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Mechanical modulation at the lamellar level in osteonal bone

Published online by Cambridge University Press:  01 August 2006

H.S. Gupta ,
U. Stachewicz ,
W. Wagermaier ,
P. Roschger ,
H.D. Wagner  and
P. Fratzl
H.S. Gupta*
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany
U. Stachewicz
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany
W. Wagermaier
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany
P. Roschger
Affiliation:
Ludwig Boltzmann Institute of Osteology, A-1140 Vienna, Austria
H.D. Wagner
Affiliation:
Department of Materials and Interfaces, Weizmann Institute of Science, Rehovot 76100, Israel
P. Fratzl
Affiliation:
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, 14424 Potsdam, Germany
*
a) Address all correspondence to this author. e-mail: [email protected]
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Abstract

The secondary osteon is the fundamental building block of compact cortical bone at the tissue level. Light and scanning electron microscopy have shown that the osteon consists of a laminated cylindrical composite of mineralized collagen fibril lamellae ∼5–7 μm thick. Using scanning nanoindentation and quantitative backscattered electron imaging on secondary osteons from the human femoral midshaft, we found that the indentation modulus shows a periodic variation between ∼24 GPa and ∼27 GPa within a single lamella. The average lamellar value remains nearly constant across the osteon and increases abruptly to more than 30 GPa at the interstitial bone interface. The local mineral content, determined from quantitative backscattered electron imaging at the indented locations, shows also a lamellar level modulation and is positively correlated with the indentation modulus at the same tissue position. We propose that such a mechanically and compositionally modulated structure may be an effective crack-stopping mechanism in bone.

Keywords

BoneScanning electron microscopy (SEM)Scanning-probe microscopy (SPM)
Type
Articles
Information
Journal of Materials Research , Volume 21 , Issue 8 , August 2006 , pp. 1913 - 1921
Copyright
Copyright © Materials Research Society 2006

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References

REFERENCES

1.Currey, J.D.: Bones—Structure and Mechanics, 2nd ed. (Princeton University Press, Princeton, NJ, 2002).CrossRefGoogle Scholar
2.Weiner, S., Traub, W., Wagner, H.D.: Lamellar bone: Structure-function relations. J. Struct. Biol. 126, 241 (1999).CrossRefGoogle ScholarPubMed
3.Ascenzi, A., Bonucci, E., Bocciare, D.S.: An electron microscope study on primary periosteal bone. J. Ultrastruct. Res. 18, 605 (1967).CrossRefGoogle Scholar
4.Ascenzi, A., Bonucci, E., Bocciare, D.S.: An electron microscope study of osteon calcification. J. Ultrastruct. Res. 12, 287 (1965).CrossRefGoogle ScholarPubMed
5.Gebhardt, W.: Regarding the functionally important assembly techniques of the small scale and large scale building blocks of the vertebral bone II: Special part: The building of the Haversian lamellar system and its functional meaning. Arch. Entwickl. Mech. Org. 20, 187 (1906).CrossRefGoogle Scholar
6.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
7.Giraudguille, M.M.: Twisted plywood architecture of collagen fibrils in human compact-bone osteons. Calcif. Tissue Int. 42, 167 (1988).Google Scholar
8.Marotti, G., Muglia, M.A., Palumbo, C.: Structure and function of lamellar bone. Clin. Rheumatol. 13, 63 (1994).Google Scholar
9.Barbos, M.P., Bianco, P., Ascenzi, A., Boyde, A.: Collagen orientation in compact-bone. 2. Distribution of lamellae in the whole of the human femoral-shaft with reference to its mechanical-properties. Metab. Bone Dis. Relat. Res. 5, 309 (1984).CrossRefGoogle Scholar
10.Ascenzi, A., Baschieri, P., Benvenuti, A.: The torsional properties of single selected osteons. J. Biomech. 27, 875 (1994).CrossRefGoogle ScholarPubMed
11.Ascenzi, A., Ascenzi, M.G., Benvenuti, A., Mango, F.: Pinching in longitudinal and alternate osteons during cyclic loading. J. Biomech. 30, 689 (1997).CrossRefGoogle ScholarPubMed
12.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).Google Scholar
13.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. A 67A, 719 (2003).Google Scholar
14.Hoffler, C.E., Moore, K.E., Kozloff, K., Zysset, P.K., Brown, M.B., Goldstein, S.A.: Heterogeneity of bone lamellar-level elastic moduli. Bone 26, 603 (2000).Google Scholar
15.Fratzl, P., Jakob, H.F., Rinnerthaler, S., Roschger, P., Klaushofer, K.: Position-resolved small-angle x-ray scattering of complex biological materials. J. Appl. Crystallogr. 30, 765 (1997).Google Scholar
16.Zizak, I., Roschger, P., Paris, O., Misof, B.M., Berzlanovich, A., Bernstorff, S., Amenitsch, H., Klaushofer, K., Fratzl, P.: Characteristics of mineral particles in the human bone/cartilage interface. J. Struct. Biol. 141, 208 (2003).CrossRefGoogle ScholarPubMed
17.Tesch, W., Eidelman, N., Roschger, P., Goldenberg, F., Klaushofer, K., Fratzl, P.: Graded microstructure and mechanical properties of human crown dentin. Calcif. Tissue Int. 69, 147 (2001).CrossRefGoogle ScholarPubMed
18.Weiner, S., Wagner, H.D.: The material bone: Structure mechanical function relations. Ann. Rev. Mater. Sci. 28, 271 (1998).CrossRefGoogle Scholar
19.Jaschouz, D., Paris, O., Roschger, P., Hwang, H.S., Fratzl, P.: Pole figure analysis of mineral nanoparticle orientation in individual trabecula of human vertebral bone. J. Appl. Crystallogr. 36, 494 (2003).CrossRefGoogle Scholar
20.Zizak, I., Paris, O., Roschger, P., Bernstorff, S., Amenitsch, H., Klaushofer, K., Fratzl, P.: Investigation of bone and cartilage by synchrotron scanning-SAXS and -WAXD with micrometer spatial resolution. J. Appl. Crystallogr. 33, 820 (2000).CrossRefGoogle Scholar
21.Gupta, H.S., Schratter, S., Tesch, W., Roschger, P., Berzlanovich, A., Schoeberl, T., Klaushofer, K., Fratzl, P.: Two different correlations between nanoindentation modulus and mineral content in the bone-cartilage interface. J. Struct. Biol. 149, 138 (2005).CrossRefGoogle ScholarPubMed
22.Roschger, P., Gupta, H.S., Berzlanovich, A., Ittner, G., Dempster, D.W., Fratzl, P., Cosman, F., Parisien, M., Lindsay, R., Nieves, J.W., Klaushofer, K.: Constant mineralization density distribution in cancellous human bone. Bone 32, 316 (2003).Google Scholar
23.Oliver, W.C., Pharr, G.M.: An improved technique for determining hardness and elastic-modulus using load and displacement sensing indentation experiments. J. Mater. Res. 7, 1564 (1992).Google Scholar
24.Stachewicz, U.: Mechanical mapping of compact bone with lamellar resolution. M.Sc. Thesis, Faculty of Materials Science and Ceramics, Department of Biomaterials, AGH University of Science and Technology, Krakow, Poland (2004).Google Scholar
25.Goldman, H.M., Bromage, T.G., Thomas, C.D.L., Clement, J.G.: Preferred collagen fiber orientation in the human mid-shaft femur. Anatomical Record A—Disc. Molecular Cellular Evolutionary Bio. 272A, 434 (2003).Google Scholar
26.Katz, J.L., Meunier, A.: Scanning acoustic microscope studies of the elastic properties of osteons and osteon lamallae. J. Biomech. Eng.—Trans. ASME 115, 543 (1993).Google Scholar
27.Rho, J.Y., Mishra, S.R., Chung, K., Bai, J., Pharr, G.M.: Relationship between ultrastructure and the nanoindentation properties of intramuscular herring bones. Ann. Biomed. Eng. 29, 1082 (2001).CrossRefGoogle ScholarPubMed
28.Fratzl, P., Gupta, H.S., Paschalis, E.P., Roschger, P.: Structure and mechanical quality of the collagen-mineral nano-composite in bone. J. Mater. Chem. 14, 2115 (2004).Google Scholar
29.Suresh, S., Sugimura, Y., Ogawa, T.: Fatigue cracking in materials with brittle surface-coatings. Scripta Metall. Mater. 29, 237 (1993).Google Scholar
30.Erdogan, F.: Fracture-mechanics of functionally graded materials. Compos. Eng. 5, 753 (1995).CrossRefGoogle Scholar
31.Kolednik, O.: The yield stress gradient effect in inhomogeneous materials. Int. J. Solids Struct. 37, 781 (2000).Google Scholar
32.Peterlik, H., Roschger, P., Klaushofer, K., Fratzl, P.: From brittle to ductile fracture of bone. Nat. Mater. 5, 52 (2006).CrossRefGoogle ScholarPubMed
33.Qiu, S.J., Rao, D.S., Fyhrie, D.P., Palnitkar, S., Parfitt, A.M.: The morphological association between microcracks and osteocyte lacunae in human cortical bone. Bone 37, 10 (2005).Google Scholar
34.Bruet, B.J.F., Qi, H.J., Boyce, M.C., Panas, R., Tai, K., Frick, L., Ortiz, C.: Nanoscale morphology and indentation of individual nacre tablets from the gastropod mollusc Trochus niloticus. J. Mater. Res. 20, 2400 (2005).Google Scholar
35.Li, X., Chang, W-C., Chao, Y.J., Wang, R., Chang, M.: Nanoscale structural and mechanical characterization of a natural nanocomposite material: The shell of red abalone. Nano Lett. 4, 613 (2004).CrossRefGoogle Scholar
36.Johnson, K.L.: Contact Mechanics (Cambridge University Press, Cambridge, UK, 1985).CrossRefGoogle Scholar
37.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
38.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).Google Scholar
39.Hoffler, C.E., Guo, X.E., Zysset, P., Moore, K.E., and Goldstein, S.A.: Evaluation of bone microstructural properties: Effect of testing conditions, depth, repetition, time delay and displacement rate, in Proceedings of the 1997 Bioengineering Conference, Sun River, OR, 1997, edited by Chandran, K.B., Vanderby, R., Jr., and Hefzy, M.S., (ASME International, New York), pp. 567–568.Google Scholar
40.Weaver, J.K.: Microscopic hardness of bone. J. Bone Joint Surg. Am. A48, 273 (1966).CrossRefGoogle Scholar
41.Fratzl, P., Groschner, M., Vogl, G., Plenk, H., Eschberger, J., Fratzl-Zelman, N., Koller, K., Klaushofer, K.: Mineral crystals in calcified tissues—A comparative study by SAXS. J. Bone Miner. Res. 7, 329 (1992).CrossRefGoogle ScholarPubMed
42.Landis, W.J., Paine, M.C., Glimcher, M.J.: Electron microscopic observations of bone tissue prepared anhydrously in organic solvents. J. Ultrastruct. Res. 59, 1 (1977).Google Scholar
43.Oyen, M.L., Cook, R.F.: Load-displacement behavior during sharp indentation of viscous-elastic-plastic materials. J. Mater. Res. 18, 139 (2003).CrossRefGoogle Scholar