Why are soft collagenous tissues so tough?

Bovine pericardium is the tissue of choice for replacing heart valves of human patients in minimally invasive surgery. The tissue has an extraordinarily high toughness of ~100 kilojoules per square meter. Here, we investigate the origin of the toughness through mechanical tests and microscopic observations. In the tissue, crimped, long, strong collagen fibers are embedded in a soft matrix. As a crack grows in the matrix, the fibers decrimp, reorient, slip, and bridge the crack. These microscopic processes enable the fibers to transmit high tension over a long distance. Using two types of experiments, we measure the bridging traction as a function of crack separation, σ(δ). The peak traction is σ(0) ~ 60 megapascals. The maximum separation is δ(0) ~ 6 millimeters, two to four orders of magnitude higher than that of hard tissues. Both the high traction and large separation of the bovine pericardium contribute to its high toughness.