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Measurement of ventricular volumes by cine magnetic resonance imaging in complex congenital heart disease with morphologically abnormal ventricles
Congenital Heart Disease
Measurement of ventricular volumes by cine magnetic resonance imaging in complex congenital heart disease with morphologically abnormal ventricles Koichiro Niwa, MD, Mika Uchishiba, MD, Hiroyuki Aotsuka, MD, Kimimasa Tobita, MD, Koz0 Matsuo, MD, Tadashi Fujiwara, MD, Shigeru Tateno, MD, and Hiromichi Hamada, MD
Chiba, Japan
This study assessed the validity of cine magnetic resonance imaging (MRI) for measuring right and left ventricular volumes by using Simpson's rule in children with complex congenital heart disease. Forty-five patients with complex congenital heart disease (average age 2.6 years) and 10 controls (average age 2.3 years) were evaluated. The whole heart was encompassed by contiguous transverse sections. Ventricular volumes were calculated by adding luminal areas determined in each section at end diastole and end systole. End-diastolic and end-systolic volumes by MRI in both groups correlated well with those by ventriculography (r > 0.89). Comparison of the ejection fraction in both ventricles in both groups yielded a good correlation between MRI and ventriculography (r>0.67). MRI technique in both groups had low intraobserver and interobserver variation (<6%). Cine MRI provides a suitable noninvasive means of quantifying ventricular volume in children with complex congenital heart disease. (AM HEART J 1996;131:567-75,)
With the remarkable improvement of surgical results for complex congenital heart disease in recent years, it has become increasingly important to accurately evaluate ventricular volumes to develop a proper strategy for treating these patients. Complex congenital heart disease is sometimes associated with various anatomical abnormalities, malposition (dextrocardia, mesocardia, etc.), and malrotation of the heart. Therefore the validity of geometric formuFrom the Departments of Cardiology and Cardiovascular Surgery, Chiba Children's Hospital, and the Department of Pediatrics, School of Medicine, Chiba University. Received for publication March 31, 1995; accepted Aug 1, 1995. Reprint requests: Koichiro Niwa, MD, Department of Cardiology, Chiba Children's Hospital, 579-1 Hetacho, Midoriku, Chiba 266 Japan. Copyright © 1996 by Mosby-Year Book, Inc. 0002-8703/96/$5.00 + 0 4/1/68575
las to derive volumes 1-8 of right and left ventricles with various morphologic shapes, as in complex congenital heart disease, is problematic. There are some studies concerning the usefulness of magnetic resonance imaging (MRI) for diagnosing complex congenital heart disease. 9-1°However, there are few studies 11, 12 of measuring ventricular volumes in congenital heart disease with MRI. In contrast, application of MRI to evaluate myocardial function in adults or ventricular casts has been well described.13-23 In these studies, measuring ventricular volume was undertaken by either the spin-echo method or gradient recalled imaging technique. Numerous methods of calculating ventricular volumes such as the area-length method, 11, 15-17,19 modified Simpson's rule, 12 and true Simpson's rule, 14-16,18-24 have been reported. MRI can easily and noninvasively provide multiple tomographic sections of the entire ventricle in patients with ventricular and cardiac deformities. Therefore ventricular volumes can be calculated by summing the areas of the cavities in contiguous slices (Simpson's rule) without making geometric assumptions concerning ventricular shape, which lead to inaccurate assessment in complex congenital heart disease with morphologically abnormal ventricles. However, studies concerning the application of Simpson's rule to MRI for measuring ventricular volumes in patients with complex congenital heart disease are rare. This study assessed the validity and usefulness of cine MRI for measuring right and left ventricular volumes by using Simpson's rule in children with complex congenital heart disease and morphologically abnormal ventricles. 567
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Table I. Diagnoses of 45 patients and 10 controls Diagnosis
Fig. 1. Right and left ventricular cavity are shown in coronal image to divide chamber into six axial segments to calculate volumes by Simpson's rule. Representative slice, 7 mm thick.
METHODS Patients. The study population included 45 patients with various types of complex congenital heart disease (group A, range 4 months to 8 years, average age 2.6 years) and 10 control patients (group B, range 1 to 5 years, average age 2.3 years) who were hospitalized between January 1991 and June 1994. Diagnoses of the 45 patients and the 10 control patients are listed in Table I. The study was approved by our hospital's Review Board, and the parents of all patients gave written informed consent for the angiographies and the MRI. MRI. Imaging was performed with a commercially available superconducting magnet operating at 0.5 tesla (General Electric Resona System). Images were obtained by the GRASS method (gradient-recalled acquisition in steady state), which uses a low flip angle of 30 degrees and an echo time of 20 msec. The repetition time was 50 to 60 msec. The acquisition matrix was 128 × 256 or 128 x 128 or lower, and the field of view was 25 x 25 cm or 20 × 20 cm. Heart phase interval was 65 msec. A coronal image was obtained from each patient by using a gated spin-echo technique to localize transaxial cine MRI. Cine MRI was then obtained for the entire heart from the apex to the most caudal portion of the ventricle. Images of the entire right and left ventricles were taken in all patients. In each patient, six different scans (one slice for each scan) were needed to calculate volumes. Therefore, slice thickness was 5, 7, or 10 mm without gap according to the ventricular cephalocaudal length (Fig. 1). All axial images were reconstructed at 9 to 13 frames for a cardiac cycle (varied with patient's heart rate) and displayed in a dynamic fashion (Fig. 2). The largest and smallest blood pool images were visually chosen for each slice of right and left ventricles and were taken as end diastole and end systole. For each image, a region of interest was then manually traced, excluding papillary muscles and large trabeculations of the right ventricle, for
Tetralogy of Fallot Tetralogy of Fallot, pulmonary atresia Corrected TGA, VSD, pulmonary atresia Double-outlet right ventricle Pure pulmonary atresia Single right ventricle Single left ventricle Tricuspid atresia Complete TGA Aortic atresia TOTAL Kawasaki disease with regression of the coronary artery aneurysm with anatomically normal ventricles TOTAL
No.
7 2 5 5 7 9 3 4 2 45 10 10
TGA, Transposition of the great arteries; VSD, ventricular septal defect.
the right and left ventricular blood pool on the transaxial plane. The number of image voxels within this region of interest was determined by the computer, and blood pool volume per slice could be calculated by multiplying this number by voxel size (Fig. 3). The end-diastolic and endsystolic volumes of all slices were then added to determine total right and left ventricular end-diastolic volume and end-systolic volume (Simpson's rule). We used a cylindric head coil with an aperture of 30 x 30 cm. All patients except one were sedated with oral monosodium trichlorethyl phosphate (80 mg/kg of body weight). The patients were monitored by pulse oximeter (Biox 3700, Omeda, Boulder, Colo.) in the MRI control room, and the monitoring line was shielded from the magnetic field. For infants, blankets and towels were used to prevent heat loss during examination. The patients did not take anything orally from two hours before the examination. In patients with single left ventricle with rudimentary chamber, we traced the biventricular cavity, excluding the interventricular septum. We counted the number of ventricles in single left ventricle with rudimentary chamber as one left ventricle. In single right ventricle, we counted the number of ventricles as one right ventricle. In patients with pure pulmonary atresia and tricuspid atresia with an extremely tiny right ventricular cavity, we could assessed left ventricle only. Thus there were 39 right ventricles and 35 left ventricles in this study. Yentriculography. Right and left ventricular volume determinations were performed from biplane cineangiographies obtained during routine diagnostic cardiac catheterization in all patients in this study. Biplane ventriculography was performed with 5F to 6F Bermann angiographic catheter at 50 frames per second (KXO-2050, Toshiba Inc., Tokyo, Japan). For calibration, a grid of 1 cm x 1 cm fine steel wire enbedded in Plexiglass was filmed perpendicular to the anteroposterior and lateral radiograph tubes at the exact position that the left or right ventricle had been during the ventriculography. 2' 6 Ventricu-
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Fig. 2. Tetralogy of Fallot with pulmonary atresia in 1-year-old girl. Transaxial plane. Third slice from caudal of ventricular segment in Fig. 1. Nine alternate frames from 14-image set of cine MRI, equally spaced within one cardiac cycle showing contraction of right and left ventricles. Diastole occurred in top left image, and systole occurred in middle right image.
lographies were traced by a single observer who took care to avoid post-ectopic beats. The ventriculographies were considered satisfactory for biplane volume analysis only if there were three consecutive, opacified sinus beats. The third beat was used for volume analysis. End systole was chosen as the smallest ventricular silhouette when the atrioventricular valve was closed. End diastole was chosen as the frame with the largest ventricular silhouette. The tracings were digitized with an NEC 9801 Desktop computer interfaced with an X-Y plotter and progTammed to calculate the ventricular volume with modifled Simpson's rule according to the method of Chapman and Graham 4-6 with the regression equation by Graham.2, 6 All patients were intravenously sedated with pethidine hydrochloride (1 mg/kg), and diazepam (0.5 rag/ kg). The patients did not take anything orally from three hours before the examination. Ventriculography was performed within 2 days after MRI. Data from these two modalities were evaluated prospectively by different observers who had no knowledge of the results of the other studies. Reproducibility. To determine the interobserver error
for MRI, volumes were analyzed by a further independent investigator. To determine intraobserver error for both techniques, studies were reanalyzed by the same observer after at least 3 months, with the observer blind to the original results. Statistics. MRI volumes and ventriculographic volumes were compared by linear regression analysis. Similarly, intraobserver variation and interobserver variation were analyzed with linear regression analysis of paired data from each patient. In addition, the mean and SD of paired differences ([measurement 1 - measurement 2]/Mean of the two measurements) between measurements by the two observers and the two measurements of one of the two observers were calculated as a measure of individual variability.
RESULTS Analysis time. All 45 patient studies were evalu-
ated. Mean acquisition and reconstruction times were 48 minutes, group A, and 45 minutes, group B. Regression data of ventricular volumes. Regression
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Fig. 3. Same patient as in Fig. 1. Single image from 14-image series at end diastole (A) and end systole (C). Sharp border between blood pool and left and right ventricular myocardium in top image. RV, right ventricle; LV, left ventricle. Region of interest outlined for determining slice volume at end diastole (B) and end systole D. Large papillary muscle of RV and normal-sized papillary muscle of LV were excluded from volume calculation.
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Fig. 4. Regression line between MRI and angiographically measured right ventricular volume in group A. End-diastolic volume (EDV) on left, end-systolic volume (ESV) on right. RVG, right ventriculography; SEE, standard error of estimate. data for MRI versus angiography in group A are shown in Figs. 4, 5, and 6. End-diastolic volume and end-systolic volume in both ventricles in group A by MRI correlated well with but appeared to underestimate the volume by angiography (r > 0.89). Ejection fraction in left ventricles in group A by MRI correlated well with the ejection fraction by angiography (r = 0.84). Similarly, ejection fraction in the right ventricle in group A by MRI correlated well with t h a t
by angiography, but it appeared to be a lower correlation t h a n for the left ventricle (r = 0.67). Regression data for MRI versus angiography in group B are shown in Figs. 7, 8, and 9. End-diastolic volume and end-systolic volume in both ventricles in group B by MRI correlated well with but appeared to underestimate the volume by angiography (r > 0.91). Ejection fraction in both ventricles in group B by MRI correlated well with the fraction by angiography (r > 0.73).
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Reproducibility. Regression data between the two observers and the repeat MRI studies are shown in Table II. The correlation coefficients for the repeat MRI studies as measured by a single observer (intraobserver variation) in end-diastolic and endsystolic volumes in both ventricles in both groups were more t h a n 0.95. The correlation coefficients between the two observers (interobserver variation) for end-diastolic and end-systolic volumes in both ventricles in both groups were more t han 0.92. The interstudy percent variabilities and standard deviations are shown in Table III. In both groups, end-diastolic volumes, end-systolic volumes, and ejection fraction showed little variability. The m ean coeffi-
cient of variation was less t han 6% for all volumes in both groups.
DISCUSSION Various meansfor evaluatingventricularvolumes in children. Currently, the most common means of measuring ventricular volumes in children are right and left ventriculography and echocardiography. However, these modalities have some limitations in pediatric cases. Ventriculography provides good delineation of the right and left ventricular cavities with high temporal resolution. The calculation methods employed for biventricular volumes (area-length method, 1, 3 mod-
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Fig. 8. Regression line between MRI and angiographically measured left ventricular volume in group B. End-diastolic volume (EDV) on left, end-systolic volume (ESV) on right. ified Simpson's method, etc., 4.s however, rely on geometric assumptions concerning the shape of the right and left ventricle by using a regression equation that leads to inaccurate assessment in patients with complex congenital heart disease and morphologically abnormal ventricles. In addition, the examination is invasive and involves radiation exposure. Therefore applying ventriculography for routine monitoring of cardiac function is impractical. Twodimensional echo has been widely used to evaluate left ventricular volume in children. 25 However, it is frequently difficult to obtain images of the entire right ventricle. 26 Visualizing the entire right and left ventricles in complex congenital heart disease is more difficult, especially when associated with malrotation, malposition, or severe deformity of the
heart. Furthermore, it is also thought to be difficult to make proper simple geometric assumptions for calculating deformed right and left ventricles such as those in complex congenital heart disease. Therefore there have been few reports of measuring the ventricular volumes in patients with complex congenital heart disease. Gated blood-pool scintigraphy is an accurate means of determining left ventricular volumes and is relatively independent of geometric assumptions. 27 The technique is noninvasive and requires minimal exposure to radiation. But spatial resolution, especially in infants and small children, is sometimes poor or limited; in addition, the atrial blood pool cannot be clearly separated from the ventricu]ar region Of interest. 27 Computed tomography with Simpson's rule has been validated in a canine
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Fig. 9. Regression line between MRI and angiographically measured right and left ventricular ejection fraction (RVEF and LVEF, respectively) in group B. Table II. Intraobserver and interobserver correlations Group A RVEDV RVESV RVEF LVEDV LVESV LVEF
Intra r r r r r r
= = = = = =
0.97 0.96 0.73 0.98 0.95 0.73
(5.4) (3.5) (0.1) (5.1) (4.2) (0.1)
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= = = = = =
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Group B
0.95 0.94 0.69 0.97 0.94 0.79
RVEDV RVESV RVEF LVEDV LVESV LVEF
(7.1) (4.3) (0.1) (6.4) (4.6) (0.1)
Intra r r r r r r
= = = = = =
0.95 0.95 0.90 0.96 0.95 0.72
(4.4) (2.5) (0.1) (5.9) (2.6) (0.1)
Inter r r r r r r
= = = = = =
0.93 0.92 0.80 0.94 0.92 0.76
(5.2) (3.1) (0.1) (6.9) (3.2) (0.1)
RVEDV, Right ventricular end-diastolic volume; RVESV, right ventricular end-systolic volume; RVEF, right ventricular ejection fraction; LVEDV, left yentricular end-diastolic volume; LVESV, left ventricular end-systolic volume; LVEF, left ventricular ejection fraction; r, correlation coefficient (standard error of the estimate).
Table III. Intraobserver and interobserver percentage variability Group A RVEDV RVESV RVEF LVEDV LVESV LVEF
Intra 4.0 4.6 2.9 3.3 5.4 5.i
(4.7) (5.7) (3.8) (3.7) (6.1) (7.5)
Inter 5.4 5.4 4.2 4.5 6.7 4.1
(6.1) (6.1) (3.5) (5.0) (7.3) (6.0)
Group B RVEDV RVESV RVEF LVEDV LVESV LVEF
Intra 2.4 3.1 2.2 3.1 4.5 4.2
(2.8) (3.4) (3.2) (3.4) (5.3) (5.3)
Inter 4.1 4.5 3.0 5.6 7.5 1.8
(3.5) (5.0) (2.4) (6.4) (3.0) (2.5)
Abbreviations as in Table II.
model for assessing left and right ventricular volume. 2s However, this technique requires injection of radiopaque contrast medium and uses ionizing radiation. Therefore applying these examinations for routine evaluation of biventricular function in complex congenital heart disease is impractical. Cine MRI for evaluating ventricular volumes in children. It is reported t h a t singie-plane measurements of left ventricular volume by MRI can be made accu~'ately and are sufficient for routine clinical use except in patients with a pronounced wall motion
abnormality.16, 19 It is also reported t h a t comparisons of the left ventricular volume, measured by MRI with the area-length method 11 and modified Simpson's rule, 12 yielded a high correlation between MRI and ventriculography in children with simple congenital heart disease. However, when applying these methods to calculate ventricular volume, geometrical assumptions are required. Therefore these methods are thought to be inaccurate when measuring morphologically abnormal ventricles such as those in complex congenital heart disease. By using MRI, we
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can calculate right and left ventricular volumes by adding the areas of the cavities in contiguous slices without making geometric assumptions concerning the ventricular shape and without a regression equation for the papillary muscles. MRI is therefore a suitable modality for measuring ventricular volumes with Simpson's rule. Previous MRI studies concerning ventricular volume measurement in a cardiac cast reported that correlation between the actual cast volume and the calculated volume by MRI was excellent. 14, 22, 24 Comparing the ventricular volumes in adult patients with normally structured ventricles yields a good correlation between MRI and ventriculography has also been reported.15, 16, 19-22Furthermore, the correlation of the calculated right and left ventricular volumes between cine MRI and ventriculography in control patients was good in this study. From the findings of these studies, the measurement of biventricular volumes in patients with morphologically n o r m a l ventricles by cine MRI with Simpson's rule is thought to be methodologically reliable. Cine MRI for evaluating ventricular volumes in complex congenital heart disease. By summing up the vol-
umes of ventricular cavity intersections (Simpson's rule) as previously cited, we could calculate right and left ventricular volumes in patients with severely deformed ventricles and normally structured ventricles in the same fashion. 14, 22, 24 In this study, the correlations between cine MRI and ventriculography in measurements of right and left ventricular volumes in control patients and patients with complex congenital heart disease were excellent. Furthermore, MRI technique in both groups in this study had low intraobserver and interobserver variations. Semelka 23 indicated that cine MRI has a high interstudy reproducibility and is therefore suitable for sequential studies even in patients with morphologically abnormal ventricles. From these findings and reports, right and left ventricular volumes in patients with complex congenital heart disease and abnormal ventricle are thought to be measured accurately by cine MRI with Simpson's rule. Furthermore, different from measuring ventricular volumes by echocardiography and ventriculography, we can calculate the right and left ventricular volume simultaneously from the same contiguous slices by cine MRI with Simpson's rule. Furthermore, highly complicated complex congenital heart disease such as heterotaxia could be easily and accurately diagnosed by MRIg, 10 Therefore the whole ventricular cavity in complex congenital heart disease with morphologically abnormal ventricles is easily visualized by MRI. Advantage of cine mode MRI. The major advantages
of cine MRI are the much shorter acquisition times and the increased time resolution from many frames or phases within the cardiac cycle. For calculating ventricular volume in complex congenital heart disease, cine MRI is therefore thought to be superior to spin-echo sequence. Proper slices for calculating ventricular volumes in complex congenital heart disease by MRI. Tt has been
postulated that the assessment of left ventricular geometry and function is more accurate on the short axis than on a transverse imaging plane because angulation errors and partial volume effects can be minimized on a short-axis plane. 29 Buser et al. 21 reported that left ventricular volume m e a s u r e m e n t s obtained with cine MRI by Simpson's rule in a transverse and short-axis imaging plane were nearly identical, and they speculated that partial volume effect might have similarly affected both transverse and short-axis volume measurement. In a transverse imaging plane, it is easy to visualize the cardiovascular anomalies, the sites of atrioventricular and semilunar valves, and the whole ventricular cavity in complex congenital heart disease. 9, 10 In this study, we could easily visualize the proper slices for measuring ventricular volumes on a transverse image. Furthermore, ventricular volumes in both groups by MRI correlated well with those by ventriculography. Therefore for calculating ventricular volumes in complex congenital heart disease, transverse image is thought to be useful. Analysis time. We could reduce the examination time by using a small matrix size (128 x 128 or smaller); in this study, however, we thought that the imaging time was still too long for routine clinical use. However, in the near future, this disadvantage will be overcome by u s i n g ultrafast MRI, which is faster than the apparatus currently available. 3° Conclusion. By using cine MRI with Simpson's rule, the right and left ventricular volumes in complex congenital heart disease can be easily evaluated. Furthermore, the ventricular volumes obtained are independent of geometric assumptions and may be more accurate than ventriculography in complex congenital heart disease with morphologically abnormal ventricles. Measuring biventricular volumes in complex congenital heart disease with this method is a promising modality in conjunction with the development of ultrafast MRI.
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17. Buckwalter KA, Aisen AM, Dilworth LE, Mancini GBJ, Buda AJ. Gated cardiac MRI: ejection-fraction determination using the right anterior oblique view. AJR 1986;147:33-7. 18. Rher RB, Malloy CR, Filipchuk NG, Peshock RM. Left ventricular volumes measured by MR imaging. Radiology 1985;156:717-9. 19. Cranny GB, Lotan CS, Dean L, Baxley W, Bouchard A, Pohost GM. Left ventricular volume measurement using cardiac axis nuclear magnetic resonance imaging, validation by calibrated ventricular angiography. Circulation 1990;82:154-63. 20. Utz JA, Herfkens RJ, Heinsimer JA, Bashore T, CaliffR, Glover G, Pelc N, Shimakawa A. Cine MR determination of left ventricular ejection fraction. AJR 1987;148:839-43. 21. Buser PT, Auffermann W, Holt WW, Wagner S, Kirchner B, Wolfe C, Higgins CB. Noninvasive evaluation of global left ventricular fimction with use of cine nuclear magnetic resonance. J Am Cell Cardiol 1989; 6:1924-30. 22. Sechtem U, Pflugfelder PW, Gould RG, Cassidy MM, Higgins CB. Measurement of right and left ventricular volumes in healthy individuals with cine MR imaging. Radiology 1987;163:697-702. 23. Semelka RC, Tomei E, Wagner S, Mayo J, Caputo G, O'Sullivan M, Parmley WW, Chatterjee K, Wolfe C, Higgins CB. Interstudy reproducibility of dimensional and functional measurement between cine magnetic resonance studies in the morphologically abnormal left ventricle. AM HEARTJ 1990;119:1367-73. 24. Watanabe M, Hosoda Y, Longmore DB. Left and right ventricular dimensions and functions measured by ECG-gated NMR cardiac imaging. J Cardiography 1986;16:343-52. 25. Silverman NH, Ports TA, Sulder R, Schiller NB, Carlsson E, Heilbron DC. Determination of left ventricular volume in children: echocardiographic and angiographic comparisons. Circulation 1980;62:548-57. 26. Silverman NH, Hudson S. Evaluation of right ventricular volume and ejection fraction in children by two-dimensional ecbocardiography. Pediatr Cardiol 1984;4:197-204. 27. Parrish M, Graham T, Born M, Jones J. Radionuclide evaluation of right and left ventricular function in children: validation of methodology. Am J Cardiol 1982;49:1241-7. 28. Reiter SJ, Rumberger JA, Fefring AJ, Stanford W, Marcus ML. Precision of measurements of right and left ventricular volume by cine computed tomography. Circulation 1986;74:890-900. 29. Kaul S, Wismer GL, Brady TJ, Weyman AE, Okada RD, Dinsmore RE. Measurement of noITaal left heart dimensions using optimally oriented MR images. AJR 1986;146:75-9. 30. Matsumura K, Haiyama T, Takeo K, Shimizu K, Yamasaki K, Kohno K. Determination of cardiac ejection fraction and left ventricular volume: contrast-enhanced ultrafast cine-MR imaging vs IV digital subtraction ventriculegraphy. AJR 1993;160:979-85.
AVAILABILITY OF JOURNAL BACK ISSUES As a service to our subscribers, copies of back issues of the AMERICAN HEART JOURNAL for the preceding 5 years are maintained and are available for purchase from the publisher, Mosby, at a cost of $11.00 per issue. The following quantity discounts are available: 25% off on quantities of 12 to 23, and one-third off on quantities of 24 or more. Please write to Mosby-Year Book, Inc., Subscription Services, 11830 Westline Industrial Drive, St. Louis, MO 63146-3318, or call (800)453-4351 or (314)453-4351 for information on availability of particular issues. If unavailable from the publisher, photocopies of complete issues are available from University Microfilms International, 300 N. Zeeb Rd., Ann Arbor, MI 48106, (313)761-4700.
Measurement of ventricular volumes by cine magnetic resonance imaging in complex congenital heart disease with morphologically abnormal ventricles Koichiro Niwa, MD, Mika Uchishiba, MD, Hiroyuki Aotsuka, MD, Kimimasa Tobita, MD, Koz0 Matsuo, MD, Tadashi Fujiwara, MD, Shigeru Tateno, MD, and Hiromichi Hamada, MD
Chiba, Japan
This study assessed the validity of cine magnetic resonance imaging (MRI) for measuring right and left ventricular volumes by using Simpson's rule in children with complex congenital heart disease. Forty-five patients with complex congenital heart disease (average age 2.6 years) and 10 controls (average age 2.3 years) were evaluated. The whole heart was encompassed by contiguous transverse sections. Ventricular volumes were calculated by adding luminal areas determined in each section at end diastole and end systole. End-diastolic and end-systolic volumes by MRI in both groups correlated well with those by ventriculography (r > 0.89). Comparison of the ejection fraction in both ventricles in both groups yielded a good correlation between MRI and ventriculography (r>0.67). MRI technique in both groups had low intraobserver and interobserver variation (<6%). Cine MRI provides a suitable noninvasive means of quantifying ventricular volume in children with complex congenital heart disease. (AM HEART J 1996;131:567-75,)
With the remarkable improvement of surgical results for complex congenital heart disease in recent years, it has become increasingly important to accurately evaluate ventricular volumes to develop a proper strategy for treating these patients. Complex congenital heart disease is sometimes associated with various anatomical abnormalities, malposition (dextrocardia, mesocardia, etc.), and malrotation of the heart. Therefore the validity of geometric formuFrom the Departments of Cardiology and Cardiovascular Surgery, Chiba Children's Hospital, and the Department of Pediatrics, School of Medicine, Chiba University. Received for publication March 31, 1995; accepted Aug 1, 1995. Reprint requests: Koichiro Niwa, MD, Department of Cardiology, Chiba Children's Hospital, 579-1 Hetacho, Midoriku, Chiba 266 Japan. Copyright © 1996 by Mosby-Year Book, Inc. 0002-8703/96/$5.00 + 0 4/1/68575
las to derive volumes 1-8 of right and left ventricles with various morphologic shapes, as in complex congenital heart disease, is problematic. There are some studies concerning the usefulness of magnetic resonance imaging (MRI) for diagnosing complex congenital heart disease. 9-1°However, there are few studies 11, 12 of measuring ventricular volumes in congenital heart disease with MRI. In contrast, application of MRI to evaluate myocardial function in adults or ventricular casts has been well described.13-23 In these studies, measuring ventricular volume was undertaken by either the spin-echo method or gradient recalled imaging technique. Numerous methods of calculating ventricular volumes such as the area-length method, 11, 15-17,19 modified Simpson's rule, 12 and true Simpson's rule, 14-16,18-24 have been reported. MRI can easily and noninvasively provide multiple tomographic sections of the entire ventricle in patients with ventricular and cardiac deformities. Therefore ventricular volumes can be calculated by summing the areas of the cavities in contiguous slices (Simpson's rule) without making geometric assumptions concerning ventricular shape, which lead to inaccurate assessment in complex congenital heart disease with morphologically abnormal ventricles. However, studies concerning the application of Simpson's rule to MRI for measuring ventricular volumes in patients with complex congenital heart disease are rare. This study assessed the validity and usefulness of cine MRI for measuring right and left ventricular volumes by using Simpson's rule in children with complex congenital heart disease and morphologically abnormal ventricles. 567
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Table I. Diagnoses of 45 patients and 10 controls Diagnosis
Fig. 1. Right and left ventricular cavity are shown in coronal image to divide chamber into six axial segments to calculate volumes by Simpson's rule. Representative slice, 7 mm thick.
METHODS Patients. The study population included 45 patients with various types of complex congenital heart disease (group A, range 4 months to 8 years, average age 2.6 years) and 10 control patients (group B, range 1 to 5 years, average age 2.3 years) who were hospitalized between January 1991 and June 1994. Diagnoses of the 45 patients and the 10 control patients are listed in Table I. The study was approved by our hospital's Review Board, and the parents of all patients gave written informed consent for the angiographies and the MRI. MRI. Imaging was performed with a commercially available superconducting magnet operating at 0.5 tesla (General Electric Resona System). Images were obtained by the GRASS method (gradient-recalled acquisition in steady state), which uses a low flip angle of 30 degrees and an echo time of 20 msec. The repetition time was 50 to 60 msec. The acquisition matrix was 128 × 256 or 128 x 128 or lower, and the field of view was 25 x 25 cm or 20 × 20 cm. Heart phase interval was 65 msec. A coronal image was obtained from each patient by using a gated spin-echo technique to localize transaxial cine MRI. Cine MRI was then obtained for the entire heart from the apex to the most caudal portion of the ventricle. Images of the entire right and left ventricles were taken in all patients. In each patient, six different scans (one slice for each scan) were needed to calculate volumes. Therefore, slice thickness was 5, 7, or 10 mm without gap according to the ventricular cephalocaudal length (Fig. 1). All axial images were reconstructed at 9 to 13 frames for a cardiac cycle (varied with patient's heart rate) and displayed in a dynamic fashion (Fig. 2). The largest and smallest blood pool images were visually chosen for each slice of right and left ventricles and were taken as end diastole and end systole. For each image, a region of interest was then manually traced, excluding papillary muscles and large trabeculations of the right ventricle, for
Tetralogy of Fallot Tetralogy of Fallot, pulmonary atresia Corrected TGA, VSD, pulmonary atresia Double-outlet right ventricle Pure pulmonary atresia Single right ventricle Single left ventricle Tricuspid atresia Complete TGA Aortic atresia TOTAL Kawasaki disease with regression of the coronary artery aneurysm with anatomically normal ventricles TOTAL
No.
7 2 5 5 7 9 3 4 2 45 10 10
TGA, Transposition of the great arteries; VSD, ventricular septal defect.
the right and left ventricular blood pool on the transaxial plane. The number of image voxels within this region of interest was determined by the computer, and blood pool volume per slice could be calculated by multiplying this number by voxel size (Fig. 3). The end-diastolic and endsystolic volumes of all slices were then added to determine total right and left ventricular end-diastolic volume and end-systolic volume (Simpson's rule). We used a cylindric head coil with an aperture of 30 x 30 cm. All patients except one were sedated with oral monosodium trichlorethyl phosphate (80 mg/kg of body weight). The patients were monitored by pulse oximeter (Biox 3700, Omeda, Boulder, Colo.) in the MRI control room, and the monitoring line was shielded from the magnetic field. For infants, blankets and towels were used to prevent heat loss during examination. The patients did not take anything orally from two hours before the examination. In patients with single left ventricle with rudimentary chamber, we traced the biventricular cavity, excluding the interventricular septum. We counted the number of ventricles in single left ventricle with rudimentary chamber as one left ventricle. In single right ventricle, we counted the number of ventricles as one right ventricle. In patients with pure pulmonary atresia and tricuspid atresia with an extremely tiny right ventricular cavity, we could assessed left ventricle only. Thus there were 39 right ventricles and 35 left ventricles in this study. Yentriculography. Right and left ventricular volume determinations were performed from biplane cineangiographies obtained during routine diagnostic cardiac catheterization in all patients in this study. Biplane ventriculography was performed with 5F to 6F Bermann angiographic catheter at 50 frames per second (KXO-2050, Toshiba Inc., Tokyo, Japan). For calibration, a grid of 1 cm x 1 cm fine steel wire enbedded in Plexiglass was filmed perpendicular to the anteroposterior and lateral radiograph tubes at the exact position that the left or right ventricle had been during the ventriculography. 2' 6 Ventricu-
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Fig. 2. Tetralogy of Fallot with pulmonary atresia in 1-year-old girl. Transaxial plane. Third slice from caudal of ventricular segment in Fig. 1. Nine alternate frames from 14-image set of cine MRI, equally spaced within one cardiac cycle showing contraction of right and left ventricles. Diastole occurred in top left image, and systole occurred in middle right image.
lographies were traced by a single observer who took care to avoid post-ectopic beats. The ventriculographies were considered satisfactory for biplane volume analysis only if there were three consecutive, opacified sinus beats. The third beat was used for volume analysis. End systole was chosen as the smallest ventricular silhouette when the atrioventricular valve was closed. End diastole was chosen as the frame with the largest ventricular silhouette. The tracings were digitized with an NEC 9801 Desktop computer interfaced with an X-Y plotter and progTammed to calculate the ventricular volume with modifled Simpson's rule according to the method of Chapman and Graham 4-6 with the regression equation by Graham.2, 6 All patients were intravenously sedated with pethidine hydrochloride (1 mg/kg), and diazepam (0.5 rag/ kg). The patients did not take anything orally from three hours before the examination. Ventriculography was performed within 2 days after MRI. Data from these two modalities were evaluated prospectively by different observers who had no knowledge of the results of the other studies. Reproducibility. To determine the interobserver error
for MRI, volumes were analyzed by a further independent investigator. To determine intraobserver error for both techniques, studies were reanalyzed by the same observer after at least 3 months, with the observer blind to the original results. Statistics. MRI volumes and ventriculographic volumes were compared by linear regression analysis. Similarly, intraobserver variation and interobserver variation were analyzed with linear regression analysis of paired data from each patient. In addition, the mean and SD of paired differences ([measurement 1 - measurement 2]/Mean of the two measurements) between measurements by the two observers and the two measurements of one of the two observers were calculated as a measure of individual variability.
RESULTS Analysis time. All 45 patient studies were evalu-
ated. Mean acquisition and reconstruction times were 48 minutes, group A, and 45 minutes, group B. Regression data of ventricular volumes. Regression
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Fig. 3. Same patient as in Fig. 1. Single image from 14-image series at end diastole (A) and end systole (C). Sharp border between blood pool and left and right ventricular myocardium in top image. RV, right ventricle; LV, left ventricle. Region of interest outlined for determining slice volume at end diastole (B) and end systole D. Large papillary muscle of RV and normal-sized papillary muscle of LV were excluded from volume calculation.
RVEDV
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(ml)
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Fig. 4. Regression line between MRI and angiographically measured right ventricular volume in group A. End-diastolic volume (EDV) on left, end-systolic volume (ESV) on right. RVG, right ventriculography; SEE, standard error of estimate. data for MRI versus angiography in group A are shown in Figs. 4, 5, and 6. End-diastolic volume and end-systolic volume in both ventricles in group A by MRI correlated well with but appeared to underestimate the volume by angiography (r > 0.89). Ejection fraction in left ventricles in group A by MRI correlated well with the ejection fraction by angiography (r = 0.84). Similarly, ejection fraction in the right ventricle in group A by MRI correlated well with t h a t
by angiography, but it appeared to be a lower correlation t h a n for the left ventricle (r = 0.67). Regression data for MRI versus angiography in group B are shown in Figs. 7, 8, and 9. End-diastolic volume and end-systolic volume in both ventricles in group B by MRI correlated well with but appeared to underestimate the volume by angiography (r > 0.91). Ejection fraction in both ventricles in group B by MRI correlated well with the fraction by angiography (r > 0.73).
Volume 131, Number 3 American Heart Journal
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LVEDV
LVESV
(ml) 120- Y=0.93X+3.4 100- r=0.94 SEE=8.7 N35 = ~ n
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(%)
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6. Regression line between MRI and angiographically measured right and left ventricular ejection fraction (RVEF and LVEF, respectively) in group A.
Reproducibility. Regression data between the two observers and the repeat MRI studies are shown in Table II. The correlation coefficients for the repeat MRI studies as measured by a single observer (intraobserver variation) in end-diastolic and endsystolic volumes in both ventricles in both groups were more t h a n 0.95. The correlation coefficients between the two observers (interobserver variation) for end-diastolic and end-systolic volumes in both ventricles in both groups were more t han 0.92. The interstudy percent variabilities and standard deviations are shown in Table III. In both groups, end-diastolic volumes, end-systolic volumes, and ejection fraction showed little variability. The m ean coeffi-
cient of variation was less t han 6% for all volumes in both groups.
DISCUSSION Various meansfor evaluatingventricularvolumes in children. Currently, the most common means of measuring ventricular volumes in children are right and left ventriculography and echocardiography. However, these modalities have some limitations in pediatric cases. Ventriculography provides good delineation of the right and left ventricular cavities with high temporal resolution. The calculation methods employed for biventricular volumes (area-length method, 1, 3 mod-
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Niwa et al.
RVEDV (ml) 80 Y--0.94X+2.9 r=0.93 60
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j •
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Fig. 7, Regression line between MRI and angiographically measured right ventricular volume in group B. End-diastolic volume (EDV) on left, end-systolic volume (ESV) on right.
LVEDV
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(ml) 80Y=0.89X+2.2 r=0.96 SEE-4.7 60 N=10
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Fig. 8. Regression line between MRI and angiographically measured left ventricular volume in group B. End-diastolic volume (EDV) on left, end-systolic volume (ESV) on right. ified Simpson's method, etc., 4.s however, rely on geometric assumptions concerning the shape of the right and left ventricle by using a regression equation that leads to inaccurate assessment in patients with complex congenital heart disease and morphologically abnormal ventricles. In addition, the examination is invasive and involves radiation exposure. Therefore applying ventriculography for routine monitoring of cardiac function is impractical. Twodimensional echo has been widely used to evaluate left ventricular volume in children. 25 However, it is frequently difficult to obtain images of the entire right ventricle. 26 Visualizing the entire right and left ventricles in complex congenital heart disease is more difficult, especially when associated with malrotation, malposition, or severe deformity of the
heart. Furthermore, it is also thought to be difficult to make proper simple geometric assumptions for calculating deformed right and left ventricles such as those in complex congenital heart disease. Therefore there have been few reports of measuring the ventricular volumes in patients with complex congenital heart disease. Gated blood-pool scintigraphy is an accurate means of determining left ventricular volumes and is relatively independent of geometric assumptions. 27 The technique is noninvasive and requires minimal exposure to radiation. But spatial resolution, especially in infants and small children, is sometimes poor or limited; in addition, the atrial blood pool cannot be clearly separated from the ventricu]ar region Of interest. 27 Computed tomography with Simpson's rule has been validated in a canine
Volume 131, Number 3 American Heart Journal
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RVEF
(%) 100
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/
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Fig. 9. Regression line between MRI and angiographically measured right and left ventricular ejection fraction (RVEF and LVEF, respectively) in group B. Table II. Intraobserver and interobserver correlations Group A RVEDV RVESV RVEF LVEDV LVESV LVEF
Intra r r r r r r
= = = = = =
0.97 0.96 0.73 0.98 0.95 0.73
(5.4) (3.5) (0.1) (5.1) (4.2) (0.1)
r r r r r r
= = = = = =
Inter
Group B
0.95 0.94 0.69 0.97 0.94 0.79
RVEDV RVESV RVEF LVEDV LVESV LVEF
(7.1) (4.3) (0.1) (6.4) (4.6) (0.1)
Intra r r r r r r
= = = = = =
0.95 0.95 0.90 0.96 0.95 0.72
(4.4) (2.5) (0.1) (5.9) (2.6) (0.1)
Inter r r r r r r
= = = = = =
0.93 0.92 0.80 0.94 0.92 0.76
(5.2) (3.1) (0.1) (6.9) (3.2) (0.1)
RVEDV, Right ventricular end-diastolic volume; RVESV, right ventricular end-systolic volume; RVEF, right ventricular ejection fraction; LVEDV, left yentricular end-diastolic volume; LVESV, left ventricular end-systolic volume; LVEF, left ventricular ejection fraction; r, correlation coefficient (standard error of the estimate).
Table III. Intraobserver and interobserver percentage variability Group A RVEDV RVESV RVEF LVEDV LVESV LVEF
Intra 4.0 4.6 2.9 3.3 5.4 5.i
(4.7) (5.7) (3.8) (3.7) (6.1) (7.5)
Inter 5.4 5.4 4.2 4.5 6.7 4.1
(6.1) (6.1) (3.5) (5.0) (7.3) (6.0)
Group B RVEDV RVESV RVEF LVEDV LVESV LVEF
Intra 2.4 3.1 2.2 3.1 4.5 4.2
(2.8) (3.4) (3.2) (3.4) (5.3) (5.3)
Inter 4.1 4.5 3.0 5.6 7.5 1.8
(3.5) (5.0) (2.4) (6.4) (3.0) (2.5)
Abbreviations as in Table II.
model for assessing left and right ventricular volume. 2s However, this technique requires injection of radiopaque contrast medium and uses ionizing radiation. Therefore applying these examinations for routine evaluation of biventricular function in complex congenital heart disease is impractical. Cine MRI for evaluating ventricular volumes in children. It is reported t h a t singie-plane measurements of left ventricular volume by MRI can be made accu~'ately and are sufficient for routine clinical use except in patients with a pronounced wall motion
abnormality.16, 19 It is also reported t h a t comparisons of the left ventricular volume, measured by MRI with the area-length method 11 and modified Simpson's rule, 12 yielded a high correlation between MRI and ventriculography in children with simple congenital heart disease. However, when applying these methods to calculate ventricular volume, geometrical assumptions are required. Therefore these methods are thought to be inaccurate when measuring morphologically abnormal ventricles such as those in complex congenital heart disease. By using MRI, we
March 1996 American Heart Journal
574 Niwa et al.
can calculate right and left ventricular volumes by adding the areas of the cavities in contiguous slices without making geometric assumptions concerning the ventricular shape and without a regression equation for the papillary muscles. MRI is therefore a suitable modality for measuring ventricular volumes with Simpson's rule. Previous MRI studies concerning ventricular volume measurement in a cardiac cast reported that correlation between the actual cast volume and the calculated volume by MRI was excellent. 14, 22, 24 Comparing the ventricular volumes in adult patients with normally structured ventricles yields a good correlation between MRI and ventriculography has also been reported.15, 16, 19-22Furthermore, the correlation of the calculated right and left ventricular volumes between cine MRI and ventriculography in control patients was good in this study. From the findings of these studies, the measurement of biventricular volumes in patients with morphologically n o r m a l ventricles by cine MRI with Simpson's rule is thought to be methodologically reliable. Cine MRI for evaluating ventricular volumes in complex congenital heart disease. By summing up the vol-
umes of ventricular cavity intersections (Simpson's rule) as previously cited, we could calculate right and left ventricular volumes in patients with severely deformed ventricles and normally structured ventricles in the same fashion. 14, 22, 24 In this study, the correlations between cine MRI and ventriculography in measurements of right and left ventricular volumes in control patients and patients with complex congenital heart disease were excellent. Furthermore, MRI technique in both groups in this study had low intraobserver and interobserver variations. Semelka 23 indicated that cine MRI has a high interstudy reproducibility and is therefore suitable for sequential studies even in patients with morphologically abnormal ventricles. From these findings and reports, right and left ventricular volumes in patients with complex congenital heart disease and abnormal ventricle are thought to be measured accurately by cine MRI with Simpson's rule. Furthermore, different from measuring ventricular volumes by echocardiography and ventriculography, we can calculate the right and left ventricular volume simultaneously from the same contiguous slices by cine MRI with Simpson's rule. Furthermore, highly complicated complex congenital heart disease such as heterotaxia could be easily and accurately diagnosed by MRIg, 10 Therefore the whole ventricular cavity in complex congenital heart disease with morphologically abnormal ventricles is easily visualized by MRI. Advantage of cine mode MRI. The major advantages
of cine MRI are the much shorter acquisition times and the increased time resolution from many frames or phases within the cardiac cycle. For calculating ventricular volume in complex congenital heart disease, cine MRI is therefore thought to be superior to spin-echo sequence. Proper slices for calculating ventricular volumes in complex congenital heart disease by MRI. Tt has been
postulated that the assessment of left ventricular geometry and function is more accurate on the short axis than on a transverse imaging plane because angulation errors and partial volume effects can be minimized on a short-axis plane. 29 Buser et al. 21 reported that left ventricular volume m e a s u r e m e n t s obtained with cine MRI by Simpson's rule in a transverse and short-axis imaging plane were nearly identical, and they speculated that partial volume effect might have similarly affected both transverse and short-axis volume measurement. In a transverse imaging plane, it is easy to visualize the cardiovascular anomalies, the sites of atrioventricular and semilunar valves, and the whole ventricular cavity in complex congenital heart disease. 9, 10 In this study, we could easily visualize the proper slices for measuring ventricular volumes on a transverse image. Furthermore, ventricular volumes in both groups by MRI correlated well with those by ventriculography. Therefore for calculating ventricular volumes in complex congenital heart disease, transverse image is thought to be useful. Analysis time. We could reduce the examination time by using a small matrix size (128 x 128 or smaller); in this study, however, we thought that the imaging time was still too long for routine clinical use. However, in the near future, this disadvantage will be overcome by u s i n g ultrafast MRI, which is faster than the apparatus currently available. 3° Conclusion. By using cine MRI with Simpson's rule, the right and left ventricular volumes in complex congenital heart disease can be easily evaluated. Furthermore, the ventricular volumes obtained are independent of geometric assumptions and may be more accurate than ventriculography in complex congenital heart disease with morphologically abnormal ventricles. Measuring biventricular volumes in complex congenital heart disease with this method is a promising modality in conjunction with the development of ultrafast MRI.
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1. Dodge HT, Sandler H, BaUew DW, Lord JD Jr. Use of biplane angiocardiography for the measurement of left ventricular volume in man. AM HEART J 1960;60:762-76. 2. Graham TP Jr, Jarmakani JM, Canet RV Jr, Marrow MN. Left
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