Life-threatening hemoptysis following the Fontan procedure

Abstract

Two cases of life-threatening recurrent hemoptysis occurring 10 years after a Fontan operation are presented. Bleeding from aortopulmonary collateral vessels was responsible for this complication in both cases, and the importance of systematic selective angiography of all potential origins of such abnormal vessels, including those arising from the abdominal aorta, is highlighted. Although coil embolization of aortopulmonary collateral vessels is usually definitive, pulmonary lobectomy may be necessary. The present report demonstrates, for the first time, that rescue extracorporeal membrane oxygenation support can be used as a bridge to surgery in case of severe uncontrollable hemoptysis in such cases.

The Fontan procedure was first used in 1971 for the surgical management of tricuspid atresia, and it has become the definitive palliative surgical treatment for all forms of univentricular congenital heart disease. Hemoptysis is a rare and life-threatening complication attributed to the bleeding from aortopulmonary collateral vessels, which may occur several years after the Fontan procedure (1,2). We describe two patients who suffered from severe recurrent hemoptysis late after undergoing the Fontan procedure, and we also discuss the incidence, pathophysiology and management of this potentially fatal complication.

CASE PRESENTATIONS

Patient 1

A 19-year-old male patient with no history of a bleeding disorder presented with recurrent life-threatening hemoptysis. The patient’s history included tricuspid atresia for which he underwent a classic Fontan-type operation at the age of five years, with anastomosis of the right atrium to the pulmonary artery using the right atrial appendage. An atrial septal defect was left at that time, and his baseline oxygen saturation was 90%. He had a first episode of hemoptysis 10 years after the Fontan operation that was attributed to the presence of aortopulmonary collateral vessels arising from the right bronchial arteries and both internal mammary arteries, which were embolized with 14 microcoils (Tornado; Cook Medical, USA) and polyvinyl alcohol particles of 350 μm to 500 μm (Boston Scientific, France). Significant hemoptyses recurred approximately two years after the first episode, and embolization of additional aortopulmonary collateral vessels from the right intercostal arteries and the right thyrocervical trunk was successfully performed with 19 microcoils (Tornado; Cook Medical). Right catheterization showed a mean pulmonary arterial pressure of 9 mmHg, and pulmonary angiography ruled out the presence of any pulmonary arteriovenous malformation. Two months later, the patient was admitted for a third episode of life-threatening hemoptysis. An aortopulmonary vessel proximal to the previously occluded right internal mammary artery and a small left bronchial artery were embolized with 11 microcoils (Tornado; Cook Medical) and polyvinyl alcohol particles (Boston Scientific). Thirty-six hours later, the bleeding recurred, and embolization of an aortopulmonary collateral branch arising from the celiac artery toward the left inferior pulmonary lobe was performed with eight microcoils (Tornado; Cook Medical) and polyvinyl alcohol particles (Boston Scientific). However, on the following day, severe hemoptysis occurred again and required a third catheterization procedure, including selective injection of all vessels arising from the abdominal aorta. Collateral vessels from the inferior phrenic artery toward the left lower lobe were embolized (Figure 1). Abnormal ramifications from gastric and celiac arteries coursing through the diaphragm toward the left hilum were also embolized with 12 microcoils (Tornado; Cook Medical, and VortX Diamond; Boston Scientific, Ireland). During this procedure, hemoptysis persisted, leading to critical hypoxemia. Extracorporeal membrane oxygenation (ECMO) support had to be installed in the catheterization laboratory as a bridge to left inferior lobectomy. A pathological histology examination revealed intra-bronchial and intraparenchymal hemorrhage associated with markedly enlarged, tortuous and often dilated blood vessels in the submucosa of many bronchioles and small cartilaginous bronchi, some of which also showed small hemorrhagic ulcers (Figure 2). These abnormal vessels were interpreted as the source of the hemorrhage and were consistent with abnormal collateral vascularization of the bronchial arterial circulation. Following surgery, the patient had multiple complications, including inferior vena cava and left iliac vein thrombosis with pulmonary embolism, paradoxical embolism with splenic and renal infarcts, and pneumonia. After several weeks of rehabilitation, his oxygen saturation was 80% at rest and he was discharged home with oxygen. The patient did not have any neurological sequelae. A modification of his Fontan physiology with a lateral tunnel was performed six months after the last episode of hemoptysis, and no other recurrences had occurred after a follow-up of 12 months.

Figure 1.

A Collateral vessel (arrow) from inferior phrenic artery coursing to the left lower lobe. B Embolization of a collateral vessel (arrow) coursing from the inferior phrenic artery

Figure 2.

A Focal hemorrhagic bronchiolar ulceration with associated hemorrhage in the surrounding alveoli, including hemosiderin-laden macrophages (hematoxylin-eosin stain). B Markedly enlarged subepithelial arteriole (Verhoeff von Gieson stain)

Patient 2

A 16-year-old male patient with no history of a bleeding disorder was admitted because of recurrent hemoptysis. His medical history was significant for a double-inlet left ventricle, pulmonary valvular stenosis, atrial and ventricular septal defect, and levo-transposition of the great arteries. He underwent a Fontan-type operation at five years of age, with direct anastomosis of the superior vena cava to the right pulmonary artery, and a fenestrated lateral tunnel between the inferior vena cava and the pulmonary artery. His baseline oxygen saturation was 89%. Ten years after the Fontan procedure, the patient was admitted after three episodes of massive hemoptysis. He was rapidly intubated, and flexible bronchoscopy showed considerable bleeding from the left lower lobe. Pulmonary and aortic angiography were performed but failed to show any significant abnormal vessels. Right catheterization showed a mean pulmonary artery pressure of 8 mmHg, and pulmonary angiography ruled out the presence of any pulmonary arteriovenous malformation. Two days later, his oxygen saturation decreased again and right superior lobe opacity was noted on chest x-ray. He was taken again to the catheterization laboratory, where, by selective injection, multiple aortopulmonary collateral vessels were demonstrated to be coursing from the left and right internal mammary arteries and the right intercostal arteries. Successful embolization of all these aortopulmonary collateral vessels was performed with a total of 13 microcoils (Tornado; Cook Medical). Three days after this procedure, recurrent massive hemoptysis, arising again from the left lower lobe, required a third catheterization procedure, with embolization of two collateral branches from a left intercostal artery with seven microcoils (Tornado; Cook Medical). There was no recurrence after this last procedure, and the patient was discharged with an oxygen saturation of 90%. There were no other recurrences after a follow-up of 24 months.

DISCUSSION

The incidence of hemoptysis as a long-term complication following the Fontan operation is not known. These two cases of life-threatening hemoptysis occurring 10 years after the Fontan operation were selected from a total of 65 survivors of the procedure who are currently being followed at our institution, with a median follow-up time of 12 years (range six months to 25 years). The event rate was 3.1%, suggesting that the occurrence of this complication may be more frequent than previously thought, and that it can potentially increase, because the follow-up period for patients having undergone the Fontan procedures is extended.

In accordance with previous individual case reports (1,2), these two cases showed that hemoptysis after the Fontan procedure was secondary to the bleeding from aortopulmonary collateral vessels, and this was confirmed by lung pathology features in patient 1. Triedman et al (3) found a 30% prevalence of aortopulmonary vessels following the Fontan operation, most of them arising from the internal mammary arteries, the thyrocervical trunk and/or the intercostal arteries. The present study highlights the importance of performing selective and extensive injections of all these arteries in case of hemoptysis to find and embolize all abnormal aortopulmonary vessels, even those not directly involved in an active hemoptysic episode, and avoid potentially fatal recurrences. Furthermore, the case of patient 1 demonstrates that these abnormal vessels can also arise from the abdominal aorta, suggesting the need for a systematic exploration of this vascular territory even if other potential sources of pulmonary bleeding have been detected in the thoracic aorta. While the presence of aortopulmonary collateral vessels has been associated with a higher complication rate (pleural effusion, cardiac failure) during the Fontan operation (4), the clinical impact of these vessels in the mid-and long-term prognosis of such patients is not well-known. Considering the life-threatening nature of hemoptyses secondary to aortopulmonary collateral vessels, it is reasonable to implement systematic research and preventive occlusion of such vessels in all patients undergoing the Fontan procedure, especially in view of the low risk associated with the vessel coil embolization procedure. However, the potential advantages and cost-effectiveness of such a strategy should be determined by appropriately designed prospective studies. Moreover, the risk associated with the radiation used in these procedures has to be taken into account. Thus, the cumulative radiation doses were 34.955 cGy/cm² and 15.330 cGy/cm² for patients 1 and 2, respectively, and radiation has been associated with an increased risk of developing neoplastic diseases at follow-up (5). To minimize this risk, the use of magnetic resonance imaging or high-resolution multidetector computed tomographic scanning before catheterization should be considered in such cases to define the number and location of aortopulmonary collateral vessels (6). Unfortunately, the unavailability of these imaging modalities in our centre at the time, where the patients were admitted, and the urgency of treating such life-threatening hemoptysis episodes precluded the performance of any imaging exploration before catheterization in both cases. The precise causes of aortopulmonary collateral vessels following the Fontan procedure are not known. A decreased volume, velocity and pulsatility of flow in the pulmonary arteries have been suggested as potential stimuli. In addition, a history of one or more Blalock-Taussig shunt procedures has also been associated with the presence of collateral vessels (3). Moreover, chronic hypoxemia has also been suggested as an important stimulus for the persistence and growth of aortopulmonary collateral vessels. The present two cases had a persistent right-to-left atrial shunt, with oxygen saturation lower than 91% in both cases, and one may wonder whether improving chronic hypoxemia by surgical or percutaneous closure of such atrial shunts would have prevented pulmonary bleeding.

Finally, hemoptysis occurring after the Fontan procedure is a potentially lethal complication, with challenging management. The case of patient 1 demonstrates, for the first time, that rescue ECMO support can be a life-saving measure as a bridge to pulmonary lobectomy in Fontan circulation patients who have severe and inexhaustible pulmonary bleeding. ECMO had been previously used as support during the perioperative period in patients with Fontan circulation (7). The present study extends its use to patients with severe pulmonary bleeding complications.