1) The document describes a study comparing early prenatal diagnosis of fetal tetralogy of Fallot (fTOF) between 12-17 weeks gestation to diagnosis after 17 weeks.
2) It found that while detailed assessment of cardiac anatomy was possible in most early cases, referral indications and pregnancy outcomes differed significantly between early and later diagnosis groups.
3) Specifically, early diagnosis was usually due to extracardiac abnormalities, and resulted in termination 80% of the time, compared to 33% termination for later diagnoses usually due to suspected cardiac abnormalities on routine ultrasound.
2. Fetal tetralogy of Fallot (fTOF) and its variants,
like its postnatal counterpart relies on demonstra-
tion of a conoventricular septal defect, conal sep-
tal malalignment, aortic override, and pulmonary
outflow obstruction. While these features are rec-
ognizable at echocardiography, the extent and
level of pulmonary stenosis, precise measure-
ments of the pulmonary arteries, ductal and arch
anatomy, source of pulmonary blood flow, and
other anatomic features such as systemic and
pulmonary venous connections are also critical
for making a detailed and complete diagnosis in
anticipation of surgical intervention. Such details
are deemed necessary for accurate and complete
prenatal counseling at any gestational age as
they have implications for urgency of postnatal
repair as well as for type of repair and potential
need for reoperation throughout the lifetime of
the individual.
In this study, we retrospectively review our
experience with fTOF and its variants, comparing
early (12–17 weeks gestation) with later (17
completed weeks gestation) diagnosis to deter-
mine the efficacy of early fetal echocardiography
in defining cardiac anatomy, and impact of early
diagnosis on clinical outcome.
Methods:
Study Design:
This was a retrospective review of our experience
from 2003 to 2008 with the echocardiographic
diagnosis of fTOF and its variants from 12 weeks
gestation to term. All echocardiograms with the
basic diagnosis of fTOF (large malalignment
conoventricular ventricular septal defect (VSD),
aortic override, pulmonary outflow obstruction)
and variants were reviewed. Fetal cases with a
diagnosis of fTOF and pulmonary stenosis, fTOF
and pulmonary atresia (also referred to as pulmo-
nary atresia with VSD), fTOF-type of double out-
let right ventricle, fTOF with absent pulmonary
valve syndrome, and fTOF with atrioventricular
septal defect were included. Demographic infor-
mation, referral indications, chromosomal or
extracardiac associations at the time of first or
subsequent studies as well as follow-up informa-
tion including confirmation of diagnosis and
pregnancy outcome were analyzed. The study
was approved by the Institutional Review Board
at the University of California, San Francisco.
Fetal Echo Protocol:
The standard fetal echocardiography protocol
adopted by our laboratory was used in all cases.
This included the following: determination of
gestational age using femur length (when appro-
priate) and biparietal diameter, visceral and atrial
situs, systemic and pulmonary venous anatomy
and Doppler flow profiles, axial four chamber
views, outflow views, ductal and aortic arch later-
ality and Doppler flow patterns, branch pulmo-
nary arteries, qualitative assessment of ventricular
systolic function and spectral Doppler assessment
of ventricular inflows and outflows, inferior vena
cava, ductus venosus and umbilical vessel flow,
fetal heart rate and rhythm.
Most studies were performed using a Siemens
Sequoia ultrasound machine (Siemens Medical
Solutions, Mountain View, CA, USA) using 6 or
8 MHz curvilinear and 10 MHz phased array
transducers for transabdominal imaging and 8 or
10 MHz endovaginal transducers for transvaginal
imaging. Transvaginal studies were carried out if
the transabdominal study was inconclusive or did
not yield adequate diagnostic information to
make a definitive diagnosis. Measurements were
made off line even if they had been measured in
the original study so as to exclude interobserver-
or operator-dependant variations. Serial fetal
echocardiograms were offered in all pregnancies
and recommended in all Group I cases per our
institutional protocol for first trimester fetal
screening and anomaly diagnosis.
Scoring System:
We developed a 10-point scoring system to
objectify visualization of specific anatomic fea-
tures and for comparison between initial and
serial echocardiograms in both groups which is
detailed in Table I.
Diagnosis Confirmation:
A Group I diagnosis was considered confirmed if
the anatomy on the first/early study was more
confidently seen on a mid-trimester study, if an
autopsy confirmed the anatomy on termination
of pregnancy, or if there was a live birth with
confirmed anatomy postnatally.
Results:
Demographics and Referral Indications:
The total study group of fTOF comprised 35
pregnancies. A total of 62 fetal echocardiograms,
including 18 pregnancies with a single study
and 17 with two or more studies were reviewed.
Of the 35, there were 10 pregnancies in Group I
(Table II) and 25 pregnancies in Group II
(Table III). The mean gestational age at presenta-
tion in Group I was 14 weeks (range 12–17
weeks) and 23.5 weeks in Group II (range 18–
36 weeks). Indication for referral for fetal
echocardiography was for an omphalocele in
two, ectopia cordis in two (Fig. 1), increased NT
in four (one a trichorionic quadruplet pregnancy,
one a monochorionic twin pregnancy), and
suspected FHD in two (both 17-week diagnoses,
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Bhat, et al.
3. one with confirmed trisomy 21). In Group II, the
most common reason for referral was FHD sus-
pected at the time of the routine mid-trimester
fetal ultrasound (64%).
Fetal Cardiovascular Assessment:
While transabdominal approach was adequate in
all Group II cases, transvaginal imaging was
diagnostic in three with limited transabdominal
image resolution and contributory in two cases in
Group I (Figs. 2 and 3). VSD, aortic override, and
a four-chamber view could be demonstrated in
all Group I and Group II fetuses. The three-vessel
view was successfully visualized in most cases and
great artery discrepancy (ascending aorta larger
than main pulmonary artery) revealed in this
view. Color Doppler was useful to establish flow
in diminutive structures that were difficult to
appreciate on two-dimensional (2D) echo, such
as the pulmonary outflow (Fig. 2) and the ductus
arteriosus (Fig. 3). Multiple views were analyzed
for each structure.
In Group I, there were seven fetuses with
pulmonary stenosis and antegrade flow through
the ductus arteriosus. One fTOF referred for
increased NT at 14 weeks in a set of monochor-
ionic diamniotic twins, had more commitment of
the overriding aorta to the right ventricle and
additional cardiovascular features consistent
with left atrial isomerism. In addition to the basic
features of fTOF, the early exam documented
interruption of the inferior vena cava, bilateral
superior vena cavae, atrioventricular septal
defect, and atrial bigeminy. The main pulmonary
artery was very diminutive and the source of pul-
monary blood flow could not be demonstrated.
TABLE I
Scoring System Used to Evaluate Completeness of Fetal Echocardiographic Assessment of fTOF
Points Given 0 0.5 1
RVOT obstruction
(RVOTO) level and
severity
Not clearly
visualized
Some but not all of these
aspects demonstrated
Clearly demonstrated
Pulmonary valve (PV) Not clearly
visualized
Not seen well enough to
measure
Measurement possible
Branch pulmonary
artery diameter at
origin (PA)
Not clearly
visualized, PA
not measurable
One PA demonstrated well
and measurable
Both PAs measurable
RVOT and PA flow
with color Doppler
Not clearly
visualized
Partially demonstrated Pulmonary outflow, main
and branch PA flow demonstrated
Pulmonary and
systemic venous anatomy
Pulmonary veins
not clearly
visualized
At least one right and one
left pulmonary vein
demonstrated on
2D imaging
AND
2D, Color and pulsed-Doppler
flow in at least one pulmonary
vein on each side demonstrated
AND
SVC and IVC not
clearly visualized
SVC (including LSVC
when present) and
IVC visualized by
2D imaging
SVC, IVC blood flow demonstrated
by pulsed and color Doppler
(including LSVC when present)
Ductus arteriosus anatomy Not clearly
visualized
Visualized but not
measurable
Measured close to its
origin at PA end
Ductus arteriosus blood flow
direction by color or pulsed
Doppler
Not clearly
demonstrated
Partially demonstrated Clearly demonstrated
Aortic and ductal
arch sidedness
Not demonstrated Partially demonstrated Clearly demonstrated based on
relationship with the trachea
and position of the descending aorta
Atrioventricular
valve anatomy
Inadequately
visualized or not
measurable
Only one measurable AV valve concordance, annular size, and
competence of both mitral
and tricuspid valve clearly
demonstrated and annulus measurable
Ventricular Function Not clearly
demonstrated in
short axis
Qualitative systolic
assessment performed,
diastolic assessment
not possible
Biventricular systolic (qualitative) as well
as diastolic function (ventricular inflow
patterns, systemic venous Dopplers and
IVRT) assessed
AV = atrioventricular; IVRT = isovolumic relaxation time; IVC = inferior vena cava; LSVC = left superior vena cava; PA = pulmonary
artery, RVOT = right ventricular outflow tract; SVC = superior vena cava.
83
Early Fetal Diagnosis of Tetralogy of Fallot
4. These anatomic details were confirmed later in
the mid-trimester prior to selective reduction of
the twin. One fetus had fTOF and pulmonary
atresia with retrograde ductal blood flow (Fig. 3),
and in another that underwent termination,
although pulmonary atresia was suspected due
to lack of forward flow through the pulmonary
artery, the source of pulmonary blood flow could
never be demonstrated.
In Group II, there were nine cases of fTOF
with pulmonary stenosis. Nine others were fTOF
pulmonary atresia variants (including three with
aortopulmonary collaterals and seven with an
identified ductus arteriosus as the source of pul-
monary blood flow) (Table III). One pregnancy
that was referred at 35 weeks for fetal tachycar-
dia and hydrops was found to have, in addition
to an incessant supraventricular tachycardia and
early hydrops, a large VSD, aortic override, and
suspected right ventricular outflow obstruction
with a smaller main pulmonary artery compared
with the ascending aorta consistent with mild
TABLE II
Summary of Group I fTOF Cases
GA (weeks) Indication for Referral Cardiac Diagnosis Extracardiac Diagnosis Outcome*
12 Increased NT in one of triplets fTOF – Selective reduction
12 Ectopia cordis fTOF – Pregnancy termination
14 Suspected fetal heart disease fTOF Single kidney Pregnancy termination
14 Increased NT fTOF/pulmonary
atresia,
bilateral SVC
– Pregnancy termination
14 Omphalocele fTOF ectopia cordis Pentalogy of Cantrell Pregnancy termination
14.5 Increased NT in
monochorionic twin
fTOF/pulmonary atresia,
left atrial isomerism,
bilateral SVC
Cystic hygroma Selective reduction
14.5 Omphalocele fTOF Omphalocele Pregnancy termination
17 Multiple anomalies fTOF/DORV,
ectopia cordis
Pentalogy of Cantrell Intrauterine fetal demise
17 Suspected fetal heart disease fTOF – Live birth at term
17 Suspected fTOF fTOF Trisomy 21 Pregnancy termination
*Termination of pregnancies performed in singleton pregnancies and selective reduction in multiple pregnancies leaving a viable
fetus. DORV = double outlet right ventricle; fTOF = fetal tetralogy of Fallot (with pulmonary stenosis unless otherwise specified);
GA = gestational age in weeks; NT = nuchal translucency; SVC = superior vena cava.
TABLE III
Summary of Group II fTOF Cases
Anatomic Subgroup
Gestational Age in
Weeks, Range (Mean) Indication for Referral Extracardiac Diagnosis (n) Outcome (n)
fTOF/pulmonary
stenosis (n = 9)
18.5–36 (23.6) Suspected fetal heart
disease including one
with tachycardia (6),
other fetal anomaly (3)
Mosaic polyploidy (1),
22q11.2 deletion with
severe cerebellar h
ypoplasia (1),
trisomy 21 (1),
Vermian hypogenesis (1)
Pregnancy
termination (2),
Live birth (6),
lost to F/U (1)
fTOF/APV (n = 4) 19–33 (23.6) Suspected fetal heart
disease (3), other fetal
anomaly (1)
22q11.2 deletion (2) IUFD (1),
live birth (3)
fTOF/pulmonary
atresia (n = 9)
19–33 (24) Suspected fetal heart
disease (6), other fetal
anomaly (3)
Trisomy 21 (1), 8p deletion (1) Pregnancy
termination (4),
IUFD (1),
live birth (4)
fTOF/DORV
variant (n = 3)
18–30 (24) Suspected fetal heart
disease (1), other fetal
anomaly (2)
Pentalogy of Cantrell (1),
hydrocephalus and polycystic
kidneys (1), trisomy 13 (1)
Pregnancy
termination (1)
APV = absent pulmonary valve; DORV = double outlet right ventricle; fTOF = fetal tetralogy of Fallot; SVT = supraventricular tachy-
cardia; TOP = termination of pregnancy; F/U = follow up; IUFD = intrauterine fetal death.
84
Bhat, et al.
5. fTOF. This pregnancy was treated with sotalol
with satisfactory rate control and resolution of
hydrops. Following delivery, postnatal echocardi-
ography suggested the presence of a single large
perimembranous VSD with mild aortic over-
ride and no pulmonary outflow obstruction. This
was the only confirmed false positive case in our
series.
Diagnostic Detail at Early versus Late
Gestational Age:
Group I at a mean gestational age of 14.6 weeks
had a mean anatomic score of 6.4 (range 2.5–9,
median 7.5). Group II, at a mean gestational age
of 23.5 weeks had a mean anatomic score of 8.4
(range 6.5–10, median 9) (Fig. 4).
Fetal Echo Follow-Up Data:
At serial fetal echocardiography in four Group I
pregnancies, the anatomic score remained 8 in
one, increased from 8 to 9 in one, from 9 to 10
in one, and substantially improved from 2.5 in a
fetus initially seen at 17 weeks with particularly
difficult windows to 10 by 19 weeks. The remain-
ing six did not have a serial scan. In Group II,
serial echo was performed in 14 of 25 cases, with
no improvement in score in eight cases and
improvement in score in six. Mean score
improvement was 1.8 (1–3.5). This change in
score did not reflect disease progression, but
rather improved visualization of structures. In no
cases in either group did the scores decrease on
later examination.
Outcome and Confirmation:
Of the 10 cases in Group I, eight had pregnancy
termination, including four with significant extra-
Figure 1. Seventeen-week gestational age fetus with pental-
ogy of Cantrell. A transabdominal image demonstrating tho-
racoabdominal ectopia cordis and an omphalocele in a fetus
with tetralogy of Fallot, all features of pentalogy of Cantrell.
LV = left ventricle; RV = right ventricle; VSD = ventricular septal
defect.
A B
C D
Figure 2. Echocardiographic features in a 14-week gesta-
tional age fetus with tetralogy of Fallot. After insufficient
images were documented by transabdominal imaging, trans-
vaginal approach was used to evaluate this pregnancy
referred for increased nuchal translucency of 5 mm. A. The
four-chamber view demonstrated symmetric left and right
atria and ventricles, but the cardiac axis was significantly lev-
orotated. At least one right and one left pulmonary vein are
noted to enter the left atrium (arrows). B. The long-axis
image of the heart demonstrated the malalignment ventricu-
lar septal defect (arrow) and aortic override above it. C. The
three-vessel view was clearly abnormal with a dilated ascend-
ing aorta and a diminutive main pulmonary artery. D. Color
flow Doppler demonstrated patency of the right ventricular
outflow tract (arrow). R = right; L = left; VSD = ventricular sep-
tal defect; Ao = aorta; PA = pulmonary artery; SVC = superior
vena cava.
A B
Figure 3. Retrograde ductus arteriosus flow in a 14-week
fetus with tetralogy of Fallot and pulmonary atresia. Although
a primary diagnosis of tetralogy of Fallot was made by trans-
abdominal imaging, transvaginal imaging demonstrated a
tortuous left-sided ductus arteriosus (arrow) by (A) Two-
dimensional imaging with (B) retrograde flow by color flow
mapping in keeping with critical pulmonary outflow tract
obstruction.
85
Early Fetal Diagnosis of Tetralogy of Fallot
6. cardiac pathology (three after a confirmatory
mid-trimester fetal echocardiography, two others
with autopsy confirmation), one had late fetal
demise (following late mid-trimester fetal echo-
cardiography), and one had postnatal confirma-
tion of the fTOF diagnosis. In Group II, of 24 with
follow-up, seven had pregnancy termination,
two had fetal demise, 15 delivered with con-
firmed postnatal anatomy (Table IV).
Discussion:
Advances in ultrasound technology have pro-
vided enhanced resolution, acquisition, and post-
processing optimization so that more diminutive
fetal structures can be interrogated with greater
confidence and late first–early second trimester
fetal echocardiography is now considered feasi-
ble.1
To be of utility to the managing team and
the family, all components of the evaluation need
to be as accurate as possible. While several pub-
lished studies have addressed feasibility, to our
knowledge there has been no publication to date
that has focused on the extent of anatomic visu-
alization lending weight to a complete diagnosis
that compares with the minute detail expected in
later fetal echocardiography and postnatally. By
adopting a customized scoring system to accom-
modate all relevant and additional details, we
sought to both objectify our impressions and also
apply a standard where a structure was consid-
ered adequately imaged if it was actually measur-
able (e.g. branch pulmonary arteries) and not
just visualized by 2D imaging, and if pulsed-
Doppler waveforms could be acquired in addition
to color flow mapping. On this basis, our scores
for early trimester scans were, as we expected,
lower than those achieved in the same pregnancy
further on or in later trimesters. Our findings are
similar to those of other groups who have docu-
mented improvement in fetal anatomic screening
of normal pregnancies in the late first trimester
with a decrease in inadequate cardiac visuali-
zation from 42% at 13-week scans to 1.6% in
mid-trimester scans.3
However, our experience
suggests that early fetal trimester cardiac scans
can yield substantial anatomic detail allowing for
accurate diagnosis of cardiac pathology.
While the role of fetal echocardiography in
prenatal diagnosis is now unequivocally estab-
lished and accepted, the timing of this evaluation
remains a moving target. In its infancy, fetal
echocardiography was predominantly under-
taken in mid to late trimester, mostly prompted
by a suspicious general fetal scan, extracardiac
anomaly, or family history of congenital heart dis-
ease. While these indications remain true in the
current era, an additional significant number of
pregnancies with increased NT, abnormal fetal
karyotype, or early examinations for maternal
risks demand that the fetal heart be diagnosti-
cally evaluated simultaneously, even as early
as the first trimester,6–14
or, at the latest by
17–18 weeks. This referral pattern was true in
our patient subset. Interestingly, while the pre-
dominant indications for referral of our first and
early mid-trimester cases were extracardiac con-
cerns including the presence of increased NT, the
predominant referral indication in the 18-week
and higher group and even the two 17-week
pregnancies was suspected FHD at obstetric
ultrasound. With greater experience in early fetal
cardiac screening and recognition of more subtle
TABLE IV
Outcome Following Prenatal Diagnosis of Tetralogy of Fallot
Group Total
Pregnancy
Termination IUFD
Live
Birth
Lost to
Follow-Up
I 10 8 1 1 0
II 25 7 2 15 1
All 35 15 3 16 1
IUFD = intrauterine fetal death.
Figure 4. Histogram comparing mean scores for the individual components between groups I and II. AV = atrioventricular valves;
PA = pulmonary artery; PV = pulmonary valve; RVOT = right ventricular outflow tract; RVOTO = right ventricular outflow tract
obstruction. The last pair of columns on this histogram is illustrative of difference in overall mean score in each group. The mean
score in Group I was 6.4 (median 7.5) and in Group II, the mean score was 8.4 (median 9).
86
Bhat, et al.
7. abnormalities of the fetal heart, we suspect
the indications for early fetal echocardiography
referral may change.
fTOF is amenable to early diagnosis on screen-
ing obstetric scans as many views can cause
suspicion in isolation; the four-chamber view
demonstrates a more leftward cardiac axis,
angling towards the fetal outflows (Fig. 2) VSD
and overriding aorta can be demonstrated, and
the outflow sweeps and three-vessel view dem-
onstrate discrepancy in great artery size. Due to
these factors, as well as the relative frequency of
this fetal diagnosis in our institution’s experience
resulting in a reasonable cohort size, fTOF was
selected as an illustrative lesion for this study.
Within the larger scope of early fetal cardiac
scans, there is lesser consensus on specifics such
as patient selection, timing of first echo, opera-
tor, i.e., obstetric sonographer versus pediatric
cardiologist, approach, i.e., transabdominal ver-
sus transvaginal.3,12
As a tertiary referral center,
our study reflects some referral bias, and most
low-risk pregnancies would not have been evalu-
ated. Studies were performed as soon as a referral
request was made, they were all performed by
sonographers who are trained in pediatric and
fetal cardiology, they were all interpreted by
pediatric and fetal cardiologists, and transvaginal
approach was used where transabdominal
images were limited or inadequate. As such,
there is certainly an element of operator depen-
dence in that perhaps other centers with novice
sonographers or young fetal programs may not
be able to completely extrapolate these results.
Still, with increased experience in late first trimes-
ter and early second trimester fetal cardiac diag-
nosis, more detailed evaluation is possible. Due
to the small number of patients who underwent
transvaginal scanning, we did not utilize our scor-
ing system to determine improved visualization
from this modality as compared with transab-
dominal scanning. With increased use of transva-
ginal scanning in fetal echocardiography labs,
such comparative information would certainly be
useful.
Although our study suggests the diagnosis of
fTOF can be made in the late first and early sec-
ond trimester, permitting counseling regarding
this diagnosis, the lack of serial assessment and
postnatal follow-up of these early-gestation preg-
nancies in general limits our ability to counsel
regarding the natural history of fTOF when diag-
nosed at an earlier gestational age. fTOF diag-
nosed later in gestation has been associated in
some with progressive right ventricular outflow
tract obstruction, main and branch pulmonary
artery hypoplasia, all of which may complicate
postnatal care.15
Such information should be
considered in both early and late diagnoses.
Summary and Conclusions:
Fetal fTOF can be diagnosed in first and early sec-
ond trimester pregnancy, with reasonable defini-
tion of anatomic variables in many. While these
early assessments are not always as consistently
detailed as those in later gestation due to image
resolution limitations, they have considerable
potential to impact the management and out-
come of fetal cardiac abnormalities. Serial follow-
up of continued pregnancies is necessary at this
time to better define the natural history of fTOF
when diagnosed earlier in pregnancy.
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