QCT-based finite element models predict human vertebral strength in vitro significantly better than simulated DEXA

wbldb

Dall’Ara, E.¹; Pahr, D.¹; Varga, P.¹; Kainberger, F.²; Zysset, P.¹

QCT-based finite element models predict human vertebral strength in vitro significantly better than simulated DEXA

Osteoporos Int. February 2012;23(2):563-572

©2011 International Osteoporosis Foundation and National Osteoporosis Foundation

Affiliations

¹Institute of Lightweight Design and Structural Biomechanics, Vienna University of Technology, Vienna, Austria

²Department of Radiology, Medical University of Vienna, Vienna, Austria
Abstract and keywords

Summary: While dual energy X-ray absorptiometry (DXA) is considered the gold standard to evaluate fracture risk in vivo, in the present study, the quantitative computed tomography (QCT)-based finite element modeling has been found to provide a quantitative and significantly improved prediction of vertebral strength in vitro. This technique might be used in vivo considering however the much larger doses of radiation needed for QCT.

Introduction: Vertebral fracture is a common medical problem in osteoporotic individuals. Bone mineral density (BMD) is the gold standard measure to evaluate fracture risk in vivo. QCT-based finite element (FE) modeling is an engineering method to predict vertebral strength. The aim of this study was to compare the ability of FE and clinical diagnostic tools to predict vertebral strength in vitro using an improved testing protocol.

Methods: Thirty-seven vertebral sections were scanned with QCT and high resolution peripheral QCT (HR-pQCT). Bone mineral content (BMC), total BMD (tBMD), areal BMD from lateral (aBMD-lat), and anterior-posterior (aBMD-ap) projections were evaluated for both resolutions. Wedge-shaped fractures were then induced in each specimen with a novel testing setup. Nonlinear homogenized FE models (hFE) and linear micro-FE (μFE) were generated from QCT and HR-pQCT images, respectively. For experiments and models, both structural properties (stiffness, ultimate load) and material properties (apparent modulus and strength) were computed and compared.

Results: Both hFE and μFE models predicted material properties better than structural ones and predicted strength significantly better than aBMD computed from QCT and HR-pQCT (hFE: R² = 0.79, μFE: R² = 0.88, aBMD-ap: R² = 0.48−0.47, aBMD-lat: R² = 0.41−0.43). Moreover, the hFE provided reasonable quantitative estimations of the experimental mechanical properties without fitting the model parameters.

Conclusions: The QCT-based hFE method provides a quantitative and significantly improved prediction of vertebral strength in vitro when compared to simulated DXA. This superior predictive power needs to be verified for loading conditions that simulate even more the in vivo case for human vertebrae.

Keywords: Finite element modeling; Bone mineral density; DXA; Bone strength; Osteoporosis; Mechanical testing
Links

DOI: 10.1007/s00198-011-1568-3

PubMed: 21344244

WoS: 000299306300016
History

Received: 2010-07-15

Accepted: 2011-02-01

Online: 2011-02-23

Cited Works (37)

Year	Entry
1998	Silva MJ, Keaveny TM, Hayes WC. Computed tomography-based finite element analysis predicts failure loads and fracture patterns for vertebral sections. J Orthop Res. May 1998;16(3):300-308.
2009	Rincón-Kohli L, Zysset PK. Multi-axial mechanical properties of human trabecular bone. Biomech Model Mechanobiol. June 2009;8(3):195-208.
2000	Boivin GY, Chavassieux PM, Santora AC, Yates J, Meunier PJ. Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women. Bone. November 2000;27(5):687-694.
2008	MacNeil JA, Boyd SK. Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone. June 2008;42(6):1203-1213.
1996	Zysset PK, Curnier A. A 3D damage model for trabecular bone based on fabric tensors. J Biomech. December 1996;29(12):1549-1558.
2010	Cristofolini L, Schileo E, Juszczyk M, Taddei F, Martelli S, Viceconti M. Mechanical testing of bones: the positive synergy of finite–element models and in vitro experiments. Philos Trans R Soc A-Math Phys Eng Sci. June 13, 2010;368(1920):2725-2763.
1998	Laib A, Häuselmann HJ, Rüegsegger P. In vivo high resolution 3D-QCT of the human forearm. Technol Health Care. 1998;6(5-6):329-337.
1994	Keaveny TM, Guo XE, Wachtel EF, McMahon TA, Hayes WC. Trabecular bone exhibits fully linear elastic behavior and yields at low strains. J Biomech. 1994;27(9):1127-1136.
2002	Turner CH. Biomechanics of bone: determinants of skeletal fragility and bone quality. Osteoporos Int. February 2002;13(2):97-104.
2009	Chevalier Y, Pahr D, Zysset PK. The role of cortical shell and trabecular fabric in finite element analysis of the human vertebral body. J Biomech Eng. November 2009;131(11):111003.
2009	Pahr DH, Zysset PK. From high-resolution CT data to finite element models: development of an integrated modular framework. Comput Methods Biomech Biomed Eng. 2009;12(1):45-57.
2003	Zysset PK. A review of morphology–elasticity relationships in human trabecular bone: theories and experiments. J Biomech. October 2003;36(10):1469-1485.
2008	Arbenz P, van Lenthe GH, Mennel U, Müller R, Sala M. A scalable multi‐level preconditioner for matrix‐free µ‐finite element analysis of human bone structures. Int J Num Meth Eng. February 12, 2008;73(7):927-947.
2006	Augat P, Schorlemmer S. The role of cortical bone and its microstructure in bone strength. Age Ageing. September 2006;35(suppl 2):ii27-ii31.
2007	McDonnell P, McHugh PE, O’Mahoney D. Vertebral osteoporosis and trabecular bone quality. Ann Biomed Eng. February 2007;35(2):170-189.
2009	Mueller TL, Stauber M, Kohler T, Eckstein F, Müller R, van Lenthe GH. Non-invasive bone competence analysis by high-resolution pQCT: an in vitro reproducibility study on structural and mechanical properties at the human radius. Bone. February 2009;44(2):364-371.
2004	Homminga J, Van-Rietbergen B, Lochmüller EM, Weinans H, Eckstein F, Huiskes R. The osteoporotic vertebral structure is well adapted to the loads of daily life, but not to infrequent “error” loads. Bone. March 2004;34(3):510-516.
2006	Imai K, Ohnishi I, Bessho M, Nakamura K. Nonlinear finite element model predicts vertebral bone strength and fracture site. Spine. July 15, 2006;31(16):1789-1794.
1999	Ulrich D, van Rietbergen B, Laib A, Rüegsegger P. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone. 1999;25(1):55-60.
2000	Kanis JA, Glüer C-C; Committee of Scientific Advisors, International Osteoporosis Foundation. An update on the diagnosis and assessment of osteoporosis with densitometry. Osteoporos Int. March 2000;11(3):192-202.
2004	Siris ES, Chen Y-T, Abbott TA, Barrett-Connor E, Miller PD, Wehren LE, Berger ML. Bone mineral density thresholds for pharmacological intervention to prevent fractures. Arch Intern Med. May 24, 2004;164(10):1108-1112.
2004	Dong XN, Guo XE. The dependence of transversely isotropic elasticity of human femoral cortical bone on porosity. J Biomech. August 2004;37(8):1281-1287.
2004	Kanis JA, Oden A, Johnell O, De Laet C, Jonsson B. Excess mortality after hospitalisation for vertebral fracture. Osteoporos Int. February 2004;15(2):108-112.
2009	Varga P, Baumbach S, Pahr D, Zysset PK. Validation of an anatomy specific finite element model of Colles’ fracture. J Biomech. August 7, 2009;42(11):1726-1731.
2000	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(1):32-40.
1996	Wenzel TE, Schaffler MB, Fyhrie DP. In vivo trabecular microcracks in human vertebral bone. Bone. August 1996;19(2):89-95.
2007	Buckley JM, Loo K, Motherway J. Comparison of quantitative computed tomography-based measures in predicting vertebral compressive strength. Bone. March 2007;40(3):767-774.
2008	Helgason B, Perilli E, Schileo E, Taddei F, Brynjólfsson S, Viceconti M. Mathematical relationships between bone density and mechanical properties: a literature review. Clin Biomech (Bristol, Avon). 2008;23(2):135-146.
2003	Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33(4):744-750.
2003	Ammann P, Rizzoli R. Bone strength and its determinants. Osteoporos Int. March 2003;14(suppl 3):S13-S18.
2005	Johnell O, Kanis J. Epidemiology of osteoporotic fractures. Osteoporos Int. March 2005;16(suppl 2):S3-S7.
2009	Garcia D, Zysset PK, Charlebois M, Curnier A. A three-dimensional elastic plastic damage constitutive law for bone tissue. Biomech Model Mechanobiol. April 2009;8(2):149-165.
2006	Viguet-Carrin S, Garnero P, Delmas PD. The role of collagen in bone strength. Osteoporos Int. March 2006;17(3):319-336.
2008	Chevalier Y, Charlebois M, Pahr D, Varga P, Heini P, Schneider E, Zysset P. A patient-specific finite element methodology to predict damage accumulation in vertebral bodies under axial compression, sagittal flexion and combined loads. Comput Methods Biomech Biomed Eng. October 2008;11(5):477-487.
2006	Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. December 2006;17(12):1726-1733.
1996	Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ. May 18, 1996;312(7041):1254-1259.
2003	Bouxsein ML. Bone quality: where do we go from here? Osteoporos Int. September 2003;14(suppl 5):S118-S127.

Cited By (34)

Year	Entry
2013	Dall'Ara E, Luisier B, Schmidt R, Kainberger F, Zysset P, Pahr D. A nonlinear QCT-based finite element model validation study for the human femur tested in two configurations in vitro. Bone. January 2013;52(1):27-38.
2023	Song F, Wei Y, Feng W, Fu R, Li Z, Gao X, Cheng X, Yang H. Biomechanical CT-computed bone strength predicts the risk of subsequent vertebral fracture. Bone. January 2023;166:116601.
2023	Gao X, Din RU, Cheng X, Yang H. Biomechanical MRI detects reduced bone strength in subjects with vertebral fractures. Bone. August 2023;173:116810.
2021	Ferreira AC, Cohen-Solal M, D’Haese PC, Ferreira A; European Renal Osteodystrophy (EUROD), an initiative of the CKD-MBD working group of the ERA-EDTA. The role of bone biopsy in the management of CKD-MBD. Calcif Tiss Int. April 2021;108(4):528-538.
2017	Dall’Ara E, Peña-Fernández M, Palanca M, Giorgi M, Cristofolini L, Tozzi G. Precision of digital volume correlation approaches for strain analysis in bone imaged with micro-computed tomography at different dimensional levels. Front Mater. November 8, 2017;4:31.
2019	Werner B, Ovesy M, Zysset PK. An explicit micro‐FE approach to investigate the post‐yield behaviour of trabecular bone under large deformations. Int J Num Meth Biomed Eng. May 2019;35(5):e3188.
2016	Jackman TM, DelMonaco AM, Morgan EF. Accuracy of finite element analyses of CT scans in predictions of vertebral failure patterns under axial compression and anterior flexion. J Biomech. January 25, 2016;49(2):267-275.
2017	Palanca M, Bodey AJ, Giorgi M, Viceconti M, Lacroix D, Cristofolini L, Dall'Ara E. Local displacement and strain uncertainties in different bone types by digital volume correlation of synchrotron microtomograms. J Biomech. June 14, 2017;58:27-36.
2018	Hussein AI, Louzeiro DT, Unnikrishnan GU, Morgan EF. Differences in trabecular microarchitecture and simplified boundary conditions limit the accuracy of quantitative computed tomography-based finite element models of vertebral failure. J Biomech Eng. February 2018;140(2):021004.
2014	Kopperdahl DL, Aspelund T, Hoffmann PF, Sigurdsson S, Siggeirsdottir K, Harris TB, Gudnason V, Keaveny TM. Assessment of incident spine and hip fractures in women and men using finite element analysis of CT scans. J Bone Miner Res. March 2014;29(3):570-580.
2015	Zysset P, Qin L, Lang T, Khosla S, Leslie WD, Shepherd JA, Schousboe JT, Engelke K. Clinical use of quantitative computed tomography–based finite element analysis of the hip and spine in the management of osteoporosis in adults: the 2015 ISCD official positions—part II. J Clin Densitom. July–September 2015;18(3):359-392.
2018	Oliviero S, Giorgi M, Dall'Ara E. Validation of finite element models of the mouse tibia using digital volume correlation. J Mech Behav Biomed Mater. October 2018;86:172-184.
2020	Doi T, Hirai S, Kaneko M, Ohashi S, Nakajima K, Oguchi F, Kato S, Taniguchi Y, Matsubayashi Y, Hayashi N, Tanaka S, Oshima Y. Bone strength of the proximal femur in healthy subjects with ossification of the posterior longitudinal ligament. Osteoporos Int. April 2020;31(4):757-763.
2020	Mosleh H, Rouhi G, Ghouchani A, Bagheri N. Prediction of fracture risk of a distal femur reconstructed with bone cement: QCSRA, FEA, and in-vitro cadaver tests. Phys Eng Sci Med. March 2020;43(1):269-277.
2017	Costa MC, Tozzi G, Cristofolini L, Danesi V, Viceconti M, Dall’Ara E. Micro finite element models of the vertebral body: validation of local displacement predictions. PLoS One. July 11, 2017;12(7):e0180151.
2014	Fonseca H, Moreira-Gonçalves D, Coriolano H-JA, Duarte JA. Bone quality: the determinants of bone strength and fragility. Sports Med. January 2014;44(1):37-53.
2013	Hussein Ali AI. 3-D Visualization and Prediction of Spine Fractures Under Axial Loading [PhD thesis]. Boston University; 2013.
2015	Jackman TM. Prediction of Vertebral Fractures Under Axial Compression and Anterior Flexion [PhD thesis]. Boston University; 2015.
2016	Florencio FL. Multiscale Modelling of Trabecular Bone: From Micro to Macroscale [PhD thesis]. Edinburgh, Scotland: University of Edinburgh; 2016.
2019	Fleps I. Assessing the Risk of Hip Fracture: Subject-Specific Dynamic Models for the Simulation of Sideways Fall Impact [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2019.
2022	Peruzzi CRP. Nanoscale Deformation Mechanisms and Yield Prediction of Lamellar Bone [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2022.
2018	Zimmermann Y. Développement d'une modélisation par éléments finis pour caractérisation non destructive de la biomécanique osseuse à partir d'images MICRO-CT [Master's thesis]. École polytechnique de Montréal; December 2018.
2018	Groenen KHJ. Spinal (in)stability in Metastatic Bone Disease: Experimental, Computational, and Clinical Perspectives [PhD thesis]. Radboud University; 2018.
2014	Bradke BS. The Role of Cortical and Cancellous Bone Quality on Vertebral Fragility [PhD thesis]. Troy, NY: Rensselaer Polytechnic Institute; April 2014.
2017	Owen R. Tissue Engineering an in Vitro Model of Osteoporosis [PhD thesis]. Sheffield, UK: University of Sheffield; October 2017.
2018	Costa MC. Prediction of the Risk of Vertebral Fracture in Patients With Metastatic Bone Lesions as a Tool for More Effective Patients’ Management [PhD thesis]. University of Sheffield; November 2018.
2019	Oliviero S. Non-Invasive Prediction of Bone Mechanical Properties of the Mouse Tibia in Longitudinal Preclinical Studies [PhD thesis]. University of Sheffield; January 2019.
2012	Dall'Ara E. QCT Based Finite Element Models of the Human Vertebra and Femur: Validation With Experiments and Comparison With Bone Densitometry [PhD thesis]. Vienna University of Technology; October 2012.
2018	Patel RR. Does Patient-Specific Implant Design Reduce Subsidence Risk in Lumbar Interbody Fusion? A Bottom Up Analysis of Methods to Reduce Vertebral Endplate Stress [PhD thesis]. University of Colorado Denver; 2018.
2013	Hosseini HS. Constitutive Modeling of Trabecular Bone in Large Strain Compression [PhD thesis]. Universität Bern; May 2013.
2013	Maquer G. Image-Based Biomechanical Assessment of Vertebral Body and Intervertebral Disc in the Human Lumbar Spine [PhD thesis]. Universität Bern; March 2013.
2017	Palanca M. In Vitro Full-Field Methods for the Biomechanical Characterization of Spine Segments [PhD thesis]. University of Bologna; March 2017.
2022	Xiao P. Medical Image-Based AI Techniques in Prediction of Trabecular Bone Microarchitecture and Mechanical Properties [PhD thesis]. San Antionio, TX: University of Texas at San Antonio; December 2022.
2019	Knowles NK. Improving Material Mapping in Glenohumeral Finite Element Models: A Multi-Level Evaluation [PhD thesis]. University of Western Ontario; 2019.