Electromechanical properties of bone at the nanometre and micrometre scale

The mechanical and electromechanical behaviour of bone such as elasticity and piezoelectricity have long been considered to be a consequence of its hierarchical architecture, the basic building block of which, at the nanostructural level, is a finely interleaved composite of collagen fibrils and apatite, a substituted calcium orthophosphate. Also, stress generated surface charge in bone in the form of piezoelectricity and streaming potential is believed to be the driving force behind bone remodelling. However, very little is known about the basic mechanism for dissipating stress and surface charge at the local level of organisation between the composites. In this study, the relationship between electromechanical properties of bone and its molecular foundation is investigated. To achieve this, the organic and inorganic constituents of a bovine bone were separated from each other using chemical extraction methods. Microscopic techniques were then employed to analyse the morphology of the unextracted (raw) bone and the results were compared with that of the extracted bone. Chemical characterisation techniques were used to determine the purity of the extracted constituents of bone. The electromechanical properties of bone were studied using both vertical and lateral Piezoresponse Force Microscopy (PFM). To obtain a common framework for comparison of quantitative values obtained for piezoelectricity measured in both nano and microscopic scales, the standard equivalent single crystal structures of bone was resorted. For this, a transformation of reference axes was necessary to take into consideration the PFM probe/sample orientation as well as the mode of scanning. Piezoelectric coefficients measured in lateral PFM (represented as d34 constants) showed a trend of increasing value when the angle of the sample was varied between 0°, 45° and 90° with respect to the bone’s macroscopic axis. The shear piezoelectricity measured by PFM in micro and nanoscopic scale, 3.48±0.08 pC/N and 4.06±0.30 pC/N respectively, are comparable to collagen’s macroscopic piezoelectric constant (1.4 pC/N) and its single crystal equivalent standards (2.89 pC/N). Finally, the work revisited the original investigation of the orientation dependence of macroscopically measured piezoelectricity in light of the PFM technique and suggested that there was a variation in PFM response for bone and collagen if one switches from a transverse lateral measurement to a longitudinal lateral measurement. While the subject matter of this article is bone and collagen, this developed methodology can be useful in quantitative analysis of nano and microscopic piezoresponse measured on any piezoelectric composite or biopolymer possessing uniaxial texture.