Toughening of fibrous scaffolds by mobile mineral deposits.

Partially mineralized fibrous tissue situated between tendon and bone is believed to be tougher than either tendon or bone, possibly serving as a compliant, energy absorptive, protective barrier between the two. This tissue does not reform following surgical repair (e.g., rotator cuff tendon-to-bone re-attachment) and might be a factor in the poor outcomes following such surgeries. Towards our long-term goal of tissue engineered solutions to functional tendon-to-bone re-attachment, we tested the hypotheses that partially mineralized fibrous matrices can derive toughness from mobility of mineral along their fibers, and that in such cases toughness is maximized at levels of mineralization sufficiently low to allow substantial mobility. Nanofibrous electrospun poly(lactic-co-glycolic acid) (PLGA) scaffolds mineralized for prescribed times were fabricated as model systems to test these hypotheses. Tensile tests performed at varying angles relative to the dominant fiber direction confirmed that mineral cross-linked PLGA nanofibers without adhering to them. Peel tests revealed that fracture toughness increased with mineralization time up to a peak value, then subsequently decreased with increasing mineralization time back to the baseline toughness of unmineralized scaffolds. These experimental results were predicted by a theoretical model combining mineral growth kinetics with fracture energetics, suggesting that toughness increased with mineralization time until mineral mobility was attenuated by steric hindrance, then returned to baseline levels following the rigid percolation threshold. Results supported our hypotheses, and motivate further study of the roles of mobile mineral particles in toughening the tendon-to-bone attachment.

STATEMENT OF SIGNIFICANCE: Effective surgical repair of interfaces between tendon and bone remains an unmet clinical need, in part due to a lack of understanding of how toughness is achieved in the healthy tissue. Using combined synthesis, experiment, and modeling approaches, the current work supported the hypothesis that toughening of a fibrous scaffold arises from brittle mineral particles that crosslink the fibers, but only if the particles are free to slide relative to the fibers. In the case of the tendon-to-bone interface, this suggests that partially mineralized tissue between tendon and bone, with mobile mineral but relatively low stiffness, may serve as a compliant, energy-absorbing barrier that guards against injury. These results suggest an opportunity for fabrication of tough and strong fibrous scaffolds for tissue engineering applications.