Decreased wall shear stress at high-pressure areas predicts the rupture point in ruptured intracranial aneurysms

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OBJECTIVE

Degenerative cerebral aneurysm walls are associated with aneurysm rupture and subarachnoid hemorrhage. Thin-walled regions (TWRs) represent fragile areas that may eventually lead to aneurysm rupture. Previous computational fluid dynamics (CFD) studies reported the correlation of maximum pressure (Pmax) areas and TWRs; however, the correlation with aneurysm rupture has not been established. This study aims to investigate this hemodynamic correlation.

METHODS

The aneurysmal wall surface at the Pmax areas was intraoperatively evaluated using a fluid flow formula under pulsatile blood flow conditions in 23 patients with 23 saccular middle cerebral artery (MCA) bifurcation aneurysms (16 unruptured and 7 ruptured). The pressure difference (Pd) at the Pmax areas was calculated by subtracting the average pressure (Pave) from the Pmax and normalized by dividing this by the dynamic pressure at the aneurysm inlet side. The wall shear stress (WSS) was also calculated at the Pmax areas, aneurysm dome, and parent artery. These hemodynamic parameters were used to validate the correlation with TWRs in unruptured MCA aneurysms. The characteristic hemodynamic parameters at the rupture points in ruptured MCA aneurysms were then determined.

RESULTS

In 13 of 16 unruptured aneurysms (81.2%), Pmax areas were identified that corresponded to TWRs. In 5 of the 7 ruptured cerebral aneurysms, the Pmax areas coincided with the rupture point. At these areas, the Pd values were not higher than those of the TWRs in unruptured cerebral aneurysms; however, minimum WSS, time-averaged WSS, and normalized WSS at the rupture point were significantly lower than those of the TWRs in unruptured aneurysms (p < 0.01).

CONCLUSIONS

At the Pmax area of TWRs, decreased WSS appears to be the crucial hemodynamic parameter that indicates the risk of aneurysm rupture.

ABBREVIATIONS CFD = computational fluid dynamics; CTA = CT angiography; DSA = digital subtraction angiography; IA = intracranial aneurysm; MCA = middle cerebral artery; NWSS = normalized WSS; Pave = average pressure; Pd = pressure difference; Pmax = maximum pressure; SAH = subarachnoid hemorrhage; TAWSS = time-averaged WSS; TWR = thin-walled region; WSS = wall shear stress; WSSmin = minimum WSS.

Article Information

Correspondence Aman B. Patel: Massachusetts General Hospital and Harvard Medical School, Boston, MA. abpatel@mgh.harvard.edu.

INCLUDE WHEN CITING Published online March 15, 2019; DOI: 10.3171/2018.12.JNS182897.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Illustration of the CFD model, including the CFD analysis domain (A) and inlet mass flow rate (B). Vin = mean velocity of the aneurysm inlet.

  • View in gallery

    Examples of analytical CFD. Left: The Pmax point of the aneurysm dome is indicated by an arrow. Right: Intraoperative view. Neurosurgeons score the area indicated by arrows on a 5-point scale relative to the normal, healthy vessel. The average aneurysm wall scores are 4.8 (upper left) and 3.0 (lower left).

  • View in gallery

    Intraoperative views (left column), Pd (center column), and WSS at end-diastole (right column) of 4 representative unruptured aneurysms. The Pmax areas (arrows and crosshairs) correspond to the TWRs of the aneurysm domes. The WSS values at the Pmax areas are relatively low, but within the normal range. A: Score of 5.0, Pd 0.99, WSS 2.89. B: Score of 5.0, Pd 1.30, WSS 2.35. C: Score of 5.0, Pd 1.12, WSS 2.20. D: Score of 3.8, Pd 0.51, WSS 3.07.

  • View in gallery

    Regression analysis of the Pd, WSSmin, TAWSS, and NWSS at TWRs. WSSmin, TAWSS, and NWSS at the TWRs do not correlate with the aneurysm wall score. In contrast, Pd at the TWRs does correlate with the aneurysm wall score. N.S. = not significant.

  • View in gallery

    Intraoperative views, Pd, and WSS at end-diastole (left to right, respectively) of 4 representative ruptured aneurysms. The Pmax areas (arrows and crosshairs) correspond to the rupture points of the aneurysm domes. The WSS at the Pmax areas are remarkably low (< 1.0). A: Pd 1.82, WSS 0.18. B: Pd 0.97, WSS 0.33. C: Pd 0.73, WSS 0.80. D: Pd 1.06, WSS 0.29.

  • View in gallery

    A: Representative ruptured aneurysm. The rupture point (arrow) is localized in the right temporal lobe, and internal hemorrhage is seen on a CT scan. B: The rupture point corresponds to the Pmax area and impingement zone (crosshair). The iso-velocity surfaces (surfaces that show the same value of velocity magnitude) are 0.25 m/sec; Pd 0.88, WSS 0.21.

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