Trabecular Plate Loss and Deteriorating Elastic Modulus of Femoral Trabecular Bone in Intertrochanteric Hip Fractures

Abstract

Osteoporotic hip fracture is associated with significant trabecular bone loss, which is typically characterized as low bone density by dual-energy X-ray absorptiometry (DXA) and altered microstructure by micro-computed tomography (μCT). Emerging morphological analysis techniques, e.g. individual trabecula segmentation (ITS), can provide additional insights into changes in plate-like and rod-like trabeculae, two major microstructural types serving different roles in determining bone strength. Using ITS, we evaluated trabecular microstructure of intertrochanteric bone cores obtained from 23 patients undergoing hip replacement surgery for intertrochanteric fracture and 22 cadaveric controls. Micro-finite element (μFE) analyses were performed to further understand how the abnormalities seen by ITS might translate into effects on bone strength. ITS analyses revealed that, near fracture site, plate-like trabeculae were seriously depleted in fracture patients, but trabecular rod volume was maintained. Besides, decreased plate area and rod length were observed in fracture patients. Fracture patients also showed decreased elastic moduli and shear moduli of trabecular bone. These results provided evidence that in intertrochanteric hip fracture, preferential loss of plate-like trabeculae led to more rod-like microstructure and deteriorated mechanical competence adjacent to the fracture site, which increased our understanding of the biomechanical pathogenesis of hip fracture in osteoporosis.

References

[1] Burge R, Dawson-Hughes B, Solomon DH, Wong JB, King A, Tosteson A. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res, 2007, 22: 465-475

[2] Riggs BL, Melton LJ 3rd. The worldwide problem of osteoporosis: insights afforded by epidemiology. Bone, 1995, 17: 505S-511S

[3] Gullberg B, Johnell O, Kanis JA. World-wide projections for hip fracture. Osteoporos Int, 1997, 7: 407-413

[4] Szulc P, Boutroy S, Vilayphiou N, Chaitou A, Delmas PD, Chapurlat R. Cross-sectional analysis of the association between fragility fractures and bone microarchitecture in older men: the STRAMBO study. J Bone Miner Res, 2011, 26: 1358-1367

[5] Wainwright SA, Marshall LM, Ensrud KE, Cauley JA, Black DM, Hillier TA, Hochberg MC, Vogt MT, Orwoll ES Study of Osteoporotic Fractures Research Group Hip fracture in women without osteoporosis. J Clin Endocrinol Metab, 2005, 90: 2787-2793

[6] Riggs BL, Melton Iii LJ 3rd, Robb RA, Camp JJ, Atkinson EJ, Peterson JM, Rouleau PA, McCollough CH, Bouxsein ML, Khosla S. Population-based study of age and sex differences in bone volumetric density, size, geometry, and structure at different skeletal sites. J Bone Miner Res, 2004, 19: 1945-1954

[7] Boutroy S, Vilayphiou N, Roux JP, Delmas PD, Blain H, Chapurlat RD, Chavassieux P. Comparison of 2D and 3D bone microarchitecture evaluation at the femoral neck, among postmenopausal women with hip fracture or hip osteoarthritis. Bone, 2011, 49: 1055-1061

[8] Thomas CD, Mayhew PM, Power J, Poole KE, Loveridge N, Clement JG, Burgoyne CJ, Reeve J. Femoral neck trabecular bone: loss with aging and role in preventing fracture. J Bone Miner Res, 2009, 24: 1808-1818

[9] Carballido-Gamio J, Harnish R, Saeed I, Streeper T, Sigurdsson S, Amin S, Atkinson EJ, Therneau TM, Siggeirsdottir K, Cheng X, Melton LJ 3rd, Keyak J, Gudnason V, Khosla S, Harris TB, Lang TF. Proximal femoral density distribution and structure in relation to age and hip fracture risk in women. J Bone Miner Res, 2013, 28: 537-546

[10] Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA. Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res, 2000, 15: 32-40

[11] Milovanovic P, Djonic D, Marshall RP, Hahn M, Nikolic S, Zivkovic V, Amling M, Djuric M. Microstructural basis for particular vulnerability of the superolateral neck trabecular bone in the postmenopausal women with hip fractures. Bone, 2012, 50: 63-68

[12] Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Cosman F, Nieves J, Shane E, Guo XE. 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, 2012, 27: 263-272

[13] Cui WQ, Won YY, Baek MH, Lee DH, Chung YS, Hur JH, Ma YZ. Age- and region-dependent changes in three-dimensional microstructural properties of proximal femoral trabeculae. Osteoporos Int, 2008, 19: 1579-1587

[14] Singh M, Nagrath AR, Maini PS. Changes in trabecular pattern of the upper end of the femur as an index of osteoporosis. J Bone Joint Surg Am, 1970, 52: 457-467

[15] Li W, Kornak J, Harris T, Keyak J, Li C, Lu Y, Cheng X, Lang T. Identify fracture-critical regions inside the proximal femur using statistical parametric mapping. Bone, 2009, 44: 596-602

[16] Ding M, Hvid I. Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone, 2000, 26: 291-295

[17] Liu XS, Cohen A, Shane E, Stein E, Rogers H, Kokolus SL, Yin PT, McMahon DJ, Lappe JM, Recker RR, Guo XE. Individual trabeculae segmentation (ITS)–based morphological analysis of high-resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis. J Bone Miner Res, 2010, 25: 1496-1505

[18] Liu XS, Sajda P, Saha PK, Wehrli FW, Bevill G, Keaveny TM, Guo XE. 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, 2008, 23: 223-235

[19] Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE. Quantification of the roles of trabecular microarchitecture and trabecular type in determining the elastic modulus of human trabecular bone. J Bone Miner Res, 2006, 21: 1608-1617

[20] Liu XS, Walker MD, McMahon DJ, Udesky J, Liu G, Bilezikian JP, Guo XE. Better skeletal microstructure confers greater mechanical advantages in Chinese-American women versus white women. J Bone Miner Res, 2011, 26: 1783-1792

[21] Thomas C, Clement J. The Melbourne femur collection: How a forensic anthropological collection came to have broader applications//Stout S, Crowder C (eds.) Bone Histology: an Anthropological Perspective, 2012 CRC Press Inc

[22] Saha PK, Chaudhuri BB, Majumder DD. A new shape preserving parallel thinning algorithm for 3D digital images. Pattern Recogn, 1997, 30: 1939-1955

[23] Saha PK, Chaudhuri BB. 3D digital topology under binary transformation with applications. Comput Vis Image Und, 1996, 63: 418-429

[24] Guo XE, Goldstein SA. Is trabecular bone tissue different from cortical bone tissue? Forma, 1997, 12: 185-196

[25] Hollister SJ, Brennan JM, Kikuchi N. A homogenization sampling procedure for calculating trabecular bone effective stiffness and tissue level stress. J Biomech, 1994, 27: 433-444

[26] Amin S, Kopperdhal DL, Melton LJ 3rd, Achenbach SJ, Therneau TM, Riggs BL, Keaveny TM, Khosla S. Association of hip strength estimates by finite-element analysis with fractures in women and men. J Bone Miner Res, 2011, 26: 1593-1600

[27] Dufour AB, Roberts B, Broe KE, Kiel DP, Bouxsein ML, Hannan MT. The factor-of-risk biomechanical approach predicts hip fracture in men and women: the Framingham Study. Osteoporos Int, 2012, 23: 513-520

[28] Koivumaki JE, Thevenot J, Pulkkinen P, Salmi JA, Kuhn V, Lochmuller EM, Link TM, Eckstein F, Jamsa T. Does femoral strain distribution coincide with the occurrence of cervical versus trochanteric hip fractures? An experimental finite element study. Med Biol Eng Comput, 2010, 48: 711-717