Two‐dimensional and color Doppler imaging

The performance of a fetal echocardiogram requires a comprehensive, systematic approach, including the determination of visceral and atrial situs, segmental anatomy, atrioventricular (AV) and ventriculoarterial (VA) concordance, and aortic and ductal arch morphology and position. Cross‐sectional and sagittal images through the fetal chest and short‐ and long‐axis imaging of the fetal heart are valuable in the evaluation of both normal and abnormal fetal cardiac anatomy. The vascular structures are positioned within the fluid‐filled lungs, providing a unique opportunity to appreciate the relationship of these structures to each other and their position within the thorax itself, akin to magnetic resonance imaging after birth.

Delineation of visceral and atrial situs requires an orientation to fetal position. This is one of the most challenging tasks for the fetal echocardiographer as there are innumerable fetal positions that may change throughout the course of the study. Fetal position should be determined by scanning from inferior to superior along the maternal abdomen. Examples of fetal position include vertex or cephalic, breech, and transverse. The fetal spine helps distinguish the anterior and posterior aspects of the body. Once the fetal position has been established, use of a doll or model can facilitate recognition of the left and right sides of the fetal body. In another technique described by Cordes et al. [20], the groove of the transducer is oriented to align with the long axis of the fetus with the head of the fetus on the right side of the screen. The transducer is subsequently rotated 90° clockwise to produce a cross‐sectional or transverse image of the fetal chest. In this manner, the scanner has oriented the fetus as breech, i.e., head into the screen. After determining anterior and posterior from the position of the spine, the left and right sides of the fetal body may be determined (Video 44.1). Whatever the technique, labeling may be appropriate. It is also important to note that any of the techniques may be prone to error and often necessitate a hands‐on approach by the reading physician, particularly in the context of more complex disease.

Once the left and right sides of the fetus have been determined, cross‐sectional sweeps from the abdomen to the chest provide information regarding visceral and atrial situs. A right‐dominant liver, left stomach and spleen, and right inferior vena cava (IVC) suggest visceral situs solitus (Figure 44.1). Sweeping to the fetal chest, the superior vena cava (SVC) moves anteriorly to connect to the floor of the right atrium (RA), just beneath the septum primum. A cross‐sectional image through the fetal chest provides images of the four chambers of the heart (Figure 44.2, Video 44.2). The heart should be roughly one‐third the size of the fetal chest. The cardiac axis, which is the axis of the ventricular septum relative to the midline of the fetal chest, is 43 ± 7° throughout the second and third trimesters in normal fetuses [21]. Interestingly, the heart is more mesocardic in the first trimester, rotating to the left by the twelfth week [22].

In the normal fetus, the RA and a portion of the RV are to the right of the midline. The left atrium (LA), left ventricle (LV), and a portion of the RV are to the left of the midline. Any change in cardiac axis or position of the four chambers relative to the midline should prompt a search for either intracardiac or intrathoracic (extracardiac) pathology, such as unilateral lung hypoplasia, congenital pulmonary airway malformation, pulmonary sequestration, or diaphragmatic hernia [23–25]. The LA is the most posterior four‐chamber structure, positioned just anterior to the descending aorta in the normal heart. At least one left and one right pulmonary vein on either side of the descending aorta should be demonstrated connecting to the LA at this level. Color Doppler settings need to be optimized, with an appropriately reduced Nyquist limit and increased color gain, to show the low‐velocity venous flow (Figure 44.3).

Evaluation of the atrial and ventricular septa is best accomplished from planes of imaging perpendicular to the septa, thus preventing dropout of thinner structures such as septum primum and the membranous ventricular septum. Assessment of the atrial septum should include imaging of septum secundum and primum and the foramen ovale. The “flap” of septum primum should be visualized in the LA consistent with right‐to‐left shunting at the foramen ovale in the normal fetus. Color flow Doppler should confirm low‐velocity right‐to‐left shunting at the atrial level (Figure 44.4). Sweeping posteriorly and inferiorly from the four‐chamber view, the coronary sinus is visualized as it courses within the left posterior atrioventricular groove. Dilation of the coronary sinus, which may be misinterpreted as an atrial septal defect at its mouth into the RA, suggests the presence of a persistent left superior vena cava (LSVC).

The mitral and tricuspid valves should be evaluated from both four‐chamber and short‐axis views. In the normal heart, there is a subtle offset of the valves with a more apically displaced septal leaflet of the tricuspid relative to the anterior leaflet of the mitral valve (Figure 44.2, Video 44.2). Sagittal views demonstrate the right SVC and IVC as they enter the RA (“bicaval view”), provide another view of the foramen ovale, and allow for visualization of the atrioventricular (AV) valve morphology en face (Figure 44.5). The anterior leaflet of the mitral valve may be inspected for a cleft and the papillary muscle architecture may be evaluated from this view.

The assessment of ventricular morphology may be more challenging in the fetus than the neonate owing to less prominent trabecular patterns. The RV has a more pyramidal shape with a trabeculated sinus and outflow or infundibulum from which one or both great arteries arise. Identification of the moderator band, best recognized in a four‐chamber image, is useful. In contrast, the LV is more bullet‐shaped and has a smooth septal surface. The AV valves, when of normal morphology, can further assist in defining the ventricles. The tricuspid valve is slightly apically displaced and consists of attachments to the ventricular septum. There are three leaflets with a variable number of papillary muscles. On the other hand, the mitral valve is comprised of two leaflets, both removed from the ventricular septum, and two papillary muscles (Figure 44.5d). In normal fetal anatomy, there is continuity between the anterior mitral valve leaflet and aortic valve (Figure 44.6a).

The ventricular septum, including the inlet, membranous, muscular, and outlet (conal septum) portions, is evaluated in multiple planes. At a minimum, 2D and color sweeps in the four‐chamber view (inferior to superior) and in the short‐axis view (right to left) should be performed. Additional oblique sweeps, akin to a postnatal parasternal long‐axis view, may be performed to assess the septum further. Slow sweeps with color flow imaging at lower‐velocity settings may permit detection of smaller ventricular septal defects.

Sweeping to the fetal head from a four‐chamber view, the ventricular outflow tracts and great arteries can be demonstrated (Figure 44.6, Video 44.3). The LV outflow tract (LVOT) arises more posterior and leftward relative to the right ventricular outflow tract (RVOT), and courses towards the right. The RVOT begins more anterior and courses leftward, wrapping around the LVOT to ultimately meet the pulmonary valve and main pulmonary artery. The main pulmonary artery is positioned to the left of the midline in the anterior–superior aspect of the fetal chest.

The three‐vessel view (3VV) facilitates the recognition of normal and abnormal great artery and arch anatomy relative to the trachea [26]. It is a cross‐sectional image obtained through the superior mediastinum. In normal fetuses, the 3VV demonstrates the relationship of the right SVC, ascending aorta, and main pulmonary artery to each other and to other structures within the fetal chest (Figure 44.7a, Video 44.4). The main pulmonary artery is the largest, most anterior and leftward vessel; the ascending aorta is the next biggest, rightward and slightly posterior to the main pulmonary artery; and the right SVC is the smallest, most rightward and posterior vessel. The right pulmonary artery may be seen coursing posterior to the ascending aorta and SVC, whereas visualization of the left pulmonary artery often requires a slight rotation of the transducer from a straight cross‐sectional plane as it courses slightly more inferiorly relative to the right pulmonary artery. The presence of an additional structure to the left of the main pulmonary artery and anterior to the left pulmonary artery often indicates the presence of a persistent LSVC.

The main pulmonary artery can be visualized joining the ductus arteriosus in the 3VV (Figure 44.7a, Video 44.4). The ductus arteriosus dives straight back just to the left of the midline to meet the left‐sided descending aorta in a normal fetus. Sweeping more superiorly towards the fetal head, the aortic arch can be seen coursing from right anterior to left posterior, crossing the midline towards the left of the trachea to ultimately join the descending aorta as well. These findings confirm the presence of left‐sided ductal and aortic ductal arches. If either arch reaches the descending aorta by coursing rightward of the trachea, then a vascular ring should be suspected.

The 3VV is important not only for evaluating the relationship of the great arteries and arches but also for assessing their relative sizes. The size relationship can assist in identifying subtle lesions or outflow tract obstruction. For example, a dilated right SVC may suggest an interrupted SVC with azygos continuation or a vein of Galen aneurysm, whereas aortic hypoplasia may indicate coarctation [27]. For the latter, color flow evaluation is particularly helpful. Flow persistence at the isthmus or even reversal in the transverse arch may be a potent marker of arch obstruction [28].

From the 3VV, one can rotate the transducer 90° to obtain sagittal or long‐axis images of the arches. By convention, the fetal head should be on the right of the screen.

The ascending aorta begins centrally and gives rise to the three brachiocephalic arteries before meeting the descending aorta posteriorly. In normally related great arteries, it has a “candy cane” shape (Figure 44.7b). Regardless of the orientation of the great arteries, it is the more superior arch. The ductus arteriosus arises anteriorly (in the context of normally related great arteries) and inferiorly and should not give rise to other vessels along its course. It has a more flat, “hockey‐stick” shape, joining the descending aorta at a nearly 90° angle (Figure 44.7c). Both arches may be visualized in a sweep with slight counterclockwise rotations.

Early in gestation, the left and right sides of the heart are usually symmetric or nearly symmetric in the normal fetus, particularly prior to 16 weeks. Later in gestation, however, the RA, RV, main pulmonary artery, and ductus arteriosus are mildly larger than the left‐sided structures [29,30]. Recognition of the normal degree of asymmetry is important in the detection of more subtle obstructive lesions, including coarctation of the aorta [31]. Use of nomograms and z‐scores for fetal cardiac dimensions, including valve size, ventricular dimensions, and great artery size, and the use of gestational age‐based z‐scores can help differentiate normal anatomy from abnormal pathology [32–34].

Spectral Doppler interrogation

Spectral Doppler interrogation is important for the evaluation of fetal function and rhythm and for the assessment of specific pathologic conditions, such as valve regurgitation or stenosis or ductal restriction. Routine interrogation of the ventricular inflows, outflows, arches, and pulmonary and systemic veins should be performed (Figure 44.8). Moreover, Doppler evaluation of the ductus venosus, umbilical artery and vein, and middle cerebral artery provides important information regarding overall fetal well‐being and peripheral flow (Figure 44.9).

Fetal heart function

Evaluation of fetal heart function requires an understanding of normal fetal cardiovascular physiology as well as developmental changes that occur over the course of gestation. At a minimum, function should be assessed qualitatively on all studies. Certain pathologic lesions require more extensive quantitative assessment, especially if fetal therapy is being considered.

Cardiomegaly and the presence or absence of hydrops may provide initial clues regarding fetal heart function. The fetal heart size may be measured by the cardiothoracic area ratio, where normal is considered <0.35. Systolic function is often assessed qualitatively, but it may be assessed quantitatively by measurement of the shortening fraction from either M‐mode or 2D images. In the normal fetus, the left and right ventricular shortening fraction is 34 ± 3% [35]. Normal is considered >28%. Although the use of ejection fraction has been documented using Simpson’s technique [36], the reproducibility is poor [37] and, therefore, this approach is not recommended. 3D and 4D echocardiography may ultimately provide the most accurate means of volumetric and mass assessment of the fetal heart (see section “Evolving and future directions”) [38–42].

Stroke volume and cardiac output can be readily assessed by fetal echocardiogram. However, the accuracy and reproducibility of these measurements have not been systematically evaluated. In the normal fetus, the RV contributes 60–65% of the cardiac output, while the LV contributes 35–40% [43–45]. Determination of cardiac output requires accurate measurements of semilunar valve diameters and Doppler interrogation of the outflow tracts with an angle of insonation of <20° to reduce errors. Using the following equation, the stroke volume is calculated: π(diameter/2)² × velocity time integral). Multiplying by heart rate yields the cardiac output. Given the unique nature of the fetal circulation, the combined cardiac output is often more useful. Normal combined output is 450 ± 50 mL/kg/min. Increased cardiac output may lead to high‐output cardiac failure and/or hydrops in various volume‐loading conditions, such as anemia, sacrococcygeal teratoma, agenesis of the ductus venosus, arteriovenous malformations, and acardiac twin gestations [46–49]. Since measurement of fetal combined cardiac output by echocardiography is subject to inherent variability of multiple measurements and a “gold standard” is not readily available, serial evaluation may be more important than individual measurements to help assess the clinical course and guide management and indication for fetal therapy.

Fetal diastolic function may be evaluated by utilizing tools similar to those used in postnatal echocardiography. Spectral Doppler assessment of the ventricular inflows, SVC, ductus venosus, and umbilical vein is critical to recognize alterations in diastolic function and should be performed routinely on fetal echocardiogram. Changes in diastolic function more than systolic function place the fetus at risk of heart failure and hydrops from elevated central venous pressure [50,51].

As gestation progresses, there is an increase in the E‐wave velocity of both ventricular inflows, which reflects developmental changes in the fetal myocardium that permits more efficient relaxation and greater compliance [52,53]. Simultaneous assessment of LV inflow and outflow by spectral Doppler permits measurement of the LV isovolumic relaxation time, which is 43 ± 8 ms (heart rate‐corrected) in the normal fetus from 20 weeks’ gestation to term [54]. Using tissue Doppler imaging (TDI), the same method may be applied to measure the RV isovolumic relaxation time.

The Tei or myocardial performance index may be used to assess global fetal myocardial function [55]. The Tei index equals the sum of the isovolumic relaxation and contraction times divided by the ejection time. It can be calculated for either the LV or RV using either PWD or TDI. In the normal second‐ or third‐trimester fetus, the Tei index decreases with gestational age, with the LV index showing a greater decline than the RV index [56]. The Tei index does not, however, discriminate between changes in systolic, diastolic, or combined cardiac dysfunction and may be difficult to measure and reproduce. As such, the Tei index is most often used to evaluate cardiac dysfunction in specific circumstances, such as cardiomyopathy or twin–twin transfusion syndrome [57].

TDI has been described in the assessment of fetal heart function for nearly two decades [58,59]. As is true for the postnatal patient, maximizing the frame rate, minimizing the angle of interrogation, and using a small Doppler gate are essential. In clinical practice, fetal TDI can be obtained in the majority of cases. Normal values for TDI, from 18 weeks’ gestational age to term, have been established for the LV wall, RV wall, and interventricular septum. LV and RV E/e′ normal values have also been published [60]. Generally, pulse‐wave TDI values increase as gestational age increases, with E/e′ values steadily decreasing. Color TDI has also been used to assess tissue strain and strain rate in the fetus [61]. The benefits of color TDI include being able to choose any region of interest offline for assessment [61,62]. However, like pulse‐wave TDI, color TDI remains angle dependent and requires special software that is only available for some systems.

More recently, 2D speckle‐tracking echocardiography (STE) has been applied to the fetal heart [63–65]. One of the main benefits of STE is that, unlike TDI, it is angle independent. This can help overcome some of the specific technical challenges that variable fetal position poses. STE allows for assessment of tissue motion at multiple sites and in multiple different planes (longitudinal, radial, and circumferential). Although STE may provide useful insights into fetal myocardial function and adaptation to pathologic conditions, there are technical challenges. High frame rates are essential, measurements may be time‐consuming, and significant differences in vendor platforms limit comparability across cohorts. As a result, STE currently remains largely a research tool.

Fetal rhythm assessment

A complete fetal echocardiogram includes assessment of fetal heart rate and rhythm. This is accomplished through the use of either M‐mode or PWD techniques that demonstrate the mechanical events of atrial and ventricular contraction by wall motion or flow, respectively (Figures 44.10 and 44.11) [66,67]. Several PWD techniques have been described to assess flow during atrial and ventricular contraction: simultaneous LV inflow and outflow (Figure 44.11a and b); pulmonary artery and pulmonary vein flow [68]; and SVC and ascending aortic flow [69] (Figure 44.11c and d). The mechanical PR interval may be measured readily from the simultaneous LV inflow and outflow tracing. These techniques are inherently limited by image resolution and fetal position and may require experience in interpreting the tracings. TDI with simultaneous evaluation of atrial and ventricular wall movement at multiple sites may prove to be the most effective echocardiographic technique for assessment of arrhythmias as it is less limited by image resolution and fetal position and may be easier to interpret [70].