AJR 2002; 179:237-243
© American Roentgen Ray Society
Signs of Acute Stroke Seen on Fluid-Attenuated Inversion Recovery MR Imaging
Smitha Makkat1,
Jan E. Vandevenne2,
Geert Verswijvel2,
Toon Ijsewijn3,
Martijn Grieten2,
Yvan Palmers2,
Arthur M. De Schepper1 and
Paul M. Parizel1
1 Department of Radiology, University Hospital Antwerp, University of Antwerp,
Wilrijkstraat 10, B-2650 Edegem, Belgium.
2 Department of Radiology, Ziekenhuis Oost Limburg (Campus St-Jan), Schiepse Bos
6, B-3600 Genk, Belgium.
3 Department of Neurology, Ziekenhuis Oost Limburg (Campus St-Jan), B-3600 Genk,
Belgium.
Received August 6, 2001;
accepted after revision January 10, 2002.
Address correspondence to P. M. Parizel.
Introduction
Stroke is defined clinically as a neurologic deficit of sudden onset. The
prompt diagnosis of the cause—such as infarction or hemorrhage—is
critical for the immediate initiation of the appropriate therapy, which
differs for different causes. In recent years, MR imaging has become an
established tool for the evaluation of stroke in patients in the hyperacute
(typically 0-6 hr from symptom onset) and acute (first few days after symptom
onset) stages. Although diffusion- and perfusion-weighted sequences have been
acknowledged as the most sensitive in the hyperacute stage, more widely
available conventional techniques such as fluid-attenuated inversion recovery
(FLAIR) MR sequences also reveal interesting signs in both hyperacute and
acute stages of stroke. In this pictorial essay, we present an overview of the
unique signs observed on FLAIR images during the first 24 hr after the onset
of symptoms.
Principles and Methods
The FLAIR MR imaging sequence produces a heavily T2-weighted image with
nulling of the signal of cerebrospinal fluid using an inversion time that
usually ranges from 1800 to 2500 msec. By suppressing the signal intensity of
bulk water, FLAIR images increase the conspicuity of lesions located in areas
adjacent to or filled with cerebrospinal fluid. This property gives FLAIR
images their unique characteristics.
Two often mentioned disadvantages of FLAIR MR sequences are cerebrospinal
fluid flow artifacts and the long acquisition time required for imaging a
limited number of slices. Pulsatile cerebrospinal fluid flow generates inflow
effects in the selected slice during the inversion time interval, which cause
incomplete nulling of cerebrospinal fluid signal intensities. As a result,
hyperintense artifacts appear in areas of prominent cerebrospinal fluid
pulsation, such as the foramen of Monro, third and fourth ventricles, and the
prepontine cistern [1]. These
pulsation artifacts can be remedied by increasing the width of the
slice-selective inversion section beyond that of the imaging section, so that
inflowing spins from cerebrospinal fluid outside the imaging section are not
nulled. The limitation of long acquisition times can be overcome either by
applying fast or turbo techniques to the FLAIR sequence or by combining FLAIR
with echoplanar imaging in a sequence.
Imaging Features
Hyperintense Vessel Sign
Increased signal intensity in the lumen of large and small vessels may be
observed on FLAIR images as the only indication of infarction, a finding that
has been called the "hyperintense vessel sign" or arterial
hyperintensity [2] (Fig.
1A,1B,1C,1D).
The physiopathologic basis of this phenomenon remains unclear. Several
hypotheses have been proposed, such as slowly moving or stationary blood,
intraluminal thrombus or embolus, or even retrograde collateral circulation
[2,3,4].
Maeda et al. [5] found that the
hyperintense vessel sign was most frequently observed at the sylvian fissure
(87%), followed by the cortical sulci (54%) and the horizontal segments of the
middle cerebral arteries (29%) in the affected middle cerebral artery
distribution. The hyperintense vessel sign is seen less frequently in the
posterior cerebral arteries
[3]. The sensitivity of the
hyperintense vessel sign is highest during the first 6 hr after symptom onset;
thereafter, the detection rate declines over time
[6].
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Fig. 1A. —Superiority of hyperintense vessel sign on fluid-attenuated
inversion recovery (FLAIR) MR image over visualization of lack of flow void on
T2-weighted MR image in diagnosing vascular occlusion in 62-year-old man with
left hemiparesis. Patient underwent scanning approximately 10 hr after symptom
onset. FLAIR MR image at level of mesencephalon shows hyperintense vessel sign
in M1 and M2 segments (arrows) of right middle cerebral artery.
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Fig. 1B. —Superiority of hyperintense vessel sign on fluid-attenuated
inversion recovery (FLAIR) MR image over visualization of lack of flow void on
T2-weighted MR image in diagnosing vascular occlusion in 62-year-old man with
left hemiparesis. Patient underwent scanning approximately 10 hr after symptom
onset. T2-weighted MR image at level of mesencephalon shows lack of flow void
in M1 and M2 segments of right middle cerebral artery, which is poorly
demarcated from surrounding brain tissue and bright cerebrospinal fluid
(arrow).
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Fig. 1C. —Superiority of hyperintense vessel sign on fluid-attenuated
inversion recovery (FLAIR) MR image over visualization of lack of flow void on
T2-weighted MR image in diagnosing vascular occlusion in 62-year-old man with
left hemiparesis. Patient underwent scanning approximately 10 hr after symptom
onset. FLAIR MR image at level of foramen of Monro shows hyperintense swelling
in right insula and putamen (arrowheads).
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Fig. 1D. —Superiority of hyperintense vessel sign on fluid-attenuated
inversion recovery (FLAIR) MR image over visualization of lack of flow void on
T2-weighted MR image in diagnosing vascular occlusion in 62-year-old man with
left hemiparesis. Patient underwent scanning approximately 10 hr after symptom
onset. Diffusion-weighted MR image at level of foramen of Monro shows high
signal intensity in right middle cerebral arterial territory, suggesting
infarction (arrow).
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Occlusion of intracranial arteries is visible as the lack of a flow void in
bright cerebrospinal fluid on T2-weighted MR images (Fig.
1A,1B,1C,1D).
However, FLAIR MR images show intraarterial thrombus or slow arterial flow
more clearly as a hyperintense vessel surrounded by hypointense cerebrospinal
fluid [3]. In particular, the
involvement of small insular arteries is better seen on FLAIR images than on
T2-weighted images (Figs. 2A
and 2B). The mechanisms of
intravascular enhancement on contrast-enhanced T1-weighted imaging and the
hyperintense vessel sign are related. Although the hyperintense vessel sign is
usually less conspicuous and less extensive than arterial enhancement, when
present, this finding represents an early sign of infarction
[6] (Fig.
3A,3B,3C).
Likewise, the hyperintense vessel sign on FLAIR images corresponds to a loss
of high intraluminal signal on three-dimensional time-of-flight MR angiography
(Fig.
3A,3B,3C).
However, the FLAIR sequence has proven to be more useful than MR angiography
in predicting ischemic areas
[4].
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Fig. 2A. —65-year-old woman with right-sided weakness and speech
disturbances. MR imaging, performed within 90 min of onset of symptoms, shows
hyperintense vessels and perfusion deficit but, at this time, only slightly
restricted diffusion. Fluid-attenuated inversion recovery MR image shows
punctiform hyperintense vessels in left sylvian fissure (arrows),
suggesting slow flow or thrombosis in insular branches of middle cerebral
artery.
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Fig. 2B. —65-year-old woman with right-sided weakness and speech
disturbances. MR imaging, performed within 90 min of onset of symptoms, shows
hyperintense vessels and perfusion deficit but, at this time, only slightly
restricted diffusion. T2-weighted MR image shows lack of flow void in insular
branches of left middle cerebral artery (arrows). Compare with normal
contralateral side.
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Fig. 3A. —Hyperintense vessel sign and intravascular contrast
enhancement in 68-year-old woman with right-sided weakness. MR imaging was
performed within 4 hr of symptom onset. Fluid-attenuated inversion recovery MR
image shows tubular area of hyperintense signal in M2 segment of left middle
cerebral artery (arrow); this finding corresponds to slow flow or
thrombosis.
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Fig. 3B. —Hyperintense vessel sign and intravascular contrast
enhancement in 68-year-old woman with right-sided weakness. MR imaging was
performed within 4 hr of symptom onset. Three-dimensional time-of-flight MR
angiogram obtained in coronal plane confirms absence of normal flow in left
middle cerebral artery (arrow).
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Fig. 3C. —Hyperintense vessel sign and intravascular contrast
enhancement in 68-year-old woman with right-sided weakness. MR imaging was
performed within 4 hr of symptom onset. Contrast-enhanced T1-weighted MR image
shows vascular enhancement in insular branches of left middle cerebral artery
(arrows), which is consistent with stasis of arterial contrast
material.
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The presence of the hyperintense vessel sign, along with positive
diffusion-weighted MR imaging findings, indicates impending infarction and
should prompt consideration of revascularization and flow augmentation
strategies [3,
6]. Occasionally, the
hyperintense vessel sign on FLAIR MR images can precede diffusion
abnormalities [6] (Fig.
2A,2B,2C,2D,2E).
Toyoda et al. [3] reported that
the area of the hyperintense vessel sign was almost equal to that of a
perfusion abnormality, particularly in patients examined within 6 hr of
symptom onset. The hyperintense vessel sign can easily be missed if the
radiologist does not actively look for it.
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Fig. 2C. —65-year-old woman with right-sided weakness and speech
disturbances. MR imaging, performed within 90 min of onset of symptoms, shows
hyperintense vessels and perfusion deficit but, at this time, only slightly
restricted diffusion. Three-dimensional time-of-flight MR angiogram obtained
in coronal plane reveals absence of normal flow in left middle cerebral artery
(arrow) beyond M1 segment.
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Fig. 2D. —65-year-old woman with right-sided weakness and speech
disturbances. MR imaging, performed within 90 min of onset of symptoms, shows
hyperintense vessels and perfusion deficit but, at this time, only slightly
restricted diffusion. Perfusion MR image shows prolongation of
"time-to-peak" in left middle cerebral artery distribution
(arrows).
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Fig. 2E. —65-year-old woman with right-sided weakness and speech
disturbances. MR imaging, performed within 90 min of onset of symptoms, shows
hyperintense vessels and perfusion deficit but, at this time, only slightly
restricted diffusion. Diffusion-weighted MR image does not show marked
diffusion restriction. Among various explanations for this rare observation,
most convincing possibility is that cerebral blood flow is at intermediate
level—below threshold for neuronal dysfunction (symptom onset) but above
that of restricted diffusion
[6]. Note periventricular
hyperintense signal caused by white matter anisotropy.
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Hyperintense Swollen Cortical Gyri
Acute cerebral infarcts can appear on the FLAIR MR image as swollen
cortical gyri of increased signal intensity
[2]. Typically these gyriform
areas are moderately hyperintense and are not sharply demarcated (Fig.
4A,4B).
These findings represent edema of brain parenchyma (cytotoxic edema), which
develops more rapidly in gray matter than in white matter because of its
higher metabolic activity. During the acute stage of infarction, the increase
in parenchymal water is estimated to be 3%
[2]. This change results in
slightly prolonged T2 relaxation of edematous cortical gyri, which is shown as
areas of high signal intensities on both FLAIR and T2-weighted MR images.
FLAIR imaging depicts these areas more clearly than T2-weighted imaging by
suppressing the signal of the cerebrospinal fluid in the adjacent cortical
sulci and the neighboring brain parenchyma (Fig.
5A,5B,5C).
Hyperintense swollen cortical gyri are well related to the areas of acute
ischemia on diffusion-weighted MR images (Figs.
5A,5B,5C
and
6A,6B).
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Fig. 4A. —Hyperintense swollen cortical gyri in 36-year-old woman
receiving anticoagulant therapy who developed sudden onset of speech
disturbance and right-sided weakness. MR imaging was performed within 8 hr
after symptom onset. Fluid-attenuated inversion recovery MR image shows
multiple swollen hyperintense cortical gyri in left insula (thick
arrow). These gyriform, hazy areas of hyperintensity are not sharply
demarcated. Compare these areas of hyperintensity with hyperintensity of old
infarct in left frontal lobe anteriorly, which is more sharply demarcated
(thin arrow). Note tubular area of hyperintense signal in M2 segment
of left middle cerebral artery.
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Fig. 4B. —Hyperintense swollen cortical gyri in 36-year-old woman
receiving anticoagulant therapy who developed sudden onset of speech
disturbance and right-sided weakness. MR imaging was performed within 8 hr
after symptom onset. Diffusion-weighted MR image shows high signal intensity
in left middle cerebral artery territory (arrow); this finding is
indicative of acute ischemia. Lack of diffusion restriction in lesion
anteriorly in frontal lobe indicates that this lesion is not acute
infarct.
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Fig. 5A. —28-year-old woman with right hemiplegia and aphasia who
underwent MR imaging 2 hr after symptom onset. Hyperintense swollen cortical
gyri are well related to areas of acute ischemia on diffusion-weighted MR
imaging. Fluid-attenuated inversion recovery MR image shows area of
hyperintensity and loss of insular ribbon in left insular cortex
(arrow), which are suggestive of cytotoxic edema. Old infarct appears
as area of well-demarcated hyperintensity in left posterior temporal lobe
cortex.
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Fig. 5B. —28-year-old woman with right hemiplegia and aphasia who
underwent MR imaging 2 hr after symptom onset. Hyperintense swollen cortical
gyri are well related to areas of acute ischemia on diffusion-weighted MR
imaging. Diffusion-weighted MR image confirms diffusion restriction
(arrow) in this area, which is indicative of acute ischemia.
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Fig. 5C. —28-year-old woman with right hemiplegia and aphasia who
underwent MR imaging 2 hr after symptom onset. Hyperintense swollen cortical
gyri are well related to areas of acute ischemia on diffusion-weighted MR
imaging. Corresponding apparent diffusion coefficient map shows area of acute
infarct as hypointense region (arrow).
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Fig. 6A. —53-year-old man with acute onset of speech disturbance. MR
imaging at 6 hr after onset of symptoms shows acute infarct in Broca area on
left. Fluid-attenuated inversion recovery MR image shows one hyperintense
swollen gyrus in left frontal lobe (arrow). This finding represents
cytotoxic edema of cortical gray matter, which gradually diminishes toward
inner aspect and thus appears hazy.
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Fig. 6B. —53-year-old man with acute onset of speech disturbance. MR
imaging at 6 hr after onset of symptoms shows acute infarct in Broca area on
left. Diffusion-weighted MR image confirms diffusion restriction
(arrow), which is indicative of acute ischemia.
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Hyperintense Intracranial Hemorrhage
Hyperacute hemorrhagic lesions are well visualized on FLAIR MR images as
high-signal-intensity areas against a muted background of nulled cerebrospinal
fluid signal and low-signal-intensity brain tissue
[7]. Epidural and subdural
hemorrhages often exhibit a particular morphology, depending on their location
(Fig.
7A,7B).
FLAIR sequences are most useful in detecting subarachnoid hemorrhage (Fig.
8A,8B)
and intraventricular hemorrhage (Fig.
9). Bloody cerebrospinal fluid differs markedly in relaxation
times from normal cerebrospinal fluid and will appear hyperintense
[8]. Bakshi et al.
[9] found that FLAIR MR imaging
had a sensitivity of 92% and a specificity of 100% in the detection of acute
intraventricular hemorrhage in the lateral ventricles. The sensitivity of
FLAIR imaging for detection of hemorrhage is high, but its role compared with
CT and gradient-echo sequences has yet to be established.
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Fig. 7A. —58-year-old man with subdural hemorrhage who underwent MR
imaging within 24 hr after onset of symptoms. Fluid-attenuated inversion
recovery MR image shows hyperintense area with concave inner margin overlying
right frontoparietal cerebral convexity (arrow).
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Fig. 7B. —58-year-old man with subdural hemorrhage who underwent MR
imaging within 24 hr after onset of symptoms. T2-weighted MR image in which
hematoma is not visible because of poor contrast between subdural hemorrhage
and cerebrospinal fluid.
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Fig. 8A. —63-year-old woman with acute onset of right hemiplegia. CT
and MR imaging, performed within 2 hr after onset of symptoms, show
subarachnoid hemorrhage. Fluid-attenuated inversion recovery (FLAIR) MR image
shows high signal intensity in subarachnoid space overlying cortical gyri in
left insula. Note also high signal intensity surrounding splenium of corpus
callosum and in sulci on medial side of occipital lobes (arrows).
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Fig. 8B. —63-year-old woman with acute onset of right hemiplegia. CT
and MR imaging, performed within 2 hr after onset of symptoms, show
subarachnoid hemorrhage. CT image obtained at same level as A shows
hyperdensities in same locations (arrows) as on FLAIR image
(A), thus confirming diagnosis of subarachnoid hemorrhage.
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Fig. 9. —Intraventricular hemorrhages in 47-year-old woman appear as
high-signal-intensity foci on fluid-attenuated inversion recovery (FLAIR) MR
image. Hemorrhagic sedimentation levels are seen in third ventricle and in
occipital horns of lateral ventricles (arrows). FLAIR MR imaging is
highly sensitive and specific in detection of intraventricular hemorrhage in
lateral ventricles. However, detection of intraventricular hemorrhage in third
and fourth ventricles may be compromised by artifacts.
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Venous Thrombosis
Thrombosis of the dural venous sinuses is observed as an intravascular area
of high signal intensity on FLAIR MR images. The bright signal within the
dural sinuses or bridging veins can be explained by the presence of slow
venous flow or thrombus (paradoxical enhancement). However, phase-contrast MR
angiography and contrast-enhanced T1-weighted spin-echo MR imaging are
superior in the detection of venous thrombosis.
Conclusion
FLAIR MR images are useful in evaluating patients presenting with symptoms
of acute stroke. The cardinal findings of acute ischemic stroke on FLAIR
images are the hyperintense vessel sign and the presence of hyperintense
swollen cortical gyri. In our opinion, the addition of a FLAIR sequence to the
routine stroke protocol facilitates the decision to start thrombolytic
therapy. On the other hand, FLAIR imaging may be useful in showing
intracranial hemorrhage (especially subarachnoid hemorrhage and
intraventricular hemorrhages), which contraindicates thrombolytic therapy.
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Introduction
Principles and Methods
