Hemodynamic Changes Caused by Multiple Stenting in Vertebral Artery Fusiform Aneurysms: A Patient-Specific Computational Fluid Dynamics Study

Discussion

Intracranial fusiform aneurysms are dilations of the parent artery without a clear aneurysmal neck. Similar to the widespread application of intracranial stent placement, endovascular treatment of fusiform aneurysms has been an important method and has greatly improved the long-term prognosis.⁸ This effect was even more significant when multiple overlapping stents were used.^9,10 Although flow-diverter stents have been demonstrated to be an efficient treatment for aneurysms, their safety in posterior fusiform aneurysms still needs to be established by more evidence, especially because some important branches of smaller arteries might become covered.¹¹ Therefore, stepwise overlapping stent placement is still a safe and feasible choice when dealing with posterior fusiform aneurysms.

In saccular aneurysm studies, both in vivo and in silico experiments have demonstrated that multiple stent implantations can reduce injective blood flow and create a hemodynamic environment, which will promote thrombus formation and finally cure the aneurysm.¹² However, few hemodynamic studies have focused on intracranial fusiform aneurysms, in which hemodynamic patterns are different from those of saccular lesions. The application of the CFD technique makes hemodynamic studies in aneurysms more feasible and measurable. The fast virtual stent technique, first introduced by Larrabide et al,⁷ provides an accurate and efficient method to consider the behavior of stents in patient-specific aneurysm models. Being different from previous finite element analysis and porous medium methods, the fast virtual stent method shows a high consistency with real stents and an impressive efficiency.^5,13 On the basis of this technique, we simulated the Enterprise stent and investigated the performance of different stent-placement strategies in 10 patient-specific VAFA models, aiming to obtain more evidence for clinical decision-making.

Thrombus formation in the aneurysm sac and consequent reconstruction of the parent artery are the primary goals of stent placement in fusiform aneurysms. The stents should increase the time of blood flow staying in the aneurysm to create an environment for thrombosis, to achieve these goals.¹⁴ RRT is an important parameter that reflects the disturbed blood flow and its prolonged residence time in the aneurysmal sac. Tanemura et al⁶ demonstrated that a single Enterprise stent could increase the RRT by 20% in a previous CFD study. Our study further demonstrated that the RRT gradually increases by sequential stent placements, which would likely provide a better environment for thrombus formation.

WSS is the most studied hemodynamic parameter that has been demonstrated to play an important role in aneurysm initiation, rupture, and recanalization.¹⁵ Previous studies on saccular aneurysms suggested that stent implantation can lead to reduction of WSS and that this effect is related to the stent porosity—the lower the stent porosity, the more significantly the WSS decreased, and the distribution of WSS of the aneurysm became more uniform.¹⁶ In our study, progressive reduction of WSS was observed in VAFAs as the number of stents increased, which was similar to that in saccular aneurysms. However, lower WSS might also increase the risk of aneurysmal growth and even rupture, which has been shown in our previous CFD studies in saccular lesions. We therefore deduce that if thrombosis does not occur in a relatively short time, the aneurysms would be at risk of deterioration.

Another concern is the observed elevation of the pressure in every case and even for only a single stent. In a hemodynamic study of flow diverters by Cebral et al,¹⁷ a significant increase in pressure in some cases was observed after flow-diverter implantation, which, as those authors wrote, might lead to aneurysm rupture. However, some researchers had reported controversial results of a pressure decrease through virtual stent implantation in a fusiform aneurysm.¹⁸ These findings indicate that the modification of pressure may be related to patient-specific characteristics, which, in turn, might be related to the morphologic differences of aneurysms and stents. The average elevation of pressure in this study was 28.2%. Coils might play a protective role in these VAFAs and should be considered, especially in cases in which CFD indicates a pressure increase.

The intra-aneurysmal flow pattern, reflecting the overall hemodynamic characteristics of an intracranial aneurysm, is reported to be more complex in ruptured aneurysms.¹⁷ Stent implantation might modify the complex flow pattern into a simplified pattern by reducing the power of vortices and secondary flows, which may create favorable conditions for intra-aneurysmal thrombosis. In the present study, most of the cases had >2 independent vortices before stent placement and the number of vortices changed during the cardiac cycle in the most complex situations. After stent deployment, weakening of the intensity of the vortices and shifting of the vortex center from the aneurysmal wall were observed in most cases, indicating an improvement of the flow pattern.

According to the results of multiple comparisons among different groups, single stents might not affect the hemodynamics as significantly as multiple stents. This possibility is consistent with clinical experience in that multiple stents improved the long-term results in VAFAs. However, as the number of stents increases, lower WSS and higher pressure might amplify the risk of rupture and recanalization; moreover, there was a greater theoretic chance for occlusion of some vital perforating branches. Although no hemorrhage or ischemic events were encountered in these patients, careful decision-making for the stent-placement strategy and timely follow-up are required.

There are several limitations in this study that might influence the results. First, because this is a patient-specific study and each case might have its own characteristics, the small sample size may be the main limitation. Second, the boundary conditions of the simulations were unified, and some perforating branches were neglected artificially. We did not consider potential changes of the inflow and outflow conditions, which might occur after stent placement. Changes of these boundary conditions will modify the absolute values of the investigated hemodynamic parameters. The observed trends however (ie, decrease in WSS, OSI, and RRT and an increase in pressure) are mostly driven by the separation of the hemodynamic environment of the aneurysmal sac from the parent artery and therefore should remain valid in a small or moderate variation of the boundary conditions. Absolute values derived from computational simulations should always be considered with caution and should be confirmed with actual measurements. In addition, the biologic process of thrombosis formation was too complex to simulate and was omitted.