Cooperative deformation of mineral and collagen in bone at the nanoscale

Abstract

In biomineralized tissues such as bone, the recurring structural motif at the supramolecular level is an anisotropic stiff inorganic component reinforcing the soft organic matrix. The high toughness and defect tolerance of natural biomineralized composites is believed to arise from these nanometer scale structural motifs. Specifically, load transfer in bone has been proposed to occur by a transfer of tensile strains between the stiff inorganic (mineral apatite) particles via shearing in the intervening soft organic (collagen) layers. This raises the question as to how and to what extent do the mineral particles and fibrils deform concurrently in response to tissue deformation. Here we show that both mineral nanoparticles and the enclosing mineralized fibril deform initially elastically, but to different degrees. Using in situ tensile testing with combined high brilliance synchrotron X-ray diffraction and scattering on the same sample, we show that tissue, fibrils, and mineral particles take up successively lower levels of strain, in a ratio of 12:5:2. The maximum strain seen in mineral nanoparticles (Ϸ0.15-0.20%) can reach up to twice the fracture strain calculated for bulk apatite. The results are consistent with a staggered model of load transfer in bone matrix, exemplifying the hierarchical nature of bone deformation. We believe this process results in a mechanism of fibril-matrix decoupling for protecting the brittle mineral phase in bone, while effectively redistributing the strain energy within the bone tissue.biomineralization ͉ deformation mechanisms ͉ in situ tensile testing ͉ micromechanics of bone ͉ synchrotron radiation

Large Deformation Mechanisms, Plasticity, and Failure of an Individual Collagen Fibril With Different Mineral Content

“…The composite combines the optimal properties of both constituents to form a remarkably stiff and tough low‐density material 2. Although the larger‐scale bone structure varies depending on bone type and species, the mineralized collagen fibril structure is highly conserved among species and represents the universal building block of bone 12, 13. Collagen–apatite composites are not only the basic building blocks of human bone, but they are also among the most abundant class of biomineralized materials in the animal kingdom 2, 5…”

“…However, the size and complexity of the structure of mineralized collagen fibrils make it challenging to understand the nanoscale mechanisms governing the fibril mechanics. Other studies based on analytical models have uncovered some key mechanistic features of mineralized tissues where experiments reach their limits, shedding some light on the role of mineral platelets in material strengthening 13, 18, 19, 20, 21, 22. These models help link the nanostructure of the tissue to the organ's mechanical response by integrating some levels of the complex hierarchical structure of bone.…”

On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone

“…Surprisingly, this issue is often ignored but has become of importance as in situ testing with high-energy synchrotron x-ray diffraction [25][26][27][28][29][30][31] and tomography imaging [32,33] is now commonly used to identify the micrometer and even sub-micrometer deformation and fracture mechanisms in mineralized tissues.…”

Measurement of the Mechanical Properties of Bone: A Recent History

“…For example, Nyman et al [36] found that in men's bones the amount of bound water decreased with age, and the toughness decreased concomitantly. Synchrotron radiation can be used in various modes, either as a source of light to examine strains in the different components of bone [22] or for more straightforward tomography, producing images of relatively large specimens [52]. Apart from the capital and running costs of a synchrotron facility, synchrotron radiation is ideal in many ways for doing a whole range of mechanical and characterization studies.…”

“…There has been progress over the years [17,24,25,43,59]. Recently these efforts have taken on new importance because it is becoming possible to measure the mechanical properties of very small pieces of bone, so the relationship between theory and reality is gradually becoming clearer, though it has not yet arrived [21][22][23].…”