Kinematics of collagen fibers in carotid arteries under tension-inflation loading

Abstract

Biomechanics of the extracellular matrix in arteries determines their macroscopic mechanical behavior. In particular, the distribution of collagen fibers and bundles plays a significant role. Experimental data showed that in most arterial walls there are preferred fiber directions. However, the realignment of collagen fibers during tissue deformation is still controversial: whilst authors claim that fibers should undergo affine deformations, others showed the contrary. In order to have an insight about this important question of affine deformations at the microscopic scale, we measured the realignment of collagen fibers in the adventitia layer of carotid arteries using multiphoton microscopy combined with an unprecedented Fourier based method. We compared the realignment for two types of macroscopic loading applied on arterial segments: axial tension under constant pressure (scenario 1) and inflation under constant axial length (scenario 2). Results showed that, although the tissue underwent macroscopic stretches beyond 1.5 in the circumferential direction, fiber directions remained unchanged during scenario 2 loading. Conversely, fibers strongly realigned along the axis direction for scenario 1 loading. In both cases, the motion of collagen fibers did not satisfy affine deformations, with a significant difference between both cases: affine predictions strongly under-estimated fiber reorientations in uniaxial tension and over-estimated fiber reorientations during inflation at constant length. Finally, we explained this specific kinematics of collagen fibers by the complex tension-compression interactions between very stiff collagen fibers and compliant surrounding proteins. A tensegrity representation of the extracellular matrix in the adventitia taking into account these interactions was proposed to model the motion of collagen fibers during tissue deformation.

Quantification of the regional bioarchitecture in the human aorta

“…The wavelengths of the individual collagen fibrils observed in Krasny et al. (), which are two to three times the fibril thickness, 60 nm (Hansen et al. ), are not observed at the magnification used in this study, where the pixel resolution was 500 nm.…”

“…2C, where MATLAB (R2017b, Math-Works Inc., Natick, MA, USA) based von Mises mixture models is fit to the individual datasets to estimate the number of fibre families present based on the log-likelihood function (Hung et al 2012;Schymura, 2019). The wavelengths of the individual collagen fibrils observed in Krasny et al (2018), which are two to three times the fibril thickness, 60 nm (Hansen et al 2009), are not observed at the magnification used in this study, where the pixel resolution was 500 nm. Therefore, the individual fibril undulations did not affect the von Mises distributions measured.…”

Bone Ultrastructure as Composite of Aligned Mineralized Collagen Fibrils Embedded Into a Porous Polycrystalline Matrix: Confirmation by Computational Electrodynamics

“…At the same time, it is obvious that the deviations of model predictions from experiments beyond k z > 0.35 nm −1 may motivate additional investigations toward a more refined ultrastructural representation, and also the prediction of SAXS patterns emerging through bone under mechanical load, based on devices pioneered by Gupta et al [111,114] and Karunaratne et al [115], appears as an interesting topic for the future. At the same time, the current developments may also serve as a basis for a deeper investigation of configurational changes provoked by excessive mechanical loading of soft tissues, such changes having gained recent interest both experimentally [116,117], and computationally [118].…”

Non‐affine fiber kinematics in arterial mechanics: a continuum micromechanical investigation

“…While this concept frequently provided very satisfactory results, in particular so in the context of mitral valve leaflet modeling, we also note several experimental observations where the fibers do not follow such a deformation pattern. These observations concern the adventitia layer of carotid arteries, but also tissues beyond the cardiac realm, such as the human liver capsule and murine skin . Typically, the aforementioned deformation patterns are associated with large shear strains in the soft matrix being situated in‐between the fibers; and such discrepancies between macroscopic and microscopic strains, being incompatible with affine deformation characteristics, have also been reported for tendon fascicles .…”