Bone microdamage, remodeling and bone fragility: how much damage is too much damage?

Abstract

Microdamage resulting from fatigue or 'wear and tear' loading contributes to bone fragility; however, the full extent of its influence is not completely understood. Linear microcracks (∼50-100 μm) and diffuse damage (clusters of sublamellar-sized cracks) are the two major bone microdamage types, each with different mechanical and biological consequences. Healthy bone, due to its numerous microstructural interfaces and its ability to affect matrix level repair, deals effectively with microdamage. From a material standpoint, healthy bone behaves much like engineering composites like carbon-fiber reinforced plastics. Both materials allow matrix damage to form during fatigue loading and use microstructural interfaces to dissipate energy and limit microcrack propagation to slow fracture. The terms fracture toughness and 'toughening mechanism', respectively, describe mechanical behavior and microstructural features that prevent crack growth and make it harder to fracture a material. Critically, toughness is independent of strength. In bone, primary toughening features include mineral and collagen interfaces, lamellae and tissue heterogeneity among osteons. The damage tolerance of bone and other composites can be overcome with sustained loading and/or matrix changes such that the microstructure no longer limits microcrack propagation. With reduced remodeling due to aging, disease or remodeling suppression, microdamage accumulation can occur along with loss of tissue heterogeneity. Both contribute additively to reduced fracture toughness. Thus, the answer to the key question for bone fragility of how much microdamage is too much is extremely complex. It ultimately depends on the interplay between matrix damage content, internal repair and effectiveness of matrix-toughening mechanisms.

Figure 1

Photomicrograph of cross-section of basic fuchsin-stained human compact bone from a 65-year-old donor. Arrows point linear microcracks that had occurred under physiological loading conditions.

Figure 2

Fluorescence photomicrograph showing diffuse damage stained with basic fuchsin, and diffuse damage was created in vivo in a rat model. Enlarged image on right shows that diffuse damage comprised many ultrastructural small cracks.

Figure 3

Representative curves showing that cyclical loading causes modulus loss and microdamage accumulation in three distinct phases.

Figure 4

Experimentally induced microcracks (μCr, arrows) in cortical bone shown in association with newly activated intracortical resorption spaces (RsSp) at 10 days after fatigue loading of rat ulna in vivo (Photomicrograph field width 560 μm.) (Figure adapted from Bentolila et al. by permission.)

Figure 5

Schematic showing the mutually dependent relationship between bone remodeling, microdamage context and intrinsic bone material properties (especially fracture toughness). Each of which must be considered in the context of global fracture risk.