PROGRESS IN CARDIOLOGY
Magnetic resonance measurement
of velocity
and flow: Technique, validation, and
cardiovascular
applkations
Sidney A. Rebergen, MD, Ernst E. van der Wall, MD, Joost Doornbos,
Albert de ROOS, MD Leiden, The Netherlands
In the early years of clinical cardiovascular
magnetic
resonance (MR) imaging, analysis of complex anatomy and cardiac masses were important indications
for performing
an MR study. Important
features of
MR imaging that have contributed
to its increasing
uses for the study of heart and vessels were the free
choice of image planes and the natural contrast between flowing blood and bordering tissues, enabling
clear depiction of cardiovascular
anatomy. Cardiac
MR now comprises gradient echo tine and ultrafast
techniques,
angiography,
flow imaging, myocardial
tagging, and spectroscopy,
enabling quantitative
analysis of congenital
heart disease,l ventricular
mass22 3 and volumes,4 valvular disease,5 ventricular
dysfunction6J
7 coronary artery anatomy,8 myocardial perfusion9 and infarctionlO
wall motion analysis *l-l3 and cardiac metabolism.i4
The extension of MR imaging to the analysis of
cardiovascular
function was greatly enhanced by the
introduction
of gradient echo sequences. Instead of
using radiofrequency
pulses to recall the MR signal
as in. spin echo, gradient echo MR uses a reversal of
the magnetic field gradient to rephase the spins. In
addition, gradient echo is characterized
by a short
echo time, a short repetition time, and a reduced flip
angle, enabling the reconstruction
of images that
represent
time frames of the cardiac cycle with a
small (20 to 30 msec) time interval. Cine loop display
From the Interuniversity
Cardiology Institute of the Netherlands,
Utrecht,
The Netherlands and the Departments
of Diagnostic Radiology and Cardiology, University
Hospital, Leiden.
Received for publication
April 9, 1993; accepted May 28,1993.
Reprint requests: Sidney A. Rebergen, MD, Department
of Diagnostic Radiology, University Hospital Leiden, Building 1, C2-S, Rijnsburgerweg
10,
2333 AA Leiden, The Netherlands.
AM HEART J 1993;126:1439-56.
Copyright Q 1993 by Mosby-Year
Book, Inc.
0002.8703/93/$1.00
+ .lO 4/l/49914
PhD, and
of these images facilitates
the study of cardiac
performance.
Moreover, gradient echo imaging uses
flow compensation
that normally warrants
high-signal intensity
in areas of flow. In regurgitant
or
stenotic valvular lesions, disturbed
flow will cause
loss of signal on gradient images, despite the use of
flow compensation.
This feature of MR can be used
for the detection and semiquantitative
estimation of
valvular heart disease.5p i5-lg
Even before the imaging aspects of MR were
introduced,
quantitative
flow measurement
by MR
was proposed by Singer. 2o Clinical application of MR
flow quantification
was not reported until several
years later. 21-26 Measurement
of blood flow is now
performed with a modified gradient echo sequence,
frequently referred to as MR velocity mapping or velocity-encoded
tine MR. Unlike conventional
(spin
echo or gradient echo) images that are reconstructed
from the amplitude of the signal that is emitted from
nuclei within the imaging section, velocity maps are
reconstructed
from the phase information
of the MR
signal.
Doppler echocardiography
is now regarded as the
noninvasive
technique
of choice for quantitative
analysis of flow dynamics. MR velocity mapping may
add important
information
to Doppler echocardiographic data because flow velocity is obtained twodimensionally
by MR, enabling the calculation
of
average velocity and volume flow. This is of special
importance
in the great vessels that often display
nonuniform
flow profiles.27-2g Several studies30F36
have reported on the accuracy of MR velocity mapping, and clinical uses are now increasingly explored.
This article discusses the principles of MR velocity
measurements
and reviews the’literature
on both
validation
and clinical application
of MR velocity
mapping.
1439
1440
Rebergen et al.
Amwicdh
December
1993
H&art Journal
Fig. 1. Intravascular magnetic spins that move along magnetic field gradient accumulate phase-shift that
is proportional to flow velocity. Spins in stationary tissue will not acquire phase change.
TECHNICAL ASPECTS
MR flow measurement
options. Generally
MR blood
flow quantitation
methods are either based on timeof-flight or phase-shift effects that are both wellknown phenomena in MR flow imaging.37-44 Although some studiesz2p 45-48have used time-of-flight
techniques for semiquantification
or measurement of
flow velocity, these methods do not provide two-dimensional velocity profiles, and the time-of-flight
approach has not been used as successfully as the
phase-shift technique. MR phase imaging was applied initially for qualitative purposes; for example,
the differentiation
between thrombus
and slow
flo~.~‘-~~ A quantitative
approach with encoding of
velocity in the phase of the MR signal was advocated
by Moran. 21 As soon as phase encoding sequences
that were suitable for routine use,23-26 became available, many clinical applications
emerged.55-58 The
principles of MR phase-encoding of velocity will be
discussed here.
Principles of MR phase-shift velocity mapping. Magnetic spins of intravascular protons that flow along a
magnetic field gradient acquire a phase-shift that is
proportional to flow velocity (Fig. 1). When the phase
is measured velocity can be derived.23p 24,26 Measurement of the phase of the MR signal requires a certain
signal amplitude.
Gradient echo MR imaging provides -the obligatory high-signal intensity from regions of flow and has served as a basis for the development of a number of MR phase-shift velocity
mapping
sequences by different manufacturers.
These sequences carry acronyms like VEC (velocity
encoded tine), FEER (field even echo rephasing) or
FLAG (flow-adjusted gradient). These techniques
will be further explained by using the FLAG sequence developed by Groen et al.5g and Van Dijk et
al.60 as an example.
First of all, flow compensation (also known as gradient moment nulling or even echo rephasing) is essential for velocity mapping because it ensures the
preservation of signal amplitude from regions of flow
(Fig. 2, A). In addition, the gradient waveform is
slightly modified to induce a phase shift in spins that
move (or flow) along this gradient.23> 24r26 This velocity-encoding gradient will verify that a certain flow
velocity is represented by a proportionally
corresponding phase shift. For the purpose of measuring
volume flow, the direction of velocity-encoding
must
be set perpendicular
to the imaging section. Alignment of the direction of flow and the direction of velocity encoding is achieved by orienting the imaging
section perpendicular
to the vessel of interest with
the use of oblique magnetic field gradients. In-plane
flow encoding has been used mainly to measure peak
flow velocity,35> 61-63 and the reliability
of in-plane
velocity measurements depends on several critical
imaging parameters.s2> 64
The maximum phase shift range of -180 degrees to
f180 degrees is tailored to a window of expected
maximum velocities by slightly modifying the wave-
Volume 126, Number 6
American
Heart Journal
Rebergen et al.
1441
Fig. 2. A, Gradient-echo MR imagein transverseplane perpendicular to aorta at level of right pulmonary
artery. High signalamplitude is preservedin great vessels,enablingreconstruction of phaseimage. B, Phase
imagecorrespondingto A beforesubstraction showsphaseshifts establishedby flow but with artificial phase
changessuperimposed.C, Mask image correspondingto A, reflecting differentation between noise (dark
grey), stationary tissue (midgrey) and areasof flow (light grey) basedon their relative signal amplitude
as obtained from A. Zero offset can be corrected for after detection in stationary tissue. D, Velocity map
correspondingto A, after subtraction and correction of zero offset. Midgrey pixel intensity in stationary
tissue (thoracic wall) indicates zero velocity, high-pixel intensity in ascendingaorta, and low-pixel intensity in descendingaorta-superior caval vein reflects flow into and out of imagingsection,respectively. Noise
generated by low signal is seenas chaotic patterns in lungs and outside subject.
form of the velocity-encoding gradient. For example,
when the maximum phase shift is set to occur with a
velocity of 300 cm/set, zero velocity will cause a phase
shift of 0 degrees and 150 cm/set will result in a 90degree phase shift. Negative velocity values (flow in
the opposite direction) will be represented by corresponding negative phase values.
On a phase image (Fig. 2, B), the gray value of a
pixel (image element) represents the phase of the
magnetization of the corresponding voxel (tissue
volume element); theoretically the phase in static
tissue voxels should be zero. However, factors other
than flow (such as inhomogeneities of the magnetic
field) may cause additional phase shifts that will
cause erroneous interpretation of the local velocity.
In the FLAG sequence, a velocity-compensating gradient and a velocity-encoding gradient are applied
interleaved in successive cardiac cycles, and the
phase errors are eliminated by subtracting the phase
images acquired with the velocity-compensated gradient from the corresponding velocity-encoded phase
images. The resulting net phase shift is determined
only by flow.
Finally, to obtain an accurate two-dimensional
display of velocity across the imaging plane, it may be
necessary to perform additional correction of zerophase offset as detected in stationary tissue (Fig. 2,
C and D). Alternatively, under the assumption of an
interval of zero flow in the vessel of interest, zero offset can also be removed by measuring the phase error on an image representing this zero flow period and
then subtracting the detected phase-error from the
subsequent images.31,32It must be realized that MR
velocity mapping does not measure flow velocities in
relation to the vessel wall but measures velocity with
respect to the image plane. However, in the major
vesselswall motion is very slow compared with blood
flow velocity and may be neglected.33
December
1442
Rebergenet al.
American
Heart
1993
Journal
Fig. 3. A, Midsystolic velocity map, correspondingto Fig. 2 after applying threshold to remove noisepixels. B, Diastolic velocity map of image set of Fig. 2 showinglittle flow in great arteries but distinct flow in
superior caval vein. C, Irregular region of interests (IROI) of ascendingand descendingaorta and superior
caval vein are defined on (zoomed)amplitude imageto be subsequentlyprojected on correspondingvelocity map (B, D). Tracing IROI on velocity map directly may be difficult on diastolic imageswith low velocities. D, Diastolic velocity map with IROIs superimposed.
To display the variations in flow during the cardiac
cycle, a set (usually between 16 and 30) of velocity
maps is collected (Fig. 3, A and B). Data acquisition
is initiated by the R wave of the electrocardiogram
(ECG) and performed with high temporal resolution
enabled by the gradient echo character of the FLAG
sequence. It must be emphasized that each image is
built up over several hundred (typically 256) cardiac
cycles, The resultant image set represents an average
cardiac cycle during the imaging interval. Quantitative data on flow velocity and flow volume are
obtained, from the velocity maps through an irregular region of interest (IROI) function. An IROI is
manually traced along the margin of a vessel of
interest either directly on the velocity map or preferably65 on the co&esponding modulus image (Fig. 3,
C) with subsequent projection pn the velocity map
(Fig. 3,-O). Whenever necessary the IROI is adjusted
for movement and changes in diameter of the vessel
during the cardiac cycle. A computer routine converts
the average and the peak phase values within each
IROI to average and peak velocity values that can be
plotted against time. Instantaneous volume flow is
computed from the product of average flow velocity
and IROI area. Time integration over the R-R interval (area-under-curve) of these instantaneous volume data yields the stroke flow volume, the volume
of blood passing the IROI in one cardiac cycle (Fig.
4).
Technical limitations and potential sources of error. In
MR sequences that are now routinely used for
cardiovascular imaging, data collection is triggered
by the R wave of the ECG. Therefore studies of patients with arrhythmias are troublesome. It is also
important that most imaging systems require a certain time (e.g., 150 msec) before the next R wave
during which interval data cannot be acquired; this
implies that atria1 contraction cannot be sampled.
Because the “atrial kick” can be an important deter.minant of flow dynamics in certain vessels,28simple
extrapolation of data66 may not always be appropriate. Extending data acquisition over the next cardiac
cycle6iJ 67is another strategy, but this will double the
imaging time. Moreover, beat-to-beat variations may
introduce errors in end-diastolic flow quantitation
Retrospective gating allows raw data to be acquired asynchronously to the cardiac cycle. Simultaneously, every R-R interval length is monitored and
Volume 126, Number 6
American
Heart Journal
Rebergen et al.
1443
per second) plotted against time (milliseconds)
after R wave of ECG. InFig. 4. Volume flow (milliliters
stantaneous flow volumes measured from each velocity map are summed to give stroke flow of each vessel.
ASC AO, Ascending aorta; DESC AO, descending aorta; SVC, superior caval vein.
120
100
3 *O
!Eg 6o
E
40
20
0
0
20
40
60
80
time of the cardiac cycle (%)
Fig. 5. Volume flow (milliliters
per second) in pulmonary
connection. Atria1 contraction may contribute
considerably
Data were acquired with retrospective
gating.
stored@ 6g and image reconstruction is performed
after reordering the raw data according to the ECG
information. Compared to conventional triggering
techniques, imaging time is increased only a ‘few
minutes and atria1 influences on flow dynamics can be
readily appreciated57 (Fig. 5). This technique requires high quality of the ECG signal; otherwise,
prominent T waves or noise spikes may be falsely interpreted as R waves, causing errors in the process of
reordering.
artery in patient with atriopulmonary
Fontan
to forward flow as is illustrated
in this graph.
Clearly, most currently used MR velocity mapping
sequencesdo not provide real-time information, and
instantaneous respiratory or beat-to-beat variations
in flow remain unrevealed. However, the effects of
respiration on systemic venous return appear to be of
minor importance as demonstrated by Mohiaddin et
a1.,28who used combined cardiac and respiratory
gating. Furthermore, because of prolonged imaging
times, respiratory gating is not routinely used.
An important pitfall of MR flow quantitation is the
1444
Rabergen et al.
loss of signal amplitude that, occurs when the ,degaee
of acceleration and other higher orders of motion
preclude recovery of coherent signal, even when using the dedicated flow-compensating
gradient echo
sequences. Under these circumstances, a range of
different velocities may be present within one voxel
and the corresponding phase shifts will cancel out.
Voxel size and echo time are therefore important parameters in the relation between velocity and phase
shift.70 To obtain maximum
signal, the echo time
chosen is as short as possible within the limitations
of the imaging system, mostly between 7 and 15 msec,
but MR imaging systems with shorter echo times are
becoming commercially
available. Shortening
the
echo time reduces the interval during which velocity
fluctuations of turbulent flow proceed, #Initially, relatively long echo times up to 27 rnsec? 55p71 have
been used, and signal loss was frequently observed
even when studying the ascending aorta of normal
volunteers.35 The length of echo time may also be of
particular importance
in infants and children because greater velocities and stronger acceleration occur in the great vessels of pediatric patients.29 Kilner
et a1.62 demonstrated that a very short echo time (3
to 4 msec) is required to recover signal from very fast
or turbulent flow, as in severe aortic stenosis. However, the Kilner et al. experiments were performed
with an imaging system operating at a magnetic field
strength of 0.5 T, and it was shown58 that such a very
short echo time is not an absolute requirement
to
measure velocities over 5 m/see when a 1.5 T system
is used (Fig. 6, A and B).
Aliasing or phase-wrap occurs when velocities exceed the anticipated
range, causing a phase shift
greater than 180 degrees that cannot be differentiated from a negative phase shift, indicating velocity
in the opposite direction. 64*72Aliasing can sometimes
be corrected retrospectively by shifting the velocity
window.32> 73 In addition, flow quantification
in the
aorta was shown to be less subject to error when the
lower velocities that occur in the diastolic phase of
the cardiac cycle are anticipated
by subsequently
applying different velocity encoding windows during
systole and diastole. 65 Other potential sources of error, well described by other authors,621 64 are listed in
brief: edge spikes (artificially large phase shifts, resulting from partial signal loss near the vessel wall
that may cause overestimation of peak velocity if not
recognized) may be of particular importance if peak
velocities are to be used for estimating pressure drop
across a stenosis by using the Bernoulli formula; partial volume averaging, (particularly
when imaging
small vessels nonperpendicularly)
image section ele-
American
December
1993
Heart Journal
ments (voxels) may contain both flowing and stationary spins, and velocity will be underestimated.
Mitalignment
of veloc$ty encoding, where velocity
is underestimated
when the direction of velocity encoding does not coincide with the direction of true
flow. To a certain extent overestimation
of cross-sectional area will cancel out the underestimation
of velocity in volume flow calculations. Furthermore, true
velocity and measured velocity are interrelated
by
the cosine value of, the’angle % between the direction
of velocity encoding and true flow:, Vme%ured =
Vtrue x cos +. This cosine relation implicates small
errors at low angles, and several authors34F % 74 have
successfully used this formula to correct misalignment. However, at high angles of obliquity, partial
volume effects. become increasingly important
and
cos 9 correction is insufficient.
Spatial
misregistration,
where, as a result of
in-plane movement in the time-interval
signal excitation and signal detection, flow signal may be misplaced and overlay stationary tissue, thus introducing partial volume. This can be minimized by imaging perpendicularly
to the direction of flow.
VALIDATION OF MR FLOW QUANTITATION
TECHNIQUES
In vitro validation. Phantom experiments
with both
continuous and pulsatile flow have shown close correspondence between MR-measured
flow and true
flow.* Some of these studies included the use of
stenotic phantoms to simulate severe valvular stenosis62 by establishing flow velocities of up to 6 m/set
and to assess the accuracy of MR velocity mapping in
complex flo~.~O
Doppler echocardiography.
Experiments that compared MR velocity mapping with Doppler echocardiography for the measurement of flow velocity and
flow rate in the great vessels have shown corresponding results with both techniques.? In 18 patients with
a stenotic ventriculopulmonary
conduit or stenosis of
the mitral or the aortic valve, Kilner et a1.62 found
good correlation between results of MR and Doppler.
Although Doppler echocardiography
is regarded an
established technique for the measurement of flow
velocity, its role as a refererme standard can be questioned.7g Nevertheless, these comparative
studies
provide a validation for the MR velocity mapping
technique.
MR ventricular volume studies and interna’l standards.
The ability
to measure ventricular
*31,
34, 36, 58, 62, 66, 70, 71
t31,
32, 34, 35,67,
75-78
volumes
accu-
Volume 126, Number 6
American
Heart Journal
Rebergen et al.
1445
6. A, Oblique transversegradient echoimageperpendicular to main pulmonary artery in patient with
supravalvular pulmonary stenosis.This imagewasacquired with 1.5 T systemand echotime of 8 msec;signal is preserved in central area of high flow velocity. B, Midsystolic velocity map correspondingto A with
high signalintensity only in central area of pulmonary artery representing peak flow velocity of 5 meters
per second.Dark pixels, typical edgespike artifacts.
Fig.
rately from a set of contiguous MR images was demonstrated by Longmore et aLgo in 1985. Their findings have been confirmed by others, who mostly used
gradient echo MR imaging.4T81-87Using this MR appreach, Firmin et a1.30measured ventricular stroke
volumes to validate MR velocity mapping measure-
ments of aortic stroke flow volume in 10 volunteers.
Since then similar in vivo validation studies have
been performed by other investigators who used
either ventricular
stroke volumes33y34z67p88 or
flow through related vessels as internal standmds
33-35,67,89
1446
Rebergen et al.
American
Invasive studies. Mgigelvang et a1,88derived cardiac
output data from MR stroke flow measurements in
the ascending aorta df seven voluntee& and showed
overall good agreement with the results from indicator dilution measurements. Kilner et al.@ applied the
Berndulli formula to peak flow velocities measured
by MI$ and found pressure gradients that were fairly
similar to those measured at catheterization
in eight
patients with a stenotic valve or residual stenosis
across a ventriculopulmonary
conduit.
These investigatiqns,
in which various independent approaches’were used, demonstrate the reliability and &curacy of MR flow quantitation
and enable
the application in several clinical fields.
CLINtCAL APPLtCATtONS
Pioneering efforts regarding clinical application of
MR velocity mapping were’made by ‘Underwood et
a1.55 in 1987; they proposed a wide range Gf cardiovascular uses for this technique, ideluding congenital
heart disease, coronary artery bypass graft patency,
valvular stenosis, valvular regurgitation,
and peripheral vascular thrombosis. Since then a great number
of technical and clinical papel”s canie from their institution and from several other research groups that
will be reviewed here. Studies that included MR velocity mapping in patients are listed in Table I.
Ascending aorta and coronary
Aortic flow profile. Klipstein
flow
et aLso used MR velocity mapping to study flow velocity profiles in the
ascending aorta in 10 volunteers. They described a
slightly skewed systolic plug flbw pattern, an observation that has been confirmed by other investigatom.327 35, 71 The highest antegrade flow velocities in
systole and a diastolic retrograde flow channel both
occurred in the left posterior region of the ascending
aorta.g0 In another study of 24 yolunteers, Bogren et
a1.33confirmed the existence of end-systolic to diastolic reversed aortic flow that, was directed mainly
toward the left coronary sinus. Bogren et al. presumed this phenomenon to pIay a role in coronary
perfusion and supported their theory by emphasizing
that coronary artery flow occurs predominantly
in
early diastole, during which interval the aortic valve
is closed, implying that coronary flow must be supplied from the ascending aorta.33 The same groupgl
also demonstrated diminished aortic compliance together with reduced retrograde flow in nine patients
with’ coronary’ artery disease when compared with
normal subjects. The patients also showed relatively
less retrograde flow over the left and right coronary
sinus; flow toward the noncoronary sinus had increased. Thus the abnormal aortic flow pattern may
December 1993
Heart Journal
be related to decreased. coronary perfusion. Changes
in compliance, lo&plaques,
and abnormal wave reflection may all contribute to decreased reverse Aow.
These findings agree with the theory that atherosclerosis starts in the aorta and spreads to, among other
vessels, the coronary arteries; it appears that in patients with ischemic heart disease, left ventricular
function is compromised both by decreased myocardial perfusion and reduced aortic compliance.g1 MR
velocity mapping can also be used for monitoring
aortic wall elasticity by measuring the aortic flow
wave veLocity.g2
Aortic sten,osis and aortic regurgitation.
Kilner et
a1.62already demonstrated that flow velocities of >5
m/s, which occur in severe aortic stenosis, can be
measured by MR velocity mapping. Recently, Engels
et a1.77were also successful in applying velocity mapping to a group of patients with aortic stenosis, and
they stress the advantages of MR over Doppler echocardiography
in asymmetric stenosis or complex
flow patterns. Before MR flow quantitation
techniques were introduced, valvular stenosis and regurgitation could be assessed semiquantitatively
by MR
through the size of the signal void on gradient echo
MR images.5J 15-lgy93 Regurgitation
volumes can be
derived from ventricular stroke volume differences
measured on multisection
gradient echo images,g4
but this approach is rather time consuming because
these volume ,studies require extensive manual contour tracing. Dulce et al. g5 showed high interstudy
reproducibility
and high interobserver reproducibility of MR velocity mapping in’ 10 patients with
chronic aortic regurgitation. Dulce et al. found closely
corresponding results when they compared regurgitant flow volume with the difference between left
and right ventricular stroke volumes measured from
a contiguous set of MR images; they advocate the use
of MR velocity mapping for timing of valve replacement and .for drug therapy monitoring.g5
Recently
Honda et a1.78 have also reported low interobserver and intraobserver variation of measurements
of
aortic regurgitation
by MR velocity mapping in 26
patients
and in five healthy
volunteers,
and
the velocity mapping results agreed well with Doppler echocardiographic
and aortographic
gradings
of aortic regurgitation. I8 Eichenberger
and Von
Schulthessg! used MR velocity mapping of aortic flow
in combination
with blood pressure data to reconstruct left ventricular pressure-volume loops in patients with aortic stenosis and aortic regurgitation.
They were able to demonstrate
increased cardiac
work in all patients compared to normals.
Coronary
circulation.
MR velocity mapping of
Volume 126, Number 6
American
Heart Journal
Table
1. Clinical
Rebergen
application
Author
et al.
et al. 198gg1
Rees et al. 198956
Bogren
et al. 198gz7
Mohiaddin
199028
Kilner
et al.
et al. 199162
Mohiaddin
19919s
et al.
Mohiaddin
199161
et al.
Kondo
6 Patients
with
3 Patients
with
X
8 Patients
with
shunt lesions
26 Volunteers
4 Patients
with
CAD
syndrome
AA
congenital
AA,
MPA,
LPA,
MPA
9 Volunteers
9 Patients
after
SLT
MPA, LPA,
RPA
10 Volunteers
5 Patients
with
MS
MV,
AI
AA
Brenner
et al.
1992107
11 Patients
with
ASD
MPAIAA
Engels
15 Patients
with
AS
AA
Rebergen
199367
et al.
et al.
Honda et al.
199378
AA, Ascending
myopathy;
HT,
7 Volunteers
6 Patients
(CMP,
aorta; AI, aortic ins&ciency;
hypertension;
WC, inferior
PC, pericardiel
constriction;
tricular
dysplasia;
RVSV,
PH, pulmonary
right ventricular
MPA,
AI
-
Doppler:
good
agreement
AA: r = 0.97
LVSV-RVSV:
r = 0.97
Interstudy:
r = 0.97
RVSVjLVSV:r
= 0.94
Oximetry:
r = 0.91
Interobserver:
r = 0.94
Doppler:
r = 0.91
AA
LPA,
r = 0.99
good agreement
fair agreement
-
PV
HT)
AA
with
Phantom:
Doppler:
Catheter:
MPA
17 Volunteers
14 Fontan
patients
5 Volunteers
26 Patients
IVC
Multiple
with
Magelvang
199288
= 0.93
-
svc,
10 Patients
et al. 199277
LVSV:r
13 Volunteers
13 Patients
with TI, PH,
PC
and RVD
36 Patients
with stenotic
valves, conduits,
etc.
PH
et al. 1992g5
RPA
PH
10 Volunteers
10 Patients
with
Dulce
et al. 199276
Topic
Validation
Multiple
13 Patients
1447
mapping
Application
Subjects
Underwood
198755
Bogren
of MR velocity
et al.
RPA,
AA
Indicator
dilution:
r = 0.96
LVSWr
= 0.95
RVSV:r
= 0.98
Phantom:
r = 0.99
LPA
+ RPA
0.90
RVSV
(MPA):
LVSV
(AA):
Clinical
application
in septal
defect, valvular
disease,
CABG, etc.
Reduced
reverse aortic flow
towards
coronary
sinuses in
patients
Noninvasive
measurement
of
unequal
levels of pulmonary
and systemic flow
Mostly
antegrade
plug flow in
volunteers;
irregular
antegrade
and retrograde
flow
and increased
retrograde
flow
in patients
Biphasic
caval flow in controls;
total caval flow independent
of respiration;
disturbance
of
biphasic
pattern
in patients
High signal from flow across
stenosis using very short TE;
application
at sites with
limited
access for
echocardiography
Similar
flow to both lungs in
volunteers
and a 3:l perfusion
ratio (transplanted
vs native
lung) in patients
Biphasic
flow pattern
through
MV and in PV of volunteers;
semicontinuous
MV flow in
patients
with MS
Retrograde
flow proportional
to
pulmonary
vascular
resistance
in patients
Validation
Validation
Validation
Application
in aortic
with complex
flow
Validation
Validation
Pulmonary
Fontan
(MPA):
stenosis
patterns
flow profiles
surgery
after
0.97
0.96
Doppler:
good
agreement
Interobserver:
r = 0.96
Validation
ASD, atria1 septal defect;
C&G,
coronary
artery
bypass graft; CAD, coronary
artery
disease; CMP, cardiovena cava; LPA, left pulmonary
artery;
MPA, main pulmonary
artery;
MV, mitral valve; MS, mitral
stenosis;
hypertension;
stroke
volume;
PV, pulmonary
vein; SVC,
SLT, single lung transplant;
superior
caval
TI, tricuspid
vein; RPA,
insufhciency.
right
pulmonary
artery;
RVD,
right
ven-
1448
Rebergenet al.
American
December
1993
Heart J&mill
Fig. 7. A, Transverse spin echo image of aortic root of patient with coronary artery to pulmonary artery
fistula. Enlargement of left coronary artery is evident (From Rebergen SA et al. Cardiovasc Imaging
1992;4:175-81.)B, Volume flow curve obtained from velocity mapsperpendicular to origin of left coronary
artery in A. Typical biphasic pattern with predominant peak in diastole is seen.Size of left-to-right shunt
is indicated by stroke flow. (From Rebergen SA et al. Cardiovasc Imaging 1992;4:175-81.)
coronary artery flow is complicated by the vessels’
tortuosity, small size, motion, and the complex flow
patterns and acceleration phenomena in stenotic arteries. Occasionally flow has been measure,d directly
in a coronary artery to pulmonary artery fistula56
(Fig. 7, A and B) and in coronary artery bypass
grafts.55 Van Rossum et al .@ studied 24 healthy volunteers with MR velocity mapping by measuring flow
in the coronary venous sinus that has a relatively
large diameter with less turbulent flow -and’that receives approximately 96 % of left ventricular perfusion. They confirmed previous invasive studies by
demonstrating a biphasic coronary sinus flow pattern
with peaks in systole and in early d&stole t&t are
synchronous with the X and Y descent of the right
atrial pressure curve. The maximum flow velocity
occurred in diastole and significant systolic variations in sinus diameter suggested a capacitance
function forvenous outflow. Despite the complexity
of direct coronary artery flow measurements by MR,
Edelman and Lig7 were recently able to report significant progress in this field by using breath-held turbo
tine MR sequences in healthy volunteers. With an
echo planar technique, Poncelet et alg8 demonstrated coronary flow velocity changes that were related to exercise. However, further technical improvements are required to make coronary artery
flow quantification by MR ‘a clinical .option.
Volume 126, Number 6
American
Heart Journal
Rebergen et al.
250
time after R-wave
1449
500
(ms)
Fig. 8. Volume flow in main pulmonary artery in patient with pulmonary hypertension. Typical flow curve
with midsystolic dip of net forward flow shows and simultaneous systolic retrograde flow.
Pulmonary arteries
Separate assessment of left and right pulmonary
artery flow. MR velocity mapping allows noninvasive
measurement of blood flow to each lung separately.
This information can be of great value in a wide range
of pulmonary (acute pneumonia, embolism, asthma,
mucous plugs, radiation therapy, scoliosis, SwyerJames syndrome, al-antitrypsin
deficiency, and cystic fibrosis) or cardiac disease (pulmonary
artery
stenosis, intracardiac shunts, and after surgical procedures like pulmonary artery banding and palliative
shunts) especially because currently available radionuclide techniques have their limitations.74
Both Caputo et a1.74 and Rebergen et a1.67 have
performed measurements of separate left and right
pulmonary artery flow in nine healthy volunteers and
demonstrated the right-to-left
predominance of pulmonary perfusion that was already known from radionuclide studies and that is compatible
with the
greater volume of the right lung. Mohiaddin
et algg
measured left and right pulmonary artery flow in nine
patients after a single lung transplant. These patients
have blood ejected into separate vascular beds with
different resistance and flow dynamics, which may be
important in adaptation. Compared to nine healthy
volunteers in whom flow to both lungs was similar,
flow to the transplanted
lung in the patients was
three times that of the native lung. Flow to the
transplanted
lung was also continuously
forward
during entire systole and during most of diastole
while; flow to the native lung was characterized by a
narrow early systolic peak of forward flow (suggesting markedly decreased pulmonary artery compliance) and by reversed flow in late systole and most of
diastole. These phenomena were previously reported
from radionuclide
studies and can be explained by
the difference in vascular resistance between the
transplanted and the native lungs. Fortunately, reduced physiologic shunting and enhanced gas exchange are important consequencesgg
Pulmonary artery flow profile and changes that occur
in pulmonary hypertension. Bogren et a1.27foundmostly
antegrade plug flow skewed toward the posterior in
the pulmonary
artery of 26 normal volunteers. A
small amount of end-systolic to early diastolic retrograde flow is presumed to assist in pulmonic valve
closure. A subsequent small second peak of forward
flo~~~ is induced by diastolic recoil of the pulmonary
arteries that have been distended in systole. Patients
with pulmonary hypertension show two peaks of systolic forward flow (reflecting midsystolic semiclosure
of the ,pulmonic valve) in combination with extensive
and rapid retrograde flow, that occurs already in systole and continues in diastole (Fig. 8). In pulmonary
hypertension the vessel wall is stretched more from
its original length, distensibility
is reduced, and peak
flow velocity is reached much earlier, as shown with
MR.27 But forward flow is overall slower, which
explains the relatively high intravascular signal intensity on spin echo images of the pulmonary arteries in these patients. Bogren et al. propose a role for
MR in the clinical assessment of pulmonary hypertension, especially because the complexity
of the
pulm’onary artery flow pattern implicates that Doppler results in these patients strongly depend on the
position of the sample volume.27
Findings similar to those of Bogren were reported
by Kondo et al., 76 who compared 10 patients with
1450
Bebergenet al.
pulmonary hypertension with 10 healthy volunteers.
Kondo et al. demonstrated that retrograde flow was
inversely proportional
to flow volume and directly
proportional
to vascular resistance and cross-sectional area, stressing the hemodynamical
significance
of these findings. Kondo et al. suggested that retrograde flow in pulmonary hypertension may be caused
by augmented reflection of pulse wave with increased
vascular resistance, decreased capacitance of the arterial system, and eddy flow in dilated arteries. Clinically it is important that retrograde flow may compromise right ventricular ejection; Kondo et al. propose the use of MR velocity mapping to assess
pulmonary vascular resistance in patients with pulmonary hypertension.16
Intracardiac
flow
venous flow. Mitral and
pulmonary venous flow are regarded as important
indexes in the evaluation of left ventricular diastolic
function and mitral valve disease. Mohiaddin
et a16i
demonstrated
a biphasic mitral flow pattern in 10
normal volunteers, with an initial peak reflecting
passive filling in early ventricular diastole and a second peak during atria1 contraction. In five patients
with mitral stenosis, mitral flow persisted throughout
diastole with increased velocity. In normals, peaks of
pulmonary venous flow occurred in ventricular systole and diastole with small backflow during atria1
contraction. The propulsive force behind pulmonary
venous flow remains controversial.61
Galjee et al.ioo recently confirmed the biphasic
pulmonary venous flow pattern and extended their
experience to 13 patients with mitral regurgitation, in
whom they were able to demonstrate an inverse relationship between end-systolic pulmonary venous
flow and end-systolic pulmonary
capillary wedge
pressure. Furthermore,
they showed that with increasing mitral regurgitation end-systolic pulmonary
venous flow declined and finally reversed. Karwatowski et al.iol compared MR velocity mapping and
Doppler echocardiography
for the measurement of
transmitral
flow velocities in 13 patients and found
good agreement for early filling veIocities but an underestimation
by MR of Doppler velocities during
atria1 contraction.
Caval and tricuspid fIow. Mohiaddin
et alz8 used
MR velocity mapping to measure flow in the caval
veins of 13 controls and 13 patients with right-sided
heart disease. The controls showed systolic and diastolic peaks of caval flow, but patients with tricuspid
incompetence demonstrated a reduced systolic peak
and occasional retrograde flow in the inferior vena
cava. Reduced right ventricular diastolic compliance
in patients with pulmonary hypertension, pericardial
Mitral
and pulmonary
American
December
1993
Heart Journal
constriction, and right ventricular dysplasia was reflected by flattening of the diastolic peak. Additional
respiratory gating in six control subjects showed reduced systolic inferior vena cava peaks at end expiration, but total caval flow was unchanged; the
authors suggest that the heart may act partly as
pressure suction pump, independent of respiration.28
Van Rossum et a1.35 also found a biphasic flow pattern that corresponded with the atrial pressure curve
in both superior and inferior vena cava of 17 healthy
volunteers. Mostbeck et a1.63 compared MR velocity
mapping (performed both in the horizontal and vertical long-axis planes) with Doppler ultrasound for
the measurement of early and late diastolic tricuspid
flow velocities in 10 healthy volunteers and found
similar early to late velocity ratios with both techniques. However, velocities measured by Doppler
were underestimated
by MR; the authors provide
several explanations
for this discrepancy, such as
different measurement positions and different temporal resolution.63
Intraventricular
flow patterns and cardiac wall
motion analysis. Recently, some groups have applied
velocity-encoding
MR techniques to the analysis of
ventricular
wall motion and intraventricular
flow
patterns. Eichenberger et allo were able to demonstrate normokinetic
left ventricular wall motion in
five healthy volunteers and dyskinetic regions in four
patients with coronary artery disease. Karwatowski
et aLlo lo4 studied 19 patients with ischemic heart
disease and found that Doppler-assessed early diastolic mitral flow velocity and deceleration correlated
with MR-measured
early diastolic left ventricular
wall velocities along the long axis of the heart. Segmental wall motion analysis enabled the detection of
inhomogeneous
and reduced wall motion in these
patients. Walker et a1.1°5 introduced a new application for MR velocity encoding by demonstrating
the
feasibility of reconstructing vector plot images of intraventricular
flow patterns in a healthy volunteer.
McKinnon and Von Schulthessio6 provided an alternative for myocardial tagging techniques by using
velocity encoding of the heart wahfor the measurement of strain in the normal heart.
Congenital
heart disease. Rees et a1.56 emphasized
the combination
of anatomic images with flow measurements as an important advantage of MR imaging
in patients with congenital heart disease. Cardiac
catheterization,
frequently performed for the assessment of systemic to pulmonary flow ratios, is invasive; flow measurements
are not entirely accurate.
Therefore Rees et al. proposed MR velocity mapping
for the direct measurement of aortic and pulmonary
flow in seven patients with various congenital shunt
Volume
American
126, Number
Heart
6
Journal
lesions like atrial and ventricular
septal defects, persistent ductus arteriosus,
truncus
arteriosus,
and
coronary to pulmonary
artery fistula.56
The suitability
of MR velocity mapping for the
quantification
of atrial-level left-to-right
shunts was
later demonstrated
by Brenner et a1.,io7 who measured aortic and pulmonary stroke flow in 11 patients
with atria1 septal defect. MR velocity mapping of
shunt size correlated well with oximetry and with MR
ventricular
volumetry and showed low interobserver
variability.
The authors
stress the invasive and
unreliable character
of oximetry
and the lack of
techniques that are ideally suited for the assessment
of shunt size.lo7 Sieverding
et al.2g also used MR
velocity mapping to measure stroke flow volumes in
the great arteries and showed close agreement with
MR-determined
ventricular
stroke volumes in six
patients with congenital heart disease. Systemic to
pulmonary flow ratios measured with MR were confirmed by catheterization
studies.2g
Functional
evaluation of postoperative
flow dynamics in patients after surgery for congenital heart
disease, especially adults, may be compromised
by
limited acoustic windows that fail to visualize posterior structures
within the thoracic cavity. Results
may also be unsatisfactory
as a result of the presence
of sutures, scar tissue, and bon.y deformations;
the
success of echocardiographic
examination
in these
cases is strongly operator-dependent.
Rebergen et
a1.67 used MR velocity mapping to measure flow to
each lung separately in a group of 14 postoperative
Fontan procedure patients. They showed that the
surgical incorporation
of the hypoplastic
right ventricle to support pulmonary
perfusion may result in
the establishment
of the desired arterial pulmonary
flow pattern in some patients. Furthermore,
it appeared from their experiments
that Doppler echocardiography,
measuring flow velocity but not volume flow, may not always be sufficient to judge the
success of right ventricular
incorporation.
In another
study, Rebergen et ‘al.los quantified pulmonary
regurgitation volumes in patients after repair of tetralogy of Fallot. Regurgitant volume flow measured with
MR velocity mapping was shown to be similar to the
regurgitation
volume calculated from the difference
between left and right ventricular
stroke volume.
Thus accurate regurgitation
volume measurements
by MR may be of assistance in revealing the true
clinical relevance of postoperative
pulmonary regurgitation. Obviously,
there are many other applications in postoperative
congenital heart disease, such
as evaluation of coarctation
surgery and residual
shunt lesions57 or residual stenosis across ventriculopulmonary
conduits.62
Rebergen et al.
1451
Descending aorta and abdominal arteries
Descelzding aorta. Both Maier et a1.32 and St&lberg et al.71 have studied the velocity profile in the
descending aorta and demonstrated
mild retrograde
flow in early diastole. A recent study of 10 healthy
volunteers by Amanuma et allog described flow measurements in the abdominal aorta at three axial levels and in the superior mesenteric
artery simultaneously. From these data, flow to the coeliac and
renal arteries that branch from between the measurements positions could be derived. Furthermore,
they demonstrated
that diastolic reverse flow in the
aorta proximal to the renal artery was less than at the
level below the renal arteries. Reverse flow below the
renal arteries may be caused by high peripheral vascular resistance in the legs and is important in maintaining renal perfusion during diastole.iog
Pelt et al.li” quantified flow through the portal
vein, renal veins, renal arteries, and common iliac arteries in eight dogs and showed close correspondence
of the MR results with electromagnetic
flow ,meter
measurements
in all vessels. They proposed the use
of MR flow quantitation
techniques for the measurement of volume flow and for the application in vessels where other techniques
have limited access.
Sommer et al.lli attempted to measure renal arterial
and venous blood flow directly
in nine healthy
volunteers and used a clearance technique as a reference standard.
MR measurements
of venous flow
were reproducible
and correlated with clearance results. However, arterial measurements
did not correlate ,with the standard, and several sources of error
are to be eliminated before this application
can be
used in clinical routine. However, Lundin et a1.8grecently measured blood flow in the renal arteries
directly by-MR velocity mapping in 14 healthy volunteers; they found good correlation with the difference between infrarenal and suprarenal aortic blood
flow and with the expected renal blood flow based on
a clearance method.
Asrtic
dissection
and the detection of thrombi.
Recently MR imaging was reported to be similar in
sensitivity
but superior in specificity
compared to
transesophageal
echocardiography
for the evaluation
of suspected aortic dissection.l12 Velocity mapping
may further increase the diagnostic value of MR in
patients with aortic dissection35> l13-i15 by demonstrating differential flow phenomena in the true and
false lumen, which may help to detect the entry jet
and to distinguish slow flow from thrombus. The additional ability of MR to quantify aortic regurgitation may obviate the need for invasive studies.i14
Peripheral
arteries. The presence of a triphasic
flow pattern in the peripheral
arteries was already
1452
Rebergenet al.
known from Doppler studies, and pulsatility may be
reduced or absent in obstructed vessels. Stahlberg et
aL71 confirmed the occurrence of pronounced backflow in popliteal artery by using MR velocity mapping. Caputo et a1.75 used MR velocity mapping to
demonstrate triphasic velocity waveform profiles in
the popliteal and tibioperoneal
arteries of 10 healthy
volunteers. They propose velocity mapping to be
used with MR angiography to warrant more accurate
evaluation of a stenotic lesion.
Cerebrospinal fluid flaw. Stahlberg et aL71 demonstrated significant and pulsatile cerebrospinal fluid
flow by MR velocity mapping with good reproducibility. Others have proposed clinical application of
MR flow techniques to quantify flow through cerebraspinal fluid shunts116 and to measure abnormal
cerebrospinal fluid motion.i17
FUTURE
PROSPECTS
Echo planar and beam-directed real-time MR sequences that allow flow quantification
are currently
being introduced. 77,r18-120 Additional
technical improvements are required, for instance, with regard to
the limited spatial resolution of echo planar techniques. Furthermore,
significant progress is being
made in the challenging field of MR coronary artery
flow quantification.
It can be expected that with these
new,developments
MR imaging and MR flow quantification will enhance the establishment of MR as an
important
additional tool in cardiovascular diagnosis. However, the disagreement
between MR and
Doppler velocity measurements in some cases63ylo1
requires further attention. Finally, some economic
and logistic aspects will undoubtedly have to be dealt
with before MR imaging and MR velocity mapping
will be fully included in the range of cardiovascular
diagnostii modalities.121, 122
It is concluded that noninvasiveness, free choice of
imaging planes, wide field of view, the combination of
anatomic and functional analysis in one session, and
obtaining .a11information
without the need for radiation or contrast media, are generally recognized advantages of MR imaging. MR velocity mapping
allows additional
functional analysis by providing
two-dimensional
velocity profiles at frequent intervals throughout the cardiac cycle. This advantage of
MR velocity mapping over Doppler eehocardiography is of importance in the great vessels because they
often display nonuniform flow profiles.27-2g~ 33s62,go In
addition, MR velocity mapping can be performed in
any plane with unlimited access, and this technique
has been shown to be accurate for the measurement
of velocity and flow in a number ,of cardiovascular
applications. The clinical use of MR velocity map-
American
December 1993
Heart J6urnal
ping will benefit’from real-time d,ata acquisition and
technical improvements
that will ultitiately
allow
noninvasive measurement of coronary artery flow.
SUMMARY
With a newly developed magnetic resonance (MR)
technique for blood flow measurements, qualitative
and quantitative
information
on both flow volume
and flow velocity in the great vessels can be obtained.
MR flow quantitation
is performed with a gradientecho MR sequence with high temporal resolution enabling measurements at frequent intervals throughout the cardiac cycle. MR flow quantitation
uses the
phase rather than the amplitude of the MR signal to
reconstruct the images. These images, often referred
to as MR velocity maps or velocity-encoded tine MR
images, are two-dimensional
displays of flow velocity.
From these velocity maps, velocity and volume flow
data can be obtained. Previous validation experiments have demonstrated the accuracy of MR velocity mapping, and this technique is now being applied
successfully in several clinical fields. MR velocity
mapping may be of considerable value when Doppler
echocardiography results are unsatisfactory or equivocal, particularly because MR is suited’for the analysis of volumetric flow and complex flow patterns.
Among the vastly growing number of clinical cardiovascular applications that have been reported are the
great arteries and veins, coronary vessels, valvular
disease, and the abdominal and peripheral vessels.
These items are reviewed, and some aspects of the
technique that need improvement
are discussed.
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RDCS, Thomas
There has been extensive experience with Doppler
velocity measurements in the assessment of volumetric flow in the aorta and pulmonary artery and across
each of the cardiac valves. Sequeira et al17 2 initially
demonstrated a good correlation between the timeaveraged velocity or velocity integral in the ascending aorta and invasively measured stroke volume.
Subsequent investigations3-6 have shown that stroke
volume can be calculated as the product of the time
velocity integral and the cross-sectional area of the
valve or vessel at the sample site. Cardiac output is
then obtained by multiplying
the stroke volume by
the heart rate. The application of these principles has
From
Louis
121.
St.
St. Louis University
Medical
Vista Avenue
at Grand Blvd.,
Decemkr
1993
H&f Journar
L. Cravens, RN, and
allowed avariety of clinical Doppler measurements of
cardiac blood flow, including absolute blood flow,
calculation of intracardiac shunts,7> 8 estimation of
aortic valve area,g and assessment of regurgitant
fractions.lOl l1 In making these measurements a number of assumptions must be accepted, including (1)
the laminarity of blood flow; (2) a Doppler interrogation angle of <20 degrees; and (3) a relatively blunt
flow profile from which the measurement is calculated. Although these assumptions are generally true
for measurement of blood flow in the heart and great
vessels, inadequate data exist validating
these assumptions in smaller (<6 mm diameter) arteries.
Direct measurement of coronary bIood flow in human coronary arteries has been limited, to a large extent, by the available technology. Transcutaneous
interrogation
of coronary floti has generally been beyond the resolution of commercially available instruments. Recent reports have indicated that the Doppler measurements of coronary flow might be possible in selected patients by using transesophageal