A new theory of bone lamellation

Abstract

A comparative polarized light (PLM), scanning (SEM), and transmission (TEM) electron microscopy study was carried out on cross- and longitudinal sections of human lamellar bone in the tibiae of four male subjects aged 9, 23, 45, and 70 years. SEM analysis was also performed on rectangular-prismatic samples in order to observe each lamella sectioned both transversely and longitudinally. The results obtained do not confirm the model hitherto suggested to explain the lamellar appearance of bone. In particular, the classic description by Gebhardt (still accepted by the majority of bone researchers), which suggests that collagen fibers alternate between longitudinal and transversal in successive lamellae, or that they have spiral paths of different pitches, appears to be no longer acceptable in the light of our findings. In fact, SEM and TEM observations here reported agree in demonstrating that lamellar bone is made up of alternating collagen-rich (dense lamellae) and collagen-poor (loose lamellae) layers, all having an interwoven arrangement of fibers. No interlamellar cementing substance was observed between the lamellae, and collagen bundles form a continuum throughout lamellar bone. Preliminary measurements of lamellar thickness indicate that dense lamellae are significantly (P < 0.001) thinner than loose lamellae. Compared with the classic model of Gebhardt, the dense lamellae correspond to the transverse lamellae and are birifringent under PLM, whereas the loose lamellae correspond to the longitudinal lamellae and are extinguished. Collagen-fiber organization in dense and loose lamellae is discussed in terms of bone biomechanics and osteogenesis.