Disorder protects collagen networks from fracture

TL;DR

This study reveals that structural disorder in collagen networks enhances their resistance to fracture, with network connectivity and hierarchical structure playing key roles in tissue strength.

Contribution

It demonstrates that disorder in collagen networks acts as a protective mechanism against fracture, a novel insight into tissue biomechanics.

Findings

Lower connectivity increases fracture strain.

Hierarchical structure provides structural plasticity.

Disorder enhances tissue resistance to fracture.

Abstract

Collagen forms the structural scaffold of connective tissues in all mammals. Tissues are remarkably resistant against mechanical deformations because collagen molecules hierarchically self-assemble in fibrous networks that stiffen with increasing strain. Nevertheless, collagen networks do fracture when tissues are overloaded or subject to pathological conditions such as aneurysms. Prior studies of the role of collagen in tissue fracture have mainly focused on tendons, which contain highly aligned bundles of collagen. By contrast, little is known about fracture of the orientationally more disordered collagen networks present in many other tissues such as skin and cartilage. Here, we combine shear rheology of reconstituted collagen networks with computer simulations to investigate the primary determinants of fracture in disordered collagen networks. We show that the fracture strain is controlled by the coordination number of the network junctions, with less connected networks fracturing at larger strains. The hierarchical structure of collagen fine-tunes the fracture strain by providing structural plasticity at the network and fiber level. Our findings imply that structural disorder provides a protective mechanism against network fracture that can optimize the strength of biological tissues.