Stent-Assisted Coiling of Intracranial Bifurcation Aneurysms Leads to Immediate and Delayed Intracranial Vascular Angle Remodeling

Discussion

Bifurcation stent coiling results in a decrease of the effective neck and straightening of the vascular divider angle, which may effectively convert the morphology of a bifurcation aneurysm closer to that of a sidewall type. This study delineates the presence of a previously undefined immediate and delayed effect of stent deployment on the angular configuration of vascular bifurcations undergoing stent-mediated coiling by using self-expanding intracranial microstents. Previous studies have described the effect of balloon inflation−induced straightening of vessels during balloon-mounted stent deployment,^10,11 with Zenteno et al¹⁰ suggesting that the resulting change in angulation of the parent artery could facilitate thrombosis of the aneurysm. Nonetheless, those results differ from the remodeling phenomenon reported here, which was seen in self-expanding stents that have a lower radial force and are deployed without use of balloon inflation. Furthermore, unlike the current study that involved the evaluation of bifurcation aneurysms, Zenteno et al mainly studied sidewall and fusiform aneurysms off a parent nonbifurcating vessel.

The Neuroform and Enterprise stents used in this study are both flexible and self-expanding nitinol stents specially manufactured for use in the cerebral vasculature.^5,6,8,26 The deployment of the stents in the vessels at the bifurcation was noted in itself to significantly modify the vascular angles as demonstrated at the end of the stent-coiling procedure. The extent of the vascular modification was inversely related to the vessel proximal diameter and pretreatment angle δ. The greatest angular remodeling was seen at the AcomA, followed by the BA and MCA, then by the ICA bifurcations, contrary to the order of the vessel caliber at these locations. This finding suggests that the greater the vessel size is, the greater is the resistance of the vessel against the straightening force exerted by the bent stent (F_bending). The smaller the prestenting vascular angle δ is, the greater is the deformation of the stent and its bending angle θ and consequently the greater is the straightening force of the stent, which causes greater angular modification following stent placement. This finding was also corroborated by the greater remodeling seen in the Enterprise stent subset, which was found to have a greater longitudinal stiffness and greater reactive force to bending (Fig 3A). However, at the time these procedures were performed, we were not aware of the difference in the longitudinal stiffness between the Enterprise and the Neuroform stents, and the finding was made retrospectively after we noticed a few cases of significant vessel straightening with the Enterprise stent.

With the passage of time, the persistent self-straightening tendency of these self-expanding shape-memory alloy stents was continually exerted on the cerebral vasculature, leading to the observed longer-term delayed greater angular expansion and vascular remodeling. Nonetheless, this phenomenon was noted to be more prominent during the earlier time periods (1–6 months) of follow-up, reaching steady-state subsequently, because the potential energy was mostly released by the stent, since the latter reverted to a shape closer to its preferred native straight configuration. Nevertheless, the late-follow-up remodeling of the stented angle was still significantly different (P < .05) compared with immediate poststenting angles. It can be imagined that when the elasticity of the metal stent is fully released and the straightening force of the stent and the resistance exerted by the 3D structure of the cerebral vasculature reach a balance, the vascular angle will have reached a steady-state (Fig 1).

The apex of bifurcations is the site of maximum hemodynamic stress in a vascular network because of the direct impact, deflection, and separation of the blood flow streamlines and vortex formation at the lateral angles.^27,28 The layer with the highest velocity of blood flow moves toward and directly impinges at the bifurcation apex where blood flow is divided. Thus, the arterial bifurcation apex experiences highly variable regions of wall shear stress, characteristic of flow separation. Regions of elevated shear stress are believed to cause injury to the endothelial cells of the vessel wall and predispose the vessel to diseases.^27,29,30 The bifurcation angle may affect disease formation at the apex by influencing the tensile or stretching forces at the arterial bifurcation.³¹ The bifurcation angle may affect the formation of flow turbulence near the bifurcation apex.³²

After studying the characteristics of aneurysms on the ICA bifurcation, Sakamoto et al³¹ reported that all the ICA bifurcation aneurysms deviated to the side of the A1 segment of the anterior cerebral artery, which formed a smaller angle with the ICA than that formed between the MCA and the ICA. Their result suggested higher hemodynamic stress experienced on the side of the A1 segment. Aneurysm formation might be related to branching characteristics that locally increase the hemodynamic stresses,^33,34 and normal cerebrovascular geometry may be a risk factor in this context.

The studies by Rossitti and Lofgren^28,35 demonstrated that the branching angles of cerebral arteries may vary widely and that the apex of the bifurcation may lie in a nonoptimal position relative to the dividing streamline of the flow in the parent vessel, resulting in turbulence, vibrations, and increased shear stress on the vessel wall at the apical region, despite the fact that the blood flow/vessel radius relation is optimal. If aneurysm initiation or progression is related to the bifurcation angle at the vascular divider, then the balance of hemodynamic forces responsible likely will be altered by the stent-induced remodeling described in the current study. Furthermore, the angular remodeling properties of self-expanding stents, suggested to be at least partly the result of longitudinal stiffness in the current report, should be taken into consideration when evaluating stent design performance.

However, at the current stage, we are not sure what hemodynamic effect is induced by the angular remodeling caused by the longitudinal stiffness of the self-expanding stent. On one hand, this effect may be beneficial in the case of converting an aneurysm from bifurcation to sidewall because the flow would be diverted away from the aneurysm neck. On the other hand, it may be detrimental if a bifurcation aneurysm is converted into an endwall aneurysm such as may occur in the use of the waffle-cone technique. These theoretic hypotheses have to be both confirmed by hemodynamic modeling and, then, have to be corroborated clinically with long-term angiographic outcomes.

One additional point of concern raised by the angular remodeling described here relates to the theoretic possibility that the shape change may result in a relative movement of the coil mass, which could slowly impinge on the other branches at the vascular divider, possibly leading to delayed occlusion; this phenomenon was not witnessed in any of the cases herein.