Skip to main content
Log in

Mechanical and microarchitectural analyses of cancellous bone through experiment and computer simulation

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

Abstract

The relationship between microarchitecture to the failure mechanism and mechanical properties can be assessed through experimental and computational methods. In this study, both methods were utilised using bovine cadavers. Twenty four samples of cancellous bone were extracted from fresh bovine and the samples were cleaned from excessive marrow. Uniaxial compression testing was performed with displacement control. After mechanical testing, each specimen was ashed in a furnace. Four of the samples were exemplarily scanned using micro-computed tomography (μCT) and three dimensional models of the cancellous bones were reconstructed for finite element simulation. The mechanical properties and the failure modes obtained from numerical simulations were then compared to the experiments. Correlations between microarchitectural parameters to the mechanical properties and failure modes were then made. The Young’s modulus correlates well with the bone volume fraction with R 2 = 0.615 and P value 0.013. Three different types of failure modes of cancellous bone were observed: oblique fracture (21.7%), perpendicular global fracture (47.8%), and scattered localised fracture (30.4%). However, no correlations were found between the failure modes to the morphological parameters. The percentage of error between computer predictions and the actual experimental test was from 6 to 12%. These mechanical properties and information on failure modes can be used for the development of synthetic cancellous bone.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Kaneko TS, Bell JS, Pejcic MR, Tehranzadeh J, Keyak JH (2004) Mechanical properties, density and quantitative CT scan data of trabecular bone with and without metastases. J Biomech 37:523–530

    Article  PubMed  Google Scholar 

  2. Majumdar S, Kothari M, Augat P, Newitt DC, Link TM, Lin JC, Lang T, Lu Y, Genant HK (1998) High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone 22:445–454

    Article  PubMed  CAS  Google Scholar 

  3. van Lenthe GH, Stauber M, Müller R (2006) Specimen-specific beam models for fast and accurate prediction of human trabecular bone mechanical properties. Bone 39:1182–1189

    Article  PubMed  Google Scholar 

  4. Shim VPW, Yang LM, Liu JF, Lee VS (2005) Characterisation of the dynamic compressive mechanical properties of cancellous bone from the human cervical spine. Int J Impact Eng 32:525–540

    Article  Google Scholar 

  5. 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  PubMed  Google Scholar 

  6. Verhulp E, van Rietbergen B, Müller R, Huiskes R (2008) Indirect determination of trabecular bone effective tissue failure properties using micro-finite element simulations. J Biomech 41:1479–1485

    Article  PubMed  CAS  Google Scholar 

  7. Joshua AM, Steven KB (2008) Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42:1203–1213

    Article  Google Scholar 

  8. Bourne BC, van der Meulen MCH (2004) Finite element models predict cancellous apparent modulus when tissue modulus is scaled from specimen CT-attenuation. J Biomech 37:613–621

    Article  PubMed  Google Scholar 

  9. van den Bergh JPW, van Lenthe GH, Hermus ARMM, Corstens FHM, Smals AGH, Huiskes R (2000) Speed of sound reflects Young’s modulus as assessed by microstructural finite element analysis. Bone 26:519–524

    Article  PubMed  Google Scholar 

  10. 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  PubMed  CAS  Google Scholar 

  11. Müller R, Rügsegger P (1995) Three-dimensional finite element modelling of non-invasively assessed trabecular bone structures. Med Eng Phys 17:126–133

    Article  PubMed  Google Scholar 

  12. Burghardt A, Kazakia G, Majumdar S (2007) A local adaptive threshold strategy for high resolution peripheral quantitative computed tomography of trabecular bone. Ann Biomed Eng 35:1678–1686

    Article  PubMed  Google Scholar 

  13. Pressel T, Bouguecha A, Vogt U, Meyer-Lindenberg A, Behrens B-A, Nolte I, Windhagen H (2005) Mechanical properties of femoral trabecular bone in dogs. Biomed Eng Online 4:17

    Article  PubMed  Google Scholar 

  14. Tony Keaveny M, Tania Pinilla P, Paul Crawford R, David Kopperdahl L, Lou A (1997) Systematic and random errors in compression testing of trabecular bone. J Orthop Res 15:101–110

    Article  Google Scholar 

  15. 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  PubMed  Google Scholar 

  16. Perilli E, Baleani M, Ohman C, Fognani R, Baruffaldi F, Viceconti M (2008) Dependence of mechanical compressive strength on local variations in microarchitecture in cancellous bone of proximal human femur. J Biomech 41:438–446

    Article  PubMed  CAS  Google Scholar 

  17. Chen H, Shoumura S, Emura S, Bunai Y (2008) Regional variations of vertebral trabecular bone microstructure with age and gender. Osteoporos Int 19:1473–1483

    Article  PubMed  CAS  Google Scholar 

  18. Nazarian A, Stauber M, Zurakowski D, Snyder BD, Müller R (2006) The interaction of microstructure and volume fraction in predicting failure in cancellous bone. Bone 39:1196–1202

    Article  PubMed  Google Scholar 

  19. 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  PubMed  Google Scholar 

  20. Bevill G, Farhamand F, Keaveny TM (2009) Heterogeneity of yield strain in low-density versus high-density human trabecular bone. J Biomech 42:2165–2170

    Article  PubMed  Google Scholar 

  21. Morgan EF, Bayraktar HH, Keaveny TM (2003) Trabecular bone modulus-density relationships depend on anatomic site. J Biomech 36:897–904

    Article  PubMed  Google Scholar 

  22. McCalden RW, McGeough JA, Court-Brown CM (1997) Age-related changes in the compressive strength of cancellous bone. The relative importance of changes in density and trabecular architecture. J Bone Joint Surg Am 79:421–427

    PubMed  CAS  Google Scholar 

  23. Samuel SP (2004) Fluid/solid interactions in cancellous bone. D. Eng., Cleveland State University, United States

  24. Smith E, Gilligan C (1991) Physical activity effects on bone metabolism. Calcif Tissue Int 49:S50–S54

    Article  PubMed  Google Scholar 

  25. Rincón-Kohli L, Zysset P (2009) Multi-axial mechanical properties of human trabecular bone. Biomech Model Mechanobiol 8:195–208

    Article  PubMed  Google Scholar 

  26. Morita M, Ebihara A, Itoman M, Sasada T (1994) Progression of osteoporosis in cancellous bone depending on trabecular structure. Ann Biomed Eng 22:532–539

    Article  PubMed  CAS  Google Scholar 

  27. Perilli E, Baleani M, Ohman C, Baruffaldi F, Viceconti M (2007) Structural parameters and mechanical strength of cancellous bone in the femoral head in osteoarthritis do not depend on age. Bone 41:760–768

    Article  PubMed  CAS  Google Scholar 

  28. Joshi MG, Advani SG, Miller F, Santare MH (2000) Analysis of a femoral hip prosthesis designed to reduce stress shielding. J Biomech 33:1655–1662

    Article  PubMed  CAS  Google Scholar 

  29. Ulrich D, van Rietbergen B, Laib A, Rügsegger P (1999) The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25:55–60

    Article  PubMed  CAS  Google Scholar 

  30. Beck JD, Canfield BL, Haddock SM, Chen TJH, Kothari M, Keaveny TM (1997) Three-dimensional imaging of trabecular bone using the computer numerically controlled milling technique. Bone 21:281–287

    Article  PubMed  CAS  Google Scholar 

  31. Teo JCM, Si-Hoe KM, Keh JEL, Teoh SH (2007) Correlation of cancellous bone microarchitectural parameters from microCT to CT number and bone mechanical properties. Mater Sci Eng C 27:333–339

    Article  CAS  Google Scholar 

  32. van Lenthe GH, Huiskes R (2002) How morphology predicts mechanical properties of trabecular structures depends on intra-specimen trabecular thickness variations. J Biomech 35:1191–1197

    Article  PubMed  Google Scholar 

  33. Willems NMBK, Mulder L, Langenbach GEJ, Grunheid T, Zentner A, van Eijden TMGJ (2007) Age-related changes in microarchitecture and mineralization of cancellous bone in the porcine mandibular condyle. J Struct Biol 158:421–427

    Article  PubMed  CAS  Google Scholar 

  34. Nagaraja S, Lin ASP, Guldberg RE (2007) Age-related changes in trabecular bone microdamage initiation. Bone 40:973–980

    Article  PubMed  Google Scholar 

  35. Ford CM, Keaveny TM (1996) The dependence of shear failure properties of trabecular bone on apparent density and trabecular orientation. J Biomech 29:1309–1317

    Article  PubMed  CAS  Google Scholar 

  36. van der Linden JC, Birkenhager-Frenkel DH, Verhaar JAN, Weinans H (2001) Trabecular bone’s mechanical properties are affected by its non-uniform mineral distribution. J Biomech 34:1573–1580

    Article  PubMed  Google Scholar 

  37. Odgaard A (1997) Three-dimensional methods for quantification of cancellous bone architecture. Bone 20:315–328

    Article  PubMed  CAS  Google Scholar 

  38. Kadir M, Syahrom A, Öchsner A (2010) Finite element analysis of idealised unit cell cancellous structure based on morphological indices of cancellous bone. Med Biol Eng Comput 48:497–505

    Article  PubMed  Google Scholar 

  39. Karande TS, Ong JL, Agrawal CM (2004) Diffusion in musculoskeletal tissue engineering scaffolds: design issues related to porosity, permeability, architecture, and nutrient mixing. Ann Biomed Eng 32:1728–1743

    Article  PubMed  Google Scholar 

  40. Shin HC, Yoon YS (2006) Bone temperature estimation during orthopaedic round bur milling operations. J Biomech 39:33–39

    Article  PubMed  CAS  Google Scholar 

  41. Carter D, Hayes W (1977) The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg Am 59:954–962

    PubMed  CAS  Google Scholar 

  42. Grimm MJ, Williams JL (1997) Measurements of permeability in human calcaneal trabecular bone. J Biomech 30:743–745

    Article  PubMed  CAS  Google Scholar 

  43. Kohles SS, Roberts JB, Upton ML, Wilson CG, Bonassar LJ, Schlichting AL (2001) Direct perfusion measurements of cancellous bone anisotropic permeability. J Biomech 34:1197–1202

    Article  PubMed  CAS  Google Scholar 

  44. Rapillard L, Charlebois M, Zysset PK (2006) Compressive fatigue behavior of human vertebral trabecular bone. J Biomech 39:2133–2139

    Article  PubMed  Google Scholar 

  45. Burgers TA, Mason J, Niebur G, Ploeg HL (2008) Compressive properties of trabecular bone in the distal femur. J Biomech 41:1077–1085

    Article  PubMed  Google Scholar 

  46. Kang Q, An YH, Friedman RF (1998) Mechanical properties and bone densities of canine trabecular bone. J Mater Sci Mater Med 9:263–267

    Article  PubMed  CAS  Google Scholar 

  47. Ciarelli MJ, Goldstein SA, Kuhn JL, Cody DD, Brown MB (1991) Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res 9:674–682

    Article  PubMed  CAS  Google Scholar 

  48. Homminga J, McCreadie BR, Weinans H, Huiskes R (2003) The dependence of the elastic properties of osteoporotic cancellous bone on volume fraction and fabric. J Biomech 36:1461–1467

    Article  PubMed  Google Scholar 

  49. Morgan EF, Bayraktar HH, Yeh OC, Majumdar S, Burghardt A, Keaveny TM (2004) Contribution of inter-site variations in architecture to trabecular bone apparent yield strains. J Biomech 37:1413–1420

    Article  PubMed  Google Scholar 

  50. Bayraktar HH, Keaveny TM (2004) Mechanisms of uniformity of yield strains for trabecular bone. J Biomech 37:1671–1678

    Article  PubMed  Google Scholar 

  51. Baroud G, Wu JZ, Bohner M, Sponagel S, Steffen T (2003) How to determine the permeability for cement infiltration of osteoporotic cancellous bone. Med Eng Phys 25:283–288

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  53. Dendorfer S, Maier HJ, Hammer J (2009) Fatigue damage in cancellous bone: an experimental approach from continuum to micro scale. J Mech Behav Biomed Mater 2:113–119

    Article  PubMed  CAS  Google Scholar 

  54. Mulder L, van Ruijven LJ, Koolstra JH, van Eijden TMGJ (2007) Biomechanical consequences of developmental changes in trabecular architecture and mineralization of the pig mandibular condyle. J Biomech 40:1575–1582

    Article  PubMed  Google Scholar 

  55. Kim HS, Al-Hassani STS (2002) A morphological model of vertebral trabecular bone. J Biomech 35:1101–1114

    Article  PubMed  CAS  Google Scholar 

  56. Gefen A, Seliktar R (2004) Comparison of the trabecular architecture and the isostatic stress flow in the human calcaneus. Med Eng Phys 26:119–129

    Article  PubMed  CAS  Google Scholar 

  57. Baum, T, Carballido-Gamio, J, Huber, M, Müller, D, Monetti, R, Räth, C, Eckstein, F, Lochmüller, E, Majumdar, S, Rummeny, E, Link, T and Bauer, J (2009) Automated 3D trabecular bone structure analysis of the proximal femur—prediction of biomechanical strength by CT and DXA. Osteoporos Int

  58. Crawford RP, Cann CE, Keaveny TM (2003) Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone 33:744–750

    Article  PubMed  Google Scholar 

  59. Müller R, Rügsegger P (1996) Analysis of mechanical properties of cancellous bone under conditions of simulated bone atrophy. J Biomech 29:1053–1060

    Article  PubMed  Google Scholar 

  60. Wachter NJ, Augat P, Mentzel M, Sarkar MR, Krischak GD, Kinzl L, Claes LE (2001) Predictive value of bone mineral density and morphology determined by peripheral quantitative computed tomography for cancellous bone strength of the proximal femur. Bone 28:133–139

    Article  PubMed  CAS  Google Scholar 

  61. Yerby SA, Bay BK, Toh E, McLain RF, Drews MJ (1998) The effect of boundary conditions on experimentally measured trabecular strain in the thoracic spine. J Biomech 31:891–897

    Article  PubMed  CAS  Google Scholar 

  62. Schoenfeld C, Lautenschlager E, Meyer P (1974) Mechanical properties of human cancellous bone in the femoral head. Med Biol Eng Comput 12:313–317

    CAS  Google Scholar 

  63. Badiei A, Bottema MJ, Fazzalari NL (2007) Influence of orthogonal overload on human vertebral trabecular bone mechanical properties. J Bone Miner Res 22:1690–1699

    Article  PubMed  Google Scholar 

  64. Homminga J, McCreadie BR, Ciarelli TE, Weinans H, Goldstein SA, Huiskes R (2002) Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structure level, not on the bone hard tissue level. Bone 30:759–764

    Article  PubMed  CAS  Google Scholar 

  65. Krischak GD, Augat P, Wachter NJ, Kinzl L, Claes LE (1999) Predictive value of bone mineral density and Singh Index for the in vitro mechanical properties of cancellous bone in the femoral head. Clin Biomech 14:346–351

    Article  CAS  Google Scholar 

  66. Mitton D, Cendre E, Roux JP, Arlot ME, Peix G, Rumelhart C, Babot D, Meunier PJ (1998) Mechanical properties of ewe vertebral cancellous bone compared with histomorphometry and high-resolution computed tomography parameters. Bone 22:651–658

    Article  PubMed  CAS  Google Scholar 

  67. Kummari S, Davis A, Vega L, Ahn N, Cassinelli E, Hernandez C (2009) Trabecular microfracture precedes cortical shell failure in the rat caudal vertebra under cyclic overloading. Calcif Tissue Int 85:127–133

    Article  PubMed  CAS  Google Scholar 

  68. Stolken JS, Kinney JH (2003) On the importance of geometric nonlinearity in finite-element simulations of trabecular bone failure. Bone 33:494–504

    Article  PubMed  CAS  Google Scholar 

  69. Anderson IA, Carman JB (2000) How do changes to plate thickness, length, and face-connectivity affect femoral cancellous bone’s density and surface area? An investigation using regular cellular models. J Biomech 33:327–335

    Article  PubMed  CAS  Google Scholar 

  70. Goulet RW, Goldstein SA, Ciarelli MJ, Kuhn JL, Brown MB, Feldkamp LA (1994) The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech 27(375–377):379–389

    Google Scholar 

  71. Shi X, Wang X, Niebur G (2009) Effects of loading orientation on the morphology of the predicted yielded regions in trabecular bone. Ann Biomed Eng 37:354–362

    Article  PubMed  Google Scholar 

  72. Furuya N, Nakamura K, Kashima I (2002) Morphometric analysis of digital radiographic bone images for trabecular bone structure. Oral Radiol 18:17–29

    Article  Google Scholar 

  73. Jacobs CR, Davis BR, Rieger CJ, Francis JJ, Saad M, Fyhrie DP (1999) The impact of boundary conditions and mesh size on the accuracy of cancellous bone tissue modulus determination using large-scale finite-element modeling. J Biomech 32:1159–1164

    Article  PubMed  CAS  Google Scholar 

  74. Ladd AJC, Kinney JH (1998) Numerical errors and uncertainties in finite-element modeling of trabecular bone. J Biomech 31:941–945

    Article  PubMed  CAS  Google Scholar 

  75. Eswaran SK, Allen MR, Burr DB, Keaveny TM (2007) A computational assessment of the independent contribution of changes in canine trabecular bone volume fraction and microarchitecture to increased bone strength with suppression of bone turnover. J Biomech 40:3424–3431

    Article  PubMed  Google Scholar 

  76. McCreadie BR, Goldstein SA (2000) Biomechanics of fracture: is bone mineral density sufficient to assess risk? J Bone Miner Res 15:2305–2308

    Article  PubMed  CAS  Google Scholar 

  77. Gregory L, David K, Oleg P, Eugene K (1999) Segregation analysis reveals a major gene effect in compact and cancellous bone mineral density in 2 populations. Hum Biol 71:155

    Google Scholar 

  78. Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259

    Article  PubMed  CAS  Google Scholar 

  79. Vaccaro AR, Chiba K, Heller JG, Patel TC, Thalgott JS, Truumees E, Fischgrund JS, Craig MR, Berta SC, Wang JC (2002) Bone grafting alternatives in spinal surgery. Spine J 2:206–215

    Article  PubMed  Google Scholar 

  80. Keaveny TM, Borchers RE, Gibson LJ, Hayes WC (1993) Trabecular bone modulus and strength can depend on specimen geometry. J Biomech 26:991–995, 997, 999–1000

    Google Scholar 

  81. Bevill G, Easley SK, Keaveny TM (2007) 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 40:3381–3388

    Article  PubMed  Google Scholar 

  82. Un K, Bevill G, Keaveny TM (2006) The effects of side-artifacts on the elastic modulus of trabecular bone. J Biomech 39:1955–1963

    Article  PubMed  Google Scholar 

  83. Kopperdahl DL, Keaveny TM (1998) Yield strain behavior of trabecular bone. J Biomech 31:601–608

    Article  PubMed  CAS  Google Scholar 

  84. 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  PubMed  Google Scholar 

Download references

Acknowledgments

This project was sponsored by the Ministry of Science, Technology, and Innovation, Malaysia. The authors would also like to thank the Research Management Centre, Universiti Teknologi Malaysia, for managing the project.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mohammed Rafiq Abdul Kadir.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Syahrom, A., Abdul Kadir, M.R., Abdullah, J. et al. Mechanical and microarchitectural analyses of cancellous bone through experiment and computer simulation. Med Biol Eng Comput 49, 1393–1403 (2011). https://doi.org/10.1007/s11517-011-0833-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-011-0833-0

Keywords

Navigation