Musculoskeletal Health in Premature Ovarian Insufficiency. Part One: Muscle

Navira Samad; Hanh H. Nguyen; David Scott; Peter R. Ebeling; Frances Milat

doi:10.1055/s-0040-1721797

Seminars in Reproductive Medicine, Table of Contents

Semin Reprod Med 2020; 38(04/05): 277-288
DOI: 10.1055/s-0040-1721797

Review Article

Musculoskeletal Health in Premature Ovarian Insufficiency. Part One: Muscle

Authors

Navira Samad

¹Department of Medicine, School of Clinical Sciences, Monash University, Clayton, Victoria, Australia

²Department of Endocrinology, Monash Health, Clayton, Victoria, Australia

³Department of Medicine, School of Clinical Sciences, Faculty of Medicine, Nursing and Health Sciences, Monash University, Victoria, Australia
Hanh H. Nguyen

¹Department of Medicine, School of Clinical Sciences, Monash University, Clayton, Victoria, Australia

²Department of Endocrinology, Monash Health, Clayton, Victoria, Australia

⁴Department of Endocrinology and Diabetes, Western Health, Victoria, Australia
David Scott

¹Department of Medicine, School of Clinical Sciences, Monash University, Clayton, Victoria, Australia

⁵Institute for Physical Activity and Nutrition, School of Exercise and Nutrition Sciences, Deakin University, Geelong, Victoria, Australia
Peter R. Ebeling

¹Department of Medicine, School of Clinical Sciences, Monash University, Clayton, Victoria, Australia

²Department of Endocrinology, Monash Health, Clayton, Victoria, Australia
Frances Milat

¹Department of Medicine, School of Clinical Sciences, Monash University, Clayton, Victoria, Australia

²Department of Endocrinology, Monash Health, Clayton, Victoria, Australia

⁴Department of Endocrinology and Diabetes, Western Health, Victoria, Australia

Abstract

Accelerated bone loss and muscle decline coexist in women with premature ovarian insufficiency (POI), but there are significant gaps in our understanding of musculoskeletal health in POI. This article is the first of a two-part review which describes estrogen signaling in muscle and its role in musculoskeletal health and disease. Current evidence regarding the utility of available diagnostic tests and therapeutic options is also discussed. A literature review from January 2000 to March 2020 was conducted to identify relevant studies. Women with POI experience significant deterioration in musculoskeletal health due to the loss of protective effects of estrogen. In addition to bone loss, muscle decay and dysfunction is now increasingly recognized. Nevertheless, there is a paucity of validated tools to assess muscle parameters. There is a growing need to acknowledge bone–muscle codependence to design new therapies which target both muscle and bone, resulting in improved physical performance and reduced morbidity and mortality. More high-quality research and international collaborations are needed to address the deficiencies in our understanding and management of musculoskeletal health in women with POI.

Keywords

premature ovarian insufficiency - osteoporosis - bone - muscle - early menopause

Full Text

References

References
1 Webber L, Davies M, Anderson R. et al; European Society for Human Reproduction and Embryology (ESHRE) Guideline Group on POI. ESHRE Guideline: management of women with premature ovarian insufficiency. Hum Reprod 2016; 31 (05) 926-937
2 Baber RJ, Panay N, Fenton A. IMS Writing Group. 2016 IMS Recommendations on women's midlife health and menopause hormone therapy. Climacteric 2016; 19 (02) 109-150
3 The 2017 hormone therapy position statement of The North American Menopause Society. Menopause 2018; 25 (11) 1362-1387
4 Mendoza N, Juliá MD, Galliano D. et al. Spanish consensus on premature menopause. Maturitas 2015; 80 (02) 220-225
5 Hamoda H. British Menopause Society and Women's Health Concern. The British Menopause Society and Women's Health Concern recommendations on the management of women with premature ovarian insufficiency. Post Reprod Health 2017; 23 (01) 22-35
6 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 summary. Med J Aust 2019; 211 (05) 224-229
7 Gallagher D, Visser M, De Meersman RE. et al. Appendicular skeletal muscle mass: effects of age, gender, and ethnicity. J Appl Physiol (1985) 1997; 83 (01) 229-239
8 Phillips SK, Rook KM, Siddle NC, Bruce SA, Woledge RC. Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy. Clin Sci (Lond) 1993; 84 (01) 95-98
9 Calmels P, Vico L, Alexandre C, Minaire P. 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 Occup Physiol 1995; 70 (02) 180-186
10 Beato M, Klug J. Steroid hormone receptors: an update. Hum Reprod Update 2000; 6 (03) 225-236
11 Tsai MJ, O'Malley BW. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 1994; 63: 451-486
12 Ponglikitmongkol M, Green S, Chambon P. Genomic organization of the human oestrogen receptor gene. EMBO J 1988; 7 (11) 3385-3388
13 Sand P, Luckhaus C, Schlurmann K, Götz M, Deckert J. Untangling the human estrogen receptor gene structure. J Neural Transm (Vienna) 2002; 109 (5-6): 567-583
14 Kos M, Reid G, Denger S, Gannon F. Minireview: genomic organization of the human ERalpha gene promoter region. Mol Endocrinol 2001; 15 (12) 2057-2063
15 Enmark E, Pelto-Huikko M, Grandien K. et al. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab 1997; 82 (12) 4258-4265
16 Thomas P, Pang Y, Filardo EJ, Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 2005; 146 (02) 624-632
17 Almeida M, Laurent MR, Dubois V. et al. Estrogens and androgens in skeletal physiology and pathophysiology. Physiol Rev 2017; 97 (01) 135-187
18 Yaşar P, Ayaz G, User SD, Güpür G, Muyan M. Molecular mechanism of estrogen-estrogen receptor signaling. Reprod Med Biol 2016; 16 (01) 4-20
19 Kumar R, Zakharov MN, Khan SH. et al. The dynamic structure of the estrogen receptor. J Amino Acids 2011; 2011: 812540
20 Bartell SM, Han L, Kim HN. et al. Non-nuclear-initiated actions of the estrogen receptor protect cortical bone mass. Mol Endocrinol 2013; 27 (04) 649-656
21 Fuentes N, Silveyra P. Estrogen receptor signaling mechanisms. Adv Protein Chem Struct Biol 2019; 116: 135-170
22 Almeida M, Iyer S, Martin-Millan M. et al. Estrogen receptor-α signaling in osteoblast progenitors stimulates cortical bone accrual. J Clin Invest 2013; 123 (01) 394-404
23 Barros RP, Gustafsson JÅ. Estrogen receptors and the metabolic network. Cell Metab 2011; 14 (03) 289-299
24 Ventura-Clapier R, Piquereau J, Veksler V, Garnier A. Estrogens, estrogen receptors effects on cardiac and skeletal muscle mitochondria. Front Endocrinol (Lausanne) 2019; 10: 557
25 Hevener AL, Ribas V, Moore TM, Zhou Z. The impact of skeletal muscle ERα on mitochondrial function and metabolic health. Endocrinology 2020; 161 (02) bqz017
26 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 (06) 1276-1287
27 Li X, Fan L, Zhu M, Jiang H, Bai W, Kang J. Combined intervention of 17β-estradiol and treadmill training ameliorates energy metabolism in skeletal muscle of female ovariectomized mice. Climacteric 2020; 23 (02) 192-200
28 Cabelka CA, Baumann CW, Collins BC. et al. Effects of ovarian hormones and estrogen receptor α on physical activity and skeletal muscle fatigue in female mice. Exp Gerontol 2019; 115: 155-164
29 Collins BC, Mader TL, Cabelka CA, Iñigo MR, Spangenburg EE, Lowe DA. Deletion of estrogen receptor α in skeletal muscle results in impaired contractility in female mice. J Appl Physiol (1985) 2018; 124 (04) 980-992
30 Collins BC, Arpke RW, Larson AA. et al. Estrogen regulates the satellite cell compartment in females. Cell Rep 2019; 28 (02) 368-381.e6
31 Fry CS, Lee JD, Mula J. et al. Inducible depletion of satellite cells in adult, sedentary mice impairs muscle regenerative capacity without affecting sarcopenia. Nat Med 2015; 21 (01) 76-80
32 Murphy MM, Lawson JA, Mathew SJ, Hutcheson DA, Kardon G. Satellite cells, connective tissue fibroblasts and their interactions are crucial for muscle regeneration. Development 2011; 138 (17) 3625-3637
33 Kamanga-Sollo E, Thornton KJ, White ME, Dayton WR. Role of G protein-coupled estrogen receptor-1 in estradiol 17β-induced alterations in protein synthesis and protein degradation rates in fused bovine satellite cell cultures. Domest Anim Endocrinol 2017; 58: 90-96
34 Hansen M, Skovgaard D, Reitelseder S, Holm L, Langbjerg H, Kjaer M. Effects of estrogen replacement and lower androgen status on skeletal muscle collagen and myofibrillar protein synthesis in postmenopausal women. J Gerontol A Biol Sci Med Sci 2012; 67 (10) 1005-1013
35 Zsakai A, Mascie-Taylor N, Bodzsar EB. Relationship between some indicators of reproductive history, body fatness and the menopausal transition in Hungarian women. J Physiol Anthropol 2015; 34: 35
36 Finkelstein JS, Brockwell SE, Mehta V. et al. Bone mineral density changes during the menopause transition in a multiethnic cohort of women. J Clin Endocrinol Metab 2008; 93 (03) 861-868
37 Maltais ML, Desroches J, Dionne IJ. Changes in muscle mass and strength after menopause. J Musculoskelet Neuronal Interact 2009; 9 (04) 186-197
38 Ezzat-Zadeh Z, Kim J-S, Chase PB, Arjmandi BH. The cooccurrence of obesity, osteoporosis, and sarcopenia in the ovariectomized rat: a study for modeling osteosarcopenic obesity in rodents. J Aging Res 2017; 2017: 1454103
39 Hertrampf T, Seibel J, Laudenbach U, Fritzemeier KH, Diel P. Analysis of the effects of oestrogen receptor alpha (ERalpha)- and ERbeta-selective ligands given in combination to ovariectomized rats. Br J Pharmacol 2008; 153 (07) 1432-1437
40 Gravholt CH, Hjerrild BE, Mosekilde L. et al. Body composition is distinctly altered in Turner syndrome: relations to glucose metabolism, circulating adipokines, and endothelial adhesion molecules. Eur J Endocrinol 2006; 155 (04) 583-592
41 Álvarez-Nava F, Racines M, Witt J, Guarderas J, Estévez M, Lanes R. Anthropometric variables as cardiovascular risk predictors in a cohort of adult subjects with Turner syndrome. Diabetes Metab Syndr Obes 2019; 12: 1795-1809
42 Corrigan EC, Nelson LM, Bakalov VK. et al. Effects of ovarian failure and X-chromosome deletion on body composition and insulin sensitivity in young women. Menopause 2006; 13 (06) 911-916
43 Michalakis K, Coppack SW. Primary ovarian insufficiency: relation to changes in body composition and adiposity. Maturitas 2012; 71 (04) 320-325
44 Maurel DB, Jähn K, Lara-Castillo N. Muscle-bone crosstalk: emerging opportunities for novel therapeutic approaches to treat musculoskeletal pathologies. Biomedicines 2017; 5 (04) E62
45 Gomarasca M, Banfi G, Lombardi G. Myokines: the endocrine coupling of skeletal muscle and bone. Adv Clin Chem 2020; 94: 155-218
46 Loro E, Ramaswamy G, Chandra A. et al. IL15RA is required for osteoblast function and bone mineralization. Bone 2017; 103: 20-30
47 Colaianni G, Storlino G, Sanesi L, Colucci S, Grano M. Myokines and osteokines in the pathogenesis of muscle and bone diseases. Curr Osteoporos Rep 2020; 18 (04) 401-407
48 Tagliaferri C, Wittrant Y, Davicco MJ, Walrand S, Coxam V. Muscle and bone, two interconnected tissues. Ageing Res Rev 2015; 21: 55-70
49 Consensus development conference. Consensus development conference: diagnosis, prophylaxis, and treatment of osteoporosis. Am J Med 1993; 94 (06) 646-650
50 Shuhart CR, Yeap SS, Anderson PA. et al. Executive summary of the 2019 ISCD Position Development Conference on Monitoring Treatment, DXA Cross-calibration and Least Significant Change, Spinal Cord Injury, Peri-prosthetic and Orthopedic Bone Health, Transgender Medicine, and Pediatrics. J Clin Densitom 2019; 22 (04) 453-471
51 Ferrari S, Bianchi ML, Eisman JA. et al; IOF Committee of Scientific Advisors Working Group on Osteoporosis Pathophysiology. Osteoporosis in young adults: pathophysiology, diagnosis, and management. Osteoporos Int 2012; 23 (12) 2735-2748
52 Cruz-Jentoft AJ, Bahat G, Bauer J. et al; Writing Group for the European Working Group on Sarcopenia in Older People 2 (EWGSOP2), and the Extended Group for EWGSOP2. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019; 48 (01) 16-31
53 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 (07) 1410-1418
54 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 (07) 1429-1437
55 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 (07) 1317-1323
56 Visser M, Schaap LA. Consequences of sarcopenia. Clin Geriatr Med 2011; 27 (03) 387-399
57 Scott D, Seibel M, Cumming R. et al. Does combined osteopenia/osteoporosis and sarcopenia confer greater risk of falls and fracture than either condition alone in older men? The Concord Health and Ageing in Men Project. J Gerontol A Biol Sci Med Sci 2019; 74 (06) 827-834
58 Hirschfeld HP, Kinsella R, Duque G. Osteosarcopenia: where bone, muscle, and fat collide. Osteoporos Int 2017; 28 (10) 2781-2790
59 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 (02) 233-242
60 Wells GD, O'Gorman CS, Rayner T. et al. Skeletal muscle abnormalities in girls and adolescents with Turner syndrome. J Clin Endocrinol Metab 2013; 98 (06) 2521-2527
61 Rolland YM, Perry III HM, Patrick P, Banks WA, Morley JE. Loss of appendicular muscle mass and loss of muscle strength in young postmenopausal women. J Gerontol A Biol Sci Med Sci 2007; 62 (03) 330-335
62 Aloia JF, McGowan DM, Vaswani AN, Ross P, Cohn SH. Relationship of menopause to skeletal and muscle mass. Am J Clin Nutr 1991; 53 (06) 1378-1383
63 Toth MJ, Poehlman ET, Matthews DE, Tchernof A, MacCoss MJ. Effects of estradiol and progesterone on body composition, protein synthesis, and lipoprotein lipase in rats. Am J Physiol Endocrinol Metab 2001; 280 (03) E496-E501
64 Smith GI, Reeds DN, Hall AM, Chambers KT, Finck BN, Mittendorfer B. Sexually dimorphic effect of aging on skeletal muscle protein synthesis. Biol Sex Differ 2012; 3 (01) 11
65 Smith GI, Yoshino J, Reeds DN. et al. Testosterone and progesterone, but not estradiol, stimulate muscle protein synthesis in postmenopausal women. J Clin Endocrinol Metab 2014; 99 (01) 256-265
66 Kamanga-Sollo E, White ME, Hathaway MR, Weber WJ, Dayton WR. Effect of Estradiol-17beta on protein synthesis and degradation rates in fused bovine satellite cell cultures. Domest Anim Endocrinol 2010; 39 (01) 54-62
67 Ronda AC, Vasconsuelo A, Boland R. 17β-Estradiol protects mitochondrial functions through extracellular-signal-regulated kinase in C2C12 muscle cells. Cell Physiol Biochem 2013; 32 (04) 1011-1023
68 La Colla A, Vasconsuelo A, Boland R. Estradiol exerts antiapoptotic effects in skeletal myoblasts via mitochondrial PTP and MnSOD. J Endocrinol 2013; 216 (03) 331-341
69 Vasconsuelo A, Milanesi L, Boland R. Participation of HSP27 in the antiapoptotic action of 17beta-estradiol in skeletal muscle cells. Cell Stress Chaperones 2010; 15 (02) 183-192
70 Boland R, Vasconsuelo A, Milanesi L, Ronda AC, de Boland AR. 17Beta-estradiol signaling in skeletal muscle cells and its relationship to apoptosis. Steroids 2008; 73 (9-10): 859-863
71 Stupka N, Lowther S, Chorneyko K, Bourgeois JM, Hogben C, Tarnopolsky MA. Gender differences in muscle inflammation after eccentric exercise. J Appl Physiol (1985) 2000; 89 (06) 2325-2332
72 Kerksick C, Taylor IV L, Harvey A, Willoughby D. Gender-related differences in muscle injury, oxidative stress, and apoptosis. Med Sci Sports Exerc 2008; 40 (10) 1772-1780
73 Kangas R, Pöllänen E, Rippo MR. et al. Circulating miR-21, miR-146a and Fas ligand respond to postmenopausal estrogen-based hormone replacement therapy—a study with monozygotic twin pairs. Mech Ageing Dev 2014; 143-144: 1-8
74 Wang H, Alencar A, Lin M. et al. Activation of GPR30 improves exercise capacity and skeletal muscle strength in senescent female Fischer344 × Brown Norway rats. Biochem Biophys Res Commun 2016; 475 (01) 81-86
75 Hershko A, Ciechanover A, Varshavsky A. Basic medical research award. The ubiquitin system. Nat Med 2000; 6 (10) 1073-1081
76 Svensson J, Movérare-Skrtic S, Windahl S, Swanson C, Sjögren K. Stimulation of both estrogen and androgen receptors maintains skeletal muscle mass in gonadectomized male mice but mainly via different pathways. J Mol Endocrinol 2010; 45 (01) 45-57
77 Dieli-Conwright CM, Spektor TM, Rice JC, Sattler FR, Schroeder ET. Influence of hormone replacement therapy on eccentric exercise induced myogenic gene expression in postmenopausal women. J Appl Physiol (1985) 2009; 107 (05) 1381-1388
78 Pöllänen E, Ronkainen PH, Suominen H. et al. Muscular transcriptome in postmenopausal women with or without hormone replacement. Rejuvenation Res 2007; 10 (04) 485-500
79 Ogawa M, Yamaji R, Higashimura Y. et al. 17β-Estradiol represses myogenic differentiation by increasing ubiquitin-specific peptidase 19 through estrogen receptor α. J Biol Chem 2011; 286 (48) 41455-41465
80 Wing SS. Deubiquitinating enzymes in skeletal muscle atrophy—an essential role for USP19. Int J Biochem Cell Biol 2016; 79: 462-468
81 Lee JH, Lee MJ. Emerging roles of the ubiquitin-proteasome system in the steroid receptor signaling. Arch Pharm Res 2012; 35 (03) 397-407
82 Tiidus PM. Benefits of estrogen replacement for skeletal muscle mass and function in post-menopausal females: evidence from human and animal studies. Eurasian J Med 2011; 43 (02) 109-114
83 Greising SM, Baltgalvis KA, Lowe DA, Warren GL. Hormone therapy and skeletal muscle strength: a meta-analysis. J Gerontol A Biol Sci Med Sci 2009; 64 (10) 1071-1081
84 Morley JE, Baumgartner RN, Roubenoff R, Mayer J, Nair KS. Sarcopenia. J Lab Clin Med 2001; 137 (04) 231-243
85 Brown M. Skeletal muscle and bone: effect of sex steroids and aging. Adv Physiol Educ 2008; 32 (02) 120-126
86 Widrick JJ, Maddalozzo GF, Lewis D. et al. Morphological and functional characteristics of skeletal muscle fibers from hormone-replaced and nonreplaced postmenopausal women. J Gerontol A Biol Sci Med Sci 2003; 58 (01) 3-10
87 Jørgensen SB, Richter EA, Wojtaszewski JF. Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J Physiol 2006; 574 (Pt 1): 17-31
88 Osler ME, Zierath JR. Adenosine 5′-monophosphate-activated protein kinase regulation of fatty acid oxidation in skeletal muscle. Endocrinology 2008; 149 (03) 935-941
89 Campbell SE, Febbraio MA. Effect of the ovarian hormones on GLUT4 expression and contraction-stimulated glucose uptake. Am J Physiol Endocrinol Metab 2002; 282 (05) E1139-E1146
90 Moran AL, Warren GL, Lowe DA. Removal of ovarian hormones from mature mice detrimentally affects muscle contractile function and myosin structural distribution. J Appl Physiol (1985) 2006; 100 (02) 548-559
91 Wohlers LM, Sweeney SM, Ward CW, Lovering RM, Spangenburg EE. Changes in contraction-induced phosphorylation of AMP-activated protein kinase and mitogen-activated protein kinases in skeletal muscle after ovariectomy. J Cell Biochem 2009; 107 (01) 171-178
92 Qaisar R, Renaud G, Hedstrom Y. et al. Hormone replacement therapy improves contractile function and myonuclear organization of single muscle fibres from postmenopausal monozygotic female twin pairs. J Physiol 2013; 591 (09) 2333-2344
93 Wattanapermpool J, Reiser PJ. Differential effects of ovariectomy on calcium activation of cardiac and soleus myofilaments. Am J Physiol 1999; 277 (02) H467-H473
94 Gregorich ZR, Peng Y, Cai W. et al. Top-down targeted proteomics reveals decrease in myosin regulatory light-chain phosphorylation that contributes to sarcopenic muscle dysfunction. J Proteome Res 2016; 15 (08) 2706-2716
95 Lai S, Collins BC, Colson BA, Kararigas G, Lowe DA. Estradiol modulates myosin regulatory light chain phosphorylation and contractility in skeletal muscle of female mice. Am J Physiol Endocrinol Metab 2016; 310 (09) E724-E733
96 Miller MS, Bedrin NG, Callahan DM. et al. Age-related slowing of myosin actin cross-bridge kinetics is sex specific and predicts decrements in whole skeletal muscle performance in humans. J Appl Physiol (1985) 2013; 115 (07) 1004-1014
97 Soucek O, Lebl J, Matyskova J. et al. Muscle function in Turner syndrome: normal force but decreased power. Clin Endocrinol (Oxf) 2015; 82 (02) 248-253
98 Nijhuis-Van der Sanden MW, Van Asseldonk EH, Eling PA, Van Galen GP. Slow motor performance in girls with Turner syndrome is not related to increased neuromotor noise. Mot Contr 2003; 7 (02) 111-133
99 Milde K, Tomaszewski P, Stupnicki R. Physical fitness of schoolgirls with Turner syndrome. Pediatr Exerc Sci 2013; 25 (01) 27-42
100 Ronkainen PH, Kovanen V, Alén M. et al. Postmenopausal hormone replacement therapy modifies skeletal muscle composition and function: a study with monozygotic twin pairs. J Appl Physiol (1985) 2009; 107 (01) 25-33
101 Javed AA, Mayhew AJ, Shea AK, Raina P. Association between hormone therapy and muscle mass in postmenopausal women: a systematic review and meta-analysis. JAMA Netw Open 2019; 2 (08) e1910154-e1910154
102 Kim S-W, Kim R. The association between hormone therapy and sarcopenia in postmenopausal women: the Korea National Health and Nutrition Examination Survey, 2008-2011. Menopause 2020; 27 (05) 506-511
103 Meeuwsen IB, Samson MM, Duursma SA, Verhaar HJ. Muscle strength and tibolone: a randomised, double-blind, placebo-controlled trial. BJOG 2002; 109 (01) 77-84
104 Dobs AS, Nguyen T, Pace C, Roberts CP. Differential effects of oral estrogen versus oral estrogen-androgen replacement therapy on body composition in postmenopausal women. J Clin Endocrinol Metab 2002; 87 (04) 1509-1516
105 Davis SR, McCloud P, Strauss BJ, Burger H. Testosterone enhances estradiol's effects on postmenopausal bone density and sexuality. Maturitas 2008; 61 (1-2): 17-26
106 Zuckerman-Levin N, Frolova-Bishara T, Militianu D, Levin M, Aharon-Peretz J, Hochberg Z. Androgen replacement therapy in Turner syndrome: a pilot study. J Clin Endocrinol Metab 2009; 94 (12) 4820-4827
107 Dalton JT, Barnette KG, Bohl CE. et al. The selective androgen receptor modulator GTx-024 (enobosarm) improves lean body mass and physical function in healthy elderly men and postmenopausal women: results of a double-blind, placebo-controlled phase II trial. J Cachexia Sarcopenia Muscle 2011; 2 (03) 153-161
108 Papanicolaou DA, Ather SN, Zhu H. et al. A phase IIA randomized, placebo-controlled clinical trial to study the efficacy and safety of the selective androgen receptor modulator (SARM), MK-0773 in female participants with sarcopenia. J Nutr Health Aging 2013; 17 (06) 533-543
109 Ari M, Bakalov VK, Hill S, Bondy CA. The effects of growth hormone treatment on bone mineral density and body composition in girls with turner syndrome. J Clin Endocrinol Metab 2006; 91 (11) 4302-4305
110 Watson K, Baar K. mTOR and the health benefits of exercise. Semin Cell Dev Biol 2014; 36: 130-139
111 Xiang X, Zhao J, Xu G, Li Y, Zhang W. mTOR and the differentiation of mesenchymal stem cells. Acta Biochim Biophys Sin (Shanghai) 2011; 43 (07) 501-510
112 Osawa Y, Oguma Y. Effects of resistance training with whole-body vibration on muscle fitness in untrained adults. Scand J Med Sci Sports 2013; 23 (01) 84-95
113 Zamboni M, Mazzali G, Fantin F, Rossi A, Di Francesco V. Sarcopenic obesity: a new category of obesity in the elderly. Nutr Metab Cardiovasc Dis 2008; 18 (05) 388-395
114 Binder EF, Yarasheski KE, Steger-May K. et al. Effects of progressive resistance training on body composition in frail older adults: results of a randomized, controlled trial. J Gerontol A Biol Sci Med Sci 2005; 60 (11) 1425-1431
115 Watson SL, Weeks BK, Weis LJ, Harding AT, Horan SA, Beck BR. High-intensity resistance and impact training improves bone mineral density and physical function in postmenopausal women with osteopenia and osteoporosis: the LIFTMOR randomized controlled trial. J Bone Miner Res 2018; 33 (02) 211-220
116 Gianoudis J, Bailey CA, Ebeling PR. et al. Effects of a targeted multimodal exercise program incorporating high-speed power training on falls and fracture risk factors in older adults: a community-based randomized controlled trial. J Bone Miner Res 2014; 29 (01) 182-191
117 Winters-Stone KM, Dobek J, Nail LM. et al. Impact + resistance training improves bone health and body composition in prematurely menopausal breast cancer survivors: a randomized controlled trial. Osteoporos Int 2013; 24 (05) 1637-1646
118 Sherrington C, Fairhall N, Wallbank G. et al. Exercise for preventing falls in older people living in the community: an abridged Cochrane systematic review. Br J Sports Med 2020; 54 (15) 885-891
119 Mikami Y, Amano J, Kawamura M. et al. Whole-body vibration enhances effectiveness of “locomotion training” evaluated in healthy young adult women. J Phys Ther Sci 2019; 31 (11) 895-900
120 Lai CC, Tu YK, Wang TG, Huang YT, Chien KL. Effects of resistance training, endurance training and whole-body vibration on lean body mass, muscle strength and physical performance in older people: a systematic review and network meta-analysis. Age Ageing 2018; 47 (03) 367-373
121 Hardee JP, Lynch GS. Current pharmacotherapies for sarcopenia. Expert Opin Pharmacother 2019; 20 (13) 1645-1657
122 Becker C, Lord SR, Studenski SA. et al; STEADY Group. Myostatin antibody (LY2495655) in older weak fallers: a proof-of-concept, randomised, phase 2 trial. Lancet Diabetes Endocrinol 2015; 3 (12) 948-957
123 Rooks D, Praestgaard J, Hariry S. et al. Treatment of sarcopenia with bimagrumab: results from a phase II, randomized, controlled, proof-of-concept study. J Am Geriatr Soc 2017; 65 (09) 1988-1995
124 Garbers C, Heink S, Korn T, Rose-John S. Interleukin-6: designing specific therapeutics for a complex cytokine. Nat Rev Drug Discov 2018; 17 (06) 395-412
125 Onder G, Penninx BW, Balkrishnan R. et al. Relation between use of angiotensin-converting enzyme inhibitors and muscle strength and physical function in older women: an observational study. Lancet 2002; 359 (9310): 926-930
126 Di Bari M, van de Poll-Franse LV, Onder G. et al; Health, Aging and Body Composition Study. Antihypertensive medications and differences in muscle mass in older persons: the Health, Aging and Body Composition Study. J Am Geriatr Soc 2004; 52 (06) 961-966
127 Pahor M, Anton SD, Beavers DP. et al; The ENRGISE Pilot Randomized Clinical Trial. Effect of losartan and fish oil on plasma IL-6 and mobility in older persons. J Gerontol A Biol Sci Med Sci 2019; 74 (10) 1612-1619
128 Delafontaine P, Yoshida T. The renin-angiotensin system and the biology of skeletal muscle: mechanisms of muscle wasting in chronic disease states. Trans Am Clin Climatol Assoc 2016; 127: 245-258
129 Passos-Silva DG, Verano-Braga T, Santos RA. Angiotensin-(1-7): beyond the cardio-renal actions. Clin Sci (Lond) 2013; 124 (07) 443-456
130 Zhou G, Myers R, Li Y. et al. Role of AMP-activated protein kinase in mechanism of metformin action. J Clin Invest 2001; 108 (08) 1167-1174
131 Long DE, Peck BD, Martz JL. et al. Metformin to augment strength training effective response in seniors (MASTERS): study protocol for a randomized controlled trial. Trials 2017; 18 (01) 192
132 Panay N, Fenton A. Premature ovarian insufficiency: working towards an international database. Climacteric 2012; 15 (04) 295-296
133 Janssen I, Heymsfield SB, Ross R. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 2002; 50 (05) 889-896
134 Newman AB, Kupelian V, Visser M. et al; Health ABC Study Investigators. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc 2003; 51 (11) 1602-1609
135 Cawthon PM. Assessment of lean mass and physical performance in sarcopenia. J Clin Densitom 2015; 18 (04) 467-471
136 Kuchnia AJ, Binkley N. Diagnosis of osteosarcopenia—imaging. In: Duque G. ed. Osteosarcopenia: Bone, Muscle and Fat Interactions. Cham: Springer International Publishing; 2019: 243-263
137 Messina C, Maffi G, Vitale JA, Ulivieri FM, Guglielmi G, Sconfienza LM. Diagnostic imaging of osteoporosis and sarcopenia: a narrative review. Quant Imaging Med Surg 2018; 8 (01) 86-99
138 Boutin RD, Yao L, Canter RJ, Lenchik L. Sarcopenia: current concepts and imaging implications. AJR Am J Roentgenol 2015; 205 (03) W255-W266
139 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 (05) 1011-1014
140 Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr 2000; 71 (04) 885-892
141 Kyle UG, Bosaeus I, De Lorenzo AD. et al; Composition of the ESPEN Working Group. Bioelectrical impedance analysis—Part I: Review of principles and methods. Clin Nutr 2004; 23 (05) 1226-1243
142 Morley JE, Abbatecola AM, Argiles JM. et al; Society on Sarcopenia, Cachexia and Wasting Disorders Trialist Workshop. Sarcopenia with limited mobility: an international consensus. J Am Med Dir Assoc 2011; 12 (06) 403-409
143 Anonymous. Bioelectrical impedance analysis in body composition measurement. Proceedings of a National Institutes of Health Technology Assessment Conference. Bethesda, Maryland, December 12-14, 1994. Am J Clin Nutr 1996; 64 (3, Suppl): 387S-532S
144 Shankaran M, Czerwieniec G, Fessler C. et al. Dilution of oral D3-creatine to measure creatine pool size and estimate skeletal muscle mass: development of a correction algorithm. J Cachexia Sarcopenia Muscle 2018; 9 (03) 540-546
145 Cawthon PM, Blackwell T, Cummings SR. et al; Osteoporotic Fractures in Men (MrOS) Study Research Group.. Muscle mass assessed by D3-creatine dilution method and incident self-reported disability and mortality in a prospective observational study of community dwelling older men. J Gerontol A Biol Sci Med Sci 2020; glaa111
146 Cooper C, Fielding R, Visser M. et al. Tools in the assessment of sarcopenia. Calcif Tissue Int 2013; 93 (03) 201-210
147 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
148 Abdalla PP, Dos Santos Carvalho A, Dos Santos AP. et al. Cut-off points of knee extension strength allometrically adjusted to identify sarcopenia risk in older adults: a cross-sectional study. Arch Gerontol Geriatr 2020; 89: 104100
149 Beaudart C, McCloskey E, Bruyère O. et al. Sarcopenia in daily practice: assessment and management. BMC Geriatr 2016; 16 (01) 170
150 Alcazar J, Kamper RS, Aagaard P. et al. Relation between leg extension power and 30-s sit-to-stand muscle power in older adults: validation and translation to functional performance. Sci Rep 2020; 10 (01) 16337
151 Cesari M, Kritchevsky SB, Newman AB. et al; Health, Aging and Body Composition Study. Added value of physical performance measures in predicting adverse health-related events: results from the Health, Aging And Body Composition Study. J Am Geriatr Soc 2009; 57 (02) 251-259
152 Bergland A, Strand BH. Norwegian reference values for the Short Physical Performance Battery (SPPB): the Tromsø Study. BMC Geriatr 2019; 19 (01) 216
153 Podsiadlo D, Richardson S. The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 1991; 39 (02) 142-148
154 Vestergaard S, Patel KV, Bandinelli S, Ferrucci L, Guralnik JM. Characteristics of 400-meter walk test performance and subsequent mortality in older adults. Rejuvenation Res 2009; 12 (03) 177-184
155 Bean JF, Kiely DK, LaRose S, Alian J, Frontera WR. Is stair climb power a clinically relevant measure of leg power impairments in at-risk older adults?. Arch Phys Med Rehabil 2007; 88 (05) 604-609

Supplementary Material

Supplementary Material (PDF)