Increased tissue-level storage modulus and hardness with age in male cortical bone and its association with decreased fracture toughness

Abstract

The incidence of bone fracture increases with age, due to both declining bone quantity and quality. Toward the goal of an improved understanding of the causes of the age-related decline in the fracture toughness of male cortical bone, nanoindentation experiments were performed on femoral diaphysis specimens from men aged 21-98 years. Because aged bone has less matrix-bound water and dry bone is less viscoelastic, we used a nanoindentation method that is sensitive to changes in viscoelasticity. Given the anisotropy of bone stiffness, longitudinal (n = 26) and transverse (n = 25) specimens relative to the long axis of the femur diaphysis were tested both dry in air and immersed in phosphate buffered saline solution. Indentation stiffness (storage modulus) and hardness increased with age, while viscoelasticity (loss modulus) was independent of donor age. The increases in indentation stiffness and hardness with age were best explained by increased mineralization with age. Indentation stiffness and hardness were negatively correlated with previously acquired fracture toughness parameters, which is consistent with a tradeoff between material strength and toughness. In keeping with the complex structure of bone, a combination of tissue-level storage modulus or hardness, bound water, and osteonal area in regression models best explained the variance in the fracture toughness of male human cortical bone. On the other hand, viscoelasticity was unchanged with age and was not associated with fracture toughness. In conclusion, the age-related increase in stiffness and hardness of male cortical bone may be one of the multiple tissue-level characteristics that contributes to decreased fracture toughness.

Keywords: Aging; Bone; Cortical; Fracture; Mineralization; Nanoindentation.

Figure 1:

Examples of osteonal and interstitial indents for the longitudinal (a) and transverse (b) specimens.

Figure 2:

Effect of age group on E′ and H data. Significant age group differences are indicated by the comparison lines located above the boxes. Wet vs. dry and longitudinal vs. transverse comparison lines are not shown, since in each instance dry > wet and transverse > longitudinal (Table 3).

Figure 3:

Scatterplots of E′ and H vs. ge in the wet hydration condition. The legend contains information on the aging trend, as determined by the iteratively reweighted least squares (IRLS) best fit line shown in each plot. Both E′ and H increased with age, and the relative magnitude of the aging trend was the same for the longitudinal and transverse sections.

Figure 4:

Scatterplots of E′ vs. tissue mineral density (TMD), with I LS best fit lines. As seen in the correlation information in the legends, E′ and TMD were positively correlated for each of the 4 section–condition combinations (p ≤ 0.065).