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Erschienen in: Osteoporosis International 4/2021

23.09.2020 | Original Article

Effects of age at estrogen replacement therapy initiation on trabecular bone score in Japanese adults with Turner syndrome

verfasst von: S. Saito, E. Koga, Y. Okada, T. Tsuburai, H. Yoshikata, E. Miyagi, H. Sakakibara

Erschienen in: Osteoporosis International | Ausgabe 4/2021

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Abstract

Summary

The effects of the age at estrogen replacement therapy (ERT) initiation on bone quality in Turner syndrome were evaluated using trabecular bone score. Early puberty ERT positively correlated with increase in bone quality. Early initiation of ERT is necessary for the acquisition of bone quality as well as bone density.

Introduction

Studies have reported associations between bone mineral density and estrogen replacement therapy (ERT) in Turner syndrome (TS) patients; however, few studies exist on the effect on bone quality. The aim of this study was to evaluate the effects of the age at ERT initiation on bone quality of Japanese TS patients, cross-sectionally and longitudinally.

Methods

Cross-sectionally, 95 TS patients were divided into three groups based on their age at initiation of ERT: A (12–14 years, 11 patients), B (15–17 years, 47 patients), and C (over 18 years, 37 patients). To assess bone quality, trabecular bone score (TBS) was used. The effects of age at initiation and duration of ERT on TBS were examined using multiple regression analysis. In the longitudinal study, 48 patients who underwent dual-energy X-ray absorptiometry multiple times were divided into three groups: D (12–14 years, 8 patients), E (15–17 years, 18 patients), and F (over 18 years, 22 patients). Each group was analyzed for the rate of change in TBS per year.

Results

Cross-sectionally, the TBS showed significant differences among the three groups (TBS A, 1.302; B, 1.299; C, 1.245) (p = 0.013); group C was significantly lower than B (p = 0.014); bone quality was degraded. Multiple regression analysis revealed that age at ERT initiation significantly affected the increase in TBS (p = 0.002). Longitudinally, the rate of change of TBS was not significantly different in the three groups (p = 0.73).

Conclusion

Early initiation of ERT may have positive effects on bone quality in TS. Large prospective studies will be needed.
Literatur
1.
Zurück zum Zitat Bondy CA, Turner Syndrome Study Group (2007) Care of girls and women with Turner syndrome: a guideline of the Turner Syndrome Study Group. J Clin Endocrinol Metab 92:10–25CrossRef Bondy CA, Turner Syndrome Study Group (2007) Care of girls and women with Turner syndrome: a guideline of the Turner Syndrome Study Group. J Clin Endocrinol Metab 92:10–25CrossRef
2.
Zurück zum Zitat Wolff DJ, Van Dyke DL, Powell CM (2010) Laboratory guideline for Turner syndrome. Genet Med 12:52–55CrossRef Wolff DJ, Van Dyke DL, Powell CM (2010) Laboratory guideline for Turner syndrome. Genet Med 12:52–55CrossRef
3.
Zurück zum Zitat Pasquino AM, Passeri F, Pucarelli I, Segni M, Municchi G (1997) Spontaneous pubertal development in Turner’s Syndrome. Italian Study Group for Turner’s Syndrome. J Clin Endocrinol Metab 82:1810–1813PubMed Pasquino AM, Passeri F, Pucarelli I, Segni M, Municchi G (1997) Spontaneous pubertal development in Turner’s Syndrome. Italian Study Group for Turner’s Syndrome. J Clin Endocrinol Metab 82:1810–1813PubMed
4.
Zurück zum Zitat Shore RM, Chesney RW, Mazess RB, Rose PG, Bargman GJ (1982) Skeletal demineralization in Turner's syndrome. Calcif Tissue Int 34:519–522CrossRef Shore RM, Chesney RW, Mazess RB, Rose PG, Bargman GJ (1982) Skeletal demineralization in Turner's syndrome. Calcif Tissue Int 34:519–522CrossRef
5.
Zurück zum Zitat Davies MC, Gulekli B, Jacobs HS (1995) Osteoporosis in Turner's syndrome and other forms of primary amenorrhoea. Clin Endocrinol 43:741–746CrossRef Davies MC, Gulekli B, Jacobs HS (1995) Osteoporosis in Turner's syndrome and other forms of primary amenorrhoea. Clin Endocrinol 43:741–746CrossRef
6.
Zurück zum Zitat Gravholt CH, Vestergaard P, Hermann AP, Mosekilde L, Brixen K, Christiansen JS (2003) Increased fracture rates in Turner's syndrome: a nationwide questionnaire survey. Clin Endocrinol 59:89–96CrossRef Gravholt CH, Vestergaard P, Hermann AP, Mosekilde L, Brixen K, Christiansen JS (2003) Increased fracture rates in Turner's syndrome: a nationwide questionnaire survey. Clin Endocrinol 59:89–96CrossRef
7.
Zurück zum Zitat Manolagas SC, O'Brien CA, Almeida M (2013) The role of estrogen and androgen receptors in bone health and disease. Nat Rev Endocrinol 9:699–712CrossRef Manolagas SC, O'Brien CA, Almeida M (2013) The role of estrogen and androgen receptors in bone health and disease. Nat Rev Endocrinol 9:699–712CrossRef
8.
Zurück zum Zitat Soucek O, Schönau E, Lebl J, Willnecker J, Hlavka Z, Sumnik Z (2018) A 6-year follow-up of fracture incidence and volumetric bone mineral density development in girls with Turner syndrome. J Clin Endocrinol Metab 103:1188–1197CrossRef Soucek O, Schönau E, Lebl J, Willnecker J, Hlavka Z, Sumnik Z (2018) A 6-year follow-up of fracture incidence and volumetric bone mineral density development in girls with Turner syndrome. J Clin Endocrinol Metab 103:1188–1197CrossRef
9.
Zurück zum Zitat Hansen MA, Overgaard K, Riis BJ, Christiansen C (1991) Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12 year study. BMJ 303:961–964CrossRef Hansen MA, Overgaard K, Riis BJ, Christiansen C (1991) Role of peak bone mass and bone loss in postmenopausal osteoporosis: 12 year study. BMJ 303:961–964CrossRef
10.
Zurück zum Zitat Riis BJ, Hansen MA, Jensen AM, Overgaard K, Christiansen C (1996) Low bone mass and fast rate of bone loss at menopause: equal risk factors for future fracture: a 15-year follow-up study. Bone 19:9–12CrossRef Riis BJ, Hansen MA, Jensen AM, Overgaard K, Christiansen C (1996) Low bone mass and fast rate of bone loss at menopause: equal risk factors for future fracture: a 15-year follow-up study. Bone 19:9–12CrossRef
11.
Zurück zum Zitat Nakamura T, Tsuburai T, Tokinaga A, Nakajima I, Kitayama R, Imai Y, Nagata T, Yoshida H, Hirahara F, Sakakibara H (2015) Efficacy of estrogen replacement therapy (ERT) on uterine growth and acquisition of bone mass in patients with Turner syndrome. Endocr J 62:965–970CrossRef Nakamura T, Tsuburai T, Tokinaga A, Nakajima I, Kitayama R, Imai Y, Nagata T, Yoshida H, Hirahara F, Sakakibara H (2015) Efficacy of estrogen replacement therapy (ERT) on uterine growth and acquisition of bone mass in patients with Turner syndrome. Endocr J 62:965–970CrossRef
12.
Zurück zum Zitat Nguyen HH, Wong P, Strauss BJ, Jones G, Ebeling PR, Milat F, Vincent A (2017) Delay in estrogen commencement is associated with lower bone mineral density in Turner syndrome. Climacteric 20:436–441CrossRef Nguyen HH, Wong P, Strauss BJ, Jones G, Ebeling PR, Milat F, Vincent A (2017) Delay in estrogen commencement is associated with lower bone mineral density in Turner syndrome. Climacteric 20:436–441CrossRef
13.
Zurück zum Zitat Kodama M, Komura H, Kodama T, Nishio Y, Kimura T (2012) Estrogen therapy initiated at an early age increases bone mineral density in Turner syndrome patients. Endocr J 59:153–159CrossRef Kodama M, Komura H, Kodama T, Nishio Y, Kimura T (2012) Estrogen therapy initiated at an early age increases bone mineral density in Turner syndrome patients. Endocr J 59:153–159CrossRef
14.
Zurück zum Zitat Cameron-Pimblett A, Davies MC, Burt E, Talaulikar VS, La Rosa C, King TFJ, Conway GS (2019) Effects of estrogen therapies on outcomes in Turner syndrome: assessment of induction of puberty and adult estrogen use. J Clin Endocrinol Metab 104:2820–2826CrossRef Cameron-Pimblett A, Davies MC, Burt E, Talaulikar VS, La Rosa C, King TFJ, Conway GS (2019) Effects of estrogen therapies on outcomes in Turner syndrome: assessment of induction of puberty and adult estrogen use. J Clin Endocrinol Metab 104:2820–2826CrossRef
15.
Zurück zum Zitat Gravholt CH, Andersen NH, Conway GS, Dekkers OM, Geffner ME, Klein KO, Lin AE, Mauras N, Quigley CA, Rubin K, Sandberg DE, Sas TCJ, Silberbach M, Söderström-Anttila V, Stochholm K, van Alfen-van derVelden JA, Woelfle J, Backeljauw PF (2017) 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 177:G1–G70CrossRef Gravholt CH, Andersen NH, Conway GS, Dekkers OM, Geffner ME, Klein KO, Lin AE, Mauras N, Quigley CA, Rubin K, Sandberg DE, Sas TCJ, Silberbach M, Söderström-Anttila V, Stochholm K, van Alfen-van derVelden JA, Woelfle J, Backeljauw PF (2017) 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 177:G1–G70CrossRef
16.
Zurück zum Zitat Silva BC, Broy SB, Boutroy S, Schousboe JT, Shepherd JA, Leslie WD (2015) Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD Official Positions Part 2: trabecular bone score. J Clin Densitom 18:309–330CrossRef Silva BC, Broy SB, Boutroy S, Schousboe JT, Shepherd JA, Leslie WD (2015) Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD Official Positions Part 2: trabecular bone score. J Clin Densitom 18:309–330CrossRef
17.
Zurück zum Zitat Bouxsein ML (2005) Determinants of skeletal fragility. Best Pract Res Clin Rheumatol 19:897–911CrossRef Bouxsein ML (2005) Determinants of skeletal fragility. Best Pract Res Clin Rheumatol 19:897–911CrossRef
18.
Zurück zum Zitat McCloskey EV, Odén A, Harvey NC, Leslie WD, Hans D, Johansson H, Barkmann R, Boutroy S, Brown J, Chapurlat R, Elders PJM, Fujita Y, Glüer CC, Goltzman D, Iki M, Karlsson M, Kindmark A, Kotowicz M, Kurumatani N, Kwok T, Lamy O, Leung J, Lippuner K, Ljunggren Ö, Lorentzon M, Mellström D, Merlijn T, Oei L, Ohlsson C, Pasco JA, Rivadeneira F, Rosengren B, Sornay-Rendu E, Szulc P, Tamaki J, Kanis JA (2016) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 31:940–948CrossRef McCloskey EV, Odén A, Harvey NC, Leslie WD, Hans D, Johansson H, Barkmann R, Boutroy S, Brown J, Chapurlat R, Elders PJM, Fujita Y, Glüer CC, Goltzman D, Iki M, Karlsson M, Kindmark A, Kotowicz M, Kurumatani N, Kwok T, Lamy O, Leung J, Lippuner K, Ljunggren Ö, Lorentzon M, Mellström D, Merlijn T, Oei L, Ohlsson C, Pasco JA, Rivadeneira F, Rosengren B, Sornay-Rendu E, Szulc P, Tamaki J, Kanis JA (2016) A meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J Bone Miner Res 31:940–948CrossRef
19.
Zurück zum Zitat Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26:2762–2769CrossRef Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26:2762–2769CrossRef
20.
Zurück zum Zitat Harvey NC, Glüer CC, Binkley N, McCloskey EV, Brandi ML, Cooper C, Kendler D, Lamy O, Laslop A, Camargos BM, Reginster JY, Rizzoli R, Kanis JA (2015) Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78:216–224CrossRef Harvey NC, Glüer CC, Binkley N, McCloskey EV, Brandi ML, Cooper C, Kendler D, Lamy O, Laslop A, Camargos BM, Reginster JY, Rizzoli R, Kanis JA (2015) Trabecular bone score (TBS) as a new complementary approach for osteoporosis evaluation in clinical practice. Bone 78:216–224CrossRef
21.
Zurück zum Zitat Nguyen HH, Wong P, Strauss BJ, Ebeling PR, Milat F, Vincent A (2018) A cross-sectional and longitudinal analysis of trabecular bone score in adults with Turner syndrome. J Clin Endocrinol Metab 103:3792–3800CrossRef Nguyen HH, Wong P, Strauss BJ, Ebeling PR, Milat F, Vincent A (2018) A cross-sectional and longitudinal analysis of trabecular bone score in adults with Turner syndrome. J Clin Endocrinol Metab 103:3792–3800CrossRef
22.
Zurück zum Zitat Nour MA, Burt LA, Perry RJ, Stephure DK, Hanley DA, Boyd SK (2016) Impact of growth hormone on adult bone quality in Turner syndrome: a HR-pQCT study. Calcif Tissue Int 98:49–59CrossRef Nour MA, Burt LA, Perry RJ, Stephure DK, Hanley DA, Boyd SK (2016) Impact of growth hormone on adult bone quality in Turner syndrome: a HR-pQCT study. Calcif Tissue Int 98:49–59CrossRef
23.
Zurück zum Zitat Barthe N, Braillon P, Ducassou D, Basse-Cathakinat B (1997) Comparison of two Hologic DXA systems (QDR 1000 and QDR 4500/A). Br J Radiol 70:728–739CrossRef Barthe N, Braillon P, Ducassou D, Basse-Cathakinat B (1997) Comparison of two Hologic DXA systems (QDR 1000 and QDR 4500/A). Br J Radiol 70:728–739CrossRef
24.
Zurück zum Zitat Orimo H, Hayashi Y, Fukunaga M, Sone T, Fujiwara S, Shiraki M, Kushida K, Miyamoto S, Soen S, Nishimura J, Oh-Hashi Y, Hosoi T, Gorai I, Tanaka H, Igai T, Kishimoto H (2001) Diagnostic criteria for primary osteoporosis: year 2000 revision. J Bone Miner Metab 19:331–337CrossRef Orimo H, Hayashi Y, Fukunaga M, Sone T, Fujiwara S, Shiraki M, Kushida K, Miyamoto S, Soen S, Nishimura J, Oh-Hashi Y, Hosoi T, Gorai I, Tanaka H, Igai T, Kishimoto H (2001) Diagnostic criteria for primary osteoporosis: year 2000 revision. J Bone Miner Metab 19:331–337CrossRef
25.
Zurück zum Zitat Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29:518–530CrossRef Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the DXA image. J Bone Miner Res 29:518–530CrossRef
26.
Zurück zum Zitat Cintron D, Rodriguez-Gutierrez R, Serrano V, Latortue-Albino P, Erwin PJ, Murad MH (2017) Effect of estrogen replacement therapy on bone and cardiovascular outcomes in women with turner syndrome: a systematic review and meta-analysis. Endocrine 55:366–375CrossRef Cintron D, Rodriguez-Gutierrez R, Serrano V, Latortue-Albino P, Erwin PJ, Murad MH (2017) Effect of estrogen replacement therapy on bone and cardiovascular outcomes in women with turner syndrome: a systematic review and meta-analysis. Endocrine 55:366–375CrossRef
27.
Zurück zum Zitat Tritos NA, Klibanski A (2016) Chapter Nine – Effects of growth hormone on bone. in. Prog Mol Biol Transl Sci 138:193–211CrossRef Tritos NA, Klibanski A (2016) Chapter Nine – Effects of growth hormone on bone. in. Prog Mol Biol Transl Sci 138:193–211CrossRef
28.
Zurück zum Zitat Kužma M, Killinger Z, Jackuliak P, Vaňuga P, Hans D, Binkley N, Payer J (2019) Pathophysiology of growth hormone secretion disorders and their impact on bone microstructure as measured by trabecular bone score. Physiol Res 68:S121–S129CrossRef Kužma M, Killinger Z, Jackuliak P, Vaňuga P, Hans D, Binkley N, Payer J (2019) Pathophysiology of growth hormone secretion disorders and their impact on bone microstructure as measured by trabecular bone score. Physiol Res 68:S121–S129CrossRef
29.
Zurück zum Zitat Bilezikian JP, Hattersley G, Fitzpatrick LA, Harris AG, Shevroja E, Banks K, Leder BZ, Zanchetta JR, Hans D (2018) Abaloparatide-SC improves trabecular microarchitecture as assessed by trabecular bone score (TBS): a 24-week randomized clinical trial. Osteoporos Int 29:323–328CrossRef Bilezikian JP, Hattersley G, Fitzpatrick LA, Harris AG, Shevroja E, Banks K, Leder BZ, Zanchetta JR, Hans D (2018) Abaloparatide-SC improves trabecular microarchitecture as assessed by trabecular bone score (TBS): a 24-week randomized clinical trial. Osteoporos Int 29:323–328CrossRef
30.
Zurück zum Zitat McClung MR, Lippuner K, Brandi ML, Zanchetta JR, Bone HG, Chapurlat R, Hans D, Wang A, Zapalowski C, Libanati C (2017) Effect of denosumab on trabecular bone score in postmenopausal women with osteoporosis. Osteoporos Int 28:2967–2973CrossRef McClung MR, Lippuner K, Brandi ML, Zanchetta JR, Bone HG, Chapurlat R, Hans D, Wang A, Zapalowski C, Libanati C (2017) Effect of denosumab on trabecular bone score in postmenopausal women with osteoporosis. Osteoporos Int 28:2967–2973CrossRef
31.
Zurück zum Zitat Shawwa K, Arabi A, Nabulsi M, Maalouf J, Salamoun M, Choucair M, Hans D, El-Hajj Fuleihan G (2016) Predictors of trabecular bone score in school children. Osteoporos Int 27:703–710CrossRef Shawwa K, Arabi A, Nabulsi M, Maalouf J, Salamoun M, Choucair M, Hans D, El-Hajj Fuleihan G (2016) Predictors of trabecular bone score in school children. Osteoporos Int 27:703–710CrossRef
32.
Zurück zum Zitat Dowthwaite JN, Winzenrieth R, Binkley N, Krueger D, Scerpella TA (2017) A focused evaluation of lumbar spine trabecular bone score in the first year post-menarche. Arch Osteoporos 12:90CrossRef Dowthwaite JN, Winzenrieth R, Binkley N, Krueger D, Scerpella TA (2017) A focused evaluation of lumbar spine trabecular bone score in the first year post-menarche. Arch Osteoporos 12:90CrossRef
33.
Zurück zum Zitat Donaldson AA, Feldman HA, O'Donnell JM, Gopalakrishnan G, Gordon CM (2015) Spinal bone texture assessed by trabecular bone score in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab 100:3436–3442CrossRef Donaldson AA, Feldman HA, O'Donnell JM, Gopalakrishnan G, Gordon CM (2015) Spinal bone texture assessed by trabecular bone score in adolescent girls with anorexia nervosa. J Clin Endocrinol Metab 100:3436–3442CrossRef
34.
Zurück zum Zitat Levy-Shraga Y, Tripto-Shkolnik L, David D, Vered I, Stein D, Modan-Moses D (2019) Low trabecular bone score in adolescent female inpatients with anorexia nervosa. Clin Nutr 38:1166–1170CrossRef Levy-Shraga Y, Tripto-Shkolnik L, David D, Vered I, Stein D, Modan-Moses D (2019) Low trabecular bone score in adolescent female inpatients with anorexia nervosa. Clin Nutr 38:1166–1170CrossRef
Metadaten
Titel
Effects of age at estrogen replacement therapy initiation on trabecular bone score in Japanese adults with Turner syndrome
verfasst von
S. Saito
E. Koga
Y. Okada
T. Tsuburai
H. Yoshikata
E. Miyagi
H. Sakakibara
Publikationsdatum
23.09.2020
Verlag
Springer London
Erschienen in
Osteoporosis International / Ausgabe 4/2021
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-020-05652-1

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