Time-dependent biaxial mechanical behavior of the aortic heart valve leaflet

Abstract

Despite continued progress in the treatment of aortic valve (AV) disease, current treatments continue to be challenged to consistently restore AV function for extended durations. Improved approaches for AV repair and replacement rests upon our ability to more fully comprehend and simulate AV function. While the elastic behavior the AV leaflet (AVL) has been previously investigated, time-dependent behaviors under physiological biaxial loading states have yet to be quantified. In the current study, we performed strain rate, creep, and stress-relaxation experiments using porcine AVL under planar biaxial stretch and loaded to physiological levels (60 N/m equi-biaxial tension), with strain rates ranging from quasi-static to physiologic. The resulting stress-strain responses were found to be independent of strain rate, as was the observed low level of hysteresis ( approximately 17%). Stress relaxation and creep results indicated that while the AVL exhibited significant stress relaxation, it exhibited negligible creep over the 3h test duration. These results are all in accordance with our previous findings for the mitral valve anterior leaflet (MVAL) [Grashow, J.S., Sacks, M.S., Liao, J., Yoganathan, A.P., 2006a. Planar biaxial creep and stress relaxatin of the mitral valve anterior leaflet. Annals of Biomedical Engineering 34 (10), 1509-1518; Grashow, J.S., Yoganathan, A.P., Sacks, M.S., 2006b. Biaxial stress-stretch behavior of the mitral valve anterior leaflet at physiologic strain rates. Annals of Biomedical Engineering 34 (2), 315-325], and support our observations that valvular tissues are functionally anisotropic, quasi-elastic biological materials. These results appear to be unique to valvular tissues, and indicate an ability to withstand loading without time-dependent effects under physiologic loading conditions. Based on a recent study that suggested valvular collagen fibrils are not intrinsically viscoelastic [Liao, J., Yang, L., Grashow, J., Sacks, M.S., 2007. The relation between collagen fibril kinematics and mechanical properties in the mitral valve anterior leaflet. Journal of Biomechanical Engineering 129 (1), 78-87], we speculate that the mechanisms underlying this quasi-elastic behavior may be attributed to inter-fibrillar structures unique to valvular tissues. These mechanisms are an important functional aspect of native valvular tissues, and are likely critical to improve our understanding of valvular disease and help guide the development of valvular tissue engineering and surgical repair.

Figure 1

(a) Representative AV loading and unloading curves during 15 s, 1 s, 0.5 s, 0.1 s, and 0.05 s half cycle times. Results indicate consistent tension-stretch responses for all protocols and no observable stretch rate sensitivity. (b) To quantify test repeatability, the initial 1.0 s half cycle protocol was compared to an additional protocol performed after testing. High levels of repeatability indicate that the biaxial device capable of accurately controlling high strain rate tests while not causing tissue damage.

Figure 2

(a) Averaged AVL peak stretch behavior (n=8). Circumferential and radial peak stretch is significantly different while peak stretches at the 60 N/m equibiaxial tension state revealed no significant differences for any loading time (p = 0.821 and p = 0.486 for the circumferential and radial peak stretch respectively). These results support the observation that AVL tension is independent of the rate of stretch. (b) Similarly, the mitral valve anterior leaflet exhibited peak stretch rate independence.

Figure 3

Representative loading and unloading curves for the (a) AV and the (b) MVAL depicting minimal energy loss. Mean (c) AV and (d) MVAL energy storage and dissipation for all stretch rates. Hysteresis is defined as the area under tension-areal stretch curve. This definition was utilized as it represents the total tissue membrane strain energy in units of N/m. 0.05 s half cycle time is not presented due to unavoidable fluid currents during the unloading phase. AV hysteresis changes due to increased strain rate were not significantly different. Loading - p=0.342. Unloading - p=0.083. Change in energy - p=0.387

Figure 4

(a) Representative stress relaxation behavior of the AVL. (b) Percent relaxation at 3 hours for the AV (n=6) and MVAL biaxial stress relaxation behavior. The observed AV relaxation in the circumferential direction was statistically different from the radial relaxation response (p=0.007). The AVL exhibited comparable levels of relaxation in both the circumferential and radial directions to the MVAL that were not statically significant (circumferential: p=0.068. Radial: p=0.431)

Figure 5

(a) Representative AV planar biaxial creep behavior for the circumferential and radial directions over the 3 hour test. The highly anisotropic behavior of the AVL was clearly observable. (b) The mean stretch observed during creep tests (n=6), indicating that creep in both the circumferential and radial axes was negligible for all time points.

Figure 6

Ultrastructural interaction in fibrosa, spongiosa, and ventricularis layers revealed with TEM and Cuperomeronic Blue staining. The image shows proteoglycans, marked with solid dark arrows, interacting with ECM components such as collagen fibers. It is our hypothesis, that intricate interactions between collagen and other ECM components, such as proteoglycans, significantly contributes to the unique time dependent material properties exhibited by valvular tissues.