Annals of Biomedical Engineering

, Volume 44, Issue 4, pp 1204–1223 | Cite as

Apparent- and Tissue-Level Yield Behaviors of L4 Vertebral Trabecular Bone and Their Associations with Microarchitectures

  • He Gong
  • Lizhen Wang
  • Yubo Fan
  • Ming Zhang
  • Ling Qin
Article

Abstract

The precise quantification of vertebral trabecular bone strength and the associations between the microarchitecture and nonlinear mechanics of trabecular bone under various loading conditions may provide insights into trabecular bone quality and trabecular strength prediction based on microarchitectures. In this research, 44 cubic L4 vertebral trabecular bone specimens (5 × 5 × 5 mm3) were selected from six male Chinese donors aged 62–70 years. For each vertebral trabecular cube, micro-computed tomography image-based nonlinear micro-finite element analyzes were conducted under compressive and tensile loadings along two orthogonal directions. A bilinear tissue constitutive model was used to describe the nonlinearity of bone tissue material. In each analysis, apparent Young’s modulus and initial apparent yield point were determined; the average tissue von Mises stress at the apparent yield point was also calculated, and the amount of tissue elements yielded was obtained. Principal components (PCs) analysis revealed three independent components of the microarchitectural parameters of the vertebral trabecular bones; these three PCs can account for 80.744% of the total variability of trabecular microarchitectures; the first PC (PC1) included bone volume fraction, connectivity density and trabecular number; the second PC (PC2) comprised structure model index and degree of anisotropy; and the third PC (PC3) represented trabecular thickness and age. Multivariate linear regression analysis showed that the PCs were strongly predictive of the apparent- and tissue-level mechanical parameters of the vertebral trabecular bone. To gain further insights into the mechanical properties of trabecular bone, we divided the six vertebral bodies into two groups based on the microarchitectural parameters: high-quality group and low-quality group. We then compared the differences in the mechanical parameters between tension and compression, as well as along longitudinal and transverse loading directions. Results showed that the apparent Young’s moduli of the high-quality group were significantly greater than those of the low-quality group in longitudinal and transverse directions. Only the apparent yield strains of the two groups under the longitudinal compressive loading condition were significantly different. The apparent yield stresses and the average tissue von Mises stresses of the trabeculae in the trabecular cubes of the high-quality group were significantly greater than those of the low-quality group under the four loading conditions. This study provided quantitative information regarding the nonlinear mechanical properties of vertebral trabecular bone. This study also described the associations of these mechanical properties with microarchitectures. Our findings may help estimate vertebral strength and the related fracture risk.

Keywords

Vertebral body Trabecular bone Nonlinear micro-finite element analysis Longitudinal direction Transverse direction Yield behavior 

Notes

Acknowledgments

This work is supported by the grants from National Natural Science Foundation of China (Nos. 11322223, 11432016, 81471753, 11202017, and 11421202), and the Program for New Century Excellent Talents in University (NCET-12-0024).

Conflict of interest

None.

References

  1. 1.
    Adam, M. A., and P. Dolan. Intervertebral disc degeneration: evidence for two distinct phenotypes. J. Anat. 221:497–506, 2012.CrossRefGoogle Scholar
  2. 2.
    Ali, A. A., L. Cristofolini, E. Schileo, H. Hu, F. Taddei, R. H. Kim, P. J. Rullkoetter, and P. J. Laz. Specimen-specific modeling of hip fracture pattern and repair. J. Biomech. 47:536–543, 2014.CrossRefPubMedGoogle Scholar
  3. 3.
    Bayraktar, H. H. and T. M. Keaveny. A computational investigation of the nonlinear behavior of human trabecular bone. In: Transactions of the 12th Annual Pre-ORS Symposium on Computational Methods in Orthopaedic Biomechanics, vol 2, 2004b.Google Scholar
  4. 4.
    Bayraktar, H. H., E. F. Morgan, G. L. Niebur, G. Morris, E. Wong, and T. Keaveny. Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. J. Biomech. 37:27–35, 2004.CrossRefPubMedGoogle Scholar
  5. 5.
    Bessho, M., I. Ohnishi, J. Matsuyama, T. Matsumoto, K. Imai, and K. Nakamura. Prediction of strength and strain of the proximal femur by a CT-based finite element method. J. Biomech. 40:1745–1753, 2007.CrossRefPubMedGoogle Scholar
  6. 6.
    Borah, B., T. E. Dufresne, P. A. Chmielewski, G. J. Gross, M. C. Prenger, and R. J. Phipps. Risedronate preserves trabecular architecture and increases bone strength in vertebra of ovariectomized minipigs as measured by three-dimensional microcomputed tomography. J. Bone Miner. Res. 17:1139–1147, 2002.CrossRefPubMedGoogle Scholar
  7. 7.
    Cyganik, Ł., M. Binkowski, G. Kokot, T. Rusin, P. Popik, F. Bolechała, R. Nowak, Z. Wróbel, and A. John. Prediction of Young’s modulus of trabeculae in microscale using macro-scale’s relationships between bone density and mechanical properties. J. Mech. Behav. Biomed. Mater. 36:120–134, 2014.CrossRefPubMedGoogle Scholar
  8. 8.
    Depalle, B., R. Chapurlat, H. Walter-le-Berre, B. Bou-Saïd, and H. Follet. Finite element dependence of stress evaluation for human trabecular bone. J. Mech. Behav. Biomed. Mater. 18:200–212, 2013.CrossRefPubMedGoogle Scholar
  9. 9.
    Giambini, H., H. Wang, C. Zhao, Q. Chen, A. Nassr, and K. An. Anterior and posterior variations in mechanical properties of human vertebrae measured by nanoindentation. J. Biomech. 46:456–461, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Gong, H., M. Zhang, and Y. Fan. Micro-finite element analysis of trabecular bone yield behaviour—effects of tissue non-linear material properties. J. Mech. Med. Biol. 11:563–580, 2011.CrossRefGoogle Scholar
  11. 11.
    Gong, H., M. Zhang, L. Qin, X. Guo, and S. Q. Shi. Regional variations in microstructural properties of vertebral trabeculae with structural model groups. Spine 31:24–32, 2006.CrossRefPubMedGoogle Scholar
  12. 12.
    Gong, H., M. Zhang, L. Qin, and Y. Hou. Regional variations in the apparent and tissue-level mechanical parameters of vertebral trabecular bone with aging using micro-finite element analysis. Ann. Biomed. Eng. 35:1622–1631, 2007.CrossRefPubMedGoogle Scholar
  13. 13.
    Gong, H., M. Zhang, H. Y. Yeung, and L. Qin. Regional variations in microstructural properties of vertebral trabeculae with ageing. J. Bone Miner. Metab. 23:174–180, 2005.CrossRefPubMedGoogle Scholar
  14. 14.
    Gunaratne, G. H., C. S. Rajapaksa, K. E. Bassler, K. K. Mohanty, and S. J. Wimalawansa. Model for bone strength and osteoporotic fractures. Phys. Rev. Lett. 88:068101, 2002.CrossRefPubMedGoogle Scholar
  15. 15.
    Hildebrand, T., and T. Rüegsegger. Quantification of bone microarchitecture with the structure model index. Comput. Methods Biomech. Biomed. Eng. 1:15–23, 1997.CrossRefGoogle Scholar
  16. 16.
    Homminga, J., B. R. McCreadie, T. E. Ciarelli, H. Weinans, S. A. Goldstein, and R. Huiskes. Cancellous bone mechanical properties from normal and patients with hip fractures differ on the structural level, not on the bone hard tissue level. Bone 30:759–764, 2002.CrossRefPubMedGoogle Scholar
  17. 17.
    Homminga, J., H. Weinans, W. Gowin, D. Felsenberg, and R. Huiskes. Osteoporosis changes the amount of vertebral trabecular bone at risk of fracture but not the vertebral load distribution. Spine 26:1555–1561, 2001.CrossRefPubMedGoogle Scholar
  18. 18.
    Huiskes, R., R. Ruimerman, G. H. Van Lenthe, and J. D. Janssen. Effects of mechanical factors on maintenance and adaptation of form in trabecular bone. Nature 405:704–706, 2000.CrossRefPubMedGoogle Scholar
  19. 19.
    Jiroušek, O., J. Němecek, D. Kytyr, J. Kunecky, P. Zlamal, and T. Doktor. Nanoindentation of trabecular bone—comparison with uniaxial testing of single trabecula. Chem. Listy 105:668–671, 2011.Google Scholar
  20. 20.
    Jolliffe, I. T. Statistics (2nd ed.). New York: Spinger, 2002.Google Scholar
  21. 21.
    Judex, S., S. Boyd, Y. X. Qin, S. Turner, K. Ye, R. Müller, and C. Rubin. Adaptations of trabecular bone to low magnitude vibrations result in more uniform stress and strain under load. Ann. Biomed. Eng. 31:12–20, 2003.CrossRefPubMedGoogle Scholar
  22. 22.
    Kopperdahl, D. L., and T. M. Keaveny. Yield strain behavior of trabecular bone. J. Biomech. 31:601–608, 1998.CrossRefPubMedGoogle Scholar
  23. 23.
    Liebschner, M. A. K., R. Müller, S. J. Wimalawansa, C. S. Rajapakse, and G. H. Gunaratne. Testing two predictions for fracture load using computer models of trabecular bone. Biophys. J . 89:759–767, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Liu, X. S., E. Shane, D. J. McMahon, and X. E. Guo. Individual trabecula segmentation (ITS)-based morphological analysis of micro-scale images of human tibial trabecular bone at limited spatial resolution. J. Bone Miner. Res. 26:2184–2193, 2011.CrossRefPubMedGoogle Scholar
  25. 25.
    Melton, L. J., E. A. Chrischilles, C. Cooper, A. W. Lane, and B. L. Riggs. Perspective: how many women have osteoporosis? J. Bone Miner. Res. 7:1005–1010, 1992.CrossRefPubMedGoogle Scholar
  26. 26.
    Milovanovic, P., J. Potocnik, D. Djonic, S. Nikolic, V. Zivkovic, M. Djuric, and Z. Rakocevic. Age-related deterioration in trabecular bone mechanical properties at material level: nanoindentation study of the femoral neck in women by using AFM. Exp. Gerontol. 47:154–159, 2012.CrossRefPubMedGoogle Scholar
  27. 27.
    Morgan, E. F., H. H. Bayraktar, O. C. Yeh, S. Majumdar, A. Burghardt, and T. M. Keaveny. Contribution of inter-site variations in architecture to trabecular bone apparent yield strains. J. Biomech. 37:1413–1420, 2004.CrossRefPubMedGoogle Scholar
  28. 28.
    Niebur, G. L., M. J. Feldstein, and T. M. Keaveny. Biaxial failure behavior of bovine tibial trabecular bone. J. Biomech. Eng. 124:699–705, 2002.CrossRefPubMedGoogle Scholar
  29. 29.
    Niebur, G., M. J. Feldstein, J. C. Yuen, T. J. Chen, and T. M. Keaveny. High-resolution finite element models with tissue strength asymmetry accurately predict failure of trabecular bone. J. Biomech. 33:1575–1583, 2000.CrossRefPubMedGoogle Scholar
  30. 30.
    Shi, X., X. S. Liu, X. Wang, X. E. Guo, and G. L. Niebur. Type and orientation of yielded trabeculae during overloading of trabecular bone along orthogonal directions. J. Biomech. 43:2460–2466, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Shi, X., X. Wang, and G. L. Niebur. Effects of loading orientation on the morphology of the predicted yielded regions in trabecular bone. Ann. Biomed. Eng. 37:354–362, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Szabó, M. E., J. Zekonyte, O. L. Katsamenis, M. Taylor, and P. J. Thurner. Similar damage initiation but different failure behaviour in trabecular and cortical bone tissue. J. Mech. Behav. Biomed. Mater. 4:1787–1796, 2011.CrossRefPubMedGoogle Scholar
  33. 33.
    Thomsen, J. S., E. N. Ebbsesen, and L. I. Mosekilde. Age-related differences between thinning of horizontal and vertical trabecular in human lumbar bone as assessed by a new computerized method. Bone 31:136–142, 2002.CrossRefPubMedGoogle Scholar
  34. 34.
    Verhulp, E., B. van Rietbergen, R. Muller, and R. Huiskes. Micro-finite element simulation of trabecular-bone post-yield behavior—effects of material model, element size and type. Comput. Methods Biomech. Biomed. Eng. 11:389–395, 2008.CrossRefGoogle Scholar
  35. 35.
    Walker, M. D., X. S. Liu, B. Zhou, S. Agarwal, G. Liu, D. J. McMahon, J. P. Bilezikian, and X. E. Guo. Premenopausal and postmenopausal differences in bone microstructure and mechanical competence in Chinese-American and white women. J. Bone Miner. Res. 28:1308–1318, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Wolfram, U., H. J. Wilke, and P. K. Zysset. Rehydration of vertebral trabecular bone: influences on its anisotropy, its stiffness and the indentation work with a view to age, gender and vertebral level. Bone 46:348–354, 2010.CrossRefPubMedGoogle Scholar
  37. 37.
    Zhang, R., H. Gong, D. Zhu, J. Gao, J. Fang, and Y. Fan. Seven day insertion rest in whole body vibration improves multi-level bone quality in tail suspension rats. PLoS ONE 9:e92312, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Zhou, B., X. S. Liu, J. Wang, X. L. Lu, A. J. Fields, and X. E. Guo. Dependence of mechanical properties of trabecular bone on plate-rod microstructure determined by individual trabecula segmentation (ITS). J. Biomech. 47:702–708, 2014.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Biomedical Engineering Society 2015

Authors and Affiliations

  • He Gong
    • 1
  • Lizhen Wang
    • 1
  • Yubo Fan
    • 1
  • Ming Zhang
    • 2
  • Ling Qin
    • 3
  1. 1.School of Biological Science and Medical EngineeringBeihang UniversityBeijingChina
  2. 2.Department of Health Technology and InformaticsThe Hong Kong Polytechnic UniversityHong KongChina
  3. 3.Department of Orthopaedics and TraumatologyThe Chinese University of Hong KongHong KongChina

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