John
Huston
III, MD
#{149} Daniel
A. Rufenacht,
MD
#{149} Richard
L. Ehman,
MD
#{149} David
0. Wiebers,
MD
Intracranial Aneurysms and Vascular Malformations: Comparison of Time-of-Flight and Phase-Contrast MR Angiography’ Twenty-seven patients with 14 aneurysms and 17 vascular malformations were each examined with both timeof-flight (TF) and phase-contrast (PC) magnetic resonance angiography of the head. Three-dimensional (3D) PC imaging depicted the patent lumen of the aneurysms, while 3D TF imaging depicted the patent lumen and a subacute thrombus if present. The 3D PC techniques were superior to 3D TF methods in depicting aneurysms larger than 15 mm. PC angiography allowed velocity resolution of vascular lesions and yielded functional flow information by directly depicting collateral flow to vascular lesions. Artifacts present on TF images were due to substances with short Ti, hemosiderin, and surgical clips. Artifacts present on PC images were due to flow-related aliasing. The results showed that PC techniques have specific advantages over TF techniques, including identification of large aneurysms, velocity resolution of vascular lesions, depiction of flow direclion about the circle of Willis, and less degradation by artifacts. Index terms: teriovenous
Cerebral Magnetic studies ogy,17.1214
Radiology
Aneurysm,
cerebral,
malformations,
blood
vessels,
resonance #{149} Magnetic
1991;
10.73
cerebral,
MR studies,
(MR), comparative resonance (MR.),
Ar-
#{149}
10.75
17.1214
T was
181:721-730
known
long
of magnetic nesoto flow phenomena before
the
cessfully
applied
to intracranial
dis-
ease (8-il). A significant drawback to PC imaging has been the long imaging time, which ranges up to 37 mmutes pen acquisition (10). New PC pulse sequences have substantially shortened the examination time (12). studies
systematically
comparing
PC and TF techniques as regards their ability to contribute to the clinical evaluation of vascular lesions have been reported, to our knowledge. The
purpose
of this study
was to compare
and contrast three-dimensional (3D) PC and 3D TF MR angiographic techniques in patients with intracranial aneurysms
From the Departments of Diagnostic ogy Q.H., D.A.R., R.L.E.) and Neurology I
Radiob-
(DOW.), Mayo Clinic and Mayo Foundation, 200 First St SW, Rochester, MN 55905. From the 1990 RSNA scientific assembly. Received February 21, 1991; revision requested April 3; final revision received July 8; accepted July 15. Address reprint requests to J.H. C RSNA, 1991
and
vascular
tages in the lesions.
evaluation
of vascular
technique
was applied to imaging. With the onset of MR imaging, flowing blood was noted to have distinct appearances (1). Initial efforts were directed to eliminating the complex flow effects from blood by using presatunation and gradient-moment-nubling techniques (2,3). Subsequently, pulse sequences and image-processing techniques were developed to provide projection angiographic images of flowing blood. The two major techniques for this purpose are time-offlight (TF) (4,5) and phase-contrast (PC) (6,7) angiography. TF imaging exploits the inflow of fully magnetized blood into a saturated stationary tissue. PC techniques make use of bipolar pulse sequences to detect a shift in the phase caused by blood flowing through a magnetic field gradient. Recently, both TF and PC MR angiographic techniques have been suc-
No technob-
sensitivity nance (MR)
HE
malforma-
tions. For that reason, the patients were studied with both techniques and the results were compared with those of conventional angiography, MR imaging, and computed tomography (CT). One of the hypotheses of the study was that the versatile velocity-sensitive capability of PC angiognaphy would provide specific advan-
MATERIALS
AND
Twenty-seven
METHODS
consecutive
patients
with
14 aneurysms and I 7 vascular malformations were examined with a I .5-T super-
conducting imaging system (Signa; GE Medical Systems, Milwaukee). Twenty-six of the patients underwent conventional arteriography, 27 underwent
16 underwent CT, standard spin-echo
and all MR im-
aging at the time of their MR angiography examinations. Standard MR head imaging was performed with sagittal Ti-weighted (repetition time msec/echo time msec 192
=
500-600/13-20;
views)
and
transaxial
(2,300-2,500/30, sequences.
80;
two excitations; T2-weighted
one excitation;
192
views)
Vascular
MR
imaging
was
performed
with the Multisequence Vascular Package (GE Medical Systems) with use of 3D IF, two-dimensional (2D) PC, and 3D PC techniques. The 2D and 3D PC sequences used
in this study
encode
have
for maximum
the capability
velocities
to
ranging
from 5 to 400 cm/sec. The echo time in all studies was automatically set to a minimum by the vascular imaging software.
The frequency-encoding anteroposterior
direction
in all cases.
Flow
was compen-
sation in the read and section direction was used with the TF and PC 3D sequences. In the PC studies, bipolar flow-encoding gradients were used. A 28section 3D IF sequence required approximately 3 minutes and a 60-section sequence, approximately 7 minutes. The 3D PC technique required approximately 7 minutes for a 28-section and 14 minutes for a 60-section volume acquisition. Approximately 20 minutes was required for the reconstruction and projection image postprocessing of a 60-section 3D PC study. During reconstruction and postprocessing, additional imaging was per-
formed.
Abbreviations:
AVM
=
arteriovenous
malfor-
mation, MIP = maximum intensity projection, PC = phase contrast, IF = time of flight, 3D three-dimensional, 2D = two-dimensional.
=
721
Figure 1. PC collapse
Sagittal image
2D PC scout with posterior
image (a), 3D subvolume
outlined (b), 3D collapse image with right carotid subvobume outlined (c), and 3D PC posterior subvolume (d) of a 70-year-old man with a 4-mm basilar tip aneurysm (arrowhead in d), obtained with use of 60 sections 1 mm thick. Images include the posterior infenor cerebeblar arteries. Note segment of right internal carotid artery partially included in the posterior subvolume (arrow in d) and black-and-white-reversed photographic technique.
Aneurysms A sagittal 2D PC scout image with 30cm/sec maximum velocity encoding was obtained to localize the volume for 3D TF and 3D PC imaging. Then 3D TF imaging was performed (40/4.3-4.9; one excitation; 192 views; flip angle, 20#{176}; field of view, 18 cm) with use of 28 or 60 axial sections be-
tween
0.7 and
1.0 mm thick.
3D PC angiography 36/7.4-8.2;
angle,
one
128
(26-
views;
flip
18 cm; maxi-
velocity encoding, 30-60 cm/sec) use of 28 or 60 axial sections between and
1.0
mm
nique proved medium and useful
as an
tab scout With quences, sity
excitation;
b.
Additionally,
performed
15#{176}-20#{176}; field of view,
mum with 0.7
was
a.
thick.
The
2D
PC
tech-
inadequate to evaluating small aneurysms but was approximate
2’/2-minute
for
sagit-
sequence. both the 3D IF and 3D PC sepostprocessing maximum inten-
projection
(MIP)
images
through
the
entire imaging volume were automatically generated. This resulted in 19 MIP images perpendicular (projection
eliminate sels,
to the axial imaging images) at 10#{176} increments.
the problem
postprocessing
tamed.
These
plane To
of overlapping subvolumes
subvolumes
were
yes-
were
ob-
selected
from the MIP image along the axial imaging plane (collapse image) of both the 3D IF and the 3D PC series. The collapse im-
age is a composite
of all the flow informa-
tion contained in the individual contiguous axial sections. A circle was used for the posterior circulation and a rectangle for
the right
and left carotid
distributions,
with care taken to include the anterior communicating artery in both carotid volumes (Fig 1). Viewing the individual subvolumes in a cine loop on an independent monitor enhanced the perception of the 3D relationship of the vessels and facii-
tated identification of small aneurysms. Surgical aneurysm clipping confirmed the
presence
of seven
aneurysms
in seven
of the 12 patients.
Vascular
Malformations
quently, 3D PC angiography was performed (25-33/4.7-9.7; one excitation; 128 views; flip angle, 15#{176}-20#{176}; field of view, 20 cm; maximum velocity encoding, 10-120 cm/sec) with use of 60 axial sections between 0.7 and 2.0 mm thick. Imaging of six of 17 patients with vascular lesions included use of the contrast agent gadopen-
tetate
722
#{149} Radiology
dimeglumine
(Magnevist;
Berbex
Imaging, Wayne, PC examinations
NJ). The 3D TF and 3D made use of the same
section
for
thickness
each
patient.
The
sec-
tion thickness was selected to encompass the entire vascular malformation and anticipated venous drainage as depicted on the 2D PC scout image, the standard MR head image, and the conventional angiogram. Nineteen MIP images in 10#{176} increments through the entire imaging volume were automatically generated with the 3D pulse sequences. Frequently, no additional postprocessing
A sagittab 2D PC scout image at 30-cm/ sec maximum velocity encoding was obtamed to localize the volume for 3D TF and 3D PC imaging. Then 3D TF angiography was performed (40/4.3-4.9; one excitation; 192 views; flip angle, O; field of view, 20 cm) with use of 60 axial sections between 0.7 and 2.0 mm thick. Subse-
d.
C.
subvolumes
were
obtained.
Some small vascular lesions required additional postprocessing subvolumes for complete evaluation. The conventional angiographic, CT, and MR images were reviewed together by two neuroradiobogists Q.H., D.A.R.). Therefore, the reviewers had knowledge of the
conventional
angiographic
findings
when
analyzing
the
MR angiographic
studies.
RESULTS
Aneurysms MR angiographic techniques permitted detection of all 14 aneurysms in the 12 patients previously identifled as having aneurysms by means of conventional angiography (Table 1). Aneurysms
were both size
even,
between
increased
the
nique. lumen artery carotid
beyond
15 mm
15 mm,
3D PC technique
gressively
seen
3 and
equally well demonstrated with techniques (Fig 2). As aneurysm
superior
how-
was
to the
pro-
3D TF tech-
IF imaging did not depict the of a 30-mm posterior cerebral aneurysm (Fig 3), and a 20-mm siphon lesion was very faintly on
the
collapse
image
but
not
detected on the projection images. The size of aneunyms as determined with MR angiognaphy was comparable
during
with
conventional
the
size
measured
angiography December
1991
Table
1
Results
of Evaluation
of Aneurysms MR
Conventional
Angiography
TF Technique
Size (mm )
PC Technique
S ize (mm)
Size
Signal Patient/Age
(y)/Sex
Location
of Aneurysm
1/43/M 2/70/M 3/70/M 4/49/M 5/38/M 6/65/F
Left anterior cerebral Anterior communicating* Basilar tip Right middle cerebral Anterior communicating Right superior cerebellart
7/27/M 8/52/F
Left middle cerebral Right cavernous ICA
9/63/F 10/61/F
SI
Right ICA siphon Left ophthalmic Right
ophthalmic
Right cavernous
:
11/30/F 12/64/M
Left posterior Fusiformbasilar*
Note.-AP = anteroposterior, * Subacute thrombus present. t Acute and subacute thrombi
ICA
=
ICA cerebral
internal
carotid
Angiography
#{192}Y RL
SI
AP
RL
(mm
Intensity
Signablntensity
of Fbowjet
SI
AP
RL
of FlowJet
3 3
3 3
3 3
3 5
3 5
3 5
ND ND
3 3
3 3
3 3
ND ND
4
4
4
4
4
4
High
4
4
4
High
5 8 6
5 6 5
5 6 9
9 11
10 8
. . .t
5 10 13 8
5 6 8 10
5 6 10 9
ND ND High High
5 10 4 8
5 6 3 10
5 6 5 9
ND Low Low High
8
11
10
10
High
11
10
10
High
7 4
11 4
10 4
7 4
10 4
9 4
High ND
7
9
9
High ND
. .
ND
.
5
5
5
4
4
4
19
19
28
...
20
25
High
20
25
27 44
29 11
33 12
45
ND 31
28
High ND
24 32
25 9
artery,
ND
=
not demonstrated,
RL
=
right to left, SI
ND
. . .
=
#{149}
.
#{149
High
. .*
30 7
High ND
superoinferior.
present.
Measurement not available. S The 2D PC technique in this case alone proved to be inadequate Aneurysm faintly visible on collapse image only.
in the evaluation
of small -
---- -----
aneurysms.
----.
I Figure
2.
a 3-mm
.-----.------------------------
Images
of a 43-year-old
left anterior
rysm. oblique
(a) Conventional view with
right)
shows
weighted
(arrow).
shows
containing
man
artery
angiogram head turned
the
aneurysm
image
rhage
cerebral
(lateral to the
(b) Ti-
subarachnoid
hemor-
methemoglobin,
is no evidence
with
aneu-
but there
of an aneurysm.
TR
=
repeti-
tion time, TE = echo time. The 3D TF (c) and 3D PC (d) projection images (both obtained with use of 28 sections 0.7 mm thick) demonstrate
the
aneurysm
(arrow)
equally
eral oblique views with the head the left). An air-bone susceptibility is evident
on
the
well
(bat-
turned to gradient
3D TF angiogram
(arrow-
head in c). Some of the signal intensity adjacent to the aneurysm on the 3D IF anglogram is due to the subarachnoid hemorrhage containing
methemogbobin.
b.
a.
short
Ti
(Fig
4). A maximum
velocity
encoding of 30 cm/sec with the 3D PC sequence best demonstrated slow flow within aneurysms. The intrinsic flow pattern within the aneurysm was frequently seen in aneurysms larger than 5 mm (Table 2). The orientation of the entry flow jet in relation to the parent artery as well as the neck and dome of the aneurysm was often cleanly seen (Fig 3). Patient 6 had a significantly smaller
r d.
C.
--- .--“-
“
lumen at 3D PC imaging ventional angiography. studies thrombus
(Table patent tional Volume
1). PC techniques lumen as depicted angiograms, while 181
#{149} Number
3
reflected the on convenIF tech-
niques as well taming
represented as a subacute methemoglobin
the patent lumen thrombus conthat had a
showed that
evidence decreased
than at conCT and MR of an the
acute
lumen
during the 10 days between penformance of conventional angiography and performance of MR angiography. Radiology
#{149} 723
Vascular
Malformations
MR angiognaphic techniques albowed detection of 11 arteniovenous malformations (AVM5), one brain anteniovenous fistula, one dural arteriovenous fistula, and a venous angioma previously
identified
with
conven-
tional angiography (Table 3). Also identified was a lesion consistent with a cryptic vascular malformation in a patient who did not undergo conventional angiography (13-15). With use of the angiographic and standard MR images, the nidus was comparable
size of the AVMs with that at conven-
tional angiognaphy. A 5 x 8 x 12-mm slow-flow AVM and a small thalamic cavernous hemangioma were not visualized at MR angiognaphy. However, both lesions were easily seen on gadolinium-enhanced thin-section Ti-weighted images. Two patients had aneurysms on the feeding artenies to their
AVMs.
The 3D IF technique permitted visualization of the feeding arteries and the size of the nidus of mediumand high-flow AVMs. The proximity of the AVM nidus to the internal carotid and basilar arteries was related to the intensity
of the
nidus, Those
eral
signal
within
to saturation
lesions
that
had
cause
flow
owing lower
the
were
signal
feeding
the
effects. more
periph-
intensity
vessels
be-
traveled
through more of the saturated imaging volume. The 3D PC technique depicted the feeding arteries, nidus, and draining veins of mediumand high-flow AVMs,
depending
on
coding. A maximum ing of 10-20 cm/sec and medium-velocity tunes,
while
of greater
cm/sec
yielded
arteries, nidus, veins (Fig 5). The number was
identified quite
velocity
en-
encod-
highlighted
slow-
venous
a maximum
coding
branches raphy
the
velocity
of the
to 60 feeding
ity encoding was tiate the high-flow
high-velocity
of feeding with variable.
maximum
velocity
3D PC image of a left (patient 13). Frequently, obscured adjacent seen during the
MR angiogAll of the
encoding
PC images. of
conventional angiography. Angiographicalby proved direct anteriovenous fistulas were seen associated with AVMs in two patients or isolated in one patient. The 3D PC technique with high maximum veboc724
#{149} Radiology
fis-
Patient 7, who had a large single direct arteriovenous fistula, showed an associated aneurysm with distinct MR angiographic characteristics of an internab flow jet on both 3D IF and 3D
pnecentral AVM the nidus
arteries clearly early arterial phase
useful to differenanteniovenous
tula from the associated AVM. MR angiographic findings for arteniovenous fistulas included a small nidus compared with the relatively large size of the arterial feeding arteries and barge ectatic veins with high flow.
arterial
feeding arterial branches identified with conventional angiography were identified at MR angiography in only one patient. This occurred on a 60cm/sec
Figure 3. Images of a 30-year-old woman with a giant fusiform aneurysm (30 mm) of the proximal left posterior cerebral artery. (a) Flow jet (arrow) is demonstrated on an early arterial image obtained with digital subtraction angiography. (b) Sagittal 2D PC image obtained in the midline with 30-cm/sec maximum velocity encoding demonstrates the giant aneurysm (arrow). (c) A 3D PC projection image obtained with use of 60 sections 0.7 mm thick demonstrates the flow jet (arrow) and aneurysmal lumen (arrowheads). (d) A 3D TF projection image obtained with use of 60 sections 0.7 mm thick demonstrates the flow jet (arrow) but does not depict the lumen. The 3D TF collapse image also failed to depict the lumen. Note the wider arterial lumina on the 3D PC image compared with those on the 3D IF image.
en-
or equal
images
and
struc-
velocity
than
d.
C.
In retrospect,
this
mum
3D PC technique velocity
sec allowed
encoding
identification
with
vascular
malformations.
Six of the
seven patients with deep venous drainage were identified with use of a maximum velocity encoding of 20 cm/sec
or slower.
Gadolinium enhancement improved the visualization of the vasculan structures with both 3D IF and 3D PC techniques. The increased visibility was more tunes (Fig 7).
evident
in venous
struc-
aneu-
rysm was visible on the conventional angiogram but not clearly distinguishable from adjacent, rapidly filling yenous structures (Fig 6).
The
draining veins observed with conventional angiognaphy in four of the 14
a maxi-
of 10-20
cm/
of all the
DISCUSSION Previous reports have efficacy of MR angiography
explored th in depict-
ing intracranial
structures.
These
studies
vascular have
used
either
December
IF
1991
Table 2
Depiction Flow
of Aneurysmal
Internal
Jets
No. of Flow Jets Seen with Technique Aneurysm Size (mm)
Total No. of Aneurysms
3D TF
3D PC
5 >5
6 8
1 6
1 7
techniques were performed with somewhat different matrix sizes and total acquisition times. The 3D IF studies
were
spatial
b.
a.
performed
resolution
with
than
higher
the 3D PC
studies and required less acquisition time when performed with use of parameters similar to those reported in
published trix sizes studies,
studies (8,9). If similar mawere used in the 3D PC the
acquisition
time
would
be
unacceptably long. In planning this study, it was hypothesized that the use of fewer phase-encoding steps for 3D PC studies may
be acceptable
given
unique
physical
of these
tions. sitions
basis
Nevertheless, the were approximately
the
3D
acquisi-
PC acquitwice as
long. It is conceivable that some of the results of the 3D IF studies could have been improved by allowing an acquisition time similar to that of the PC studies. For instance, it may have been possible to improve the depiction of slow-flowing blood by reducing saturation effects (16). However, some
of the
areas
in which
demonstrated special the 3D PC technique on
d.
C.
Figure 4. Images of a 64-year-old man aneurysm. (a) Conventional angiogram posterior view). The proximal aneurysmab
weighted
MR image
extrinsic maximum angiogram.
lumen
shows
a large
with a partially thrombosed obtained by means of left lumen is outlined with
amount
to the patent lumen (arrow). TR velocity encoded 3D PC projection Slow flow through the fusiform
size (arrows)
image does not ing methemoglobin.
to saturation
allow
effects.
unsaturated
blood
when
compared
with
of subacute repetition
=
image, aneurysm
that
thrombus time, TE
The left posterior the
anterior
cerebral
=
on the conventional
artery
fusiform basilar vertebral injection arrows. (b) Sagittal
containing echo time.
from the of the
(arrow)
artery (anteroTi-
methemoglobin (c) A 45-cm/sec
which is analogous to the results in an underestimation
differentiation of the patent lumen Slow flow resulted in nonvisualization from
the
angiogram.
(d) The 3D IF
is visualized
due
containowing
to inflow
of
circulation.
or PC
(9,10)
techniques.
The
goal of this study was to directly compare and contrast 3D IF and 3D PC angiographic sequences in a series of patients with intracranial aneurysms and vascular malformations. The main differences in the results obVolume
181
#{149} Number
3
physical
basis
resistance
with IF in depiction
ena, depiction short Ii, and
and
PC techniques of flow phenom-
of substances having the specific artifacts that
affect each technique. In reviewing these be noted that the 3D
it should 3D PC
arti-
Phenomena
While all aneurysms were identifled as morphologic abnormalitiesanalogous to the results achieved with conventional angiographyinternal
flow
jets
3). Creation
dependently
and
disruption
of
were addibe observed
of subvolumes
view
to in-
carotid
arteries
and evaluation of aneurysms. flow jets were demonstrated
aging
aneurysms
in seven (Table
crucial
and
cation Internal and
was
the
basilar
in eight results, IF and
of the
to certain
flow in the parent artery tional findings that could tamed were
results
These capabilities include background suppression, of functional flow informa-
and
Flow
conventional of the
subacute thrombus distal basilar artery
tion, facts.
(Fig (8,11)
unique
method. superior provision
the
capabilities for seem dependent
with
aneurysms
for
identifi-
PC
imaging
with
IF
2). In all saccular
Radiology
im-
aneu-
#{149} 725
--
banger than ing demonstrated All flow jets were of increased signal IF technique. Six observed with PC rysms
as increased
bow-intensity to phase complex the internal aneurysms, ous studies niques
5 mm, 3D PC imagan internal flow jet. depicted as streams intensity with the of the eight flow jets imaging were seen signal intensity. The two flow jets were attributed dispersion associated with flow. Ihe flow jet indicated flow pattern within the as demonstrated by previin which cine MR tech-
were
used
(17-19).
The
artifact
of MIP
display
the
amount
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