Plasticity and toughness in bone

crystals, water, and ions, bone forms the lightweight but tough and protective load-bearing framework of the body. Bone’s elastic modulus—its stiffness during elastic deformation—spans 15–25 GPa, roughly a third of metallic aluminum; its strength, the applied stress at the onset of plastic deformation, is a few hundred MPa, comparable with alumina ceramics; and its fracture toughness, a measure of the material’s resistance to fracture, is typically 3−10 MPa/m, some 3 to 10 times as high as silicon. Although other materials may be mechanically superior, bone is unique for its capacity for self-repair and adaptation.1 Unfortunately, aging-related changes to the musculoskeletal system increase bone’s susceptibility to fracture,2 which can be especially serious in the case of the elderly. Several variables are involved, among them the frequency of traumatic falls, prior fractures, and loading history, but bone tissue itself appears to deteriorate with age.3 A primary factor in that deterioration is bone quality, a loosely defined term used to describe some, but not yet all, microscopic and macroscopic structural characteristics that influence bone’s mechanical properties. Traditional thinking on bone’s deterioration has focused on bone quantity—described by the bone mass or bonemineral density (BMD)—as a predictor of fracture risk. For example, the elevation in bone repair activity, known as remodeling, among aging postmenopausal women in particular can lead to osteoporosis. Disease statistics from the National Osteoporosis Foundation bear out the magnitude of the problem: One in two women and one in four men over the age of 50 will suffer an osteoporosisrelated fracture over their remaining lifetimes. Mounting evidence indicates that low BMD, however, is not the sole factor responsible for the fracture risk. A landmark study 20 years ago by Sui Hui and colleagues showed a roughly 10-fold increase in fracture risk with aging, independent of BMD.2 That result and the fact that BMD alone cannot explain therapeutic benefits of antiresorptive agents in treating osteoporosis emphasize the need to understand the factors that control bone quality. Although bone is a simple composite of a mineral phase, calcium phosphate–based hydroxyapatite, embedded in an organic matrix of collagen protein, its structure is highly complex and hierarchical: Features at smaller length scales form the basis for features at higher ones,4 as shown in figure 1. A vital question is the origin of the material’s fracture resistance in those various structural elements. The physics of fracture is characterized by dissipation of elastically stored energy from an applied load. Materials begin to fracture when the elastic energy dissipated by the advance of a crack is equal to or larger than the energy required to create a new surface. Thus, the more energydissipation (or toughening) mechanisms that exist, the more difficult it is to break a material. One hypothesis is that in bone, toughening mechanisms exist at all characteristic length scales. But as bone changes with age, so can structural features and phenomena—from the cross-linking of collagen proteins to the actual macroscopic path taken by a crack. Unfortunately, it’s difficult to discern the roles that structural constituents play during the initiation of a crack and the crack’s subsequent propagation. If the links between biological factors, bone structure (from molecular to macroscopic levels), fracture mechanism, and toughness can be established, then the concept of bone quality will hopefully become a quantifiable entity. Moreover, once the structural mechanisms underlying any change in bone quality are identified, it is entirely feasible that new and perhaps more effective therapeutic treatments can be developed to treat bone disorders. In this article, we outline what is known about how bone derives its resistance to permanent deformation and fracture by examining the multidimensional nature of its structure.