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Current Concepts of Cerebrovascular Disease and Stroke
Magnetic Resonance Angiography
Cerebrovascular Applications
Paul M. Ruggieri, MD; Thomas J. Masaryk, MD; and Jeffrey S. Ross, MD
M
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agnetic resonance angiography (MRA) can
provide significant additional information to
complement the routine spin-echo MR examination of the brain.1"13 The idea of a combined study
has gained favor because it provides a noninvasive
alternative for the complete study of patients with
suspected cerebrovascular disease. Because of the relatively short time of acquisition, MRA sequences can be
easify added to the traditional parenchymal study without significantly prolonging the overall examination
time (Figure 1).
Magnetic resonance is able to create anatomic images
through the use of radiofrequency (RF) excitation and
refocusing pulses as well as spatial localizing magnetic
field gradients. Motion (blood flow) in the presence of
the RF pulse sequence creates time-of-flight (TOF)
effects on the signal of moving protons, while proton
motion during the application and in the direction of
the magnetic field gradients produces spin phase phenomena. Each of these effects can be manipulated
relatively independently to create vascular contrast
within a given scan and thus angiographic images.
TOF techniques create vascular contrast via the
inflow of blood protons into a region of interest previously prepared by an RF excitation, inversion, or saturation pulse. The most popular techniques consist of
relatively simple gradient echo pulse sequences where
the inflow of spins produces high signal within the
vessels on the basis of the TOF effects known as "entry
slice phenomenon" or "flow-related enhancement."
Angiographic images can then be derived from such
data sets through the use of computer post-processing
techniques which obviate the need for mask acquisitions
to create a subtraction angiogram. Since TOF MRA
requires only a single data set, the acquisition is less
susceptible to problems, such as patient motion and
eddy currents, which arise with longer examination
times and multiple data sets.111 TOF data also require
less computer memory and post-processing following
the acquisition. Although the phase contrast techniques
are more sensitive to very slow flow, the TOF techniques may be less vulnerable to the phase dispersion
(and signal loss) that accompanies complex motion
typically seen in regions of arterial flow (i.e., tortuous
vessels, stenoses).12-13
All MRA techniques may be implemented in a 2D or
3D mode. Two-dimensional Fourier transform imaging
(2DFT) acquires data in the conventional fashion in
which individually acquired image slices are stacked
sequentially. With 3D Fourier transform (3DFT) acquisitions an entire block or "slab" of anatomic digital data
is acquired. This may then be displayed as individual
slices reconstructed in any plane or perhaps subjected to
a post-processing algorithm which displays only selected
tissues (Figure 1). While 2D MRA examinations are
superior for the demonstration of slow flow (e.g., venous) lesions, 3DFT sequences can provide thinner
image slices with higher spatial resolution, as well as
shorter echo times which minimize artifact responsible
for the overestimation of (carotid) stenoses.
TOF techniques have been most extensively tested in
the evaluation of carotid artery atherosclerotic disease
and a variety of vascular abnormalities involving the
larger vessels of the intracranial circulation. Both areas
are particularly amenable to investigation by TOF studies because of the relatively rapid, constant flow in these
vessels (particularly the carotid arteries) which results
in high vascular contrast, the lack of significant physiologic motion (e.g., respiration), and the availability of
coils which are especially well suited to these applications. With the exception of venous studies, intracranial
investigations have been primarily performed with 3D
sequences because of the complex flow and the demands
for high spatial resolution.16-10 The carotid arteries have
been studied with both 2D and 3D sequences.2-4
Extracranial Applications: Carotid Bifurcation
MRA techniques will likely have their greatest clinical impact in the evaluation of carotid bifurcation
atherosclerotic disease.14-15 Traditional MR imaging is
particularly sensitive to the parenchymal sequelae of
cerebral vascular disease, and many patients are now
evaluated by MR for the extent and distribution of
ischemic damage. Hence the interest in developing a
technique that can be combined with the traditional MR
brain examination to evaluate the severity of carotid
bifurcation occlusive disease in the same sitting.14
A number of studies have been conducted which
demonstrate the efficacy of 2D and 3D-TOF MRA
techniques in the evaluation of the carotid bifurcation.2-41617 The sequential 2D-MRA technique has the
advantage of high vessel/soft tissue contrast from strong
flow-related enhancement which is maintained even in
the setting of relatively slow flow (e.g., severe, long
segment stenosis). On the other hand, minor motion by
From the Section of Neuroradiology, Cleveland Clinic Foundathe patient during the scan can cause a severe stair-step
tion, Cleveland, Ohio.
Reprinted from Current Concepts of Cerebrovascular Disease and misregistration artifact. Also, higher gradient strengths
are necessary to define thin slices in sequential 2DFT
Stroke 1991;26:29-36.
Ruggieri et al
Cerebrovascular Applications of MRA
775
Initial studies have shown a high degree of correlation in the degree of stenosis when comparing 3D-TOF
MRA images (using a single thick volume) with the
accepted gold standard, intra-arterial digital subtraction
angiography (IADSA).2-19 Estimation of the vessel caliber was not significantly impaired by local field inhomogeneities or the complex motion within and immediately distal to the stenoses.19 The more severe stenoses
(greater than or equal to 70%) tended to be slightly
overestimated as a result of these higher order motion
terms, but this degree of error was felt to be acceptable
for the purpose of a screening examination. Other
clinical studies have suggested that an accurate evaluation of carotid occlusive disease may be possible noninvasively through a combination of 2D or 3D-TOF MRA
and ultrasound examinations of the carotid arteries.20-21
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FIGURE 1. Normal MR angiographic study of the intracranial circulation. Anteroposterior (A) and left anterior oblique
(B) maximum intensity projections of an axial volume sequence, obtained with 64 slices and a rectangular field of view,
allow for high spatial resolution with an overall imaging time
of 5 min, 50 sec. There is good definition of the carotid siphons
bilaterally (open arrows), the basilar artery (short arrow), and
the more distal branches such as the anterior (long arrow) and
middle cerebral arteries (curved arrows) and the posterior
cerebral arteries. Spatial resolution is sufficient to allow
visualization of the superior cerebellar artery (two small
arrows).
imaging. This requirement places limitations on the
spatial resolution and the echo time which can be
implemented in these sequences. Both factors contribute to the degree of phase dispersion within the individual voxels. As a result the signal from the protons is
partially (or completely) cancelled, and the carotid
artery may be incompletely visualized in regions of
severe narrowing.
Lower gradients are needed to define the larger 3D
volumes. After excitation of a large 3D volume or
"slab," individual slices are spatially defined by phase
encoding in the slice-select direction. The resultant
thinner individual slices, higher in-plane spatial resolution, and shorter echo times in the 3D acquisitions
reduce the variation of phase across each voxel.2 Consequently, less intravascular signal loss should occur in
the region of local field inhomogeneities (e.g., air,
calcification) or higher order motion terms (acceleration, jerk, turbulence) of the arterial blood at the site of
narrowing. The reduced phase dispersion translates into
improved vessel definition. The main disadvantage of
the 3D studies is the potential saturation of slowly
moving spins in areas far "down-stream" within the
volume or distal to a severe stenosis (Figure 2). Thin,
overlapping, stacked 3D volumes have been proposed as
a solution to this problem although a 'Venetian blind"
artifact can be introduced, which is related to signal
variations at the edges of the volumes or patient movement between the different acquisitions.18 Motion artifact can also be a problem since it is reflected along two
planes because of the additional phase-encoding gradient used in the slice-select direction in the 3D studies.2
Intracranial Applications
TOF MRA has been applied in the head to the
evaluation of patients with intracranial aneurysms, large
vessel atherosclerotic disease, arteriovenous malformations, and dural sinus occlusions. Each of these entities
has its own unique parenchymal sequelae which are
investigated by the accompanying spin-echo examination. The MRA images enhance the specificity of the
traditional brain study and provide additional information to the clinician and neuroradiologist to aid in
making a decision regarding a subsequent invasive study
or management.
Aneurysms
With an acute subarachnoid hemorrhage and a presumed intracranial aneurysm, patients are more appropriately studied by nonenhanced CT and conventional
arteriography. The combination of an MRA and a
conventional spin-echo study is better implemented in
patients with a subacute onset of symptoms in whom an
aneurysm might explain the clinical presentation (Figure 3). It is also appealing to consider using MRA as a
screening test in patients with an increased risk of
aneurysms (e.g., family history, polycystic kidney disease, fibromuscular disease, aortic coarctation).
Preliminary retrospective studies comparing 3D-TOF
MRA images with IADSA have yielded promising results.18-9 Ross et al8 detected aneurysms as small as 3-4
mm with sensitivities of 67% when evaluating the MRA
images alone and 86% when evaluating the MRA
images along with the original 3D slices and spin-echo
images.
Nevertheless, TOF images are still somewhat limited
by the nature of the pathology, the technique itself, and
hardware limitations. Hypointense thrombus in the aneurysm lumen (e.g., acute or chronic thrombosis) may
artificially reduce or obliterate the aneurysm's lumen,
but the same problem exists with catheter arteriography. Correlation with the spin-echo exam, the original
3D slices, or multiplanar reconstructions of these slices
provides a more accurate assessment of the aneurysm
lumen in this situation. Parenchymal and subarachnoid
hemorrhage can also be misleading because the high
intensity of subacute hemorrhage will also be picked up
by the reconstruction program and may obscure the
aneurysm. A large aneurysm or one that is compressing
the lumen of the parent vessel may be poorly or
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FIGURE 2. Severe left carotid
stenosis. (A) T2-weigfUed axial
spin-echo study of the brain
demonstrates a left hemispheric
infarct. (B) An inferior slice
through the level of the cavernous sinus shows absence of the
normal flow void from the left
carotid siphon (arrow) representing either thrombosis or very
slow flow. Compare the left cavernous carotid with the normal
flow void on the right (open
arrow). (C) Lateral maximum
intensity projection MR angiogram of the left carotid bifurcation demonstrates abrupt termination of the signal from the
origin of the left internal carotid
artery, suspicious for occlusion.
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(D) However, a second axial
intracranial MRA (submentovertex view) centered on the circle of Willis demonstrates flow
within the left carotid siphon
(arrow) and distal left internal
carotid artery. The signal intensity within the left carotid siphon
is less than that on the right
(open arrow), presumably because of slow flow within the
siphon with resultant saturation
of the signal intensity. Slowed
flow and saturation of signal
distal to the severe stenosis also
explain the apparent total occlusion of the proximal internal carotid artery (double arrowheads,
middle cerebral arteries; single
arrowheads, posterior cerebral
arteries). Because of the residual
signal intensity from the left carotid siphon, the examination
was interpreted as a high-grade
stenosis of the left internal carotid origin but not a complete
occlusion. (E,F) Lateral views
from the intra-arterial DSA
study confirm the severe stenosis
(arrow) involving the origin of
the left internal carotid artery
(E) with slowed flow in a patent
cervical internal carotid artery
(F) (arrows).
incompletely visualized because of impaired inflow of
the fresh, unsaturated spins which provides the flowrelated enhancement necessary to see the aneurysm
lumen.9 Vasospasm may have the same effect. (Phase
contrast techniques may not be subject to such prob-
lems.12-13) Although less a problem with the 3D-TOF
method, the parent vessel may be difficult to see if the
spins moving within this segment demonstrate a large
amount of higher order motion. Regardless, the 3D
relation between the aneurysm and the parent vessel is
Ruggieri et al
Cerebrovascular Applications of MRA
777
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FIGURE 3. Left ophthalmic artery aneurysm. Anteroposterior (AP) (A) and lateral (B) maximum intensity projections from an
axial volume MR angiographic sequence demonstrate a large, rounded area of increased signal intensity involving the superior
aspect of the left carotid siphon (open arrow) in the region of the origin of the left ophthalmic artery (arrow). Basilar artery signal
(arrowhead) overlaps the aneurysm on the AP view but is definitely posterior to the aneurysm on the lateral projection. Comparison
AP (C) and lateral views (D) from the intra-arterial DSA study confirm the presence of a large aneurysm arising from the origin
of the ophthalmic artery in a configuration and size similar to that defined by the MR angiographic study.
still generally visible either on the MR arteriogram
images or in multiplanar reconstructions of the high
resolution 3D data sets.
Arterial Occlusive Disease
Preliminary clinical studies have also demonstrated
the ability of 3D-TOF MRA to identify occlusive disease of the larger intracranial vessels.1-5'10-22 Confirmation of a tandem lesion in the distal internal carotid
artery or an isolated stenosis in the proximal middle
cerebral artery can have a significant impact on the
clinical decision-making process in a patient with atherosclerotic narrowing at the carotid bifurcation. This
may lead to a more definitive catheter study, for example, in a patient who has had a prior ultrasound
examination documenting mild to moderate carotid
bifurcation disease. On the other hand, a negative study
may avoid a conventional angiogram. This option would
be particularly valuable in older patients with suspected
occlusive disease of the posterior circulation where the
risk of the procedure itself is quite high. MRA may also
permit noninvasive imaging of acute middle cerebral
artery embolic occlusion, which is potentially treatable
with thrombolytic agents.
The studies conducted to date have demonstrated
occlusion or stenosis of the distal internal carotid artery
or the Ml segment of the middle cerebral artery. A
group of infants with a ligated internal carotid artery
and internal jugular vein (for extracorporeal membrane
oxygenation) were studied to confirm adequate crossfilling and venous drainage for both cerebral hemi-
spheres. These results provided significant long-term
prognostic information about the children.5 Children
with sickle cell disease were also studied to identify
large vessel occlusive disease.10-22
The combination of MRA and a spin-echo parenchymal study can directly visualize the vascular stenosis and
the parenchymal consequences in the corresponding
vascular territory at the same sitting. Without additional
acquisition time the corresponding phase images can be
examined to document the direction of flow in other
large vessels that may be supplying collateral flow.
Selective MRA studies have also been designed to
confirm the contributions from other vascular territories.23 An appropriately positioned saturation pulse, for
example, can eliminate the inflow from one internal
carotid artery to determine the extent of collateral flow
(from the circle of Willis) to the territory of a severely
stenotic carotid siphon.
Little has been done to evaluate occlusive disease of
the posterior circulation specifically. Since the vascular
disorders of the posterior fossa, such as dissection and
partial basilar artery thrombosis, tend to have relatively
slow flow, an appropriately designed sequential 2D
study would be the most successful TOF study. Although the vascular abnormality is frequently apparent
on the spin-echo images, MRA can be helpful to
confirm the pathology in those cases with confusing
intraluminal signal. The TOF images themselves can be
confusing with incomplete, subacute thrombosis of the
basilar artery. Evaluation of the corresponding phase
images can settle the issue.
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Difficulties similar to those which arise in the evaluation of stenosis of the carotid bifurcation are also
demonstrated in the examination of intracranial occlusive disease. Because of higher order motion terms in
the blood flowing within and immediately distal to the
stenoses, the resulting phase dispersion causes an overestimation of the degree of stenosis. An additional
complicating factor in the head is the size of even the
larger intracranial vessels. Hardware limitations (i.e.,
system gradient capability) in the commercially available whole-body imaging systems impose restrictions on
the echo time and spatial resolution which affect the
degree to which these problems can be addressed.
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Vascular Malformations
TOF MRA images can provide useful information in
the evaluation of parenchymal and dural arteriovenous
(AV) fistulas. A venous angioma typically appears on
conventional MR as a single large vessel extending from
the ventricular margin to the cortical surface. The very
slow flow and small size of the feeding vessels in
cavernous angiomas and capillary telangiectasias prevent their visualization by any form of MRA. In any
event the clinically significant cavernous angiomas are
generally recognizable on the spin-echo examination by
the blood products from prior hemorrhage.
Parenchymal AV fistulas are visible because of the
cluster of flow voids representing the nidus, the associated ischemic steal, or the results of prior intervention
(e.g., surgery, embolization). Preliminary clinical results
have shown that MRA is useful in demonstrating the 3D
relations between the vascular nidus and the primary
afferent and efferent vessels.16-13'24'25 Dural fistulas are
unique in that they are frequently undetectable with
routine MR imaging unless the excessive flow causes
enlargement of the cortical veins or venous thrombosis.26 In these cases the preliminary clinical diagnosis is
confirmed by the MRA images.
The rapid, complex flow in the larger afferent arteries
make the 3D-T0F MRA sequences desirable for imaging AV fistulas. Shorter echo times and the thinner 3D
slices also effectively reduce the motion-induced
dephasing which is necessary to visualize these arteries
accurately. On the other hand, the saturation of the
inflowing spins impairs the visualization of the slower
flow in the smaller arteries and veins.1-6'11-18 High vessel/
soft tissue contrast is better maintained throughout the
imaging volume with the use of a 2D-TOF technique.
Although the smaller arteries and veins are better seen
with this approach, the large afferent vessels are incompletely visualized because of the necessarily thicker
slices and longer echo times.24 The best compromise
seems to be the use of small, overlapping 3D volumes to
combine the advantages of both the 2D and 3D techniques.6'18 If this 3D MRA is combined with intravenous
gadolinium, the difficulty with spin saturation (and
intravascular signal loss) in the draining veins and distal
nidus vessels is further reduced.6
Regardless of the technique MRA cannot provide the
physiologic information that can be derived from traditional catheter angiography such as the arteriovenous
circulation time and arterial stump pressures. Edelman
et al23-24 showed that it was possible to obtain some
functional information with respect to identifying feed-
ing vessels through the use of appropriately positioned
saturation pulses. Saturation of one main feeding vessel
prevents the inflow of fresh spins from that artery. A
simple 2D-TOF image of the nidus, with the selective
saturation pulse, would show a smaller or less intense
nidus if that vessel contributed significantly to the
malformation.
Dural Sinus Occlusion
The question of occlusion of the dural venous sinuses
is often raised in patients with predisposing disease
processes, such as adjacent paranasal sinus or parenchymal infection, head trauma, dehydration, or hypercoagulable states. Previously, the only definitive means of
diagnosing such an occlusion was through invasive studies. With the advent of MR and MRA, an invasive study
can be avoided. It is often possible to identify occlusion
of the larger dural sinuses on the routine spin-echo
images of the head. This is best evaluated on the late
echo T2-weighted images, which are oriented perpendicular to the primary direction of flow for the sinus in
question. With this arrangement the spins in the sinus
are least apt to experience both the 90 and 180 pulses
such that a flow void will be seen in the images if flow is
present. For example, axial images would be most likely
to demonstrate a flow void in the sigmoid sinus in a
patient who was studied because of severe mastoiditis or
a cholesteatoma which had caused bony destruction of
the petrous ridge. Alternatively, coronal images would
be the most appropriate orientation for patients with a
parasagittal mass lesion compressing the adjacent superior sagittal sinus.
On occasion the spin-echo images demonstrate confusing intraluminal signal in the sinuses, particularly if
the T2-weighted study is not optimally oriented for the
sinus in question (e.g., atypical anatomy), the slices are
relatively thick, the second echo is relatively short, the
venous flow is quite slow, or the sinus contains acute
thrombus (isointense on Tl- and hypointense on T2weighted images). In such cases TOF MRA studies of
the dural sinuses can provide more definitive information with little additional examination time.27 The slow
flow in the dural sinuses demands the use of a 2D-TOF
study. Visualization of the dural sinuses would be
impaired by saturation effects in a 3D-TOF study unless
the 3D study was performed after intravenous gadolinium administration.28
Potentially, 2D-TOF studies can provide misleading
information if the sinus contains subacute thrombus and
this is not apparent on the spin-echo study. The high
signal intensity of the extracellular methemoglobin can
mimic flow-related enhancement and suggest patency.
Reconstructing the phase images from the spin-echo
study can eliminate this ambiguity without prolonging
scan time. Sequences can be designed such that the
images are sensitive to flow in the slice-select direction
as slow as 0.5 cm/sec or as slow as 2.5 cm/sec in the
frequency direction.2930 It is also possible to quantitate
the flow velocities in the sinuses through the use of
paired gradient-recalled sequences or narrow in-plane
saturation pulses (i.e., bolus tagging).31
Future Prospects
Large, carefully controlled, prospective clinical trials
must still be conducted to define more clearly the role
Ruggieri et al Cerebrovascular Applications of MRA
MRA will play in the evaluation of patients with clinically suspected cerebral vascular disease. At the moment TOF-MRA images cannot replace traditional
arteriography of the carotid arteries and intracranial
vasculature. The discrepancy between the modalities is
particularly evident in the intracranial circulation where
the spatial resolution demands are high. Irregularity of
the vessel caliber is related, in part, to errors introduced
by the maximum intensity projection post-processing
algorithm used with present TOF angiography sequences. The most commonly used maximum intensity
projection technique may be unable to identify accurately the vessels in the original data because of variations in the background signal intensity, inadequate
flow-related enhancement, and/or volume averaging
effects.32 These problems have stimulated the development of alternative, more sophisticated post-processing
algorithms and the use of various background suppression techniques for the MRA acquisitions.
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Another important factor contributing to the irregularity of a vessel lumen and focal discontinuities in a
vessel is the intravascular phase dispersion secondary to
complex motion and local field inhomogeneities. Reducing the minimum field echo time limits the motioninduced dephasing and was shown to be possible on
routine imaging systems through the use of truncated
RF pulses and asymmetric data sampling.7 Other innovations in data post-processing and image reconstruction should complement these strategies and improve
the clinical usefulness of the MR arteriograms.33-35
Further reductions in the field echo time and voxel
dimensions have been achieved through the use of
specialized head coils with serf-contained gradients.
These coils have higher peak gradient strengths and
permit more rapid switching times than the standard
imaging coils. Preliminary tests with prototype gradient
RF head coils have shown the expected but nevertheless
exciting results in phantoms and normal volunteers.36-37
Although these sequences have not yet been extensively
tested in patients, it is expected that the MR arteriograms will display a significantly higher correlation with
the traditional angiographic images than was demonstrated previously and the technique will therefore be of
greater diagnostic value.
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