The structural motifs of mineralized hard tissues from nano- to mesoscale: A future perspective for material science

Abstract

Biological tissues have developed structures that fulfil their various specific requirements. Mineralized tissues, such as tooth and bone, are often of mechanical competence for load bearing. Tooth enamel is the hardest and toughest mineralized tissue. Despite a few millimeters thick and with minimal regenerative capacity, human tooth enamel maintains its functions throughout a lifetime. Bone provides skeletal support and essential metabolism to our body. Degenerative diseases and ageing induce the loss of mechanical integrity of the bone, increasing the susceptibility to fractures. Tooth and bone share certain commonalities in chemical components and material characteristics, both consisting of nanocrystalline apatite and matrix proteins as their basic foundational structural units. Although the mechanical properties of such mineralized hard tissues remain unclear, it is plausible that they have an inherent toughening mechanism. Nanoindentation is able to characterize the mechanical properties of tooth enamel and bone at multiscale levels, and the results suggest that such toughening mechanisms of enamel and bone may be mainly associated with the smallest-scale structure-function relationships. These findings will benefit the development of advanced biomaterials in the field of material science and will further our understanding of degenerative bone disease in the clinical community.

Keywords: Bone; Mechanical property; Mineralized tissue; Nanoindentation; Tooth.

Fig. 1

Hierarchical structure of tooth enamel (license: Creative Commons CC-BY). (a) A schematic 3D structure of enamel, showing keyhole-like rods aligned in parallel. The rods contain organized and bundled apatite crystals. (b) Rods viewed along their longitudinal direction. (c) Rods viewed along their transverse direction. (d) The structure of partially aligned apatite nanowires viewed from a cross-section parallel to the direction of the rods. The alignment angle φ with respect to the global X-axis is also shown.

Fig. 2

Nanoindentation tests of enamel rods (license number: 5375690944827). Representative atomic force microscopy image of a polished enamel surface. The indentation points are marked with arrows.

Fig. 3

a) The typical schema of performing nanoindentation with a Berkovich diamond indenter. Generally, the test is performed by applying the controlled load ($P_{\mathit{max}}$) and then, recording the material’s deformation by sensing the contact depth ($h_{\mathit{c}}$) while the force ramping and unloading. b) A typical nanoindentation force-displacement curve from the test of an elastic-plastic material (license: 5375740175063). The hardness and the elastic modulus of the material can be obtained by analysing the contact stiffness (S) of unloading segment. The plasticity is indicated as the displacement is not returning to zero.

Fig. 4

Schematic illustration of the exceptional elastic response (left) and the estimated theoretical elastic deformation (right) of enamel induced by a spherical indenter. The figure shows the indenter tip radius (R), the total penetration depth (ht), the contact depth (hc), and the (temporary) pile-up depth (hs). The h values are much smaller than R in reality. An extension of the contact area prevents frictional sliding between nanocrystals or detachment of the protein glue, and there is therefore an enhanced elastic limit (left). Enhanced contact stiffness resulting from an increase in the true contact area (left) as a function of the estimated contact area calculated from quasi-static elastic theory (right) results in an apparent high elastic modulus (license: 5375750655737).

Fig. 5

Schematic drawing of the basic principle of the sacrificial bond–hidden length mechanism (license: 5374611137473). Before a sacrificial bond is broken, only the black length of the molecule contributes to entropic spring, and therefore to the force with which the molecule resists stretching. The red length of the molecule is hidden from the applied force by the sacrificial bond. When the bond breaking force is reached, only a small amount of energy is needed to break the sacrificial bond. Subsequently, the whole length (black plus red) contributes to the entropy of the molecule. In total, the increase in the energy required to break the molecule can be determined from the shaded area under the first peak.

Fig. 6

Schematic illustrations of bone hierarchical structures , (license: 5375790444716).

Fig. 7

Typical nanoindentation strategy for viscoelastic materials. a). An example of load-displacement curve for viscoelastic material if the holding time is not applied, showing notable hysteresis loop. The viscosity results a notable ‘nose’ in the curve, indicating the large delay in strain responses. The apparent contact stiffness (S) is negative in this case. b) The loading function for viscoelastic materials. Ṗ_L is the loading rate and Ṗ_u is the unloading rate at the onset of unloading slope. The applied load is held for a period ($T_{\mathit{hold}}$) when reaches maximum ($P_{\mathit{max}}$). c) A correction for elastic modulus determination may be made by replacing S with the effective contact stiffness Se . The viscoelastic hysteresis loop can be reduced with the application of a holding time (license: 5375740175063).

Fig. 8

Linear viscoelastic deviator creep models, where G is the elastic spring and η is the viscous dashpot: (a) the 3-parameter Maxwell model; (b) the 4-parameter Kelvin–Voigt model; (c) the 5-parameter combined Kelvin–Voigt–Maxwell model (license: 5375800418098).