New insights into the diagnosis and management of bone health in premature ovarian insufficiency

References

• Webber L, Davies M, Anderson R, et al. ESHRE Guideline: management of women with premature ovarian insufficiency. Hum Reprod. 2016;31(5):926–937.
   PubMed Web of Science ®Google Scholar
• Deeks AA, Gibson-Helm M, Teede H, et al. Premature menopause: a comprehensive understanding of psychosocial aspects. Climacteric. 2011;14(5):565–572.
   PubMed Web of Science ®Google Scholar
• Singer D, Mann E, Hunter MS, et al. The silent grief: psychosocial aspects of premature ovarian failure. Climacteric. 2011;14(4):428–437.
   PubMed Web of Science ®Google Scholar
• Panay N, Anderson RA, Nappi RE, et al. Premature ovarian insufficiency: an International Menopause Society White Paper. Climacteric. 2020;23(5):426–446.
   PubMed Web of Science ®Google Scholar
• Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organization technical report series. Vol. 843; 1994. p. 1–129.
   Google Scholar
• Cummings SR, Melton LJ. Epidemiology and outcomes of osteoporotic fractures. Lancet. 2002;359(9319):1761–1767.
   PubMed Web of Science ®Google Scholar
• Nguyen HH, Wong P, Strauss BJ, et al. Delay in estrogen commencement is associated with lower bone mineral density in Turner syndrome. Climacteric. 2017;20(5):436–441.
   PubMed Web of Science ®Google Scholar
• Gallagher JC. Effect of early menopause on bone mineral density and fractures. Menopause. 2007;14(3):567–571.
   PubMed Web of Science ®Google Scholar
• Popat VB, Calis KA, Vanderhoof VH, et al. Bone mineral density in estrogen-deficient young women. J Clin Endocrinol Metab. 2009;94(7):2277–2283.
   PubMed Web of Science ®Google Scholar
• Fakkert IE, Teixeira N, Abma EM, et al. Bone mineral density and fractures after surgical menopause: systematic review and meta-analysis. BJOG. 2017;124(10):1525–1535.
   PubMed Web of Science ®Google Scholar
• Xu X, Jones M, Mishra GD. Age at natural menopause and development of chronic conditions and multimorbidity: results from an Australian prospective cohort. Hum Reprod. 2020;35(1):203–211.
   PubMed Web of Science ®Google Scholar
• Viuff MH, Berglund A, Juul S, et al. sex hormone replacement therapy in Turner Syndrome: impact on morbidity and mortality. J Clin Endocrinol Metab. 2020;105(2):dgz039.
   PubMed Web of Science ®Google Scholar
• Bachelot A, Nicolas C, Gricourt S, et al. Poor compliance to hormone therapy and decreased bone mineral density in women with premature ovarian insufficiency. PloS One. 2016;11(12):e0164638.
   PubMed Web of Science ®Google Scholar
• Sullivan SD, Lehman A, Nathan NK, et al. Age of menopause and fracture risk in postmenopausal women randomized to calcium + vitamin D, hormone therapy, or the combination: results from the Women's Health Initiative Clinical Trials. Menopause. 2017;24(4):371–378.
   PubMed Web of Science ®Google Scholar
• Goh M, Nguyen HH, Khan NN, et al. Identifying and addressing osteoporosis knowledge gaps in women with premature ovarian insufficiency and early menopause: a mixed-methods study. Clin Endocrinol. 2019;91(4):498–507.
   PubMed Web of Science ®Google Scholar
• Jones AR, Goh M, Langham R, et al. Osteoporosis and premature ovarian insufficiency: geographic variation in clinicians' and consumers' knowledge gaps and barriers to care. Arch Osteoporos. 2020;15(1):38.
   PubMed Web of Science ®Google Scholar
• Khosla S, Oursler MJ, Monroe DG. Estrogen and the skeleton. Trends Endocrinol Metab. 2012;23(11):576–581.
   PubMed Web of Science ®Google Scholar
• Manolagas SC, O'Brien CA, Almeida M. The role of estrogen and androgen receptors in bone health and disease. Nat Rev Endocrinol. 2013;9(12):699–712.
   PubMed Web of Science ®Google Scholar
• Kondo H, Searby ND, Mojarrab R, et al. Total-body irradiation of postpubertal mice with (137)Cs acutely compromises the microarchitecture of cancellous bone and increases osteoclasts. Radiat Res. 2009;171(3):283–289.
   PubMed Web of Science ®Google Scholar
• Soucek O, Zapletalova J, Zemkova D, et al. Prepubertal girls with Turner syndrome and children with isolated SHOX deficiency have similar bone geometry at the radius. J Clin Endocrinol Metab. 2013;98(7):E1241–E1247.
   PubMed Web of Science ®Google Scholar
• Frederiksen AL, Hansen S, Brixen K, et al. Increased cortical area and thickness in the distal radius in subjects with SHOX-gene mutation. Bone. 2014;69:23–29.
   PubMed Web of Science ®Google Scholar
• Cardona Attard C, Cameron-Pimblett A, Puri D, et al. Fracture rate in women with oestrogen deficiency – comparison of Turner syndrome and premature ovarian insufficiency. Clin Endocrinol. 2019;91(6):743–749.
   PubMed Web of Science ®Google Scholar
• Han TS, Cadge B, Conway GS. Hearing impairment and low bone mineral density increase the risk of bone fractures in women with Turner's syndrome. Clin Endocrinol. 2006;65(5):643–647.
   PubMed Web of Science ®Google Scholar
• Landin-Wilhelmsen K, Bryman I, Windh M, et al. Osteoporosis and fractures in Turner syndrome-importance of growth promoting and oestrogen therapy. Clinical Endocrinol. 1999;51(4):497–502.
   PubMed Web of Science ®Google Scholar
• Nijhuis-van Der Sanden MWG, Eling PATM, Otten BJ. A review of neuropsychological and motor studies in Turner Syndrome. Neurosci Biobehav Rev. 2003;27(4):329–338.
   PubMed Web of Science ®Google Scholar
• Faienza MF, Ventura A, Colucci S, et al. Bone fragility in Turner Syndrome: mechanisms and prevention strategies. Frontiers Endocrinol. 2016;7:34.
   PubMed Web of Science ®Google Scholar
• Shea AK, Buwembo A, Mayhew A, et al. The association between primary ovarian insufficiency and osteoporosis in the Canadian Longitudinal Study on Aging. Menopause. 2021 Mar 1. doi: https://doi.org/10.1097/GME.0000000000001756
   Google Scholar
• Nguyen HH, Wong P, Strauss BJ, et al. A cross-sectional and longitudinal analysis of trabecular bone score in adults with Turner Syndrome. J Clin Endocrinol Metab. 2018;103(10):3792–3800.
   PubMed Web of Science ®Google Scholar
• Cleemann L, Hjerrild BE, Lauridsen AL, et al. Long-term hormone replacement therapy preserves bone mineral density in Turner syndrome. Eur J Endocrinol. 2009;161(2):251–257.
   PubMed Web of Science ®Google Scholar
• Suganuma N, Furuhashi M, Hirooka T, et al. Bone mineral density in adult patients with Turner's syndrome: analyses of the effectiveness of GH and ovarian steroid hormone replacement therapies. Endocr J. 2003;50(3):263–269.
   PubMed Web of Science ®Google Scholar
• Cintron D, Rodriguez-Gutierrez R, Serrano V, et al. Effect of estrogen replacement therapy on bone and cardiovascular outcomes in women with Turner syndrome: a systematic review and meta-analysis. Int J Basic Clin Endocrinol. 2017;55(2):366–375.
   Google Scholar
• Soucek O, Schönau E, Lebl J, et al. A 6-year follow-up of fracture incidence and volumetric bone mineral density development in girls with Turner Syndrome. J Clin Endocrinol Metab. 2018;103(3):1188–1197.
   PubMed Web of Science ®Google Scholar
• Brotto M, Bonewald L. Bone and muscle: interactions beyond mechanical. Bone. 2015;80:109–114.
   PubMed Web of Science ®Google Scholar
• Samad N, Nguyen HH, Scott D, et al. Musculoskeletal health in premature ovarian insufficiency. Part One: muscle. Semin Reprod Med. 2021;38(4-05):277–288.
   Web of Science ®Google Scholar
• Barros RP, Gustafsson J. Estrogen receptors and the metabolic network. Cell Metab. 2011;14(3):289–299.
   PubMed Web of Science ®Google Scholar
• Laakkonen EK, Soliymani R, Karvinen S, et al. Estrogenic regulation of skeletal muscle proteome: a study of premenopausal women and postmenopausal MZ cotwins discordant for hormonal therapy. Aging Cell. 2017;16(6):1276–1287.
   PubMed Web of Science ®Google Scholar
• Li X, Fan L, Zhu M, et al. Combined intervention of 17β-estradiol and treadmill training ameliorates energy metabolism in skeletal muscle of female ovariectomized mice. Climacteric. 2020;23(2):192–200.
   PubMed Web of Science ®Google Scholar
• van Geel TACM, Geusens PP, Winkens B, et al. Measures of bioavailable serum testosterone and estradiol and their relationships with muscle mass, muscle strength and bone mineral density in postmenopausal women: a cross-sectional study. Eur J Endocrinol. 2009;160(4):681–687.
   PubMed Web of Science ®Google Scholar
• Gallagher D, Visser M, De Meersman RE, et al. Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol. 1997;83(1):229–239.
   PubMed Web of Science ®Google Scholar
• Phillips SK, Rook KM, Siddle NC, et al. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci. 1993;84(1):95–98.
   PubMed Web of Science ®Google Scholar
• Calmels P, Vico L, Alexandre C, et al. Cross-sectional study of muscle strength and bone mineral density in a population of 106 women between the ages of 44 and 87 years: relationship with age and menopause. Eur J Appl Physiol. 1995;70(2):180–186.
   Web of Science ®Google Scholar
• Soucek O, Matyskova J, Anliker E, et al. The muscle-bone interaction in Turner syndrome. Bone. 2015;74:160–165.
   PubMed Web of Science ®Google Scholar
• Cruz-Jentoft AJ, Bahat G, Bauer J, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing. 2019;48(1):16–31.
   PubMed Web of Science ®Google Scholar
• Bhasin S, Travison TG, Manini TM, et al. Sarcopenia definition: the position statements of the sarcopenia definition and outcomes consortium. J Am Geriatr Soc. 2020;68(7):1410–1418.
   PubMed Web of Science ®Google Scholar
• Cawthon PM, Manini T, Patel SM, et al. Putative cut-points in sarcopenia components and incident adverse health outcomes: an SDOC analysis. J Am Geriatr Soc. 2020;68(7):1429–1437.
   PubMed Web of Science ®Google Scholar
• Cawthon PM, Travison TG, Manini TM, et al. Establishing the link between lean mass and grip strength cut points with mobility disability and other health outcomes: proceedings of the sarcopenia definition and outcomes consortium conference. J Gerontol A Biol Sci Med Sci. 2020;75(7):1317–1323.
   PubMed Web of Science ®Google Scholar
• Hirschfeld HP, Kinsella R, Duque G. Osteosarcopenia: where bone, muscle, and fat collide. Osteoporos Int. 2017;28(10):2781–2790.
   PubMed Web of Science ®Google Scholar
• Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int. 2003;14 (S3):13–18.
   PubMed Web of Science ®Google Scholar
• Engelke K, Adams JE, Armbrecht G, et al. Clinical use of quantitative computed tomography and peripheral quantitative computed tomography in the management of osteoporosis in adults: the 2007 ISCD Official Positions. J Clin Densitom. 2008;11(1):123–162.
   PubMed Web of Science ®Google Scholar
• Kushida K. [Bone mineral density measurements for diagnosis of osteoporosis and the risk assessment]. Clin Calcium. 2004;14(12):11–17.
   PubMedGoogle Scholar
• Ferrari S, Bianchi ML, Eisman JA, et al. Osteoporosis in young adults: pathophysiology, diagnosis, and management. Osteoporos Int. 2012;23(12):2735–2748.
   PubMed Web of Science ®Google Scholar
• 2019 International Society for Clinical Densitometry Official Positions (Adult). Accessed 2021 March 2. Available from: https://iscd.org/learn/official-positions/adult-positions/
   Google Scholar
• Kanis JA, Johansson H, Harvey NC, et al. A brief history of FRAX. Arch Osteoporos. 2018;13(1):118.
   PubMed Web of Science ®Google Scholar
• Silva BC, Leslie WD, Resch H, et al. Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res. 2014;29(3):518–530.
   PubMed Web of Science ®Google Scholar
• Saito S, Koga E, Okada Y, et al. Effects of age at estrogen replacement therapy initiation on trabecular bone score in Japanese adults with Turner syndrome. Osteoporos Int. 2021;32(4):671–680.
   PubMed Web of Science ®Google Scholar
• Faulkner KG, Wacker WK, Barden HS, et al. Femur strength index predicts hip fracture independent of bone density and hip axis length. Osteoporos Int. 2006;17(4):593–599.
   PubMed Web of Science ®Google Scholar
• Whittier DE, Boyd SK, Burghardt AJ, et al. Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography. Osteoporos Int. 2020;31(9):1607–1627.
   PubMed Web of Science ®Google Scholar
• Nour MA, Burt LA, Perry RJ, et al. Impact of growth hormone on adult bone quality in Turner Syndrome: a HR-pQCT study. Calcif Tissue Int. 2016;98(1):49–59.
   PubMed Web of Science ®Google Scholar
• Gravholt CH, Lauridsen AL, Brixen K, et al. Marked disproportionality in bone size and mineral, and distinct abnormalities in bone markers and calcitropic hormones in adult Turner syndrome: a cross-sectional study. J Clin Endocrinol Metab. 2002;87(6):2798–2808.
   PubMed Web of Science ®Google Scholar
• Szulc P, Seeman E, Delmas PD. Biochemical measurements of bone turnover in children and adolescents. Osteoporos Int. 2000;11(4):281–294.
   PubMed Web of Science ®Google Scholar
• Faienza MF, Brunetti G, Ventura A, et al. Mechanisms of enhanced osteoclastogenesis in girls and young women with Turner's Syndrome. Bone. 2015;81:228–236.
   PubMed Web of Science ®Google Scholar
• Lane NE, Saag K, O’Neill TJ, et al. Real-world bone turnover marker use: impact on treatment decisions and fracture. Osteoporos Int. 2021;32(5):831–840.
   PubMed Web of Science ®Google Scholar
• Lambrinoudaki I, Paschou SA, Lumsden MA, et al. Premature ovarian insufficiency: a toolkit for the primary care physician. Climacteric. 2021:1–13. doi: https://doi.org/10.1080/13697137.2020.1859246
   Google Scholar
• Gravholt CH, Andersen NH, Conway GS, et al. Clinical practice guidelines for the care of girls and women with Turner syndrome: proceedings from the 2016 Cincinnati International Turner Syndrome Meeting. Eur J Endocrinol. 2017;177(3):G1–G70.
   PubMed Web of Science ®Google Scholar
• Messina C, Maffi G, Vitale JA, et al. Diagnostic imaging of osteoporosis and sarcopenia: a narrative review. Quant Imaging Med Surg. 2018;8(1):86–99.
   PubMed Web of Science ®Google Scholar
• Boutin RD, Yao L, Canter RJ, et al. Sarcopenia: current concepts and imaging implications. Am J Roentgenol. 2015;205(3):W255–66.
   PubMed Web of Science ®Google Scholar
• Reeder SB, Hu HH, Sirlin CB. Proton density fat-fraction: a standardized MR-based biomarker of tissue fat concentration. J Magn Reson Imaging. 2012;36(5):1011–1014.
   PubMed Web of Science ®Google Scholar
• Kyle UG, Bosaeus I, De Lorenzo AD, et al. Bioelectrical impedance analysis-part II: utilization in clinical practice. Clin Nutr. 2004;23(6):1430–1453.
   PubMed Web of Science ®Google Scholar
• Kim M, Shinkai S. Prevalence of muscle weakness based on different diagnostic criteria in community-dwelling older adults: a comparison of grip strength dynamometers. Geriatr Gerontol Int. 2017;17(11):2089–2095.
   PubMed Web of Science ®Google Scholar
• Kiriakova V, Cooray SD, Yeganeh L, et al. Management of bone health in women with premature ovarian insufficiency: systematic appraisal of clinical practice guidelines and algorithm development. Maturitas. 2019;128:70–80.
   PubMed Web of Science ®Google Scholar
• Burgos N, Cintron D, Latortue-Albino P, et al. Estrogen-based hormone therapy in women with primary ovarian insufficiency: a systematic review. Endocrine. 2017;58(3):413–425.
   PubMed Web of Science ®Google Scholar
• Ha J, Park SS, Park S, et al. Effects of hormone replacement therapy on bone mass after allogeneic hematopoietic stem cell transplantation. J Clin Endocrinol Metab. 2020;105(9):dgaa406.
   PubMed Web of Science ®Google Scholar
• Tauchmanova L, De Simone G, Musella T, et al. Effects of various antireabsorptive treatments on bone mineral density in hypogonadal young women after allogeneic stem cell transplantation. Bone Marrow Transplant. 2006;37(1):81–88.
   PubMed Web of Science ®Google Scholar
• Cartwright B, Robinson J, Seed PT, et al. Hormone replacement therapy versus the combined oral contraceptive pill in premature ovarian failure: a randomized controlled trial of the effects on bone mineral density. J Clin Endocrinol Metab. 2016;101(9):3497–3505.
   PubMed Web of Science ®Google Scholar
• Crofton PM, Evans N, Bath LE, et al. Physiological versus standard sex steroid replacement in young women with premature ovarian failure: effects on bone mass acquisition and turnover. Clin Endocrinol. 2010;73(6):707–714.
   PubMed Web of Science ®Google Scholar
• Gazarra LBC, Bonacordi CL, Yela DA, et al. Bone mass in women with premature ovarian insufficiency: a comparative study between hormone therapy and combined oral contraceptives. Menopause. 2020;27(10):1110–1116.
   PubMed Web of Science ®Google Scholar
• Cleemann L, Holm K, Kobbernagel H, et al. Dosage of estradiol, bone and body composition in Turner syndrome: a 5-year randomized controlled clinical trial. Eur J Endocrinol. 2017;176(2):233–242.
   PubMed Web of Science ®Google Scholar
• Upton CE, Daniels JP, Davids MC. Premature ovarian insufficiency: the need for evidence on the effectiveness of hormonal therapy. Climacteric. 2021;24:00.
   Web of Science ®Google Scholar
• Fouda MA, Khan AA, Sultan MS, et al. Evaluation and management of skeletal health in celiac disease: position statement. Can J Gastroenterol. 2012;26(11):819–829.
   PubMed Web of Science ®Google Scholar
• Canonico M, Carcaillon L, Plu-Bureau G, et al. Postmenopausal hormone therapy and risk of stroke: impact of the route of estrogen administration and type of progestogen. Stroke. 2016;47(7):1734–1741.
   PubMed Web of Science ®Google Scholar
• Mohammed K, Abu Dabrh AM, Benkhadra K, et al. Oral vs Transdermal estrogen therapy and vascular events: a systematic review and meta-analysis. J Clin Endocrinol Metab. 2015;100(11):4012–4020.
   PubMed Web of Science ®Google Scholar
• Zuckerman-Levin N, Frolova-Bishara T, Militianu D, et al. Androgen replacement therapy in Turner syndrome: a pilot study. J Clin Endocrinol Metab. 2009;94(12):4820–4827.
   PubMed Web of Science ®Google Scholar
• Popat VB, Calis KA, Kalantaridou SN, et al. Bone mineral density in young women with primary ovarian insufficiency: results of a three-year randomized controlled trial of physiological transdermal estradiol and testosterone replacement. J Clin Endocrinol Metab. 2014;99(9):3418–3426.
   PubMed Web of Science ®Google Scholar
• Bidet M, Bachelot A, Bissauge E, et al. Resumption of ovarian function and pregnancies in 358 patients with premature ovarian failure. J Clin Endocrinol Metab. 2011;96(12):3864–3872.
   PubMed Web of Science ®Google Scholar
• Cremers SC, Pillai G, Papapoulos SE. Pharmacokinetics/pharmacodynamics of bisphosphonates: use for optimisation of intermittent therapy for osteoporosis. Clin Pharmacokinet. 2005;44(6):551–570.
   PubMed Web of Science ®Google Scholar
• Baron R, Ferrari S, Russell RG. Denosumab and bisphosphonates: different mechanisms of action and effects. Bone. 2011;48(4):677–692.
   PubMed Web of Science ®Google Scholar
• Gralow JR, Biermann JS, Farooki A, et al. NCCN task force report: bone health in cancer care. J Natl Compr Canc Netw. 2013;11 (Suppl 3):S1–S50.
   PubMed Web of Science ®Google Scholar
• Powles TJ, Hickish T, Kanis JA, et al. Effect of tamoxifen on bone mineral density measured by dual-energy x-ray absorptiometry in healthy premenopausal and postmenopausal women. JCO. 1996;14(1):78–84.
   PubMed Web of Science ®Google Scholar
• Sverrisdóttir A, Fornander T, Jacobsson H, et al. Bone mineral density among premenopausal women with early breast cancer in a randomized trial of adjuvant endocrine therapy. JCO. 2004;22(18):3694–3699.
   PubMed Web of Science ®Google Scholar
• Fisher B, Costantino JP, Wickerham DL, et al. Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. J Natl Cancer Inst. 2005;97(22):1652–1662.
   PubMed Web of Science ®Google Scholar
• Love RR, Mazess RB, Barden HS, et al. Effects of tamoxifen on bone mineral density in postmenopausal women with breast cancer. N Engl J Med. 1992;326(13):852–856.
   PubMed Web of Science ®Google Scholar
• Gnant M, Mlineritsch B, Luschin-Ebengreuth G, et al. Adjuvant endocrine therapy plus zoledronic acid in premenopausal women with early-stage breast cancer: 5-year follow-up of the ABCSG-12 bone-mineral density substudy. Lancet Oncol. 2008;9(9):840–849.
   PubMed Web of Science ®Google Scholar
• Fogelman I, Blake GM, Blamey R, et al. Bone mineral density in premenopausal women treated for node-positive early breast cancer with 2 years of goserelin or 6 months of cyclophosphamide, methotrexate and 5-fluorouracil (CMF). Osteoporos Int. 2003;14(12):1001–1006.
   PubMed Web of Science ®Google Scholar
• Grossmann M, Ramchand SK, Milat F, et al. Assessment and management of bone health in women with oestrogen receptor-positive breast cancer receiving endocrine therapy: position statement of the Endocrine Society of Australia, the Australian and New Zealand Bone & Mineral Society, the Australasian Menopause Society and the Clinical Oncology Society of Australia. Clin Endocrinol. 2018;89(3):280–296.
   PubMed Web of Science ®Google Scholar
• Gnant M, Mlineritsch B, Stoeger H, et al. Zoledronic acid combined with adjuvant endocrine therapy of tamoxifen versus anastrozol plus ovarian function suppression in premenopausal early breast cancer: final analysis of the Austrian Breast and Colorectal Cancer Study Group Trial 12. Ann Oncol. 2015;26(2):313–320.
   PubMed Web of Science ®Google Scholar
• Shapiro CL, Halabi S, Hars V, et al. Zoledronic acid preserves bone mineral density in premenopausal women who develop ovarian failure due to adjuvant chemotherapy: final results from CALGB trial 79809. Eur J Cancer. 2011;47(5):683–689.
   PubMed Web of Science ®Google Scholar
• Hadji P, Kauka A, Ziller M, et al. Effects of zoledronic acid on bone mineral density in premenopausal women receiving neoadjuvant or adjuvant therapies for HR + breast cancer: the ProBONE II study. Osteoporos Int. 2014;25(4):1369–1378.
   PubMed Web of Science ®Google Scholar
• Compston JE. Osteoporosis. Clin Endocrinol 1990:33(5):653–682.
   PubMed Web of Science ®Google Scholar
• Papagianni V, Deligeoroglou E, Makrakis E, Botsis D, Creatsas G. Response to hormonal treatment of young females with primary or very premature ovarian failure. Gynecol Endocrinol. 2011;27(5):291–299.
   Google Scholar