Transition from viscous to elastic-based dependency of mechanical properties of self-assembled type I collagen fibers

Fibrous collagen networks are the major elements that provide mechanical integrity to tissues; they are composed of fiber forming collagens in combination with proteoglycans and elastic fibers. Using uniaxial incremental tensile stress-strain tests we have studied the viscoelastic mechanical properties of self-assembled collagen fibers formed at pHs between 5.5 and 8.5 and temperatures of 25 and 37°C. Fibers formed at pH 7.5 and 37°C and crosslinked by aging at 22°C and 1 atmosphere pressure were also tested. Analysis of the mechanical tests showed that the ultimate tensile strength (UTS), and slopes of the total, elastic and viscous stress-strain curves were related directly to the volume fraction of polymer. Further analysis suggested that the UTS, and slopes of the total, elastic, and viscous stress-strain curves showed the highest correlation coefficient with the calculated effective fibril length and axial ratio. The mechanical data suggested that at low levels of crosslinking the mechanical properties were dominated by the viscous sliding of collagen molecules and fibrils by each other, which appears to be dependent on the collagen fibril length and axial ratio, while at higher levels of crosslinking the mechanical behavior is dominated by elastic stretching of the nonhelical ends, crosslinks, and collagen triple helix. The latter behavior appears to be dependent on the presence of crosslinks that stabilize fibrillar units. These results lead to the hypothesis that early in development viscous sliding of fibrils plays an important role in the mechanical response of animal tissues to forces experienced in utero, while later in development when locomotion is required, mechanical stability is primarily a result of elastic deformation of the different parts of the collagen molecule within crosslinked fibrils.