A mechanistic model on the role of “radially-running” collagen fibers on dissection properties of human ascending thoracic aorta

Abstract

Aortic dissection (AoD) is a common condition that often leads to life-threatening cardiovaular emergency. From a biomechanics viewpoint, AoD involves failure of load-bearing microstructural components of the aortic wall, mainly elastin and collagen fibers. Delamination strength of the aortic wall depends on the load-bearing capacity and local micro-architecture of these fibers, which may vary with age, disease and aortic location. Therefore, quantifying the role of fiber micro-architecture on the delamination strength of the aortic wall may lead to improved understanding of AoD. We present an experimentally-driven modeling paradigm towards this goal. Specifically, we utilize collagen fiber microarchitecture, obtained in a parallel study from multi-photon microopy, in a predictive mechanistic framework to characterize the delamination strength. We then validate our model against peel test experiments on human aortic strips and utilize the model to predict the delamination strength of separate aortic strips and compare with experimental findings. We observe that the number density and failure energy of the radially-running collagen fibers control the peel strength. Furthermore, our model suggests that the lower delamination strength previously found for the circumferential direction in human aorta is related to a lower number density of radially-running collagen fibers in that direction. Our model sets the stage for an expanded future study that could predict AoD propagation in patient-specific aortic geometries and better understand factors that may influence propensity for occurrence.

Failure of the Porcine Ascending Aorta: Multidirectional Experiments and a Unifying Microstructural Model

“…As already noted, the work of Pal et al [61] provides a different and intriguing view of interlamellar failure by tearing versus pull-out effects. Additionally, our current model used collagen orientation tensor with eigenvalues of 0.9 and 1.0, corresponding roughly to collagen aligned within 18 deg of the circumferential axis (sin 2 (18 deg) ¼ 0.1).…”

“…Sommer et al [26] suggested that the anisotropic behavior may be a protective mechanism since dissection in the axial direction is often associated with failure across elastic laminae, whereas dissection in the circumferential direction typically propagates between adjacent laminae. Pal et al [61] suggested based on histology of peeled samples that the anisotropy may be due to stitching of the fibers, with failure in circumferential peeling occurring via a pull-out mechanism, whereas failure in axial peeling occurs via a tearing mechanism. This interesting conceptual description cannot be captured in our current model but clearly merits further investigation.…”

“…This approach was successful in matching a wide range of tissue mechanical tests, including one-radial extension to failure-that was not used during the fitting process, and it has the potential to be extended to the more disorganized (and thus more complex) architecture of the aneurysm, especially as better imaging and image-based modeling methods emerge [67,68]. The work of Pal et al [61] represents an excellent example of this approach, developing a theoretical model of peel failure based on known structure. Pal's approach could be extended to a more general stress field using a strategy similar to ours.…”

Structure-based constitutive model can accurately predict planar biaxial properties of aortic wall tissue

“…Out-of-plane fiber components would only be important for the radial wall properties, e.g. to investigate wall dissection [58].…”

“…Although phenomenological approaches [17][18][19][20] may reflect the biomechanical properties of the vascular wall, their material parameters lack physical interpretation, and these models are unreliable for predictions beyond the strain range used in parameter estimation. In contrast, histomechanical constitutive models [12,[21][22][23][24][25]58], i.e. structurally motivated mathematical descriptions of the tissue biomechanical properties, are supposed to overcome this drawback.…”