Preliminary experience with cardiovascular magnetic resonance in evaluation of fetal cardiovascular anomalies
© Dong et al.; licensee BioMed Central Ltd. 2013
Received: 3 February 2012
Accepted: 15 April 2013
Published: 21 May 2013
The cardiovascular system is the part of the fetal anatomy that most frequently suffers from congenital pathology. This study shows our preliminary experience with fetal cardiovascular magnetic resonance (CMR) to evaluate congenital cardiovascular abnormalities.
Between January 2006 and June 2011, Prenatal routine obstetric ultrasound (US), echocardiography and CMR data from 68 pregnant women carrying fetuses with congenital cardiovascular anomalies were compared with postnatal diagnoses (postnatal imagings, surgery and autopsy). All prenatal CMR was performed at 1.5 T. Imaging sequences included steady-state free-precession (SSFP) sequences, real-time SSFP and single-shot turbo spin echo (SSTSE) sequences. The images were analyzed with an anatomic segmental approach by two radiologists.
Fetal CMR yielded the same diagnosis as postnatal findings in 79% (54/68) of patients. The diagnostic sensitivity of routine obstetric US for cardiac anomalies was 46% (31/68). The diagnostic sensitivity of fetal echocardiographic examination by a fetal cardiac specialist was 82% (56/68). In 2 (3%) of 68 cases, diagnoses with both echocardiography and CMR were incorrect when compared with postnatal diagnosis. In ten (15%) cases, diagnosis at echocardiography was incorrect and that at CMR was correct. In twelve (18%) cases, diagnosis at echocardiography was correct and that at CMR was incorrect. Ten cases missed or misdiagnosed by echocardiography but correctly diagnosed by fetal CMR included asplenia syndrome (n = 2), interrupted inferior vena cava of polysplenia syndrome (n = 1), tricuspid incompetence (n = 1), double outlet right ventricle (n = 2), double aortic arch (n = 1), right pulmonary artery hypoplasia (n = 1), right-sided aortic arch of tetralogy of Fallot (n = 1) and hypoplastic left heart syndrome of a twin fetus (n = 1).
Fetal CMR is a promising diagnostic tool for assessment of congenital cardiovascular abnormalities, especially in situations that limit echocardiography.
The cardiovascular system is the part of the fetal anatomy that most frequently suffers from congenital pathology . The fetal heart is routinely studied using first level obstetric ultrasound (US). If a fetus is considered to have a cardiovascular defect, a detailed echocardiographic examination is required. The role of fetal cardiovascular magnetic resonance (CMR) as a tool additional to ultrasound has grown exponentially. Unlike ultrasound imaging, however, CMR is relatively unaffected by maternal and fetal conditions such as obesity, oligohydramnios and fetal complex malformations of various organ systems which particularly impair sonographic visualization of the fetal heart and great vessels. CMR avoids exposure to ionizing radiation and to the best of our knowledge, no clinical or experimental evidence has indicated that CMR has any adverse effects on the human fetus . Recently, the successful development of new sequences during free breathing without cardiac triggering has established the beginning of a potential role for CMR in the study of the fetal cardiovascular system [3–5]. The literatures regarding the CMR diagnosis of fetal cardiovascular anomalies is composed essentially of case reports [6–8]. To the best of our knowledge, however, a large group of patients with a fetal cardiovascular abnormality diagnosed by CMR has rarely been reported either from a single center or as pooled data from multiple centers . Here, we review 68 cases and report our preliminary experience with fetal CMR in the diagnosis of the cardiac and vascular malformations.
Postnatal evaluation methods to determine the final diagnoses
No. of neonates
CMR and echocardiography
Cardiac CT and echocardiography
Cardiac angiography and echocardiography
Surgery and echocardiography and CMR or CT
Magnetic resonance imaging
Between January 2006 and December 2010, prenatal CMR was performed using a 1.5-T unit (Signa Echospeed; GE Medical Systems, Milwaukee, WI, with 33 mT/m gradients) and an eight-channel phased array cardiac coil. After December 2010, prenatal CMR was performed using a 1.5-T unit (Achieva Nova dual; Philips Medical Systems, Best, The Netherlands, with 60 mT/m gradients) and an sixteen-channel sense-xl-torso coil. In order to minimize claustrophobia, the patients were placed in the magnet in a supine, feet-first position. Imaging sequences of GE included a fast imaging employing steady-state acquisition (FIESTA) sequence (TR/TE, 3.6/1.8 msec; field of view, 260–340 mm2; section thickness, 4–5 mm; spacing, 0–0.5 mm; matrix, 224 × 224–256 × 256; flip angle, 45–60°), a “real-time” non-gated FIESTA cine CMR sequence and a single-shot fast spin-echo (SSFSE) sequence (TR/TE, 1150–1450/90–135 msec; field of view, 250–300 mm2; section thickness, 4–6 mm; spacing, 0–0.5 mm; matrix, 256 × 160–256 × 192; flip angle, 90°). Imaging sequences of Philips included a balanced turbo field echo (B-TFE) sequence (TR/TE, 3.6/1.8 msec; field of view, 260–325 mm2; section thickness, 4–6 mm; spacing, -2–4 mm; matrix, 172 × 173–216 × 218; flip angle, 80°), a “real-time” B-TFE (B-TFE-RLT) sequence and a single-shot turbo spin echo (SSTSE) sequence (TR/TE, 12000/80 msec; field of view, 260–355 mm2; section thickness, 4–6 mm; spacing, 0–0.5 mm; matrix, 172 × 173–236 × 220; flip angle, 90°).
SSFP and SSTSE sequences provide T2-weighted images [5, 10]. SSFP images were acquired in the transverse, four-chamber, short-axis, coronal and oblique sagittal views. SSTSE images were acquired only in an oblique coronal view in order to show the bronchus and for evaluation of the visceroatrial situs. Non-gated SSFP cine CMR was acquired in the transverse and short axis views. The total acquisition time was approximately 10–20 seconds per SSFP or SSTSE sequence, and the examination duration averaged approximately 20 min. No sedatives, intravenous gadolinium-based contrast media, or fetal cardiac gating were used.
All fetal MR examinations were performed and the images interpreted in consensus by two authors (S.Z.Dong and M. Zhu). S.Z. Dong had 10 years of experience in fetal US imaging and 8 years of experience in fetal CMR, M. Zhu had 30 years of experience in pediatric cardiac imaging and 8 years of experience in fetal CMR. All examinations were performed with prior knowledge of the first level obstetric ultrasonographic findings. The echocardiography results were available and known in 41 (60%) of 68 cases and not known in other 27 (40%) cases to the CMR radiologist at the time of acquisition and interpretation of MR images. But all postnatal results were not known to the CMR radiologist when MR images were interpreted.
Visceroatrial situs: The stomach normally lies to the left and the liver and inferior vena cava to the right. Assessment of the situs in relation to the bronchial tree was attempted in each case. The embryologically normal left main bronchus is long with no early division and runs under the left pulmonary artery, whereas the right one is short, closer to vertical, has an early division and runs behind the right pulmonary artery.
Position of the heart, cardiac apex and cardiac axis: Most of the heart normally lies in the left thorax with the cardiac apex to the left, only a small portion of the left atrium, about half the right atrium and a tiny corner of right ventricle lie in the right thorax. The normal cardiac axis lies at a 45°angle (range 22–75°) between the true sagittal plane (between the spine and the anterior chest wall) and a plane along the interventricular septum.
Ventricular looping: In a normal D-loop, the more anterior ventricle is the morphologic right one with a trabeculated septal wall and the most posterior is the morphologic left one.
Atrioventricular junction and cardiac chambers: In concordant AV connection, the right atrium connects to the morphologically right ventricle and the left atrium to the morphologically left ventricle. Seen in a balanced four-chamber view, the number of cardiac chambers, relative size of both atria and both ventricles were evaluated.
Ventriculoarterial connections: Normally the aorta is connected to the morphologically left ventricle. The pulmonary artery normally is connected to a morphologic right ventricle and bifurcates at its distal end. The aorta can be traced in a regular arch that gives rise to three neck vessels. The main pulmonary artery crosses above the aortic root in a sagittal plane. The relative size of the aorta and pulmonary artery was evaluated.
The systemic and pulmonary venous connections: Normally, both superior and inferior vena cava join the right atrium, and two right and two left pulmonary veins connect to the left atrium. The number of superior and inferior vena cava was evaluated.
The following cardiac and other organ structures also were analyzed: Number and side of the aortic arch, intactness of interventricular septum, atrioventricular and great arterial valves, appearance and location of the liver and presence, appearance, and number of spleens.
Frequency of confirmed fetal cardiovascular anomalies
Frequency of confirmed congenital cardiovascular anomalies by means of postnatal final diagnosis (reference standard)
Frequency of abnormalities of the cardiovascular system
No. of fetuses
Heterotaxy, cardiosplenic syndromes
Persistent left superior vena cava without other CHD
Atrial septal aneurysm
Atrioventricular canal defects
Ventricular septal defect
Double outlet right ventricle
Persistent truncus arteriosus
Transposition of great arteries
Coarctation of the aorta
Interruption of the aortic arch
Double aortic arch
Right-sided aortic arch without TOF
Pulmonary atresia with VSD (PA/VSD)
Absent one pulmonary artery
Right pulmonary artery hypoplasia
Tetralogy of Fallot
Hypoplastic left heart syndrome
Comparison between all diagnostic results
Comparison between prenatal echocardiographic results, fetal CMR and postnatal findings
Both echo and CMR incorrect
Echo correct, CMR incorrect
Echo incorrect, CMR correct
TI (right cardiomegaly diagnosed at both)
Two atrioventricular canal defects (common atrioventricular valve missed at CMR)
Asplenia syndrome with omphalocele (cardiac structure not clearly showed at Echo)
Persistent truncus arteriosus (PA/VSD suspected at both)
*Two TA (absent TV not clearly showed at CMR)
Asplenia syndrome with CDH (RAoA, PLSVC, DAo and IVC on the same side missed at Echo)
Ebstein anomaly (dilated right atrium diagnosed at CMR)
Polysplenia syndrome (interrupted IVC missed at Echo)
Two small VSD (3 mm,missed at CMR)
*TI (thinned DA missed at Echo)
CoA (mild, missed at CMR)
DORV with VSD, bilateral multicystic dysplastic kidney and oligohydramnios (DORV missed at Echo)
PS (not clearly showed at CMR)
DORV with CAVC and polyhydramnios (DORV missed at Echo)
*Two right pulmonary artery hypoplasia (hypoplastic pulmonary artery not clearly showed at CMR)
Double aortic arch (not clearly showed at Echo)
TOF (overriding aorta not clearly showed at CMR)
Right pulmonary artery hypoplasia (only one scoliosis diagnosed at Echo)
* TOF (right-sided aortic arch missed at Echo)
HLHS of a twin fetus (cardiac structure not clearly showed at Echo)
In twelve (18%) cases, diagnosis at echocardiography was correct and that at CMR was incorrect. In 2 (17%) of 12, tricuspid atresia (TA) was correctly suspected by CMR according to significantly reduced right ventricle, but absent tricuspid valve was not clearly showed at CMR. In 2 (17%) of 12, hypoplastic right pulmonary artery was not clearly showed at CMR, but right lung hypoplasia was correctly diagnosed by CMR. Other eight (67%, 8/12) cases included two cases of atrioventricular canal defects, one case of Ebstein anomaly, two cases of small ventricular septal defects (VSD, 3 mm), one case of coarctation of the aorta (CoA), one case of pulmonary stenosis (PS) and one case of the overriding aorta of tetralogy of Fallot (TOF) (Table 3). In twelve cases, fetal CMR was performed at gestational age from 22 to 26 weeks.
Prenatal cardiac imaging is critical for the early diagnosis of congenital cardiovascular anomalies as well as for the management of the pregnancy in terms of counseling and delivery planning. CMR has now been confirmed as an important complementary tool to add to obstetric ultrasound for examining the fetal central nervous system, fetal non-central nervous system disorders, and placental and uterine diseases [12–15]. CMR has also emerged as a powerful approach to imaging congenital heart disease in neonates and infants. CMR avoids exposure to ionizing radiation, and at present, there is no evidence that short-term exposure to electromagnetic fields of 1.5 T or less harms the fetus [2, 16, 17]. CMR has the potential to expand its ability to image the fetal congenital cardiovascular abnormalities [9, 18]. The very preliminary work presented here suggests that diagnoses of fetal congenital cardiovascular anomalies can be obtained in most patients using fetal CMR.
Although fetal echocardiography has been used successfully for many years in the diagnosis of fetal congenital cardiovascular abnormalities, there is a need at times for additional information without limitation to the acoustic windows . The usual timing of fetal echocardiography for the premature diagnosis of congenital heart disease is at approximately 20–26 weeks of gestation. During the later phases of gestation, the development of certain conditions (e.g., relative reduction of the amniotic fluid volume and intensification of calcification in the ribs) may impair the quality of the fetal echocardiography examination . In this study, in the majority of ten cases missed by echocardiography, fetal echocardiography was performed at gestational age less than 22 weeks or greater than 28 weeks.
CMR has no such limitations. CMR is also relatively unaffected by maternal and fetal conditions such as obesity, twins, oligohydramnios, polyhydramnios and fetal complex malformations of various organ systems [12, 21], which particularly impair echocardiographic visualization of the fetal heart and vessels. Therefore, if structures cannot be visualized by fetal echocardiography, CMR can be considered as an alternative imaging modality. In this study, after suspected cardiac abnormalities or unclear cardiac structure with routine obstetric US or echocardiography, 68 fetuses have been referred for CMR to corroborate the diagnosis and search for associated extracardiac anomalies. The results showed that 50% (5/10) cases missed by echocardiography were associated with extracardiac abnormalities that alter the anatomy of torso or abnormal amniotic fluid volume thus affecting the diagnosis of the cardiovascular malformations, but the cases with extracardiac malformations were all correctly diagnosed by fetal CMR. In addition, a twin fetus with hypoplastic left ventricle syndrome, owing to large gestational age (32w) and twin pregnancy, was not clearly showed at echocardiography, but successfully diagnosed using fetal CMR. It is because this group of patients including many cases of complex heart defects and complex extracardiac malformations of various organ systems, the diagnostic accuracy of fetal echocardiography was slightly lower (82%).
As regards to technical matters, SSFP sequences produce good quality images of the fetal heart and vessels. On SSFP images, blood is characterized by a high signal intensity, thereby improving the blood-to-tissue contrast at the endocardial surface, and thus permitting the cardiac chambers and vessels to be imaged [3, 18]. On non-gated cine MR images, the movements of the atria and the ventricles are reproduced as a video, thus allowing the cardiac kinetics to be evaluated, especially cardiac valve regurgitation and shunt which are not seen on the static SSFP images. However, the temporal and spatial resolution of the images on the non-gated cine SSFP sequence are usually not very good. If one was only to image with static SSFP, that is generally adequate for anatomic imaging. The most efficient technique for characterizing the fetal cardiac anatomy appears to be SSFP sequences used in conjunction with non-gated SSFP cine sequences. Radiofrequencies pose a potential safety risk for the fetus. In our examination, the ceiling of the specific absorption rate was 3.0 W/kg. We found that the flip angle could be changed in order to the control of specific absorption rate and that the image remained almost unchanged. With advances in CMR technology such as self-gating, real cardiac gating and metric optimized gating [22–24], both temporal and spatial resolution will improve. Accordingly, images will be considerably clearer, and take less time to acquire. In the future, CMR will become a more important diagnostic tool for fetal congenital cardiac and vascular abnormalities.
When compared to echocardiography, fetal CMR does have some limitations. Fetal movements can affect imaging. Cardiac contractility and valvular functionality (atrioventricular and vascular) cannot be currently evaluated reliably with fetal CMR. CMR sometimes missed small ventricular septal defects and hypoplastic great vessels.
Our study has limitations. The number of cases of each pathology is small. Types of cases does not include pulmonary vein anomalies.
In conclusion, CMR avoids exposure to ionizing radiation and is relatively unaffected by the conditions that impair echocardiographic visualization. Fetal CMR can be a promising diagnostic tool for assessment of congenital cardiovascular abnormalities, especially in situations that limit echocardiography. Our initial CMR results demonstrate that CMR is a useful adjunct in the assessment of fetal complex malformations of various organ systems (cardiac and extracardiac) and cardiosplenic syndromes. Further advances in technology will expand the role of fetal CMR in the evaluation of the fetal heart and vessels in the future.
This work was supported by a grant from National Natural Science Foundation of China (30970795) and by a grant from Science and Technology Commission of Shanghai Municipality (10DZ1951200 and 10DZ1951201).
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