Skip to main content
Log in

Modeling orthotropic elasticity, localized plasticity and fracture in trabecular bone

  • Original Paper
  • Published:
Computational Mechanics Aims and scope Submit manuscript

Abstract

This work develops a model for the mechanical response of trabecular bone including plasticity, damage and fracture. It features a resultant lamellar orientation that captures trabecular strut anisotropic elasticity, and introduces asymmetric J2 plasticity with isotropic hardening to capture evolving strut tensile and compressive dissipative properties. A continuum compatibility based damage and fracture criterion is also proposed to model fracture surface generation. We investigated fracture of a trabecular bone network under a compressive load, for which failure modes of both tension and compression were identified at the strut level. The predicted trabecular network response was found to fall within the range of experimental results reported in literature. We also investigated the response of idealized struts under compression, tension and bending using our model. Individual struts were found to exhibit micro-buckling under compression and micro-necking under tension. These instabilities are however masked by the multiplicity and complexity of strut orientations at the trabecular network level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15

Similar content being viewed by others

References

  1. Rho J-Y, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20:92–102

    Article  Google Scholar 

  2. 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 33:1575–1583

    Article  Google Scholar 

  3. Niebur GL, Keaveny TM (2010) Computational modeling of trabecular bone. Comput Model Biomech 305:277–306

    Article  Google Scholar 

  4. Cummings SR, Karpf DB, Harris F, Genant HK, Ensrud K, Lacroix AZ, Black DM (2002) Improvement in spine bone density and reduction in risk of vertebral fractures during treatment with antiresorptive drugs. Am J Med 112:281–289

    Article  Google Scholar 

  5. Stölken J, Kinney J (2003) On the importance of geometric nonlinearity in finite-element simulations of trabecular bone failure. Bone 33:494–504

    Article  Google Scholar 

  6. Bayraktar HH, Keaveny TM (2004) A computational investigation of the nonlinear behavior of human trabecular bone. Transactions of the 12th annual pre-ORS symposium on computational methods in orthopaedic biomechnics

  7. Ritchie RO, Buehler MJ, Hansma P (2009) Plasticity and toughness in bone. Phys Today 62:41–47

    Article  Google Scholar 

  8. Chevalier Y, Pahr D, Allmer H, Charlebois M, Zysset P (2007) Validation of a voxel-based FE method for prediction of the uniaxial apparent modulus of human trabecular bone using macroscopic mechanical tests and nanoindentation. J Biomech 40:3333–3340

    Article  Google Scholar 

  9. Yeh OC, Keaveny TM (2001) Relative roles of microdamage and microfracture in the mechanical behavior of trabecular bone. J Orthop Res 19:1001–1007

    Article  Google Scholar 

  10. van Rietbergen B, Weinans H, Huiskes R, Odgaard A (1995) A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. J Biomech 28:69–81

    Article  Google Scholar 

  11. Bevill G, Keaveny TM (2009) Trabecular bone strength predictions using finite element analysis of micro-scale images at limited spatial resolution. Bone 44:579–584

    Article  Google Scholar 

  12. Harrison NM, McDonnell P, Mullins L, Wilson N, O’Mahoney D, McHugh PE (2013) Failure modelling of trabecular bone using a non-linear combined damage and fracture voxel finite element approach. Biomech Model Mechanobiol 12:225–241

    Article  Google Scholar 

  13. Keaveny TM, Morgan EF, Niebur GL, Yeh OC (2001) Biomechanics of trabecular bone. Annu Rev Biomed Eng 3:307–333

    Article  Google Scholar 

  14. Akhtar R, Eichhorn S, Mummery P (2006) Microstructure-based finite element modelling and characterisation of bovine trabecular bone. J Bionic Eng 3:3–9

    Article  Google Scholar 

  15. Gong H, Wang L, Fan Y, Zhang M, Qin L (2015) Apparent-and tissue-level yield behaviors of l4 vertebral trabecular bone and their associations with microarchitectures. Ann Biomed Eng 44:1–20

    Google Scholar 

  16. Sanyal A, Keaveny TM (2013) Biaxial normal strength behavior in the axial-transverse plane for human trabecular boneeffects of bone volume fraction, microarchitecture, and anisotropy. J Biomech Eng 135:121010

    Article  Google Scholar 

  17. Sanyal A, Gupta A, Bayraktar HH, Kwon RY, Keaveny TM (2012) Shear strength behavior of human trabecular bone. J Biomech 45:2513–2519

    Article  Google Scholar 

  18. Tsouknidas A, Maliaris G, Savvakis S, Michailidis N (2015) Anisotropic post-yield response of cancellous bone simulated by stress–strain curves of bulk equivalent structures. Comput Methods Biomech Biomed Engin 18:839–846

    Article  Google Scholar 

  19. Lü L, Meng G, Gong H, Zhu D, Gao J, Fan Y (2015) Tissue level microstructure and mechanical properties of the femoral head in the proximal femur of fracture patients. Acta Mech Sin 31:1–9

    Article  MathSciNet  Google Scholar 

  20. Wolfram U, Gross T, Pahr DH, Schwiedrzik J, Wilke H-J, Zysset PK (2012) Fabric-based tsai-wu yield criteria for vertebral trabecular bone in stress and strain space. J Mech Behav Biomed Mater 15:218–228

    Article  Google Scholar 

  21. Nawathe S, Juillard F, Keaveny TM (2013) Theoretical bounds for the influence of tissue-level ductility on the apparent-level strength of human trabecular bone. J Biomech 46:1293–1299

    Article  Google Scholar 

  22. 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 39:1218–1225

    Article  Google Scholar 

  23. Bayraktar HH, Morgan EF, Niebur GL, Morris GE, Wong EK, Keaveny TM (2004) Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J Biomech 37:27–35

    Article  Google Scholar 

  24. Guillén T, Zhang Q-H, Tozzi G, Ohrndorf A, Christ H-J, Tong J (2011) Compressive behaviour of bovine cancellous bone and bone analogous materials, microct characterisation and Fe analysis. J Mech Behav Biomed Mater 4:1452–1461

    Article  Google Scholar 

  25. Gross T, Pahr D (2013) Influence of mesh size and element type on apparent yield properties of microct based finite element models of human trabecular bone. Comput Vis Med Image Process IV VIPIMAGE 2013:415

    Google Scholar 

  26. Kelly N, McGarry JP (2012) Experimental and numerical characterisation of the elasto-plastic properties of bovine trabecular bone and a trabecular bone analogue. J Mech Behav Biomed Mater 9:184–197

    Article  Google Scholar 

  27. Schwiedrzik J, Gross T, Bina M, Pretterklieber M, Zysset P, Pahr D (2015) Experimental validation of a nonlinear \(\mu \)fe model based on cohesive-frictional plasticity for trabecular bone. Int J Numer Method Biomed Eng 32:1–12

    Google Scholar 

  28. Mercer C, He M, Wang R, Evans A (2006) Mechanisms governing the inelastic deformation of cortical bone and application to trabecular bone. Acta Biomater 2:59–68

    Article  Google Scholar 

  29. Verhulp E, Van Rietbergen B, Müller R, Huiskes R (2008) Micro-finite element simulation of trabecular-bone post-yield behaviour-effects of material model, element size and type. Comput Methods Biomech Biomed Engin 11:389–395

    Article  Google Scholar 

  30. Shi X, Liu XS, Wang X, Guo XE, Niebur GL (2010) Effects of trabecular type and orientation on microdamage susceptibility in trabecular bone. Bone 46:1260–1266

    Article  Google Scholar 

  31. Hambli R (2013) Micro-CT finite element model and experimental validation of trabecular bone damage and fracture. Bone 56:363–374

    Article  Google Scholar 

  32. Martin R, Ishida J (1989) The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech 22:419–426

    Article  Google Scholar 

  33. Benecke G, Kerschnitzki M, Fratzl P, Gupta HS (2011) Digital image correlation shows localized deformation bands in inelastic loading of fibrolamellar bone. J Mater Res 24:421–429

    Article  Google Scholar 

  34. Jungmann R, Szabo M, Schitter G, Tang RY-S, Vashishth D, Hansma P, Thurner P (2011) Local strain and damage mapping in single trabeculae during three-point bending tests. J Mech Behav Biomed Mater 4:523–534

    Article  Google Scholar 

  35. Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P (2006) Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci USA 103:17741–17746

    Article  Google Scholar 

  36. Thurner P, Erickson B, Jungmann R, Schriock Z, Weaver J, Fantner G, Schitter G, Morse D, Hansma P (2007) High-speed photography of compressed human trabecular bone correlates whitening to microscopic damage. Eng Fract Mech 74:1928–1941

    Article  Google Scholar 

  37. Aerssens J, Boonen S, Lowet G, Dequeker J (1998) Interspecies differences in bone composition, density, and quality: potential implications for in vivo bone research. Endocrinology 139:663–670

    Google Scholar 

  38. Ingomar Jäger PF (2000) Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. Biophys J 79:1737–1746

    Article  Google Scholar 

  39. Kabel J, van Rietbergen B, Dalstra M, Odgaard A, Huiskes R (1999) The role of an effective isotropic tissue modulus in the elastic properties of cancellous bone. J Biomech 32:673–680

    Article  Google Scholar 

  40. Zysset P, Goulet R, Hollister S (1998) A global relationship between trabecular bone morphology and homogenized elastic properties. J Biomech Eng 120:640–646

    Article  Google Scholar 

  41. Fantner GE, Hassenkam T, Kindt JH, Weaver JC, Birkedal H, Pechenik L, Cutroni Ja, Cidade GaG, Stucky GD, Morse DE, Hansma PK (2005) Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat Mater 4:612–616

    Article  Google Scholar 

  42. Fantner GE, Oroudjev E, Schitter G, Golde LS, Thurner P, Finch MM, Turner P, Gutsmann T, Morse DE, Hansma H, Hansma PK (2006) Sacrificial bonds and hidden length: unraveling molecular mesostructures in tough materials. Biophys J 90:1411–1418

    Article  Google Scholar 

  43. Gupta HS, Wagermaier W, Zickler G a, Raz-Ben Aroush D, Funari SS, Roschger P, Wagner HD, Fratzl P (2005) Nanoscale deformation mechanisms in bone. Nano Lett 5:2108–2111

    Article  Google Scholar 

  44. Garcia D, Zysset PK, Charlebois M, Curnier A (2009) A three-dimensional elastic plastic damage constitutive law for bone tissue. Biomech Model Mechanobiol 8:149–165

    Article  MATH  Google Scholar 

  45. Bayraktar HH, Gupta A, Kwon RY, Papadopoulos P, Keaveny TM (2005) The modified super-ellipsoid yield criterion for human trabecular bone. J Biomech Eng 126:677–684

    Article  Google Scholar 

  46. Cazacu O, Barlat F (2004) A criterion for description of anisotropy and yield differential effects in pressure-insensitive metals. Int J Plast 20:2027–2045

    Article  MATH  Google Scholar 

  47. Terrier A, Rakotomanana R, Ramaniraka A, Leyvraz P (1997) Adaptation models of anisotropic bone. Comput Methods Biomech Biomed Engin 1:47–59

    Article  Google Scholar 

  48. Fan Z, Rho J, Swadener J (2004) Three-dimensional finite element analysis of the effects of anisotropy on bone mechanical properties measured by nanoindentation. J Mater Res 19:114–123

    Article  Google Scholar 

  49. Hill R (1948) A theory of the yielding and plastic flow of anisotropic metals. Proc R Soc Lond Ser A 193:281–297

    Article  MathSciNet  MATH  Google Scholar 

  50. Belytschko T, Liu W, Moran B, Elkhodary K (2013) Nonlinear finite elements for continua and structures. Wiley, Chichester

    MATH  Google Scholar 

  51. Engelen RAB, Fleck NA, Peerlings RHJ, Geers MGD (2006) An evaluation of higher-order plasticity theories for predicting size effects and localisation. Int J Solids Struct 43:1857–1877

    Article  MATH  Google Scholar 

  52. Vernerey FJ, Liu WK, Moran B, Olson G (2006) A micromorphic model for the multiple scale failure of heterogeneous materials. J Mech Phys Solids 56:1320–1347

    Article  MathSciNet  MATH  Google Scholar 

  53. Vernerey FJ, Liu WK, Moran B (2007) Multiscale micromorphic theory for hierarchical materials. J Mech Phys Solids 55:2603–2651

    Article  MathSciNet  MATH  Google Scholar 

  54. Lai WM, Rubin DH, Rubin D, Krempl E (2009) Introduction to continuum mechanics. Butterworth-Heinemann, New York

    MATH  Google Scholar 

  55. Elkhodary K, Zikry M (2011) A fracture criterion for finitely deforming crystalline solids—the dynamic fracture of single crystals. J Mech Phys Solids 59:2007–2022

    Article  MATH  Google Scholar 

  56. Elkhodary K, Zikry M (2012) Dynamic crack nucleation and propagation in polycrystalline aluminum aggregates subjected to large inelastic deformations. Int J Fract 175:95–108

    Article  Google Scholar 

  57. Kröner E (1981) Continuum theory of defects. In: Balian R (ed) Proceedings of summer school on the physics of defects. North-Holland, Amsterdam, Les Houches, Fr., pp 215–315

  58. Hibbit H, Karlsson B, Sorensen P (2007) ABAQUS analysis user’s manual, 6.7, ABAQUS. http://scholar.google.com/scholar?q=Hibbitt+ABAQUS++2007&btnG=&hl=en&as_sdt=0,14#4

  59. Song J, Wang H, Belytschko T (2008) A comparative study on finite element methods for dynamic fracture. Comput Mech 42:239–250

  60. Ulrich D, Rietbergen BV, van Rietbergen B, Weinans H, Rüegsegger P (1998) Finite element analysis of trabecular bone structure: a comparison of image-based meshing techniques. J Biomech 31:1187–1192

    Article  Google Scholar 

  61. Zhang Y, Hughes T, Bajaj C (2010) An automatic 3D mesh generation method for domains with multiple materials. Comput Methods Appl Mech Eng 199:405–415

    Article  MATH  Google Scholar 

  62. Zhang Y, Bajaj C, Sohn B (2005) 3D finite element meshing from imaging data. Comput Methods Appl Mech Eng 194:5083–5106

    Article  MATH  Google Scholar 

  63. Zhang Y, Bajaj C (2006) Adaptive and quality quadrilateral/hexahedral meshing from volumetric data. Comput Methods Appl Mech Eng 195:942–960

    Article  MathSciNet  MATH  Google Scholar 

  64. Zhang Y, Xu G, Bajaj C (2006) Quality meshing of implicit solvation models of biomolecular structures. Comput Aided Geom Des 23:510–530

    Article  MathSciNet  MATH  Google Scholar 

  65. Zhang Y, Bajaj C, Xu G (2009) Surface smoothing and quality improvement of quadrilateral/hexahedral meshes with geometric flow. Commun Numer Methods Eng 25:1–18

    Article  MathSciNet  MATH  Google Scholar 

  66. Martin R, Boardman D (1993) The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties. J Biomech 26:1047–1054

    Article  Google Scholar 

  67. Goldstein SA, Wilson DL, Sonstegard DA, Matthews LS (1983) The mechanical properties of human tibial trabecular bone as a function of metaphyseal location. J Biomech 16:965–969

    Article  Google Scholar 

Download references

Acknowledgments

D.T. O’Connor would like acknowledge the National Physical Sciences Consortium (NPSC) and Argonne National Laboratory for their partial support. K.I. Elkhodary gratefully acknowledges the financial and technical support received from AUC for this research. J. Qian and Y. Zhang were supported in part by NSF CAREER Award OCI-1149591.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. I. Elkhodary.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

O’Connor, D.T., Elkhodary, K.I., Fouad, Y. et al. Modeling orthotropic elasticity, localized plasticity and fracture in trabecular bone. Comput Mech 58, 423–439 (2016). https://doi.org/10.1007/s00466-016-1301-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00466-016-1301-3

Keywords

Navigation