Download Assessment of the Contribution of the External Carotid

Assessment of the Contribution of the External Carotid
Artery to Brain Perfusion in Patients With Internal
Carotid Artery Occlusion
Peter Jan van Laar, MD, PhD; Jeroen van der Grond, PhD; Jochem P. Bremmer, MD;
Catharina J.M. Klijn, MD, PhD; Jeroen Hendrikse, MD, PhD
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Background and Purpose—The purpose of this study was to prospectively investigate the contribution of the ipsilateral
external carotid artery (ECA) to cerebral perfusion in patients with internal carotid artery occlusion.
Methods—Institutional Review Board approval and informed consent were obtained. Thirty functionally independent
patients (24 men, 6 women; mean age, 63 years) with an angiographically proven unilateral internal carotid artery
occlusion and transient or minor disabling ischemic attacks ipsilateral to the side of the internal carotid artery occlusion
were included. Grading of ECA collateral flow was performed with intraarterial digital subtraction angiography. The
contribution of the ECA to regional cerebral blood flow was assessed with selective arterial spin labeling MRI.
Differences in regional cerebral blood flow were analyzed with Student t test.
Results—Twenty percent of the patients had ECA Grade 0 collateral flow (no filling of ophthalmic artery), 20% Grade 1
(filling of carotid siphon), and 60% Grade 2 (filling of anterior and/or middle cerebral artery) as demonstrated on digital
subtraction angiography. Although in the Grade 1 group, the ECA supplied a smaller region of the brain compared with
the Grade 2 group, the mean regional cerebral blood flow of the perfusion territory supplied by the ECA is similar
(P⫽0.70) in the Grade 1 group (mean⫾SD 57⫾16 mL/min/100 g) and the Grade 2 group (60⫾12 mL/min/100g).
Conclusion—In patients with symptomatic internal carotid artery occlusion, focal brain regions may strongly depend on the
contribution to cerebral perfusion of the ECA ipsilateral to the side of the internal carotid artery occlusion, even in patients
with limited ECA collateral supply as demonstrated on digital subtraction angiography. (Stroke. 2008;39:3003-3008.)
Key Words: carotid artery occlusion 䡲 cerebral hemodynamics
䡲 collateral circulation 䡲 magnetic resonance imaging
I
n patients with symptomatic internal carotid artery (ICA)
occlusion, collateral pathways are used to compensate for
diminished blood flow.1 These collaterals include the connections through the circle of Willis, the connections arising
from leptomeningeal anastomoses on the brain surface, and
the extracranial-to-intracranial collaterals, most often through
the ipsilateral external carotid (ECA) artery and the ophthalmic artery.2
The results of several studies in patients with occlusive
disease of the ICA have demonstrated that presence of ECA
collateral flow may prevent the development of failure of the
brain’s blood supply.3,4 In contrast, findings from one study
showed no beneficial effect of ECA collateral flow,5 and
findings from other studies showed that the presence of
collateral circulation through the ECA was associated with
hemodynamic impairment.6,7
The actual contribution of the individual collateral pathways is difficult to assess and to quantify. Magnetic reso-
nance angiography and transcranial Doppler may show the
presence of collateral flow, but they do not show the actual
contribution to brain perfusion.3– 6 Intraarterial digital subtraction angiography (DSA) offers more information and
shows also the distal arteries of the collateral pathway.7–9
However, to visualize all the collateral pathways, this technique requires an invasive, selective 3-vessel approach (ie,
both the common carotid arteries, and the vertebrobasilar
arteries [VBA]).
Recently, selective arterial spin labeling (ASL) MRI was
introduced as a method to assess the contribution of individual arteries to the perfusion of the brain.10 The aim of the
present study was to investigate the contribution of the
ipsilateral ECA to cerebral perfusion in patients with ICA
occlusion. We hypothesized that patients with higher grades
of ECA collateral flow on DSA show a larger ECA flow
territory and a reduced regional cerebral blood flow (rCBF)
with selective ASL MRI.
Received January 6, 2008; final revision received March 26, 2008; accepted March 27, 2008.
From the Departments of Radiology (P.J.v.L, J.v.d.G., J.H.) and Neurology (J.P.B., C.J.M.K.), University Medical Center Utrecht, Utrecht, The
Netherlands; the Department of Radiology (P.J.v.L.), Meander Medical Center Amersfoort, Amersfoort, The Netherlands; and the Department of
Radiology (J.v.d.G.), Leiden University Medical Center, Leiden, The Netherlands.
Correspondence to Peter Jan van Laar, MD, PhD, University Medical Center Utrecht, Department of Radiology, PO Box 85500, 3508 GA Utrecht, The
Netherlands. E-mail [email protected]
© 2008 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.108.514265
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Figure 1. Intracranial anteroposterior
(AP) and lateral (LAT) views of selective
angiograms of the common carotid
artery on the side of the ICA occlusion in
3 patients, demonstrating the degree of
collateral flow from the ipsilateral ECA
on the side of the ICA occlusion. ECA
Grade 0, no filling of ophthalmic artery;
ECA Grade 1, retrograde flow in ophthalmic artery with filling of carotid siphon;
ECA Grade 2, to MCA and/or ACA.
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Methods
The ethics committee of our institution approved the study protocol,
and written informed consent was obtained from all participants.
Patients
Thirty consecutive patients (24 men and 6 women; mean age, 63
years ⫾10 SD) who met our study criteria were included between
June 2004 and December 2006. All patients had transient or minor
disabling ischemic attacks (modified Rankin score 0 to 3) within 6
months before referral ipsilateral to the side of the ICA occlusion.
Patients who had experienced a severe stroke in the past that caused
major disability (modified Rankin score 3 to 5) were not included.11
All patients had an angiographically proven unilateral proximal
ICA occlusion.
Intraarterial Digital Substraction Angiography
To assess the presence of ECA collateral pathways, biplane (anteroposterior and lateral) DSA intracranial views were examined. After
a selective common carotid artery injection on the side of the ICA
occlusion, ECA collaterals were recognized on the angiogram by the
contrast filling of the ECA, ophthalmic artery, carotid siphon, middle
cerebral artery (MCA), or anterior cerebral artery (ACA). The
appearance of the ECA collaterals was then graded on a 3-point
scale9: 0, slight collateral distribution, often with dilution (eg, no
filling of ophthalmic artery); 1, small but definite collateral supply
(eg, retrograde flow in ophthalmic artery with filling of carotid
siphon); or 2, full collateral filling (eg, to MCA and/or ACA; Figure
1). Grading of ECA obstruction was performed with DSA. The mean
degree of stenosis in the ipsilateral ECA was 23% (⫾31% SD). Four
(13%) of 30 patients had an ECA stenosis of 70% or greater.
MRI
MRI was performed using a 1.5-T or 3.0-T whole-body system
(Philips Medical Systems, Best, The Netherlands). Thirteen patients
were scanned on 1.5 T and 17 patients on 3.0 T. Perfusion territory
imaging of the ipsilateral ECA and the other brain feeding arteries
(contralateral ICA and VBA) was achieved by using a regional
perfusion imaging sequence,10 which is based on a pulsed ASL
transfer insensitive labeling technique.12–14 An optimized sequence
has been used for selective ASL at 3.0 T, which has shown to have
a high labeling efficiency at 3.0 T.15 With regional perfusion
imaging, selective labeling is obtained by using the sharp labeling
profiles of the transfer insensitive labeling technique pulses16 and by
interactively planning the spatially selective inversion slabs to invert
the targeted artery only. Subsequent to the labeling pulses, 3 90°
saturation pulses followed by strong dephasing gradients were
applied on the imaging sections to remove the direct effect of the
labeling pulses. Each saturation pulse was followed by a series of
strong dephasing gradients in all 3 directions to spoil all remaining
transverse magnetization. In the present study, no vascular crushers
were used. Planning of the selective labeling volume was performed
on the basis of transversal source images of the time-of-flight MR
angiography of the brain feeding arteries (Figure 2). Five imaging
sections were planned parallel to the orbitomeatal angle and were
acquired in the cranial to caudal direction with a delay time of 25 ms
between sections. The labeling delay time (inversion time) was set at
1600 ms. For image acquisition, a single-shot echoplanar imaging
readout was used. Other MR parameters for regional perfusion
imaging were 3000/5.6 repetition time ms/echo time ms (1.5 T);
4000/23 repetition time ms/echo time ms (3.0 T); 62% partial Fourier
acquisition; 8-mm slice thickness; 1-mm section gap; 240⫻240-mm
field of view; 64⫻64 matrix; zero filling to a 128⫻128 matrix; 30
signals acquired at 1.5 T and 20 signals acquired at 3.0 T; regional
perfusion imaging scan time 3 minutes per territory at 1.5 T; and 2
minutes 40 seconds per territory at 3.0 T. Four ASL acquisitions
were performed for each patient: selective ASL measurements of the
ECA, the contralateral ICA, and the VBA and an acquisition at
multiple TI to quantify the rCBF of the ECA.
Figure 2. Planning of the selective arterial spin labeling MRI slabs in a patient
with a left-sided ICA occlusion for perfusion territory imaging of the left ECA,
right nonoccluded ICA, and VBA. The
labeling slabs are planned based on the
transverse source images of the time-offlight MR angiography of the brainfeeding arteries (TR, 23; TE, 3.5; 18° flip
angle).
van Laar et al
Contribution of ECA to Brain Perfusion
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Figure 3. Transverse segmented perfusion territory maps of the ECA ipsilateral
to the ICA occlusion, the nonoccluded
contralateral unilateral ICA, and VBA in
all patients with ICA occlusion. Colors
correspond to the color bar, which indicates the percentage of patients who
demonstrated perfusion in that region of
the brain: 100% (red color) indicates that
all subjects demonstrated perfusion in
that region; 50% (green color) indicates
that half of the subjects demonstrated
perfusion in that region; 3.3% (violet
color) indicates that one subject demonstrated perfusion in that region; 0% (no
overlaid color) indicates the region of the
brain that none of the subjects demonstrated perfusion.
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To quantify the contribution of the ipsilateral ECA to the rCBF (in
milliliters per minute per 100 g tissue), a multi-inversion time
selective ASL sequence was used. Five imaging sections were
planned parallel to the orbitomeatal angle. For selective ASL at
multiple inversion times, the detection part of the regional perfusion
imaging pulse sequence10 was replaced by a series of 13 excitation
pulses (flip angles of 35°) with increasing delay times from 200 ms
to 2600 ms with a constant interval of 200 ms followed by
single-shot gradient echoplanar imaging readout.17
rate of blood)⫽0.71 s⫺1 (1.5 T) or 0.61 s⫺1 (3.0 T); ␭ (brain/blood
partition coefficient of water)⫽0.9 mL/g.10,15,22
Statistical Analysis
Difference in mean rCBF between the Grade 1 group and the Grade
2 group was analyzed with Student t test. A probability value of
⬍0.05 was considered to indicate a significant difference. For
statistical analysis, SPSS for Windows, version 10.0.7 was used.
Results
Data Processing
The postprocessing method (segmentation and registration) has been
described and illustrated in detail previously.18 In brief, data were
analyzed using MATLAB (Mathworks, Natick, Mass). Perfusionweighted images of the flow territories of the selectively labeled
arteries were obtained by subtraction of the labeled from the control
images. After visual evaluation of the resulting subtracted images,
one of the authors (P.J.v.L.; 5 years of experience) manually outlined
and filled the perfusion images. A single experienced user performed
the analysis of the extent of the flow territories, thus eliminating any
interobserver variability. The segmented images were registered on a
standard brain (SPM, Wellcome Department of Cognitive Neurology, Institute of Neurology, London, UK).19 Absence of ECA flow
was assessed by the absence of perfusion signal on the selective ASL
images of the ECA. This process was performed for all flow
territories of all subjects. Because no significant differences in
perfusion territories were found between patients with left-sided ICA
occlusion and those with right-sided ICA occlusion, all patients with
ICA occlusions were pooled. The perfusion territory maps of patients
with left-sided ICA occlusion were mirrored in the midline, whereas
perfusion territory maps of patients with right-sided symptomatic
ICA occlusion remained unchanged. To create groups, the flow
territories (registered on the standard brain) from the individual
subjects were combined. These combined flow territory maps were
color-coded and expressed as probability maps: 100% (region of the
brain with red color) indicates that all subjects demonstrated perfusion in that region; and 0% (region of the brain without overlaid
color) indicates the region of the brain that no subject demonstrated
perfusion.
For rCBF quantification, one author (P.J.v.L.) selected regionsof-interest that enclosed the brain perfusion territory of the ECA
closely. For region-of-interest selection in patients with ECA Grade
0 collateral flow (eg, no filling of ophthalmic artery on DSA), the
entire brain area was used as a “control perfusion mask” to extract
rCBF number from the whole brain. For the drawing of the
regions-of-interest on the selective ASL images, these images have
been windowed at the same level. Quantification was performed on
the basis of established kinetic perfusion models20,21 with the
following values for the physical constants: ␣ (efficiency of the
inversions pulse)⫽1.0; R1 (longitudinal relaxation rate of tissue)⫽1.0 s⫺1 (1.5 T) or 1.2 s⫺1 (3.0 T); R1a (longitudinal relaxation
Perfusion Territories
The segmented perfusion territory maps of the ECA, the
contralateral ICA, and the VBA for all patients with unilateral
ICA occlusion (n⫽30) showed a relatively large variation in
perfusion territories (Figure 3).
An example of representative images of a 62-year-old
patient with transient ischemic attacks associated with a
right-sided ICA occlusion shows the ECA collateral pathways on DSA and the ASL MRI perfusion territories of the
ECA on the side of the occlusion, the left-sided nonoccluded
ICA, and the VBA (Figure 4).
Six (20%) of 30 patients with unilateral ICA occlusion had
ECA Grade 0 collateral flow, 6 (20%) patients had ECA
Grade 1 collateral flow, and 18 (60%) patients had ECA
Grade 2 collateral flow as demonstrated on DSA. Subcategories of patients with ECA Grade 0, Grade 1, and Grade 2
showed considerably lower variation in perfusion territories
of the ECA ipsilateral to the side of the ICA occlusion
compared with the group as a whole (Figure 5). The perfusion
territory maps in patients with ECA Grade 0 demonstrated
that the ECA in these patients did not contribute to the
cerebral perfusion. In patients with Grade 1, the ECA
supplied a focal region of the ipsilateral MCA territory, and in
patients with Grade 2, the ECA supplied the MCA and, to a
lesser extent, the ACA perfusion territory ipsilateral to the
side of the occlusion.
Regional Cerebral Blood Flow
Although the brain region that is supplied by the ECA is
larger in the Grade 2 group than in the Grade 1 group, the
mean rCBF of the brain perfusion territory supplied by the
ECA showed no significant difference (P⫽0.70) in rCBF
between the Grade 1 group (57⫾16 mL/min/100 g) and the
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Figure 4. Top, Intracranial anteroposterior (AP) and lateral (LAT) views of the
selective angiogram of the common
carotid artery on the side of the ICA
occlusion in a 62-year-old patient with
transient ischemic attacks associated
with a right-sided ICA occlusion demonstrating Grade 2 ECA collateral flow: filling to MCA and ACA. Bottom, Transverse arterial spin labeling MRI perfusion
territory images in the same patient (TR,
3000; TE, 5.6; TI, 1600 ms, 90° flip
angle). When the ECA on the side of the
ICA occlusion was labeled selectively,
perfusion signal was observed in the
right MCA territory. When labeling the
left-sided nonoccluded ICA, signal was
detected in the left MCA territory and in
both the left and right ACA territories.
The perfusion territory of the VBA supplied the posterior part of the imaging
slices and extended into the MCA territory ipsilateral to the side of the ICA
occlusion. Red line, outline of segmented ECA perfusion territory images.
Grade 2 group (60⫾12 mL/min/100 g). The mean rCBF of
the entire brain in the ECA Grade 0 group was 5⫾13
mL/min/100 g.
Discussion
Our study in patients with symptomatic unilateral ICA
occlusion demonstrated that although the brain region that is
supplied by the ECA is larger in the Grade 2 group than in the
Grade 1 group, the mean rCBF of the perfusion territory
supplied by the ECA is not significantly different between
both groups.
The ipsilateral ECA can be an important extracranial-tointracranial collateral in patients with symptomatic ICA
occlusion.2 In our study, 24 (80%) of 30 patients with
unilateral ICA occlusion had retrograde, collateral flow in the
ophthalmic artery ipsilateral to the side of the occlusion on
DSA. In previous studies of patients with unilateral ICA
occlusion, researchers demonstrated that the percentage of
Figure 5. Transverse segmented perfusion territory maps of the ECA in
patients with unilateral ICA occlusion.
Colors correspond to the color bar,
which indicates the percentage of
patients who demonstrated perfusion in
that region of the brain.
van Laar et al
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patients with retrograde flow in the ophthalmic artery varied
between 36% and 89%.3,5,7,8,23 The inclusion of patients who
had no major neurological deficit may explain the relative
high prevalence of collateral flow in the ophthalmic artery in
our study. Thus far, the extent of the contribution of the
ipsilateral ECA to cerebral perfusion in patients with symptomatic ICA occlusion has remained unclear. The presence of
collateral flow through the ECA as assessed with transcranial
Doppler has been associated with relatively preserved cerebral hemodynamics.3,4 Other studies have found contradicting
results and showed that the presence of ECA collateral
pathways assessed with DSA or transcranial Doppler was
associated with impaired cerebral hemodynamic measurements.6,7 In these studies, collateral supply through the ECA
was only assessed as present or absent and could not be
quantified as is possible by the method we have presented in
this study. This may explain the discrepant findings of either
favorable or impaired cerebral hemodynamics with presence
of ECA collateral flow.
The results of previous postmortem and in vivo studies
have shown large variability in perfusion territories of the
major brain-feeding arteries (ICA and VBA) in healthy
subjects and in patients with carotid occlusive disease.18,24,25
In this light, it is not surprising that our results show a
considerable variation in individual ECA territorial distribution. Because we examined patients with ICA occlusion who
had no major neurological deficit, collateral pathways are
expected to exist in these patients to reroute blood to
compensate for absent ipsilateral ICA flow, thereby resulting
in altered territorial supply. To our knowledge, our study is
the first to actually show the extent of the altered ECA
perfusion territories in patients with ICA occlusion.
In the past decade, numerous selective ASL methods have
been developed to image the perfusion territories of individual brain-feeding arteries. Selective ASL techniques have
been introduced to assess the perfusion territories of the
individual common carotid arteries,26 –28 the individual ICAs,
and the VBA.10,29 –32 Although selective ASL could potentially detect certain boundary areas that are shared between
the ECA and the other arteries, these boundary areas with
combined perfusion were not observed in the present study.
Other selective ASL methods have enabled perfusion territory mapping of intracranial arteries such as the ACA and
MCA.31,33 Thus far, no method was presented to selectively
label the ECA. The combination of ICA occlusion and the
selective ASL method enabled us to perform perfusion
territory mapping of the ECA ipsilateral to the side of the
occlusion.
Currently, DSA is the standard for visualizing the cerebral
vascular tree and for assessing collateral flow at the level of
the circle of Willis or leptomeningeal anastomoses at the
brain surface. DSA offers excellent information on the
presence of collateral flow, showing also the distal arteries of
a collateral pathway. However, DSA does not provide quantitative information on the actual perfusion of the brain, and
to visualize all the collateral pathways, this technique requires
an invasive, selective multivessel approach. In the future,
selective ASL MRI may be capable of replacing diagnostic
DSA in a selected group of patients. For instance, in patients
Contribution of ECA to Brain Perfusion
3007
with a severe stenosis of an ECA ipsilateral to an ICA
occlusion, knowledge of the actual contribution of the ECA to
cerebral perfusion as assessed by ASL MRI may help to
select patients who may benefit most from endarterectomy of
the ipsilateral ECA.34
A limitation of our study may be that perfusion territory
segmentation was performed at a single delay time between
labeling and imaging. In general, this delay time is sufficient
for adequate exchange of the label with the brain. However,
with severe obstruction of the main brain-feeding arteries,
and subsequent presence of collateral flow, labeled blood
may have delayed arrival at the brain tissue. This may result
in an underestimation of the flow territory. However, a
previous study in patients with ICA occlusion demonstrated
that a delay time of 1600 ms (used in our study) is a good
tradeoff between signal-to-noise ratio, washout of the tracer,
and T1 relaxation.35 Similar to the quantification of rCBF
with nonselective ASL MRI, rCBF quantification in patients
with ICA occlusion requires more advanced selective ASL
techniques.35 With delayed collateral flow, the label will have
a delayed arrival at the brain tissue and ASL techniques with
measurements at a single time point may suffer from underestimation of the rCBF in the areas with collateral blood
supply. Acquiring images at multiple time points as we did in
our study can prevent underestimation of rCBF. In addition to
ASL at multiple time points, several methods have been
developed to render ASL MRI relatively insensitive to transit
delays by applying saturation pulses to obtain sharply defined
and a uniform shape of the bolus profile.36,37 In the present
study, we had a relatively small sample size. The number of
patients might have been too small to demonstrate potential
small differences in rCBF between ECA Grade 1 and 2
groups.
With selective ASL, there may be some contamination of
arteries from other vascular territories. When labeling the
VBA, the curved anatomy of the ICA in the neck will
incidentally lead to superfluous labeling of the proximal
ICAs. This artifactual residual labeling of the ICAs will
however be very small.10 With respect to the selective
labeling of the ECA on the side of an occluded ICA, the
selective labeling of the ECA will be easily separated from
the other brain-feeding arteries in the neck, and no artifactual
labeling of other arteries will occur. For selective ASL
methods, the labeling efficiency may be lower than 1.0 both
for both 1.5 and 3.0 T due to partial labeling of the proximal
arterial tree to the angulation of the labeling slab. This means
that we might have slightly underestimated the extent of the
flow territories. Furthermore, although ASL MRI rCBF
measurements are highly comparable with rCBF measurements obtained with positron emission tomography,38 ASL is
well known to yield slightly overestimated rCBF values in the
gray matter owing to the presence of label in the
vasculature.39
In conclusion, we showed that in patients with symptomatic ICA occlusion, focal brain regions may strongly depend
on the contribution to cerebral perfusion of the ECA ipsilateral to the side of the ICA occlusion, even in patients with
limited ECA collateral supply as demonstrated on DSA. The
actual contribution of the ECA as assessed by ASL MRI
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November 2008
could be taken into account when considering vascular
intervention of an ECA stenosis in patients with symptomatic
ICA occlusion.
Sources of Funding
C.J.M.K. is supported by a clinical fellowship from the Netherlands
Organization for Health Research and Development (grant 907– 00103) and by The Netherlands Heart Foundation (grant 2003B263).
Disclosures
None.
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Assessment of the Contribution of the External Carotid Artery to Brain Perfusion in
Patients With Internal Carotid Artery Occlusion
Peter Jan van Laar, Jeroen van der Grond, Jochem P. Bremmer, Catharina J.M. Klijn and Jeroen
Hendrikse
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Stroke. 2008;39:3003-3008; originally published online August 7, 2008;
doi: 10.1161/STROKEAHA.108.514265
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