A quantitative collagen fibers orientation assessment using birefringence measurements: Calibration and application to human osteons

Even though mechanical properties depend strongly on the arrangement of collagen fibers in mineralized tissues, it is not yet well resolved. Only a few semi-quantitative evaluations of the fiber arrangement in bone, like spectroscopic techniques or circularly polarized light microscopy methods are available. In this study the out-of-plane collagen arrangement angle was calibrated to the linear birefringence of a longitudinally fibered mineralized turkey leg tendon cut at variety of angles to the main axis. The calibration curve was applied to human cortical bone osteons to quantify the out-of-plane collagen fibers arrangement. The proposed calibration curve is normalized to sample thickness and wavelength of the probing light to enable a universally applicable quantitative assessment. This approach may improve our understanding of the fibrillar structure of bone and its implications on mechanical properties.

[1]  Richard Weinkamer,et al.  Nature’s hierarchical materials , 2007 .

[2]  O. Akkus,et al.  Local variations in the micromechanical properties of mouse femur: the involvement of collagen fiber orientation and mineralization. , 2007, Journal of biomechanics.

[3]  P. Fratzl,et al.  Bone osteonal tissues by Raman spectral mapping: orientation-composition. , 2006, Journal of structural biology.

[4]  P. Zysset,et al.  Elastic anisotropy of human cortical bone secondary osteons measured by nanoindentation. , 2009, Journal of biomechanical engineering.

[5]  A. Glazer,et al.  Three-dimensional birefringence imaging with a microscope tilting stage. II. Biaxial crystals , 2006 .

[6]  A. Ascenzi,et al.  The compressive properties of single osteons , 1968, The Anatomical record.

[7]  A. M. Glazer,et al.  Three-dimensional birefringence imaging with a microscope tilting stage , 2005 .

[8]  Sonja Gamsjaeger,et al.  Cortical bone composition and orientation as a function of animal and tissue age in mice by Raman spectroscopy. , 2010, Bone.

[9]  G. Langenbach,et al.  Determination of the relationship between collagen cross-links and the bone-tissue stiffness in the porcine mandibular condyle. , 2011, Journal of biomechanics.

[10]  R. Martin,et al.  The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. , 1989, Journal of biomechanics.

[11]  Himadri S. Gupta,et al.  Nanoscale deformation mechanisms in bone. , 2005, Nano letters.

[12]  A. Boyde,et al.  The quantitative study of the orientation of collagen in compact bone slices. , 1990, Bone.

[13]  P. Fratzl,et al.  Raman imaging of two orthogonal planes within cortical bone. , 2007, Bone.

[14]  Elliot P. Douglas,et al.  Bone structure and formation: A new perspective , 2007 .

[15]  G W Marshall,et al.  Mechanical properties of mineralized collagen fibrils as influenced by demineralization. , 2008, Journal of structural biology.

[16]  H Follet,et al.  The degree of mineralization is a determinant of bone strength: a study on human calcanei. , 2004, Bone.

[17]  P. Zysset,et al.  Morphological and Mechanical Properties of Bone Structural Units: A Two-Case Study , 2002 .

[18]  Guy Cox,et al.  3-dimensional imaging of collagen using second harmonic generation. , 2003, Journal of structural biology.

[19]  H. Winet,et al.  Interpreting cortical bone adaptation and load history by quantifying osteon morphotypes in circularly polarized light images. , 2009, Bone.

[20]  A. Ascenzi,et al.  The tensile properties of single osteons , 1967, The Anatomical record.

[21]  A. Boskey,et al.  Microstructure and nanomechanical properties in osteons relate to tissue and animal age. , 2011, Journal of biomechanics.

[22]  C. Lovejoy,et al.  Collagen fiber orientation in the femoral necks of apes and humans: do their histological structures reflect differences in locomotor loading? , 2002, Bone.

[23]  V. A. Gibson,et al.  Collagen fiber organization is related to mechanical properties and remodeling in equine bone. A comparison of two methods. , 1996, Journal of biomechanics.

[24]  Thomas Siegmund,et al.  Failure of mineralized collagen fibrils: modeling the role of collagen cross-linking. , 2008, Journal of biomechanics.

[25]  Alan Boyde,et al.  Circularly polarized light standards for investigations of collagen fiber orientation in bone. , 2003, Anatomical record. Part B, New anatomist.

[26]  R. Pidaparti,et al.  The anisotropy of osteonal bone and its ultrastructural implications. , 1995, Bone.

[27]  P. Zysset,et al.  Elastic anisotropy of bone lamellae as a function of fibril orientation pattern , 2011, Biomechanics and modeling in mechanobiology.

[28]  Dieter H. Pahr,et al.  Sensitivity analysis and parametric study of elastic properties of an unidirectional mineralized bone fibril-array using mean field methods , 2010, Biomechanics and modeling in mechanobiology.

[29]  E. H. Linfoot Principles of Optics , 1961 .

[30]  S. Weiner,et al.  Lamellar bone: structure-function relations. , 1999, Journal of structural biology.

[31]  C. Thomas,et al.  Preferred collagen fiber orientation in the human mid-shaft femur. , 2003, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[32]  G Boivin,et al.  The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients. , 2008, Bone.

[33]  Walter Gebhardt,et al.  Über funktionell wichtige Anordnungsweisen der feineren und gröberen Bauelemente des Wirbeltierknochens , 1905, Archiv für Entwicklungsmechanik der Organismen.

[34]  Kaminsky,et al.  Images of absolute retardance L.Δn, using the rotating polariser method , 2000, Journal of microscopy.

[35]  W. Kaminsky,et al.  Simultaneous false‐colour imaging of birefringence, extinction and transmittance at camera speed , 2007, Journal of microscopy.

[36]  M. Burghammer,et al.  Spiral twisting of fiber orientation inside bone lamellae , 2006, Biointerphases.

[37]  S. Weiner,et al.  Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays. , 1997, Bone.

[38]  M. Pandy,et al.  Differences in the degree of bone tissue mineralization account for little of the differences in tissue elastic properties. , 2011, Bone.