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Ann Thorac Surg 2000;70:1918-1922
© 2000 The Society of Thoracic Surgeons

Original article: cardiovascular

Development of pulmonary arteriovenous fistulas after bidirectional cavopulmonary shunt

Soo Jin Kim, MDa, Eun Jung Bae, MDa, Do Jun Cho, MDa, In Seung Park, MDa, Yang Min Kim, MDb, Woong-Han Kim, MDc, Seong Ho Kim, MDa

a Department of Pediatric Cardiology, Sejong Heart Institute, Sejong General Hospital, Puchon City, South Korea
b Department of Radiology, Sejong Heart Institute, Sejong General Hospital, Puchon City, South Korea
c Department of Cardiac Surgery, Sejong Heart Institute, Sejong General Hospital, Puchon City, South Korea

Accepted for publication May 11, 2000.

Address reprint requests to Dr Bae, Department of Pediatric Cardiology, Sejong Heart Institute, Sejong General Hospital, 91-121 Sosa Bon 2-dong, Sosa-ku, Puchon City, Kyonggi-do, 422-232, South Korea


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. A high incidence of pulmonary arteriovenous fistulas (PAVF) has been reported after bidirectional cavopulmonary shunt (BCPS) or total cavopulmonary shunt (TCPS; BCPS in patients with interrupted inferior vena cava). However, the definite diagnostic criteria or standard diagnostic modality of PAVF has not yet been defined. The goal of this study was to evaluate the diagnostic modalities and the prevalence of PAVF.

Methods. We selected 10 patients with TCPS and 27 patients with BCPS. Lung perfusion scan, contrast echocardiogram, and pulmonary angiogram were performed. The results were compared among groups of patients and among each diagnostic modality.

Results. All 10 patients with TCPS and 16 and 13 patients with BCPS showed positive results on contrast echocardiograms and lung scans, respectively. Six patients with TCPS and 4 patients with BCPS showed positive results on pulmonary angiograms. All patients with TCPS developed subclinical or clinical PAVF and 19 patients with BCPS developed subclinical PAVF and none of them had clinical PAVF during the short-term follow-up.

Conclusions. Most patients with bidirectional cavopulmonary anastomosis have subclinical evidence of right-to-left intrapulmonary shunting. This problem can be demonstrated with various diagnostic modalities.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
Bidirectional cavopulmonary shunting (BCPS) has been increasingly applied as a preparatory procedure toward the staged Fontan operation. However, the high incidence of pulmonary arteriovenous fistulas (PAVF) has been reported after BCPS or total cavopulmonary shunt (TCPS; Kawashima type operation; BCPS in left atrial isomerism with interrupted inferior vena cava [IVC]). Therefore, the delayed and progressive hypoxemia by PAVF [1, 2] has given us great concern about this procedure. Recently, it was reported that the inclusion of hepatic blood flow to the pulmonary circulation alleviates PAVF [3, 4], so early identification of PAVF may avoid morbidity and mortality [3].

The contrast echocardiogram, lung perfusion scan, and pulmonary angiogram are useful to detect intrapulmonary right-to-left shunts [5] and have been used for the diagnosis of the PAVF. The purposes of the present study were to compare the results of the three diagnostic modalities for PAVF and to assess the incidence of clinical and possible subclinical PAVF after BCPS and TCPS.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Patients
Between January 1989 and November 1999, 98 patients underwent BCPS or TCPS for various anomalies of single ventricle physiology at Sejong Heart Institute. Among these 98 patients, completion to a Fontan operation was performed in 50 patients, and among these patients, those who previously underwent a Fontan operation were excluded from this study. From the remaining 48 patients, 37 (27 patients with BCPS and 10 patients with TCPS) were selected. We excluded 11 cases with venous collaterals of more than moderate degree by Trussler’s report [6] in superior or inferior vena cava venography, because of possible false-positive results at lung perfusion scan and contrast echocardiography.

The mean age at operation in this study was significantly older in the TCPS group than in the BCPS group. Other hemodynamic data before operation are summarized in Table 1. For the control group, we selected patients with tetralogy of Fallot who had undergone total correction without any residual intracardiac shunt, because these patients were more suitable for lung perfusion scans and had experienced cavopulmonary bypass most consistently.


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  		Table 1. Clinical and Hemodynamic Data of Patients

 
Contrast echocardiography
Two-dimensional contrast echocardiography was performed with agitated saline as a contrast agent in all patients. We injected 10 mL of agitated saline into a peripheral vein of the arm or the subclavian vein on the side of the cavopulmonary anastomosis. After the injection, we observed the patient’s heart in a parasternal four-chamber view or subcostal coronal view by using a 5-MHz transducer. We considered the study as positive when there was prompt appearance of echo contrast in the pulmonary venous atrium (Fig 1). To ensure that the procedure did not produce a false-positive result, we carried out the same procedure in 10 control patients. We graded the positive results into mild (very short, faint, and inhomogeneous echoes), moderate (between mild and severe), and severe (homogeneously strong echoes with an echo density similar to that of the adjacent myocardial wall) degrees. We defined the study as negative when two consecutive injections failed to demonstrate positive results. The result of the study was graded by the agreement between two observers.



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  		Fig 1. Contrast echocardiogram (subcostal coronal view) of patients who underwent bidirectional cavopulmonary anastomosis. (A) Negative; no appearance of echo contrast in the pulmonary venous atrium is suggestive of absent intrapulmonary right-to-left shunt. (B) Positive; the appearance of echo contrast in the pulmonary venous atrium is suggestive of pulmonary arteriovenous fistulas. (CA = common atrium; CAVV = common atrioventricular valve; SV = single ventricle.)

 
Lung perfusion scan
Lung perfusion scan was performed by injecting 2 to 3 mCi 99 mTc-MAA (Dupont Pulmolite; Billerica, MA) into a peripheral vein of the arm on the side of the cavopulmonary anastomosis in the supine position. Intrapulmonary right-to-left shunting was detected by the uptake of radionuclide in peripheral organs except for the lung (Fig 2). The intrapulmonary right-to-left shunt fraction was calculated by the following formula:

We considered the study positive when the shunt fraction exceeded 11% (97th percentile of the control group of 30 patients).



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  		Fig 2. Lung perfusion scan after injection of macroaggregated albumin labeled with 99 mTc. (A) Negative. (B) Positive: the extrapulmonary isotope fixation on the brain (arrow) is suggestive of intrapulmonary right-to-left shunt.

 
Pulmonary angiography
Angiography was performed in the ipsilateral superior vena cava in all patients and in the IVC in the case of IVC interruption if we could observe the shape of pulmonary arterial branches. The time lag of the first appearance of contrast dye at the hilar pulmonary artery and the lobar pulmonary vein was measured as the pulmonary transit time. In addition to typical reticular or snowflake-like appearances of peripheral pulmonary arteries, rapid pulmonary transit time (early visualization of contrast dye in the pulmonary veins and pulmonary venous chamber while predominance of contrast dye was still present in the pulmonary artery, implying bypass of the capillary system) was considered as a PAVF-positive result (Fig 3).



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  		Fig 3. Pulmonary angiogram of patient with total cavopulmonary shunt. An injection through a catheter placed in the superior vena cava (RSVC) shows typical reticular or snowflake-like appearance of the peripheral pulmonary artery. Note the course of catheter (arrow) through a left hemiazygos vein, left superior vena cava, pulmonary artery, and right superior vena cava. (p < 0.05.)

 
Diagnosis of pulmonary arteriovenous fistula
We diagnosed clinical PAVF if all of the following criteria were met: (1) detection of progressive resting systemic arterial desaturation by pulse oximetry, without any evidence of parenchymal lung disease, (2) aortic oxygen saturation of 80% or less in room air during cardiac catheterization, and (3) one or more positive results of the three diagnostic modalities: (a) extrapulmonary shunt fraction more than 11% at lung perfusion scan, (b) positive contrast echocardiogram, and (c) positive pulmonary angiographic results. Also we defined subclinical PAVF with the following criteria: (1) absent progressive systemic arterial desaturation; SaO2 more than 80%, and (2) one or more positive results of three diagnostic modalities for PAVF as described previously.

Data analysis
Numeric data are presented as mean ± SD. Because of the small size of the study groups, which did not allow any assumption about the distribution of the studied values, continuous variables were analyzed by the two-tailed Mann–Whitney U test or Kruskal–Wallis test. Discrete variables were analyzed by {chi}-square test and Fisher’s exact test when the expected number of subjects for observation was small. Statistical significance was assumed to be p less than 0.05. Statistical analysis was carried out with the SPSS statistical software package, version 8.0 (SPSS Inc, Chicago, IL).


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Incidence of pulmonary arteriovenous fistula
All 10 patients of the TCPS group developed PAVF and 19 of 27 patients (70%) of the BCPS group developed PAVF. In the BCPS group, all patients were classified with subclinical PAVFs. However in the TCPS group 5 patients had clinical and the other 5 patients had subclinical PAVF.

Contrast echocardiogram
The result was negative in all patients of the control group. Among 27 patients of the BCPS group, the result was positive in 16 patients and of a mild, moderate, or severe degree in 5, 6, and 5 patients, respectively. The result was positive in all patients of the TCPS group, of which 7 of 10 patients showed severe degree of echo contrast. All patients with clinical PAVF showed severe degree of echo contrast and 3 patients with subclinical PAVF showed negative results.

Lung perfusion scan
The result was positive in 13 patients in the BCPS group and all patients in the TCPS group. Controls (n = 30) showed 6.9% ± 2.1% of right-to-left shunt fraction. The fractions of right-to-left shunt were 11.5% ± 5.5% in the BCPS group and 31.4% ± 18.9% in the TCPS group. The difference in shunt fractions between the BCPS and TCPS groups was statistically significant (p < 0.05) (Fig 4). Mean shunt fractions of absent, subclinical, and clinical PAVF were 6.9 ± 1.7, 14.2 ± 5.7, and 45.6 ± 16.0, respectively, and significant differences were noted between the groups (p < 0.05).



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  		Fig 4. Shunt fraction on lung perfusion scan of each patient group. (BCPS = bidirectional cavopulmonary shunt; TCPS = total cavopulmonary shunt.)

 
Pulmonary angiogram
Of 37 patients, 10 patients (4 of 27 patients with BCPS and 6 of 10 patients with TCPS) showed angiographic findings of typical PAVF. The pulmonary transit times of the patients with positive angiographic finding were shorter (43.9 ± 20.0/60 s) than those of the patients with negative angiography (96.7 ± 9.0/60 s; p < 0.05). Mean transit time of absent, subclinical, and clinical PAVF were 88.0 ± 25.1, 89.3 ± 36.9, and 40.6 ± 6.9 seconds, respectively, and significant differences were noted between groups (p = 0.022).

Comparisons among the diagnostic methods
Sensitivity of contrast echocardiograms (89.7%) was higher than that of lung scans (79.3%) or pulmonary angiograms (34.3%). We compared each diagnostic test with the {chi}-square test with a measure of agreement (kappa). There were fair agreements between contrast echocardiograms and lung scans (kappa = 0.460, p = 0.008) but poor agreement between lung scans and pulmonary angiograms (kappa = 0.368, p = 0.006) and between contrast echocardiograms and pulmonary angiograms (kappa = 0.180, p = 0.224). Eight patients presented negative results in all diagnostic tests and were diagnosed with absent PAVFs as defined in the Method section. Five patients with clinically overt PAVFs showed positive results in all diagnostic methods (Table 2).


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  		Table 2. Comparison of Results of Diagnostic Methods

 
Comparisons of clinical hemodynamic data among groups by diagnostic criteria
The age at investigation, the age at operation, and the interval between operation and investigation showed no statistically significant difference among the groups according to development of PAVF. Statistical differences were noted in pulmonary vascular resistance (p = 0.012) and arterial oxygen saturation (p = 0.002) (Table 3). Development of PAVF according to time interval between age at operation and investigation is shown in Figure 5.


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  		Table 3. Comparison of Clinical and Hemodynamic Data According to the Development of PAVF

 


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  		Fig 5. Development of pulmonary arteriovenous fistulas (PAVF) according to time interval.

 

   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
Pulmonary arteriovenous fistula is a major cause of late clinical deterioration in patients treated with BCPS or TCPS [1, 2, 4]. Untreated PAVF may result in significant mortality and morbidity. Several reports have demonstrated a combined mortality of 11% and a combined significant morbidity of 27% after 7 years of follow-up [7].

It has been suggested that the mechanism for development of PAVF is interruption of hepatic venous return to the pulmonary circulation. Several reports documented that surgical inclusion of hepatic flow in the pulmonary circulation resulted in the resolution of PAVF [3, 8]. In support of this theory, PAVF also develops in patients with hepatic dysfunction, such as liver cirrhosis, and PAVF has been reported to resolve after liver transplantation or improvement in liver function [9–11]. These findings suggest that the existence of a biochemical agent produced by the healthy liver plays some inhibitory role during initial passage through the lung, preventing the development of PAVF. After a TCPS, if the main pulmonary artery is divided or ligated, the entire hepatic venous blood supply bypasses the lungs and is shunted directly into the systemic circulation.

However, currently BCPS procedures have not been shown to cause significant PAVF [3, 12]. One reason may be that they are usually performed as part of a two-stage approach, in which most patients proceed relatively quickly to incorporation of inferior vena caval and hepatic flow into the pulmonary circulation, hence, completion of the Fontan operation.

Our studies have demonstrated that the prevalence of clinical PAVF after TCPS is 50%. Interestingly, no patients had clinical PAVF after BCPS but 19 patients (70%) had intrapulmonary right-to-left shunts at contrast echocardiograms or lung perfusion scans before severe hypoxemia. In our data, subclinical PAVFs were found in as many as 64.8% (24 of 37patients) of patients in the TCPS or BCPS group. In this study, contrast echocardiography and lung perfusion scan seemed to be useful in the early detection of PAVF even without clinical hypoxemia, and in quantifying the amount of intrapulmonary shunt in patients after cavopulmonary anastomosis. We believe that it is important to look carefully for this subclinical PAVF.

The patients’ profiles of the TCPS and BCPS group were not similar. The age at operation and the interval between operation and investigation were older and longer in the TCPS group than in the BCPS group. Although the clinical PAVF incidence after TCPS was high, up to 50% at mean 41 months after operation in this study, we cannot conclude that the TCPS group was at more risk for PAVF than the BCPS group. It appears that a higher rate of clinical PAVF develops with a longer follow-up period after cavopulmonary anastomosis.

In conclusion, most patients with bidirectional cavopulmonary anastomosis have subclinical evidence of right-to-left intrapulmonary shunting. Furthermore, with contrast echocardiography or lung scan we can detect the PAVF even without clinical evidence of hypoxemia. Further studies are warranted to observe the progression of subclinical PAVF.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Cloutier A., Ash J.M., Smallhorn J.F., et al. Abnormal distribution of pulmonary blood flow after the Glenn shunt or Fontan procedure: risk of development of arteriovenous fistulae. Circulation 1985;72:471-479.[Abstract/Free Full Text]
  2. Stümper O., Wright J.G., Sadiq M., De Giovanni J.V. Late systemic desaturation after total cavopulmonary shunt operations. Br Heart J 1995;74:282-286.[Abstract/Free Full Text]
  3. Shah M.J., Rychik J., Fogel M.A., Murphy J.D., Jacobs M.L. Pulmonary AV malformations after superior cavopulmonary connection: resolution after inclusion of hepatic veins in the pulmonary circulation. Ann Thorac Surg 1997;63:960-963.[Abstract/Free Full Text]
  4. Knight W.B., Mee R.B.B. A cure for pulmonary arteriovenous fistulas?. Ann Thorac Surg 1995;59:999-1001.[Abstract/Free Full Text]
  5. Murakami T., Nakanishi M., Konishi T., Hase N., Sakiyama Y. Diffuse pulmonary arteriovenous fistulae shown by contrast echocardiography and pulmonary angiography. Pediatr Radiol 1991;21:128.[Medline]
  6. Trusler G.A., Williams W.G., Cohen A.J., et al. The cavopulmonary shunt. Evolution of a concept. Circulation 1990;82(Suppl 4):131-138.
  7. Moore J.W., Kirby W.C., Madden W.A., Gaither N.S. Development of pulmonary arteriovenous malformations after modified Fontan operations. J Thorac Cardiovasc Surg 1989;98:1045-1050.[Abstract]
  8. Srivastava D., Preminger T., Lock J.E., et al. Hepatic venous blood and the development of pulmonary arteriovenous malformation in congenital heart disease. Circulation 1995;92:1217-1222.[Abstract/Free Full Text]
  9. Barbe T., Losay J., Grimon G., et al. Pulmonary arteriovenous shunting in children with liver disease. J Pediatr 1995;126:571-579.[Medline]
  10. Sherlock S. Disorders of the liver and biliary system, 8th ed. Oxford, UK: Blackwell Scientific, 1989:82-85.
  11. Laberge J.M., Brandt M.L., Lebecque P., et al. Reversal of cirrhosis related pulmonary shunting in two children by orthotopic liver transplantation. Transplantation 1992;53:1135-1138.[Medline]
  12. Lamberti J.J., Spicer R.I., Waldman J.D., et al. The bidirectional cavopulmonary shunt. J Thorac Cardiovasc Surg 1990;100:22-30.[Abstract]



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