Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture

Properties of the organic matrix of bone1 as well as its function in the microstructure2 could be the key to the remarkable mechanical properties of bone3. Previously, it was found that on the molecular level, calcium-mediated sacrificial bonds increased stiffness and enhanced energy dissipation in bone constituent molecules4,5. Here we present evidence for how this sacrificial bond and hidden length mechanism contributes to the mechanical properties of the bone composite, by investigating the nanoscale arrangement of the bone constituents6,7,8 and their interactions. We find evidence that bone consists of mineralized collagen fibrils and a non-fibrillar organic matrix2, which acts as a ‘glue’ that holds the mineralized fibrils together. We believe that this glue may resist the separation of mineralized collagen fibrils. As in the case of the sacrificial bonds in single molecules5, the effectiveness of this mechanism increases with the presence of Ca2+ ions.

[1]  M. Young.  Bone matrix proteins: their function, regulation, and relationship to osteoporosis , 2003, Osteoporosis International.

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

[3]  D. Burr.  The contribution of the organic matrix to bone's material properties. , 2002, Bone.

[4]  W. Ambrosius,et al.  Does microdamage accumulation affect the mechanical properties of bone? , 1998, Journal of biomechanics.

[5]  S. Goldstein,et al.  Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography , 1991, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[6]  Quyen Q. Hoang,et al.  Bone recognition mechanism of porcine osteocalcin from crystal structure , 2003, Nature.

[7]  P Zioupos,et al.  Mechanical properties and the hierarchical structure of bone. , 1998, Medical engineering & physics.

[8]  Ralph Müller,et al.  The Zürich Experience: One Decade of Three-Dimensional High-Resolution Computed Tomography , 2002, Topics in magnetic resonance imaging : TMRI.

[9]  L. Klenerman,et al.  Altered organization of non-collagenous bone matrix in osteoporosis. , 1987, Bone.

[10]  Paul K. Hansma,et al.  Bone indentation recovery time correlates with bond reforming time , 2001, Nature.

[11]  M. Rief,et al.  Reversible unfolding of individual titin immunoglobulin domains by AFM. , 1997, Science.

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

[13]  M Raspanti,et al.  Different patterns of collagen-proteoglycan interaction: a scanning electron microscopy and atomic force microscopy study. , 2000, European journal of histochemistry : EJH.

[14]  R. Ritchie,et al.  Mechanistic fracture criteria for the failure of human cortical bone , 2003, Nature materials.

[15]  Mario Viani,et al.  Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites , 1999, Nature.

[16]  T. Hefferan,et al.  Structure and molecular regulation of bone matrix proteins , 1993, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[17]  M. Grynpas,et al.  The distribution of soluble, mineral-bound, and matrix-bound proteins in osteoporotic and normal bones. , 1994, Bone.

[18]  P. Braidotti,et al.  Scanning electron microscopy of human cortical bone failure surfaces. , 1997, Journal of biomechanics.

[19]  H. Hansma,et al.  Molecular nanosprings in spider capture-silk threads , 2003, Nature materials.

[20]  D. Fyhrie,et al.  A rate-dependent microcrack-bridging model that can explain the strain rate dependency of cortical bone apparent yield strength. , 2003, Journal of biomechanics.

[21]  M. McKee,et al.  Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: Ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair , 1996, Microscopy research and technique.

[22]  T. Norman,et al.  Diffuse damage accumulation in the fracture process zone of human cortical bone specimens and its influence on fracture toughness , 2001, Journal of materials science. Materials in medicine.

[23]  Georg E Fantner,et al.  High-resolution AFM imaging of intact and fractured trabecular bone. , 2004, Bone.

[24]  R O Ritchie,et al.  Effect of aging on the toughness of human cortical bone: evaluation by R-curves. , 2004, Bone.

[25]  T. A. Taton.  Nanotechnology: Boning up on biology , 2001, Nature.

[26]  J. Currey.  Biomaterials: Sacrificial bonds heal bone , 2001, Nature.

[27]  H. Gaub,et al.  Probing solid surfaces with single polymers. , 2003, Chemphyschem : a European journal of chemical physics and physical chemistry.

[28]  G. Reilly,et al.  The effects of damage and microcracking on the impact strength of bone. , 2000, Journal of biomechanics.

[29]  Zhigang Suo,et al.  Deformation mechanisms in nacre , 2001 .