Flow reversal in distal collaterals as a possible mechanism of delayed intraparenchymal hemorrhage after flow diversion treatment of cerebral aneurysms

Abstract

Background and Purpose: Delayed intraparenchymal hemorrhages (DIPHs) are one of the most serious complications of cerebral aneurysm treatment with flow diverters (FD), yet their causes are largely unknown. This study analyzes distal hemodynamic alterations induced by the treatment of intracranial aneurysms with FDs. Methods: A realistic model of the brain arterial network was constructed from MRA images and extended with a constrained constructive optimization technique down to vessel diameters of approximately $50\mu m$ . Different variants of the circle of Willis were created by alternatively occluding communicating arteries. Collateral vessels connecting different arterial trees were then added to the model, and a distributed lumped parameter approach was used to model the pulsatile blood flow in the arterial network. The treatment of an ICA aneurysm was modeled by changing the local resistance, flow inertia, and compliance of the aneurysmal segment. Results: The maximum relative change in distal pressure induced by the aneurysm treatment was below 1%. However, for certain combinations of the circle of Willis and distal collateralization, important flow reversals (with a wall shear stress larger than approximately $1.0dyne/c{m}^2$ ) were observed in collateral vessels, both ipsilaterally and contralaterally to the treated aneurysm. Conclusion: This study suggests the hypothesis that flow diverters treatment of intracranial aneurysms could cause important flow reversal in distal collaterals. Flow reversal has previously been shown to be pro-inflammatory and pro-atherogenic and could therefore have a detrimental effect on these collateral vessels, and thus could be a suitable explanation of DIPHs, while the small distal pressure increase is not.

Keywords: cerebral aneurysm; delayed intraparenchymal hemorrhage; flow diversion; flow reversal; mechanism.

FIGURE 1

Anatomical model construction: (A) arteries reconstructed from MRA images (different arterial trees are rendered with different colors), (B) extension of arterial trees using CCO approach (intermediate stage), (C) pressure distribution calculated along arterial trees and used for generation of collateral vessels in extended arterial model, (D) example of good level of collateralization (superior-inferior view), only collateral branches are visualized, and (E) example of poor collateralization.

FIGURE 2

Anatomical model containing over 100,000 arterial branches constructed by extending MRA-based model with CCO method: (A) anterior-posterior view, (B) superior-inferior view, (C) right-left view, (D) left-right view. Different arterial trees are rendered with different colors: left-ACA = green, left-MCA = blue, left-PCA = magenta, right-ACA = yellow, right-MCA = red, right-PCA = cyan, main feeding vessels and circle of Willis (ICAs, VAs, BA, PCOMs, ACOM) are rendered in white.

FIGURE 3

Histograms showing the frequency of maximum relative pressure change for each of the six cerebral arterial trees obtained for the different scenarios considered: (A) LACA, (B) LMCA, (C) LPCA, (D) RACA, (E) RMCA, (F) RPCA. These histograms show that the largest change was below 0.15% (maximum change occurred in the posterior cerebral artery trees).

FIGURE 4

Histograms showing the frequency of maximum relative change of pulsatility for each of the six cerebral arterial trees obtained for the different scenarios considered: (A) LACA, (B) LMCA, (C) LPCA, (D) RACA, (E) RMCA, (F) RPCA. These histograms show that the largest change was approximately 0.85% (maximum change occurred in the posterior cerebral artery trees).

FIGURE 5

Examples of flow reversal in distal collaterals: (A) Example 1: WSS in collateral between left MCA and ACA trees (ipsilateral to aneurysm and FD), (B) Example 2: WSS in collateral between right MCA and PCA trees (contralateral to aneurysm and FD), (C) Example 3: WSS reversal in collateral between right MCA and PCA trees, and (D) Example 4: accentuation of flow reversal in collateral between right MCA and PCA. Anatomical location of the example collaterals (marked with circles and numbered) are shown on the right column in three orthogonal views.