This chapter is also covered by accompanying online material
Catherine Fredouille
CHAPTER CONTENTS
General notions
Review
Application to fetal cardiopathies
The heart examination is a critical moment in fetal ultrasound (US). After birth, cardiologists carry out this examination, but before then the fetal heart is seen by non-cardiologists. While it is not necessary to have the level of knowledge of a pediatric cardiologist to perform this systematic prenatal check-up, it is essential to acquire a simple, solid knowledge base if we are to carry out fetal heart examinations that are valid and have a long-term prognostic value.1
We hope that this will be the sort of book that we would have wanted to find years ago when we began studying fetal hearts. There are now excellent “classical” reference books that teach fetal cardiology. They usually contain much more than what is needed in our daily practice, and because of this, require long and attentive research to find the answers essential to fetal US. What we are trying to do here is provide a practical guide for the US practitioner, underlining the elements that we have found to be essential based on our experience.
The three of us are practicing fetal US specialists, each with different but constantly evolving and complementary interests and skills. Claudio Lombardi joined our team for this new edition because of his expertise in first trimester examination.2 Jean-Eric Develay–Morice is still involved in the technical aspects of our craft, specifically concentrating on finding new ways to diagnose previously “undiagnosable” pathologies. I spent many years in the anatomic examination of thousands of normal and pathological fetal hearts, using a strict segmental analysis. I apply this work to US–anatomic correlations. Over the years of close collaboration, we found that, above all, the US specialist needed tools to test for what we call “normality”.
Our experience has shown that the pathologies involved in the fetuses with the worst prognosis were always of the same type. We learned that what is “essential” is to be able to say that a fetal heart looks normal by checking for simple warning signs, rather than being able to precisely diagnose all types of pathologies. This is seen to be true in a great majority of cases.
When faced with a cardiopathy, the first role of the practitioner is to ensure that there is not an associated extracardiac pathology.
The warning signs we propose are simple, and we explain how to check for them. We do this using visual comparisons, which come from our experience gained during teaching numerous workshops in France and the Mediterranean region. We also kept what worked best in our original French edition, the same style, and the same conscious insistence on repetition.
Repetition has proved to be an essential part of our methodology, providing a book that is fundamental and practical for daily use. To increase its value as a training and reference tool, we have added references and clips which include US sequences, a large section on fetal heart anatomy, and anatomic and US correlations. We hope that you will find in this book and its clips practical keys to the practice of fetal heart US.
One of our primary intentions is to introduce information that is indispensable for verifying normal fetal heart architecture, as well as information useful in the detection of important pathologies. The precise diagnosis of cardiopathies, and their prognoses, remains the realm of the pediatric cardiologist.
The US practitioner has several aims. One is to verify normal fetal cardiac architecture, which also involves looking for cardiopathies in the case where another anomaly has presented itself during morphological examination. The discovery of an isolated cardiopathy is a rare event.
Here we will lay out a simple methodology capable of verifying normal fetal cardiac architecture in 3 steps and 10 key points. These key points have been defined through a series of US–anatomic correlations and tested by numerous US specialists. The diagnostic criteria are easily accessible and allow us to eliminate the cardiopathies as defined by an expert consensus.3
We begin by reviewing the knowledge essential in understanding what is normal, as well as pathologic, in the fetal heart. We then touch on those physical principles crucial in optimizing the examination itself, finally introducing our methodology. Next, we study the pathologies themselves, outlining the pitfalls involved in studying each one while proposing the best methods for avoiding these traps. Finally, we will describe the type of morphological examination necessary in those cases where a cardiopathy has been discovered, concluding with a review of points to remember.
General notions
In the fetus there are two types of cardiopathies that are important to detect:
• Cardiopathies that are warning signs of chromosomal anomalies, syndromes or associations. Our own fetal pathologic experience, as well as that of other teams,4 has shown that they mostly belong to two families: atrioventricular septal defects (AVSD) and conotruncal cardiopathies (CTC). In these pathologies, the cardiopathies are almost always linked to other markers essential when performing morphological US examinations.
• Complex cardiopathies (those that will become critical at birth). These cardiopathies are well tolerated in utero due to the presence of physiologic shunts. The karyotype and morphological studies are normal. After a very attentive verification of their isolated character during the morphological examination, the fetus is referred to the pediatric cardiologist. The pediatric cardiologist will then further clarify the diagnosis, considering the prognosis and organizing appropriate care at birth. In this category of critical cardiopathies we find complete transposition of the great vessels (TGV) that should be an obsession of every US specialist during examination of the fetus.
In this category of cardiopathies, you must equally eliminate the possibility of:
• An interruption of the aortic arch (IAA).
• An abnormal total anomalous pulmonary venous return (TAPVR)
• Critical pulmonary stenosis.
When faced with certain cardiopathies whose prognosis is very bleak, or when the cardiopathy itself is a warning sign of a more complex pathology, the pediatric cardiologist might be led to propose a medical termination of pregnancy (MTP). Fetal pathologic verification is therefore highly recommended.5 With the family's agreement, the fetal pathologist searches for those markers that were not visible during US in order to determine if the cardiopathy can be classified as a genetic syndrome or association. The results of this research allow us to propose appropriate genetic counseling for future pregnancies.
Half of the observed cardiopathies, with a frequency that has been consistently estimated at around 8 per 1000 births,6,7 will only develop after hemodynamic modifications take place after birth. Only 1 fetus in 250 carries a cardiopathy that is possibly detectable in utero.
Sonographic measurement of the nuchal translucency (NT) thickness at 11–13 weeks is a well-established screening method for aneuploidies and other major anomalies. Fetuses with increased nuchal translucency and normal karyotype have a high frequency of congenital heart disease (CHD).8,9 This justifies an early fetal heart examination.10
However, the main goal of first trimester scan will be to offer a systematic US investigation of fetal structures as a significant number of major anomalies (CHD included) are present in fetuses with normal NT.
In pregnancies without particular problems, the heart is systematically verified by morphological US at 20–22 weeks. Even when considered normal at this stage, the heart should be observed by growth US at 32 weeks. It seems clear that a strictly architectural pathology could not have begun to form between the 22nd and 32nd gestational weeks. For instance, a heart found to have an AVSD at a gestational age of 32 weeks was not normal earlier at 22 weeks; AVSD was present during the very first weeks of development. On the other hand, certain pathologies, even architectural ones, evolve in relation to flow. Pathologies such as pulmonary stenosis, which were invisible or poorly visualized, even passing unseen at 22 gestational weeks, can be individually observed at 32 weeks.
The result of such screening on the detection of CHD has been studied in Europe,11 showing variations depending on the different methods and protocols in use. The countries having the best results are those where every woman has access to three US examinations (at 12 weeks for NT, around the 22nd week with a morphological examination, and the third examination at 32 gestational weeks to check growth and re-verify the morphology). In certain countries, where legislation has modified this practice, the first trimester examination is now of first importance12 and give significant results13 when practised as explained in Chapter 5 of this book.
Though rarely seen, the predictive value of cardiac anomalies is an extremely important warning sign of other anomalies (when considering all CHD taken together, and in relation to the increased risk of chromosomal abnormalities). Because of these observations, when a cardiopathy is discovered using US, the practice of determining the karyotype becomes indispensable.14 This is especially true because we now know that there are chromosomal anomalies in more than 33% of the cases studied (more than 15% in those cases where the cardiopathy appears isolated, and around 40% in those cases reported when the morphological examination reveals an associated anomaly).15 A complementary examination researching the deletion of chromosome 22q11 will be requested in the case of conotruncal malformations.16 Here we see the important role the fetal pathologic examination plays when a pregnancy has been medically terminated for an “isolated” cardiopathy. Markers that were difficult or impossible to see during US can be present here, such as a dysmorphology or visceral situs anomalies. This will allow us to identify known or unknown polymalformation syndromes.17
The frequency of karyotype anomalies also varies depending on the type of cardiopathy observed. We know that there is an occurrence of nearly 40% of trisomy 21 (T21) when an AVSD has been diagnosed.18For instance, when faced with complete AVSD (Figs 1.1 and 1.2), if the karyotype is not known, we should first verify fetal nasal bone (NB).19 It is important to note that an incorrect size or absence (Fig. 1.3) here, like an amesophalangy or a brachymesophalangy (Fig. 1.4), represents an important complementary element. It is equally important to remember that in cases of IAA and coarctation of the B2 type (Figs 1.5 and 1.6),20which is a rare form of CTC, over 80% show a microdeletion in 22q11. Note also that in this particular CTC, provoked by a neural crest pathology,21 the presence of an outlet VSD is constant (Fig. 1.7).
FIGURE 1.1 Apical four-chamber view. Complete AVSD associating an ASD ostium primum with LIAVV and inlet VSD.
FIGURE 1.2 Illustration of the same complete AVSD as in Figure 1.1 (apical view).
FIGURE 1.3 Ultrasound profile of a T21 fetus; NB absent. Note the lingual protrusion and the width of the prefrontal panicle (arrows).
FIGURE 1.4 Hand of a T21 fetus with a brachymesophalangy (arrow) of the fifth digit.
FIGURE 1.5 Heart with a B2 IAA (dotted line) in a fetus with 22q11 deletion.
FIGURE 1.6 Diagram of an IAA in a B2 fetus.
FIGURE 1.7 US view: aorta overriding an outlet VSD.
Attention given to these confirmed anatomic findings in fetal pathology allow us to be sensitive to the presence of these pathologies, guiding our investigations. We know that:
• In all forms of AVSD, true linearity of the atrioventricular valves (AVV) is always found with a consistent absence of offsetting.22
• In all CTCs there exists a constant outlet VSD caused in most cases by misalignment, with the subsequent loss of left ventricle–aorta (LV–Ao) alignment.
These findings have led us to focus our research, not on all the important pathologic elements that could be detected, but rather to identify the minimum diagnostic criteria necessary, which, when used through systematic US examination of the heart, allow us eliminate these suspect pathologies.
The key to understanding our methodology is that it is based on the verification of the criteria for normality allowing us to eliminate any suspicion of important pathologies, rather than a strict sequential, segmental analysis,23 which creates an exhaustive search for each marker or each sign of any individual pathology. To use our method, we must clearly identify those elements that allow this verification, determining which views and images make this possible.
Criteria For Normality
1. In the four-chamber view (Fig. 1.8), the crux of the heart, with the two normally offset auricular–ventricular septal leaflets, allows us to eliminate the presence of the AVSD,24 which is a well-known marker for T21, as well as other pathologies.
FIGURE 1.8 On this view of four normal chambers we see normal offsetting and visualization of two pulmonary veins. We do not find any form of the AVSD spectrum or TAPVR.
2. One or two pulmonary veins extending into the left atrium (LA) in the four-chamber view (with or without Doppler) rules out the eventuality of TAPVR.25
3. A septal–aortic alignment in several incidences used to explore outflow allows us to rule out the diagnosis of VSD by misalignment, a type of VSD present in a large majority of CTCs (Fig. 1.9).
FIGURE 1.9 On this normal LV–Ao view we see a normal septal aortic continuity. There is no VSD by misalignment nor any atrioventricular discordance.
4. Two concordant and crossed arched vessels viewed together statically (Fig. 1.10), and one after the other in dynamic views, should allow us to eliminate the diagnosis of TGV.26
FIGURE 1.10 In this US view there is a normal ventricular–arterial concordance. There is no TGV or ventricular–arterial discordance.
5. A complete arch of regular diameter with normal branching, seen eventually in color Doppler (Fig. 1.11), rules out the suspicion of IAA. Its origin, at the center of the heart, is a negative argument to eliminate the diagnosis of TGV. Size here reassures us of the balance between the aorta and pulmonary trunk (PT), due to the fact that this is usually modified in most instances of CTC as well as right- or left-tract hypoplasias.
FIGURE 1.11 In this US view the aorta is seen rising in the center of the heart with a regular arch. IAA; TGV, and CTC are unlikely.
!!! Attention !!!
The ultrasound specialist who detects a cardiac anomaly during morphological ultrasound investigations, rather than attempting a precise cardiopathologic diagnosis, should continue the examination by searching for associated signs through a thorough and well-directed morphological examination.
Review
Simple points concerning the development, anatomy, and hemodynamic qualities of the fetal heart will improve our understanding and make the examination easier.
Development
While we know that simplistic explanations (we know to be “not really true”) can be of great help for the practitioner, we will not discuss here the recent and very complex findings about the heart development.27,28
The heart—whose architecture is definitive at a gestational age of 10 weeks in a fetus with a cranial rump length (CRL) of less than 4 cm—is the size of a grain of rice and beats at more than 160 times per minute.
Its evolution depends on genes of development and lateralization, primary and secondary heart fields as well as neural crests. The flow which begins to pass through it by the fifth week of gestation also contributes.
Seeing this in a very schematic way, the initial tube develops out of the islands of angioforming cells whose origin is splanchnopleuric and that are situated on the anterior pole of the embryo. Next, during the phase of delimitation, the explosive growth of the cephalic pole induces a coiling of the anterior pole of the embryo, causing the cardiac primordium to pivot by 180°. This then becomes ventral in relation to the cephalic pole and the stomodeum (the future mouth). The most anterior part of these tubes, formed by a symmetric tube pair that has become fused at their most distal section in the pericardiac cavity, becomes the cardiac tube itself. This tube then binds to the venous cardinal and vitellin systems (Fig. 1.12).
FIGURE 1.12 Left view of the cardiac tube with caudocranial flow.
The intrapericardiac portion of the fused tube, due to its growth in a limited space, will normally form a right loop (Fig. 1.13). This will then develop into an organ that is both uneven and asymmetric.
FIGURE 1.13 Left view of the tube after the formation of the right loop showing inlet and outlet flows.
The initial section, situated before the loop or inlet, is formed by a primitive atrium receiving the venous returns and communicating through a unique anulus, called the atrioventricular canal (AVC), with the primitive ventricle.
The distal section, situated after the loop, or outlet, is followed by the arterial system which is formed out of the common arterial trunk (CAT) and then followed by the aortic arches.
The evolution of this tube, with its chambers connected in series, is made by the compartmentalization of the inlet section. This section is located before the loop in a relatively orthogonal way in four chambers with:
• Auricular septation with two septa. The septum primum will only close at the end of AVC development. The initial AVC will produce two offset anuli (Figs 1.14 and 1.15).
FIGURE 1.14 Anterior view: vertical diagram of the heart before the division of the AVC and the initial CAT.
FIGURE 1.15 Anterior left view with a diagram of the stages of the transformation of the AVC into two annuli.
• At the same time the closing of the inlet section of the interventricular septum (IVS) will take place.
These phenomena, which are far more complex in reality, are still the focus of much fundamental research.28
We now arrive at the formation of parallel inlet tracts (Fig. 1.16), situated in the same plane.
FIGURE 1.16 Left view diagram of the “verticalized” heart: septation achieved. Black parallel arrows represent the inlet flow; the orthogonal white arrows represent the outlet flow.
It is this inlet plane that we have selected as the “optimal” four-chamber US view.
The outlet section undergoes far more complex modifications. Located after the loop, the distal section of the tube in which outflow is seen, is under the influence of neural crests.29 Here:
• The closing of the interventricular septum's outflow section occurs, which is located under the CAT. It appears more complex (role of a secondary heart field) than the closing of the inflow septum (Fig. 1.17). This septum, with alignment, closes under the aorta, while the conal or infundibular septum separates the two great vessels.
FIGURE 1.17 Diagram of the “verticalized” and opened heart. Localization of the inlet septum (yellow) and the outlet septum (alignment septum in white; infundibular in purple).
• Above the outlet septum, the walling in and spiraling of the common arterial trunk develops into two crossed vessels (Figs 1.18–1.23). They develop like this, above the alignment septum, each one out of its own outflow tract. These two crossed and arched vessels are separated by the infundibular or conal septum. Initially, in continuity with the right outlet flow, the aorta should be joined eventually to the left chamber to ensure left outlet flow.
FIGURE 1.18 Posterior right view of the fetal heart after ablation of the atria and the great vessels, showing the initial CAT and initial AVC.
FIGURE 1.19 Intermediary stage. Evolution: partial AVC dominated by two vessels in the process of spiraling and wall development.
FIGURE 1.20 Final stage. Inlet: two anuli on the same plane; outlet: two conjoined, superimposed, and orthogonal anuli (the inlet septum is yellow, the membranous septum is green, the alignment septum is represented by a dotted line, and the infundibular is purple).
FIGURE 1.21 Diagram of Figure 1.18 as seen from the posterior right.
FIGURE 1.22 Diagram of Figure 1.19 as seen from the posterior right.
FIGURE 1.23 Diagram of Figure 1.20 as seen from the posterior right.
The vessels have orifices that are conjoined but orthogonal, situated in superimposed levels (Fig. 1.24). They are linked to vessels derived from the aortic arches. This 6° arch gives rise to the right outlet: the PT; the pulmonary arteries and ductus arteriosus (DA). The 4° arch gives rise to the left outlet: the aorta and right subclavian artery (Fig. 1.25).
The position of the outlet tracts, with their superimposed orifices, initially has quasi-perpendicular trajectories whose objective is to join together the same vessel. This explains the necessity for multiple views using both static and dynamic methods in order to explore their subsequent trajectory.
FIGURE 1.24 Diagram of the outlet vessels with conjoined and orthogonal annuli over a closed IVS.
FIGURE 1.25 Evolution of the aortic arches: the 4° left arch becomes the aorta and the 6° arch becomes the pulmonary vessels (PT, PAs, and DA).
By our understanding of these simple observations, a verification of cardiac architecture involving several steps and at different levels can be performed: verification of position and that of the inlet and the outlet. These different steps become our guiding light, which, leading us from the normal to the pathologic, allows the development of a system for the classification of cardiopathies which is especially applicable in prenatal US examinations.
Anatomic Ultrasound Correlations
The heart—whose architecture is definitive by the time of its observation by US—has a size that varies between that of a chickpea (at 12 weeks) to that of an olive (at 22 weeks); by 32 weeks it is the size of an almond (Fig. 1.26).
FIGURE 1.26 Comparison of the size of a fetal heart at 12, 22, and 32 weeks' gestation.
Establishing the anatomic relationships within such a small organ is important, especially an organ that beats between 120 and 160 times per minute. It is also important to recognize that these relationships within the fetal heart differ in certain points from those in the adult heart. During its fetal existence, the heart has a left axis which makes an angle of 45° with the anteroposterior axis.
The heart is seen to be lying horizontally on the diaphragm, which is situated on the axial plane of the fetus.
This distinctive quality in relation to postnatal anatomy is explained by the volume of the fetal liver, and pulmonary vacuity (Fig. 1.27). The fetal heart is situated flat on the diaphragm, the apex directed to the left.
FIGURE 1.27 Fetal heart–lung block (HLB). The fetal heart is placed flat on the diaphragm (white line) with the apex pointed to the left.
Apart from the positioning of the heart itself, it is essential to differentiate the inlet and outlet. (Figs 1.28–1.30).
FIGURE 1.28 Posterior right view of the fetal heart after an ablation of the atria and the great vessels: inlet (black parallel arrows situated in the same plane); outlet (white orthogonal arrows seen in superimposed planes).
FIGURE 1.29 View of the fetal heart opened to the left: left inlet (yellow arrow) and outlet (black arrow). The red line, which rejoins the green triangle (representing the membranous septum), marks the limit between inlet and outlet.
FIGURE 1.30 The same view as in Figure 1.29 on a “verticalized” heart opened to the left (inlet: yellow; outlet: trabecular in white; and infundibular or conal in purple).
The inlet involves the pulmonary venous return (PVR) (Fig. 1.31) and the systemic venous return (SVR), which enter respectively into the left atrium (LA) and right atrium (RA).
FIGURE 1.31 Heart–lung block, front view. Heart swung to the right, “exposing” the left inferior pulmonary vein.
The primary element involved in the anchoring of the heart (the LA) is in a median position just before the spine. It is attached to the lungs (Figs 1.32 and 1.33) by the four pulmonary veins, which constitute the pulmonary venous return. The RA is right lateral, more anterior, and receives the systemic venous return. It is composed of three elements: the venae cavae, superior and inferior, which are situated in the cranial–caudal axis; and the coronary sinus (Fig. 1.34). This coronary sinus, which forms the SVR of the heart, heads towards the RA in the left atrioventricular groove.
FIGURE 1.32 Heart–lung block, posterior view. Systemic venous return by the ICV and SCV as obtained by probe and the PVR as shown by the yellow arrows.
FIGURE 1.33 Fetal heart, posterior view. Left atrium in front of the descending aorta; venous return by the four pulmonary veins.
FIGURE 1.34 Fetal heart, posterior view. Systemic venous return into the RA by the SVC and IVC and the CS.
Each inlet ventricular chamber should be in concordance with its homologous atrium: the RA with its right ventricular inflow chamber, and the same for the LA, which should be in concordance with the left ventricular inlet chamber. These four chambers, atrial and ventricular inlet chambers, are in the same axial plane and can be examined using the four-chamber view.
The “optimal” four-chamber view (Fig. 1.35)25 is defined to give us a reference view for examining all the key points concerning inlet, at the same time creating reproducible observations that can be referred to later, and clearly understood both in terms of fetal pathology and US. Situated on the same axial plane of the fetus, the view is defined by three reference points; these are the apex and the two inferior pulmonary veins.
FIGURE 1.35 Heart–lung block cut at the level of the optimal four-chamber view (the apex and two inferior PVs). The probe shows the trajectory of oxygenated flow from the IVC towards the RA through the FO. e, eustachian valve.
On this “optimal” view we can verify that:
• The apex of the heart is formed by the left ventricle (LV), itself characterized by the smoothness of the septum in this cavity.
• The anterior right ventricle (RV), which is retrosternal, is characterized by its coarse trabeculations.
• The crux of the heart is where the septal leaflets of the AVVs can be seen inserted in an offset fashion. The tricuspid detaches from the IVS closer to the apex, and the leaflet is linked to this septum by a septal attachment. The septal leaflet of the mitral valve has no such septal attachment.
Note the situation of the coronary sinus (Fig. 1.36), which is cut at the level of its initial section in the atrioventricular groove between the LV and the LA. Arriving after a posterior trajectory in the groove entering the RA, it is in proximity to the base of the interatrial septum (IAS).
FIGURE 1.36 “Optimal” anatomic four-chamber view. The probe is here at the emergence of the CS in the RA. The dotted line marks the posterior trajectory of the CS in the left inter-atrioventricular groove.
The Crux Of The Heart
It is here we find the essential foundation for our key point used in screening for AVSD pathologies (Fig. 1.37). Using the histologic examination (Fig. 1.38) and its various components will allow us to understand the differences in echogenicity that are important in order to be able to interpret this correctly.24
FIGURE 1.37 Macroscopic view of the crux of the heart: mitral leaflet without septal attachment whereas the tricuspid septal leaflet is “stuck” to the IVS in its initial section. The asterisks (*) mark the offset of the AV valves.
FIGURE 1.38 Histologic four-chamber view: Note the offsetting “*” in the insertion of the atrioventricular valves in the IVS.
• The anterior section of the IAS (the septum intermedium), where the valve of the foramen ovale (FO) is attached, is composed of muscular fibers that are transversally cut. It is thus echogenic no matter what US access is employed; it appears as a dotted image in this figure (Fig. 1.39).
FIGURE 1.39 Diagram of the crux of the heart. The dotted line marks the portion of the IAS that is hyperechogenic because of the transversal section of fibers of the septum intermedium.
• The fibers of the IVS are longitudinal to the axis of the septum; they are thus difficult to see by an apical incidence. When the ultrasonic beams are parallel, you can imagine observing a defect, whereas transverse access highlights this composition particularly well.
• The mitral leaflet, which is without attachment to the IVS, is of a fibrous nature and, in reality, is continuous with the septal tricuspid leaflet, which is of the same nature.
Between the IAS and the IVS the septal portions of the two leaflets are linked by an oblique intermediary zone (see Fig. 1.36).24 Given its fibrous nature this zone should be seen in US as an oblique line, which, by the mirroring effect, appears hyperechogenic when it is approached perpendicularly. It will not be seen if the approach is made along its axis.
It is the obliqueness of the intermediate zone that is responsible for the impression of offsetting the valves.
These specific histologic characteristics explain the constant echogenic character of the IAS (“the head” of the crux) and the poor visualization of the IVS when seen from the apex.
Outflow
This is composed of two arched tracts.
1. The left outlet uses the aorta (Figs 1.40 and 1.41), which begins in the center of the heart in continuity with the IVS, and also with the mitral anulus and the tricuspid anulus. The septal aortic continuity as well as the mitral aortic continuity are visible by a view which is close to the four-chamber view making an acute angle to them. The adjacency of the aortic and pulmonary anuli (conjoined but orthogonal) allows us to examine the two at once in the sagittal plane of the fetus by cutting the aortic anulus transversally and the pulmonary anulus longitudinally (Figs 1.42 and 1.43). This is the DA view.
FIGURE 1.40 Macroscopic anatomic view of the apical long axis of the LV–Ao.
FIGURE 1.41 Histologic view of the apical incidence LV–Ao. Note the offsetting at the level of the septal–aortic musculofibrous continuity. The difference in constitution and size—the thick, muscular IVS and the thin, fibrous aortic wall—explains the “misalignment” that is already present, in the absence of the defect and which always occurs in the presence of a subaortic defect.
FIGURE 1.42 Anatomic view—the “arterial duct view” (AD)—where the aorta is cut transversally and the PT longitudinally.
FIGURE 1.43 Situation of the viewing plane in the DA view (green line) on a diagram of the great vessels.
2. The right outlet (Fig. 1.44) is brought about by the PT at the top of the infundibulum. It is thick and filled with muscular fibers, marking the clear discontinuity between the tricuspid anulus and the PT. The angle between the four-chamber view and the right outlet is clearly less acute than that made by the left inlet with the left outlet due to the interposition of the infundibulum.
FIGURE 1.44 Open fetal heart from the right: departure of the PT above the infundibulum. This is why the angle between the right inlet and right outlet is less acute than that between the left inlet and left outlet.
The great vessels
The aorta and PT arise out of the superimposed rings in an orthogonal direction. They will join together on the same vessel (Fig. 1.45), the descending aorta which runs in front and to the left of the spine.
FIGURE 1.45 Diagram of the fetal heart with the US reference points (complete ribs, apex and two pulmonary veins, and the aorta). The arrows represent the great vessels leaving at the same level to rejoin the aorta by different trajectories.
The arches
The aortic arch, beginning in the center of the heart, is described as an arch formed by an acute angle. The ductal arch takes a trajectory that is practically rectilinear, anteroposterior, beginning in the retrosternal region with a ductal arch of an obtuse angle. Soon after its emergence from the RV, the PT gives rise, on its posterior side, to the two pulmonary arteries (PA); the right PA wraps the aortic root. After branching, the PT becomes the DA sharing a short, almost parallel, trajectory which can be best seen with the three-vessel view (Figs 1.46 and 1.47). This view—axial and slightly oblique—longitudinally cuts the upper part of the arches and transversally the right superior vena cava (SVC). From right to left we can see the SVC, the aorta and the DA.
FIGURE 1.46 Superior view of the HLB anatomic view at the level of the three vessels. The pulmonary trunk and aorta are cut longitudinally, and the SVC is cut transversally.
FIGURE 1.47 Corresponding US view to that in Figure 1.46. The three-vessels view or the view of the arches.
The junction of the great vessels with the descending aorta explains why they can both be observed through a left paravertebral window, giving us the possibility of a posterior approach through the three-vessel view as we have for the aortic arch.
The exploration of the great vessels, combined like a guédoufle (Fig. 1.48), can be visualized dynamically by passing from one tract to the other (Fig. 1.49). Depending on the angle, whether it is apical or oblique (Figs 1.50 and 1.51), the anatomic aspects of the views differ.
FIGURE 1.48 Guédoufle: the side containing oil represents the right outflow tract (RV–PT), the side containing vinegar represents the left outflow tract (LV–Ao). Guédoufle was described by Rabelais, a French author of the Renaissance period. This device contains vinegar and oil in two separated cavities which empty through two crossed tubes. Therefore, it looks similar to the heart cavities and the great vessels
FIGURE 1.49 Diagram of the “verticalized” heart showing sweeping movements of the RV–PT/LV–Ao.
FIGURE 1.50 Guédoufle: view of the ventricles with right outflow, RV–PT. Notice the moderator band in the right ventricle and two papillary muscles; one inferior, the other superior in the left ventricle.
FIGURE 1.51 Guédoufle: view of ventricles with left outflow: LV–Ao. The right pulmonary artery is cut transversally while wrapping the aortic root. The probe is in the left appendage.
If the complete verification of the two great vessels, both statically and dynamically, is not possible, the certainty of a normal ventricular arterial concordance is reassuring. When we see RV–PT or LV–Ao concordance, it allows us to assume, by definition, that transposition of the great vessels has not occurred, with the ventriculo-arterial discordance being the hallmark of this pathology.
In fact, an RV–PT concordance (Figs 1.52 and 1.53) is always accompanied by an LV–Ao concordance because while two appendages of the same type in isomerisms can exist, when there are two ventricles they are always different.
Knowledge of anatomic relationships allows us to understand that, contrary to the inlet tract with its four chambers situated in the same axial plane allowing exploration by the four-chamber view alone, the verification of the outlet, with its crossed and superimposed vessels, needs—more often than not—varied and complementary views, which are both static and dynamic.
FIGURE 1.52 Anatomic view of the vessels, the small axis. The RPA is cut longitudinally while wrapping the aortic root. There is a ventricular arterial concordance.
FIGURE 1.53 Ultrasound view of the same short axis view as in Figure 1.52.
Several Fetal Hemodynamic Elements
Fetal blood flow begins early, being identifiable by the fifth gestational week. This flow is an important element in the modeling of the heart. First linear, and then caudal–cranial, the flow undergoes an angulation during the formation of the heart loop which allows us to differentiate it in Figure 1.54: an inlet flow directed anteriorly and towards the left, in an axial plane, parallel with the diaphragm and in a continuum followed by an outlet flow located after the right loop and in a more cranial direction.
FIGURE 1.54 Left view of the cardiac tube after the right loop: identification of the inlet and outlet.
While the architecture is definite by ten weeks, the hemodynamics develop throughout pregnancy,30 resulting in the architecture of certain pathologies. The two physiologic shunts should be noted. The particularity of the fetal–maternal circulation rests on the existence of these shunts which close soon after birth. They are:
• The shunt passing through the FO from the RA (Fig. 1.55) towards the LA. Doppler demonstrates that the flow is caudal–cranial because it is coming up from the ICV.
FIGURE 1.55 Diagram of fetal hemodynamics: venous return and inlet. The red line shows the oxygenated flow coming from the IVC towards the left tract through the FO. Ar–Arantius canal.
• The shunt passing through the DA from the PT towards the descending aorta is an anteroposterior flow.
Two simple concepts help us to understand this:
1. The fetal heart ejects the flow it receives.
2. The size of the chamber or vessel is proportional to the flow that crosses it.
Normally, one sees the convergence of the systemic venal return (SVR) at the level of the entrance of the inlet tract in the RA. This includes:
• The flow of the SVC draining the upper part of the body.
• The majority of the flow of the inferior vena cava (IVC) draining the lower half.
• The coronary sinus (CS), which is the venous return of the heart.
The PVR converges into the LA by the four pulmonary veins, but also the oxygenated flow of the IVC. The oxygenated flow arrives by the umbilical vein and is then, in part, shunted towards the liver through the canal of Arantius. Here it reaches the LA where it is directed up by the Eustachian valve through the FO; this is the first physiologic shunt.
The balance of the RA/LA shunt is manifested by the normal presence of the valve of the FO in the LA, pushed by the flow.
The inlet flow then enters the chambers of the RV and LV, respectively, entering through the tricuspid and mitral valves.
Examples of inlet pathologies
Several examples of pathologies at the level of the inflow tract include:
• The lack of balance between the atria caused by an excess of inlet flow in the RA. For example:
– In the case of a partially abnormal PVR into a persistent left SVC, the coronary sinus (CS) drains a part of the pulmonary flow towards the RA. In certain circumstances the CS can be dilated to the point where it obstructs the entry flow into the LV.31
– In the case of tricuspid atresia, due to the failure of inflow entering the RV, the increase in right flow “pushes” the valve of the FO, which being “forced,” appears to be even more deviated to the left than normal.
• Inversion of the RA/LA flow in case of obstacles in the left tracts, an example being mitral atresia where there is an inversion of interauricular flow, the valve of the FO being in the RA instead of the LA.
A lack of balance between the atriums has repercussions on the ventricles.
Inlet anomalies are found using the four-chamber view.
Normally the outlets develop out of the two balanced ventricles separated by an intact septum and composed of two crossed vessels of comparable diameter, though the diameter of the PT is slightly superior to that of the aorta. These crossed vessels are superimposed with their conjoined anuli situated in two orthogonal planes (Fig. 1.56). Despite their different points of origin, the great vessels rejoin the same vessel, the descending aorta, situated in the back of the left section of the LA. The PT, after the emergence of the two pulmonary arteries (the RPA and LPA), is called the arterial duct; this is the second shunt. It has a rectilinear transit, anteroposterior, until reaching the descending aorta. The aorta describes a large, hook-shaped curve—the arch—before joining the descending aorta.
FIGURE 1.56 Diagram of fetal hemodynamics: the ductus arteriosus.
Flow in these two arches should occur in the same direction, and any inversion of flow in either of these vessels is always pathologic.32
Examples of outlet pathologies
When one of the two outlet tracts is stenotic or atresic, the other is dilated.
A large aorta is always accompanied by a small PA (and vice versa).
For the above reason, during the Doppler examination on the three-vessel view, we sometimes find the direction of the flow reversed in the ducts, which signifies a reverse flow of one of these vessels coming from the other; this is always pathologic.
If the ventricles situated under the unbalanced great vessels are balanced, we can equally assume the existence of a VSD, for example a large aorta coming out of the two ventricles, seen as being balanced in the four-chamber view, is inevitably overriding a VSD. It should be noted that in the case of an overriding aorta, the axis of the inlet of the heart is modified (with an axis steeper than 45°).33
These outlet anomalies can be researched using all views that explore outlet flow.
One should especially take note of aortic physiology. The coronary vessels, which are indispensable for support of the cardiac muscle, must at least receive minimal flow. In the case of aortic atresia, a retrograde vascularization by the DA is indispensable.
During the fetal period, this retrograde vascularization permits a tolerance for a cardiopathy called “duct dependent” until the closing of the DA after birth.
Other cardiopathies are also duct dependent, that is to say, dependent on the maintenance of a permeability of the CA. Their prognosis33 depends on the quality of care the newborn receives in appropriate settings. This is the case for TGV34 and certain cases of pulmonary atresia with VSD (PA with OS). In the case of TGV, the perinatal hemodynamic problems involving the DA and the FO require a follow-up with intensive cardiopediatric care. At the same time, in certain forms of PA with OS the initial portion of the PT is either difficult to observe or nonexistent, and the pulmonary vascularization is accomplished by collateral aortic arteries or main aortic–pulmonary collateral arteries (MAPCA).35 This systemic palliative vascularization can continue after birth, but its long-term consequences are harmful.
Application to fetal cardiopathies
Out of this very simplified vision of fetal development, anatomy, and hemodynamics, we created a classification that is of practical use in the investigation of the fetal heart.
This practical classification of prenatal screening begins with three principal categories:
• position anomalies
• inlet anomalies
• outlet anomalies.
Certain complex cardiopathies belong to several of the above categories. In each of these categories further anomalies associated with flow can be a part of the cardiopathy, increasing the severity. Examples are described below.
The Concept Of The Architectural Spectrum
An important idea coming out of our observations of fetal pathology is the concept of a spectrum of malformations. Of course there is not one type of complete AVSD and one type of partial AVSD any more than there is one type of normal heart; instead there is a large spectrum of AVSD malformations, with numerous intermediary forms.
We begin with a complete form of AVSD with a total absence of closing of the initial AVSD. Here we see that the large defect (Fig. 1.57) is due to the confluence of the ASD ostium primum and of the inlet VSD above the atrioventricular bridging leaflet, which remains in common (Figs 1.58 and 1.59). The minor form, which we discovered and published earlier,22,23 exhibits the absence of any offsetting between the AVV, with the linear insertion of these valves, or an LIAVV without any defect (Fig. 1.60). This also includes all other forms of partial AVSD; one type involves a mitral cleft associated with an ASD ostium primum (Fig. 1.61) or an inlet VSD (Fig. 1.62).
FIGURE 1.57 Diagram of the major form of complete AVSD: very incomplete auricular septation with a large septal defect.
FIGURE 1.58 Diagram of complete AVSD with intermedium septum (round and pointed with the departure of the flap valve).
FIGURE 1.59 Diagram of complete AVSD with attachment of the bridging leaflets on the top of the ventricular crest.
FIGURE 1.60 Diagram of partial AVSD: IAS defect (ostium primum type) associated with a mitral cleft.
FIGURE 1.61 Diagram of partial AVSD: IVS defect.
FIGURE 1.62 Diagram of the minor form AVSD: LIAVV without defect.
Building on the idea of these spectrum classifications we come to their practical application. We search systematically for warning signs which are the “lowest common denominator,” or the slightest sign, of these pathologies. In the case of the AVSD spectrum it appears to be the absence of a normal offsetting of the septal valves at the level of the crux of the heart, or linear insertion. This observation is more important, and easier to see, than the defects associated with AVSD itself.
In all cardiopathies of the AVSD spectrum, the AVV are linear.
For the CTC spectrum (Fig. 1.63), the outlet VSD is constant, usually by misalignment, with a loss of the septal–aortic continuity. This type of misalignment VSD is found in the great majority of anomalies of this spectrum including the CAT. There is also a spectrum which is defined by the direction of the swing of the infundibular septum. When there is an anterior swing that creates a progressive stenosis of the PT, we have a range of pathologies from tetralogy of Fallot (ToF) to PA with OS. In the case of a posterior swing of the infundibular septum, where it is the aorta which experiences stenosis, we observe (at the mild end of the spectrum) a syndrome of aortic coarctation through to (on the severe end of this same spectrum) an IAA. Concerning a posterior swing, the VSD observed is more frequently infundibular, thus very difficult to detect by echo. When we find ourselves in this situation, it is primarily the asymmetry of the vessel diameter that attracts our attention.
FIGURE 1.63 CTC spectrum shown starting with the major form (the CAT) to the minor form (the outlet septal defect). In the case of an anterior swing this is seen from tetralogy of Fallot to PA with OS. In the case of posterior swing, this is the syndrome of coarctation to IAA.
Our concept of spectrums exists equally for the following types:
• A spectrum of recurring familial cardiopathies. In certain familial hypoplasia of the left tract the spectrum can even reach extreme forms of LV hypoplasia (mitral atresia associated with or without aortic atresia) as well as simple bicuspid aorta, often ignored or asymptomatic, but which must be considered as a minor feature of the same disease.
• There is also a hemodynamic spectrum, which explains the evolutionary character of certain pathologies during the course of the pregnancy. An example is the evolution during pregnancy of a minor form of ToF into a major form such as PA with OS.
This system of classification does not rely on clinical knowledge, as do postnatal cardiology classifications,36 instead it is based on our extensive anatomic experience of fetal hearts. In effect, the cardiopathies of chromosomal anomalies, associations, sequences and polymalformation syndromes, which form the basis for decisions to medically interrupt pregnancy, for the most part, belong to the families of cardiopathies and major forms of the different spectrums listed above. They are very different from the pathologies seen by the pediatric cardiologist postnatally. To further underline and simplify this idea, we will now discuss several important points.
Certain simple anatomic warning signs are rarely used systematically, even though they optimize the examination itself.
Here are three examples:
• Two contiguous vessels of equal diameter, parallel at the abdominal level and behind the RA, signal an impairment of the anomalous SVR with interruption of the suprarenal portion of the IVC.37 This sign, very evocative of a visceral–atrial heterotaxia (VAH) with a left isomerism, is much easier to detect than the complex associated cardiopathies which are frequent, but far more difficult to diagnose.
• A right descending aorta is much easier to see on the four-chamber view than on the three-vessel view,38 and it is an excellent warning sign of CTC.
• The modification of the axis of the IVS,33 used in fetal pathology to judge asymmetry when inspecting an anatomic specimen, is equally easy to observe in US when we actually look for it.
Etiologic Orientation
Each family of cardiac pathologies is related to a type of fetal pathology and thus determines the morphological examination.
Faced with a position anomaly, we search for the normality of the karyotype39 and look for other vascular and/or morphological elements which are frequent in VAH.
Faced with an inlet anomaly belonging to the spectrum of AVSD, we first search, before the karyotype is known, for signs associated with T2111 and that of other chromosomal pathologies. If the karyotype is known to be normal,39 we must rather consider VAH and other syndromes, especially skeletal ones.
Faced with an outlet VSD, of a conotruncal variety, after searching for markers associated with the number of the chromosomal abnormalities, we look for those associated with deletions of the chromosome 22q11,16 then, if the results are negative, we search for signs of malformations.
We are not going to touch on rhythm or structural abnormalities at this time. These pathologies, which are very infrequent, modify the cardiac rhythm or the echogenicity of the heart. For this reason, they always attract attention, and should be referred immediately to the expertise of the pediatric cardiologist.
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