Age-Associated Vasospasm in Aneurysmal Subarachnoid

Hemorrhage

Sushant P. Kale, MD, MPH,* Randall C. Edgell, MD,*† Amer Alshekhlee, MD,*
Afshin Borhani Haghighi, MD,*‡ Justin Sweeny, MD,† Jason Felton, MD,†
Jacob Kitchener, MD,* Nirav Vora, MD,* Bruce K. Bieneman, MD,x
Salvador Cruz-Flores, MD, MPH,* and Saleem Abdulrauf, MD†

The relationship between age and vasospasm caused by subarachnoid hemorrhage

(SAH) is controversial. We evaluated this relationship in a contemporary sample
from a single institution. In a retrospective study design, we included patients
with SAH caused by ruptured intracranial aneurysms. All patients underwent an
evaluation that included head imaging, cerebral angiography, and treatment for
the underlying aneurysm. Vasospasm was classified as absent, any vasospasm, or
symptomatic vasospasm. Age was classified into 2 categories with a cutoff of
50 years, and also was stratified by decade. All patients had received preventative
and therapeutic measures for vasospasm. Logistic regression analysis was used to
assess the association between age and the occurrence of vasospasm. A total of
108 patients were included in this analysis, 67 of whom were age $50 years. The
older patients had a higher incidence of vascular risk factors, and the younger pa-
tients had a higher incidence of smoking and illicit substance abuse. The mean
age of the patients with any vasospasm (n 5 41) was 48.51 6 11.23 years, compared
with 59.67 6 13.30 years in those without vasospasm (P , .0001). Adjusted analysis
found a greater risk of vasospasm in the younger patients compared with the older
patients (odds ratio, 5.83; 95% confidence interval, 2.41-14.12 for any vasospasm;
odds ratio, 2.66; 95% confidence interval, 1.008-7.052 for symptomatic vasospasm).
This risk of vasospasm decreased with advanced age (P , .0001). Our findings sug-
gest that patients age ,50 years are at 5-fold greater risk of any vasospasm com-
pared with older patients, and that age-adjusted prevention protocols may need
to be considered. Key Words: Cerebral angiography—spasm—prevention—
demographics.
Ó 2013 by National Stroke Association

Cerebral arterial vasospasm after subarachnoid hemor-

From the *Departments of Neurology and Psychiatry; rhage (SAH) is one of the major determinants of outcome.1,2
†Neurosurgery, Saint Louis University, St Louis, Missouri, MO; Arterial vasospasm has been associated with increased
‡Transgenic Technology Research Center, Shiraz University of Medi- mortality and morbidity rates and can lead to delayed
cal Sciences, Shiraz, Iran; and xDepartment of Radiology, Saint Louis
ischemic neurologic deficit in 17%-40% of patients
University, St Louis, Missouri, MO.
Received December 1, 2010; revision received April 28, 2011;
with aneurysmal SAH.3,4 The relationship between the
accepted May 21, 2011. incidence of vasospasm and age is controversial and has
Address correspondence to Amer Alshekhlee, MD, Saint Louis not been studied in the setting of modern neurocritical
University, Souers Stroke Institute, Department of Neurology and care and neuroendovascular techniques. The nature of
Psychiatry, 1438 S Grand Blvd, St Louis, MO 63104. E-mail:
this relationship becomes important when one considers
[email protected].
1052-3057/$ - see front matter
the risk associated with these techniques, especially in the
Ó 2013 by National Stroke Association elderly population. Although no studies have focused
doi:10.1016/j.jstrokecerebrovasdis.2011.05.024 specifically on the role of age in association with the

22 Journal of Stroke and Cerebrovascular Diseases, Vol. 22, No. 1 (January), 2013: pp 22-27
AGE AND VASOSPASM IN SUBARACHNOID HEMORRHAGE 23

incidence of vasospasm, older studies examining a variety serial transcranial Doppler ultrasonography studies at
of possible predictors reached varying conclusions about baseline and during the monitoring period to measure
the importance of this factor. Several studies found mean arterial velocity. A mean arterial velocity exceeding
a trend toward less vasospasm with advancing age.5,6 200 m/s or a rapid increase in velocity from baseline was
However, a post hoc analysis of a randomized trial of considered to indicate radiographic vasospasm. If vaso-
nicardipine in SAH found no relationship between age spasm was suspected clinically or based on the transcra-
and angiographic spasm and actually found an increased nial Doppler or computed tomography angiography
incidence of symptomatic vasospasm in the older data, then maximal medical therapy, including induced
population.7 These previous studies did not include the hypertension, was implemented. In addition, diagnostic
use of spasm-preventing medications, such as hydroxy- cerebral angiography was performed to evaluate the se-
3-methylglutaryl-coenzyme A (HMG-CoA) reductase in- verity and anatomy of the spastic arteries and to assess
hibitors, magnesium sulfate, and albumin, which in current the feasibility of local therapy. Interventional therapies
use or under study in many neurocritical care units. In for vasospasm included intra-arterial vasodilators (ie,
addition, these studies included the very early stages of en- local infusion of a calcium channel blocker into the spastic
dovascular treatment of vasospasm. Finally, these studies vessel) and/or angioplasty for a focal spastic lesion.
are limited by restrictive selection criteria in some cases
and by limited numbers in others. Independent and Outcome Variables
In the present study, we examined the association be-
Independent demographic variables included patient
tween age and the occurrence of vasospasm in a modern,
age, sex, and ethnicity (white, black, and other). Age
unselected population of consecutive patients with SAH
was stratified into 2 groups, young (age ,50 years) and
due to ruptured cerebral aneurysm. In addition, we eval-
old (age $50 years), as well as by decade of life. Vascular
uated age-associated outcomes, including the presence of
risk factors included diabetes, hypertension, dyslipide-
vasospasm, stroke, and modified Rankin scale (mRS) at
mia, coronary artery disease, smoking, family history of
hospital discharge.
cerebral aneurysm or SAH, and illicit substance abuse.
Outcome variables included the presence of vasospasm
Methods (any vasospasm or symptomatic vasospasm). Age also
Study Population and Protocol was assessed in association with mRS score at hospital
discharge. The mRS score ranges from 0 to 6, with 0 indi-
In a retrospective internal review board–approved
cating no symptoms and 6 indicating death. The score
single-center protocol, we collected information about pa-
was dichotomized as a favorable outcome (score of 0-2)
tients admitted with SAH due to ruptured cerebral aneu-
or unfavorable outcome (score of 3-6).11
rysm to Saint Louis University Hospital between July
2007 and July 2009. In addition to a clinical history consis-
Statistical Analysis
tent with SAH, the inclusion criteria included confirma-
tory imaging studies, such as computed tomography The Student t test and Wilcoxon rank-sum test were
scan or brain magnetic resonance imaging. The clinical used to compare the mean and median of continuous var-
and radiologic severity of SAH was based on the Hunt– iables. The c2 or Fisher exact test was used to compare cat-
Hess grade and Fisher grade, respectively. Patients with egories. The significance level was set a priori at P ,.05. A
SAH due to other causes, such as head trauma, vascular stepwise logistic multiple regression model was fitted to
malformation, and brain tumors, were excluded from determine the independent association of significant vari-
the study. ables (P , .20 on bivariate analysis) with the outcome of
All patients underwent diagnostic cerebral angiogra- any vasospasm. Another model was constructed using
phy to evaluate the anatomy of the aneurysm. Treatment the same variables for patients with symptomatic vaso-
for these aneurysms, such as coil embolization, surgical spasm only. Model goodness of fit was assessed using
clipping, or medical therapy alone, was ascertained. All the Hosmer–Lemeshow test. The Cochran–Armitage test
patients were monitored in the intensive care unit for at was used to evaluate linear trends of discrete variables
least 14 days. During the monitoring period, patients re- (age category stratified by decade in relation to vaso-
ceived prophylaxis and treatment for seizure and vaso- spasm and mRS score).
spasm. Our institutional protocol for vasospasm
prophylaxis included intravenous fluid and magnesium Results
infusion,8 along with HMG-CoA reductase inhibition
Cohort Demographics
(with statins)9 and nimodipine.10 The clinical diagnosis
of symptomatic vasospasm was based on the develop- Our study cohort comprised 108 patients admitted with
ment of focal neurologic deficits or a sudden decline in a diagnosis of SAH. Table 1 presents basic demographic
mental state without an identifiable cause other than con- data stratified by age. Forty-one patients were aged ,50
firmed vasospasm. In addition, all patients underwent years, with a mean age of 42.65 6 5.93 years; 67 patients
24 S.P. KALE ET AL.

Table 1. Demographic of the study cohort stratified by age

Age ,50 years (n 5 41) Age $50 years (n 5 67) P value

Age, years, mean 6 SD 42.65 6 5.93 63.25 6 10.79 ,.0001

Race, n (%) .41
White 25 (60.98) 48 (71.64)
Black 11 (26.83) 11 (16.42)
Others 5 (12.20) 8 (11.94)
Sex, n (%) .09
Male 8 (19.51) 23 (34.33)
Female 33 (80.49) 44 (65.67)
Vascular risk factors, n (%)
Diabetes 0 8 (11.94) .02
Hypertension 13 (31.71) 38 (56.70) .01
Coronary artery disease 0 4 (5.97) .11
Dyslipidemia 0 6 (8.95) .04
Substance abuse 7 (17.07) 4 (5.97) .06
Smoking 23 (56.10) 16 (23.88) .0007
Family history of 5 (12.20) 4 (5.97) .25
aneurysm/SAH
Hunt–Hess scale, n (%) .76
Grade 1 1 (2.44) 2 (2.99)
Grade 2 16 (39.02) 24 (35.82)
Grade 3 15 (36.59) 19 (28.36)
Grade 4 5 (12.20) 14 (20.90)
Grade 5 4 (9.76) 8 (11.94)
Fisher scale, n (%) .10
Grade 1 2 (4.88) 1 (1.49)
Grade 2 11 (26.83) 9 (13.43)
Grade 3 13 (31.71) 18 (26.87)
Grade 4 15 (36.59) 39 (58.21)
Treatment, n (%) .25
None 4 (9.76) 11 (16.42)
Surgical clipping 14 (34.15) 14 (20.90)
Endovascular coiling 23 (56.10) 42 (62.69)
Vasospasm, n (%)* .0005
None 16 (39.2) 51 (76.11)
Any vasospasm 25 (60.09) 16 (23.88)
Symptomatic vasospasm 12 (29.27) 9 (13.43)
mRS score, n (%)y .69
Favorable 15 (36.59) 22 (32.84)
Unfavorable 26 (63.41) 45 (67.16)

*Patients with symptomatic vasospasm are subset of those with any vasospasm; thus the number of these cells does not match the total number
of patients in each age category.
yThe mRS score was dichotomized as favorable if the scale was 0-2 and as unfavorable if the scale was 3-6.

were aged $50 years, with a mean age of 63.25 6 10.79 age groups (P 5 .76); whereas the majority of patients
years. There was no significant difference in ethnicity or were in Fisher grades 3 and 4 (P 5.10). Similar proportions
sex distribution in the 2 age categories (P . .05); however, of patients had received the treatments for aneurysm (P 5
predictably, the older patients had a higher incidence of .25). Compared with the old group category, the younger
vascular risk factors (hypertension, diabetes mellitus, population had higher incidence of any vasospasm
and dyslipidemia; P , .05), whereas the younger patients (60.09% v 23.88%) as well as symptomatic vasospasm
had higher prevalences of smoking (56.10% v 23.88%; (29.27% v 13.43%). mRS score at hospital discharge was es-
P 5 .0007) and illicit substance abuse (17.07% v 5.97%; sentially similar in the 2 age groups (P 5.69). Table 2 dem-
P 5 .06). The severity of SAH based on the clinical onstrates the same cohort stratified by the presence of any
(Hunt–Hess grade) and radiologic (Fisher grade) scales vasospasm. Forty one (37.9%) patients had any vaso-
was not different between the 2 age categories. The major- spasm; 21 (51.2%) of those were symptomatic. Patients
ity of patients were in Hunt-Hess grades 2 and 3 in both with any vasospasm were younger (48.51 6 11.23 versus
AGE AND VASOSPASM IN SUBARACHNOID HEMORRHAGE 25

Table 2. Bivariate analysis stratified by the presence of clinical vasospasm

No vasospasm (n 5 67) Any vasospasm (n 5 41) P value

Age, years, mean 6 SD 59.67 6 13.30 48.51 6 11.23 ,.0001

Age category, n (%) .003
Young (,50 years) 39 (58.2) 35 (85.4)
Old ($50 years) 28 (41.8) 6 (14.6)
Race, n (%) .46
White 43 (64.2) 30 (73.2)
Black 14 (20.9) 8 (19.5)
Others 10 (14.9) 3 (7.3)
Sex, n (%) .43
Male 21 (31.3) 10 (24.4)
Female 46 (68.7) 31 (75.6)
Vascular risk factors, n (%)
Diabetes 7 (10.5) 1 (2.4) .12
Hypertension 31 (46.3) 20 (48.8) .79
Coronary artery disease 3 (4.5) 1 (2.44) .58
Dyslipidemia 6 (8.96) 0 .04
Substance abuse 8 (11.9) 3 (7.3) .44
Smoking 22 (32.8) 17 (41.5) .36
Family history of 4 (5.97) 5 (12.2) .25
aneurysm/SAH
Hunt-Hess scale, n (%) .15
Grade 1 2 (2.99) 1 (2.44)
Grade 2 25 (37.31) 15 (36.59)
Grade 3 17 (25.37) 17 (41.46)
Grade 4 12 (17.91) 7 (17.07)
Grade 5 11 (16.42) 1 (2.44)
Fisher scale, n (%) .60
Grade 1 1 (1.49) 2 (4.88)
Grade 2 14 (20.90) 6 (14.63)
Grade 3 20 (29.85) 11 (26.83)
Grade 4 32 (47.76) 22 (53.66)
MRS score, n (%)* .66
Favorable 24 (35.82) 13 (31.71)
Unfavorable 43 (64.18) 28 (68.29)

*The mRS score was dichotomized as favorable if the scale was 0–2 and unfavorable if the scale was 3-6.

59.67 6 13.30; P ,.0001). Among those without evident va- 5.83; 95% confidence interval [CI], 2.41-14.12). Younger
sospasm, 39/67 (58.2%) were younger than 50 and 28/67 age also predicted symptomatic vasospasm (OR, 2.66;
(41.8%) were older than 50. Among the vasospasm group, 95% CI, 1.008-7.052) compared to the older population
35/41 (85.4%) were age ,50 years, and 6/41 (14.3%) were (Table 3). None of the basic demographic data or vascular
age $50 years. Other than age, none of the basic demo- risk factors was associated with vasospasm. Three patients
graphics (sex and ethnicity), or the vascular risk factors in the younger age group had sustained stroke with resid-
were significantly different between the groups (P ..05). ual deficit as a result of vasospasm, compared with none in
Six patients without vasospasm had dyslipidemia com- the older age group. Further trend analysis of age catego-
pared to none in the vasospasm group (P 5 .04). The rized by decade of life (Table 4) found a clear decline in
mRS score on hospital discharge was similar among those the risk of any vasospasm with advanced age (P , .0001).
with and without vasospasm (P 5 .66). Among those A similar decline in the risk of symptomatic vasospasm
treated with surgical clipping, 12/28 (42.86%) had vaso- with advancing age was noted (P 5.04). Only 1 patient un-
spasm, compared to 28/65 (43.08%) among those treated der age 30 had any vasospasm while hospitalized; how-
with coil embolization (P 5 .98). ever, all patients under age 40 (n 5 26) had evidence of
clinical or radiologic vasospasm. The majority of patients
in both age categories had an unfavorable outcome
Outcomes
(67.2% in those aged ,50 and 63.4% in those age $50).
Age was the only predictor for any vasospasm on mul- The overall distribution of mRS scores was similar in the
tivariate logistic regression analysis (odds ratio [OR], 2 age groups (Fig 1), including mortality rates (19.5% in
26 S.P. KALE ET AL.

Table 3. Multivariate logistic regression analysis for outcome of symptomatic vasospasm and asymptomatic vasospasm

Odds ratio Goodness of fit

(95% confidence interval) P value (P value)*

Any vasospasm, young 5.83 (2.41-14.12) ,.0001 .70

(reference, old)
Symptomatic vasospasm, 2.66 (1.008-7.052) .04 .62
young (reference, old)

*The Hosmer-Lemeshow test was used for the goodness of fit of the model.

the younger patients, 19.4% in the older patients). Unfa- in the pathogenesis of atherosclerosis and subsequent
vorable outcome stratified by decade of age suggest that arterial stiffness, its association with vasospasm has not
greater disability is more likely to occur with advanced been determined. The cerebral vessels of elderly patients
age, but with no clear trend (P 5 .15). may be less responsive to oxygen-reactive species as well
as to endothelin, the biology of which has been implicated
in chronic hypertension.12 Endothelin receptor antagonists
Discussion
may prevent the occurrence of vasospasm associated with
Our findings support the inverse relationship between SAH due to ruptured cerebral aneurysm, even though they
patient age and the incidence of vasospasm.5,6 Although fail to improve clinical outcomes.13,14 Interestingly,
previous studies have evaluated many variables affecting smoking (more prevalent in those aged ,50 years in our
the incidence of vasospasm, this study is the first to cohort) increases the production of endothelin and
specifically explore the hypothesis that the incidence of reduces the production and bioavailability of nitric oxide,
vasospasm in SAH decreases with advancing age. Indeed, factors associated with vasospasm in the younger
we found a higher incidence of vasospasm (60.09%) in population.15 Despite this plausible biological evidence,
patients aged ,50 years. Further age stratification by our regression analysis failed to show any association be-
decade suggests that the highest incidence of vasospasm tween smoking or chronic hypertension with vasospasm
occurred in those age ,50. Our sample included only 1 in SAH. Finally, the abuse of illicit substances, especially co-
patient younger than 30 who experienced asymptomatic caine, has been associated with an increased risk of SAH;
vasospasm. SAH in general and symptomatic vasospasm those patients are at a 2.8-fold increase risk of vasospasm.16
in particular are associated with an unfavorable This effect was not seen in our cohort, perhaps due to the
prognosis.7 Although the incidence of vasospasm de- small number of patients abusing illegal substances.
creased with advancing age in our cohort, stratification of The use of preventative therapies, such as magnesium sul-
age by decade suggests a nonsignificant trend in outcome fate, HMG-CoA reductase inhibitors, and albumin, was
as assessed by mRS score at hospital discharge. a part of our institutional protocol, even though these agents
The pathophysiological explanation for the decreasing are still considered investigational. In addition, the use of
incidence of vasospasm with age is not well understood. coil embolization and endovascular management of vaso-
It is plausible that the higher prevalence and longer dura- spasm has increased dramatically over the last decade.17
tion of vascular risk factors in the older population may The addition of these treatment modalities might provide
play a role. Although chronic hypertension is implicated a benefit for patients at high risk for vasospasm; however,

Table 4. Trends for vasospasm and mRS score stratified by age

Age, years (n 5 108) Any vasospasm, n (%) Symptomatic vasospasm, n (%) Unfavorable mRS score, n (%)*

21-30 (n 5 1) 1 (100.0) 0 0
31-40 (n 5 15) 10 (66.6) 5 (33.3) 9 (60.0)
41-50 (n 5 25) 14 (56.0) 7 (28.0) 17 (68.0)
51-60 (n 5 35) 11 (31.4) 6 (17.1) 22 (62.8)
61-70 (n 5 14) 2 (14.2) 1 (7.1) 8 (57.1)
71-80 (n 5 13) 3 (23.1) 2 (15.4) 10 (76.9)
.80 (n 5 5) 0 0 5 (100.0)
P value for trendy ,.0001 .04 .15

*Unfavorable mRS score if the scale was 3-6, with 6 indicating death.
yThe Cochran–Armitage test was used for trend analysis.
AGE AND VASOSPASM IN SUBARACHNOID HEMORRHAGE 27

4. Haley EC Jr, Kassell NF, Torner JC, et al. A randomized

trial of two doses of nicardipine in aneurysmal subarach-
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with 0 indicating no symptoms and 6 indicating death. The scale was dichot- do older patients fare worse? J Neurosurg 1996;
omized as a favorable outcome (a score of 0-2) or unfavorable outcome (a score 85:410-418.
of 3-6), with 6 being death. †Percentages in bracket indicate the proportion of 8. Zhao XD, Zhou YT, Zhang X, et al. A meta-analysis of
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groups (P 5 .69). fate. J Clin Neurosci 2009;16:1394-1397.
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in the elderly population, the risk–benefit ratio must be con- statin treatment on vasospasm, delayed cerebral ische-
sidered carefully. The components of so-called ‘‘triple-H’’ mia, and functional outcome in patients with aneurysmal
subarachnoid hemorrhage: A systematic review and
therapy (hemodilution, hypertension, and hypervolemia) meta-analysis update. Stroke 2010;41:e47-e52.
may be associated with neurolologic and medical 10. Deshaies EM, Boulos AS, Drazin D, et al. Evidence-based
complications, such as worsening cerebral edema and pharmacotherapy for cerebral vasospasm. Neurol Res
hemorrhagic infarction, pulmonary edema, dilutional 2009;31:615-620.
hyponatremia, and myocardial infarction.18,19 These 11. Molyneux A, Kerr R, Stratton I, et al. International Sub-
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