The Ultrastructure of Bone and Its Relevance to Mechanical Properties

Henry P. Schwarcz,Iwona Jasiuk,Diab Abueidda

doi:10.3389/fphy.2017.00039

Henry P. Schwarcz, Iwona Jasiuk + Show 1 more

Open Access

https://doi.org/10.3389/fphy.2017.00039

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Abstract

Bone is a biologically generated composite material comprised of two major structural components: crystals of apatite and collagen fibrils. Computational analysis of the mechanical properties of bone must make assumptions about the geometric and topological relationships between these components. Recent transmission electron microscope (TEM) studies of samples of bone prepared using ion milling methods have revealed important previously unrecognized features in the ultrastructure of bone. These studies show that most of the mineral in bone lies outside the fibrils and is organized into elongated plates 5 nanometers (nm) thick, ~ 80 nm wide and hundreds of nm long. These so-called mineral lamellae (MLs) are mosaics of single 5 nm-thick, 20 – 50 nm wide crystals bonded at their edges. MLs occur either stacked around the 50 nm-diameter collagen fibrils, or in parallel stacks of 5 or more MLs situated between fibrils. About 20% of mineral is in gap zones within the fibrils. MLs are apparently glued together into mechanically coherent stacks which break across the stack rather than delaminating. ML stacks should behave as cohesive units during bone deformation. Finite element computations of mechanical properties of bone show that the model including such features generates greater stiffness and strength than are obtained using conventional models in which most of the mineral, in the form of isolated crystals, is situated inside collagen fibrils.

Highlights

One of the main functions of bone in land-living vertebrates is to provide a support for the animal and a framework to which musculature can be attached
We summarized our recent transmission electron microscopy observations pointing out to an alternate collagen-mineral arrangement in bone at the nanoscale
This model proposes mineral lamellae surrounding outer surfaces of collagen fibrils, as opposed to minerals being mainly embedded in a collagen fibril

Summary

INTRODUCTION

One of the main functions of bone in land-living vertebrates is to provide a support for the animal and a framework to which musculature can be attached. We study computationally the novel geometric model of a mineralized collagen fibril, described in Section Three-Dimensional Organization of Bone at Nanoscale and shown, involving the extrafibrillar mineral lamellae encircling a collagen fibril, and compare it with a classical model involving isolated minerals in a collagen fibril Such newly proposed geometrical arrangement of collagen and apatite crystals at the nanoscale should have a significant impact on the mechanical properties of bone at the nanoscale and higher scales. We consider two cases, one involving mineral-mineral interfaces connected via the traction-separation interface model and one assuming a protein layer between the mineral lamellae and taking the properties of that layer same as of the collagen, for simplicity This layer could physically represent non-collagenous proteins, as mentioned in Section Three-Dimensional Organization of Bone at Nanoscale. Note that the Model II with no interphase shows highest stiffness and strength while Model I gives highest strain at failure

Findings

Discussion of Finite Element Results

SUMMARY