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Magnetic resonance imaging in congenital heart disease of newborns: preliminary results in 23 patients
European Journal of Radiology, 10 (1990) 109-l 17 Elsevier
EURRAD
109
00028
Magnetic resonance imaging in congenital heart disease of newborns: preliminary results in 23 patients Bruno Kastler ‘, Angelo Livolsi 2, Philippe Germain 3, Georg Zollner ‘, Daniel Willard2 and Auguste Wackenheim’ ‘Department Radiologie I, Hospices Civilsde Strasbourg and Departments ‘Pt!diahie II and 3Cardiologie,H6pital de Hautepierre, Strasbourg, France (Received
Key words: Congenital
12 July 1989; revised version received 6 November
heart disease; Newborn;
1989; accepted
MR imaging, heart; Two-dimensional
12 November
1989)
Doppler echocardiography;
Heart, MRI
Abstract Until now little attention has been paid to the potential of MR imaging in congenital heart disease of the newborn. ECG-gated MRI was therefore performed at 0.5 tesla in 23 newborns (mean age 7.5 days) with suspected congenital heart disease. Two newborns were controlled after surgery (switch, Blalock-Taussig procedure). All had undergone prior evaluation by two-dimensional Doppler echocardiography (2-D DE). MR imaging was of a satisfying quality in all but one newborn. The aim of this study was to assess complementary information provided by MRI in comparison to 2-D DE. Pre-operatively MRI missed some abnormalities shown by 2-D DE: one coartaction, one ductus arteriosus and one pulmonary atresia. MRI demonstrated lesions that echocardiography had either failed to visualize or found inconclusive, including double aortic arch (one patient), muscular ventricular septum defect (two patients) and severe ductus arteriosus (one patient). In one of the two patients with a ventricular septum defect, angiography was avoided and in the other patient it merely confirmed the MRI results. Post-operatively, MRI demonstrated information complementary to that obtained from to 2-D DE: (1) clearly visualizing the reinsertion of the coronary arteries in the ‘switched’ transposition of the great vessels, (2) appreciating the diameter and patency of the palliative shunt in the Blalock-Taussig procedure.
Introduction Recent articles on the use of MRI in congenital heart disease have emphasized the role that this non-invasive technique plays in demonstrating congenital cardiac abnormalities [l-7,13,15,22]. Previously published series have been restricted to adults or young children. As far as we know little consideration has been given to the possible role of cardiac MR imaging in newborns [ 18,241 (patients, age in the range 1 week to 16 years: mean age 46 months). Although many congenital abnormalities of the heart may be well visualized by 2-D DE in infants because of the generally excellent sonic transmission through the chest wall, in some cases 2-D DE still remains inconclusive. Consequently, angiographic procedures are usually necessary for diagnosis. Address for reprints: B. Kastner, M.D., Department of Radiology, Hospices Civils de Strasbourg, 67091 Strasbourg Cedex, France. 0720-048X/90/$03.50
0 1990 Elsevier Science Publishers
Indeed, angiography has drawbacks such as invasive features and potential radiation hazards. In this report on our initial experience with cardiac MR imaging in newborns, we show the feasability of cardiac MRI in a pediatric population of young age and we attempt to determine the clinical benefits of this new imaging technique. Patients and Methods Twenty-three newborns aged l-33 days (mean age 7.5 days) with suspected congenital heart disease were examined with MR imaging. The same imaging procedure was also applied to four patients with no known heart pathology who served as a control group for normal cardiac anatomy. Six of the 23 neonates were growth retarded and four were premature. Patients were not selected but represented our referrals over a 4-month period. Informed consent was obtained in
B.V. (Biomedical
Division)
110
each case from the patients’ parents. One MRI study in a 4-day-old newborn with suspected atresia of the aortic arch was deemed inadequate because of motion artefacts and was excluded from this investigation. The remaining 22 patients included: coarctation of the aorta (four patients); double aortic arch (one patient); transposition of the great vessels (five patients, one had additional situs inversus); ductus arteriosus with pulmonary hypertension (one patient); complete atrioventricular canal (three patients); truncus arteriosus (one patient); left ventricular hypoplasia (one patient); tricuspide atresia with pulmonary stenosis (two patients); ventricular septum defect with pulmonary atresia (two patients); tetralogy of Fallot (two patients). Two patients were controlled post-operatively: one transposition of the great vessels 13 days after a switch (performed after 2 weeks), and one pulmonary atresia 15 days after a Blalock-Taussig shunting procedure (performed after one week). Images were obtained with a 0.5 T superconducting magnet (GE-CGR) by ECG-gated single echo multislice technique, with an echo time of 26 ms and a repetition time determined by heart rate (approx. 300 ms because of the spontaneously high heart rate of the newborns). Sections thickness was 5 mm with no interslice gap. Because even the slightest patient motion distorts the MR images, sedation was compulsory. Adequate sedation of all children was achieved with 3-4 mg of Nembutal or choral hydrate 30-40 mg/kg coupled with feeding 20 min before examination. The patients were placed in the supine or prone position using either the head coil or a surface coil. Imaging was initially performed in the sag&al projection with a nongated gradient echo sequence. Then, spin echo sequences were obtained in axial and in left anterior oblique equivalent planes (LAO) (along the course of the aortic arch), small axis views and/or sag&al views. Each set of ten to twelve images required about 5 min (depending on the heart rate). A complete study (three runs) required approx. 35 min. Echocardiography was performed prior to MR imaging in all patients, with standard commercially available equipment that had a wide angle, pulsed and continuous Doppler capabilities and a high frequency transducer (7.5 MHz). In three patients, intravenous digital substraction angiography (IV-DSA) was also performed. MRI studies were evaluated by two of the authors (B.K. and A.L.). Since the observers were aware of the echocardiographic diagnosis, the study was focused on the complementary information provided by MRI. In all but two patients, the final diagnosis was obtained either by autopsy, surgery or angiography.
Results All newborns withstood the examination by the previously described method well. Suprisingly, the continuous, monotonous noise of the MR imager seemed to soothe the newborns, most of them no longer moving once scanning began. The quality of the MR images is dependent on the fact that the neonates remain motionless during scanning time. Diagnostic MR images were obtained in all but one patient who was not well sedated and whose motion degraded the image quality. In all other patients excellent MR images (comparable to adults) were obtained in spite of the relatively long acquisition times. The rapidly flowing blood within the vessels and cardiac chambers is seen in sharp contrast to the high intensity of the mediastinal fat and medium intensity of the vascular and cardiac walls. Other distinct advantages of this imaging modality are a large field of view and the ability to image multiple projections which allow a step-by-step approach to segmental cardiac and vascular anatomy. The axial planes are suitable for analyzing the position of the ascending aorta with respect to the pulmonary artery, identifying the right and left ventricles which have different anatomic characteristics (i.e., the level of attachement of the septal leaflets of the AV valves), visualizing ventricular or atrial septum defects, and evaluating the pulmonary veins merging into the left atrium. The small axis planes clearly separating the right and left cardiac chambers provide confirmation of transposition of the great vessels, ventricular and atrial septum defects, as well as analysis of the right ventricular outflow tract. The sag&al views are most useful for analyzing the conotruncunal region of the heart. The coronal planes are suited to identify the right atrium, to localize the inferior vena cava, the ascending and descending aorta, the viscera (liver, stomach, spleen) and to visualize the bronchi and the trachea. Two-dimensional Doppler echocardiography provides high-quality images of the cardiovascular system in newborns, because of the great number of echo windows available and the good sonic transmission [ 12,141. Indeed 2-D DE precisely demonstrated most of the various cardiac abnormalities. The diagnosis had therefore been established by 2-D DE prior to MR imaging in all cases but for the double aortic arch. Presurgical results of echocardiographic, MRI and angiographic procedures are summarized in Table I. In three patients with coarctation of the aorta, the lesion was completely visualized on LAO equivalent
111 TABLE
I
Results of 2-D DE - MRI - angiography
in 20 newborns
Case/age (days)/ Clinical diagnosis sex
l/W 2PlM 3/10/F 4/7/M
5/33/M
VIM 1/4/M 8/3/M 9/7/M
10/2/F 11/6/F 12/2/M 13/5/M 14/2/F
15/l/F 16/3/M 11/2/M 18/6/F 19/6/F
20/8/M 20/5/M 22/l/F
+ , diagnosed;
Coarctation Coarctation Coarctation Coarctation
of of of of
the the the the
2-D DE
aorta aorta aorta (S) aorta (S)
MR imaging
Angiography
+
0
+
0
+ -
0 0
Double aortic arch (S) Transposition of the great vessels (S)
+
+ f
0
Transposition Transposition Transposition
+
zk
0
f f
+
+
+
0
+
+
0
+ + +
+
0
+
0
+
0
f
+
+
Truncus arteriosius type I (PM) Left ventricular hypoplasia (PM) Tricuspid atresia with pulmonary stenosis (S) Tricuspid atresia with pulmonary stenosis (S) Ventricular septum defect with pulmonary atresia (S)
+
0
+
0
+
0
+
0
+
0
Ventricular septum defect with pulmonary atresia (S) Tetralogy of Fallot (S) Tetralogy of Fallot (S)
+
0
+
0
+
0
of the great vessels (S) of the great vessels (S) of the great vessels (S)
Transposition of the great vessels, situs inversus and pulmonary stenosis (S) Complete atrioventricular canal (S) Complete atrioventricular canal (S) Complete atrioventricular canal (S) Ductus arteriosus with pulmonary hypertension (S)
+, incomplete
diagnosis;
- , not diagnosed;
Comment (case)
Entire aorta not in one LAO MR projection (4)
+ Ductus arteriosus not visualized by MR imaging (6)
VSD not visualized by 2 DE (8.9) post-surgical MRI at day 21 (switch at day 14)
2 DE not well visualized pulmonary veins (14)
Small axis view did not allow correct diagnosis of pulmonary stenosis (18) Depiction of pulmonary atresia required a 3rd run of MR images (sagittal views) (19) Post-surgical MRI at day 23 (Blalock-Taussig at day 8)
0, study not done; S, surgery; PM, post-mortem.
images displaying the entire aortic arch. In the other patient with coarctation of the aorta, the site of the coarctation could not be directly visualized. In one of the two patients with tricuspid atresia the pulmonary stenosis (diagnosed with 2-D DE) could not be well visualized by MRI on small axis views. In transposition of the great vessels, the anterior posterior relation of the great vessels was clearly seen in all live patients with 2-D DE as well as with MR imaging (Figs. 1 and 2). However, in two patients, 2-D DE did not show distal muscular septum defects (Fig. 3) responsible for left ventricular failure (recurrent pulmonary oedema).
In one of these patients controlled after surgery (switch), only MRI clearly depicted the reinsertion of the coronary arteries in the ‘switched’ aorta (Figs. 4 (a and b) and 5). In the pulmonary stenosis with ventricular septum defect, pre-operatively both imaging procedures were satisfactory, after the Blalock-Taussig procedure, only MRI completely visualized and confirmed the patency of the anastomosis (Fig. 5). In one patient, a patent ductus arteriosus well diagnosed by 2-D DE was not entirely visualized by MR imaging. Intravenous digital subtraction angiography was performed in one infant with a suspected double aortic
Fig. 1. Transposition of the great vessels. LAO image shows the aorta (1) anterior to the pulmonary artery (2) which arises from the left ventricle. Note the ductus arteriosus (straight arrow).
arch, in one newborn with ductus arteriosus and pulmonary hypertension (in order to eliminate an associated pathology like partial anomalous pulmonary venous return) and in one with transposition of the great vessels (to confirm the presence and to appreciate the severity of a muscular ventricular septum defect). In general (pre-operatively), MRI provided more information then 2-D DE in four patients including a
Fig. 3. Transposition of the great vessels with a ventricular septum defect (arrow) clearly depicted by MRI. It was not visualized by 2-D Doppler echocardiography.
double aortic arch (one patient), muscular ventricular septum defect (two patients) and severe ductus arteriosus (one patient). Post-operatively, MRI furnished information complementary to that obtained from 2-D DE in both patients. Discussion
Fig. 2. Transposition of the great vessels. LAO view. The aorta (2) is anterior to the pulmonary trunk (3) and the descending aorta (straight arrow) is well visualized. 1, right atrium; 4, left atrium.
MR imaging, which provides detailed sectional anatomy in multiple body planes, demonstrates congenital intracardiac and great vessel abnormalities in adults and young children as has been reported in several recent articles [l-7,13,15,22]. Our aim was to prove the feasibility and to find applications for cardiac MR imaging in this pediatric population of a young age. We encountered no major difIiculties in ima@g the newborns, thus there is no lower age limit for cardiac MR imaging. This procedure is applicable to and even well tolerated by premature patients. Using the previously described method, the image quality is satisfactory and the pathologic lesions are visualized in most patients [ 17,18,19,21]. MR imaging offers the non-invasive advantages of 2-D DE as well as its ability to image multiple planes; it is non-operator dependent and has a large field of view. But MRI requires sedation and is more expensive, time consuming and less accessible than 2-D DE. Other limits of our MR imager in comparison with 2-D DE are
Fig. 5. Right sided Blalock-Taussig shunt. MRI oblique coronal view (oriented along the course of the right pulmonary artery) displays the anastomosis entirely (size, course, patency as well as pulmonary and subclavian insertion). The shunt (arrow) is patent (signal void). 1, right pulmonary artery; 2, right subclavian artery.
Fig. 4. Transposition of the great vessels. Post-operative axial images (‘switch’). (a) The reinsertion ofthe right coronary artery into the ‘switched’ aorta is clearly depicted (arrow). (b) Note that the left coronary trunc is visible until its bifurcation into circonflex and anterior descending branch (arrow head). The left pulmonary artery (g) is anterior to the ascending aorta. 1, aorta; 2, pulmonary trunc; 3, vena cava superior; 4, left atrium.
the slice thickness (minimum 5 mm for correct signal to noise ratio) and the absence of dynamic heart imaging. 2-D DE is highly sensitive and specific for visualizing the heart and great vessels in neonates and small infants [ 141. Because of the small size of neonates, the good sonic transmission through the chest and the lungs, high
frequency transducers (7 MHz) which greatly increase spatial resolution can be used. Other advantages of 2-D DE are that it allows bedside examination, real time motion studies, multiplane thin slice (2 mm) imaging (because of the great number of available echo windows in the newborn). Therefore, it remains the prime imaging method of congenital heart abnormalities in small infants and newborns. However, 2-D DE even combined with Doppler has limitations such as for-the evaluation of the great arteries, distal muscular ventricular septum defect and posterior cardiac structures (i.e., anomalous pulmonary venous returns and aortic arch anomalies). In adults and young children other authors have found MR imaging to be very useful [1,3,9-l 1,251. This is not suprising because as children grow, the performance of 2-D DE decreases and extra-cardiac structures become difficult to visualize. In our four cases of coarctation of the aorta (visualized by 2-D DE), MR imaging could not determine the exact site of coarctation in one patient. This patient had marked buckling of the aortic arch which therefore could not be displayed entirely on one LAO equivalent
114
image and had to be synthesized from adjacent contiguous slices. However, MR imaging on axial images clearly showed hypoplasia of the aortic arch which can be associated with coarctation. The optimal approach to the diagnosis of vascular rings is a matter of considerable controversy among pediatricians and varies from the recommendation of chest X-ray and barium oesophagography alone to more complex procedures like angiography. Our single case of double aortic arch (not diagnosed by 2-D DE)
cannot resolve this controversy, however the relative ease with which MR can be performed and the experience of others [3,9,16,20,25], justify this procedure for precise anatomic definition and confirmation of diagnosis. MR imaging demonstrated the airway obstruction, the vascular relationship, as well as the relative size and patency of the arches (Fig. 6). As usual, the right arch was higher and larger than the left one which was sectioned at operation. Angiographic images were comparable to MR images. Therefore, MR
Fig. 6. Double aortic arch. (A) axial MR image. (B,C,D) coronal MR images from front to rear. The ascending aorta (a) gives rise to the right (1) and left (2) arches. The right arch is usually larger and higher than the let? arch. The arches encircle the trachea (arrow) which is compressed and converge again to form the descending aorta (d). v, superior vena cava.
115
imaging seems to be the method of choice as it is noninvasive and requires a less heavy sedation than angiography. Transposition
of the great arteries is easily visualized
Fig. 7. Complete atrioventricular canal. Axial images show interventricular communication (curved arrow) limited caudaly by the floor of the common atrioventricular valve (straight arrow). There is also a large atria1 septal defect. The left ventricle (L) is small and the right ventricle (R) is dilated.
Fig. 8. Truncus arteriosus (type I). LAO equivalent projection displays the aorta (1) and the pulmonary artery (2) originating from a common truncus (straight arrow).
Fig. 9. (a) Troncus arteriosus. Transverse image revealing a large ventricular septum defect (arrow). 1, left ventricle; 2, right ventricle. (b) Small axis view of the same patient as in (a). The ventricular septum defect (arrow) is thus confirmed. 1, left ventricle; 2, right ventricle.
116
with 2-D DE in infants and children [ 121. Similarly, MR imaging readily demonstrated abnormal connections among auricular, ventricular and arterial compartments (Figs. 1 and 2). Furthermore, in two cases, MR imaging clearly showed distal muscular ventricular septum defects that could not be identified by 2-D DE (Fig. 3). In both neonates, the ventricular septum defects were responsible for unexplained recurrent left ventricular failure (by shunt excess). Due to the similarity of these cases, angiography was not performed in the second case. In one of two patients with tricuspid atresia and pulmonary stenosis, the pulmonary stenosis was not diagnosed on small axis MR images. This patient was one of the first included in this study and we did not realize that the sag&al views are actually better suited for displaying the right ventricular outflow tract and the initial portion of the pulmonary trunc. We encountered the same difficulties in trying to identify the pulmonary stenosis in the other patient which was readily depicted (better than 2-D DE) only on sag&al views. In the patient with severe ductus arteriosus, angiography was required to eliminate an anomalous pulmonary venous return. Contrary to 2-D DE, MR imaging correctly visualized the pulmonary veins merging into the left atrium. Angiography did not give more clinically relevant information than MR imaging. In all the other cases, including complete atrial ventricular canal (Fig. 7), truncus arteriosus (Figs. 8,9a and 9b) left ventricular hypoplesia, two ventricular septum defects with pulmonary atresia and two tetralogies of Fallot, both MR imaging and 2-D DE provided excellent diagnostic images. After surgical repair, contrary to 2-D DE (because of well-known limited accessibility of extracardiac structures), MRI appreciated the patency of small vascular structures perfectly (initial segment of the coronary arteries and palliative shunting procedure) (Figs. 4 (a and b) and 5). The non-invasive assessment capabilities of MRI in palliative shunting procedure have already been reported in older children [ 8,201. Contrary to the findings of these authors, the shunt in our neonate was entirely visualized on one single view. This may be explained in part by the fact that the diameter of the shunt is small compared with our slice thickness, but also because we use coronal oblique planes oriented along the course of the pulmonary artery (ensuring visualization of the pulmonary insertion of the shunt)
[191. In addition, MRI was capable of visualizing both size and patency of the main and branch pulmonary arteries. Overall, in three patients MRI missed cardiac abnor-
malities but this was not of clinical importance because these lesions (one coarctation of the aorta, one ductus arteriosus, one puhnonary stenosis) were easily depicted by 2-D DE which should nevertheless remain the prime cardiac imaging modality in newborns. MRI yielded more detailed information and therefore usefully complemented echocardiography in five cases: one double aortic arch and two ventricular septum defects (in two transposition of the great vessels) and in the two post-surgical controls. It was not the purpose of this study to suggest that MRI should replace 2-D DE but to show the feasability of MRI in a very young pediatric population and to illustrate its potential complementary role. Noninvasive diagnostic management of congenital heart disease has indeed greatly improved with the introduction of 2-D DE [ 12,141 and Doppler flow mapping. At present, in most cases angiography is no longer required in neonates. But, as sonic transmission through the chest wall becomes poorer with growth of children, and/or chest surgery, MR imaging will certainly play an increasingly important role in the pre- and post-operative assessment of complex congenital heart disease [8,18-21,241. Our preliminary experience is not su&cient to conclude the extent to which MR imaging could replace angiography. But in three neonates where 2-D DE was insufficient and angiography was required (one double aortic arch, one transposition of the great vessels, one severe ductus arteriosus), angiography did not provide more clinically relevant information than MRI. In one patient with transposition of the great vessels and a muscular septum defect (well visualized by MR imaging and not detected by 2-D DE) angiography was avoided. Even with digital substraction angiography (less irradiating), a heavier sedation is required than with MR imaging and the use of contrast media increases the risks as it is an invasive technique. Nevertheless, invasive procedures like angiography and catheterization are presently still mandatory to explore coronary arteries, peripheral pulmonary vessels or to measure cardiac and pulmonary pressures. Our results with static spin-echo images show that MR imaging provides detailed anatomic images of congenital heart disease in the newborn and may be valuable whenever there is a need for more information than echocardiography can provide. MR imaging is a rapidly evolving technique: recent developments such as tine MRI [5,23,24], MR angiography and fast scanning techniques will undoubtedly enhance our ability to use cardiac MR imaging in this very young pediatric population and may therefore offer a serious non-invasive alternative to angiography.
117
References Amparo EG, Higgins CB, Shafton EP. Demonstration of coarctation of the aorta by magnetic resonance imaging. AJR, 1984; 143: 1192-1194. Bank ER, Hemandez RJ. CT and MR of congenital heart disease. Radio1 Clin North Am 1988; 26: 241-262. Bisset GS, Strife JL, Kirks DR, Bailey WW. Vascular rings: MR imaging. AJR 1987; 149: 251-256. Boxer RA, Singh S, Lacorte MA, et al. Cardiac magnetic resonance imaging in congenital heart disease. J Pediatr 1986; 109 : 460-464. Chung KJ, Simpson IA, Newman R, et al. Cine MRI for evaluation of congenital heart disease: role in pediatric cardiology compared with echocardiography and angiography. J Pediatr 1988; 113: 1028-1035. Dider D, Higgins CB, Fisher MR, et al. Congenital heart disease: gated MR imaging in 72 patients. Radiology 1986, 158: 221-235. Fletcher BD, Jacobstein MD, Nelson AD, et al. Gated magnetic resonance imaging of cardiac malformation. Radiology 1984; 150: 137-140. Fletcher BD, Jacobstein MD, Nelson AD, et al. MR imaging: evaluation of palliative systemic pulmonary artery shunts. Circulation 1984; 70: 650-656. Fletcher BD, Jacobstein MD. MRI of congenital abnormalities of the great arteries. AJR 1986; 146: 941-948. 10 Fletcher BD, Dearborn DG, Mulopulos GP. MR imaainz _ _ in infants with airway obstruction. Preliminary observations. Radiology 1986; 160: 245-249. Gomes AS, Lois JF, George B, Alpan G, Williams RG. Congenital abnormalities of the great arteries. Radiology 1987; 165: 691-695. Gutgesell HP, Huhta JC, Latson LA, Huffines LD, McNamata DG. Accuracy of two dimensional echocardiography in the diagnosis of congenital heart disease. Am. J. Cardiol., 1985,55: 514-518. Higgins CB, Byrd BF, Farmer DW, et al. Magnetic resonance imaging in patients with congenital heart disease. Circulation, 1984, 70: 851-860.
14 Huhta JC, Gutgesell HP, Latson LA, Hufftines FD. Two dimensional echocardiographic assessment of aorta in infants and children with congenital heart disease. Circulation, 1984, 70: 417-424. 15 Jacobstein MD, Fletcher BD, Nelson AD, et al. ECG gated nuclear magnetic resonance imaging: appearance of the congenitally malformed heart. Am Heart J, 1984, 107: 1014-1020. 16 Julsrud PR, Ehman RL. MR Imaging of vascular rings. Mayo Clin Proc, 1986, 61: 181-185. 17 Kastler B, Livolsi A, Willard D, Wackenheim A. Diagnostic impact of MR Imaging in congenital heart disease of newborns. RSNA 74th Scientific Assembly and Annual Meeting, 1988, Chigaco. Radiology, 1988, 169, abstract 707. 18 Kastler B, Livolsi A, Tajahmady T, Willard D, Wackenheim A. Inter& de I’IRM dans le diagnostic et le suivi post-operatoire des cardiopathies congenitales en p&ode ndonatale. Radiologie (accepted). 19 Kastler B, Livolsi A, Germain P, Willard D, Wackenheim A. MRI in the pre- and post-surgical evaluation of congenital heart disease in newborns. RSNA, 75th Scientific Assembly and Annual Meeting, 1989, Chicago. 20 Katz ME, Glazer HS, Siegel MJ, et al. Mediastinal vessels: post-operative evaluation with MR imaging. Radiology, 1986, 161: 647-651. 21 Livolsi A, Kastler B, Willard D. Etude pre- et post-optratoire dune transposition des gros vaisseaux en ptriode ntonatale par l’IRM. Ann Cardiol Angtio, 1989, 38: 261-264. 22 Reed Jr, Soulen RL. Cardiovascular MRI: current role in patient management. Radio1 Clin North Am 1988; 26: 589-606. 23 Sechtem U, Plugfelder PW, White RD, et al. Cine MR imaging: potential ofthe evaluation of cardiovascular function. AJR 1987; 148: 239. 24 Simpson IA, Kyung, JC, Glass RF, Shan DJ, Shedman FS, Hesselink J. Cine MRI for evaluation of anatomy and flow relations in infants and children with coarctation of the aorta. Circulation 1988: 78: 142-148. 25 Soulen RL, Donner M. Advances in non-invasive evaluation of congenital anormalies of the thoracic aorta. Radio1 Clin North Am 1985; 23: 727-736.
EURRAD
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00028
Magnetic resonance imaging in congenital heart disease of newborns: preliminary results in 23 patients Bruno Kastler ‘, Angelo Livolsi 2, Philippe Germain 3, Georg Zollner ‘, Daniel Willard2 and Auguste Wackenheim’ ‘Department Radiologie I, Hospices Civilsde Strasbourg and Departments ‘Pt!diahie II and 3Cardiologie,H6pital de Hautepierre, Strasbourg, France (Received
Key words: Congenital
12 July 1989; revised version received 6 November
heart disease; Newborn;
1989; accepted
MR imaging, heart; Two-dimensional
12 November
1989)
Doppler echocardiography;
Heart, MRI
Abstract Until now little attention has been paid to the potential of MR imaging in congenital heart disease of the newborn. ECG-gated MRI was therefore performed at 0.5 tesla in 23 newborns (mean age 7.5 days) with suspected congenital heart disease. Two newborns were controlled after surgery (switch, Blalock-Taussig procedure). All had undergone prior evaluation by two-dimensional Doppler echocardiography (2-D DE). MR imaging was of a satisfying quality in all but one newborn. The aim of this study was to assess complementary information provided by MRI in comparison to 2-D DE. Pre-operatively MRI missed some abnormalities shown by 2-D DE: one coartaction, one ductus arteriosus and one pulmonary atresia. MRI demonstrated lesions that echocardiography had either failed to visualize or found inconclusive, including double aortic arch (one patient), muscular ventricular septum defect (two patients) and severe ductus arteriosus (one patient). In one of the two patients with a ventricular septum defect, angiography was avoided and in the other patient it merely confirmed the MRI results. Post-operatively, MRI demonstrated information complementary to that obtained from to 2-D DE: (1) clearly visualizing the reinsertion of the coronary arteries in the ‘switched’ transposition of the great vessels, (2) appreciating the diameter and patency of the palliative shunt in the Blalock-Taussig procedure.
Introduction Recent articles on the use of MRI in congenital heart disease have emphasized the role that this non-invasive technique plays in demonstrating congenital cardiac abnormalities [l-7,13,15,22]. Previously published series have been restricted to adults or young children. As far as we know little consideration has been given to the possible role of cardiac MR imaging in newborns [ 18,241 (patients, age in the range 1 week to 16 years: mean age 46 months). Although many congenital abnormalities of the heart may be well visualized by 2-D DE in infants because of the generally excellent sonic transmission through the chest wall, in some cases 2-D DE still remains inconclusive. Consequently, angiographic procedures are usually necessary for diagnosis. Address for reprints: B. Kastner, M.D., Department of Radiology, Hospices Civils de Strasbourg, 67091 Strasbourg Cedex, France. 0720-048X/90/$03.50
0 1990 Elsevier Science Publishers
Indeed, angiography has drawbacks such as invasive features and potential radiation hazards. In this report on our initial experience with cardiac MR imaging in newborns, we show the feasability of cardiac MRI in a pediatric population of young age and we attempt to determine the clinical benefits of this new imaging technique. Patients and Methods Twenty-three newborns aged l-33 days (mean age 7.5 days) with suspected congenital heart disease were examined with MR imaging. The same imaging procedure was also applied to four patients with no known heart pathology who served as a control group for normal cardiac anatomy. Six of the 23 neonates were growth retarded and four were premature. Patients were not selected but represented our referrals over a 4-month period. Informed consent was obtained in
B.V. (Biomedical
Division)
110
each case from the patients’ parents. One MRI study in a 4-day-old newborn with suspected atresia of the aortic arch was deemed inadequate because of motion artefacts and was excluded from this investigation. The remaining 22 patients included: coarctation of the aorta (four patients); double aortic arch (one patient); transposition of the great vessels (five patients, one had additional situs inversus); ductus arteriosus with pulmonary hypertension (one patient); complete atrioventricular canal (three patients); truncus arteriosus (one patient); left ventricular hypoplasia (one patient); tricuspide atresia with pulmonary stenosis (two patients); ventricular septum defect with pulmonary atresia (two patients); tetralogy of Fallot (two patients). Two patients were controlled post-operatively: one transposition of the great vessels 13 days after a switch (performed after 2 weeks), and one pulmonary atresia 15 days after a Blalock-Taussig shunting procedure (performed after one week). Images were obtained with a 0.5 T superconducting magnet (GE-CGR) by ECG-gated single echo multislice technique, with an echo time of 26 ms and a repetition time determined by heart rate (approx. 300 ms because of the spontaneously high heart rate of the newborns). Sections thickness was 5 mm with no interslice gap. Because even the slightest patient motion distorts the MR images, sedation was compulsory. Adequate sedation of all children was achieved with 3-4 mg of Nembutal or choral hydrate 30-40 mg/kg coupled with feeding 20 min before examination. The patients were placed in the supine or prone position using either the head coil or a surface coil. Imaging was initially performed in the sag&al projection with a nongated gradient echo sequence. Then, spin echo sequences were obtained in axial and in left anterior oblique equivalent planes (LAO) (along the course of the aortic arch), small axis views and/or sag&al views. Each set of ten to twelve images required about 5 min (depending on the heart rate). A complete study (three runs) required approx. 35 min. Echocardiography was performed prior to MR imaging in all patients, with standard commercially available equipment that had a wide angle, pulsed and continuous Doppler capabilities and a high frequency transducer (7.5 MHz). In three patients, intravenous digital substraction angiography (IV-DSA) was also performed. MRI studies were evaluated by two of the authors (B.K. and A.L.). Since the observers were aware of the echocardiographic diagnosis, the study was focused on the complementary information provided by MRI. In all but two patients, the final diagnosis was obtained either by autopsy, surgery or angiography.
Results All newborns withstood the examination by the previously described method well. Suprisingly, the continuous, monotonous noise of the MR imager seemed to soothe the newborns, most of them no longer moving once scanning began. The quality of the MR images is dependent on the fact that the neonates remain motionless during scanning time. Diagnostic MR images were obtained in all but one patient who was not well sedated and whose motion degraded the image quality. In all other patients excellent MR images (comparable to adults) were obtained in spite of the relatively long acquisition times. The rapidly flowing blood within the vessels and cardiac chambers is seen in sharp contrast to the high intensity of the mediastinal fat and medium intensity of the vascular and cardiac walls. Other distinct advantages of this imaging modality are a large field of view and the ability to image multiple projections which allow a step-by-step approach to segmental cardiac and vascular anatomy. The axial planes are suitable for analyzing the position of the ascending aorta with respect to the pulmonary artery, identifying the right and left ventricles which have different anatomic characteristics (i.e., the level of attachement of the septal leaflets of the AV valves), visualizing ventricular or atrial septum defects, and evaluating the pulmonary veins merging into the left atrium. The small axis planes clearly separating the right and left cardiac chambers provide confirmation of transposition of the great vessels, ventricular and atrial septum defects, as well as analysis of the right ventricular outflow tract. The sag&al views are most useful for analyzing the conotruncunal region of the heart. The coronal planes are suited to identify the right atrium, to localize the inferior vena cava, the ascending and descending aorta, the viscera (liver, stomach, spleen) and to visualize the bronchi and the trachea. Two-dimensional Doppler echocardiography provides high-quality images of the cardiovascular system in newborns, because of the great number of echo windows available and the good sonic transmission [ 12,141. Indeed 2-D DE precisely demonstrated most of the various cardiac abnormalities. The diagnosis had therefore been established by 2-D DE prior to MR imaging in all cases but for the double aortic arch. Presurgical results of echocardiographic, MRI and angiographic procedures are summarized in Table I. In three patients with coarctation of the aorta, the lesion was completely visualized on LAO equivalent
111 TABLE
I
Results of 2-D DE - MRI - angiography
in 20 newborns
Case/age (days)/ Clinical diagnosis sex
l/W 2PlM 3/10/F 4/7/M
5/33/M
VIM 1/4/M 8/3/M 9/7/M
10/2/F 11/6/F 12/2/M 13/5/M 14/2/F
15/l/F 16/3/M 11/2/M 18/6/F 19/6/F
20/8/M 20/5/M 22/l/F
+ , diagnosed;
Coarctation Coarctation Coarctation Coarctation
of of of of
the the the the
2-D DE
aorta aorta aorta (S) aorta (S)
MR imaging
Angiography
+
0
+
0
+ -
0 0
Double aortic arch (S) Transposition of the great vessels (S)
+
+ f
0
Transposition Transposition Transposition
+
zk
0
f f
+
+
+
0
+
+
0
+ + +
+
0
+
0
+
0
f
+
+
Truncus arteriosius type I (PM) Left ventricular hypoplasia (PM) Tricuspid atresia with pulmonary stenosis (S) Tricuspid atresia with pulmonary stenosis (S) Ventricular septum defect with pulmonary atresia (S)
+
0
+
0
+
0
+
0
+
0
Ventricular septum defect with pulmonary atresia (S) Tetralogy of Fallot (S) Tetralogy of Fallot (S)
+
0
+
0
+
0
of the great vessels (S) of the great vessels (S) of the great vessels (S)
Transposition of the great vessels, situs inversus and pulmonary stenosis (S) Complete atrioventricular canal (S) Complete atrioventricular canal (S) Complete atrioventricular canal (S) Ductus arteriosus with pulmonary hypertension (S)
+, incomplete
diagnosis;
- , not diagnosed;
Comment (case)
Entire aorta not in one LAO MR projection (4)
+ Ductus arteriosus not visualized by MR imaging (6)
VSD not visualized by 2 DE (8.9) post-surgical MRI at day 21 (switch at day 14)
2 DE not well visualized pulmonary veins (14)
Small axis view did not allow correct diagnosis of pulmonary stenosis (18) Depiction of pulmonary atresia required a 3rd run of MR images (sagittal views) (19) Post-surgical MRI at day 23 (Blalock-Taussig at day 8)
0, study not done; S, surgery; PM, post-mortem.
images displaying the entire aortic arch. In the other patient with coarctation of the aorta, the site of the coarctation could not be directly visualized. In one of the two patients with tricuspid atresia the pulmonary stenosis (diagnosed with 2-D DE) could not be well visualized by MRI on small axis views. In transposition of the great vessels, the anterior posterior relation of the great vessels was clearly seen in all live patients with 2-D DE as well as with MR imaging (Figs. 1 and 2). However, in two patients, 2-D DE did not show distal muscular septum defects (Fig. 3) responsible for left ventricular failure (recurrent pulmonary oedema).
In one of these patients controlled after surgery (switch), only MRI clearly depicted the reinsertion of the coronary arteries in the ‘switched’ aorta (Figs. 4 (a and b) and 5). In the pulmonary stenosis with ventricular septum defect, pre-operatively both imaging procedures were satisfactory, after the Blalock-Taussig procedure, only MRI completely visualized and confirmed the patency of the anastomosis (Fig. 5). In one patient, a patent ductus arteriosus well diagnosed by 2-D DE was not entirely visualized by MR imaging. Intravenous digital subtraction angiography was performed in one infant with a suspected double aortic
Fig. 1. Transposition of the great vessels. LAO image shows the aorta (1) anterior to the pulmonary artery (2) which arises from the left ventricle. Note the ductus arteriosus (straight arrow).
arch, in one newborn with ductus arteriosus and pulmonary hypertension (in order to eliminate an associated pathology like partial anomalous pulmonary venous return) and in one with transposition of the great vessels (to confirm the presence and to appreciate the severity of a muscular ventricular septum defect). In general (pre-operatively), MRI provided more information then 2-D DE in four patients including a
Fig. 3. Transposition of the great vessels with a ventricular septum defect (arrow) clearly depicted by MRI. It was not visualized by 2-D Doppler echocardiography.
double aortic arch (one patient), muscular ventricular septum defect (two patients) and severe ductus arteriosus (one patient). Post-operatively, MRI furnished information complementary to that obtained from 2-D DE in both patients. Discussion
Fig. 2. Transposition of the great vessels. LAO view. The aorta (2) is anterior to the pulmonary trunk (3) and the descending aorta (straight arrow) is well visualized. 1, right atrium; 4, left atrium.
MR imaging, which provides detailed sectional anatomy in multiple body planes, demonstrates congenital intracardiac and great vessel abnormalities in adults and young children as has been reported in several recent articles [l-7,13,15,22]. Our aim was to prove the feasibility and to find applications for cardiac MR imaging in this pediatric population of a young age. We encountered no major difIiculties in ima@g the newborns, thus there is no lower age limit for cardiac MR imaging. This procedure is applicable to and even well tolerated by premature patients. Using the previously described method, the image quality is satisfactory and the pathologic lesions are visualized in most patients [ 17,18,19,21]. MR imaging offers the non-invasive advantages of 2-D DE as well as its ability to image multiple planes; it is non-operator dependent and has a large field of view. But MRI requires sedation and is more expensive, time consuming and less accessible than 2-D DE. Other limits of our MR imager in comparison with 2-D DE are
Fig. 5. Right sided Blalock-Taussig shunt. MRI oblique coronal view (oriented along the course of the right pulmonary artery) displays the anastomosis entirely (size, course, patency as well as pulmonary and subclavian insertion). The shunt (arrow) is patent (signal void). 1, right pulmonary artery; 2, right subclavian artery.
Fig. 4. Transposition of the great vessels. Post-operative axial images (‘switch’). (a) The reinsertion ofthe right coronary artery into the ‘switched’ aorta is clearly depicted (arrow). (b) Note that the left coronary trunc is visible until its bifurcation into circonflex and anterior descending branch (arrow head). The left pulmonary artery (g) is anterior to the ascending aorta. 1, aorta; 2, pulmonary trunc; 3, vena cava superior; 4, left atrium.
the slice thickness (minimum 5 mm for correct signal to noise ratio) and the absence of dynamic heart imaging. 2-D DE is highly sensitive and specific for visualizing the heart and great vessels in neonates and small infants [ 141. Because of the small size of neonates, the good sonic transmission through the chest and the lungs, high
frequency transducers (7 MHz) which greatly increase spatial resolution can be used. Other advantages of 2-D DE are that it allows bedside examination, real time motion studies, multiplane thin slice (2 mm) imaging (because of the great number of available echo windows in the newborn). Therefore, it remains the prime imaging method of congenital heart abnormalities in small infants and newborns. However, 2-D DE even combined with Doppler has limitations such as for-the evaluation of the great arteries, distal muscular ventricular septum defect and posterior cardiac structures (i.e., anomalous pulmonary venous returns and aortic arch anomalies). In adults and young children other authors have found MR imaging to be very useful [1,3,9-l 1,251. This is not suprising because as children grow, the performance of 2-D DE decreases and extra-cardiac structures become difficult to visualize. In our four cases of coarctation of the aorta (visualized by 2-D DE), MR imaging could not determine the exact site of coarctation in one patient. This patient had marked buckling of the aortic arch which therefore could not be displayed entirely on one LAO equivalent
114
image and had to be synthesized from adjacent contiguous slices. However, MR imaging on axial images clearly showed hypoplasia of the aortic arch which can be associated with coarctation. The optimal approach to the diagnosis of vascular rings is a matter of considerable controversy among pediatricians and varies from the recommendation of chest X-ray and barium oesophagography alone to more complex procedures like angiography. Our single case of double aortic arch (not diagnosed by 2-D DE)
cannot resolve this controversy, however the relative ease with which MR can be performed and the experience of others [3,9,16,20,25], justify this procedure for precise anatomic definition and confirmation of diagnosis. MR imaging demonstrated the airway obstruction, the vascular relationship, as well as the relative size and patency of the arches (Fig. 6). As usual, the right arch was higher and larger than the left one which was sectioned at operation. Angiographic images were comparable to MR images. Therefore, MR
Fig. 6. Double aortic arch. (A) axial MR image. (B,C,D) coronal MR images from front to rear. The ascending aorta (a) gives rise to the right (1) and left (2) arches. The right arch is usually larger and higher than the let? arch. The arches encircle the trachea (arrow) which is compressed and converge again to form the descending aorta (d). v, superior vena cava.
115
imaging seems to be the method of choice as it is noninvasive and requires a less heavy sedation than angiography. Transposition
of the great arteries is easily visualized
Fig. 7. Complete atrioventricular canal. Axial images show interventricular communication (curved arrow) limited caudaly by the floor of the common atrioventricular valve (straight arrow). There is also a large atria1 septal defect. The left ventricle (L) is small and the right ventricle (R) is dilated.
Fig. 8. Truncus arteriosus (type I). LAO equivalent projection displays the aorta (1) and the pulmonary artery (2) originating from a common truncus (straight arrow).
Fig. 9. (a) Troncus arteriosus. Transverse image revealing a large ventricular septum defect (arrow). 1, left ventricle; 2, right ventricle. (b) Small axis view of the same patient as in (a). The ventricular septum defect (arrow) is thus confirmed. 1, left ventricle; 2, right ventricle.
116
with 2-D DE in infants and children [ 121. Similarly, MR imaging readily demonstrated abnormal connections among auricular, ventricular and arterial compartments (Figs. 1 and 2). Furthermore, in two cases, MR imaging clearly showed distal muscular ventricular septum defects that could not be identified by 2-D DE (Fig. 3). In both neonates, the ventricular septum defects were responsible for unexplained recurrent left ventricular failure (by shunt excess). Due to the similarity of these cases, angiography was not performed in the second case. In one of two patients with tricuspid atresia and pulmonary stenosis, the pulmonary stenosis was not diagnosed on small axis MR images. This patient was one of the first included in this study and we did not realize that the sag&al views are actually better suited for displaying the right ventricular outflow tract and the initial portion of the pulmonary trunc. We encountered the same difficulties in trying to identify the pulmonary stenosis in the other patient which was readily depicted (better than 2-D DE) only on sag&al views. In the patient with severe ductus arteriosus, angiography was required to eliminate an anomalous pulmonary venous return. Contrary to 2-D DE, MR imaging correctly visualized the pulmonary veins merging into the left atrium. Angiography did not give more clinically relevant information than MR imaging. In all the other cases, including complete atrial ventricular canal (Fig. 7), truncus arteriosus (Figs. 8,9a and 9b) left ventricular hypoplesia, two ventricular septum defects with pulmonary atresia and two tetralogies of Fallot, both MR imaging and 2-D DE provided excellent diagnostic images. After surgical repair, contrary to 2-D DE (because of well-known limited accessibility of extracardiac structures), MRI appreciated the patency of small vascular structures perfectly (initial segment of the coronary arteries and palliative shunting procedure) (Figs. 4 (a and b) and 5). The non-invasive assessment capabilities of MRI in palliative shunting procedure have already been reported in older children [ 8,201. Contrary to the findings of these authors, the shunt in our neonate was entirely visualized on one single view. This may be explained in part by the fact that the diameter of the shunt is small compared with our slice thickness, but also because we use coronal oblique planes oriented along the course of the pulmonary artery (ensuring visualization of the pulmonary insertion of the shunt)
[191. In addition, MRI was capable of visualizing both size and patency of the main and branch pulmonary arteries. Overall, in three patients MRI missed cardiac abnor-
malities but this was not of clinical importance because these lesions (one coarctation of the aorta, one ductus arteriosus, one puhnonary stenosis) were easily depicted by 2-D DE which should nevertheless remain the prime cardiac imaging modality in newborns. MRI yielded more detailed information and therefore usefully complemented echocardiography in five cases: one double aortic arch and two ventricular septum defects (in two transposition of the great vessels) and in the two post-surgical controls. It was not the purpose of this study to suggest that MRI should replace 2-D DE but to show the feasability of MRI in a very young pediatric population and to illustrate its potential complementary role. Noninvasive diagnostic management of congenital heart disease has indeed greatly improved with the introduction of 2-D DE [ 12,141 and Doppler flow mapping. At present, in most cases angiography is no longer required in neonates. But, as sonic transmission through the chest wall becomes poorer with growth of children, and/or chest surgery, MR imaging will certainly play an increasingly important role in the pre- and post-operative assessment of complex congenital heart disease [8,18-21,241. Our preliminary experience is not su&cient to conclude the extent to which MR imaging could replace angiography. But in three neonates where 2-D DE was insufficient and angiography was required (one double aortic arch, one transposition of the great vessels, one severe ductus arteriosus), angiography did not provide more clinically relevant information than MRI. In one patient with transposition of the great vessels and a muscular septum defect (well visualized by MR imaging and not detected by 2-D DE) angiography was avoided. Even with digital substraction angiography (less irradiating), a heavier sedation is required than with MR imaging and the use of contrast media increases the risks as it is an invasive technique. Nevertheless, invasive procedures like angiography and catheterization are presently still mandatory to explore coronary arteries, peripheral pulmonary vessels or to measure cardiac and pulmonary pressures. Our results with static spin-echo images show that MR imaging provides detailed anatomic images of congenital heart disease in the newborn and may be valuable whenever there is a need for more information than echocardiography can provide. MR imaging is a rapidly evolving technique: recent developments such as tine MRI [5,23,24], MR angiography and fast scanning techniques will undoubtedly enhance our ability to use cardiac MR imaging in this very young pediatric population and may therefore offer a serious non-invasive alternative to angiography.
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