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Ann Thorac Surg 1997;63:960-963
© 1997 The Society of Thoracic Surgeons

Original Article: Cardiovascular

Pulmonary AV Malformations After Superior Cavopulmonary Connection: Resolution After Inclusion of Hepatic Veins in the Pulmonary Circulation

Maully J. Shah, MBBS, Jack Rychik, MD, Mark A. Fogel, MD, John D. Murphy, MD, Marshall L. Jacobs, MD

Divisions of Cardiology and Cardiothoracic Surgery, The Children's Hospital of Philadelphia, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania

Accepted for publication August 24, 1996.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
 Comment
 Acknowledgments
 References
 
Background. A high incidence of pulmonary arteriovenous malformations (PAVMs) has been reported in patients who have polysplenia and congenital heart disease after superior cavopulmonary anastomosis. Interruption of hepatic venous return to the pulmonary circulation is believed to potentiate the development of PAVMs. Surgical inclusion of hepatic flow in the pulmonary circulation may result in their resolution.

Methods. We reviewed 3 patients with congenital heart disease and polysplenia in whom PAVMs developed and who had subsequent hepatic vein inclusion in the pulmonary circulation.

Results. Patients underwent superior cavopulmonary connection at a median age of 8 months. The PAVMs were diagnosed at a median duration of 8 months after operation (arterial saturation <75% in room air). Hepatic venous flow was included in the pulmonary circulation at operation. Resolution of PAVMs occurred at a median duration of 7 months after operation (arterial saturation >90% in room air).

Conclusions. Surgical inclusion of hepatic venous blood in the pulmonary circulation results in the resolution of PAVMs. Electively associating the hepatic veins with the pulmonary vasculature may prevent the development of PAVMs in patients who are at risk.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
 Comment
 Acknowledgments
 References
 
The surgical connection of the superior vena cava to the right pulmonary artery as described by Glenn [1] was initially considered a satisfactory means of palliation for various forms of cyanotic congenital heart disease. Substantial morbidity and mortality from the late onset of pulmonary arteriovenous malformations (PAVMs), however, contributed to the abandonment of this procedure [2]. Recently, interest in various other forms of superior cavopulmonary artery connections (bidirectional Glenn, hemi-Fontan procedures) has increased for palliation of single-ventricle anomalies in the first year of life [3]. Although physiologically similar to the classic Glenn operation, current techniques of superior cavopulmonary artery connection have not been shown to cause PAVMs as a common complication [4]. One reason may be that it is usually performed as part of a two-stage approach, with most patients proceeding relatively quickly to incorporation of inferior vena caval flow and hepatic venous flow into the pulmonary circulation, and hence completion of the Fontan operation.

For editorial comment, see page 930.

An exception to this two-stage strategy for total cavopulmonary incorporation is in children with polysplenia syndrome and interruption of the inferior vena cava when there is azygos continuation to the superior vena cava, and in which the hepatic veins drain directly into the atrium. Superior cavopulmonary connection alone in these patients incorporates most of the systemic venous return into the pulmonary circulation, excluding coronary sinus and hepatic venous flow [5]. This typically results in arterial oxygen saturations in the range of 85% to 90% and is believed to obviate the need for further operation. However, a high incidence of PAVMs (21%) has been reported recently in patients with polysplenia who have had superior cavopulmonary anastomosis alone as their final procedure [6].

It has been suggested that patients may be predisposed to the development of PAVMs when hepatic venous return is diverted away from the pulmonary circulation. If this is so, then operative redirection and inclusion of hepatic venous blood in the pulmonary circulation may influence the presence of PAVMs [7]. We report our experience with 3 children with polysplenia and congenital heart disease in whom PAVMs developed and in whom surgical inclusion of hepatic venous blood in the pulmonary circulation has successfully resolved PAVMs and eliminated cyanosis.


   Material and Methods
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 Footnotes
 Abstract
 Introduction
 Material and Methods
Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
 Comment
 Acknowledgments
 References
 
Patients
Between 1990 and 1995, 400 patients less than 2 years of age underwent the hemi-Fontan operation for various forms of single-ventricle anomaly at The Children's Hospital of Philadelphia. Of these, 19 (4.8%) had heterotaxia syndrome, 3 of whom had polysplenia with interruption of the inferior vena cava with azygos continuation to the superior vena cava; these 3 were diagnosed with PAVMs after hemi-Fontan (Table 1Go). Two patients had single ventricle of the dominant right ventricular type, and one had dominant left ventricular type. All 3 had blood flow to the pulmonary vasculature before the hemi-Fontan procedure delivered by a 3- to 4-mm tube graft interposed between the right innominate artery and the right pulmonary artery. One patient had biliary atresia treated with a Kasai portoenterostomy procedure at 3 weeks of age. Hemodynamic indices and angiography results at cardiac catheterization before creation of the hemi-Fontan were not indicative of PAVMs.


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  		Table 1. . Patient Characteristics
 
Patients underwent a hemi-Fontan procedure at a median age of 8 months (range, 6 to 9 months). The hemi-Fontan [3] consisted of a side to side anastomosis of the superior vena cava with the branch pulmonary arteries, occlusion of inflow of the superior vena cava into the right atrium, and augmentation of the confluence of the branch pulmonary arteries. Two patients also had connection of a left superior vena cava to the left pulmonary artery. Patients 2 and 3 had transient pleural effusions after the hemi-Fontan procedure, which were successfully drained by pleurocentesis. Median hospitalization after the hemi-Fontan procedure was 9 days (range, 7 to 42 days). Progressive cyanosis was noted at a median duration of 8 months (range, 7 to 27 months) after the hemi-Fontan operation. Diagnostic cardiac catheterization was performed at a median duration of 13 months (range, 8 to 36 months) after the hemi-Fontan.


   Diagnosis of Pulmonary Arteriovenous Malformation
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Diagnosis of Pulmonary...
Method of Hepatic Vein...
 Results
 Comment
 Acknowledgments
 References
 
We diagnosed PAVMs if the following criteria were present: (1) detection of progressive resting systemic desaturation by pulse oximetry, without evidence of parenchymal lung disease on chest roentgenogram; (2) room-air aortic saturation on cardiac catheterization of 75% or less; and (3) pulmonary angiography results showing the appearance of dilated distal pulmonary arteries and a classic reticular pattern [6, 8], in addition to rapid pulmonary arterial-to-venous transit time (early visualization of contrast in the pulmonary veins and left atrium while predominance of contrast is still present in the pulmonary artery, implying bypass of the capillary system (Fig 1Go). We considered PAVMs to be resolved when, on cardiac catheterization, aortic saturation was greater than 90% in room air and when a normal pulmonary arterial to venous transit time was noted on pulmonary angiogram (Fig 2Go). In the 1 patient who has not yet undergone cardiac catheterization after hepatic vein inclusion, saturation by pulse oximetry in room air was considered.



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  		Fig 1. . Pulmonary arteriogram of pulmonary arteriovenous malformation after cavopulmonary anastomosis. An injection through a catheter placed in the superior vena cava–right pulmonary artery (RPA) junction shows simultaneous visualization of contrast in the right pulmonary artery as well as the pulmonary veins. There is a diffuse reticular pattern of the vasculature and an absent capillary phase. Selective left pulmonary arteriogram showed a similar appearance in the left lung. (AZG.V = azygos vein; RPV = right pulmonary veins.)

 


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  		Fig 2. . Pulmonary arteriogram after surgical inclusion of hepatic venous blood in the pulmonary circulation. Catheter placed through the azygos vein into the superior vena cava–right pulmonary artery (RPA)–right atrial confluence shows normal pulmonary architecture and absence of diffuse reticular pattern. (HEP.V = hepatic veins; LPA = left pulmonary artery.)

 

   Method of Hepatic Vein Inclusion in the Pulmonary Circulation
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 Footnotes
 Abstract
 Introduction
 Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
Results
 Comment
 Acknowledgments
 References
 
A third-stage operation was undertaken in each of the 3 patients (median age, 23 months; range, 16 to 55 months) to associate the hepatic venous effluent with the pulmonary circulation. Using cardiopulmonary bypass and deep hypothermia with circulatory arrest, we widely excised the homograft patch that had been used to occlude the inflow of the right superior vena cava into the right atrium, creating a patulous communication between the right atrium and the operatively created confluence of the superior vena cava with the branch pulmonary arteries. In 2 cases, association of the hepatic veins with the pulmonary arteries and superior vena cava was accomplished by a "lateral tunnel" technique. A 10-mm segment of polytetrafluoroethylene graft was split longitudinally and then tailored to create the medial portion of the lateral tunnel. Inferiorly, the graft was sewn around the opening of the hepatic veins into the right atrium and then along the floor of the right atrium lateral to the intraatrial communication. Superiorly, the graft was sewn around the opening of the right atrium into the superior vena cava and branch pulmonary arteries. The anterior edge of the polytetrafluoroethylene graft was incorporated into the closure of the atriotomy incision, thus creating a lateral tunnel consisting medially of polytetrafluoroethylene and laterally of right atrial wall. In the other patient (patient 3), connection of the hepatic veins to the confluence of the superior vena cava and pulmonary arteries was accomplished in a different fashion. Because of the presence of anomalous pulmonary venous connection, the lateral atrial tunnel technique was not used, to minimize the likelihood of pulmonary venous obstruction. Instead, a 10-mm polytetrafluoroethylene graft was cut to the appropriate length and interposed between the opening of the hepatic veins into the lowest part of the right atrium inferiorly, and the opening of the atrium into the right superior vena cava and the confluence of the pulmonary arteries superiorly. Three small fenestrations were created in the wall of the graft in 2 patients (2.7 mm in patient 3, and 14-gauge needle fenestrations in patient 2).


   Results
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 Abstract
 Introduction
 Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
Comment
 Acknowledgments
 References
 
All 3 patients successfully underwent the hepatic vein inclusion operation without complication. Hospitalization after operation ranged from 6 to 14 days (median, 7 days). No patient had substantial pleural or pericardial effusion after the procedure. Oxygen saturation values by pulse oximetry 7 to 10 days after operation ranged from 80% to 84%. Cardiac catheterization was performed at 4 months and at 7 months after operation in 2 patients. Pulse oximetry saturation in patient 2 was obtained at 12 months postoperatively. In all, room-air saturation increased to greater than 92% and hemoglobin levels decreased to less than 13.5 g/dL (Table 2Go). In 2 patients, angiography in the systemic venous baffle revealed resolution of PAVMs, with patency of one fenestration in patient 3. Pulmonary arterial transit time appeared normal in both; however, subtle dilatation in the peripheral arterial vasculature was still present in patient 3.


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  		Table 2. . Hemodynamic and Laboratory Data Before and After Hepatic Venous Blood Inclusion in the Pulmonary Circulation
 

   Comment
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 Footnotes
 Abstract
 Introduction
 Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
 Comment
Acknowledgments
 References
 
The etiology of PAVMs is unknown and treatment options are limited, with most patients dying of progressive hypoxemia. On the basis of experience with the Glenn procedure, low-velocity, nonpulsatile flow was initially implicated as the cause of PAVMs [9]. This hypothesis is unsatisfactory because similar flow dynamics are present after the Fontan operation, yet PAVMs are not seen often after this procedure. Furthermore, Srivastava and colleagues [6] have reported 2 patients with congenital heart disease and biliary atresia in whom PAVMs developed despite having pulsatile blood flow to the lungs. Based on the high incidence of PAVMs in patients with polysplenia who have had superior cavopulmonary connection alone as their final palliation, the absence of hepatic venous blood reaching the lung vasculature has been implicated as a cause of PAVMs in congenital heart disease [6]. In support of this theory, PAVMs have been identified in patients with liver disease, and resolution has been reported after successful orthotopic liver transplantation [10]. We have further demonstrated the role of the liver in the development of PAVMs by our report of the disappearance of PAVMs after channeling of hepatic venous blood into the pulmonary vasculature at operation. It is plausible to hypothesize the existence of a biochemical agent produced by the liver that mitigates against the development of PAVMs. The absence of this hepatic agent in the pulmonary vasculature-by virtue of either poor hepatic synthetic function or poor delivery to the target organ (lung) secondary to anomalous hepatic venous drainage-results in the development of PAVMs. This is exemplified by patient 2 in our series, who had both poor synthetic function and anomalous hepatic venous drainage. Despite a successful Kasai procedure, PAVMs developed after superior cavopulmonary connection, which then resolved after normal hepatic venous blood was channeled to the lungs.

Surgical treatment of PAVMs and embolization therapy have been reported successful for isolated PAVMs, but effective therapy can be elusive in diffuse disease [11, 12]. In this report, we have demonstrated the reversibility of diffuse bilateral PAVMs by operative redirection of hepatic venous blood flow to the pulmonary vasculature. The median duration of follow-up of our patients since the documented disappearance of PAVMs is 6 months, with the longest follow-up being 2 years. Still uncertain is whether the reversal of PAVMs after surgical redirection of hepatic venous blood flow is a transient or permanent phenomenon. The time course for development of PAVMs after superior cavopulmonary connection in patients with polysplenia can be strikingly rapid. This suggests that association of the hepatic venous blood with the pulmonary circulation may be appropriate in all such patients. Such a strategy may prevent the development of PAVMs in patients with congenital heart disease who are at risk.


   Acknowledgments
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 Footnotes
 Abstract
 Introduction
 Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
 Comment
 Acknowledgments
References
 
We acknowledge Dr William I. Norwood, Jr, for the operative management of one of the patients presented in this article.


   Footnotes
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 Footnotes
Abstract
 Introduction
 Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Rychik, Division of Cardiology, The Children's Hospital of Philadelphia, 34th and Civic Center Blvd, Philadelphia, PA 19104.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Diagnosis of Pulmonary...
 Method of Hepatic Vein...
 Results
 Comment
 Acknowledgments
 References
 

  1. Glenn WW. Circulatory bypass of the right side of the heart. IV: Shunt between superior vena cava and distal right pulmonary artery-report of clinical application. N Engl J Med 1958;258:117–20.
  2. McFaul RC, Tajik AJ, Mair DD, Danielson GK, Seward JB. Development of pulmonary arteriovenous shunts after superior vena cava-pulmonary artery (Glenn) anastomosis. Circulation 1977;55:212–6.[Abstract/Free Full Text]
  3. Jacobs ML, Norwood WI Jr. Fontan operation: influence of modifications on morbidity and mortality. Ann Thorac Surg 1994;58:945–52.[Abstract]
  4. Lamberti JJ, Spicer RL, Waldman JD, et al. The bidirectional cavopulmonary shunt. J Thorac Cardiovasc Surg 1990;100:22–30.[Abstract]
  5. Kawashima Y, Kitamaru S, Matsuda H, Shimazaki Y, Nakano S, Hirose H. Total cavopulmonary shunt operation in complex cardiac anomalies: a new operation. J Thorac Cardiovasc Surg 1984;87:74–81.[Abstract]
  6. Srivastava D, Preminger T, Lock JE, et al. Hepatic venous blood and the development of pulmonary arteriovenous malformation in congenital heart disease. Circulation 1995;92:1217–22.[Abstract/Free Full Text]
  7. Knight WB, Mee RBB. A cure for pulmonary arteriovenous fistulas? Ann Thorac Surg 1995;59:999–1001.[Abstract/Free Full Text]
  8. Sherlock S. Disorders of the liver and biliary system. 8th ed. Oxford: Blackwell Scientific Publications, 1989:82–5.
  9. Kobayashi J, Matsuda H, Nakano S, et al. Hemodynamic effects of bidirectional cavopulmonary shunt with pulsatile pulmonary flow. Circulation 1991;84(Suppl 3):219–25.
  10. Laberge JM, Brandt ML, Lebeque P, et al. Reversal of cirrhosis related pulmonary shunting in two children by orthotopic liver transplantation. Transplantation 1992;53:1135–8.[Medline]
  11. Van Den Bogaert-Van Heesvelde AM, Derom F, Kunner M, Van Egmond H, Devlon-Blancquert A. Surgery for arteriovenous fistulas and dilated vessels in the right lung after the Glenn procedure. J Thorac Cardiovasc Surg 1978;76:195–7.[Abstract]
  12. Terry PB, Bearth KH, Kaufman SL, White RI. Balloon embolization for treatment of pulmonary arteriovenous fistulas. N Engl J Med 1980;302:1189–90.[Medline]

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