In this study, the mineralized bone, osteocytes form a multifunctional mechanosensitive network orchestrating bone remodelling. A preserved osteocyte population is a crucial determinant of bone quality. Mineralization of the bone matrix was determined using backscattered electron imaging.

In human auditory ossicles, the early decrease in osteocyte numbers but maintained integrity remains an unexplained phenomenon that might serve for sound transmission from air to the labyrinth. Here we analysed the frequency, size and composition of osteocyte lacunae in the auditory ossicles of 22 individuals from early postnatal period to old age.

The human auditory ossicles malleus, incus and stapes present with their final morphology at birth, while in later life decades only minor morphological changes occur. The ossicles are in the air-filled middle ear and serve for transmission of sound-induced mechanical vibrations from the eardrum to the oval window of the fluid-filled cochlea.

Damage deformation of the ossicular chain lead to conductive hearing loss. While malleus and incus develop from the first pharyngeal arch, the stapes which is the smallest bone in the human body has two embryologically distinct parts. In fact, the cranial end of the second pharyngeal arch forms an independent anlage, which develops into a superior and an inferior part.

The superior part gives origin to the base of the stapes, whereas the inferior part forms the limbs and the head of the stapes. The natural lifespan of osteocytes is believed to be about 25 years. Our results in the auditory ossicles show a dramatic decrease in viable osteocytes already in early childhood, which indicates that the lifespan of osteocytes might be highly site-specific.

Our results indicate that high-frequency vibration in auditory ossicles goes along with osteocyte apoptosis. It is generally known that viable osteocytes provide anti-resorptive signals, while osteocyte apoptosis normally attracts osteoclasts to resorb the bone at the site.

However, the pronounced osteocyte death and subsequent massive accumulation of dead osteocytes without increased bone resorption suggest that there is a factor inhibiting bone resorption in the ossicles, which could be of major interest for the treatment of human bone loss syndromes i.e., osteoporosis.

The subsequent excessive formation of hypermineralized lacunae represents a unique feature in auditory ossicles, as no other skeletal site has shown micropetrotic lacunae in this order of magnitude.

Furthermore, our results strongly underline that the age-dependent changes in auditory ossicles do not only include highly dynamic changes in osteocyte number and mineralization but also an increasing resistance as testified by decreasing indentation depths. Furthermore, early age-related increases in the average unloading slope suggest stiffening of the material at higher mineralization levels.

The indentation distance increase (IDI), which can be interpreted a measure of plasticity, revealed a significant, logarithmic decrease with aging, which may seem contradictory to previous findings.