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Doppler Investigation of the Fetal Inferior Vena Cava Yoshihide Chiba, Toru Kanzaki, Zeev Weiner

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Inferior vena cava (IVC) flow velocity waveforms re- present both right atrial function and the blood flow pattern within the venous tree of the lower fetal body.

Flow velocity waveforms obtained close to the venous entrance into the right atrium reflect mostly right at- rial activity. Therefore the information obtained by studying blood flow patterns within the IVC includes (1) whether there is normal atrial filling; (2) detec- tion of a fetal arrhythmia and the resulting blood flow pattern; and (3) estimation of hemodynamic dis- turbances in severely compromised fetuses.

In this chapter we describe the normal pattern of IVC blood flow and the various components of the IVC flow velocity waveforms. Typical alterations of the IVC flow velocity waveforms in hydropic fetuses, fetuses with arrhythmias, and severely compromised fetuses are discussed. Finally, special attention is de- voted to the significance of umbilical vein pulsations.

Normal Blood Flow Pattern in Fetal IVC

A Doppler waveform in a fetal IVC under normal si- nus rhythm shows a pulsating pattern synchronized

with cardiac motions. There are three components in a cardiac cycle: the monophasic blood flow retrograd- ing from the right atrium to the inferior vena cava, the initial forward flow, and the second forward flow.

The reverse flow occurs during atrial contraction.

The initial forward flow coincides with atrial diastole and ventricular systole, and the second forward flow coincides with ventricular diastole (Fig. 27.1) [1, 2].

Fetal movements, particularly fetal breathing movements, influence the blood flow, changing the pattern not only in the IVC but also in the umbilical vein. Blood flow in the IVC has a complicated pattern during fetal breathing movements [3].

Many studies have reported that blood flow in an adult vena cava has a pulsating pattern synchronized with cardiac movements [4±8]. The cause of each component of the blood flow in an adult vena cava has been analyzed from the viewpoint of the atrial pressure [7±9], with the conclusion that the cause of reverse flow is an increase in atrial pressure due to contraction of the right atrium. The cause of systole forward flow is controversial. Some authors have esti- mated it only for atrial dilatation [4, 5]. However, others have suggested that the cause of the forward flow is movement of the tricuspid annulus toward the

Doppler Investigation of the Fetal Inferior Vena Cava

Yoshihide Chiba, Toru Kanzaki, Zeev Weiner

Fig. 27.1. Time relation of venous return in the inferior vena cava with a cardiac cycle. A reverse flow, Sf initial forward flow, Df second forward flow

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apex at ventricular systole [9±11]. Some have sug- gested that both factors are responsible [6, 8, 12]. The cause of diastole forward flow is the decreased atrial pressure due to rapid ventricular filling.

Generally the blood flow pattern in the fetal IVC is similar to that in the adult, as is the cause. We be- lieve, in addition, that the pressure of the left atrium and movement of the mitral annulus may influence flow in the fetal vena cava.

Changes of the IVC flow velocity waveforms throughout gestation were studied by Huisman et al.

[13] and Wladimiroff et al. [14]. These authors de- scribed a significant increase in time-averaged velo- city and a significant decrease in percent reverse flow with advancing gestational age. Such changes, which could be seen as early as 11±16 weeks' gestation, cor- responded with the increasing peak E wave/A wave ratio. We may conclude therefore that the changes in the IVC flow velocity waveforms observed during pregnancy represent increased cardiac compliance during this period. Rizzo et al. studied the blood flow pattern in the umbilical vein during early gestation [15]. They reported pulsations in the umbilical vein in all cases until 8 weeks' gestation, after which the pulsations disappeared progressively until 13 weeks' gestation. The presence of umbilical venous pulsa- tions correlated with reverse flow within the IVC dur- ing atrial contractions.

Doppler Evaluation of Preload Condition in the Fetal Vena Cava and the Umbilical Vein

Among 101 cases of nonimmune hydrops, 30 cases were complicated structural heart diseases. The prog- nosis of such cardiogenic hydrops is poor: the mor- tality was 86.7% [16]. To determine the best timing for delivery and the indications for intrauterine thera- py of the fetus, one must understand the cardiac functions of the fetus with nonimmune hydrops.

The subjects for our study of cardiac function were divided into three groups according to diagnosis [3, 17]. The first group comprised those with structural heart disease associated with hydrops; the second had structural heart disease without hydrops; and the third contained those with hydrops but without heart disease.

We evaluated four parameters to establish the car- diac function of the three pathologic groups and that of normal fetuses. The first parameter, the cardiothor- acic area ratio (CTAR), was the simplest and easiest to understand. The CTAR measures the dimensions of the heart with a four-chamber view. The next pa-

rameter was heart contractility, measured by Pombo's method. The third parameter was measurement of the peak systolic blood flow velocity in the descend- ing aorta (U

max

). The final parameter was the Dop- pler blood flow pattern in the IVC. We knew that fe- tuses with congenital heart disease associated with hydrops have high velocity of atrial reverse flow in the IVC, and based on that we defined two new in- dices, the preload index (PLI), which is calculated from the Doppler shift of the atrial reverse flow and that of systolic forward flow in a fetal IVC. During the evaluation of fetal cardiac functions using these four parameters, the PLI showed the highest sensitiv- ity and specificity for the cardiogenic hydrops fetus versus the normal fetus. It also showed good resolu- tion between the cardiogenic hydrops fetus and the fetus with structural heart disease not associated with hydrops.

Preload Index

The blood flow pattern in an IVC with normal sinus rhythm showed a pulsating pattern synchronized with the cardiac cycle. The Doppler waveform of the IVC includes three components: reverse flow (A), which occurs during atrial contraction; an initial forward flow (Sf), which coincides with atrial diastole and ventricular systole; and a second forward flow (Df), which is seen with ventricular diastole. A new index, the preload index (PLI), is defined as PLI=

A/Sf. The PLI is independent of the angle between the Doppler beam incidence and the blood flow (Fig. 27.2) [3].

Fig. 27.2. Definition of the preload index (PLI). A blood flow from the right atrium occurring at atrial contraction, Sf blood flow into the right atrium coinciding with ventric- ular systole, Df blood flow into the right atrium coinciding with ventricular diastole

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Normal Fetuses

The PLI value of normal fetuses ranged from 0 to 0.37 (median 0.13). The PLI gradually decreased after 20 weeks (Fig. 27.3) [18]. The decrease was so slight after 24 weeks of gestation that the influence of age can be ignored on any analysis done beyond 24 weeks of pregnancy [3].

Fetuses with Hydrops and Heart Disease The PLI values in the three groups of fetuses with disease are compared in Fig. 27.4. The PLI values for those with hydrops associated with heart disease (group 1) are significantly higher than those for nor- mals and for the group with heart disease without hydrops (group 2). PLI values for group 1 ranged from 0.52 to 1.05. All PLI values in this group with cardiogenic hydrops were more than 0.5. PLI values

Fig. 27.3. Chronological change

of the preload index (PLI) after 20 weeks of gestation. (With permission from [18])

Fig. 27.4. Preload index (PLI) among con- trols and those with fetal disease. Group 1, hydrops associated with heart disease (n=9); group 2, structural heart disease without hydrops (n=8); group 3, hydrops without heart disease (n=11)

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for the third group (those with hydrops without heart disease) were in a wide range, from 0 to 1.08. Accord- ing to the results of our studies [3, 17], cardiogenic hydrops is associated with less contractility of the heart, lower flow velocity in the descending aorta, and a significantly higher PLI in the IVC.

Another study has shown that umbilical venous pressure is higher in the presence of hydrops fetalis [19]. Thus it is logical to assume that excessive pre- load is present in the fetus with cardiogenic hydrops.

Half of the fetuses with hydrops without heart disease had a higher PLI in our study. It is again reasonable to assume, then, that they might have secondary car- diac dysfunction, as their hydrops is not primarily cardiogenic. Thus we have assigned them a new des- ignation: secondary cardiogenic hydrops (Fig. 27.5).

Blood Flow Change During Fetal Therapy A high PLI in fetuses showing pleural effusion is al- ways decreased in value by aspiration of the pleural effusion (Figs. 27.6, 27.7). This phenomenon suggests shunting surgery for hydrothorax (Fig. 27.8). In Japan between 1996 and 1999, 28 cases of hydrothorax un- derwent shunting surgery. In 20 of the 28 cases, sur- gery was judged effective by the committee on peri- natal medicine of the Japan Society of Obstetrics and Gynecology [20].

Blood Flow Dynamics

in Fetal Central Veins During Labor

Our studies of venous blood flow during labor sup- port the suggestion that high preload influences blood flow of the fetal central vein [22]. For example, during the recovering period from cord compression or during late deceleration, we recognize high reverse flow in the IVC. It is speculated that blood flow vol-

ume increases the total cardiac output during the recovering period due to cord compression. During late deceleration the blood flow volume may be rela- tively higher than the cardiac output. Pulsation of blood flow was observed in the umbilical vein under the same conditions during the recovering period from cord compression or during late deceleration (Fig. 27.9).

Fig. 27.5. An example of hyper preload condition. Higher preload index (PLI) in the recipient of twin-to-twin transfu- sion syndrome (TTTS)

Fig. 27.6. Following aspiration of hydrothorax, the preload index (PLI) decreased from 1.40 to 0.67, the thoracic pres- sure also decreased from 25 mmHg to 9 mmHg. (With per- mission from [19])

Fig. 27.7. Change in preload index (PLI) by the aspiration of hydrothorax, before and after

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IVC Blood Flow at an Early Stage of Pregnancy

The high preload may present at an early stage of gestation in a normal fetus, an observation supported by our findings [23]. A statistical analysis was per- formed on the Doppler waveforms in the IVC during early pregnancy, as well as in the umbilical artery, middle cerebral artery, and descending aorta [23].

This study shows that the PLI values significantly in- creased from 9 to 12 weeks of gestation (p<0.05).

The PLI values decreased gradually after 13 weeks' gestation (p<0.05) (Fig. 27.10). This study also shows that the resistance indices of the umbilical artery be- gan to decrease at almost the same age (12 weeks' gestation). There was no end-diastolic component be- fore 11 weeks of pregnancy (Fig. 27.11). It is logical to assume that at 12 weeks of pregnancy the compli- ance of the placental circulation may begin to de- crease and the venous blood flow may tentatively in- crease [24].

Abnormal IVC Blood Flow Patterns with Fetal Arrhythmias

Many studies of the IVC in human adults [4±8] have contributed to our understanding of the mechanisms that cause variations of flow in a fetal vena cava. We have reported the characteristic blood flows asso- ciated with fetal arrhythmias elsewhere [1].

Fig. 27.8a,b. Fetal therapy for hydrothorax using a double basket catheter. a During shunting surgery under ultra- sound guidance and b immediately after birth

a

b

Fig. 27.9. Flow changes with fe- tal breathing movements before cord compression but begins to decrease with compression.

Then, during the period of re- covery from cord compression, blood flow pulsation is synchro- nized with cardiac motion, shown by the fetal electrocar- diogram

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Blood Flow Pattern

of Premature Contractions

During premature atrial contractions (PACs), the sys- tolic forward flow is suddenly interrupted by the re- verse flow of the atrial contraction with a higher ve- locity than usual. The higher reverse flow is desig- nated dominant A. The forward flow after dominant A has a biphasic pattern, with each phase corre- sponding to ventricular systole and diastole (Fig.

27.12) [1].

With premature ventricular contractions (PVCs), the dominant reverse flow suddenly interrupts the diastolic forward flow. This dominant reverse flow co- incides with premature ventricular systole. The subse- quent forward flow is monophasic, representing dia- stolic forward flow [1].

Bradycardic Arrhythmia

With bigeminy of a blocked PAC, the usual reverse flow (A) and dominant reverse flow (dominant A) ap- pear alternately. The time from the preceding flow A to the dominant A is shorter than that from domi- nant A to the next flow A (Fig. 27.13) [1].

With complete atrioventricular block, reverse flow (including both normal reverse or flow and dominant reverse flow) appears regularly. The reverse flow coin- cides with the atrial contraction. Dominant reverse flow appears when an atrial contraction occurs dur- ing ventricular systole. The forward flow takes vari- able forms depending on the time relation between the P wave and the QRS complex on the fetal electro- cardiogram (ECG) (Fig. 27.14) [1].

Tachyarrhythmias

With atrial flutters and 2:1 conduction, reverse flow appears twice as often as the QRS complex on the ECG. When the fetal ECG is not monitored, the Dop- pler waveform in a descending aorta may help to de- termine the rate of appearance of ventricular systole (Fig. 27.15) [1]. With supraventricular tachycardia,

Fig. 27.10. Dynamics of preload index (PLI) from 9 to 20

weeks of normal pregnancy. IVC inferior vena cava

Fig. 27.11. Changes of resistance index (RI) from 9 to 20 weeks of normal pregnancy. UmbA umbilical artery

Fig. 27.12. Biphasic forward flow immediately after the dominant reverse flow in a case of premature atrial con- traction of the fetus

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Fig. 27.13. Blood flow in an inferior vena cava during fetal bigeminy of a blocked premature atrial contraction

Fig. 27.14. Blood flow patterns of an inferior vena cava (IVC) and a descending aorta (D Ao) in a case of fetal complete atrioventricular block

Fig. 27.15. Blood flow in an inferior vena cava (IVC) of a case of fetal atrial flutter with 2:1 conduction

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the blood flow pattern in an IVC is almost same as the normal sinus rhythm (Fig. 27.16).

Determination of Fetal Therapy According to the Type of Tachycardia

Some types of fetal tachycardia can be diagnosed by the Doppler waveform at the IVC. However, some conditions were difficult to diagnose, for example, Wolff-Parkinson-White Syndrome. It is necessary to establish the etiology of the tachycardia when we se- lect an antiarrhythmic drug. We require a precise di- agnosis to consider the type of intrauterine fetal ther- apy. We previously published some reports regarding the differential diagnosis of fetal tachycardia by mag- netocardiography and direct fetal electrocardiography (Fig. 27.17) [25±29].

IVC and Umbilical Vein Blood Flow Patterns in High-Risk Fetuses

The occurrence of umbilical venous pulsations in ab- normal and normal pregnancies has been described by several authors. Nakai et al. [30], Indik et al. [31], and Gudmundsson et al. [32] reported pulsatile flow in the umbilical vein with changes in the IVC blood flow pattern in hydropic fetuses. Arduini et al. [33]

found that fetuses with absent end-diastolic velocity in the umbilical artery who present with umbilical ve- nous pulsations deteriorate rapidly. In their study, fe- tuses with umbilical venous pulsations developed ab- normal fetal heart rate patterns within a shorter time than did fetuses with normal umbilical venous flow.

As already mentioned, umbilical venous pulsations can be observed in normal pregnancies during the first trimester, and Nakai et al. [22] found such pulsa- tions during the third trimester in normal fetuses.

They concluded that umbilical venous pulsations in normal fetuses are due to pulsations of the umbilical artery. Their theory was supported by the fact that umbilical venous pulsations in normal fetuses were observed only transiently and only in the free loop of the umbilical vein.

We conclude that an abnormal blood flow pattern in the venous system represents hemodynamic dete- rioration in severely compromised fetuses.

Fig. 27.16. Blood flow in an inferior vena cava (IVC) in a case of fetal supraventricular tachycardia

Fig. 27.17. Averaged fetal magnetocardiography of Wolff- Parkinson-White syndrome of the fetus

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References

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2. Chiba Y, Utsu M, Kanzaki T, Hasegawa T (1983) Changes in venous flow and intratracheal flow in fetal breathing movements. Ultrasound Med Biol 11:43±49 3. Kanzaki T, Chiba Y (1990) Evaluation of the preload

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15. Rizzo G, Arduini D, Romanini C (1992) Umbilical vein pulsations: a physiologic finding in early gestation. Am J Obstet Gynecol 167:675±677

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analysis of cardiac function in nonimmunological hy- drops fetalis. Fetal Diagn Ther 5:175±188

18. Kanagawa T, Kanzaki T, Chiba Y (2002) Chronologic change in the PLI value at the fetal inferior vena cava in the Japanese fetus. J Med Ultrasound 10:94±98

19. Weiner CP, Heilskov J, Pelzer G et al (1989) Normal values for human umbilical venous and amniotic fluid pressure and their alteration by fetal disease. Am J Ob- stet Gynecol 161:714±717

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21. Chiba Y (2001) Fetal therapy, today and future (Japa- nese). Acta Neonatologica Japonica 37:582±588 22. Murakami M, Kanzaki T, Utsu M, Chiba Y (1985)

Changes in the umbilical venous flow of human fetuses in labor. Acta Obstet Gynecol Jpn 37:776±782

23. Itoh S, Chiba Y, Kanzaki T, Kobayashi H, Murakami N (1995) The dynamics of blood flow in fetal inferior vena cava in early pregnancy, evaluated with those in the umbilical artery, the middle cerebral artery and the descending aorta. J Matern Fetal Invest 5:20±24 24. Gunzman ER, Schulman H, Karmel B, Higgins P

(1990) Umbilical artery Doppler velocimetry in preg- nancies of less than 21 weeks' duration. J Ultrasound Med 9:655±659

25. Hosono T, Chiba Y, Shinto M, Kandori A, Tsukada K (2001) A fetal Wolff-Parkinson-White syndrome diag- nosed prenatally by magnetocardiography. Fetal Diagn Ther 16:215±217

26. Kandori A, Miyashita T, Tsukada K, Hosono T, Miya- shita S, Chiba Y, Horigome H, Shigemitsu S, Asaka M (2001) Prenatal diagnosis of QT prolongation by fetal magnetocardiogram ± use of QRS and T-waves cur- rent-arrow maps. Physiol Meas 22:377±378

27. Kandori A, Hosono T, Kanagawa T, Miyashita S, Chiba Y, Murakami M, Miyashita T, Tsukada K (2002) Detec- tion of atrial-flutter and atrial-fibrillation waveforms by fetal magnetocardiograms. Med Biol Eng Comput 40:213±217

28. Hosono T, Shinto M, Chiba Y, Kandori A, Tsukada K (2002) Prenatal diagnosis of fetal complete atrioventric- ular block with QT prolongation and alternating ven- tricular pacemakers using multi-channel magnetocar- diography and current-arrow maps. Fetal Diagn Ther 17:173±176

29. Ishi K, Chiba Y, Sasaki Y, Kawamata K, Miyashita S (2003) Fetal atrial tachycardia diagnosed by magneto- cardiography and direct fetal electrocardiography, a case report of treatment with propranolol hydrochlo- ride. Fetal Diagn Ther 18:463±466

30. Nakai Y, Miyazaki Y, Matsuoka Y (1992) Pulsatile um- bilical venous flow and its clinical significance. Br J Obstet Gynaecol 99:977±980

31. Indik JK, Chen V, Reed KH (1991) Association of um- bilical venous with inferior vena cava blood flow veloc- ities. Obst Gynecol 77:551±557

32. Gudmundsson S, Huhta JC, Wood DC et al (1991) Ve- nous Doppler ultrasonography in the fetus with non- immune hydrops. Am J Obstet Gynecol 164:33±37 33. Arduini D, Rizzo G, Romanini C (1993) The develop-

ment of abnormal heart rate patterns after absent end- diastolic velocity in umbilical artery: analysis of risk factors. Am J Obstet Gynecol 168:43±50

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