Bimodal collagen fibril diameter distributions direct age-related variations in tendon resilience and resistance to rupture

Abstract

Scaling relationships have been formulated to investigate the influence of collagen fibril diameter ( D) on age-related variations in the strain energy density of tendon. Transmission electron microscopy was used to quantify D in tail tendon from 1.7- to 35.3-mo-old (C57BL/6) male mice. Frequency histograms of D for all age groups were modeled as two normally distributed subpopulations with smaller ( DD1) and larger ( DD2) mean Ds, respectively. Both DD1 and DD2 increase from 1.6 to 4.0 mo but decrease thereafter. From tensile tests to rupture, two strain energy densities were calculated: 1) uE [from initial loading until the yield stress (σ Y)], which contributes primarily to tendon resilience, and 2) uF [from σ Y through the maximum stress (σ U) until rupture], which relates primarily to resistance of the tendons to rupture. As measured by the normalized strain energy densities uE/σ Y and uF/σ U, both the resilience and resistance to rupture increase with increasing age and peak at 23.0 and 4.0 mo, respectively, before decreasing thereafter. Multiple regression analysis reveals that increases in uE/σ Y (resilience energy) are associated with decreases in DD1 and increases in DD2, whereas uF/σ U (rupture energy) is associated with increases in DD1 alone. These findings support a model where age-related variations in tendon resilience and resistance to rupture can be directed by subtle changes in the bimodal distribution of Ds.