AFTER cavopulmonary anastomosis, pulmonary arteriovenous malformations (PAVMs) may develop in nearly all pre-Fontan patients, but only about 20% are clinically important. 1They are thought to be the persistence of arteriovenous communications of the fetal and neonatal pulmonary circulation. It is speculated that the lack of hepatic venous blood flowing through the lungs and, hence, the absence of some stimulating or suppressive factor, may contribute to this condition. 2The PAVMs may lead to progressive desaturation (>5%) in the years after undergoing Glenn anastomosis. However, normal arterial oxygenation does not exclude the presence of persisting PAVMs. 1The diagnosis is made by the detection of a rapid appearance of contrast dye in the pulmonary veins after injection into the pulmonary arteries or by contrast echocardiography.

This is a report of successful administration of nitric oxide (NO) in a patient after Fontan repair with severe life-threatening hypoxemia due to preoperatively undetected PAVMs, thus avoiding extracorporeal membrane oxygenation (ECMO) support.

A 4-yr-old boy (body weight, 13 kg; height, 103 cm) was scheduled for a fenestrated extracardiac Fontan procedure. In the neonatal period, he had undergone a Damus-Kaye-Stansel operation with right-sided Blalock-Taussig (BT) shunt and coarctation repair because of a single ventricle with a subaortic chamber, restrictive bulboventricular foramen, transposition of the great arteries, hypoplastic aorta, and coarctation of the aorta. At age 8 months, the boy underwent bidirectional Glenn anastomosis. The preoperative angiogram revealed an unobstructed flow through the Glenn anastomosis and the pulmonary vascular tree, as well as a mean pulmonary pressure of 13 mmHg. The superior vena cava pressure was 14 mmHg, oxygen saturation 65%. Selective catheterization of the pulmonary veins was not performed. Arterial oxygen saturation (Sao2) in room air was 75%, blood pressure was 110/55 mmHg, and heart rate was 100 beats/min.

Anesthesia was induced and maintained as a total intravenous anesthetic with midazolam (total dosage, 13 mg) and sufentanil (375 μg); muscle relaxation was performed with pancuronium (5 mg). Prebypass Sao2was 80% with an Fio2of 0.5, central venous pressure (femoral vein) 10 mmHg, arterial blood pressure 100/50 mmHg. The operation took 4.5 h and was performed using moderate hypothermic extracorporeal circulation (bypass time, 113 min; esophagus temperature, 32°C). Following anastomosis of the inferior vena cava and pulmonary artery and fenestration of the right atrium, the surgeon inserted a left atrial indwelling catheter and pacing wires. At that time, the child was normothermic (37°C esophagus) and the hematocrit concentration was 32%. We were ready to stop the extracorporeal circulation (ECC) with inotropic support of 5 μg · kg−1· min−1dopamine, 10 μg · kg−1· min−1amrinone, and 5 μg · kg−1· min−1nitroglycerin. However, weaning from ECC failed because of severe hypoxemia (Sao2decreased to 30%), whereas hemodynamic parameters remained stable (arterial blood pressure, 120/60 mmHg; central venous pressure, 17 mmHg; left atrial pressure, 10 mmHg; transpulmonary pressure gradient, 7 mmHg). The transpulmonary pressure gradient did not change during the following events. Both lungs could easily be ventilated without signs of increased airway resistance or reduced lung compliance. Blood drawn from the left atrial catheter showed a Pao2of 30 mmHg. Since ventilation with 100% oxygen failed to improve oxygenation, the decision to use ECMO was made. While awaiting the equipment, we decided to start NO-inhalation at 25 ppm. The Sao2increased to 80–87% and, finally, 4 h after the first attempt, the child could be weaned from ECC without using ECMO.

In the intensive care unit, oxygenation continued to be highly dependent on NO inhalation. Accidental discontinuation resulted in severe hypoxemia (Sao2<50%). Selective angiography of the left pulmonary artery performed 3 days later revealed a pulmonary arteriovenous malformation of the left lower lobe (fig. 1). The rapid appearance of contrast dye in the pulmonary veins during the first angiography had been underestimated by the cardiologist. Balloon occlusion of the left lower lobe artery resulted in a marked increase in Sao2from 81 to 86% in radial artery blood and from 86 to 92% in left atrial blood. In contrast, occlusion of the fenestration (conduit to right atrium) only resulted in a slight increase of Sao2from 81 to 82%. During angiography, the inspired oxygen concentration still was 80% and NO was administered into the breathing circuit at a concentration of 25 ppm. It took 8 days to wean the patient from mechanical ventilation. Thereafter, NO inhalation was continued via  face mask until the tenth postoperative day. The boy was discharged from the intensive care unit with an Sao2between 86 and 92%.

Fig. 1. The catheter has been introduced through the vena cava inferior (IVC) into the left pulmonary artery (LPA) and advanced to the left lower lobe artery. After injection of contrast dye into the artery (arrow ), it appeared immediately in a pulmonary vein (PV) running back to the left atrium (LA).

Fig. 1. The catheter has been introduced through the vena cava inferior (IVC) into the left pulmonary artery (LPA) and advanced to the left lower lobe artery. After injection of contrast dye into the artery (arrow ), it appeared immediately in a pulmonary vein (PV) running back to the left atrium (LA).

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Because of the unpredictable development of PAVMs, there has been concern about the timing of the Fontan procedure in children after bidirectional Glenn anastomosis. PAVMs are likely to occur in the time period between early Glenn operation (in the first 6 months of life) and the final Fontan procedure. 3As the fenestrated extracardiac Fontan operation 4is favored by our pediatric surgeon, the children get their “final step” at the age of 4 yr or with a body weight of at least 15 kg. 5Then, the 20-mm extracardiac conduit can be placed easily by the surgeon. This size of conduit is preferred because it meets the patient's flow requirements later during adulthood, and therefore a reoperation is also unlikely.

Extracorporeal circulation may reduce lung compliance and increase intrapulmonary shunting, interstitial lung water, and pulmonary vascular resistance. 6In this case, however, a marked decrease of lung compliance or increase in airway pressure could not be observed. In addition, the transpulmonary gradient, as an indicator of a functioning Fontan circulation, was low (7 mmHg) and remained stable even in presence of severe hypoxemia, giving an erroneous impression of low pulmonary vascular resistance. The increased pulmonary resistance after extracorporeal circulation was masked by blood flow being predominantly directed through the PAVMs and bypassing gas exchange.

After reducing pulmonary vascular resistance by NO inhalation, blood flow was redistributed to the normal vascular bed, enabling adequate gas exchange. The shunt flow across the 4-mm fenestration as a possible cause of desaturation was excluded by balloon occlusion during angiography. After balloon occlusion of the fenestration Sao2changed only slightly from 81 to 82%.

Inhaled NO dilates pulmonary blood vessels in ventilated lung areas, thus facilitating gas exchange by improvement of perfusion in ventilated areas. Previous studies have shown that the reduction of pulmonary vascular resistance after cardiopulmonary bypass (CPB) by NO administration is even more prominent than before. Wessel et al.  7showed a twofold stronger decrease of pulmonary vascular resistance after CPB than before CPB. In a randomized trial, Russell et al.  8demonstrated that NO reduces the increased pulmonary artery pressure (>50% mean systemic arterial pressure) that developed after pediatric cardiopulmonary bypass.

The ECMO may be an ideal method to restore oxygenation, but it does not reverse the right-to-left shunt across the PAVMs and is associated with significant adverse side effects. 9Bacha et al.  9describe three patients with PAVMs after bidirectional cavopulmonary anastomosis. In one patient, they used ECMO and balloon occlusion, the second patient died after development of severe coagulopathy, which made balloon occlusion and ECMO impossible, and the third patient was treated with ECMO, but could not be weaned from mechanical support before NO inhalation over 14 days. Balloon occlusion of PAVMs is not always possible because of the diffuse nature of the malformations. In our case, a coil embolization of the malformation was postponed after the oxygenation had improved with NO because of our knowledge that these malformations usually resolve after Fontan procedure. In our patient, the collateral was indeed no longer detectable in angiography performed 3 months later.

The perioperative course of this case demonstrates that inhaled NO may be successful in the treatment of severe hypoxemia due to PAVMs after Fontan repair, and it may even avoid the use of ECMO and its associated adverse side effects, such as hemorrhage, neurologic injury, or infections.

Bernstein HS, Brook MM, Silverman NH, Bristow J: Development of pulmonary arteriovenous fistulae in children after cavopulmonary shunt. Circulation 1995; 92: II309–14
Justino H, Benson LN, Freedom RM: Development of unilateral pulmonary arteriovenous malformations due to unequal distribution of hepatic venous flow. Circulation 2001; 103: e39–43
Jonas RA: Indications and timing for the bidirectional Glenn shunt ver-sus the fenestrated Fontan circulation. J Thorac Cardiovasc Surg 1994; 108: 522–4
Lemler MS, Scott WA, Leonard SR, Stromberg D, Ramaciotti C: Fenestration improves clinical outcome of the Fontan procedure. Circulation 2002; 105: 207–16
Petrossian E, Reddy VM, McElhinney DB, Akkersdijk GP, Moore P, Parry AJ, Thompson LD, Hanley FL: Early results of the extracardiac conduit Fontan operation. J Thorac Cardiovasc Surg 1999; 117: 688–96
Gamillscheg A, Zobel G, Urlesberger B, Berger J, Dacar D, Stein JI, Rigler B, Metzler H, Beitzke A: Inhaled nitric oxide in patients with critical pulmonary perfusion after fontan-type procedures and bidirectional Glenn anastomosis. J Thorac Cardiovasc Surg 1997; 113: 435–42
Wessel DL: Inhaled nitric oxide for the treatment of pulmonary hypertension before and after cardiopulmonary bypass. Crit Care Med 1993; 21: S344–5
Russell IA, Zwass MS, Fineman JR, Balea M, Rouine-Rapp K, Brook M, Hanley FL, Silverman NH, Cahalan MK: The effects of inhaled nitric oxide on postoperative pulmonary hypertension in infants and children undergoing surgical repair of congenital heart disease. Anesth Analg 1998; 87: 46–51
Bacha EA, Jonas RA, Mayer JE Jr, Perry S, del Nido PJ: Management of pulmonary arteriovenous malformations after surgery for complex congenital heart disease. J Thorac Cardiovasc Surg 2000; 119: 175–6