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Theses Doctoral

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

Golman, Mikhail

Use of load-bearing materials whose functionality arises from architectured microstructures, so called architectured materials, has been hindered by the challenge of connecting them. A solution in nature is found at the tendon enthesis, a tissue that connects tendon and bone, two vastly different natural architectured materials. The tendon enthesis provides stability and allows for mobility of a joint though effective transfer of muscle forces from tendon to bone, while exhibiting toughness across a wide range of loadings. Unfortunately, many painful and physically debilitating conditions occur at or near this interface when the enthesis architecture is compromised due to injury or degeneration. Surgical and natural repairs do not reconstitute the natural toughening mechanisms of the enthesis and often fail. Hence, understanding the architectural mechanisms by which healthy and pathologic tendon entheses achieve strength and toughness would inform the development of both biological and engineered attachments.Integrating biomechanical analyses, failure characterizations, numerical simulations, and novel imaging, this thesis presents architectural mechanisms of enthesis toughening in a mouse model.

Imaging uncovered fibrous architecture within the enthesis, which controlled trade-offs between strength and toughness. Ex vivo enthesis failure modes exhibited nanoscale differences in damage, milliscale differences in fiber load-sharing, and macroscale differences in energy absorption that depended on structure, composition, and the nature of loading. The elastic and failure responses of the tendon enthesis also varied with the direction of loading. This variation was due to the fibrous nature of the tendon enthesis, with a clear role for bony anatomy and fiber recruitment in enthesis toughening behavior.

In vivo, , the loss of toughening mechanisms at the enthesis due to pathologic loading was evaluated by either increased (i.e., overuse) loading via downhill treadmill running or decreased (i.e., underuse) loading via botulinum toxin A induced paralysis. These loading environments led to changes in the mineralization and architecture at the tendon enthesis. These micro-architectural adaptations compromised the trade-offs between strength and toughness; overuse loading prompted active reinforcement and stiffening of the underlying trabeculae, leading a maintenance of strength and a compromise in overall toughness, whereas underloading prompted active resorption of the underlying trabecular architecture, leading to a compromise in both strength and toughness.

The mouse models of the tendon enthesis failure revealed a correlation between tendon enthesis architecture and injury prevention (i.e., toughening) mechanisms. To test this concept in a clinical setting, an injury classification system was developed for patellar tendinopathy and partial patellar tendon tears. This classification system identified the stages of tear progression and prognosis by tracking changes to patellar tendon architecture. Results revealed a relationship between patellar tendon thickness and likelihood of improvement with nonoperative treatment.

Taken together, this dissertation revealed how fibrous architecture can be tailored to toughen attachments between vastly different materials. This understanding can have prognostic value: tracking changes to enthesis architecture can be used as a tool for identifying candidates for various treatment options, as we showed for the patellar tendon clinical example. Furthermore, the toughening mechanisms identified here provide guidance for enhancing enthesis surgical repair and designing enthesis tissue engineered scaffolds, as well as motivating biomimetic approaches for attachment of architectured engineering material systems.

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More About This Work

Academic Units
Biomedical Engineering
Thesis Advisors
Thomopoulos, Stavros
Guo, X. Edward
Degree
Ph.D., Columbia University
Published Here
June 14, 2021