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

Published online by Cambridge University Press:  01 August 2006

Eve Donnelly ,
Rebecca M. Williams ,
Seth A. Downs ,
Michelle E. Dickinson ,
Shefford P. Baker  and
Marjolein C.H. van der Meulen
Eve Donnelly*
Affiliation:
Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, New York 14853
Rebecca M. Williams
Affiliation:
Department of Applied and Engineering Physics, Cornell University, Ithaca, New York 14853
Seth A. Downs
Affiliation:
Hysitron, Inc., Eden Prairie, Minnesota 55344
Michelle E. Dickinson
Affiliation:
Hysitron, Inc., Eden Prairie, Minnesota 55344
Shefford P. Baker
Affiliation:
Department of Materials Science and Engineering, Cornell University, Ithaca, New York 14853
Marjolein C.H. van der Meulen
Affiliation:
Sibley School of Mechanical and Aerospace Engineering, Cornell University, Ithaca, New York 14853and Musculoskeletal Integrity Program, Hospital for Special Surgery, New York, New York 14853
*
a) Address all correspondence to this author. e-mail: [email protected]
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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.

Keywords

BoneHardnessMicrostructure
Type
Articles
Information
Journal of Materials Research , Volume 21 , Issue 8 , August 2006 , pp. 2106 - 2117
Copyright
Copyright © Materials Research Society 2006

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References

REFERENCES

1.Weiner, S., Wagner, H.D.: The material bone: Structure-mechanical function relations. Annu. Rev. Mater. Sci. 28, 271 (1998).CrossRefGoogle 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).Google Scholar
3.Cummings, S.R., Nevitt, M.C., Browner, W.S., Stone, K., Fox, K.M., Ensrud, K.E., Cauley, J., Black, D., Vogt, T.M.: Risk factors for hip fracture in white women. N. Engl. J. Med. 332, 767 (1995).CrossRefGoogle ScholarPubMed
4.Carter, D.R., Hayes, W.C.: The compressive behavior of bone as a two-phase porous structure. J. Bone Joint Surg. 59A, 954 (1977).CrossRefGoogle Scholar
5.Gibson, L.J.: The mechanical behaviour of cancellous bone. J. Biomech. 18, 317 (1985).CrossRefGoogle ScholarPubMed
6.Rice, J.C., Cowin, S.C., Bowman, J.A.: On the dependence of the elasticity and strength of cancellous bone on apparent density. J. Biomech. 21, 155 (1988).CrossRefGoogle ScholarPubMed
7.Ulrich, D., van Rietbergen, B., Laib, A., Rüegsegger, P.: The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25, 55 (1999).CrossRefGoogle ScholarPubMed
8.Hert, J., Liskova, M., Landa, J.: Reaction of bone to mechanical stimuli. Part 1: Continuous and intermittent loading of tibia in rabbit. Folia Morph. Prag. 19, 290 (1971).Google Scholar
9.Fritton, J.C., Myers, E.R., Wright, T.M., van der Meulen, M.C.H.: Loading induces site-specific increases in mineral content assessed my microcomputed tomography of the mouse tibia. Bone 36, 1030 (2005).CrossRefGoogle Scholar
10.Christofferson, J., Landis, W.J.: A contribution with review to the description of mineralization of bone and other calcified tissues in vivo. Anat. Rec. 230, 435 (1991).CrossRefGoogle Scholar
11.Dickson, I.R.Bone, in Connective Tissue and Its Heritable Disorders edited by Royce, P.M. and Steinmann, B. (Wiley-Liss, New York, 1993), p. 249.Google Scholar
12.Boyde, A., Hobdell, M.H.: Scanning electron microscopy of lamellar bone. Z. Zellforsch. 93, 213 (1969).CrossRefGoogle ScholarPubMed
13.Ziv, V., Sabanay, I., Arad, T., Traub, W., Weiner, S.: Transitional structures in lamellar bone. Microsc. Res. Tech. 33, 203 (1996).3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
14.Ascenzi, A., Bonucci, E., Bocciarelli, D.S.R.M.S.B.J.: An electron microscope study of osteon calcification. J. Ultrastruct. Res. 12, 287 (1965).CrossRefGoogle ScholarPubMed
15.Giraud-Guille, M.M.: Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif. Tissue Int. 42, 167 (1988).CrossRefGoogle ScholarPubMed
16.Hobdell, M.H., Boyde, A.: Microradiography and scanning electron microscopy of bone sections. Z. Zellforsch. 94, 487 (1969).CrossRefGoogle ScholarPubMed
17.Marotti, G.: A new theory of bone lamellation. Calcif. Tissue Int. 53, S47 (1993).CrossRefGoogle ScholarPubMed
18.Weiner, S., Arad, T., Sabanay, I., Traub, W.: Rotated plywood structure of primary lamellar bone in the rat: Orientations of the collagen fibril arrays. Bone 20, 509 (1997).CrossRefGoogle ScholarPubMed
19.Donnelly, E., Baker, S.P., Boskey, A.L., van der Meulen, M.C.H.: Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J. Biomed. Mater. Res. 77A, 426 (2006).CrossRefGoogle Scholar
20.Hengsberger, S., Kulik, A., Zysset, P.: Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 30, 178 (2002).CrossRefGoogle ScholarPubMed
21.Xu, J., Rho, J-Y., Mishra, S.R., Fan, Z.: 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).CrossRefGoogle Scholar
22.Landis, W.J., Hodgens, K.J., Arena, J., Song, M.J., McEwan, B.F.: Structural relations between collagen and mineral in bone as determined by high voltage electron tomography. Microsc. Res. Tech. 33, 192 (1996).3.0.CO;2-V>CrossRefGoogle Scholar
23.Weiner, S., Arad, T., Traub, W.: Crystal organization in rat bone lamellae. FEBS Lett. 285, 49 (1991).CrossRefGoogle ScholarPubMed
24.Kozloff, K.M., Carden, A., Bergwitz, C., Forlino, A., Uveges, T.E., Morris, M.D., Marini, J.C., Goldstein, S.A.: Brittle IV mouse model for osteogenesis imperfecta IV demonstrates postpubertal adaptations to improve whole bone strength. J. Bone Miner. Res. 19, 614 (2004).CrossRefGoogle ScholarPubMed
25.Jepsen, K.J., Schaffler, M.B., Kuhn, J.L., Goulet, R.W., Bonadio, J., Goldstein, S.A.: Type I collagen mutation alters the strength and fatigue behavior of Mov13 cortical tissue. J. Biomech. 30, 1141 (1997).CrossRefGoogle ScholarPubMed
26.Mohler, W., Millard, A.C., Campagnola, P.J.: Second harmonic generation imaging of endogenous structural proteins. Methods 29, 97 (2003).CrossRefGoogle ScholarPubMed
27.Cox, G., Kable, E., Jones, A., Fraser, I., Manconi, F., Gorrell, M.D.: Three-dimensional imaging of collagen using second harmonic generation. J. Struct. Biol. 141, 53 (2003).CrossRefGoogle Scholar
28.Williams, R.M., Zipfel, W.R., Webb, W.W.: Interpreting second-harmonic generation images of collagen I fibrils. Biophys. J. 88, 1377 (2005).CrossRefGoogle ScholarPubMed
29.Zipfel, W.R., Williams, R.M., Christie, R., Nikitin, A.Y., Hyman, B.T., Webb, W.W.: Live tissue intrinsic emission microscopy using multiphoton-excited native fluorescence and second harmonic generation. Proc. Natl. Acad. Sci. USA 100, 7075 (2003).CrossRefGoogle ScholarPubMed
30.Campagnola, P.J., Loew, L.M.: Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms. Nat. Biotechnol. 21, 1356 (2003).CrossRefGoogle ScholarPubMed
31.Galante, J., Rostoker, W., Ray, R.D.: Physical properties of trabecular bone. Calcif. Tissue Res. 5, 236 (1970).CrossRefGoogle ScholarPubMed
32.Rho, J-Y., Roy, M.E., Tsui, T.Y., Pharr, G.M.: Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. J. Biomed. Mater. Res. 45, 48 (1999).3.0.CO;2-5>CrossRefGoogle Scholar
33.Roy, M.E., Rho, J-Y., Tsui, T.Y., Evans, N.D., Pharr, G.M.: Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J. Biomed. Mater. Res. 44, 191 (1999).3.0.CO;2-G>CrossRefGoogle ScholarPubMed
34.Rho, J-Y., Zioupos, P., Currey, J.D., Pharr, G.M.: Variations in the individual thick lamellar properties within osteons by nanoindentation. Bone 25, 295 (1999).CrossRefGoogle ScholarPubMed
35.Oliver, W.C., Pharr, G.M.: Improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7, 1564 (1992).CrossRefGoogle Scholar
36.Johnson, K.L.: Contact Mechanics (Cambridge University Press, Cambridge, UK, 1985).CrossRefGoogle Scholar
37.Baker, S.P. Analysis of depth-sensing indentation data, in Thin Films: Stresses and Mechanical Properties IV edited by Townsend, P.H., Weihs, T.P., Sanchez, J.E., Jr., and P. Borgesen (Mater. Res. Soc. Symp. Proc.308, Pittsburgh, PA, 1993), p. 209.Google Scholar
38.Loubet, J-L., Lucas, B.N., Oliver, W.C.: Some measurements of viscoelastic properties with the help of nanoindentation. NIST Special Publications 896, 31 (1996).Google Scholar
39.Asif, S.A. Syed, Pethica, J.B. Nanoscale visoelastic properties of polymer materials, in Thin-Films—Stresses and Mechanical Properties VII edited by Cammarata, R.C., Nastasi, M., Busso, E.P., and Oliver, W.C. (Mater. Res. Soc. Symp. Proc. 505, Warrendale, PA, 1998), p. 103.Google Scholar
40.Asif, S.A. Syed, Wahl, K.J., Colton, R.J., Warren, O.L.: Quantitative imaging of nanoscale mechanical properties using hybrid nanoindentation and force modulation. J. Appl. Phys. 90, 1192 (2001).CrossRefGoogle Scholar
41.Zipfel, W.R., Williams, R.M., Webb, W.W.: Nonlinear magic: Multiphoton microscopy in the biosciences. Nat. Biotechnol. 21, 1369 (2003).CrossRefGoogle ScholarPubMed
42.Donnelly, E., Williams, R.M., Baker, S.P., and van der Meulen, M.C.H.: 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 Fratzl, P., Landis, W.J., Wang, R., and Silver, F.H. (Mater. Res. Soc. Symp. Proc. 874, Warrendale, PA, 2005), L7.5, p. 73.Google Scholar
43.Boyd, R.W.: Nonlinear Optics, 2nd ed. (Academic Press, Amsterdam, The Netherlands, 2003).Google Scholar
44.Moreaux, L., Sandre, O., Mertz, J.: Membrane imaging by second-harmonic generation microscopy. J. Opt. Soc. Am. B Opt. Phys. 17, 1685 (2000).CrossRefGoogle Scholar
45.Donnelly, E., Xiao, C., Baker, S.P., Mendelsohn, R., Boskey, A.L., van der Meulen, M.C.H.: Systematic variations in bone tissue micromechanical properties relate to composition. Trans. Orthop. Res. Soc. 30, 672 (2005).Google Scholar
46.Lakes, R.S., Katz, J.L., Sternstein, S.S.: Viscoelastic properties of wet cortical bone. I. Torsional and biaxial studies. J. Biomech. 12, 657 (1979).CrossRefGoogle ScholarPubMed
47.Yamashita, J., Li, X., Furman, B.R., Rawls, H.R., Wang, X., Agrawal, C.M.: Collagen and bone viscoelasticity: A dynamic mechanical analysis. J. Biomed. Mater. Res. 63, 31 (2002).CrossRefGoogle ScholarPubMed
48.Yee, A.F., Smith, S.A.: Molecular structure effects on the dynamic mechanical spectra of polycarbonates. Macromolecules 14, 54 (1981).CrossRefGoogle Scholar
49.Rho, J-Y., Pharr, G.M.: Effects of drying on the mechanical properties of bovine femur measured by nanoindentation. J. Mater. Sci.: Mater. Med. 10, 485 (1999).Google ScholarPubMed
50.Bushby, A.J., Ferguson, V.L., Boyde, A.: Nanoindentation of bone: Comparison of specimens tested in liquid and embedded in polymethylmethacrylate. J. Mater. Res. 19, 249 (2004).CrossRefGoogle Scholar
51.Glimcher, M.J.: Molecular biology of mineralized tissues with particular reference to bone. Rev. Mod. Phys. 13, 359 (1959).CrossRefGoogle Scholar
52.Ferguson, V.L., Bushby, A.J., Boyde, A.: Nanomechanical properties and mineral concentration in articular calcified cartilage and subchondral bone. J. Anat. 203, 191 (2003).CrossRefGoogle ScholarPubMed
53.Les, C.M., Vance, J.L., Christopherson, G., Turner, A.S., Fyhrie, D.P.: Anisotropy in compact bone viscoelastic properties is enhanced by long-term estrogen depletion in sheep. Trans. Orthop. Res. Soc. 27, 24 (2002).Google Scholar