Ageing Changes in the Tensile Properties of Tendons: Influence of Collagen Fibril Volume Fraction

Connective tissues are biological composites comprising of collagen fibrils embedded in (and reinforcing) the hydrated proteoglycan-rich (PG) gel within the extracellular matrices (ECMs). Age-related changes to the mechanical properties of tissues are often associated with changes to the structure of the ECM, namely, fibril diameter. However, quantitative attempts to correlate fibril diameter to mechanical properties have yielded inconclusive evidence. Here, we described a novel approach that was based on the rule of mixtures for fiber composites to evaluate the dependence of age-related changes in tendon tensile strength $(σ)$ and stiffness $(E)$ on the collagen fibril cross-sectional area fraction $(ρ)$⁠, which is related to the fibril volume fraction. Tail tendons from C57BL6 mice from age groups $1.6–35.3months$ old were stretched to failure to determine $σ$ and $E$⁠. Parallel measurements of $ρ$ as a function of age were made using transmission electron microscopy. Mathematical models (rule of mixtures) of fibrils reinforcing a PG gel in tendons were used to investigate the influence of $ρ$ on ageing changes in $σ$ and $E$⁠. The magnitudes of $σ$⁠, $E$⁠, and $ρ$ increased rapidly from $1.6monthsto4.0months$ (⁠$P$-values $<0.05$⁠) before reaching a constant (age independent) from $4.0monthsto29.0months$ (⁠$P$-values $>0.05$⁠); this trend continued for $E$ and $ρ$ (⁠$P$-values $>0.05$⁠) from $29.0monthsto35.3months$⁠, but not for $σ$⁠, which decreased gradually (⁠$P$-values $<0.05$⁠). Linear regression analysis revealed that age-related changes in $σ$ and $E$ correlated positively to $ρ$ (⁠$P$-values $<0.05$⁠). Collagen fibril cross-sectional area fraction $ρ$ is a significant predictor of ageing changes in $σ$ and $E$ in the tail tendons of C57BL6 mice.