozbeh N. Protocol for systematic review and meta-analysis: hop (Humulus lupulus L.) for menopausal vasomotor symptoms. BMJ Open 2016;6:e010734
   PubMed Web of Science ®Google Scholar
• Albertazzi P. Purified phytoestrogens in postmenopausal bone health: is there a role for genistein? Climacteric 2002;5:190–6
   PubMed Web of Science ®Google Scholar
• Ricci E, Cipriani S, Chiaffarino F, Malvezzi M, Parazzini F. Soy isoflavones and bone mineral density in perimenopausal and postmenopausal Western women: a systematic review and meta-analysis of randomized controlled trials. J Women's Health 2010;19:1609–17
   PubMed Web of Science ®Google Scholar
• Adlercreutz H, Mazur W. Phyto-oestrogens and Western diseases. Ann Med 1997;29:95–120
   PubMed Web of Science ®Google Scholar
• Somekawa Y, Chiguchi M, Ishibashi T, Aso T. Soy intake related to menopausal symptoms, serum lipids, and bone mineral density in postmenopausal Japanese women. Obstet Gynecol 2001;97:109–15
   PubMed Web of Science ®Google Scholar
• Weaver CM, Cheong JMK. Soy isoflavones and bone health: the relationship is still unclear. J Nutr 2005;135:1243–7
   PubMed Web of Science ®Google Scholar
• Messina MJ. Soy foods and soybean isoflavones and menopausal health. Nutr Clin Care 2002;5:272–82
   PubMedGoogle Scholar
• Sharif PS, Nikfar S, Abdollahi M. Prevention of bone resorption by intake of phytoestrogens in postmenopausal women: a meta-analysis. Age 2011;33:421–31
   PubMed Web of Science ®Google Scholar
• Wei P, Liu M, Chen Y, Chen D-C. Systematic review of soy isoflavone supplements on osteoporosis in women. Asian Pacific J Trop Med 2012;5:243–8
   PubMed Web of Science ®Google Scholar
• Garrard J. Health Sciences Literature Review Made Easy: The Matrix Method, 3rd edn. London: Jones & Bartlett Publishers, 2011
   Google Scholar
• Higgins JP, Altman DG, Gøtzsche PC, et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 2011;343:d5928
   PubMed Web of Science ®Google Scholar
• Huang H-Y, Yang H-P, Yang H-T, Yang T-C, Shieh M-J, Huang S-Y. One-year soy isoflavone supplementation prevents early postmenopausal bone loss but without a dose-dependent effect. J Nutr Biochem 2006;17:509–17
   PubMed Web of Science ®Google Scholar
• Wu J, Oka J, Ezaki J, Ohtomo T, et al. Possible role of equol status in the effects of isoflavone on bone and fat mass in postmenopausal Japanese women: a double-blind, randomized, controlled trial. Menopause 2007;14:866–74
   PubMed Web of Science ®Google Scholar
• Ye YB, Tang XY, Verbruggen MA, Su YX. Soy isoflavones attenuate bone loss in early postmenopausal Chinese women: a single-blind randomized, placebo-controlled trial. Eur J Nutr 2006;45:327–34
   PubMed Web of Science ®Google Scholar
• Tousen Y, Ezaki J, Fujii Y, Ueno T, Nishimuta M, Ishimi Y. Natural S-equol decreases bone resorption in postmenopausal, non-equol-producing Japanese women: a pilot randomized, placebo-controlled trial. Menopause 2011;18:563–74
   PubMed Web of Science ®Google Scholar
• Chi X-X, Zhang T. The effects of soy isoflavone on bone density in north region of climacteric Chinese women. J Clin Biochem Nutr 2013;53:102–7
   PubMed Web of Science ®Google Scholar
• Alekel DL, Van Loan MD, Koehler KJ, et al. The soy isoflavones for reducing bone loss (SIRBL) study: a 3-y randomized controlled trial in postmenopausal women. Am J Clin Nutr 2010;91:218–30
   PubMed Web of Science ®Google Scholar
• Tai T, Tsai K, Tu S, et al. The effect of soy isoflavone on bone mineral density in postmenopausal Taiwanese women with bone loss: a 2-year randomized double-blind placebo-controlled study. Osteoporos Int 2012;23:1571–80
   PubMed Web of Science ®Google Scholar
• Levis S, Strickman-Stein N, Ganjei-Azar P, Xu P, Doerge DR, Krischer J. Soy isoflavones in the prevention of menopausal bone loss and menopausal symptoms: a randomized, double-blind trial. Arch Intern Med 2011;171:1363–9
   PubMed Web of Science ®Google Scholar
• Kenny AM, Mangano KM, Abourizk RH, et al. Soy proteins and isoflavones affect bone mineral density in older women: a randomized controlled trial. Am J Clin Nutr 2009;90:234–42
   PubMed Web of Science ®Google Scholar
• Vupadhyayula PM, Gallagher JC, Templin T, Logsdon SM, Smith LM. Effects of soy protein isolate on bone mineral density and physical performance indices in postmenopausal women – a 2-year randomized, double-blind, placebo-controlled trial. Menopause 2009;16:320–8
   PubMed Web of Science ®Google Scholar
• Roughead ZK, Hunt JR, Johnson LK, Badger TM, Lykken GI. Controlled substitution of soy protein for meat protein: effects on calcium retention, bone, and cardiovascular health indices in postmenopausal women. J Clin Endocrinol Metab 2005;90:181–9
   PubMed Web of Science ®Google Scholar
• Turhan NO, Bolkan F, Duvan Cİ, Ardiçoğlu Y. The effect of isoflavones on bone mass and bone remodelling markers in postmenopausal women. Turk J Med Sci 2008;38:145–52
   Web of Science ®Google Scholar
• Albertazzi P, Steel S, Bottazzi M. Effect of pure genistein on bone markers and hot flushes. Climacteric 2005;8:371–9
   PubMed Web of Science ®Google Scholar
• Marini H, Minutoli L, Polito F, et al. Effects of the phytoestrogen genistein on bone metabolism in osteopenic postmenopausal women: a randomized trial. Ann Intern Med 2007;146:839–47
   PubMed Web of Science ®Google Scholar
• Zhang G, Qin L, Shi Y. Epimedium‐derived phytoestrogen flavonoids exert beneficial effect on preventing bone loss in late postmenopausal women: a 24‐month randomized, double‐blind and placebo‐controlled trial. J Bone Min Res 2007;22:1072–9
   PubMed Web of Science ®Google Scholar
• Brink E, Coxam V, Robins S, et al. Long-term consumption of isoflavone-enriched foods does not affect bone mineral density, bone metabolism, or hormonal status in early postmenopausal women: a randomized, double-blind, placebo controlled study. Am J Clin Nutr 2008;87:761–70
   PubMed Web of Science ®Google Scholar
• Arjmandi BH, Lucas EA, Khalil DA, et al. One year soy protein supplementation has positive effects on bone formation markers but not bone density in postmenopausal women. Nutr J 2005;4:8
   PubMed Web of Science ®Google Scholar
• Gui J-C, Brašić J, Liu X-D, et al. Bone mineral density in postmenopausal Chinese women treated with calcium fortification in soymilk and cow's milk. Osteoporos Int 2012;23:1563–70
   PubMed Web of Science ®Google Scholar
• Thorup AC, Lambert MN, Kahr HS, Bjerre M, Jeppesen PB. Intake of novel red clover supplementation for 12 weeks improves bone status in healthy menopausal women. Evid Based Complement Alternat Med 2015;2015:689138
   PubMed Web of Science ®Google Scholar
• Clifton-Bligh P, Nery M, Clifton-Bligh R, et al. Red clover isoflavones enriched with formononetin lower serum LDL cholesterol – a randomized, double-blind, placebo-controlled study. Eur J Clin Nutr 2015;69:134–42
   PubMed Web of Science ®Google Scholar
• Radhakrishnan G, Rashmi NA, Vaid NB. Evaluation of isoflavone rich soy protein supplementation for postmenopausal therapy. Pakistan J Nutr 2009;8:1009–17
   Google Scholar
• Stathopoulos KD, Zoubos AB, Papaioannou NA, et al. Differences of bone mineral mass, volumetric bone mineral density, geometrical and structural parameters and derived strength of the tibia between premenopausal and postmenopausal women of different age groups: a peripheral Quantitative Computed Tomography (pQCT) study. J Musculoskelet Neuronal Interact 2016;16:113–21
   PubMed Web of Science ®Google Scholar
• Greendale GA, Tseng CH, Han W, et al. Dietary isoflavones and bone mineral density during midlife and the menopausal transition: cross-sectional and longitudinal results from the Study of Women's Health Across the Nation Phytoestrogen Study. Menopause 2015;22:279–88
   PubMed Web of Science ®Google Scholar
• Mortensen A, Kulling SE, Schwartz H, et al. Analytical and compositional aspects of isoflavones in food and their biological effects. Molec Nutr Food Res 2009;53(Suppl 2):S266–S309
   PubMed Web of Science ®Google Scholar
• Zheng X, Lee SK, Chun OK. Soy isoflavones and osteoporotic bone loss: a review with an emphasis on modulation of bone remodeling. J Med Food 2016;19:1–14
   PubMed Web of Science ®Google Scholar
• Taku K, Melby MK, Takebayashi J, et al. Effect of soy isoflavone extract supplements on bone mineral density in menopausal women: meta-analysis of randomized controlled trials. Asia Pacific J Clin Nutr 2010;19:33–42
   PubMed Web of Science ®Google Scholar
• Ho SC, Chan SG, Yi Q, Wong E, Leung PC. Soy intake and the maintenance of peak bone mass in Hong Kong Chinese women. J Bone Miner Res 2001;16:1363–9
   PubMed Web of Science ®Google Scholar
• Michelin RM, Al-Nakkash L, Broderick TL, Plochocki JH. Genistein treatment increases bone mass in obese, hyperglycemic mice. Diabetes, Metab Syndr Obes 2016;9:63–70
   PubMed Web of Science ®Google Scholar
• Poulsen RC, Kruger MC. Soy phytoestrogens: impact on postmenopausal bone loss and mechanisms of action. Nutr Rev 2008;66:359–74
   PubMed Web of Science ®Google Scholar
• Weaver CM, Cheong JM. Soy isoflavones and bone health: the relationship is still unclear. J Nutr 2005;135:1243–7
   PubMed Web of Science ®Google Scholar