The human osteocyte lacunocanalicular network structure in osteons of the iliac crest of elderly women depends on mineral content but not individual age

Osteocytes provide essential functions for the maintenance of healthy bone tissue. They are embedded in lacunar pores within the mineralised bone matrix and communicate through interconnected dendritic cell processes that are housed in canalicular channels constituting the osteocyte lacunocanalicular network (LCN). Ageing is associated with increased fracture risk and bone fragility, particularly in elderly women. Despite the LCN playing a critical role in bone remodelling, characteristics of the network in bone tissue of different individual age and mineral content is thus far largely unexplored. Confocal laser scanning microscopy was used to image the fluorescent-stained LCN of cortical osteons in iliac crest bone specimens from female donors with mean age 60 years (n = 6) and 94 years (n = 6) in 3D. Quantitative backscattered electron imaging was also used to assess osteonal mineral content to compare LCN structure in highly and lowly mineralised osteons. Network defects were identified in one-third of osteons, which were further investigated using focussed ion beam scanning electron microscopy. Assessment of the LCN revealed no influence of individual age on the canalicular density, the volume of the lacunae or the degree of the lacunae, whereas canalicular density is inversely correlated with osteonal mineral content. An increase in the volume of non-mineralised matrix is demonstrated in defective regions that are prevalent in all individuals. While relative osteon age, as characterised by mineral content, influences the density of the canaliculi in the LCN, there is no influence of the age of the individual women over 60 years. STATEMENT OF SIGNIFICANCE: Osteocytes play a central and ongoing role in bone health throughout the lifespan: they orchestrate bone remodelling by regulating osteoclastic bone resorption and osteoblastic bone deposition, as well as controlling subsequent bone mineralisation. Deterioration of the osteocyte lacunocanalicular network may contribute to the decline in bone quality observed with age. Consequently, we studied this communication system in 3D in bone from middle-aged to elderly donors. Unexpectedly, individual age had no influence on network characteristics, but the density of the network was decreased in older osteons. Furthermore, we observed network defects that are surprisingly common at all ages investigated. The size of these defects increases with age, suggesting a possible link to the concurrent reduction in bone quality.