Neuroradlology Heinrich Dennis
Mattle,
MD
J. Atkinson,
Middle ofFlow
#{149} Robert
MS
R. Edelman, Ellert,
Velocity
measurements
were
terms:
angiography,
Blood, 17.1214
MR studies, 17.1214 (MR), experimental, Radiology
1991;
flow dynamics #{149} Cerebral #{149} Cerebral blood vessels, #{149} Magnetic resonance 17.1214
181:527-530
number such (2),
U. Wentz,
MD
#{149} Moshe
A. Reis,
PhD
Determination MR Angiography’
with
made in a phantom and in the middle cerebral artery of six volunteers. Velocities were assessed in the volunteers before, during, and after finger movement. Average values for mean maximal velocities determined with MR angiography were 69.8 cm/sec before, 77.2 cm/sec during, and 69.6 cm/sec after finger movement. Correlations between values obtained with MR angiography and transcranial Doppler (TCD) sonography were r = .86 and P = .0001 for values obtained at rest and r = .84 and P = .0001 for values obtained during finger movement. The velocity increase during finger movement compared with that at rest was 11% for MR angiography and 11.3% for TCD sonography. Values measured with TCD sonography, however, were less than those measured with MR angiography (P = .001). The results show the feasibility of measuring flow velocities in intracranial arteries with MR angiography. Index
#{149} Klaus
Artery:
Cerebral Velocities
A magnetic resonance (MR) angiographic technique for noninvasive measurement of flow velocities in the intracranial cerebral arteries was studied.
MD MD
#{149} Thomas
MR angiography studies were formed with a 1.5-T whole-body
of pathologic conditions as stenosis (1), vasospasm
arteriovenous
malformation
(3),
system
(Magnetom;
tems,
Iselin,
Siemens
NJ)
with
perimaging
Medical
a quadrature
Syshead
cerebral infarction (4), and occlusive disease of the extracranial cerebral arteries (4,5) alter the velocity and pulse waveform in the intracranial
coil. The basic technique for this method for flow measurement is to apply a radio-frequency presaturation pulse to eliminate
arteries.
signal
To
date,
the
only
means for detecting has been transcranial sonography
(6,7).
resonance have been
noninvasive
these changes Doppler (TCD) Recently,
images
(8-12).
from
the brain
and
intracranial
over
a user-defined rectangular Basically, it is a modification
ume.
yesvolof dy-
bolus tracking. A time interval, t, is then allowed to elapse for fresh, unsaturated spins to flow into the presaturation slab. The in-flowing spins appear to have high signal intensity and are easily distinguished from the dark background tissues, namic
magnetic
(MR) imaging methods developed for creating
giogramlike
sets
an-
Typically,
MR angiograms are created by postprocessing images obtained with either two- or three-dimensional flowsensitive gradient-echo techniques. MR angiography can demonstrate the anatomy of the basal cerebral arteries (13). Functional information (eg, flow velocities or the dynamics of vessel filling as observed in sequential subtraction angiography) (14,15), however, is not directly available from such images. To optimize evaluation of flow dynamics, we applied a modifled version of a previously described method to measure flow velocities in the middle cerebral artery (MCA) (1618). The flow velocities obtained with MR angiography were compared with those measured with TCD sonography.
as well
as from
dark
blood
that
spins
is calculated
the equation
from
v
d/t, traveled =
the
to the cardiac
cycle with
gating
surements
images
with
the time is synchronized
during
electrocardio-
to provide
at multiple
The yearterial
where d is the maxiby the high-signal-
mal distance intensity in-flowing spins interval t. Data acquisition graphic
mi-
was
tially in the area of presaturation. locity (v) of the fastest flowing
meaof the car-
velocity
phases
diac
cycle. The MR imager used for this permits arbitrary angulation and positioning of the presaturation regions and imaging sections. As a result, it was study
feasible
to orient
a single
along
the
length
MCA
and to obtain
imaging
of the main
velocity
stem
section of the
measurements
with a single acquisition. Careful positioning of the imaging section is necessary, however, to ensure that the vessel under
is entirely encompassed in the imaging section. If the vessel courses out of the study
AND
MATERIALS
imaging
METHODS
section, falsely low velocity meawill be made. Scout images were obtained in sagittal and axial planes to localize the MCA. Then, the main stem of the MCA was imaged in an oblique (coronal/sagittal) plane. Third, bolus tracking was per-
surements
Six MCAs of six volunteers were exammed to measure flow velocities at rest and to determine whether MR angiography can depict flow velocity changes in the contralateral
MCA
lion. The mean 40 years
(range,
during
finger
stimula-
age of the volunteers 30-48
was
years).
I From Harvard Medical School, Boston (H.M.); Department of Radiology, New England Deaconess Hospital, Boston (H.M.); Department of Radiology, Beth Israel Hospital, 330 Brookline Ave. Boston, MA 02215 (H.M., R.R.E., MAR., D.J.A.); Department of Radiology, University of Heidelberg, Klinikum Mannheim, Mannheim, Germany (K.U.W., T.E.); and Siemens Medical Systems, Iselin, NJ (D.J.A.). Received August 29, 1989; revision requested November 7; final revision received June 3, 1991; accepted June 24. Address reprint requests to R.R.E. C RSNA, 1991
formed
in the plane
of the MCA main
stem. Imaging parameters for the bolus tracking sequence were as follows: repetition times of 40-60 msec, echo time of 10
Abbreviations:
SD
=
standard
MCA
deviation,
= middle
TCD
cerebral
artery,
= transcraniat
Doppler.
527
msec,
flip
eraged.
angle
of 30#{176}, and
Time
between
presaturation
and
acquisition view was 5 mm
readout
matrix 23 cm,
(Fig
perpendicular
tamed
to determine
19.3
were
cardiac
image
av-
of was
obtained
cycle.
at
Finally,
to the the
msee,
x 256, field thickness
images
of the
signal
was
was 192 and section
1). The
15 phases
one
radio-frequency
MCA
area
an
was
of the
ob-
vessel
lumen. Imaging time for velocity measurement was approximately 3 minutes. TCD sonography measurements were performed within 30 minutes after the MR examination with a transcranial Doppler instrument
(TC2-64;
Elektronik
Eden
GmbH,
many). pulsed
It is a low-frequency, Doppler system
the
The probe zygomatic
With
was positioned arch
and
basal
courses sound
at an beam.
arteries,
acute angle The center
ume of the instrument of 55 mm to receive The
close
the
ear.
in this and
plane the
MCA
to the ultraof the sample
vol-
was
to the
resulting
to the
was in the same
cerebral
spectrum
just above
anterior
performed
the probe
as the
pene-
beam through of the temporal
the examination
manner,
Ger2-MHz enables
that
tration of the ultrasound the squamous portion
bone.
Medizinische
Ueberlingen,
a. Figure
b.
1. Modified bolustracking ages obtained along the main stem increased displacement of the dark, tagged bolus of flowing blood.
technique in a volunteer. Oblique bolus-tracking of the MCA during early (a) and peak (b) systole. tagged bolus in the MCA. Arrow = trailing edge
MR imNote the of dark
set at a depth
Doppler shift origin of the MCA.
Doppler
shift
spectrum
is
displayed with a fast Fourier-transform sequence with 64 frequency points and 17p.sec time resolution. The measurements were documented on a Sony video graphic printer UP-811 (Japan). Flow yelocity
readings
were
made
in centimeters
per second from the envelope pler shift spectrum as recorded copies.
Both
TCD
angiography tamed
of the Dopon hard
sonography
and
measurements at the
cardiac
same
MR
were
15 time
ob-
points
in the
cycle.
To
test
flow
the
MR
phantoms
same sisted radius ranged
angiography
were
pulse sequence. of a circular of 1.44 mm. within the
technique,
imaged
with
the
The phantom eontubing with an inner The tubing was arhead coil so that the
tube paralleled the imaging plane 5 cm to avoid additional in-plane tion effects. Continuous flow was
for only saturagener-
ated with a pump that was connected the tubing. Reference flow volumes measured with a flow meter working the basis of electromagnetic induction
(FCM; flow
Gambro, velocities
Lund, (Vme.,,,)
Sweden). were
to were on
Mean
calculated
with
the formula Va,,.,,, flow volume/rr r . The velocity of the fastest moving spins was measured with MR angiography with the same technique used to study the MCA of the
volunteers.
from
The
5 em/see
Comparison and Doppler angiography made with
flow
velocities
ranged
to 82 em/see.
of the MR angiography results in volunteers and MR results in the phantom were simple regression analysis of
corresponding
values
and
matched-pairs
signed
ranks
the
Witeoxon
test.
RESULTS Contrast and
528
between
nonpresaturated #{149} Radiology
quate nation Mean
to permit flow velocity determiwith MR imaging in all MCAs. maximal velocities measured
with
MR angiography
are given in Tables I and was a significant correlation alt mean maximal velocities with MR angiography and TCD sonography (r = .602, F = 9.1, and P = .008). Moreover, in each of
the
18 measurements
relation surements
mined
presaturated
spins
was
ade-
between the in a cardiac
with
there
was
a cor-
15 velocity meacycle as deter-
MR angiography
and
in the plane higher than those TCD sonography
of the MCA, determined
(P
=
.001).
The
TCD
for
be corrected
sional locity,
since
sonography could the three-dimenof the MCA to ob-
for
angulation a true
estimate the
of exact
the
correct
position
yeof
the
Doppler probe in relation to the course of the main stem of the MCA was not known. A graphic display of a velocity
measurement in a single both MR angiography and TCD sonography and averaged vetocity measurements at rest are shown in Figure 2. artery
During
TCD sonography (P values ranged from .049 to .0001). The average vatues for MR angiography and TCD sonography correlated at rest and during finger movement (r = .86, F = .37.2, P = .0001 and r = .84, F = 30.9, P = .0001, respectively); however, the velocities determined with MR angiography, which were were with
not
tam
TCD
sonography 2. There between obtained
obtained
the
and
velocities
with
finger
movement,
the
in-
of mean maximal velocities was 11% (SD, 6.1%; range, 5.0%-21.1%) at MR angiography and 11.3% (SD, 4.5%; range, 6.5%-20%) at TCD sonography. The velocities obtained during finger movement were significantly higher than those at rest both for MR angiography (P = .025) and TCD sonography (P = .025), and the velocities at rest before and after finger movement did not differ. During finger movement, TCD sonography crease
November
1991
120 0 a
,
-.#{149}.--
MR
-#{149}--
TCD
100
20
100
0 >.
so
80
a >
60
40
20 20
o
“0
20
15
Measurementnumber In cardiac
0
1
2
3
cycle
4
5
#{149}
i”ias’i’iet
a.
,
$
ii,’ibs’
#{149}10
111213141
caithac
rycie
S
velocities measured as assessed with movement
as
assessed
MCA with Vertical
MR imaging lines indicate
TCD sonography.
with
y
= 16.990
Vertical
1.3967x
+
-
R’2
20
40
60
flow v.Ioctty
80
(cm/sc)
Figure
3 shows
mean
velocities
this
measurement showed a significant velocity increase of 4.4% (SD, 2.0%; range,
comparison,
crease,
however,
that
hemisphere
were
(P
The
outline
urated laminar culated Vrnean
the
activated
=
MCA
X
lOX
for
as cat-
also
referred
locity
(7).
area,
where
15 peak
during
one
volunteers
was 138-161
MCA
max
in the ±
io
ii
cida
a
ii
t
is
cycle
There
only
indirectly
by vessel
intensity of flowing study demonstrated
catty
is not
MR
angiography
available
and
with
MR
can
accurately
of flow
enable
velocities
extracranial
in
relatively
large
and veins. correlation measured
Our study shows a good between the velocities with MR angiography and with The
arteries
TCD sonogravelocities ob-
tamed with MR angiography, however, were higher than those measured with TCD sonography. The MR measurements were obtained directly
in the
plane
of the
MCA.
In
flow calculations, however, was significantly limited by the in-plane resolution of the images. In conclusion, we have shown that MR angiography can be applied to determine flow velocities in the MCA
uration pulses, the origin and direction of flow can be depicted and functional information about collateral circulation is provided, which typi-
using
method
presat-
was
MR angiography depicts vascular structure. Flow dynamics are mdicated
MCA.
since ages
in the phan(or 73.5 cm/sec
velocities).
in the
blood. that
of from
by
8.3
g
size
For
ye-
the displacement spins into the pre2
of MR
DISCUSSION
is
#{149}
ii’ibs,
TCD sonography, there is an unknown angle between the ultrasound beam and the main stem of the MCA. Flow velocity measurements obtained with TCD sonography are, therefore, expected to be lower than those obtamed with MR angiography, where there is no angle correction necessary. In addition, our study demonstrates that velocity changes induced by physiologic maneuvers can be detected with MR angiography. Motor cortex activation by means of finger movement increased flow velocities by 11%. Moreover, MR angiography permits estimation of flow volumes,
mean
calculated
measurements 36.7 cm/sec mean
mean with
six
mL/min).
#{149} Number
two
geometric
velocities
and signal A previous
cycle,
maximal
150 mL/min
In the phantom, of the unsaturated 181
Vn,can
cardiac flow
mean
unsat-
velocities
to as mean Mean
the
geometric measured 71.7 cm/sec.
significant correlation between the values displayed in Figure 3 (r = .962, F= 288,P= .0001).
MR angiogra-
of the
measured
Volume
than
cerebral
in-flowing
The velocities was
the flow tom was
spins was parabolic, indicating flow. Thus, flow could be calaccording to the formula ‘/ x
mean
(range,
with
of the
the
Measurements
.005).
not obtained in this side.
phy
smaller
was
in the directly
#{149} iieI
velocity
those measured phy in volunteers.
culated from the flow volume measurements in relation to the peak yelocities as measured with MR angiography. the peak angiography
flow
determination
saturation slab showed a parabolic profile and indicated laminar flow.
in-
5
This vessel represents a particular challenge because of its high flow yelocities (peak velocity often exceeding 1 m/sec during systole) and relatively small diameter (approximately 3 mm). Previous MR studies with bolus tracking techniques have shown that
Figure 3. Mean flow velocities in the phantom as calculated from the flow volume in relation to the peak flow velocities as measured with MR angiography.
fingers, activation .005). The
4
raphy alone (19). In the present study, we demonstrate the use of MR angiography with presaturation to
0.926
quantify
mean
ipsilateral to the moving probably due to cortical over callosal fibers (P =
‘i
lCD sonography. (b) Graph of average velocities in six SD from the mean value. (c) Graph of average velocilines indicate ±1 SD from the mean value.
0
hemisphere
3
and ±1
U 0
in the
2
c.
in a single MR imaging.
200
1.8%-7.4%)
1
asie
b.
Figure 2. (a) Graph of flow MCAs during finger movement ties in six MCAs during finger
0
angiog-
a
it provides of the MCA.
cross-sectional The accuracy
Radiology
imof our
#{149} 529
and that it provides good correlation with TCD sonography. At present, evaluation of these methods is limited by the lack of a true standard of reference. TCD sonography is certainly a fast and inexpensive bedside tool for measurement of flow velocity. Measurements of flow volume with Doppler involve a more detailed analysis of the Fourier power spectrum, however, and the validity of the measurements is controversial (20,21). MR angiography has the advantage of providing both velocity and crosssectional area of intracranial vessels, allowing direct flow-volume calculation. This capability may eventually permit measurement of cerebral blood flow in the territories of the main cerebral arteries. It should prove complementary to MR angiography techniques for assessment of regional cerebral blood flow dynamics (22) and perfusion and diffusion measurements (23). U
3.
4.
5.
6.
8.
Aaslid
R, Huber
of cerebrovaseular Doppler ultrasound. 37-41.
530
#{149} Radiology
P. Nornes
H.
spasm with J Neurosurg
9. 10.
ME,
Bernstein
15.
16.
12.
13.
MR angiography. 799. Rivoir R, Huber Neuroradiology
P. Sequential 1974; 8:85-90.
subtraction.
Huber
R, Magun
Investiga-
P, Rivoir
by magnetic
Reson 17.
18.
resonance.
Science
1985;
230:946-
19.
20.
22.
1988;
WT, Du
LN,
angiograms
of blood
fast passage.
3:454-462. Ruggieri
PM,
12:377-382.
Faul
Laub
DD,
et at.
labeled
Magn
Reson
son
DJ.
nor
sagittal
GA,
Masaryk
by
1986;
TJ, Modic
imaging.
Magn
4:199-205.
quantification
sinus
in the
with
MR.
supe-
Neurology
40:813-815.
Edelman Magnetic
RR, Mattle resonance in the
circle
H, O’Reilly GV, imaging of flow of Willis.
Stroke
et al. dy1990;
Aaslid
R, Lindegaard
KF,
Sorteberg
W,
Nornes namics
H. Cerebral autoregulation dyin humans. Stroke 1989; 20:45-52.
Kontos
HA.
Edelman
Validity
calculations (editorial). RR,
Mattle
of cerebral
from Stroke HP,
arterial
velocity mea1989; 20:1-3.
Atkinson
DJ,
et at.
Cerebral blood flow dynamics: assessment with dynamic contrast-enhanced T2* weighted MR imaging at 1.5 T. Radiology 1990; 176:211-220.
adia-
MT. Intracranial circulation: pulsesequence considerations in three-dimensionat (volume) MR angiography. Radiology 1989; 171:785-791. Masaryk TJ, Modie MT, Ross JS, et at. Intracranial circulation: preliminary clinical results with three-dimensional (volume)
Flow
blood flow surements
Projec-
Med
1986;
Edelman RR, Mattte H, Kleefietd J, Silver MS. Quantification of blood flow with dynamic MR imaging and presaturation botus tracking. Radiology 1989; 171:551556. Mattle HP, Edelman RR, Reis MA, Atkin-
namics
Assist
Tomogr
H.
171:793-
21:56-65.
21.
Dixon
1989;
resonance
Imaging
1990;
sonog1986. et al. with
Radiology
tion of early ifiling veins by sequential subtraction. Neuroradiology 1975; 10:35-41. Axet L, Shimakawa A, MaeFallJ. A timeof-flight method of measuring flow velocity
EF,
948. Dumoulin CL, Hart HR. MR angiography. Radiology 1986; 161 :717-720. Laub GA, Kaiser WA. MR angiography with gradient motion rephasing. J Comput
batie
Evaluation
transeranial 1984; 60:
Rossman
Aaslid R, ed. Transeranial Doppler raphy. New York: Springer-Verlag, Wedeen VJ, Meuli RA, Edelman RR, Projective imaging of pulsatite flow
tion
Lindegaard KF, Bakke SJ, Aaslid R, Nornes H. Doppler diagnosis of intracranial artery occlusive disorders. J Neurol Neurosurg Psychiatr 1986; 49:510-518.
PA,
Torem 5, Ringelstein EB, Otis SM. Effect of internal carotid artery occlusion on intracranial hemodynamics: transeranial Doppler evaluation and clinical correlation. Stroke 1988; 19:589-593. Aaslid R, Markwalder TM, Nornes H. Noninvasive transeraniat Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982; 57:769-
magnetic
References
2.
Schneider
14.
774. 7.
11. 1.
Lindegaard KF, Grolimund P, Aaslid R, Nornes H. Evaluation of AVM’s using transeranial Doppler ultrasound. J Neurosurg 1986; 65:335-344. Mattle H, Grolimund P. Huber P. Sturzenegger M, Zurbrugg HR. Transeranial Doppler sonographic findings in middle cerebral artery disease. Arch Neurol 1988; 45:289-295.
23.
Le Bihan
of perfusion.
D.
Magnetic
Magn
resonance
Reson
Med
imaging
1990;
14:
283-292.
November
1991
Mattle,
MD
J. Atkinson,
Middle ofFlow
#{149} Robert
MS
R. Edelman, Ellert,
Velocity
measurements
were
terms:
angiography,
Blood, 17.1214
MR studies, 17.1214 (MR), experimental, Radiology
1991;
flow dynamics #{149} Cerebral #{149} Cerebral blood vessels, #{149} Magnetic resonance 17.1214
181:527-530
number such (2),
U. Wentz,
MD
#{149} Moshe
A. Reis,
PhD
Determination MR Angiography’
with
made in a phantom and in the middle cerebral artery of six volunteers. Velocities were assessed in the volunteers before, during, and after finger movement. Average values for mean maximal velocities determined with MR angiography were 69.8 cm/sec before, 77.2 cm/sec during, and 69.6 cm/sec after finger movement. Correlations between values obtained with MR angiography and transcranial Doppler (TCD) sonography were r = .86 and P = .0001 for values obtained at rest and r = .84 and P = .0001 for values obtained during finger movement. The velocity increase during finger movement compared with that at rest was 11% for MR angiography and 11.3% for TCD sonography. Values measured with TCD sonography, however, were less than those measured with MR angiography (P = .001). The results show the feasibility of measuring flow velocities in intracranial arteries with MR angiography. Index
#{149} Klaus
Artery:
Cerebral Velocities
A magnetic resonance (MR) angiographic technique for noninvasive measurement of flow velocities in the intracranial cerebral arteries was studied.
MD MD
#{149} Thomas
MR angiography studies were formed with a 1.5-T whole-body
of pathologic conditions as stenosis (1), vasospasm
arteriovenous
malformation
(3),
system
(Magnetom;
tems,
Iselin,
Siemens
NJ)
with
perimaging
Medical
a quadrature
Syshead
cerebral infarction (4), and occlusive disease of the extracranial cerebral arteries (4,5) alter the velocity and pulse waveform in the intracranial
coil. The basic technique for this method for flow measurement is to apply a radio-frequency presaturation pulse to eliminate
arteries.
signal
To
date,
the
only
means for detecting has been transcranial sonography
(6,7).
resonance have been
noninvasive
these changes Doppler (TCD) Recently,
images
(8-12).
from
the brain
and
intracranial
over
a user-defined rectangular Basically, it is a modification
ume.
yesvolof dy-
bolus tracking. A time interval, t, is then allowed to elapse for fresh, unsaturated spins to flow into the presaturation slab. The in-flowing spins appear to have high signal intensity and are easily distinguished from the dark background tissues, namic
magnetic
(MR) imaging methods developed for creating
giogramlike
sets
an-
Typically,
MR angiograms are created by postprocessing images obtained with either two- or three-dimensional flowsensitive gradient-echo techniques. MR angiography can demonstrate the anatomy of the basal cerebral arteries (13). Functional information (eg, flow velocities or the dynamics of vessel filling as observed in sequential subtraction angiography) (14,15), however, is not directly available from such images. To optimize evaluation of flow dynamics, we applied a modifled version of a previously described method to measure flow velocities in the middle cerebral artery (MCA) (1618). The flow velocities obtained with MR angiography were compared with those measured with TCD sonography.
as well
as from
dark
blood
that
spins
is calculated
the equation
from
v
d/t, traveled =
the
to the cardiac
cycle with
gating
surements
images
with
the time is synchronized
during
electrocardio-
to provide
at multiple
The yearterial
where d is the maxiby the high-signal-
mal distance intensity in-flowing spins interval t. Data acquisition graphic
mi-
was
tially in the area of presaturation. locity (v) of the fastest flowing
meaof the car-
velocity
phases
diac
cycle. The MR imager used for this permits arbitrary angulation and positioning of the presaturation regions and imaging sections. As a result, it was study
feasible
to orient
a single
along
the
length
MCA
and to obtain
imaging
of the main
velocity
stem
section of the
measurements
with a single acquisition. Careful positioning of the imaging section is necessary, however, to ensure that the vessel under
is entirely encompassed in the imaging section. If the vessel courses out of the study
AND
MATERIALS
imaging
METHODS
section, falsely low velocity meawill be made. Scout images were obtained in sagittal and axial planes to localize the MCA. Then, the main stem of the MCA was imaged in an oblique (coronal/sagittal) plane. Third, bolus tracking was per-
surements
Six MCAs of six volunteers were exammed to measure flow velocities at rest and to determine whether MR angiography can depict flow velocity changes in the contralateral
MCA
lion. The mean 40 years
(range,
during
finger
stimula-
age of the volunteers 30-48
was
years).
I From Harvard Medical School, Boston (H.M.); Department of Radiology, New England Deaconess Hospital, Boston (H.M.); Department of Radiology, Beth Israel Hospital, 330 Brookline Ave. Boston, MA 02215 (H.M., R.R.E., MAR., D.J.A.); Department of Radiology, University of Heidelberg, Klinikum Mannheim, Mannheim, Germany (K.U.W., T.E.); and Siemens Medical Systems, Iselin, NJ (D.J.A.). Received August 29, 1989; revision requested November 7; final revision received June 3, 1991; accepted June 24. Address reprint requests to R.R.E. C RSNA, 1991
formed
in the plane
of the MCA main
stem. Imaging parameters for the bolus tracking sequence were as follows: repetition times of 40-60 msec, echo time of 10
Abbreviations:
SD
=
standard
MCA
deviation,
= middle
TCD
cerebral
artery,
= transcraniat
Doppler.
527
msec,
flip
eraged.
angle
of 30#{176}, and
Time
between
presaturation
and
acquisition view was 5 mm
readout
matrix 23 cm,
(Fig
perpendicular
tamed
to determine
19.3
were
cardiac
image
av-
of was
obtained
cycle.
at
Finally,
to the the
msee,
x 256, field thickness
images
of the
signal
was
was 192 and section
1). The
15 phases
one
radio-frequency
MCA
area
an
was
of the
ob-
vessel
lumen. Imaging time for velocity measurement was approximately 3 minutes. TCD sonography measurements were performed within 30 minutes after the MR examination with a transcranial Doppler instrument
(TC2-64;
Elektronik
Eden
GmbH,
many). pulsed
It is a low-frequency, Doppler system
the
The probe zygomatic
With
was positioned arch
and
basal
courses sound
at an beam.
arteries,
acute angle The center
ume of the instrument of 55 mm to receive The
close
the
ear.
in this and
plane the
MCA
to the ultraof the sample
vol-
was
to the
resulting
to the
was in the same
cerebral
spectrum
just above
anterior
performed
the probe
as the
pene-
beam through of the temporal
the examination
manner,
Ger2-MHz enables
that
tration of the ultrasound the squamous portion
bone.
Medizinische
Ueberlingen,
a. Figure
b.
1. Modified bolustracking ages obtained along the main stem increased displacement of the dark, tagged bolus of flowing blood.
technique in a volunteer. Oblique bolus-tracking of the MCA during early (a) and peak (b) systole. tagged bolus in the MCA. Arrow = trailing edge
MR imNote the of dark
set at a depth
Doppler shift origin of the MCA.
Doppler
shift
spectrum
is
displayed with a fast Fourier-transform sequence with 64 frequency points and 17p.sec time resolution. The measurements were documented on a Sony video graphic printer UP-811 (Japan). Flow yelocity
readings
were
made
in centimeters
per second from the envelope pler shift spectrum as recorded copies.
Both
TCD
angiography tamed
of the Dopon hard
sonography
and
measurements at the
cardiac
same
MR
were
15 time
ob-
points
in the
cycle.
To
test
flow
the
MR
phantoms
same sisted radius ranged
angiography
were
pulse sequence. of a circular of 1.44 mm. within the
technique,
imaged
with
the
The phantom eontubing with an inner The tubing was arhead coil so that the
tube paralleled the imaging plane 5 cm to avoid additional in-plane tion effects. Continuous flow was
for only saturagener-
ated with a pump that was connected the tubing. Reference flow volumes measured with a flow meter working the basis of electromagnetic induction
(FCM; flow
Gambro, velocities
Lund, (Vme.,,,)
Sweden). were
to were on
Mean
calculated
with
the formula Va,,.,,, flow volume/rr r . The velocity of the fastest moving spins was measured with MR angiography with the same technique used to study the MCA of the
volunteers.
from
The
5 em/see
Comparison and Doppler angiography made with
flow
velocities
ranged
to 82 em/see.
of the MR angiography results in volunteers and MR results in the phantom were simple regression analysis of
corresponding
values
and
matched-pairs
signed
ranks
the
Witeoxon
test.
RESULTS Contrast and
528
between
nonpresaturated #{149} Radiology
quate nation Mean
to permit flow velocity determiwith MR imaging in all MCAs. maximal velocities measured
with
MR angiography
are given in Tables I and was a significant correlation alt mean maximal velocities with MR angiography and TCD sonography (r = .602, F = 9.1, and P = .008). Moreover, in each of
the
18 measurements
relation surements
mined
presaturated
spins
was
ade-
between the in a cardiac
with
there
was
a cor-
15 velocity meacycle as deter-
MR angiography
and
in the plane higher than those TCD sonography
of the MCA, determined
(P
=
.001).
The
TCD
for
be corrected
sional locity,
since
sonography could the three-dimenof the MCA to ob-
for
angulation a true
estimate the
of exact
the
correct
position
yeof
the
Doppler probe in relation to the course of the main stem of the MCA was not known. A graphic display of a velocity
measurement in a single both MR angiography and TCD sonography and averaged vetocity measurements at rest are shown in Figure 2. artery
During
TCD sonography (P values ranged from .049 to .0001). The average vatues for MR angiography and TCD sonography correlated at rest and during finger movement (r = .86, F = .37.2, P = .0001 and r = .84, F = 30.9, P = .0001, respectively); however, the velocities determined with MR angiography, which were were with
not
tam
TCD
sonography 2. There between obtained
obtained
the
and
velocities
with
finger
movement,
the
in-
of mean maximal velocities was 11% (SD, 6.1%; range, 5.0%-21.1%) at MR angiography and 11.3% (SD, 4.5%; range, 6.5%-20%) at TCD sonography. The velocities obtained during finger movement were significantly higher than those at rest both for MR angiography (P = .025) and TCD sonography (P = .025), and the velocities at rest before and after finger movement did not differ. During finger movement, TCD sonography crease
November
1991
120 0 a
,
-.#{149}.--
MR
-#{149}--
TCD
100
20
100
0 >.
so
80
a >
60
40
20 20
o
“0
20
15
Measurementnumber In cardiac
0
1
2
3
cycle
4
5
#{149}
i”ias’i’iet
a.
,
$
ii,’ibs’
#{149}10
111213141
caithac
rycie
S
velocities measured as assessed with movement
as
assessed
MCA with Vertical
MR imaging lines indicate
TCD sonography.
with
y
= 16.990
Vertical
1.3967x
+
-
R’2
20
40
60
flow v.Ioctty
80
(cm/sc)
Figure
3 shows
mean
velocities
this
measurement showed a significant velocity increase of 4.4% (SD, 2.0%; range,
comparison,
crease,
however,
that
hemisphere
were
(P
The
outline
urated laminar culated Vrnean
the
activated
=
MCA
X
lOX
for
as cat-
also
referred
locity
(7).
area,
where
15 peak
during
one
volunteers
was 138-161
MCA
max
in the ±
io
ii
cida
a
ii
t
is
cycle
There
only
indirectly
by vessel
intensity of flowing study demonstrated
catty
is not
MR
angiography
available
and
with
MR
can
accurately
of flow
enable
velocities
extracranial
in
relatively
large
and veins. correlation measured
Our study shows a good between the velocities with MR angiography and with The
arteries
TCD sonogravelocities ob-
tamed with MR angiography, however, were higher than those measured with TCD sonography. The MR measurements were obtained directly
in the
plane
of the
MCA.
In
flow calculations, however, was significantly limited by the in-plane resolution of the images. In conclusion, we have shown that MR angiography can be applied to determine flow velocities in the MCA
uration pulses, the origin and direction of flow can be depicted and functional information about collateral circulation is provided, which typi-
using
method
presat-
was
MR angiography depicts vascular structure. Flow dynamics are mdicated
MCA.
since ages
in the phan(or 73.5 cm/sec
velocities).
in the
blood. that
of from
by
8.3
g
size
For
ye-
the displacement spins into the pre2
of MR
DISCUSSION
is
#{149}
ii’ibs,
TCD sonography, there is an unknown angle between the ultrasound beam and the main stem of the MCA. Flow velocity measurements obtained with TCD sonography are, therefore, expected to be lower than those obtamed with MR angiography, where there is no angle correction necessary. In addition, our study demonstrates that velocity changes induced by physiologic maneuvers can be detected with MR angiography. Motor cortex activation by means of finger movement increased flow velocities by 11%. Moreover, MR angiography permits estimation of flow volumes,
mean
calculated
measurements 36.7 cm/sec mean
mean with
six
mL/min).
#{149} Number
two
geometric
velocities
and signal A previous
cycle,
maximal
150 mL/min
In the phantom, of the unsaturated 181
Vn,can
cardiac flow
mean
unsat-
velocities
to as mean Mean
the
geometric measured 71.7 cm/sec.
significant correlation between the values displayed in Figure 3 (r = .962, F= 288,P= .0001).
MR angiogra-
of the
measured
Volume
than
cerebral
in-flowing
The velocities was
the flow tom was
spins was parabolic, indicating flow. Thus, flow could be calaccording to the formula ‘/ x
mean
(range,
with
of the
the
Measurements
.005).
not obtained in this side.
phy
smaller
was
in the directly
#{149} iieI
velocity
those measured phy in volunteers.
culated from the flow volume measurements in relation to the peak yelocities as measured with MR angiography. the peak angiography
flow
determination
saturation slab showed a parabolic profile and indicated laminar flow.
in-
5
This vessel represents a particular challenge because of its high flow yelocities (peak velocity often exceeding 1 m/sec during systole) and relatively small diameter (approximately 3 mm). Previous MR studies with bolus tracking techniques have shown that
Figure 3. Mean flow velocities in the phantom as calculated from the flow volume in relation to the peak flow velocities as measured with MR angiography.
fingers, activation .005). The
4
raphy alone (19). In the present study, we demonstrate the use of MR angiography with presaturation to
0.926
quantify
mean
ipsilateral to the moving probably due to cortical over callosal fibers (P =
‘i
lCD sonography. (b) Graph of average velocities in six SD from the mean value. (c) Graph of average velocilines indicate ±1 SD from the mean value.
0
hemisphere
3
and ±1
U 0
in the
2
c.
in a single MR imaging.
200
1.8%-7.4%)
1
asie
b.
Figure 2. (a) Graph of flow MCAs during finger movement ties in six MCAs during finger
0
angiog-
a
it provides of the MCA.
cross-sectional The accuracy
Radiology
imof our
#{149} 529
and that it provides good correlation with TCD sonography. At present, evaluation of these methods is limited by the lack of a true standard of reference. TCD sonography is certainly a fast and inexpensive bedside tool for measurement of flow velocity. Measurements of flow volume with Doppler involve a more detailed analysis of the Fourier power spectrum, however, and the validity of the measurements is controversial (20,21). MR angiography has the advantage of providing both velocity and crosssectional area of intracranial vessels, allowing direct flow-volume calculation. This capability may eventually permit measurement of cerebral blood flow in the territories of the main cerebral arteries. It should prove complementary to MR angiography techniques for assessment of regional cerebral blood flow dynamics (22) and perfusion and diffusion measurements (23). U
3.
4.
5.
6.
8.
Aaslid
R, Huber
of cerebrovaseular Doppler ultrasound. 37-41.
530
#{149} Radiology
P. Nornes
H.
spasm with J Neurosurg
9. 10.
ME,
Bernstein
15.
16.
12.
13.
MR angiography. 799. Rivoir R, Huber Neuroradiology
P. Sequential 1974; 8:85-90.
subtraction.
Huber
R, Magun
Investiga-
P, Rivoir
by magnetic
Reson 17.
18.
resonance.
Science
1985;
230:946-
19.
20.
22.
1988;
WT, Du
LN,
angiograms
of blood
fast passage.
3:454-462. Ruggieri
PM,
12:377-382.
Faul
Laub
DD,
et at.
labeled
Magn
Reson
son
DJ.
nor
sagittal
GA,
Masaryk
by
1986;
TJ, Modic
imaging.
Magn
4:199-205.
quantification
sinus
in the
with
MR.
supe-
Neurology
40:813-815.
Edelman Magnetic
RR, Mattle resonance in the
circle
H, O’Reilly GV, imaging of flow of Willis.
Stroke
et al. dy1990;
Aaslid
R, Lindegaard
KF,
Sorteberg
W,
Nornes namics
H. Cerebral autoregulation dyin humans. Stroke 1989; 20:45-52.
Kontos
HA.
Edelman
Validity
calculations (editorial). RR,
Mattle
of cerebral
from Stroke HP,
arterial
velocity mea1989; 20:1-3.
Atkinson
DJ,
et at.
Cerebral blood flow dynamics: assessment with dynamic contrast-enhanced T2* weighted MR imaging at 1.5 T. Radiology 1990; 176:211-220.
adia-
MT. Intracranial circulation: pulsesequence considerations in three-dimensionat (volume) MR angiography. Radiology 1989; 171:785-791. Masaryk TJ, Modie MT, Ross JS, et at. Intracranial circulation: preliminary clinical results with three-dimensional (volume)
Flow
blood flow surements
Projec-
Med
1986;
Edelman RR, Mattte H, Kleefietd J, Silver MS. Quantification of blood flow with dynamic MR imaging and presaturation botus tracking. Radiology 1989; 171:551556. Mattle HP, Edelman RR, Reis MA, Atkin-
namics
Assist
Tomogr
H.
171:793-
21:56-65.
21.
Dixon
1989;
resonance
Imaging
1990;
sonog1986. et al. with
Radiology
tion of early ifiling veins by sequential subtraction. Neuroradiology 1975; 10:35-41. Axet L, Shimakawa A, MaeFallJ. A timeof-flight method of measuring flow velocity
EF,
948. Dumoulin CL, Hart HR. MR angiography. Radiology 1986; 161 :717-720. Laub GA, Kaiser WA. MR angiography with gradient motion rephasing. J Comput
batie
Evaluation
transeranial 1984; 60:
Rossman
Aaslid R, ed. Transeranial Doppler raphy. New York: Springer-Verlag, Wedeen VJ, Meuli RA, Edelman RR, Projective imaging of pulsatite flow
tion
Lindegaard KF, Bakke SJ, Aaslid R, Nornes H. Doppler diagnosis of intracranial artery occlusive disorders. J Neurol Neurosurg Psychiatr 1986; 49:510-518.
PA,
Torem 5, Ringelstein EB, Otis SM. Effect of internal carotid artery occlusion on intracranial hemodynamics: transeranial Doppler evaluation and clinical correlation. Stroke 1988; 19:589-593. Aaslid R, Markwalder TM, Nornes H. Noninvasive transeraniat Doppler ultrasound recording of flow velocity in basal cerebral arteries. J Neurosurg 1982; 57:769-
magnetic
References
2.
Schneider
14.
774. 7.
11. 1.
Lindegaard KF, Grolimund P, Aaslid R, Nornes H. Evaluation of AVM’s using transeranial Doppler ultrasound. J Neurosurg 1986; 65:335-344. Mattle H, Grolimund P. Huber P. Sturzenegger M, Zurbrugg HR. Transeranial Doppler sonographic findings in middle cerebral artery disease. Arch Neurol 1988; 45:289-295.
23.
Le Bihan
of perfusion.
D.
Magnetic
Magn
resonance
Reson
Med
imaging
1990;
14:
283-292.
November
1991
