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

Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used high‐resolution peripheral quantitative computed tomography (HR‐pQCT) to measure standard morphological parameters of bone geometry and microarchi...

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Published inJournal of bone and mineral research Vol. 27; no. 8; pp. 1794 - 1803
Main Authors Hansen, Stinus, Brixen, Kim, Gravholt, Claus H
Format Journal Article
LanguageEnglish
Published Hoboken Wiley Subscription Services, Inc., A Wiley Company 01.08.2012
Wiley
Oxford University Press
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Online AccessGet full text
ISSN0884-0431
1523-4681
1523-4681
DOI10.1002/jbmr.1624

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Abstract Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used high‐resolution peripheral quantitative computed tomography (HR‐pQCT) to measure standard morphological parameters of bone geometry and microarchitecture, as well as estimated bone strength by finite element analysis (FEA) to assess bone characteristics beyond bone mineral density (BMD) that possibly contribute to the increased risk of fracture. Thirty‐two TS patients (median age 35, range 20–61 years) and 32 healthy control subjects (median age 36, range 19–58 years) matched with the TS participants with respect to age and body‐mass index were studied. A full region of interest (ROI) image analysis and a height‐matched ROI analysis adjusting for differences in body height between groups were performed. Mean bone cross‐sectional area was lower in TS patients in radius (−15%) and tibia (−13%) (both p < 0.01) whereas cortical thickness was higher in TS patients in radius (18%, p < 0.01) but not in tibia compared to controls. Cortical porosity was lower in TS patients at both sites (−32% in radius, −36% in tibia, both p < 0.0001). Trabecular integrity was compromised in TS patients with lower bone volume per tissue volume (BV/TV) (−27% in radius, −22% in tibia, both p < 0.0001), trabecular number (−27% in radius, −12% in tibia, both p < 0.05), and higher trabecular spacing (54% in radius, 23% in tibia, both p < 0.01). In the height‐matched ROI analysis, differences remained significant apart from total area at both sites, cortical thickness in radius, and trabecular number in tibia. FEA estimated failure load was lower in TS patients in both radius (−11%) and tibia (−16%) (both p < 0.01) and remained significantly lower in the height‐matched ROI analysis. Conclusively, TS patients had compromised trabecular microarchitecture and lower bone strength at both skeletal sites, which may partly account for the increased risk of fracture observed in these patients. © 2012 American Society for Bone and Mineral Research.
AbstractList Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used high‐resolution peripheral quantitative computed tomography (HR‐pQCT) to measure standard morphological parameters of bone geometry and microarchitecture, as well as estimated bone strength by finite element analysis (FEA) to assess bone characteristics beyond bone mineral density (BMD) that possibly contribute to the increased risk of fracture. Thirty‐two TS patients (median age 35, range 20–61 years) and 32 healthy control subjects (median age 36, range 19–58 years) matched with the TS participants with respect to age and body‐mass index were studied. A full region of interest (ROI) image analysis and a height‐matched ROI analysis adjusting for differences in body height between groups were performed. Mean bone cross‐sectional area was lower in TS patients in radius (−15%) and tibia (−13%) (both p < 0.01) whereas cortical thickness was higher in TS patients in radius (18%, p < 0.01) but not in tibia compared to controls. Cortical porosity was lower in TS patients at both sites (−32% in radius, −36% in tibia, both p < 0.0001). Trabecular integrity was compromised in TS patients with lower bone volume per tissue volume (BV/TV) (−27% in radius, −22% in tibia, both p < 0.0001), trabecular number (−27% in radius, −12% in tibia, both p < 0.05), and higher trabecular spacing (54% in radius, 23% in tibia, both p < 0.01). In the height‐matched ROI analysis, differences remained significant apart from total area at both sites, cortical thickness in radius, and trabecular number in tibia. FEA estimated failure load was lower in TS patients in both radius (−11%) and tibia (−16%) (both p < 0.01) and remained significantly lower in the height‐matched ROI analysis. Conclusively, TS patients had compromised trabecular microarchitecture and lower bone strength at both skeletal sites, which may partly account for the increased risk of fracture observed in these patients. © 2012 American Society for Bone and Mineral Research.
Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used high-resolution peripheral quantitative computed tomography (HR-pQCT) to measure standard morphological parameters of bone geometry and microarchitecture, as well as estimated bone strength by finite element analysis (FEA) to assess bone characteristics beyond bone mineral density (BMD) that possibly contribute to the increased risk of fracture. Thirty-two TS patients (median age 35, range 20-61 years) and 32 healthy control subjects (median age 36, range 19-58 years) matched with the TS participants with respect to age and body-mass index were studied. A full region of interest (ROI) image analysis and a height-matched ROI analysis adjusting for differences in body height between groups were performed. Mean bone cross-sectional area was lower in TS patients in radius (-15%) and tibia (-13%) (both p<0.01) whereas cortical thickness was higher in TS patients in radius (18%, p<0.01) but not in tibia compared to controls. Cortical porosity was lower in TS patients at both sites (-32% in radius, -36% in tibia, both p<0.0001). Trabecular integrity was compromised in TS patients with lower bone volume per tissue volume (BV/TV) (-27% in radius, -22% in tibia, both p<0.0001), trabecular number (-27% in radius, -12% in tibia, both p<0.05), and higher trabecular spacing (54% in radius, 23% in tibia, both p<0.01). In the height-matched ROI analysis, differences remained significant apart from total area at both sites, cortical thickness in radius, and trabecular number in tibia. FEA estimated failure load was lower in TS patients in both radius (-11%) and tibia (-16%) (both p<0.01) and remained significantly lower in the height-matched ROI analysis. Conclusively, TS patients had compromised trabecular microarchitecture and lower bone strength at both skeletal sites, which may partly account for the increased risk of fracture observed in these patients. © 2012 American Society for Bone and Mineral Research. [PUBLICATION ABSTRACT]
Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used high-resolution peripheral quantitative computed tomography (HR-pQCT) to measure standard morphological parameters of bone geometry and microarchitecture, as well as estimated bone strength by finite element analysis (FEA) to assess bone characteristics beyond bone mineral density (BMD) that possibly contribute to the increased risk of fracture. Thirty-two TS patients (median age 35, range 20-61 years) and 32 healthy control subjects (median age 36, range 19-58 years) matched with the TS participants with respect to age and body-mass index were studied. A full region of interest (ROI) image analysis and a height-matched ROI analysis adjusting for differences in body height between groups were performed. Mean bone cross-sectional area was lower in TS patients in radius (-15%) and tibia (-13%) (both p < 0.01) whereas cortical thickness was higher in TS patients in radius (18%, p < 0.01) but not in tibia compared to controls. Cortical porosity was lower in TS patients at both sites (-32% in radius, -36% in tibia, both p < 0.0001). Trabecular integrity was compromised in TS patients with lower bone volume per tissue volume (BV/TV) (-27% in radius, -22% in tibia, both p < 0.0001), trabecular number (-27% in radius, -12% in tibia, both p < 0.05), and higher trabecular spacing (54% in radius, 23% in tibia, both p < 0.01). In the height-matched ROI analysis, differences remained significant apart from total area at both sites, cortical thickness in radius, and trabecular number in tibia. FEA estimated failure load was lower in TS patients in both radius (-11%) and tibia (-16%) (both p < 0.01) and remained significantly lower in the height-matched ROI analysis. Conclusively, TS patients had compromised trabecular microarchitecture and lower bone strength at both skeletal sites, which may partly account for the increased risk of fracture observed in these patients.Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used high-resolution peripheral quantitative computed tomography (HR-pQCT) to measure standard morphological parameters of bone geometry and microarchitecture, as well as estimated bone strength by finite element analysis (FEA) to assess bone characteristics beyond bone mineral density (BMD) that possibly contribute to the increased risk of fracture. Thirty-two TS patients (median age 35, range 20-61 years) and 32 healthy control subjects (median age 36, range 19-58 years) matched with the TS participants with respect to age and body-mass index were studied. A full region of interest (ROI) image analysis and a height-matched ROI analysis adjusting for differences in body height between groups were performed. Mean bone cross-sectional area was lower in TS patients in radius (-15%) and tibia (-13%) (both p < 0.01) whereas cortical thickness was higher in TS patients in radius (18%, p < 0.01) but not in tibia compared to controls. Cortical porosity was lower in TS patients at both sites (-32% in radius, -36% in tibia, both p < 0.0001). Trabecular integrity was compromised in TS patients with lower bone volume per tissue volume (BV/TV) (-27% in radius, -22% in tibia, both p < 0.0001), trabecular number (-27% in radius, -12% in tibia, both p < 0.05), and higher trabecular spacing (54% in radius, 23% in tibia, both p < 0.01). In the height-matched ROI analysis, differences remained significant apart from total area at both sites, cortical thickness in radius, and trabecular number in tibia. FEA estimated failure load was lower in TS patients in both radius (-11%) and tibia (-16%) (both p < 0.01) and remained significantly lower in the height-matched ROI analysis. Conclusively, TS patients had compromised trabecular microarchitecture and lower bone strength at both skeletal sites, which may partly account for the increased risk of fracture observed in these patients.
Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used high-resolution peripheral quantitative computed tomography (HR-pQCT) to measure standard morphological parameters of bone geometry and microarchitecture, as well as estimated bone strength by finite element analysis (FEA) to assess bone characteristics beyond bone mineral density (BMD) that possibly contribute to the increased risk of fracture. Thirty-two TS patients (median age 35, range 20-61 years) and 32 healthy control subjects (median age 36, range 19-58 years) matched with the TS participants with respect to age and body-mass index were studied. A full region of interest (ROI) image analysis and a height-matched ROI analysis adjusting for differences in body height between groups were performed. Mean bone cross-sectional area was lower in TS patients in radius (-15%) and tibia (-13%) (both p < 0.01) whereas cortical thickness was higher in TS patients in radius (18%, p < 0.01) but not in tibia compared to controls. Cortical porosity was lower in TS patients at both sites (-32% in radius, -36% in tibia, both p < 0.0001). Trabecular integrity was compromised in TS patients with lower bone volume per tissue volume (BV/TV) (-27% in radius, -22% in tibia, both p < 0.0001), trabecular number (-27% in radius, -12% in tibia, both p < 0.05), and higher trabecular spacing (54% in radius, 23% in tibia, both p < 0.01). In the height-matched ROI analysis, differences remained significant apart from total area at both sites, cortical thickness in radius, and trabecular number in tibia. FEA estimated failure load was lower in TS patients in both radius (-11%) and tibia (-16%) (both p < 0.01) and remained significantly lower in the height-matched ROI analysis. Conclusively, TS patients had compromised trabecular microarchitecture and lower bone strength at both skeletal sites, which may partly account for the increased risk of fracture observed in these patients.
Author Brixen, Kim
Hansen, Stinus
Gravholt, Claus H
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  fullname: Gravholt, Claus H
  organization: Department of Endocrinology and Internal Medicine, Aarhus University Hospital, Aarhus, Denmark
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Issue 8
Keywords Chromosomal aberration
Human
Radius
Dysgenesia
High resolution
Genital system
Sexual differentiation disorder
FINITE ELEMENT ANALYSIS
Turner syndrome
Female genital diseases
Osteoarticular system
BONE STRENGTH
Vertebrata
Mammalia
Malformation
Gonad
Tibia
Cross sectional study
HR-PQCT
Adult
Bone
BONE MICROARCHITECTURE
Strength
Language English
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– name: Oxford University Press
References Chiu J, Robinovitch SN. Prediction of upper extremity impact forces during falls on the outstretched hand. J Biomech. 1998 Dec; 31(12): 1169- 76.
Wang Q, Alen M, Nicholson P, Lyytikainen A, Suuriniemi M, Helkala E, Suominen H, Cheng S. Growth patterns at distal radius and tibial shaft in pubertal girls: a 2-year longitudinal study. J Bone Miner Res. 2005 Jun; 20(6): 954- 61.
Olsen BR, Reginato AM, Wang W. Bone development. Annu Rev Cell Dev Biol. 2000; 16: 191- 220.
Melton LJ III, Riggs BL, van Lenthe GH, Achenbach SJ, Muller R, Bouxsein ML, Amin S, Atkinson EJ, Khosla S. Contribution of in vivo structural measurements and load/strength ratios to the determination of forearm fracture risk in postmenopausal women. J Bone Miner Res. 2007; Sep; 22(9): 1442- 8.
Shaw NJ, Rehan VK, Husain S, Marshall T, Smith CS. Bone mineral density in Turner's syndrome-a longitudinal study. Clin Endocrinol (Oxf). 1997 Sep; 47(3): 367- 70.
Schoenau E, Neu CM, Rauch F, Manz F. Gender-specific pubertal changes in volumetric cortical bone mineral density at the proximal radius. Bone. 2002 Jul; 31(1): 110- 3.
Ogata T, Matsuo N, Nishimura G. SHOX haploinsufficiency and overdosage: impact of gonadal function status. J Med Genet. 2001 Jan; 38(1): 1- 6.
Sabherwal N, Blaschke RJ, Marchini A, Heine-Suner D, Rosell J, Ferragut J, Blum WF, Rappold G. A novel point mutation A170P in the SHOX gene defines impaired nuclear translocation as a molecular cause for Leri-Weill dyschondrosteosis and Langer dysplasia. J Med Genet. 2004 Jun; 41(6): e83.
Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S. Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res. 2010 May; 25(5): 983- 93.
Hanson J. Standardization of femur BMD. J Bone Miner Res. 1997 Aug; 12(8): 1316- 7.
Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Rüegsegger P. Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone. 2002 Jun; 30(6): 842- 8.
Pors NS, Kolthoff N, Barenholdt O, Kristensen B, Abrahamsen B, Hermann AP, Brot C. Diagnosis of osteoporosis by planar bone densitometry: can body size be disregarded?. Br J Radiol. 1998 Sep; 71(849): 934- 43.
Laib A, Hildebrand T, Häuselmann HJ, Rüegsegger P. Ridge number density: a new parameter for in vivo bone structure analysis. Bone. 1997; Dec; 21(6): 541- 6.
Frost HM. The Utah paradigm of skeletal physiology: an overview of its insights for bone, cartilage and collagenous tissue organs. J Bone Miner Metab. 2000; 18(6): 305- 16.
Sas TC, de Muinck Keizer-Schrama SM, Stijnen T, van Teunenbroek A, van Leeuwen WJ, Asarfi A, van RijnRR, Drop SL, Dutch Advisory Group on Growth Hormone. Bone mineral density assessed by phalangeal radiographic absorptiometry before and during long-term growth hormone treatment in girls with Turner's syndrome participating in a randomized dose-response study. Pediatr Res. 2001 Sep; 50(3): 417- 22.
Nishiyama KK, Macdonald HM, Buie HR, Hanley DA, Boyd SK. Postmenopausal women with osteopenia have higher cortical porosity and thinner cortices at the distal radius and tibia than women with normal aBMD: an in vivo HR-pQCT study. J Bone Miner Res. 2010 Apr; 25(4): 882- 90.
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 quantitative computed tomography. J Clin Endocrinol Metab. 2001 Dec; 86(12): 5819- 23.
Huber C, Rosilio M, Munnich A, Cormier-Daire V. High incidence of SHOX anomalies in individuals with short stature. J Med Genet. 2006 Sep; 43(9): 735- 9.
Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. 2005 Dec; 90(12): 6508- 15.
Lanes R, Gunczler P, Esaa S, Martinis R, Villaroel O, Weisinger JR. Decreased bone mass despite long-term estrogen replacement therapy in young women with Turner's syndrome and previously normal bone density. Fertil Steril. 1999 Nov; 72(5): 896- 9.
Soucek O, Lebl J, Snajderova M, Kolouskova S, Rocek M, Hlavka Z, Cinek O, Rittweger J, Sumnik Z. Bone geometry and volumetric bone mineral density in girls with Turner syndrome of different pubertal stages. Clin Endocrinol (Oxf). 2011 Apr; 74(4): 445- 52.
Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Rüegsegger P. Image-based micro-finite-element modeling for improved distal radius strength diagnosis: moving from bench to bedside. J Clin Densitom. 2004; 7(2): 153- 60.
Sato N, Nimura A, Horikawa R, Katumata N, Tanae A, Tanaka T. Bone mineral density in Turner syndrome: relation to GH treatment and estrogen treatment. Endocr J. 2000 Mar; 47 Suppl: S115- 9.
Rao E, Weiss B, Fukami M, Rump A, Niesler B, Mertz A, Muroya K, 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 cause growth failure in idiopathic short stature and Turner syndrome. Nat Genet. 1997 May; 16(1): 54- 63.
Wang Q, Alen M, Nicholson PH, Halleen JM, Alatalo SL, Ohlsson C, Suominen H, Cheng S. Differential effects of sex hormones on peri- and endocortical bone surfaces in pubertal girls. J Clin Endocrinol Metab. 2006 Jan; 91(1): 277- 82.
Neely EK, Marcus R, Rosenfeld RG, Bachrach LK. Turner syndrome adolescents receiving growth hormone are not osteopenic. J Clin Endocrinol Metab. 1993; Apr; 76(4): 861- 6.
Nissen N, Gravholt CH, Abrahamsen B, Hauge EM, Jensen JE, Mosekilde L, Brixen K. Disproportional geometry of the proximal femur in patients with Turner syndrome: a cross-sectional study. Clin Endocrinol (Oxf). 2007; Dec; 67(6): 897- 903.
Bakalov VK, Axelrod L, Baron J, Hanton L, Nelson LM, Reynolds JC, Hill S, Troendle J, Bondy CA. Selective reduction in cortical bone mineral density in turner syndrome independent of ovarian hormone deficiency. J Clin Endocrinol Metab. 2003 Dec; 88(12): 5717- 22.
Hanton L, Axelrod L, Bakalov V, Bondy CA. The importance of estrogen replacement in young women with Turner syndrome. J Womens Health (Larchmt). 2003 Dec; 12(10): 971- 7.
Gravholt CH, Juul S, Naeraa RW, Hansen J. Morbidity in Turner syndrome. J Clin Epidemiol. 1998; Feb; 51(2): 147- 58.
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 (Oxf). 2006 Nov; 65(5): 643- 7.
Nishiyama KK, Macdonald HM, Moore SA, Fung T, Boyd SK, McKay HA. Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study. J Bone Miner Res. 2012 Feb; 27(2): 273- 82.
Bondy CA, Ceniceros I, Lange E, Bakalov VK. Declining estrogen use in young women with Turner syndrome. Arch Intern Med. 2006 Jun 26; 166(12): 1322.
Chen J, Wildhardt G, Zhong Z, Roth R, Weiss B, Steinberger D, Decker J, Blum WF, Rappold G. Enhancer deletions of the SHOX gene as a frequent cause of short stature: the essential role of a 250 kb downstream regulatory domain. J Med Genet. 2009 Dec; 46(12): 834- 9.
Bakalov VK, Chen ML, Baron J, Hanton LB, Reynolds JC, Stratakis CA, Axelrod LE, Bondy CA. Bone mineral density and fractures in Turner syndrome. Am J Med. 2003 Sep; 115(4): 259- 64.
Marchini A, Marttila T, Winter A, Caldeira S, Malanchi I, Blaschke RJ, Häcker B, Rao E, Karperien M, Wit JM, Richter W, Tommasino M, Rappold GA. The short stature homeodomain protein SHOX induces cellular growth arrest and apoptosis and is expressed in human growth plate chondrocytes. J Biol Chem. 2004 Aug 27; 279(35): 37103- 14.
Landin-Wilhelmsen K, Bryman I, Windh M, Wilhelmsen L. Osteoporosis and fractures in Turner syndrome-importance of growth promoting and oestrogen therapy. Clin Endocrinol (Oxf). 1999 Oct; 51(4): 497- 502.
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: a cross-sectional study. J Clin Endocrinol Metab. 2002 Jun; 87(6): 2798- 808.
Hansen S, Beck Jensen JE, Rasmussen L, Hauge EM, Brixen K. Effects on bone geometry, density, and microarchitecture in the distal radius but not the tibia in women with primary hyperparathyroidism: a case-control study using HR-pQCT. J Bone Miner Res. 2010 Sep; 25(9): 1941- 7.
Gravholt CH, Vestergaard P, Hermann AP, Mosekilde L, Brixen K, Christiansen JS. Increased fracture rates in Turner's syndrome: a nationwide questionnaire survey. Clin Endocrinol (Oxf). 2003 Jul; 59(1): 89- 96.
Marchini A, Hacker B, Marttila T, Hesse V, Emons J, Weiss B, Karperien M, Rappold G. BNP is a transcriptional target of the short stature homeobox gene SHOX. Hum Mol Genet. 2007; Dec 15; 16(24): 3081- 7.
Munns CF, Glass IA, LaBrom R, Hayes M, Flanagan S, Berry M, Hyland VJ, Batch JA, Philips GE, Vickers D. Histopathological analysis of Leri-Weill dyschondrosteosis: disordered growth plate. Hand Surg. 2001 Jul; 6(1): 13- 23.
Vanderschueren D, Venken K, Ophoff J, Bouillon R, Boonen S. Clinical Review: Sex steroids and the periosteum-reconsidering the roles of androgens and estrogens in periosteal expansion. J Clin Endocrinol Metab. 2006 Feb; 91(2): 378- 82.
Holroyd CR, Davies JH, Taylor P, Jameson K, Rivett C, Cooper C, Dennison EM. Reduced cortical bone density with normal trabecular bone density in girls with Turner syndrome. Osteoporos Int. 2010 Dec; 21(12): 2093- 9.
Rauch F, Neu C, Manz F, Schoenau E. The development of metaphyseal cortex-implications for distal radius fractures during growth. J Bone Miner Res. 2001 Aug; 16(8): 1547- 55.
2004; 41
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Han (2024020318273999700_bib13) 2006; 65
Melton (2024020318273999700_bib29) 2007; 22
Ogata (2024020318273999700_bib3) 2001; 38
Sabherwal (2024020318273999700_bib4) 2004; 41
Hanson (2024020318273999700_bib23) 1997; 12
Chiu (2024020318273999700_bib28) 1998; 31
Lanes (2024020318273999700_bib9) 1999; 72
Bondy (2024020318273999700_bib12) 2006; 166
Soucek (2024020318273999700_bib20) 2011; 74
Bakalov (2024020318273999700_bib35) 2003; 88
Holroyd (2024020318273999700_bib18) 2010; 21
Munns (2024020318273999700_bib44) 2001; 6
Rauch (2024020318273999700_bib37) 2001; 16
Pistoia (2024020318273999700_bib27) 2002; 30
Wang (2024020318273999700_bib42) 2006; 91
Olsen (2024020318273999700_bib45) 2000; 16
Marchini (2024020318273999700_bib2) 2007; 16
Laib (2024020318273999700_bib24) 1997; 21
Schoenau (2024020318273999700_bib38) 2002; 31
Bechtold (2024020318273999700_bib19) 2001; 86
Landin-Wilhelmsen (2024020318273999700_bib31) 1999; 51
Vanderschueren (2024020318273999700_bib41) 2006; 91
Hanton (2024020318273999700_bib36) 2003; 12
Burghardt (2024020318273999700_bib25) 2010; 25
Pistoia (2024020318273999700_bib22) 2004; 7
Sas (2024020318273999700_bib39) 2001; 50
Neely (2024020318273999700_bib15) 1993; 76
Nissen (2024020318273999700_bib17) 2007; 67
Frost (2024020318273999700_bib32) 2000; 18
Wang (2024020318273999700_bib34) 2005; 20
Gravholt (2024020318273999700_bib10) 1998; 51
Hansen (2024020318273999700_bib30) 2010; 25
Pors (2024020318273999700_bib14) 1998; 71
Bakalov (2024020318273999700_bib7) 2003; 115
Gravholt (2024020318273999700_bib8) 2002; 87
Chen (2024020318273999700_bib5) 2009; 46
Shaw (2024020318273999700_bib16) 1997; 47
Sato (2024020318273999700_bib40) 2000; 47
Huber (2024020318273999700_bib6) 2006; 43
Nishiyama (2024020318273999700_bib26) 2010; 25
Nishiyama (2024020318273999700_bib33) 2012; 27
Rao (2024020318273999700_bib1) 1997; 16
Marchini (2024020318273999700_bib43) 2004; 279
Gravholt (2024020318273999700_bib11) 2003; 59
Boutroy (2024020318273999700_bib21) 2005; 90
References_xml – reference: Marchini A, Hacker B, Marttila T, Hesse V, Emons J, Weiss B, Karperien M, Rappold G. BNP is a transcriptional target of the short stature homeobox gene SHOX. Hum Mol Genet. 2007; Dec 15; 16(24): 3081- 7.
– reference: Pors NS, Kolthoff N, Barenholdt O, Kristensen B, Abrahamsen B, Hermann AP, Brot C. Diagnosis of osteoporosis by planar bone densitometry: can body size be disregarded?. Br J Radiol. 1998 Sep; 71(849): 934- 43.
– reference: Hanton L, Axelrod L, Bakalov V, Bondy CA. The importance of estrogen replacement in young women with Turner syndrome. J Womens Health (Larchmt). 2003 Dec; 12(10): 971- 7.
– reference: 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: a cross-sectional study. J Clin Endocrinol Metab. 2002 Jun; 87(6): 2798- 808.
– reference: Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. 2005 Dec; 90(12): 6508- 15.
– reference: Munns CF, Glass IA, LaBrom R, Hayes M, Flanagan S, Berry M, Hyland VJ, Batch JA, Philips GE, Vickers D. Histopathological analysis of Leri-Weill dyschondrosteosis: disordered growth plate. Hand Surg. 2001 Jul; 6(1): 13- 23.
– reference: Hanson J. Standardization of femur BMD. J Bone Miner Res. 1997 Aug; 12(8): 1316- 7.
– reference: Neely EK, Marcus R, Rosenfeld RG, Bachrach LK. Turner syndrome adolescents receiving growth hormone are not osteopenic. J Clin Endocrinol Metab. 1993; Apr; 76(4): 861- 6.
– reference: Wang Q, Alen M, Nicholson P, Lyytikainen A, Suuriniemi M, Helkala E, Suominen H, Cheng S. Growth patterns at distal radius and tibial shaft in pubertal girls: a 2-year longitudinal study. J Bone Miner Res. 2005 Jun; 20(6): 954- 61.
– reference: Shaw NJ, Rehan VK, Husain S, Marshall T, Smith CS. Bone mineral density in Turner's syndrome-a longitudinal study. Clin Endocrinol (Oxf). 1997 Sep; 47(3): 367- 70.
– reference: Vanderschueren D, Venken K, Ophoff J, Bouillon R, Boonen S. Clinical Review: Sex steroids and the periosteum-reconsidering the roles of androgens and estrogens in periosteal expansion. J Clin Endocrinol Metab. 2006 Feb; 91(2): 378- 82.
– reference: Sas TC, de Muinck Keizer-Schrama SM, Stijnen T, van Teunenbroek A, van Leeuwen WJ, Asarfi A, van RijnRR, Drop SL, Dutch Advisory Group on Growth Hormone. Bone mineral density assessed by phalangeal radiographic absorptiometry before and during long-term growth hormone treatment in girls with Turner's syndrome participating in a randomized dose-response study. Pediatr Res. 2001 Sep; 50(3): 417- 22.
– reference: Rao E, Weiss B, Fukami M, Rump A, Niesler B, Mertz A, Muroya K, 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 cause growth failure in idiopathic short stature and Turner syndrome. Nat Genet. 1997 May; 16(1): 54- 63.
– reference: Marchini A, Marttila T, Winter A, Caldeira S, Malanchi I, Blaschke RJ, Häcker B, Rao E, Karperien M, Wit JM, Richter W, Tommasino M, Rappold GA. The short stature homeodomain protein SHOX induces cellular growth arrest and apoptosis and is expressed in human growth plate chondrocytes. J Biol Chem. 2004 Aug 27; 279(35): 37103- 14.
– reference: Bakalov VK, Axelrod L, Baron J, Hanton L, Nelson LM, Reynolds JC, Hill S, Troendle J, Bondy CA. Selective reduction in cortical bone mineral density in turner syndrome independent of ovarian hormone deficiency. J Clin Endocrinol Metab. 2003 Dec; 88(12): 5717- 22.
– reference: Laib A, Hildebrand T, Häuselmann HJ, Rüegsegger P. Ridge number density: a new parameter for in vivo bone structure analysis. Bone. 1997; Dec; 21(6): 541- 6.
– reference: Nissen N, Gravholt CH, Abrahamsen B, Hauge EM, Jensen JE, Mosekilde L, Brixen K. Disproportional geometry of the proximal femur in patients with Turner syndrome: a cross-sectional study. Clin Endocrinol (Oxf). 2007; Dec; 67(6): 897- 903.
– reference: Wang Q, Alen M, Nicholson PH, Halleen JM, Alatalo SL, Ohlsson C, Suominen H, Cheng S. Differential effects of sex hormones on peri- and endocortical bone surfaces in pubertal girls. J Clin Endocrinol Metab. 2006 Jan; 91(1): 277- 82.
– reference: Bondy CA, Ceniceros I, Lange E, Bakalov VK. Declining estrogen use in young women with Turner syndrome. Arch Intern Med. 2006 Jun 26; 166(12): 1322.
– reference: 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 quantitative computed tomography. J Clin Endocrinol Metab. 2001 Dec; 86(12): 5819- 23.
– reference: Rauch F, Neu C, Manz F, Schoenau E. The development of metaphyseal cortex-implications for distal radius fractures during growth. J Bone Miner Res. 2001 Aug; 16(8): 1547- 55.
– reference: Gravholt CH, Juul S, Naeraa RW, Hansen J. Morbidity in Turner syndrome. J Clin Epidemiol. 1998; Feb; 51(2): 147- 58.
– reference: Frost HM. The Utah paradigm of skeletal physiology: an overview of its insights for bone, cartilage and collagenous tissue organs. J Bone Miner Metab. 2000; 18(6): 305- 16.
– reference: Chen J, Wildhardt G, Zhong Z, Roth R, Weiss B, Steinberger D, Decker J, Blum WF, Rappold G. Enhancer deletions of the SHOX gene as a frequent cause of short stature: the essential role of a 250 kb downstream regulatory domain. J Med Genet. 2009 Dec; 46(12): 834- 9.
– reference: Hansen S, Beck Jensen JE, Rasmussen L, Hauge EM, Brixen K. Effects on bone geometry, density, and microarchitecture in the distal radius but not the tibia in women with primary hyperparathyroidism: a case-control study using HR-pQCT. J Bone Miner Res. 2010 Sep; 25(9): 1941- 7.
– reference: Huber C, Rosilio M, Munnich A, Cormier-Daire V. High incidence of SHOX anomalies in individuals with short stature. J Med Genet. 2006 Sep; 43(9): 735- 9.
– reference: Holroyd CR, Davies JH, Taylor P, Jameson K, Rivett C, Cooper C, Dennison EM. Reduced cortical bone density with normal trabecular bone density in girls with Turner syndrome. Osteoporos Int. 2010 Dec; 21(12): 2093- 9.
– reference: Sato N, Nimura A, Horikawa R, Katumata N, Tanae A, Tanaka T. Bone mineral density in Turner syndrome: relation to GH treatment and estrogen treatment. Endocr J. 2000 Mar; 47 Suppl: S115- 9.
– reference: Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Rüegsegger P. Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone. 2002 Jun; 30(6): 842- 8.
– reference: Gravholt CH, Vestergaard P, Hermann AP, Mosekilde L, Brixen K, Christiansen JS. Increased fracture rates in Turner's syndrome: a nationwide questionnaire survey. Clin Endocrinol (Oxf). 2003 Jul; 59(1): 89- 96.
– reference: 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 (Oxf). 2006 Nov; 65(5): 643- 7.
– reference: Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S. Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res. 2010 May; 25(5): 983- 93.
– reference: Schoenau E, Neu CM, Rauch F, Manz F. Gender-specific pubertal changes in volumetric cortical bone mineral density at the proximal radius. Bone. 2002 Jul; 31(1): 110- 3.
– reference: Sabherwal N, Blaschke RJ, Marchini A, Heine-Suner D, Rosell J, Ferragut J, Blum WF, Rappold G. A novel point mutation A170P in the SHOX gene defines impaired nuclear translocation as a molecular cause for Leri-Weill dyschondrosteosis and Langer dysplasia. J Med Genet. 2004 Jun; 41(6): e83.
– reference: Lanes R, Gunczler P, Esaa S, Martinis R, Villaroel O, Weisinger JR. Decreased bone mass despite long-term estrogen replacement therapy in young women with Turner's syndrome and previously normal bone density. Fertil Steril. 1999 Nov; 72(5): 896- 9.
– reference: Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Rüegsegger P. Image-based micro-finite-element modeling for improved distal radius strength diagnosis: moving from bench to bedside. J Clin Densitom. 2004; 7(2): 153- 60.
– reference: Bakalov VK, Chen ML, Baron J, Hanton LB, Reynolds JC, Stratakis CA, Axelrod LE, Bondy CA. Bone mineral density and fractures in Turner syndrome. Am J Med. 2003 Sep; 115(4): 259- 64.
– reference: Soucek O, Lebl J, Snajderova M, Kolouskova S, Rocek M, Hlavka Z, Cinek O, Rittweger J, Sumnik Z. Bone geometry and volumetric bone mineral density in girls with Turner syndrome of different pubertal stages. Clin Endocrinol (Oxf). 2011 Apr; 74(4): 445- 52.
– reference: Melton LJ III, Riggs BL, van Lenthe GH, Achenbach SJ, Muller R, Bouxsein ML, Amin S, Atkinson EJ, Khosla S. Contribution of in vivo structural measurements and load/strength ratios to the determination of forearm fracture risk in postmenopausal women. J Bone Miner Res. 2007; Sep; 22(9): 1442- 8.
– reference: Nishiyama KK, Macdonald HM, Moore SA, Fung T, Boyd SK, McKay HA. Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study. J Bone Miner Res. 2012 Feb; 27(2): 273- 82.
– reference: Ogata T, Matsuo N, Nishimura G. SHOX haploinsufficiency and overdosage: impact of gonadal function status. J Med Genet. 2001 Jan; 38(1): 1- 6.
– reference: Olsen BR, Reginato AM, Wang W. Bone development. Annu Rev Cell Dev Biol. 2000; 16: 191- 220.
– reference: Landin-Wilhelmsen K, Bryman I, Windh M, Wilhelmsen L. Osteoporosis and fractures in Turner syndrome-importance of growth promoting and oestrogen therapy. Clin Endocrinol (Oxf). 1999 Oct; 51(4): 497- 502.
– reference: Nishiyama KK, Macdonald HM, Buie HR, Hanley DA, Boyd SK. Postmenopausal women with osteopenia have higher cortical porosity and thinner cortices at the distal radius and tibia than women with normal aBMD: an in vivo HR-pQCT study. J Bone Miner Res. 2010 Apr; 25(4): 882- 90.
– reference: Chiu J, Robinovitch SN. Prediction of upper extremity impact forces during falls on the outstretched hand. J Biomech. 1998 Dec; 31(12): 1169- 76.
– volume: 67
  start-page: 897
  issue: 6
  year: 2007
  end-page: 903
  article-title: Disproportional geometry of the proximal femur in patients with Turner syndrome: a cross‐sectional study
  publication-title: Clin Endocrinol (Oxf).
– volume: 12
  start-page: 971
  issue: 10
  year: 2003
  end-page: 7
  article-title: The importance of estrogen replacement in young women with Turner syndrome
  publication-title: J Womens Health (Larchmt).
– volume: 16
  start-page: 54
  issue: 1
  year: 1997
  end-page: 63
  article-title: Pseudoautosomal deletions encompassing a novel homeobox gene cause growth failure in idiopathic short stature and Turner syndrome
  publication-title: Nat Genet.
– volume: 41
  start-page: e83
  issue: 6
  year: 2004
  article-title: A novel point mutation A170P in the SHOX gene defines impaired nuclear translocation as a molecular cause for Leri‐Weill dyschondrosteosis and Langer dysplasia
  publication-title: J Med Genet.
– volume: 30
  start-page: 842
  issue: 6
  year: 2002
  end-page: 8
  article-title: Estimation of distal radius failure load with micro‐finite element analysis models based on three‐dimensional peripheral quantitative computed tomography images
  publication-title: Bone.
– volume: 51
  start-page: 497
  issue: 4
  year: 1999
  end-page: 502
  article-title: Osteoporosis and fractures in Turner syndrome‐importance of growth promoting and oestrogen therapy
  publication-title: Clin Endocrinol (Oxf).
– volume: 47
  start-page: 367
  issue: 3
  year: 1997
  end-page: 70
  article-title: Bone mineral density in Turner's syndrome—a longitudinal study
  publication-title: Clin Endocrinol (Oxf).
– volume: 90
  start-page: 6508
  issue: 12
  year: 2005
  end-page: 15
  article-title: In vivo assessment of trabecular bone microarchitecture by high‐resolution peripheral quantitative computed tomography
  publication-title: J Clin Endocrinol Metab.
– volume: 74
  start-page: 445
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SSID ssj0006566
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Snippet Although bone mass appear ample for bone size in Turner syndrome (TS), epidemiological studies have reported an increased risk of fracture in TS. We used...
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StartPage 1794
SubjectTerms Absorptiometry, Photon
Adolescent
Adult
Anthropometry
Biological and medical sciences
Bone Density
BONE MICROARCHITECTURE
BONE STRENGTH
Case-Control Studies
Cross-Sectional Studies
Female
FINITE ELEMENT ANALYSIS
Fundamental and applied biological sciences. Psychology
HR-PQCT
Humans
Middle Aged
Radius - diagnostic imaging
Radius - pathology
Radius - physiopathology
Regression Analysis
Skeleton and joints
Tibia - diagnostic imaging
Tibia - pathology
Tibia - physiopathology
Tomography, X-Ray Computed
TURNER SYNDROME
Turner Syndrome - diagnostic imaging
Turner Syndrome - pathology
Turner Syndrome - physiopathology
Vertebrates: osteoarticular system, musculoskeletal system
Young Adult
Title 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
URI https://api.istex.fr/ark:/67375/WNG-FGLP7SMG-9/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fjbmr.1624
https://www.ncbi.nlm.nih.gov/pubmed/22492464
https://www.proquest.com/docview/1355714680
https://www.proquest.com/docview/1027041175
https://www.proquest.com/docview/1038615383
Volume 27
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