Understanding the effects of damage on the failure behavior of trabecular bone is important for elucidating its role in osteoporosis and age related fragility. Microdamage accumulation has been associated with a degradation of material properties, but its role in fractures is not fully understood. As such, we sought to establish the relative effects of BMD, architecture, and damage on the toughness of trabecular bone. Because of the destructive nature of the tests, we did not directly measure microdamage, but instead used modulus reduction as a surrogate. The toughness of samples was dependent on the bone mineral density and on architectural parameters. In contrast, damage did not measurably affect the toughness to failure for on-axis loading, regardless of the magnitude of modulus reduction. Although the damaging loads decreased the modulus, strength, and elastic toughness, the overall toughness was primarily determined by the total strain to failure. This indicates that the normal variations in toughness due to density and architecture of trabecular bone are greater than the changes due to damage at the levels induced in this study. The effects of damage on toughness may be limited because formation of new damage dominates the propagation of existing microdamage in trabecular bone [12
There are several notable strengths of this study. First, it considered the effects of damage on toughness, rather than strength. Because toughness represents a material’s ability to absorb energy, the data provide better insight into the relative roles of the effects of damage and architecture on fractures due to falls, which are energy-limited. Second, the two strain levels were selected to induce damage to two levels to quantify the effects of damage and were based on reported data of trabecular bone yield and ultimate strains [13
]. These strain levels have been shown to produce damage levels consistent with in vivo damage in human bone [12
], and the presence of damage was verified by the decreases in modulus and elastic toughness. Finally, well-validated testing methods were used to ensure precision of measurements [25
There are also several limitations to our experimental protocol that should be considered when interpreting the data. First, the specimens were taken from a single anatomic site with limited architectural variability. Additionally, the bone was taken from young animals and may not represent the aging human skeleton. However, the use of this bone eliminated the confounding effects of pre-existing damage and heterogeneity of mineralization, which would be unavoidable in human bone. The toughness was measured at a strain to 7.5% rather than to overt fracture. Indeed, only two of the 30 specimens actually fractured at this strain level. Moreover, identifying the fracture point during testing or by analyzing the data was inconsistent. We also investigated the differences in toughness measured to the ultimate strain (data not shown) and found no difference between overload and failure curves in the high-damage group. The lack of direct histological measurements to quantify the microdamage is also a limitation. However, based on existing literature, the level of microdamage in both damage groups would be expected to be greater than in the control group, as young bovine bone has almost no in vivo microdamage [12
] while microdamage increases with increasing modulus reduction [13
]. Finally, this study focused on damage in excised trabecular bone specimens. However, it is also important to understand the role of microdamage on the failure behavior of the whole bone at any anatomical site. The surrounding trabecular network and the cortical shell will also play a role in whole bone fracture. This study provides data that could be incorporated into such whole bone studies.
Measuring toughness in trabecular bone is sensitive to the protocol used. Although the elastic toughness significantly decreased following overloading, the toughness measured to the ultimate strain did not. Decreases in the ultimate stress were accompanied by increases in ultimate strain, resulting in no overall change in toughness to the ultimate stress. This suggests that changes in trabecular bone toughness measurements occur primarily in the elastic and initial plastic ranges, prior to the ultimate strain. Given the relatively small effects of microdamage on toughness to the ultimate and higher strains, the role of microdamage in trabecular bone quality may primarily be in the elastic behavior and its affect on stress redistribution in the whole bone.
Architectural parameters can provide insight into the mechanisms of trabecular bone toughness, but the effects can be obscured by those of BV/TV, which is highly correlated to several relevant architectural parameters. We found that SMI and trabecular slenderness were the key architectural features to determine toughness. The sensitivity of the toughness to each parameter was quantified by substituting the mean values into the relationships and varying each parameter by one standard deviation. A one standard deviation increase in BV/TV and BMD resulted in a 31.0% and 27.4% increase in toughness, respectively. Toughness was similarly sensitive to changes in slenderness, with a one standard deviation decrease resulting in a 18.3% increase in toughness, while a decrease in SMI led to a 16.2% increase in toughness. In contrast, the decrease in elastic toughness due to damage averaged 34.2 ± 19.7% and 54.9 ± 12.7% for the low- and high-damage groups, respectively.
Together, SMI and slenderness ratio can be interpreted in the context of cellular solid modeling [30
]. Decreasing trabecular slenderness results in plastic yielding of the trabeculae rather than buckling [30
], and hence a greater energy absorption. Similarly, lower SMI indicates a transition to a network of plates, which are subject to buckling along a single axis whereas rods are less constrained. In large-deformation finite element analysis of human trabecular bone, such a transition from plates to rods was the primary factor mediating the failure mechanisms of trabecular bone [31
Mechanical damage, rather than microdamage, was used to differentiate between groups in this study. However, propagation of microcracks into trabecular fractures would be one expected mechanism of toughness degradation. As such, variability in microdamage levels within groups may have affected the outcome. Microdamage increases with increasing SMI, decreasing BV/TV, and decreasing Tb.Th in both mechanically damaged bovine trabecular bone [12
] and in human vertebral trabecular bone [32
]. These same variables affected the toughness in this study. However, even after correcting for these parameters, the effects of damage level were not detectable between groups. As such, accounting for the mechanical effects of microdamage using population-based studies may prove difficult, and highly controlled experimental designs are needed to reduce these effects.
The modulus reductions found in this study were lower than previous reports. Modulus reductions in bovine tibial trabecular bone compressed to 1.5% and 2.5% strain were 38.5% and 64.7%, respectively [11
], compared to 9.6% and 24.3% here and in previous studies from our lab [12
]. These differences are in part due to the method used to determine the modulus in this study [28
] compared to earlier work [11
]. Moduli measured from the initial slope of the stress strain curve are consistently higher than those measured using linear fits, and reflect the nonlinear elastic behavior of trabecular bone [28
]. When the secant modulus at the end of overloading was used, as in previous studies [11
], the modulus reductions were comparable.
The results complement a recent study where overloads did not significantly affect the strength or toughness of human vertebral trabecular bone in orthogonal loading directions [15
]. Similarly, we found that the ultimate strengths following damage were not significantly different between damage groups. Likewise, the damaged toughness measured to the ultimate strength was not significantly different between groups. However, in contrast to our results, these authors reported that on-axis toughness was correlated with Tb.N but not SMI, Tb.Th, or DA [15
]. This may be attributed to the larger range of architectural parameters in our specimens. For example, the variation in SMI in these samples was over two times larger than in the samples studied by Badiei [15
], which allows for stronger correlations. In addition, differences in tissue level behavior between aged human and young bovine trabecular bone may play a role.
In an in vivo study, treatment with raloxifene for 12 months increased the microdamage burden in dogs, indicated by a significantly higher mean crack length versus the control group. However, the toughness was unchanged or higher compared to controls in canine vertebral and femoral trabecular bone, respectively [34
]. These results are consistent with the present findings that density and architecture are the primary contributors to trabecular bone toughness.
Taken together, the data provide insight into the mechanisms of fracture risk reduction by anti-resorptive treatments. Although these agents are known to increase the microdamage burden [36
], they also increase bone mineral density [37
] and prevent degradation of architecture [36
]. For example, microdamage levels of 2.9 and 3.7 times that of controls were found in dogs treated with clinically relevant doses of risedronate and alendronate, respectively, which are similar to the effects reported in humans [44
]. After normalizing for volume fraction, there was no significant difference in toughness between the treatment and vehicle groups, although the alendronate group tended toward significant differences in toughness [35
]. In a more recent study, the energy to failure as a function of BMD was lower in alendronate treated dogs than in control or risedronate treated dogs [45
]. As such, toughness may begin to decline at higher microdamage burdens. Moreover, the affects may be different in osteoporotic bone due to degradation of architecture and density. As such, additional controlled studies are warranted.