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Ann Thorac Surg 1997;63:930-932
© 1997 The Society of Thoracic Surgeons

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Editorial

Cavopulmonary Shunt and Pulmonary Arteriovenous Malformations

National Cardiovascular Center, Osaka, Japan

Pulmonary arteriovenous malformation (PAVM) after Glenn operation initially was considered a consequence of excessive perfusion of the lower lobe. However, after the Fontan as well as the Kreutzer operation, both of which bypass the right ventricle as well, this catastrophic sequela was seldom reported. Although right atrial contraction as a pumping force of blood into the pulmonary circulation had been negated experimentally [1], the presence of pulsation in the pulmonary artery after the Fontan-type operation had been considered the difference between the Glenn operation and the Fontan operation with respect to PAVM development.

The total cavopulmonary shunt (TCPS) operation [2], which my colleagues and I developed and used clinically since 1978 for polysplenic patients with interrupted inferior vena cava and azygos or hemiazygos continuation, brought us excellent early postoperative results as this operation had as one advantage the elimination of any complicated intraatrial procedure to separate the complex systemic and pulmonary venous returns. Soon, however, postoperative development of PAVM was reported as seen after the Glenn operation.

See also page 960.

As the TCPS operation bypasses not only the right ventricle but also the right atrium, there is no pulsation in the pulmonary artery. Therefore, the absence of pulsation in the pulmonary artery was considered one of the reasons for the difference from the Fontan operation. Alternatively, the absence of some putative substance that is found in the hepatic venous blood, and that prohibits the development of PAVM, in the pulmonary artery in patients who underwent the TCPS operation was also speculated as an important reason for the development of PAVM.

De Leval and associates [3] advocated the advantage of a total cavopulmonary connection operation, wherein the inferior vena cava is connected to the pulmonary artery with a composite channel or a prosthetic tube excluding most or all of the right atrium. In principle, this is an advancement of the TCPS operation and has been widely accepted. It is, in fact, now the standard procedure employed in the Fontan-type operation. However, reports of PAVM in patients undergoing the total cavopulmonary connection operation have been quite scarce in spite of the lack of pulsation in the pulmonary artery.

The "pulsation theory" thus lost its grounds for contention as the cause of PAVM, with most investigators coming to consider the absence of some physiologic compound contained in the healthy hepatic venous blood as the pathway for the development of PAVM.

Srivastava and colleagues [4] presented an excellent article in 1995 dealing with PAVM in congenital heart disease in relation to hepatic venous blood. They reviewed the histories of 10 patients with congenital heart disease associated with PAVM. It had developed in 8 of them after some type of cavopulmonary anastomosis. Six of these 8 patients had associated interruption of the inferior vena cava. In 4 of 8 patients undergoing cavopulmonary anastomosis, hepatic venous blood flow had been excluded from the pulmonary circulation with the bilateral development of PAVM. In the remaining 4 patients, cavopulmonary anastomosis excluded hepatic venous blood flow from one lung, with unilateral development of PAVM in the lung excluded from hepatic venous blood. In the other 2 patients who did not undergo cavopulmonary anastomosis, PAVM was associated with biliary atresia.

From these findings Srivastava and colleagues concluded that the development of PAVM after cavopulmonary anastomosis may be related to the exclusion of hepatic venous blood containing some putative substance from the pulmonary circulation. They also speculated that redirection of hepatic venous blood to pulmonary circulation in some patients after cavopulmonary anastomosis may reverse the PAVM.

This speculation was based on the pathologic similarity of PAVM after cavopulmonary anastomosis in an autopsied patient to that reported in patients with hepatic cirrhosis, as well as on the report of 2 children [5] in whom PAVM reversed after orthotopic liver transplantation for biliary atresia.

This important speculation has been strongly supported by recent studies reporting the regression of PAVM after surgical inclusion of hepatic venous blood to the pulmonary circulation in patients who had undergone the TCPS operation and in whom PAVM developed.

Knight and Mee [6] reported that, in a 5-year-old girl who had undergone TCPS operation and had development of PAVM, the fistulas regressed after the surgical inclusion of hepatic venous blood to the pulmonary circulation performed 25 months after the initial operation. Shah and associates [7] reported 3 such infants with polysplenia and interrupted inferior vena cava. The infants started to demonstrate cyanosis 7 to 27 months after the hemi-Fontan operation, which consisted of a side-to-side anastomosis of the superior vena cava with the branch pulmonary arteries, occlusion of the inflow of the superior vena cava into the right atrium, and augmentation of the confluence of the branch pulmonary arteries. Inclusion of the hepatic vein to the pulmonary circulation resulted in the resolution of PAVM at a median duration of 7 months after the conversion operation.

I speculate that the fact that PAVM seldom developed in older patients supports the "substance theory" as in the older patients the putative substance in hepatic venous blood could be transported to the lung through well-developed bronchial collaterals. In a multiinstitutional study [8] we have performed, it was revealed that PAVM did not develop in any of the 14 patients who underwent TCPS operation at the age of 12 years or older.

However, as PAVM is seen only in a minority of patients with polysplenia after TCPS [4], it should be kept in mind that there may be another factor that either prohibits or promotes the development of PAVM after TCPS. Among 5 patients we have converted from TCPS to total cavopulmonary connection, PAVM was aggravated after conversion in 2 patients. This also suggests the existence of factor(s) in the development or promotion of PAVM other than the putative substance in hepatic venous blood.

Although the TCPS operation is now used only under particular circumstances, the bidirectional cavopulmonary shunt (BCPS), which had been used as a part of TCPS, is now widely used as a palliative procedure, particularly in patients who are considered less than ideal candidates for a Fontan-type operation. In cases where the blood flow through the pulmonary artery trunk or through the systemic-to-pulmonary arterial shunt is closed by BCPS, PAVM should develop in some patients as the hepatic venous blood is excluded from the pulmonary circulation in this circumstance. However, reports of this sequela seem to be very few, if any.

There are two possible reasons why PAVM does not develop after BCPS. One is that the patients, mostly young patients, proceed to the final Fontan-type operation rather soon after BCPS. Second, as the amount of blood through the BCPS is not sufficient in cases without azygos continuation, the blood flow through either the pulmonary arterial trunk or a systemic-to-pulmonary arterial shunt is often left untouched so that the hepatic venous blood is not completely excluded from the pulmonary circulation.

Recently, however, there was a report on the results of BCPS including hemi-Fontan operation [9] performed in 85 consecutive infants less than 6.5 months old, 2 of them with interrupted inferior vena cava. All previous systemic-to-pulmonary arterial shunts as well as any additional sources of pulmonary blood flow were either ligated or removed except in 1 patient. Follow-up was on average 23 months, and nothing was mentioned about the postoperative development of PAVM.

The discrepancy in the frequency of PAVM development between TCPS and BCPS is another one of the grounds supporting the speculation that the polysplenia itself is one of the risk factors of PAVM, as the TCPS operation is usually performed only for patients with polysplenia. However, Srivastava and colleagues [4] reported that PAVM developed in only 1 of the 56 polysplenic patients without cavopulmonary anastomosis, and this patient also had biliary atresia.

Thus polysplenia alone does not lead to the development of PAVM, but it could be one of the predisposing risk factors for PAVM in association with the presence of liver abnormality or the exclusion of hepatic venous flow to the lung. As it has been reported that BCPS in the presence of forward flow from the ventricle, unless it is too excessive, has no adverse effect on pulmonary circulation, we now maintain the policy of leaving the forward blood flow to the pulmonary artery through either the stenotic pulmonary arterial trunk or a previously created systemic-to-pulmonary arterial shunt.

If we could measure and control the amount of blood flow through the pulmonary arterial trunk or systemic-to-pulmonary arterial shunt precisely before or during the operation, it might be possible to make the TCPS operation a permanent palliation. For this to be the case, the amount of blood flow thus delivered to the pulmonary circulation containing hepatic venous blood must be enough to prevent PAVM from developing and not so excessive as to disturb circulatory stability.

Resolution of PAVM after liver transplantation or inclusion of hepatic venous flow to the lung suggests that PAVM develops by the dilation of preexisting small vessels, and this speculation had been supported histologically. Pulmonary arteriovenous malformation after TCPS resembles the huge collaterals seen in patients with Kawasaki disease after complete occlusion of the major coronary arteries. These vessels, unlike those associated with adult coronary artery disease, are quite tremendous, disappearing soon after the creation of aortocoronary bypass and reappearing when the bypass is closed. Although there is a substantial difference between arterial collaterals and arteriovenous malformations, appearance and disappearance seem to occur more easily when patients are young. From the similarity in both reversibility and easy development, the younger age may also be an additional risk factor that promotes the development of PAVM. This speculation may also be supported by the fact that many of the cases of PAVM in patients suffering from liver cirrhosis are in young patients.

Further investigations are obviously mandatory to determine the risk factor(s) developing or promoting PAVM other than the exclusion of the speculated putative substance that inhibits dilation of the pulmonary precapillary or capillary vessels in the pulmonary circulation, as well as to identify this substance.

Footnotes

Address reprint requests to Dr Kawashima, National Cardiovascular Center, 5-7-1 Fujishiro-dai, Suita, Osaka 565, Japan.

References

1. Matsuda H, Kawashima Y, Takano H, Miyamoto K, Mori T. Experimental evaluation of atrial function in right atrium--pulmonary artery conduit operation for tricuspid atresia. J Thorac Cardiovasc Surg 1981;81:762–7.[Abstract]
2. Kawashima Y, Kitamura 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]
3. De Leval MR, Kilner P, Gewillig M, et al. Total cavopulmonary connection. A logical alternative to atriopulmonary connection for complex Fontan operation. J Thorac Cardiovasc Surg 1988;96:682–95.[Abstract]
4. Srivastava D, Preminger T, Lock JE, et al. Hepatic venous blood and the development of pulmonary arteriovenous malformations in congenital heart disease. Circulation 1995;92:1217–22.[Abstract/Free Full Text]
5. Laberge JM, Braudt ML, Lebecque P, et al. Reversal of cirrhosis-related pulmonary shunting in two children by orthotopic liver transplantation. Transplantation 1992;53:1135–8.[Medline]
6. Knight WB, Mee RBB. A cure for pulmonary arteriovenous fistulas? Ann Thorac Surg 1995;59:999–1001.[Abstract/Free Full Text]
7. Shah MJ, Rychik J, Fogel MA, Murphy JD, Jacobs ML. Pulmonary arteriovenous malformations after superior cavopulmonary connection: resolution after inclusion of hepatic veins in the pulmonary circulation. Ann Thorac Surg 1997;63:960–3.[Abstract/Free Full Text]
8. Kawashima Y, Matsuki O, Yagihara T, Matsuda H. Total cavopulmonary shunt operation. Semin Thorac Cardiovasc Surg 1994;6:17–20.[Medline]
9. Bradley SM, Mosca RS, Hennein HA, Crowley DC, Kulik TJ, Bove EL. Bidirectional superior cavopulmonary connection in young infants. Circulation 1996;94(Suppl 2):5–11.

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