What is the effect of cell network topology on the poro-elastic properties of bone?Part of:
The microscopic porosity in bone forms a network-like structure which houses in its lacunae the cell bodies of osteocytes and in its canaliculi the long processes of these cells. It is thought that fluid flow through the canalicular network contributes to nutrition and mineral transport and to mechanotransduction by stimulating osteocytes due to shear forces. Poroelastic models have therefore been used to study the fluid flow through this network. However, these networks have a very heterogeneous topology  which has been neglected in these studies. We hypothesize that the network topology has a significant impact on fluid flow properties. The aim of our study was to use 3D imaging of actual networks and computational fluid flow analysis to perform a functional assessment of two common, but very different types of human osteons: 1) normal secondary osteons and 2) osteon-in-osteons, which consist of a newly formed smaller osteon within an existing parental osteon.
Confocal microscopy was used to image the osteocyte canalicular network in human osteons of both types. The 3D data was then translated into network models where the edges represented the canaliculi and nodes represented intersections of canaliculi (i.e. intersections of edges) and the lacunae . Functional network analysis methods, inspired by the existing poro-elastic models of bone , were then used to simulate compression induced fluid flow and pressure patterns in the imaged networks.
Being based on real network topologies our analyses provide predictions of the variability of the fluid flow in human osteons. Although in both osteon types the network density is heterogeneous, only osteon-in-osteons show a particular heterogeneous network structure with a ring of low network connectivity. This ring is bridged by few canaliculi, leading to locally high fluid flow velocities and steep pressure gradients in osteon-in-osteons during dynamic loading of the bone. The network in the normal osteons is closely connected to the rest of the network, while the osteon-in-osteons have regions which are relatively isolated. This could be interpreted as a compromised nutrient transport. On the other hand, the locally higher fluid flow in osteon-in-osteons could result in higher mechanical shear forces and, therefore, a more efficient mechanotransduction compared to normal osteons. Our analysis suggests that different osteon types could contribute differently to the overall mechanosensitivity of bone.