Fractures in the Horse. Группа авторов
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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].
Figure 3.1 Schematic illustration of bone microstructure showing major osteonal components.
Loading Modes
The biomechanical response of bone to loading is dependent on its geometry and material composition, and the loading environment. Loading characteristics include the direction, rate, magnitude, frequency and duration of applied loads. Loads may be applied locally (e.g. at the tips of microcracks) or globally (e.g. in the far‐field, acting on the whole bone).
Locally Acting Loading Modes
Compact bone invariably contains microcracks, and an understanding of the modes of fracture must take into account their presence [31, 32]. The direction of crack propagation within the bone and the microstructure of the bone material have profound influences on fracture resistance. Transverse cracking, where the crack must course through longitudinally oriented osteons, is tougher than longitudinal cracking, where the crack splits osteons along the longitudinal axis of the bone [33, 34]. The process of bone remodelling increases resistance to crack propagation by adding secondary osteons and cement lines throughout the structure and by reorganizing osteons and trabeculae along directions of high stresses.
Globally Acting Loading Modes and Resulting Fracture Configurations
During normal daily activity, forces and moments are applied to whole bone structures in various directions simultaneously [35]. Loading conditions are often simplified to single axis loading in tension, compression, shear, bending, torsion or combined loading of a homogeneous structure with isotropic material properties (Figure 3.2). Such analyses provide insight into the circumstances that led to bone fracture, but may not accurately reflect the in vivo loading conditions.
Bone is an anisotropic material, meaning its mechanical properties depend on the direction of the applied forces. In general, because of the structure and orientation of osteons, compact bone is strongest in axial compression, weaker in tension and weakest in shear. As a result, fractures usually propagate along tension and shear planes. Shear planes run at approximately 45° angles from compressive and tensile stresses. Fractures will also follow the path of least resistance. Therefore, fracture lines or cracks will often be diverted around heavily buttressed areas. Likewise, fractures may terminate at suture lines or pre‐existing cracks as these dissipate fracture energy more efficiently.
Classic loading modes and fracture configurations are readily applicable to long bones, and diaphyseal fractures are mostly used to illustrate these concepts. They are also recognized in some types of epiphyseal [37], proximal sesamoid [38] and carpal cuboidal bone fractures [39, 40] in horses. However, these loading modes and associated fracture configurations are currently not well understood in relation to a number of other common equine sites, such as distal phalangeal, distal sesamoidean and tarsal cuboidal bone fractures.
Tension
Tensile loading occurs when equal and opposite loads are applied to distract