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Logo of interneuroInterventional Neuroradiology
 
Interv Neuroradiol. 2016 August; 22(4): 389–395.
Published online 2016 February 27. doi:  10.1177/1591019916633243
PMCID: PMC4984379

The effect of basilar artery bifurcation angle on rates of initial occlusion, recanalization, and retreatment of basilar artery apex aneurysms following coil embolization

Abstract

Background

Arterial bifurcations are common locations for aneurysm development given the altered hemodynamic forces and shear stress variations present at these locations. Recent reports indicate that a wide basilar artery bifurcation angle is an independent predictor of aneurysm development, growth, and subsequent rupture.

Methods

To determine the effect of basilar artery bifurcation angle on rates of initial occlusion, recanalization, and retreatment of basilar artery apex aneurysms following coil embolization, the records of 46 patients with basilar artery apex aneurysms treated with endovascular coil embolization from 2007 to 2013 were analyzed.

Results

A wide basilar artery bifurcation angle was associated with a Raymond–Roy Occlusion Classification (RROC) III occlusion in univariate analysis, but was not a statistically significant factor in multivariate modeling. An increasing basilar artery bifurcation angle was not associated with aneurysm recanalization or retreatment following coil embolization. Increasing packing density (p < .01) was the only statistically significant predictor of a RROC I or II closure. The initial RROC designation was the most powerful predictor of both eventual aneurysm recanalization (p = .01) and retreatment (p = .02). While increasing aneurysm size (p < .01), increasing aneurysm volume (p < .01), and increasing neck size (p < .01) were associated with wide basilar artery bifurcation angles, neck size (p = .03) was the only statistically significant predictor of basilar artery bifurcation angle on multivariate analyses.

Conclusion

Basilar artery bifurcation angle fails to predict rates of initial occlusion, recanalization, and retreatment on multivariate modeling in our series. Basilar artery apex aneurysm neck size independently correlates with basilar artery bifurcation angle.

Keywords: Arterial bifurcation angles, basilar artery, endovascular coil embolization, intracranial aneurysm, subarachnoid hemorrhage

Introduction

Endovascular coil embolization has emerged as the dominant treatment modality for intracranial aneurysms.1,2 The widespread utilization of endovascular approaches, however, has been met with concerns regarding increased rates of recanalization and retreatment relative to microsurgical clip occlusion.3,4 Well-defined risk factors for aneurysm recanalization and retreatment include ruptured aneurysm, intraluminal thrombus, low coil packing density, and incomplete initial aneurysm occlusion.5,6 Morphological features of the aneurysm and parent vessel may also influence initial occlusion and recurrence rates after coil embolization.7

In healthy patients without basilar artery apex aneurysms, the basilar artery bifurcates into the bilateral P1 posterior cerebral arteries (PCAs) at angles that range from 30° to 180° (mean: 109–117°).8 Recent reports indicate that a wide basilar artery bifurcation angle (mean: 147–164°) is an independent predictor of aneurysm development, growth, and subsequent rupture.911 Could this phenomenon, presumed secondary to altered hemodynamic forces at the basilar artery apex, have an effect on the outcome of basilar artery apex aneurysms treated with coil embolization? In this report, we sought to determine the association of basilar artery bifurcation angle on rates of initial occlusion, recanalization, and retreatment of basilar artery apex aneurysms following coil embolization.

Methods

Patients and data collection

We performed an observational, retrospective, single-center study to determine the effect of basilar artery bifurcation angle on rates of initial occlusion, recanalization, and retreatment of basilar artery apex aneurysms following coil embolization. Following institutional review board approval at Massachusetts General Hospital (MGH), the records of 484 patients with 517 intracranial saccular aneurysms, of which 46 were located at the basilar artery apex, treated with endovascular coil embolization between January 2007 and December 2013 were reviewed. The study sample was collected by reviewing the MGH cerebrovascular surgery and radiology databases within the study period. Infectious, dissecting, and fusiform aneurysms were not included in the study sample. All historical, clinical, radiographic, and follow-up information was collected from the electronic medical record in accordance with the Health Insurance Portability and Accountability Act.

The basilar artery bifurcation angle10 and basilar artery diameter11 were calculated and recorded as previously described. Recanalization, or recurrence, was defined as an increase in opacification of the neck or dome of the aneurysm at the time of first and/or last angiographic follow-up as compared with the initial post-treatment cerebral angiogram. The Raymond–Roy Occlusion Classification (RROC) was used to grade the degree of initial aneurysm occlusion, as follows: Class I, complete occlusion; Class II, residual neck; and Class III, residual aneurysm.12

Statistical analyses

Descriptive statistics were calculated for clinical and radiographic factors, using the median as a measure of central tendency. A univariate analysis of clinical characteristics and outcomes was performed. Comparisons of continuous variables with non-normal distributions were made using Spearman ρ correlations or non-parametric Mann–Whitney U-tests. Contingency statistics on categorical variables were performed with Fisher exact or χ2 tests. To determine predictors of basilar artery bifurcation angle and initial aneurysm occlusion, recanalization, and retreatment of basilar artery apex aneurysms following coil embolization, variables that reached statistical significance on univariate analyses in addition to variables suspected to contribute to a given outcome were entered into multivariate logistic regression models (standard least squares or nominal logistic). All statistical tests were two-sided and p < .05 was prospectively determined to establish statistical significance. All analyses were performed using SPSS Statistics version 22 (IBM; Armonk, NY) or JMP Pro 12 (SAS; Cary, NC).

Results

Patient, aneurysm, and procedural data

Forty-six patients with 46 basilar artery apex aneurysms were analyzed. Table 1 summarizes the patient, aneurysm, and procedural details of this cohort. The median age was 54.2 years, and 84.8% of the cohort was female. A history of smoking and hypertension was confirmed in 29 (63.0%) and 27 (58.7%) patients, respectively. A family history notable for intracranial aneurysms was confirmed in seven (15.2%) patients. Fifteen (32.6%) patients harbored more than one intracranial aneurysm.

Table 1.
Characteristics of 46 basilar artery apex aneurysms treated with endovascular coil embolization.

The median aneurysm size was 7.5 mm, with 34 (73.9%) aneurysms measuring less than 10 mm. The median aneurysm volume was 112.4 mm3 and the median neck size was 3.4 mm. Seventeen (37.0%) aneurysms harbored blebs or dome irregularities and four (8.7%) aneurysms had intrasaccular thrombus. The median basilar artery bifurcation angle and basilar artery diameter were 128.8° and 2.6 mm, respectively. Of the 46 coiled aneurysms, 14 (30.4%) were ruptured.

Stand-alone coiling was performed on 38 (82.6%) aneurysms, whereas seven (15.2%) aneurysms were treated with stent assistance and one (2.2%) aneurysm was treated with balloon assistance. The median packing density following initial coil embolization was 33.3%. Two (4.3%) patients suffered an intraprocedural aneurysm rupture and three patients (6.5%) experienced an intraprocedural thromboembolic complication.

Outcome data

Table 2 lists the parameters associated with initial RROC I or II closures, recanalization, and need for retreatment. Decreasing aneurysm size (p = .01), decreasing neck size (p = .01), decreasing basilar artery bifurcation angle (p = .03), and increasing packing density (p < .01) were associated with an initial RROC I or II occlusion. Increasing packing density (p < .01) emerged as the only significant predictor of a RROC I or II closure on nominal logistic regression analysis. Decreasing aneurysm size (p = .02), decreasing neck size (p = .03), decreasing aneurysm volume (p = .03), absence of intraluminal thrombus (p = .04), increasing packing density (p = .03), and an initial RROC I or II occlusion (p < .01) were associated with stable aneurysm occlusion (no recanalization) following coil embolization. Decreasing aneurysm size (p = .02) and an initial RROC I or II occlusion (p = .01) were associated with a durable aneurysm occlusion (no retreatment) following coil embolization. Basilar artery bifurcation angle was not associated with rates of recanalization (p = .09) or retreatment (p = .49). A RROC I or II initial closure emerged as the only variable that predicted aneurysm recanalization (p = .01) or retreatment (p = .02) on multivariate analyses.

Table 2.
Univariate analyses evaluating degree of initial occlusion, recanalization, and retreatment from 46 patients with basilar artery apex aneurysms treated with coil embolization.

Table 3 details aneurysm-specific factors that correlated with basilar artery bifurcation angles. Increasing aneurysm size (p < .01), increasing aneurysm volume (p < .01), and increasing neck size (p < .01) (Figure 1) were associated with a widened basilar artery bifurcation angle on univariate Spearman ρ correlation analyses. There was no association between widened basilar artery bifurcation angle and ruptured aneurysm. Subsequent standard least squares regression analyses demonstrated that neck size (p = .03) was the only statistically significant predictor of basilar artery bifurcation angle (Figure 2).

Figure 1.
(a) Multiplanar reconstruction (MPR) and (b) three-dimensional rendering of a large basilar artery apex aneurysm with a large basilar artery angle and a wide aneurysm neck. (c) MPR and (d) three-dimensional rendering of a small basilar artery apex aneurysm ...
Figure 2.
The correlation of basilar artery (BA) angle and (a) aneurysm size, (b) aneurysm volume, and (c) neck size. Data is shown as leverage plots derived from standard least squares regression analysis. Neck size emerged as the only statistically significant ...
Table 3.
Univariate analysis and multivariate modeling evaluating basilar artery bifurcation angle from 46 patients with basilar artery apex aneurysms treated with coil embolization.

Discussion

The precise etiology of sporadic intracranial aneurysms remains unknown, but likely involves a complex interplay of genetic predispositions, environmental and acquired risk factors, and hemodynamic and morphological parameters. With the technical advancement and increasing availability of non- and minimally-invasive vascular imaging techniques coupled with computational fluid dynamic (CFD) modeling, the effect of parent vessel and aneurysm morphology along with local hemodynamic forces on aneurysm formation has become an area of active research and investigation.10,13

Arterial bifurcations represent a preferred site of aneurysm development given the abnormal hemodynamic forces and shear stresses present at these locations.14 With respect to the basilar artery bifurcation, one hypothesis of aneurysm formation is that as blood is diverted into the superior cerebellar arteries and PCAs there is a resulting decrease in blood flow velocity and kinetic energy at the basilar artery apex, which leads to a gradual weakening of the arterial wall with subsequent aneurysm development.15,16 This alteration in hemodynamic forces at the basilar artery apex may be exacerbated by wide PCA angles of divergence, further lowering the wall shear stress (WSS) at the basilar artery apex and inciting a cascade of biological reactions that lead to vessel wall degradation and aneurysm formation.13 To demonstrate this principle in a contemporary intracranial aneurysm series, Tütüncü et al. compared basilar artery bifurcation angles in 45 patients with basilar artery apex aneurysms with 65 patients with intracranial aneurysms at locations other than the basilar artery apex and 103 patients without intracranial aneurysms, and discovered that patients with basilar artery apex aneurysms had significantly wider basilar artery bifurcation angles (mean: 146.7° versus 111.7° and 103.0°, respectively). In this series, using CFD models, the authors also demonstrated that as the basilar artery bifurcation increases, the WSS value at the basilar artery apex decreases and is diffused over a larger surface area of vessel wall.10 Similarly, Can et al. studied 33 patients with basilar artery apex aneurysms and 33 patients with intracranial aneurysms at locations other than the basilar artery apex, and also noted that wide basilar artery bifurcation angles (mean: 163.6° versus 112.2°) predicted the presence of basilar artery apex aneurysms.11 Finally, Jagadeesan et al. observed that patients with ruptured basilar artery apex aneurysms had wider basilar artery bifurcation angles than patients with non-aneurysmal perimesencephalic subarachnoid hemorrhage (mean: 135.0° versus 87.7°).17

Despite the well-described correlation between large basilar artery bifurcation angles and the presence of a basilar artery apex aneurysm, no study to date has evaluated whether basilar artery bifurcation angle influences degrees of initial occlusion, recanalization, and retreatment following coil embolization of basilar artery apex aneurysms. Given the described hemodynamic changes that occur with widening of the basilar artery bifurcation angle, it is reasonable to postulate that these same hemodynamic forces and stress variations may influence basilar artery apex aneurysm recanalization and the need for retreatment following coil embolization. To this end, we analyzed 46 patients with unruptured or ruptured basilar artery apex aneurysms treated with coil embolization. While a narrow basilar artery bifurcation angle was associated with RROC I and II occlusions on univariate analyses, increasing packing density was the only significant predictor of RROC I and II closures on multivariate testing. In addition, basilar artery bifurcation angle was not associated with either aneurysm recanalization or retreatment in our series; initial RROC designation emerged as the only reliable predictor of eventual aneurysm recanalization or retreatment. This finding is mirrored by data from large-scale studies on posterior circulation aneurysms treated with coil embolization, in which the degree of initial aneurysm occlusion was the strongest predictor of recurrence and retreatment.18,19

The lack of an observed relationship between basilar artery bifurcation angle and basilar artery apex aneurysm recanalization and retreatment following coil embolization may result from the lack of a truly causative relationship between basilar artery bifurcation angle and basilar artery apex aneurysm development. In the series by Tütüncü et al., increasing aneurysm size, increasing aneurysm height, and increasing neck size were associated with larger basilar artery bifurcation angles on univariate analyses, but neck size emerged as the only significant predictor of basilar artery bifurcation angle on multivariate analyses.10 This same phenomenon was observed in our series, suggesting that a wide basilar artery bifurcation angle may be an effect, rather than a cause, of aneurysm development that directly correlates with the size of the aneurysm’s neck. To this end, it is conceivable that the PCAs are gradually pushed laterally relative to the basilar artery apex as an aneurysm develops, and that the degree to which the PCAs diverge is directly related to size of the diseased basilar artery apex, as reflected by the size of the aneurysm neck.

Despite the inability of basilar artery bifurcation angles to predict the degree of aneurysm occlusion, recanalization, or retreatment of basilar artery apex aneurysms following coil embolization in our series, the incorporation of morphological determinants and hemodynamic factors into risk models for these outcome measures is important. Current classification schema for aneurysm recanalization and retreatment may have limited predictive capacity given their reliance on static factors,5,6,12,20,21 and the use of dynamic anatomical and hemodynamic variables in these grading systems may increase their clinical utility and reliability. The incorporation of these dynamic parameters into existing classification systems is possible given the widespread availability of non- and minimally-invasive vascular imaging modalities and emerging CFD modeling techniques.

Our study has the limitations inherent in any single institution, retrospective series. Compared with the total number of aneurysms treated via coil embolization during the study period, basilar artery apex aneurysms represented only a small fraction. Therefore, while several comparisons in our study met statistical significance, such observations should be validated in larger populations and across multiple high-volume centers. In addition, basilar artery bifurcation angle was measured manually using three-dimensional renderings and multiplanar reconstructions and, therefore, the measurements are subject to human error. Computerized models that measure such anatomical and morphological factors as well as the degree and location of aneurysm recanalization may in the future be more objective and accurate.

Conclusion

The identification of parameters that influence the degree of aneurysm occlusion, recanalization, and retreatment following coil embolization is clinically important. While a widened basilar artery bifurcation angle is associated with RROC III closures of basilar artery apex aneurysms following coil embolization on univariate analyses, basilar artery bifurcation angle fails to predict rates of initial occlusion, recanalization, and retreatment on multivariate analyses in our series. Basilar artery apex aneurysm neck size independently correlates with basilar artery bifurcation angle.

Acknowledgments

CJS and JIK contributed equally to this work. All authors had integral participation in the study. CJS, JIK, BPW, CMT, and ABP conceived of the project idea. CJS, JIK, and CMT performed the data collection. CJS, CMT, and MJK performed the angiographic review. CJS, BPW, and PKA performed the statistical analysis and figure/table presentation. All authors were involved in the manuscript preparation and final approval.

Declaration of conflicting interests

The authors declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: ABP is a consultant for Penumbra, Inc. (Alameda, CA) and Covidien (Medtronic; Minneapolis, MN). The remaining authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

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