Skip to main content
Top
Published in: Endocrine 2/2019

01-02-2019 | Meta-Analysis

Association between age at menopause and fracture risk: a systematic review and meta-analysis

Authors: Panagiotis Anagnostis, Pavlos Siolos, Nifon K. Gkekas, Nikoletta Kosmidou, Aikaterini-Maria Artzouchaltzi, Konstantinos Christou, Stavroula A. Paschou, Michael Potoupnis, Eustathios Kenanidis, Eleftherios Tsiridis, Irene Lambrinoudaki, John C. Stevenson, Dimitrios G. Goulis

Published in: Endocrine | Issue 2/2019

Login to get access

Abstract

Purpose

Early menopause (EM, age at menopause < 45 years) and premature ovarian insufficiency (POI, age at menopause < 40 years) are associated with an increased risk of osteoporosis. However, their association with increased fracture risk has not been established, with studies yielding conflicting results. The primary aim of this systematic review and meta-analysis was to synthesize studies evaluating the association between age at menopause and fracture risk. The secondary aim was to evaluate this effect concerning the site of fractures.

Methods

A comprehensive search was conducted in PubMed, CENTRAL and Scopus, up to 31 January 2018. Data were expressed as odds ratio (OR) with 95% confidence intervals (CI). The I2 index was employed for quantifying heterogeneity.

Results

Eighteen studies were included in the qualitative and quantitative analysis (462,393 postmenopausal women, 12,130 fractures). Compared with women with age at menopause > 45 years, women with EM demonstrated higher fracture risk (OR 1.36, 95% CI 1.11–1.66, p < 0.002, I² 81.5%). Women with POI did not display any difference in fracture risk compared either with women with age at menopause > 40 (OR 1.23, 95% CI 0.72–2.09, p = 0.436, I² 62.5%) or >45 years (OR 0.54, 95% CI 0.22–1.29, p = 0.17, I2 0%). No difference was evident when a separate analysis was performed for vertebral, non-vertebral and hip fractures.

Conclusions

This is the first meta-analysis showing that EM is associated with increased fracture risk compared with normal age at menopause, without any distinct effect on the site of the fracture.
Appendix
Available only for authorised users
Literature
1.
go back to reference D.M. Black, C.J. Rosen, Clinical practice. Postmenopausal osteoporosis. N. Engl. J. Med. 374(3), 254–262 (2016)CrossRef D.M. Black, C.J. Rosen, Clinical practice. Postmenopausal osteoporosis. N. Engl. J. Med. 374(3), 254–262 (2016)CrossRef
2.
go back to reference C. Pike, H.G. Birnbaum, M. Schiller, H. Sharma, R. Burge, E.T. Edgell, Direct and indirect costs of non-vertebral fracture patients with osteoporosis in the US. Pharmacoeconomics 28(5), 395–409 (2010)CrossRef C. Pike, H.G. Birnbaum, M. Schiller, H. Sharma, R. Burge, E.T. Edgell, Direct and indirect costs of non-vertebral fracture patients with osteoporosis in the US. Pharmacoeconomics 28(5), 395–409 (2010)CrossRef
3.
go back to reference P. Vestergaard, L. Rejnmark, L. Mosekilde, Increased mortality in patients with a hip fracture-effect of pre-morbid conditions and post-fracture complications. Osteoporos. Int. 18(12), 1583–1593 (2007)CrossRef P. Vestergaard, L. Rejnmark, L. Mosekilde, Increased mortality in patients with a hip fracture-effect of pre-morbid conditions and post-fracture complications. Osteoporos. Int. 18(12), 1583–1593 (2007)CrossRef
4.
go back to reference S.R. Davis, I. Lambrinoudaki, M. Lumsden, G.D. Mishra, L. Pal, M. Rees, N. Santoro, T. Simoncini, Menopause. Nat. Rev. Dis. Prim. 1, 15004 (2015)CrossRef S.R. Davis, I. Lambrinoudaki, M. Lumsden, G.D. Mishra, L. Pal, M. Rees, N. Santoro, T. Simoncini, Menopause. Nat. Rev. Dis. Prim. 1, 15004 (2015)CrossRef
5.
go back to reference J.S. Finkelstein, S.E. Brockwell, V. Mehta, G.A. Greendale, M.R. Sowers, B. Ettinger, J.C. Lo, J.M. Johnston, J.A. Cauley, M.E. Danielson, R.M. Neer, Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J. Clin. Endocrinol. Metab. 93(3), 861–868 (2008). https://doi.org/10.1210/jc.2007-1876. CrossRefPubMed J.S. Finkelstein, S.E. Brockwell, V. Mehta, G.A. Greendale, M.R. Sowers, B. Ettinger, J.C. Lo, J.M. Johnston, J.A. Cauley, M.E. Danielson, R.M. Neer, Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J. Clin. Endocrinol. Metab. 93(3), 861–868 (2008). https://​doi.​org/​10.​1210/​jc.​2007-1876.​ CrossRefPubMed
6.
go back to reference S.S. Faubion, C.L. Kuhle, L.T. Shuster, W.A. Rocca, Long-term health consequences of premature or early menopause and considerations for management. Climacteric 18(4), 483–491 (2015)CrossRef S.S. Faubion, C.L. Kuhle, L.T. Shuster, W.A. Rocca, Long-term health consequences of premature or early menopause and considerations for management. Climacteric 18(4), 483–491 (2015)CrossRef
7.
go back to reference L.T. Shuster, D.J. Rhodes, B.S. Gostout, B.R. Grossardt, W.A. Rocca, Premature menopause or early menopause: long-term health consequences. Maturitas 65(2), 161–166 (2010)CrossRef L.T. Shuster, D.J. Rhodes, B.S. Gostout, B.R. Grossardt, W.A. Rocca, Premature menopause or early menopause: long-term health consequences. Maturitas 65(2), 161–166 (2010)CrossRef
8.
go back to reference R.G. Cumming, R.J. Klineberg, Breastfeeding and other reproductive factors and the risk of hip fractures in elderly women. Int. J. Epidemiol. 22(4), 684–691 (1993)CrossRef R.G. Cumming, R.J. Klineberg, Breastfeeding and other reproductive factors and the risk of hip fractures in elderly women. Int. J. Epidemiol. 22(4), 684–691 (1993)CrossRef
9.
go back to reference F. Parazzini, A. Tavani, E. Ricci, C. La Vecchia, Menstrual and reproductive factors and hip fractures in post menopausal women. Maturitas 24(3), 191–196 (1996)CrossRef F. Parazzini, A. Tavani, E. Ricci, C. La Vecchia, Menstrual and reproductive factors and hip fractures in post menopausal women. Maturitas 24(3), 191–196 (1996)CrossRef
10.
go back to reference A. Papaioannou, L. Joseph, G. Ioannidis, C. Berger, T. Anastassiades, J.P. Brown, D.A. Hanley, W. Hopman, R.G. Josse, S. Kirkland, T.M. Murray, W.P. Olszynski, L. Pickard, J.C. Prior, K. Siminoski, J.D. Adachi, Risk factors associated with incident clinical vertebral and nonvertebral fractures in postmenopausal women: the Canadian Multicentre Osteoporosis Study (CaMos). Osteoporos. Int. 16(5), 568–578 (2005)CrossRef A. Papaioannou, L. Joseph, G. Ioannidis, C. Berger, T. Anastassiades, J.P. Brown, D.A. Hanley, W. Hopman, R.G. Josse, S. Kirkland, T.M. Murray, W.P. Olszynski, L. Pickard, J.C. Prior, K. Siminoski, J.D. Adachi, Risk factors associated with incident clinical vertebral and nonvertebral fractures in postmenopausal women: the Canadian Multicentre Osteoporosis Study (CaMos). Osteoporos. Int. 16(5), 568–578 (2005)CrossRef
11.
go back to reference M. Tuppurainen, H. Kroger, R. Honkanen, E. Puntila, J. Huopio, S. Saarikoski, E. Alhava, Risks of perimenopausal fractures—a prospective population-based study. Acta Obstet. Gynecol. Scand. 74(8), 624–628 (1995)CrossRef M. Tuppurainen, H. Kroger, R. Honkanen, E. Puntila, J. Huopio, S. Saarikoski, E. Alhava, Risks of perimenopausal fractures—a prospective population-based study. Acta Obstet. Gynecol. Scand. 74(8), 624–628 (1995)CrossRef
12.
go back to reference A. Paganini-Hill, K.A. Atchison, J.A. Gornbein, A. Nattiv, S.K. Service, S.C. White, Menstrual and reproductive factors and fracture risk: the Leisure World Cohort Study. J. Womens. Health. 14(9), 808–819 (2005)CrossRef A. Paganini-Hill, K.A. Atchison, J.A. Gornbein, A. Nattiv, S.K. Service, S.C. White, Menstrual and reproductive factors and fracture risk: the Leisure World Cohort Study. J. Womens. Health. 14(9), 808–819 (2005)CrossRef
13.
go back to reference D.F. Stroup, J.A. Berlin, S.C. Morton, I. Olkin, G.D. Williamson, D. Rennie, D. Moher, B.J. Becker, T.A. Sipe, S.B. Thacker, Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15), 2008–2012 (2000)CrossRef D.F. Stroup, J.A. Berlin, S.C. Morton, I. Olkin, G.D. Williamson, D. Rennie, D. Moher, B.J. Becker, T.A. Sipe, S.B. Thacker, Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15), 2008–2012 (2000)CrossRef
15.
go back to reference M. Varenna, L. Binelli, F. Zucchi, P. Beltrametti, M. Gallazzi, L. Sinigaglia, Is the metatarsal fracture in postmenopausal women an osteoporotic fracture? A cross-sectional study on 113 cases. Osteoporos. Int. 7(6), 558–563 (1997)CrossRef M. Varenna, L. Binelli, F. Zucchi, P. Beltrametti, M. Gallazzi, L. Sinigaglia, Is the metatarsal fracture in postmenopausal women an osteoporotic fracture? A cross-sectional study on 113 cases. Osteoporos. Int. 7(6), 558–563 (1997)CrossRef
16.
go back to reference D. Huo, D.S. Lauderdale, L. Li, Influence of reproductive factors on hip fracture risk in Chinese women. Osteoporos. Int. 14(8), 694–700 (2003)CrossRef D. Huo, D.S. Lauderdale, L. Li, Influence of reproductive factors on hip fracture risk in Chinese women. Osteoporos. Int. 14(8), 694–700 (2003)CrossRef
17.
go back to reference D.J. van Der Voort, P.H. van Der Weijer, R. Barentsen, Early menopause: increased fracture risk at older age. Osteoporos. Int. 14(6), 525–530 (2003)CrossRef D.J. van Der Voort, P.H. van Der Weijer, R. Barentsen, Early menopause: increased fracture risk at older age. Osteoporos. Int. 14(6), 525–530 (2003)CrossRef
18.
go back to reference M. van der Klift, C.E. de Laet, E.V. McCloskey, O. Johnell, J.A. Kanis, A. Hofman, H.A. Pols, Risk factors for incident vertebral fractures in men and women: the Rotterdam Study. J. Bone Miner. Res. 19(7), 1172–1180 (2004)CrossRef M. van der Klift, C.E. de Laet, E.V. McCloskey, O. Johnell, J.A. Kanis, A. Hofman, H.A. Pols, Risk factors for incident vertebral fractures in men and women: the Rotterdam Study. J. Bone Miner. Res. 19(7), 1172–1180 (2004)CrossRef
19.
go back to reference M.R. Jenkins, A.V. Denison, Smoking status as a predictor of hip fracture risk in postmenopausal women of northwest Texas. Prev. Chronic Dis. 5(1), A09 (2008)PubMed M.R. Jenkins, A.V. Denison, Smoking status as a predictor of hip fracture risk in postmenopausal women of northwest Texas. Prev. Chronic Dis. 5(1), A09 (2008)PubMed
20.
go back to reference E. Banks, G.K. Reeves, V. Beral, A. Balkwill, B. Liu, A. Roddam, Million Women Study, C.: Hip fracture incidence in relation to age, menopausal status, and age at menopause: prospective analysis. PLoS. Med. 6(11), e1000181 (2009)CrossRef E. Banks, G.K. Reeves, V. Beral, A. Balkwill, B. Liu, A. Roddam, Million Women Study, C.: Hip fracture incidence in relation to age, menopausal status, and age at menopause: prospective analysis. PLoS. Med. 6(11), e1000181 (2009)CrossRef
21.
go back to reference E. Lespessailles, F.E. Cotte, C. Roux, P. Fardellone, F. Mercier, A.F. Gaudin, Prevalence and features of osteoporosis in the French general population: the Instant study. Jt. Bone Spine 76(4), 394–400 (2009)CrossRef E. Lespessailles, F.E. Cotte, C. Roux, P. Fardellone, F. Mercier, A.F. Gaudin, Prevalence and features of osteoporosis in the French general population: the Instant study. Jt. Bone Spine 76(4), 394–400 (2009)CrossRef
22.
go back to reference F.A. Tremollieres, J.M. Pouilles, N. Drewniak, J. Laparra, C.A. Ribot, P. Dargent-Molina, Fracture risk prediction using BMD and clinical risk factors in early postmenopausal women: sensitivity of the WHO FRAX tool. J. Bone Miner. Res. 25(5), 1002–1009 (2010)CrossRef F.A. Tremollieres, J.M. Pouilles, N. Drewniak, J. Laparra, C.A. Ribot, P. Dargent-Molina, Fracture risk prediction using BMD and clinical risk factors in early postmenopausal women: sensitivity of the WHO FRAX tool. J. Bone Miner. Res. 25(5), 1002–1009 (2010)CrossRef
23.
go back to reference C.S. Shin, M.J. Kim, S.M. Shim, J.T. Kim, S.H. Yu, B.K. Koo, H.Y. Cho, H.J. Choi, S.W. Cho, S.W. Kim, S.Y. Kim, S.O. Yang, N.H. Cho, The prevalence and risk factors of vertebral fractures in Korea. J. Bone Miner. Metab. 30(2), 183–192 (2012)CrossRef C.S. Shin, M.J. Kim, S.M. Shim, J.T. Kim, S.H. Yu, B.K. Koo, H.Y. Cho, H.J. Choi, S.W. Cho, S.W. Kim, S.Y. Kim, S.O. Yang, N.H. Cho, The prevalence and risk factors of vertebral fractures in Korea. J. Bone Miner. Metab. 30(2), 183–192 (2012)CrossRef
24.
go back to reference A.K. Pfister, C.A. Welch, M.K. Emmett, N.W. Sheets, Risk factors predicting fractures in early postmenopausal women. W. V. Med. J. 109(3), 14–15 (2013). 8-12 A.K. Pfister, C.A. Welch, M.K. Emmett, N.W. Sheets, Risk factors predicting fractures in early postmenopausal women. W. V. Med. J. 109(3), 14–15 (2013). 8-12
25.
go back to reference S.D. Sullivan, A. Lehman, F. Thomas, K.C. Johnson, R. Jackson, J. Wactawski-Wende, M. Ko, Z. Chen, J.D. Curb, B.V. Howard, Effects of self-reported age at nonsurgical menopause on time to first fracture and bone mineral density in the Women’s Health Initiative Observational Study. Menopause 22(10), 1035–1044 (2015)CrossRef S.D. Sullivan, A. Lehman, F. Thomas, K.C. Johnson, R. Jackson, J. Wactawski-Wende, M. Ko, Z. Chen, J.D. Curb, B.V. Howard, Effects of self-reported age at nonsurgical menopause on time to first fracture and bone mineral density in the Women’s Health Initiative Observational Study. Menopause 22(10), 1035–1044 (2015)CrossRef
26.
go back to reference I. Lambrinoudaki, M. Flokatoula, E. Armeni, P. Pliatsika, A. Augoulea, A. Antoniou, A. Alexandrou, M. Creatsa, C. Panoulis, S. Dendrinos, X. Papacharalambous, Vertebral fracture prevalence among Greek healthy middle-aged postmenopausal women: association with demographics, anthropometric parameters, and bone mineral density. Spine J. 15(1), 86–94 (2015)CrossRef I. Lambrinoudaki, M. Flokatoula, E. Armeni, P. Pliatsika, A. Augoulea, A. Antoniou, A. Alexandrou, M. Creatsa, C. Panoulis, S. Dendrinos, X. Papacharalambous, Vertebral fracture prevalence among Greek healthy middle-aged postmenopausal women: association with demographics, anthropometric parameters, and bone mineral density. Spine J. 15(1), 86–94 (2015)CrossRef
27.
go back to reference S.R. Cummings, M.C. Nevitt, W.S. Browner, K. Stone, K.M. Fox, K.E. Ensrud, J. Cauley, D. Black, T.M. Vogt, Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. N. Engl. J. Med. 332(12), 767–773 (1995)CrossRef S.R. Cummings, M.C. Nevitt, W.S. Browner, K. Stone, K.M. Fox, K.E. Ensrud, J. Cauley, D. Black, T.M. Vogt, Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. N. Engl. J. Med. 332(12), 767–773 (1995)CrossRef
28.
go back to reference B.L. Riggs, S. Khosla, L.J. Melton 3rd, : Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 23(3), 279–302 (2002)CrossRef B.L. Riggs, S. Khosla, L.J. Melton 3rd, : Sex steroids and the construction and conservation of the adult skeleton. Endocr. Rev. 23(3), 279–302 (2002)CrossRef
29.
go back to reference J.E. Rossouw, G.L. Anderson, R.L. Prentice, A.Z. LaCroix, C. Kooperberg, M.L. Stefanick, R.D. Jackson, S.A. Beresford, B.V. Howard, K.C. Johnson, J.M. Kotchen, J. Ockene, Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women’s health initiative randomized controlled trial. JAMA 288(3), 321–333 (2002)CrossRef J.E. Rossouw, G.L. Anderson, R.L. Prentice, A.Z. LaCroix, C. Kooperberg, M.L. Stefanick, R.D. Jackson, S.A. Beresford, B.V. Howard, K.C. Johnson, J.M. Kotchen, J. Ockene, Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women’s health initiative randomized controlled trial. JAMA 288(3), 321–333 (2002)CrossRef
30.
go back to reference G.L. Anderson, M. Limacher, A.R. Assaf, T. Bassford, S.A. Beresford, H. Black, D. Bonds, R. Brunner, R. Brzyski, B. Caan, R. Chlebowski, D. Curb, M. Gass, J. Hays, G. Heiss, S. Hendrix, B.V. Howard, J. Hsia, A. Hubbell, R. Jackson, K.C. Johnson, H. Judd, J.M. Kotchen, L. Kuller, A.Z. LaCroix, D. Lane, R.D. Langer, N. Lasser, C.E. Lewis, J. Manson, K. Margolis, J. Ockene, M.J. O’Sullivan, L. Phillips, R.L. Prentice, C. Ritenbaugh, J. Robbins, J.E. Rossouw, G. Sarto, M.L. Stefanick, L. Van Horn, J. Wactawski-Wende, R. Wallace, S. Wassertheil-Smoller, Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women’s Health Initiative randomized controlled trial. JAMA 291(14), 1701–1712 (2004)CrossRef G.L. Anderson, M. Limacher, A.R. Assaf, T. Bassford, S.A. Beresford, H. Black, D. Bonds, R. Brunner, R. Brzyski, B. Caan, R. Chlebowski, D. Curb, M. Gass, J. Hays, G. Heiss, S. Hendrix, B.V. Howard, J. Hsia, A. Hubbell, R. Jackson, K.C. Johnson, H. Judd, J.M. Kotchen, L. Kuller, A.Z. LaCroix, D. Lane, R.D. Langer, N. Lasser, C.E. Lewis, J. Manson, K. Margolis, J. Ockene, M.J. O’Sullivan, L. Phillips, R.L. Prentice, C. Ritenbaugh, J. Robbins, J.E. Rossouw, G. Sarto, M.L. Stefanick, L. Van Horn, J. Wactawski-Wende, R. Wallace, S. Wassertheil-Smoller, Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women’s Health Initiative randomized controlled trial. JAMA 291(14), 1701–1712 (2004)CrossRef
31.
go back to reference H. Mizunuma, Y. Taketani, H. Ohta, H. Honjo, I. Gorai, A. Itabashi, M. Shiraki, Dose effects of oral estradiol on bone mineral density in Japanese women with osteoporosis. Climacteric 13(1), 72–83 (2010)CrossRef H. Mizunuma, Y. Taketani, H. Ohta, H. Honjo, I. Gorai, A. Itabashi, M. Shiraki, Dose effects of oral estradiol on bone mineral density in Japanese women with osteoporosis. Climacteric 13(1), 72–83 (2010)CrossRef
32.
go back to reference F.A. Tremollieres, J.M. Pouilles, C. Ribot, Withdrawal of hormone replacement therapy is associated with significant vertebral bone loss in postmenopausal women. Osteoporos. Int. 12(5), 385–390 (2001)CrossRef F.A. Tremollieres, J.M. Pouilles, C. Ribot, Withdrawal of hormone replacement therapy is associated with significant vertebral bone loss in postmenopausal women. Osteoporos. Int. 12(5), 385–390 (2001)CrossRef
33.
go back to reference G. Papadakis, D. Hans, E. Gonzalez-Rodriguez, P. Vollenweider, G. Waeber, P.M. Marques-Vidal, O. Lamy, The benefit of menopausal hormone therapy on bone density and microarchitecture persists after its withdrawal. J. Clin. Endocrinol. Metab. 101(12), 5004–5011 (2016)CrossRef G. Papadakis, D. Hans, E. Gonzalez-Rodriguez, P. Vollenweider, G. Waeber, P.M. Marques-Vidal, O. Lamy, The benefit of menopausal hormone therapy on bone density and microarchitecture persists after its withdrawal. J. Clin. Endocrinol. Metab. 101(12), 5004–5011 (2016)CrossRef
34.
go back to reference N.B. Watts, J.A. Cauley, R.D. Jackson, A.Z. LaCroix, C.E. Lewis, J.E. Manson, J.M. Neuner, L.S. Phillips, M.L. Stefanick, J. Wactawski-Wende, C. Crandall, No increase in fractures after stopping hormone therapy: results from the women’s health initiative. J. Clin. Endocrinol. Metab. 102(1), 302–308 (2017)PubMed N.B. Watts, J.A. Cauley, R.D. Jackson, A.Z. LaCroix, C.E. Lewis, J.E. Manson, J.M. Neuner, L.S. Phillips, M.L. Stefanick, J. Wactawski-Wende, C. Crandall, No increase in fractures after stopping hormone therapy: results from the women’s health initiative. J. Clin. Endocrinol. Metab. 102(1), 302–308 (2017)PubMed
35.
go back to reference E.B. Gold, S.L. Crawford, N.E. Avis, C.J. Crandall, K.A. Matthews, L.E. Waetjen, J.S. Lee, R. Thurston, M. Vuga, S.D. Harlow, Factors related to age at natural menopause: longitudinal analyses from SWAN. Am. J. Epidemiol. 178(1), 70–83 (2013)CrossRef E.B. Gold, S.L. Crawford, N.E. Avis, C.J. Crandall, K.A. Matthews, L.E. Waetjen, J.S. Lee, R. Thurston, M. Vuga, S.D. Harlow, Factors related to age at natural menopause: longitudinal analyses from SWAN. Am. J. Epidemiol. 178(1), 70–83 (2013)CrossRef
36.
go back to reference U. Stepaniak, K. Szafraniec, R. Kubinova, S. Malyutina, A. Peasey, H. Pikhart, A. Pajak, M. Bobak, Age at natural menopause in three central and eastern European urban populations: the HAPIEE study. Maturitas 75(1), 87–93 (2013)CrossRef U. Stepaniak, K. Szafraniec, R. Kubinova, S. Malyutina, A. Peasey, H. Pikhart, A. Pajak, M. Bobak, Age at natural menopause in three central and eastern European urban populations: the HAPIEE study. Maturitas 75(1), 87–93 (2013)CrossRef
37.
go back to reference V. Mpalaris, P. Anagnostis, D.G. Goulis, I. Iakovou, Complex association between body weight and fracture risk in postmenopausal women. Obes. Rev. 16(3), 225–233 (2015)CrossRef V. Mpalaris, P. Anagnostis, D.G. Goulis, I. Iakovou, Complex association between body weight and fracture risk in postmenopausal women. Obes. Rev. 16(3), 225–233 (2015)CrossRef
38.
go back to reference M.C. Navarro, M. Sosa, P. Saavedra, P. Lainez, M. Marrero, M. Torres, C.D. Medina, Poverty is a risk factor for osteoporotic fractures. Osteoporos. Int. 20(3), 393–398 (2009)CrossRef M.C. Navarro, M. Sosa, P. Saavedra, P. Lainez, M. Marrero, M. Torres, C.D. Medina, Poverty is a risk factor for osteoporotic fractures. Osteoporos. Int. 20(3), 393–398 (2009)CrossRef
39.
go back to reference J.S. Laven, Genetics of early and normal menopause. Semin. Reprod. Med. 33(6), 377–383 (2015)CrossRef J.S. Laven, Genetics of early and normal menopause. Semin. Reprod. Med. 33(6), 377–383 (2015)CrossRef
40.
go back to reference L. Stolk, J.R. Perry, D.I. Chasman, C. He, M. Mangino, P. Sulem, M. Barbalic, L. Broer, E.M. Byrne, F. Ernst, T. Esko, N. Franceschini, D.F. Gudbjartsson, J.J. Hottenga, P. Kraft, P.F. McArdle, E. Porcu, S.Y. Shin, A.V. Smith, S. van Wingerden, G. Zhai, W.V. Zhuang, E. Albrecht, B.Z. Alizadeh, T. Aspelund, S. Bandinelli, L.B. Lauc, J.S. Beckmann, M. Boban, E. Boerwinkle, F.J. Broekmans, A. Burri, H. Campbell, S.J. Chanock, C. Chen, M.C. Cornelis, T. Corre, A.D. Coviello, P. d’Adamo, G. Davies, U. de Faire, E.J. de Geus, I.J. Deary, G.V. Dedoussis, P. Deloukas, S. Ebrahim, G. Eiriksdottir, V. Emilsson, J.G. Eriksson, B.C. Fauser, L. Ferreli, L. Ferrucci, K. Fischer, A.R. Folsom, M.E. Garcia, P. Gasparini, C. Gieger, N. Glazer, D.E. Grobbee, P. Hall, T. Haller, S.E. Hankinson, M. Hass, C. Hayward, A.C. Heath, A. Hofman, E. Ingelsson, A.C. Janssens, A.D. Johnson, D. Karasik, S.L. Kardia, J. Keyzer, D.P. Kiel, I. Kolcic, Z. Kutalik, J. Lahti, S. Lai, T. Laisk, J.S. Laven, D.A. Lawlor, J. Liu, L.M. Lopez, Y.V. Louwers, P.K. Magnusson, M. Marongiu, N.G. Martin, I.M. Klaric, C. Masciullo, B. McKnight, S.E. Medland, D. Melzer, V. Mooser, P. Navarro, A.B. Newman, D.R. Nyholt, N.C. Onland-Moret, A. Palotie, G. Pare, A.N. Parker, N.L. Pedersen, P.H. Peeters, G. Pistis, A.S. Plump, O. Polasek, V.J. Pop, B.M. Psaty, K. Raikkonen, E. Rehnberg, J.I. Rotter, I. Rudan, C. Sala, A. Salumets, A. Scuteri, A. Singleton, J.A. Smith, H. Snieder, N. Soranzo, S.N. Stacey, J.M. Starr, M.G. Stathopoulou, K. Stirrups, R.P. Stolk, U. Styrkarsdottir, Y.V. Sun, A. Tenesa, B. Thorand, D. Toniolo, L. Tryggvadottir, K. Tsui, S. Ulivi, R.M. van Dam, Y.T. van der Schouw, C.H. van Gils, P. van Nierop, J.M. Vink, P.M. Visscher, M. Voorhuis, G. Waeber, H. Wallaschofski, H.E. Wichmann, E. Widen, C.J. Wijnands-van Gent, G. Willemsen, J.F. Wilson, B.H. Wolffenbuttel, A.F. Wright, L.M. Yerges-Armstrong, T. Zemunik, L. Zgaga, M.C. Zillikens, M. Zygmunt, A.M. Arnold, D.I. Boomsma, J.E. Buring, L. Crisponi, E.W. Demerath, V. Gudnason, T.B. Harris, F.B. Hu, D.J. Hunter, L.J. Launer, A. Metspalu, G.W. Montgomery, B.A. Oostra, P.M. Ridker, S. Sanna, D. Schlessinger, T.D. Spector, K. Stefansson, E.A. Streeten, U. Thorsteinsdottir, M. Uda, A.G. Uitterlinden, C.M. van Duijn, H. Volzke, A. Murray, J.M. Murabito, J.A. Visser, K.L. Lunetta, Meta-analyses identify 13 loci associated with age at menopause and highlight DNA repair and immune pathways. Nat. Genet. 44(3), 260–268 (2012)CrossRef L. Stolk, J.R. Perry, D.I. Chasman, C. He, M. Mangino, P. Sulem, M. Barbalic, L. Broer, E.M. Byrne, F. Ernst, T. Esko, N. Franceschini, D.F. Gudbjartsson, J.J. Hottenga, P. Kraft, P.F. McArdle, E. Porcu, S.Y. Shin, A.V. Smith, S. van Wingerden, G. Zhai, W.V. Zhuang, E. Albrecht, B.Z. Alizadeh, T. Aspelund, S. Bandinelli, L.B. Lauc, J.S. Beckmann, M. Boban, E. Boerwinkle, F.J. Broekmans, A. Burri, H. Campbell, S.J. Chanock, C. Chen, M.C. Cornelis, T. Corre, A.D. Coviello, P. d’Adamo, G. Davies, U. de Faire, E.J. de Geus, I.J. Deary, G.V. Dedoussis, P. Deloukas, S. Ebrahim, G. Eiriksdottir, V. Emilsson, J.G. Eriksson, B.C. Fauser, L. Ferreli, L. Ferrucci, K. Fischer, A.R. Folsom, M.E. Garcia, P. Gasparini, C. Gieger, N. Glazer, D.E. Grobbee, P. Hall, T. Haller, S.E. Hankinson, M. Hass, C. Hayward, A.C. Heath, A. Hofman, E. Ingelsson, A.C. Janssens, A.D. Johnson, D. Karasik, S.L. Kardia, J. Keyzer, D.P. Kiel, I. Kolcic, Z. Kutalik, J. Lahti, S. Lai, T. Laisk, J.S. Laven, D.A. Lawlor, J. Liu, L.M. Lopez, Y.V. Louwers, P.K. Magnusson, M. Marongiu, N.G. Martin, I.M. Klaric, C. Masciullo, B. McKnight, S.E. Medland, D. Melzer, V. Mooser, P. Navarro, A.B. Newman, D.R. Nyholt, N.C. Onland-Moret, A. Palotie, G. Pare, A.N. Parker, N.L. Pedersen, P.H. Peeters, G. Pistis, A.S. Plump, O. Polasek, V.J. Pop, B.M. Psaty, K. Raikkonen, E. Rehnberg, J.I. Rotter, I. Rudan, C. Sala, A. Salumets, A. Scuteri, A. Singleton, J.A. Smith, H. Snieder, N. Soranzo, S.N. Stacey, J.M. Starr, M.G. Stathopoulou, K. Stirrups, R.P. Stolk, U. Styrkarsdottir, Y.V. Sun, A. Tenesa, B. Thorand, D. Toniolo, L. Tryggvadottir, K. Tsui, S. Ulivi, R.M. van Dam, Y.T. van der Schouw, C.H. van Gils, P. van Nierop, J.M. Vink, P.M. Visscher, M. Voorhuis, G. Waeber, H. Wallaschofski, H.E. Wichmann, E. Widen, C.J. Wijnands-van Gent, G. Willemsen, J.F. Wilson, B.H. Wolffenbuttel, A.F. Wright, L.M. Yerges-Armstrong, T. Zemunik, L. Zgaga, M.C. Zillikens, M. Zygmunt, A.M. Arnold, D.I. Boomsma, J.E. Buring, L. Crisponi, E.W. Demerath, V. Gudnason, T.B. Harris, F.B. Hu, D.J. Hunter, L.J. Launer, A. Metspalu, G.W. Montgomery, B.A. Oostra, P.M. Ridker, S. Sanna, D. Schlessinger, T.D. Spector, K. Stefansson, E.A. Streeten, U. Thorsteinsdottir, M. Uda, A.G. Uitterlinden, C.M. van Duijn, H. Volzke, A. Murray, J.M. Murabito, J.A. Visser, K.L. Lunetta, Meta-analyses identify 13 loci associated with age at menopause and highlight DNA repair and immune pathways. Nat. Genet. 44(3), 260–268 (2012)CrossRef
41.
go back to reference M.G. Braem, M. Voorhuis, Y.T. van der Schouw, P.H. Peeters, L.J. Schouten, M.J. Eijkemans, F.J. Broekmans, N.C. Onland-Moret, Interactions between genetic variants in AMH and AMHR2 may modify age at natural menopause. PLoS. One. 8(3), e59819 (2013)CrossRef M.G. Braem, M. Voorhuis, Y.T. van der Schouw, P.H. Peeters, L.J. Schouten, M.J. Eijkemans, F.J. Broekmans, N.C. Onland-Moret, Interactions between genetic variants in AMH and AMHR2 may modify age at natural menopause. PLoS. One. 8(3), e59819 (2013)CrossRef
42.
go back to reference A. La Marca, G. Sighinolfi, C. Argento, V. Grisendi, L. Casarini, A. Volpe, M. Simoni, Polymorphisms in gonadotropin and gonadotropin receptor genes as markers of ovarian reserve and response in in vitro fertilization. Fertil. Steril. 99(4), 970–978.e971 (2013)CrossRef A. La Marca, G. Sighinolfi, C. Argento, V. Grisendi, L. Casarini, A. Volpe, M. Simoni, Polymorphisms in gonadotropin and gonadotropin receptor genes as markers of ovarian reserve and response in in vitro fertilization. Fertil. Steril. 99(4), 970–978.e971 (2013)CrossRef
43.
go back to reference U. Styrkarsdottir, B.V. Halldorsson, S. Gretarsdottir, D.F. Gudbjartsson, G.B. Walters, T. Ingvarsson, T. Jonsdottir, J. Saemundsdottir, J.R. Center, T.V. Nguyen, Y. Bagger, J.R. Gulcher, J.A. Eisman, C. Christiansen, G. Sigurdsson, A. Kong, U. Thorsteinsdottir, K. Stefansson, Multiple genetic loci for bone mineral density and fractures. N. Engl. J. Med. 358(22), 2355–2365 (2008)CrossRef U. Styrkarsdottir, B.V. Halldorsson, S. Gretarsdottir, D.F. Gudbjartsson, G.B. Walters, T. Ingvarsson, T. Jonsdottir, J. Saemundsdottir, J.R. Center, T.V. Nguyen, Y. Bagger, J.R. Gulcher, J.A. Eisman, C. Christiansen, G. Sigurdsson, A. Kong, U. Thorsteinsdottir, K. Stefansson, Multiple genetic loci for bone mineral density and fractures. N. Engl. J. Med. 358(22), 2355–2365 (2008)CrossRef
44.
go back to reference G.R. Ji, M. Yao, C.Y. Sun, Z.H. Li, Z. Han, BsmI, TaqI, ApaI, and FokI polymorphisms in the vitamin D receptor (VDR) gene and risk of fracture in Caucasians: a meta-analysis. Bone 47(3), 681–686 (2010)CrossRef G.R. Ji, M. Yao, C.Y. Sun, Z.H. Li, Z. Han, BsmI, TaqI, ApaI, and FokI polymorphisms in the vitamin D receptor (VDR) gene and risk of fracture in Caucasians: a meta-analysis. Bone 47(3), 681–686 (2010)CrossRef
45.
go back to reference A.E. Weel, A.G. Uitterlinden, I.C. Westendorp, H. Burger, S.C. Schuit, A. Hofman, T.J. Helmerhorst, J.P. van Leeuwen, H.A. Pols, Estrogen receptor polymorphism predicts the onset of natural and surgical menopause. J. Clin. Endocrinol. Metab. 84(9), 3146–3150 (1999)PubMed A.E. Weel, A.G. Uitterlinden, I.C. Westendorp, H. Burger, S.C. Schuit, A. Hofman, T.J. Helmerhorst, J.P. van Leeuwen, H.A. Pols, Estrogen receptor polymorphism predicts the onset of natural and surgical menopause. J. Clin. Endocrinol. Metab. 84(9), 3146–3150 (1999)PubMed
46.
go back to reference V. Dvornyk, J.R. Long, P.Y. Liu, H. Shen, R.R. Recker, H.W. Deng, Polymorphisms of the vitamin D receptor gene predict the onset of surgical menopause in Caucasian females. Gynecol. Endocrinol. 22(10), 552–556 (2006)CrossRef V. Dvornyk, J.R. Long, P.Y. Liu, H. Shen, R.R. Recker, H.W. Deng, Polymorphisms of the vitamin D receptor gene predict the onset of surgical menopause in Caucasian females. Gynecol. Endocrinol. 22(10), 552–556 (2006)CrossRef
47.
go back to reference D.M. Black, J.A. Cauley, R. Wagman, K. Ensrud, H.A. Fink, T.A. Hillier, L.Y. Lui, S.R. Cummings, J.T. Schousboe, N. Napoli, The ability of a single BMD and fracture history assessment to predict fracture over 25 years in postmenopausal women: the study of osteoporotic fractures. J. Bone Miner. Res. 33(3), 389–395 (2018)CrossRef D.M. Black, J.A. Cauley, R. Wagman, K. Ensrud, H.A. Fink, T.A. Hillier, L.Y. Lui, S.R. Cummings, J.T. Schousboe, N. Napoli, The ability of a single BMD and fracture history assessment to predict fracture over 25 years in postmenopausal women: the study of osteoporotic fractures. J. Bone Miner. Res. 33(3), 389–395 (2018)CrossRef
Metadata
Title
Association between age at menopause and fracture risk: a systematic review and meta-analysis
Authors
Panagiotis Anagnostis
Pavlos Siolos
Nifon K. Gkekas
Nikoletta Kosmidou
Aikaterini-Maria Artzouchaltzi
Konstantinos Christou
Stavroula A. Paschou
Michael Potoupnis
Eustathios Kenanidis
Eleftherios Tsiridis
Irene Lambrinoudaki
John C. Stevenson
Dimitrios G. Goulis
Publication date
01-02-2019
Publisher
Springer US
Published in
Endocrine / Issue 2/2019
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-018-1746-6

Other articles of this Issue 2/2019

Endocrine 2/2019 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.