Toughening mechanisms for the attachment of architectured materials: The mechanics of the tendon enthesis

Abstract

Architectured materials offer tailored mechanical properties but are limited in engineering applications due to challenges in maintaining toughness across their attachments. The enthesis connects tendon and bone, two vastly different architectured materials, and exhibits toughness across a wide range of loadings. Understanding the mechanisms by which this is achieved could inform the development of engineered attachments. Integrating experiments, simulations, and previously unexplored imaging that enabled simultaneous observation of mineralized and unmineralized tissues, we identified putative mechanisms of enthesis toughening in a mouse model and then manipulated these mechanisms via in vivo control of mineralization and architecture. Imaging uncovered a fibrous architecture within the enthesis that controls trade-offs between strength and toughness. In vivo models of pathology revealed architectural adaptations that optimize these trade-offs through cross-scale mechanisms including nanoscale protein denaturation, milliscale load-sharing, and macroscale energy absorption. Results suggest strategies for optimizing architecture for tough bimaterial attachments in medicine and engineering.

Enthesis strength, toughness and stiffness: an image-based model comparing tendon insertions with varying bony attachment geometries

“…Strength, stiffness and toughness decreased dramatically beyond a loading angle of 90°. The model reproduced many of the trends and variations in mechanical behaviour seen in tendon enthesis mechanical testing experiments [33] (electronic supplementary material, figure S1). Additional simulation results, using the range of parameters from table 1, are shown in electronic supplementary material, figure S2.…”

“…However, this alignment changes dramatically over the course of shoulder motion, with significant consequences for the strength of the attachment [11,14]. We recently applied mercury (II) chloride staining to enable simultaneous imaging of the fibrous and bony architecture of the supraspinatus enthesis in a murine supraspinatus tendon and found that the fibrous architecture, when incorporated into a model of interactions between the tendon and bone, could explain the direction-dependence of strength, stiffness, and toughness at the supraspinatus enthesis [33]. In that work, we studied the response of enthesis tendon fibres wrapped around a semicircular bone ridge, representative of the rotator cuff tendon enthesis.…”

A discrete shear lag model of the mechanics of hitchhiker plants, and its prospective application to tendon-to-bone repair

“…Tendon has a short toe region in which the stress-strain curve is nonlinear followed by an extensive linear elastic region [43,44]. Further nonlinearity is expected at loads sufficiently high to engage the many hierarchical toughening mechanisms in tendon [30][31][32][33]. Our focus was to study an intermediate range leading to the first stages of suture pullout, in which the tendon is strained beyond the toe region, but significant sliding of tendon fibres and fibrils has not yet begun.…”

“…Our own work on these suture 'locking' strategies [26][27][28][29] suggests that they are effective in increasing pullout strength, in part because they harness intrinsic load sharing methods that tendon fibres present over the course of failure [30][31][32][33]. However, the process of failure at a repair site begins before these mechanisms engaged.…”

Regulating Macrophages through Immunomodulatory Biomaterials Is a Promising Strategy for Promoting Tendon-Bone Healing

“…However, the cross-sectional areas gradually decreased, while fiber curvature increased [ 17 ]. The stress would peak, theoretically, at the tendon-to-bone interface as a result of observed fiber alignment, implying that there may be a unique mechanism to reduce stress concentration at the tendon-to-bone interface [ 17 , 18 ]. Using a customized confocal microscopy–mechanical loading system, Rossetti et al [ 2 ] found a transitional zone of 500 μm in the tendon-to-bone interface.…”