Doppler Ultrasonography and Fetal Well-being
Allison Lankford
Ozhan M. Turan
Introduction
Doppler velocimetry of the maternal and fetal circulations is a noninvasive clinical tool that provides detailed information on the development of the maternal-fetal-placental unit. Assessment of the maternal and fetal circulations is essential for a better understanding of the pathophysiology of a variety of pathologic processes in pregnancy, and the information gained from arterial and venous Doppler ultrasound helps to guide clinical management. The characteristics of the Doppler waveform depend on the vascular bed that is being examined. Arterial Doppler waveforms are influenced by vascular resistance and provide information about the impedance to blood flow in the distal fetal circulation. Changes in vascular resistance depend on vessel tone, which is mediated by regulatory and compensatory mechanisms within the fetus. Alternatively, venous Doppler waveforms provide information about venous blood returning to the fetal heart. They reflect forward cardiac function by assessing compliance, contractility, and afterload of the heart.1 For example, higher resistance in venous circulation indicates increased right heart afterload and increased intraventricular pressure secondary to myocardial hypoxemia.2 Both arterial and venous Doppler flow assessments of maternal and fetal circulations have become essential in the evaluation of fetal growth restriction (FGR), congenital heart defects and arrhythmias, fetal hematologic conditions, monochorionic twin pregnancies, and in the screening of cardiac defects and/or chromosomal abnormalities.
Physics of Doppler
The use of Doppler ultrasound to investigate the pattern of waveforms in obstetrics has evolved significantly since the first description of the umbilical artery in 1977.3 Specific patterns of waveforms are derived from changes in the ultrasound frequency of the Doppler signal, which targets circulating fetal red blood cells. Santomura in Japan, in 1956, was the first to describe that red blood cells can reflect ultrasound waves, thus changing the frequency in accordance with the Doppler effect. Because blood flow velocity is directly proportional to the Doppler frequency shift, the information made available to the clinician by the Doppler instrumentation is a blood flow velocity waveform (FVW).4 The FVWs from the fetoplacental circulation are dependent on several factors: fetal cardiac contraction force, density of the blood, vessel wall elasticity, and peripheral or downstream resistance.5
There are several different methods of Doppler sonography used in obstetrics: continuous-wave Doppler, pulsed-wave Doppler, and color and power Doppler. These Doppler techniques differ in a number of ways. Continuous-wave Doppler is sensitive to small vessels and has no upper velocity limit. One drawback is that there is no spatial resolution because the reflected echoes from any moving structure within the ultrasound beam are detected. Continuous-wave Doppler is used in simple fetal heart rate detectors.4 Pulsed-wave Doppler has the advantage of depth resolution and a variable sample volume. However, there must be sufficient time to characterize the Doppler shift frequency before the next pulse is emitted, and because of this, pulsed-wave Doppler is susceptible to aliasing. Color Doppler is a development of pulsed-wave Dopper where the frequency shift is mapped on the two-dimensional image. The flow toward and away from the transducer is plotted as different colors. Power Doppler is more sensitive than color Doppler for detection and demonstration of blood flow but could not provide information about the direction of the blood flow.6 Doppler assessment of the maternal and fetal circulation in this chapter primarily focuses on pulsed-wave Doppler.
Doppler Indices
Nondimensional analysis of the flow waveform shape is useful to investigate many vascular beds and can provide information about the proximal (adult peripheral arterial circulation) and distal (fetal circulation) vascular changes.7 The shape of the waveform can be considered a characteristic of the vascular site. For example, waveforms recorded from arteries supplying low-impedance vascular beds (umbilical and uterine arteries) exhibit relatively high forward velocities throughout diastole. The flow waveform may be described or characterized by the presence or absence of particular features, for example, in the absence of end-diastolic flow and the presence of a postsystolic notch. A triphasic waveform, where there is a period of reverse flow in diastole, is characteristic of vascular sites with high impedance to flow. In addition to the qualitative (shape) assessment of a Doppler waveform, quantitative (absolute velocity and volume flow) and semiquantitative (Doppler indices) measurements can be obtained from each vessel (Table 20.1).
Table 20.1 Assessment of Maternal and Fetal Doppler Waveforms Using Different Assessment Methods | ||||||||||||||||||||||||||
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 Figure 20.1 This figure depicts the calculation of the semiquantitative Doppler indices on an arterial waveform. The gray-filled area defines time-averaged maximum velocity (Tmax). D, end diastole; S, peak systole. |
Calculation of the absolute flow within a vessel using Doppler ultrasound is extremely challenging, and errors in calculation may arise due to the inaccurate measurement of the vessel cross-sectional area.7 These errors are further exaggerated when flow calculations are made in small vessels. Therefore, clinicians rely on the semiquantitative Doppler indices in clinical practice. Commonly used semiquantitative Doppler indices include the resistance index (RI), pulsatility index (PI), and systolic/diastolic (S/D) ratio. Among these indices, the PI has a smaller measurement error, narrower reference limit, and is measurable when end-diastolic flow is absent, making it the preferred index. The indices are calculated as ratios between peak systolic velocity (PSV) (A), end-diastolic peak velocity (B), and mean velocity (mean) (Figure 20.1).8
Fetal Circulation
An understanding of the fetal circulation is essential to the interpretation and clinical application of Doppler techniques. In the fetus, gas exchange occurs in the placenta. Oxygenated blood from the placenta reaches the systemic fetal systemic circulation through a series of vascular shunts that preferentially divert blood away from the fetal lungs and limit the intermixing of oxygenated and deoxygenated blood that returns to the heart. In circumstances of fetal stress, compensatory mechanisms allow the redistribution of blood flow to critical organs such as the brain.
In the fetal circulation, the umbilical venous blood is the most highly oxygen-saturated blood. The umbilical vein enters the fetal abdomen and is directed to the porta hepatis and into the liver. A portion of the umbilical venous blood flow supplies the liver and the remainder passes through the ductus venosus (DV).9 At the point where the umbilical vein joins the portal vein to the right, it divides so that a thicker walled DV continues upward and connects the umbilical vein-portal confluence to the inferior vena cava (IVC). In normal fetal development, approximately 50% of the umbilical blood flow passes through the DV and the remaining volume is diverted to the low-resistance hepatic circulation.10
Within the thoracic IVC, there are two streams of blood flow: the well-oxygenated blood from the DV and the less oxygenated blood from the abdominal IVC, which drains the lower body. These streams of blood do not mix, and the streaming of blood leads to preferential shunting of well-oxygenated blood from the DV through the foramen ovale toward the left atrium, bypassing the pulmonary circulation. A right-to-left shunt at the level of the foramen ovale allows the oxygenated and nutrient-rich blood to be delivered directly to the cephalic and coronary circulation.
Of the total blood volume that is returned to the right atrium from the thoracic IVC, approximately 40% crosses the foramen ovale to the left atrium and 60% enters the right ventricle across the tricuspid valve.9 Blood from the hepatic circulation and the superior vena cava is also directed toward the right ventricle. The third vascular shunt, the DA (ductus arteriosus), directs approximately 90% of blood exiting from the right ventricle to the descending aorta. The descending aorta branches into the right and left hypogastric arteries, which distally become the umbilical arteries and return deoxygenated blood to the placenta (Figure 20.2).
 Figure 20.2 Depiction of fetal circulation. The umbilical vein (UV) carries the well-oxygenated blood from the placenta. A portion of the umbilical venous blood flow supplies the liver, and the remainder passes through the ductus venosus (DV) (depicted as green “Y”-shaped organ). Within the thoracic inferior vena cava (IVC), there are two blood flow streams: (1) the well-oxygenated blood from the DV (red arrow) and (2) the less oxygenated blood from the abdominal IVC. These bloodstreams do not mix, and the streaming of blood leads to preferential shunting of well-oxygenated blood from the DV through the foramen ovale (FO) toward the left atrium (LA). The well-oxygenated blood supplies vital organs such as the coronary artery and brain. Blood from the IVC and the superior vena cava (SVC) is directed toward the right ventricle (RV) (blue arrows). RV leads less oxygenated blood to the pulmonary artery (blue arrow). The flow in the pulmonary artery (blue) and aorta (red) mixes at the ductus arteriosus and continues as mixed oxygenated blood (purple) through the descending aorta. The descending aorta branches into the right and left hypogastric arteries, which distally become the umbilical arteries (UA) and return deoxygenated blood to the placenta. |
Arterial Doppler Measurements
Uterine Artery Doppler
Uterine artery (UtA) Doppler assessment provides information about the maternal side of the placenta and acts as surrogate marker for effective
trophoblastic invasion and remodeling of the maternal spiral arteries. The UtAs arise from the anterior division of internal iliac arteries and divide into the arcuate, radial, and spiral arteries. Impedance to blood flow in the UtAs decreases as gestational age advances with the development of a low-resistance vascular bed (Figure 20.3). The initial fall in vascular resistance during the first and second trimesters is attributed to trophoblastic invasion of spiral arteries. The continued decrease in resistance in the UtAs into the third trimester may be explained by a hormonal effect on the elasticity of the arterial walls.7 These physiologic changes in spiral arteries result in an increase in the end-diastolic flow of the uterine arteries.11 Placental ischemic lesions and abnormal development of the spiral arteries may be depicted in the uterine arteries by increased resistance and/or presence of a diastolic notch, which is associated with hypertensive disorders of pregnancy (Chapter 27) and FGR.11 Color Doppler should be used to locate the UtAs as they cross medial to the external iliac arteries (Figure 20.4).12 The region of interest revealed by Doppler should be magnified, and a color box should be placed. The Doppler gate is placed within the straight portion of the UtA before it enters the myometrium.
trophoblastic invasion and remodeling of the maternal spiral arteries. The UtAs arise from the anterior division of internal iliac arteries and divide into the arcuate, radial, and spiral arteries. Impedance to blood flow in the UtAs decreases as gestational age advances with the development of a low-resistance vascular bed (Figure 20.3). The initial fall in vascular resistance during the first and second trimesters is attributed to trophoblastic invasion of spiral arteries. The continued decrease in resistance in the UtAs into the third trimester may be explained by a hormonal effect on the elasticity of the arterial walls.7 These physiologic changes in spiral arteries result in an increase in the end-diastolic flow of the uterine arteries.11 Placental ischemic lesions and abnormal development of the spiral arteries may be depicted in the uterine arteries by increased resistance and/or presence of a diastolic notch, which is associated with hypertensive disorders of pregnancy (Chapter 27) and FGR.11 Color Doppler should be used to locate the UtAs as they cross medial to the external iliac arteries (Figure 20.4).12 The region of interest revealed by Doppler should be magnified, and a color box should be placed. The Doppler gate is placed within the straight portion of the UtA before it enters the myometrium.
 Figure 20.3 Uterine artery waveforms at first, second, and third trimesters in normal pregnancy. The resistance in uterine arteries according to gestational age in normal pregnancies is depicted. Increasing diastolic flow (white circles) and disappearance of the diastolic notch (white arrows) with advancing gestation correlates with decreasing resistance in uterine arteries. The graph with the black triangle depicts decreased resistance during gestation. |
 Figure 20.4 Ultrasound visualization of the uterine artery during the first (A) and second (B) trimesters using color Doppler. A, Sagittal view of the uterus in the first trimester. Doppler gate was placed over the uterine artery. B, Identification of the uterine artery (white lines) over the iliac artery and vein (yellow lines). |
Umbilical Artery Doppler
Umbilical artery (UA) Doppler is a reflection of villous branching in the fetal side of the placenta. During normal pregnancy, there is a progressive increase in end-diastolic velocity in the UA due to decreasing downstream impedance to flow as the placenta vessels grow. A review of normal ranges for UA measurements illustrates the importance of knowledge of gestational age before an index is considered abnormal (Figure 20.5). Similar to UtA development, high resistance is seen in the UA in instances of incomplete trophoblastic invasion of maternal spiral arteries. Doppler indices in the
UA generally do not start to increase until approximately 60% to 70% of the placental vascular tree is not functioning.2 This highlights the presence of extensive disease before Doppler detection is possible and emphasizes the reserve capacity of the placenta.4 The abnormal UA Doppler waveform is characterized by a pattern of present, absent, or reversed diastolic flow velocities relative to the PSV (Figure 20.6).
UA generally do not start to increase until approximately 60% to 70% of the placental vascular tree is not functioning.2 This highlights the presence of extensive disease before Doppler detection is possible and emphasizes the reserve capacity of the placenta.4 The abnormal UA Doppler waveform is characterized by a pattern of present, absent, or reversed diastolic flow velocities relative to the PSV (Figure 20.6).
 Figure 20.5 Umbilical artery waveforms at first, early second, and late third trimesters in normal pregnancy. Increasing diastolic flow (white circles) with advancing gestation correlates with decreasing resistance in the umbilical artery. The absence of diastolic flow at first trimester is a normal finding in the first trimester. The chart with the black triangle depicts decreased resistance during gestation. |
UA Doppler assessment should be taken in a free-floating midcord segment because the location of the Doppler sampling site in the umbilical cord affects the Doppler waveform. The impedance indices are significantly higher at the fetal end of the cord compared to the placental cord insertion. The color box and magnification should target the area of interest only, and the pulsed Doppler gate should be positioned between the walls of the vessel. External compression of the UA by the transducer has the potential to affect the flow pattern by changing the vascular resistance.
Middle Cerebral Artery
The middle cerebral artery (MCA) arises from the circle of Willis and is the larger terminal branch of the internal carotid artery. Doppler velocimetry of the MCA allows the clinician to assess impedance to blood flow in the fetal brain circulation. As gestational age advances, normal development leads to an increase in the PSV and average diastolic velocity in the MCA. In abnormal pregnancies, vasodilation of the MCA is considered to be a compensatory mechanism in the fetus to allow increased blood flow to the fetal brain circulation, and this phenomenon is referred to as the “brain-sparing effect.” The resistance to blood flow within the vessel can be measured with the PI, which is used in the management of FGR. A reduced PI reflects vasodilation of the MCA. The PSV in the MCA can also be used in assessing fetal anemia and is accurate in any circumstance in which fetal anemia may occur, such as parvovirus infection, hemoglobinopathies, and rhesus alloimmunization.
 Figure 20.6 Normal (A) and abnormal (B-D) umbilical artery Doppler waveforms in the third trimester. The diastolic flow is marked with white circles. The white arrows demonstrate flow during diastole. Increased placental resistance first reduces the blood flow during diastole (B). The blood flow stops during diastole (C) or moves backward (D) when the resistance in the placental bed is too high. |
Utilizing the correct technique to sample the MCA is critical for obtaining accurate measurements. The first step is to obtain a transverse view of the fetal brain at the level of the biparietal diameter. Using color flow imaging, the color box is placed over the region of interest. The MCA runs anterolaterally at the borderline between the anterior and middle cerebral fossae. The pulsed Doppler gate is placed over the vessel, as close as possible to its origin. The point of measurement is critical because the MCA-PSV decreases as the distance from the point of origin increases. The angle of insonation between the ultrasound beam and the direction of blood flow should be kept to 0° (Figure 20.7). It does not matter whether the near or far side vessel is interrogated. While angle of correction is not necessary when measuring the MCA-PI, PSV measurement should use angle correction and the angle of incidence
should be <30°; optimally as close to 0° as possible. Angle correction can be used to measure PSV in the fetal MCA.13,14 The region of interest should be magnified so that the MCA occupies more than 50% of the screen, and the full length of the MCA should be visualized. Fetal breathing and excessive pressure on the fetal head by the transducer may change the MCA waveform. The highest PSV value should be measured, and these steps should be repeated at least three times to improve the accuracy and reproducibility of the measured PSV.15
should be <30°; optimally as close to 0° as possible. Angle correction can be used to measure PSV in the fetal MCA.13,14 The region of interest should be magnified so that the MCA occupies more than 50% of the screen, and the full length of the MCA should be visualized. Fetal breathing and excessive pressure on the fetal head by the transducer may change the MCA waveform. The highest PSV value should be measured, and these steps should be repeated at least three times to improve the accuracy and reproducibility of the measured PSV.15
 Figure 20.7 Identification of middle cerebral artery (MCA) with color Doppler using a transsphenoidal plane (A). The Doppler gate (green box) placed over the MCA with a “0°” of insonation angle (white arrow). Normal MCA Doppler waveform is demonstrated in (B). Reduced resistance in MCA (brain sparing) is shown in (C). The waveform resembles umbilical artery waveform because of the increased diastolic flow (white circle). The peak systolic velocity was increased (D) due to fetal anemia. |
Venous Doppler Assessment
Ductus Venosus
Doppler ultrasonography of the fetal venous circulation has improved our understanding of numerous fetal diseases, and this chapter focuses on the assessment of the DV and the umbilical vein. The DV is different from the hepatic vein and the IVC in that there is a persistence of forward flow throughout the cardiac cycle and retrograde flow during diastole is only seen in pathologic conditions.
The DV is a critical vascular shunt in utero that directs oxygenated blood from the umbilical vein to the IVC. Because the DV regulates the amount of umbilical venous return that flows into the heart, it is a direct reflection of cardiac function. As a fetus becomes significantly hypoxemic, myocardial contractility and cardiac output decrease due to increase in right ventricular end-diastolic pressure consequent to an increase in right ventricular afterload. These changes in fetal cardiovascular hemodynamics are reflected in the DV waveform. The DV has a multiphasic blood flow pattern, which depicts cardiac pressure and volume changes in the heart: systolic ventricular ejection (S), declining venous velocities as the ventricles reach the end of systole (v-descent), diastolic velocities (D), and atrial contraction (a-wave) (Figure 20.8).
The primary assessment of the DV FVW is PI velocity (PIV) that predominantly reflect S/a and to a lesser degree D/a and S/D velocity relationships, or by qualitative analysis focusing on the a-wave. These assessments have limitations in assessing the primary underlying cardiac functional component when the Doppler index is elevated.16,17 The recognition of distinct venous waveform patterns provides a better understanding of fetal cardiovascular physiology. The a-wave abnormalities are a sensitive marker of impaired venous forward flow but less specific as to the underlying mechanism. In contrast, v-wave abnormalities may be more specific for myocardial relaxation and compliance issues, which would be compromised in FGR. The D-wave abnormalities reflect global diastolic venous dysfunction that is common in right-sided heart defects.18
The origin of the DV from the umbilical vein should be identified in a midsagittal view of the upper abdomen or in a cross-sectional plane of the abdomen at the level of the stomach. The color flow box should be applied to the area of the DV, and the portion of the DV with the highest velocity should
be identified. This area is identified by looking for an aliasing effect where the blood flow velocity accelerates due to the narrow lumen of the DV. A pulsed-wave Doppler gate of 1 mm in width should be placed over this area, and the waveform should be obtained with the smallest possible angle of insonation (Figure 20.9). When five constant waveforms with a good signal-to-noise ratios are obtained, the frozen image can be traced, outlining the waveform from the beginning of ventricular systole to the end of atrial systole.18 The DV waveform is influenced by several intrinsic fetal factors including fetal breathing movements, behavioral states, and cardiac arrhythmias. The DV should be sampled during fetal rest and in the absence of fetal breathing.
be identified. This area is identified by looking for an aliasing effect where the blood flow velocity accelerates due to the narrow lumen of the DV. A pulsed-wave Doppler gate of 1 mm in width should be placed over this area, and the waveform should be obtained with the smallest possible angle of insonation (Figure 20.9). When five constant waveforms with a good signal-to-noise ratios are obtained, the frozen image can be traced, outlining the waveform from the beginning of ventricular systole to the end of atrial systole.18 The DV waveform is influenced by several intrinsic fetal factors including fetal breathing movements, behavioral states, and cardiac arrhythmias. The DV should be sampled during fetal rest and in the absence of fetal breathing.
 Figure 20.8 Assessment of the ductus venosus waveform. Ventricular systole (S), diastole (D), the opening of atrioventricular valves (v), and atrial contraction (a) were marked on the waveform. Individual velocities can be measured from the maximum velocity of each wave (blue horizontal lines) to baseline. Double-headed white arrows represents individual velocities. A qualitative assessment based on a-wave is demonstrated with the white circle. The a-wave could be present, absent, or reversed. The semiquantitative assessment could be performed tracing a single waveform (yellow dashed line). The ultrasound machine can calculate the pulsatility index of the vein using S, D, and Tmax (time-averaged maximum velocity). Another semiquantitative assessment is the velocity ratios (S/D, S/v, v/D, S/a, D/a, v/a). |
 Figure 20.9 Identification of ductus venosus at first (A) and third trimesters (B). The aliasing effect is marked with white circles. Green box in (B) represents color Doppler box. |
Umbilical Vein
The umbilical vein (UV) delivers the oxygenated and nutrient-rich blood from the placenta to the fetus, maintaining a continuous nonpulsatile flow velocity profile throughout the pregnancy. The UV is easy to measure by means of Doppler velocimetry as it courses along with the umbilical arteries. Variations in the UV Doppler waveforms may be demonstrated and will be discussed below in the context of pathologic clinical conditions. The UV should be measured in a free-loop midcord segment with proper magnification (Figure 20.10). Reduced velocity in the UV typically indicates increased resistance and reduced blood flow through the vein.
 Figure 20.10 Measurement of umbilical venous flow from the free loop. Two umbilical arteries and a vein identified using color Doppler (white arrows). The green box is the Doppler box, and yellow dashed line demonstrates Doppler gate. The gate was on the umbilical vein (A). Normal venous flow (B and C) and an abnormal flow (D) due to increased placental resistance are demonstrated for comparison. |
Doppler Ultrasound in Normal Pregnancies
First-Trimester Screening for Chromosomal Abnormalities and Congenital Heart Defects
The use of fetal Doppler at the first trimester as a screening tool for certain conditions has shown to be effective. Matias et al demonstrated the feasibility of assessing DV blood flow at 10 to 14 weeks of gestation by Doppler ultrasound, both transabdominally and transvaginally.19 Their results suggested that in chromosomally abnormal fetuses with an increased nuchal translucency, abnormal ductal flow (absent or reversed flow during atrial contraction) could be seen in the absence of cardiac defects. In addition, abnormal ductal flow was also seen in chromosomally normal fetuses with major cardiac defects. The authors also reported that the abnormal ductal flow may be a temporary phenomenon.19 These findings were corroborated by Antolin et al when they evaluated the role of the DV-PIV in fetal aneuploidy screening. The DV-PIV was a useful adjunct to the nuchal translucency as a method to reduce the false-positive rate and potentially reduce the number of invasive procedures.20
In a retrospective analysis performed by Timmerman et al, the authors concluded that the risk of congenital heart defects (CHDs) in euploid fetuses with an enlarged nuchal translucency is increased threefold when the DV-PIV is greater than the 95th percentile.21 Multiple authors have suggested that one way to utilize the DV in the first trimester is by using a two-step screening approach. This method may reduce the false-positive rates in fetuses that are considered at increased risk based on nuchal translucency and serum analyte screening and can be used to identify chromosomally normal fetuses that require fetal echocardiogram in the first and second trimesters.20,21,22,23,24
The pathophysiologic mechanism explaining abnormal DV waveform patterns in fetuses with increased nuchal translucency and CHD is not completely understood. Several proposed mechanisms include underlying cardiac dysfunction with
reduced myocardial compliance and fluid accumulation; impaired neural crest cell migration to the neck and conotruncus secondary to a hypoxic insult; and abnormal innervation or endothelial thickening of the DV.25,26,27,28 In fetuses with normal nuchal translucency measurements, abnormalities in the DV waveform are associated with adverse pregnancy outcomes, including cardiovascular defects, FGR, renal anomalies, and perinatal death.24 Identification of abnormalities in the DV waveform in the first trimester should be a clue to the clinician that such pregnancies should be monitored closely, and additional surveillance may include fetal echocardiography and third-trimester growth ultrasound in addition to the routine detailed anatomic review at 18 to 20 weeks’ gestation.
reduced myocardial compliance and fluid accumulation; impaired neural crest cell migration to the neck and conotruncus secondary to a hypoxic insult; and abnormal innervation or endothelial thickening of the DV.25,26,27,28 In fetuses with normal nuchal translucency measurements, abnormalities in the DV waveform are associated with adverse pregnancy outcomes, including cardiovascular defects, FGR, renal anomalies, and perinatal death.24 Identification of abnormalities in the DV waveform in the first trimester should be a clue to the clinician that such pregnancies should be monitored closely, and additional surveillance may include fetal echocardiography and third-trimester growth ultrasound in addition to the routine detailed anatomic review at 18 to 20 weeks’ gestation.
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