Osteocytic Canalicular Networks: Morphological Implications for Altered Mechanosensitivity

Osteocytes are ramified bone cells distributed throughout the bone matrix within a network of micrometer-scale cavities (lacunae) and numerous nanometer-thick tunnels (canaliculi). The integrity of the canalicular network might influence bone quality and reflect its mechanosensory potential. In this study, we applied an acid etching technique to embedded bone specimens that allows 3D observation of the canalicular network across a 2D plane to quantitatively assess the canalicular connections in cortical bone specimens from young and aged individuals. Our results showed a nearly 30% reduction in the number of canaliculi per osteocyte lacuna in aged individuals (N.Ot.Ca/Ot.Lc: 15.92 +/- 1.5 in aged vs 22.10 +/- 2.82 in young; p < 0.001); moreover, canalicular number was found to be inversely related to the osteonal tissue age represented by Ca/P ratio (p < 0.001). We frequently observed the phenomenon that canaliculi of osteocytes located near the osteon's periphery did not end at the osteon's cement line boundary but penetrated through the cement line and spread into the surrounding bone matrix, thus establishing an "external rooting" or "connection", which might have significant relevance to bone quality. Our findings showed that not only does the aging process diminish the canalicular network within osteons, but it also significantly reduces the probability of external osteonal rooting and connections with the surrounding bone tissue. Deterioration in the canalicular network with age reduces the connectivity between osteocytes and between osteons/interstitial tissue, which affects the supply of nutrients to osteocytes, degrades their mechanosensitivity, and contributes to increased bone fragility in the elderly.