Collagen and the Mechanical Properties of Bone and Calcified Cartilage

In bone type I collagen is mineralized by very small crystals of carbonated hydroxyapatite. There is usually some water present. These three materials together produce a composite whose mechanical properties are unlike that of any of the constituents. The mechanical behavior of bone is not strange and will eventually be explained in terms of standard composite theory. However, that time is not yet, particularly because there is still considerable dispute about some fundamental features of bone, for instance the size and shape of the mineral crystals and their topographical relationship to the collagen. Calcified cartilage, made by the calcification of type II collagen, is the stiff structural element in the skeleton of many chondrichthyean fish. It shows interesting similarities to and differences from bone.

[1]  Peter Zioupos,et al.  Mechanical properties of nacre and highly mineralized bone , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  E. Radin,et al.  Bone remodeling in response to in vivo fatigue microdamage. , 1985, Journal of biomechanics.

[3]  P. Donoghue,et al.  Early evolution of vertebrate skeletal tissues and cellular interactions, and the canalization of skeletal development. , 2006, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[4]  Peter Zioupos,et al.  Notch sensitivity of mammalian mineralized tissues in impact , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[5]  R. G. Paul,et al.  Glycation of collagen: the basis of its central role in the late complications of ageing and diabetes. , 1996, The international journal of biochemistry & cell biology.

[6]  S. Tadano,et al.  Relationship between bone tissue strain and lattice strain of HAp crystals in bovine cortical bone under tensile loading. , 2007, Journal of biomechanics.

[7]  B F McEwen,et al.  Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography , 1996, Microscopy research and technique.

[8]  A. Bailey,et al.  Age-Related Changes in the Biochemical Properties of Human Cancellous Bone Collagen: Relationship to Bone Strength , 1999, Calcified Tissue International.

[9]  A. Summers,et al.  Stiffening the stingray skeleton — an investigation of durophagy in Myliobatid stingrays (Chondrichthyes, Batoidea, Myliobatidae) , 2000, Journal of morphology.

[10]  P. Fratzl,et al.  Collagen from the osteogenesis imperfecta mouse model (oim) shows reduced resistance against tensile stress. , 1997, The Journal of clinical investigation.

[11]  Adam P. Summers,et al.  Mineralized cartilage in the skeleton of chondrichthyan fishes. , 2006, Zoology.

[12]  C. M. Agrawal,et al.  Age-related changes in the collagen network and toughness of bone. , 2002, Bone.

[13]  P. Fratzl,et al.  Mineralized collagen fibrils: a mechanical model with a staggered arrangement of mineral particles. , 2000, Biophysical journal.

[14]  M. Dean,et al.  Functional morphology of jaw trabeculation in the lesser electric ray Narcine brasiliensis, with comments on the evolution of structural support in the Batoidea , 2006, Journal of morphology.

[15]  Huajian Gao,et al.  Materials become insensitive to flaws at nanoscale: Lessons from nature , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Peter Zioupos,et al.  The Bone Tissue of the Rostrum of a Mesoplodon Densirostris Whale: a Mammalian Biomineral Demonstrating Extreme Texture , 1999 .

[17]  Franco Marinozzi,et al.  Microtensile measurements of single trabeculae stiffness in human femur. , 2002, Journal of biomechanics.

[18]  S. Weiner,et al.  Rostrum of a toothed whale: ultrastructural study of a very dense bone. , 1998, Bone.

[19]  S. Cowin,et al.  On the dependence of the elasticity and strength of cancellous bone on apparent density. , 1988, Journal of biomechanics.

[20]  W. Horton,et al.  Immunohistochemistry of types I and II collagen in undecalcified skeletal tissues. , 1983, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[21]  P. Donoghue,et al.  HISTOLOGY OF THE GALEASPID DERMOSKELETON AND ENDOSKELETON, AND THE ORIGIN AND EARLY EVOLUTION OF THE VERTEBRATE CRANIAL ENDOSKELETON , 2005 .

[22]  D. Vashishth,et al.  Influence of nonenzymatic glycation on biomechanical properties of cortical bone. , 2001, Bone.

[23]  John D. Currey,et al.  Bones: Structure and Mechanics , 2002 .

[24]  D R Carter,et al.  Bone creep-fatigue damage accumulation. , 1989, Journal of biomechanics.

[25]  J. Katz Hard tissue as a composite material. I. Bounds on the elastic behavior. , 1971, Journal of biomechanics.

[26]  S. Weiner,et al.  Bone crystal sizes: a comparison of transmission electron microscopic and X-ray diffraction line width broadening techniques. , 1994, Connective tissue research.

[27]  G. Pharr,et al.  Variations in the individual thick lamellar properties within osteons by nanoindentation. , 1999, Bone.

[28]  M. Ishiyama,et al.  Cellular influence in the formation of enameloid during odontogenesis in bony fishes , 2006 .

[29]  Wolfgang Wagermaier,et al.  Cooperative deformation of mineral and collagen in bone at the nanoscale , 2006, Proceedings of the National Academy of Sciences.

[30]  S A Goldstein,et al.  Type‐I collagen mutation compromises the post‐yield behavior of Mov13 long bone , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[31]  Margaret Tzaphlidou,et al.  The role of collagen in bone structure: an image processing approach. , 2005, Micron.

[32]  A J Bailey,et al.  Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. , 1998, Bone.

[33]  W. Dabin,et al.  Histology and growth of the cetacean petro-tympanic bone complex , 2004 .

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

[35]  Christian Hellmich,et al.  'Universal' microstructural patterns in cortical and trabecular, extracellular and extravascular bone materials: micromechanics-based prediction of anisotropic elasticity. , 2007, Journal of theoretical biology.

[36]  S. Stock,et al.  Internal strains and stresses measured in cortical bone via high-energy X-ray diffraction. , 2005, Journal of structural biology.

[37]  N. Sasaki,et al.  Orientation of mineral in bovine bone and the anisotropic mechanical properties of plexiform bone. , 1991, Journal of biomechanics.

[38]  Richard Mendelsohn,et al.  Chemical Structure-Based Three-Dimensional Reconstruction of Human Cortical Bone from Two-Dimensional Infrared Images , 2002 .

[39]  A. Biewener,et al.  In vivo locomotor strain in the hindlimb bones of alligator mississippiensis and iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture , 1999, The Journal of experimental biology.

[40]  J. Currey,et al.  What determines the bending strength of compact bone? , 1999, The Journal of experimental biology.

[41]  J. Currey,et al.  Young's modulus, density and material properties in cancellous bone over a large density range , 1992 .

[42]  W. Walsh,et al.  Compressive properties of cortical bone: mineral-organic interfacial bonding. , 1994, Biomaterials.

[43]  Daniel P Nicolella,et al.  Osteocyte lacunae tissue strain in cortical bone. , 2006, Journal of biomechanics.

[44]  R. Pidaparti,et al.  Bone mineral lies mainly outside collagen fibrils: predictions of a composite model for osteonal bone. , 1996, Journal of biomechanics.

[45]  N. Traverso,et al.  Scanning force microscopy reveals structural alterations in diabetic rat collagen fibrils: role of protein glycation , 2000, Diabetes/metabolism research and reviews.

[46]  John Currey,et al.  Incompatible mechanical properties in compact bone. , 2004, Journal of theoretical biology.

[47]  D. Vashishth,et al.  Effects of non-enzymatic glycation on cancellous bone fragility. , 2007, Bone.

[48]  S. Stock,et al.  Micromechanical response of mineral and collagen phases in bone. , 2007, Journal of structural biology.

[49]  Marianne E. Porter,et al.  Material properties and biochemical composition of mineralized vertebral cartilage in seven elasmobranch species (Chondrichthyes) , 2006, Journal of Experimental Biology.

[50]  P. Fratzl,et al.  Age- and genotype-dependence of bone material properties in the osteogenesis imperfecta murine model (oim). , 2001, Bone.

[51]  S. Weiner,et al.  On the relationship between the microstructure of bone and its mechanical stiffness. , 1992, Journal of biomechanics.

[52]  A. Bailey,et al.  Phenotypic expression of osteoblast collagen in osteoarthritic bone: production of type I homotrimer. , 2002, The international journal of biochemistry & cell biology.

[53]  A. Burstein,et al.  The elastic and ultimate properties of compact bone tissue. , 1975, Journal of biomechanics.

[54]  Peter Zioupos,et al.  Mechanical properties of the rostrum of the whale Mesoplodon densirostris, a remarkably dense bony tissue , 1997 .

[55]  D T Davy,et al.  Anisotropic yield behavior of bone under combined axial force and torque. , 1985, Journal of biomechanics.

[56]  C. Hellmich,et al.  Are mineralized tissues open crystal foams reinforced by crosslinked collagen? Some energy arguments. , 2002, Journal of biomechanics.

[57]  P Zioupos,et al.  The role of collagen in the declining mechanical properties of aging human cortical bone. , 1999, Journal of biomedical materials research.

[58]  Y. Yeni,et al.  Calculation of porosity and osteonal cement line effects on the effective fracture toughness of cortical bone in longitudinal crack growth. , 2000, Journal of biomedical materials research.

[59]  T. Belytschko,et al.  Biological Structures Mitigate Catastrophic Fracture Through Various Strategies , 2005 .

[60]  David Taylor,et al.  Bone as a composite material: The role of osteons as barriers to crack growth in compact bone , 2007 .

[61]  J. Currey,et al.  Mechanical properties of bone tissues with greatly differing functions. , 1979, Journal of biomechanics.

[62]  J. Currey,et al.  The microhardness and fracture surface of the petrodentine of Lepidosiren (Dipnoi), and of other mineralised tissues. , 2003, Archives of oral biology.

[63]  K. Weiss,et al.  Genetic basis for the evolution of vertebrate mineralized tissue. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[64]  P Zioupos,et al.  Experimental and theoretical quantification of the development of damage in fatigue tests of bone and antler. , 1996, Journal of biomechanics.

[65]  Masahiro Taniguchi,et al.  Atomic force microscopic studies on the structure of bovine femoral cortical bone at the collagen fibril-mineral level , 2002, Journal of materials science. Materials in medicine.

[66]  S. Cowin Bone mechanics handbook , 2001 .

[67]  H. Toda,et al.  Fatigue properties of bovine compact bones that have different microstructures , 2007 .

[68]  Peter Zioupos,et al.  Accumulation of in‐vivo fatigue microdamage and its relation to biomechanical properties in ageing human cortical bone , 2001, Journal of microscopy.

[69]  P Zioupos,et al.  Tensile fatigue in bone: are cycles-, or time to failure, or both, important? , 2001, Journal of theoretical biology.

[70]  Michael D Morris,et al.  Three structural roles for water in bone observed by solid-state NMR. , 2006, Biophysical journal.