Case report

An asymptomatic 8-year-old boy was referred to our unit for assessment of left atrial and ventricular enlargement. He had been diagnosed in the neonatal period with usual atrial arrangement but right-sided heart, and had a small muscular ventricular septal defect which subsequently closed spontaneously. When first seen, his weight and height were at the 25th centile, and the vital signs where normal, with a blood pressure of 79 over 47 millilitres of mercury. There was a right precordial bulge, normal heart sounds, and a continuous murmur over the left infraclavicular area graded at 2 out of 6. The scalar electrocardiogram revealed a wandering atrial pacemaker, the tracings were compatible with a right-sided heart. The chest radiograph confirmed that the heart was right-sided, and showed a small left lung with increased vascular markings. The echocardiogram revealed a left aortic arch, left atrial and ventricular enlargement, with end-diastolic dimensions of 3.1 and 5.7 centimetres, respectively. The left ventricular ejection fraction was 83 percent, while the right ventricular end-diastolic dimension was normal. No septal defects or arterial duct were seen. The child underwent computed tomographic angiography and cardiac catheterization (Figs 1 and 2). The studies confirmed usual arrangement of the organs, with a right-sided liver, left-sided stomach, and a single spleen. The main part of the heart was positioned in the right thorax, with its apex directed to the right. This abnormal cardiac position was associated with neither hypoplasia of the right lung, nor hyperinflation of the left lung. We diagnosed a primary positional abnormality of the heart. There were bilateral superior caval veins without a bridging vein. Otherwise, the heart showed normal segmental connections and no intracardiac malformations. The volume of the left lung was smaller than that of the right, and the left diaphragm was elevated. The left pulmonary artery measured 8 by 7 millimetres, while the right pulmonary artery measured 13 by 13 millimetres. The left pulmonary artery supplied the central two-thirds of the left lung. The peripheral part of the left lung was supplied from multiple arterial branches arising from an internal thoracic artery, a large branch from the dilated left subclavian artery that coursed along the lateral thoracic wall, and two aberrant arterial branches arising from the coeliac trunk and the abdominal aorta immediately above the origin of the coeliac trunk. These branches traversed the pleural envelop along the chest wall and diaphragm to the left lung. There were no identifiable intraparenchymal communications between the intrapericardial pulmonary arterial supply and the systemic arterial branches. Computed tomographic images showed a stripe of watershed zone between the central zone supplied by the left pulmonary arterial branches, and the peripheral zone supplied by the systemic arterial branches. Both zones were drained to the left atrium by the same unobstructed pulmonary venous channels, which crossed the watershed zone. There was normal aeration without evidence of sequestration from the tracheobronchial tree, or cystic or solid masses. Radioisotopic perfusion and ventilation scans demonstrated ventilation-perfusion mismatch of the peripheral zone of the lung, with uptake on ventilation but no uptake on perfusion scanning.

Figure 1. A left pulmonary arteriogram obtained in the late arterial and capillary phase (a) shows the left pulmonary arterial branches supplying the central left lung. The peripheral rim of the left lung is not opacified. The left subclavian arteriogram (b) shows a markedly dilated left subclavian artery (LSA) that gives rise to the dilated left internal mammary artery (LIMA) and a large unnamed artery (asterisks) along the inner surface of the bony lateral thoracic wall. Both branches give rise to numerous branches to the peripheral zone of the left lung that was not opacified by left pulmonary arteriography. Multiple pulmonary veins (v) drain both the peripheral and central zones of the left lung. An abdominal aortogram (c) demonstrates two aberrant arteries from the aorta (Ao) supplying the basal part of the basal segments of the left lower lobe. There were no obvious communicating channels between the pulmonary and systemic arterial branches.

Figure 2. Reformatted computerized tomographic images in oblique coronal (a) and axial (b) planes show distinct differences in vascularity between the intrapericardial pulmonary arterial and the peripheral systemic arterial zones. The pulmonary arterial branches barely reach the peripheral zone, forming a sort of water-shed. Dilated pulmonary veins (v) traverse this water-shed zone draining both peripheral and central zones of the left lung.

Discussion

Pulmonary sequestration is defined as a developmental anomaly in which a mass of nonfunctioning pulmonary tissue lacks a normal connection with the tracheobronchial tree and receives an aberrant systemic arterial blood supply.^{1, 2} In our case, the aberrant systemic arteries supplied pulmonary tissue that was not isolated, an entity which has been called anomalous systemic arterial supply to normal lung, or sequestration from the pulmonary arterial connection without tracheobronchial disconnection.^3–5 This can occur as an isolated anomaly, with the arterial supply usually connecting to the basal segments of the left lung.

In patients with tetralogy of Fallot and pulmonary atresia, with major aortopulmonary collateral arteries, or the aberrant systemic arterial branches to the lungs with or without sequestration, the systemic arteries enter the lung through the pulmonary hilum and its inferior extension, which is called the inferior pulmonary ligament.^6–8 The inferior pulmonary ligament is considered to be a remnant of the developmental pathway through which the lungs had had splanchnic blood supply in the embryonic period.⁸ On the other hand, it is speculated that the systemic arterial branches connecting to the lungs are due to abnormal persistence of the splanchnic blood supply.⁹ It is very natural, therefore, for the abnormal systemic arteries of congenital origin to enter the lungs along their regular pathways, namely the pulmonary hilums and inferior pulmonary ligaments. It is also suggested that the diseased lung tissue may acquire parasitic arterial supply through the same routes, explaining the acquired etiology of at least some of the cases with intralobar type of pulmonary sequestration.^{6, 7} In contrast to the naturally occurring routes, transpleural systemic arterial supply to the lungs has been regarded as acquiring its routes through the adherent pleura that is damaged by prior surgical procedure or infection.^{6, 7, 10} The transpleural routes of systemic arterial supply to the lungs in our case, however, are most likely congenital in origin, because there are no signs of previous pleural infection or history of thoracotomy.

Our case, therefore, shows an unreported form of anomalous systemic arterial supply, in which the supply is to the peripheral parts of the whole left lung instead of showing a segmental or lobar distribution. Also unique to our case was a watershed zone between the lung tissue supplied by the intrapericardial pulmonary circulation and the systemic arterial branches. Additionally, to the best of our knowledge, the association with a right-sided heart has not been previously described.^3–5

During embryonic development, the lung receives a dual blood supply from the aorta consisting of bronchial and splanchnic vessels.⁹ In our case, there was no dual supply, and both systems shared the same venous return. The child underwent successful embolization of the anomalous vessels without producing pulmonary infarction, suggesting the presence of additional nutrient sources of arterial flow.

Acknowledgement

Robert M. Freedom made critical comments on this paper, but sadly passed away before the manuscript was completed. We thank him for his life dedicated to teaching, and for his constant encouragement.