Local electronic structure and nanolevel hierarchical organization of bone tissue: theory and NEXAFS study

Abstract

Theoretical and experimental investigations of native bone are carried out to understand relationships between its hierarchical organization and local electronic and atomic structure of the mineralized phase. The 3D superlattice model of a coplanar assembly of the hydroxyapatite (HAP) nanocrystallites separated by the hydrated nanolayers is introduced to account the interplay of short-, long- and super-range order parameters in bone tissue. The model is applied to (i) predict and rationalize the HAP-to-bone spectral changes in the electronic structure and (ii) describe the mechanisms ensuring the link of the hierarchical organization with the electronic structure of the mineralized phase in bone. To check the predictions the near-edge x-ray absorption fine structure (NEXAFS) at the Ca 2p, P 2p and O 1s thresholds is measured for native bone and compared with NEXAFS for reference compounds. The NEXAFS analysis has demonstrated the essential hierarchy induced HAP-to-bone red shifts of the Ca and P 2p-to-valence transitions. The lowest O 1s excitation line at 532.2 eV in bone is assigned with superposition of core transitions in the hydroxide OH(HO) anions, Ca(HO) cations, the carboxyl groups inside the collagen and [PO] and [PO] anions with unsaturated P-O bonds.

Thermal changes in young and mature bone nanostructure probed with Ca 2p excitations

“…This number agrees with the experimental values extracted from the X-ray, neutron scattering and EXAFS measurements [53  56]. Thus, the suppression of both the absorption peak at 532.2 eV and the vibration band at 3400 cm -1 in heated bone [18,51,52] makes evident importance of the dehydration and restructuring mechanisms in the hydrated-layer-NOH-Ap-surface network in bone tissue.…”

“…In the framework of the "black-nanoboxes-in-muddy-waters" concept [18] the 3DSL model describes the electronic structure of mineralized bone in terms of the electro-optical characteristics of its nanoelements.…”

“…As an example, we use the values 3d ≈ 2 eV [51], ≈ 0.8 [47], ̃≤ 2 nm and 〈 〉 = 1 3 (20 + 7.5 + 3.5) ≈ 10 nm [18], apply (3) and obtain the OH-Ap-to-bone red shift in mature bone 3d ≤ 0.3 eV. Thus, the 3DSL model estimation of the shift is in good agreement with the experimental data in table 1.…”

“…In general these values agree with the model shift ≈ 0.4 eV computed in assumption that empty spaces separate the equal NOH-Ap in their coplanar assembly. Note that this estimate gives the maximal value of the red shift [18]. To understand why the larger shifts have been detected the authors of [24] have pointed out that the extracted shifts are obtained from the NEXAFS spectra of bone samples by using different techniques to prepare them and different methods to calibrate the absolute energy of X-ray transitions.…”

Site-Dependent Peculiarities of Calcium Bonds in Bone Tissue

“…Material analytical science and biomedical studies disclose the complex hierarchy of the skeleton designs going from the macro level to the nano level. − Bone constituted from organic collagen and mineral bioapatite matrices is a subject of substantial interplay between both adjacent and distant hierarchical levels. Nanoscale research on skeletal structure–function properties encounters great difficulty because the relationship between the hierarchical organization of the skeleton and the electronic and atomic structure and chemical bonding in bone has not been studied enough.…”