Clin Osteol 2017; 22(1): 9-18
Modern diagnosis of osteoporosis and assessment of fracture risk in girls with Turner syndromeOriginal contributions
This condition is also associated with osteoporosis and frequent fractures. The aims were to determine volumetric bone mineral density and bone strength, to measure muscle function, to evaluate their relationships and differences from healthy controls, and to test associations with the duration of hormone replacement therapy and the incidence of fractures.
Patients, material and methods: Included in the study were 67 (39) girls with Turner syndrome. Volumetric bone mineral density (vBMD) and bone strength parameters at the radius were determined by peripheral quantitative computed tomography (pQCT) and compared with the published reference norms. For measurements at the tibia/fibula, a control group of 67 healthy girls was included. Trabecular BMD and bone strength were measured at the metaphysis (bone strength index, BSI) and diaphysis (strength strain index, SSI) of the tibia using pQCT. The impact of TS on the muscle-bone unit was tested by multiple linear regression.
Results: Trabecular vBMD at the radius was significantly reduced in TS (mean Z-score 0.7 + 1.3; p < 0.001) compared to the normal values; cortical vBMD adjusted for cortical thickness was increased (Z-score 1.1 + 1.0; p < 0.001). TS was not significantly associated with Fmax after adjustment for age, height and weight; however, there were negative associations with trabecular vBMD (coefficient -0.22 + 0.045, p < 0.001) and both bone strength indices at the tibia (coefficients -0.24 + 0.07, p < 0.001 for BSI and -0.096 + 0.035, p < 0.01 for SSI). With identical Fmax, BSI and SSI were reduced by 18 % (p < 0.01) and 7 % (p = 0.027), respectively, in TS patients as compared with healthy girls. Neither therapy nor the incidence of fractures had significant effects on the tested muscle and bone parameters.
Conclusion: In girls with TS, the same muscle strength is associated with lower bone strength as compared with their healthy counterparts. This is probably due to changes in the sensitivity of bones to mechanical loading.
Keywords: Turnerův syndrom, denzita kostního minerálu, svalové funkce, periferní kvantitativní počítačová tomografie, mechanografie ~ SUMMARY
Published: June 11, 2017 Show citation
References
- Stochholm K, Juul S, Juel K, Naeraa RW, Gravholt CH. Prevalence, cidence, diagnostic delay, and mortality in Turner syndrome. J Clin Endocrinol Metab 2006;91:3897-3902.
Go to original source... - Gravholt CH, Juul S, Naeraa RW, Hansen J. Morbidity in Turner drome. J Clin Epidemiol 1998;51:147-158.
Go to original source... - Gravholt CH, Vestergaard P, Hermann AP, Mosekilde L, Brixen K, Christiansen JS. Increased fracture rates in Turner's syndrome: a na tionwide questionnaire survey. Clin Endocrinol (Oxf) 2003;59:89-96.
Go to original source... - Gravholt CH, Lauridsen AL, Brixen K, Mosekilde L, Heickendorff L, Christiansen JS. Marked disproportionality in bone size and mineral, and distinct abnormalities in bone markers and calcitropic hormones in adult turner syndrome Metab 2002;87:2798-2808.
Go to original source... - Bakalov VK, Chen ML, Baron J, Hanton LB, Reynolds JC, Strata CA, Axelrod LE, Bondy CA. Bone mineral density and fractures in Turner syndrome. Am J Med 2003;115:259-264.
Go to original source... - Lage AZ, Brandao CA, Mendes JR, Huayllas MK, Liberman B, Mendonca BB, Costa EM, Verreschi IT, Lazaretti-Castro M. High de gree of discordance between three-dimensional and two-dimensio lumbar spine bone mineral density in Turner's syndrome. J Clin Densitom 2005;8:461466.
Go to original source... - Carrascosa A, Gussinye M, Terradas P, Yeste D, Audi L, Vicens-Ca E. Spontaneous, but not induced, puberty permits adequate bone mass acquisition in adolescent Turner syndrome patients. JBone Miner Res 2000;15:2005-2010.
Go to original source... - Gussinye M, Terrades P, Yeste D, Vicens-Calvet E, Carrascosa A. Low areal bone mineral density values in adolescents and young adult tur ner syndrome patients increase aft therapy. Horm Res 2000;54:131-135.
Go to original source... - Hanton L, Axelrod L, Bakalov V, Bondy CA. The importance o gen replacement in young women with Turner syndrome. J Womens Health (Larchmt) 2003;12:971-977.
Go to original source... - Rao E, Weiss B, Fukami M, Rump A, Niesler B, Mertz A, Binder G, Kirsch S, Winkelmann M, Nordsiek G, Heinrich U, Breuning MH, Ranke MB, Rosenthal A, Ogata T, Rappold GA. Pseudoautosomal deletions encompassing a novel homeobox gene cau se growth failure in idiopathic short stature and Turner syndrome Genet 1997;16:54-63.
- Ross JL, Stefanatos GA, Kushner H, Bondy C, Nelson L, Zinn A, Roeltgen D. The effect of genetic differences and ovarian failure: in cognitive function in adult women with premature ovarian failure ver sus turner syndrome. J Clin Endocrinol Metab 2004;89:1817-1822.
Go to original source... - Zinn AR, Roeltgen D, Stefanatos G, Ramos P, Elder FF, Kushner H, Kowal K, Ross JL. A Turner syndrome neurocognitive phenotype maps to Xp22.3. Behav Brain Funct 2007;3:24.
Go to original source... - Souček O, Šumník Z, Lébl J. Kostní denzita a parametry pevnosti kos ti: vztah k riziku fraktur u dětí. Diabetologie, endokrinologie, m lizmus a výživa 2009;12:20-27.
- Weatherholt AM, Avin KG, Hurd AL, Cox JL, Marberry ST, Santoni BG, Warden SJ. Peripheral Quantitative Computed Tomography Predicts Humeral Diaphysis Torsional Mechanical Properties With Good Short-Term Precision. J Clin Densitom 2015;18:551-559.
Go to original source... - Rauch F, Schoenau E. Peripheral quantitative computed tomography of the distal radius in young subjects - new reference data and inter tion of results. J Musculoskelet Neuronal Interact 2005;5:119-126.
- Rauch F, Schoenau E. Peripheral quantitative computed tomography of the proximal radius in young subjects - new reference data and pretation of results. J Musculoskelet Neuronal Interact 2008;8: 217-226.
- Moyer-Mileur LJ, Quick JL, Murray MA. Peripheral quantitative c puted tomography of the tibia: pediatric reference values. J Clin Densitom 2008;11:283-294.
Go to original source... - Frost HM. Muscle, bone, and the Utah paradigm: a 1999 overview. Med Sci Sports Exerc 2000;32:911-917.
Go to original source... - Schiessl H, Frost HM, Jee WS. Estrogen and bone-muscle stren mass relationships. Bone 1998;22:1-6.
Go to original source... - Schoenau E. From mechanostat theory to development of the "Functional Muscle-Bone-Unit". J Musculoskelet Neuronal Interact 2005;5:232-238.
- Frost HM. The mechanostat: a proposed pathogenic mechanism of teoporoses and the bone mass effects of mechanical and nonmechani cal agents. Bone Miner 1987;2:73-85.
- Anliker E, Toigo M. Functional assessment of the muscle-bone u in the lower leg. J Musculoskelet Neuronal Interact 2012;12:46-55.
- Hebert LJ, Maltais DB, Lepage C, Saulnier J, Crete M, Perron M. Isometric muscle strength in youth assessed by hand-held dynamome try: a feasibility, reliability, and validity study. Pediatr Phys Ther 2 23:289-299.
- Rauch F, Neu CM, Wassmer G, Beck B, Rieger-Wettengl G, Rietschel E, Manz F, Schoenau E. Muscle analysis by measurement of ma ximal isometric grip force: new reference data and clinical applications in pediatrics. Pediatr Res 2002;51:505-510.
Go to original source... - Anliker E, Rawer R, Boutellier U, Toigo M. Maximum ground reaction force in relation to tibial bone mass in children and adults. Med Sci Sports Exerc 2011;43:2102-2109.
Go to original source... - Veilleux LN, Rauch F. Reproducibility of jumping mechanography in healthy children and adults. J Musculoskelet Neuronal Interact 2010; 10:256-266.
- Busche P, Rawer R, Rakhimi N, Lang I, Martin DD. Mechanography in childhood: references for force and power in counter movement jumps and chair rising tests. J Musculoskelet Neuronal Interact 2013; 13:213-226.
Go to original source... - Lang I, Busche P, Rakhimi N, Rawer R, Martin DD. Mechanography in childhood: references for grip force, multiple one-leg hopping force and whole body stiffness. J Musculoskelet Neuronal Interact 2013; 13:227-235.
- Sumnik Z, Matyskova J, Hlavka Z, Durdilova L, Soucek O, Zem kova D. Reference data for jumping mechanography in healthy child ren and adolescents aged 6-18 years. J Musculoskelet Neuronal Interact 2013;13:297-311.
- Kobzova J, Vignerova J, Blaha P, Krejcovsky L, Riedlova J. The 6th tionwide anthropological survey of children and adolescents in the Czech Republic in 2001. Cent Eur J Public Health 2004;12:126-130.
- Saenger P, Wikland KA, Conway GS, Davenport M, Gravholt CH, Hintz R, Hovatta O, Hultcrantz M, Landin-Wilhelmsen K, Lin A, Lippe B, Pasquino AM, Ranke MB, Rosenfeld R, Silberbach M. Recommendations for the diagnosis and management of Turner syn drome. J Clin Endocrinol Metab 2001;86:3061-3069.
Go to original source... - Kontulainen S, Sievanen H, Kannus P, Pasanen M, Vuori I. Effect of long-term impact-loading on mass, size, and estimated strength of hu merus and radius of female racquet-sports players: a peripheral quanti tative computed tomography study between young and old starters and controls. J Bone Miner Res 2003;18:352-359.
Go to original source... - R Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL. http://www.R-project.org/
- Ross JL, Long LM, Feuillan P, Cassorla F, Cutler GB, Jr. Normal bo ne density of the wrist and spine and increased wrist fractures in with Turner's syndrome. J Clin Endocrinol Metab 1991;73:355-359.
Go to original source... - Shaw NJ, Rehan VK, Husain S, Marshall T, Smith CS Bone mineral density in Turner's syndrome-a longitudinal study. Clin Endocrinol (Oxf) 1997;47:367-370.
Go to original source... - Nanao K, Tsuchiya Y, Kotoh S, Hasegawa Y. Low vertebral cancell bone density in peripubertal girls with Turner's syndrome and boys with hypogonadism. J Pediatr Endocrinol Metab 2002;15:1537-1542.
Go to original source... - Bechtold S, Rauch F, Noelle V, Donhauser S, Neu CM, Schoenau E, Schwarz HP. Musculoskeletal analyses of the forearm in young women with Turner syndrome: a study using peripheral quantit tomography. J Clin Endocrinol Metab 2001;86:5819-5823.
Go to original source... - Holroyd CR, Davies JH, Taylor P, Jameson K, Rivett C, Cooper C, Dennison EM. Reduced cortical bone density with normal trabecular bone density 21:2093-2099.
- Bakalov VK, Axelrod L, Baron J, Hanton L, Nelson LM, Reynolds JC, Hill S, Troendle J, Bondy CA. Selective reduction in cortical bone neral density in turner syndrome independent of ovarian hormone de ficiency. J Clin Endocrinol Metab 2003;88:5717-5722.
Go to original source... - Schoenau E, Neu CM, Rauch F, Manz F. Gender-specific pubertal changes in volumetric corti dius. Bone 2002;31:110-113.
Go to original source... - Rittweger J, Michaelis I, Giehl M, Wusecke P, Felsenberg D. Adjusting for the partial volume effect in cortical bone analyses of pQCT imag J Musculoskelet Neuronal Interact 2004;4:436-441.
- Hansen S, Brixen K, Gravholt CH. Compromised trabecular microar chitecture and lower finite element estimates of radius and tibia bone strength in adults with turner syndrome: a cross-sectional study u high-resolution-pQCT. J Bone Miner Res 2012;27:1794-1803.
Go to original source... - Soucek O, Lebl J, Matyskova J, Snajderova M, Kolouskova S, Pruhova S, Hlavka Z, Sumnik Z. Muscle function in Turner syndrome: normal force but decreased power. Clin Endocrinol (Oxf) 2015; 82:248-253.
Go to original source... - Milde K, Tomaszewski P, Stupnicki R. Physical fitn with Turner syndrome. Pediatr Exerc Sci 2013;25:27-42.
Go to original source... - Clark C, Klonoff H, Hayden M. Regional cerebral g in Turner syndrome. Can J Neurol Sci 1990;17:140-144.
Go to original source... - Ackerman KE, Pierce L, Guereca G, Slattery M, Lee H, Goldstein M, Misra M. Hip structural analysis in adolescent and young adu menorrheic and eumenorrheic athletes and nonathletes. J Clin Endocrinol Metab 2013;98:1742-1749.
Go to original source... - Torres-Santiago L, Mericq V, Taboada M, Unanue N, Klein KO, Singh R, Hossain J, Santen RJ, Ross JL, Mauras N. Metabolic effects of oral versus transdermal 17beta-estradiol (E(2)): a randomized clinical in girls with Turner syndrome. J Clin Endocrinol Metab 2013;98: 2716-2724.
Go to original source... - Khastgir G, Studd JW, Fox SW, Jones J, Alaghband-Zadeh J, Chow JW. A longitudinal study of the effect of subcutaneous estro cement on bone in young women with Turner's syndrome. J Bone Miner Res 2003;18:925-932.
Go to original source... - Eser P, Frotzler A, Zehnder Y, Wick L, Knecht H, Denoth J, Schiessl H. Relationship between the duration of paralysis and bone struc a pQCT study of spinal cord injured individuals. Bone 2004;34: 869-880.
Go to original source... - Soucek O, Zapletalova J, Zemkova D, Snajderova M, Novotna D, Hirschfeldova K, Plasilova I, Kolouskova S, Rocek M, Hlavka Z, Lebl J, Sumnik Z. Prepubertal girls with Turner syndrome and child ren with isolated SHOX deficiency have similar bone radius. J Clin Endocrinol Metab 2013;98:E1241-1247.
Go to original source... - Soucek O, Lebl J, Zapletalova J, Novotna D, Plasilova I, Kolous Zemkova D, Rocek M, Hlavka Z, Hirschfeldova K, Sumnik Z. Bone geometry and volumetric bone density at the radius in patients with isolated SHOX deficiency. Exp Clin Endocrinol Diabetes 2013;121: 109-114.
Go to original source... - Munns CJ, Haase HR, Crowther LM, Hayes MT, Blaschke R, Rappold G, Glass IA, Batch JA Expression of SHOX in human fetal and childhood growth plate. J Clin Endocrinol Metab 2004;89: 4130-4135.
Go to original source...

