Effect of collagen fibril orientation on the anisotropic properties of peri-implant bone.

In orthopedic and dental surgery, the implantation of biomaterials within the bone to restore the integrity of the treated organ has become a standard procedure. Their long-term stability relies on the osseointegration phenomena, where bone grows onto and around metallic implants, creating a bone-implant interface. Bone is a highly hierarchical material that evolves spatially and temporally during this healing phase. A deeper understanding of its biomechanical characteristics is needed, as they are determinants for surgical success. In this context, we propose a multiscale homogenization model to evaluate the effective elastic properties of bone as a function of the distance from the implant, based on the tissue's structure and composition at lower scales. The model considers three scales: hydroxyapatite foam (nanoscale), ultrastructure (microscale), and tissue (mesoscale). The elastic properties and the volume fraction of the elementary constituents of bone matrix (mineral, collagen, and water), the orientation of the collagen fibril relative to the implant surface, and the mesoscale porosity constitute the input data of the model. The effect of a spatiotemporal variation in the collagen fibrils' orientation on the bone anisotropic properties in the proximity of the implant was investigated. The findings revealed a strong variation of the components of the effective elasticity tensor of the bone as a function of the distance from the implant. The effective elasticity appears to be primarily sensitive to the porosity (mesoscale) rather than to the collagen fibrils' orientation (sub-micro scale). However, the orientation of the fibrils has a significant influence on the isotropy of the bone. When analyzing the symmetry properties of the effective elasticity tensor, the ratio between the isotropic and hexagonal components is determined by a combination of the porosity and the fibrils' orientation. A decrease in porosity leads to a decrease in bone isotropy and, in turn, an increase in the impact of the fibrils' orientation. These results demonstrate that the collagen fibril orientation should be taken into account to properly describe the effective elastic anisotropy of bone at the organ scale.

Design and assessment of the biomimetic capabilities of a Voronoi-based cancellous microstructure.

Parameterized cellular microstructures allow for the development of efficient multiscale optimization strategies for the design of Functionally Graded Scaffolds (FGSs). This work assesses the biomimetic capabilities of the Voronoi-based cancelous bone microstructure introduced by Fantini et al. (2016) in terms of histomorphometric and elastic properties. Histomorphometric data of 23 bovine bone specimens and elastic data of 140 human bone specimens are used as reference. Based on the key findings that there exists a strong correspondence between the trabecular thickness and the solid volume fraction for natural cancelous bone, and that the stretching of the Voronoi microstructure is an effective means to induce anisotropy, the generative procedure by Fantini et al. (2016) is assessed and tuned to account for anisotropy and elastic properties. It is shown that the resulting mimetic microstructures have histomorphometric features and elastic properties that are in very good accordance to those of the natural samples. The outcomes of this work are a step forward towards the integration of the Voronoi-based microstructure into multiscale design tools.

Multiscale design of artificial bones with biomimetic elastic microstructures.

Cancellous bone is a highly porous, heterogeneous, and anisotropic material which can be found at the epiphyses of long bones and in the vertebral bodies. The hierarchical architecture makes cancellous bone a prime example of a lightweight natural material that combines strength with toughness. Better understanding the mechanics of cancellous bone is of interest for the diagnosis of bone diseases, the evaluation of the risk of fracture, and for the design of artificial bones and bone scaffolds for tissue engineering. A multiscale optimization method to maximize the stiffness of artificial bones using biomimetic cellular microstructures described by a finite set of geometrical micro-parameters is presented here. The most outstanding characteristics of its implementation are the use of: an interior point optimization algorithm, a precalculated response surface methodology for the evaluation of the elastic tensor of the microstructure as an analytical function of the micro-parameters, and the adjoint method for the computation of the sensitivity of the macroscopic mechanical response to the variation of the micro-parameters. The performance and effectiveness of the tool are evaluated by solving a problem that consists in finding the optimal distribution of the microstructures for a proximal end of a femur subjected to physiological loads. Two strategies for the specification of the solid volume fraction constraints are assessed. The results are compared with data of a computed tomography study of an actual human bone. The model successfully predicts the main features of the spatial arrangement of the trabecular and cortical microstructures of the natural bone.

Mimetization of the elastic properties of cancellous bone via a parameterized cellular material.

Bone tissue mechanical properties and trabecular microarchitecture are the main factors that determine the biomechanical properties of cancellous bone. Artificial cancellous microstructures, typically described by a reduced number of geometrical parameters, can be designed to obtain a mechanical behavior mimicking that of natural bone. In this work, we assess the ability of the parameterized microstructure introduced by Kowalczyk (Comput Methods Biomech Biomed Eng 9:135-147, 2006. doi: 10.1080/10255840600751473 ) to mimic the elastic response of cancellous bone. Artificial microstructures are compared with actual bone samples in terms of elasticity matrices and their symmetry classes. The capability of the parameterized microstructure to combine the dominant isotropic, hexagonal, tetragonal and orthorhombic symmetry classes in the proportions present in the cancellous bone is shown. Based on this finding, two optimization approaches are devised to find the geometrical parameters of the artificial microstructure that better mimics the elastic response of a target natural bone specimen: a Sequential Quadratic Programming algorithm that minimizes the norm of the difference between the elasticity matrices, and a Pattern Search algorithm that minimizes the difference between the symmetry class decompositions. The pattern search approach is found to produce the best results. The performance of the method is demonstrated via analyses for 146 bone samples.

Calculation of cancellous bone elastic properties with the polarization-based FFT iterative scheme.

The Fast Fourier Transform-based method, originally introduced by Moulinec and Suquet in 1994 has gained popularity for computing homogenized properties of composites. In this work, the method is used for the computational homogenization of the elastic properties of cancellous bone. To the authors' knowledge, this is the first study where the Fast Fourier Transform scheme is applied to bone mechanics. The performance of the method is analyzed for artificial and natural bone samples of 2 species: bovine femoral heads and implanted femurs of Hokkaido rats. Model geometries are constructed using data from X-ray tomographies, and the bone tissue elastic properties are measured using microindentation and nanoindentation tests. Computed results are in excellent agreement with those available in the literature. The study shows the suitability of the method to accurately estimate the fully anisotropic elastic response of cancellous bone. Guidelines are provided for the construction of the models and the setting of the algorithm.