Wall Mechanical Properties and Hemodynamics of Unruptured Intracranial Aneurysms

Abstract

Background and purpose: Aneurysm progression and rupture is thought to be governed by progressive degradation and weakening of the wall in response to abnormal hemodynamics. Our goal was to investigate the relationship between the intra-aneurysmal hemodynamic conditions and wall mechanical properties in human aneurysms.

Materials and methods: A total of 8 unruptured aneurysms were analyzed. Computational fluid dynamics models were constructed from preoperative 3D rotational angiography images. The aneurysms were clipped, and the domes were resected and mechanically tested to failure with a uniaxial testing system under multiphoton microscopy. Linear regression analysis was performed to explore possible correlations between hemodynamic quantities and the failure characteristics and stiffness of the wall.

Results: The ultimate strain was correlated negatively to aneurysm inflow rate (P = .021), mean velocity (P = .025), and mean wall shear stress (P = .039). It was also correlated negatively to inflow concentration, oscillatory shear index, and measures of the complexity and instability of the flow; however, these trends did not reach statistical significance. The wall stiffness at high strains was correlated positively to inflow rate (P = .014), mean velocity (P = .008), inflow concentration (P = .04), flow instability (P = .006), flow complexity (P = .019), wall shear stress (P = .002), and oscillatory shear index (P = .004).

Conclusions: In a study of 8 unruptured intracranial aneurysms, ultimate strain was correlated negatively with aneurysm inflow rate, mean velocity, and mean wall shear stress. Wall stiffness was correlated positively with aneurysm inflow rate, mean velocity, wall shear stress, flow complexity and stability, and oscillatory shear index. These trends and the impact of hemodynamics on wall structure and mechanical properties should be investigated further in larger studies.

Fig 1.

Bottom, Stress-strain relationships. Examples of an aneurysm with stiff walls and low ultimate strain and stress (CA15) and an aneurysm with softer walls and greater ultimate stress and ultimate strain (CA26) are highlighted in red and green, respectively. Top, Picture of a sample with grips before stretching (left) and after it fails (right). Note that the tear occurs near the middle of the sample, not at the grips.

Fig 2.

Relationships between hemodynamic variables and ultimate wall strain. Each correlation that reached statistical significance (95% confidence) is marked with an asterisk. In the top-left panel, aneurysms CA26 and CA15, exemplified in Figs 4 and 5, are marked with green and red circles, respectively. corelen indicates vortex core-line length; ICI, inflow concentration index; LSA, area under low wall shear stress relative to the parent vasculature; OSI, mean oscillatory shear index; podent, POD entropy; Q, aneurysm inflow rate; SCI, shear concentration index (a measure of concentration of the wall shear stress distribution); VE, aneurysm mean velocity; WSS, mean wall shear stress.

Fig 3.

Relationships between hemodynamic variables and wall stiffness at high stress. Each correlation that reached statistical significance (95% confidence) is marked with an asterisk. In the top-left panel, aneurysms CA26 and CA15, exemplified in Figs 4 and 5, are marked with green and red circles, respectively. Corelen indicates vortex core-line length; ICI, inflow concentration index; LSA, area under low wall shear stress relative to the parent vasculature; OSImean, mean oscillatory shear index; podent, POD entropy; Q, aneurysm inflow rate; SCI, shear concentration index; VE, aneurysm mean velocity; WSSmean, mean wall shear stress.

Fig 4.

Flow and collagen fibers in 2 example aneurysms. Aneurysm CA26 (top) corresponds to the green circles in Figs 2 and 3 and the green curve in Fig 1, and aneurysm CA15 (bottom) corresponds to the red circles in Figs 2 and 3 and the red curve in Fig 1.

Fig 5.

Abluminal view of collagen fiber recruitment during uniaxial loading of aneurysm sample CA26 (green in Figs 1–3) obtained by using the uniaxial MPM system. The images were obtained at stretches of 1.0 (A), 1.15 (B), 1.3 (C), and 1.4 (D) and were formed from a projection of stacks over an approximately 95-μm depth of tissue. E–H, Histograms of fiber-orientation distribution of the MPM images at stretches of 1.0, 1.15, 1.3, and 1.4, respectively. The horizontal direction on the image is 0°, and the vertical direction is 90° (as shown in A).