 |
|
Lesion Patterns and Mechanism of Ischemia in Internal Carotid Artery Disease
A Diffusion-Weighted Imaging Study
Dong-Wha Kang, MD, PhD;
Kon Chu, MD;
Sang-Bae Ko, MD;
Seon-Joo Kwon, MD;
Byung-Woo Yoon, MD, PhD;
Jae-Kyu Roh, MD, PhD
Arch Neurol. 2002;59:1577-1582.
ABSTRACT
| |
Context Although embolism and low-flow phenomenon are the 2 main mechanisms
of stroke in internal carotid artery (ICA) occlusive disease, the mechanism
of border-zone infarction remains controversial. Diffusion-weighted imaging
(DWI) can more easily detect small or multiple ischemic lesions than conventional
imaging.
Objectives To investigate the ischemic lesion patterns on DWI and to discuss the
mechanisms of stroke in ICA disease.
Design Case series.
Setting A tertiary referral center.
Patients We enrolled 35 consecutive patients who had an acute ischemic stroke
and ( 70%) stenosis or an occlusion of the extracranial ICA confirmed by
cerebral angiography and an acute relevant stroke lesion on DWI within 1 week
of onset, but without cardiac sources of embolism and tandem intracranial
arterial disease.
Main Outcome Measures The lesion pattern on DWI was categorized as territorial or border zone.
Multiple ischemic lesions were defined as noncontiguous lesions on DWI in
more than 1 vascular territory.
Results There were 3 distinctive stroke lesion patterns. (1) A territorial lesion
without a border-zone lesion was found in 21 patients: superficial and superficial
territorial in 9, superficial and deep territorial in 7, and single in 5.
(2) A border-zone lesion with or without a territorial lesion was found in
10 patients: border zone and territorial in 9 and border zone alone in 1.
(3) Bilateral hemispheric lesions were found in 4 patients. Multiple ischemic
lesions were found in 29 (82.9%) of the 35 patients. No patient had episodes
of hemodynamic compromise.
Conclusions An acute ischemic lesion in ICA occlusive disease is mainly multiple.
Border-zone infarction was mostly associated with territorial infarction.
These results support the fact that embolism is the predominant stroke mechanism
in ICA occlusive disease.
INTRODUCTION
THE CLINICAL syndromes from extracranial internal carotid artery (ICA)
occlusive disease result from 2 basic mechanisms—from embolism and from
low flow due to inadequate collateral circulation distal to a hemodynamically
significant stenosis or occlusion.1 Concurrently,
regarding the topography of the ischemic stroke lesion in extracranial ICA
disease, territorial and border-zone infarctions are the 2 major patterns.
Although hemodynamic compromise due to low flow in the border-zone areas has
usually been postulated to explain the infarcts in these regions,2-3 the actual cause of border-zone infarction
is still controversial.
Diffusion-weighted imaging (DWI) is sensitive to acute cellular injury
in cerebral ischemia and can detect ischemic lesions within the first few
hours.4 Diffusion-weighted imaging is superior
to conventional magnetic resonance imaging (MRI) especially for detecting
small or multiple new ischemic lesions.5-10
With this new MRI technique, we observed acute multiple ischemic lesions in
both the territorial and border-zone areas in patients with extracranial ICA
occlusive disease. Based on these observations, we aimed to investigate the
ischemic lesion patterns resulting from ICA occlusive disease using DWI and
to discuss their mechanism.
PATIENTS AND METHODS
We considered 51 consecutive patients with acute ischemic stroke who
were admitted to our stroke unit from July 1997 to June 2001, who had stenosis
(70%) or occlusion of extracranial ICA confirmed by cerebral angiography
using a catheter and had an acute ischemic lesion seen on DWI within 1 week
of the onset of stroke. To determine the stroke pattern caused by ICA disease
itself, we excluded 16 patients with potential cardiac sources of embolism
(n = 4), tandem intracranial occlusive disease (n = 5), or irrelevant ischemic
lesion to ICA disease (n = 7, infratentorial stroke in 4 and contralateral
hemispheric stroke caused by middle cerebral artery [MCA] disease in 3). Thus,
the ischemic lesion patterns in the remaining 35 patients (32 men and 3 woman;
mean age [SD] 63.5 [8.6] years) who had acute ischemic lesion relevant to
ICA disease were analyzed.
CLINICAL EVALUATION
All patients underwent systematic investigations including complete
blood cell count, blood chemistry studies, lipid profiles, coagulation testing,
urinalysis, chest radiography, electrocardiography, transthoracic echocardiography,
computed tomographic scan, MRI, MR angiography, and cerebral angiography.
In selected patients, transesophageal echocardiography including a microbubble
test, 24-hour electrocardiographic monitoring, and transcranial Doppler were
also performed.
The risk factors included hypertension (blood pressure >160/90 mm Hg
on 2 separate occasions), hypercholesterolemia (cholesterol concentration
>0.16 mg/dL [>6.22 mmol/L] or a low-density lipoprotein cholesterol level
>0.11 mg/dL [4.14 mmol/L]), diabetes mellitus, regular cigarette smoking,
myocardial ischemia, arrhythmia, valvular heart disease, a family history
of stroke or ischemic heart disease, and a history of vascular disease or
migraine. Patients with potential cardiac sources of embolism11
were excluded from this study.
ANGIOGRAPHIC EVALUATION
Intra-arterial cerebral angiography by femoral catheterization was performed
within 30 days from the date of the MRI evaluation (mostly within 10 days),
with informed consent from all patients. The degree of stenosis of the extracranial
ICA indicated by angiography was evaluated using the North American Symptomatic
Carotid Endarterectomy Trial method for stenosis measurements.12
Patients with tandem intracranial arterial stenosis (>50%) or occlusion or
dissection of the ICA were excluded from this study.
In an attempt to evaluate the perfusion status, the collateralization
through the circle of Willis, leptomeningeal vessels, and ophthalmic artery
was graded on the basis of capillary blush in cases of ICA occlusion. In cases
of ICA stenosis, it was determined based on the capillary blush by the flow
distal to the stenosis or by collateral flows. The cerebral perfusion was
classified as "poor" if no or minimal capillary blush in the MCA territory
was visible; it was classified as "good" if there were moderate capillary
blush with some filling defect or intact capillary blush in the entire MCA
territory. Perfusion status was blindly determined to the clinical and MRI
data.
MAGNETIC RESONANCE IMAGING
All patients underwent conventional MRI and DWI on a 1.5-T system with
an echoplanar imaging capability (Signa Horizon, Echospeed; General Electric
Medical Systems, Milwaukee, Wis) within 1 week of stroke onset. The conventional
MRI consisted of transverse T2-weighted sequences (repetition time/echo time,
4000/98 milliseconds, 3 excitations) and sagittal T1-weighted sequences (repetition
time/echo time, 450/10 milliseconds, 2 excitations) with 5-mm-thick slices.
Diffusion-weighted imaging was obtained in the transverse plane using a single-shot
echoplanar, spin-echo pulse sequence with a repetition time/echo time of 6500/107
milliseconds, 1 excitation, and 2 b values (0 and 1000 s/mm2).
The diffusion-gradient pulse duration was 31 milliseconds with a gradient
separation of 33 milliseconds and a gradient strength of 2.16 g/cm. The diffusion-gradients
were applied simultaneously along the 3 axes (x, y, and z).
TOPOGRAPHY OF THE ISCHEMIC LESION
The topography of the ischemic lesion was determined using the commonly
accepted arterial supply templates for the territorial13-14
and border-zone areas.15-16 The
arterial territories were divided for the anterior circulation as follows:
ICA, anterior cerebral artery (ACA), superior division of the MCA, inferior
division of the MCA, perforating branches of the MCA, and anterior choroidal
artery. The arterial territories for the posterior circulation were posterior
cerebral artery, basilar artery, and cerebellar arteries.9-10
The diagnosis of multiple ischemic lesions on DWI was made if there were noncontiguous
high-signal intensities on DWI that were present in more than 1 vascular territory.
An uninterrupted lesion visible in contiguous territories was considered a
single lesion.9-10
We divided the ischemic lesion pattern into the territorial and border
zone. The categorization of territorial infarcts was given if the lesion was
located within the corticosubcortical vascular territories of the large cerebral
arteries and their major pial branches.17 Territorial
infarcts were also divided into superficial and deep infarcts. Superficial
infarcts are located in the superficial cortical areas or the vascular territories
supplied by the pial branches of the large cerebral arteries. Deep infarcts
include striatocapsular infarcts and perforating vessel infarcts. A categorization
of striatocapsular infarct was given if the lesion was 15 mm or larger in
diameter and restricted to the territory of the lenticulostriate arteries.18 A perforating vessel infarct was defined as any infarct
with a diameter smaller than 15 mm involving the area supplied by perforators
of the MCA, ACA, ICA, or anterior choroidal artery. Border-zone ischemic lesions
were considered when the lesions involved either the border zone between the
superficial territories of the MCA and ACA (anterior border zone), the border
zone between the superficial territories of the MCA and posterior cerebral
artery (posterior border zone), or the border zone between the superficial
and deep territories of the MCA (subcortical border zone).15-16
Ischemic lesion patterns were also determined without knowing the clinical
and angiographic data.
DATA ANALYSES
The Fisher exact test or  2 test was performed to determine
the presence of a relationship between lesion patterns and various clinical
or radiological findings. Statistical significance was set at P<.05, 2-sided.
RESULTS
GENERAL FEATURES
The neurologic manifestations and radiological features of all patients
are summarized in Figure 1. Twenty-six
patients had first-ever stroke, and 9 patients had recurrent ischemic stroke.
No patient had an episode of hemodynamic compromise that included systemic
hypotension, dehydration, or diarrhea. No patients suffered more than 1 clinical
event from the beginning of the stroke to the neuroradiological evaluation.
The situation at the time of the stroke was normal activity in 19 patients,
on awakening in 15, and traumatic in 1. The mode of symptom progression before
hospitalization was sudden maximal deficit at onset in 16 patients, progressive
in 15, and fluctuating in 4. A history of transient ischemic attack was present
in 12 patients. The risk factors for stroke were regular smoking in 22 patients,
hypertension in 21, diabetes mellitus in 14, a family history of stroke in
6, hypercholesterolemia in 4, ischemic heart disease in 2, malignancies in
2, and peripheral vascular disease in 1. There were no identifiable risk factors
for stroke in 1 patient. No patient had polycythemia (hematocrit of >50%),
but 20 patients had hyperfibrinogenemia (fibrinogen level of >302.63 g/dL
[>10.3 µmol/L]).
|
|
|
|
Clinical and imaging findings in 21 patients with a territorial lesion
without a border-zone lesion (A); 10 patients with a border-zone lesion with
or without a territorial lesion (B); and 4 patients with bilateral hemispheric
lesions (C). Patient 34 had a common anterior cerebral artery trunk supplied
from the left carotid artery for the bilateral anterior cerebral artery territories.
DWI indicates diffusion-weighted imaging; R, right; and L, left.
|
|
|
Twenty-eight patients had unilateral (15 on the right side and 13 on
the left side) ICA occlusive disease; an occlusion in 14 patients, 90% to
99% stenosis in 7, and 70% to 89% stenosis in 7. In those patients who had
stenosis, 7 had a mild stenosis of the contralateral ICA (50%-69% in 3, <50%
in 4). Bilateral ICA occlusive diseases were found in 7 patients; bilateral
occlusions in 1 patient, bilateral stenoses (90%-99%) in 1, unilateral occlusion
and contralateral stenosis (70%-89%) in 2, and unilateral stenosis (90%-99%)
and contralateral stenosis (70%-89%) in 3. Based on the angiographic capillary
blush, 27 patients had good cerebral perfusion and 8 had poor cerebral perfusion.
DISTRIBUTION OF ISCHEMIC LESIONS
Diffusion-weighted imaging was superior to conventional MRI in 23 patients
(65.7%). Diffusion-weighted imaging demonstrated additional ischemic lesions
not observed on conventional MRI in 12 patients. Diffusion-weighted imaging
discriminated recent infarcts from old ones or nonspecific, periventricular
high-signal intensities in 13 patients.
We found 3 distinctive patterns of acute ischemic lesion distribution
(Table 1). First, territorial
distribution without a border-zone lesion in the unilateral hemisphere was
found in 21 patients (Figure 1A). In these patients, 9 had a superficial and superficial pattern (Nos. 1-9),
7 had a superficial and deep pattern (Nos. 10-16), and another 5 had single
lesion (Nos. 17-21).
|
|
|
|
Table 1. Ischemic Lesion Topography of 35 Patients With internal Carotid
Artery Occlusive Disease
|
|
|
Second, border-zone distribution with or without a territorial lesion
in the unilateral hemisphere was found in 10 patients (Figure 1B); 9 of them were associated with superficial or deep territorial
lesion (Nos. 22-30) and only 1 had an acute lesion in the border-zone area
alone (No. 31). The border-zone lesion distribution in those 10 patients was
anterior or posterior cortical border zone in 5, subcortical border zone in
3, and corticosubcortical border zone in 2.
Third, bilateral hemispheric stroke lesions were demonstrated in 4 patients
(Figure 1C). Three patients (Nos.
32, 33, and 35) had bilateral ICA occlusive diseases. All 3 patients had elevated
fibrinogen levels. The other patient (No. 34) with unilateral left-sided ICA
stenosis had a common ACA trunk supplied from the left carotid for the bilateral
ACA territories, which resulted in an ACA infarct contralateral to ICA disease.
Overall, multiple ischemic lesions were found in 29 patients (82.9%).
Among those, 3 patients (Nos. 9, 16, and 33) had multiple lesions in the anterior
and posterior circulations and all 3 had fetal-type posterior cerebral artery
circulation or prominent posterior communicating artery.
CLINICORADIOLOGICAL DIFFERENCE BETWEEN THE PATIENTS WITH TERRITORIAL
LESION ALONE AND THOSE WITH BORDER-ZONE LESION
The various clinical and radiological findings between the patients
with territorial ischemia without (n = 21) and with (n = 10) a border-zone
lesion were compared. No statistically significant difference between these
2 groups in terms of the mode of stroke onset and symptom progression, a history
of transient ischemic attack, hyperfibrinogenemia, bilaterality of ICA disease,
degree of stenosis, and cerebral perfusion status was found (Table 2).
|
|
|
|
Table 2. Comparison Between the Patients With a Territorial Lesion
Alone and Those With a Border-Zone Lesion*
|
|
|
COMMENT
In this study, an attempt was made to analyze the topographical patterns
of acute ischemic lesions in ICA occlusive disease. Despite the small number
of patients, the following methodological advantages were noted. The degree
of ICA stenosis or occlusion was evaluated by cerebral angiography using a
catheter according to the North American Symptomatic Carotid Endarterectomy
Trial method in all patients, providing a high rate of accuracy for assessing
ICA stenosis. Diffusion-weighted imaging was used to determine the ischemic
lesion patterns, giving a high sensitivity for detecting small or multiple
lesions. The patients with potential sources of cardioembolism or tandem intracranial
arterial diseases were excluded; thus the infarct pattern caused by the extracranial
ICA disease itself could be determined.
It was surprising that multiple ischemic lesions were found in 29 patients
with ICA occlusive disease (82.9%) in this study. There have been few studies
that have addressed multiple stroke lesions in ICA disease. A recent study19 reported that only 9% of patients with ICA stenosis
greater than 50% had multiple pial or deep infarcts. The frequency of multiple
infarcts in that study may have been underestimated because they did not use
DWI in evaluating infarct topography. In about two thirds of the patients
in this study, diffused-weighted imaging could identify additional ischemic
lesions that were not observed on conventional MRI or discriminate recent
infarcts from old ones or nonspecific periventricular high-signal intensities.
The overall frequency of acute multiple ischemic lesions on DWI was
reportedly 17%9 and 28.9%.10
Another recent study using DWI20 reported that
57.8% of the patients with ICA disease had various types of multiple ischemic
lesions including subcortical ischemia with embolus fragmentation, disseminated
lesions in distal cortical regions, or multiple lesions in hemodynamic risk
zones. The different frequency between these previous studies and the present
study may partly be owing to the differences in the interval between stroke
onset and imaging, the definition of multiple lesions, inclusion criteria,
and sample size. In addition, large territorial infarction was rare in the
present study, while it was reported to constitute 29.4% of the patients with
ICA disease.20 We believe that the patients
with large territorial infarction could not undergo conventional angiography
owing to severe disability and were possibly excluded from this study.
The main mechanism of acute multiple ischemic lesions was presumed to
be embolism. They could be caused by multiple emboli or the breakup of an
embolus.9 Additionally hypercoagulability and
vascular anatomical variations might also play a role in the pathogenesis
of bihemispheric ischemic lesions.10 Although
no patients had more than 1 clinical event between the stroke onset and the
neuroimaging evaluation in this study, a relatively long interval (1 week)
between onset and imaging might have contributed to the high frequency of
multiple ischemic lesions. Therefore, in the current study multiple lesions
may have occurred simultaneously or within a few days of the clinically relevant
lesion. Nevertheless, these results support the idea that the predominant
mechanism of ischemic stroke in ICA occlusive disease is embolic.21-24
The most common topographical pattern was superficial and superficial
territorial distribution in our study population. It was reported that the
most frequent type of infarct in patients with double infarction in 1 cerebral
hemisphere was also superficial and superficial (47%), and the most common
cause of stroke in that study was ipsilateral ICA disease (72%).25
According to another study, all 7 patients with superficial acute multiple
infarcts in the unilateral cerebral hemisphere were associated with ipsilateral
or bilateral ICA disease, although 2 of them also had a tandem intracranial
carotid stenosis or atrial fibrillation.26
The authors also reported that 4 of 5 patients with multiple ischemic lesions
in the superficial and superficial territories in 1 cerebral hemisphere were
associated with ipsilateral ICA disease.10
It is believed that multiple emboli or the breakup of an embolus that originated
from proximal ICA disease have a high chance of passing through the superior
and inferior divisions of the MCA.
Ten patients (28.6%) with ischemic lesions in border-zone areas were
identified, and 9 of them were associated with a superficial or deep territorial
lesion. This was the other most frequent topographical pattern. Several authors
previously assumed that the mechanism of border-zone infarcts was hemodynamic
based on the computed tomography or MRI topography of these infarcts.27-32
However, Belden et al33 reported in 1999 that
embolism was the predominant stroke mechanism in unilateral posterior border-zone
infarcts, whereas bilateral lesions were due to systemic hypotension. They
suggested that variability of the territories of the major cerebral arteries,34-36 the passage of emboli
to the border-zone areas, and the decreased clearance (washout) of the emboli
in these areas37 could be explanations for
the unilateral border-zone lesions.33 The coexistence
of a border-zone lesion with multiple embolic infarcts on DWI has recently
been documented in patients with neurologic complications after cardiac surgery.38 As postulated by Caplan and Hennerici,37
altered physics of blood flow probably caused by decreased perfusion in hemodynamically
significant ICA disease may encourage emboli to reach border-zone regions,
and decreased blood flow also likely impedes clearance of emboli because perfusion
is most impaired in border-zone regions. The fact that no patient in our study
had a documented systemic hypotension and border-zone infarction was mostly
associated with a territorial infarct supports the idea that the mechanism
of border-zone infarct is predominantly embolic.
Bilateral hemispheric infarcts associated with bilateral ICA disease
were identified in 3 patients (8.6%). All 3 patients had elevated fibrinogen
levels. We believe that bilateral cerebral infarcts were probably caused by
bilateral ICA disease because we could not find either potential cardiac sources
of embolism or any systemic causes for stroke in these patients. It was previously
reported that bilateral cerebral infarcts were caused mainly by large artery
atherosclerosis and were significantly associated with malignancy, an elevated
fibrinogen level, and polycythemia.10 Although
the factors that determine the contemporary bilateral infarcts remain still
unclear, hypercoagulable state, infection, or inflammatory process might increase
acute-phase reactants and render bilateral ICA occlusive lesions symptomatic
at the same time.
Bogousslavsky and Regli15, 30
reported that syncope at onset, focal limb shaking, hemodynamically significant
cardiopathy, increased hematocrit, or severe contralateral ICA disease were
significantly associated with unilateral border-zone infarction. However,
no patient with syncope at onset or focal limb shaking was identified in this
study. Furthermore, no difference was found between the patients with territorial
lesion alone and those with border-zone lesion in terms of the mode of stroke
onset and symptom progression, a previous history of transient ischemic attack,
an elevated fibrinogen level, bilaterality of ICA disease, the degree of stenosis,
and cerebral perfusion status. This again suggested an embolic mechanism for
these infarcts.
CONCLUSIONS
This study shows that the ischemic lesion patterns caused by ICA occlusive
disease are mainly multiple, and most border-zone ischemic lesions are accompanied
by territorial ischemia. We suggest that these results provide supporting
evidence that embolism is the predominant stroke mechanism in patients who
have ICA disease.
AUTHOR INFORMATION
Accepted for publication April 5, 2002.
Author contributions: Study concept and design (Drs Kang, Chu, Ko, Yoon, and Roh); acquisition of data (Drs Kang, Chu, Ko, Kwon, and Yoon); analysis and interpretation
of data (Drs Kang, Chu, Ko, and Yoon); drafting of
the manuscript (Drs Kang, Chu, Ko, and Yoon); critical
revision of the manuscript for important intellectual content (Drs Kang, Chu, Ko, Kwon, and Yoon); obtained funding (Dr Roh); administrative, technical, and material support (Drs Kang, Chu, Ko, Yoon, and Roh); study supervision (Drs Kang, Chu, Ko, Yoon, and Roh).
This study was supported by the Seoul National University Hospital Research
Fund.
Corresponding author and reprints: Jae-Kyu Roh, MD, PhD, Department
of Neurology, Seoul National University Hospital, 28 Yongon-dong, Chongno-gu,
Seoul, 110-744, South Korea (e-mail: rohjk{at}snu.ac.kr).
From the Department of Neurology and Clinical Research Institute, Seoul
National University Hospital, Neuroscience Research Institute of Seoul University
Medical Research Center, Seoul, South Korea (Drs Kang, Chu, Ko, Kwon, Yoon,
and Roh); and the Section on Stroke Diagnostics and Therapeutics, National
Institute of Neurological Disorders and Stroke, Bethesda, Md (Dr Kang).
REFERENCES
| |
1. Mohr JP, Gautier JC, Pessin MS. Internal carotid artery disease. In: Barnett HJM, Mohr JP, Stein BM, Yatsu FM, eds. Stroke: Pathophysiology, Diagnosis, and Management. Philadelphia, Pa:
WB Saunders Co; 1998:355-400.
2. Adams JH, Brierley JB, Connor RC, Treip CS. The effects of systemic hypotension upon the human brain: clinical
and neuropathological observations in 11 cases. Brain. 1966;89:235-268.
FREE FULL TEXT
3. Brierley JB, Prior PF, Calverley J, Jackson SJ, Brown AW. The pathogenesis of ischaemic neuronal damage along the cerebral arterial
boundary zones in Papio anubis. Brain. 1980;103:929-965.
FREE FULL TEXT
4. Schabitz WR, Fisher M. Diffusion weighted imaging for acute cerebral infarction. Neurol Res. 1995;17:270-274.
ISI
| PUBMED
5. Warach S, Gaa J, Siewert B, Wielopolski P, Edelman RR. Acute human stroke studied by whole brain echo planar diffusion-weighted
magnetic resonance imaging. Ann Neurol. 1995;37:231-241.
FULL TEXT
|
ISI
| PUBMED
6. Lutsep HL, Albers GW, de Crespigny A, Kamat GN, Marks MP, Moseley ME. Clinical utility of diffusion-weighted magnetic resonance imaging in
the assessment of ischemic stroke. Ann Neurol. 1997;41:574-580.
FULL TEXT
|
ISI
| PUBMED
7. Schlaug G, Siewert B, Benfield A, Edelman RR, Warach S. Time course of the apparent diffusion coefficient (ADC) abnormality
in human stroke. Neurology. 1997;49:113-119.
FREE FULL TEXT
8. Singer MB, Chong J, Lu D, Schonewille WJ, Tuhrim S, Atlas SW. Diffusion-weighted MRI in acute subcortical infarction. Stroke. 1998;29:133-136.
FREE FULL TEXT
9. Baird AE, Lovblad KO, Schlaug G, Edelman RR, Warach S. Multiple acute stroke syndrome: marker of embolic disease? Neurology. 2000;54:674-678.
FREE FULL TEXT
10. Roh JK, Kang DW, Lee SH, Yoon BW, Chang KH. Significance of acute multiple brain infarction on diffusion-weighted
imaging. Stroke. 2000;31:688-694.
FREE FULL TEXT
11. Adams HP Jr, Bendixen BH, Kappelle LJ, et al for TOAST (Trial of Org 10172 in Acute Stroke Treatment). Classification of subtype of acute ischemic stroke: definitions for
use in a multicenter clinical trial. Stroke. 1993;24:35-41.
FREE FULL TEXT
12. The North American Symptomatic Carotid Endarterectomy Trial collaborators. Beneficial effects of carotid endarterectomy in symptomatic patients
with high-grade carotid stenosis. N Engl J Med. 1991;325:445-453.
ABSTRACT
13. Ghika JA, Bogousslavsky J, Regli F. Deep perforators from the carotid system: template of the vascular
territories. Arch Neurol. 1990;47:1097-1100.
FREE FULL TEXT
14. Tatu L, Moulin T, Bogousslavsky J, Duvernoy H. Arterial territories of the human brain: cerebral hemisphere. Neurology. 1998;50:1699-1708.
ABSTRACT
15. Bogousslavsky J, Regli F. Unilateral watershed cerebral infarcts. Neurology. 1986;36:373-377.
FREE FULL TEXT
16. Ringelstein EB, Stögbauer F. Border-zone infarcts. In: Bogousslavsky J, Caplan L, eds. Stroke Syndromes. 2nd ed. New York, NY: Cambridge University Press; 2001:564-582.
17. Damasio H. A computed tomographic guide to the identification of cerebral vascular
territories. Arch Neurol. 1983;40:138-142.
FREE FULL TEXT
18. Ringelstein EB, Weiller C, Weckesser M, Weckesser S. Cerebral vasomotor reactivity is significantly reduced in low-flow
as compared to thromboembolic infarctions: the key role of the circle of Willis. J Neurol Sci. 1994;121:103-109.
FULL TEXT
|
ISI
| PUBMED
19. Tsiskaridze A, Devuyst G, de Freitas GR, van Melle G, Bogousslavsky J. Stroke with internal carotid artery stenosis. Arch Neurol. 2001;58:605-609.
FREE FULL TEXT
20. Szabo K, Kern R, Gass A, Hirsch J, Hennerich M. Acute stroke patterns in patients with internal carotid artery disease:
a diffusion-weighted magnetic resonance imaging study. Stroke. 2001;32:1323-1329.
FREE FULL TEXT
21. Fieschi C, Argentino C, Lenzi GL, Sacchetti ML, Toni D, Bozzao L. Clinical and instrumental evaluation of patients with ischemic stroke
within the first six hours. J Neurol Sci. 1989;91:311-321.
FULL TEXT
|
ISI
| PUBMED
22. Ringelstein EB, Biniek R, Weiller C, Ammeling B, Nolte PN, Thron A. Type and extent of hemispheric brain infarctions and clinical outcome
in early and delayed middle cerebral artery recanalization. Neurology. 1992;42:289-298.
FREE FULL TEXT
23. Wolpert SM, Bruckmann H, Greenlee R, Wechsler L, Pessin MS, del Zoppo G for the rt-PA Acute Stroke Study Group. Neuroradiologic evaluation of patients with acute stroke
treated with recombinant tissue plasminogen activator. Am J Neuroradiol. 1993;14:3-13.
ABSTRACT
24. Klijn CJ, Kappelle LJ, Tulleken CA, van Gijn J. Symptomatic carotid artery occlusion: a reappraisal of hemodynamic
factors. Stroke. 1997;28:2084-2093.
FREE FULL TEXT
25. Bogousslavsky J. Double infarction in one cerebral hemisphere. Ann Neurol. 1991;30:12-18.
FULL TEXT
|
ISI
| PUBMED
26. Bogousslavsky J, Bernasconi A, Kumral E. Acute multiple infarction involving the anterior circulation. Arch Neurol. 1996;53:50-57.
FREE FULL TEXT
27. Wodarz R. Watershed infarctions and computed tomography: a topographical study
in cases with stenosis or occlusion of the carotid artery. Neuroradiology. 1980;19:245-248.
ISI
| PUBMED
28. Ringelstein EB, Zeumer H, Angelou D. The pathogenesis of strokes from internal carotid artery occlusion:
diagnostic and therapeutical implications. Stroke. 1983;14:867-875.
FREE FULL TEXT
29. Rodda RA. The arterial patterns associated with internal carotid disease and
cerebral infarcts. Stroke. 1986;17:69-75.
FREE FULL TEXT
30. Bogousslavsky J, Regli F. Borderzone infarctions distal to internal carotid artery occlusion:
prognostic implications. Ann Neurol. 1986;20:346-350.
FULL TEXT
|
ISI
| PUBMED
31. Leblanc R, Yamamoto YL, Tyler JL, Diksic M, Hakim A. Borderzone ischemia. Ann Neurol. 1987;22:707-713.
FULL TEXT
|
ISI
| PUBMED
32. Mounier-Vehier F, Leys D, Pruvo JP. Stroke patterns in unilateral atherothrombotic occlusion of the internal
carotid artery. Stroke. 1995;26:422-425.
FREE FULL TEXT
33. Belden JR, Caplan LR, Pessin MS, Kwan E. Mechanisms and clinical features of posterior border-zone infarcts. Neurology. 1999;53:1312-1318.
FREE FULL TEXT
34. van der Zwan A, Hillen B, Tulleken CA, Dujovny M, Dragovic L. Variability of the territories of the major cerebral arteries. J Neurosurg. 1992;77:927-940.
ISI
| PUBMED
35. van der Zwan A, Hillen B, Tulleken CA, Dujovny M. A quantitative investigation of the variability of the major cerebral
arterial territories. Stroke. 1993;24:1951-1959.
FREE FULL TEXT
36. van der Zwan A, Hillen B. Review of the variability of the territories of the major cerebral
arteries. Stroke. 1991;22:1078-1084.
FREE FULL TEXT
37. Caplan LR, Hennerici M. Impaired clearance of emboli (washout) is an important link between
hypoperfusion, embolism, and ischemic stroke. Arch Neurol. 1998;55:1475-1482.
FREE FULL TEXT
38. Wityk RJ, Goldsborough MA, Hillis A, et al. Diffusion- and perfusion-weighted brain magnetic resonance imaging
in patients with neurologic complications after cardiac surgery. Arch Neurol. 2001;58:571-576.
FREE FULL TEXT
 CiteULike  Connotea  Del.icio.us  Digg  Reddit  Technorati
What's this?
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
|
Quantitative Assessment of Mixed Cerebral Vascular Territory Supply With Vessel Encoded Arterial Spin Labeling MRI
Kansagra and Wong
Stroke 2008;39:2980-2985.
ABSTRACT
| FULL TEXT
Early neurological deterioration in acute ischaemic stroke: predictors, mechanisms and management
Thanvi et al.
Postgrad. Med. J. 2008;84:412-417.
ABSTRACT
| FULL TEXT
Higher prevalence of cortical lesions observed in patients with acute stroke using high-resolution diffusion-weighted imaging.
Benameur et al.
Am. J. Neuroradiol. 2006;27:1987-1989.
ABSTRACT
| FULL TEXT
Internal and Cortical Border-Zone Infarction: Clinical and Diffusion-Weighted Imaging Features
Yong et al.
Stroke 2006;37:841-846.
ABSTRACT
| FULL TEXT
Lesion Patterns and Stroke Mechanism in Atherosclerotic Middle Cerebral Artery Disease: Early Diffusion-Weighted Imaging Study
Lee et al.
Stroke 2005;36:2583-2588.
ABSTRACT
| FULL TEXT
Diffusion-Weighted Magnetic Resonance Imaging in Symptomatic Vertebrobasilar Atherosclerosis and Dissection
Koch et al.
Arch Neurol 2005;62:1228-1231.
ABSTRACT
| FULL TEXT
Predictors of Early Arterial Reocclusion After Tissue Plasminogen Activator-Induced Recanalization in Acute Ischemic Stroke
Rubiera et al.
Stroke 2005;36:1452-1456.
ABSTRACT
| FULL TEXT
Mechanisms of Bihemispheric Brain Infarctions in the Anterior Circulation on Diffusion-Weighted Images
Saito et al.
Am. J. Neuroradiol. 2005;26:809-814.
ABSTRACT
| FULL TEXT
The Pathophysiology of Watershed Infarction in Internal Carotid Artery Disease: Review of Cerebral Perfusion Studies
Momjian-Mayor and Baron
Stroke 2005;36:567-577.
ABSTRACT
| FULL TEXT
Infarct patterns in atherosclerotic middle cerebral artery versus internal carotid artery disease
Lee et al.
Neurology 2004;62:1291-1296.
ABSTRACT
| FULL TEXT
Diffusion-Weighted Magnetic Resonance Imaging in Internal Carotid Artery Dissection
Koch et al.
Arch Neurol 2004;61:510-512.
ABSTRACT
| FULL TEXT
Association of Ischemic Lesion Patterns on Early Diffusion-Weighted Imaging With TOAST Stroke Subtypes
Kang et al.
Arch Neurol 2003;60:1730-1734.
ABSTRACT
| FULL TEXT
From the library
Br. J. Ophthalmol. 2003;87:520-520.
FULL TEXT
|
