Assessment of Intracranial Collateral Flow by Using
Dynamic Arterial Spin Labeling MRA and Transcranial
Color-Coded Duplex Ultrasound
Fabrizio Sallustio, MD; Rolf Kern, MD; Matthias Günther, PhD; Kristina Szabo, MD;
Martin Griebe, MD; Stephen Meairs, MD; Michael Hennerici, MD; Achim Gass, MD
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Background and Purpose—To evaluate the potential of a new dynamic MRA sequence (DynAngio) based on arterial spin
labeling for the assessment of intracranial collateral flow.
Methods—Twelve patients with unilateral internal carotid artery obstruction were investigated. Different patterns of
collateral flow were compared between DynAngio, transcranial color-coded duplex ultrasound, and time-of-flight MRA.
Results—There was a good agreement between the methods, with sensitivities between 80% and 90%. Small collateral
vessels were detected more frequently with DynAngio compared to time-of-flight MRA.
Conclusion—DynAngio provides anatomic and similar to transcranial color-coded duplex ultrasound functional information on collateral flow for the assessment of intracranial hemodynamics. (Stroke. 2008;39:1894-1897.)
Key Words: carotid stenosis 䡲 collateral circulation 䡲 diagnostic imaging 䡲 magnetic resonance angiography
䡲 transcranial ultrasound
T
he first pathoanatomical description of the intracranial
arterial circle by Fallopius and Johann Jakob Wepfer1
dates back to 1561 and 1658, whereas its anastomotical
function was discovered by Sir Thomas Willis2 in 1664. To
date, it is still of high relevance to study collateral function of
the circle of Willis, because this may allow the estimation of
the individual patient’s risk and prognosis of subsequent
stroke.3,4
Transcranial color-coded duplex ultrasound (TCCD) and
time-of-flight MRA (TOF-MRA) are well-established noninvasive methods for the evaluation of intracranial collateral
flow (CF), whereas digital subtraction angiography is considered the gold standard.5,6 Arterial spin labeling is a MR
technique using magnetization of inflowing blood to obtain
subsequent images of its arrival into the intracranial circulation. We compared a new arterial spin labeling based dynamic angiography (DynAngio)7 with TCCD and TOF-MRA
for the assessment of intracranial CF in patients with severe
unilateral internal carotid artery (ICA) obstruction.
transtemporal approach. According to standard ultrasound protocols,8 mean flow velocities from all major intracranial arteries
including the anterior communicating artery and both posterior
communicating arteries (PCoA) were assessed. Relevant anterior
collateral flow (aCF) via anterior communicating artery to the middle
cerebral artery was defined to be present when the color-coded
Doppler signals and Doppler spectra showed flow reversal in the A1
segment of the anterior cerebral artery ipsilateral to ICA obstruction.
Relevant posterior collateral flow (pCF) through the PCoA was
defined to be present when the flow in the ipsilateral PCoA was
directed from the P1 segment of the posterior cerebral artery to the
ICA (Figure 1). If the PCoA was not detectable pCF was established
by a side-to-side difference of mean flow velocities in the P1
segments of ⱖ20%.9
MRA studies were performed with a 1.5-Tesla MR system
(Magnetom Sonata; Siemens Medical) within 6 hours from TCCD
examination. The DynAngio sequence combines a flow-alternating
inversion recovery scheme with a segmented FLASH Look-Locker
sampling strategy.7 This results in consecutive time-resolved images
of blood inflow into the arterial tree. Thirty-six different phases of
inflow with a temporal resolution of 36 ms and an interpolated
in-plane resolution of 0.52 mm were acquired within 2 minutes 20
seconds. Color-coded parameter maps were calculated for each voxel
using the mean signal of the time series and the time when the
maximum of the signal curve is reached (Figure 2).
We assessed CF on TOF-MRA based on the hypothesis that
visible collateral arteries are patent and potentially capable of
supplying CF.10 In addition to vessel visibility, CF on DynAngio was
evaluated on the basis of blood bolus arrival times. aCF was defined
to be present when there was an at least 36 ms earlier appearance of
blood in the contralateral A1 segment and consecutive blood inflow
to the ipsilateral middle cerebral artery. pCF was considered relevant
Patients and Methods
We prospectively studied 12 patients after hemispheric stroke or TIA
(6 women; mean age, 65 years; age range, 45 to 85 years) with severe
(⬎80%) unilateral ICA stenosis or occlusion causing CF as diagnosed by TCCD. The study was approved by the local ethics
committee and written informed consent was obtained.
TCCD was performed using a Philips HDI 5000 system (Philips
Medical Systems) with a 2- to 4-MHz sector transducer from the
Received October 24, 2007; accepted November 14, 2007.
From Department of Neurology, Universitätsklinikum Mannheim, University of Heidelberg, Mannheim, Germany.
F.S. and R.K. contributed equally to the preparation of the manuscript.
Correspondence to Rolf Kern, MD, Department of Neurology, Universitätsklinikum Mannheim, University of Heidelberg, 68135 Mannheim, Germany;
E-mail [email protected]
© 2008 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.org
DOI: 10.1161/STROKEAHA.107.503482
1894
Sallustio et al
Assessment of Collateral Flow With DynAngio and TCCD
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Figure 1. TCCD example of CF in a patient with left ICA occlusion. Recruitment of aCF is represented by the reversal of flow in the left
A1 segment and by the high flow velocities in the anterior communicating artery and the contralateral A1 segment. Compared to the
contralateral artery the flow velocity is ⬎20% higher in the left P1 segment as criteria for relevant pCF. The normal flow velocity of the
left middle cerebral artery may indirectly imply that the CF can be considered efficient.
when the side-to-side difference of blood bolus arrival times between
the P1 segments was ⱖ36 ms with an earlier appearance of the
ipsilateral P1 segment, or when there was blood flow from the
ipsilateral PCoA toward the middle cerebral artery.
Three different patterns of CF were defined for comparison of
TCCD and MRA results: type 1 recruitment of aCF and pCF, type II
aCF only, and type III pCF only. Sensitivity, specificity, and positive
and negative predictive values of DynAngio and of TOF-MRA to
detect CF in comparison to TCCD were calculated.
Results
The Table lists the CF patterns as detected by TCCD,
TOF-MRA, and DynAngio.
DynAngio allowed detailed visualization of the dynamics
of inflowing blood to the circle of Willis and its main
branches in high quality in 11 of 12 patients (91.6%). Both
A1 segments were detected in 10 of 12 patients on DynAngio
and TOF-MRA. The dynamic character of the time-resolved
information allowed direct visualization of anterior communicating artery more frequently with DynAngio compared to
TOF-MRA (8 vs 5 patients). The ipsilateral P1 segment was
visible in all patients, whereas both PCoAs were detected
more frequently with DynAngio (8 vs 5 patients).
On TCCD both A1 segments were detected in 10 patients
with reversal of flow in the ipsilateral A1 segment in 9 of 10
patients; direct visualization of the anterior communicating
artery was possible in 2 cases. P1 segments could be detected
in all patients and pCF was present in 9 patients. However,
the ipsilateral PCoA was visible in 3 cases only.
There was a good overall agreement (79.2%) between
TCCD and MRA findings (Table). The sensitivity of DynAngio for the detection of CF was 84.2% (aCF, 80%; pCF,
88.9%), and the positive predictive value was 88.9%. Specificity and negative predictive values were moderate (50%)
because of the low number of cases with absent collateral
flow included to this analysis. The sensitivity of TOF-MRA
was 81% (aCF, 80%; pCF, 81.8%); positive predictive value
was 94.4% (aCF, 88.9%; pCF, 100%). Specificity (66.7%)
and negative predictive values were moderate (33.3%).
Discussion
DynAngio provides detailed anatomic and dynamic blood
flow information in the circle of Willis. It demonstrates
indications of CF and corresponds well with TOF-MRA and
TCCD findings. Our results are consistent with a recent study
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June 2008
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Figure 2. The color-coded DynAngio map (upper left) describes the time point of maximum blood inflow to arterial vessels; warm colors (red and yellow) indicate early arrival of blood, whereas cold colors (green and blue) indicate later arrival. It shows an earlier arrival
in the ipsilateral P1 segment and in the contralateral siphon in this patient with left ICA occlusion. Consecutive time-resolved images of
DynAngio (right) demonstrate the blood inflow to the left middle cerebral artery from the contralateral A1 segment (red arrows) and from
the ipsilateral P1 segment and PCoA (green arrows).
using DynAngio for quantification of extracranial carotid
stenosis with respect to associated CF.11
Similar to TCCD, DynAngio allows the evaluation of
functional changes attributable to the combination of temporal and spatial data. Given the short acquisition time and
Table. Comparison of DynAngio, TOF-MRA, and TCCD for
Assessment of Different Patterns of CF
Pattern of CF
(TCCD)
Pattern of CF
(DynAngio)
Pattern of CF
(TOF-MRA)
1
Type I
Type I
Type I
2
Type I
Type I
Type I
3
Type I
Type I
Type I
4
Type I
Type I
Type I
5
Type I
Type I
Type I
6
Type I
No CF
Type I
1–6
Agreement*
10 (83.3%)
12 (100%)
7
Type II
Type II
Type II
8
Type II
Type II
Type III
9
Type II
Type I
Type I
7–9
Agreement*
5 (83.3%)
3 (50%)
10
Type III
Type III
Type III
11
Type III
Type I
Type I
Patient No.
12
Type III
Type I
Type I
10–12
Agreement*
4 (66.7%)
4 (66.7%)
1–12
Overall agreement*
19 (79.2%)
19 (79.2%)
*Combined calculation for aCF and pCF.
highly dynamic character, DynAngio also appears preferable
over previous TOF-MRA sequences when using saturation
slabs to obtain information on flow directionality and CF.6
TCCD and DynAngio both provide hemodynamic information from intracranial vessels and have the potential to
determine velocity and directionality of blood flow.12
For the assessment of short vessel segments with a small
diameter, eg, PCoA, spatial resolution and time resolution are
of great importance. Determination of flow directionality is
particularly difficult in small arteries because it requires
demonstration of blood inflow on consecutive time-resolved
DynAngio images. Nevertheless, flow directionality of anterior and posterior collateral arteries was definable in the
majority of patients using this technique. In 3 patients
DynAngio was even able to detect blood flow in the PCoA
when TOF-MRA was unable to demonstrate this vessel
segment, indicating that DynAngio may be more sensitive to
detect small and low-flow collaterals. When confirmed in
larger study populations the use of DynAngio is likely to add
complementary information to other techniques for noninvasive assessment of CF, which may altogether limit the need to
perform digital subtraction angiography.
Disclosures
None.
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Assessment of Intracranial Collateral Flow by Using Dynamic Arterial Spin Labeling
MRA and Transcranial Color-Coded Duplex Ultrasound
Fabrizio Sallustio, Rolf Kern, Matthias Günther, Kristina Szabo, Martin Griebe, Stephen Meairs,
Michael Hennerici and Achim Gass
Downloaded from http://stroke.ahajournals.org/ by guest on June 15, 2017
Stroke. 2008;39:1894-1897; originally published online April 10, 2008;
doi: 10.1161/STROKEAHA.107.503482
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