Warren

B. Gefter,

Harold

I. Palevsky,

MD MD

#{149} Hiroto

Hatabu,

#{149} Nathaniel

MD2 Reichek,

J Dinsmore,

#{149} Barbara

MD

#{149} Mark

MD

L. Schiebler,

#{149} Leon

MD3

Pulmonary Vascular Cine MR Imaging: A Noninvasive Approach to Dynamic of the Pulmonary Circulation’ Cine gradient-recalled magnetic resonance (MR) imaging, which has flow sensitivity and high temporal resolution, may potentially yield both morphologic and dynamic flow-related information in the pulmonary vasculature. used this modality monary vessels in

The

pulsubwith a vandisorders.

12 healthy

jects and in 14 patients ety of cardiopulmonary Normal

authors

to evaluate

pulmonary

arteries

and

veins were characterized by distinctive signal intensity and diameter variations as well as motion of the vessels during the cardiac cycle. Patients with pulmonary arterial hypertension demonstrated loss of the normal

pulsatile

systolic

increase

and diastolic decline in velocity-related signal intensity and in diameter of the proximal pulmonary arteries. Disorders of pulmonary venous signal and diameter profiles during the cardiac cycle, which show a characteristic biphasic pattern in healthy subjects, were identified in five patients with mitral valvular disease. These initial results mdicate that cine MR imaging techniques hold promise in the evaluation of pathophysiologic conditions in the pulmonary circulation. Index terms: Hypertension, pulmonary, 564.78, 565.78 #{149}Lung, MR studies, 60.1214. Magnetic resonance (MR), cine study #{149}Pulmo564.91 . Pulmonary 564.91 #{149} Pulmonary 564.1214 #{149} Pulmonary Pulmonary veins, MR studies,

nary

arteries,

dynamics, studies,

Radiology

1

From

B.J.D.,

1990;

veins, 565.1214

flow

MR 565.91

176:761-770

HE appearance vessels on

(MR) the

images pulse

of the magnetic

is highly

sequence

pulmonary resonance

dependent used

and

on

the

phase of the cardiac cycle (1-3). On ebectrocardiogram-gated spin-echo (SE) images, the normal pulmonary vessels increase in signal during diastole but lose signal due to increased velocity during systole (1). Abnormal persistence of signal in the pulmonary arteries during the systolic penod on SE images has been used to identify patients with pulmonary antenial hypertension (4,5). We recently demonstrated the ability to image pulmonary vessels using a single breath-hold GRASS technique (gradient-necalled acquisition in the steady state) (2). The applications of such vascular imaging with static GRASS scans can be lengthened by using dynamic cine GRASS (6). The flow sensitivity and high temporal resolution of cine GRASS has proved useful for cardiac imaging (6-8). Cine GRASS

can also

be used

to evaluate

the

pul-

monary circulation. Although a numben of factors influence vascular signal intensity on cine GRASS images, flow phantom studies using cine

GRASS

have

demonstrated

that

sig-

nal intensity of vascular flow is highly correlated with pulsatile flow mean velocity up to approximately 30 cm/sec (9). Moreover, graphs of signal intensity changes over the cardiac cycle also show a high correlation with pulsatile flow velocity profiles for velocities of 4.0-16.6 cm/sec (9). Therefore, this noninvasive technique has the potential to yield both

the Departments

L.A.,

M.L.S.,

of Radiology (David W. Devon Medical Imaging Center) (W.B.G., H.H., and Medicine (HIP., N.R.), Hospital of the University of PennsylvaSt, Philadelphia, PA 19104. Received August 10, 1989; revision requested SeptemH.Y.K.)

nia, 3400 Spruce ben 13; revision received April 2 Current address: Department pan. 3 Current address: Department c RSNA,

arteries, arteries,

T

1990

27, 1990;

accepted

of Radiology

April

30. Address

and Nuclear

Medicine,

reprint

Kyoto

requests

Axel,

#{149} Herbert

University

of North

Carolina,

MD

.

Kressel,

MD

morphologic and dynamic fbow-related information in the pulmonary vessels as well as information about their relation to cardiac events. To evaluate this application of cine MR imaging, we analyzed the appearance of pulmonary vessels in a group of healthy subjects and assessed variations from that appearance in a sebected group of patients with documented cardiopulmonary disorders. These initial results form the basis of this report.

SUBJECTS

METHODS

AND

Twenty-six subjects were studied: 12 normal subjects (nine men, three women; age range, 24-38 years) and 14 patients. The patient group included eight with pulmonary arterial hypertension: four women with primary pulmonary hypertension (age range, 19-45 years), three patients with chronic pulmonary emboli (two men, one woman; age range, 51-69 years; two studied prior to thromboendarterectomy, one studied following sungery), and one man with bong-standing atrial septal defect. The mean pulmonary artery pressures in these patients with pulmonary hypertension ranged from 36 to 73 mm Hg, with a mean of 52.8 mm Hg ± 13.6. The patient group also included four patients with mitral regurgitation, one with mitral stenosis, and one with valvular pulmonic stenosis. Examinations were performed on a 1.5T imager (Signa; GE Medical Systems, Milwaukee). After obtaining a short repetition time (TR)/echo time (TE) coronal localizing image and electrocardiogramgated axial images (TR RR interval, TE = 20-25 msec), we obtained axial cine GRASS images that encompassed the 1evels of the main pulmonary artery, proximal (intrapericardiab) right pulmonary artery, and proximal descending right and left pulmonary arteries. The cine sequence used a TR of 25 msec, TE of 13 msec, and flip angle of 30#{176}. Section thickness was 5-10 mm, field of view was 24-

to W.B.G.

University, Chapel

Y

Imaging

Kyoto,

JaAbbreviations:

of Radiology,

PhD,

Hill,

NC.

acquisition TE = echo

GRASS

gradient-recalled

in the steady state, time, TR = repetition

SE

spin

echo,

time.

761

a.

b.

Figure

dent

2.

Increase

on images

in

and signal intensity of pulmonary arteries (arrows) is eviin systole (a) compared with those obtained in diastole (b).

diameter

obtained

Figure 1. Cine image obtained during systole (127 msec after R wave) in a 28-year-old healthy man (pixel size 0.94 X 1.90 mm). Pulmonary vessels are visualized to subsegmental branches.

cm, matrix size was 256 X 128, and four signal averages were used. From five to 30 frames were acquired through the cardiac cycle; most examinations consisted of seven to 15 cardiac phases per cycle obtained by interleaving three acquisitions, each comprising three anatomic levels. This resulted in an effective TR of 75 msec for each section. The cine GRASS sequence utilizes first-order (velocity) 40

compensation

by

gradient

moment

null-

ing in the section-select and readout directions. Both qualitative and quantitative image analyses were performed. For the qualitative evaluation, images were displayed on the monitor in cinematic mode. The size of peripheral pulmonary vessels imaged was determined by two radiologists in terms of the number of generations of branching vessels visualized. To assess the ability to differentiate peripheral pubmonary arteries from veins, vessels were evaluated with regard to signal intensity and diameter variations from systole to diastole as well as their motion (centnipetal versus centrifugal motion during systobe). Synchronization of these parametens with those recorded in larger, anatomically defined central arteries and veins served as a reference. Quantitative image analysis was performed in six of the healthy subjects and in 12 of the 14 patients by means of still frames on the monitor. Signal intensities and diameters at each phase of the cardiac cycle were measured in the main pubmonary artery, proximal right pulmonary artery (posterior to the ascending aorta), proximal descending right and left pubmonary

arteries,

and

inferior

pulmonary

veins just proximal to the left atrium. A complete data set for all locations could not be obtained for every patient. The distribution of these measurements is summarized in Table 1. The signal intensity within the vessel lumen was measured with existing region-of-interest software. This intensity was calculated as 762

#{149} Radiology

follows: (signal intensity of the vessel background signal intensity)/(muscbe on fat signal intensity background signal intensity). The percentage of increase in pulmonary

artery

signal

tole relative to diastole follows: [(maximum stolic 51)/end-diastolic SI = signal intensity. ters were calculated sors. Window width maximize

visualization

intensity

in sys-

was calculated as systolic SI - end-diaSI] X 100, where The vessel diamewith electronic curand level were set to of the

lateral

walls of the main pulmonary artery. The percentage of change in pulmonary artery diameter during the cardiac cycle was calculated as follows: E(Dmax Dmin)/ Dmin] X 100, where Dmax maximum diameter of the pulmonary artery and Dmjn = minimum diameter of the pulmonary artery. The signal intensities and diametens for each location were plotted against the phase of the cardiac cycle (trigger delay following the R wave expressed as absolute time or percentage of total RR interval). Graphs demonstrating characteristic

candiosynchronous

intensity

and

diameter profiles were selected for illustration. The quantitative measurements were made with knowledge of the subjects’ di-

agnoses. Inter- and intraobserver vaniabilities in these measurements were tested by two radiologists (W.B.G., B.J.D.) in a subset of both healthy subjects (n 2) and patients (n 2) encompassing all yessel locations, cardiac phases, and section levels. Interobserver variability showed correlation coefficients of .97 for signal intensity of the vessel (74 paired samples) and .97 for vessel diameter (30 paired samples). Intraobserver variability showed correlation coefficients of .97 for signal intensity of the vessel (30 paired samples) and .98 for vessel diameter (30 paired samples).

RESULTS Normal

Pulmonary

Vessels

Vessel branches could be traced to at least the fifth generation in 83.3% of the healthy subjects and to at least the fourth-generation (subsegmentab) branches in 92.0% of them (Fig 1). In 90.0% of the cases, pulmonary arteries and veins could readily be distinguished according to their pattern of

September

1990

3.2

3.0

2.8

2.6

2.4

2.2

2.0 0

200

400

600 TIME

800

1000

(MS)

a.

c.

b. 3.0

T’

2.8

ed a characteristic biphasic curve with signal intensity peaks in both systole and diastole, the latter being more prominent (Fig Sc). Although little variation in caliber of the central pulmonary veins at their junction with the left atrium was observed through the cardiac cy-

2.6

2.4

2.2

:: TIME

_j 120

(%RjR) flME

d.

(% R.R)

e.

Figure 3. (a) Signal intensity of the main pulmonary artery versus time during the cardiac cycle in two healthy subjects. Time EMS] delay in milliseconds after R wave. The early systolic decrease in signal in the bottom curve corresponds to normal systolic turbulence, evident in the cine MR image (arrow in b). (C) After systolic ejection, there is return to higher signal intensity reflecting more laminar flow. (d) Signal intensity versus time measured in the proximal right pulmonary artery in two healthy subjects. (e) Prominent systolic peak in signal intensity (solid arrow) is evident in the normal interbobar right pulmonary artery. The smaller diastolic signal peak (open arrow) may represent a flow wave generated by diastolic recoil of the main pulmonary artery. In d and e, Time (% R/R) time expressed as a percentage of the RR interval.

pulsation, movement, and direction of the propagation of pulsation, as well as the ability to show continuity with a central artery or vein. Normal pulmonary arteries.-The cinematic display demonstrated that the pulmonary arteries showed a pubsatile increase in diameter and signal intensity during systole compared

brief decline in signal intensity duning the very early part of systole was recorded in the normal main and proximal night pulmonary arteries; this decline corresponded to normal transient turbulence (Fig 3a-3d). A second bower amplitude peak was observed in diastole in the descending pulmonary arteries (Fig 3e).

with diastobe (Fig 2). Frequently, a centrifugal propagation of the signal intensity wave could be identified. In addition, the arteries moved in con-

Measurements of normal pulmonary arterial diameters throughout the cardiac cycle showed an abrupt increase in vessel diameters in systobe and rapid decline in diastole (Fig 4). Normal pulmonary veins.-Unlike the normal arteries, the normal pulmonary veins showed little fluctuation in size and signal intensity duning the cardiac cycle (Fig 5a, Sb). On

cert outward systole. These firmed

from

observations quantitative

by

of pulmonary diameters

cle.

the

artery throughout

Among

the

hilum

in

were conmeasurements

intensities the

healthy

cardiac

and cy-

subjects,

measurements of signal intensity within the proximal pulmonary anteries confirmed a systolic peak duning systole (Fig 3). In the main pulmonary artery there was a more gradual rise and fall in signal intensity than observed more distally in the right and left pulmonary arteries. A

Volume

176

#{149} Number

3

cle, diameter

measurements

of the

in-

fenion pulmonary veins indicate that small biphasic increases may occur in systole and early diastole (Fig Sd). Unlike the pulmonary arteries, which show a centrifugal motion, the pulmonary veins exhibited an inwand motion toward the hilum, coincident with left atrial emptying, duning both diastole and atnial systole.

Pulmonary

Vascular

Disorders

Pulmonary arterial hypertension. The patients with pulmonary hypertension showed not only the anticipated dilatation and pruning of the central pulmonary arteries with attenuation of peripheral branches but also demonstrated a marked flattening of the diameter-time curves in the proximal arteries (ie, relatively little change in vessel caliber throughout the cardiac cycle) (Fig

close observation, central pulmonary veins displayed a biphasic signal intensity pattern with small increases in both systole and diastole. This was confirmed with analysis of quantitative signal intensity/time curves of

6a-6c). The calculated percentages of change in the diameters of pulmonary arteries in systole versus diastobe in healthy subjects compared with patients with pulmonary hypertension are shown in Table 2. The differences in the mean values between the two groups was significant for each location (unpaired Student test). A comparison of the diameter data from the proximal right pulmonary artery is shown graphically in Figure 6d. In addition, in contrast to healthy subjects, patients with pulmonary hypertension showed a marked flattening of the signal intensity-time

the signal pulmonary

curves in the nary arteries,

measured veins,

in the central which demonstrat-

right and demonstrating

left

pulmorelative-

Radiology

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100

120

c.

Figure 4. Normal pubsatile systolic rise and diastolic fall in vessel diameter is demonstrated in the main (a), proximal right bar right (c) pulmonary arteries in two healthy subjects. Time (% R/R) time expressed as a percentage of the RR interval.

(b), and

interbo-

by little

change in signal intensity from systole through diastole (Fig 7a). This boss of the normal systolic increase and diastolic decline in signal intensity is reflected in the graph in Figure 7b, which compares the percentage increase in signal intensity in the proximal right pulmonary artery in systole relative to the signal intensity in end diastole in healthy subjects and patients with pulmonary hypertension. Calculations of the percentage of systolic increase in signal intensity in healthy subjects yensus that of patients with pulmonary hypertension for each vessel location are summarized in Table 3. The differences were significant (unpaired Student t test). Signal intensity curves obtained from the main pulmonary artery in patients with pulmonary hypertension showed a more rapid rise and fall and a shorter time to peak signal intensity compared with those of healthy subjects (Fig 7c). The patient with severe pulmonary hypertension secondary to long-standing atrial septal defect with Eisenmengen syndrome demonstrated an unusually marked degree of systolic turbulence in the marked-

by dilated

main

and

proximal

gle patient with valvular pulmonic stenosis showed a pronounced systolic turbulent jet in the main and left pulmonary arteries, with normal laminar high-signal-intensity flow in the night pulmonary artery (Fig lOalOc). This was confirmed by quantitative signal intensity measurements (Fig lOd). These data are consistent #{149} Radiology

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pulmonary arteries (Fig 8). Two patients with thromboembolic pulmonary arterial hypertension who were examined preoperatively displayed focal low-signal-intensity mural defects that remained constant throughout the cardiac cycle (Fig 9). These fixed defects were consistent with chronic thrombus. Valvular pulmonic stenosis.-The sin-

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systole

differentiated These

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20

1000

(MS)

(a)

and

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show (b).

arteries, only

Pulmonary (c) Quantitative

pulmonary

fluctuations

veins

in diameter

artery and vein intensity-time

(open and

arrows signal

intensity

branches thus can be readily plot in a normal inferior

on the cine display. just proximal to the left atrium shows characteristic correlate with Doppler flow profiles, the systolic peak

vein

peaks

small

normal

biphasic

(solid

flow

arrow)

pattern.

occurring

with atnial relaxation and the diastolic peak (open arrow) with transmitral ventricular filling. Time (MS) delay in milliseconds after R wave. (d) Diameter-time curves show that there may be only small fluctuations in the caliber of normal veins through the cardiac cycle. Time (% R-R) time expressed as a percentage of the RR interval.

with a poststenotic jet directed preferentially into the left pulmonary artery. Mitral valvular disease.-The normal biphasic venous flow pattern was absent in patients with mitral

valvular disease. A decrease in intensity from late systole to early diastole was measured in the veins in patients with mitral regurgitation (Fig ha). The cine images showed that this flow pattern resulted from retrograde

September

1990

curve was markedly flattened, with absence of the normal systolic and diastobic signal intensity peaks (Fig 12). Pulmonary vein diameters in the patient with mitral stenosis were abnormalby large throughout the cardiac cycle.

DISCUSSION The that seen

results

of all cases,

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SUBJECTS

d. Figure

6.

primary

(a) Systolic pulmonary

image

(obtained

hypertension

212 msec

shows

dilatation

after

R wave)

of main

and

in a 45-year-old right

woman

pulmonary

(rPA)

with arter-

ies with little change relative to diastolic diameters (b). (c) Unlike pulmonary arteries in healthy subjects, the pulmonary arteries in patients with pulmonary hypertension were not only dilated but failed to show normal systolic distention and diastolic collapse, as illustrated by diameter-time measurements in the proximal right pulmonary artery. Time (% R-R) = time expressed as a percentage of the RR interval. (d) Percentage diameter changes in the pulmonary arteries during the cardiac cycle are significantly reduced in patients with pubmonary hypertension. Data are from the proximal right pulmonary artery. The difference in the means for the two groups was significant, P < .001 (see Table 1). This decreased “distensibility”

correlates

with

observed

decreases

in

tients. Number mum diameters

at the top of each bar represents divided by minimum diameter

propagation from the

of the atrium

nary

left

veins

(Fig

negurgitant into the

jet pulmo-

1 lb-lid).

Diameter-time curves measured in the central inferior pulmonary veins in patients with severe mitral negurgitation,

Volume

unlike

176

those

#{149} Number

of healthy

3

sub-

pulmonary

arterial

the difference

compliance

between

in

maximum

these

and

pa-

mini-

X 100.

jects, showed a prominent pulsatile, early systolic dilatation (Fig 1 le), consistent with retrograde distention by regurgitant flow from the left atrium. In the patient with mitral stenosis, the venous signal intensity-time

of this

the pulmonary well with cine

vessels

study vessels GRASS.

indicate can be In 83.3%

out to at least

fifth-generation branches were visualized, and vessels as peripheral as the fourth generation (subsegmental) were seen in 92.0% of all cases. In each study, the differing appearances of arteries and veins could be appreciated. This distinction supports the possibility that cine MR may be useful for depicting function as well as morphology in the pulmonary circulation. Normal pulmonary arteries were characterized by a rapid increase in signal intensity and diameter in systole with a rapid decrease during diastole. These vessels “blink” during the cardiac cycle. In arteries parallel to the image plane, centrifugal propagation of high signal intensity was noted, at times even in the fifth-generation branches. Also evident was an outwand motion of the arteries during the systolic pulse. In the normal main and proximal night pulmonary arteries, areas of decreased signal intensity were seen briefly during earby systole, representing a flow distunbance presumably secondary to highvelocity flow and turbulence at the angulation between the main and right pulmonary arteries. A secondany diastolic intensity peak was observed in the descending pulmonary arteries. The significance of this peak is uncertain, but it may represent a flow wave propagated by diastolic collapse of the compliant main pulmonany artery, analogous to the windkessel model in the aorta. Unlike normal pulmonary arteries, the normal pulmonary veins could be characterized by signal intensity peaks in both systole and diastole. Such a biphasic signal intensity pattern is consistent with reported data obtained with pulsed Doppler echocardiography and experimental electromagnetic flow probes (10-16). According to Keren et al (10), the initial peak in pulmonary venous flow occurs in ventricular systole with atnial relaxation, simultaneously with the reduction of left atnial pressure; the second peak occurs in diastole with

Radiology

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Figure 7. (a) Note boss of the normal systolic-diastolic variation in signal intensity during the cardiac cycle in the proximal right pulmonary artery in two patients with primary pulmonary hypertension (lower curves) compared with systolic-diastolic variation in two healthy subjects. (b) Percentage increase in signal intensity in systole relative to diastobe measured in the proximal right pulmonary artery of healthy subjects is increased in comparison with that in patients with pulmonary hypertension. (Difference in mean values for the two groups was significant, P < .01; Student unpaired t test.) This reflects the decreased systolic velocity and damped flow pulse observed in pulmonary hypertension. Number at the top of each bar represents percentage of increase in signal intensity. Max = maximum systolic signal intensity, ED.

sion

end-diastolic demonstrates

signal a more

=

pertension (arrow) creased impedance

intensity. rapid rise

(c) Flow-related and fall compared

signal with

intensity in the main those of two healthy

pulmonary

artery

correlates with Doppler echocardiographic findings and in pulmonary hypertension. In a and c, Time (% R/R) = time

with

pulmonary

hyperten-

expressed

as a percentage

of the

RR interval.

b.

a.

Figure

8.

monary

(a) A marked

artery

(solid

arrow)

degree

of systolic in this patient

turbulence is present in the with Eisenmenger syndrome

proximal secondary

right pubto long-

standing

atnial septal defect. Turbulence to this degree was not observed in the patients with pulmonary hypertension. The bow signal turbulence is distinguished from clot by the high flow-related signal in diastole (b). Note that the “pruned,” markedly dilated central vessels (open arrow) show no diameter changes between systobe and diastole. primary

left ventricular relaxation and rapid transmitral filling of the ventricle. A biphasic centnipetal motion of the pulmonary veins, in contrast to the arteries, is also associated with mechanical events taking place in the left atrium. The veins move centrally synchronously with emptying of the left atrium during diastole and atrial systole. Inflow of high-signal-intensity blood from the pulmonary veins into the left atrium could be identified frequently during systole and diastole, manifested by turbulent areas within the left atrium at the entrance of these veins. Although the number of abnormal cases analyzed in our study was small, these initial results would suggest a role for cine MR imaging in revealing altered vascular dynamics in the pulmonary circulation. Patients 766

in a patient

subjects. The triangular velocity profile in pulmonary hyis a result of reduced pulmonary artery compliance and in-

#{149} Radiology

with pulmonary arterial hypertension demonstrated not only dilatation of the central pulmonary vessels, but a loss of the normal systolic-todiastolic variations in vessel distention and velocity-related signal intensity. The loss of the normal “distensibibity” of the central pulmonary vessels in these patients may be related to observed decreases in pulmonary arterial compliance and damping of the flow pulse, which have been measured in pulmonary hypertension (17-19). Bogren et al (20) also recently demonstrated reduced pulmonary artery distensibility in patients with pulmonary hypertension using cine MR phase velocity mapping with the field even-echo rephasing method. Von Schubthess et al (4) and Didier and Higgins (5) reported increased systolic signal in-

Figure

nary

9.

Chronic

thromboembolic

hypertension.

ty defect

in the

This right

pubmo-

bow-signal-intensi-

pulmonary

artery

(an-

row), which remained fixed throughout the cardiac cycle, was found at surgery to represent organized thrombus. (A right pleural effusion is present.)

tensity in the night pulmonary artery on SE images that correlated with increases in pulmonary vascular resistance. Such increased signal intensity has been attributed to abnormally slow velocity during systobe in these patients. Signal intensity measurements obtained in the right and left pulmonary arteries on our cine studies show with greater temporal resolution this loss of the normal systolic velocity peak occurring in pulmonary hypertension. Moreover, measurements of the signal intensity profile in the main pulmonary artery in patients with pulmonary hypertension showed a more rapid rise and fall than measurements in healthy subjects. This correlates well with pulsed Doppler echocandiographic studies showing a more rapid accelenation and deceleration and an eanli-

September

1990

signal intensities observed in normal subjects versus those pulmonary hypertension. The number of frames per cardiac was nine for both groups. In tion, there was no significant ence (unpaired Student t test) mean heart rates between the

the with mean cycle addidifferin the two

groups that may have influenced the results, being 71 beats per minute for the healthy subjects and 79 for the patients with pulmonary hypertension.

Three of the nary hypertension

MR imaging a.

b.

MPA / -

-.---..

DESCRPA

2

.

i

:

-

1

200

100

300

500

400

600

700

T)ME(MS)

d.

C.

Figure

10.

Valvular

pubmonic

stenosis.

(a) Image

intensity due to turbulent jet in main pulmonary sity jet is propagated preferentially down the

left

obtained artery (long pulmonary

during arrow). artery

systole This (open

shows

low signal

bow-signal-intenarrow), resulting

in a lower signal intensity than that of the right pulmonary artery (short arrow). (b) Diastolic image at similar bevel now shows high-signal-intensity laminar flow in a dilated left pulmonary artery (arrow). (c) Image obtained at diastole at lower level confirms preferential flow down left pulmonary artery (solid arrow) compared with flow down right pulmonary artery (open arrow). (d) Quantitative signal intensity-time measurements also reflect the poststenotic jet directed into the descending left pulmonary artery (DESC LPA), the signal profile of which tracks with that of the main pulmonary artery (MPA) and is increased over that of the descending right pulmonary artery (DESC RPA).

800

patients with pulmostudied with cine

had

documented

chron-

ic pulmonary emboli. In two patients studied before thromboendanterectomy, the cine studies showed eccentnic low-signal-intensity foci along the walls of the proximal night, descending right, and/or left pulmonary arteries. These bow-signal-intensity defects, corresponding to organized clot, remained fixed throughout the cardiac cycle. The cine study of the third patient, obtained after thromboendarterectomy, demonstrated absence of such central filling defects. The distinction between thrombus and intraluminal signal due to slow flow is potentially more easily made with cine GRASS than SE pulse sequences because of the high contrast between flowing and stationary tissue on cine GRASS images, signal loss due to magnetic susceptibility inhomogeneity from hemosidenin in clot on cine GRASS images, (24), and the ability to observe signal intensity variations throughout the cardiac cycle. Unlike that of clot, signal loss due to turbulence would be expected to show temporal variability throughout the cardiac cycle. Cine MR imaging vividly depicted the high-velocity poststenotic jet dinected preferentially into a dilated left pulmonary artery in the case of valvular pulmonic stenosis. This represents an extension of the applica-

en time to peak with pulmonary

23). This

velocity in patients hypertension (21-

triangular

configuration

of

the velocity profile is again believed to be a consequence of reduced pubmonary artery compliance and in-

Volume

176

#{149} Number

3

creased impedance in pulmonary hypertension (17,21). Although there was some variability in the cine technique used in our subjects, this was not sufficient to account for the differences in vessel

tion of cine MR imaging in the identification of cardiac valvular dysfunction (7,25,26). Pulmonary venous changes could also be identified in the several cases of mitral valvular disease. Retrograde propagation of the regungitant jet from the left atrium into pulmonary veins was identified in four cases of mitral insufficiency, manifested by a decrease in signal intensity during systole in combination with a coincident increase in vessel diameter. Loss of the normal systolic and diastolic venous signal intensity peaks associated with increased venous diameter

Radiology

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(% R.R)

b.

a.

C. 10

throughout the cardiac cycle was observed in the single patient with mitral stenosis who was evaluated. These preliminary results suggest a new noninvasive approach to the study of pathophysiology in the pulmonary venous circuit. Such a technique, for example, may be used to study the effects of acute and chronic left ventricular failure on the distribution of pulmonary blood flow. A number of factors could affect the visualization of the pulmonary vessels with this cine technique. The signal intensity varies in relation to the angle with which the vessel is oriented relative to the image section, with signal increasing with a perpendicular

orientation

(27).

Areas

of turbulent flow or shear may produce regions of signal boss (28). Magnetic susceptibility differences between the vessels and adjacent aircontaining lung might also result in some degree of signal loss at the edge of vessels. It is recognized that calculating vessel diameters with the intraluminal region of increased signal intensity on cine images could potentially cause underestimation of the true vessel size. In addition, diameters perpendicular to the true axis of the vessels are not always obtained; thus, sources of potential error are introduced. Respiratory motion may also cause problems related to partial volume averaging as well as motion artifacts.

The

latter

may

be improved

with increased numbers of signal averages. The results of this study are descniptive and semiquantitative. Evans et al (9) showed a high correlation (r =

.97)

between

signal

intensity

of

flow phantoms using cine GRASS and pubsatile flow mean velocity up to 30.1 cm/sec. The graphs of change in vascular signal intensity through the cardiac cycle were virtually superimposable on the actual pulsatile flow velocity profiles (r .897) for velocities between 4.0 and 16.6 cm! 768

#{149} Radiology

I

A

*_

r

______

/

NORMAL

9

1’ 00 00

#{163}4

.j 4

/ ‘,

\

/

,,

A--A

A 6

5 )

20

40

60

100

80

120

TIME (% R.R)

d.

e.

(M REGURG). (a) Two patients with mitral regurgitation showed loss of the normal biphasic venous flow pattern, with late systolic to early diastolic drop in signal intensity (arrow). (b) End diastobe. (c) Systole. (d) Early diastobe. As demonstrated on these cine images (b-d), the drop in signal intensity seen in a reflects the bow-signab-intensity regurgitant jet (open arrow) propagated retrograde from the left atrium into the pulmonary vein (solid arrow). (e) Abnormal early systolic pulmonary vein distention (arrow) is evident in this patient with severe mitral regurgitation. This systolic increase in venous diameter reflects retrograde propagation of regurgitant flow from the left atrium. In a and e, Time (% R-R) time expressed as a percentage of the RR interval. Figure

11.

Mitral

regurgitation

sec (9). Although vascular signal intensity on cine GRASS images has thus been correlated with flow vebocity, it is not a direct quantitative measure of such velocity. Higher order motions and turbulence will act to decrease signal intensity. This was particularly evident in the main pubmonary

artery

during

early

vascular signal intensity images that is caused by enhancement reaches a

maximum

when

is suffi-

ciently high that upstream, fully magnetized spins totally replace the previously excited spins within a section during the interval TR. The yebocity at which sity is reached

this maximum (d/TR, where

inten-

section thickness) (29) will therefore decrease with thinner sections. The velocity dependence of vascular signal intensity in gradient refocused imaging is also influenced by the TR, TE, and flip angle used (27,30,31). This

mized

velocity

with

dependence

the

use

:

systole.

In addition, on GRASS flow-related

velocity

.-‘+-.

d

is maxi-

of a short

TR,

_- --.Ht

)

20

j....

60 TiME

Figure

12.

Mitral

.

40

NORMA).

(S

stenosis.

/

I

80

100

10

A-A)

Pulmonary

ye-

nous signal intensity-time curves demonstrate loss of both the systolic and diastolic flow peaks in a patient with mitral stenosis (bottom curve) compared with those in a healthy subject (top curve). Time (% R-R) time expressed as a percentage of the RR intenvab.

short TE, and 90#{176} flip angle. In the cine sequence, however, all of the above parameters are held constant throughout the cardiac cycle, with the exception of flow velocity (and higher order terms), turbulence, and some

slight

variations

in the

onienta-

September

1990

tion of the vessels due to movement. Therefore, within these limitations the velocity-sensitive intensity waveforms analyzed in our study are believed to be valid indicators of the velocity variations in the pulmonary vessels occurring throughout the cardiac cycle. Quantitative phase-encoded velocity maps (20,32,33) could

veins in patients with mitral valvular disease. Further development and applications of velocity-encoded cine MR imaging hold great potential for the investigation of pathophysiobogy in the pulmonary circulation and in the clinical evaluation of patients with pulmonary vascular disease. U

potentially

Acknowledgments: to the following

allow

cine

MR

imaging

to

be a powerful modality in the noninvasive assessment of pulmonary blood flow yielding temporal profiles of both flow velocity and volume flow. Techniques such as these hold promise in extending the range of pulmonary vessels amenable to examination beyond those accessible to examination with Doppler echocardiography, which is limited to velocity measurements sampled in the main pulmonary artery and central pulmonary veins (10,11,22,23,34,3S). Aside from the limitations in quantification of flow, the cine technique we used has the disadvantages of relatively long acquisition times and the need to average data from multiple cardiac cycles. With the technique used in our study, acquisition of three sections requires 7-8 minutes. Because the data are acquired from 128 cardiac cycles, information on instantaneous flow is not available, nor can one sequentially track the passage of blood through the pulmonary circulation. Velocity-encoded cine techniques (20,32,33,36), ultrafast MR imaging (37), and cine bolus tracking (38-40) are potential methods of overcoming these limitations. In conclusion, this study demonstrates that cine gradient-recalled MR imaging represents a new approach to dynamic imaging of morphology and blood flow patterns in the pul-

persons

The authors for their

are

grateful

generous

sistance: Lawrence Dougherty, BS, for help in implementing the cine technique; Christine Harris, RT, for conducting many of the MR imaging studies; Karen Weiss, BS, for technical assistance in preparing the manuscript; John

Kahler, BS, for help in producing the graphs; and Robert Lenkinski, PhD, for helpful sugges-

References 1.

Ann Radiol 2.

Hatabu

WB,

Kressel

HY,

3.

Haacke

EM,

stein with

5.

6.

GW,

Jacob-

of Magnetic

Resonance

program and abImag 1987; 5:78. Fisher MR. Higgins CB. Pathologic blood flow in pulmonary vascular disease as shown by gated magnetic resonance imaging. Ann Intern Med 1985; 103:317-323. Didier D, Higgins CB. Estimation of pulmonary vascular resistance by MRI in patients with congenital cardiovascular shunt lesions. AJR 1986; 146:919-924. Glover GH, PeIc NJ. A rapid-gated cine

In: Kressel

netic resonance annual Raven, 1988; 299-333.

1988.

Sechtem

PW,

U, Pflugfelder

New

with

24. White

RD.

Gould

RG, Holt W, Lipton MJ, Higgins Cine MR imaging: potential for the evaluation of cardiovascular function. AJR 1987; 148:239-246.

CB.

posi-

contrast as well as good spatial temporal resolution. Potential applications of this technique indude preoperative evaluation of the peripheral pulmonary arteries in patients with congenital forms of pubmonary hypoplasia or atresia (41-43), identification of acute and chronic central pulmonary embobi (24,44), evaluation of vascular lung lesions such as arteriovenous malformations (45), and identification of patients with pulmonic stenosis. Moreover, the current study has shown the ability of this technique to depict altered flow dynamics in pulmonary arteries in patients with pulmonary arterial hypertension and in pulmonary Volume

176

#{149} Number

3

23.

York:

and gradient

vessels

22.

HY, ed. Mag-

tive

pulmonary

21.

Imaging

fifth annual meeting stracts. Magn Reson von Schulthess GK,

MRI technique.

7.

B, Lenz

M. Pulmonary vessel identification magnetic resonance imaging (abstr).

Society

4.

Fletcher

in

and

depicts

has

Reuben

L,

JA,

Herfkens

RJ,

refocussed

Heinsimer

echoes

JA,

25.

1 1.

12.

13.

SR.

Compliance

of the

human

9:254-260.

Bogren HG, Klipstein RH, Mohiaddin RH, et al. Magnetic resonance studies of pubmonary artery distensibility and blood flow patterns in normal subjects and in patients with pulmonary arterial hypertension (abstr). In: Book of abstracts: Society of Magnetic Resonance in Medicine 1989. Vol 1. Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1989; 315. Okamoto M, Miyatake K, Kinoshita N, Sakakibara H, Nimura Y. Analysis of blood flow on pulmonary hypertension with the pulsed Doppler flowmeter combined with cross-sectional echocardiography. Br Heart J 1984; 51:407-415. Kitabatake A, Inoue M, Asao M, et al. Noninvasive evaluation of pulmonary hypertension by a pulsed Doppler technique. Circulation 1983; 68:302-309. Kosturakis

D, Goldberg

SJ, Allen

HD,

Loeber C. Doppler echocardiographic prediction of pulmonary arterial hypertension in congenital heart disease. Am Cardiol 1984; 53:1110-1115. Posteraro RH, Sostman HD, Spritzer CE, Herfkens RJ. Cine-gradient-refocused MR imaging of central pulmonary emboli. AJR 1989; 152:465-468. Schiebler

M,

A.xel

So27.

28.

Tomogr

Sechtem

et al.

ciety

10.

Car-

pulmonary arterial system in disease. Circ Res 1971; 29:40-50. Greenfield JC, Griggs DM. Relation between pressure and diameter in main pulmonary artery of man. J AppI Physiol 1963; 18:557-559. Kirby BJ. Pulmonary artery compliance in pulmonary heart disease. Prog Resp Res

Assist

26.

of Magnetic Resonance Imaging fifth annual meeting program and abstracts. Magn Res Imag 1987; 5:48. Keren G, Meisner JS, Sherez J, Yellin EL, Laniado S. Interrelationship of mid-diastole mitral valve motion, pulmonary yenous flow, and transmitral flow. Circulation 1986; 74:36-44. Keren G, Sherez J, Megidish R, Levitt B, Laniado S. Pulmonary venous flow pattern: its relationship to cardiac events-a pulsed Doppler echocardiographic study. Circulation 1985; 71:1105-1112. Keren G, Bier A, Sherez J, Miura D, Keefe D, Lejemtel T. Atrial contraction is an important determinant of pulmonary yenous flow. J Am Coil Cardiol 1986; 7:693695. Pickoff AS, Bennett V. Soler P. Ferrer PL. Detection of pulmonary venous flow by

I.

L, Reicheck

N,

et al.

Correlation of cine MR imaging with twodimensional pulsed Doppler echocardiography in valvular insufficiency. J Comput

et al.

(abstr).

veins.

1979; 13:677-683. B, Bertram CD, Stallard T, Lee GD. Blood flow in pulmonary veins. III. Simultaneous measurements of their dimensions, intravascular pressure and flow. Cardiovasc Res 1979; 13:684-692.

1975;

A.xel

Lenkinski RE. Pulmonary vasculature: high-resolution MR imaging-work progress. Radiology 1989; 171:391-395.

9.

modality

17.

20.

T, Lee G

in pulmonary

and left sides of the heart.

16.

18.

in chil-

Studies in dogs and man. Cardiovasc Res 1979; 13:667-676. Rajagopalan B, Friend JA, Stallard T, Lee G de J. Blood flow in pulmonary veins. II. The influence of events transmitted from diovasc Res Rajagopalan

1985; 28:299-307.

H, Gefter

Blood flow

the right

19.

Lallemand D, Wesbey GE, Gooding CA. Cardiosynchronous MRI intensity changes of the great vessels and pulmonary circulation: a preliminary report.

Cine MR determination of left ventricular ejection fraction. AJR 1987; 148:839-843. Evans AJ, Herfkens RJ, Hedlund LW, Blinder R, Fram EK, Utz JA. Evaluation of pulsatile flow using limited flip angles

The

of being completely and tomographic and

15.

tions.

Utz

circulation.

the advantages noninvasive

de J.

as-

8.

monary

14.

pulsed Doppler echocardiography dren. Am Heart J 1983; 105:826. Rajagopalan B, Friend JA, Stallard

1987;

11:627-632.

U, Pflugfelder

Mitral

PW,

or aortic

Cassidy

regurgitation:

MM,

quan-

tification of regurgitant volumes with cine MR imaging. Radiology 1988; 167:425-430. Simons MA, Gullberg GT, Wehrli FW. Slab reformation of vascular images using gradient refocusing for high vessel contrast: work in progress (abstr). In: Book of abstracts: Society of Magnetic Resonance in Medicine 1987. Vol ?. Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1987; 42. Evans

AJ,

Herfkens

FJ,

Spnitzer

CE,

Blind-

er RA, Frame EK, Hedlund LW. The effect of turbulent flow on MRI signal intensity

29.

using

gradient

refocused

echoes

(abstr). In: Book of abstracts: Society of Magnetic Resonance in Medicine 1987. Vol 1 . Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1987; 354. Bradley WG, Waluch W. Blood flow: magnetic resonance imaging. Radiology 1985; 154:443-450.

Radiology

#{149} 769

30.

Fram E, Hedlund L, Dimick R, Glover G, Herfkens R. Parameters determining the signal of flowing fluid in gradient refocused imaging: flow velocity, TR, and flip-angle (abstr). In: Book of abstracts: Society

of Magnetic

1986. Vol Magnetic

Resonance

1. Berkeley, Resonance

in

35.

Gao

J, Holland

tion

of blood

5K, Gore JC. flow

NMR

37.

strength

in

Society

Medicine Magnetic

of Magnetic

Resonance

1988. Berkeley, Calif: Resonance in Medicine,

34.

Society

DN,

Nayler

GL,

Klipstein

38.

in

Society of 1988; RH,

Nayler

GL,

flow

I

Firmin

imaging Comput

DN,

Longmore

A, Glover

(abstr). Vol

GH.

In: Book

of Magnetic

1989.

Lee

151-155.

MR

Phase

of ab-

Resonance

1. Berkeley.

in

Calif:

system.

AJR

1987;

42.

So-

ciety of Magnetic Resonance in Medicine, 1989; 101. Rzedzian RR, Pykett IL. Instant images the human heart using a new, whole-body

Shimizu Visualization

tive

analysis

of blood

flow

Radiology

T, et al. quantita-

velocity

43.

44.

using

1986; 159:195-

In

39.

Wehrli

HI.

FW,

Listerud

A cine bolus

quantitation of flow in arteries stracts: Society Medicine 1989.

DB.

by cine magnetic resAssist Tomogr 1986;

flow velocity and volume (abstr). In: Book of abof Magnetic Resonance in Vol 1. Berkeley, Calif: So-

10:715-722.

ciety

IP, Ross J, Mintz GS. Effect of sampling site on assessment of pulmonary artery blood flow by doppler echocardiography. Amer J Cardiol 1986; 58:1145-1147.

1989; 100. Edelman RR, Mattle MS. Quantification

Panidis

40.

dynamic bolus

of Magnetic

MR tracking.

J, Chao P. Goldberg tracking technique for

Resonance

in Medicine,

HP, Kleefield of blood flow

imaging Radiology

and

45.

Clin

North

Am

1988;

Mazer MJ, Carroll FE, Falke cal aspects of gated magnetic imaging

199.

Un-

Hernandez RJ, Bank ER, Shaffer EM, Snider AR, Rosenthal A. Comparative evaluation of the pulmonary arteries in patients with right ventricular outflow tract obstructive lesions. AJR 1987; 148:1189-1194. Reed JD, Soulen RL. Cardiovascular MRI: current role in patient management. Radiol

of

149:245-

K, Matsuda T, Sakurai of moving fluid:

MR imaging.

Firmin

Blood onance.

cine

41.

ultra-

250.

derwood SR. Rees RSO, Longmore DB. vivo validation of MR velocity imaging. Comput Assist Tomogr 1987; 11:751-756. 33.

1982;

MR imaging

126. 32.

Doppler Philadelphia:

Shimakawa

Medicine

spoiled and refocused FLASH sequence work in progress (abstr). In: Book of abstracts:

NJ,

stracts:

Determina-

signal

Pelc

contract

of 1986;

BA.

in cardiography.

& Febiger, 36.

84-85.

31.

L, Angelsom

sound

Medicine

Calif: Society in Medicine,

Hatle

of the

pulmonary

Imag 1988; 3:73-84. Gefter WB, Palevsky

26:589-606.

THM. Practiresonance artery.

HI, Dinsmore

J Thorac BJ, Rei-

chek N, de Roos A, Kressel HY. Identification of chronic thromboembolic pulmonary hypertension with MR imaging (abstr). Radiology 1988; 169(P):218. Dinsmore BJ, Gefter WB, de Roos A, et al. Cine MR in the evaluation of pulmonary vascular abnormalities (abstr). In: Book of abstracts: Society of Magnetic Resonance in Medicine 1988. Vol 2. Berkeley, Calif: Society of Magnetic Resonance in Medicine, 1988; 805.

J, Silver with

presaturation 1989;

171:551-

556.

770

#{149} Radiology

September

1990