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DOI: 10.1148/radiol.2422060179
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(Radiology 2007;242:526-534.)
© RSNA, 2007


Neuroradiology

Symptomatic Carotid Artery Occlusion: Flow Territories of Major Brain-Feeding Arteries1

Peter Jan van Laar, MD, Jeroen Hendrikse, MD, PhD, Catharina J. M. Klijn, MD, PhD, L. Jaap Kappelle, MD, PhD, Matthias J. P. van Osch, PhD and Jeroen van der Grond, PhD

1 From the Departments of Radiology (P.J.v.L., J.H.) and Neurology (C.J.M.K., L.J.K.), University Medical Center Utrecht, Heidelberglaan 100, 3584 CX Utrecht, the Netherlands; and Department of Radiology, Leiden University Medical Center, Leiden, the Netherlands (M.J.P.v.O., J.v.d.G.). Received January 30, 2006; revision requested March 28; revision received April 3; accepted April 19; final version accepted June 15. C.J.M.K. is supported by a clinical fellowship from the Netherlands Organization for Health Research and Development and by the Netherlands Heart Foundation. Address correspondence to P.J.v.L. (e-mail: p.j.vanlaar{at}azu.nl).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Purpose: To prospectively investigate the extent of flow territories of the contralateral internal carotid artery (ICA) and vertebrobasilar arteries in patients with symptomatic ICA occlusion.

Materials and Methods: Ethics committee approval and informed consent were obtained. Flow territory mapping of the ICA contralateral to the occluded ICA and mapping of the vertebrobasilar arteries were performed by using selective arterial spin-labeling magnetic resonance imaging in 23 functionally independent patients (22 men, one woman; mean age, 58 years ± 8 [standard deviation]) with symptomatic ICA occlusion. The control group consisted of 68 subjects (57 men, 11 women; mean age, 59 years ± 9) without hemodynamically significant ICA obstruction. Voxel-based {chi}2 testing with Bonferroni correction was performed to analyze significant differences in the extent of the flow territories.

Results: Flow territory maps in patients with symptomatic ICA occlusion showed significant differences in the flow territories of the contralateral ICA and vertebrobasilar arteries compared with those in control subjects (P < .05).

Conclusion: In functionally independent patients with symptomatic ICA occlusion, the middle cerebral artery flow territory ipsilateral to the occluded ICA is mainly supplied by the vertebrobasilar arteries, whereas the anterior cerebral artery flow territory on the occluded side is mainly supplied by the contralateral ICA.

© RSNA, 2007


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
In patients with occlusive disease of the internal carotid artery (ICA), collateral circulation is important to maintain adequate cerebral perfusion (1,2). The primary collateral pathway is the circle of Willis, with the possibility of redistributing flow from the contralateral ICA via the anterior communicating artery or from the vertebrobasilar arteries via the posterior communicating artery. Secondary collateral pathways include the external carotid artery via the ophthalmic artery and leptomeningeal anastomoses at the brain surface (3).

The results of several studies have demonstrated that adequate collateral circulation may prevent the development of hemodynamic failure (48). In contrast, findings from one study showed no beneficial effect of increased flow to the brain or of increased intracranial collateral flow (9), and findings from other studies showed that the presence of leptomeningeal collateral flow was associated with an increased risk of future ischemic stroke (10,11).

The actual contribution of the individual collateral pathways is difficult to assess and quantify. Magnetic resonance (MR) angiography and transcranial Doppler ultrasonography (US) may show the presence of collateral flow, but they do not show the actual contribution of collateral flow to brain perfusion. Intraarterial digital subtraction angiography (DSA) offers more information and shows the distal arteries of the collateral pathway (5). However, to visualize all the collateral pathways, this technique requires an invasive and selective three-vessel approach.

Recently, selective arterial spin-labeling MR imaging was introduced as a noninvasive means of studying the selective contribution of individual arteries to brain perfusion (12). The purpose of our study was to prospectively investigate the extent of flow territories of the contralateral ICA and vertebrobasilar arteries in patients with symptomatic ICA occlusion.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
The ethics committee of the University Medical Center Utrecht approved the study protocol, and written informed consent was obtained from all participants.

Patients, Control Subjects, and Sample Size
Twenty-three consecutive patients (22 men, one woman; mean age, 58 years ± 8 [standard deviation]) who met our study criteria were included between March and November 2003. All patients had ICA occlusion that was associated with transient or minor disabling ischemic attacks (modified Rankin score of 0–2) within 6 months prior to referral (13). Patients who had experienced a severe stroke in the past that caused major disability (modified Rankin score of 3–5) were not included. Eighteen patients (17 men, one woman; mean age, 57 years ± 8) had unilateral ICA occlusion, and five patients (all men; mean age, 59 years ± 5) had bilateral ICA occlusion. The diagnosis and grading of ICA obstruction and vertebrobasilar artery lesions were performed with intraarterial DSA according to the criteria of the North American Symptomatic Carotid Endarterectomy Trial (14).

The presence of collateral flow in the circle of Willis (ie, via the ipsilateral A1 segment or via the posterior communicating artery) was assessed with intraarterial DSA and MR angiography according to a previously published protocol (15). Collateral flow in the leptomeningeal anastomoses was judged to be present if intraarterial DSA showed cortical branches extending from the posterior cerebral artery into the vascular territory of the middle cerebral artery (MCA). Anterior collateral flow in the circle of Willis may comprise (a) flow from the nonoccluded side across the anterior communicating artery to the A2 segment on the side of the ICA occlusion only or (b) flow from the nonoccluded side across the anterior communicating artery and retrograde flow in the A1 segment on the occluded side that supplies both the A2 segment and the MCA on the side of the ICA occlusion.

In our study, anterior collateral flow was defined as flow across the anterior communicating artery and as retrograde flow in the A1 segment on the occluded side that supplied both the A2 segment and the MCA on the side of the occlusion. Therefore, flow across only the anterior communicating artery that supplied the A2 segment on the occluded side was not considered anterior collateral flow. Posterior collateral flow was defined as antegrade flow in the posterior communicating artery or as the presence of leptomeningeal anastomoses. In the group of patients with unilateral ICA occlusion (n = 18), 12 patients had both posterior collateral flow and anterior collateral flow, five patients had posterior collateral flow only, and one patient had anterior collateral flow only.

The control group consisted of 68 age-matched subjects (57 men, 11 women; mean age, 59 years ± 9) without abnormalities on MR images and MR angiograms of the brain and without hemodynamically significant ICA stenosis (less than 70% reduction in diameter) or ICA occlusion on duplex US scans. All control subjects had a nonvariant-type circle of Willis. Subjects with stroke, transient ischemic attack, or known intracerebral vascular abnormalities were excluded from the control group.

The sample size was calculated by using the results of previous studies that investigated the prevalence of differences in posterior and anterior collateral flow patterns between patients with ICA occlusion and control subjects (15,16). In these studies, researchers showed that 40% of patients with ICA obstruction (15) and 10% of control subjects (16) had reversed flow in the posterior communicating artery.

By using a type 1 error ({alpha}) of .05 and a type 2 error (ß) of .10, we determined that the minimum sample size required to demonstrate possible differences in posterior flow territories was 78. To demonstrate possible differences in anterior flow territories, the minimum required sample size was 22 (50% of patients with ICA obstruction and 0% of control subjects with reversed flow in the A1 segment of the anterior cerebral arteries [ACAs] on the symptomatic side). Our total sample size was 91.

MR Imaging
MR imaging was performed by using a 1.5-T whole-body system (Gyroscan ACS-NT; Philips Medical Systems, Best, the Netherlands). Flow territory imaging was achieved by using a regional perfusion imaging sequence (12), which is based on a pulsed arterial spin-labeling transfer insensitive labeling technique (1719). With regional perfusion imaging, selective labeling is obtained by using the sharp labeling profiles of the transfer insensitive labeling pulses (20) and by interactively planning the spatially selective inversion slabs to invert the targeted artery only.

To generate the perfusion images, control images and labeled images were obtained. For the labeled images, inflowing spins were inverted by applying two consecutive section-selective 90° radiofrequency pulses in a single slab. For the control images, the phase of the second 90° radiofrequency pulse was shifted by 180°, resulting in a 0° net effect (ie, 90° minus 90°), whereas global magnetization transfer effects were identical.

Subsequent to the labeling pulses, three 90° saturation pulses followed by strong dephasing gradients were applied to the imaging sections to remove the direct effects of the transfer insensitive labeling pulses. Each saturation pulse was followed by a series of strong dephasing gradients in all three directions to spoil all remaining transverse magnetization. When this saturation and dephasing scheme is not used, a high-intensity band is present on the perfusion-weighted images (label and control) at the point of intersection between the labeling slab and the imaging sections. In our study, the range of the saturation slab was set from 10 mm below the lowest imaging section to 45 mm above the highest imaging section. This asymmetric saturation slab was used to reduce the signal contribution of the veins.

The labeling delay time (inversion time) was set at 1600 msec. 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 msec between sections. For image acquisition, a single-shot echo-planar imaging readout was used. Other MR parameters for regional perfusion imaging were 3000/5.6 (repetition time msec/echo time msec), 62% partial Fourier acquisition, five sections acquired, 8-mm section thickness, 1-mm section gap, 240 x 240-mm field of view, 64 x 64 matrix, zero filling to a 128 x 128 matrix, 3336.7-Hz bandwidth per pixel, 30 signals acquired, and a regional perfusion imaging time of 3 minutes per territory.

The size of the labeling slab can be adjusted in one direction and is infinite in the other two directions. Planning of the selective labeling volume was performed on the basis of phase-contrast surveys in the coronal (14/7, 20° flip angle, 250 x 250-mm field of view, four signals acquired, one section acquired, and 60-mm section thickness) and sagittal (14/7, 20° flip angle, 250 x 250-mm field of view, four signals acquired, two sections acquired, 50-mm section thickness with –5-mm section gap [overlapping sections], 30-cm/sec velocity sensitivity, and 35-second imaging time) planes and time-of-flight MR angiograms of the circle of Willis (30/6.9, 20° flip angle, 100 x 100-mm field of view, 256 x 256 matrix, two signals acquired, 1.2-mm section thickness with 0.6-mm overlap, 50 sections acquired, and 2-minute imaging time), with subsequent maximum intensity projection reconstruction.

For the selective labeling of the ICA, an oblique sagittal labeling slab was chosen on the basis of the maximum intensity projection of the circle of Willis and the coronal phase-contrast survey. The slab was aligned so that a single ICA was labeled and the signal contribution from the basilar artery and vertebral arteries was minimized (Fig 1). For selective labeling of the vertebrobasilar arteries, a coronal labeling slab was used on the basis of the maximum intensity projection of the circle of Willis and the sagittal phase-contrast survey.


Figure 1A
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Figure 1a: The oblique sagittal labeling slab for selective labeling of the left ICA (2) was planned by using (a) coronal phase-contrast survey (14/7, 20° flip angle) and (b) transverse maximum intensity projection of the time-of-flight MR angiograms of the circle of Willis (30/6.9, 20° flip angle). The coronal labeling slab for selective labeling of the vertebrobasilar arteries was planned by using (c) sagittal phase-contrast survey (14/7, 20° flip angle) and (d) transverse maximum intensity projection of the time-of-flight of the circle of Willis (30/6.9, 20° flip angle). 1 = basilar artery.

 

Figure 1B
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Figure 1b: The oblique sagittal labeling slab for selective labeling of the left ICA (2) was planned by using (a) coronal phase-contrast survey (14/7, 20° flip angle) and (b) transverse maximum intensity projection of the time-of-flight MR angiograms of the circle of Willis (30/6.9, 20° flip angle). The coronal labeling slab for selective labeling of the vertebrobasilar arteries was planned by using (c) sagittal phase-contrast survey (14/7, 20° flip angle) and (d) transverse maximum intensity projection of the time-of-flight of the circle of Willis (30/6.9, 20° flip angle). 1 = basilar artery.

 

Figure 1C
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Figure 1c: The oblique sagittal labeling slab for selective labeling of the left ICA (2) was planned by using (a) coronal phase-contrast survey (14/7, 20° flip angle) and (b) transverse maximum intensity projection of the time-of-flight MR angiograms of the circle of Willis (30/6.9, 20° flip angle). The coronal labeling slab for selective labeling of the vertebrobasilar arteries was planned by using (c) sagittal phase-contrast survey (14/7, 20° flip angle) and (d) transverse maximum intensity projection of the time-of-flight of the circle of Willis (30/6.9, 20° flip angle). 1 = basilar artery.

 

Figure 1D
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Figure 1d: The oblique sagittal labeling slab for selective labeling of the left ICA (2) was planned by using (a) coronal phase-contrast survey (14/7, 20° flip angle) and (b) transverse maximum intensity projection of the time-of-flight MR angiograms of the circle of Willis (30/6.9, 20° flip angle). The coronal labeling slab for selective labeling of the vertebrobasilar arteries was planned by using (c) sagittal phase-contrast survey (14/7, 20° flip angle) and (d) transverse maximum intensity projection of the time-of-flight of the circle of Willis (30/6.9, 20° flip angle). 1 = basilar artery.

 
Data Processing
Data were analyzed with mathematic software (MATLAB; Mathworks, Natick, Mass). Perfusion-weighted images of the flow territories of the selectively labeled cerebral arteries were obtained by subtracting the labeled images from the control images. After visual evaluation of the resulting subtracted images, one author (P.J.v.L., with 5 years of experience) manually outlined and filled the perfusion images. These segmented images were registered on a standard brain template by using computer software (SPM; Wellcome Department of Cognitive Neurology, Institute of Neurology, London, England) (21,22) (Fig 2). This process was performed for all flow territories in all subjects.


Figure 2
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Figure 2: Pictorial description of postprocessing method (based on one set of transverse images in patient with symptomatic right-sided ICA occlusion) resulting from selective labeling of left ICA with regional perfusion imaging (3000/5.6/1600 [repetition time msec/echo time msec/inversion time msec], 90° flip angle). By subtracting labeled images from control images, perfusion-weighted images of the left ICA flow territory were obtained. Subtracted images were manually outlined, filled, and registered on a standard brain template. Bottom row shows combined flow territory maps of individual subjects (n = 18), expressed as a probability map. Colors correspond to the color bar, which indicates the percentage of individuals who demonstrated perfusion in that region of the brain.

 
Because no significant differences in flow territories were found between patients with left-sided ICA occlusion and those with right-sided ICA occlusion, all patients with symptomatic ICA occlusions were pooled. The flow territory maps of patients with left-sided symptomatic ICA occlusion were mirrored in the midline, whereas flow territory maps of patients with right-sided symptomatic ICA occlusion remained unchanged.

To create groups, the flow territories (registered on a standard brain template) of the individual subjects were combined. These combined flow territory maps were color coded and expressed as probability maps. A probability of 100% (ie, a region of the brain with red overlay) indicated that all subjects demonstrated perfusion in that region of the brain, and a probability of 0% (ie, the region of the brain with no color overlay) indicated that no subjects demonstrated perfusion in that region of the brain.

Statistical Analysis
Voxel-based {chi}2 testing with Bonferroni correction (corrected for the number of brain voxels in the regional perfusion imaging sections) was performed to analyze significant differences in the extent of flow territories between patients and control subjects. After correction, P values of less than .05 were considered to indicate a statistically significant difference. Areas of infarction were a priori excluded from the data analysis (six patients with a cortical lesion, one patient with a subcortical lesion, and four patients with a cortical and subcortical lesion). Because the flow territory maps were expressed as a percentage, the exclusion of cerebral infarcts influenced the power of the statistical analysis only. For statistical analysis, mathematic software (MATLAB; Mathworks) was used.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Patients with Unilateral ICA Occlusion
The segmented flow territory maps of the contralateral nonoccluded ICA and vertebrobasilar arteries that were projected on a standard brain template for all patients with symptomatic unilateral ICA occlusion (n = 18) showed a relatively large variation in flow territories (Fig 3). The flow territory maps of the control subjects (Fig 3) indicated a considerably lower variation in flow territories.


Figure 3A
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Figure 3a: Transverse flow territory maps projected onto a standard brain template in (a) patients with unilateral ICA occlusion (n = 18) of the contralateral ICA and vertebrobasilar arteries (VBA) and (b) control subjects (n = 68). In a, the side with symptomatic occlusion was standardized to the right ICA. Colors correspond to the color bar, which indicates the percentage of individuals who demonstrated perfusion in that region of the brain. (c) Significant differences are seen in the left ICA and vertebrobasilar artery flow territories between patients with unilateral symptomatic ICA occlusion and control subjects. Colors correspond to the color bar, which uses a logarithmic scale to indicate significant P  values. In all regions with significant differences, the percentage of individuals who demonstrated flow territories was higher for patients than for control subjects.

 

Figure 3B
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Figure 3b: Transverse flow territory maps projected onto a standard brain template in (a) patients with unilateral ICA occlusion (n = 18) of the contralateral ICA and vertebrobasilar arteries (VBA) and (b) control subjects (n = 68). In a, the side with symptomatic occlusion was standardized to the right ICA. Colors correspond to the color bar, which indicates the percentage of individuals who demonstrated perfusion in that region of the brain. (c) Significant differences are seen in the left ICA and vertebrobasilar artery flow territories between patients with unilateral symptomatic ICA occlusion and control subjects. Colors correspond to the color bar, which uses a logarithmic scale to indicate significant P  values. In all regions with significant differences, the percentage of individuals who demonstrated flow territories was higher for patients than for control subjects.

 

Figure 3C
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Figure 3c: Transverse flow territory maps projected onto a standard brain template in (a) patients with unilateral ICA occlusion (n = 18) of the contralateral ICA and vertebrobasilar arteries (VBA) and (b) control subjects (n = 68). In a, the side with symptomatic occlusion was standardized to the right ICA. Colors correspond to the color bar, which indicates the percentage of individuals who demonstrated perfusion in that region of the brain. (c) Significant differences are seen in the left ICA and vertebrobasilar artery flow territories between patients with unilateral symptomatic ICA occlusion and control subjects. Colors correspond to the color bar, which uses a logarithmic scale to indicate significant P  values. In all regions with significant differences, the percentage of individuals who demonstrated flow territories was higher for patients than for control subjects.

 
Significant differences (P < .05) in the flow territories of the nonoccluded ICA and vertebrobasilar arteries between patients with symptomatic unilateral ICA occlusion and control subjects (Fig 3) demonstrated that, in patients with unilateral ICA occlusion, the vertebrobasilar arteries supplied a significantly larger part of the MCA flow territory ipsilateral to the side of the ICA occlusion. In these patients, the flow territory of the contralateral ICA was substantially extended into the ACA flow territory on the side of the ICA occlusion.

Flow territory maps in patients with symptomatic unilateral ICA occlusion who had both posterior collateral flow and anterior collateral flow (n = 12) (Fig 4) showed that the nonoccluded contralateral ICA supplied the ACA and, to a lesser extent, the MCA flow territory ipsilateral to the side of the ICA occlusion. The vertebrobasilar arteries supplied the largest part of the MCA flow territory on the side of the occlusion. Flow territory maps in the five patients with no anterior collateral flow (Fig 4) indicated that the vertebrobasilar arteries supplied the MCA flow territory on the side of the ICA occlusion. The flow territory of the contralateral ICA was extended to the ipsilateral ACA only and not to the ipsilateral MCA flow territory.


Figure 4A
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Figure 4a: Transverse flow territory maps of patients who had unilateral ICA occlusion with (a) anterior and posterior collateral flow (n = 12) or (b) posterior collateral flow (n = 5). In a, the side with symptomatic occlusion was standardized to the right ICA. Anterior collateral flow indicates retrograde flow in ipsilateral A1 segment, and posterior collateral flow indicates flow in posterior communicating artery or leptomeningeal anastomoses. Colors correspond to the color bar, which indicates the percentage of patients who demonstrated perfusion in that region of the brain. VBA = vertebrobasilar arteries.

 

Figure 4B
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Figure 4b: Transverse flow territory maps of patients who had unilateral ICA occlusion with (a) anterior and posterior collateral flow (n = 12) or (b) posterior collateral flow (n = 5). In a, the side with symptomatic occlusion was standardized to the right ICA. Anterior collateral flow indicates retrograde flow in ipsilateral A1 segment, and posterior collateral flow indicates flow in posterior communicating artery or leptomeningeal anastomoses. Colors correspond to the color bar, which indicates the percentage of patients who demonstrated perfusion in that region of the brain. VBA = vertebrobasilar arteries.

 
Patients with Bilateral ICA Occlusion
Because the ICA was occluded on both sides, only the vertebrobasilar arteries were labeled (Fig 5) on vertebrobasilar artery flow territory maps in patients with bilateral ICA occlusion (n = 5). Significant differences (P < .05) in the flow territories of the vertebrobasilar arteries between patients with bilateral ICA occlusion and control subjects were noted (Fig 5). In patients with bilateral ICA occlusion, the vertebrobasilar arteries supplied a significantly (P < .05) larger part of the MCA and ACA flow territories compared with those in the control subjects.


Figure 5A
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Figure 5a: Transverse flow territory maps of the vertebrobasilar arteries (VBA) in (a) patients with symptomatic bilateral ICA occlusion (n = 5) and (b) control subjects (n = 68); colors correspond to the color bar, which indicates the percentage of individuals who demonstrated perfusion in that region of the brain. Note that b corresponds to the bottom row of Figure 3b. (c) Significant differences in the vertebrobasilar artery flow territories are seen between patients with symptomatic bilateral ICA occlusion and control subjects. Colors correspond to the color bar, which uses a logarithmic scale to indicate significant P  values. In all regions with significant differences, the percentage of individuals who demonstrated a flow territory was higher for patients than for control subjects.

 

Figure 5B
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Figure 5b: Transverse flow territory maps of the vertebrobasilar arteries (VBA) in (a) patients with symptomatic bilateral ICA occlusion (n = 5) and (b) control subjects (n = 68); colors correspond to the color bar, which indicates the percentage of individuals who demonstrated perfusion in that region of the brain. Note that b corresponds to the bottom row of Figure 3b. (c) Significant differences in the vertebrobasilar artery flow territories are seen between patients with symptomatic bilateral ICA occlusion and control subjects. Colors correspond to the color bar, which uses a logarithmic scale to indicate significant P  values. In all regions with significant differences, the percentage of individuals who demonstrated a flow territory was higher for patients than for control subjects.

 

Figure 5C
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Figure 5c: Transverse flow territory maps of the vertebrobasilar arteries (VBA) in (a) patients with symptomatic bilateral ICA occlusion (n = 5) and (b) control subjects (n = 68); colors correspond to the color bar, which indicates the percentage of individuals who demonstrated perfusion in that region of the brain. Note that b corresponds to the bottom row of Figure 3b. (c) Significant differences in the vertebrobasilar artery flow territories are seen between patients with symptomatic bilateral ICA occlusion and control subjects. Colors correspond to the color bar, which uses a logarithmic scale to indicate significant P  values. In all regions with significant differences, the percentage of individuals who demonstrated a flow territory was higher for patients than for control subjects.

 

    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 
Flow territory maps in patients with symptomatic ICA occlusion showed significant differences in the flow territories of the contralateral ICA and vertebrobasilar arteries compared with those in the control subjects. In patients with ICA occlusion, the MCA flow territory ipsilateral to the ICA occlusion was mainly supplied by the vertebrobasilar arteries, whereas the ACA flow territory on the side of the occlusion was mainly supplied by the contralateral ICA.

The results of previous postmortem studies have shown large variability in the vascular territories of the human brain (23,24). In this light, it is not surprising that our results show a considerable variation in individual territorial distribution. Because we examined patients with symptomatic ICA occlusion who had no major neurologic 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 these altered flow territories in patients with symptomatic ICA occlusion.

Our results show that variation in the flow territories of the contralateral ICA and vertebrobasilar arteries in patients with unilateral ICA occlusion is partly caused by differences in the collateral flow pattern in the circle of Willis. In the subgroup of patients with anterior collateral flow (defined as retrograde flow in the ipsilateral A1 segment), the contralateral ICA supplied the ACA flow territory ipsilateral to the ICA occlusion and only a small part of the ipsilateral MCA flow territory. In the subgroup of patients with no anterior collateral flow, the contralateral ICA still supplied the ipsilateral ACA via the anterior communicating artery but did not supply the ipsilateral MCA flow territory.

Irrespective of the presence of anterior collateral flow, the vertebrobasilar arteries supply most of the MCA flow territory on the side of the ICA occlusion. This indicates the importance of the vertebrobasilar arteries for blood supply in the MCA flow territory on the side of the ICA occlusion. In previous studies in patients with unilateral ICA occlusion, researchers demonstrated the relative importance of collateral flow originating from the contralateral ICA via the anterior communicating artery (2529) or vertebrobasilar arteries (16,3032) for the perfusion of the hemisphere on the side of the ICA occlusion.

Compared with flow territory maps in control subjects, the flow territory maps in patients with bilateral ICA occlusion demonstrate that the vertebrobasilar arteries contribute significantly more to the MCA and ACA flow on both sides. This finding is consistent with the results of previous studies of patients with symptomatic bilateral ICA occlusion. It was found that, when both ICAs were occluded, flow through the basilar artery was increased 2.5-fold compared with that in the control subjects, indicating that the basilar artery is the main supplying artery (4).

Thirteen (72%) of 18 patients with unilateral ICA occlusion had collateral flow in the A1 segment, and 10 (56%) of 18 patients had collateral flow in the posterior communicating artery. In previous studies of patients with unilateral ICA occlusion, researchers demonstrated that the percentage of patients with collateral flow in the A1 segment varied between 43% and 72%, whereas the prevalence of collateral flow in the posterior communicating artery varied between 32% and 76% (6,8,11,15,29,33). Seven (39%) of 18 patients had posterior collateral flow in leptomeningeal anastomoses. The results of a recent review of leptomeningeal anastomoses demonstrated large interindividual variability in the distribution, size, and number of leptomeningeal anastomoses (34).

A limitation of our study may be that selective arterial spin labeling was performed at a single delay time between labeling and imaging. In general, this delay time is sufficient for adequate exchange of the label within the brain. However, with severe obstruction of the main feeding arteries and the subsequent presence of collateral flow, the arrival time of the labeled blood at the brain may have been delayed. This may have resulted in an underestimation of the flow territory. However, the results of a previous study in patients with ICA occlusion demonstrated that a delay time of 1600 msec (which was also used in our study) is a good trade-off among signal-to-noise ratio, tracer washout, and T1 relaxation (35).

The flow territory maps of the vertebrobasilar arteries in patients with bilateral ICA occlusion showed brain areas that demonstrated no perfusion. Other sources of cerebral blood collateral flow (eg, the external carotid artery via the ophthalmic artery or leptomeningeal anastomoses) may be important for these regions (3). The imaging technique used in our study does not take into account flow from the ipsilateral external carotid artery. In previous studies, researchers found that nearly all patients with bilateral ICA occlusion had retrograde flow in the ophthalmic artery (15).

In conclusion, functionally independent patients with symptomatic ICA occlusion have a large variation in flow territories ipsilateral to the ICA occlusion. In these patients, the MCA flow territory on the side of the ICA occlusion is mainly dependent on collateral flow originating from the vertebrobasilar arteries, whereas the contralateral ICA is important for ACA flow territories on both sides.


    ADVANCES IN KNOWLEDGE
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 


    FOOTNOTES
 

Abbreviations: ACA = anterior cerebral artery • DSA = digital subtraction angiography • ICA = internal carotid artery • MCA = middle cerebral artery

Authors stated no financial relationship to disclose.

Author contributions: Guarantors of integrity of entire study, P.J.v.L., J.H., J.v.d.G.; study concepts/study design or data acquisition or data analysis/interpretation, all authors; manuscript drafting or manuscript revision for important intellectual content, all authors; manuscript final version approval, all authors; literature research, P.J.v.L.; clinical studies, all authors; statistical analysis, P.J.v.L., J.H., M.J.P.v.O., J.v.d.G.; and manuscript editing, all authors


    References
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 ADVANCES IN KNOWLEDGE
 References
 

  1. Powers WJ. Cerebral hemodynamics in ischemic cerebrovascular disease. Ann Neurol 1991;29:231–240.[CrossRef][Medline]
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P. J. van Laar, J. van der Grond, and J. Hendrikse
Brain Perfusion Territory Imaging: Methods and Clinical Applications of Selective Arterial Spin-labeling MR Imaging
Radiology, February 1, 2008; 246(2): 354 - 364.
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