Skip to main content
Log in

Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization

  • Article
  • Published:
Journal of Materials Research Aims and scope Submit manuscript

Abstract

Cancellous bone plays a crucial structural role in the skeleton, yet little is known about the microstructure-mechanical property relationships of the tissue at the microscale. Cancellous tissue is characterized by a microstructure consisting of layers interspaced with transition zones with different proportions of collagen and mineral. In this study, the quasistatic and dynamic mechanical properties of lamellar and interlamellar tissue in human vertebrae were assessed with nanoindentation, and the collagen content and organization were characterized with second harmonic generation microscopy. Lamellar tissue was 35% stiffer, 25% harder, and had a 13% lower loss tangent relative to interlamellar tissue. The stiff, hard lamellae corresponded to areas of highly ordered, collagen-rich material, with a relatively low loss tangent, whereas the compliant, soft interlamellar regions corresponded to areas of disordered or collagen-poor material. These data suggest an important role for collagen in the tissue-level mechanical properties of 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.

Similar content being viewed by others

References

  1. S. Weiner, H.D. Wagner: The material bone: Structure-mechanical function relations. Annu. Rev. Mater. Sci. 28, 271 (1998).

    Article  CAS  Google Scholar 

  2. United States Department of Health and Human Services: Bone Health and Osteoporosis: A Report of the Surgeon General (U.S. Department of Health and Human Services, Office of the Surgeon General, Rockville, MD, 2004).

  3. S.R. Cummings, M.C. Nevitt, W.S. Browner, K. Stone, K.M. Fox, K.E. Ensrud, J. Cauley, D. Black, T.M. Vogt: Risk factors for hip fracture in white women. N. Engl. J. Med. 332, 767 (1995).

    Article  CAS  Google Scholar 

  4. D.R. Carter, W.C. Hayes: The compressive behavior of bone as a two-phase porous structure. J. Bone Joint Surg. 59A, 954 (1977).

    Article  Google Scholar 

  5. L.J. Gibson: The mechanical behaviour of cancellous bone. J. Biomech. 18, 317 (1985).

    Article  CAS  Google Scholar 

  6. J.C. Rice, S.C. Cowin, J.A. Bowman: On the dependence of the elasticity and strength of cancellous bone on apparent density. J. Biomech. 21, 155 (1988).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. J. Hert, M. Liskova, J. Landa: Reaction of bone to mechanical stimuli. Part 1: Continuous and intermittent loading of tibia in rabbit. Folia Morph. Prag. 19, 290 (1971).

    CAS  Google Scholar 

  9. J.C. Fritton, E.R. Myers, T.M. Wright, M.C.H. van der Meulen: Loading induces site-specific increases in mineral content assessed my microcomputed tomography of the mouse tibia. Bone 36, 1030 (2005).

    Article  CAS  Google Scholar 

  10. J. Christofferson, W.J. Landis: A contribution with review to the description of mineralization of bone and other calcified tissues in vivo. Anat. Rec. 230, 435 (1991).

    Google Scholar 

  11. I.R. Dickson: Bone, in Connective Tissue and Its Heritable Disorders edited by P.M. Royce and B. Steinmann (Wiley-Liss, New York, 1993), p. 249.

  12. A. Boyde, M.H. Hobdell: Scanning electron microscopy of lamellar bone. Z. Zellforsch. 93, 213 (1969).

    CAS  Google Scholar 

  13. V. Ziv, I. Sabanay, T. Arad, W. Traub, S. Weiner: Transitional structures in lamellar bone. Microsc. Res. Tech. 33, 203 (1996).

    CAS  Google Scholar 

  14. A. Ascenzi, E. Bonucci, D.S.R.M.S.B.J. Bocciarelli: An electron microscope study of osteon calcification. J. Ultrastruct. Res. 12, 287 (1965).

    CAS  Google Scholar 

  15. M.M. Giraud-Guille: Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif. Tissue Int. 42, 167 (1988).

    CAS  Google Scholar 

  16. M.H. Hobdell, A. Boyde: Microradiography and scanning electron microscopy of bone sections. Z. Zellforsch. 94, 487 (1969).

    CAS  Google Scholar 

  17. G. Marotti: A new theory of bone lamellation. Calcif. Tissue Int. 53, S (1993).

    Google Scholar 

  18. S. Weiner, T. Arad, I. Sabanay, W. Traub: Rotated plywood structure of primary lamellar bone in the rat: Orientations of the collagen fibril arrays. Bone 20, 509 (1997).

    CAS  Google Scholar 

  19. E. Donnelly, S.P. Baker, A.L. Boskey, M.C.H. van der Meulen: Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J. Biomed. Mater. Res. 77A, 426 (2006).

    CAS  Google Scholar 

  20. S. Hengsberger, A. Kulik, P. Zysset: Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 30, 178 (2002).

    CAS  Google Scholar 

  21. J. Xu, J.Y. Rho, S.R. Mishra, Z. Fan: Atomic force microscopy and nanoindentation characterization of human lamellar bone prepared by microtome sectioning and mechanical polishing technique. J. Biomed. Mater. Res. 67A, 719 (2003).

    CAS  Google Scholar 

  22. W.J. Landis, K.J. Hodgens, J. Arena, M.J. Song, B.F. McEwan: Structural relations between collagen and mineral in bone as determined by high voltage electron tomography. Microsc. Res. Tech. 33, 192 (1996).

    CAS  Google Scholar 

  23. S. Weiner, T. Arad, W. Traub: Crystal organization in rat bone lamellae. FEBS Lett. 285, 49 (1991).

    CAS  Google Scholar 

  24. K.M. Kozloff, A. Carden, C. Bergwitz, A. Forlino, T.E. Uveges, M.D. Morris, J.C. Marini, S.A. Goldstein: Brittle IV mouse model for osteogenesis imperfecta IV demonstrates postpubertal adaptations to improve whole bone strength. J. Bone Miner. Res. 19, 614 (2004).

    Google Scholar 

  25. K.J. Jepsen, M.B. Schaffler, J.L. Kuhn, R.W. Goulet, J. Bonadio, S.A. Goldstein: Type I collagen mutation alters the strength and fatigue behavior of Mov13 cortical tissue. J. Biomech. 30, 1141 (1997).

    CAS  Google Scholar 

  26. W. Mohler, A.C. Millard, P.J. Campagnola: Second harmonic generation imaging of endogenous structural proteins. Methods 29, 97 (2003).

    CAS  Google Scholar 

  27. G. Cox, E. Kable, A. Jones, I. Fraser, F. Manconi, M.D. Gorrell: Three-dimensional imaging of collagen using second harmonic generation. J. Struct. Biol. 141, 53 (2003).

    CAS  Google Scholar 

  28. R.M. Williams, W.R. Zipfel, W.W. Webb: Interpreting second-harmonic generation images of collagen I fibrils. Biophys. J. 88, 1377 (2005).

    CAS  Google Scholar 

  29. W.R. Zipfel, R.M. Williams, R. Christie, A.Y. Nikitin, B.T. Hyman, W.W. Webb: Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc. Natl. Acad. Sci. USA 100, 7075 (2003).

    CAS  Google Scholar 

  30. P.J. Campagnola, L.M. Loew: Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nat. Biotechnol. 21, 1356 (2003).

    Article  CAS  Google Scholar 

  31. J. Galante, W. Rostoker, R.D. Ray: Physical properties of trabecular bone. Calcif. Tissue Res. 5, 236 (1970).

    Article  CAS  Google Scholar 

  32. J.Y. Rho, M.E. Roy, T.Y. Tsui, G.M. Pharr: Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. J. Biomed. Mater. Res. 45, 48 (1999).

    Article  CAS  Google Scholar 

  33. M.E. Roy, J.Y. Rho, T.Y. Tsui, N.D. Evans, G.M. Pharr: Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J. Biomed. Mater. Res. 44, 191 (1999).

    Article  CAS  Google Scholar 

  34. J.Y. Rho, P. Zioupos, J.D. Currey, G.M. Pharr: Variations in the individual thick lamellar properties within osteons by nanoindentation. Bone 25, 295 (1999).

    Article  CAS  Google Scholar 

  35. W.C. Oliver, G.M. Pharr: Improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7, 1564 (1992).

    Article  CAS  Google Scholar 

  36. K.L. Johnson: Contact Mechanics (Cambridge University Press, Cambridge, UK, 1985).

    Book  Google Scholar 

  37. S.P. Baker: Analysis of depth-sensing indentation data, in Thin Films: Stresses and Mechanical Properties IV edited by P.H. Townsend, T.P. Weihs, J.E. Sanchez, Jr., and P. Borgesen (Mater. Res. Soc. Symp. Proc.308, Pittsburgh, PA, 1993), p. 209.

    CAS  Google Scholar 

  38. J.L. Loubet, B.N. Lucas, W.C. Oliver: Some measurements of viscoelastic properties with the help of nanoindentation. NIST Special Publications 896, 31 (1996).

    CAS  Google Scholar 

  39. S.A. Syed Asif, J.B. Pethica: Nanoscale visoelastic properties of polymer materials, in Thin-Films—Stresses and Mechanical Properties VII edited by R.C. Cammarata, M. Nastasi, E.P. Busso, and W.C. Oliver (Mater. Res. Soc. Symp. Proc. 505, Warrendale, PA, 1998), p. 103.

    Google Scholar 

  40. S.A. Syed Asif, K.J. Wahl, R.J. Colton, O.L. Warren: Quantitative imaging of nanoscale mechanical properties using hybrid nanoindentation and force modulation. J. Appl. Phys. 90, 1192 (2001).

    CAS  Google Scholar 

  41. W.R. Zipfel, R.M. Williams, W.W. Webb: Nonlinear magic: Multiphoton microscopy in the biosciences. Nat. Biotechnol. 21, 1369 (2003).

    CAS  Google Scholar 

  42. E. Donnelly, R.M. Williams, S.P. Baker, and M.C.H. van der Meulen: Collagen content and organization relate to bone nanomechanical properties. Nano-scale viscoelastic properties of polymer materials, in Structures and Mechanical Behavior of Biological Materials edited by P. Fratzl, W.J. Landis, R. Wang, and F.H. Silver (Mater. Res. Soc. Symp. Proc. 874, Warrendale, PA, 2005), L7.5, p. 73.

    CAS  Google Scholar 

  43. R.W. Boyd: Nonlinear Optics, 2nd ed. (Academic Press, Amsterdam, The Netherlands, 2003).

    Google Scholar 

  44. L. Moreaux, O. Sandre, J. Mertz: Membrane imaging by second-harmonic generation microscopy. J. Opt. Soc. Am. B Opt. Phys. 17, 1685 (2000).

    CAS  Google Scholar 

  45. E. Donnelly, C. Xiao, S.P. Baker, R. Mendelsohn, A.L. Boskey, M.C.H. van der Meulen: Systematic variations in bone tissue micromechanical properties relate to composition. Trans. Orthop. Res. Soc. 30, 672 (2005).

    Google Scholar 

  46. R.S. Lakes, J.L. Katz, S.S. Sternstein: Viscoelastic properties of wet cortical bone. I. Torsional and biaxial studies. J. Biomech. 12, 657 (1979).

    CAS  Google Scholar 

  47. J. Yamashita, X. Li, B.R. Furman, H.R. Rawls, X. Wang, C.M. Agrawal: Collagen and bone viscoelasticity: A dynamic mechanical analysis. J. Biomed. Mater. Res. 63, 31 (2002).

    Article  CAS  Google Scholar 

  48. A.F. Yee, S.A. Smith: Molecular structure effects on the dynamic mechanical spectra of polycarbonates. Macromolecules 14, 54 (1981).

    Article  CAS  Google Scholar 

  49. J.Y. Rho, G.M. Pharr: Effects of drying on the mechanical properties of bovine femur measured by nanoindentation. J. Mater. Sci.: Mater. Med. 10, 485 (1999).

    CAS  Google Scholar 

  50. A.J. Bushby, V.L. Ferguson, A. Boyde: Nanoindentation of bone: Comparison of specimens tested in liquid and embedded in polymethylmethacrylate. J. Mater. Res. 19, 249 (2004).

    CAS  Google Scholar 

  51. M.J. Glimcher: Molecular biology of mineralized tissues with particular reference to bone. Rev. Mod. Phys. 13, 359 (1959).

    Google Scholar 

  52. V.L. Ferguson, A.J. Bushby, A. Boyde: Nanomechanical properties and mineral concentration in articular calcified cartilage and subchondral bone. J. Anat. 203, 191 (2003).

    Google Scholar 

  53. C.M. Les, J.L. Vance, G. Christopherson, A.S. Turner, D.P. Fyhrie: Anisotropy in compact bone viscoelastic properties is enhanced by long-term estrogen depletion in sheep. Trans. Orthop. Res. Soc. 27, 24 (2002).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eve Donnelly.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Donnelly, E., Williams, R.M., Downs, S.A. et al. Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization. Journal of Materials Research 21, 2106–2117 (2006). https://doi.org/10.1557/jmr.2006.0259

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1557/jmr.2006.0259

Navigation