, Volume 13, Issue 3, pp 353–360 | Cite as

Usefulness of phalangeal quantitative ultrasound in identifying reduced bone mineral status and increased fracture risk in adolescents with Turner syndrome

  • Francesco Vierucci
  • Marta Del Pistoia
  • Paola Erba
  • Giovanni Federico
  • Giuseppe Saggese
Research paper


OBJECTIVE. Bone health is a major concern in patients with Turner syndrome (TS). There are few studies assessing bone mineral status in TS adolescents and none have reported a clear relationship with the risk of fracture. We assessed bone mineral status at three different skeletal sites by two different densitometric techniques in a group of TS adolescents. DESIGN. In 24 TS adolescents (17.1 ± 3.1 years) we evaluated lumbar and femoral volumetric bone mineral density (vBMD) with dual energy X-ray absorptiometry (DXA), amplitude-dependent speed of sound (AD-SoS) and bone transmission time (BTT) with phalangeal quantitative ultrasound (QUS). RESULTS. Mean lumbar vBMD Z-score was normal, while mean femoral vBMD, ADSoS and BTT Z-score were reduced. 8/24 (33.3%) and 13/24 (54.2%) girls had AD-SoS and BTT ≤-2 Z-score, respectively, while lumbar vBMD and femoral vBMD were ≤-2 Z-score only in 2/24 (8.4%) and 1/24 (4.2%) patients. Overall, we documented 15 fractures (three pathological) in 8 girls. Patients who reported at least one fracture had lower AD-SoS and BTT Z-score values than fracture-free girls. The presence of a value of BTT ≤-2.0 Z-score was associated with a significant OR of positive history of fracture of 11.67 (χ2 = 5.906, p =0.015, C.I. 95% 1.14–119.54). Lumbar and femoral vBMD were not related to fracture risk. CONCLUSIONS. TS adolescents may have impaired bone mineral status in skeletal sites with predominant cortical bone. Phalangeal QUS represents a useful method to identify subjects with increased fracture risk.

Key words

Bone mineral status Dual energy X-ray absorptiometry Quantitative ultrasound Turner syndrome 


  1. 1.
    Turner HH, 1938 A syndrome of infantilism, congenital webbed neck, and cubitus valgus. Endocrinology 23: 566–574.CrossRefGoogle Scholar
  2. 2.
    Shore RM, Chesney RW, Mazess RB, Rose PG, Bargman GJ, 1982 Skeletal demineralization in Turner’s syndrome. Calcif Tissue Int 34: 519–522.CrossRefGoogle Scholar
  3. 3.
    Davies MC, Gulekli B, Jacobs HS, 1995 Osteoporosis in Turner’s syndrome and other forms of primary amenorrhoea. Clin Endocrinol 43: 741–746.CrossRefGoogle Scholar
  4. 4.
    Landin-Wilhelmsen K, Bryman I, Windh M, Wilhelmsen L, 1999 Osteoporosis and fractures in Turner syndrome: importance of growth promoting and oestrogen therapy. Clin Endocrinol 51: 497–502.CrossRefGoogle Scholar
  5. 5.
    Pitukcheewanont P, Numbenjapon N, Safani D, Rossmiller S, Gilsanz V, Costin G, 2011 Bone size and density measurements in prepubertal children with Turner syndrome prior to growth hormone therapy. Osteoporos Int 22: 1709–1715.CrossRefGoogle Scholar
  6. 6.
    El-Mansoury M, Barrenäs ML, Bryman I, et al, 2007 Chromosomal mosaicism mitigates stigmata and cardiovascular risk factors in Turner syndrome. Clin Endocrinol (Oxf) 66: 744–751.CrossRefGoogle Scholar
  7. 7.
    Oliveira CS, Alves C, 2011 The role of the SHOX gene in the pathophysiology of Turner syndrome. Endocrinol Nutr 58: 433–442.CrossRefGoogle Scholar
  8. 8.
    Soucek O, Zapletalova J, Zemkova D, et al, 2013 Prepubertal girls with Turner syndrome and children wth isolated SHOX deficiency have similar bone geometry at the radius. J Clin Endocrinol Metab 98: E1241–1247.CrossRefGoogle Scholar
  9. 9.
    Holroyd CR, Davies JH, Taylor P, et al, 2010 Reduced cortical bone density with normal trabecular bone density in girls with Turner syndrome. Osteoporos Int 21: 2093–2099.CrossRefGoogle Scholar
  10. 10.
    Soucek O, Lebl J, Snajderova M, et al, 2011 Bone geometry and volumetric bone mineral density in girls with Turner syndrome of different pubertal stages. Clin Endocrinol (Oxf) 74: 445–452.CrossRefGoogle Scholar
  11. 11.
    Bechtold S, Rauch F, Noelle V, et al, 2001 Musculoskeletal analyses of the forearm in young women with Turner syndrome: a study using peripheral quantitative computed tomography. J Clin Endocrinol Metab 86: 5819–5823.CrossRefGoogle Scholar
  12. 12.
    Mora S, Weber G, Guarneri MP, Nizzoli G, Pasolini D, Chiumello G, 1992 Effect of estrogen replacement therapy on bone mineral content in girls with Turner syndrome. Obstet Gynecol 79: 747–751.PubMedGoogle Scholar
  13. 13.
    Bertelloni S, Cinquanta L, Baroncelli GI, Simi P, Rossi S, Saggese G, 2000 Volumetric bone mineral density in young women with Turner’s syndrome treated with estrogens or estrogens plus growth hormone. Horm Res 53: 72–76.PubMedGoogle Scholar
  14. 14.
    Bakalov VK, Chen ML, Baron J, et al, 2003 Bone mineral density and fractures in Turner syndrome. Am J Med 115: 259–264.CrossRefGoogle Scholar
  15. 15.
    Shaw NJ, Rehan VK, Husain S, Marshall T, Smith CS, 1997 Bone mineral density in Turner’s syndrome — a longitudinal study. Clin Endocrinol (Oxf) 47: 367–370.CrossRefGoogle Scholar
  16. 16.
    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: 153–159.CrossRefGoogle Scholar
  17. 17.
    Högler W, Briody J, Moore B, Garnett S, Lu PW, Cowell CT, 2004 Importance of estrogen on bone health in Turner syndrome: a cross-sectional and longitudinal study using dual-energy X-ray absorptiometry. J Clin Endocrinol Metab 89: 193–199.CrossRefGoogle Scholar
  18. 18.
    Bakalov VK, Van PL, Baron J, Reynolds JC, Bondy CA, 2004 Growth hormone therapy and bone mineral density in Turner syndrome. J Clin Endocrinol Metab 89: 4886–4889.CrossRefGoogle Scholar
  19. 19.
    Aycan Z, Cetinkaya E, Darendeliler F, et al, 2008 The effect of growth hormone treatment on bone mineral density in prepubertal girls with Turner syndrome: a multicentre prospective clinical trial. Clin Endocrinol (Oxf) 68: 769–772.CrossRefGoogle Scholar
  20. 20.
    Ari M, Bakalov VK, Hill S, Bondy CA, 2006 The effects of growth hormone treatment on bone mineral density and body composition in girls with Turner syndrome. J Clin Endocrinol Metab 91: 4302–4305.CrossRefGoogle Scholar
  21. 21.
    Ross JL, Long LM, Feuillan P, Cassorla F, Cutler GB Jr, 1991 Normal bone density of the wrist and spine and increased wrist fractures in girls with Turner’s syndrome. J Clin Endocrinol Metab 73: 355–359.CrossRefGoogle Scholar
  22. 22.
    Bakalov VK, Bondy CA, 2008 Fracture risk and bone mineral density in Turner syndrome. Rev Endocr Metab Disord 9: 145–151.CrossRefGoogle Scholar
  23. 23.
    Gravholt CH, Juul S, Naeraa RW, Hansen J, 1998 Morbidity in Turner syndrome. J Clin Epidemiol 51: 147–158.CrossRefGoogle Scholar
  24. 24.
    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: 10–25.CrossRefGoogle Scholar
  25. 25.
    Boot AM, de Ridder MA, Pols HA, Krenning EP, de Muinck Keizer-Schrama SM, 1997 Bone mineral density in children and adolescents: relation to puberty, calcium intake, and physical activity. J Clin Endocrinol Metab 82: 57–62.PubMedGoogle Scholar
  26. 26.
    Kroger H, Kotaniemi A, Vainio P, Alhava E, 1992 Bone densitometry of the spine and femur in children by dual— energy X-ray absorptiometry. Bone Miner 17: 75–85.CrossRefGoogle Scholar
  27. 27.
    Baroncelli GI, Federico G, Vignolo M, et al, 2006 Cross-sectional reference data for phalangeal quantitative ultrasound from early childhood to young-adulthood according to gender, age, skeletal growth, and pubertal development. Bone 39: 159–173.CrossRefGoogle Scholar
  28. 28.
    Cole TJ, Green PJ, 1992 Smoothing reference centile curves: the LMS method and penalized likelihood. Stat Med 11: 1305–1319.CrossRefGoogle Scholar
  29. 29.
    Schoenau E, Saggese G, Peter F, et al, 2004 From bone biology to bone analysis. Horm Res 61: 257–269.CrossRefGoogle Scholar
  30. 30.
    Kroger H, Kotaniemi A, Kroger L, Alhava E, 1993 Development of bone mass and bone density of the spine and femoral neck. A prospective study of 65 children and adolescents. Bone Miner 23: 171–182.CrossRefGoogle Scholar
  31. 31.
    Cadossi R, Canè V, 1996 Pathways of transmission of ultrasound energy through the distal metaphysis of the second phalanx of pigs: an in vitro study. Osteoporos Int 6: 196–206.CrossRefGoogle Scholar
  32. 32.
    Barkmann R, Rohrschneider W, Vierling M, et al, 2002 German paediatric reference data for quantitative transverse transmission ultrasound of finger phalanges. Osteoporos Int 13: 55–61.CrossRefGoogle Scholar
  33. 33.
    Landin LA, 1983 Fracture patterns in children. Analysis of 8,682 fractures with special reference to incidence, etiology and secular changes in a Swedish urban population 1950–1979. Acta Orthop Scand Suppl 202: 1–109.PubMedGoogle Scholar
  34. 34.
    Bertelloni S, Baroncelli GI, Mora S, 2010 Bone health in disorders of sex differentiation. Sex Dev 4: 270–284.CrossRefGoogle Scholar
  35. 35.
    Garden AS, Diver MJ, Fraser WD, 1996 Undiagnosed morbidity in adult women with Turner’s syndrome. Clin Endocrinol (Oxf) 45: 589–593.CrossRefGoogle Scholar
  36. 36.
    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 (Oxf) 59: 89–96.CrossRefGoogle Scholar
  37. 37.
    Han TS, Cadge B, Conway GS, 2006 Hearing impairment and low bone mineral density increase the risk of bone fractures in women with Turner’s syndrome. Clin Endocrinol (Oxf) 65: 643–647.CrossRefGoogle Scholar
  38. 38.
    Zuckerman-Levin N, Yaniv I, Schwartz T, Guttmann H, Hochberg Z, 2007 Normal DXA bone mineral density but frail cortical bone in Turner’s syndrome. Clin Endocrinol (Oxf) 67: 60–64.CrossRefGoogle Scholar
  39. 39.
    Bakalov VK, Axelrod L, Baron J, et al, 2003 Selective reduction in cortical bone mineral density in turner syndrome independent of ovarian hormone deficiency. J Clin Endocrinol Metab 88: 5717–5722.CrossRefGoogle Scholar
  40. 40.
    Hansen S, Brixen K, Gravholt CH, 2012 Compromised trabecular microarchitecture and lower finite element estimates of radius and tibia bone strength in adults with turner syndrome: A cross-sectional study using high-resolution-pQCT. J Bone Miner Res 27: 1794–1803.CrossRefGoogle Scholar
  41. 41.
    Baroncelli GI, 2008 Quantitative ultrasound methods to assess bone mineral status in children: technical characteristics, performance, and clinical application. Pediatr Res 63: 220–228.CrossRefGoogle Scholar
  42. 42.
    Di Iorgi N, Calandra E, Secco A, et al, 2010 Quantitative ultrasound detects bone changes following bone marrow transplantation in pediatric subjects with hematological diseases: a longitudinal study. J Endocrinol Invest 33: 478–482.CrossRefGoogle Scholar
  43. 43.
    Baroncelli GI, Vierucci F, Bertelloni S, Erba P, Zampollo E, Giuca MR, 2013 Pamidronate treatment stimulates the onset of recovery phase reducing fracture rate and skeletal deformities in patients with idiopathic juvenile osteoporosis: comparison with untreated patients. J Bone Miner Metab 31: 533–543.CrossRefGoogle Scholar
  44. 44.
    Mussa A, Bertorello N, Porta F, et al, 2010 Prospective bone ultrasound patterns during childhood acute lymphoblastic leukemia treatment. Bone 46: 1016–1020.CrossRefGoogle Scholar
  45. 45.
    Zywiec J, Pluskiewicz W, Adamczyk P, Skubala A, Gumprecht J, 2012 Phalangeal quantitative ultrasound measurements in chronic hemodialysis patients: a 4-year follow-up. Ultrasound Med Biol 38: 962–971.CrossRefGoogle Scholar
  46. 46.
    Mussa A, Porta F, Baldassarre G, et al, 2012 Phalangeal quantitative ultrasound in 1,719 children and adolescents with bone disorders. Osteoporos Int 23: 1987–1998.CrossRefGoogle Scholar

Copyright information

© Hellenic Endocrine Society 2014

Authors and Affiliations

  • Francesco Vierucci
    • 1
  • Marta Del Pistoia
    • 1
  • Paola Erba
    • 2
  • Giovanni Federico
    • 1
  • Giuseppe Saggese
    • 1
  1. 1.U.O. Pediatria Universitaria, Dipartimento Materno-InfantileAzienda Ospedaliero-Universitaria PisanaPisaItaly
  2. 2.U.O. Medicina Nucleare, Dipartimento di Scienze Oncologiche e RadiologicheAzienda Ospedaliero-Universitaria PisanaPisaItaly

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