Functional Implications of the Lacunocanalicular Network Structure in Bone

Bone's ability to adapt its structure is intrinsically linked to osteocytes and their organization within the lacunocanalicular network (LCN). The LCN consists of pores called lacunae, which are interconnected with each other by submicrometer diameter channels called canaliculi. The lacunae accommodate the cell bodies of osteocytes, while the cell processes run within the canaliculi. The stunning density of the LCN is demonstrated by the fact that one cubic centimeter of human osteonal bone comprises 74 kilometers of canaliculi [1]. Multiple functions are attributed to the LCN and the osteocyte network. Besides facilitating transport and signaling, e.g. during bone mineralization [2], the network structures are hypothesized to play a crucial role in mechanosensing and the orchestration of bone remodeling [3]. The Fluid Flow Hypothesis states that deformation of our bones by physical activity results in load-induced fluid flow through the LCN. This flow generates shear and drag forces, which can be sensed by osteocytes. We have developed an experimental and computational workflow which allows us to (i) image the three-dimensional architecture of the LCN using confocal laser scanning microscopy; (ii) quantify the architecture of the spatial network; (iii) calculate the fluid flow through the network. Our study investigates the architecture and the resulting fluid flow through the LCN in human osteons [4]. Specifically, we aim to (i) quantitatively describe how the geometrical asymmetry of osteons influences LCN architecture; and (ii) characterize how bone aging and the occurrence of micropetrosis (the mineralization of lacunae after osteocyte death) influences the fluid flow through the LCN. We pursue this aim by systematically “closing” specific lacunae in the computational model and analyze the effect on the fluid flow pattern. Our analysis should clarify the resilience of the LCN - in clinical terms, how much micropetrosis contributes to a reduced mechanosensation of osteonal bone with age.