The relationship between ruptured aneurysm location, subarachnoid hemorrhage clot thickness, and incidence of radiographic or symptomatic vasospasm in patients enrolled in a prospective randomized controlled trial

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Object

Cerebral vasospasm following subarachnoid hemorrhage (SAH) causes significant morbidity in a delayed fashion. The authors recently published a new scale that grades the maximum thickness of SAH on axial CT and is predictive of vasospasm incidence. In this study, the authors further investigate whether different aneurysm locations result in different SAH clot burdens and whether any concurrent differences in ruptured aneurysm location and maximum SAH clot burden affect vasospasm incidence.

Methods

Two hundred fifty patients who were part of a prospective randomized controlled trial were reviewed. Most outcome and demographic variables were included as part of the prospective randomized controlled trial. Additional variables were also collected at a later time, including vasospasm data and maximum clot thickness.

Results

Aneurysms were categorized into 1 of 6 groups: intradural internal carotid artery aneurysms, vertebral artery (VA) aneurysms (including the posterior inferior cerebellar artery), basilar trunk or basilar apex aneurysms, middle cerebral artery aneurysms, pericallosal aneurysms, and anterior communicating artery aneurysms. Twenty-nine patients with nonaneurysmal SAH were excluded. Patients with pericallosal aneurysms had the least average maximum clot burden (5.3 mm), compared with 6.4 mm for the group overall, but had the highest rate of symptomatic vasospasm (56% vs 22% overall, OR 4.9, RR 2.7, p = 0.026). Symptomatic vasospasm occurrence was tallied in patients with clinical deterioration attributable to delayed cerebral ischemia. There were no significant differences in maximum clot thickness between aneurysm sites. Middle cerebral artery aneurysms resulted in the thickest mean maximum clot (7.1 mm) but rates of symptomatic and radiographic vasospasm in this group were statistically no different compared with the overall group. Vertebral artery aneurysms had the worst 1-year modified Rankin scale (mRS) scores (3.0 vs 1.9 overall, respectively; p = 0.0249). A 1-year mRS score of 0–2 (good outcome) was found in 72% of patients overall, but in only 50% of those with pericallosal and VA aneurysms, and in 56% of those with basilar artery aneurysms (p = 0.0044). Patients with stroke from vasospasm had higher mean clot thickness (9.71 vs 6.15 mm, p = 0.004).

Conclusions

The location of a ruptured aneurysm minimally affects the maximum thickness of the SAH clot but is predictive of symptomatic vasospasm or clinical deterioration from delayed cerebral ischemia in pericallosal aneurysms. The worst 1-year mRS outcomes in this cohort of patients were noted in those with posterior circulation aneurysms or pericallosal artery aneurysms. Patients experiencing stroke had higher mean clot burden.

Abbreviations used in this paper:ACoA = anterior communicating artery; BA = basilar artery; BNI = Barrow Neurological Institute; BRAT = Barrow Ruptured Aneurysm Trial; ICA = internal carotid artery; MCA = middle cerebral artery; mRS = modified Rankin Scale; PICA = posterior inferior cerebellar artery; SAH = subarachnoid hemorrhage; VA = vertebral artery.

Object

Cerebral vasospasm following subarachnoid hemorrhage (SAH) causes significant morbidity in a delayed fashion. The authors recently published a new scale that grades the maximum thickness of SAH on axial CT and is predictive of vasospasm incidence. In this study, the authors further investigate whether different aneurysm locations result in different SAH clot burdens and whether any concurrent differences in ruptured aneurysm location and maximum SAH clot burden affect vasospasm incidence.

Methods

Two hundred fifty patients who were part of a prospective randomized controlled trial were reviewed. Most outcome and demographic variables were included as part of the prospective randomized controlled trial. Additional variables were also collected at a later time, including vasospasm data and maximum clot thickness.

Results

Aneurysms were categorized into 1 of 6 groups: intradural internal carotid artery aneurysms, vertebral artery (VA) aneurysms (including the posterior inferior cerebellar artery), basilar trunk or basilar apex aneurysms, middle cerebral artery aneurysms, pericallosal aneurysms, and anterior communicating artery aneurysms. Twenty-nine patients with nonaneurysmal SAH were excluded. Patients with pericallosal aneurysms had the least average maximum clot burden (5.3 mm), compared with 6.4 mm for the group overall, but had the highest rate of symptomatic vasospasm (56% vs 22% overall, OR 4.9, RR 2.7, p = 0.026). Symptomatic vasospasm occurrence was tallied in patients with clinical deterioration attributable to delayed cerebral ischemia. There were no significant differences in maximum clot thickness between aneurysm sites. Middle cerebral artery aneurysms resulted in the thickest mean maximum clot (7.1 mm) but rates of symptomatic and radiographic vasospasm in this group were statistically no different compared with the overall group. Vertebral artery aneurysms had the worst 1-year modified Rankin scale (mRS) scores (3.0 vs 1.9 overall, respectively; p = 0.0249). A 1-year mRS score of 0–2 (good outcome) was found in 72% of patients overall, but in only 50% of those with pericallosal and VA aneurysms, and in 56% of those with basilar artery aneurysms (p = 0.0044). Patients with stroke from vasospasm had higher mean clot thickness (9.71 vs 6.15 mm, p = 0.004).

Conclusions

The location of a ruptured aneurysm minimally affects the maximum thickness of the SAH clot but is predictive of symptomatic vasospasm or clinical deterioration from delayed cerebral ischemia in pericallosal aneurysms. The worst 1-year mRS outcomes in this cohort of patients were noted in those with posterior circulation aneurysms or pericallosal artery aneurysms. Patients experiencing stroke had higher mean clot burden.

Cerebral vasospasm in the setting of subarachnoid hemorrhage (SAH) leads to delayed ischemic damage to the brain and is the greatest cause of significant morbidity following aneurysmal SAH.1,5,10 Prediction of a patient's risk of cerebral vasospasm based on CT findings has been a field of great interest. Several grading scales stratify risk for cerebral vasospasm, including the Fisher scale.2,4 We have previously published a study that provides a simple quantitative assessment of the risk of vasospasm based on the maximum burden of SAH in the basal cisterns or fissures.9

We sought to further study the relationship between aneurysm location and maximum SAH burden in patients enrolled in a prospective randomized controlled trial. In addition to assessing differences in bleed thickness with different aneurysm types, we also investigated whether differences in the location of ruptured aneurysms can further influence the risk for developing symptomatic or radiographic vasospasm.

Methods

Study Criteria and Data Acquisition

We analyzed 250 patients with SAH who had been enrolled in a prospective randomized controlled trial and reviewed their hospital charts retrospectively for vasospasm occurrence (whether radiographic or clinical) and clot thickness; these variables had not been collected in the prospective study. The methods for determination of these variables have been published previously.9 All other data points, including demographics, aneurysm characteristics, aneurysm location, aneurysm size, presenting clinical neurological status, neurological outcomes (modified Rankin Scale [mRS] and Glasgow Outcome Scale scores), and treatment modality, as well as other data were collected in a prospective and blinded fashion in the Barrow Ruptured Aneurysm Trial (BRAT).6,8 This study was approved by the St. Joseph's Hospital Institutional Review Board.

We excluded 29 patients with nonaneurysmal SAH. In the initial report,9 we excluded 2 patients who did not have admission CT scans available for review and 1 patient who died before treatment; these patients were also excluded for this report. In addition, for this report, we also excluded 2 patients with cavernous internal carotid artery (ICA) aneurysms because of their extradural location. Aneurysm treatment included coil embolization or microsurgical clip placement.

Clinical Course

Patients underwent routine and standardized SAH treatment in an intensive care unit as previously described,8,9 including ventricular drainage when necessary, nimodipine use in all patients, and routine transcranial Doppler monitoring 3 times weekly. Hypertensive therapy was instituted as required by symptomatic or radiographic vasospasm. Most patients received routine surveillance conventional angiography approximately 7 days after ictus, even in the absence of vasospasm. A minority of patients who were asymptomatic with a good clinical examination and assumed low risk for vasospasm did not undergo conventional angiography. Computed tomography angiography was obtained for neurological status alteration (often in the setting of increased transcranial Doppler velocities), followed by hypertensive therapy and then conventional angiography, if warranted by the CT angiography findings. Endovascular intervention, including balloon angioplasty or calcium channel blocker infusion, was performed based on angiographic findings in patients with symptomatic vasospasm (clinical deterioration from delayed cerebral ischemia).

Vasospasm Determination

The methods for determination of vasospasm used in this study have been published previously.9 The presence of radiographic vasospasm and degree of vasospasm were determined by an independent neuroradiologist. Conventional angiography was obtained in all but 3 patients; 1 patient each underwent CT angiography, MR angiography, or CT perfusion as confirmatory tests for vasospasm in the absence of angiography. Symptomatic vasospasm, also referred to as clinical deterioration attributable to delayed cerebral ischemia, was recorded for patients with neurological findings concurrent to radiographic vasospasm occurring in the affected vascular territory, or in patients with radiographic vasospasm who responded to hypertensive therapy with resolution of their symptoms. Patients with symptomatic or radiographic vasospasm with clear evidence of infarction on either CT or MRI (for all confirmed cases except 1 case) were tabulated as having stroke (cerebral infarction) attributable to vasospasm.

Barrow Neurological Institute Scale

The Barrow Neurological Institute (BNI) Scale9 determines the risk for vasospasm based on SAH thickness. This scale documents the maximum clot thickness on 32-slice, axial, noncontrast head CT scans in any subarachnoid space with the thickness measured perpendicular to the direction of the long axis of the cistern or fissure in which it is measured. Measurements were made based on the patients' CT scans within the first 3 hours of admission by 1 neurosurgeon (D.A.W.) who was blinded to the clinical course and vasospasm incidence in all patients. The reliability of the scale was confirmed by 2 additional neurosurgeons in a blinded fashion; when comparing the interobserver variability of the Fisher scale to the BNI scale, there was a mean κ coefficient of 0.65 for the BNI scale, which was better than the κ coefficient (0.51) for the Fisher scale. The intraobserver variability was also superior for the BNI scale (mean 0.81) compared with the Fisher scale (mean 0.35). The scale consists of 5 grades: no blood on CT (Grade 1), clot thickness less than 5 mm (Grade 2), clot thickness 5–10 mm (Grade 3), clot thickness 10–15 mm (Grade 4), and clot thickness greater than 15 mm (Grade 5).

Grouping of Aneurysms by Location

The aneurysms in the patients were grouped into 1 of 6 locations based on cistern or fissure proximity (Table 1, Fig. 1). Intradural ICA aneurysms were placed into a single location group. Another group was designated as the vertebral artery (VA) location. This group included patients with aneurysms of the intradural VA, the posterior inferior cerebellar artery (PICA), and those at or proximal to the vertebrobasilar junction. The third group included basilar artery (BA) aneurysms, including aneurysms of the anterior inferior cerebellar artery origin, superior cerebellar artery origin, basilar trunk, basilar apex, and P1/P2 segment of the posterior cerebral artery. The fourth group included aneurysms of the middle cerebral artery (MCA), almost exclusively located at the MCA bifurcation. The fifth group included aneurysms involving the pericallosal arteries (A2/A3 or A3/A4), and the final group was designated as anterior communicating artery (ACoA) aneurysms, which also included aneurysms classified as at the A1/A2 junction. In this fashion, we were able to account for all aneurysms that were eligible for inclusion with the exception of 2 cavernous ICA aneurysms; these were excluded due to their extradural location.

TABLE 1:

Distribution of aneurysms by location*

GroupNo. of Patients (n = 216)LocationIncluded Aneurysms
ICA70intradural ICAPCoA, anterior choroidal artery, ophthalmic artery, ICA terminus
VA16lower vertebrobasilar regionPICA, VA
BA18upper vertebrobasilar regionbasilar trunk, AICA, SCA, P1/P2, basilar apex
MCA36MCAproximal MCA, MCA bifurcation
pericallosal arteries9pericallosal regionpericallosal artery
ACoA67ACoA complexA1/A2 junction, ACoA

A1 = first segment of anterior cerebral artery; A2 = second segment of anterior cerebral artery; AICA = anterior inferior cerebellar artery; PCA = posterior cerebral artery; PCoA = posterior communicating artery; SCA = superior cerebellar artery.

Fig. 1.
Fig. 1.

Schematic representation of the stratification of ruptured aneurysms into 6 location zones for the purposes of analysis in this study. Aneurysm groups include pericallosal artery aneurysm, MCA aneurysms, upper posterior circulation aneurysms (BA), lower posterior circulation aneurysms (VA), intradural ICA aneurysms, and ACoA aneurysms. Used with permission from Dreamstime LLC.

Statistical Analysis

Statistical analysis was performed using GraphPad Prism Software (GraphPad Inc.). For categorical variables, the Fisher exact test was used when comparing 2 groups with 2 outcome categories. The chi-square test for independence was used when analyzing contingency data for more than 2 groups; in cases of small sample sizes in certain contingency groups, 2 groups were combined into a single group, because the chi-square test for independence is not valid when groups contain zero patients. In 1 instance, the Fisher exact test was used rather than the chi-square test to obtain statistical significance for a 2 × 6 matrix with sparsely populated cells (Table 2); the analysis was performed using an exact analysis (http://www.physics.csbsju.edu/stats/exact_NROW_NCOLUMN_form.html). For continuous variables, the Mann-Whitney (nonparametric) test was used for comparing 2 populations with continuous data, while the Kruskal-Wallis (nonparametric) test was used for comparing more than 2 groups with continuous data. Univariate linear regression analysis was used to compare the relationship between clot thickness and aneurysm size using the Pearson correlation coefficient; p values < 0.05 were considered significant. Continuous values were reported as means ± SD; figures depicting means are shown with error bars depicting the standard error of the mean.

TABLE 2:

Demographic and outcome variables by location

VariableOverallICAVABAMCAPericallosal ArteriesACoAp Value
no. of patients21670161836967
mean age ± SD (yrs)53.7 ± 11.955.4 ± 12.954.5 ± 9.856.4 ± 8.452.2 ± 13.157.2 ± 13.051.2 ± 10.90.158
sex (%)
 female73.69037.583.377.766.661.2
 male26.41062.516.622.233.338.8
mean Hunt & Hess grade ± SD2.6 ± 1.02.4 ± 1.03.25 ± 1.12.7 ± 1.12.7 ± 1.02.8 ± 1.22.6 ± 0.90.1134
mean aneurysm size ± SD (mm)6.6 ± 3.36.4 ± 3.35.6 ± 2.67.6 ± 3.77.6 ± 3.76.2 ± 3.56.2 ± 3.10.1399
mean SAH max thickness ± SD (mm)6.4 ± 4.66.3 ± 5.36.0 ± 3.06.2 ± 3.77.1 ± 5.15.3 ± 3.26.4 ± 4.20.898
mean BNI scale grade ± SD2.8 ± 0.92.80 ± 1.12.9 ± 0.62.8 ± 0.93.1 ± 1.02.7 ± 0.72.8 ± 0.80.778
BNI scale grade (%)0.629*
 13.77.1017000
 23336255.6334439
 3443962.561394443
 412.57.112.517161115
 56.511001103
symptomatic vasospasm (%)0.171
 yes22252017225616
 no78758083784484
radiographic vasospasm (%)0.662
 yes50495344517848
 no50514756492252
stroke (%)0.250§
 yes6.54.36.3011.122.27.5
 no93.595.793.710088.977.892.5
mean 1-yr mRS score ± SD1.9 ± 1.91.8 ± 1.73.0 ± 2.22.1 ± 1.91.9 ± 2.02.1 ± 1.41.7 ± 1.90.175
1-yr mRS score (%)0.098
 0–272785056745078
 3–628225044265022

When combining BNI Grades 1 and 2, BNI Grades 4 and 5 for the purpose of using the chi-square test for independence.

Clinical deterioration related to delayed cerebral ischemia.

Cerebral infarction from vasospasm.

Calculated using the Fisher exact test in a 2 × 6 matrix.

Results

Two hundred sixteen patients were included in this study (57 males and 159 females, mean age 53.7 ± 11.9 years). Seventy patients had aneurysms located in the intradural ICA, 16 had aneurysms in the VA location, 18 in the BA segment, 36 had MCA aneurysms, 9 had pericallosal aneurysms, and 67 patients had ACoA aneurysms (Table 1).

Demographic Data

Overall, no significant difference was found on presentation between age and aneurysm location or between Hunt & Hess grade and aneurysm location (Table 2). Differences in sex distribution across the 6 groups of aneurysms were significant; all aneurysm locations except the VA location group had a significantly higher proportion of female patients than male patients (Table 2).

Aneurysm Characteristics

No significant difference in aneurysm size existed between groups (Table 2). The mean aneurysm size for the entire group of 216 patients was 6.6 ± 3.3 mm. When analyzing aneurysm size as a function of the BNI scale, no statistically significant difference in the mean aneurysm size was found between any of the 5 BNI scale grades (p = 0.92; Fig. 2A). Using linear regression to compare the relationship of aneurysm size to SAH clot thickness in a fissure or cistern revealed a positive correlation, but this correlation did not reach significance (slope = 0.15 ± 0.09, Pearson correlation coefficient = 0.1098 [95% CI −0.024 to 0.24], p = 0.1085; Fig. 2B).

Fig. 2.
Fig. 2.

Results from different analyses. A: Graph of aneurysm size stratified by BNI scale grade. There was no significant difference in the mean aneurysm size in any of the 5 groups of BNI scale grades (p = 0.92). B: Scatterplot of SAH maximum clot thickness (mm) versus ruptured aneurysm size (mm). There was a slight positive correlation (p = 0.1085). Solid line = trend line; dashed lines = 95% CIs. C: Graph of the presence of any symptomatic or radiographic vasospasm in each of the 6 aneurysm location groups. There was no overall statistically significant difference between groups (p = 0.70). Peri = pericallosal arteries. D: Graph of 1-year mean mRS outcomes for the VA aneurysm location compared with aneurysms of all other locations, showing that the higher mRS score at 1 year was statistically different (p = 0.0249). E: Graph of mRS outcomes at 1 year in each of the 6 aneurysm location groups shown as either good (mRS score 0–2) or poor outcome (mRS score 3–6; p = 0.098). F: Graph showing the good outcomes (mRS score 0–2) at 1 year were much less frequent in ruptured aneurysms of the posterior circulation and pericallosal aneurysm locations when compared with aneurysms of all other locations (p = 0.0044).

Distribution Between Patients Receiving Clip Placement or Coil Embolization

There was no statistical difference in the mean aneurysm size between the coil embolization and clip placement groups in the groups studied here (p = 0.460, Table 3). There was also no statistical difference in the overall distribution of aneurysm locations in the coiled and clipped groups (p = 0.493, chi-square test).

TABLE 3:

Comparison of aneurysm size and location in the surgical clip placement and endovascular treatment groups

Aneurysm VariableClip PlacementCoil Embolizationp Value
location (%)0.493
 ICA47 (32.4)22 (31.4)
 VA9 (6.2)7 (10)
 BA11 (7.6)7 (10)
 MCA29 (20)7 (10)
 pericallosal arteries6 (4.1)3 (4.3)
 ACoA43 (30)24 (34.3)
mean size ± SD (mm)6.56 ± 3.426.68 ± 3.050.460

Subarachnoid Hemorrhage Clot Burden on Presentation

The mean clot thickness measured on presentation CT was 6.4 ± 4.6 mm. Comparing the 6 aneurysm location groups overall revealed no statistically significant difference in clot thickness (p = 0.898; Table 2). The overall average BNI scale grade was 2.8 ± 0.9; no significant difference in BNI scale grade was found between aneurysm locations (p = 0.778; Table 2). The largest mean clot thickness (7.1 mm) and highest BNI scale grade (3.1 on average) occurred in MCA aneurysms. The smallest mean clot thickness (5.3 mm) and lowest BNI scale grade (2.7 on average) occurred in pericallosal aneurysms.

Vasospasm Incidence

Vasospasm, either radiographic or clinical, occurred in 107 (50.7%) of 211 patients with recorded data. There was a much higher incidence of any vasospasm (77.7%) at the pericallosal location despite the lowest mean clot thickness at this location (Fig. 2C). Radiographic vasospasm occurred in 106 (50.2%) of 211 patients. No significant difference in the incidence of radiograph vasospasm was found between aneurysm groups (p = 0.66; Table 2).

Symptomatic vasospasm (clinical deterioration from delayed cerebral ischemia) occurred in 47 patients (22%; Table 2). The pericallosal aneurysm location had a 56% incidence of symptomatic vasospasm. Comparing the incidence in this aneurysm location to symptomatic vasospasm at all other locations (55% vs 22%), the increased risk for pericallosal artery aneurysms was significant (p = 0.0261, Fisher exact test; OR 4.85, RR 2.71; Table 4). In patients with symptomatic (clinical) vasospasm, 71.7% had intraventricular hemorrhage compared with 55.4% of patients who did not exhibit symptomatic vasospasm, but the difference was not statistically significant (p = 0.0622).

TABLE 4:

Risk of symptomatic vasospasm (clinical deterioration from delayed cerebral ischemia) by aneurysm location

Aneurysm LocationOR*RR*p Value
ICA1.21.30.60
VA0.880.901.0
BA0.70.70.77
MCA1.01.01.0
pericallosal arteries4.92.70.026
ACoA0.670.600.22

Compared to all other aneurysm locations.

There was also no significant difference in the incidence of infarcts attributed to vasospasm between groups (p = 0.25; Table 2). However, when comparing the mean clot thickness in 14 patients who had a stroke (cerebral infarction) attributed to vasospasm versus the mean clot thickness in the 202 patients who did not, the difference was significant (9.71 vs 6.15 mm, respectively; p = 0.004).

Outcomes

The mean mRS score in 190 patients at the 1-year follow-up was 1.9 ± 1.9. There was no significant difference in 1-year mRS score overall (p = 0.175; Table 2). The VA aneurysm group had a worse mean mRS score at 1 year (3.0 ± 2.2) compared with all other aneurysms (mean = 1.8 ± 1.8); this difference was significant (p = 0.0249; Fig. 2D).

Outcomes were also dichotomized into 2 groups: good outcome (mRS score 0–2) and poor outcome (mRS score 3–6). There were good outcomes in 137 (72%) of 190 patients. The difference in good outcome occurrence between the 6 locations was not significant (p = 0.098; Table 2, Fig. 2E). All mRS outcomes at the 1-year follow-up are listed in Table 5. When posterior circulation and pericallosal aneurysms were analyzed together, only 20 (53%) of 38 patients had 1-year mRS scores of 0–2. The likelihood of a good outcome at 1 year was 1.5 (RR) or 3.0 (OR) times higher for an aneurysm at all other locations compared with the posterior circulation and pericallosal artery aneurysms (77% vs 53%, p = 0.0044; Fig. 2F).

TABLE 5:

One-year mRS outcomes stratified by aneurysm location*

mRS ScoreICA (n = 63)VA (n = 14)BA (n = 16)MCA (n = 31)Pericallosal Arteries (n = 8)ACoA (n = 58)
0190252312.526
1414325392545
217761312.57
381431637.57
4570312.53
5000000
69.52912.516012

All data given as percentages.

Discussion

Delayed ischemia from cerebral vasospasm is the greatest cause of morbidity in patients with SAH.3,5,10 Identifying patients at the greatest risk for cerebral vasospasm is an important prognosticator in the setting of SAH and may identify patients who will likely need hypertensive therapy, or potential endovascular treatment of vasospasm, or both. A comprehensive review of the literature by Harrod et al. from 1996 to 2005 showed that the only factor that has shown to be predictive of cerebral vasospasm is the burden of blood at the time of SAH.3 A previous study from our center corroborates this finding and stratifies the maximum clot burden into 5 categories.9 In a study of 41 patients, the same group responsible for the Fisher scale2 investigated the relation of cerebral vasospasm to the extent and location of blood.5 Their findings indicated that the location of blood is well correlated with the arterial territory that later develops severe vasospasm,5 as previous authors have re-demonstrated when correlating the territory of cerebral infarction with aneurysm location.7 However, the study was limited to 41 patients, of whom even fewer actually experienced vasospasm.5

In a retrospective study of 211 patients, another group examined predictors of vasospasm and found that only age and modified Fisher grade were predictive of vasospasm.10 Aneurysm location in their study was stratified into 4 groups: no aneurysm, anterior circulation, posterior circulation, or unclear.10 A retrospective review of 178 patients investigated factors related to symptomatic cerebral vasospasm, but while aneurysm location was described, it was not mentioned in the analysis of predictors of vasospasm, perhaps due to a large number of aneurysm locations (n = 12).

In our series of 216 patients in a randomized controlled trial with treated ruptured aneurysms, we investigated the relationship between ruptured aneurysm location (when stratified into 6 groups) and vasospasm. Concurrently, we sought to address the influence of the ruptured aneurysm type on maximum clot burden, the most influential of all predictors of cerebral vasospasm in SAH. Our findings demonstrated that when stratified into 6 different aneurysm locations, maximum SAH clot thickness or burden did not differ between ruptured aneurysm groups. Although the ruptured aneurysm location groups had similar overall clot burden, the effect of this similar clot burden on cerebral vasospasm also did not vary by location; that is, most groups had similar (nonstatistically different) rates of vasospasm, radiographic or symptomatic in the setting of nonstatistically different clot burden. The exception was the pericallosal artery aneurysm group; these aneurysms had the lowest overall clot burden. They also had the highest risk of symptomatic vasospasm or clinical deterioration from delayed cerebral ischemia (p = 0.026).

Several notable findings included the highest average maximum clot thickness at the MCA location, despite a lower than average overall vasospasm risk. The opposite was true for pericallosal aneurysms. Pericallosal aneurysms rupture into the confines of the interhemispheric fissure, where it is possible for subarachnoid blood to cause irritation of fairly small caliber vessels (the distal anterior cerebral arteries) from both hemispheres. This symptomatic vasospasm may be related to the smaller diameter of the pericallosal arteries at baseline, which may make them more prone to the deleterious effects of further narrowing; this possibility requires further investigation. The pericallosal group consisted of a small sample size of just 9 patients; although the result was statistically significant, it remains a small sample of patients. Aneurysms of the MCA rupture into the sylvian fissure and sometimes intraparenchymally, and their bleed location is theoretically the most distant from the contralateral cistern or fissure.

When stratifying the risk for symptomatic vasospasm (or clinical deterioration due to delayed cerebral ischemia) using the BNI scale, the higher the grade, the more likely the risk for vasospasm. Comparing patients with a BNI scale grade of 5 to patients with a grade of 1 produced an odds ratio greater than 11. Aneurysms of the pericallosal artery may have a significantly higher risk for symptomatic vasospasm than other aneurysms of similar BNI scale score, demonstrated by ruptured pericallosal artery aneurysms harboring the lowest mean maximum clot thickness and highest rates of vasospasm. We also found that a significantly higher mean clot thickness was found in patients with stroke (cerebral infarction) from vasospasm than those without (9.71 vs 6.15 mm, p = 0.004). Our results also show that the mean size of aneurysms did not differ by BNI scale grade; that is, larger aneurysms were no more likely to have a higher maximum SAH clot burden using the BNI scale. Similarly, while there was a slight linear relationship between aneurysm size and clot thickness, it was not significant (p = 0.1085).

Patients with lower VA aneurysms had the worst overall mean 1-year mRS scores; the difference between outcomes in patients with these aneurysms and all others was significant (p = 0.0249). The reason for this difference may be the increased morbidity associated with bleeds in the vicinity of the lower cranial nerves, associated with an increased risk of ventilator dependency and swallowing dysfunction, and later in the need for tracheostomy and percutaneous feeding tube placement. In the overall BRAT cohort,6 patients with PICA aneurysms underwent clip placement more often than coil embolization; those with VA aneurysms not at PICA underwent coil embolization more often. Of the 16 patients in this study, 9 underwent clip placement (mostly PICA aneurysms) and 7 underwent coil embolization (mostly non-PICA VA aneurysms).

This report inherently exhibits some of the limitations of a retrospective study, as not all of the data collected was part of a prospective randomized controlled trial, nor were some of the outcome measures discussed here decided upon prior to study initiation. Furthermore, it should be noted that certain patients were excluded in this study, including 1 patient who died before treatment, 2 patients without admission CT scans available for review, 2 patients with ICA aneurysms with a cavernous location, and 29 patients with nonaneurysmal SAH. Additionally, outcomes documented in this study cannot be generalized to the BRAT study: these are patients in whom additional data were analyzed retrospectively and the study does not involve the entire BRAT population. This vasospasm study includes those patients in whom vasospasm data were collected and who were selected at random, as has been previously reported.9

Conclusions

In this study, we found that there is some variability in the thickness of SAH relative to the site of the ruptured aneurysm, but the differences in clot thickness and BNI scale grade between different aneurysm locations overall were not statistically significant. Although it was evident in a small sample of 9 patients, aneurysms of the pericallosal artery, which rupture into the interhemispheric fissure, have a statistically significantly greater risk of symptomatic vasospasm despite having the lowest mean clot thickness. Additionally, there was a higher mean clot thickness in the 14 patients who were found to have infarct attributable to vasospasm (p = 0.004). The patients in this study were also found to have worse mean 1-year mRS outcome when they harbored aneurysms of the VA location (including the PICA); furthermore, patients had a lower proportion of good outcomes (mRS score 0–2) when aneurysms were located in the posterior circulation or pericallosal arteries.

Disclosure

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

Author contributions to the study and manuscript preparation include the following. Conception and design: all authors. Acquisition of data: all authors. Analysis and interpretation of data: Abla. Drafting the article: Abla. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Spetzler. Statistical analysis: Abla. Administrative/technical/material support: all authors. Study supervision: all authors.

This article contains some figures that are displayed in color online but in black-and-white in the print edition.

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  • 8

    Spetzler RMcDougall CAlbuquerque FZabramski JHills NPartovi S: The Barrow Ruptured Aneurysm Trial: 3-year results. Clinical article. J Neurosurg 119:1461572013

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  • 9

    Wilson DANakaji PAbla AAUschold TDFusco DJOppenlander ME: A simple and quantitative method to predict symptomatic vasospasm after subarachnoid hemorrhage based on computed tomography: beyond the Fisher scale. Neurosurgery 71:8698752012

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  • 10

    Yin LMa CYLi ZKWang DDBai CM: Predictors analysis of symptomatic cerebral vasospasm after subarachnoid hemorrhage. Acta Neurochir Suppl 110:1751782011

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Article Information

Address correspondence to: Robert F. Spetzler, M.D., c/o Neuroscience Publications, Barrow Neurological Institute, St. Joseph's Hospital and Medical Center, 350 W. Thomas Rd., Phoenix, AZ 85013. email: neuropub@dignityhealth.org.

Please include this information when citing this paper: published online December 6, 2013; DOI: 10.3171/2013.10.JNS13419.

© AANS, except where prohibited by US copyright law.

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Figures

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    Schematic representation of the stratification of ruptured aneurysms into 6 location zones for the purposes of analysis in this study. Aneurysm groups include pericallosal artery aneurysm, MCA aneurysms, upper posterior circulation aneurysms (BA), lower posterior circulation aneurysms (VA), intradural ICA aneurysms, and ACoA aneurysms. Used with permission from Dreamstime LLC.

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    Results from different analyses. A: Graph of aneurysm size stratified by BNI scale grade. There was no significant difference in the mean aneurysm size in any of the 5 groups of BNI scale grades (p = 0.92). B: Scatterplot of SAH maximum clot thickness (mm) versus ruptured aneurysm size (mm). There was a slight positive correlation (p = 0.1085). Solid line = trend line; dashed lines = 95% CIs. C: Graph of the presence of any symptomatic or radiographic vasospasm in each of the 6 aneurysm location groups. There was no overall statistically significant difference between groups (p = 0.70). Peri = pericallosal arteries. D: Graph of 1-year mean mRS outcomes for the VA aneurysm location compared with aneurysms of all other locations, showing that the higher mRS score at 1 year was statistically different (p = 0.0249). E: Graph of mRS outcomes at 1 year in each of the 6 aneurysm location groups shown as either good (mRS score 0–2) or poor outcome (mRS score 3–6; p = 0.098). F: Graph showing the good outcomes (mRS score 0–2) at 1 year were much less frequent in ruptured aneurysms of the posterior circulation and pericallosal aneurysm locations when compared with aneurysms of all other locations (p = 0.0044).

References

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    Spetzler RMcDougall CAlbuquerque FZabramski JHills NPartovi S: The Barrow Ruptured Aneurysm Trial: 3-year results. Clinical article. J Neurosurg 119:1461572013

    • Search Google Scholar
    • Export Citation
  • 9

    Wilson DANakaji PAbla AAUschold TDFusco DJOppenlander ME: A simple and quantitative method to predict symptomatic vasospasm after subarachnoid hemorrhage based on computed tomography: beyond the Fisher scale. Neurosurgery 71:8698752012

    • Search Google Scholar
    • Export Citation
  • 10

    Yin LMa CYLi ZKWang DDBai CM: Predictors analysis of symptomatic cerebral vasospasm after subarachnoid hemorrhage. Acta Neurochir Suppl 110:1751782011

    • Search Google Scholar
    • Export Citation

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