Abstract
For assessing mechanical properties of osteoporotic bone, biomechanical testing combined with in silico modeling plays a key role. The present study focuses on microscopic mechanical bone properties in a rat model of postmenopausal osteoporosis. Female Sprague–Dawley rats were (1) euthanized without prior interventions, (2) sham-operated, and (3) subjected to ovariectomy combined with a multi-deficiencies diet. Rat vertebrae (corpora vertebrae) were imaged by micro-CT, their stiffness was determined by compression tests, and load-induced stress states as well as property changes due to the treatment were analyzed by finite-element modeling. By comparing vertebra stiffness measurements with finite-element calculations of stiffness, an overall microscopic Young’s modulus of the bone was determined. Macroscopic vertebra stiffness as well as the microscopic modulus diminish with progression of osteoporosis by about 70 %. After strong initial changes of bone morphology, further decrease in macroscopic stiffness is largely due to decreasing microscopic Young’s modulus. The micromechanical stress calculations reveal particularly loaded vertebra regions prone to failure. Osteoporosis-induced changes of the microscopic Young’s modulus alter the fracture behavior of bone, may influence bone remodeling, and should be considered in the design of implant materials.







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Balay S, Brown J, Buschelman K, Gropp WD, Kaushik D, Knepley MG, Curfman McInnes L, Smith BF, Zhang H (2012) PETSc. http://www.mcs.anl.gov/petsc
Bevill G, Eswaran SK, Gupta A, Papadopoulos P, Keaveny TM (2006) Influence of bone volume fraction and architecture on computed large-deformation failure mechanisms in human trabecular bone. Bone 39(6):1218–1225
Broulik PD, Vondrova J, Ruzicka P, Sedlacek R, Zima T (2010) The effect of chronic alcohol administration on bone mineral content and bone strength in male rats. Physiol Res 59(4):599–604
Busse B, Hahn M, Soltau M, Zustin J, Püschel K, Duda GN, Amling M (2009) Increased calcium content and inhomogeneity of mineralization render bone toughness in osteoporosis: mineralization, morphology and biomechanics of human single trabeculae. Bone 45(6):1034–1043
Chappard D, Retailleau-Gaborit N, Legrand E, Basle MF, Audran M (2005) Comparison insight bone measurements by histomorphometry and microCT. J Bone Miner Res 20:1177–1184
Christensen RM (1991) Mechanics of composite materials. Krieger Publishing, Malabar, FL
El Khassawna T, Böcker W, Govindarajan P, Schliefke N, Hürter B, Kampschulte M, Schlewitz G, Alt V, Lips KS, Faulenbach M, Möllmann H, Zahner D, Dürselen L, Ignatius A, Bauer N, Wenisch S, Langheinrich AC, Schnettler R, Heiss C (2013) Effects of multi-deficiencies-diet on bone parameters of peripheral bone in ovariectomized mature rat. PLoS ONE 8:e71665
Frost HM (1994) Wolff’s law and bone’s structural adaptations to mechanical usage: an overview for clinicians. Angle Orthod 64:175–188
Govindarajan P, Schlewitz G, Schliefke N, Weisweiler D, Alt V, Thormann U, Lips KS, Wenisch S, Langheinrich AC, Zahner D, Hemdan NY, Böcker W, Schnettler R, Heiss C (2013) Implications of combined ovariectomy/multi-deficiency diet on rat bone with age-related variation in done parameters and bone loss at multiple skeletal sites by DEXA. Med Sci Monit Basic Res 19:76–86
Guo XE, Goldstein SA (2000) Vertebral trabecular bone microscopic tissue elastic modulus and hardness do not change in ovariectomized rats. J Orthop Res 18(2):333–336
Heiss C, Govindarajan P, Schlewitz G, Hemdan NY, Schliefke N, Alt V, Thormann U, Lips KS, Wenisch S, Langheinrich AC, Zahner D, Schnettler R (2012) Induction of osteoporosis with its influence on osteoporotic determinants and their interrelationships in rats by DEXA. Med Sci Monit 18:199–207
Henss A, Rohnke M, El Khassawna T, Govindarajan P, Schlewitz G, Heiss C, Janek J (2013) Applicability of ToF-SIMS for monitoring compositional changes in bone in a long-term animal model. J R Soc Interface 6:1742–5662
Kinney JH, Haupt DL, Balooch M, Ladd AJC, Ryaby JT, Lane NE (2000) Three-dimensional morphometry of the L6 vertebra in the ovariectomized rat model of osteoporosis: biomechanical implications. J Bone Miner Res 15(10):1981–1991
Ladd AJC, Kinney JH (1998) Numerical errors and uncertainties in finite-element modeling of trabecular bone. J Biomech 31(10):941–945
Ladd AJC, Kinney JH, Haupt DL, Goldstein SA (1998) Finite-element modeling of trabecular bone: comparison with mechanical testing and determination of tissue modulus. J Orthop Res 16(5):622–628
Lewis G, Nyman JS (2008) The use of nanoindentation for characterizing the properties of mineralized hard tissues: State-of-the art review. J Biomed Mater Res Appl Biomater 87B(1):286–301
Madi K, Aufort G, Gasser A, Forest S (2010) Prediction of the elastic modulus of the trabecular bone based on X-ray computed tomography. In: Lim CT, Goh JCH (eds) WCB 2010, IFMBE proceedings 31. Springer, Berlin, pp 800–803
Mueller TL, Stauber M, Kohler T, Eckstein F, Müller R, van Lenthe GH (2009) Non-invasive bone competence analysis by high-resolution pQCT: an in vitro reproducibility study on structural and mechanical properties at the human radius. Bone 44(2):364–371
Mueller TL, Christen D, Sandercott S, Boyd SK, van Rietbergen B, Eckstein F, Lochmüller EM, Müller R, van Lenthe GH (2011) Computational finite element bone mechanics accurately predicts mechanical competence in the human radius of an elderly population. Bone 48:1232–1238
Niebur GL, Feldstein MJ, Yuen JC, Chen TJ, Keaveny TM (2000) High-resolution finite element models with tissue strength asymmetry accurately predict failure of trabecular bone. J Biomech 33(12):1575–1583
Novitskaya E, Chen PY, Hamed E, Li J, Lubarda VA, Jasiuk I, McKittrick J (2011) Recent advances on the measurement and calculation of the elastic moduli of cortical and trabecular bone: a review. Theor Appl Mech 38(3):209–297
Pistoia W, van Rietbergen B, Lochmüller EM, Lill CA, Eckstein F, Rüegsegger 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(6):842–848
Rho JY, Ashman RB, Turner CH (1993) Young’s modulus of trabecular and cortical bone material: ultrasonic and microtensile measurements. J Biomech 26(2):111–119
Stemper BD, Board D, Yoganandan N, Wolfla CE (2010) Biomechanical properties of human thoracic spine disc segments. J Craniovertebr Junction Spine 1(1):18–22
Tsafnat N, Wroe S (2011) An experimentally validated micromechanical model of a rat vertebra under compressive loading. J Anat 218(1):40–46
Uhthof HK, Finneagan M (1983) The effects of metal plates on post-traumatic remodelling and bone mass. J Bone Joint Surg Br 65B:66–71
van Lenthe GH, Stauber M, Müller R (2006) Specimen-specific beam models for fast and accurate prediction of human trabecular bone mechanical properties. Bone 39(6):1182–1189
Vondrova J, Lukes J, Sedlacek R, Suchy T, Ruzicka P (2009) Comparative study of macro vs. micro test of osteoporotic rat bones. Bull Appl Mech 5(20):93–95
Wachtel EF, Keaveny TM (1997) Dependence of trabecular damage on mechanical strain. J Orthop Res 15(5):781–787
Acknowledgments
Our appreciation is to Gunhild Martels (Justus-Liebig-University, Gießen) for excellent technical support and to Anita Ignatius and Lutz Dürselen (University of Ulm, Medical Faculty) for making the compression tests possible. We thank Michael Kücken for critically reading the manuscript. This work was supported by the Deutsche Forschungsgemeinschaft (DFG) through SFB/TR 79. We gratefully acknowledge support from the German Excellence Initiative via the Cluster of Excellence EXC 1056 “Center for Advancing Electronics Dresden” (cfAED). The authors thank the Center for Information Services and High Performance Computing (ZIH) at the Dresden University of Technology for computational resources and the Cluster of excellence “Center for Regenerative Therapies Dresden” (CRTD) for additional help.
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Müller, R., Kampschulte, M., Khassawna, T.E. et al. Change of mechanical vertebrae properties due to progressive osteoporosis: combined biomechanical and finite-element analysis within a rat model. Med Biol Eng Comput 52, 405–414 (2014). https://doi.org/10.1007/s11517-014-1140-3
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DOI: https://doi.org/10.1007/s11517-014-1140-3