Hostname: page-component-76fb5796d-dfsvx Total loading time: 0 Render date: 2024-04-26T17:35:40.249Z Has data issue: false hasContentIssue false
  • English
  • Français

Investigating the role of natural phyto-oestrogens on bone health in postmenopausal women

Published online by Cambridge University Press:  26 October 2011

Silvia Valtueña ,
Kevin Cashman ,
Simon P. Robins ,
Aedin Cassidy ,
Alwine Kardinaal  and
Francesco Branca
Silvia Valtueña
Affiliation:
Unit of Human Nutrition, National Institute for Research on Food and Nutrition, Via Ardeatina 546, 1-00179 Rome, Italy
Kevin Cashman
Affiliation:
Nutritional Sciences, Department of Food Science, Food Technology and Nutrition, University College, Cork, Republic of Ireland
Simon P. Robins
Affiliation:
Rowett Research Institute, Bucksburn, Aberdeen AB21 9SB, UK
Aedin Cassidy
Affiliation:
Unilever Research, Molecular Nutrition and Physiology Unit, Colworth House, Sharnbrook, Bedford MK44 1LQ, UK
Alwine Kardinaal
Affiliation:
Department of Nutritional Physiology, TNO Nutrition and Food Research Institute, PO Box 360, 3700 AJ Zeist, The Netherlands
Francesco Branca*
Affiliation:
Unit of Human Nutrition, National Institute for Research on Food and Nutrition, Via Ardeatina 546, 1-00179 Rome, Italy
*
*Corresponding author: Dr F. Branca, fax +39 06 50 31 592, email f.branca@agora.it
Rights & Permissions [Opens in a new window]

Extract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Research on the bone effects of natural phyto-oestrogens after menopause is at a relatively early stage. Published studies are few, difficult to compare and often inconclusive, due in part to design weaknesses. Currently, many questions remain to be answered including to what extent a safe daily intake may prevent postmenopausal bone loss. These questions can only be addressed by conducting well-planned, randomised clinical trials that take into consideration present knowledge in the oestrogen, phyto-oestrogen and bone fields. This review is intended to provide hints for critical decision-making about the selection of subjects, type of intervention, suitable outcome measures and variables that need to be controlled.

Keywords

IsoflavonesMenopauseClinical trials
Type
Research Article
Information
British Journal of Nutrition , Volume 89 , Issue S1: Effects of Phyto-oestrogens on Bone Health: the VENUS Concerted Action , June 2003 , pp. S87 - S99
Copyright
Copyright © The Nutrition Society 2003

References

Alekel, D, St. Germain, A, Peterson, C, Hanson, K, Stewart, J & Toda, T (2000) Isoflavone-rich soy protein isolate attenuates bone loss in the lumbar spine of perimenopausal women. American Journal of Clinical Nutrition 72, 844–852.CrossRefGoogle ScholarPubMed
Anderson, J & Ambrose, W (1995) Orally dosed genistein from soy and prevention of cancellous bone loss in two ovariectomized rat models. Journal of Nutrition 125, Suppl., 799S.Google Scholar
Appel, LJ, Moore, TJ, Obarzanek, E, Bray, GA, Vogt, TM, Cutler, JA, Windhauser, MM, Lin, PH & Karanja, N (1997) A clinical trial of the effects of dietary patterns on blood pressure. DASH Collaborative Research Group. New England Journal of Medicine 336, 1117–1124.CrossRefGoogle ScholarPubMed
Arjmandi, B, Birnbaum, R, Goyal, N, Getlinger, M, Juma, S, Alekel, L, Hasler, C, Drum, M, Hollis, B & Kukreja, S (1998 a) Bonesparing effect of soy protein in ovarian hormone-deficient rats is related to its isoflavone content. American Journal of Clinical Nutrition 68, Suppl., 1364S–1368S.CrossRefGoogle ScholarPubMed
Arjmandi, B, Birnbaum, R, Juma, S, Barengolts, E & Kukreja, S (2000) The synthetic phyto-oestrogen, ipriflavone, and oestrogen prevent bone loss by different mechanisms. Calcified Tissue International 66, 61–65.CrossRefGoogle Scholar
Arjmandi, B, Getlinger, M, Goyal, N, Alekel, L, Hasler, C, Joma, S, Drum, M, Hollis, B & Kukreja, S (1998 b) Role of soy protein with normal or reduced isoflavone content in reversing bone loss induced by ovarian hormone deficiency in rats. American Journal of Clinical Nutrition 68, Suppl., 1358S–1363S.CrossRefGoogle ScholarPubMed
Arjmandi, B, Slekel, L, Hollis, B, Amin, D, Stacewicz-Sapuntzakis, M, Guo, P & Kukreja, SC (1996) Dietary soybean protein prevents bone loss in an ovariectomized rat model of osteo-porosis. Journal of Nutrition 126, 161–167.CrossRefGoogle Scholar
Augat, P, Gordon, C, Lang, T, Iida, H & Genant, H (1998) Accuracy of cortical and trabecular bone measurements with peripheral quantitative computed tomography (pQCT). Physics in Medicine and Biology 43, 2873–2883.CrossRefGoogle ScholarPubMed
Augat, P, Reeb, H & Claes, L (1996) Prediction of fracture load at different skeletal sites by geometric properties of the cortical shell. Journal of Bone and Mineral Research 11, 1356–1363.CrossRefGoogle ScholarPubMed
Bagger, Y, Jorgensen, H, Heegaard, A, Bayer, L, Hansen, L & Hassager, C (2000) No major effect of oestrogen receptor gene polymorphisms on bone mineral density or bone loss in postmenopausal Danish women. Bone 26, 111–116.CrossRefGoogle ScholarPubMed
Bauer, D, Sklarin, P, Stone, K, Black, D, Nevitt, M, Ensrud, K, Arnaud, C, Genant, H, Garnero, P, Delmas, P, Lawaetz, H & Cummings, SR (1999) Biochemical markers of bone turnover and prediction of hip bone loss in older women: the study of osteoporotic fractures. Journal of Bone and Mineral Research 14, 1404–1410.CrossRefGoogle ScholarPubMed
Berard, A, Bravo, G & Gauthier, P (1997) Meta-analysis of the effectiveness of physical activity for the prevention of bone loss in postmenopausal women. Osteoporosis International 7, 331–337.CrossRefGoogle ScholarPubMed
Beresford, S, Weiss, N, Voight, L & McKnight, B (1997) Risk of endometrial cancer in relation to use of oestrogen combined with cyclic progestagen therapy in postmenopausal women. Lancet 349, 458–461.CrossRefGoogle ScholarPubMed
Biro, G, Hulshof, K, Oversen, L & Amorim Cruz, J (2002) Selection of methodology to assess food intake. European Journal of Clinical Nutrition, in press.CrossRefGoogle Scholar
Bonde, M, Qvist, P, Fledelius, C, Riis, BJ & Christiansen, C (1994) Immunoassay for quantifying type I degradation products in urine evaluated. Clinical Chemistry 40, 2022–2025.CrossRefGoogle Scholar
Bouxein, M, Myburg, K, van der Meulenm, M, Linderberg, E & Marcus, R (1994) Age-related differences in cross sectional geometry of the forearm bones in healthy women. Calcified Tissue International 54, 113–118.CrossRefGoogle Scholar
Brady, J, Ju, J & Robins, S (1999) Isoaspartyl bond formation within N-terminal sequences of collagen type I: implications for their use as markers of collagen degradation. Clinical Science 96, 209–215.CrossRefGoogle ScholarPubMed
Brandt, J, Krogh, T, Jensen, C, Frederiksen, J & Teisner, B (1999) Thermal instability of the trimeric structure of the N-terminal propeptide of human procollagen type I in relation to assay technology. Clinical Chemistry 45, 47–53.CrossRefGoogle ScholarPubMed
Cassidy, A, Bingham, S & Setchell, K (1994) Biological effects of a diet of soy protein rich in isoflavones on the menstrual cycle of premenopausal women. American Journal of Clinical Nutrition 60, 333–340.CrossRefGoogle Scholar
Cawte, SA, Pearson, D, Green, DJ, Maslanka, WB, Miller, CG & Rogers, AT (1999) Cross-calibration, precision and patient dose measurements in preparation for clinical trials using dual energy X-ray absorptiometry of the lumbar spine. British Journal of Radiology 72, 354–362.CrossRefGoogle ScholarPubMed
Chrischilles, E, Shireman, T & Wallace, R (1994) Cost and health effects of osteoporotic fractures. Bone 15, 337–386.CrossRefGoogle ScholarPubMed
Clemens, J, Herrick, M, Singer, F & Eyre, D (1997) Evidence that serum N-terminal cross-linked peptide of type I collagen; (collagen-type I N-telopeptides) can act as an immunochemical marker of bone resorption. Clinical Chemistry 43, 2058–2063.CrossRefGoogle Scholar
Cloos, P & Fledelius, C (2000) Collagen fragments in urine derived from bone resorption are highly racemized and isomerized: a biological clock of protein aging with clinical potential. Biochemical Journal 345, 473–480.CrossRefGoogle ScholarPubMed
Colditz, G, Hankinson, S, Hunter, D, Willett, W, Manson, J, Stampfer, M, Hennekens, C, Rosner, B & Speizer, F (1995) The use of oestrogens and progestins and the risk of breast cancer in postmenopausal women. New England Journal of Medicine 332, 1589–1593.CrossRefGoogle ScholarPubMed
Cooper, C & Melton, LI (1996) Magnitude of the impact of osteoporosis and fractures. In Osteoporosis, pp. 419–434 [Marcus, R, Feldman, D and Kelsey, J, editors], San Diego, CA: Academic Press.Google Scholar
Coxam, V (2003) Prevention of osteopaenia by phyto-oestrogens: animal studies. British Journal of Nutrition 89, Suppl. 1, S75–S85.CrossRefGoogle ScholarPubMed
Cummings, S, Black, D, Nevitt, M, Browner, W, Cauley, J, Ensrud, K, Genant, H, Palermo, L, Scott, J & Vogt, T (1993) Bone density at various sites for prediction of hip fractures. Lancet 341, 72–75.CrossRefGoogle ScholarPubMed
Cummings, S, Nevitt, M, Browner, W, Stone, K, Fox, K, Ensrud, K, Cauley, J, Black, D & Vogt, T (1995) Risk factors for hip fracture in white women. New England Journal of Medicine 332, 767–773.CrossRefGoogle ScholarPubMed
Dalais, F, Rice, G, Wahlqvist, M, Grehan, M, Murkies, A, Medley, G, Ayton, R & Strauss, B (1998) Effects of dietary phyto-oestrogens in postmenopausal women. Climateric 1, 124–129.CrossRefGoogle ScholarPubMed
Dawson-Hughes, B, Harris, S, Krall, E & Dallal, G (1997) Effect of calcium and vitamin D supplementation on bone density in men and women 65 years of age or older. New England Journal of Medicine 337, 670–676.CrossRefGoogle ScholarPubMed
Delmas, P (1990) Biochemical markers of bone turnover for the clinical assessment of metabolic bone disease. Endocrinology and Metabolism Clinics of North America 19, 1–18.CrossRefGoogle ScholarPubMed
Delmas, PD (2001) Bone marker nomenclature. Bone 28, 575–576.CrossRefGoogle ScholarPubMed
Deng, H, Li, J, Li, JL, Johnson, M, Gong, G & Recker, R (1999) Association of VDR and oestrogen receptor genotypes with bone mass in postmenopausal Caucasian women: different conclusions with different analyses and the implications. Osteoporosis International 9, 499–507.CrossRefGoogle ScholarPubMed
Deng, HW, Li, J, Li, JL, Johnson, M, Gong, G, Davis, K & Recker, RR (1998) Change of bone mass in postmenopausal Caucasian women with and without hormone replacement therapy is associated with vitamin D receptor and oestrogen receptor genotypes. Human Genetics 103, 576–585.CrossRefGoogle ScholarPubMed
Draper, C, Edel, M, Dick, I, Randall, A, Martin, G & Prince, R (1997) Phyto-oestrogens reduce bone loss and bone resorption in ovariectomized rats. Journal of Nutrition 127, 1795–1799.CrossRefGoogle Scholar
Eastell, R, Mallinak, N, Weiss, S, Ettinger, M, Pettinger, M, Cain, D, Fressland, K & Chesnut, CR (2000) Biological variability of serum and urinary N-telopeptides of type I collagen in postmenopausal women. Journal of Bone and Mineral Research 15, 594–598.CrossRefGoogle ScholarPubMed
Ebbsesen, E, Thomsen, J, Beck-Nielsen, H, Nepper-Rasmussen, H & Mosekilde, L (1999) Age- and gender-related differences in vertebral bone mass, density, and strength. Journal of Bone Mineral Research 14, 1394–1403.CrossRefGoogle Scholar
Enmark, E, Pelto-Huikko, M, Grandien, K, Lagercrantz, S, Lagercrantz, J, Fried, G, Nordenskjold, M & Gustafsson, J-A (1997) Human oestrogen receptor beta-gene structure, chromosomal localization, and expression pattern. Journal of Clinical Endocrinology and Metabolism 82, 4258–4265.Google ScholarPubMed
Fanti, P, Monier-Faugere, M, Geng, Z, Schmith, J, Morris, P, Cohen, D & Malluch, H (1998) The phyto-oestrogen genistein reduces bone loss in short-term ovariectomized rats. Osteoporosis International 8, 274–281.CrossRefGoogle ScholarPubMed
Faulkner, KG (2001) Update on bone density measurement. Rheumatic Diseases Clinics of North America 27, 81–99.CrossRefGoogle ScholarPubMed
Faulkner, KG & Pocock, N (2001) Future methods in the assessment of bone mass and structure. Best Practice Research in Clinical Rheumatology 15, 359–383.CrossRefGoogle ScholarPubMed
Fedarko, NS, Fohr, B, Robey, PG, Young, MF & Fisher, LW (2000) Factor H binding to bone sialoprotein and osteopontin enables tumor cell evasion of complement-mediated attack. Journal of Biological Chemistry 275, 16666–16672.CrossRefGoogle ScholarPubMed
Fedarko, NS, Jain, A, Karadag, A, Van Eman, MR & Fisher, LW (2001) Elevated serum bone sialoprotein and osteopontin in colon, breast, prostate, and lung cancer. Clinical Cancer Research 7, 4060–4066.Google ScholarPubMed
Fledelius, C, Johnsen, A, Cloos, P, Bonde, M & Qvist, P (1997) Characterization of urinary degradation products derived from type I collagen. Identification of a beta-isomerized Asp–Gly sequence within the C-terminal telopeptide (al) region. Journal of Biological Chemistry 272, 9755–9763.CrossRefGoogle Scholar
Formica, CA, Nieves, JW, Cosman, F, Garrett, P & Lindsay, R (1998) Comparative assessment of bone mineral measurements using dual X-ray absorptiometry and peripheral quantitative computed tomography. Osteoporosis International 8, 460–467.CrossRefGoogle ScholarPubMed
Fuleihan, G, Testa, M, Angell, J, Porrino, N & Leboff, M (1995) Reproducibility of dual-energy X-ray absorptiometry; absorptiometry: a model for bone loss estimates. Journal of Bone and Mineral Research 10, 1004–1014.CrossRefGoogle Scholar
Gambacciani, M, Ciaponi, M, Cappagli, B, Piaggesi, L & Genazzani, A (1997) Effects of combined low dose of the isoflavone derivative ipriflavone and oestrogen replacement on bone mineral density and metabolism in postmenopausal women. Maturitas 28, 75–81.CrossRefGoogle Scholar
Garnero, P & Delmas, P (1993) Assessment of the serum levels of bone alkaline phosphatase with a new immunoradiometric assay in patients with metabolic bone disease. Journal of Clinical Endocrinology and Metabolism 77, 1046–1053.Google ScholarPubMed
Garnero, P, Grimaux, M, Seguin, P & Delmas, P (1994) Characterisation of immunoreactive forms of human osteocalcin generated in vivo and in vitro. Journal of Bone and Mineral Research 9, 255–264.CrossRefGoogle ScholarPubMed
Garnero, P, Hausherr, E, Chapuy, M, Marcelli, C, Grandjean, H, Muller, C, Cormier, C, Breart, G, Meunier, P & Delmas, P (1996 a) Markers of bone resorption predict hip fracture in elderly women: the EPIDOS prospective study. Journal of Bone and Mineral Research 11, 1531–1538.CrossRefGoogle ScholarPubMed
Garnero, P, Sornay-Rendu, E, Chapuy, M & Delmas, P (1996 b) Increased bone turnover in late postmenopausal women is a major determinant of osteoporosis. Journal of Bone and Mineral Research 11, 337–349.CrossRefGoogle Scholar
Garnero, P, SornayRendu, E, Duboeuf, F & Delmas, P (1999) Markers of bone turnover predict postmenopausal forearm bone loss over 4 years: the OFELY study. Journal of Bone and Mineral Research 14, 1614–1621.CrossRefGoogle ScholarPubMed
Gennari, C, Adami, S, Agnusdei, D, Bufalino, L, Cervetti, R, Crepaldi, G, Di Marco, C, Di Munno, O, Fantasia, L, Isaia, G, Mazzuoli, G, Ortolani, S, Passeri, M, Serni, U & Vecchiet, L (1997) Effect of chronic treatment with ipriflavone in postmenopausal women with low bone mass. Calcified Tissue International, S19–S22.CrossRefGoogle Scholar
Gennari, C, Agnusdei, D, Crepaldi, G, Isaia, G, Mazzuoli, G, Ortolani, S, Bufalino, L & Passeri, M (1998 a) Effect of ipriflavone — a synthetic derivative of natural isoflavones — on bone mass loss in the early years after menopause. Menopause 5, 9–15.Google Scholar
Gennari, L, Becherini, L, Masi, L, Mansani, R, Gonnelli, S, Cepollaro, C, Martini, S, Montagnani, A, Lentini, G, Becorpi, A & Brandi, M (1998 b) Vitamin D and oestrogen receptor allelic variants in Italian postmenopausal women: evidence of multiple gene contribution to bone mineral density. Journal of Clinical Endocrinology and Metabolism 83, 939–944.CrossRefGoogle ScholarPubMed
Gomez, B, Ardakani, S, Evans, B, Merrell, L, Jenkins, D & Kung, V (1996) Monoclonal antibody assay for free urinary pyridinium cross-links. Clinical Chemistry 42, 1168–1175.CrossRefGoogle ScholarPubMed
Gomez, B, Ardakani, S, Ju, J, Jenkins, D, Cerelli, M, Daniloff, G & Kung, V (1995) Monoclonal antibody assay for measuring bone-specific alkaline phosphatase activity in serum. Clinical Chemistry 41, 1560–1566.CrossRefGoogle ScholarPubMed
Gotfredsen, A, Baeksgaard, L & Hilsted, J (1997) Body composition analysis by dual-energy X-ray absorptiometry; by using dynamically changing samarium filtration. Journal of Applied Physiology 82, 1200–1209.CrossRefGoogle ScholarPubMed
Greendale, GA, Wells, B, Marcus, R & Barrett Connor, E (2000) How many women lose bone mineral density while taking hormone replacement therapy? Results from the Postmenopausal Oestrogen/Progestin Interventions Trial. Archives of Internal Medicine 160, 3065–3071.CrossRefGoogle ScholarPubMed
Hadjidakis, D, Kokkinakis, E, Sfakianakis, M & Raptis, S (1999) The type and time of menopause as decisive factors for bone mass changes. European Journal of Clinical Investigation 29, 877–885.CrossRefGoogle ScholarPubMed
Halleen, JM, Alatalo, SL, Suominen, H, Cheng, S, Janckila, AJ & Vaananen, HK (2000) Tartrate-resistant acid phosphatase 5b: a novel serum marker of bone resorption. Journal of Bone and Mineral Research 15, 1337–1345.CrossRefGoogle ScholarPubMed
Han, K, Choi, J, Moon, I, Yoon, H, Han, I, Min, H, Kim, Y & Choi, Y (1999) Non-association of oestrogen receptor genotypes with bone mineral density and bone turnover in Korean pre-, peri-, and postmenopausal women. Osteoporosis International 9, 290–295.CrossRefGoogle ScholarPubMed
Han, K, Moon, I, Kang, Y, Chung, H, Min, H & Han, I (1997) Non-association of oestrogen receptor genotypes with bone mineral density and oestrogen responsiveness to hormone replacement therapy in Korean postmenopausal women. Journal of Clinical Endocrinology and Metabolism 82, 991–995.CrossRefGoogle Scholar
Hanson, D, Weis, M, Bollen, A, Maslan, S, Singer, F & Eyre, D (1992) A specific immunoassay for monitoring human bone resorption: quantitation of type I collagen cross-linked N-telo-peptides in urine. Journal of Bone and Mineral Research 7, 1251–1258.CrossRefGoogle ScholarPubMed
Hassager, C, Jensen, S & Christiansen, C (1994) Non-responders to hormone replacement therapy for the prevention of postmenopausal bone loss: do they exist? Osteoporosis International 4, 36–41.CrossRefGoogle ScholarPubMed
Heaney, R (1996) Nutrition and risk for osteoporosis. In Osteoporosis, pp. 483–509 [Marcus, R, Feldman, D and Kelsey, J, editors]. San Diego, CA: Academic Press.Google ScholarPubMed
Heaney, R (1998) Excess dietary protein may not adversely affect bone. Journal of Nutrition 128, 1054–1057.CrossRefGoogle Scholar
Horiuchi, T, Onouchi, T, Takahashi, M, Ito, H & Orimo, H (2000) Effect of soy protein on bone metabolism in postmenopausal Japanese women. Osteoporosis International 11, 721–724.CrossRefGoogle Scholar
Hsu, CS, Shen, WW, Hsueh, YM & Yeh, SL (2001) Soy isoflavone supplementation in postmenopausal women. Effects on plasma lipids, antioxidant enzyme activities and bone density. Journal of Reproductive Medicine 46, 221–226.Google ScholarPubMed
Hui, S, Wiske, H, Norton, JA & Johnston, CC Jr (1982) A prospective study of change in bone mass with age in postmenopausal women. Journal of Chronic Diseases 35, 715–725.CrossRefGoogle ScholarPubMed
Ishimi, Y, Miyaura, C, Ohmura, M, Onoe, Y, Sato, T, Uchiyama, Y, Ito, M, Wang, X, Suda, T & Ikegami, S (1999) Selective effects of genistein, a soybean isoflavone, on B-lymphopoiesis and bone loss caused by oestrogen deficiency. Endocrinology 140, 1893–1900.CrossRefGoogle Scholar
James, I & Perrett, D (1998) Automated on-line solid-phase extraction and high-performance liquid chromatographic analysis of total and free pyridinium crosslinks in serum. Journal of Chromatography 79A, 159–166.CrossRefGoogle Scholar
Jayo, M, Anthony, M, Register, T, Rankin, S, Vest, T & Clakson, T (1997) Dietary soy isoflavones and bone loss in ovariectomized monkeys. FASEB Journal 11, 228, Abstr.Google Scholar
Jiang, Y, Zhao, J, Augat, P, Ouyang, X, Lu, Y, Majumdar, S & Genant, H (1998) Trabecular bone mineral and calculated structure of human bone specimens scanned by peripheral quantitative computed tomography: relation to biomechanical properties. Journal of Bone and Mineral Research 13, 1783–1790.CrossRefGoogle ScholarPubMed
Kanis, J (1993) The incidence of hip fracture in Europe. Osteoporosis International 1, Suppl., 10S–15S.CrossRefGoogle Scholar
Kardinaal, A, Morton, M, Bruggermann-Rotgans, I & Van Beresteijn, E (1998) Phyto-oestrogen excretion and rate of bone loss in postmenopausal women. European Journal of Clinical Nutrition 52, 850–855.CrossRefGoogle ScholarPubMed
Karmatschek, M, Maier, I, Seibel, M, Woitge, H, Ziegler, R & Armbruster, F (1997) Improved purification of human bone sialoprotein and development of a homologous radioimmunoassay. Clinical Chemistry 43, 2076–2082.CrossRefGoogle ScholarPubMed
Kiely, M, Faughnan, M, Wähälä, K, Brants, H & Mulligan, A (2003) Phyto-oestrogen levels in foods: the design and construction of the Vegetal Estrogens in Nutrition and the Skeleton database. British Journal of Nutrition 89, Suppl. 1, S19–S23.CrossRefGoogle ScholarPubMed
Kobayashi, S, Inoue, S, Hosoi, T, Ouchi, Y, Shiraki, M & Orimo, H (1996) Association of bone mineral density with polymorphism of the oestrogen receptor gene. Journal of Bone and Mineral Research 11, 306–311.CrossRefGoogle Scholar
Komulainen, M, Kröger, H, Tuppurainen, M, Heikkinen, A-M, Alhava, E, Honkanen, R, Jurvelin, J & Saarikoski, S (1999) Prevention of femoral and lumbar bone loss with hormone replacement therapy and vitamin D3 in early postmenopausal women: a population-based 5-year randomized trial. Journal of Clinical Endocrinology and Metabolism 84, 546–552.Google ScholarPubMed
Kuiper, GG, Carlsson, B, Grandien, K, Enmark, E, Haggblad, J, Nilsson, S & Gustafsson, JA (1997) Comparison of the ligand binding specificity and transcript tissue distribution of oestrogen receptors alpha and beta. Endocrinology 138, 863–870.CrossRefGoogle ScholarPubMed
Kuiper, GG, Lemmen, JG, Carlsson, B, Corton, JC, Safe, SH, van der Saag, PT, van der Burg, B & Gustafsson, JA (1998) Interaction of oestrogenic chemicals and phyto-oestrogens with oestrogen receptor beta. Endocrinology 139, 4252–4263.CrossRefGoogle Scholar
Lang, T, Augat, P, Majumdar, S, Ouyang, X & Genant, H (1998) Noninvasive assessment of bone density and structure using computed tomography and magnetic resonance. Bone 22, Suppl. 5, 149S–153S.CrossRefGoogle ScholarPubMed
Lang, TF, Keyak, JH, Heitz, MW, Augat, P, Lu, Y, Mathur, A & Genant, HK (1997) Volumetric quantitative computed tomography of the proximal femur: precision and relation to bone strength. Bone 21, 101–108.CrossRefGoogle ScholarPubMed
Lanyon, LE (1996) Using functional loading to influence bone mass and architecture: objectives, mechanisms, and relationship with oestrogen of the mechanically adaptive process in bone. Bone 18, 37S–43S.CrossRefGoogle ScholarPubMed
Lindsay, R, Hart, D, Aitken, J, MacDonald, E, Anderson, J & Clarke, A (1976) Long-term prevention of postmenopausal osteoporosis by oestrogen: evidence for an increased bone mass after delayed onset of oestrogen treatment. Lancet 1, 1038–1041.CrossRefGoogle ScholarPubMed
McClung, M, Clemmesen, B, Daifotis, A, Gilchrist, N, Eisman, J, Weinstein, R, Fuleihan, G, Reda, C, Yates, A & Ravn, P (1998) Alendronate prevents postmenopausal bone loss in women without osteoporosis. Annals of Internal Medicine 128, 253–261.CrossRefGoogle ScholarPubMed
Mahonen, A, Turunen, A, Kroger, H & Maenpaa, P (1997) Oestrogen receptor polymorphism is associated with bone mineral density in perimenopausal Finnish women. Journal of Bone and Mineral Research 12, T614.Google Scholar
Majumdar, S, Link, T, Augat, P, Lin, J, Newitt, D, Lane, N & Genant, H (1999) Trabecular bone architecture in the distal radius using magnetic resonance imaging in subjects with fractures of the proximal femur. Magnetic Resonance Science Center and Osteoporosis and Arthritis Research Group. Osteoporosis International 10, 231–239.CrossRefGoogle ScholarPubMed
Martin, P, Horwitz, K, Ryan, D & McGuire, W (1978) Phyto-oestrogen interaction with oestrogen receptors in human breast cancer cells. Endocrinology 103, 1860–1867.CrossRefGoogle ScholarPubMed
Massey, L (1998) Does dietary protein adversely affect bone? Journal of Nutrition 128, 1048–1050.CrossRefGoogle ScholarPubMed
Mazzuoli, G, Acca, M, Pisani, D, Diacinti, D, Scarda, A, Scarnecchia, L, D'Erasmo, E, Minisola, S, Bianchi, G & Manfredi, G (2000) Annual skeletal balance and metabolic bone marker change in healthy early postmenopausal women: results of a prospective study. Bone 26, 381–386.CrossRefGoogle ScholarPubMed
Melkko, J, Kauppila, S, Niemi, S, Risteli, L, Haukipuro, K, Jukkola, A & Risteli, J (1996) Immunoassay for intact aminoterminal propeptide of human type I procollagen. Clinical Chemistry 42, 947–954.CrossRefGoogle ScholarPubMed
Melkko, J, Niemi, S, Risteli, L & Risteli, J (1990) Radioimmunoassay of the carboxy terminal propeptide of human type I procollagen. Clinical Chemistry 36, 1328–1332.CrossRefGoogle ScholarPubMed
Melton, LD (1995) Epidemiology of fractures. In Osteoporosis: Etiology, Diagnosis, and Management, pp. 225–247 [Riggs, B and Melton, LD, editors]. Philadelphia, PA: Lippincott-Raven.Google Scholar
Messina, M (1999) Legumes and soybeans: overview of their nutritional profiles and health effects. American Journal of Clinical Nutrition 70, Suppl., 439S–450S.CrossRefGoogle ScholarPubMed
Mizunuma, H, Hosoi, T, Okano, H, Soda, M, Tokizawa, T, Kagami, I, Miyamoto, S, Ibuki, Y, Inoue, S, Shiraki, M & Ouchi, Y (1997) Oestrogen receptor gene polymorphism and bone mineral density at the lumbar spine of pre- and postmenopausal women. Bone 21, 379–383.CrossRefGoogle ScholarPubMed
National Institutes of Health Consensus Statement (2000) Osteoporosis Prevention, Diagnosis, and Therapy, vol. 17. Bethesda, MD: National Institutes of Health.Google Scholar
Nawata, H, Tanaka, S, Tanaka, S, Takayanagi, R, Sakai, Y, Yanase, T, Ikuyama, S & Haji, M (1995) Aromatase in bone cell: association with osteoporosis in postmenopausal women. Journal of Steroid Biochemistry and Molecular Biology 53, 65–74.CrossRefGoogle ScholarPubMed
Nguyen, T, Jones, G, Sambrook, P, White, C, Kelly, P & Eisman, J (1995) Effects of oestrogen exposure and reproductive factors on bone mineral density and osteoporotic fractures. Journal of Clinical Endocrinology and Metabolism 80, 2709–2714.Google Scholar
Nielsen, P, Barenholdt, O, Diessel, E, Armbrust, S & Felsenberg, D (1998) Linearity and accuracy errors in bone densitometry. British Journal of Radiology 71, 1062–1068.CrossRefGoogle Scholar
Nilas, L (1993) Calcium intake and osteoporosis. In Osteoporosis: Nutritional Aspects, 1st ed. pp. 1–27 [Simopoulos, A and Galli, C, editors]. World Review of Nutrition and Dietetics vol. 73. Basel: Karger.CrossRefGoogle Scholar
North American Menopause Society (2000) The role of isoflavones in menopausal health: consensus opinion of the North American Menopause Society. Menopause 7A, 215–229.Google Scholar
Ogawa, S, Hosoi, T, Shiraki, M, Orimo, H, Emi, M, Muramatsu, M, Ouchi, Y & Inoue, S (2000) Association of oestrogen receptor beta gene polymorphism with bone mineral density. Biochemical and Biophysical Research Communications 269, 537–541.CrossRefGoogle ScholarPubMed
Ongphiphadhanakul, B, Chanprasertyothin, S, Payatikul, P, Tung, S, Piaseu, N, Chailurkit, L, Chansirikarn, S, Puavilai, G & Rajatanavin, R (2000) Oestrogen-receptor-alpha gene polymorphism affects response in bone mineral density to oestrogen in post-menopausal women. Clinical Endocrinology 52, 581–585.CrossRefGoogle ScholarPubMed
Ongphiphadhanakul, B, Rajatanavin, R, Chanprasertyothin, S, Piaseu, N, Chailurkit, L, Sirisriro, R & Komindr, S (1998) Oestrogen receptor gene polymorphism is associated with bone mineral density in premenopausal women but not in postmenopausal women. Journal of Endocrinological Investigation 21, 487–493.CrossRefGoogle Scholar
Pearson, J, Dequeker, J, Reeve, J, Felsenberg, D, Henley, M, Bright, J, Lunt, M, Adams, J, Diaz Curiel, M & Galan, F (1995) Dual X-ray absorptiometry of the proximal femur: normal European values standardized with the European Spine Phantom. Journal of Bone and Mineral Research 10, 315–324.CrossRefGoogle ScholarPubMed
Potter, S, Baum, J, Teng, H, Stillman, R, Shay, N & Erdman, J Jr (1998) Soy protein and isofiavones: their effects on blood lipids and bone density in postmenopausal women. American Journal of Clinical Nutrition 68, Suppl., 1375S–1379S.CrossRefGoogle Scholar
Reinli, K & Block, G (1996) Phyto-oestrogen content of foods — a compendium of literature values. Nutrition and Cancer 26, 123–148.CrossRefGoogle Scholar
Riggs, B & Melton, LJ III (1986) Involutional osteoporosis. New England Journal of Medicine 14, 1676–1686.CrossRefGoogle Scholar
Robins, S, Woitge, H, Hesley, R, Ju, J, Seyedin, S & Seibel, M (1994) Direct, enzyme-linked immunoassay for urinary deoxypyridinoline as a specific marker for measuring bone resorption. Journal of Bone and Mineral Research 9, 1643–1649.CrossRefGoogle ScholarPubMed
Rosenkranz, K, Hinney, A, Ziegler, A, Hermann, H, Fichter, M, Mayer, H, Siegfried, W, Young, J, Remschmidt, H & Hebebrand, J (1998) Systematic mutation screening of the oestrogen receptor beta gene in probands of different weight extremes: identification of several genetic variants. Journal of Clinical Endocrinology and Metabolism 83, 4524–4527.CrossRefGoogle ScholarPubMed
Rosenquist, C, Fledelius, C, Christgau, S, Pedersen, B, Bonde, M, Qvist, P & Christiansen, C (1998) Serum CrossLaps One Step ELISA. First application of monoclonal antibodies for measurement in serum of bone-related degradation products from C-terminal telopeptides of type I collagen. Clinical Chemistry 44, 2281–2289.CrossRefGoogle ScholarPubMed
Ross, P, Heilbrun, L, Wasnich, R, Davis, J & Vogel, J (1989) Perspectives: methodological issues in evaluating risk factors for osteoporotic fractures. Journal of Bone and Mineral Research 4, 649–656.CrossRefGoogle ScholarPubMed
Ross, PD, Norimatsu, H, Davis, JW, Yano, K, Wasnich, RD, Fujiwara, S, Hosoda, Y & Melton, LJ (1991) A comparison of hip fracture incidence among native Japanese, Japanese Americans, and American Caucasians. American Journal of Epidemiology 133, 801–809.CrossRefGoogle ScholarPubMed
Roubenoff, R, Kehayias, J, Dawson-Hughes, B & Heymsfield, S (1993) Use of dual-energy x-ray absorptiometry in body composition studies: not yet a ‘gold standard’. American Journal of Clinical Nutrition 58, 589–591.CrossRefGoogle Scholar
Rowland, I, Faughnan, M, Hoey, L, Wähälä, K, Williamson, G & Cassidy, A (2003) Bioavailability of phyto-oestrogens. British Journal of Nutrition 89, Suppl. 1, S45–S58.CrossRefGoogle ScholarPubMed
Salmen, T, Heikkinen, A, Mahonen, A, Kroger, H, Komulainen, M, Saarikoski, S, Honkanen, R & Maenpaa, P (2000) Early postmenopausal bone loss is associated with Pvu II oestrogen receptor gene polymorphism in Finnish women: effect of hormone replacement therapy. Journal of Bone and Mineral Research 15, 315–321.CrossRefGoogle Scholar
Sano, M, Inoue, S, Hosoi, T, Ouchi, Y, Emi, M, Shiraki, M & Orimo, H (1995) Association of oestrogen receptor dinucleotide repeat polymorphism with osteoporosis. Biochemical and Biophysical Research Communications 215, 378–383.CrossRefGoogle Scholar
Scheiber, MD, Liu, JH, Subbiah, MT, Rebar, RW & Setchell, KD (2001) NAMS Fellowship Findings: Dietary inclusion of whole soy foods results in significant reductions in clinical risk factors for osteoporosis and cardiovascular disease in normal postmenopausal women. Menopause 8, 384–392.CrossRefGoogle Scholar
Seibel, M, Woitge, H, Pecherstorfer, M, Karmatschek, M, Horn, E, Ludwig, H, Armbruster, F & Ziegler, R (1996) Serum immunoreactive bone sialoprotein as a new marker of bone turnover in metabolic and malignant bone disease. Journal of Clinical Endocrinology and Metabolism 81, 3289–3294.Google ScholarPubMed
Setchell, K & Cassidy, A (1999) Dietary isoflavones: biological effects and relevance to human health. Journal of Nutrition 129, 758S–767S.CrossRefGoogle ScholarPubMed
Setchell, KD, Brown, NM, Desai, P, Zimmer Nechemia, L, Wolfe, BE, Brashear, WT, Kirschner, AS, Cassidy, A & Heubi, JE (2001) Bioavailability of pure isoflavones in healthy humans and analysis of commercial soy isoflavone supplements. Journal of Nutrition 131, 1362S–1375S.CrossRefGoogle ScholarPubMed
Siffert, R, Luo, G, Cowin, S & Kauffman, J (1996) Dynamic relationships of trabecular bone density, architecture, and strength in a computational model of osteopenia. Bone 18, 197–206.CrossRefGoogle Scholar
Somekawa, Y, Chiguchi, M, Ishibashi, T & Aso, T (2001) Soy intake related to menopausal symptoms, serum lipids, and bone mineral density in postmenopausal Japanese women. Obstetrics and Gynecology 97, 109–115.Google ScholarPubMed
Thorsen, K, Kristoffersson, A & Lorentzon, R (1996) The effects of brisk walking on markers of bone and calcium metabolism in postmenopausal women. Calcified Tissue International 58, 221–225.CrossRefGoogle ScholarPubMed
Valsta, L, Kilkkinen, A, Mazur, W, Nurmi, T, Lampi, A-M, Ovaskainen, M-L, Korhonen, T, Adlercreutz, H & Pietinen, P (2003) Phyto-oestrogen database of foods and average intake in Finland. British Journal of Nutrition 89, Suppl. 1, S31–S38.CrossRefGoogle ScholarPubMed
Valtueña, S, Sette, S & Branca, F (2001) Influence of Mediterranean diet and Mediterranean lifestyle on calcium and bone metabolism. International Journal for Vitamin and Nutrition Research 71, 189–202.CrossRefGoogle ScholarPubMed
van Daele, P, Seibel, M, Burger, H, Hofman, A, Grobbee, D, van Leeuwen, J, Birkenhaeger, JC & Pols, HAP (1996) Case-control analysis of bone resorption markers, disability and hip fracture risk: the Rotterdam study. British Medical Journal 312, 482–483.CrossRefGoogle ScholarPubMed
Vandevyver, C, Vanhoof, J, Declerck, K, Stinissen, P, Vandervorst, C, Michiels, L, Cassiman, J, Boonen, S, Raus, J & Geusens, P (1999) Lack of association between oestrogen receptor genotypes and bone mineral density, fracture history, or muscle strength in elderly women. Journal of Bone and Mineral Research 14, 1576–1582.CrossRefGoogle ScholarPubMed
van Erp-Baart, AMJ, Brants, HAM, Kiely, M, Mulligan, A, Turrini, A, Sermoneta, C, Kilkkinen, A & Valsta, LM (2003) Isoflavone intake in four different European countries: the Vegetal Estrogens in Nutrition and the Skeleton. approach. British Journal of Nutrition 89, Suppl. 1, S25–S30.CrossRefGoogle Scholar
Van Loan, M, Johnson, H & Barbiery, T (1998) Effects of weight loss on bone mineral content and bone mineral density in obese women. American Journal of Clinical Nutrition 67, 734–738.CrossRefGoogle Scholar
Vitolins, M, Anthony, M & Burke, G (2001) Soy protein isoflavones, lipids and arterial disease. Current Opinion in Lipidology 12, 433–437.CrossRefGoogle ScholarPubMed
Wangen, KE, Duncan, AM, Xu, X & Kurzer, MS (2001) Soy isoflavones improve plasma lipids in normocholesterolemic and mildly hypercholesterolemic postmenopausal women. American Journal of Clinical Nutrition 73, 225–231.CrossRefGoogle ScholarPubMed
Willing, M, Sowers, M, Aron, D, Clark, M, Burns, T, Bunten, C, Crutchfield, M, Dagostino, D & Jannausch, M (1998) Bone mineral density and its change in white women: oestrogen and vitamin D receptor genotypes and their interaction. Journal of Bone and Mineral Research 13, 695–705.CrossRefGoogle ScholarPubMed
Wolff, I, van Croonenborg, JJ, Kemper, HC, Kostense, PJ & Twisk, JW (1999) The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporosis International 9, 1–12.CrossRefGoogle Scholar
World Health Organization (1994) Assessment of Fracture Risk and Its Application to Screening for Postmenopausal Osteoporosis. Geneva: World Health Organization.Google Scholar