Toughening of fibrous scaffolds by mobile mineral deposits

Publication date: Available online 19 May 2017
Source:Acta Biomaterialia
Author(s): Justin Lipner, John J. Boyle, Younan Xia, Victor Birman, Guy M. Genin, Stavros Thomopoulos
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 significanceThere remains an unmet clinical need to repair connections between compliant unmineralized tissues such as tendon and stiff mineralized tissues such as bone. The current work revealed a novel mechanism by which engineered scaffolds can be fabricated to address this need. Typical material systems that combine a compliant fibrous component with stiff brittle inclusions must compromise toughness for increased strength. However, mobile mineral in the current study was able to both toughen and strengthen a fibrous polymer scaffold at intermediate levels of mineralization. This mechanism was consistent with a multiscale model that combined nucleation kinetics with the energetics of fracture. These results reveal a significant opportunity for fabrication of tough and strong fibrous scaffolds for tissue engineering applications.

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