A computational model for understanding the micro-mechanics of collagen fiber network in the tunica adventitia

Abdominal aortic aneurysm is a prevalent cardiovascular disease with high mortality rates. The mechanical response of the arterial wall relies on the organizational and structural behavior of its microstructural components, and thus, a detailed understanding of the microscopic mechanical response of the arterial wall layers at loads ranging up to rupture is necessary to improve diagnostic techniques and possibly treatments. Following the common notion that adventitia is the ultimate barrier at loads close to rupture, in the present study, a finite element model of adventitial collagen network was developed to study the mechanical state at the fiber level under uniaxial loading. Image stacks of the rabbit carotid adventitial tissue at rest and under uniaxial tension obtained using multi-photon microscopy were used in this study, as well as the force-displacement curves obtained from previously published experiments. Morphological parameters like fiber orientation distribution, waviness, and volume fraction were extracted for one sample from the confocal image stacks. An inverse random sampling approach combined with a random walk algorithm was employed to reconstruct the collagen network for numerical simulation. The model was then verified using experimental stress-stretch curves. The model shows the remarkable capacity of collagen fibers to uncrimp and reorient in the loading direction. These results further show that at high stretches, collagen network behaves in a highly non-affine manner, which was quantified for each sample. A comprehensive parameter study to understand the relationship between structural parameters and their influence on mechanical behavior is presented. Through this study, the model was used to conclude important structure-function relationships that control the mechanical response. Our results also show that at loads close to rupture, the probability of failure occurring at the fiber level is up to 2%. Uncertainties in usually employed rupture risk indicators and the stochastic nature of the event of rupture combined with limited knowledge on the microscopic determinants motivate the development of such an analysis. Moreover, this study will advance the study of coupling microscopic mechanisms to rupture of the artery as a whole.