Osteoporosis International

, Volume 29, Issue 2, pp 409–419 | Cite as

Characterization of trabecular bone microstructure in premenopausal women with distal radius fractures

  • T. D. RozentalEmail author
  • F. Johannesdottir
  • K. C. Kempland
  • M. L. Bouxsein
Original Article



Individual trabecular segmentation was utilized to identify differences in trabecular bone structure in premenopausal women with wrist fractures and non-fracture controls. Fracture subjects had reduced trabecular plate volume, number, thickness, and connectivity. Identifying altered trabecular microarchitecture in young women offers opportunities for counseling and lifestyle modifications to reduce fracture risk.


Premenopausal women with distal radius fractures (DRF) have worse trabecular bone microarchitecture than non-fracture controls (CONT), yet the characteristics of their trabecular bone structure are unknown.


Premenopausal women with DRF (n = 40) and CONT (n = 80) were recruited. Primary outcome variables included trabecular structure at the distal radius and tibia, assessed by volumetric decomposition of individual trabecular plates and rods from high-resolution peripheral quantitative CT images. Trabecular morphology included plate and rod number, volume, thickness, and connectivity. Areal bone mineral density (aBMD) of the femoral neck (FN aBMD), and ultradistal radius (UDR aBMD) were measured by DXA.


Trabecular morphology differed between DRF and CONT at the radius and tibia (OR per SD decline 1.58–2.7). At the radius, associations remained significant when adjusting for age and FN aBMD (ORs = 1.76–3.26) and age and UDR aBMD (ORs = 1.72–3.97). Plate volume fraction, number and axially aligned trabeculae remained associated with DRF after adjustment for trabecular density (ORs = 2.55–2.85). Area under the curve (AUC) for discriminating DRF was 0.74 for the proportion of axially aligned trabeculae, compared with 0.60 for FN aBMD, 0.65 for UDR aBMD, and 0.69 for trabecular density. Plate number, plate-plate junction, and axial bone volume fraction remained associated with DRF at the tibia (ORs = 2.14–2.77) after adjusting for age, FN aBMD, or UDR aBMD. AUCP.P.Junc.D was 0.72 versus 0.61 for FNaBMD, 0.66 for UDRaBMD, and 0.70 for trabecular density.


Premenopausal women with DRF have lower trabecular plate volume, number, thickness, and connectivity than CONT. Identification of young women with altered microarchitecture offers opportunities for lifestyle modifications to reduce fracture risk.


Bone mineral density (BMD) Distal radius fracture (DRF) High-resolution peripheral quantitative CT (HR-pQCT) Individual trabecular segmentation (ITS) Osteoporosis 



We thank X. Edward Guo at Columbia University for sharing the ITS analysis program. Purchase of the HR-pQCT machine was made possible through an NCRR shared equipment grant (NIH/NCRR 1 S10 RR023405).


This work was supported by a Clinical Research Grant from the Ruth Jackson Orthopedic Society and Zimmer, Inc., as well as Sanofi LLC.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no competing interests.


  1. 1.
    Burge R, Dawson-Hughes B, Solomon DH et al (2007) Incidence and economic burden of osteoporosis-related fractures in the United States, 2005-2025. J Bone Miner Res 22(3):465–475. CrossRefPubMedGoogle Scholar
  2. 2.
    Cummings SR, Melton LJ (2002) Epidemiology and outcomes of osteoporotic fractures. Lancet 359(9319):1761–1767. CrossRefPubMedGoogle Scholar
  3. 3.
    Stone KL, Seeley DG, Lui LY et al (2003) BMD at multiple sites and risk of fracture of multiple types: long-term results from the study of osteoporotic fractures. J Bone Miner Res 18(11):1947–1954. CrossRefPubMedGoogle Scholar
  4. 4.
    Wainwright SA, Marshall LM, Ensrud KE et al (2005) Hip fracture in women without osteoporosis. J Clin Endocr Metab 90(5):2787–2793. CrossRefPubMedGoogle Scholar
  5. 5.
    Schuit SC, van der Klift M, Weel AE et al (2004) Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam study. Bone 34(1):195–202. CrossRefPubMedGoogle Scholar
  6. 6.
    Boutroy S, Khosla S, Sornay-Rendu E et al (2016) Microarchitecture and peripheral BMD are impaired in postmenopausal white women with fracture independently of total hip T-score: an international multicenter study. J Bone Miner Res 31:1158–1166. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J clin Endocr Metab 90(12):6508–6515. CrossRefPubMedGoogle Scholar
  8. 8.
    Sornay-Rendu E, Boutroy S, Munoz F, Delmas PD (2007) Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res 22(3):425–433. CrossRefPubMedGoogle Scholar
  9. 9.
    Vico L, Zouch M, Amirouche A et al (2008) High-resolution pQCT analysis at the distal radius and tibia discriminates patients with recent wrist and femoral neck fractures. J Bone Miner Res 23(11):1741–1750. CrossRefPubMedGoogle Scholar
  10. 10.
    Vilayphiou N, Boutroy S, Sornay-Rendu E et al (2010) Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in postmenopausal women. Bone 46(4):1030–1037. CrossRefPubMedGoogle Scholar
  11. 11.
    Szulc P, Boutroy S, Vilayphiou N et al (2011) Cross-sectional analysis of the association between fragility fractures and bone microarchitecture in older men: the STRAMBO study. J Bone Miner Res 26(6):1358–1367. CrossRefPubMedGoogle Scholar
  12. 12.
    Vilayphiou N, Boutroy S, Szulc P et al (2011) Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res 26(5):965–973. CrossRefPubMedGoogle Scholar
  13. 13.
    Liu XS, Stein EM, Zhou B et al (2012) Individual trabecula segmentation (ITS)-based morphological analyses and microfinite element analysis of HR-pQCT images discriminate postmenopausal fragility fractures independent of DXA measurements. J Bone Miner Res 27(2):263–272. CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Melton LJ (2009) Application of technology to push epidemiology forward. Osteoporosis Int 20(Suppl 3):S235–S236. CrossRefGoogle Scholar
  15. 15.
    Stein EM, Liu XS, Nickolas TL et al (2010) Abnormal microarchitecture and reduced stiffness at the radius and tibia in postmenopausal women with fractures. J Bone Miner Res 25(12):2572–2581. CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Liu XS, Cohen A, Shane E et al (2010) Bone density, geometry, microstructure, and stiffness: relationships between peripheral and central skeletal sites assessed by DXA, HR-pQCT, and cQCT in premenopausal women. J Bone Miner Res 25(10):2229–2238. CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Rozental TD, Deschamps LN, Taylor A et al (2013) Premenopausal women with a distal radial fracture have deteriorated trabecular bone density and morphology compared with controls without a fracture. J Bone Joint Surg Am 95(7):633–642. CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Liu XS, Sajda P, Saha PK et al (2007) Complete volumetric decomposition of individual trabecular plates and rods and its morphological correlations with anisotropic elastic moduli in human trabecular bone. J Bone Miner Res 23(2):223–235. CrossRefPubMedCentralGoogle Scholar
  19. 19.
    Stein EM, Kepley A, Walker M et al (2014) Skeletal structure in postmenopausal women with osteopenia and fractures is characterized by abnormal trabecular plates and cortical thinning. J Bone Miner Res 29(5):1101–1109. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Zhou B, Wang J, Stein EM et al (2014) Bone density, microarchitecture and stiffness in Caucasian and Caribbean Hispanic postmenopausal American women. Bone Res 2:14016. CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Putman MS, EW Y, Lin D et al (2017) Differences in trabecular microstructure between black and white women assessed by individual trabecular segmentation analysis of HR-pQCT images. J Bone Miner Res 32(5):1100–1108. CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Walker MD, Kepley A, Nishiyama K, Zhou B, Guo E, Nickolas TL (2017) Cortical microstructure compensates for smaller bone size in young Caribbean Hispanic versus non-Hispanic white men. Osteoporis Int 28(348):1–8. CrossRefGoogle Scholar
  23. 23.
    Mitchell DM, Tuck P, Ackerman KE et al (2015) Altered trabecular bone morphology in adolescent and young adult athletes with menstrual dysfunction. Bone 81:24–30. CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Putman MS, Greenblatt LB, Sicilian L et al (2016) Young adults with cystic fibrosis have altered trabecular microstructure by ITS-based morphological analysis. Osteoporis Int 27(8):2497–2505. CrossRefGoogle Scholar
  25. 25.
    Bala Y, Bui QM, Wang XF et al (2015) Trabecular and cortical microstructure and fragility of the distal radius in women. JBMR 30:621–629. CrossRefGoogle Scholar
  26. 26.
    Fricker R, Jupiter J, Kastelec M (n.d.) Distal forearm AO classification. Retrieved September 20, 2017, from
  27. 27.
    Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE (2006) Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Miner Res 21(10):1608–1617. CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Khosla S, Riggs BL, Atkinson EJ et al (2006) Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res 21(1):124–131. CrossRefPubMedGoogle Scholar
  29. 29.
    Popp KL, Hughes JM, Martinez-Betancourt A et al (2017) Bone mass, microarchitecture and strength are influenced by race/ethnicity in young adult men and women. Bone 103:200–208. CrossRefPubMedGoogle Scholar
  30. 30.
    Pistoia W, van Rietbergen B, Lochmuller EM, Lill CA, Eckstein F, Ruegsegger P (2002) Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images. Bone 30:842–848. CrossRefPubMedGoogle Scholar
  31. 31.
    Cohen A, Liu XS, Stein EM et al (2009) Bone microarchitecture and stiffness in premenopausal women with idiopathic osteoporosis. J Clin Endocr Metab 94(11):4351–4360. CrossRefPubMedGoogle Scholar
  32. 32.
    Goulding A, Grant AM, Williams SM (2005) Bone and body composition of children and adolescents with repeated forearm fractures. J Bone Miner Res 20(12):2090–2096. CrossRefPubMedGoogle Scholar
  33. 33.
    Pye SR, Tobias J, Silman AJ, Reeve J, O’Neill TW (2009) Childhood fractures do not predict future fractures: results from the European prospective osteoporosis study. J Bone Miner Res 24(7):1314–1318. CrossRefPubMedGoogle Scholar
  34. 34.
    Matkovic V, Jelic T, Wardlaw GM et al (1994) Timing of peak bone mass in Caucasian females and its implication for the prevention of osteoporosis. Inference from a cross-sectional model. J Clin Invest 93(2):799–808. CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Sigurdsson G, Halldorsson BV, Styrkarsdottir U, Kristjansson K, Stefansson K (2008) Impact of genetics on low bone mass in adults. J Bone Miner Res 23(10):1584–1590. CrossRefPubMedGoogle Scholar
  36. 36.
    Fox KM, Cummings SR, Powell-Threets K, Stone K (1998) Family history and risk of osteoporotic fracture. Study of osteoporotic fractures research group. Osteoporosis Int 8(6):557–562CrossRefGoogle Scholar
  37. 37.
    Chevalley T, J-philippe B, Ferrari S, Rizzoli R (2009) Deleterious effect of late menarche on distal tibia microstructure in healthy 20-year-old and premenopausal middle-aged women. J Bone Miner Res 24(1):144–152. CrossRefPubMedGoogle Scholar
  38. 38.
    Galuska DA, Sowers MR (1999) Menstrual history and bone density in young women. J Women Health Gen-b 8(5):647–656. CrossRefGoogle Scholar
  39. 39.
    Ruffing JA, Nieves JW, Zion M et al (2007) The influence of lifestyle, menstrual function and oral contraceptive use on bone mass and size in female military cadets. Nutr Metab 4:17. CrossRefGoogle Scholar
  40. 40.
    Cadogan J, Eastell R, Jones N, Barker ME (1997) Milk intake and bone mineral acquisition in adolescent girls: randomised, controlled intervention trial. Brit Med J 315(7118):1255–1260. CrossRefPubMedGoogle Scholar
  41. 41.
    Chan GM, Hoffman K, McMurry M (1995) Effects of dairy products on bone and body composition in pubertal girls. J Pediatr 126(4):551–556. CrossRefPubMedGoogle Scholar
  42. 42.
    Modlesky CM, Majumdar S, Dudley GA (2008) Trabecular bone microarchitecture in female collegiate gymnasts. Osteoporosis Int 19(7):1011–1018. CrossRefGoogle Scholar
  43. 43.
    Heinonen A, Kannus P, Sievänen H et al (1996) Randomised controlled trial of effect of high-impact exercise on selected risk factors for osteoporotic fractures. Lancet 348(9038):1343–1347. CrossRefPubMedGoogle Scholar
  44. 44.
    Modlesky CM, Majumdar S, Narasimhan A, Dudley GA (2004) Trabecular bone microarchitecture is deteriorated in men with spinal cord injury. J Bone Miner Res 19(1):48–55. CrossRefPubMedGoogle Scholar
  45. 45.
    Slade JM, Bickel CS, Modlesky CM, Majumdar S, Dudley GA (2005) Trabecular bone is more deteriorated in spinal cord injured versus estrogen-free postmenopausal women. Osteoporosis Int 16(3):263–272. CrossRefGoogle Scholar
  46. 46.
    Ingle BM, Hay SM, Bottjer HM, Eastell R (1999) Changes in bone mass and bone turnover following distal forearm fracture. Osteoporosis Int 10(5):399–407. CrossRefGoogle Scholar
  47. 47.
    Liu XS, Zhang XH, Sekhon KK et al (2010) High-resolution peripheral quantitative computed tomography can assess microstructural and mechanical properties of human distal tibial bone. J Bone Miner Res 25(4):746–756. CrossRefPubMedGoogle Scholar
  48. 48.
    Singer BR, McLauchlan GJ, Robinson CM, Christie J (1998) Epidemiology of fractures in 15,000 adults: the influence of age and gender. J Bone Joint Surg Br 80(2):243–248CrossRefGoogle Scholar
  49. 49.
    Cummings SR, Black DM, Rubin SM (1989) Lifetime risks of hip, Colles’, or vertebral fracture and coronary heart disease among white postmenopausal women. Arch Intern Med 149(11):2445–2448. CrossRefPubMedGoogle Scholar
  50. 50.
    Cuddihy MT, Gabriel SE, Crowson CS, O’Fallon WM, Melton LJ (1999) Forearm fractures as predictors of subsequent osteoporotic fractures. Osteoporosis Int 9(6):469–475. CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2017

Authors and Affiliations

  • T. D. Rozental
    • 1
    Email author
  • F. Johannesdottir
    • 2
  • K. C. Kempland
    • 1
  • M. L. Bouxsein
    • 2
  1. 1.Department of Orthopaedic Surgery, Beth Israel Deaconess Medical Center, Harvard Medical SchoolHarvard UniversityBostonUSA
  2. 2.Department of Orthopaedic Surgery, Beth Israel Deaconess Medical CenterOrthopedic Biomechanics LaboratoryBostonUSA

Personalised recommendations