Chapter 12: COLOR DOPPLER SONOGRAPHY IN OBSTETRICS

Screening ultrasonography is generally performed with gray- scale two-dimensional (2D) ultrasonography, whereas more advanced studies can now utilize a vast array of technologies including three-dimensional (3D) ultrasonography, color Doppler sonography, power Doppler sonography, pulsed-wave Doppler sonography, continuous-wave Doppler sonography, tissue Doppler sonography, and B-flow imaging. Most of these techniques are mastered by experienced operators only, but color Doppler (CDUS) and power Doppler (PDUS) ultrasonography can also be used during the screening examination to reduce examination time and increase diagnostic confidence, especially in the case of an inadequate acoustic window (mainly due to maternal obesity).

Recently, CDUS/PDUS have also been used with 3D and four-dimensional (4D) techniques to display the vascular architecture of several organs and of the heart. In this chapter, the use of CDUS/PDUS is demonstrated to provide sonologists with some useful tools to use in their everyday practice. The use of 3D and 4D CDUS/PDUS for the prenatal diagnosis of congenital heart disease and vascular abnormalities is also discussed.

In the advanced prenatal diagnostic setting, CDUS/ PDUS can be used in several ways and with different objectives, as listed below.

1. To demonstrate normal/abnormal fetal cardiovascular anatomy. In fetal echocardiography, CDUS can be employed both in the sequential analysis and for the assessment of cardiac function. In the latter instance, it is used to demonstrate valve insufficiency and stenosis and to diagnose retrograde blood flow in cases of complete obstruction.¹ As far as sequential analysis is concerned, CDUS/PDUS allow faster identification of pulmonary and systemic venous returns and of normal/abnormal ventriculoarterial connections. CDUS is also needed to further examine fetal arteriovenous malformations, such as aneurysm of the vein of Galen, twin-to-twin transfusion syndrome, or TRAP (twin reversed arterial perfusion) syndrome, and sacrococcygeal teratoma.

2. To help identify circulatory characteristics of nonvascular fetal organs. CDUS can also be employed to enhance gray-scale recognition of fetal organs, especially in the case of a small acoustic window. For example, the visualization of soft tissues can be severely hampered in patients with severe obesity. In this case, CDUS may be used to trace vessels supplying certain organs to demonstrate their presence or absence. A common application of this principle is demonstrated by the detection of both renal arteries to confirm the presence of both kidneys. Another example is the display of both umbilical arteries in the fetal pelvis to help confirm the presence of the fetal bladder.

3. To guide pulsed-wave Doppler sampling of maternal and fetal vessels. In particular, assessment of uterine artery velocimetry requires the use of CDUS for identifying the corporal branch of the uterine artery at its crossing with the external iliac artery, which cannot be reproducibly visualized on gray-scale imaging.² Similarly, optimal peak systolic velocity measurements in the middle cerebral artery require CDUS of a vessel segment that is adjacent to the circle of Willis.³

4. To study the placenta and the umbilical cord, in those rare conditions in which abnormalities of the fetal adnexa are suspected. These include placenta accreta, and velamentous cord insertion or vasa previa.^4,5 In addition, CDUS/PDUS is also used to facilitate the assessment of the cord morphology (ie, single umbilical artery, coiling index, etc).

CDUS/PDUS are important techniques that can provide unique clinical findings often of decisive diagnostic importance. However, extraction of useful information from CDUS/PDUS depends on a correct setup. In fact, different types of applications require completely different and often opposite settings. Major considerations include distance of a vascular structure to the ultrasound transducer, vascular anatomy, blood flow velocity and pulsatility, and likelihood of gross movements in the explored anatomic region. All these variables should be considered prior to using CDUS/PDUS for the Doppler study of maternal or fetal vessels. Examiners should have a practical understanding of the physics of Doppler principles and how to optimize related settings on their ultrasound system. In this chapter, we briefly review the key settings that are used to optimize CDUS/PDUS sensitivity and for specific types of obstetrical investigations.

1. Angle of insonation. The key to a successful CDUS/PDUS examination is a correct alignment between the ultrasound beam and the axis of flow in the insonated vessel. This angle should be as close as possible to 0 degrees; beyond approximately 20 degrees, the sampling error and flow evaluation become increasingly unreliable if absolute blood flow is being measured.

2. Arterial blood flow. Arterial blood flow is pulsatile by definition and ranges, in main arteries, from 40 to 80 cm/s at midgestation. These 2 factors should be considered when adjusting the Doppler settings. In particular, for arterial blood flow, the pulse repetition frequency (PRF) should be kept relatively high and the wall filter medium. The probe transmission frequency should be targeted onto the specific region of interest, with lower frequencies selected for deeper examinations. The image persistence should generally be set from low to intermediate for the pulsatile flow to be optimally displayed (Figure 12-1). After adopting these settings, reasonably good CDUS/PDUS images can be obtained both in the fetal heart and peripheral circulation. For the latter, the PRF should be somewhat reduced, considering that the blood flow velocity decreases from the heart to the periphery. Finally, the priority or "balance" should be adjusted to ensure that optimal color Doppler information is displayed without obscuring adjacent gray-scale anatomy.

3. Venous blood flow. Venous blood flows have much less pulsatility than arterial ones and show velocities ranging from 10 to 30 cm/s. Hence, the Doppler settings should be adjusted to these figures, ie, low PRF and low wall filter. As for the priority, more emphasis should be applied for the color Doppler signal in order to display small vessels such as the intraparenchymal pulmonary veins, which are typically difficult to visualize on gray-scale imaging (Figure 12-2).

4. Differences between CDUS and PDUS. There are some basic differences between CDUS and PDUS that the reader should be aware of. These differences account for the preferential use of one of the 2 Doppler imaging methods for different applications and objectives. The main technical differences between CDUS and PDUS regard the display of velocity, direction, and turbulence of blood flow. In particular, CDUS indicates flow direction within a vessel, displayed by hues of blue and red, with lighter colors indicating higher velocities. Specific types of variance color maps are available in some ultrasound systems that provide additional information about the degree of flow turbulence that is present. At the same time, the laminar versus turbulent aspect of flow can be gathered, with turbulent flow shown as a mosaic flow with mixed blue and red pixels. Conversely, PDUS is also less angle dependent that CDUS, and is more effective in displaying small vessels and low velocities. Some of the newer hybrid forms of PDUS not only provide relatively improved sensitivity for the detection of low blood velocity, but information about flow direction as well. As a result, CDUS is generally employed in the assessment of central cardiovascular connections (Figure 12-3) and of valve competence (Figure 12-4), whereas PDUS is more appropriately used for the assessment of venous return, aortic arch branching patterns, and for the peripheral circulation (Figure 12-5).

A last note regarding the terminology used for CDUS/PDUS when used in association with 3D and 4D ultrasonography: In the literature, several terms have been used, but in this chapter only the simple "glassbody" mode will be used to describe the simultaneous rendering of soft tissues and blood vessels within the same volume data set. This modality is used to display cardiovascular structures within the context of an organ structure that is transparently shown with gray-scale imaging.

Fetal Heart

In this section, we briefly review the key features that CDUS can demonstrate in the fetal heart. Subsequently, we will also review the use of CDUS/PDUS to assess the peripheral circulation.

CDUS represents a mandatory component of fetal echocardiography.⁶ This imaging technique should be used to derive functional information on the fetal heart, but it can also be used to obtain anatomic information in the case of impaired acoustic window, eg, due to maternal obesity or fetal position. In the normal fetal heart, CDUS is used to demonstrate regular blood flow across atrioventricular and semilunar valves (see Figure 12-3). The flow across these valves should be laminar, which means that it is displayed as a smooth red/blue color with only minor changes to lighter hues of the same color across the valves if the Nyquist limit is almost reached by the blood flow velocity (the Nyquist limit is the maximum velocity allowed for any given PRF value after which the color map is inverted). At the same time, CDUS should rule out any valve regurgitation or stenosis. The former is diagnosed whenever retrograde, high-velocity, turbulent blood flow is detected during the phase of the cardiac cycle in which there should be no leakage across that valve, eg, during systole for atrioventricular valves (see Figure 12-4A). Heart valve stenosis is diagnosed when turbulent, high velocity blood flow is detected through a valve during the phase of the cardiac cycle in which it should indeed be open, eg, during systole for semilunar valves (see Figure 12-4B). As previously discussed, CDUS can also be used to confirm retrograde blood flow across the ductus arteriosus or the aortic arch in the case of complete outflow tract obstruction: the former is detected in cases of pulmonary valve atresia with an intact ventricular septum (Figure 12-6), the latter in cases of aortic atresia usually in the context of a hypoplastic left heart syndrome (Figure 12-7). The importance of the detection of retrograde blood flow across the ductus arteriosus or aortic arch is due to the fact that this finding identifies ductus dependency, and consequently tags the heart defect as a neonatal emergency. In fact, this means that that particular congenital heart disease requires the ductus to be patent for the neonate to survive. As soon as the ductus arteriosus closes, the neonate develops acute cardiac failure and dies. These concepts are more extensively illustrated in Chapter 6, where major congenital heart diseases are described.

In fetal echocardiography, CDUS is also used to confirm abnormal anatomy as seen on gray-scale imaging, whenever the confidence of the diagnosis is questionable. Examples of this confirmatory role of CDUS are shown in Figures 12-8 and 12-9. On the 4-chamber view CDUS can demonstrate (see Figure 12-8) the single atrioventricular orifice in atrioventricular septal defect (Figure 12-8C); the absent filling of one hypoplastic chamber in the case of tricuspid atresia or hypoplastic left heart syndrome; severe insufficiency of the tricuspid valve in the case of Ebstein anomaly or pulmonary atresia with intact ventricular septum (Figure 12-8A); ventricular disproportion in the case of aortic coarctation (Figure 12-8B); and confirmation of the existence of a ventricular septal defect by showing bidirectional shunt across it (Figure 12-8D). When used to assess the outflow tracts, CDUS can demonstrate (see Figure 12-9) the double right ventriculoarterial connection in double-outlet right ventricle; the ventriculoarterial discordance in transposition of the great arteries; and the malalignment ventricular septal defect with overriding aorta in tetralogy of Fallot.

If used routinely while scanning, it can also reveal unforeseen findings, such as small muscular ventricular septal defects not visible on gray-scale ultrasonography (Figure 12-10A), or mild flow insufficiency across a sonographically unremarkable tricuspid valve (Figure 12-10B), which could represent a finding associated with trisomy 21 in both the first and second trimesters.⁷

However, CDUS can also be effectively used to assess central cardiac connections when the acoustic window is inadequate during the screening examination of obese women. This challenge is becoming a pressing problem due to the global trend towards obesity.^8,9 In instances when even the existence of the 4-chambers and of the 2 outflow tracts are in doubt, the use of CDUS (with the lowest transmission frequency setting) can at least demonstrate the atrioventricular and ventriculoarterial connections that confirm the existence of 2 atria, 2 ventricles, and 2 outflows tracts.⁹

Another relatively novel application is 3D or 4D CDUS/PDUS, which has been recently employed to study heart defects that are difficult to characterize by conventional 2D ultrasonography. In particular, the spatiotemporal image correlation (STIC) algorithm has been advantageously employed to assess the neck vessels and the spatial orientation of the great arteries in conotruncal anomalies (Figure 12-11).^10,11 However, this tool can also be used to teach normal anatomy in training courses; in this case, the use of the glassbody visualization mode allows direct demonstration of the crossover of the great arteries (Figure 12-12A), and makes the identification of the pulmonary veins draining into the left atrium much more straightforward (Figure 12-12B).

Another application of CDUS is early fetal echocardiography. This examination is performed trasvaginally or transabdominally from 12 to 15 weeks of gestation for selected indications.^12,13 A list of the most common indications for early fetal echocardiography follows, in decreasing order of frequency:

• Enlarged nuchal translucency (NT) with normal karyotype

• Extracardiac anomaly detected on early fetal ultrasound

• Two or more siblings/relatives with major congenital heart disease

• Reassurance after a previous child has died of major congenital heart disease

In early pregnancy, the recognition of the central cardiovascular connection is greatly enhanced by the identification of blood flow across them. As an example, in Figure 12-13 the sequential analysis of a heart at 12 gestational weeks is shown with the help of tomographic ultrasound imaging, a display technique that provides sequential parallel views of the fetal heart on a single panel. As is evident, the recognition of the cardiac chambers and outflows as well as of the normalcy of flow across them is immediate, if CDUS is used.

In conclusion, the application of these Doppler techniques, possibly with volume sonography, represents an important component of an advanced examination of the fetal heart. The appropriate and limited use of CDUS may also be very helpful in the screening setting, both to shorten the time of examination and to improve anatomic assessment in cases where the image quality is limited mainly due to maternal obesity.

Central Venous System

As mentioned in the introduction to this chapter, CDUS/PDUS represent the best way to study vascular malformations, such as abnormal course and branching of major vessels or arteriovenous malformations. As far as the first group of conditions is concerned, ie, abnormal course and branching of major systemic arteries, we will show several cases in which a diagnosis of such abnormalities may involve clinical considerations. However, imaging techniques that combine CDUS/PDUS and volume sonography can be used to further investigate the flow characteristics of the entire fetal circulation. In particular, with the high-frequency transvaginal ultrasound transducers it is possible to demonstrate the whole fetal circulation as early as the 12th week of pregnancy (Figures 12-14 and 12-15). Using very sensitive power Doppler algorithms, it is also very simple to demonstrate normal vascular supply to most organs from 12 weeks' gestation onward (Figures 12-16 and 12-17). Using the same technique, it is possible to demonstrate the origin and course of the 2 umbilical arteries and their relationships with the femoral vessels (Figure 12-18).

Abnormalities of the systemic venous return, such as the umbilical vein and ductus venosus, are relatively common. Starting from the umbilical vein, the first abnormalitiy that can be disclosed by CDUS/PDUS is the persistence of the right umbilical vein (Figure 12-19). During the sixth gestational week, the right umbilical vein degenerates while the left one persists. The portion of the left umbilical vein between the liver and the sinus venosus subsequently involutes and the ductus venosus, connecting the left umbilical vein to the inferior vena cava, continues to develop.¹⁴ After birth, the left umbilical vein becomes the ligamentum teres. The right umbilical vein can abnormally persist with the left vein and can even completely replace the function of the left umbilical vein. In some cases, anomalous venous return has been reported to bypass the liver with aberrant drainage of blood directly into the right atrium. Persistence of the right umbilical vein has an incidence of about 1:450 in fetuses.¹⁵ Sonographically, this anomaly can be diagnosed because the intra-abdominal portion is seen to the right of the gall bladder, which is slightly displaced towards the midline. In contrast, the more frequent persistence of a left umbilical vein occurs when the midline vessel and the gall bladder are normally found in the right abdomen (see Figure 12-19). This finding can be considered as a normal variant because it is not associated with increased risk of fetal demise or associated structural anomalies.¹⁵

Occasionally, CDUS/PDUS are used to characterize a dilated intra-abdominal portion of the umbilical vein (Figures 12-20 and 12-21). This sonographic finding can involve the proximal intra-abdominal tract or the central intrahepatic umbilical vein. Some studies have reported an increased risk of fetal demise and structural abnormalities with umbilical vein varices.^16,17 Therefore, it has been proposed that early delivery at 32 to 34 weeks might avoid the risk of late unexplained fetal death associated in affected fetuses.¹⁶ However, this increased risk is probably limited to those cases in which there is abnormal, turbulent, high velocity blood flow across or near the varix (see Figure 12-20). In most cases, the risks related to this anomaly cease with delivery, because the intrahepatic portion of the umbilical vein will involute after the cord is severed. The only exception involves much more rare cases in which the varix is associated with partial failure to form critical porto-umbilical anastomoses.¹⁸ These fetuses can develop abnormal portohepatic shunting that may be responsible for abnormal liver function tests such as galactosemia and hyperammonemia.¹⁹ However, the shunt usually disappears after a few weeks and the liver function tests return to normal.

A third example of abnormal central venous return involves the ductus venosus. This vessel can be completely absent and replaced by collateral venous drainage that bypasses the liver. Collateral vessels have been found to course along the anterior liver surface before draining directly into the right atrium or into the infracardiac portion of the inferior vena cava (Figure 12-22). This anomaly is important to detect because it is often associated with signs of cardiac failure (pleural effusions, hydrops) and fetal anomalies.¹⁸

Abnormalities of the venae cavae can also occur during fetal development. In the early embryo, there are 2 superior venae cavae; the left one usually involutes, and the cerebral venous return from the left side is directed into the right superior vena cava through the innominate vein. However, the left superior vena cava more rarely persists either in association with the right one or as the only venous return from the fetal head. Usually, when it coexists with the right superior vena cava, the vein may drain directly into the right atrium or, more frequently, into the coronary sinus, which will consequently dilate to accommodate increased blood flow (Figure 12-23). Although this anomaly has been associated with major structural abnormalities, most investigators do not consider it clinically significant as an isolated finding.^20,21

Another aberration of the systemic venous return development is represented by interruption of the inferior vena cava, usually in the context of cardiosplenic syndromes (left atrial isomerism) (Figure 12-24). In these cases, the systemic venous return often relies on either azygos or hemi-azygous continuation into a right superior vena cava or persistent left superior vena cava, respectively (Figure 12-25).

The Aortic Arch

Major anomalies of the aortic arch, such as right or double arch, can occur with a variety of neck vessel branching patterns.²² In this section, we present only those variants associated with a retrotracheal sling, because newborn infants can develop dysphagia and respiratory embarassment due to esophageal and/or tracheal compression. The reason why we are illustrating these anomalies in this chapter is that these are only rarely detected on gray-scale ultrasonography but are readily detectable using CDUS/ PDUS. Doppler imaging techniques can be combined with volume sonography to improve characterization of these lesions. A retrotracheal sling can develop as a result of several aortic branching abnormalities that include double aortic arch, right aortic arch with aberrant origin of the right left subclavian artery, and left arch with an aberrant origin of the right subclavian artery (Figure 12-26). The latter anomaly, namely the aberrant right subclavian artery, has been found to be associated with Down syndrome both after birth and in utero.²³

The Normal Cerebral Circulation

Contemporary ultrasound equipment allows a detailed assessment of the cerebral circulation, especially if the examination is carried out with a transvaginal approach. In addition, the use of high-frequency transducers has made the assessment of the cerebral circulation feasible also in the late first trimester. We will initially review the application of CDUS/PDUS for evaluating the normal cerebral circulation in the first trimester fetus. The use of these imaging modalities will also be described in the second trimester fetus when assessment of the cerebral arteries and veins are more likely to be clinically relevant.

The latest advances in 4D ultrasonography and Doppler technologies permit demonstration of the cerebral circulation as early as 8 to 9 weeks of gestation. At this stage, both PDUS and B-flow techniques can be used to demonstrate the main branching of both internal carotid arteries as well as the basilar artery. Thereafter, the cerebral arteries and veins can be thoroughly studied. Both the spinal and the cerebral vessels can be clearly demonstrated at 12 to 14 weeks of gestation (Figure 12-27).

During the second and third trimesters, transvaginal neurosonography²⁴ can be used to demonstrate the cerebral blood supply, from the main arteries to the tiny parenchymal branches. The normal cerebral circulation is demonstrated in Figures 12-28,12-29, and 12-30. On the midsagittal view, the anterior cerebral artery with the pericallosal artery and its branches are visible (see Figure 12-28). Using the same plane, the larger veins are shown (see Figure 12-29), with the straight sinus coursing from the posterior aspect of the corpus callosum to the torcular herophili, and the superior sagittal sinus coursing under the calvarial vault. Close to the cranial base, the basilar artery and the internal carotid arteries are visible. If the fetal head is scanned from the posterior fontanell, the cerebellar blood supply and the torcular herophili can also be studied (see Figure 12-29). If attention is focused on the cortex, reducing the PRF to show low velocity vessels, tiny branches can be seen penetrating the white matter in a radial pattern (see Figures 12-29 and 12-30).

Considering the high resolution with which the normal circulation of the fetal brain can be demonstrated, it is not surprising that CDUS/PDUS can be used to both demonstrate blood vessel abnormalities (eg, vein of Galen aneurysm) and confirm abnormal central nervous system anatomy by demonstration of its abnormal vessel course and/or branching (eg, incomplete branching of the pericallosal artery for agenesis of the corpus callosum).

Cerebral Arteriovenous Malformations

The most important group of extracardiac anomalies that can be evaluated using CDUS/PDUS are the arteriovenous malformations that usually affect the cerebral circulation. It is believed that these malformations result from a disorder of the embryonic capillary maturation process, which leads to the formation of an arteriovenous shunt.²⁵ These arteriovenous malformations generally consist of a feeding artery, 1 or more mostly dilated draining veins, and a centrally located vascular nidus. The nidus itself is a conglomerate of atypical vessels of variable diameter and wall thickness, which does not contain normal capillaries. Alternatively, the central nidus can be absent and a large fistula connects the feeding artery with an aneurysmatic vein. These vascular abnormalities are relatively rare in the fetus, but can be well characterized by CDUS/PDUS. In most cases, cardiac overload or overt decompensation is already present by the time of diagnosis. The most common form of cerebral arteriovenous malformation in the fetus is represented by an aneurysm of the vein of Galen.^26,27 However, the architecture of the vascular malformation can vary significantly, with several variants being described after birth, when a detailed angiographic assessment of the lesion can be carried out.²⁵ The most common sites of cerebral arteriovenous malformations include, in addition to the vein of Galen, the torcular herophili and the anterior cerebral artery.

In the fetus, the diagnosis of a cerebral arteriovenous malformation is suspected on 2D ultrasonography when a large anechoic area is seen on the midline of the fetal brain, resembling, to a certain extent, a severely enlarged third ventricle (Figure 12-31A). The diagnosis is then confirmed by CDUS/PDUS that demonstrate the turbulent and vascular nature of the lesion (Figure 12-31B). As already mentioned, the site and the architecture of the vascular anomaly may vary, but it can be thoroughly mapped by CDUS/PDUS. Another vein of Galen aneurysm is shown in Figure 12-32. In most cases, severe cardiac overload is already present at the time of diagnosis (Figure 12-31D), and in some fetuses, cerebral hemorrhage and secondary ventricular dilatation may also be present (Figure 12-31A).

Other Conditions Associated with Arteriovenous Shunt

This group of anomalies includes neoplastic conditions characterized by a high blood flow, such as sacrococcygeal teratoma, twin-to-twin transfusion syndrome, and twin reversed arterial perfusion or TRAP sequence.

As far as the first condition is concerned, there is little interest in mapping the vascular bed of a large tumor, unless direct fetal interventional surgery is planned, in order to reduce the risk of high-output cardiac failure. In this case, it is important to identify the best vessel for possible alcohol ablation or laser therapy (Figure 12-33).²⁸

TRAP sequence, acardiac anomaly, or chorioangopagus parasiticus (acardius) are synonymous terms referring to a very rare complication of monochorionic multiple pregnancies. In this condition, the acardiac twin is abnormally perfused by a structurally normal co-twin (the pump twin) through a single superficial artery-to-artery placental anastomosis. The condition results in retrograde arterial blood flow from the "pump twin" towards the affected fetus. The affected fetus is commonly referred to as a "parasite twin" because it is hemodynamically dependent upon the pump twin (Figure 12-34). The main prenatal problems associated with the TRAP sequence are congestive heart failure of the pump twin, polyhydramnios, and preterm delivery, although intrauterine death of the pump twin has been reported even in the absence of such features.²⁹ In the TRAP sequence, the anastomosis between the pump twin and the acardiac twin can take several distinct forms that include a Y shaped, velamentous insertion of one cord, or with different insertions of the cord on the parasite twin. CDUS/PDUS is of fundamental importance to trace and display the circulatory anatomy for presurgical planning of cord coagulation in twin pregnancies with TRAP sequence.³⁰

As underlined in the Introduction, CDUS/PDUS can also be used to help identify fetal organs, or the absence thereof, by demonstrating their blood supply. At the same time, color Doppler demonstration of an aberrant blood supply is needed to confirm the diagnosis of some abnormalities, such as pulmonary sequestration. The former concept applies primarily to the corpus callosum: in fact, the sonographic visualization of this cerebral structure may be difficult in some cases, and it is well known that the pericallosal artery is malformed or absent in fetuses with callosal dysgenesis (Figure 12-35). Along the same lines, the renal arteries are sought to demonstrate the presence or absence of kidneys in cases of severe oligohydramnios (Figure 12-36).³¹ In this case, or if unilateral renal agenesis is suspected and the side of the fetus distant from the transducer is difficult to visualize, the use of CDUS/PDUS may help solve the diagnostic query by showing the presence or the absence of the corresponding renal artery and vein (see Figure 12-36C). The study of the renal blood supply is also useful in the characterization of rare anomalies such as duplex kidney, horseshoe kidney, or crossed ectopia (Figure 12-37). In fact, all these kidney abnormalities are associated with an abnormal branching pattern of the renal arteries from the aorta.³²

The fetal bladder can also be evaluated using CDUS/PDUS because it helps to differentiate cystic masses in the fetal pelvis. Color Doppler identification of both vesical arteries branching from the internal iliac arteries is of significant help (Figure 12-38). The color Doppler identification of the vesical arteries can be used to evaluate the possibility of bladder extrophy (Figure 12-39). This is a severe abnormality that is often difficult to diagnose and characterize, especially if it is not associated with an omphalocele and cloacal malformation. In bladder extrophy, the bladder wall does not close on the ventral side and lies open on the midline, between the cord insertion and external genitalia. The external genitalia can also be abnormal (eg, epispadius or hypospadius). The diagnosis of this rare anomaly is not always straightforward, and the additional information regarding the course of both vesical arteries may be helpful. For example, the 2 arteries show a converging course around a normal bladder, with an acute ventral angle (see Figure 12-38A). In the case of bladder extrophy, both arteries show a more parallel course, for the absence of bladder (see Figure 12-39). Both vesical arteries are also visualized to demonstrate a single umbilical artery, because these vessels are in direct connection with the umbilical arteries.

The prenatal diagnosis of congenital diaphragmatic hernia may also benefit from the application of CDUS/ PDUS. This malformation has a variable prognosis, depending on the presence of other anomalies, chromosomal aberrations, and the anatomic characteristics of the herniated abdominal contents into the chest. As further discussed in Chapter 13, a couple of significant poor prognostic indicators have been identified for isolated diaphragmatic hernia, namely a low lung-to-head ratio³³ and the presence of the liver in the thorax.³⁴ The assessment of the former relies on simple measurements using the gray-scale image. However, identification of the hepatic lobe in the thorax may offer some difficulties, considering that the echogenicity of the liver and the lung is quite similar. This is why CDUS/PDUS has been used to identify the suprahepatic veins and to confirm the intrathoracic position of the liver.³⁴ The use of CDUS/PDUS with low PRF can clearly demonstrate the intrathoracic location of suprahepatic veins, if the left hepatic lobe (or the right one in less common right-sided hernias) is indeed displaced into the thorax (Figure 12-40).

In addition to the localization of a normal or ectopic organ, such as the kidney or the bladder, CDUS/PDUS imaging is also needed for the differential diagnosis of hyperechoic lung lesions. It is well known that a homogeneously hyperechoic mass located within the lung could represent both a cystic adenomatoid malformation of the lung, microcystic variant, and an intralobar pulmonary sequestration. The differential diagnosis between the 2 conditions relies on the CDUS/PDUS demonstration of an afferent vessel branching off the descending aorta in the sequestration.³⁵ The same applies if the pulmonary sequestration appears to be extralobar, being apparently located below the diaphragm. Also in this case, an afferent vessel branching off the abdominal aorta should be visualized in order to reach the final diagnosis (Figure 12-41).

A final comment should be made regarding the use of CDUS/PDUS to assess the movements of amniotic fluid through the fetal high airways that include the nasal cavity, buccal cavity, pharynx, esophagus, and trachea. It is well established that the fetus expels and swallows lung fluid with breathing movements. Placement of a color Doppler sampling window or pulsed Doppler sample gate near the fetal nose, mouth, pharynx, or larynx easily detects fluid movement across the upper airway.³⁶ This may be helpful for assessing the integrity of the posterior palate and of the muscular reflex that may be impaired in some severe abnormalities of the musculoskeletal system, such as fetal akinesia deformation sequence.³⁷ However, such an approach is mainly used to evaluate the anatomy of the posterior and soft palate in those rare cases in which the fetus is at risk of a posterior cleft, either because of familial positive history or from suspicion of a more complex syndromic condition that may also include an abnormal posterior palate.³⁸

The use of CDUS/PDUS significantly reduces the exposure time that is typically required for pulsed-wave Doppler ultrasonography by making the identification of all maternal and fetal vessels easier and more straightforward. Hence, the examiner can use these imaging modalities to guide placement of the Doppler sample volume whenever there are difficulties in locating the adequate region of interest for a specific maternal and/or fetal vessel. In this section, we will describe only those Doppler testing procedures that have been established as clinically relevant for obstetrical care.

Uterine Artery in Screening Protocols for Intrauterine Growth Restriction/Preeclampsia

The medical literature regarding screening protocols for intrauterine growth restriction (IUGR) and/or preeclampsia is enormous. A discussion of the accuracy and results of screening protocols that are based on Doppler assessment of the uterine velocimetry is beyond the scope of this chapter. Uterine artery Doppler screening has yielded controversial results regarding its clinical usefulness in low-risk pregnancies, whereas it is unanimously accepted in high-risk cases.^{39,40, and 41} The sampling site and standardized measurement technique must be reproducible with consideration of factors that may influence the calculated pressure gradient and resistance indices as they change with the degree of branching from the main uterine artery.⁴² Hence, it has been proposed that uterine artery Doppler studies during pregnancy should be based on a sampling site at the ascending corporal branch as it crosses the external iliac vessels.⁴² This specific site can be confidently identified if this region of interest is assessed using CDUS (Figure 12-42).

Ductus Venosus in the Staging of Vascular Compromise in Fetuses with IUGR

The ductus venosus is another vessel that has proved very important, during the last decade, for the assessment of severe growth restriction.^43,44 From initial reports, it seems that its velocimetry may help identify the best timing for extraction of growth-restricted fetuses with evidence of hemodynamic compromise (eg, absent diastolic umbilical cord flow). The clinical usefulness of Doppler evaluation for the ductus arteriosus is currently under evaluation in a randomized clinical trial, the TRUFFLE (Trial of Umbilical and Fetal Flow in Europe) study.⁴⁵ Color Doppler ultrasonography can be very useful for guiding a pulsed-wave Doppler sample gate into the correct vessel for rapid and reliable flow velocity measurements (Figure 12-43).

Middle Cerebral Artery for Noninvasive Diagnosis and Monitoring of Fetal Anemia

The relationship between anemia and peak systolic velocity in the middle cerebral artery has been known for several years,⁴⁶ but only recently has its use for the diagnosis of fetal anemia been validated.^3,47 Assessment of the peak systolic velocity in the middle cerebral artery has now become an established tool in the diagnosis and follow-up of fetuses with anemia from different etiologies, including rhesus immunization,^47,48 parvovirus infection,⁴⁹ and twin-to-twin-transfusion syndrome.⁵⁰ A key point for reliable and clinically relevant evaluation of the peak systolic velocity in the middle cerebral artery is a proper sampling technique, for it has been shown that an improper approach can be the source of false-positive results.⁵¹ The accepted procedure for optimal sampling of this vessel is reported in the original paper by Mari et al.³ A transthalamic axial view of the fetal head should be obtained without applying excessive pressure on the maternal abdomen. The scanning plane should be moved caudally until the wings of the sphenoid bone become visible, color Doppler mode is activated with an adequate PRF, and the transducer is ideally tilted with an angle of insonation that is parallel to flow. The image should be magnified so that the circle of Willis occupies about half of the screen (Figure 12-44). Finally, the pulsed-wave Doppler mode is activated and a series of 3 or more velocity waveforms are recorded for subsequent measurements.

Conventional real-time gray-scale sonography provides excellent visualization of the placenta, the membranes, and umbilical cord. The 3 vessels of the cord, the placental and fetal cord insertion sites, the placental body, and its chorionic plate can all be demonstrated in most cases. Nevertheless, there are situations in which CDUS/PDUS may provide clinically relevant additional information.

Placenta and Membranes

CDUS/PDUS provides clinically useful information for several placental abnormalities. Chorioangioma was already discussed while describing the use of Doppler techniques to characterize arteriovenous malformations as an important cause for high-output cardiac failure.

Placenta accreta is a potentially life-threatening condition for the mother in which the placental chorion is not limited to the decidual lining and penetrates into the thickness of the myometrium. Under these circumstances, the placenta may only partially separate from the uterine wall, and this may lead to life-threathening hemorrhage.^4,52 Prospective diagnosis of this condition is extremely important, but unfortunately there is no completely sensitive and specific test for this condition.⁴ However, in those cases in which there are significant clinical risk factors, some investigators have described the use of CDUS/PDUS for enhancing diagnostic accuracy.⁵³ Lerner et al⁵⁴ used CDUS and transvaginal sonography to examine the placental flow patterns of 21 patients with persistent placenta previa. They found that turbulent blood flow extending from the placenta into surrounding tissues was very sensitive and correctly identified 5 patients with accreta. This finding was not present in any of the patients without accreta (Figure 12-45). The prenatal diagnosis of placenta accreta is further examined in Chapter 8.

Amniotic band syndrome has numerous and varied presentations. It is usually caused from ruptured membranes with successive wrapping of membranes around fetal body parts. The consequences may be devastating and lethal, as in the case of body stalk anomaly. Facial clefting and exencephaly can also be caused by amniotic bands involving the fetal head. However, there are also abnormalties that result from membranes wrapping around fetal limbs (Figure 12-46). In these cases, CDUS/PDUS may play a double role. On one hand, they can demonstrate if the cord is involved with the limb stricture.⁵⁵ On the other, these techniques can also be used to estimate the degree of constriction by using pulsed-wave Doppler ultrasonography to evaluate the limb blood flow: if forward flow is detected, then the band is not tight and ischemic necrosis of the extremity is unlikely, at least temporarily. If CDUS/PDUS fails to demonstrate flow in the limb arteries and veins or shows only very limited, high resistance forward flow, this finding suggests the presence of local ischemia that may cause limb amputation.⁵⁶ This type of functional assessment can be used to guide fetoscopy for removing the amniotic band in order to avoid the possibility of spontaneous limb amputation.⁵⁷

Umbilical Cord

One of the most important cord abnormalities for which CDUS/PDUS is of the greatest relevance is vasa previa. This condition occurs when anomalous placental vessels, which are usually confined to the placental chorionic plate, run along the membranes reaching the internal os of the cervix. This condition may be associated with a velamentous insertion of the umbilical cord or a succenturiate placental lobe. In such cases, there is great risk of fetal demise during labor due to compression or tearing of these unsupported vessels. Gray-scale ultrasonography can be used to detect this abnormality, but CDUS/PDUS are of fundamental importance in confirming the diagnosis (Figure 12-47).⁵⁸

The umbilical cord can typically be seen using gray-scale ultrasonography in most cases. However, CDUS/ PDUS certainly enhances its visualization under difficult conditions. The normal presence of 2 vesical arteries can be easily used to confirm a 2- or 3-vessel umbilical cord using CDUS/PDUS. Occasionally, these Doppler techniques can be used to detect aneurysmatic dilatation of a single umbilical artery (Figure 12-48). Color Doppler assessment of a free cord loop can be used to document the occurrence of a hypoplastic artery (Figure 12-49). On the same image, the coiling index, an increase of which has been associated with fetal demise, IUGR, and aneuploidy, can also be evaluated.^59,60

Doppler evaluation of the umbilical cord can be useful in the presence of severe oligohydramnios. In this case, CDUS/PDUS may demonstrate poorly visualized loops of cord within the uterus that may be mistaken for small amniotic fluid pockets. These techniques may also provide diagnostic clues for the presence of prolapsed umbilical cord in the presence of severe oligohydramnios as a result of premature ruptured membranes (Figure 12-50).

CDUS/PDUS is also the method of choice for demonstrating cord entanglement in monoamniotic twin pregnancies (Figure 12-51).⁶¹ In selected monochorionic twins with cord entanglement, Middeldorp et al have reported elective umbilical cord occlusion and transection in order to optimize the chances for a satisfactory outcome for one co-twin.⁶²

In this chapter we described potential applications of CDUS/PDUS for the study of the fetus and maternal circulation. Most of these concepts will also be addressed in other parts of this textbook edition, according to their most relevant clinical context. However, we believe that a summary of major applications for 2D and 3D color imaging is helpful for the reader. In addition to the diagnostic benefit for Doppler imaging during pregnancy, this technology may also help to reduce examination time during the course of routine diagnostic imaging practice.

Highlighted References