3 Pathophysiology of Fractures

       J.L. Pye and S.M. Stover

       UC Davis School of Veterinary Medicine, University of California, Davis, CA, USA

Material Features of Bone Failure

      Bones are composite structures of heterogeneous materials that have unique capacities to resist structural failure, self‐repair, and adapt to changes in mechanical usage [1–4]. The hierarchical composite structure of bone results in structural properties that are greater than that of the individual components. Mechanisms of failure are related to the hierarchical structures and components, although the roles that specific microstructural constituents play in crack initiation, propagation and final unstable fracture are incompletely understood [5, 6].

      Bone is a biphasic composite comprised of organic and inorganic components, and water in approximate volumetric proportions of 35, 40, and 25% respectively [7]. The inorganic component is primarily crystalline hydroxyapatite [Ca₃(PO₄)₂]₃Ca(OH)₂. The organic matrix is comprised mainly of type I collagen. The degree of mineralization confers strength and stiffness [8–10], and the collagen phase contributes ductility and overall toughness [11, 12].

On the nanoscale level, type I collagen fibres consisting of staggered collagen molecules are reinforced by hydroxyapatite crystals [13–16]. Type I collagen is a triple helix containing three chains of amino acids that are cross‐linked by hydrogen bonds to form tropocollagen molecules. Staggered arrays of multiple tropocollagen molecules are covalently bonded together to form a collagen fibril. Fibril arrays twist into individual collagen fibres. Hydroxyapatite crystals assemble in gaps between collagen fibrils, resulting in mineralization of fibrils as the bone forms and matures (Figure 3.1). Collagen fibre organization varies from random in rapidly formed woven bone to highly organized in lamellar bone.

      Haversian systems are present in compact bone to provide vascularization to osteocytes embedded in bone matrix. Concentric lamellae that surround a central blood vessel in Haversian canals make up the osteons of the Haversian system in compact bone [17]. Primary osteons are the first to be laid down during bone formation and growth. During postnatal growth, increase in long bone diameter is achieved through periosteal formation of woven bone that provides the structure for the formation of primary osteons or circumferential lamellae. Throughout life, there is continual replacement of bone through remodelling. Bone tissues are resorbed and replaced with secondary osteons [18, 19]. Secondary osteons can be recognized by the presence of peripheral cement lines, an approximately 2 μm thick, collagen‐deficient region at their outer boundary [17, 20]. Cement lines are formed by osteoblasts at the time of transition from bone resorption to formation [21–23].

      Mineralization and crystallinity are closely metabolically regulated and modulated to optimize mineral homeostasis and mechanical function. Bone tissue matrix is not fully saturated with mineral. Higher mineralization increases the load required to initiate cracks, but enhances propagation of cracks because the structure is less able to dissipate energy [5]. Excessive mineralization increases brittleness and susceptibility to microcracks at lower levels of deformation [24, 25]. Conversely, low mineralization weakens the bone and increases fragility [16, 25].

      Collagen does not contribute significantly to matrix strength and stiffness but is critical to toughness, the energy required to cause failure [11]. Collagen comprises >90% of the organic component of bone and is largely responsible for its viscoelastic properties [7]. Collagen has increased stiffness with increased loading rate, while the mineral phase is largely unaffected [26]. Higher loading rates therefore reduce bone compliance at the microstructural level, resulting in increased brittleness and a reduction in fracture resistance [26]. This rate‐dependent change in fracture toughness results in a transition from ductile to brittle behaviour [27–30].