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(Circulation. 1995;91:129-138.)
© 1995 American Heart Association, Inc.

Articles

Assessment of Fetal Compromise by Doppler Ultrasound Investigation of the Fetal Circulation

Arterial, Intracardiac, and Venous Blood Flow Velocity Studies

Kurt Hecher, MD; Stuart Campbell, MD; Pat Doyle, PhD; Kevin Harrington, MD; Kypros Nicolaides, MD

From the Department of Obstetrics and Gynaecology, King's College School of Medicine and Dentistry, Denmark Hill, London, and the Department of Epidemiology and Population Sciences, London School of Hygiene and Tropical Medicine, University of London.

Correspondence to Kurt Hecher, MD, Department of Prenatal Diagnosis and Therapy, AKH Barmbek, Rübenkamp 148, 22291 Hamburg, FRG.

	Abstract

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Background Doppler studies of the fetal circulation in intrauterine growth retardation and hypoxia have demonstrated a compensatory redistribution of arterial blood flow with increased flow to the cerebrum and myocardium and decreased flow to the periphery. The aim of this study was to evaluate the significance of changes in fetal venous blood flow waveforms in high-risk pregnancies and to investigate the time relation between alterations in venous and arterial Doppler waveform indices in compromised fetuses.

Methods and Results The cross-sectional study consisted of 108 high-risk singleton pregnancies between 23 and 42 weeks' gestation without fetal chromosomal abnormalities or major malformations. Blood flow velocity waveforms were recorded from the umbilical arteries, descending thoracic aorta, middle cerebral artery, tricuspid and mitral ventricular inflow, ductus venosus, inferior vena cava, and the right hepatic vein. The mean velocity and pulsatility index were calculated for arterial vessels, the E/A ratio for atrioventricular blood flow, and peak forward velocities during ventricular systole and early diastole, the lowest forward velocity or peak reverse velocity during atrial contraction, and time-averaged maximum velocity for venous vessels. Two ratios for venous waveforms, one of which is the equivalent of the pulsatility index, were calculated. Fetal biophysical assessment was based on a computerized cardiotocogram and the biophysical profile score. The compromised group consisted of 37 fetuses delivered by cesarean section for an abnormal heart rate trace (n=21) or severe preeclampsia (n=9) or which died in utero (n=7) within 10 days of their last Doppler investigation. This group showed significant alterations in arterial and venous flow velocity waveforms but not in atrioventricular inflow. Additionally, to find out whether venous Doppler investigation may help to detect a worsening of the situation in fetuses already showing arterial blood flow redistribution, we analyzed the data of these fetuses separately. The 41 fetuses that had an aorta/middle cerebral artery pulsatility index ratio >95th percentile were divided into compromised and noncompromised groups according to their biophysical assessment and whether or not they developed fetal distress (cesarean section for abnormal heart rate trace or intrauterine death). The mean values for Doppler parameters of the compromised groups differed significantly from the noncompromised groups in all venous vessels, whereas differences on the arterial side were much less pronounced. Velocity ratios of venous waveforms were significantly higher, and absent or reverse flow in the ductus venosus with atrial contraction indicated a poor prognosis, with a perinatal mortality of 5 out of 8.

Conclusions Fetal compromise is associated with significant alterations in the fetal arterial and venous circulation. Significant changes in venous Doppler waveforms develop due to increased afterload and perhaps myocardial failure in late deterioration after fetal arterial redistribution is established and seem to be closely related to abnormal biophysical assessment findings. Therefore, Doppler investigation of the fetal venous circulation may play an important role in monitoring the redistributing growth retarded fetus and thereby may help to determine the optimal time for delivery.

Key Words: blood flow • circulation • veins • ultrasonics

	Introduction

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Doppler studies of the fetal circulation in intrauterine growth retardation and hypoxia have demonstrated increased resistance to flow in the umbilical arteries and redistribution in the fetal circulation with reduced resistance and increased velocity in the internal carotid and middle cerebral artery and the opposite in the descending thoracic aorta.^{1 2 3} There are also intracardiac hemodynamic changes demonstrating an increase in left and a decrease in right cardiac output,^{4 5} which are consistent with the findings of animal experiments that showed a redistribution of blood to the brain and the myocardium at the expense of the lower part of the body.⁶ The observation of pulsations in the umbilical vein and an increase in the reverse component of flow from the right atrium into the inferior vena cava with atrial contraction indicates alterations in cardiac function and heart failure in cases of severely increased placental resistance, arrhythmias, and nonimmune hydrops.^{7 8 9} The amplitude of inferior vena cava blood flow pulsations increased during hypoxia in fetal sheep.¹⁰

The inferior vena cava, hepatic veins, and the ductus venosus play a major role in venous return flow to the fetal heart. Well-oxygenated blood from the placental circulation flows through the ductus venosus and is preferentially directed toward the foramen ovale and the left atrium.¹¹ Animal experiments have shown that on average approximately 53% of umbilical vein blood flow enters the ductus venosus and accounts for more than 98% of its blood flow.¹² Portal blood flow is directed almost exclusively to the right lobe of the liver, whereas the left lobe receives blood from the umbilical vein, resulting in a higher oxygen saturation of left hepatic vein blood compared with that of the right. Blood from the left hepatic vein follows the pathway of ductus venosus blood across the foramen ovale, whereas right hepatic venous blood follows the stream of distal inferior vena cava blood, which has the lowest oxygen saturation, through the tricuspid valve.¹³ Color Doppler allows clear visualization of blood flow in the fetal venous circulation. Recently, the feasibility of blood flow studies of the ductus venosus in human fetuses has been shown, and its relation to the foramen ovale has been investigated.^{14 15 16} The waveform pattern is similar to that in the inferior vena cava, but the velocities are significantly higher, and there is forward flow throughout the whole heart cycle.

The aim of this study was to evaluate the significance of changes in fetal venous blood flow waveforms in high-risk pregnancies and to investigate the relation between alterations in venous, arterial, and intracardiac Doppler waveform indices in a high-risk fetal population. Doppler results of the fetal circulation were compared with well-established routine parameters of fetal assessment such as the biophysical profile score.¹⁷ The purpose was to investigate the possibility of recognizing fetal deterioration and to predict fetal compromise within a certain time period after assessment of the fetal circulation and before other parameters demand acute intervention.

	Methods

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Patients
The study population was derived in sequence from a high-risk fetal assessment clinic within a period of 10 months. It consisted of 108 consecutively referred singleton pregnancies between 23 and 42 weeks' gestation without fetal chromosomal abnormalities or major malformations. All patients gave informed consent, and the study protocol was approved by the King's College Hospital Research Ethics Committee. The main indications for inclusion in the study were the diagnosis of small-for-gestational-age fetus (abdominal circumference <5th percentile for gestational age), abnormal uterine artery Doppler waveforms indicating high placental resistance,¹⁸ and pregnancy-induced hypertension. Table 1 gives maternal, fetal, and perinatal characteristics of these pregnancies. Forty (37%) fetuses were delivered by cesarean section because of an abnormal fetal heart rate trace or preeclampsia (proteinuric pregnancy-induced hypertension). There were 8 intrauterine deaths, and 55 (51%) fetuses had a birthweight 3rd percentile corrected for gestational age and fetal sex.¹⁹

View this table: [in this window] [in a new window]   Table 1. Maternal, Fetal, and Perinatal Characteristics of the Study Population (n=108)

For the purpose of analysis, the study population was divided into two groups based on outcome (Table 2). If cesarean section was performed within 10 days of the last Doppler examination because of fetal compromise (abnormal heart rate pattern) or rapidly worsening severe preeclampsia or if intrauterine death occurred within 10 days, the pregnancy was allocated to the compromised group (n=37). If fetal compromise did not occur within 10 days of examination, regardless of the interval between the last Doppler examination and delivery if it was a vaginal delivery, then the pregnancy was allocated to the noncompromised group (n=66). Five cases had to be excluded from the analysis because they were delivered by elective cesarean section <10 days after their last Doppler investigation for other reasons than abnormal fetal heart rate or preeclampsia. Therefore, no classification according to the development of fetal compromise within 10 days of last measurement could be made.

View this table: [in this window] [in a new window]   Table 2. Subgroups of the Study Population Used for Statistical Analysis and Their Obstetrical Outcome

We included cases delivered because of severe preeclampsia in the compromised group, although they were delivered by cesarean section for maternal distress and not for an abnormal cardiotocogram (CTG). We feel this is justified, as in cases with severe preeclampsia in which there is increased placental resistance,¹⁸ the fetus is always jeopardized, and it is only a question of time whether the deteriorating maternal or fetal condition demands delivery.

Fetal Assessment
Fetal growth was estimated by measurements of the biparietal diameter, head and abdominal circumference, and the femur length. Fetal biophysical assessment included measurement of the deepest amniotic fluid pool and registration of fetal movements and breathing movements. From 26 weeks' gestation onward, a biophysical profile score¹⁷ was performed at each Doppler examination, including a 60-minute CTG (Oxford Sonicaid, System 8000, objective CTG analysis system) that evaluated the fetal heart rate trace based on different criteria such as baseline rate, accelerations and decelerations, and mean variation in milliseconds.²⁰ The lower limit for normality for amniotic fluid volume was 2 cm; fetal heart rate variation, 30 milliseconds; and biophysical profile score, 8 out of 10.

Doppler Examination
Pulsed-wave Doppler ultrasound studies of the fetal circulation were performed with a color Doppler system (Acuson 128) with a 3.5- or 5-MHz curved-array transducer with spatial peak temporal average intensities below 100 mW/cm². The high-pass filter was set at 125 Hz. The size of the sample volume was adapted to the vessel diameter to cover it entirely. All recordings used for measurements were obtained in the absence of fetal breathing movements and when the fetal heart rate was between 120 and 160 beats per minute. The angle between the ultrasound beam and the direction of blood flow was always less than 50°.

On the arterial side, blood flow velocity waveforms were recorded from the umbilical arteries, the middle cerebral artery, and the descending thoracic aorta, as previously described.^{3 21} The pulsatility index (PI), as defined by Gosling and King,²² was calculated for waveforms from all three vessels, and the time-averaged intensity-weighted mean blood velocity (Vm) was calculated for the middle cerebral artery and the thoracic aorta from a minimum of three successive uniform waveforms after angle correction. If there was an umbilical artery PI >95th percentile of our reference range,²³ Doppler recordings were repeated every 2 weeks. In the presence of fetal arterial blood flow redistribution, which was defined as a thoracic aorta/middle cerebral artery PI ratio >95th percentile of our reference ranges for gestational age,²³ Doppler examinations were scheduled once or twice a week, depending on the severity of redistribution. According to this protocol, 209 Doppler examinations were performed, and 49 patients had multiple measurements (two to six).

A two-dimensional echocardiographic examination of the fetal heart was performed to exclude structural abnormalities. Tricuspid and mitral ventricular inflow waveforms were recorded from a four-chamber view of the fetal heart and the sample volume (size, 5 mm) was placed immediately below the annulus of the valves in the right and left ventricles, respectively. Peak flow velocities in early diastole (E) and late diastole with atrial contraction (A) were measured and the E/A ratio was calculated as the mean value of three heart cycles.

On the venous side of the fetal circulation, velocity waveforms were recorded from the ductus venosus, the inferior vena cava, and the right hepatic vein. The ductus venosus could be visualized either in a midsagittal longitudinal plane of the fetal trunk or in an oblique transverse plane through the upper abdomen. The sample volume was positioned at its origin from the umbilical vein, where color Doppler indicated the highest velocities. Waveforms from the inferior vena cava were recorded in a longitudinal section with the sample volume placed between the confluence of the hepatic veins and the point where the renal vein flows into the inferior vena cava. The right hepatic vein was depicted either in an oblique transverse plane more cephalad and more tilted toward the fetal heart than the one for the umbilical vein or in a sagittal-coronal view of the right lobe of the liver and the sample volume positioned in the main stem of the vessel.

Fig 1 shows the two ratios that were calculated as mean values of three consecutive uniform waveforms. The formula for the second ratio is the same as for the PI in arterial vessels, allowing for reverse flow during diastole. Therefore, it is called the pulsatility index for veins (PIV).

View larger version (17K): [in this window] [in a new window]   Figure 1. Calculation of ratios for fetal venous blood flow waveforms. S indicates peak systolic velocity; D, peak diastolic velocity; a, peak reverse velocity or nadir during atrial contraction; and TAMX, time average maximum velocity.

All measurements were entered prospectively into a computer database immediately after the measurements were done. All Doppler recordings were performed by the same investigator, who was not involved in clinical decisions regarding the further management of the pregnancy or the mode of delivery. Doppler results of the fetal arterial system were documented in the patient's notes because it is routine in our department as part of the fetal assessment in high-risk pregnancies, whereas the Doppler results of the heart and the venous system were concealed.

Doppler parameters of the arterial system and the fetal heart are gestational age dependent. Thus, it could also be assumed that the ratios for venous waveforms are gestational age dependent, and this has subsequently been proven.²⁴ To avoid the influence of different gestational ages on the study results, the study group was divided into three subgroups according to gestational age at the time of Doppler assessment: before 28 weeks' gestation, from 28 to 32 weeks, and after 32 weeks. Analysis of the data was carried out in a cross-sectional way, that is, only one set of results was used per fetus. In the case of multiple assessments of the same fetus, the selection criteria were as follows. Generally, the last measurement before delivery was taken. This applied to all fetuses in the compromised group. The assumption for the noncompromised group was that any measurement could be regarded retrospectively as not indicating fetal compromise. Therefore, to obtain balanced numbers for compromised and noncompromised fetuses in each gestational age subgroup, the last measurement within an earlier gestational age subgroup was taken for noncompromised fetuses, if available. This was necessary because fetuses in the compromised group were delivered significantly earlier than noncompromised fetuses (Table 2).

Statistical Analysis
All statistics on Doppler indices were performed on log-transformed data. Differences between means were tested using the Student's t test and between medians using the Mann-Whitney U test. All data were managed and analyzed using the statistical package SPSS (Statistical Package for the Social Sciences).

	Results

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Total Study Population
In the 103 pregnancies suitable for analysis, the success rate in obtaining good-quality Doppler signals from fetal vessels ranged from 88% for the inferior vena cava to 100% for the umbilical artery. It was 94% for the right hepatic vein, 97% for the ductus venosus, 98% for the descending aorta, and 99% for the middle cerebral artery. Forty-one percent (n=44) of fetuses showed abnormal umbilical artery waveforms (PI >95th percentile), and 16% (n=17) had absence or reversal of end-diastolic velocities; 38% (n=41) showed arterial blood flow redistribution to the cerebral circulation, and 20% (n=22) had absence of end-diastolic velocities in the thoracic aorta.

There were significant differences between the compromised and the noncompromised group in gestational age at delivery and birthweight (Table 2). The median interval between last measurements and delivery was 2 days (range, 1 to 9) in the compromised group, whereas it was 46 days (range, 1 to 111) in the noncompromised group. Table 3 gives the results for the compromised and the noncompromised groups for each vessel in each of the three gestational age categories. All vessels except the atrioventricular valves showed significant differences between compromised and noncompromised groups in their flow velocity waveforms. In the hepatic vein and the ductus venosus, these findings were confined to the two early gestational age groups <32 weeks. Ratio 1 showed no significant differences for the inferior vena cava and the hepatic vein before 28 weeks, whereas differences in ratio 2 were significant.

View this table: [in this window] [in a new window]   Table 3. Doppler Results (Mean Values and 95% Confidence Intervals) for Total Study Population (n=103) by Type of Delivery and Gestational Age

View this table: [in this window] [in a new window]   Table 3B. Continued

Exclusion of the fetuses of mothers with preeclampsia, where the reason for cesarean section was the maternal condition, did not influence the results. Fifty-five neonates had a birthweight 3rd percentile; 27 of them were in the compromised group, and 23 fetuses were in the noncompromised group. All arterial and venous Doppler parameters but not atrioventricular E/A ratios showed significant differences in mean values between both groups.

Abnormal venous waveforms were characterized by a decrease of diastolic peak forward and increase of peak reverse velocities with atrial contraction in the inferior vena cava and right hepatic vein (Fig 2). Maximum forward velocity of the a-nadir of ductus venosus waveforms was decreased (Fig 3) and became absent or reversed in the most abnormal cases.

View larger version (105K): [in this window] [in a new window]   Figure 2. Upper panels: Normal waveforms of inferior vena cava (a) and right hepatic vein (b). Lower panels (c and d): Corresponding waveforms in a compromised fetus. There is a considerable increase in reverse velocities during atrial contraction, which exceed forward velocities during early diastole.

View larger version (113K): [in this window] [in a new window]   Figure 3. Flow velocity waveforms of the ductus venosus with low pulsatility (top) and high pulsatility (bottom), which is caused by a decrease of early diastolic forward flow (D) and in particular by very low velocities during atrial contraction.

Absent or Reverse Flow in the Ductus Venosus With Atrial Contraction
Eight fetuses showed this flow pattern. Gestational age ranged from 26 to 34 weeks. All of them had a birthweight <3rd percentile (range, 390 to 1190 g) and had absent or reverse end-diastolic velocities in the umbilical arteries and descending aorta; 6 of them had a biophysical profile score below 8, and all except 1 had an abnormal CTG at the time of Doppler assessment. Five fetuses were delivered due to the CTG abnormality within 2 days; there were 4 intrauterine deaths within 1 week (1 fetus was stillborn despite an emergency cesarean section) and 1 neonatal death.

Fetuses With Arterial Redistribution
Arterial blood flow redistribution to the fetal brain with increase of peripheral vascular resistance was found in 41 fetuses at their last measurement before delivery. The median interval between measurement and delivery was 2 days (range, 1 to 25). Their gestational age ranged from 25 to 39 weeks (Fig 4). We divided these patients into groups based on the results of the following assessments and outcome: CTG, biophysical profile score, amniotic fluid volume, cesarean section for fetal distress, and stillbirth (Table 4). There were no significant differences in mean Doppler values between patients with normal and abnormal amniotic fluid volume, therefore they are not listed in Table 4. For all other features, significant differences in venous Doppler measurements were found between the normal and abnormal groups, whereas differences on the arterial side were much less pronounced and limited to the umbilical artery PI and thoracic aorta Vm (Figs 5 and 6). A significant difference in mean gestational age was found only for assignment based on normal versus abnormal CTG (33.1, SD 3.9 versus 29.5, SD 2.7), therefore further analysis according to different gestational age groups was not performed.

View larger version (36K): [in this window] [in a new window]   Figure 4. Graph: Thoracic aorta over middle cerebral artery (MCA) pulsatility index (PI) ratio in 41 redistributing fetuses compared with the reference range for gestational age in weeks.

View this table: [in this window] [in a new window]   Table 4. Doppler Results (Mean Values and 95% Confidence Intervals) in Fetuses Displaying Arterial Redistribution (n=41) According to Various Characteristics

View this table: [in this window] [in a new window]   Table 4B. Continued

View larger version (117K): [in this window] [in a new window]   Figure 5. Severe arterial blood flow redistribution with high diastolic and high mean (21 cm/s) velocities in the middle cerebral artery (a) and absence of diastolic and low mean (8 cm/s) velocities in the thoracic descending aorta (b). The ductus venosus shows reverse blood flow during atrial contraction (c), which causes synchronic end-diastolic pulsations in the umbilical vein (d). The biophysical profile score was abnormal.

View larger version (114K): [in this window] [in a new window]   Figure 6. Arterial redistribution with waveforms of the middle cerebral artery (a) similar to Fig 5. Systolic aortic velocities and, therefore, Vm are higher than in the fetus of Fig 5 (b). However, the most striking contrast is the waveform of the ductus venosus (c), which shows clearly forward blood flow during atrial contraction. The inferior vena cava (d) shows low forward velocities in early diastole, but there is no increase in reverse blood flow during atrial contraction. The biophysical profile score was normal.

	Discussion

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The results of this study show that fetal compromise is associated with significant alterations on both sides of the fetal circulation. On the arterial side, compensatory mechanisms are generated by fetal hypoxemia and are mediated by arterial chemoreceptors.²⁵ Redistribution of blood with the highest oxygen saturation, which comes from the placenta via the umbilical vein–ductus venosus–foramen ovale–left heart pathway, is designed to maintain sufficient oxygen delivery to the myocardium and the brain. Significant alterations in the fetal venous circulation seem to be closely related to abnormal findings in the fetal biophysical assessment. It could be hypothesized that the compensatory mechanism of arterial blood flow redistribution has reached its limits and is no longer able to maintain sufficient oxygen delivery to the myocardium, and, consequently, characteristic changes in venous flow velocity waveforms occur.

Fetal blood flow distribution has been studied extensively in animal experiments under different circumstances by means of the radionuclide-labeled microsphere technique.¹³ At the moment, it is impossible to perform reliable measurements of volume flow in human fetuses. Errors in measurements of the vessel diameter, in particular in vessels with pulsating blood flow, limit the use of Doppler ultrasound in this regard. Therefore, waveform analysis by angle-independent indices that reflect alterations of the shape of the waveform seem to reflect circulatory changes most reliably. Other authors described the preload index for inferior vena cava waveforms²⁶ or calculated the S/D ratio, which can be used for ductus venosus waveforms as well.^{7 15 27 28} Recently, the ductus venosus index, which is the equivalent to the resistance index for arterial waveforms, has been described.²⁹ None of these ratios and indices takes all three components of the triphasic venous waveform pattern into account. Therefore, we describe two new ratios that quantify the overall pulsatility of the waveform, one of which is the equivalent to the pulsatility index for arterial waveforms.

An increase in S/D ratio and the percentage of reverse flow with atrial contraction in the inferior vena cava has been described in fetuses with intrauterine growth retardation, absence of end-diastolic flow in the umbilical artery, and umbilical vein pulsations.^{7 8 28} Four cases of abnormal ductus venosus waveforms with absent or reverse flow during atrial contraction have been reported in 3 fetuses with cardiac abnormalities and 1 with severe uteroplacental insufficiency.^{14 29} These findings are consistent with our results showing increased venous flow velocity ratios in compromised fetuses with increased placental resistance and arterial redistribution. An increase in ventricular afterload due to high placental resistance and peripheral vasoconstriction may increase the residual volume and ventricular end-diastolic pressure, even when myocardial contractility is still normal. Thus, when atrial contraction occurs, there is an increase of reverse flow into the venous system. Although there is preferential blood flow through the foramen ovale, the effect of elevated right ventricular end-diastolic pressure on the ductus venosus waveform is the same as on the inferior vena cava and hepatic veins because there is no blood flow through the foramen ovale during atrial contraction as it is closed.³⁰ The ductus venosus is the only direct link between the inferior vena cava and the umbilical vein and is therefore the only pathway through which pressure waves causing umbilical vein pulsations can be transmitted. Studies on umbilical vein pulsations in fetuses with growth retardation show a high mortality rate (6 out of 11),⁸ which is consistent with our finding of 5 deaths in the group of 8 fetuses with absent or reverse ductus venosus flow during atrial contraction.

It is remarkable that the ductus venosus and the right hepatic vein do not show any significant differences between the compromised and noncompromised groups after 32 weeks' gestation. This contrasts with the significant differences found before 32 weeks and may be due to the fact that the earlier that growth retardation occurs, the more severe is the disease, and, therefore, the more severe are the alterations in the venous circulation. However, the finding of reverse flow in the ductus venosus during atrial contraction in a surviving fetus at 34 weeks shows that compromised fetuses after 32 weeks can have very abnormal waveforms. Additionally, with the maturation of the fetal autonomic nervous and cardiovascular system and with the establishment of well-defined fetal behavioral states in late pregnancy,³¹ there may be an increasing influence of these parameters on the regulation of ductus venosus blood flow.

In normal fetuses, flow velocity across the tricuspid and mitral valves is greater during atrial systole (A wave) than during early diastolic ventricular filling (E wave), and the E/A ratio increases for both sides with advancing gestational age.³² Unlike other authors,³³ we could not find any consistent differences in E/A ratios between compromised and noncompromised groups. In a study on the influence of preload on indices of diastolic function in adults, an increase in preload increased both E and A wave peak velocities, but it did not change the E/A ratio.³⁴ These indices show considerable intrasubject variability, which makes it difficult to separate normal from abnormal individuals.³⁵

Chronic hypoxemia enhances maximal myocardial blood flow.³⁶ This compensatory mechanism allows maximal oxygen delivery to the myocardium, but as placental insufficiency persists and placental resistance increases, it reaches its limits, and the fetal condition deteriorates. This is reflected in abnormal findings of biophysical assessment. In our study, fetuses with arterial redistribution showed significant differences in the venous waveforms between normal and abnormal CTG and biophysical profile groups. However, there were less marked changes in the arterial waveforms. This indicates that arterial redistribution has reached its maximum before alterations on the venous side occur. The fact that there was a significant difference in gestational age at last measurement between the normal and abnormal CTG groups may have influenced the results, since mean variability increases with gestational age.²⁰ However, a lack of accelerations and the occurrence of decelerations, which were found in the abnormal group as well, are suspicious at any gestational age. Abnormal venous Doppler findings also seem to be useful in separating redistributing fetuses that will need a cesarean section due to fetal distress from those that are not likely to show fetal distress within the next days. Therefore, Doppler investigation of the fetal venous circulation may play an important role in timing the delivery of the redistributing growth retarded fetus.

Recent epidemiological studies have shown that, although the fetus is able to adapt to undernutrition and thereby to survive, permanent changes in the body's physiology and metabolism may lead to cardiovascular disease in adult life.³⁷ To our knowledge, this is the first comprehensive study that compares fetal arterial and venous Doppler findings and correlates them with biophysical fetal assessment data and outcome in a high-risk population. It shows that dramatic changes in the fetal circulation occur in jeopardized fetuses and that in particular those in venous vessels are indicative of fetal deterioration. Intensive surveillance and early delivery of these fetuses may prevent adverse long-term consequences. Fetal Doppler studies may on the one hand help to determine the optimal time for delivery, while on the other allow the pregnancy to continue as long as possible to gain fetal maturity, thus avoiding obstetrical emergency situations and fetal damage. Carefully performed longitudinal studies in growth-retarded fetuses and consequently, controlled management studies, will confirm or disprove our hypothesis.

	Acknowledgments

 
Dr Hecher was supported by the Austrian Science Foundation (Erwin Schrödinger Research Fellowship J0628).

Received April 27, 1994; accepted August 15, 1994.

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