Doppler Examination of the Fetal Pulmonary Venous Circulation

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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. Physio- logic 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 four- chamber view the two inferior veins can be visualized.

Pulmonary veins in the fetus have a diameter of ap- proximately 1 mm or less and are therefore difficult to identify routinely on screening ultrasound. This is also the reason why pulmonary volume flow is ana- lyzed 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 con- trasting techniques, such as harmonic imaging or compound imaging (SonoCT, CRI, etc.; Figs. 31.1,

Doppler Examination

of the Fetal Pulmonary Venous Circulation

Rabih Chaoui, Franka Lenz, Kai-Sven Heling

Fig. 31.1. Third-trimester fetus in dorsoanterior position.

One right pulmonary vein (RPV) is visualized as the prolon- gation of the intraatrial septum. In this case we used har- monics imaging and a 5-MHz transducer. RA right atrium, LA left atrium

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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 in- clude 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 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. 31.3. 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. 31.4. Left approach to the four- chamber 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

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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 combi- nation of color Doppler with pulsed Doppler of the pulmonary vessels, since flow velocity waveforms are often abnormal in TAPVC.

Pulsed Doppler Ultrasound of Lung Veins

Physiologic Conditions

Conversely to postnatal life, where whole blood passes through the pulmonary vessels to be oxyge- nated, the pulmonary circulation in the fetus is only a small part of cardiac output. Whereas animal ex- periments in fetal sheep found that pulmonary flow is around 8% of combined cardiac output [4], Dop- pler 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 cre- ated 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.

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

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

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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 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. 31.8. 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

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])

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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 fol- lowing determinants [12]:

1. Pulmonary volume flow 2. Foramen ovale size and flow

3. Left atrial compliance (size and muscle distensibil- 4. Atrial contraction, end-diastolic pressure (e.g.,ity)

adrenergic drive, hypoxemia)

5. Left ventricular size and performance

6. Mitral valve size and function (e.g., regurgitation).

Abnormal Patterns

of Flow Velocity Waveforms

If we assume that left atrial pressure is a major deter- minant 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. 31.10. Reference range (individual values, mean and

95% data intervals) for velocities during atrial contraction in the pulmonary veins plotted against gestational age.

(From [9])

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 per- mission)

Fig. 31.12. Three types of an obstructed left atrium as re- flected in the pulmonary vein flow velocity waveforms. The upper wave is a mild obstruction with a slight reverse A- wave, the middle wave is a serious obstruction with a pro- nounced 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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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 au- topsy, 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 resem- bling inferior vena cava or a more dumped pattern in cardiac or supracardiac connections.

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] ana- lyzed this relationship in 28 healthy fetuses in the second half of pregnancy and found that pulmonary venous inflow into the left atrium occurs predomi-

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 advanc- ing gestational age.

Macklon and coworkers [18] examined the influ- ence 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

Fig. 31.13. Simultaneous pulmonary artery and vein Dop- pler 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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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).

Malformations of Pulmonary Veins and Their Diagnosis

Embryology in Summary

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 en- circles 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].

Fig. 31.14. Simultaneous pulmonary artery and vein Dop- pler 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

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

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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 bilat- eral anomalous pulmonary venous connection. This is the embryologic persistence of the connection to the systemic veins, since this remains the only path- way 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 lev- els, 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 oxy- genated 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).

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 ªtheo- reticalº ease of visualization of pulmonary veins during fetal echocardiography, diagnosis of TAPVC has been, however, reported prenatally only in case re- ports 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-

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-tra- chea 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,

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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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 extremi- ty, 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 insuffi- ciency or aortic coarctation, should be suspicious for supracardiac or cardiac TAPVC as well.

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 posteri- or 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 be- low the four-chamber view as we recently described

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.

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 three- vessel view the pulmonary trunk is ante- grade 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

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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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 dis- tance 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.

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)

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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 re- ports of such conditions leading prenatally to volume overload [27, 28]. The hint for detection was sonolu- cent 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. 31.21. 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)

Fig. 31.22. Infracardiac TAPVC. Spectral Doppler of the in- trathoracic 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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