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MR angiography of the intracranial vessels: Technical aspects and clinical

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Neuroradiology (2004) 46: 955–972
DOI 10.1007/s00234-004-1297-9 DIAGNOSTIC NEURORADIOLOGY

Özkan Özsarlak
Johan W. Van Goethem
MR angiography of the intracranial vessels:
Menno Maes technical aspects and clinical applications
Paul M. Parizel

Received: 19 April 2004

Accepted: 6 September 2004
Published online: 4 December 2004

Springer-Verlag 2004
Ö. Özsarlak (&) Æ J. W. Van Goethem
M. Maes Æ P. M. Parizel
Neuroradiology Section,
Department of Radiology,
University Hospital Antwerp,
Wilrijkstraat 10, 2650 Edegem, Belgium
E-mail: ozkan.ozsarlak@uza.be
Tel.: +32-3-8214585
Fax: +32-3-8252026
Abstract Evaluation of the intra-
cranial circulation provides valuable
information in the diagnosis and
prognosis of various intracranial
abnormalities and may influence
patient management. Technical ad-
vances in magnetic resonance angi-
ography (MRA) have improved the
accuracy of this technique in various
clinical situations, such as
aneurysms, arterial and venous ste-
no-occlusive diseases, vascular mal-
formations, inflammatory arterial
diseases, preoperative assessment of
the patency of dural sinuses, and
congenital vascular abnormalities.
In many centers, MRA has replaced
conventional digital subtraction
angiography in screening for intra-
cranial vascular disease, because of
its non-invasive and non-ionizing
character. Several MRA techniques
have been developed for the imaging
of the intracranial vascular system,
such as time-of-flight MRA (TOF
MRA), phase-contrast MRA (PC
MRA), and more recently contrast-
enhanced MRA (CE MRA). In the
evaluation of steno-occlusive dis-
ease, the three-dimensional (3D)
TOF-MRA technique is recom-
mended for arterial evaluation, and
the 2D TOF or 2D PC-MRA tech-
nique for venous evaluation. For the
evaluation of aneurysms and arte-
riovenous malformations (AVMs),
we recommend the 3D CE-MRA
technique, especially dynamic
sequences in case of AVM. In this
review, the technical aspects, limita-
tions, and optimization of these
MRA techniques will be discussed
together with their indications in
intracranial disease.
Keywords Magnetic resonance Æ
Vascular studies Æ Infarction Æ
Aneurysm Æ Intracranial Æ
Arteriovenous malformations

Technical considerations characterized by reduced signal intensity [1]. The signal

Time-of-flight magnetic resonance angiography
In time-of-flight magnetic resonance angiography (TOF
MRA), repetitive pulses are used to suppress stationary
background tissues, while the unsuppressed protons of
flowing blood create a signal. The high signal intensity in
the blood vessels during TOF MRA is attributable to
flow-related enhancement, and the absence of flow is
intensity of flowing blood depends on its velocity, the
length and course of the vessel being imaged, the flow
characteristics, and sequence parameters. The main lim-
itations of the technique are the spin dephasing that
occurs in complex or turbulent flow pattern, particularly
in three-dimensional (3D) TOF, and in vessels in close
proximity to tissues with short T1, such as fat or subacute
hemorrhage (Table 1). Signal loss may also occur in the
presence of flow resulting from the spin saturation effect,
 956

Table 1 Limitations and remedies of MR angiography techniques (TOF time-of-flight, PC phase contrast, CE contrast enhanced MR angiography, VENC velocity encoding,
MOTSA multiple overlapping thin slab acquisition)

Limitations MRA technique Effect Site Remedies

Complex flow, turbulent flow TOF PC (2D>3D) Signal loss Cavernous segment Large flip angle (45–60)
(intravoxel dephasing) Carotid bulb Smallest voxel size, thinner slices
Beyond the stenosis Lower TE (<7 msec)
In large ulcerations Flow compensation
Aneurysm Use 3D TOF MRA
Slow flow (spin saturation) TOF PC Signal loss Deeper vessels on 3D TOF Thin sections (MOTSA)
on 2D TOF
Skip sign (occlusion) Transverse flowing Longer TE
vessels on 2D TOF
Distal to a stenosis Lower flip angle
Perpendicular image plane
Gadolinium application
Lower VENC factors for PC MRA
Short T1 tissues (fat, blood) TOF CE Obscure vessel delineation Periorbital region Background suppression
(magnetization transfer, spectral
fat saturation, spectral water
excitation, image subtraction)
Peripheral vessels
Thrombus TOF Methemoglobin simulates normal Thrombus Use PC MRA
vessel (short T1 relaxation)
Deoxyhemoglobin obscures the vessel margins
(magnetic susceptibility effects)
Aliasing PC Misinterpretation Any location Higher VENC factor
Decreased vessel wall delineation PC Misinterpretation Any location Lower VENC factor

as in the case of slow flow in the distal intracranial vessels,
or becuase of intravoxel phase dispersion, as in situations
of turbulent flow or magnetic field inhomogeneities [1, 2].
Image quality on 3D TOF MRA can be improved by use
of a technique called ‘‘multiple overlapping thin slab
acquisition’’, to overcome flow saturation effects, and by
the application of magnetization transfer (MT) prepulses
to suppress the background signal of the stationary tis-
sues [3, 4]. Moreover, a judicious choice of TR (40–
50 ms) and careful selection of the imaging plane per-
pendicular to the direction of flow may further decrease
the spin saturation effects. Intravoxel spin phase disper-
sion may be overcome by the use of smaller voxel sizes,
thinner slices, and short TE (7–9 ms) [1]. Saturation ef-
fects can also be minimized by using lower flip angles (15–
20) in combination with longer TRs, thiner slices, and
the shortest possible TE [5]. The variable flip-angle
excitation technique, termed ‘‘tilted optimized nonsatu-
rating excitation’’, has also been shown to increase the
signal and lower the spin phase dispersion effect within
the vessels [6]. In this technique, the flip angle varies
across the slab that it is set lower at the inlet side and
gradually increases as it approaches the exit side to in-
crease the blood signal [6]. The remaining saturation ef-
fects of slow-flow in small arterial branches can be further
eliminated by intravenous injection of paramagnetic
contrast material, but with the disadvantages of in-
creased cost, possible superimposition of veins, and
enhancement of surrounding tissues [7]. The use of a
classic ‘‘single’’ dose of gadolinium (0.1 mmol/kg) may
obscure the arteries by excessive enhancement of the
surrounding soft tissues and the venous system [8]. For
example, venous enhancement in the cavernous sinus can
obscure the visibility of the internal carotid arteries.
Postcontrast visualization of branches of the distal
median cerebral artery is reported to improve in 69% of
cases, and 30% of branches become visible only after
administration of contrast material. Studies performed
with a smaller amount of contrast (less than 5 ml bolus)
also report an adequate visualization of the distal intra-
cranial arteries with slow flow (Fig. 1), with less inter-
ference of enhancing surrounding tissues [8, 9]. Although
depending on the matrix size and other sequence
parameters, the total acquisition time of high resolution
3D TOF MRA is about 6 min (TR 40 ms, TE 7.15 ms,
25 of flip angle, 256·512 matrix, 64 partitions, and 1 mm
slice thickness). With the application of the parallel
acquisition technique with an acceleration factor of 2,
this can be lowered to 3–4 min, without a significant
decrease in signal-to-noise ratio (SNR) [8].
Phase contrast magnetic resonance angiography
Phase contrast (PC) MRA uses a different technique to
create vascular contrast, based on manipulating the
957
Fig. 1 Low-dose contrast enhanced time-of-flight MR angiogra-
phy. A small dose of intravenously administered gadolinium
(0.5 ml) improves the visualization of the distal intracranial arterial
branches. The evaluation of the central arteries is not disturbed by
venous contamination, although limited venous enhancement
through the basal veins is visible
phase of the magnetization. This effect is obtained by
applying a bipolar phase-encoding gradient and a
velocity-encoding (VENC) factor [10, 11]. Since PC
MRA is sensitive to flow velocities, blood velocities
higher than the preselected VENC value will not be
represented or misrepresented in the image, so that the
user must choose this value carefully. Higher VENC
factors (>60–80 cm/s) are necessary to image arteries
selectively, whereas a VENC factor of 20 cm/s will
represent the veins and sinuses [11]. PC MRA can be
used with 2D or 3D techniques. The 2D PC MRA
technique displays data sets of single or multiple slices
that will contain information about the direction and
amplitude of flow. This can be applied in the evaluation
of steno-occlusive disease to demonstrate the direction
of collateral flow, and in arteriovenous malformations
(AVMs) to study the feeding and draining vessels. The
3D PC MRA technique is similar to 2D PC MRA, in
that it acquires a volume containing thin slices and uses
a maximum intensity projection (MIP) algorithm to
generate an angiogram (Fig. 2). The limitations of PC
MRA are similar to those of TOF MRA, e.g., in-plane
saturation, intravoxel dephasing, and long acquisition
times [1, 2]. Signal loss can be minimized by reducing
the voxel size and by using flow compensation and the
shortest possible TE (Table 1). In comparison with 3D
TOF, 3D PC MRA has known advantages, such as the
detection of collateral flow and flow direction, the
demonstration of slow flow particularly in complex
958
Fig. 2 Three-dimensional phase-contrast MR angiography (PC
MRA). Maximum intensity projection (MIP) image of PC MRA
with a VENC factor of 20 cm/s showing sagittal view of normal
venous anatomy
vessel structures, and aneurysms and AVMs. However,
these advantages affect predominantly small vessels and
do not result in an improvement of the detection or
grading of stenosis in the major intracranial vessels in
comparison with 3D TOF MRA [12]. Visualization of
smaller distal branches can be improved with the use of
contrast material. Another limitation of the technique
is velocity aliasing, which occurs when true velocities
exceed the peak VENC. In such cases, flow can be
incorrectly shown as being in the opposite direction.
One other major disadvantage of 3D PC MRA is that
the pulse sequence is relatively more time-consuming
than 2D acquisition. Therefore, it is currently used less
frequently. Four acquisitions are required to encode
flow in all directions, and this therefore lengthens the
scan time [13]. This problem is partially solved with
new ultrafast imaging sequences, such as flow-sensitive
gradient echo imaging and echo planar imaging [13,
14]. The benefits of 3D PC MRA include a higher
Fig. 3 Intravoxel dephasing
attributable to turbulent flow
during TOF MRA can be
solved with contrast enhanced
MRA. a, b Two MIP angio-
grams in the coronal direction
in two different patients. a TOF
MR angiography. b CE MRA.
Flow related intravoxel deph-
asing (turbulent flow) through
the carotid siphon is a common
problem in TOF-MRA. This
artifact is overcome by contrast
enhancement, particularly in
CE MRA
SNR, small voxel size, and a shorter TE when com-
pared with 2D acquisitions.
Contrast enhanced magnetic resonance angiography
Contrast enhanced (CE) MRA has a higher SNR and a
shorter acquisition time than other MRA techniques.
The MR signal on CE MRA depends on the T1 short-
ening effect of gadolinium (Fig. 3). Therefore, it has the
potential to overcome some of previously discussed
flow-related problems [7, 9, 15]. However, the disad-
vantage of this technique is its imaging window, which is
restricted to the first pass of the contrast bolus. Whereas
TOF and PC MRA are physiologic techniques showing
blood flow, CE MRA provides morphological infor-
mation concerning a blood vessel. CE MRA requires
good coordination between the contrast injection,
patient cooperation, and the starting time of the acqui-
sition. There are several methods to achieve proper
bolus timing, such as simple fixed timing delay, test
bolus, multiphase scanning, and real time fluoroscopic
detection of contrast arrival [16]. In our institution, we
prefer to use semi-automated real-time MR fluoroscopy
for the appropriate timing of bolus arrival centered at
the carotid bifurcation, and then we manually start the
CE MRA sequence through the intracranial vessels.
The values for TR and TE should be selected as short
as possible to increase the spatial and temporal resolu-
tion and to improve the stationary background sup-
pression. Recent technical advances allow further
reduction of TR and TE, enabling acquisition times of
less than 15 s. We perform acquisition in the coronal
plane to cover both intracranial and extracranial carotid
arteries, with a slice thickness of 1.0 mm. The acquisi-
tion time is a critical parameter, since the angiogram has
to be completed during the first pass of the contrast
bolus, before the occurrence of venous contamination
that may interfere with image interpretation. Usually, a
dose of 0.1 mmol/kg body weight of a gadolinium che-
late is injected at a rate of 1.5–2 ml/s, either with an
automatic injector or manually.
 959

Currently used MRA techniques, their advantages, tissue, such as orbital regions, especially when an MIP
disadvantages, and major applications are summarized algorithm is applied (Fig. 4).
in Table 2.

Background suppression: ‘‘water excitation’’
In TOF techniques, fatty tissue surrounding vascular
structures may obscure the visibility of vessels because of
its high signal intensity [15]. As a result of a small fre-
quency difference of hydrogen nuclei in fat and water,
selective saturation of fat (fat-suppression) can be
achieved by the excitation of RF pulses centered on the
average fat frequency. However, fat-saturated images
have to be acquired with a conventional fat-suppression
pulse during every repetition cycle. Therefore, the
examination time is relatively long [15]. An alternative
method for stationary background tissue suppression,
‘‘selective water excitation’’ has been described. In this
technique, the RF excitation is designed only for water
protons in the selected slice plane, without affecting the
fat protons [17]. This application is most useful when
arteries must be delineated from the surrounding fat
Subtraction technique
Another strategy to improve the contrast to background
ratio is the use of subtraction techniques [18]. These
techniques are generally applied to CE MRA, which
usually contain residual signal intensity in the tissues
adjacent to the vessels. However, any change in patient
position between the precontrast and contrast-enhanced
acquisitions results in artifacts. The main limitations of
the subtraction technique are the deletion of vascular
signal intensity caused by in-flow effects on the precon-
trast images, increased imaging time because of the
requirement of two data sets, and increased noise level.
Post-processing
After acquisition of the raw data, source images and
graphic representation of MRA data can be generated

Table 2 MRA techniques, their advantages, disadvantages, and major applications (SNR signal-to-noise ratio, VENC velocity encoding,
AVM arteriovenous malformation)

TOF MRA PC MRA CE MRA

2D 3D 2D 3D 3D

Advantages
Minimal saturation effects Less intravoxel dephasing Less saturation effects No saturation No saturation effects
effects
Coverage of large distances High SNR Direction and Excellent Reduced intravoxel
quantification background dephasing by
of flow velocities suppression gadolinium
Sensitivity to venous Smoother vessel contour Excellent background High SNR
slow flow suppression
Shorter acquisition time Shorter acquisition time Short acquisition
time, decreased
motion artifacts
Excellent background
suppression
Disadvantages
Intravoxel dephasing More saturation effects Intravoxel dephasing Long acquisition Venous puncture
Insensitive to in-plane Insensitive to slow flow Choosing an appropriate time High cost of gadolinium
blood flow VENC factor
Artifacts attributable to Artifacts attributable to Critical bolus timing and
thrombus and short thrombus and short T1 venous enhancement
T1 substances substances
Major application
Carotid bifurcation High-flow (arterial structures) Localizer Cerebral arteries Cerebral arteries
Venous flow (dural sinus AVMs Cerebral veins Cerebral veins
thrombosis, cortical Aneurysm AVMs Dynamic evaluation
vein mapping) of AVMs,
dural fistula, shunts
Carotid disease Bleeding lesions (ruptured Aneurysm and treatment
aneurysm, bleeding AVM) follow-up
Cavernous hemangioma Carotid disease
960

Fig. 4 Conventional fat satura-

tion versus ‘‘water excitation’’.
Inhomogeneous fat suppres-
sion, with still visible subcuta-
neous and retro-orbital fat, may
obscure some of the peripheral
arterial branches (a). The water
excitation technique improves
fat saturation (arrows) and
gives better delineation of the
peripheral arteries (b)

through the use of MIP algorithms. By varying the
projection angle, multiple projective images can be
obtained retrospectively [19]. For filming purposes,
segmented MIP images rotated through 180 at 18
increments with a total 11 images are sufficient.
However, the MIP algorithm overestimates stenosis
because of threshold values. Therefore, image inter-
pretation must always include the source images
(Fig. 5), particularly in the assessment of a vessel
narrowing or in complex anatomical situations. The
3D data set can also be processed with advanced
viewing algorithms, such as volume rendering or sha-
ded surface display.
Fig. 5 A 49-year-old male with right hemiparesis, immediately
after a motor vehicle accident: dissection of the left internal carotid
artery. a, b MRA and axial source images. c Coronal TOF MRA
MIP reformation demonstrates the abnormality of the left internal
carotid artery, with a smaller lumen diameter (open arrows). Based
on the MIP image only, it is not obvious whether the carotid artery
is still patent or distally occluded. The source images show the
remaining patency of the distal internal carotid artery and wall
thrombus (white arrows) caused by dissection
Multi-channel RF coils and the parallel acquisition
technique
Since their introduction, RF coil arrays containing
multiple coil elements have been increasingly used in
clinical MR studies. The main purpose of these RF
arrays is to improve the image quality and the SNR of
the MR images [15, 20]. Generally, multi-channel
phased-array coils offer increased SNR over standard
volume coils near the array elements, while preserving
the SNR at the center of the volume. Besides devel-
oping multi-channel phased-array RF coil designs, the
improvements in gradients, system hardware, and the
sequence design in recent years allow ultrafast magnetic
resonance imaging (MRI) techniques, such as the par-
allel acquisition technique (PAT) [21]. Various parallel
MRI techniques have been described, and numerous
clinical applications have been explored. Parallel MRI
techniques use spatial information from arrays of RF
detector coils to accelerate imaging [21]. Parallel
imaging reconstruction techniques include simultaneous
acquisition of spatial harmonics, sensitivity encoding,
and some newer approaches currently under develop-

ment [21, 22]. Applying PAT with an acceleration fac-
tor of 2 results in a 43% time gain, when compared
with an acquisition with the same parameters without
PAT [8] (Fig. 6). A gain in acquisition time obtained by
parallel MRI may improve the temporal and/or spatial
resolution, increase the volume coverage, and even
reduce the time-dependent artifacts, such as motion, or
breathing artifacts [23].
High-field strength (3.0-T) magnetic resonance
angiography
The published data in the literatute and experience with
high-field strength MRA of the intracranial vessels are
limited to 3D TOF MRA. The main advantage of 3.0-T
MRI is a doubling of the available SNR over 1.5-T.
The better SNR at high-magnetic-field strengths is a
well-known potential benefit for further increasing
spatial resolution in 3D TOF MRA [24]. The longer T1
relaxation times at 3.0-T may make the background
easier to suppress. However, there are important dis-
advantages, such as more rapid saturation of slowly
flowing blood, increased RF-energy deposition, and
stronger susceptibility effects [24, 25]. With high-reso-
lution 3.0-T MRI, it is possible to increase spatial
resolution with a voxel volume of 0.13 mm3
(0.30·0.44·1.00 mm) [24]. This has implications with
regard to the improvement of the visualization of small
vessel segments and vascular diseases, such as the
detection of stenosis or small aneurysms less than 5 mm
in size [24]. The smaller vessels in 3.0-T MRI are
reported to be generally sharper, in particular because
of the darker background and reduced noise [25],
although sharper visualization of the small vessels and
Fig. 6 Parallel acquisition tech-
nique (PAT) applied to 3D
TOF MRA. Axial 3D TOF MR
angiograms, without (a) and
with parallel acquisition appli-
cation (b) in the same patient.
The acquisition time of 3D
TOF MRA without using PAT
is 6 min, 30 s. PAT with an
acceleration factor of 2
decreases the imaging time to
3 min, 46 s, with no significant
decrease in vascular assessment
961
the same improved background suppression may cause
more ghosting artifacts, particularly at the proximal
vessel portions. Lowering of the TE (as short as 3.4 ms)
may reduce these undesired effects [25]. Another dis-
advantage of the high-resolution 3.0-T MRI is the
increased acquisition times up to 8 min [24]. Intracra-
nial high-resolution 3D TOF MRA at 3.0-T has taken
its place in clinical routine and will further reduce the
need for invasive diagnostic angiographies.
Clinical applications of MRA
Arterial steno-occlusive disease
Cerebral stroke is a major cause of death and disability in
the Western society. The main etiology of stroke is ath-
erosclerosis and its related complications such as steno-
sis, occlusion, or emboli originating from ulcerated
atherosclerotic plaques. The role of the neuroradiologist
in acute cerebral stroke is to confirm the clinical diag-
nosis and more specifically to identify the causative
arterial occlusion for appropriate and timely therapy [1]
(Fig. 7). Among the noninvasive imaging techniques,
MRA allows more accurate evaluation of intracranial
steno-occlusive disease and is widely used as a screening
method in stroke patients [26]. At this time, noninvasive
imaging techniques are not yet able to replace intra-
arterial digital subtraction angiography (DSA), because
of the lower spatial resolution and lack of precise he-
modynamic information. Moreover, the potential over-
estimation of stenosis on MRA is still a problem.
However, a good morphologic correlation in depicting
steno-occlusive lesions of the proximal intracranial
arteries has been reported with a sensitivity of 80%–
962
Fig. 7 A 80-year-old female with right hemiparesis and speech
difficulties: left internal carotid artery occlusion. The diffusion-
weighted image (a) reveals a small area of increased signal and a
diffusion defect attributable to cytotoxic edema in the parieto-
occipital areas. Although, there is an occlusion of the left internal
carotid artery, the arterial circulation of the left hemisphere and the
distal branches of middle cerebral artery (b, white arrows) is largely
repaired with collateral circulation through the vertebro-basilary
system (open arrow). This is probably provides an explanation of
the relatively small parenchymal (watershed) injury, but massive
proximal occlusion
100% and a specificity of 80%–99% [20]. Several types of
artifacts cause limitations in identifying and grading the
stenosis by TOF MRA [26, 27, 28]:
1. Vessels close to the skull base and around the sphe-
noid sinus are affected by artifactual narrowing or
nonvisualization because of susceptibility artifacts
caused by adjacent bone and air. In these locations,
multiplanar reformation or axial source data images
can be helpful.
2. Intravoxel dephasing caused by turbulent flow in the
carotid siphon and loss of laminar flow may also
contribute to artifactual reduced signal, which can
simulate narrowing.
3. MR angiograms of severely stenotic vessels often
show a discontinuity in a vessel (skip sign), again
caused by intravoxel spin dephasing and the acceler-
ation of flow through the stenosis.
4. MIP may create additional artifacts in the area of a
stenosis. Axial source images are more reliable than
the MIP images alone for assessing the severity of
intracranial stenosis.
5. Although the use of longer TEs may increase the
interpretation of artifactual narrowing or flow gaps,
the lower field gradient MR units (<1 T) limit the
choice of shorter TEs within an acceptable SNR.
MRA can reliably demonstrate a proximal middle
cerebral artery occlusion and, knowing the poorer
clinical outcome of these patients, it may have a role in
deciding and targeting the thrombolytic therapy [29].
Aneurysm
In the acute clinical setting of subarachnoid hemor-
rhage, one should exclude the possibility of an intra-
cranial aneurysm as the underlying cause. Because even
small aneurysms (2 mm or less) can rupture, the ideal
diagnostic test to be used should provide the best pos-
sible anatomical detail. DSA is still considered the gold
standard in the investigation for intracranial aneurysms.
False-negative rates of 5%–10% are reported in the
literature, attributable not to limitations of spatial res-
olution, but to the limited number of projections of the
neck of an aneurysm. This problem is largely overcome
with 3D rotational DSA, but this expensive technique is
not yet widely available. Nevertheless, DSA requires a
highly skilled radiologist to perform the procedure and
remains an invasive technique with arterial puncture and
intra-arterial catheter manipulation, with a 1% major
complication risk and a 0.5% rate of persistent neuro-
logical deficit [30]. Technical advances in MRA
throughout the 1990s have continued to improve the
sensitivity of this technique for detecting cerebral
aneurysms as a screening tool, and MRA has been used
as an alternative to DSA for the presurgical work-up of
aneurysmal subarachnoid hemorrhage [31]. Aneurysms
as small as 3 mm can now be detected with 3D TOF
MRA [32]. Once obtained, MRA data can be viewed
from any projection in both 2D and 3D reformation
algorithms to detect the aneurysm and to evaluate its
neck. Multiplanar reformations are particularly helpful
in defining the neck and also the parent and branch
vessels related to aneurysms [33] (Fig. 8). The detection
and treatment of an aneurysm before it ruptures with
possible lethal subarachnoid hemorrhage is an impor-
tant research topic. TOF MRA can identify aneurysms
(at least 3 mm in size) with a sensitivity of 74%–98%
[32, 34]. MRA is ideal for screening cerebral aneurysms
because the procedure is noninvasive and the patient is
not exposed to radiation. The differences in diagnostic
confidence in the detection of intracranial aneurysms are

Fig. 8 A 56-year-old male patient, 13 months after the endovas-
cular coiling of a large internal carotid artery aneurysm: residual
aneurysm. Axial TSE T2 (a) and fluid-attenuated inversion
recovery (b) show the extensive artifacts caused by coils. A small
bright signal at the periphery of the coils (arrow) suggests a residual
flow inside the aneurysm (b). CE MRA (0.01 mmol/kg, 2 ml/s)
with a coronal MIP image reveals a residual aneurysm (c). Based
on MIP images alone, the evaluation of the aneurysm neck and the
relation of the residual sac (open arrow) with the parent and
surrounding arteries is not easy. The axial source image of the
MRA (d) demonstrates the large neck of the residual aneurysm
(white arrow)
not significant between CE MRA and 3D-TOF MRA,
except for giant aneurysms in which slow and turbulent
flow may lead to flow saturation and phase dispersion
on TOF MRA (Fig. 9). Additionally, intra-aneurysmal
thrombus or perianeurysmal hemorrhage can also be
misinterpreted as intraluminal blood flow on TOF MRA
[35]. CE MRA has the potential to overcome some of
these problems because its MR signal depends more on
T1 shortening than on flow-related enhancement [36].
The role of endovascular treatment in the manage-
ment of patients with intracranial aneurysms is increas-
ing. Indications for endovascular occlusion with coils
and minimization of the risks of thromboembolic com-
plications depend on a number of factors, such as the
963
analysis of the neck/fundus ratio and the understanding
of the relationship of the aneurysm to both parent and
branch vessels [37]. If a residual aneurysm or aneurysm
regrowth is identified, retreatment is often considered
[38]. This routine follow-up is usually made with DSA.
However, a few studies with 3D TOF MRA have re-
ported the potential role of MRA in the follow-up, with
sensitivity rates ranging from 71% to 91% and the
specificity rates ranging from 89% to 100% in ruling out
residual flow [38–41]. False-negative examinations can be
explained by the presence of slow flow in the aneurysm
with a saturation phenomenon or magnetic susceptibility
artifact of the coil mass [38–41] (Fig. 10). False-positive
examinations are probably related to blood clot(s) within
the coil mass, which can be interpreted as flow [39]. The
use of an intravenous contrast material in TOF or CE
MRA can improve the evaluation of the aneurysm and is
helpful in eliminating these artifacts [39–42].
Arteriovenous malformations
AVMs of the brain are an important cause of death
and long-term morbidity resulting from intracranial
hemorrhage and epilepsy. In 9% of patients with sub-
964

recently because of the technological advances in imag-

Fig. 9 Giant aneurysm: MIP projection. Although CE MRA is
superior to TOF MR angiography in the evaluation of giant
aneurysms, the turbulent flow may cause an inhomogeneous signal.
Note the dark signal at the bottom of the giant aneurysm in the M1
segment of the right middle cerebral artery
arachnoid hemorrhage and 4% of patients with primary
intracranial hemorrhage, an AVM is the underlying
cause. The detection rate of AVMs has been increasing
ing modalities and the wide availability of non-invasive
techniques. An AVM is defined as an anastomotic net-
work of blood vessels in which arteriovenous shunting
occurs in a central nidus. To date, there is no standard
reference investigation for the diagnosis of AVM. There
are usually several tortuous high-flow feeding arteries of
different sizes and courses that converge toward the ni-
dus where the arteriovenous shunting occurs (Fig. 11).
These feeding arteries typically originate from more than
one intracranial branch of the internal carotid and/or
vertebrobasilar systems. Because of the high flow and
low resistance of an AVM, diffuse small arterial braches
from the surrounding brain tissue may form a collateral
network around the AVM [43]. MRI and particularly
MRA play an important role in the evaluation of nidus
size and its anatomical relations [44]. The draining veins
are often anomalous, because of hemodynamic stresses
causing stenosis, ectasia, or varix formation. Associated
aneurysms can be visualized in 10% of patients with
AVMs [45] (Fig. 12). These aneurysms may be multiple
and tend to be small in cases of hereditary hemorrhagic
telangiectasia and other neurocutaneous disorders, such
as Wyburn–Mason syndrome [46]. Several MR angio-
graphic techniques, such as 3D PC MRA and contrast-
enhanced 3D TOF techniques have been applied as
non-invasive means of diagnosis [11]. These MR
angiographic techniques accurately depict anatomic
details and the flow direction of AVMs; however, they
do not provide any further hemodynamic information.

Fig. 10 A 73-year-old male pa-

tient: partially thrombosed
large posterior cerebral artery
aneurysm. The 3D TOF MR
angiograms (a, b) and source
image (c) reveal a large hyper-
intensity at the right posterior
cerebral artery. Not only the
flow, but also acute thrombus is
hyperintense on TOF MR
images; this may cause a prob-
lem in the differentiation of the
flow contained in the aneurysm
from a blood clot. The coronal
(d) reformation of the pre-con-
trast 3D gradient echo T1
source image demonstrates that
the hyperintensity is caused by
acute thrombus (arrow)
 965

Fig. 11 A 25-year-old female

with a large AVM. The axial
TSE T2-weighted image
(a) shows a large tortuous sig-
nal voiding in the right parietal
lobe corresponding to the
AVM. 3D TOF MR angiogram
(b) obtained without venous
saturation reveals a large
network of arterial and venous
structures converging toward
the nidus. Note the involvement
of both anterior and middle
cerebral arteries and the dilated
venous system

Fig. 12 A 36-year-old male

patient with an extensive AVM
and associated aneurysms. Two
different MIPs of 3D TOF MR
angiography show a large AVM
in the right hemisphere. Two
associated small aneurysms
(open arrows) are present

The hemodynamics of AVMs are important in defining
the risk factors for hemorrhage, together with their large
size, deep venous drainage, and nidus aneurysm.
Although the temporal resolution is not yet sufficient,
recent reports have shown that the time-resolved con-
trast-enhanced 3D MR angiography (MR-DSA) are
capable of providing dynamic angiographic images
(Fig. 13) [47, 48]. Nevertheless, the technique has several
limitations: (1) spatial resolution is still inadequate; (2)
the section thickness is inadequate to cover relatively
966
Fig. 13 A 23-year-old female patient with an extensive AVM.
Hemodynamic evaluation of AVM by using time-resolved MRA.
Each image corresponds to a CE MRA sequence of 2 s.
Enhancement of the AVM nidus during the arterial phase, a–v
shunt, and early venous drainage can be detected in images 2–4.
Enhancement of the ventral portion of the superior sagittal sinus
shows the venous phase (images 5–10). Finally, late venous
drainage of AVM can be detected again by enhancing only the
posterior portion of superior sagittal sinus (images 11 and 12)
large AVMs; (3) venous overlap may cause problems in
areas in which arteries are close to veins, as in the car-
otid siphon. However, nowadays, MR-DSA can be
performed with two to four frames per second when the
projection sequence is combined with view-sharing
techniques [49, 50]. Conventional neurosurgery, endo-
vascular treatment, stereotactic radiosurgery, or any
combination of these is used in the treatment of AVMs,
and complete obliteration has been defined as ‘‘the ab-
sence of any angiographically visible arteriovenous
shunt’’; this may take 2–3 years [51]. MR-DSA has the
potential benefit of allowing the non-invasive evaluation
of AVMs in diagnosis, radiosurgical dose planning, and
post-treatment assessment.
 967

As a rare congenital abnormality, the vein of Galen
malformation (VGAM) (Fig. 14) is described as a true
arteriovenous malformation with severe morbidity and
mortality [52, 53]. MRI is mandatory for the accurate
assessment of the associated hematoma, ischemia, or
hydrocephalus. If there is severe parenchymal damage,
endovascular treatment cannot compensate the irre-
versible changes. Since conventional angiography is only
indicated if embolization is planned, MRI and MRA
have a role in the pre-treatment period at 3 and
6 months after birth and then following treatment, if
clinical conditions are stable [52, 53]. MRA is capable of
indicating the major vessels of supply and the tortuosity
of arterial access and venous anatomy [53].
Venous occlusive disease
Dural venous sinus thrombosis is seen in various condi-
tions, such as dehydration, hypercoagulation disorders,
infection, or direct tumoral invasion. Delayed diagnosis
of sinus thrombosis may cause morbidity and mortality
[54]. The diagnosis of a sinus thrombosis on MRI or
MRA is not always easy because both thrombus and flow
can produce high signal intensity [54, 55] (Fig. 15). Both
3D TOF MRA and 2D PC MRA are unsuitable for the
visualization of the intracranial venous system because of
strong in-plane saturation and intravoxel dephasing.
Although the quantitative determination of blood
velocities may be possible, long imaging times and the
proper setting of the VENC factor beforehand are the
major limitations of PC MRA, which is more susceptible
to motion artifacts because of the longer acquisition
times. However, this latter technique gives a better dis-
tinction between thrombus and flowing blood [56]. Ideal
venous system assessment can be achieved by using 2D
TOF MRA. However, with 2D TOF MR venography, it
is difficult to distinguish an acquired thrombosis from a
hypoplastic or absent sinus, which is a common ana-
tomical variation (Figs. 16, 17). This phenomenon is

Fig. 14 A 9-month-old baby-

boy: vein of Galen malforma-
tion. Mid-sagittal TSE T1
(a) and axial TSE T2 (b) images
showing a pathognomonic as-
pect of Galen malformation
with dilation of the great cere-
bral vein of Galen and straight
sinus. No parenchymal angio-
matous malformation is visible
that corresponds to a type-1
Galen malformation. Lateral
view of the 3D TOF MR
angiogram (c) showing the
extensive enlargement and high
velocity flow enhancement of
the great cerebral vein of Galen
and straight sinus
968
Fig. 15 A 30-year-old male with headache: dural sinus thrombosis.
Mid-sagittal TSE T1 (a), axial TSE T2 (b), and axial TSE T1
(c) images reveal an enlargement of the superior sagittal sinus
because of a thrombus (white arrows). Iso- to hyperintense signal
on T1 and high signal intensity on T2-weighted images correspond
to a late subacute thrombus. Dynamic contrast-enhanced MR
angiograms (d) demonstrate the patency of the sagittal sinus and
the presence of flow around the organized thrombus (black arrow)
known as a ‘‘transverse sinus flow gap’’ and can be ob-
served at the non-dominant transverse sinuses (usually
on the left) in as many as 31% of patients [57]. Con-
ventional catheter angiograms show the presence of
hypoplastic, but patent, non-dominant transverse sinuses
in these patients. Other pitfalls may include signal loss
because of in-plane flow saturation or complex flow,
particularly through the sigmoid sinus and jugular bulb
[57, 58]. To interpret MR angiograms accurately and to
avoid such potential pitfalls in the diagnosis, one must be
aware of the technical limitations of 2D-TOF imaging. It
is therefore desirable to set the slice thickness as small as
possible (1.0–1.5 mm) and to orient the acquisition plane
perpendicular to the long axis of the vessel. Because of
the complex 3D morphology of the venous structures, it
is sometimes necessary to repeat MR venography in
different directions (coronal, sagittal, or oblique) for full
coverage of the sinuses (Fig. 18). Recent reports recom-
mend the use of 3D contrast-enhanced magnetized pre-
pared rapid gradient echography in diseases of the large
deep veins and dural sinuses [59]. However, there are also
several pitfalls that occur with this technique, such as the
visualization of intrasinus fibrotic bands and pacchio-
nian granulation, which may be misdiagnosed as a
thrombosis, and being able to distinguish a chronic
thrombosis from normal contrast enhancement of the
sinus [60].
Other pathologies
MRI has replaced conventional angiography as the
primary imaging tool for the diagnosis and localization

Fig. 16 A 22-year-old female with headache and vomiting: throm-
bosis of the transverse sinus and venous infarction. Axial TSE T2
(a) and axial diffusion-weighted EPI (b) images reveal a cortical
infarction caused by thrombosis of the left transverse sigmoid
sinuses and jugular vein, which is clearly visible by 2D TOF MR
angiography (c)
of intracranial tumors and their vascularization patterns
and relationship to surrounding vascular structures [61].
Central nervous system (CNS) vasculitis represents a
heterogeneous group of inflammatory diseases that pri-
marily affect the small leptomeningeal or parenchymal
blood vessels of the brain. A wide range of neurological
conditions may cause CNS vasculitis, including infec-
tion, malignancy, ionizing radiation, cocaine ingestion,
and autoimmune disease [62]. MRI is highly sensitive in
Fig. 17 Transverse sinus gap
(white arrows) attributable to
the spin saturation effect of
slow flow on 2D TOF coronal
(a) and transverse (b) MR
angiograms. The patient also
has a venous angioma draining
into the superior sagittal sinus
(open arrows)
969
showing secondary manifestations of CNS vasculitis,
such as supratentorial infarctions in the cortical and
subcortical regions; however, this appearance is not
specific for vasculitis [63]. Furthermore, the correlation
between MRI and angiography is only moderate, and
even brain biopsies show high false-negative results [2].
MRA may reveal stenosis and occlusion of the proximal
intracranial arterial branches, but no prospective studies
are available on the sensitivity and specificity of MRA
[64]. Therefore, only positive MRA results can directly
influence clinical management.
Moyamoya disease is a rare progressive cerebrovas-
cular occlusive disease characterized by the development
of small arterial and arteriolar collateral vessels around
the obstructed major arteries [65]. These new vessels
show a typical angiographic appearance ‘‘like a puff of
970

Fig. 18 Double plane venous MRA. Maximum flow enhancement
can be achieved when the imaging plane is perpendicular to the
vessel being imaged. The caudal portion of the superior sagittal
sinus (open arrows) is best imaged in a and the transverse sinus
(white arrow) in b. Compare the imaging planes, the trajectory of
the vessels being imaged, and the corresponding flow enhancement
changes in different venous segments
smoke’’ or a ‘‘moyamoya’’, which is a word derived
from Japanese. Affected children have risks of cerebral
ischemia resulting in transient ischemic events or
strokes. Typical vascular changes have also been de-
scribed for other conditions, such as neurofibromatosis,
Sjögren syndrome, Down syndrome, and previous irra-
diation [65]. These secondary vascular changes are
termed ‘‘moyamoya syndrome’’, which resembles pro-
gressive occlusive vasculopathy. MRA is usually able to
demonstrate these abnormal vessel areas in most cases
and has been suggested as an alternative to the more
robust digital subtraction angiography technique in the
diagnosis [65].

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