Download Doppler Examination of the Fetal Pulmonary Venous Circulation

Chapter 31
Doppler Examination
of the Fetal Pulmonary Venous Circulation
Rabih Chaoui, Franka Lenz, Kai-Sven Heling
Introduction
The assessment of the pulmonary venous system in
the fetus has evolved dramatically in the past decade
due to the routine use of spectral and color Doppler
ultrasound. Besides checking the normal connection
of pulmonary veins during fetal echocardiography,
the interest in these veins has increased recently in
order to get insight into the mystery of the pulmonary circulation in the human fetus in vivo. Physiologic conditions and changes during pregnancy have
been assessed and have allowed the comparison with
data under abnormal conditions. This chapter briefly
reviews the clinical value of Doppler assessment of
pulmonary veins.
Visualization of Pulmonary Veins
Using Real-Time and Color Doppler
Ultrasound
There are four pulmonary veins, inferior and superior
on the right and left sides. All these veins enter the left
atrium separately and have their own ostium. Using
high-resolution real-time equipment and a perpendicular approach to the site of connection, the echolucent
veins may then be recognizable in the surrounding
gray lung (Fig. 31.1). It is generally difficult to visualize
all four pulmonary veins in the fetus, but in the fourchamber view the two inferior veins can be visualized.
Pulmonary veins in the fetus have a diameter of approximately 1 mm or less and are therefore difficult
to identify routinely on screening ultrasound. This is
also the reason why pulmonary volume flow is analyzed quantitatively on the arterial side.
In our examination technique we seek one right pulmonary vein (inferior) along a fictive line prolonging
the intra-atrial septum. In real-time this is best visualized from the right transverse or slight dorsoanterior
approach (Fig. 31.1). Using color Doppler this vein
can be visualized either by an apical approach when
(red) flow is seen toward the left atrium at the site
where the inter-atrial septum inserts (Fig. 31.2) or by
a dorsoanterior approach (flow in blue; Fig. 31.3).
The left pulmonary vein (inferior) is found as a
vessel directly pointing toward the foramen ovale flap
(Figs. 31.4, 31.5). It can be visualized in real-time
when the heart is examined from the left transverse
side (Fig. 31.4). Using color Doppler the same plane
can be used to visualize flow in blue (Fig. 31.4), or a
transverse right side to visualize blood flow in red toward the transducer (Figs. 31.2, 31.5). An apical
approach slightly more from the right thoracic side
may allow the visualization of two veins from the
right and the left coursing into the left atrium (Fig.
31.2). New color Doppler techniques, such as power
Doppler ultrasound or dynamic flow, can be very
helpful tools in visualizing pulmonary veins especially
when insonation angle is more perpendicular to the
vessels of interest (Fig. 31.6).
Real-time visualization of the pulmonary veins was
facilitated in the past few years by using new contrasting techniques, such as harmonic imaging or
compound imaging (SonoCT, CRI, etc.; Figs. 31.1,
Fig. 31.1. Third-trimester fetus in dorsoanterior position.
One right pulmonary vein (RPV) is visualized as the prolongation of the intraatrial septum. In this case we used harmonics imaging and a 5-MHz transducer. RA right atrium,
LA left atrium
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Fig. 31.3. Basal visualization of the heart in a dorsoanterior
fetal position. Both inferior and superior right pulmonary
veins (RPVi, RPVs) are seen in blue entering the left atrium
(LA). Note the color presetting as seen on the color bar
with +18 cm/s
Fig. 31.2. Apical four-chamber view in color in a 30-week
fetus demonstrates both inferior left and right pulmonary
veins (LPV, RPV) entering the left atrium (red). Flow toward
the transducer is visualized in red. On the left side the superior left pulmonary vein is seen in blue. (LA, RA left and
right atrium, LV, RV left and right ventricle)
Fig. 31.4. Left approach to the fourchamber view with one left pulmonary
vein seen in real-time image (in harmonic mode). The flow is parallel to the insonation angle and this plane is ideal
for visualizing pulmonary flow, here
seen in blue. LA left atrium
31.4). When using color Doppler, velocity range
should be reduced to a range of 15±25 cm/s (Figs.
31.3, 31.7) with low filter and high persistence as we
have described elsewhere [1]. The visualization of
pulmonary veins using color Doppler is possible from
the late first trimester by optimizing color Doppler
presets (Fig. 31.8). Whether this contributes to increased diagnosis accuracy is not yet known. We include this visualization in first trimester mainly in
cases with suspected isomerism or in targeted examination, e.g., when totally anomalous pulmonary venous connection (TAPVC) was present in a previous
child.
Usually it is sufficient to identify one pulmonary
vein on each side during a routine study [2]. If, however, there is a heart defect detected, it is advisable to
demonstrate at least three of the veins [2]. The examiner has, however, to be careful when assuming that
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Chapter 31 Doppler Examination of the Fetal Pulmonary Venous Circulation
453
Pulsed Doppler Ultrasound
of Lung Veins
Physiologic Conditions
Fig. 31.5. Left pulmonary vein is visualized from a right
lateral view of the heart. Here also the insonation angle is
ideal for a color setting and flow is visualized in red
color Doppler confirmed the correct connection of
the veins in a heart defect [3] as explained later in
this chapter. In these cases we recommend a combination of color Doppler with pulsed Doppler of the
pulmonary vessels, since flow velocity waveforms are
often abnormal in TAPVC.
Fig. 31.6. Left: Power Doppler ultrasound in a lateral four-chamber view.
With this technique pulmonary veins
and the atria and ventricles are visualized at the same time. Right: Dynamic
flow is very sensitive and arterial and
venous flow are visualized
Conversely to postnatal life, where whole blood
passes through the pulmonary vessels to be oxygenated, the pulmonary circulation in the fetus is only
a small part of cardiac output. Whereas animal experiments in fetal sheep found that pulmonary flow
is around 8% of combined cardiac output [4], Doppler studies on human fetuses in vivo suggested that
this flow is larger, being 13% at 20 gestational weeks
and increasing to 20%±25% during the last trimester
[5].
Doppler studies of volume flow were performed
mainly on the arterial side where vessel diameter is
easily measurable, whereas Doppler examination of
the pulmonary venous system focused mainly on the
study of velocity waveform. Pulmonary venous flow
patterns in the adult were demonstrated to be influenced by dynamic changes in left atrial pressure created by contraction and relaxation of the atrium and
ventricle [6]. Systolic peak (S) is caused by left atrial
pressure reduction that results from the relaxation of
the left atrium and the downward move of the mitral
valve in systole. Diastolic peak (D) is caused by rapid
emptying of the left atrium during left ventricular relaxation. During atrial contraction (A) there is a rise
in left atrial pressure which causes in the adult a reversed flow into the pulmonary vein, i.e., a negative
A-wave [7] which is not present [8, 9] (or occasionally present [10, 11]) in the fetus.
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Fig. 31.7. Spectral Doppler of a pulmonary vein with a triphasic envelope
characterized by the systolic (S) and diastolic (D) waves, and the A-wave as nadir during the atrial contraction
Fig. 31.9. Reference range (individual values, mean and
95% data intervals) for peak systolic velocity in the pulmonary veins plotted against gestational age. (From [9])
Fig. 31.8. A 13-week fetus examined transvaginally with visualization of a right pulmonary vein (RPV) entering the
left atrium (LA). In a previous pregnancy there was a right
isomerism with totally anomalous pulmonary venous connection
The fetal pulmonary vein velocity waveform is
therefore very similar to that of the venous duct, with
a forward triphasic flow throughout the heart cycle
(Fig. 31.7). Parameters of blood flow velocity waveforms have been examined in several studies in recent
years and similar results were reported [8±11]. Peak
systolic (Fig. 31.9), diastolic velocities (Fig. 31.10),
and time velocity integral (TVI) increase significantly
during the second half of pregnancy, whereas pulsatility index decreases (Fig. 31.11) [9]. The rise in
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Chapter 31 Doppler Examination of the Fetal Pulmonary Venous Circulation
455
5. Left ventricular size and performance
6. Mitral valve size and function (e.g., regurgitation).
Abnormal Patterns
of Flow Velocity Waveforms
Fig. 31.10. Reference range (individual values, mean and
95% data intervals) for velocities during atrial contraction
in the pulmonary veins plotted against gestational age.
(From [9])
If we assume that left atrial pressure is a major determinant of the pulmonary vein velocity waveform, an
obstruction of the left atrium should lead to typical
changes in the waveform envelope. This was confirmed for fetuses with hypoplastic left heart syndrome, for example, where a distinct reversed flow
during atrial contraction was demonstrated (Fig.
31.12) [13±15]. When the mitral valve is closed or severely dysplastic, left atrial blood can only escape
during atrial contraction by passing across the foramen ovale from left to right or by returning to the
lung. The larger the interatrial communication, the
less blood will return into the lung during atrial contraction, and vice versa. Better et al. [14] reported an
increase in systolic velocity and a reversal in A-velocity in such fetuses that correlated with the degree of
restriction of the atrial septum after birth. This was
Fig. 31.11. Reference range (individual values, mean and
95% data intervals) for pulsatility index of the pulmonary
veins plotted against gestational age. (From [9] with permission)
peak velocities and TVI is compatible with the increase in pulmonary blood flow during gestation.
Given that the fetal pulmonary vein waveform reflects changes in the left atrium, studies have been
performed to analyze indirectly the impact of left atrial pressure changes on the waveform. The pulmonary venous velocity pattern can be influenced by following determinants [12]:
1. Pulmonary volume flow
2. Foramen ovale size and flow
3. Left atrial compliance (size and muscle distensibility)
4. Atrial contraction, end-diastolic pressure (e.g.,
adrenergic drive, hypoxemia)
Fig. 31.12. Three types of an obstructed left atrium as reflected in the pulmonary vein flow velocity waveforms. The
upper wave is a mild obstruction with a slight reverse Awave, the middle wave is a serious obstruction with a pronounced reversed A-wave. The lower wave is severely abnormal and indicates an obstructive left atrium, often associated with thickened pulmonary veins and congestive
lungs
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R. Chaoui et al.
supported by a recent observation we reported in two
different cases of hypoplastic left heart [15], one
showing a wide patent and the other a sealed foramen
ovale. In the patent interatrial communication, the
pulmonary venous velocity waveform was normal
with a positive A-wave. In the sealed foramen ovale,
however, the waveform showed a nearly to-and-fro
pattern (Fig. 31.12), since all blood flow coming from
the lung returns back into the lung. This is associated
with congested pulmonary veins. This chronic high
pressure leads to vascular damage as observed at autopsy, with arterialization of pulmonary veins as well
as the development of lymphangiectasia of the lung
as we observed in other cases.
In a further study we examined changes of the
velocity waveforms in other heart anomalies (n = 96)
and were not able to find any changes depending on
the heart anomaly, mainly due to the interatrial conditions of obstruction [16].
Besides obstructed left atrium conditions (e.g., hypoplastic left heart, mitral atresia), we also found abnormal waveform patterns in TAPVC. In this severe
malformation pulmonary veins are not connected to
the left atrium and interestingly velocity waveforms
reflect the site of connection. When connecting to a
descending channel into the liver, infradiaphragmatic
blood flow in the pulmonary veins was shown to be
continuous [3]. Connection directly to the right atrium or indirectly via a vertical vein may show pulsations but not with the typical shape of a pulmonary
vein [12]; therefore, it has been suggested that the
routine use of pulsed Doppler of lung veins may help
in diagnosing TAPVC in the fetus.
In summary, it can be emphasized that left atrial
obstruction as seen in hypoplastic left heart syndrome or mitral atresia can be associated in most
cases with an increased pulsatile flow due to the reversal of flow during atrial contraction. A to-and-fro
pattern is suggestive for a sealed foramen ovale and
associated with severe impairment of lung development, showing a poor prognosis. Flow pulsations are
decreased or absent in TAPVC with infradiaphragmatic connection, or show an atypical pattern resembling inferior vena cava or a more dumped pattern in
cardiac or supracardiac connections.
nantly during the filling and ejection phases of the
cardiac cycle. Absolute cardiac diastolic and systolic
time intervals as well as the distribution of pulmonary venous flow velocity integrals between these cardiac time intervals remained unchanged with advancing gestational age.
Macklon and coworkers [18] examined the influence of fetal behavioral states on venous blood flow
velocity waveforms in ten normally grown fetuses at
term. The examinations were performed either during
quiet (state 1F) or active (state 2F) sleep. Whereas no
changes were observed on the arterial side, venous
pulmonary blood flow velocity waveforms demonstrated a significant increase in time-averaged peak
diastolic and end-diastolic velocity during active
sleep, suggesting an increase of pressure gradient
between the pulmonary venous system and the left
atrium in these behavioral states.
DeVore and Horenstein [19] described a new technique for the evaluation of fetal arrhythmia by simultaneous recording of the intraparenchymal pulmonary artery and vein. Since both vessels are adjacent
to each other within the lung showing opposite flow
directions, a simultaneous spectral Doppler sampling
will demonstrate waveforms on both sides of the
baseline (Fig. 31.13): the peak of the pulmonary artery reflects the ventricular systole, whereas the atrial
Other Fields of Interest Assessing
Pulmonary Vein Doppler
The relationship of pulmonary venous flow with systolic and diastolic cardiac times assessed at the level
of the mitral valve are used in cardiology to assess
diastolic function. Brezinka and coworkers [17] analyzed this relationship in 28 healthy fetuses in the
second half of pregnancy and found that pulmonary
venous inflow into the left atrium occurs predomi-
Fig. 31.13. Simultaneous pulmonary artery and vein Doppler tracing in a normal fetus. Sampling is performed in
lung parenchyma where peripheral pulmonary artery and
veins are adjacent to each other. Peak velocity on the arterial side indicates systole (S) and is observed on the venous
side as well. The nadir on the venous side indicates the
atrial contraction (A)
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Chapter 31 Doppler Examination of the Fetal Pulmonary Venous Circulation
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Malformations of Pulmonary Veins
and Their Diagnosis
Embryology in Summary
Fig. 31.14. Simultaneous pulmonary artery and vein Doppler tracing in a fetus with ectopic beat. The ectopic beat
originating from the atrium is seen as a notching on the
venous side with a reversal flow
contraction is identified by an interruption or a nadir
in venous flow (Fig. 31.13). Using this technique the
examiner is able to easily assess qualitatively the relationship of atrial to ventricular contraction and to
quantify the arteriovenous time as well. The method
seems to be helpful in differentiating arrhythmias
(Figs. 31.14, 31.15).
Fig. 31.15. Simultaneous pulmonary artery and vein Doppler tracing in a fetus
with second-degree arteriovenous block
in connective disease of the mother. For
every second atrial contraction there is
one ventricular systole recorded
Understanding embryologic development facilitates
the comprehension of different anomalies involving
the pulmonary system.
Embryology of the fetal venous system is complex
and has been reviewed several times in the past few
years [20±22] to facilitate the understanding of detected (mainly intrahepatic) venous anomalies by the
use of color Doppler. The development of the pulmonary vein system is better examined, since the anomalies are known entities in pediatric cardiology.
The sinus venosus is incorporated at the end of
the fourth week into the posterior wall of the right
and left atria. The right part of the sinus venosus encircles the superior and inferior vena cava and becomes part of the dorsal wall of the right atrium. The
left part becomes remnant and builds the coronary
sinus of the left atrium.
Separately from the development of the left atrium,
the pulmonary veins develop as part of the splanchnic venous bed. During further development pulmonary veins differentiate into the individual veins but
still connect to the systemic venous circulation. At a
certain stage these pulmonary veins connect to the
left atrium where a ªcommonº pulmonary vein arises
as a bud and they lose their connection to the central
circulation. It is still debated whether the pulmonary
veins from the lung connect with the bud resulting
from the invagination of the dorsal wall of the left
atrium or with remnants of the coronary sinus [23].
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Anomalies of the Pulmonary
Venous Connections
Failure of the meeting of the common pulmonary
vein and its splanchnic components results in various
forms of anomalous venous connections. In the case
of a complete failure to connect there is a total bilateral anomalous pulmonary venous connection. This
is the embryologic persistence of the connection to
the systemic veins, since this remains the only pathway for lung blood to return to the heart. According
to their site of connection, there are four forms of
TAPVC: at supracardiac, cardiac, and infracardiac levels, and mixed connections [2]. In partial anomalous
venous drainage there is a failing of one, two, or
three pulmonary veins to connect to the common
pulmonary vein and the vein(s) remain connected to
a systemic vein, either the superior caval, the brachiocephalic vein, or the coronary sinus. The right
pulmonary veins are more often involved than the
left.
The postnatal hemodynamic consequence of
anomalous pulmonary venous connection is that oxygenated blood from the lung reaches directly or indirectly together with the systemic veins into the right
instead of the left atrium. If arterialized blood does
not reach the left atrium, the neonate may present
with cyanosis. The obstruction can be at cardiac level, if the atrial communication is small, or at more
proximal stages either at the level of the pulmonary
veins themselves, within the course of the confluence
or at their connection with a systemic vein [2]. The
most severe form of obstruction is assumed to be the
infradiaphragmatic connection. When a TAPVC with
obstruction is present, the clinical presentation is
very early and severe after birth, whereas later clinical
appearance is observed in cases with no obstruction
and may present first late in childhood in cases with
partial anomalous pulmonary venous connection
(PAPVC).
geted examination for this condition when typical associated heart anomalies are suspected, on the other
[25]. The diagnosis can be assisted by the use of
pulsed Doppler sampling of the pulmonary veins
[25].
The diagnosis of partial anomalous pulmonary
vein connection is very difficult prenatally but can
occasionally be made. We focus on the total anomalous venous connections. The prenatal clues for diagnosis depend mainly on the site of connection and
we discuss it according to this classification.
Supracardiac TAPVC
Supracardiac TAPVC is the most common form of
anomalous connection. In most cases the four pulmonary veins form a confluence posterior to the left
atrium and connect via a vertical vein (which is the
embryologic left persistent superior vena cava) to the
brachiocephalic vein, which drains into the superior
vena cava (Fig. 31.16). This condition is rarely detected by visualizing the confluence behind the left
atrium, but by visualizing the left persistent superior
vena cava as a fourth vessel in the three-vessel-trachea view in the upper thorax (Fig. 31.17, right).
Since an LVCS is a common anomaly seen in the fetus as well, the differentiation from an isolated LVCS
is mandatory. This is achieved by means of color
Doppler (Fig. 31.17). In isolated LVCS, blood from
the jugular vein continues via the LVCS toward the
heart, which means that flow in the LVCS goes in the
direction of the heart. In supracardiac TAPVC with
connection to LVCS blood flow goes the opposite way,
Prenatal Diagnosis of Anomalous
Pulmonary Venous Connection
Total or partial anomalous pulmonary venous connections occur in 2% of all live births. They can occur as an isolated incidence or as a part of complex
heart anomalies, mainly right atrial isomerism (asplenia syndrome; see review in [24]). Despite the ªtheoreticalº ease of visualization of pulmonary veins during fetal echocardiography, diagnosis of TAPVC has
been, however, reported prenatally only in case reports or very small series [3, 25]. In large series on
fetal echocardiography this condition was among the
missed diagnoses; therefore, clues for diagnosis are
probably indirect signs, on one hand, and the tar-
Fig. 31.16. Supracardiac total anomalous pulmonary vein
connection. Lung veins are connecting to a left persistent
superior vena cava (LSVC) which drains the blood to the
anonymous vein and then to the right superior vena cava
(SVC). Blood flow in the left vena cava is toward the head
and the right superior cava in the opposite direction (compare with Fig. 31.17). (Courtesy of Philippe Jeanty from
www.thefetus.net)
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Chapter 31 Doppler Examination of the Fetal Pulmonary Venous Circulation
459
Fig. 31.17. Supracardiac totally anomalous pulmonary venous connection
(TAPVC). Left: Longitudinal view of the
upper left thorax with a left persistent
superior vena cava (LSVC) with blood
flow is seen with a perfusion toward the
fetal head (in red). Right: In the threevessel view the pulmonary trunk is antegrade perfused (blue), and the aorta is
hypoplastic and cannot be seen. On
both sides of the pulmonary trunk the
left persistent (LSVC) and right SVC are
perfused in opposite directions which is
typical for a supracardiac TAPVC
upward toward the upper thorax (Fig. 31.17, left). A
longitudinal visualization of the LVCS may therefore
help enormously (Fig. 31.17, left). Furthermore, blood
flow in the innominate vein appears increased compared with other conditions, since in addition to
blood coming from the left side of the upper extremity, blood flow of the lungs will pass through it. Even
by using a cardiac setting of color Doppler with high
velocities, the innominate vein will appear very
clearly with high flow. Pulsed Doppler of pulmonary
veins may be of help in these conditions, especially
in cases with obstruction of these veins.
The supracardiac type of TAPVC connecting directly to the superior vena cava is difficult to detect
unless the superior vena cava is dilated.
A common feature in both conditions could be the
discrepant size of the right and left heart [25]. In supracardiac and cardiac TAPVC the left side of the
heart is more narrow due to lack of blood flow to the
left and the right side is dilated due to the increased
flow; therefore, it has to be borne in mind that conditions suspicious for size discrepancy, such as right
ventricular dysfunction suggesting tricuspid insufficiency or aortic coarctation, should be suspicious for
supracardiac or cardiac TAPVC as well.
in an article on normal and abnormally dilated coronary sinus [26].
The direct connection of pulmonary veins with the
right atrium can be visualized by means of color
Doppler or power Doppler (Fig. 31.19). This is rarely
detected primarily on screening ultrasound but mainly when there is a suspicious sign. The two clues for
suspicion are either the small size of the left side of
the heart compared with the right or the presence of
right atrial isomerism (asplenia) as detected from
upper abdomen anatomy (juxtaposition of aorta and
inferior vena cava) [24]. In Fig. 31.19 one can recognize the sampling vein behind the right atrium where
the pulmonary veins drain. Pulsed Doppler demonstrates the continuous rather than the typical pulsatile
flow.
Cardiac TAPVC
In cardiac TAPVC pulmonary veins connect directly
to the coronary sinus, which becomes dilated, or less
commonly the connection is directly into the posterior wall of the right atrium (Fig. 31.18).
The first condition can be detected when a dilated
coronary sinus is found. Generally, the best plane to
visualize a coronary sinus is a cross section just below the four-chamber view as we recently described
Fig. 31.18. Cardiac TAPVC. All pulmonary veins are connected to the right atrium. (Courtesy of Philippe Jeanty
from www.Thefetus.net)
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Fig. 31.19. Cardiac TAPVC in a fetus
with right isomerism. Left: Pulmonary
veins drain into the right atrium (RA)
after coursing behind the left atrium
(LA; compare with Fig. 31.18). Right:
Color Doppler shows the vessel behind
the left atrium with a course toward the
right atrium (blue with sample volume).
Spectral Doppler demonstrates the continuous flow instead of the pulsatile
flow
Fig. 31.20. Infracardiac (or infradiaphragmatic) TAPVC
shows the four pulmonary veins draining into a vertical
vein which courses across the diaphragm and ends in
the liver vasculature. (Courtesy of Philippe Jeanty from
www.Thefetus.net)
Infracardiac TAPVC
In infracardiac TAPVC the four pulmonary veins
form a confluence which is localized behind the atria.
This confluence is connected to an anomalous descending vein which passes the diaphragm accompa-
nying the esophagus and drains into the portal veins
in most cases but occasionally into the hepatic veins
or into the ductus venosus (Fig. 31.20). In isolated
cases a discrepant size of the ventricles is not typical
and the main suspicion can only be made in cases
with right isomerism. The confluence and the descending veins are, according to our experience, so
tiny that on real-time and color Doppler examination
they appear to be part of the left atrium and are not
easily recognizable.
Three diagnostic clues can be of help:
1. The proper use of color Doppler by changing the
settings in order to visualize the proper connection
of the veins may help in detecting the confluence
(Fig. 31.21). Interestingly, in contrast to normal
connecting pulmonary veins, where a certain distance is found between the connecting sites of the
right and the left inferior pulmonary veins, in this
condition the veins connect in the same place ±
the confluence vein (Fig. 31.21).
2. Pulsed Doppler of pulmonary veins shows a continuous flow [3] as demonstrated in Fig. 31.22.
3. Of further help is the longitudinal view of the
upper abdomen and heart using color Doppler,
which can demonstrate a vessel with the opposite
color to the hepatic veins and entering the liver
from cranially (Fig. 31.23). At a time where in
IUGR conditions and most cardiac anomalies the
ductus venosus is examined routinely, the examiner could shift the transducer slightly to the left
and the right to recognize such an abnormal vessel. This should of course not be confused with the
hepatic artery showing an increased flow in fetuses
with severe IUGR, which is again easy to differentiate by means of pulsed Doppler.
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Chapter 31 Doppler Examination of the Fetal Pulmonary Venous Circulation
461
Fig. 31.21. Infracardiac TAPVC. Left: At
first sight analysis of pulmonary venous
connection may suggest a normal connection. Right: Increasing velocity range
demonstrates that both veins are draining into a vessel behind the atrium (arrows). In another plane this vein is seen
crossing the diaphragm (see Fig. 31.23)
Rare Anomalies of the Pulmonary Veins
Other anomalies of the pulmonary venous system are
the presence of arteriovenous fistulae within the lung.
In the past few years there have been some case reports of such conditions leading prenatally to volume
overload [27, 28]. The hint for detection was sonolucent echoes in the lung showing a high turbulent flow
on color Doppler (Fig. 31.24). Another rare condition
is the direct connection of the pulmonary artery
branch directly to the left atrium bypassing the vein
as we described in a case report within a series of
different cases of cardiomegaly [29].
Fig. 31.22. Infracardiac TAPVC. Spectral Doppler of the intrathoracic vein shows a continuous flow instead of the
pulsatile flow as sign of a abnormal connection (compare
with Figs. 31.7 and 31.19)
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Fig. 31.23. Infracardiac TAPVC.
Longitudinal view of abdomen
and thorax. Left: The vertical
vein is seen behind the heart
and crossing the diaphragm
(Diaph; arrows). Right: Color
Doppler shows direction of flow
toward the liver. Directly in front
of the spine the descending aorta is seen (arrows), and ventral
of the vein one hepatic vein
(HV) is seen (arrow)
Fig. 31.24. Arteriovenous fistula
in the lung. Left: In real-time a
dilated right pulmonary vein
(RPV) is seen draining into the
left atrium (LA). Right: Color
Doppler shows the turbulent
flow typical for the high perfusion in the fistula
References
1. Chaoui R, McEwing R (2003) Three cross-sectional
planes for fetal color Doppler echocardiography. Ultrasound Obstet Gynecol 21:81±93
2. Hornberger L (2000) Abnormalities of systemic and
pulmonary venous connections. In: Allan L (ed) Textbook of fetal cardiology. Greenwich Medical Media
Limited, London, pp 103±114
3. Feller PB, Allan LD (1997) Abnormal pulmonary venous return diagnosed prenatally by pulsed Doppler
flow imaging. Ultrasound Obstet Gynecol 9:347±349
4. Rudolph AM, Heymann MA (1970) Circulatory changes
during growth in the fetal lamb. Circ Res 26:289±299
5. Rasanen J, Wood DC, Weiner S, Ludomirski A, Huhta
JC (1996) Role of the pulmonary circulation in the distribution of human fetal cardiac output during the second half of pregnancy. Circulation 94:1068±1073
6. Keren G, Sherez J, Megidish R, Levitt B, Laniado S
(1985) Pulmonary venous flow pattern: its relationship
to cardiac dynamics. A pulsed Doppler echocardiographic study. Circulation 71:1105±1112
7. Akamatsu S, Terazawa E, Kagawa K, Arakawa M, Dohi
S (1993) Transesophageal Doppler echocardiographic
assessment of pulmonary venous flow pattern in subjects without cardiovascular disease. Int J Card Imaging
9:195±200
8. Laudy JA, Huisman TW, de Ridder MA, Wladimiroff
JW (1995) Normal fetal pulmonary venous blood flow
velocity. Ultrasound Obstet Gynecol 6:277±281
9. Lenz F, Chaoui R (2002) Reference ranges for Dopplerassessed pulmonary venous blood flow velocities and
pulsatility indices in normal human fetuses. Prenat Diagn 22:786±791
10. Better DJ, Kaufman S, Allan LD (1996) The normal
pattern of pulmonary venous flow on pulsed Doppler
a
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
Chapter 31 Doppler Examination of the Fetal Pulmonary Venous Circulation
examination of the human fetus. J Am Soc Echocardiogr 9:281±285
Paladini D, Palmieri S, Celentano E, Guida F, Salviati
M, Morra T et al. (1997) Pulmonary venous blood flow
in the human fetus. Ultrasound Obstet Gynecol 10:27±
31
Kiserud T (2003) Fetal venous circulation. Fetal Matern
Med Rev 14:57±95
Chaoui R, Lenz F, Bast C, Rizzo G, Taddei F, Bollmann
R (1996) Fetal pulmonary vein flow in normal hearts
and hearts with left sided obstruction. Ultrasound Obstet Gynecol 8:158
Better DJ, Apfel HD, Zidere V, Allan LD (1999) Pattern
of pulmonary venous blood flow in the hypoplastic left
heart syndrome in the fetus. Heart 81:646±649
Lenz F, Machlitt A, Hartung J, Bollmann R, Chaoui R
(2002) Fetal pulmonary venous flow pattern is determined by left atrial pressure: report of two cases of left
heart hypoplasia, one with patent and the other with
closed interatrial communication. Ultrasound Obstet
Gynecol 19:392±395
Chaoui R, Lenz F (2000) Fetal pulmonary venous Doppler flow velocity waveforms in congenital heart defects. Ultrasound Obstet Gynecol 16:64 (abstract)
Brezinka C, Laudy JA, Ursem NT, Hop WC, Wladimiroff JW (1999) Fetal pulmonary venous flow into the
left atrium relative to diastolic and systolic cardiac
time intervals. Ultrasound Obstet Gynecol 13:191±195
Macklon NS, Laudy JA, Mulder PG, Wladimiroff JW
(1999) Behavior-state-dependent changes in human
fetal pulmonary blood flow velocity waveforms. Obstet
Gynecol 93:184±188
DeVore GR, Horenstein J (1993) Simultaneous Doppler
recording of the pulmonary artery and vein: a new
technique for the evaluation of a fetal arrhythmia. J Ultrasound Med 12:669±671
Achiron R, Hegesh J, Yagel S, Lipitz S, Cohen SB, Rotstein Z (2000) Abnormalities of the fetal central veins
21.
22.
23.
24.
25.
26.
27.
28.
29.
463
and umbilico-portal system: prenatal ultrasonographic
diagnosis and proposed classification. Ultrasound Obstet Gynecol 16:539±548
Fasouliotis SJ, Achiron R, Kivilevitch Z, Yagel S (2002)
The human fetal venous system: normal embryologic,
anatomic, and physiologic characteristics and developmental abnormalities. J Ultrasound Med 21:1145±1158
Hofstaetter C, Plath H, Hansmann M (2000) Prenatal
diagnosis of abnormalities of the fetal venous system.
Ultrasound Obstet Gynecol 15:231±241
DeRuiter MC, Gittenberger-de Groot AC, Wenink AC,
Poelmann RE, Mentink MM (1995) In normal development pulmonary veins are connected to the sinus venosus segment in the left atrium. Anat Rec 243:84±92
Chaoui R (2003) Cardiac malpositions and syndromes
with right or left atrial isomerism. In: Yagel S, Silvermann N, Gembruch U (eds). Martin Dunitz, London
New York, pp 173±182
Allan LD, Sharland GK (2001) The echocardiographic
diagnosis of totally anomalous pulmonary venous connection in the fetus. Heart 85:433±437
Chaoui R, Heling KS, Kalache KD (2003) Caliber of the
coronary sinus in fetuses with cardiac defects with and
without left persistent superior vena cava and in heart
sparing effect. Prenat Diagn 23:552±557
Heling KS, Tennstedt C, Goldner B, Bollmann R (2002)
Prenatal diagnosis of intrapulmonary arteriovenous
malformation: sonographic and pathomorphological
findings. Ultrasound Obstet Gynecol 19:514±517
Russell MW, Gomez C, Nugent C, Christiansen J (2002)
Large fetal pulmonary arteriovenous fistula: impact on
pulmonary development. Pediatr Cardiol 23:454±457
Chaoui R, Bollmann R, Goldner B, Heling KS, Tennstedt C (1994) Fetal cardiomegaly: echocardiographic
findings and outcome in 19 cases. Fetal Diagn Ther
9:92±104