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(Stroke. 2001;32:1323.)
© 2001 American Heart Association, Inc.
Original Contributions |
Acute Stroke Patterns in Patients With Internal Carotid Artery Disease
A Diffusion-Weighted Magnetic Resonance Imaging Study
From the Department of Neurology, Klinikum Mannheim of the University of Heidelberg, Mannheim, Germany.
Correspondence to Dr Kristina Szabo, Department of Neurology, Klinikum Mannheim of the University of Heidelberg, Theodor-Kutzer-Ufer 1-3, 68167 Mannheim, Germany. E-mail szabo{at}neuro.ma.uni-heidelberg.de
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Abstract |
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 Top Abstract IntroductionSubjects and MethodsResultsDiscussionReferences |
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Background and Purpose—Diffusion-weighted (DW) MRI is a sensitive method that facilitates early stroke pattern identification. There are limited data about the influence of stenosis grade on the development of particular stroke patterns in internal carotid artery (ICA) disease. We therefore investigated the lesion patterns on DW MRI in acute stroke patients with ICA disease.
Methods—DW MRI was analyzed in 102 consecutive acute stroke patients with different degrees of ipsilateral ICA disease. Patients were assigned to 1 of 5 observed lesion patterns: (1) territorial ischemia, (2) subcortical ischemia without or (3) with embolus fragmentation, (4) disseminated lesions in distal cortical regions, and (5) multiple lesions in hemodynamic risk zones. In addition, perfusion-weighted (PW) MRI and MR angiography information was included in the assessment.
Results—All patterns were observed in the different stages of ICA disease. Half of the patients with high-grade or subtotal stenosis had lesions in hemodynamic risk zones. Territorial stroke occurred in 47.6% of patients with ICA occlusion. Statistical analysis showed a significant relationship between the degree of stenosis and the observed stroke pattern (P=0.001). In 77.8% of patients exhibiting high-grade ICA stenosis, subtotal stenosis, or occlusion, the perfusion lesion was larger than the diffusion lesion (PW/DW mismatch).
Conclusions—Although in the individual patient any of the infarct patterns may occur, in statistical terms the incidence of a particular stroke pattern is clearly dependent on the degree of stenosis.
Key Words: carotid artery diseases • magnetic resonance imaging, diffusion-weighted • stroke, acute
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Atherosclerotic narrowing of the extracranial vessels is a well-recognized cause of cerebral ischemia. The annual stroke risk for patients with asymptomatic internal carotid artery (ICA) stenosis amounts to approximately 1% to 2%.1 2 Both embolic and hemodynamic mechanisms are assumed to be the cause of stroke in ICA disease.3 Neuroimaging studies have been performed in an attempt to improve the understanding of the underlying stroke mechanism as a basis for the identification of patients at high risk and for the best possible therapeutic rationale. Studies based on CT have suggested that hemodynamically significant stenoses or obstructions of the extracranial ICA may cause hemodynamic changes in the distal regions of the hemispheric blood supply, the so-called border zones between major vascular territories, while embolism from ICA stenosis is believed to disproportionately affect the middle cerebral artery (MCA) stem and distal branches producing territorial infarction, often including the deep lenticulostriate territory.4 The coexistence of hypoperfusion and arterial embolism in patients with border zone stroke and ICA disease has recently been postulated.5 Since the concept of border zone ischemia as a cause of stroke in patients with severe ICA stenosis has also been challenged,6 7 uncertainty still remains regarding the occurrence and mechanism of ICA disease-related stroke.
Diffusion-weighted (DW) MRI is exquisitely sensitive to detect areas of acute ischemic tissue change.8 9 The results of recent studies using DW and perfusion-weighted (PW) MRI in acute stroke patients support the hypothesis that the detection of the acute lesion and the delineation of the area of hemodynamic compromise (by PW MRI) can improve the understanding of pathophysiological mechanisms leading to cerebral ischemia in patients with ICA disease. We used DW MRI in acute stroke patients with symptomatic, unilateral ICA disease associated with a stenosis of >50% to analyze differences in stroke patterns considering lesion size, localization, and distribution and to gather information on the pathomechanism of stroke.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Patients
In a prospective design, 102 consecutive patients (35 women, 67 men; mean age 66.2 years) admitted to the stroke unit of our hospital with acute ischemia distal to ipsilateral extracranial ICA disease with atherosclerotic narrowing >50% were analyzed. According to a standardized acute stroke care protocol, the following examinations were performed in all patients: detailed physical and neurological examination, assessment of cardiovascular risk factors, Doppler and duplex sonography of the extracranial vessels, transcranial Doppler sonography, transthoracic or transesophageal echocardiography, 24-hour ECG monitoring, and MRI. A total of 58 patients with stenosis of the MCA (n=3), infratentorial stroke (n=5), cardiac source of embolism (n=23), dissection of the ICA (n=8), or contralateral ICA disease with a stenosis degree >50% (n=19) were excluded from the study. Informed consent was obtained from all patients in writing before MRI was performed. The study had been approved by the local ethics committee.
Doppler Studies
Obstructive lesions of the ICA with a reduction in
diameter of >50% were diagnosed by noninvasive carotid studies with
the use of continuous-wave Doppler (Multi Dop T1, DWL) and duplex
sonography with frequency-based and power-based color coding (HDI 5000,
ATL).
The degree of ICA stenosis was classified as low grade in the case of slight to moderate increase in local flow (with or without pulsatility loss or systolic deceleration) in the continuous-wave Doppler study and a 50% to 70% diameter reduction in duplex imaging. Stenoses with >70% diameter reduction in the duplex scan and with a strong local flow increase (>8 kHz), systolic deceleration, and poststenotic decrease of systolic flow velocity in the continuous-wave Doppler examination were classified as high grade. Subtotal stenosis was defined as a very narrow stenosis with abnormally low flow velocities at the site of maximum narrowing. Obstructions with no detectable ICA flow information in color-coded duplex ultrasound after the application of an echo contrast agent (Levovist, Schering) were classified as occlusion.10 11 12 Doppler-diagnosed occlusion was confirmed in every case by conventional angiography or extracranial MR angiography (MRA) of the neck.
MRI Studies
MRI was performed on a 1.5-T MR system
(Magnetom Vision, Siemens Medical Systems) with
the following standardized protocol: (1) transverse, coronal, and
sagittal localizing sequences followed by transverse oblique contiguous
images (slice thickness 5 mm, field of view 240
mm2) aligned with the inferior
borders of the corpus callosum (applied on sequences 2 to 5); (2)
T2-weighted images (turbo spin echo, repetition time [TR] 2620
ms/echo time [TE] 85 ms, 192x256 matrix); (3) T1-weighted images (TR
530 ms/TE 12 ms, 192x256 matrix); (4) DW echo-planar (EP) images (TR
4000 ms/TE 100 ms,
b=0/160/360/640/1000
s/mm2, 96x128 matrix, sequential
application of 3 separate diffusion-sensitizing gradients in
perpendicular directions); (5) perfusion-weighted free induction
decay–EP sequence following the first pass of a contrast bolus
through the brain (2000/65/flip angle 90°, 11 slices, 40
acquisitions, 2-second interval, 128x128 matrix), contrast agent (15
mL Omniscan, Nycomed) injected manually through
a large-gauge venous cannula into the antecubital vein); and (6)
3-dimensional time-of-flight MRA sequence of the circle of Willis (flip
angle 20°, 165x512 matrix, slice thickness 2
mm).
Analysis of Infarct Patterns
As suggested by earlier studies, 5 patterns of
ischemic lesions were differentiated on DW MRI on the basis of
lesion size, distribution, and
localization.3 13
Patients were assigned to one of these patterns by 2 expert readers
(A.G., R.K.) unaware of the clinical data. The definition of stroke
patterns is summarized with examples in
Table 1
.
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Pattern 1 is defined as a large ischemic lesion
involving the cerebral cortex and subcortical structures in 1 or more
major cerebral artery territories, referred to as "territorial
infarction." An example of pattern 1 is given in
Figure 1. This stroke subtype is assumed to be a
partial MCA infarction if a distal MCA branch is occluded, a large MCA
infarction in the case of a proximal occlusion at the level of the
bifurcation or trifurcation paired with the absence of an efficient
collateral system,14 or a
complete anterior cerebral artery (ACA) and MCA territory infarction in
the case of a distal ICA embolism. Pattern 2 is defined as
"subcortical infarction" in the territory of deep perforating
branches originating from the distal ICA or the MCA trunk. This pattern
has been explained by the occlusion of the MCA in the presence of
patent collaterals, where the occlusion is either due to the
embolization into the MCA, resulting in a large striatocapsular lesion,
or due to the occlusion of a deep perforating artery of the carotid
system, leading to a subcortical lesion.15 16
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Pattern 3 ("territorial infarction with fragmentation")
represents a large ischemic lesion, as in pattern 1,
with additional smaller lesions either in cortical or in subcortical
regions, probably due to partial fragmentation of the
embolus.17 In pattern 4,
several disseminated small lesions are sprinkled in random fashion in
the distal territory of the MCA, involving mainly cortical regions. The
possible cause of this pattern may be a fragmented embolus or multiple
microemboli in smaller
vessels.18 Pattern 5
("border zone infarction") denotes lesions either completely or
predominantly located in regions considered to be one of the
hemodynamic risk zones between major cerebrovascular
territories19 : the
superficial or cortical border zones wedged between the ACA and MCA or
between the MCA and posterior cerebral artery (PCA), and the deep or
subcortical border zone located in the vascular territory between deep
and superficial arterial
systems.20 21 22
Figure 2 shows an example of a patient with pattern 5 stroke.
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Morphology of the Circle of Willis and the MCA
In an attempt to identify possible confounding
factors for the infarct patterns, the morphology and anatomic
variability of the vessels of the circle of Willis were
analyzed. For this purpose, coronal and transverse views of
3-dimensional MRA reconstruction were recorded in a structured
reporting form considering the presence, hypoplasia, or aplasia of the
anterior communicating artery, the A1 segment of ACA, the posterior
communicating artery, or the P1 segment of the PCA. A vessel or vessel
segment was classified as hypoplastic if it was present but was
very thin; it was classified as aplastic if there was no visible flow
signal.
In addition, the following classifications of the MCA signal were recorded: (1) absence of signal indicating vessel occlusion; (2) signal reduction in the ipsilateral MCA compared with the contralateral side, indicating reduced blood flow; and (3) normal signal. In the case of an absent MCA signal on MRA, the occlusion of the proximal MCA was confirmed in patients with sufficient bone window by transcranial duplex examination with echo contrast agent.
Evaluation of PW MRI
To obtain information about
hemodynamic alterations caused by vascular pathology,
calculated time-to-peak (TTP) images demonstrating the delay of the
contrast agent arrival in the brain parenchyma were used for
semiquantitative analysis. The average TTP value obtained in
the contralateral MCA territory as reference tissue was subtracted from
the bolus arrival time of the affected hemisphere. According to
Neumann-Haefelin et al,23 a
TTP delay >4 seconds was considered an indicator of a clinically
relevant perfusion deficit. In conformity with these findings, PW MRI
studies were classified as (1) normal, (2) perfusion deficit equal to
the DW MRI lesion, or (3) perfusion deficit larger than the DW MRI
lesion.
Statistical Analysis
The 
2 test was used to
analyze observed proportions and to determine the presence of a
relationship between the following: degree of ICA stenosis and
incidence of stroke patterns; patency of the circle of Willis and
incidence of stroke patterns; degree of ICA stenosis and
patency of the circle of Willis; extent of the ipsilateral MCA signal
and incidence of stroke patterns; and degree of ICA stenosis
and degree of perfusion abnormality. A value of
P<0.05 was considered
statistically significant.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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DW MRI lesions of the MCA territory were identified in all patients. Large territorial infarction (pattern 1) was observed in 30 cases; in 5 of these patients, additional acute lesions were noted in the ACA territory, suggesting complete carotid artery territory infarction. Four patients with direct blood supply of the PCA from the ICA had additional lesions in the PCA territory. Pattern 2 was noted in 13 patients and pattern 3 in 11 patients. Fifteen patients exhibited pattern 4 with small disseminated lesions not involving hemodynamic risk zones. Small disseminated lesions in the hemodynamic risk zones (pattern 5) were detected in 33 cases, of which the cortical risk zones were affected in 18, the subcortical regions in 8, and both the cortical and the subcortical regions in 7. In 3 patients, the readers’ initial conclusions regarding pattern classification were different because of disagreement about lesion location. After reviewing the data together, the readers agreed on pattern 5 (as opposed to pattern 4) in all cases.
Stroke Patterns in Relation to Stenosis
Grade
Low-grade ICA stenosis was present in 19
patients (18.6%), high-grade stenosis was observed in 31 cases
(30.4%), 10 cases showed subtotal stenosis (9.8%), and 42
patients had ICA occlusion (41.2%).
Table 2 summarizes the distribution of stroke patterns
in the subgroups with different ICA stenosis grade. In patients
with low-grade ICA stenosis, no clear-cut preference for a
particular pattern was observed. In contrast, 51.6% of patients with
high-grade and 50% of patients with subtotal stenosis had
lesions in hemodynamic risk zones (pattern 5).
Territorial infarction (pattern 1) was observed in 47.6% of the
patients with ICA occlusion.
Figure 3 shows the cumulative frequency distribution of stroke patterns in each of the 4 groups. The
2 analysis of the stroke pattern
proportions over the 4 stenosis grades defined above revealed a
statistically significant difference (P=0.001), indicating the
dependency of the stroke pattern distribution on the degree of
stenosis.
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Stroke Pattern Relationship to Patency of the
Circle of Willis and the MCA Signal
Three-dimensional reconstruction from MRA sequences of
the intracranial arteries was available in 84 patients; in all other
cases MRA could not be acquired in satisfactory quality because of
movement artifacts. In 14 cases (16.6%), the circle of Willis was
complete on the symptomatic side. Hypoplastic or absent
vessel segments of the ipsilateral circle of Willis were noted in 35
patients each (41.7%). In contrast to the findings regarding the
degree of ICA stenosis, 2
analysis based on a 3x5 contingency table (normal,
hypoplastic, or absent ipsilateral circle of Willis versus the 5 stroke
patterns) failed to demonstrate a statistically significant
relationship between the patency of vessel segments in the ipsilateral
circle of Willis and the occurrence of a particular stroke pattern
(P=0.879). In addition, the
analysis of the relationship between ICA stenosis grade
and circle of Willis patency did not show a statistically significant
relationship between these parameters in our study
population
(P=0.594).
Twenty-four patients (28.6%) exhibited an absence of blood
signal in the MCA, while 37 patients (44.0%) showed substantial signal
reduction. In 23 cases (27.4%), MCA signal appeared normal. In
patients with MCA occlusion, territorial infarction (pattern 1) was
present in 58.3% (n=14), while in patients with normal signal
stroke pattern 1 was seen in only 13% (n=3). A statistically
significant association was found between MCA signal and stroke pattern
distribution (P<0.001). The
findings of the MCA signal evaluation are summarized in
Table 3.
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Relationship Between PW MRI Abnormality and
Degree of ICA Stenosis
Perfusion data were acquired in 43 patients. Normal
perfusion was seen in 6 cases (13.9%), PW and DW MRI lesions were of
the same size in 7 cases (16.3%), and the PW MRI lesion was larger
than the DW MRI lesion in 30 patients (69.8%). In the patients with
PW-DW mismatch, 93.3% had ICA stenosis from high grade to
occlusion, while in patients without PW MRI lesion, low-grade ICA
stenosis was observed in 57.1%. The association between PW MRI
abnormality and the degree of underlying ICA stenosis was
statistically significant
(P=0.025). Findings of the PW
MRI evaluation are summarized in
Table 4.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The analysis of ischemic lesions on DW MRI demonstrates that stroke in patients with ICA occlusive disease is heterogeneous. The 5 stroke patterns, representing different characteristics from small embolic lesions to large territorial ischemia, were seen in all groups regardless of the degree of ICA stenosis. However, statistical analysis demonstrated that the degree of ICA obstruction may favor certain stroke patterns, indicating a preferred pathomechanism in the different ICA stenosis subgroups.
In the postmortem arteriographic and pathological study by Rodda and Path,24 massive infarcts involving 2 major cerebral artery territories were associated with distal ICA occlusion, MCA territory infarcts were seen when the ICA was occluded or stenosed, and border zone infarcts were characterized by ICA disease and limited circle of Willis anastomosis. In other studies, small border zone infarcts were seen as marker for high-grade ICA stenosis and occlusion,25 26 while this association was denied in a larger trial.6 Multiple acute lesions (pattern 4) have been recognized in recent publications as a new stroke pattern in distal and proximal stenosis,18 and they are thought to be caused by multiple emboli or the breakup of an embolus.17
In contrast to previous CT-based studies, DW MRI offers a better chance of detecting not only gross abnormalities but also very subtle acute ischemic lesions. This is the likely explanation of the discrepancy between our results and previous CT studies that suggested an association of large lesions with high-grade ICA stenosis.3 In our study 61.7% of the acute strokes in patients with some degree of ICA stenosis and 26.2% in patients with ICA occlusion presented with disseminated small acute lesions (pattern 4 and pattern 5), which may have been missed with conventional imaging. In keeping with the current concept of the hemodynamic relevance of ICA stenosis, our data show that in patients with high-grade stenosis the highest frequency of lesions occurs in the hemodynamic risk zones. PW MRI data suggest that in high-grade ICA stenosis the complete MCA territory may be hemodynamically altered despite the presence of only small acute lesions on DW MRI. Similar observations have been communicated in recent publications.27 28 While low-grade stenosis without obvious hemodynamic impairment appears to cause ischemic lesions suggestive of artery-to-artery embolism, in patients with a higher grade of ICA stenosis and obvious hemodynamic alterations, lesions were mostly seen in the arterial border zones.
In the present study 32.4% of patients demonstrated pattern 5 stroke. Several authors have postulated an association between hemodynamic compromise and subsequent brain infarction in patients with critical carotid artery disease, especially under the conditions of limited collateral circulation.22 25 The role of severe arterial hypotension causing bilateral border zone strokes has also been described and confirmed by experimental studies.29 30 A recent report suggested the interaction of embolic and hemodynamic mechanisms in the development of border zone strokes.5 Some of these theories are based on the high prevalence of emboli documented by transcranial Doppler monitoring in symptomatic high-grade carotid artery disease or during cardiac surgery, providing a possible link to the concept of embolism in a hypoperfused region.31 32 33 Our data demonstrate the high probability of lesion development in hemodynamic risk zones; however, they do not allow unequivocal conclusions about the exact pathomechanism because emboli detection was not part of the study protocol.
Although we must emphasize that all stroke patterns have been observed in patients with ICA occlusion, the development of a large territorial ischemia is the most likely consequence. Accordingly, strokes associated with atherosclerotic ICA occlusion are most likely to be caused by the formation of a large embolus that leads to the subsequent impairment of blood flow in the ipsilateral MCA.
The circle of Willis is considered an important collateral pathway in maintaining adequate cerebral blood flow in patients with ICA obstruction,34 and a noncompetent circle of Willis has been regarded as a predisposing condition for border zone infarcts.19 MRA has been used by others for the assessment of vessel patency in the circle of Willis.35 A recent investigation found that patients with ICA obstruction but no or only minor neurological deficits have a higher prevalence of a complete circle of Willis, a favorable anatomic predisposition.36 As an explanation, the authors suggested the possibility of either preexistent or acquired morphology secondary to hemodynamic adaptation. In contrast, in our patient population MRA showed a very high percentage (83.4%) of noncompetent circle of Willis vessels, and no association was found between circle of Willis patency and stroke pattern distribution or ICA stenosis grade. However, even high-resolution MRA has limitations because it provides no information on flow direction and on the existence of small communicating vessels that conventional angiography would identify. With these limitations in mind, we consider our observations as a measure of anatomic patency of collateral pathways, not a marker of functional collateralization.
On the other hand, our patients, who all suffered a complete stroke leading to some degree of disability, may represent a subgroup with a high prevalence of hypoplastic or aplastic circle of Willis, in which the cerebrovascular system is unable to adapt to reduced blood supply in an adequate manner. As a consequence, they are destined by morphological factors to develop severe stroke in the case of ICA disease. Further studies may clarify the relationship between anatomic predisposition, remodeling of collateral pathways, and stroke subtype.
In summary, we propose that the degree of ICA stenosis significantly influences the pattern of cerebral ischemia as seen on DW MRI. Our findings reflect a changing distribution of stroke patterns with increasing ICA stenosis. In high-grade ICA stenosis, multiple embolic lesions are a common feature of cerebral ischemia. The increasing degree of stenosis leads to additional hemodynamic alterations within subcortical and cortical border zone areas. The full interpretation of our study is limited both by the lack of transcranial emboli detection and by the lack of Doppler or angiographic data characterizing collateral blood supply; these methods might add clarification to the pathomechanism of stroke in ICA disease in future investigations.
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Acknowledgments |
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The authors express their gratitude to Professor Dr Tobias Back from the Department of Neurology, Philipps University, Marburg, Germany, for reviewing the manuscript.
Received October 30, 2000; revision received February 8, 2001; accepted March 8, 2001.
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 O Y Bang, P H Lee, S R Yoon, M A Lee, I S Joo, and K Huh Inflammatory markers, rather than conventional risk factors, are different between carotid and MCA atherosclerosis J. Neurol. Neurosurg. Psychiatry, August 1, 2005; 76(8): 1128 - 1134. [Abstract] [Full Text] [PDF]
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 S. Koch, M. Amir, A. A. Rabinstein, Y. Reyes-Iglesias, J. G. Romano, and A. Forteza Diffusion-Weighted Magnetic Resonance Imaging in Symptomatic Vertebrobasilar Atherosclerosis and Dissection Arch Neurol, August 1, 2005; 62(8): 1228 - 1231. [Abstract] [Full Text] [PDF]
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 C. Warmuth, M. Ruping, A. Forschler, H.-C. Koennecke, J. M. Valdueza, A. Kauert, S. J. Schreiber, R. Siekmann, and C. Zimmer Dynamic Spin Labeling Angiography in Extracranial Carotid Artery Stenosis AJNR Am. J. Neuroradiol., May 1, 2005; 26(5): 1035 - 1043. [Abstract] [Full Text] [PDF]
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K. Saito, H. Moriwaki, H. Oe, K. Miyashita, K. Nagatsuka, S. Ueno, and H. Naritomi Mechanisms of Bihemispheric Brain Infarctions in the Anterior Circulation on Diffusion-Weighted Images AJNR Am. J. Neuroradiol., April 1, 2005; 26(4): 809 - 814. [Abstract] [Full Text] [PDF]
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I. Momjian-Mayor and J.-C. Baron The Pathophysiology of Watershed Infarction in Internal Carotid Artery Disease: Review of Cerebral Perfusion Studies Stroke, March 1, 2005; 36(3): 567 - 577. [Abstract] [Full Text] [PDF]
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P. H. Lee, S. -H. Oh, O. Y. Bang, S. -Y. Joo, I. S. Joo, and K. Huh Infarct patterns in atherosclerotic middle cerebral artery versus internal carotid artery disease Neurology, April 27, 2004; 62(8): 1291 - 1296. [Abstract] [Full Text] [PDF]
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S. Koch, A. A. Rabinstein, J. G. Romano, and A. Forteza Diffusion-Weighted Magnetic Resonance Imaging in Internal Carotid Artery Dissection Arch Neurol, April 1, 2004; 61(4): 510 - 512. [Abstract] [Full Text] [PDF]
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D.-W. Kang, J. A. Chalela, M. A. Ezzeddine, and S. Warach Association of Ischemic Lesion Patterns on Early Diffusion-Weighted Imaging With TOAST Stroke Subtypes Arch Neurol, December 1, 2003; 60(12): 1730 - 1734. [Abstract] [Full Text] [PDF]
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P. H. Lee, O. Y. Bang, S. H. Oh, I. S. Joo, and K. Huh Subcortical White Matter Infarcts: Comparison of Superficial Perforating Artery and Internal Border-Zone Infarcts Using Diffusion-Weighted Magnetic Resonance Imaging Stroke, November 1, 2003; 34(11): 2630 - 2635. [Abstract] [Full Text] [PDF]
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R. H. C. Bisschops, C. J. M. Klijn, L. J. Kappelle, A. C. van Huffelen, and J. van der Grond Prevalence and Volume of Internal Border Zone Lesions in Patients With Impaired Cerebral Carbon Dioxide Vasomotor Reactivity: A Follow-up Study Arch Neurol, September 1, 2003; 60(9): 1233 - 1236. [Abstract] [Full Text] [PDF]
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R. H. C. Bisschops, C. J. M. Klijn, L. J. Kappelle, A. C. van Huffelen, and J. van der Grond Association Between Impaired Carbon Dioxide Reactivity and Ischemic Lesions in Arterial Border Zone Territories in Patients With Unilateral Internal Carotid Artery Occlusion Arch Neurol, February 1, 2003; 60(2): 229 - 233. [Abstract] [Full Text] [PDF]
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D.-W. Kang, K. Chu, S.-B. Ko, S.-J. Kwon, B.-W. Yoon, and J.-K. Roh Lesion Patterns and Mechanism of Ischemia in Internal Carotid Artery Disease: A Diffusion-Weighted Imaging Study Arch Neurol, October 1, 2002; 59(10): 1577 - 1582. [Abstract] [Full Text] [PDF]
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M. S. Hochman, J. S. Kim, A. Gass, K. Szabo, and M.G. Hennerici A diffusion-weighted MRI study of acute ischemic distal arm paresis Neurology, August 27, 2002; 59(4): 650 - 650. [Full Text] [PDF]
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W. Steinke and S. C. Ley Lacunar Stroke Is the Major Cause of Progressive Motor Deficits Stroke, June 1, 2002; 33(6): 1510 - 1516. [Abstract] [Full Text] [PDF]
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A. B. Singhal, M. A. Topcuoglu, and F. S. Buonanno Acute Ischemic Stroke Patterns in Infective and Nonbacterial Thrombotic Endocarditis: A Diffusion-Weighted Magnetic Resonance Imaging Study Stroke, May 1, 2002; 33(5): 1267 - 1273. [Abstract] [Full Text] [PDF]
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