Abstract
The second of the two chapters on congenital heart disease deals with the less common conditions. Conditions covered include double-inlet ventricle, double-outlet ventricle, atrial isomerism and Ebstein’s anomaly. The conditions are well illustrated. A section follows on the pathological features of pulmonary arterial hypertension in congenital heart disease. A large section is devoted to common surgical operations for congenital heart disease that may be encountered by the pathologist, and a section is devoted to the pathological assessment of the operated heart with congenital heart disease.
5.1 Double Inlet Ventricle
This term describes an atrioventricular connection (univentricular atrioventricular connection): both atria are connected to one ventricle, either a morphologically right or morphologically left ventricle – the dominant ventricle (Figure 5.1). The inlet may be via two separate valves or via a common valve. There may be straddling of one valve (Figure 5.2). The other ventricle is usually rudimentary and connected to the dominant ventricle via a VSD. By definition the rudimentary ventricle lacks a connection with the atria but is connected to one of the great arteries. The term univentricular heart is sometimes even applied to these cases. Two ventricles, albeit one rudimentary, are present, but the heart is functionally univentricular [1].
Figure 5.1 Double inlet left ventricle (DILV). Heart sectioned in four-chamber view. There is a dominant left ventricle that occupies all the ventricular area. Both atrioventricular valves open into this ventricle. On the right of the field towards the atrioventricular junction the ventricular wall is thickened; this represents the posterior aspect of the rudimentary right ventricle. As is usual in DILV, the aorta arose from the rudimentary ventricle and there was subpulmonary stenosis.
Figure 5.2 Double inlet left ventricle: four-chamber view looking from posteriorly. The rudimentary right ventricle is to the left of the field with a restrictive VSD. The left atrioventricular valve straddles the VSD but is committed for most of its area to the dominant left ventricle. Pacing leads are visible on the left of the picture. This reflects the abnormalities of atrioventricular conduction frequent in double inlet left ventricle.
5.1.1 Double Inlet Left Ventricle
This is the commoner of the two forms of double inlet ventricle [2]. The left ventricle is identified by the pattern of trabeculations on its apical septal surface. The rudimentary right ventricle is usually situated on the anterosuperior aspect of the ventricular mass and is delimited externally by the epicardial coronary arteries. In most cases, there is discordance of the ventriculoarterial connections, the pulmonary artery arising from the dominant left ventricle and the aorta from the rudimentary right ventricle (Figure 5.3). The VSD is usually restrictive (Figure 5.4), and there is coarctation of the aorta. There may be subpulmonary stenosis. The conduction tissue is abnormally located and the origins and epicardial distribution of the coronary arteries may be variable (Figure 5.5). There may be atrial isomerism.
Figure 5.3 An explanted heart with double inlet left ventricle cut to demonstrate the right atrioventricular junction, VSD, both ventricular cavities and both ventriculoarterial junctions. The pulmonary artery arises from the left ventricle and the aorta from the rudimentary right ventricle. The VSD is restrictive. There is a muscular outlet septum above the VSD and separating both arterial valves.
(A) DILV. Close-up view of the ventricular septal defect. The defect is itself restrictive, but there is further narrowing of the aortic outflow by a hypertrophied muscular trabeculation immediately beneath the aortic valve.
(B) Another case of DILV. The ventricular septal defect is visible in the centre of the field. It is narrow and is further narrowed by circumferential endocardial thickening around its edges.
Figure 5.5 DILV. The roots of both great arteries have been transected and viewed from above. The aortic valve is anterior and to the left of the pulmonary valve. Both coronary arteries arise from the right-facing sinus (Sinus 1) of the aortic valve. The pulmonary valve is bicuspid and dysplastic.
The term “Holmes’ heart” is applied if the ventriculoarterial connection is concordant.
5.1.2 Double Inlet Right Ventricle
This malformation is very rare and extreme forms may show double inlet and double outlet from the dominant right ventricle (Figure 5.6). The rudimentary left ventricle lies postero-inferiorly in the ventricular mass.
(A) Double inlet right ventricle. Heart cut in a four-chamber view and viewed from behind. There is a common atrioventricular valve that is almost exclusively committed to the dominant right ventricle. The rudimentary left ventricle is present on the left of the field.
(B) Double outlet right ventricle. Same heart as in part A, cut to show the ventriculoarterial junctions. The aorta (on the left of the picture) arises from the dominant right ventricle. It is separated by a muscular outlet septum from the pulmonary artery, also arising from the right ventricle (double outlet right ventricle).
Very rarely no rudimentary second chamber can be identified in the ventricular mass, and the dominant chamber is then characterised as indeterminate.
A Fontan operation is the usual surgical treatment of double inlet ventricle. A subset of patients can benefit from septation of the ventricle without the need for Fontan [3, 4].
5.2 Double Outlet Ventricle
This term describes a ventriculoarterial connection in which both great arteries (or to be more precise, more than half of each great artery) arise from the same ventricle [5]. Naturally, that ventricle may be either a right or a left ventricle – or even an indeterminate one. The term encompasses many conditions, some dominated by other features such as atrial isomerism.
5.2.1 Double Outlet Right Ventricle (DORV)
Double outlet from the right ventricle is much commoner than double outlet from the left ventricle, albeit both conditions are rare. In the setting of usual atrial arrangement and concordant atrioventricular connections, DORV shows a VSD – usually of perimembranous type – located between the limbs of the septomarginal trabeculation, beneath the outflow tract of the aortic valve. When both valves arise exclusively from the right ventricle, the aorta has a complete muscular infundibulum and the outlet septum is exclusively a right ventricular structure (Figure 5.7). It shows anterior deviation to cause subpulmonary obstruction. If the aortic valve overrides the VSD, the morphology then resembles that of tetralogy of Fallot (Figure 5.8). A less common variant is where the VSD is subpulmonary, but still between the limbs of the septomarginal trabeculation – the so-called Taussig–Bing heart. There is usually associated subaortic stenosis or coarctation of the aorta. A further variant of DORV shows a juxta-arterial doubly committed VSD with absence of the outlet septum.
Figure 5.7 Double outlet right ventricle, bilateral muscular infundibulum. Heart from an infant with DORV. The heart is viewed from the right side following removal of its parietal wall. The aorta arises anteriorly (to the right of the picture) with a subaortic VSD. It has a complete muscular infundibulum and is separated from the narrowed pulmonary outflow by a muscular outlet septum. The pulmonary valve is severely stenotic.
Figure 5.8 Double outlet right ventricle of Fallot type. The anterior part of the pulmonary outflow tract has been removed to show the obstruction caused by the anomalous anterior insertion of the supraventricular crest into the anterior limb of the septomarginal trabeculation. The VSD is not well seen. The aorta is to the left of the pulmonary artery.
Double outlet right ventricle is a common feature of hearts with right atrial isomerism, pulmonary atresia or stenosis, occurring in approximately half of the cases. Coronary artery abnormalities are frequent with DORV such as origin of both arteries from the same sinus [6].
The aim of surgical correction is to connect the aorta to the left ventricle without causing obstruction to either arterial outflow [7]. This may involve only the use of a patch (Figure 5.9), but more complex operations involving tunnels and even arterial switch may be required where the anatomy is more complex. Arterial switch is the operation of choice in the Taussig–Bing heart [8].
Figure 5.9 Double outlet right ventricle with patched VSD. A one-year-old child with DORV, subpulmonary stenosis and non-restrictive VSD treated by patch of the VSD and RV to PA conduit. The heart shows the aorta lying over the right ventricle, but the patch is inserted in such a way as to commit the aorta to the left ventricle. This new ventricular outflow tract incorporates what was originally part of the right ventricle. The left heart structures are relatively small and the VSD diameter is less than that of the aortic valve (restrictive VSD). Immediately beneath the aorta in the picture lies the RV–PA conduit.
5.3 Abnormalities of the Pulmonary Veins
5.3.1 A Preliminary Note on Terminology
Be careful with the terminology used to describe abnormal pulmonary veins. There is a difference between pulmonary venous connection and pulmonary venous drainage. Connection is an anatomical term denoting physical continuity between the pulmonary and systemic veins (either partial or total). Drainage is a physiological term denoting direction of the pulmonary venous blood to the systemic circulation. Thus, one can have normal connection with anomalous drainage as, for example, with a common atrium there is normal pulmonary venous connection but anomalous venous drainage. Anomalous connection with normal drainage does not occur.
5.3.2 Anomalous Pulmonary Venous Connection
This may be partial or total [9]. Although the veins may connect separately to an anomalous site, it is more usual for them to join to form a single channel that then connects anomalously. The anomalous connection may be to the heart itself or to the veins draining to the superior caval vein (supracardiac) (Figure 5.10)or to those draining to the inferior caval vein (infracardiac) (Figure 5.11). Frequently there is an element of obstruction to flow in the anomalous pathway. Anomalous venous connection may occur as an isolated abnormality but may also occur as part of a more complex malformation. Morphologically, the left atrium is small in total anomalous pulmonary venous connection because of the lack of pulmonary venous inflow. Pulmonary hypertension develops early. (Figure 5.12). Clinically, the infant with non-obstructive total anomalous pulmonary venous connection does not present with symptoms for the first few months of life. Respiratory difficulty and failure to thrive are the commonest features. However, if obstruction is present, the infant presents in the first few days of life with cyanosis and respiratory difficulty.
(A) The pericardium has been removed and the great vessels dissected to demonstrate an abnormal ascending vein that connects with the innominate vein on its left side. This ascending vein was formed by the confluence of the pulmonary veins that showed no attachment to the left atrium.
(B) Same case with the heart lifted upwards to demonstrate the confluence of the pulmonary veins and the ascending vein that runs on the left side (right of the field) posterior to the left pulmonary artery.
(C) Histological section of the ascending vein to demonstrate the normal pulmonary venous histology.
Figure 5.11 Total anomalous pulmonary venous connection (infracardiac). A dissection of the posterior aspect of the liver following removal of part of the quadrate and left lobes. The inferior caval vein runs obliquely over the right upper field and the portal vein on the lower left. The hepatic artery and its branches are retracted adjacent to the gallbladder. The fibrous remnant of the venous duct connects the upper border of the portal vein confluence to the inferior caval vein. The upper forceps grasp the cut end of the descending pulmonary venous confluence that enters the left portal vein.
Figure 5.12 Obstructed total pulmonary venous connection – pulmonary venous hypertension. A histological section from the lung shows a large pulmonary vein with a greatly thickened wall caused by medial and intimal deposition of collagen and elastic tissue (EvG stain).
The sites of infracardiac connection include portal vein, hepatic vein and ductus venosus. Connection is rarely directly to the inferior caval vein. Obstruction is much more likely with infracardiac connection (Figure 5.11).
Supracardiac connection is commoner and may be to superior caval vein (on either side), azygos vein or innominate vein. Cardiac connection is almost always to the coronary sinus.
Total anomalous pulmonary venous connection is usual in right atrial isomerism.
Partial anomalous pulmonary venous connection may involve one or more veins and may involve the drainage from a whole lung. Partial anomalous connection is an integral part of the sinus venosus ASD. It is also a component of the scimitar syndrome [10].
The aims of surgical correction are to achieve connection of the pulmonary veins to the left atrium without compromise to either systemic or pulmonary venous pathways. In the case of connection to the coronary sinus this can usually be effected by simple excision of the roof of the sinus. For supracardiac and infracardiac defects the anomalous pulmonary veins are connected directly to the left atrium (Figure 5.13). Mortality rates may approach 10% [11].
Figure 5.13 Total anomalous pulmonary venous connection – reconnection of pulmonary veins to the left atrium. Three-day-old infant who died following repair of total anomalous pulmonary venous connection. The heart is viewed from behind. The cannula tips are inserted in the five pulmonary veins that have been anastomosed into the wall of the left atrium.
5.3.3 Pulmonary Vein Stenosis
Pulmonary vein stenosis usually affects all four pulmonary veins, but may be unilateral or affect a single vein [12]. The vein is affected at its junction with the left atrium; the stenosis can be discrete or tubular. The narrowing may be visible externally or the affected vessels may appear macroscopically normal from the outside (Figure 5.14) [12, 13].
Obstruction to the pulmonary venous return causes pulmonary hypertension: the pulmonary veins show medial hypertrophy and fibrous intimal thickening. The parenchymal pulmonary arteries show medial hypertrophy with or without intimal fibrous proliferation (Figure 5.15). Plexiform lesions are not seen. The changes of pulmonary arterial hypertension may be present in both lungs, even in the presence of unilateral stenosis.
Figure 5.15 Pulmonary vein stenosis – histology of the lungs. There is pulmonary arterial hypertension. The muscular pulmonary arteries are tortuous and show muscular thickening of their tunica media. The small arteries are muscularised and there is very prominent dilatation of lymphatic vessels in the connective tissue of the bronchovascular bundle.
Histologically, the stenotic segment of vein shows fibroelastic thickening of the intima (Figure 5.16) [13]. There may be associated disruption and irregularity of the media. There may be associated intracardiac abnormalities. The stenosis is congenital and is thought to develop in utero after the incorporation of the pulmonary veins into the left atrium. The lesions may progress by the development of thrombus.
In its most severe form, congenital pulmonary vein stenosis is a progressive disease with rapid pulmonary hypertension and rare survival beyond the first year of life. Surgical intervention has not been successful in this group.
5.4 Ebstein’s Malformation
The essential defect in this malformation is an abnormally low attachment of the tricuspid valve. The attachment, instead of being at the atrioventricular junction, is in the inlet part of the right ventricle [14]. The valvar tissue, therefore, is attached to myocardium rather than the fibrous tissue at the atrioventricular junction. The septal and inferior leaflets show the abnormal attachment, and the septal leaflet is sometimes no more than a row of nodular excrescences descending towards the apex in an oblique line on the right aspect of the interventricular septum (Figure 5.17). The anterosuperior leaflet is also abnormal, being large and rectangular and attached to the papillary muscles in such a way as to obstruct the inflow (Figure 5.18). The valvar tissue is frequently dysplastic with excess of redundant valvar tissue. The area of ventricular myocardium incorporated into the right atrium by the abnormally low attachment of the valve becomes thin and “atrialised” (Figure 5.19). The valve is incompetent, and there is massive dilatation of the right atrium (Figure 5.20). Pulmonary stenosis (or atresia) is a frequent association. The condition may present in utero with cardiac failure and hydrops. There is also frequently associated Wolff–Parkinson–White syndrome [15]. In congenitally corrected transposition, the left-sided tricuspid valve may show Ebstein’s malformation (Figure 5.21) [16]. Surgical repair depends on the severity of the displacement of the septal and inferior leaflets and involves mobilisation of the anterosuperior leaflet, reduction of the diameter of the annulus and longitudinal plication of the atrialised right ventricular wall [17].
Figure 5.17 Ebstein’s anomaly. The right atrioventricular junction is viewed from the right side. The true atrioventricular junction in this picture runs in an arc from just beneath the coronary sinus to the pin head on the lower border used to fix the specimen in place. The septal leaflet of the AV valve is poorly formed and is not attached at this junction. Rather, it descends almost vertically from the medial commissure leaving a triangle of thinned ventricular myocardium above it as part of the right atrium.
(A) The leaflet is abnormal in shape and shows numerous short chordal attachments to the papillary muscle forming a barrier to inflow of blood at this site.
(B) Viewed from the right side, the obliteration of the normal pathway is evident. Blood is directed superiorly through the side of the leaflet rather than to the apex.
Figure 5.18 Ebstein’s anomaly: anterosuperior leaflet.
Figure 5.19 Ebstein’s anomaly – atrialisation of the right ventricle. This four-chamber view of the heart shows that most of the right ventricle is incorporated into the right atrium. Only a shallow crescent of the cavity lies beneath the level of the AV valve.
Figure 5.20 Ebstein’s anomaly – right atrial dilatation. The heart is viewed from the right side. Dysplastic valvar tissue is attached to the interventricular septum. The right atrium is dilated and is larger than the right ventricle.
(B) An unfixed heart cut in a simulated long-axis view showing the attachment of the left atrioventricular valve half way between the atrioventricular junction and the ventricular apex causing the upper part of the ventricle to be incorporated into the left atrium.
Figure 5.21 Ebstein’s anomaly of left AV valve in congenitally corrected transposition.
5.5 Tricuspid Atresia
The tricuspid valve may be very small in pulmonary atresia with intact septum, analogous to the mitral valve in hypoplastic left heart (Figure 5.22). It may at times be only a thin membrane occluding a small right atrioventricular junction. In both these instances there is a distinct right atrioventricular junction. In tricuspid atresia, by contrast the right atrium is separated from the right ventricle by a layer of muscle. Tricuspid atresia is an uncommon malformation where there is complete absence of the tricuspid valve, its site being marked by a dimple in the floor of the right atrium that is not the valve, but rather the atrioventricular membranous septum (Figure 5.23) [18]. Tricuspid atresia is associated with ASD with all the systemic venous return passing to the left ventricle; the right ventricle is small, even rudimentary, and, of necessity, connected to the left ventricle via a VSD, which is frequently restrictive (Figure 5.24) [1]. The ventriculoarterial connections are usually concordant, the restrictive VSD thus causing subpulmonary stenosis. A persistent Chiari network may be found in the right atrium in association with tricuspid atresia (Figure 5.25) [19]. Surgical palliation is by Fontan operation and may require staging [20].
Figure 5.22 Tricuspid valvar stenosis. Four-month-old infant with pulmonary atresia with intact septum. A simulated four-chamber view of the heart shows hypertrophy of the walls of the right atrium and right ventricle. The right ventricular cavity is small and the right AV valve small in comparison with the left.
Figure 5.23 Tricuspid atresia. The heart is cut in a simulated four-chamber view and viewed from behind. The right atrium and right ventricle are both small, and there is no connection between them. The left ventricular cavity is dilated and shows endocardial fibrosis. There is a large VSD between the ventricles.
Figure 5.24 Tricuspid atresia. Heart cut in a simulated four-chamber view. There is no communication between the right atrium and right ventricle. They are separated by a double layer of myocardium. There is an ASD and a VSD. The left ventricle is dilated.
5.6 Other Abnormalities of the Tricuspid Valve
5.6.1 Unguarded Tricuspid Orifice
This is a condition that clinically may mimic tricuspid atresia. It occurs in the setting of pulmonary atresia with intact septum. The right atrioventricular junction is widely patent but shows no atrioventricular valvar tissue. In contrast to most cases of pulmonary atresia with intact septum, where the right ventricle is small and very muscular, in unguarded tricuspid orifice the right ventricle is very dilated and very thin-walled. Papillary muscles are not discernible. The condition may occur on the left side in congenitally corrected transposition. When Ebstein’s malformation is present but with right ventricular dilatation, the condition may be difficult to distinguish from congenitally unguarded tricuspid orifice (Figure 5.26) [21].
Figure 5.26 Unguarded tricuspid orifice. Fetal heart from a fetus who died of fetal hydrops. The heart is cut in a simulated four-chamber view. The left atrium and ventricle are of normal size, but the right ventricle and right atrium are greatly dilated and thin-walled. No tricuspid valvar tissue is identified.
5.6.2 Absent Commissure
In cases of trisomy 21, there may be a defect in the tricuspid valve with absence of the commissure between the anterosuperior and septal leaflets, sometimes associated with enlargement of the membranous septum (Figure 5.27) [22].
Figure 5.27 Medial commissure tricuspid valve in trisomy 21. The membranous septum is enlarged and the valvar tissue of the septal and anterosuperior leaflets of the tricuspid valve does not quite meet over the septum. Viewed from the left side, such hearts show the plunging crest of the muscular interventricular septum that equates to the scooped-out crest seen in atrioventricular septal defect.
5.7 Uhl’s Anomaly
This describes the very rare condition of congenital absence of the myocardium of the parietal wall of the right ventricle [23]. It may be detected in utero [24]. It can present into adulthood, but in the neonatal period presents as cyanosis and congestive heart failure [25]. The right atrium is hypertrophied and dilated with endocardial thickening. The right ventricle is very dilated and very thin-walled. There is near complete absence of the myocardium of the parietal wall of the right ventricle. The interventricular septum is unremarkable, and the septomarginal trabeculation and the papillary muscles of the tricuspid valve are normally muscularised. The tricuspid valve is normal. The extent of thinning of the free wall of the right ventricle varies, sometimes the entire free wall, including the apex, being free of muscle and in other cases, the apical trabeculations persisting, albeit in an atrophic state (Figure 5.28). Histologically, the parietal wall shows apposition of the endocardium and epicardium, separated by a thin layer of elastic and fibrous tissue with no fatty tissue interposed between these layers. These changes are present at birth and may be detected in utero.
Figure 5.28 Uhl’s anomaly. Endomyocardial biopsy from a one-year-old boy. On echocardiography thin-walled right ventricle with dilated but normally sited tricuspid valve. The trabeculations are weedy and contain scant myocardium with thickening of the endocardium. On their own these features are not diagnostic of Uhl’s anomaly but in context are in keeping with the diagnosis.
There has been confusion of Uhl’s anomaly with arrhythmogenic right ventricular cardiomyopathy (ARVC) in the literature in the past [26]. ARVC is characterised by patchy replacement of the parietal wall of the right ventricle by fibrofatty tissue. This adipose replacement occurs primarily within the ventricular outflow tract, but can also be seen in the inlet or apical regions, sometimes spreading to involve the left ventricle [26]. ARVC is not seen in children below the age of nine to ten years. Table 5.1 shows the differentiation of the various forms of thin-walled right ventricle.
| Uhl’s anomaly | ARVC | Ebstein’s anomaly | Unguarded tricuspid orifice | |
|---|---|---|---|---|
| RV dilatation | +++ | ++ | +/− | +++ |
| RA dilatation | + | − | ++ | ++ |
| Fibrosis RV | ++ | ++ | Inlet | ++ |
| Fat RV | − | +++ | − | − |
| Tricuspid valve | N | N | Displaced septal leaflet | Absent |
| Pulmonary valve | N | N | N/atretic | Atretic |
| Usual age at presentation | Neonate | Adolescent and older | Infant and child | Neonate |
| Associated cardiac malformations | +/− | − | + | + |
| Arrhythmia | − | +++ | +/− | − |
N, normal.
Surgical treatment of Uhl’s anomaly usually consists of plication of the ventricle and establishment of cavo-pulmonary anastomosis [27].
5.8 Atrial Isomerism
Atrial isomerism represents complex anomalies of laterality. The normal arrangement of left and right atria is abolished and instead the heart has either two morphologically right atria or two morphologically left atria. It should be stressed that there is still a right-sided atrium and a left-sided atrium, but that both atria have the characteristics of either a morphologically right or of a morphologically left atrium. The recognition of morphologically right or left atrium depends on the morphology of the atrial appendage. As noted in the section on normal anatomy, the right atrium has an appendage that is broad and triangular with a broad junction with its atrium and pectinate muscles that completely surrounds the AV valve orifice; the left atrial appendage is long and tubular with a distal hook, a narrow junction with its atrium and pectinate muscles confined to the appendage proper.
Atrial isomerism, thus, can occur in right or left forms. Atrial isomerism may exist without other disturbance of laterality, but frequently occurs with isomerism of the bronchial arrangement (Figure 5.29) [28]. Normally, the right main bronchus is short and epiarterial, is that to say, it gives off its upper lobe branch at the same level as the pulmonary artery. The normal left main bronchus is long and hyparterial, that is to say, it divides below the level of the pulmonary artery on that side. In right bronchial isomerism both bronchi are short and epiarterial, while in left bronchial isomerism, both bronchi are long and hyparterial. There may be isomerism of other organs (see below). Within the chest the heart is often abnormally positioned and may be on the right, the left or in the middle, and, likewise, the apex may be directed to the left, the right or centrally [29].
(A) Right atrial isomerism. The heart has been removed to demonstrate the trachea and bronchi. Both main bronchi are short and lie practically horizontally, in keeping with right bronchial morphology. There is anomalous pulmonary venous connection with the pulmonary veins coming to a confluence beneath the carina and ascending behind the trachea.
(B) Left atrial isomerism. The main bronchi are again isomeric, but long and unbranched in keeping with left isomerism.
5.8.1 Right Atrial Isomerism
By definition, these hearts show bilateral morphologically right atrial appendages. Usually there are bilateral superior caval veins entering the roof of the atrial chamber (Figure 5.30). The inferior caval vein may be a central structure or may, less commonly, be bilateral. The interatrial septum is usually rudimentary. The coronary sinus is absent because, although draining to the right atrium, the coronary sinus is, in effect, a left-sided structure. The pulmonary venous connection is anomalous, to an extracardiac site in most cases. Typically there is double inlet ventricle with a common atrioventricular valve, discordant ventriculoarterial connection or double outlet ventricle with associated pulmonary stenosis or atresia (Figure 5.31). There may be right bronchial isomerism with bilateral tri-lobed lungs, asplenia and a central liver with symmetrical right and left lobes. The stomach may be on the left or the right side, and there is intestinal malrotation.
Figure 5.30 Right atrial isomerism. A fetus of 22 weeks’ gestation with isomerism of the right atrial appendages. There were also bilateral superior caval veins, complete atrioventricular septal defect, supracardiac total anomalous pulmonary venous connection, pulmonary atresia and aortopulmonary collateral arteries and absent arterial duct. The heart is viewed from the front after removing the aorta. There are bilateral right atrial appendages and both superior caval veins can be seen. The pulmonary trunk and pulmonary branch arteries are small. The ascending anomalous pulmonary vein can just be made out beneath the left main bronchus.
Figure 5.31 Right atrial isomerism. Double inlet right ventricle with AVSD, discordant VA connection and subpulmonary stenosis. The picture shows the aorta arising from a dominant right ventricle and the pulmonary trunk from a rudimentary left ventricle with VSD. A muscular outlet septum lies between the two outflows above the VSD. The pulmonary outflow is narrow.
5.8.2 Left Atrial Isomerism
Again, by definition, there are bilateral morphologically left atrial appendages (Figure 5.32). As with right atrial isomerism, there are usually bilateral superior caval veins. Pulmonary venous connection is usually to the atrial mass. Typically, there is interruption of the inferior caval vein with continuation as the azygos vein to the superior caval vein (Figure 5.33). The hepatic veins drain separately to the atria, sometimes bilaterally. The atrial septum tends to be better formed than in right isomerism. There is usually an atrioventricular septal defect (Figure 5.34). The ventriculoarterial connection is usually concordant with normal relations of the great arteries. Coarctation or interrupted aortic arch may be present.
Figure 5.32 Left atrial isomerism. A fetus of 13 weeks’ gestation. The heart shows bilateral morphologically left atrial appendages. There was also bilateral superior caval veins, double inlet left ventricle with common atrioventricular valve, rudimentary right ventricle with VSD and lacking an inlet, discordant ventriculoarterial connections with anterior aorta, right-sided stomach with multiple small spleens and intestinal malrotation.
Figure 5.33 Left atrial isomerism; azygos continuation of the IVC. The heart and lungs are viewed from behind; both lungs are bilobed. The aortic arch is left-sided. There are probes in both superior caval veins. An obturator is placed in the connection of the hepatic veins to the heart, and a pair of forceps is inserted into the azygos continuation of the interior caval vein that is greatly dilated and loops forward over the right main bronchus to join with the right-sided superior caval vein.
Figure 5.34 left atrial isomerism: AVSD. Fetal heart at 20 weeks’ gestation cut in a simulated four-chamber view and viewed from posteriorly. There is situs inversus with a right-directed apex. There are bilateral left atrial appendages and there is a complete atrioventricular septal defect with bridging leaflet.
The viscera may show left bronchial isomerism with bilateral two-lobed lungs, and there may be polysplenia (Figure 5.35).
Figure 5.35 Left atrial isomerism. Polysplenia. Same case as Figure 5.34. There were multiple right-sided spleens. A histological section shows multiple nodules of splenic tissue.
Table 5.2 lists the features of both forms of isomerism of the atrial appendages.
| Feature | RAA | LAA |
|---|---|---|
| Atrial appendage | Bilateral right | Bilateral left |
| Coronary sinus | Absent | Usually present |
| SVC | Bilateral | Bilateral |
| Pulmonary veins | Anomalous connection ~50% to extracardiac site | Connect to atrial mass usually bilaterally |
| IVC | Normal connection | Interruption with azygos continuation |
| Hepatic veins | Drain to IVC | Drain directly to atria |
| AV connections | Usually common junction DIRV | Usually common junction |
| VA connections | Discordant or DORV | Concordant |
| Ventricular outflow tract | RV outflow obstruction | LV outlet obstruction, coarctation, interruption of aorta |
DIRV, double inlet right ventricle; DORV, double outlet right ventricle; LAA, left atrial appendage; RAA, right atrial appendage.
5.8.3 Juxtaposition of the Atrial Appendages
In the normal situation the atrial appendages lie on either side of the great arteries. Sometimes both atrial appendages lie side by side on one side of the great arteries [30]. This situation is termed “juxtaposition of the atrial appendages”, and it is more common for the right atrial appendage to be thus abnormally located (Figure 5.36). This condition is usually associated with other cardiac malformations, particularly complete transposition [31].
Figure 5.36 Juxtaposition of the atrial appendages. Heart of a fetus of 15 weeks’ gestation viewed from the front. There is juxtaposition of the atrial appendages, both lying to the left-hand side of the aorta. The right appendage lying more to the left side than the left appendage. Internally there was pulmonary atresia with VSD.
5.9 Structural Abnormalities of the Coronary Arteries
These are dealt with in some detail in the separate chapter on the coronary arteries.
5.10 Other Abnormalities
5.10.1 Persistent Left Superior Caval Vein
This is a relatively frequent occurrence (approximately 0.5% of the general population) [32] and may occur in an otherwise normal individual. Its incidence is increased in association with congenital heart disease, and it is an almost invariable finding with right atrial isomerism (Figure 5.37). The vein drains to the coronary sinus, and the blood enters the right atrium. There is absence of the innominate vein in about 40% of cases.
Figure 5.37 Persistent left superior caval vein. Intrauterine fetal death from retroplacental haemorrhage at 24 weeks’ gestation. Following removal of the pericardium there are bilateral superior caval veins joined by a thread-like brachiocephalic vein. The left caval vein is connected to the coronary sinus, which was correspondingly enlarged. Internally there was a small ASD but no other abnormality.
5.10.2 Aberrant Origin of Right Subclavian Artery
In this anomaly the right subclavian artery does not take origin from the brachiocephalic artery but from the left side of the descending aortic arch after it gives off the left subclavian artery. There is a female preponderance. The majority of cases occur in isolation (Figure 5.38), but it may be associated with coarctation (where it more usually arises distal to the coarctation than proximal to it) or interruption of the aortic arch [33]. An aberrant left subclavian artery may arise in the setting of a right aortic arch (Figure 5.39). In these cases the arterial ligament (ligamentum arteriosum) arises from the left pulmonary artery, passes to the left of the trachea and oesophagus, and connects to the aortic arch at the site of the aortic diverticulum (Kommerell), giving rise to the aberrant artery [34].
Figure 5.38 Retro-oesophageal right subclavian artery. An eighteen-month-old child with tetralogy of Fallot (operated). The thoracic organs are viewed from behind. The aortic arch is left sided. Taking origin from the aorta as it begins to descend, there is a right subclavian artery that travels behind the oesophagus and trachea to reach the right axilla. There is no dilatation of the aorta at this point.
Figure 5.39 Aberrant origin of left subclavian artery. Fetus of 34 weeks’ gestational age with tetralogy of Fallot. The thoracic and abdominal organs are viewed from behind. There is a right-sided aortic arch, as there is in approximately 25% of cases of Fallot. The left subclavian artery takes origin from a diverticulum (of Kommerell) at the left side of the descending aorta. A left-sided arterial duct is connected to the left side of the diverticulum forming a complete vascular ring enclosing trachea and oesophagus. There is a constriction of the diverticulum at its attachment to the aorta. This vascular ring has the potential to constrict the oesophagus.
5.10.3 Kommerell’s Diverticulum
Kommerell’s diverticulum describes the presence of the aneurysm-like funnel-shaped widening at the origin and proximal-most segment of an aberrant subclavian artery – whether right or left [35]. When associated with a right aortic arch and left duct, there is a complete vascular ring, and there is potential for oesophageal or tracheal compression. The diverticulum is frequently of the same size as the aorta but does narrow at the origin of the subclavian artery. In adults aortic dissection beginning in the diverticulum is described and the diverticulum may also rupture. In adults there is a high incidence of cystic medial degeneration in the wall of the resected diverticulum [36].
Current treatment is to resect the diverticulum, divide the ligamentum arteriosum and reimplant the subclavian artery into the common carotid artery [37].
Histologically the diverticulum may show intimal proliferation and may be obstructed (Figure 5.40).
(A) Resected diverticulum from a case of right aortic arch and left retro-oesophageal subclavian artery and left arterial duct. Viewed from the side, the closed arterial duct is on the top right of the specimen. The subclavian artery arises from the left side of the specimen, and the aorta is attached at the bottom right.
(B) Histological section stained with Elastic vanGieson. The arterial duct is evident in the top right of the field, recognisable by its loose elastic structure. The ductal lumen shows fibrous obliteration. The subclavian arterial lumen is to the left and the aortic lumen to the lower right. There is a shelf-like protrusion into the lumen causing narrowing opposite the ductal insertion site.
5.10.4 Ectopia Cordis
In this rare malformation the heart lies outside the thoracic cavity. In the most common variety there is a defect of the sternum, pericardium and overlying skin, and the anteriorly displaced heart lies exposed to the external environment (Figure 5.41). There are usually associated cardiac and extracardiac defects. A less common variation is when the heart lies in the upper abdomen, usually associated with a defect of the lower sternum, the diaphragm, pericardium and upper abdominal wall with protrusion of both heart and abdominal contents onto the body surface. There are usually associated cardiac defects, most commonly VSD [38]. This combination of abnormalities is sometimes termed pentad (or pentalogy) of Cantrell.
Figure 5.41 Ectopia cordis. Termination of pregnancy at 14 weeks’ gestation for ectopia cordis. There is irregularity and pallor of the tissues above the umbilical cord that represents the ectopic location of the heart. The sternum is short and the diaphragm deficient anteriorly. The heart was elongated and distorted but showed normal vascular connections. Internally there was pulmonary stenosis and VSD.
5.10.5 Left Atrial Aneurysm
Aneurysm of left atrial appendage is rare and often an incidental finding in a patient undergoing echocardiography. It may predispose to atrial tachyarrhythmia and thromboembolism. About 40% of cases are congenital and the remainder acquired as a result of surgery, trauma, and mitral stenosis or regurgitation [39]. Presentation is usually in the third decade but may be as young as 2 years of age [40]. The example illustrated (Figure 5.42) is from a 2-year-old girl. There is focal or diffuse enlargement of the atrial appendage, sometimes to giant proportions. Surgical resection is the standard of treatment.
