Dr. Gonçalves is a Professor, Department of Obstetrics and Gynecology, Division of Fetal Imaging and a Professor, Department of Radiology; Dr. Espinoza is an Assistant Professor, Department of Obstetrics and Gynecology, Division of Fetal Imaging; and Dr. Bronsteen
is an Attending Physician, Department of Obstetrics and Gynecology,
Maternal Fetal Medicine, Division of Fetal Imaging, at Oakland
University William Beaumont School of Medicine, Rochester, MI.
Congenital heart disease (CHD) affects between 4 and 8 of every 1,000 live born infants.1,2
In studies where neonatal echocardiography was performed routinely on
every newborn, the incidence rose to approximately 75 per 1,000 live
births, with most of the difference attributed to the diagnosis of
muscular ventricular septal defects (VSDs) that escaped diagnosis by
clinical examination alone.3
Twenty-five years have elapsed since prenatal ultrasonography was introduced for screening and diagnosis of CHD.4, 5
Despite widespread availability of prenatal ultrasonography, CHD
remains under diagnosed, inclusive of the ductal-dependent lesions that
require intervention shortly after birth.6 The most likely
cause for the lower-than-expected sensitivity of prenatal
ultrasonography to diagnose ductal-dependent anomalies is the difficulty
that inexperienced sonographers have in obtaining standard views and
interpreting abnormalities of the outflow tracts.7 Indeed, it
may take an average sonographer over 2 years of practice to become
proficient in imaging the outflow tracts during routine obstetrical
One of the most effective strategies
reported to date to improve prenatal diagnosis of CHD has relied
strongly on training, continuing education, a low threshold for referral
of suspected abnormalities to specialized fetal echocardiography, and,
above all, a close collaboration between the pediatric cardiologist who
establish the final diagnosis and the ultrasonographer who suspected the
cardiac anomaly in the first place.9
development, 4-dimensional ultrasonography (4DUS) of the fetal heart,
may reduce operator dependency and improve the diagnostic accuracy for
CHD.10-16 4DUS allows examination of volume datasets of the
fetal heart using standard planes of section and rendering techniques.
In this article, we explore the available technology to perform 4DUS of
the fetal heart, tips for volume acquisition,techniques to visualize
standard planes of section, as well as techniques to obtain rendered
views of the great arteries and major veins. We also review previous
studies that addressed how often good volumes can be obtained in the
clinical setting and the diagnostic accuracy of4DUS to diagnose CHD.
Transducers for 4DUS of the fetal heart
The term 4DUS implies that the temporal dimension (motion) has been added to the 3 spatial dimensions of a volume dataset.17
For volume datasets acquired from the fetal heart, this means that a
virtual beating heart can be examined off- or online, resliced in any
plane of section, or reconstructed using rendering techniques, thus
providing the examiner with both structural and functional information.18
For example, a 4DUS volume dataset of a fetus with tricuspid
insufficiency acquired with color Doppler shows not only the tricuspid
valve but also the regurgitation jet that establishes the diagnosis
(Figure 1). This would not be possible with static 3-dimensional (3D)
volume datasets. Most commercially 4DUS transducers available today rely
on mechanical volumetric acquisition. These transducers rely on a
2-dimensional (2D) convex array mounted on a mechanical wobble and are
similar to those used for 3-dimensional ultrasonography (3DUS) of other
body parts (Figure 2). Once volume acquisition begins, the probe
automatically sweeps through a region of interest (ROI), which is
predetermined by the examiner, and a series of consecutive 2-dimensional
images are reassembled into a final volume dataset.
In order to
incorporate the temporal information that is present during acquisition,
gating technology is necessary. Gating allows synchronization of
spatial information to the specific phases of the cardiac cycle, at
which images are acquired. In adult and pediatric echocardiography, the
electrocardiogram (EKG) is used for prospective gating. In fetuses, we
use retrospective gating provided by a technology known as
spatiotemporal image correlation (STIC). STIC relies on temporal Fourier
analysis to estimate the fetal heart rate from systolic peaks that can
be identified in the raw volume dataset.19 Once the heart
rate is known, frames acquired from different spatial positions but
during the same phase of the cardiac cycle are merged into one volume
dataset. The process is repeated for each phase of the cardiac cycle
until a seriesof volume datasets are organized in sequence and played as
an endless continuous cine loop (Figure 3).13 STIC volume datasets can then be examined on- or offline using one of several volume manipulation techniques that are described later in this article.
Matrix array probes
fetal echocardiography can also be performed using electronic matrix
array technology. Matrix array probes allow realtime 4-dimensional (4D)
echocardiography and have been used mostly in adult and pediatric
patients, with fewer articles describing fetal imaging applications.20-27
Matrix array probes are designed as 2D arrays of transducer elements
(currently up to approximately 9000 elements) that can be fired either
simultaneously or in sequence. When fired simultaneously, a pyramid of
ultrasound is produced and real-time 3D examination of cardiac
structures is possible. The examiner can also control the aperture angle
of the transducer by determining how much of the matrix is active at
any time. A narrow aperture angle produces a narrow pyramid of sound
with a high frame rate and the opposite occurs when the full array is
used. If each line of the array is activated in sequence along the
elevation plane, 4DUS volumes of the fetal heart can be generated using
STIC technology, at much faster acquisition speeds than currently
possible with mechanical probes (Figure 4).
How to obtain diagnostic quality volume datasets
same limitations that an examiner faces when performing a 2-dimensional
ultrasound (2DUS) examination of the fetal heart apply to 4DUS. These
are related to poor image quality from maternal obesity, scars from
prior surgeries, artifacts from unfavorable fetal position(spine up),
and excessive fetal motion.28 Therefore, image optimization prior to volume acquisition is essential to obtain diagnostic quality volume datasets.
Two-dimensional image optimization
examiner should favor transducers with the highest possible frequency.
Harmonics may help in case of maternal obesity. It is also best to use
high contrast and low persistence settings as well as a narrow sector
angle to maximize the frame rate. Magnification should be such as to
display only the structures of interest.
few reminders are important prior to volume acquisition. The first is
that volumes acquired from axial images of the fetal heart are optimal
for examination of the 4-chamber view, 5-chamber view, or 3-vessel and
trachea view. In contrast, if the examiner is interested in
reconstructing the aortic arch, the ductal arch, or the venous return to
the heart, sagittal acquisitions work better.18 This is a
consequence of the anisotropic nature of the volume datasets obtained
with current technology, with most of the artifacts presenting in the
sagittal and coronal reconstructed planes.
The ROI to be included
in the final volume dataset should also be as narrow as possible to
maximize the frame rate and temporal resolution. This is particularly
important for acquisitions performed with color or power Doppler, since
these technologies have a negative impact in the frame rate.
most important aspect of volume acquisition, however, is a good acoustic
window to the fetal heart. Ideally, once the examiner obtains a good
quality image of the 4-chamber (4CH) view, the ROI is quickly selected
and volume acquisition is initiated. Although most examiners have a
tendency to begin volume acquisition only when a good 4CH view is
obtained, this is not really necessary. Regardless of the plane of
section displayed on the 2D image, all it takes to obtain a
diagnostic-quality volume dataset is a good acoustic window to the fetal
heart in a fetus that is relatively still. If the fetus moves
significantly, artifacts may make the final volume dataset unusable for
diagnostic purposes. In this case, the only solution is to stop the
acquisition and initiate a new one, repeating the process as many times
as necessary until a diagnostic-quality volume dataset is obtained.
factor that may contribute to motion artifacts in the final volume
dataset is heavy maternal breathing. We customarily ask the mothers to
briefly suspend breathing during acquisition. This is usually well
tolerated, particularly if acquisition time is kept short. Acquisition
time is the amount of time that it takes for the probe to sweep through
the ROI, ranging from 5 to 15 sec formost ultrasonographic equipment
manufacturers. One should keep in mind that, whenever possible, longer
acquisitions are preferred since the spatial resolution of the final
volume dataset will be better, except when there is excessive fetal
motion or maternal breathing.
One last parameter that is set by
the operator is acquisition angle. This controls the extent of the
acquisition sweep and, therefore, how much information is acquired in
the reconstructed z-plane. In general, smaller angles are selected for
young fetuses (eg, 15-20 degrees for
first and early second trimester), and larger angles for older fetuses (eg, 25-35 degrees for late second and third trimester).
Volume acquisition using color Doppler, power Doppler, and B-flow imaging
Volume datasets may be acquired with color Doppler, power Doppler, or B-flow imaging.29-32
Any of these technologies provides a “virtual contrast” to reconstruct
cardiac chambers, vessel lumen, as well as physiologic or abnormal
shunts. The advantage of color Doppler is that blood flow direction and
velocity are present in the volume dataset (Figures 1 and 5). The
disadvantages are poor sensitivity to small blood vessels and the
dependence on an optimal insonation angle (close to 0 degrees). With
power Doppler, sensitivity to low-velocity blood flow is better than
with color Doppler, at the expense of no velocity or blood flow
direction information (Figure 6).Both color and power Doppler suffer
from problems related to low frame rate and poor temporal resolution.
B-flow is a relatively novel imaging modality that allows blood flow
mapping without Doppler (Figure 7). Although the technology does not
provide information regarding velocity or direction of blood flow, it is
extremely sensitive to low-velocity blood flow. Since this technology
relies on B-mode to map blood flow,excellent acoustic window is required
for optimal B-flow imaging. Our anecdotal experience is that rendered
images of ventricular chambers and vessels performed with this
modality are of higher quality when obtained the second trimester of
pregnancy as opposed to later, probably as a result of less acoustic
Exploring the volume dataset
easiest way to explore a 4DUS volume of the fetal heart is to scroll
through the original plane of acquisition or use multiplanar
reformatting to display the structures of interest. The multiplanar
display of most commercially available equipment usually demonstrates
the original plane of acquisition in one panel (eg, the upper right
corner), with orthogonal sagittal and coronal reconstructed planes
displayed in additional panels (Figure 8). A reference dot or crosshair
representing the intersection in space of the 3-orthogonal planes is
shown in all images. The examiner can drag this reference dot on the
screen to navigate through the volume dataset and simultaneously show
the same structure in multiple planes.
Offline assessment of the
fetal heart is conducted in a manner similar to a real 2DUS examination.
The sequential segmental approach can be used to explore the volume
dataset, with the fetal heart divided into 3 basic segments (atria,
ventricles, and great arteries) connected by atrioventricular and
segmental analysis begins by determining fetal orientation and atrial
situs. Ideally, the right and left atria and their position in
relationship to each other can be defined based on the morphology of the
atrial appendages. In practice, atrial situs is often evaluated by
determining the arrangement of the abdominal great vessels with respect
to the spine at the level of the diaphragm. In situs solitus, the
inferior vena cava (IVC) lies to the right of the spine and anterior to
the left-sided aorta; the stomach is located on the left side; and the
portal vein on the right (Figure 8). This arrangement usually implies
that the morphologically right atrium is to the right of the
morphologically left atrium, regardless of the position of the heart
within the chest. Situs inversus implies a mirror-image arrangement of
the normal pattern. In right isomerism both great vessels are positioned
on the same side of the spine (either right or left), and in left
isomerism, the IVC is usually interrupted and continues with the azygous
vein towards the thorax.37
junction is examined next. If concordant, the morphologically left
atrium connects to the morphologically left ventricle, and the
morphologically right atrium to the morphologically right ventricle. The
moderator band helps to identify the right ventricle. Additional
landmarks include the more apically inserted tricuspid valve and chordal
attachments to the ventricular septum(Figure 9). The left ventricle is
smoother, does not have a moderator band, and the mitral valve only has
chordal attachments to the free wall.
connections are checked next. Here is where 4DUS can really help.
Several techniques that rely either on multi-planar display
(“three-step”,13, 15 “spin”,11 “tomographic ultrasound imaging”,38-40 STAR,41 FAST42)
or rendering algorithms have been described to consistently obtain the
outflow tracts from volume datasets acquired from the 4-chamber view.
Regardless of the technique, the goal is to demonstrate that the aorta
connects to the left ventricle and that the pulmonary artery connects to
the right ventricle (Figures 5, 6,and 10). The pulmonary artery
crisscrosses over the aorta as it leaves the heart and should be
followed to its bifurcation and to the ductus arteriosus. The ascending
aorta should be followed to the aortic arch.
The next steps are to
check the venous connections to the atrial chambers (pulmonary veins to
the left atrium and IVC and superior venacava to the right atrium),
double check AV valve morphology, and determine if there are any defects
in the ventricular septum.
Techniques to explore the volume dataset using multiplanar display
mentioned previously, a variety of techniques have been published to
explore volume datasets of the fetal heart obtained withSTIC.11,13,29,30,31,38-42 A
detailed description of each technique is beyond the scope of the
article and the reader is directed to the original references for a more
detailed description of each. Here we will focus on those techniques
that we are more familiar with and, therefore, use more frequently in
our clinical practice.
This is a simple technique that can be used to explore the full length and anatomical relationships of any cardiac structure.11
The basic principle is that once the reference dot is anchored in the
structure of interest and the volume dataset is rotated around its y- or
x-axis, the structure “opens up,” depicting previously hidden
anatomical relationships with other structures. Figure 11 illustrates
the spin technique applied to a cross-sectional view of the fetal chest
at the level of the 3-vessels and trachea view. Note the extra-vessel
located to the left of the pulmonary artery/ductus arteriosus, which is
marked with a question mark. Once the reference dot is placed on that
vessel and the volume dataset is rotated around the y-axis, it becomes
clear that the vessel in question is a persistent left superior vena
cava draining to a dilated coronary sinus.
Three-step technique to evaluate the outflow tracts
technique allows simultaneous visualization the long-axis view of the
left ventricular outflow tract and the short-axis view of the right
ventricular outflow tract in 2 separate panels displayed on the same
screen. The technique works best when the original plane of acquisition
is axial with full description and illustration provided in Figure 10.
We have previously shown good inter-and intraobserver reproducibility
for this technique.43 More recently, Rizzo et al15
reported reasonable diagnostic accuracy for this technique to diagnose
conotruncal anomalies among examiners who were blinded to both
indication and final diagnosis. In his study, volume datasets of the
fetal heart were obtained from 112 consecutive unselected and 10 fetuses
with congenital heart disease and stored for later offline examination.
Both examiners correctly detected the single abnormal case of
hypoplastic left-heart syndrome among the 112 unselected fetuses. Among
the 10 preselected cases with congenital heart disease, examiner “A”
considered 3 volumes as inadequate [2 cases of tetralogy of Fallot (TOF)
and one case corrected transposition of the great arteries (TGA)], and
correctly diagnosed 3 cases of TOF, 2 cases of complete TGA, and one
case of interrupted aortic arch. Examiner B considered 4 of the volumes
to be nondiagnostic (2 cases of TOF, one case of complete TGA, and one
case of corrected TGA), missed the diagnosis of interrupted aortic arch,
interpreted one case of TOF as double outlet right ventricle, and
correctly diagnosed 2 cases of TOF, and 2 cases of complete TGA. Figures
12 and 13 depict the use of this technique in TOF with pulmonary
atresia and complete TGA, respectively.
Technique to visualize the ductal arch from volumes obtained from the 4-chamber view
simple technique allows examiners to consistently obtain a view of the
ductal arch in the reconstructed sagittal plane from volume datasets
obtained from the 4-chamber view (Figure 14). Espinoza et al
demonstrated that failure to visualize the ductal arch with this
technique is associated with a high rate of conotruncal abnormalities
[94.4% (17/18)] when compared to normal hearts [6.9% (8/116)] or hearts
affected by other CHD [21.6% (7/34)] (p<0.01 for all comparisons).44
Tomographic ultrasound imaging
alternative to scrolling through the original plane of acquisition is
to automatically reslice the volume dataset. This has been variously
called tomographic ultrasound imaging or multislice imaging, depending
on the manufacturer.38,40 Tomographic ultrasound imaging
allows the examiner to simultaneously see the multiple planes of section
along the original acquisition plane (or alternatively sagittal or
coronal reconstructed planes) in a single screen and, therefore, may
facilitate looking at the multiple facets of complex cardiac anomalies
Manual drawing of lines in the volume dataset to obtain standard planes of section
introduced technological developments for volume manipulation allows
examiners to manually trace lines through a longitudinal view of the
ductal arch in a volume dataset and obtain the standard planes of
section required for a thorough examination of the fetal heart fairly
consistently. Two variations of the technique have been described, the
‘FAST’ and the ‘STAR’ techniques, with illustrations of each provided in
Figures 16 and 17.
Automated algorithms to examine the fetal heart by 4DUS
The normal spatial relationship of cardiac structures to each other has been mathematically described.45
Investigators have taken advantage of the relatively fixed relationship
between anatomical components of the fetal heart to develop automated
algorithms to extract standard fetal echocardiography views from volume
datasets.46,47 A preliminary study using volume datasets
collected from cases of congenital heart disease shows promise in the
prenatal diagnosis of complex disorders such as d-transposition of the
4D-rendered images of the fetal heart
of the unique capabilities of volumetric imaging is to allow rendered
reconstruction of cardiac structures. Rendered views of the great
vessels can be obtained with a variety of techniques, including
inversion mode for volume datasets acquired using gray scale only
(Figure 18, D-TGA), color Doppler (Figures 1 and 5), power Doppler
(Figure 6), and B-flow imaging (Figures 7 and 19). Prenatal diagnosis of
abnormalities involving the great vessels, such as transposition of the
great arteries, tetralogy of Fallot, truncus arteriosus, and double
outlet right ventricle have been reported by several groups using one or
more of these technologies.29,30,31,49, 50, 51-57 Of
particular interest is the exquisite characterization of difficult
abnormalities, such as major collateral pulmonary arteries in the
setting of pulmonary atresia with VSD,32 interrupted aortic arch with associated cervical origin of the right subclavian artery,56 and total anomalous pulmonary venous return54,55 (Figure 19) that have been reported using rendered images of the fetal vessels obtained with b-flow imaging.
Evaluation of cardiac biometry and function with 4D fetal echocardiography
several groups around the world have reported their initial experience
with volumetric measurements of fetal cardiac structures using 4DUS
volume datasets. Parameters such as end-diastolic volume, end-systolic
volume, ventricular mass, ventricular-septum area, and derived
functional parameters, such as ejection fraction, stroke volume and
cardiac output, have been reported with good reproducibility.58-73
Feasibility of 4D fetal echocardiography in clinical practice
relevant question is whether 4DUS can be used routinely to examine the
fetal heart in clinical practice. With the capabilities demonstrated in
previous sections of this article, a reasonable expectation is that
routine use of the technology could result in reduction of the
examination time with a concomitant increase in diagnostic accuracy.
This would likely be true if a volume dataset of sufficient diagnostic
quality could be obtained from every pregnant patient scanned.
Unfortunately, unfavorable fetal position (spine up), excessive fetal
movement, and maternal obesity are encountered frequently enough in
clinical practice to prevent less than optimal volume acquisitions in a
significant number of cases. Two studies have addressed this issue. In
the first, 2 experienced sonographers scanned 165 high-risk fetuses with
no suspected CHD. No more than 4 attempts to acquire a volume dataset
were allowed during each examination. Data was analyzed for rate of
successful volume acquisition, final number of volume datasets
considered nondiagnostic as well as factors associated with poor quality
of the volume datasets. Among the 148 cases where acquisition was
attempted, storage errors occurred in 7, and successful acquisition was
achieved in 76% of the cases. Of these, only 25% of the volumes were
considered to be of high quality (n=26), 40% (n=42) were diagnostic but
not high quality, and 35% (n=37) were considered nondiagnostic. Factors
associated with poor quality volume datasets were anterior placenta (56%
vs. 30%, p=0.05) and maternal obesity (mean BMI 26.5 kg/m2 vs. 23.8 kg/m2, p = 0.04).74
In another study, examinations conducted between 18 and 22 weeks of
gestation with a maximum allocated time of 40 min showed that the
4-chamber, left outflow tract and right outflow tract views could be
obtained in 70% to 83.8% of the time. An anterior placenta and fetal
position with the spine up were the main cause of nondiagnostic
studies have addressed the issue of diagnostic accuracy of 4D fetal
echocardiography. In one recent study, 2D video clips documenting fetal
echocardiographic examinations in 181 fetuses with CHD were reviewed
blindly and compared to volume datasets obtained in the same fetuses.
Twelve additional cardiac anomalies (right aortic arch with anomalous
branching, transposition of the great arteries with pulmonary atresia,
interrupted aortic arch, right ventricular aneurysm, total anomalous
venous return, and VSDs) were identified only by 4DUS.76 Bennasar et al10
evaluated the volume datasets of 342 fetuses referred for suspected CHD
and examined by both 2D and4DUS. Volume datasets were reviewed only one
year after the initial study and the accuracy to diagnose CHD compared
between 2DUSand 4DUS. The overall accuracy for diagnosis of CHD was 91%
for 4DUS compared to 94.2% for 2DUS, but the difference was not
statistically significant. There were 9 false-negative diagnoses with
4DUS (9 VSDs and 1 interruption of the aortic arch) compared to 3 by
2DUS(2 VSDs and 1 persistent left superior vena cava), but the
difference was not statistically significant. 4DUS had 19 false-positive
diagnoses (10 VSDs, 4 coarctation of the aorta, 2 persistent left
superior vena cava, 1 pulmonary stenosis, 1 tricuspid dysplasia, and 1
rhabdomyoma)compared to 17 false-positive diagnoses by 2DUS (11 VSDs, 4
coarctation of the aorta, 1 tricuspid dysplasia, and 1 ostium primum
atrial septal defect); again the differences were not statistically
significant. The authors reported, in their center, that successful
volume acquisition was possible in 98% of the cases, and that, given the
results of their study, 4DUS could be incorporated into the clinical
setting with accuracy for prenatal diagnosis of CHD similar to 2DUS. In
an additional multicenter study, 90 volume datasets of fetuses with and
without congenital heart disease where uploaded to a central server, and
experts at 7 different centers were asked to review the volume datasets
blinded to the final diagnosis. Sensitivity and specificity for the
diagnosis of CHD in this setting were 93% (95% CI 77 to 100%) and 96%
(95% CI 84 to 100%), respectively, with excellent intercenter agreement
echocardiography is an emerging technology that adds to the diagnostic
armamentarium of the fetal imager in the difficult task of prenatal
diagnosis of congenital heart disease. Once a volume dataset of
sufficient diagnostic quality is acquired and analyzed by experts, a
correct diagnosis can be achieved in the majority of cases.10,12
This opens up the possibility of volume datasets of the fetal heart be
used in the future for remote consultations in a telemedicine imaging
environment.77-79 The bottleneck for more ample utilization
of this technology in the clinical setting appears to be the inherent
limitations of current ultrasound technology to deal with factors that
degrade 2DUS image quality, such as fetal movement, unfavorable fetal
position, anterior placenta, and maternal obesity. We hope that future
developments that address these problems can eventually lead to more
widespread utilization of 4DUS fetal echocardiography in clinical
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