#behavioral reconstruction

Figure 4 (TOP). Visualization of microdamage in cancellous bone. Red represents microdamage and transparent white represents bone. Shown are two specimens from the same donor subjected to (A) No loading (Group 1) and (B) Fatigue loading in group 5 (Young’s modulus was reduced by 42%). (C) An enlarged view of a damage site in the cancellous bone is shown. 

Figure 5 (BOTTOM). Changes in mechanical properties with fatigue loading. (A) The proportion of creep strain to maximum strain is shown for the six specimens fatigue loaded to failure. Each color represents a different specimen. (B) The alterations in modulus and energy dissipation in one specimen fatigue loaded to failure is shown. Modulus reduction increased progressively throughout fatigue loading, with a rapid loss in stiffness close to failure. Energy dissipation remained relatively constant until in the tertiary phase, where it increased rapidly.

Microdamage Caused by Fatigue Loading in Human Cancellous Bone: Relationship to Reductions in Bone Biomechanical Performance (DOI: 10.1371/journal.pone.0083662.g001)

Floor M. Lambers, Amanda R. Bouman, Clare M. Rimnac, Christopher J. Hernandez

Abstract

Vertebral fractures associated with osteoporosis are often the result of tissue damage accumulated over time. Microscopic tissue damage (microdamage) generated in vivo is believed to be a mechanically relevant aspect of bone quality that may contribute to fracture risk. Although the presence of microdamage in bone tissue has been documented, the relationship between loading, microdamage accumulation and mechanical failure is not well understood. The aim of the current study was to determine how microdamage accumulates in human vertebral cancellous bone subjected to cyclic fatigue loading. Cancellous bone cores (n = 32) from the third lumbar vertebra of 16 donors (10 male, 6 female, age 7668.8, mean 6 SD) were subjected to compressive cyclic loading at s/E0 = 0.0035 (where s is stress and E0 is the initial Young’s modulus). Cyclic loading was suspended before failure at one of seven different amounts of loading and specimens were stained for microdamage using lead uranyl acetate. Damage volume fraction (DV/BV) varied from 0.860.5% (no loading) to 3.462.1% (fatigue-loaded to complete failure) and was linearly related to the reductions in Young’s modulus caused by fatigue loading (r2 = 0.60, p,0.01). The relationship between reductions in Young’s modulus and proportion of fatigue life was nonlinear and suggests that most microdamage generation occurs late in fatigue loading, during the tertiary phase. Our results indicate that human vertebral cancellous bone tissue with a DV/BV of 1.5% is expected to have, on average, a Young’s modulus 31% lower than the same tissue without microdamage and is able to withstand 92% fewer cycles before failure than the same tissue without microdamage. Hence, even small amounts of microscopic tissue damage in human vertebral cancellous bone may have large effects on subsequent biomechanical performance.

Highlights:

Microscopic tissue damage (microdamage) in the form of linear microcracks, diffuse damage, or trabecular microfracture occurs in vivo, shows a higher prevalence in older individuals, and is believed to be a biomechanically relevant aspect of bone quality."

"Cancellous bone tissue submitted to cyclic loading displays creep-fatigue behavior in three phases: a primary phase in which stiffness reduces relatively rapidly, a secondary phase in which stiffness declines slowly and a tertiary phase in which stiffness rapidly declines before failure."

"Six specimens were loaded to 5% strain, which we defined as failure (group 7). The value of 5% strain was defined as failure, because from preliminary tests it was found that loading to 5%strain would capture the primary, secondary, and tertiary phase."

"After mechanical testing, specimens were removed from the end-caps using a low-speed diamond saw (Isomet, Buehler Ltd., Lake Bluff, IL) and stained with lead uranyl acetate. Lead uranyl acetate binds to regions of bone tissue in which microdamage has formed and has high x-ray absorption, allowing visualization of microdamage with micro-computed tomography."

"The current study provides the first quantitative measures of stained microdamage accumulation during cyclic loading in human vertebral cancellous bone and shows that microdamage generated by cyclic loading is linearly related to reductions in specimen stiffness and non-linearly related to the proportion of fatigue life.

"Maximum strain was the single best predictor of DV/BV (tested using multivariate linear regressions), which is consistent with a strain-based failure criterion for cancellous bone, however, because creep strain and maximum strain were highly correlated it is not possible to conclude which was causative.

"Bone is a hierarchical structure with energy dissipation mechanisms at different length scales of bone [65]. To resist fracture, bone tissue can deform through fibrillar sliding or through the formation of microcracks, where larger microcracks dissipate greater amounts of energy. Our observation of a correlation between DV/BV and energy dissipation per cycle are consistent with the idea that microdamage contributes to energy dissipation in cancellous bone."

Take home message: 

"Our findings suggest that small amounts of microdamage in human vertebral cancellous bone cause reductions in fatigue life that are much greater than reductions in Young’s modulus. Therefore, even small amounts of stained microdamage may indicate large reductions in the number of loading cycles that the tissue can sustain before failure even when alterations in cancellous bone stiffness are small. Although the current study examined only the effects of microdamage generated by cyclic compressive loading, we expect our estimations of the effects of microdamage on subsequent biomechanical performance to be conservative because alterations in loading mode and mixed mode loading have been shown to be more effective at propagating microdamage."