Seminars in Fetal & Neonatal Medicine 23 (2018) 112e118

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Seminars in Fetal & Neonatal Medicine

journal homepage: www.elsevier.com/locate/siny

Advances in fetal echocardiography

Helena M. Gardiner*
The Fetal Center at Children's Memorial Hermann Hospital, McGovern Medical School at UTHealth, The University of Texas Health Sciences Center at
Houston, Houston TX, USA

a b s t r a c t
Keywords: The development of fetal echocardiography and success in prenatal cardiac screening programs over
Congenital heart disease the past 30 years has been driven by technical innovation and influenced by the different approaches
Echocardiography
of the various specialties practicing it. Screening for congenital heart defects no longer focuses on
Fetal
First trimester
examining a limited number of pregnant women thought to be at increased risk, but instead forms an
integrated part of a high-quality anatomical ultrasound performed in the second trimester using the
‘five-transverse view’ protocol. A prenatal diagnosis is feasible in almost all cardiac lesions and the
advantages to parents and to health professionals are well recognized. Prenatal evaluation can usually
determine the level of care required at delivery, thereby reducing perinatal morbidity. However, only
half of the babies undergoing surgery within the first year of life have a prenatal detection, and
practical training programs to support and provide feedback to sonographers remain essential for
continued improvement.
© 2017 Elsevier Ltd. All rights reserved.

1. Introduction
The development and growth of fetal echocardiography and
success in prenatal cardiac screening programs over the past 30
years has been driven by technical innovation and, unlike most
specialties with relatively homogeneous roots, has been influenced
by the different approaches of the various specialties practicing it.
Its original practice was pioneered by obstetricians and radiol-
ogists, and biomedical engineers. More recently, it has been
developed by specialists from fetal medicine, prenatal diagnosis,
and pediatric cardiology. Screening programs for fetal abnormal-
ities in different countries are performed by those with a technical
training or by nurses with midwifery experience.
Software development and improved computer processing po-
wer have made ultrasound a powerful tool for prenatal diagnosis.
Importantly the technology is relatively adaptable, not requiring an
expensive environment as with magnetic resonance imaging or
computed tomography, and so it has gained worldwide acceptance.
This prenatal hybrid specialty grows at scientific gatherings where
its practitioners meet to cross-fertilize ideas and produce
outstanding research. These factors make the specialty barely
* The Fetal Center, UT Health School of Medicine, 6410 Fannin Street e Suite 700,
Houston, 77030 TX, USA.
E-mail address: Helena.m.gardiner@uth.tmc.edu.
recognizable from 30 years ago and its growth is a tribute to the
efforts of expert teams and the ultrasound manufacturers who
work together to continue to push the boundaries of what can be
seen and measured. This has permitted development of fetal car-
diovascular medicine beyond its initial aim, the identification of
structural congenital heart defects, and has opened up possibilities
to observe development and function non-invasively in both
normal and complicated pregnancies.
2. Second trimester screening
The birth of a baby with a congenital heart defect (CHD) is a
relatively frequent occurrence given that CHD is one of the most
prevalent birth defects, affecting almost 1% of all pregnancies. A
prenatal diagnosis is feasible in almost all lesions and the advan-
tages to parents and to health professionals are well recognized
[1,2]. Prenatal diagnosis has been shown to improve morbidity and
pre-surgical mortality and reduce costs associated with trans-
portation and resuscitation of collapsed newborns [3,4]. Prenatal
screening programs allow the pregnant woman to discuss further
investigations including prenatal genetic testing and imaging and to
inform reproductive decision-making. The family can come to terms
with the perinatal management plan, including the prospect of
cardiac surgery, over a period of months rather than in hours when a
cardiac diagnosis is made only after delivery. However, prediction of
quality of life for children with CHD remains difficult [5,6].

https://doi.org/10.1016/j.siny.2017.11.006
1744-165X/© 2017 Elsevier Ltd. All rights reserved.
 H.M. Gardiner / Seminars in Fetal & Neonatal Medicine 23 (2018) 112e118 113

Fig. 1. The five transverse views through the fetal body displaying the cardiac screening planes. This is an educational poster developed by Dr Gardiner and GE Healthcare.

2.1. Expectations and advantages mortality [10].

In most cases a baby with CHD can be born at term by vaginal
delivery, ideally in a maternity unit within, or co-located, with the
cardiac center. Cesarean section is indicated for fetuses with com-
plete heart block who cannot be monitored safely during labor, or
with poor cardiac function. However, in practice a prenatal diag-
nosis is associated with earlier delivery and higher rates of opera-
tive delivery for a variety of reasons, usually because of associated
lesions or poor fetal growth [7,8]. There is also the option to plan for
palliative perinatal management for fetuses that are extremely sick,
or have multiple abnormalities, or life-limiting genetic disorders
[9].
Prenatal evaluation can usually determine the level of care
required at delivery, so health professionals with the appropriate
skills can confidently manage the transitional circulation and any
extra-cardiac malformations in the certainty of an accurate pre-
natal cardiac diagnosis and thereby reduce perinatal morbidity and
2.2. Screening guidelines and referral
Screening for CHD no longer focuses on examining a limited
number of pregnant women thought to be at increased risk of fetal
CHD [11,12]. Fetal echocardiography forms an integrated part of a
high-quality anatomical ultrasound performed in the second
trimester using the ‘five-transverse view’ protocol [13]. This is a
practical and effective population screening tool which uses five
ultrasound planes through the fetal body to provide views of
abdominal situs, the four-chamber view, the outflow tracts and the
three-vessel and tracheal view (Fig. 1). The details of screening
programs vary from country to country, but the most successful
programs offer pregnant women a first trimester scan, followed by
a detailed anatomical scan at around 20 gestational weeks [13e16].
Professional societies such as the International Society for Ultra-
sound in Obstetrics and Gynecology (ISUOG) and the American
114 H.M. Gardiner / Seminars in Fetal & Neonatal Medicine 23 (2018) 112e118
Fig. 2. (a) Antenatal detection rates in the UK from 2003 to 2014 and (b) compared with data submitted to the Society of Thoracic Surgeons website 2008e2012 and reported on the
National Institute for Cardiovascular Outcomes Research website [21]. The graphs represent the proportion of children undergoing surgery for major congenital heart defect during
the first year of life who have had an antenatal diagnosis.
Institute of Ultrasound in Medicine (AIUM) have updated their
screening protocol guidelines to reflect the five-transverse view
protocol [13] and provide continuing education in various aspects
of fetal cardiology [17,18]. Guidelines promoting practical protocols
that are achievable during a busy screening schedule have
improved prenatal detection of all lesions, including those one
would have expected to recognize on four-chamber views alone in
the past. Today outflow tracts and arch abnormalities are being
detected regularly for the first time in population-based studies
[19,20]. Improved detection rates result from increasing compe-
tence and confidence of the screeners, and hands-on training of the
first-line sonographers, combined with feedback from their fetal
medicine unit, will lead to improved detection rates of CHD [1].
Other aspects of an effective program for technicians and nurses are
ongoing training and local support to encourage early referral for
sonographic abnormalities. Whereas prenatal detection rates of
85% are possible in well-run, supported programs, barriers to
learning are not well understood and still require further research
[1]. The 2014 National Institute for Cardiovascular Outcomes
Research report on UK population-based screening for CHD shows a
doubling of overall antenatal diagnosis since 2003, from 23% to 48%
(Fig. 2). These values represent the proportion of children under-
going surgery for major CHD during the first year of life with an
antenatal diagnosis and are similar to recent reports from the USA
[21].
2.3. Referral for a diagnostic opinion and evaluation
Fetal echocardiography by experienced practitioners provides a
complete cardiovascular diagnosis in more than 95% of fetuses with
CHD. It is no longer considered best practice to image the fetal heart
in isolation in a pediatric cardiology setting. In many large centers
worldwide, imaging the fetal heart takes its logical place within a
fully integrated fetal medicine center and is performed by those
with an obstetric as well as cardiology training [1,12e20].
An integrated approach to the fetal cardiovascular system by
fetal medicine specialists and fetal cardiologists with support from
genetic counselors and experienced midwives allows for optimal
diagnosis and management of the pregnant woman expecting a
baby with CHD. A multidisciplinary team (MDT) is essential to
manage referrals for CHD, as one-third of pregnancies with CHD
also have genetic abnormalities, and/or involvement of other organ
systems [22]. The genetic evaluation will be based on perceived risk
following an assessment of the extended family history, specific
cardiac diagnosis and involvement of other organ systems.
Whereas about 20% of fetuses with CHD have a chromosomal
defect, attempts to describe the likelihood of aneuploidy for a
specific cardiac lesion remain poor. In part this is due to the his-
torical nature of the data, the highly selected referred populations
and lack of uniform prenatal genetic testing (chorionic villus
sampling or amniocentesis) [22,23]. More recent technologies such
as chromosomal microarrays have been incorporated into genetic
testing. The additional diagnostic gain of using array comparative
genomic hybridization (aCGH) to detect copy number variants
(CNVs) in fetal CHD was explored in a meta-analysis of 13 studies
comprising 1131 cases of CHD. This technique gave an increased
yield of 7% (95% confidence interval (CI): 5.3e8.6%) for the detec-
tion of CNVs (excluding fetuses with aneuploidy and 22q11
microdeletion). Sub-group analysis confirmed previous reports [24]
that the increased yield was greatest in pregnancies with multiple
congenital abnormalities (9.3% (95% CI: 6.6e12%)) compared with
isolated CHD at 3.4% (95% CI: 0.3e6.6%) [25]. The clinical impor-
tance of this is that it may provide additional information if kar-
yotyping and 22q11 microdeletion analysis are normal by
traditional testing with G-banded karyotype and fluorescent in-situ
hybridization. As with all new technologies, the significance of
some variants is still unknown and will require correlation with
detailed phenotypic and developmental outcomes to ascertain
their likely importance.
Some affected fetuses will require urgent or semi-urgent sur-
gery for associated malformations, such as omphalocele or dia-
phragmatic hernia after birth, and prenatal counseling with the
appropriate cardiac and pediatric surgeon or interventional cardi-
ologist is desirable.
The pregnant woman is usually seen on three or four occasions
by the fetal cardiologist before delivery to check for the develop-
ment of new or progression of obstructive lesions (Fig. 3) to
monitor heart function and importantly to check pulmonary
venous connections and monitor for signs of their obstruction in
later pregnancy [26]. The fetal medicine specialists may see the
pregnant woman monthly to monitor fetal growth and any iden-
tified pregnancy complications such as polyhydramnios, short
cervix, placenta previa or accreta.
2.4. Perinatal planning
Appropriate transfer of care for delivery in the perinatal center
will ensure that the family feels supported and that the baby
 H.M. Gardiner / Seminars in Fetal & Neonatal Medicine 23 (2018) 112e118 115

Table 1
Spectrum and comparison of prenatally and postnatally diagnosed heart defects in
Czech Republic 1986e2006.

Congenital heart defect % total CHD

Detected Detected
prenatally postnatally

Atrioventricular septal defect 15.1 3.9

Hypoplastic left heart syndrome 15.0 3.9
Ventricular septal defect 9.1 46.1
Double-outlet right ventricle 8.7 1.1
Pulmonary atresia 6.0 2.2
Transposition of the great arteries 5.4 5.4
Tetralogy of Fallot 5.2 3.8
Aortic stenosis 4.9 7.8
Single ventriclea 4.8 1.1
Common arterial trunk 3.8 1.0
Coarctation of the aorta 3.6 5.4
Tricuspid atresia 3.4 0.3
Ebstein anomaly 2.1 0.3
Pulmonary stenosis 1.6 7.8
Miscellaneous congenital heart 11.1 9.9
defects
a
Excluding hypoplastic left heart syndrome, tricuspid atresia, and some pulmo-
nary atresia.

ultrasound plane where their diagnostic features are best displayed

Fig. 3. (a) Four-chamber view shows an enlarged bright left ventricle (LV) at 21þ4
weeks secondary to aortic and mitral stenosis. (b) By 27þ3 weeks the left ventricle (LV)
has shrunk and the right ventricle (RV) wraps around it, forming the cardiac apex.
There is an aneurysmal foramen flap guarding the foramen ovale (FO).
receives the best care possible. It is useful to assign the baby a level
of care required at delivery and there are several proposed grading
systems [11]. This ensures that all members of the MDT understand
what is required in terms of preparation for management of the
newborn, including procedures such as an ex-utero intrapartum
therapy procedure in cases of airway obstruction [27], or extra-
corporeal membrane oxygenation support for severe diaphrag-
matic hernia [28].
3. Overview of congenital heart defects and their detection
Heart defects are classified in a variety of ways, most often
divided into morphological or physiological groupings, with ductal
dependency characterizing the defects as “critical CHD” [1,29].
Ductal-dependent lesions are the most important to detect before
delivery as the baby will need blood flowing through the arterial
duct to perfuse the systemic or pulmonary circulation. One
example of a ductal-dependent systemic circulation is coarctation
of the aorta, and an example of a ductal-dependent pulmonary
circulation is Tetralogy of Fallot with pulmonary atresia. As this
article deals with ultrasound screening, it is most appropriate to
characterize CHD based on their morphology and describe the
(Fig. 1). Historically, abnormalities seen on a four-chamber view are
the most frequently detected lesions. This is largely because only
the four-chamber view was used for CHD screening until about 15
years ago and sonographers remain most familiar with it. Table 1
shows the prevalence of different types of CHD and the differ-
ences in the proportions between pre- and postnatally diagnosed
lesions from a population-based study over a period of 21 years
(1986e2006) in the Czech Republic. The most frequently detected
lesions were those with four-chamber view abnormalities showing
ventricular imbalance, such as hypoplastic left heart syndrome
(Fig. 3) or those with large septal defects as in atrioventricular
septal defect (AVSD) (Fig. 4) or double-outlet right ventricle. Hearts
with absent connections such as mitral or tricuspid valves are rarer,
but should be readily identifiable as they are often associated with a
“single ventricle” appearance, or as having a dominant ventricle
and rudimentary pouch (Fig. 5).
Obstruction of the semilunar valves (aortic and pulmonary
valves) is usually associated with involution of the supporting
ventricle, which may be the first indication of valvar abnormality
and is seen on the four-chamber view (Fig. 3). Theoretically, a good
evaluation of the four-chamber view can detect about half of all
cases of CHD, but in practice this is not the case. Before the five-
transverse views were adopted as the optimal screening protocol,
detection of all lesions was as low as 29%, even for those lesions
with characteristic four-chamber view abnormalities such as AVSD
[30]. In most population studies there is a marked era effect, with
prenatal detection rising once introduction of the outflow tracts
was introduced into routine screening [21,22].
One explanation for this is greater rigor in training and the
ability to provide feedback through audit. Another factor is the rise
in detection of conotruncal lesions that include Tetralogy of Fallot
(ToF), with pulmonary stenosis or atresia, double-outlet left
ventricle lesions (DORVs) and common arterial trunk (CAT). These
lesions usually have left axis deviation and a large ventricular septal
defect (VSD) and so should theoretically be detectable on a four-
chamber view. However, although described more than 20 years
ago, recognition of the association of an abnormal fetal cardiac axis
and CHD has only recently been emphasized in both first and
second trimester screening programs [31,32]. Moreover, in con-
otruncal malformations, the VSD is often more evident in the outlet
116 H.M. Gardiner / Seminars in Fetal & Neonatal Medicine 23 (2018) 112e118
Fig. 4. (a) Four-chamber view shows complete atrioventricular septal defect (AVSD)
with balanced ventricles, a common valve (CV) with a large ventricular (V) and small
atrial (A) component. There is an aneurysmal foramen flap guarding the foramen ovale
(FO). (b) Short axis view shows details of the common atrioventricular valve
comprising superior (SBL) and inferior bridging leaflets (IBL) and the pulmonary valve
(PV).
septum and can be better appreciated by extending the screening
plane cephalad to trace the left ventricular outflow tract (LVOT).
The diagnosis of complete transposition of the great arteries (TGA)
has lagged behind that of other conotruncal abnormalities, because
the four-chamber view may seem entirely normal. Diagnosis of this
lesion requires a good appreciation of lack of crossover of the
outflow tracts. Incorporating the three-vessel and tracheal (3VT)
view into the screening program, however, provides an additional
opportunity to detect conotruncal lesions as this view is usually
abnormal, with one great artery seen instead of two. Recognition of
this allows the sonographer to re-evaluate their previous assess-
ment of the heart and helps to avoid missed diagnoses. Introduc-
tion of the 3VT plane has revolutionized the prenatal detection of
critical life-threatening lesions of the aortic arch such as coarctation
of the aorta and interrupted aortic arch as well as double aortic arch
and vascular rings [14]. These are detected more easily prenatally
than after birth in most cases. Symptoms often manifest as failure
to thrive, with inability to swallow solid foods and “asthma” with a
delay in recognizing the true diagnosis. Their prenatal detection
Fig. 5. Four-chamber view shows a solitary inlet mitral valve (MV) to a dominant left
ventricle (LV) and a rudimentary right ventricle (RV) fed by a ventricular septal defect
(VSD).
allows earlier treatment and reduces the long-term morbidity
associated with tracheal and esophageal compression during
childhood.
4. Advances in first trimester cardiac screening
Many countries offer their population a first trimester ultra-
sound screen, including cardiac views [15,16]. First trimester
screening was developed for the early detection of aneuploidy, but
as CHD is the most prevalent malformation, and frequently asso-
ciated with genetic abnormalities, the ultrasound screening also
provides an opportunity to detect CHD. The approach of first
trimester screening has changed in recent years. Initially, the
finding of an increased nuchal translucency (NT) [33] along with
abnormal ductus venosus (DV) flow and tricuspid regurgitation was
used to create a group at increased risk for CHD [34] and early fetal
echocardiography was offered to this cohort. The timing of this
cardiac scan varied but was most frequently performed after the
karyotype/microarray result was known at 14e16 weeks, when
imaging is more definitive [35,36]. In the past five years, a limited
cardiac screening protocol using two of the five transverse view
planes was introduced. The four-chamber and 3VT views with color
Doppler have been adopted with promising reports, some
achieving a 75% detection rate of the CHDs in an unselected pop-
ulation [37]. A recent study of ultrasound at 12e13 weeks in women
undergoing the combined test reported that 63% of all anomalies
were detected: 24/53 (45.3%) structural and all the chromosomal
anomalies (97% had raised nuchal translucency or combined test
>1:200). Importantly, all life-limiting abnormalities were detected
with false-positive results that were six-fold lower than at the 20-
week scan [38]. Of the 12 CHD in this population, four (TGA, VSD,
ToF, and complex CHD) were detected at the early scan, whereas
five similar lesions were not detected until the 20-week scan. One
TGA, one total anomalous pulmonary venous connection (TAPVC)
and an insignificant VSD were only detected after delivery [38].
Others have published recently on the success of first trimester
cardiac scanning, concluding that it is currently clinically worth-
while from about 11 gestational weeks and that pregnancy choices
made following this scan appear to alter the balance of cardiac
defects seen in later pregnancy [39e41].
 H.M. Gardiner / Seminars in Fetal & Neonatal Medicine 23 (2018) 112e118
5. Safety of ultrasound
First trimester ultrasound guidelines for safe practice were
published in 2009 by the British Medical Ultrasound Society
(BMUS) [42] and in 2011 by ISUOG [43]. Both urge caution; BMUS
concluded that, provided the thermal index is kept below 0.7, there
was no requirement to restrict scanning times either before or after
10 gestational weeks, but ISUOG recommend that routine color
Doppler should not be used, except for certain examinations; this
likely includes cardiac screening. ISUOG promotes the ALARA
principle, “as low as reasonably achievable” and keeping the ther-
mal index <1.0 and Doppler use short, at 5e10 min. More advanced
technology may enable the collection of more information with
shorter capture times and could lead to improved diagnostic ca-
pabilities with less risk of exposure to Doppler ultrasound [44,45].
6. Newer technologies
The quality of imaging has improved greatly with modern
transducer technology and improved processing power. There are
many advances in 2D probes, such as biplane, to allow visualization
of structures in two orthogonal planes, thus clarifying anatomical
details and shortening the examination time. Modifications to in-
crease contrast resolution allow better visualization of tissue
planes.
New electronic probes contain rows of elements that can send
and receive the ultrasound beam. Thus, image acquisition is no
longer confined to a 2D beam with a certain thickness, but rather a
broad 3D beam captures a stereoscopic volume, rather than
reflecting surface interfaces. This allows for a more realistic image
quality and true live fetal heart scanning, rather than spatio-
temporal image correlation or STIC technology. STIC obtains car-
diac volumes by ordering slices temporally over a virtual cardiac
cycle. This allows off-line manipulation and assessment by experts
through telemedicine links. In cardiac imaging, faster acquisition
now reduces the chance of artifact. Additionally the volume can be
acquired with color or power Doppler to provide more clinically
useful information and the resultant volume can be post-processed
by adding contrast enhancers displayed in tomographic slices to aid
interpretation. Measurements can be included during post-
processing by applying STIC M-mode e but because this is a vir-
tual cardiac cycle, arrhythmias cannot be assessed. Real-time 4D
fetal echo has long been anticipated and is now a reality, provided
the 2D scan is good enough. Frame rates are now sufficiently high to
appreciate structures and tomographic displays provide serial
views throughout the volume. One further advantage is that 4D
anatomical M-mode will allow an assessment of arrhythmia as the
atrial and ventricular activity can be displayed and the relationship
assessed. The course and connections of vascular structures can be
a challenge and there are several new techniques that may aid
diagnosis. Contrast imaging can be inverted to display the anechoic
areas, rather than the usually appreciated structures on 2D echo.
These images provide a cast of vessels, resembling flow. Another
alternative is volume rendering of the vessels in 4D, providing
realistic vascular appearances, potentially allowing for better
spatial recognition of structures and aiding diagnosis and surgical
planning, even before birth [46]. This combination of newer,
improved volume acquisition and less expensive web-based tech-
nology may allow for improved remote diagnosis in a variety of
settings [47,48]. However, at all gestational ages there is an
important balance between acquiring diagnostic images while
maintaining safe practice.
117
7. Future developments in fetal echocardiography
Despite technical advances, barriers to ever-earlier cardiac
assessment include the maturational features of the human heart.
Whereas the connections are present in the early first trimester,
developmental features such as delamination of valves and growth
of the atrioventricular septum may make recognition of true pa-
thology more difficult before 13 weeks [36]. Moreover, certain
defects such as isolated total anomalous pulmonary venous
connection (TAPVC) are infrequently detected, even in the second
trimester, and progression of malformations, such as stenosis of
aortic and pulmonary valves, means that diagnosis of these lesions
is only feasible in some cases later in the third trimester, or that
diagnosis may not be made prenatally at all.
As almost half of the major congenital defects can be diagnosed
in the first trimester scan, including about one-third of major car-
diac lesions, the effect of introducing first trimester cell-free DNA
testing on this early scanning opportunity has been debated [49]
and is addressed by Harris et al. in this issue of Seminars. General
opinion is that the second trimester detection of cardiac defects
will remain the bedrock of diagnosis. Assessment of efficacy of
many first trimester studies is reduced because termination of
pregnancy and spontaneous fetal demise reduces the ability to
confirm abnormal first trimester ultrasound findings in later
pregnancy, or after birth.
8. Conclusions
Collaboration between specialties will ensure continued ad-
vances in the diagnosis and assessment of fetal cardiovascular ab-
normalities in the future. Clinical application of this knowledge
requires a collaborative approach to research with sufficient power.
The Fetal Heart Society has been established with the primary aim
to encourage multicenter research to provide answers and increase
our knowledge for the benefit of families and babies with cardio-
vascular anomalies [50].
Conflicts of interest
None declared.
Funding sources
None.
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