Journal of Neuroradiology (2010) 37, 284—291

ORIGINAL ARTICLE

Perfusion CT to quantify the cerebral vasospasm

following subarachnoid hemorrhage
Quantification du vasospasme cérébral après hémorragie
sous-arachnoïdienne par scanner de perfusion

Virginie Lefournier a,∗, Alexandre Krainik a, Benjamin Gory a,

Frédéric Derderian b, Pierre Bessou a, Bertrand Fauvage b,
Jean-François Le Bas a, Jean-François Payen b

a
Department of Neuroradiology, CHU Grenoble, University Joseph-Fourier, BP 217, 38043 Grenoble cedex 9, France
b
Department of Anesthesiology and Critical Care, CHU Grenoble, University Joseph-Fourier, Grenoble, France

Available online 22 April 2010

KEYWORDS Summary
Cerebral angiography; Background and purpose. — After subarachnoid hemorrhage (SAH), vasospasm is frequent and
Perfusion computed increases the risk of stroke and poor clinical outcome. The purpose of this study was to identify
tomography; the best perfusion parameters in perfusion-CT (PCT) able to predict vasospasm diagnosed by
Subarachnoid angiography after SAH.
hemorrhage; Methods. — Seventy-six patients with SAH were investigated by PCT and cerebral angiogra-
Vasospasm phy. Using regions of interest (ROI) on parametric maps of mean transit time (MTT), time to
peak (TTP), cerebral blood volume (CBV) and cerebral blood flow (CBF), PCT data were com-
pared to an arteriographic score in two categories (severe vasospasm: ≥ 50% and non-severe
vasospasm: < 50%) for each artery. Best PCT predictors of the arteriographic score were tested
using multiparametric logistic regression.
Results. — Among the 76 patients, PCT data were reliable in 65 patients. Twenty-seven patients
had a severe vasospasm. Logistic regression showed that MTT was the best predictor of the
arteriographic score. Using MTT, odds ratios having a vasospasm were superior to 3.1 and the
occurrence of a vasospasm was accurately predicted in 78.5 to 100%, depending on the artery
considered. However, no absolute value of the MTT could be identified to predict the occurrence
of vasospasm. In fact, abnormal values of MTT ranged from 123 to 221% (m = 146%) of the control
values.
Discussion and conclusions. — PCT may accurately identify severe vasospasm and might be used
as a convenient noninvasive imaging modality to monitor patients with SAH. When detected,
severe vasospasm could be confirmed and managed using angiography and endovascular treat-
ment, appropriately.
© 2010 Elsevier Masson SAS. All rights reserved.
∗ Corresponding author. Tel.: +33 4 76 76 54 99; fax: +33 4 76 76 58 92.
E-mail address: VLefournier@chu-grenoble.fr (V. Lefournier).

0150-9861/$ – see front matter © 2010 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.neurad.2010.03.003
Perfusion CT to quantify the cerebral vasospasm following subarachnoid hemorrhage
Introduction
Subarachnoid hemorrhage (SAH) is the cause of 5% of strokes
[1]. However, despite the relatively low incidence, the dis-
ability and loss of productive life years is comparable with
brain infarction or hemorrhage [2].
Case fatality rates vary between 32 and 67% in
population-based studies while 10—20% of all patients
become disabled mostly due to delayed cerebral ischemia
(DCI), related to vasospasm [3,4].
As prognosis could be improved by better neurointensive
care management, focus should be pointed on first, early
diagnostic of vasospasm, and second the risk evaluation of
DCI induced by the vasospasm.
First, to detect the presence of vasospasm and its extent,
imaging techniques such as transcranial Doppler (TCD) ultra-
sonography [5], computed tomography angiography (CTA),
and cerebral conventional angiography [1,6] can be used.
Conventional angiography remains the gold standard tech-
nique, but is associated with a risk of related stroke of 1 to
2% [7,8].
Second, perfusion computed tomography (PCT) may be
a useful tool to identify ischemia as DCI is preceded by a
decreased cerebral perfusion [9—12].
Among new neuroimaging modalities, PCT is now rou-
tinely performed in clinical practice, allowing rapid,
minimally invasive, and quantitative evaluation of per-
fusion by generating parametric maps of cerebral blood
flow (CBF), cerebral blood volume (CBV), mean transit
time (MTT) and time to peak (TTP). PCT has been proved
to be a useful diagnostic tool to investigate brain per-
fusion related to vasospasm [9,12—17]. Small populations
were studied and very few studies have been conducted
on the diagnostic value of PCT compared to angiography
[18—20].
PCT is probably a useful tool for predicting the risk of
cerebral ischemia and could be potentially used to manage
the patients with SAH.
Although severe vasospasm can decrease perfusion, it
may not result in DCI [10], however, at an early stage,
intensive care, both medical and endovascular therapy, has
to be done in some cases to prevent ischemia and poor
outcome.
Among the different PCT parameters, the goal of this
study was to identify the best perfusion parameters in PCT
corresponding to the vasospasm diagnosed by angiography
after SAH, in order to select patients needing intensive spe-
cial care to prevent DCI.
Patients and methods
Patients
We conducted a retrospective study on radiological data
of 76 patients admitted in our institution with acute
SAH.
All patients were investigated for vasospasm with serial
neurologic examinations and TCD studies. Clinical condition
was also recorded to know the hemodynamic and respira-
tory status which could interfere with brain perfusion data.
Imaging protocol was usually scheduled around the 7th day
285
postrupture, however, when the clinical findings were sus-
picious of early vasospasm, imaging exams were brought
forward.
When present on angiography, severe vasospasm (≥ 50%)
was treated with intra-arterial milrinone and/or endovascu-
lar balloon angioplasty, medical therapeutics (nimodipine,
hypertensive therapy, etc), and external ventricular
drainage when necessary.
Imaging protocol
The angiographies and PCT were performed within the first
10 days, after a mean delay of 7 days after SAH onset. Both
angiography and PCT were performed the same day, the
former following the latter, as a routine procedure. Angiog-
raphy was performed as the gold standard technique to
detect the presence and the extent of vasospasm, and PCT
allowed analyzing its potential effect on brain perfusion,
thus leading to specific and intensive treatment on selected
patients.
Conventional angiography
Three or 4-vessels angiography was performed immediately
after PCT via a transfemoral route under monitored sedation
or general anesthesia, using a biplane digital angiographic
unit (Neurostar® Siemens, Erlangen, Germany).
PCT
Using a 4-detector CT-scanner (Philips M × 8000), the proto-
col included a whole-brain unenhanced CT and a PCT at the
level of the basal ganglia above the eye lenses. PCT con-
sisted in four adjacent 5-mm-thick sections repeated every
2 s during 40 s, during a bolus of 40 mL of nonionic contrast
agent iobitridol (XENETIX 300® , 300 mg/mL of iodine) admin-
istered via a 20-gauge line into an antecubital vein by using
a power injector at 4 mL/sec. PCT was acquired at 90 kVp
and 120 mAs.
Data processing and analysis
Conventional angiography
Angiographic data were reviewed independently by two
interventional neuroradiologists (VL, PB), blinded to clini-
cal and PCT data. Angiographic vasospasm was considered
present when there was unequivocal narrowing of the
arterial vessel lumen by visual inspection. Vasospasm was
categorized as follows: none or moderate, 0 to 50% decrease
in vessel diameter on the angiograms and severe > 50%
decrease [9,10,21].
A simplified score for each artery was thus used to iden-
tify patients without vasospasm, with vasospasm below 50%,
and with vasospasm above 50%.
Each intracranial artery ACA, MCA, and PCA was scored
on both sides. The vessel segments scored on angiography
were proximal arterial segments A1 M1 and P1 with extend-
ing vasospasm on closer segments A2 M2 and P2, to match
the corresponding PCT data located at the level of the basal
ganglia.
To estimate the severity of vasospasm and to avoid
confusion with vessel hypoplasia, equivocal spastic arterial
286
segments were compared with the same ones on the angiog-
raphy performed at initial admission.
PCT
Unenhanced CT were reviewed for grading the SAH accord-
ing to the Fisher scale. PCT data were computed using
Brain Perfusion® , Philips Medical Systems giving MTT, TTP,
CBV, and CBF maps. For each parameter, quantitative val-
ues were extracted in cerebral arterial territories, by
drawing five regions of interest (ROIs) on each hemi-
sphere symmetrically located. The ROIs were defined in
the anterior cerebral artery (ACA), middle cerebral artery
(MCA), and posterior cerebral artery (PCA) territories, as
well as in the junctional territories, the anterior junc-
tional (AJ) between MCA and ACA territories, and posterior
junctional (PJ) territories, between MCA and PCA territo-
ries.
The overall effective dose equivalent for the CT protocol
was 1.84 mSv (1 mSv for unenhanced CT and 0.84 mSv for
PCT).
Statistical analysis
Statistical analyses were conducted in two steps. First, to
identify among the perfusion parameters measured across
ROIs those significantly different between arteriographic
score, ANOVA with repeated measures were performed,
post-hoc comparisons using Student T-tests and Mann-
Whitney tests were conducted when appropriate. Second, to
determine the reliability of PCT to predict the arteriographic
score, an unconditional logistic regression with stepwise
backward selection was used. The probability value for exit
in the logistic regression was set at 0.10. Adjusted odds
ratios with 95% confidence intervals were calculated. Sta-
tistical procedures were performed using SPSS 15.0® , with
significance set for p < 0.05.
Results
Patients population
Among the 76 patients initially managed, 11 patients were
excluded from further analysis because of unreliable PCT by
poor technique (mostly due to a poor bolus due to impaired
hemodynamic), leaving 65 patients for the study, 24 men
and 41 women with a median age of 50 years (range, 20—76
years). The CT-Fisher score was recorded as grade 4 (n = 45),
grade 3 (n = 17), and grade 2 (n = 3). WFNS scores were grade
1 (n = 26), grade 2 (n = 25); grade 3 (n = 1), grade 4 (n = 12),
grade 5 (n = 1).
A total of 61 ruptured aneurysms were identified: one
internal carotid artery bifurcation, two carotid ophthalmic
arteries, 18 anterior communicating arteries (Acoms), three
pericallosal arteries, 16 MCA bifurcations, 14 posterior com-
municating arteries (Pcoms), five basilar arteries tip, two
posterior inferior cerebellar arteries, including 14 patients
with multiple aneurysms (21%). The patients were treated
either by clipping (n = 10) or coiling (n = 50), one patient
died before aneurysmal treatment. Four patients had no
aneurysm detected by angiography.
V. Lefournier et al.
Imaging examinations
Angiographic sessions
Twenty-seven patients had a severe vasospasm (41.5%)
and 38 patients had non-severe vasospasm, among those
24 patients had no vasospasm. Notably, in the severe
vasospam group, aneurysmal rupture concerned 16 Acoms
aneurysms including one pericallosal, and 15 MCA bifurca-
tions, while in the non-severe vasospasm one, aneurysmal
rupture concerned 12 posterior circulation aneurysms. Arte-
rial segments demonstrating vasospasm were located on the
ACA (59.1%), on the MCA (31.8%), and on the PCA (9.1%)
(Table 1).
PCT sessions
In patients without any vasospasm (n = 24), mean val-
ues ± standard deviation across ROI were for CBV:
3.43 ± 0.08 ml/100 g, CBF: 43.34 ± 1.1 ml/100 g/min,
MTT: 4.86 ± 0.07 s, TTP: 14.45 ± 0.24 s. For each perfusion
parameter and for each ROI, these values were compared
to those measured in patients with a vasospasm below 50%
(n = 14). No difference could be detected between patients
without any vasospasm from those with a vasospasm below
50%. Thus, data from both groups were further pooled and
labeled as patients without severe vasospasm (< 50%) in
order to be compared to those from patients with severe
vasospasm (≥ 50%).
Tables 1 and 2, and Fig. 1 summarize perfusion parame-
ters across arterial territories. An illustrative case is shown
Fig. 2.
Comparison of PCT and angiography in the diagnosis of
vasospasm
Because of significant interaction between ‘‘arteriographic
score’’ and ‘‘ROI’’, post-hoc comparisons were conducted
for all parameters in all ROI. Perfusion parameters signifi-
cantly different between arteriographic score are listed in
Table 2. In case of vasospasm, between-subjects compar-
isons showed mainly significant increase of MTT in proper
arterial territory. Additionally, MTT in adjacent junctional
territories were also increased in case of vasospasm of
MCA. TTP and CBV were increased in case of vasospasm
of ACA and left MCA. CBF were identical, but in case of
vasospasm of the right PCA where a significant decrease was
observed.
These parameters were further used in binary logis-
tic regressions to predict the arteriographic score. Results
of regressions are summarized in Table 1. For all arterial
vasospasms but in left ACA, MTT measured in the proper
arterial territory was identified as the best predictor of the
arteriographic score. In left ACA vasospasm, MTT in the ante-
rior junctional territory was the best predictor. Compared to
the control values, MTT in severe vasospasm ranged from 123
to 217% (m = 149%). No clear-cut value could be identified to
simply predict the occurrence of vasospasm. At the arterial
level and using MTT, the odds ratios to have a vasospasm
ranged from 3.1 to > 106 . The occurrence of a vasospasm
was accurately predicted in 78.5 to 100%, depending on the
artery considered.
Perfusion CT to quantify the cerebral vasospasm following subarachnoid hemorrhage 287

Table 1 Occurrence of vasospasm and logistic regressions for each artery.

Artery* Vasospasm ≥ 50%a Significant predictors (odds ratio [CI95%]) False positive/False negative
mean ± sd (control values)b (accuracy)c

Right MCA n = 13 (20.0%) MTTMCA (7.1 [2.4—20.4]) n = 2/n = 6

5.8 ± 1.0 s (4.5 ± 0.6 s) (87.7%)
Left MCA n = 8 (12.3%) MTTMCA (4.3 [1.1—16.8]) n = 1/n = 2
6.6 ± 1.8 s (4.5 ± 0.6 s) (95.4%)
TTPPJ (2.2 [1.1—4.3])
18.7 ± 2.3 s (15.0 ± 1.5 s)
Right PCA n = 3 (4.6%) MTTPCA (> 106 [0— > 106 ]) n = 0/n = 0
11.3 ± 5.0 s (5.2 ± 0.6 s) (100%)
Left PCA n = 3 (4.6%) MTTPCA (21.4 [1.3—358.9]) n = 0/n = 1
7.9 ± 2.8 s (5.2 ± 0.6 s) (98.5%)
Right ACA n = 22 (33.8%) MTTACA (6.7 [2.3—19.2]) n = 4/n = 10
5.9 ± 1.2 s (4.8 ± 0.6 s) (78.5%)
Left ACA n = 17 (26.2%) MTTAJ (3.1 [1.6—6.3]) n = 1/n = 11
5.7 ± 1.3 s (4.6 ± 0.7 s) (81.5%)
MCA: middle cerebral artery; PCA: posterior cerebral artery; ACA: anterior cerebral artery; AJ: anterior junctional; PJ: posterior
junctional.
a Occurrence of severe vasospasm among the patient sample (n = 65).
b Significant predictors for vasospasm selected from regression analyses (odds ratio to have a vasospasm with a 95% confidence interval);

mean value of the predictor ± standard deviation when vasospasm is detected.

c Performances of the model to predict severe vasospasm using significant predictors, with accuracy defined by: [(true positive + true

negative)/(total number of patient)].

Discussion Screening for vasospasm

In the present study, we showed that using perfusion-CT
(PCT), an increase of the mean transit time (MTT), ranging
from 123 to 221% (m = 146%), was the most accurate param-
eter to predict severe vasospasm in 78.5 to 100%, depending
on the artery considered.
In clinical practice, vasospasm after SAH is routinely
assessed using serial clinical examinations, TCD, and angiog-
raphy within the first two week after the onset [1].
TCD is the most widely used to detect vasospasm noninva-
sively, although it has clear limitations. It has been reported

Table 2 Perfusion parameters significantly different across arteriographic score.

ROI MTT TTP CBV CBF

a d
Proper arterial territory rMCA (p < 0.001) lMCA (p < 0.001) lMCA (p = 0.01) rPCA (p = 0.01)
lMCA (<0.001) rACA (p = 0.003) rACA (p = 0.003)
rPCA (p < 0.001) lACA (p = 0.02) lACA (p = 0.02)
lPCA (p = 0.002)
rACA (p < 0.001)
lACA (p = 0.001)
Anterior junctionalb rMCA (p = 0.01) lMCA (p = 0.002) rMCA (p = 0.01)
lMCA (p = 0.001) rACA (p = 0.01) lMCA (p = 0.02)
rACA (p < 0.001) lACA (p = 0.03) rACA (p = 0.001)
lACA (p = 0.004) lACA (p = 0.01)
Posterior junctionalc rMCA (p = 0.02) rMCA (p = 0.02) rPCA (p = 0.01)
lMCA (p = 0.001) lMCA (p < 0.001)
r: right; l: left; MCA: middle cerebral artery; PCA: posterior cerebral artery; ACA: anterior cerebral artery.
a Significant differences between patients without severe vasospasm and patients with severe vasospasm in the proper arterial territory

of each artery.
b Parameters in anterior junctional ROI were computed for MCA and ACA.
c Parameters in posterior junctional ROI were computed for MCA and PCA.
d p-value of post-hoc comparisons.
288
Figure 1 Cerebral perfusion parameters for each cerebral artery. PCT parameters for each artery in proper and adjacent ROI
when severe vasospasm (red) and non-severe vasospasm (blue) (see Table 2 for significant comparisons).
as a highly specific but less sensitive test [22]. Moreover, in
patients with disturbed autoregulation after SAH, induced
hypertension could alter cerebral blood flow velocities [23].
Indeed, increased blood flow velocities measured by TCD
do not correlate with brain perfusion values and cannot
reliably distinguish between patients with vasospasm of var-
ious severity [24]. Finally, although TCD may detect severe
vasospasm, reliable conclusion could only be obtained for
MCA [25,26]. In our series, almost 60% of vasospasm occurred
on the ACA. Thus, the use of TCD as a screening method is
questionable.
In fact, many centers rely on cerebral angiography, an
invasive technique, for the diagnosis of vasospasm [1].
Although angiography is the gold standard imaging modality
to provide morphologic depiction of macroscopic vascula-
ture, it does not allow quantitative analysis on cerebral
perfusion.
Cerebral perfusion imaging
Cerebral perfusion abnormalities during vasospasm have
already been studied with single-photon emission CT
V. Lefournier et al.
(SPECT) [27,28], positron emission tomography (TEP)
[29,30], xenon enhanced CT [16,31], perfusion-weighted
MRI [32]. Diffusion-weighted MR imaging has also been
studied [33,34] and provided predictive markers of silent
ischemic lesions and/or progression toward symptomatic
ischemia in asymptomatic vasospasm [35].
However, those methods of investigation are not easily
performed in daily clinical practice in patients with SAH
requiring neurointensive care, long time procedure, and lim-
ited clinical access.
In such patients, CT is easy to perform in clinical prac-
tice, rapid, readily available, convenient, and a less invasive
alternative to catheter angiography. Combining cerebral
morphological examination, CT angiography and PCT, is a
major interest to manage vasospasm [16].
PCT has been validated to study brain perfusion [36,37].
Moreover, it was reported to be a useful diagnostic tool to
investigate vasospasm [9,13—20].
In our study, PCT values in patients with severe
vasospasm, low CBF, high CBV and prolonged MTT, are in
agreement with previous reports [13], especially concerning
MTT as being the most sensitive parameter [16,19,20,38].
Perfusion CT to quantify the cerebral vasospasm following subarachnoid hemorrhage 289

Figure 2 Illustrative case. A 46-year-old woman, WFNS 3 Fisher 4, presenting with a sylvian hematoma after SAH related to a
right MCA ruptured aneurysm (clipped). Angiography performed 10 days after SAH shows vasospasm > 50% on the right MCA (black
arrows). At PCT, MTT is increased in the right AJ (dotted arrow) (7.76 s), MCA (arrow) (8.87 s), and PJ (large arrow) territories
(8.47 s), compared to the opposite AJ (5.29 s), MCA (4.68 s), and PJ territories (5.44 s). CBF is decreased on the right side with
34.54 ml/100 g/mn in AJ, 40.89 in MCA, and 28.64 in PJ, while the values are normal in the opposite territories. CBV is only
increased in the right MCA with 6.05 ml/100 g.

Unreliable values may occur when vasospasm is severe,
as arterial input function cannot be properly selected, thus
leading to irrelevant data; however, when it happens, this
should definitely lead to angiography for prompt endovas-
cular treatment. In acute stroke patients, the selection of
different arterial input function has been demonstrated to
have no significant effect on PCT results for an individual
patient [39].
We acknowledge that the imaging technique has some
limitations. PCT consisted of four slices located at the level
of the basal ganglia with limited coverage (in this study only
2 cm). The brain perfusion analysis thus under diagnosed
potential delayed perfusion on distal territories. However,
currently, the use of increased detectors leads to expanded
volume coverage.
MTT
The most accurate PCT parameter to predict angiographic
vasospasm was MTT. No clear-cut value could be pointed out,
contrary to a previous study, which reported a threshold at
6.4 s as the most accurate parameter for the diagnosis of
angiographic vasospasm [19]. The lack of clear-cut value is
in agreement with other studies [13—16]. Some studies were
conducted with visual observation only [18,20].
Compared to the control values, MTT increased from
123 to 221% (m = 146%). An increase of the MTT over 20%
than the mean (corresponding to 120% of the control MTT)
has been shown to indicate the progression of cerebral
vasospasm, and patients with vasospasm-related infarcts
exhibited a MTT more than 47% greater than the mean
value [16]. In diffuse vasospasm, the junctional territories,
so-called watershed area, are the first involved. Although
higher MTT values were recorded in those areas, they were
non-significant, because of overlapping MTT values both in
the vasospasm and no-vasospasm groups, the latter showing
physiological prolonged values compared to proper territory.
Nevertheless, close attention should be paid to those crit-
ical border areas since they are the first to be affected in
diffuse vasospasm.
TTP
TTP values were not significantly higher in the vasospasm-
group. Indeed, TTP is not a discriminative parameter, as
being calculated directly without any arterial input refer-
ence, opposed to MTT. Consequently, TTP is very sensitive
to extracerebral or precerebral variables, such as cardiac
function, aortic and aortic arch branch vessel stenosis and
occlusion, or even variable position of the arm with vari-
able impingement effect on the intravenous line where the
iodinated contrast material bolus is injected for the PCT
examination.
CBV and CBF
Differences between CBV and CBF reflect various moments
in the timecourse of stroke and highlight vascular autoreg-
ulation. CBV was not discriminative between patients
with and without vasospasm, as reported previously
[38]. The overall higher CBV values in patients with
vasospasm were related to preservation of the autoregu-
lation, resulting in normal or increased CBV values [40].
Conversely, declining CBV indicates impaired autoregula-
tion. Thus, low CBV is only observed in areas of infarction,
which is seen in a minority of vasospasm cases at that
stage, making CBV inappropriate as a sensitive screen-
ing parameter for vasospasm. As previously reported [16],
higher MTT may be a prerequisite for cerebral vasospasm
290
while CBV and CBF should be considered simultane-
ously.
In the vasospasm-group, aneurysmal rupture mainly
occurred in Acoms and MCA arteries with subsequently more
focal vasospasm preferentially located within both ACA and
AJ territories, as well as left MCA territory, leading to signifi-
cant higher CBV results involving the whole anterior cerebral
circulation and similarly the left MCA territory.
Despite CBF seemed decreased in patients with
vasospasm, it was not significant because changes occurred
in patients who both later experienced delayed cerebral
ischemia or recovery from vasospasm without ischemia. Dif-
ferences in CBF is thus found depending on the level of
vasospasm which varies with the time course. Indeed, signif-
icance was reached in the right PCA territory in few patients
who presented delayed ischemia. Furthermore, as PCT was
performed at early stage of vasospasm, no major decreasing
CBF had yet occurred.
Angiographic vasospasm below 50% had no significant
effect on brain PCT in our study. Notably in normal con-
ditions, CBF values were usually overestimated in MCA
territory due to cortical vessels included in the ROIs improv-
ing the values of CBV, and consequently, the CBF ones.
Conversely, CBF was usually underestimated in ACA terri-
tory because of more inclusion of white matter than in MCA
territory, and white matter has actually been proved to show
significant lower CBF and CBV than grey matter [13].
Dosimetry
Low kVp and mAs were used for PCT acquisition [41] with
an effective dose (2.0—3.0 mSv) slightly higher than that
required for routine head CT (1.5—2.5 mSv). Irradiation
remained reasonable regarding conventional angiography.
Potential impact on vasospasm management
and conclusion
As cerebral vasospasm is one of the major complications of
SAH, and remains the main cause of delayed brain ischemia,
adequate therapy is mandatory.
Our study showed the accuracy of PCT to diagnose severe
vasospasm. To avoid performing angiography to patients
without vasospasm, and because of the relatively low speci-
ficity of MTT, combining PCT to CTA would be of main interest
[19,38] in reducing false-positive results. Then, one may sug-
gest that conventional angiography could be performed only
when vasospasm is suspected on clinical and CT data to dis-
cuss endovascular treatment. Confirmatory angiography for
vasospasm could be avoided if the PCT study is negative.
PCT should finally be proposed in all patients with SAH as an
accurate screening method to select those who may need
an active therapy.
Conflict of interest
None.
V. Lefournier et al.
Acknowledgments
We gratefully acknowledge Cedric Mendoza and Patrice
Jousse for their precious help in data collecting and editing
figures.
References
[1] Bederson JB, Connolly Jr ES, Batjer HH, Dacey RG, Dion JE,
Diringer MN, et al. Guidelines for the management of aneurys-
mal subarachnoid hemorrhage: a statement for healthcare
professionals from a special writing group of the Stroke Coun-
cil, American Heart Association. Stroke 2009;40(3):994—1025.
[2] Johnston SC, Selvin S, Gress DR. The burden, trends, and
demographics of mortality from subarachnoid hemorrhage.
Neurology 1998;50(5):1413—8.
[3] Hop JW, Rinkel GJ, Algra Avan Gijn J. Case-fatality rates and
functional outcome after subarachnoid hemorrhage: a system-
atic review. Stroke 1997;28(3):660—4.
[4] Stegmayr B, Eriksson M, Asplund K. Declining mortality from
subarachnoid hemorrhage: changes in incidence and case fatal-
ity from 1985 through 2000. Stroke 2004;35(9):2059—63.
[5] Carrera E, Schmidt JM, Oddo M, Fernandez L, Claassen J, Seder
D, et al. Transcranial Doppler for predicting delayed cere-
bral ischemia after subarachnoid hemorrhage. Neurosurgery
2009;65(2):316—23 [Discussion 323—24].
[6] Ferguson SD, Rosen DS, Bardo D, Macdonald RL. Arterial diame-
ters on catheter and computed tomographic angiography. Surg
Neurol 2009. Jul 14 [Epub Ahead of Print].
[7] Willinsky RA, Taylor SM, TerBrugge K, Farb RI, Tomlinson G,
Montanera W. Neurologic complications of cerebral angiogra-
phy: prospective analysis of 2899 procedures and review of the
literature. Radiology 2003;227(2):522—8.
[8] Cloft HJ, Joseph GJ, Dion JE. Risk of cerebral angiog-
raphy in patients with subarachnoid hemorrhage, cerebral
aneurysm, and arteriovenous malformation: a meta-analysis.
Stroke 1999;30(2):317—20.
[9] Dankbaar JW, de Rooij NK, Velthuis BK, Frijns CJ, Rinkel GJ, van
der Schaaf IC. Diagnosing delayed cerebral ischemia with dif-
ferent CT modalities in patients with subarachnoid hemorrhage
with clinical deterioration. Stroke 2009;40:3493—8.
[10] Dankbaar JW, Rijsdijk M, van der Schaaf IC, Velthuis BK, Wer-
mer MJ, Rinkel GJ. Relationship between vasospasm, cerebral
perfusion, and delayed cerebral ischemia after aneurysmal
subarachnoid hemorrhage. Neuroradiology 2009;51(12):813—9.
[11] Harrod CG, Bendok BR, Batjer HH. Prediction of cerebral
vasospasm in patients presenting with aneurysmal subarach-
noid hemorrhage: a review. Neurosurgery 2005;56(4):633—54
[Discussion 633—54].
[12] Pham M, Johnson A, Bartsch AJ, Lindner C, Mullges W, Roosen
K, et al. CT perfusion predicts secondary cerebral infarc-
tion after aneurysmal subarachnoid hemorrhage. Neurology
2007;69(8):762—5.
[13] Nabavi DG, LeBlanc LM, Baxter B, Lee DH, Fox AJ, Lownie SP,
et al. Monitoring cerebral perfusion after subarachnoid hem-
orrhage using CT. Neuroradiology 2001;43(1):7—16.
[14] Harrigan MR, Magnano CR, Guterman LR, Hopkins LN. Com-
puted tomographic perfusion in the management of aneurysmal
subarachnoid hemorrhage: new application of an existent tech-
nique. Neurosurgery 2005;56(2):304—17 [Discussion 304—17].
[15] van der Schaaf I, Wermer MJ, van der Graaf Y, Hoff RG, Rinkel
GJ, Velthuis BK. CT after subarachnoid hemorrhage: relation
of cerebral perfusion to delayed cerebral ischemia. Neurology
2006;66(10):1533—8.
[16] Kanazawa R, Kato M, Ishikawa K, Eguchi T, Teramoto A. Con-
venience of the computed tomography perfusion method for
Perfusion CT to quantify the cerebral vasospasm following subarachnoid hemorrhage
cerebral vasospasm detection after subarachnoid hemorrhage.
Surg Neurol 2007;67(6):604—11.
[17] Aralasmak A, Akyuz M, Ozkaynak C, Sindel T, Tuncer R.
CT angiography and perfusion imaging in patients with sub-
arachnoid hemorrhage: correlation of vasospasm to perfusion
abnormality. Neuroradiology 2009;51(2):85—93.
[18] Moftakhar R, Rowley HA, Turk A, Niemann DB, Kienitz BA, Van
Gomple J, et al. Utility of computed tomography perfusion in
detection of cerebral vasospasm in patients with subarachnoid
hemorrhage. Neurosurg Focus 2006;21(3):E6.
[19] Wintermark M, Ko NU, Smith WS, Liu S, Higashida RT, Dillon WP.
Vasospasm after subarachnoid hemorrhage: utility of perfusion
CT and CT angiography on diagnosis and management. AJNR
Am J Neuroradiol 2006;27(1):26—34.
[20] Binaghi S, Colleoni ML, Maeder P, Uske A, Regli L, Dehdashti
AR, et al. CT angiography and perfusion CT in cerebral
vasospasm after subarachnoid hemorrhage. AJNR Am J Neu-
roradiol 2007;28(4):750—8.
[21] Lodi CA, Ursino M. Hemodynamic effect of cerebral
vasospasm in humans: a modeling study. Ann Biomed Eng
1999;27(2):257—73.
[22] Sloan MA, Haley Jr EC, Kassell NF, Henry ML, Stewart SR,
Beskin RR, et al. Sensitivity and specificity of transcra-
nial Doppler ultrasonography in the diagnosis of vasospasm
following subarachnoid hemorrhage. Neurology 1989;39(11):
1514—8.
[23] Manno EM, Gress DR, Schwamm LH, Diringer MN, Ogilvy CS.
Effects of induced hypertension on transcranial Doppler ultra-
sound velocities in patients after subarachnoid hemorrhage.
Stroke 1998;29(2):422—8.
[24] Minhas PS, Menon DK, Smielewski P, Czosnyka M, Kirkpatrick PJ,
Clark JC, et al. Positron emission tomographic cerebral per-
fusion disturbances and transcranial Doppler findings among
patients with neurological deterioration after subarachnoid
hemorrhage. Neurosurgery 2003;52(5):1017—22 [Discussion
1022—4].
[25] Lysakowski C, Walder B, Costanza MC, Tramer MR. Transcra-
nial Doppler versus angiography in patients with vasospasm due
to a ruptured cerebral aneurysm: A systematic review. Stroke
2001;32(10):2292—8.
[26] Fontanella M, Valfre W, Benech F, Carlino C, Garbossa D, Ferrio
M, et al. Vasospasm after SAH due to aneurysm rupture of the
anterior circle of Willis: value of TCD monitoring. Neurol Res
2008;30(3):256—61.
[27] Lewis DH, Eskridge JM, Newell DW, Grady MS, Cohen WA,
Dalley RW, et al. Brain SPECT and the effect of cerebral angio-
plasty in delayed ischemia due to vasospasm. J Nucl Med
1992;33(10):1789—96.
[28] Powsner RA, O’Tuama LA, Jabre A, Melhem ER. SPECT imaging
in cerebral vasospasm following subarachnoid hemorrhage. J
Nucl Med 1998;39(5):765—9.
[29] Hosono M, Machida K, Matsui T, Honda N, Takahashi T, Dei S,
et al. Non-invasive quantitative monitoring of cerebral blood
291
flow in aneurysmal subarachnoid haemorrhage with 99 mTc-
ECD. Nucl Med Commun 2002;23(1):5—11.
[30] Sviri GE, Mesiwala AH, Lewis DH, Britz GW, Nemecek A, Newell
DW, et al. Dynamic perfusion computerized tomography in
cerebral vasospasm following aneurysmal subarachnoid hem-
orrhage: a comparison with technetium-99 m-labeled ethyl
cysteinate dimer-single-photon emission computerized tomog-
raphy. J Neurosurg 2006;104(3):404—10.
[31] Yonas H, Sekhar L, Johnson DW, Gur D. Determination of irre-
versible ischemia by xenon-enhanced computed tomographic
monitoring of cerebral blood flow in patients with symptomatic
vasospasm. Neurosurgery 1989;24(3):368—72.
[32] Rowe J, Blamire AM, Domingo Z, Moody V, Molyneux A,
Byrne J, et al. Discrepancies between cerebral perfusion
and metabolism after subarachnoid haemorrhage: a mag-
netic resonance approach. J Neurol Neurosurg Psychiatry
1998;64(1):98—103.
[33] Rordorf G, Koroshetz WJ, Copen WA, Gonzalez G, Yamada
K, Schaefer PW, et al. Diffusion- and perfusion-weighted
imaging in vasospasm after subarachnoid hemorrhage. Stroke
1999;30(3):599—605.
[34] Busch E, Beaulieu C, de Crespigny A, Moseley ME. Diffusion MR
imaging during acute subarachnoid hemorrhage in rats. Stroke
1998;29(10):2155—61.
[35] Condette-Auliac S, Bracard S, Anxionnat R, Schmitt E, Lacour
JC, Braun M, et al. Vasospasm after subarachnoid hem-
orrhage: interest in diffusion-weighted MR imaging. Stroke
2001;32(8):1818—24.
[36] Wintermark M, Maeder P, Thiran JP, Schnyder P, Meuli R. Quanti-
tative assessment of regional cerebral blood flows by perfusion
CT studies at low injection rates: a critical review of the under-
lying theoretical models. Eur Radiol 2001;11(7):1220—30.
[37] Nabavi DG, Cenic A, Craen RA, Gelb AW, Bennett JD,
Kozak R, et al. CT assessment of cerebral perfusion: exper-
imental validation and initial clinical experience. Radiology
1999;213(1):141—9.
[38] Wintermark M, Dillon WP, Smith WS, Lau BC, Chaudhary S,
Liu S, et al. Visual grading system for vasospasm based on
perfusion CT imaging: comparisons with conventional angiogra-
phy and quantitative perfusion CT. Cerebrovasc Dis 2008;26(2):
163—70.
[39] Wintermark M, Lau BC, Chien J, Arora S. The anterior cerebral
artery is an appropriate arterial input function for perfusion-
CT processing in patients with acute stroke. Neuroradiology
2008;50(3):227—36.
[40] Soehle M, Czosnyka M, Pickard JD, Kirkpatrick PJ. Contin-
uous assessment of cerebral autoregulation in subarachnoid
hemorrhage. Anesth Analg 2004;98(4):1133—9 [Table of
contents].
[41] Wintermark M, Maeder P, Verdun FR, Thiran JP, Valley JF,
Schnyder P, et al. Using 80 kVp versus 120 kVp in perfusion
CT measurement of regional cerebral blood flow. AJNR Am J
Neuroradiol 2000;21(10):1881—4.