In vivo microdamage is an indicator of susceptibility to initiation and propagation of microdamage in human femoral trabecular bone

Abstract

Microdamage has been cited as an important element of trabecular bone quality and fracture risk, as materials with flaws have lower modulus and strength than equivalent undamaged materials. However, the magnitude of the effect of damage on failure properties depends on its tendency to propagate. Human femoral trabecular bone from the neck and greater trochanter was subjected to one of compressive, torsional, or combined compression and torsion. The in vivo, new, and propagating damage were then quantified in thick sections under epifluorescent microscopy. Multiaxial loading, which was intended to represent an off-axis load such as a fall or accident, caused much more damage than either simple compression or shear, and similarly caused the greatest stiffness loss. In all cases, initiation of new damage far exceeded the propagation of existing damage. This may reflect stress redistribution away from damaged trabeculae, resulting in new damage sites. However, the accumulation of new damage was positively correlated with the quantity of pre-existing damage in all loading modes, indicating that damaged bone is inherently more prone to further damage formation. Moreover, about 50% of in vivo microcracks propagated under each type of loading. Finally, damage formation was positively correlated to decreased compressive stiffness following both axial and shear loading. Taken together, these results demonstrate that damage in trabecular bone adversely affects its mechanical properties, and is indicative of bone that is more susceptible to further damage.

Quantitative relationships between microdamage and cancellous bone strength and stiffness

“…Compared to the study by Keaveny et al the reductions in Young’s modulus caused by the initial load in the current study are smaller (2.9–75.2% here v. 5.1–91.0% by Keaveny et al), while estimated changes in ultimate strength in the current study are larger (15.9–84.0% here v. 3.6–63.8%). Our study suggests that an applied strain of 2% would, on average, result in a reduction in Young’s modulus of 30%, which is more than double that reported in similar experiments using dense cancellous bone (12% on average in bovine cancellous bone [15] and human femoral cancellous bone [27]) and less than half that expected from regression models derived using human vertebral cancellous bone (70% on average [22]). The previous study in vertebral cancellous bone [22], however, used a definition of percent reduction in Young’s modulus based on a different portion of the reload curve explaining the larger percent reduction reported.…”

“…Different loading modes (compression, tension, shear) have been associated with different amounts of microdamage and reductions in mechanical performance in subsequent loading. For example, mixed mode loading (compression + shear) has been shown to cause greater reductions in stiffness and larger amounts of microdamage than a single loading mode [27] and microdamage has been shown to be more likely to propagate when the loading mode is changed [15]. Because compression loading was used for both the initial load and the reload it is likely that the effects of microdamage on subsequent biomechanical performance observed in the current study may be smaller than that expected in vivo where loading is expected to be more variable and include mixed loading modes.…”

“…In contrast, smaller amounts of stained microdamage (Cr.Dn < 1.0/mm 2 , DV/BV < 1.0%) appear to be independent of reductions in mechanical performance. Large variability in microdamage measurement (SD/Mean > 0.50) is common in two dimensional assessment of cancellous bone loaded in vitro [14–16, 18, 27, 32, 36] as well as when using three-dimensional techniques [21, 29], suggesting that the two-dimensional measurement technique is not the primary cause of variability. Microdamage in cancellous bone tends to occur in localized bands [18] and some have isolated measurement of microdamage to regions of cancellous bone with the lowest bone volume fraction where a majority of deflection and microdamage occurs during loading [21, 37].…”

“…The continuum mechanics approach describes reductions in subsequent mechanical performance, but does not provide information about stained microdamage. We are aware of only one study that has combined the stained microdamage and continuum mechanics approach in specimens of cancellous bone (human femoral bone), which found relationships between the sum of pre-existing microdamage and microdamage caused by a single overload in vitro and reductions in Young’s modulus upon reloading [27]. Studies of microdamage generated by fatigue loading also suggest that the relationship between microdamage and reductions in Young’s modulus are not observed until a sufficiently large range in microdamage is present [19, 28, 29].…”

Alterations in trabecular bone microarchitecture in the ovine spine and distal femur following ovariectomy

“…Notably, changes in SMI, Tb.Th., and Tb.Sp. were found that, in combination with decreased BV/TV, are known to contribute to decreased mechanical integrity of bone (Mittra et al 2005; Teo 2006; Garrison et al 2009; Wegrzyn et al 2010; Wu 2013). Similar changes were observed in animals followed for two years after ovariectomy, suggesting that architectural degradation occurs within the first year, but does not progress.…”