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Research Papers

J Biomech Eng. 2018;140(5):051001-051001-18. doi:10.1115/1.4038779.

Simulations of soft tissues require accurate and robust constitutive models, whose form is derived from carefully designed experimental studies. For such investigations of membranes or thin specimens, planar biaxial systems have been used extensively. Yet, all such systems remain limited in their ability to: (1) fully prescribe in-plane deformation gradient tensor F2D, (2) ensure homogeneity of the applied deformation, and (3) be able to accommodate sufficiently small specimens to ensure a reasonable degree of material homogeneity. To address these issues, we have developed a novel planar biaxial testing device that overcomes these difficulties and is capable of full control of the in-plane deformation gradient tensor F2D and of testing specimens as small as ∼4 mm × ∼4 mm. Individual actuation of the specimen attachment points, combined with a robust real-time feedback control, enabled the device to enforce any arbitrary F2D with a high degree of accuracy and homogeneity. Results from extensive device validation trials and example tissues illustrated the ability of the device to perform as designed and gather data needed for developing and validating constitutive models. Examples included the murine aortic tissues, allowing for investigators to take advantage of the genetic manipulation of murine disease models. These capabilities highlight the potential of the device to serve as a platform for informing and verifying the results of inverse models and for conducting robust, controlled investigation into the biomechanics of very local behaviors of soft tissues and membrane biomaterials.

Commentary by Dr. Valentin Fuster
J Biomech Eng. 2018;140(5):051002-051002-8. doi:10.1115/1.4038745.

Rotator cuff disorders are one of the most common causes of shoulder pain and disability in the aging population but, unfortunately, the etiology is still unknown. One factor thought to contribute to the progression of disease is the external compression of the rotator cuff tendons, which can be significantly increased by age-related changes such as muscle weakness and poor posture. The objective of this study was to investigate the baseline compressive response of tendon and determine how this response is altered during maturation and aging. We did this by characterizing the compressive mechanical, viscoelastic, and poroelastic properties of young, mature, and aged mouse supraspinatus tendons using macroscale indentation testing and nanoscale high-frequency AFM-based rheology testing. Using these multiscale techniques, we found that aged tendons were stiffer than their mature counterparts and that both young and aged tendons exhibited increased hydraulic permeability and energy dissipation. We hypothesize that regional and age-related variations in collagen morphology and organization are likely responsible for changes in the multiscale compressive response as these structural parameters may affect fluid flow. Importantly, these results suggest a role for age-related changes in the progression of tendon degeneration, and we hypothesize that decreased ability to resist compressive loading via fluid pressurization may result in damage to the extracellular matrix (ECM) and ultimately tendon degeneration. These studies provide insight into the regional multiscale compressive response of tendons and indicate that altered compressive properties in aging tendons may be a major contributor to overall tendon degeneration.

Commentary by Dr. Valentin Fuster
J Biomech Eng. 2018;140(5):051003-051003-13. doi:10.1115/1.4037947.

Microstructural properties of extracellular matrix (ECM) promote cell and tissue homeostasis as well as contribute to the formation and progression of disease. In order to understand how microstructural properties influence the mechanical properties and traction force-induced remodeling of ECM, we developed an agent-based model that incorporates repetitively applied traction force within a discrete fiber network. An important difference between our model and similar finite element models is that by implementing more biologically realistic dynamic traction, we can explore a greater range of matrix remodeling. Here, we validated our model by reproducing qualitative trends observed in three sets of experimental data reported by others: tensile and shear testing of cell-free collagen gels, collagen remodeling around a single isolated cell, and collagen remodeling between pairs of cells. In response to tensile and shear strain, simulated acellular networks with straight fibrils exhibited biphasic stress–strain curves indicative of strain-stiffening. When fibril curvature was introduced, stress–strain curves shifted to the right, delaying the onset of strain-stiffening. Our data support the notion that strain-stiffening might occur as individual fibrils successively align along the axis of strain and become engaged in tension. In simulations with a single, contractile cell, peak collagen displacement occurred closest to the cell and decreased with increasing distance. In simulations with two cells, compaction of collagen between cells appeared inversely related to the initial distance between cells. These results for cell-populated collagen networks match in vitro findings. A demonstrable benefit of modeling is that it allows for further analysis not feasible with experimentation. Within two-cell simulations, strain energy within the collagen network measured from the final state was relatively uniform around the outer surface of cells separated by 250 μm, but became increasingly nonuniform as the distance between cells decreased. For cells separated by 75 and 100 μm, strain energy peaked in the direction toward the other cell in the region in which fibrils become highly aligned and reached a minimum adjacent to this region, not on the opposite side of the cell as might be expected. This pattern of strain energy was partly attributable to the pattern of collagen compaction, but was still present when mapping strain energy divided by collagen density. Findings like these are of interest because fibril alignment, density, and strain energy may each contribute to contact guidance during tissue morphogenesis.

Commentary by Dr. Valentin Fuster

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