No abstract
The biomechanical properties of arteries are conferred by the rearrangement under load of the collagen and elastin fibers making up the arterial microstructure. Their kinematics under deformation is not yet characterized for all fiber networks. In this respect we have submitted samples of arterial tissue to uniaxial tension, simultaneously to confocal imaging of their microstructure. Our method allowed identifying for the first time the remarkable ability of adventitial collagen fibers to reorient in the direction of the load, achieving reorientation rotations that exceeded those predicted by affine kinematics, while all other networks followed the affine kinematics. Our results highlight new properties of the microstructure, which might play a role in the outcomes of vascular pathologies like aneurysms.
There is growing experimental evidence for non-affine deformations occurring in different types of fibrous soft tissues; meaning that the fiber orientations do not follow the macroscopic deformation gradient. Suitable mathematical modeling of this phenomenon is an open challenge, which we here tackle in the framework of continuum micromechanics. From a rate-based analogon of Eshelby's inhomogeneity problem, we derive strain and spin concentration tensors relating macroscopic strain rate tensors applied to the boundaries of a Representative Volume Element (RVE), to strain rates and spins within the tissue microstructure, in particular those associated with fiber rotations due to external mechanical loading. After presenting suitable algorithms for integrating the resulting rate-type governing equations, a first relevance check of the novel modeling approach is undertaken, by comparison of model results to recent experiments performed on the adventitia layer of rabbit carotid tissue. K E Y W O R D S large fiber rotations, large strain continuum micromechanics, soft tissues, spin concentration tensorThis is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Different levels of spatiotemporal heterogeneity characterize the aneurysmal and healthy ascending aorta hemodynamics, reflecting on wall shear stress topological skeleton. Peculiar wall shear stress topological skeleton features are linked to local ascending thoracic aortic aneurysms stiffness. The topological shear variation index, a measure of wall shear stress luminal contraction/expansion action variation along the cardiac cycle, is an indicator of local aortic wall degradation, performing better than canonical wall shear stress-based descriptors of flow disturbances. Wall shear stress topological skeleton analysis, combined with Complex Networks theory, contributes to better determine whether arterial wall degeneration, in combination with hemodynamic insult, leads to aneurysmal progression/rupture.
Aortic dissection is the most common catastrophe of the thoracic aorta, with a very high rate of mortality. Type A dissection is often associated with an ascending thoracic aortic aneurysm (ATAA). However, it is widely acknowledged that the risk of type A dissection cannot be reliably predicted simply by measuring the ATAA diameter and there is a pressing need for more reliable risk predictors. It was previously shown that there is a significant correlation between a rupture criterion based on the ultimate stretch of the ATAA and the local extensional stiffness of the aorta. Therefore, reconstructing regional variations of the extensional stiffness across the aorta appears highly important. In this paper, we present a novel noninvasive inverse method to identify the patient-specific local extensional stiffness of aortic walls based on preoperative gated CT scans. Using these scans, a structural mesh is defined across the aorta with a set of nodes attached to the same material points at different time steps throughout the cardiac cycle. For each node, time variations of the position are analyzed using Fourier series, permitting the reconstruction of the local strain distribution (fundamental term). Relating these strains to tensions with the extensional stiffness, and writing the local equilibrium satisfied by the tensions, the local extensional stiffness is finally derived at every position. The methodology is applied onto the ascending and descending aorta of three patients. Interestingly, the regional distribution of identified stiffness properties appears heterogeneous across the ATAA. Averagely, the identified stiffness is also compared with values obtained using other nonlocal methodologies. The results support the possible noninvasive prediction of stretch-based rupture criteria in clinical practice using local stiffness reconstruction.
Purpose. It has been reported clinically that rupture or dissections in thoracic aortic aneurysms (TAA) often occur due to hypertension which may be modelled with sudden increase of peripheral resistance, inducing acute changes of blood volumes in the aorta. There is clinical evidence that more compliant aneurysms are less prone to rupture as they can sustain such changes of volume. The aim of the current paper is to verify this paradigm by evaluating computationally the role played by the variation of peripheral resistance and the impact of aortic stiffness onto peak wall stress in ascending TAA. Methods. Fluid-Structure Interaction (FSI) analyses were performed using patient-specific geometries and boundary conditions derived from 4D MRI datasets acquired on a patient. Blood was assumed incompressible and was treated as a non-Newtonian fluid using the Carreau model while the wall mechanical properties were obtained from the bulge inflation tests carried out in vitro after surgical repair. The Navier Stokes equations were solved in ANSYS Fluent. The Arbitrary Lagrangian Eulerian formulation was used to account for the wall deformations. At the interface between the solid domain and the fluid domain, the fluid pressure was transferred to the wall and the displacement of the wall was transferred to the fluid. The two systems were connected by the System Coupling component which controls the solver execution of fluid and solid simulations in ANSYS. Fluid and solid domains were solved sequentially starting from the fluid simulations. Results. Distributions of blood flow, wall shear stress and wall stress were evaluated in the ascending thoracic aorta using the FSI analyses. We always observed a significant flow eccentricity in the simulations, in very good agreement with velocity profiles measured using 4D MRI. The results also showed significant increase of peak wall stress due to the increase of peripheral resistance and aortic stiffness. In the worst case scenario, the largest peripheral resistance (10 10 kg.s.m -4 ) and stiffness (10 MPa) resulted in a maximal principal stress equal to 702 kPa, whereas it was only 77 kPa in normal conditions. Conclusions. This is the first time that the risk of rupture of an aTAA is quantified in case of the combined effects of hypertension and aortic stiffness increase. Our findings suggest that a stiffer TAA may have the most altered distribution of wall stress and an acute change of peripheral vascular resistance could significantly increase the risk of rupture for a stiffer aneurysm.
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.
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