Sealed osteons in animals and humans: low prevalence and lack of relationship with age.

Abstract

Sealed osteons are unusual variants of secondary osteons that have received little attention, especially in non-human bones. Sealed osteons are characterized by central canals that are plugged with bone tissue. As with other variants of secondary osteons (e.g. drifting, dumbbell, multi-canal), understanding how and why sealed osteons form can shed light on the mechanisms that regulate normal bone remodeling and how this process can be perturbed with aging and some diseases. In a recent microscopic evaluation of human tibiae obtained after traumatic amputations, 4-5% of the osteons were sealed. It is suggested that this high prevalence reflects occasional localized microscopic ischemia from normal osteonal remodeling; hence sealed osteons are implicated in human skeletal fragility. Therefore, osteon prevalence would be expected to correlate with the bone remodeling seen with aging; for example, showing positive relationships between sealed osteons and the population density of typical secondary osteons (OPD). We evaluated the prevalence of partially sealed (80-99% sealed) and fully sealed osteons with respect to age and variations in OPD in 10 adult human femora (34-71years) and in various non-human appendicular bones of mature animals that were not of advanced age, including deer calcanei, equineradii and equine thirdmetacarpals. An additional sample of 10 bilateral human femora with unilateral non-cemented total hip replacements (F,+HR) and non-implanted contralateral femora (F,-HR) were evaluated (10 patients; 52-94years). In non-human bones, sealed+partially sealed osteons were rare (~0.1%) even when having relatively high OPD. When considering sealed+partially sealed osteons in femora from patients without any HR, results showed that 1.6% of the osteons were sealed or partially sealed, which was much lower than anticipated, but this is 10- to 20-fold more than in any of the non-human bones. Additionally, in all bones, sealed+partially sealed osteons were significantly smaller than typical secondary osteons (mean diameters: 125 vs. 272μm; P<0.005). In the patients with HR, the percentage of sealed+partially sealed osteons: (i) did not correlate with age, (ii) showed no significant difference between F,-HR and F,+HR (1.9 vs. 2.1%; P=0.2), and (iii) was positively correlated with OPD (r=0.67, P=0.001), which differs from the very weak or lack of correlations in the non-human bones and the other human femur sample. The lack of an age-related relationship, in addition to the very low prevalence of sealed+partially sealed osteons are inconsistent with the idea that they contribute to reduced bone quality seen in aging humans. The small size of sealed and partially sealed osteons, regardless of species affiliation, suggests that they represent closing cones at the termini of some osteons. Available evidence suggests that osteons of primates might have a greater capacity for branching that is associated with closing cones, which might explain the 10-20 times higher prevalence of sealed+partially sealed osteons in the human bones examined in this study.