Peter

M. T. Pattynama, E. van der Wall,

Ernst

MD MD

Luuk Albert

#{149} #{149}

Early Diagnosis Imaging ofthe

the

entire

were

obtained.

mass

in patients

higher (61 g

±

g

±

than

7,

13

P

ventricle

mean

was

RV wall

significantly

that in healthy subjects [standard deviation] vs 47 .005),

=

right

The

while

the

ejection

fraction was in the normal range in both groups. Interobserver agreement for measurements of both RV ejection fraction and RV wall mass was high (r = .91 for both). When a 60-g cutoff point was used to define RV hypertrophy, eight patients were considered to have cor pulmonale, which had been previously defined, on dinical grounds, in only five of these patients. It is concluded that detection of RV myocardial hypertrophy with MR imaging may aid in the early diagnosis

ing

of cor

chronic

pulmonale

complicat-

obstructive

lung

disease.

E

VALUATION

the heart for management tive pulmonary is known

1992;

182:375-379

I From the Departments of Diagnostic ogy, (P.M.T.P., A.H.S., A.d.R.). Pulmonology (L.N.A.W.), and Cardiology (E.E.v.d.W.),

sity

Hospital

2333

AA

Leiden, Leiden,

C2-S,

The

RadiolUniver-

Rijnsburgerweg

Netherlands;

and

10, Interuni-

versity Cardiology Institute, Utrecht, The Netherlands (P.M.T.P., E.E.v.d.W., A.d.R.). Received June 24, 1991; revision requested July 24; revision

dress

received

reprint

© RSNA,

and

accepted

requests 1992

September

to P.M.T.P.

Annelies

H. Smit,

#{149}

5. Ad-

of the right ventricle of is clinically important of chronic obstrucdisease. This disease

to be complicated

by

the

treatment with supplemental oxygen has been shown to improve the prognosis in patients with cor pulmonale (4,5). Early diagnosis of con pulmonate may lead to more intensive treatment

of the

RV

stroke

of cor

pulmonale,

which

definition is RV hypertrophy, at an earlier stage than has been possible until now. MR imaging is a nonionizing modality

that

permits

the

acquisition of multiple tomographic images in planes oriented to intrinsic cardiac axes (9). Whenever transverse MR imaging completely encompasses the heart, it is essentially a three-dimensional imaging modality. Because of the

intrinsic

contrast

of the

blood

pool and the myocardial wall with MR imaging, endocardial borders of the myocardium are welt depicted. MR imaging has been shown to provide valid estimates of cardiac dimensions

and

function

(10-18).

To

mea-

sure the RV chamber dimensions and RV wall volume, we used an MR imaging protocol with multiple shortaxis imaging planes, 10 mm thick and lying 1 mm apart, which encomthe

left

and

right

ventricles.

The purpose of our study was to evaluate the usefulness of MR imaging for the quantitation of both RV hypertrophy and RV pump function in patients with mild chronic obstructive pulmonary disease. We used MR imaging to compare RV chamber votumes, ejection fractions, and watt masses

in patients

and

healthy

votun-

teers.

volume

and the RV end-diastolic volume. Reliable measurement of RV dimensions and ejection fractions by use of echocardiography, angiocardiography, and radionuclide studies has been difficult because of the complex geometry of the right ventricle (6,7). Recently, magnetic resonance (MR) imaging has been introduced for more accurate measurement of RV chamber dimensions and ejection fractions. Furthermore, with MR imaging, the volume of the muscular free wall of the right ventricle can be measured (8). In vivo assessment of RV hypertrophy might enable the diagnosis

MR

passed

at a time when at least some component is reversible and the prognosis might improve. For diagnosis of cor putmonale, the function of the right ventricle may be evaluated with measurement of the RV ejection fraction, which is defined ratio

MSc

with

development of con putmonale. The World Health Organization has defined con putmonale as right ventniculan (RV) hypertrophy secondary to diseases that affect the structure or function of the lungs (1). Because con pulmonale is a determinant of survivat in patients with chronic obstructive pulmonary disease, a noninvasive technique is needed to assess this disease during life and to study the effect of treatment (2,3). Long-term

as the Index terms: Heart, function, 5i.782 #{149} Heart, hypertrophy, 51.782 #{149} Heart, MR. 51.1214 Heart, ventricles, 51.788 #{149} Lung, diseases, 60.75 #{149}Magnetic resonance (MR), cine study

Radiology

MD

ofCor Pulmonale Right Ventricle’

Right ventricular (RV) wall volumes, chamber volumes, and RV ejection fractions were assessed by means of magnetic resonance (MR) imaging in 17 patients with moderate chronic obstructive lung disease and in 11 healthy subjects. Short-axis spinecho or gradient-echo images encompassing

N. A. Willems, de Roos, MD

simultaneous

SUBJECTS Study

AND

METHODS

Subjects

Eleven [64%]) 21-68

healthy with

a mean

years)

without

volunteers

(seven

age of 35 years a history

men (range,

of cardiac

or pulmonary disease, underwent MR imaging, as did 17 patients with chronic obstructive lung disease (11 men [65%]) with

a mean

age of

62 years

(range,

36-90

years). Ten patients had lung emphysema, defined by means of clinical examination, chest radiographs, and lung function parameters. Mean forced expiratory volume

in

1

second

(FEy1) after bronchodilation

by Abbreviations:

FEV = forced expiratory volume in 1 second, Paco. = arterial partial pressure of carbon dioxide, Pao, = arterial partial pressure of oxygen, RV = right ventricular, SD = standard deviation, SE = spin echo. 375

was

49%

predicted;

to vital 56%

after

predicted.

ide

kPa

mean for

pressure (range,

partial

(Paco2)

was

hemoglobin were slightly mean ante-

kPa

and

heart.

All

ble during

of tricuspid and patients

patients

our

of con

dioxide

4.2-6.8

nonpulmonary

kPa). insuffihad

disease were

study.

was

mean

of carbon (range,

Clinically, no signs ciency were present,

(Pao2)

kPa),

pressure

concomitant

was monox-

of oxygen

6.4-12.6 5.3

of FEy1

carbon

corrected

arterial

nosis

ratio

predicted. Patients but normocapnic;

rial partial

left

mean

bronchodilation

The

diffusion

was 58% hypoxemic 9.2

the

capacity

clinically

Clinically,

putmonale

no

of the

was

sta-

the diag-

defined

by

the

presence of a raised jugular venous pressure, an enlarged tender liven, hepatojugular reflux, edema of feet, ascites, cardiac

gallop,

and

graphic

the

presence

criteria

for

(These signs combinations sures

in the

artery

were

clinical

RV

in various data on pres-

ventricle

available

practice

or pulmonary

because

in our

of routine

institution.

No

cath-

Image

etenization of the night heart is performed in this type of patient with mild chronic obstructive

MR

pulmonary

disease.

MR

performed

with

examinations

net system (Gyroscan; Philips tems International, Da Best, lands), which was upgraded 1.5-T images

field strength were obtained

during with

echo

(SE) sequence

at 0.5 T on gradient-

recalled-echo

Echo and

cine

time

was

14 msec

MR

in cine

to

the study. All either a spin-

sequence

30 msec

Sys-

MR

sequences;

view

of 30

x 30 cm2.

A Fourier

tion

to a 256

x 256-pixel

was

applied.

Scout

in coronal the

and

position

position pulmonary

display

images

sagittat

of the

transforma-

planes

apex

of the ascending trunk, and

heart,

aorta the angle

imaging localizing rotation of

the

transverse

the

right

axis

the

patient.

mm,

with

The

heart

was

base

with

eight

plane

and

the

The an

1). Imaging

around

section

thickness

intersection

then

gap

imaged

on nine

was

the electrocardiogram spective cardiac

from

was

10

apex levels

use both

of proSE and

MR imaging. Time resolution was 70-80 msec for the SE sequence, which was adequate to isolate end systole and diastote

quence, Each

(19).

For

time

resolution

SE MR

examination

the

mately 45 minutes, and amination, approximately

376

#{149} Radiology

cine

was

MR

45-50

lasted

(Fig

end-diastolic

with

enclosed

areas

se-

of

the

end-diastolic

wall

RV

the

a corn-

and

end-

chamber.

end-diastolic

umes.

The

RV

ume

and

of the

to

values

of

were and

to one another rule to obtain

occasions A.H.S.) and

mass. The RV stroke as the difference

and

the

ratio

were by

of the

who

window

Statistical

stroke

volume. on

observers the same

level

vol-

was

performed

two used

volbe-

end-systolic fraction

to the end-diastolic

sunements

appnoxi-

Mean

two

vol-

All measeparate

(P.M.T.P., window

width

settings.

volumetric

terobserven

measurements

were agreement

were

relationships mass

between RV ejection

The

subjects (range,

yen-

subjects an unDifferat the in patients

and

RV

ejection

Pao2 and Paco, and befraction and Pao2 and

tested

used

for analysis. for

measurements

by

values

for

possible

correlation.

of RV volumes,

22).

In

tive

pulmonary

the

In-

wall

to normal based

patients

with

RV ejec-

wall mass subjects

mass

47 g ± 7 (mean g). These values

was 36-59

comparable lished reports

in are

in healthy ± SD) were

values in pubon autopsies (20chronic obstruc-

disease,

RV wall

mass

was significantly higher (6i g ± 13; range, 38-87 g; P = .005) (Fig 2a). In two patients the RV mass could not be measured because of suboptimat image quality. When a cutoff point of 60 g (23) was used, eight patients were considered to have con pulmonate. In only five of these eight patients (62%), the diagnosis of con putmonate had been defined on clinical grounds previously. RV ejection fractions did not statistically differ between patients and healthy tients,

Analysis

observers

wall

RV myocardial RV

measured The

in each section section thickness

ejection

as the

The

RV

tion fractions, and RV patients and in healthy presented in Table 1.

En-

bonders

factor an#{228}added to Simpson’s

tween

.05 level.

significant

night

RESULTS in were

and by

volume.

RV wall calculated

ejection

of the

considered

ex-

frames

measured

outlined

RV

were

Paco2

borders

cursor,

epicardiat

were

the

were

end-systolic

of the

and

wall

fat

were

volumes

=

end-sys-

volumes, mass

mass

wall

msec.

each cine MR ex30 minutes.

paired ences

P

wall

watt

the interventricu-

a trackball

to assess

systolic

in all RV

endocardial

and

outlined

were

time-frame

epicardiat

1). The

calculated

(Fig

cine

end

cluded

volume

Whenever

measured, and

to obtain ume was

to

to the R wave with for

gating

of

of I mm.

imaging

triggered

axis

usually

RV chamber and wall volumes. Total RV wall volume was multiplied by the specific density of the cardiac muscle (1.06 g/mL)

left-to-

antenoposterion

wall

sections.

was

septum

puten

RV

in the same

on nine

section according

tong axis of the heart. Short-axis planes were constructed with views by means of electronic

measured

images

volumes,

stroke

and

RV

regression

in patients and in healthy tested for differences with one-tailed Student t test.

tween

of the

area measurements multiplied by the

the

and the of the

were

end-diastolic

fractions,

surements

assess

to identify

of the

(end-sys-

volumes,

between fraction,

free

obtained

volumes

The

docardiat

image

were

minimal

and linear

End-diastolic

tolic

coincided with time-frame 1, the first timeframe after the R wave of the electrocandiogram. End-systolic images generally coincided with time-frame 4 on 5. Mea-

tar

tion time was equal to the RR interval of the electrocardiogram. All images were obtained with two signal averages. Raw MR imaging data were obtained by acquisition of a 128 x 128 matrix with a field of

and

ventricular

sight.

volume

repeti-

with

tricle were

(end-diastolic)

eight

at 1.5 T.

fractions

mat

performed

in SE sequences

ejection

determined

analysis.

by

mag-

Medical The Netherfrom 0.5-

of RV

For analysis, the images were displayed on a computer monitor in a movie-loop mode. The time-frames showing the maxitolic)

were

a superconducting

Analysis

was

Imaging

Multisection

b.

Figure 1. Measurements of RV myocardial volume from a short-axis plane in a patient with con pulmonale. Note tracing (b) of the endocardial and epicandial contours, with exclusion of the interventriculan septum and epicandial fat. In a and b, repetition time msec/echo time msec = 800/30. L = left.

hypentrophy.

may be present on alone.) No right

a.

of electrocardio-

subjects 57% ±

(mean value in pain healthy subjects, 58% ± 6%) (Fig 2b). RV endsystolic volumes did not differ between patients and healthy subjects. 12%;

February

1992

____________

80

1-

-

#{149}

:

mean

.i

80

#{149}

70

#{149}

C

.;

70

-

0

#{149} .

C,,

#{149}

Until now, the early diagnosis cor pulmonate has depended on detection of a lowered RV ejection fraction. Although assessment of RV ejection fraction is helpful to

of the

tablish

put-

(u

#{149}

.

60

-

60

-

.

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>

50-

#{149}#{149}. #{149}

40

-

30

.

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50

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-;#{149}-

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#{149}

#{149}

30 c0PD n=15

diagnosis

that

patients

were

clinically

COPD

normal

they

had

n=17

n=11

right nate. ings,

heart failure In accordance the patients

- _________________________

n=11

a.

early

b.

stable,

RV

ejection

though

on

the

60-g

hypentrophied

trophy

RV mass.

compatible chronic

with

value

patients

had

con pulmonale.

obstructive

cant difference limited

Eight

pulmonary

between

patients

for assessment

an

RV mass

of 60 g on greaten,

(b) Comparison disease

and

healthy

and

of RV ejection

in ii

subjects

healthy

indicating

fraction

RV hyper-

in 17 patients

subjects.

The

that

RV ejection

indicates

chronic

ob-

lack

of a signifi-

fraction

has

of con pulmonale.

it has

been

even though episodes of

due to con pulmowith these findin our study had

normal

for

with

experienced

2. (a) Comparison of RV wall mass (in grams) in 15 patients with chronic obstructive pulmonary disease (COPD in a and b) and in 11 healthy subjects. The mean RV mass is significantly higher in patients than in healthy subjects (P = .005). Dashed horizontal line marks the Figure

level

of con

structive pulmonary disease had normat RV ejection fractions when they

#{149}#{149}

normal

the

monale, improvement is still needed. A previous study by MacNee (6) has shown

#{149}#{149}#{149}

40

#{149}

with

the es-

#{149}#{149}

fractions,

average

right strongly

they

even had

a

ventricle.

Indeed,

suggested

that

even in a hypentrophied right ventnicle the RV ejection fraction is preserved until relatively late in the course of the disease (24,25). Therefore, detection of RV myocardiat hypertrophy is probably more important for early diagnosis of con pulmonale than determination of the RV ejection fraction. Because of its capability to measure RV wall mass in vivo for detection of myocardial hypertrophy, MR imaging can likely enable detection of con putmonale at an earlier stage than would be possible with measurements of the RV ejection fraction alone. Earlier diagnosis of con putmonate may lead to earlier treatment with supplementary oxygen, which, it is hoped, will improve the eventual prognosis in this condition (4,5).

On average, stolic volumes were

however, RV end-diaand stroke volumes

smatter

in patients

than

in

healthy subjects. Values of end-diastolic and end-systolic volumes in healthy subjects were similar to nonmat values reported in previous stud-

rived from SE images, which were used in six patients and six healthy subjects, and (b) values from cine MR studies

images,

patients

and

fraction

obtained

by

the

two

observ-

ers were y = 1.OOx 1.00 and y = 0.99x + 0.92, respectively (Fig 3). No statistically significant differences were found between (a) values de-

Volume

182

#{149} Number

2

were

healthy

used

in 11

subjects.

cause

DISCUSSION

ies (7,10).

In the group of patients, no significant correlation was found between RV watt mass and Pao2 or PaCO2 or between RV ejection fraction and Pao2 or PaCo2. In addition, no significant correlation was found between RV walt mass and ejection fraction or between wall mass and RV end-systotic volume (Table 2). Interobserver agreement was good, with a correlation coefficient of .91 for both RV ejection fraction and RV wall mass. Regression tines for measurements of RV mass and RV ejection

which

five

Our has

the

study

shows

potential

that to enable

MR imaging assessment

of RV myocandial hypertnophy in patients with chronic obstructive putmonary disease. A significantly larger RV myocardial mass was detected in patients with moderate chronic obstrucfive putmonary disease than in healthy subjects (61 g ± 13 vs 47 g ± 7 [P = .005]). When g, recommended

Echocandiography, angiocardiography, and radionuctide studies are the methods currently used to evaluate RV ejection fraction. The visualization of the right ventricle may be difficult with echocandiognaphy be-

a cutoff point by Thurlbeck

of 60 (23),

was used, eight patients were considered to have con pulmonale, which by definition is synonymous with RV hypertrophy (1). RV function in these patients, characterized by the RV ejection fraction derived from MR imaging, was within normal limits, with a mean value of 57%.

of its irregular

shape

(6,26).

Fur-

thermore, echocandiographic studies are dependent on operator skill, and in patients with chronic obstructive pulmonary disease, acoustic windows may

be unavailable

because

of inter-

position of lung tissue between the transducer and the heart (27). Angiocardiography has the advantage of providing direct pressure measurements of the pulmonary artery and the right ventricle but has the disadvantage of being an invasive procedune. Reproducibility in defining the ventricular silhouette may be difficult because of the trabeculations (28). A more fundamental problem in angiocardiography is that planar projection of a three-dimensional image is likely to reduce the accuracy of measurements

and

that

each

measurement

___2#linID/Lt32_P

‘7

can only be made for the part of the right ventricle that can be rotated

away

from

overlapping

tunes. Radionuclide has an advantage

not

know

cause

the

the

cardiac

ventniculognaphy in that one need

shape

of the

radiation

c’J U)

are

overlap

of these

U) U)

section

MR

dated

imaging

in studies

toms

and

have

been

vali-

wax

phan-

indicator

techniques eral studies

w

>

r= 0.91

40

n=

50 r= 0.91 n= 28

40

26 111

40

50

60

70

40

80

50

RV WALL MASS OBS1 (G)

a.

60

70

80

RVEF OBS1 (%) b.

Figure 3. (a) Intenobserven variation of RV wall mass measurements (in grams (C 1) in 26 subjects: 15 patients with chronic obstructive pulmonary disease and 11 healthy subjects. Regression line is y = 1.OOx - 1.00, with a correlation coefficient of .9i, which indicates good intenobserver agreement. In a and b, OBS1 = observer 1, OBS2 = observer 2. (b) Intenobserven variation of RV ejection fraction (RVEF) measurements in 28 subjects: 17 patients with chronic obstructive pulmonary disease and 1 1 healthy subjects. Regression line is y = 0.99x + 0.92, with a correlation coefficient of .91, which indicates good interobsenver agreement.

dilution

were have

measurements

Li-

50#{149}

structures

in which

70

0

60

-I -J

30

and therefore inaccurate values for the RV ejection fraction (13,30). RV ejection fractions measured with MR imaging are (in adherence to definition) calculated by dividing the stroke volume by the end-diastolic volume. Volume measurements of the right ventricle obtained with multi-

0.99x

+

U)

in di-

rect proportion to the cardiac chamber volumes (29). However, it may be difficult to separate the right atrium and pulmonary artery from the right ventricle; this difficulty results in considerable

.-

70

0

RV be-

counts

y= 0.92

80

y=1.OOx-1.OO

80

struc-

used (10,13,17). 5evshown that MR of the

stroke

volumes

of the right and left ventricles in an individual are equal; this finding is a measure of internal validation (7,13,17).

ejection in casts

Left

ventricular

volumes

fractions have and in studies

angiocandiognaphic,

and

been validated performed with echocandio-

graphic, nadionuclide, and indicator dilution methods (10-12,14-17). The general agreement is that volume estimations made with MR imaging are more accurate because they are independent of geometric assumptions. Thus, in addition to its potential to directly quantitate RV myocardiat hy-

had a normal mean ejection fraction and also a normal mean RV end-systolic volume. The relatively normal RV ejection fraction and the only

pentrophy,

slightly

MR

imaging

enables

more

accurate assessment of the RV ejection fraction. In a preliminary study, Turnbull et at (31) estimated RV mass in patients with severe chronic obstructive pulmonary disease by use of static MR imaging at a low field strength. In our study,

dynamic

MR

imaging

at higher

field strengths was used in patients with moderate chronic obstructive pulmonary disease, allowing the catculation of not only RV mass but also RV ejection fraction from the same imaging data. To test our method, we selected patients structive severe

with moderate chronic obpulmonary disease without hypoxemia. These patients

generally

have

fractions,

normal

normal mean

and

RV end-diastolic

mal

or slightly

elevated

RV ejection right

atrial

pressures,

mild

why

we

pulmonary

Pao2

disease did

not

in these

probably find

the

patients

explains correlation

between RV ejection fraction and anteniat blood gas partial pressures that has

been

described

in the

cardiopul-

monany literature (32). Possible disadvantages of MR imaging should be mentioned. Among the known conditions that pnectude MR imaging, claustrophobia may be especiatly important in dyspneic patients. Furthermore, we had the overall impression that image quality in dyspneic patients was tess optimal than in healthy subjects, possibty because of more tory movement

pronounced artifacts.

respiraIn two of the

patients, the RV myocardiat mass could not be measured because of unsatisfactory

nor-

artery pressures, and slightly elevated pulmonary vascular resistances at rest (25). Indeed, the patients in our study ___7RRadinloy...

lowered

with

image

quality,

although

RV ejection fraction could be measured. In healthy subjects all examinations were of satisfactory quality. It is hoped that, with technological developments, image quality will further

improve and imaging time wilt be shortened. We measured the RV mass according to the standard method used in pathology departments to separate the cardiac ventricles, excluding the interventriculan septum and epicardial fat (22). As stated previously, a cutoff point of 60 g was used to define con pulmonate. Three patients had an RV mass greater than 60 g without other evidence of con pulmonale, but we are not sure whether these findings should be considered true-positive. Of course, a fixed cutoff point of 60 g is arbitrary, and further study should precede its use in clinical practice. When we calculated index, which is RV mass

body tween was (P

the

RV

mass

corrected for surface area, the difference bepatients and healthy subjects

statistically more significant .003) than when we calculated RV mass (P = .005). In this study we did not age-match =

patients

and

autopsy

studies

correlation mass

show

(22). that

healthy have

between However, the heart

subjects

because

established

age

and

no

RV wall

autopsies did and its ventricles

February

1992

are

approximately

one-third

6.

heavier

in male than in female subjects (21,22). To avoid bias caused by genden, the patients and the healthy subjects in our study had similar sex dis-

tributions. In summary, we believe that MR imaging has the potential to become a useful modality with which to evatuate patients with chronic obstructive pulmonary disease. It enables the noninvasive early diagnosis of con pulmonate by measuring RV hypertrophy. Whenever con pulmonale is identified in early stages, such a diagnosis

might

lead

to more

tution

to evaluate

treatment

tients with chronic pulmonary disease con putmonale.

7.

8.

9.

10.

ii.

12.

13.

14.

by

U

15.

References 1.

World Health Organization. Chronic cor pulmonale: a report of the expert committee. Circulation 1963; 27:594-598.

2.

Renzetti ADJr, McClement The Veterans Administration study

of pulmonary

in relation

function.

to respiratory

16.

JH, Litt BD. cooperative function

in

chronic 3.

4.

obstructive pulmonary disease. Am J Med 1966; 41:115-129. Traver GA, Cline MG, Burrows B. Predictors of mortality in chronic obstructive pulmonany disease: a 15year follow-up study. Am Rev Respir Dis 1979; 119:895-902. Nocturnal Oxygen Therapy Trial Group. Continuous or nocturnal oxygen therapy in hypoxemic

chronic

ease: a clinical 93:391-398. 5.

MRC

Working

ary oxygen

trial.

obstructive

Ann

182

Med

18.

therapy

Long

#{149} Number

term

in chronic

chronic 1981;

2

domicili-

hypoxic

cor

bronchitis 1:681-685.

1988;

function 75(suppl

in

Right ventricular

Measurement

20.

Lamb D. ventricular

Recent

myocardial

21.

22.

mass

23.

24.

Effects

25.

26.

Tavel ME. Normal sounds and pulses: relationships between the various events. In: Tavel ME, ed. Clinical phonocardiography and external pulse recording. Chicago: Year Book, 1978; 51-54.

advances

and assessment of In: Dyke SD, ed.

in clinical

of pulmonary

pathology,

hypertension

performance

se-

on right

in chronic

bron-

chitis and emphysema. Prog Respir Res 1985; 20:108-1 16. McFadden ER Jr. Braunwald E. Chronic con pulmonale. In: Braunwaid E, ed. Heart disease: a textbook of cardiovascular medicine. 3d ed. Philadelphia: Saunders, 1988; 1602-1616. Mason DT, De Maria AN, Berman DS. Principles of non-invasive cardiac imaging.

In: Echocardiography York:

and nuclear

New

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