Case report

A female neonate diagnosed prenatally with hypoplasia of the left heart was delivered at 39 weeks of gestation to a 19-year-old mother. Prenatal echocardiography had indicated moderate aortic and mitral stenosis, with patency of the oval foramen and suboptimal visualization of the pulmonary veins. The infant was in severe respiratory distress, and became severely cyanosed shortly after birth. She was pale, with prolonged capillary refill, and no palpable peripheral pulses. The heart rate was between 70 and 80 beats/min, and the blood pressure was 30/10 mmHg. There was a faint systolic cardiac murmur. The initial arterial blood gas revealed a pH of 6.91, with a pressure of oxygen equal to 22 mmHg, and a pressure of carbon dioxide equal to 116 mmHg.

Echocardiography showed a hypoplastic left ventricle with very poor right ventricular function. There was a thick interatrial septum, and a triangular area in the left atrium with a questionable reversal of flow of blood away from the chamber (Fig. 1a). The pulmonary veins appeared to be normally connected. Instead of the anticipated left-to-right flow across the atrial septum, a small right-to-left shunt was identified (Fig. 1b). There was retrograde filling of the ascending aorta, and a large patent arterial duct. A chest radiograph showed a reticulated cystic appearance of both lungs (Fig. 2a). The baby deteriorated rapidly despite inotropic and ventilatory support and died four hours after birth.

Figure 1. The cross-sectional echocardiogram with Doppler colour flow mapping shows (a) a triangular area with reversal of flow (blue) relative to both atriums (red) that protrudes into the left atrium, and (b) flow into the right atrium and ventricle (red), with right-to-left shunting across a patent oval foramen into the left atrium (blue, multicolored). The gross photograph of left atrium (c) shows a conical pulmonary venous chamber with a sclerotic endocardium and muscular wall (*) that protrudes into the remainder of the left atrium. The probe is seen entering the left atrium from the right through the patent oval foramen.

Figure 2. The chest roentgenogram (a) shows bilateral pulmonary cystic change in a reticulated pattern. The gross photograph of posterior mediastinum (b) shows numerous small dilated veins (arrow) extending from the lung surface to the esophagus (E) and diaphragm (D). Note the subpleural lymphedema and congestion (*). Photomicrography of the lungs (c) original magnification (40×) shows a bronchovascular bundle with a prominent congested vein (V) in addition to a pulmonary artery (A) and an airway with cartilage (*).

Postmortem examination confirmed the presence of hypoplastic left heart syndrome, with stenotic mitral and aortic valves, an atretic aorta with preductal coarctation, and a patent arterial duct. The systemic veins and coronary sinus drained normally into the right atrium. The left atrium was subdivided into a small pulmonary venous chamber, and a larger component supporting the vestibule of the mitral valve. Four pulmonary veins of normal size connected with the venous part of the chamber. The larger component received a widely patent foramen ovale, supported a typical left atrial appendage, and exited through the stenotic mitral valve. The pulmonary venous chamber protruded into the lumen of the remainder of the left atrium, ending in a blind pouch that impinged upon the oval foramen (Fig. 1c). Internally, it was trabeculated and lined by densely sclerotic endocardium. Separating the two parts of the divided left atrium was a diaphragm of 1–2 mm thickness that was composed of cardiac muscle continuous with the rest of the atrial musculature. Careful examination failed to demonstrate any communication of the pulmonary venous chamber with the remainder of the left atrium, the right atrium, or the coronary sinus.

The lungs had severe subpleural lymphedema and vascular congestion. While no major anomalous pulmonary venous connection was present, numerous small blood vessels arose directly from the postero-inferior pleural surface of both lungs, forming anastomoses with the systemic veins around the esophagus and diaphragm (Fig. 2b). Microscopically, the lungs showed arterialization of pulmonary veins and severe lymphangiectasia.² Another notable finding was the presence of prominent veins in many of the bronchovascular bundles (Fig. 2c).

Discussion

Severe respiratory distress with cyanosis in the first few hours of life is typical of patients presenting with hypoplastic left heart syndrome complicated by pulmonary venous obstruction, as is the chest roentgenogram with a ground glass reticulated pattern.⁴ An unexpected echocardiographic finding in our patient was the right-to-left shunting across the oval foramen. This is the opposite of what is expected in the “usual” variants of hypoplastic left heart syndrome, and reflects the low pressure in the left atrium due to absence of any inflow from the pulmonary veins. The pouch formed by the pulmonary venous chamber was visualized as a triangular area in the vicinity of the left atrium. The morphology of our case illustrates the differences between two rare anomalies that are related to the embryology of a primitive structure – the common pulmonary vein. It is canalization of a midpharyngeal strand that establishes this connection between the venous plexus of the lungs and the heart, with subsequent incorporation into the left atrium. If it becomes atretic, the pulmonary venous confluence is either not connected to the heart at all, or is connected by a rudimentary strand of tissue.^{4, 5} On the other hand, if a well-developed common pulmonary vein fails to incorporate fully into the left atrium, it creates an accessory venous chamber attached to the heart, such as the one seen in this patient. This creates the commonest type of divided left atrium.

Our present case is a highly unusual variant that expands the morphological and clinical spectrum of this class of malformations.⁶ There are only a few reported cases describing the coexistence of a divided left atrium with hypoplasia of the left heart.^{6, 7} A divided left atrium with an imperforate diaphragm has also been documented,⁸ but as far as we are aware, there is only one previous case that occurred along with hypoplastic left heart syndrome.⁹ In that case, there was a major anomalous pulmonary vein draining into the inferior caval vein. In contrast, our case had complete obstruction to the pulmonary venous inflow, with no major anomalous connection, creating a clinical picture very similar to atresia of the common pulmonary vein.

In the absence of a major anomalous pulmonary venous connection to the heart, the lungs relied on numerous alternate routes to achieve vascular drainage. These included recruitment of lymphatics, bronchial veins, and numerous minute collateral channels to the systemic veins around the esophagus and diaphragm. These were apparently sufficient to support the limited pulmonary circulation of fetal life, but failed to cope with the increased blood flow after birth. Microscopically, it is important to distinguish the dilated veins in the bronchovascular bundles noted in this case from the “misaligned veins” seen in the syndrome of “alveolar capillary dysplasia with misaligned veins”.¹⁰ In that condition, the pulmonary veins are aberrantly located in the bronchovascular bundles, rather than occupying their normal locations in the interlobular septums. Our case had normally situated pulmonary veins, and the additional veins in the bronchovascular bundles were most likely part of the bronchial venous system. We also did not see the other histological changes comprising the “alveolar capillary dysplasia” that is part of that entity.¹⁰

Echocardiographic identification of anomalous or obstructed pulmonary venous return³ is an important part of the assessment of patients with hypoplasia of the left heart, because this requires correction before proceeding to staged reconstruction. This case, to the best of our knowledge is unique, with its remarkable fetal echocardiographic findings, establishes an important variant among the different forms of pulmonary venous obstruction, and one that will certainly contribute to poor outcome.

Acknowledgements

We thank Dr David Solowiejczyk for his assistance with the interpretation of the echocardiographic images, and Dr Claire Langston, Texas Children’s Hospital, Houston, Texas, for her assistance with interpretation of pulmonary histology.