SummaryAging decreases the human femur's fatigue resistance, impact energy absorption, and the ability to withstand load. Changes in the osteocyte distribution and in their elemental composition might be involved in age-related bone impairment. To address this question, we carried out a histomorphometric assessment of the osteocyte lacunar distribution in the periosteal and endosteal human femoral cortexes of 16 female and 16 male donors with regard to age-and sex-related bone remodeling. Measurements of the bone mineral density distribution by quantitative backscattered electron imaging and energy dispersive X-ray analysis were taken to evaluate the osteocyte lacunar mineral composition and characteristics. Age-dependent decreases in the total osteocyte lacunar number were measured in all of the cases. This change signifies a risk for the bone's safety. Cortical subdivision into periosteal and endosteal regions of interest emphasized that, in both sexes, primarily the endosteal cortex is affected by age-dependent reduction in number of osteocyte lacunae, whereas the periosteal compartment showed a less pronounced osteocyte lacunar deficiency. In aged bone, osteocyte lacunae showed an increased amount of hypermineralized calcium phosphate occlusions in comparison with younger cases. With respect to Frost's early delineation of micropetrosis, our microanalyses revealed that the osteocyte lacunae are subject to hypermineralization. Intralacunar hypermineralization accompanied by a decrease in total osteocyte lacunar density may contribute to failure or delayed bone repair in aging bone. A decreased osteocyte lacunar density may cause deteriorations in the canalicular fluid flow and reduce the detection of microdamage, which counteracts the bone's structural integrity, while hypermineralized osteocyte lacunae may increase bone brittleness and render the bone fragile.

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.

No abstract