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Elastic anisotropy of bone lamellae as a function of fibril orientation pattern

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Abstract

In this study, the homogenized anisotropic elastic properties of single bone lamellae are computed using a finite element unit cell method. The resulting stiffness tensor is utilized to calculate indentation moduli for multiple indentation directions in the lamella plane which are then related to nanoindentation experiments. The model accounts for different fibril orientation patterns in the lamellae—the twisted and orthogonal plywood pattern, a 5-sublayer pattern and an X-ray diffraction-based pattern. Three-dimensional sectional views of each pattern facilitate the comparison to transmission electron (TEM) images of real lamella cuts. The model results indicate, that the 5-sublayer- and the X-ray diffraction-based patterns cause the lamellae to have a stiffness maximum between 0° and 45° to the osteon axis. Their in-plane stiffness characteristics are qualitatively matching the experimental findings that report a higher stiffness in the osteon axis than in the circumferential direction. In contrast, lamellae owning the orthogonal or twisted plywood fibril orientation patterns have no preferred stiffness alignment. This work shows that the variety of fibril orientation patterns leads to qualitative and quantitative differences in the lamella elastic mechanical behavior. The study is a step toward a deeper understanding of the structure—mechanical function relationship of bone lamellae.

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References

  • Akiva U, Wagner H, Weiner S (1998) Modelling the three-dimensional elastic constants of parallel-fibred and lamellar bone. J Mater Sci 33(6): 1497–1509

    Article  Google Scholar 

  • Akkus O (2005) Elastic deformation of mineralized collagen fibrils: an equivalent inclusion based composite model. J Biomech Eng 127(3): 383–390

    Article  Google Scholar 

  • Ascenzi A, Bonucci E (1967) The tensile properties of single osteons. Anat Rec 158(4): 375–386

    Article  Google Scholar 

  • Ascenzi A, Bonucci E (1968) The compressive properties of single osteons. Anat Rec 161(3): 377–391

    Article  Google Scholar 

  • Ascenzi MG, Lomovtsev A (2006) Collagen orientation patterns in human secondary osteons, quantified in the radial direction by confocal microscopy. J Struct Biol 153(1): 14–30

    Article  Google Scholar 

  • Cusack S, Miller A (1979) Determination of the elastic constants of collagen by brillouin light scattering. J Mol Biol 135(1): 39–51

    Article  Google Scholar 

  • Fan Z, Swadener JG, Rho JY, Roy ME, Pharr GM (2002) Anisotropic properties of human tibial cortical bone as measured by nanoindentation. J Orthop Res 20(4): 806–810

    Article  Google Scholar 

  • Franzoso G, Zysset PK (2009) Elastic anisotropy of human cortical bone secondary osteons measured by nanoindentation. J Biomech Eng 131(2): 021001

    Article  Google Scholar 

  • Fratzl P, Weinkamer R (2007) Nature’s hierarchical materials. Prog Mater Sci 52(8): 1263–1334

    Article  Google Scholar 

  • Fritsch A, Hellmich C (2007) ‘Universal’ microstructural patterns in cortical and trabecular, extracellular and extravascular bone materials: micromechanics-based prediction of anisotropic elasticity. J Theor Biol 244(4): 597–620

    Article  Google Scholar 

  • Gebhardt W (1906) Ueber funktionell wichtige anordnungsweisen der feineren und groeberen bauelemente des wirbeltierknochens. ii. spezieller teil. der bau der haversschen lamellensysteme und seine funktionelle bedeutung. Arch Entwickl Mech Org 20: 187–322

    Article  Google Scholar 

  • Giraud-Guille M (1988) Twisted plywood architecture of collagen fibrils in human compact bone osteons. Calcif Tissue Int 42(3): 167–180

    Article  Google Scholar 

  • Giraud-Guille M, Besseau L, Martin R (2003) Liquid crystalline assemblies of collagen in bone and in vitro systems. J Biomech 36(10): 1571–1579

    Article  Google Scholar 

  • Gupta H, Zioupos P (2008) Fracture of bone tissue: the ‘hows’ and the ‘whys’. Med Eng Phys 30(10):1209–1226, special issue to commemorate the 30th anniversary of Medical Engineering & Physics—30th Anniversary Issue

    Google Scholar 

  • Hengsberger S, Kulik A, Zysset P (2002) Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 30(1): 178–184

    Article  Google Scholar 

  • Hofmann T, Heyroth F, Meinhard H, Fränzel W, Raum K (2006) Assessment of composition and anisotropic elastic properties of secondary osteon lamellae. J Biomechan 39(12): 2282–2294

    Article  Google Scholar 

  • Jasiuk I, Ostoja-Starzewski M (2004) Modeling of bone at a single lamella level. Biomech Model Mechanobiol 3(2): 67–74

    Article  Google Scholar 

  • Lees S, Prostak KS, Ingle VK, Kjoller K (1994) The loci of mineral in turkey leg tendon as seen by atomic force microscope and electron microscopy. Calcif Tissue Int 55(3): 180–189

    Article  Google Scholar 

  • Marotti G (1993) A new theory of bone lamellation. Calcif Tissue Int 53(Suppl 1):S47–55. (discussion S56)

    Google Scholar 

  • McKee M, Nanci A (1996) Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: Ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microsc Res Tech 33(2): 141–164

    Article  Google Scholar 

  • Pahr DH, Rammerstorfer FG (2006) Buckling of honeycomb sandwiches: periodic finite element considerations. Comput Model Eng Sci 12: 229–242

    Google Scholar 

  • Pidaparti R, Chandran A, Takano Y, Turner C (1996) Bone mineral lies mainly outside collagen fibrils: predictions of a composite model for osternal bone. J Biomechan 29(7): 909–916

    Article  Google Scholar 

  • Raum K, Leguerney I, Chandelier F, Talmant M, Saied A, Peyrin F, Laugier P (2006) Site-matched assessment of structural and tissue properties of cortical bone using scanning acoustic microscopy and synchrotron radiation uct. Phys Med Biol 51: 733–746

    Article  Google Scholar 

  • Reisinger AG, Pahr DH, Zysset PK (2010) Sensitivity analysis and parametric study of elastic properties of an unidirectional mineralized bone fibril-array using mean field methods. Biomechan Model Mechanobiol. doi:10.1007/s10,237-010-0190-1

  • Rho J, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20(2): 92–102

    Article  Google Scholar 

  • Roy ME, Rho JY, Tsui TY, Evans ND, Pharr GM (1999) Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J Biomed Mater Res 44(2): 191–197

    Article  Google Scholar 

  • Suquet P (1987) Lecture notes in physics—homogenization techniques for composite media. Chapter IV. Springer, Berlin

    Google Scholar 

  • Swadener J, Pharr G (2001) Indentation of elastically anisotropic half-spaces by cones and parabolae of revolution. Philos Mag Lett 81(20): 447–466

    Google Scholar 

  • Turner CH, Chandran A, Pidaparti RMV (1995) The anisotropy of osteonal bone and its ultrastructural implications. Bone 17(1): 85–89

    Article  Google Scholar 

  • Wagermaier W, Gupta HS, Gourrier A, Burghammer M, Roschger P, Fratzl P (2006) Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1(1): 1–5

    Article  Google Scholar 

  • Weiner S, Traub W (1992) Bone structure: from angstroms to microns. FASEB J 6(3): 879–885

    Google Scholar 

  • Weiner S, Wagner H (1998) The material bone: structure-mechanical function relations. Annu Rev Mater Sci 28(1): 271–298

    Article  Google Scholar 

  • Weiner S, Arad T, Traub W (1991) Crystal organization in rat bone lamellae. FEBS Lett 285(1): 49–54

    Article  Google Scholar 

  • Weiner S, Arad T, Sabanay I, Traub W (1997) Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays. Bone 20(6): 509–514

    Article  Google Scholar 

  • Weiner S, Traub W, Wagner H (1999) Lamellar bone: structure-function relations. J Struct Biol 126(3): 241–255

    Article  Google Scholar 

  • Yao H, Ouyang L, Ching W (2007) Ab initio calculation of elastic constants of ceramic crystals. J Am Ceram Soc 90(10): 3194–3204

    Article  Google Scholar 

  • Yoon Y, Cowin S (2008) The estimated elastic constants for a single bone osteonal lamella. Biomech Model Mechanobiol 7(1): 1–11

    Article  Google Scholar 

  • Ziv V, Wagner HD, Weiner S (1996) Microstructure-microhardness relations in parallel-fibered and lamellar bone. Bone 18(5): 417–428

    Article  Google Scholar 

  • Zysset P, Guo X, Hoffler C, Moore K, Goldstein S (1999) Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech 32(10): 1005–1012

    Article  Google Scholar 

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Correspondence to Andreas G. Reisinger.

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Reisinger, A.G., Pahr, D.H. & Zysset, P.K. Elastic anisotropy of bone lamellae as a function of fibril orientation pattern. Biomech Model Mechanobiol 10, 67–77 (2011). https://doi.org/10.1007/s10237-010-0218-6

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  • DOI: https://doi.org/10.1007/s10237-010-0218-6

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