Linking collagen fiber architecture to tissue-level biaxial mechanical behaviors of porcine semilunar heart valve cusps

Abstract

The semilunar heart valves regulate the blood flow from the ventricles to the major arteries through the opening and closing of the scallop shaped cusps. These cusps are composed of collagen fibers that act as the primary loading-bearing component. The load-dependent collagen fiber architecture has been previously examined in the existing literature; however, these studies relied on chemical clearing and tissue modifications to observe the underlying changes in response to mechanical loads. In the present study, we address this gap in knowledge by quantifying the collagen fiber orientations and alignments of the aortic and pulmonary cusps through a multi-scale, non-destructive experimental approach. This opto-mechanical approach, which combines polarized spatial frequency domain imaging and biaxial mechanical testing, provides a greater field of view (10-25mm) and faster imaging time (45-50s) than other traditional collagen imaging techniques. The birefringent response of the collagen fibers was fit with a von Mises distribution, while the biaxial mechanical testing data was implemented into a modified full structural model for further analysis. Our results showed that the semilunar heart valve cusps are more extensible in the tissue's radial direction than the circumferential direction under all the varied biaxial testing protocols, together with greater material anisotropy among the pulmonary valve cusps compared to the aortic valve cusps. The collagen fibers were shown to reorient towards the direction of the greatest applied loading and incrementally realign with the increased applied stress. The collagen fiber architecture within the aortic valve cusps were found to be more homogeneous than the pulmonary valve counterparts, reflecting the differences in the physiological environments experienced by these two semilunar heart valves. Further, the von Mises distribution fitting highlighted the presence and contribution of two distinct fiber families for each of the two semilunar heart valves. The results from this work would provide valuable insight into connecting tissue-level mechanics to the underlying collagen fiber architecture-an essential information for the future development of high-fidelity aortic/pulmonary valve computational models.

Keywords: Aortic valve; Biaxial mechanical testing; Collagen fiber architecture; Collagen microstructural quantification; Pulmonary valve.