Simulation of vertebral trabecular bone loss using voxel finite element analysis

wbldb

Mc Donnell, P. ^1,2; Harrison, N.^1,2; Liebschner, M. A. K.³; Mc Hugh, P. E.^1,2

Simulation of vertebral trabecular bone loss using voxel finite element analysis

J Biomech. 2009;42(16):2789-2796

Affiliations

¹National Centre for Biomedical Engineering Science, National University of Ireland, Galway, Ireland

²Department of Mechanical and Biomedical Engineering, National University of Ireland, Galway, Ireland

³Baylor College of Medicine, Houston, TX, USA
Abstract and keywords

Trabecular bone loss in human vertebral bone is characterised by thinning and eventual perforation of the horizontal trabeculae. Concurrently, vertical trabeculae are completely lost with no histological evidence of significant thinning. Such bone loss results in deterioration in apparent modulus and strength of the trabecular core. In this study, a voxel-based finite element program was used to model bone loss in three specimens of human vertebral trabecular bone. Three sets of analyses were completed. In Set 1, strain adaptive resorption was modelled, whereby elements which were subject to the lowest mechanical stimulus (principal strain) were removed. In Set 2, both strain adaptive and microdamage mechanisms of bone resorption were included. Perforation of vertical trabeculae occurred due to microdamage resorption of elements with strains that exceeded a damage threshold. This resulted in collapse of the trabecular network under compression loading for two of the specimens tested. In Set 3, the damage threshold strain was gradually increased as bone loss progressed, resulting in reduced levels of microdamage resorption. This mechanism resulted in trabecular architectures in which vertical trabeculae had been perforated and which exhibited similar apparent modulus properties compared to experimental values reported in the literature. Our results indicate that strain adaptive remodelling alone does not explain the deterioration in mechanical properties that have been observed experimentally. Our results also support the hypothesis that horizontal trabeculae are lost principally by strain adaptive resorption, while vertical trabeculae may be lost due to perforation from microdamage resorption followed by rapid strain adaptive resorption of the remaining unloaded trabeculae.

Keywords: Cancellous bone; Osteoporosis; Remodelling
Links

DOI: 10.1016/j.jbiomech.2009.07.038

PubMed: 19782987

WoS: 000273135200025

Cited Works (28)

Year	Entry
1993	Snyder BD, Piazza S, Edwards WT, Hayes WC. Role of trabecular morphology in the etiology of age-related vertebral fractures. Calcif Tiss Int. February 1993;53(suppl 1):S14-S22.
2006	Ün K, Bevill G, Keaveny TM. The effects of side-artifacts on the elastic modulus of trabecular bone. J Biomech. 2006;39(11):1955-1963.
2003	Morgan EF, Bayraktar HH, Keaveny TM. Trabecular bone modulus–density relationships depend on anatomic site. J Biomech. July 2003;36(7):897-904.
1997	Nicholson PHF, Cheng XG, Lowet G, Boonen S, Davie MWJ, Dequeker J, Van der Perre G. Structural and material mechanical properties of human vertebral cancellous bone. Med Eng Phys. October 1997;19(8):729-737.
1998	Hou FJ, Lang SM, Hoshaw SJ, Reimann DA, Fyhrie DP. Human vertebral body apparent and hard tissue stiffness. J Biomech. November 1998;31(11):1009-1015.
2007	McNamara LM, Prendergast PJ. Bone remodelling algorithms incorporating both strain and microdamage stimuli. J Biomech. 2007;40(6):1381-1391.
1997	Mori S, Harruff R, Ambrosius W, Burr DB. Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone. December 1997;21(6):521-526.
1997	Rho J-Y, Tsui TY, Pharr GM. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials. 1997;18(20):1325-1330.
2008	Chen H, Shoumura S, Emura S, Bunai Y. Regional variations of vertebral trabecular bone microstructure with age and gender. Osteoporos Int. October 2008;19(10):1473-1483.
1998	Kopperdahl DL, Keaveny TM. Yield strain behavior of trabecular bone. J Biomech. July 1998;31(7):601-608.
1989	Mosekilde L. Sex differences in age-related loss of vertebral trabecular bone mass and structure—biomechanical consequences. Bone. 1989;10(6):425-432.
2006	Allen MR, Iwata K, Phipps R, Burr DB. Alterations in canine vertebral bone turnover, microdamage accumulation, and biomechanical properties following 1-year treatment with clinical treatment doses of risedronate or alendronate. Bone. October 2006;39(4):872-879.
2004	Bayraktar HH, Morgan EF, Niebur GL, Morris GE, Wong EK, Keaveny TM. Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech. January 2004;37(1):27-35.
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.
1997	Turner CH, Annet V, Pidaparti RMV. A uniform strain criterion for trabecular bone adaptation: do continuum-level strain gradients drive adaptation? J Biomech. June 1997;30(6):555-563.
2006	McNamara LM, Van der Linden JC, Weinans H, Prendergast PJ. Stress-concentrating effect of resorption lacunae in trabecular bone. J Biomech. 2006;39(4):734-741.
2008	Harrison NM, McDonnell PF, O’Mahoney DC, Kennedy OD, O’Brien FJ, McHugh PE. Heterogeneous linear elastic trabecular bone modelling using micro-CT attenuation data and experimentally measured heterogeneous tissue properties. J Biomech. August 7, 2008;41(11):2589-2596.
2008	Arlot ME, Burt‐Pichat B, Roux J, Vashishth D, Bouxsein ML, Delmas PD. Microarchitecture influences microdamage accumulation in human vertebral trabecular bone. J Bone Miner Res. 2008;23(10):1613-1618.
2005	Ruimerman R, Hilbers P, van Rietbergen B, Huiskes R. A theoretical framework for strain-related trabecular bone maintenance and adaptation. J Biomech. April 2005;38(4):931-941.
1997	Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford). 1997;185(1):67-75.
2007	Bevill G, Easley SK, Keaveny TM. Side-artifact errors in yield strength and elastic modulus for human trabecular bone and their dependence on bone volume fraction and anatomic site. J Biomech. 2007;40(15):3381-3388.
2002	Thomsen JS, Ebbesen EN, Mosekilde L. Age-related differences between thinning of horizontal and vertical trabeculae in human lumbar bone as assessed by a new computerized method. Bone. July 2002;31(1):136-142.
2002	Fazzalari NL, Kuliwaba JS, Forwood MR. Cancellous bone microdamage in the proximal femur: influence of age and osteoarthritis on damage morphology and regional distribution. Bone. December 2002;31(6):697-702.
1998	Mullender M, van Rietbergen B, Rüegsegger P, Huiskes R. Effect of mechanical set point of bone cells on mechanical control of trabecular bone architecture. Bone. February 1998;22(2):125-131.
1997	Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res. January 1997;12(1):6-15.
2000	Mosekilde L. Age-related changes in bone mass, structure, and strength: effects of loading. Z Rheumatol. February 2000;59(suppl 1):I1-I9.
2000	Hirano T, Turner CH, Forwood MR, Johnston CC, Burr DB. Does suppression of bone turnover impair mechanical properties by allowing microdamage accumulation? Bone. July 2000;27(1):13-20.
2000	Huiskes R, Ruimerman R, van Lenthe GH, Janssen JD. Effects of mechanical forces on maintenance and adaptation of form in trabecular bone. Nature. June 8, 2000;405(6787):704-706.

Cited By (8)

Year	Entry
2013	Harrison NM, McDonnell P, Mullins L, Wilson N, O’Mahoney D, McHugh PE. Failure modelling of trabecular bone using a non-linear combined damage and fracture voxel finite element approach. Biomech Model Mechanobiol. April 2013;12(2):225-241.
2013	Thomsen JS, Niklassen AS, Ebbesen EN, Brüel A. Age-related changes of vertical and horizontal lumbar vertebral trabecular 3D bone microstructure is different in women and men. Bone. November 2013;57(1):47-55.
2016	Fan R, Gong H, Zhang X, Liu J, Jia Z, Zhu D. Modeling the mechanical consequences of age-related trabecular bone loss by XFEM simulation. Computat Math Methods Med. 2016;2016:3495152.
2012	Kelly N, McGarry JP. Experimental and numerical characterisation of the elasto-plastic properties of bovine trabecular bone and a trabecular bone analogue. J Mech Behav Biomed Mater. May 2012;9:184-197.
2011	Yan Y-B, Qi W, Wang J, Liu L-F, Teo E-C, Tianxia Q, Ba J-j, Lei W. Relationship between architectural parameters and sample volume of human cancellous bone in micro-CT scanning. Med Eng Phys. July 2011;33(6):764-769.
2019	Du J. Mechanical Adaptation of Human Trabecular Bone: Experimental and Computational Study [PhD thesis]. Loughborough University; 2019.
2012	Kelly N. An Experimental and Computational Investigation of the Inelastic Behaviour of Trabecular Bone [PhD thesis]. Galway, Ireland: National University of Ireland Galway; September 2012.
2010	Fields AJ. Trabecular Microarchitecture, Endplate Failure, and the Biomechanics of Human Vertebral Fractures [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2010.