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Ann Thorac Surg 1999;68:969-974
© 1999 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Importance of acquired systemic-to-pulmonary collaterals in the Fontan operation

Kirk R. Kanter, MDa, Robert N. Vincent, MDb, Anthony A. Raviele, MDb

a Division of Cardio-Thoracic Surgery, Department of Surgery, Emory University School of Medicine, Atlanta, Georgia, USA
b The Children’s Heart Center, Department of Pediatrics, Emory University School of Medicine, Atlanta, Georgia, USA

Address reprint requests to Dr Kanter, Division of Cardio-Thoracic Surgery, Emory University School of Medicine, 1365 Clifton Rd, Atlanta, GA 30322
e-mail: kkanter{at}emory.org

Presented at the Thirty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 25–27, 1999.


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. Children with chronic cyanotic heart disease often develop systemic-to-pulmonary collateral arteries that can be deleterious at the time of a Fontan procedure due to excessive pulmonary blood flow. We therefore occlude all significant collaterals during cardiac catheterization.

Methods. From June 1993 to May 1998, 93 children aged 1.5 to 15.8 years (median 2.5 years) underwent a fenestrated lateral tunnel Fontan procedure. Eighty-nine (96%) had a previous bidirectional Glenn anastomosis, including 31 (33%) with a Norwood procedure.

Results. Preoperatively, 33 children (35%) required occlusion of 1 to 11 (mean 3.6) collateral vessels. Two of the three perioperative deaths (operative survival 97%) were due to excessive pulmonary blood flow from unrecognized collaterals in one and uncontrollable collaterals in the other. Postoperatively, 19 children (20%) required coil occlusion of 1 to 21 (mean 5.6) collaterals for elevated pulmonary artery pressures, heart failure, or prolonged chest tube drainage. Duration of inotropic support, postoperative ventilation, intensive care unit stay, and postoperative hospitalization were all significantly longer in the patients who had postoperative occlusion of collaterals. On follow-up of 2 to 67 months (mean 35 months), there have been four late deaths (two infections, two heart failures); 6 patients underwent successful cardiac transplantation for refractory heart failure. All 8 patients with ventricular failure required occlusion of significant collaterals postoperatively.

Conclusions. Hemodynamically significant collaterals are not uncommon in Fontan candidates, and aggressive control can result in good operative and medium-term survival. After the Fontan, significant collaterals may be a marker for eventual cardiac failure because 8 of 18 patients requiring postoperative coils went on to transplantation or died of heart failure.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
The Fontan procedure with its various modifications currently is the treatment of choice for children with single-ventricle physiology. Advances over the past decade have improved both early and late outcomes despite the application of this procedure to patients with increasingly complex anatomy [1].

These children with long-standing cyanotic heart disease can develop systemic-to-pulmonary artery collateral vessels [2–6]. Some studies have shown that patients with these abnormal vessels have prolonged pleural effusions after the Fontan procedure [7, 8] and can even have a higher mortality [9]. With this in mind, since June 1993, we have aggressively searched for these collaterals and attempted to occlude all significant collaterals at the time of cardiac catheterization. This paper reviews the results of this policy in 93 consecutive children undergoing a Fontan procedure.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
From June 1993 to May 1998, 93 consecutive children underwent a modified Fontan procedure by a single surgeon (K.R.K.). Ages at time of operation ranged from 1.5 to 15.8 years (mean 3.3 ± 2.3 years, median 2.5 years). The principal underlying diagnoses are shown in Table 1. Thirty-one children (33%) had undergone a Norwood procedure in infancy. Fourteen children had previous pulmonary artery banding, including 6 with repair of an aortic coarctation. A previous Blalock-Taussig or central shunt had been performed in 44 patients (47%), excluding the children with a Norwood procedure. Eighty-nine (96%) had a previous bidirectional Glenn anastomosis at 1.2 ± 1.4 years of age (median 9.7 months). The time interval from the bidirectional Glenn anastomosis to the Fontan procedure was 1.7 ± 0.7 years (range 3 months to 4.4 years). All four children without a previous bidirectional Glenn anastomosis were older at the time of the modified Fontan procedure (range 6.5 to 15.8 years).


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  		Table 1. Principal Diagnosis (n = 93)

 
Cardiac catheterization
All children had preoperative hemodynamic investigation by cardiac catheterization with angiography. Attempts were made to identify significant systemic-to-pulmonary artery collaterals by aortogram as well as selective injections into the internal mammary, intercostal, bronchial, and chest wall arteries as necessary. Five criteria were used to determine if a systemic to pulmonary collateral artery was significant. First was direct opacification of a pulmonary artery segment with contrast injection into the collateral artery. Second was opacification of a pulmonary vein on levophase after systemic arterial injection. A third criterion was negative washout of contrast injected into the pulmonary artery or Glenn anastomosis. The final two criteria were either a step-up in oxygen saturation in the pulmonary arteries or elevated pulmonary arterial or left atrial pressure. Once identified, efforts were made to occlude all significant collaterals percutaneously with Gianturco coils [10]. Internal mammary arteries were coil occluded only if multiple collaterals originated from them and if it was impractical to selectively occlude the individual collaterals separately. A representative case is shown in Figure 1. Occasionally, because of the multiplicity of collateral arteries and limitations of contrast load, it was necessary to occlude collaterals with more than one session in the cardiac catheterization laboratory. Postoperative cardiac catheterization was not performed routinely after the Fontan procedure unless there were clinical indications such as prolonged pleural effusions, respiratory or cardiac failure, or evidence of elevated pulmonary artery pressures.



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  		Fig 1. Angiogram of a patient before a Fontan procedure demonstrating a significant systemic-to-pulmonary collateral. (A) Contrast injection into the right internal mammary artery showing a large tortuous artery. (B) Levophase of the same injection demonstrating opacification of the pulmonary vein. (C) Repeat contrast injection into the left internal mammary artery after coil occlusion with multiple Gianturco coils showing no evidence of residual collaterals.

 
Operative techniques
All patients had complete cavopulmonary connection using an intraatrial lateral tunnel fashioned of polytetrafluoroethylene (PTFE) [11, 12]. In general, a single 2.8-mm fenestration was created in the PTFE baffle, although early in the experience, two fenestrations were used. The intracardiac portion of the operation was conducted using induced ventricular fibrillation without aortic crossclamping in 87 patients. In the remaining 6 patients, cold cardioplegic arrest was utilized to facilitate concomitant atrioventricular or semilunar valve repair or replacement. Efforts were made to divide all easily accessible pleural and pericardial adhesions. Commonly, pleural adhesions tended to be more vascular on the side of a previous thoracotomy. The internal mammary arteries were not routinely ligated in hopes of reducing the incidence of postoperative sternal complications. Postoperatively, all patients were maintained on low-dose aspirin unless a mechanical prosthetic valve had been placed, in which case warfarin was used.

Statistical methods
Values are shown as mean ± standard deviation. Differences between groups were compared using analysis of variance (ANOVA) or unpaired Student’s t test when appropriate. Differences were considered significant for p less than 0.05. Correlations were examined by simple regression analysis.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Forty-three patients in this series (46%) had coil occlusion of significant systemic to pulmonary collaterals (Table 2). Twenty-four patients had collaterals occluded only preoperatively (1 to 11 vessels/patient, mean 3.5 ± 3.1 vessels); 10 patients had collaterals occluded only postoperatively (1 to 21 vessels/patient, mean 5.5 ± 6.3 vessels); 9 patients had collaterals occluded both preoperatively and postoperatively (2 to 17 vessels/patient, mean 9.6 ± 5.0 vessels). There was no statistically significant difference in the need for collateral occlusion in patients grouped by principal diagnosis or by whether or not they had a Norwood procedure, a previous Blalock-Taussig or central shunt, a pulmonary artery band, or a coarctation repair. Younger age at time of Fontan correlated with the need for coils preoperatively (p < 0.01), but the time interval between Glenn and Fontan did not correlate with collateral formation.


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  		Table 2. Incidence of Coil Occlusion of Systemic-to-Pulmonary Collateral Arteries

 
There were three perioperative deaths in this series (operative survival 97%). Two of these deaths were collateral related. One patient early in the experience died in the operating room after takedown of the Fontan because of elevated left atrial pressures despite good systolic ventricular function and low estimated pulmonary vascular resistance. Retrospective review of the preoperative angiograms revealed previously unrecognized significant systemic-to-pulmonary collaterals from the descending aorta. The other collateral related death was in a child known to have significant collaterals who died 38 days postoperatively of unrelenting heart failure due to a persistently large left-to-right shunt despite occlusion of 15 collateral vessels both preoperatively and postoperatively and despite attempts at operative elimination of residual collaterals.

In the 90 operative survivors, we analyzed duration of inotropic support, postoperative ventilation, intensive care unit (ICU) stay, and hospital stay (Table 3). For those operative survivors who underwent coil occlusion of significant systemic-to-pulmonary artery collaterals either preoperatively or postoperatively (n = 42), there were no significant differences in these variables compared with the children who did not have any vessels coil occluded, except for a longer hospital stay (14.9 ± 15.4 vs 9.5 ± 9.0 days, coil vs no coil, p = 0.04). Comparing patients receiving preoperative coils (n = 32) with those who did not (n = 58), there were no statistically significant differences for these variables, although interestingly, postoperative ventilation and ICU stay seemed to be shorter in those survivors who had preoperative coils (Table 3). However, comparison of the 18 operative survivors who underwent coil occlusion after the Fontan procedure with the 72 patients who did not undergo postoperative coil occlusion revealed that all variables examined were statistically significantly longer (Fig 2; Table 3).


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  		Table 3. Comparison of Postoperative Variables

 


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  		Fig 2. Comparison of the 72 operative survivors who did not have occlusion of systemic-to-pulmonary collaterals postoperatively with the 18 patients who had postoperative coil occlusion. Error bars represent 95% confidence limits. Vent = duration of ventilation; inotrope = duration of inotropic support; ICU = intensive care unit stay; hosp = duration of postoperative hospitalization.

 
The 90 operative survivors have been followed from 2 months to 5.5 years (mean 2.9 years). Two patients died of pneumonia 2.5 and 11 months after the Fontan procedure. Eight patients developed refractory heart failure and were evaluated for cardiac transplantation. One had an unacceptably high level of preformed antibodies and died 5 months after the Fontan procedure. This patient, in fact, originally had been evaluated for cardiac transplantation before his Fontan, but due to his high antibody levels, underwent a Fontan procedure in the hopes of improving his cardiac status without success. Another patient listed for transplantation died while on the transplant waiting list before a suitable donor could be identified. Six others underwent successful cardiac transplantation on average 17 months after the Fontan procedure (range 2 months to 4 years). All 8 patients with refractory heart failure required coil occlusion of significant systemic-to-pulmonary artery collaterals postoperatively.


   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
In this study reviewing 93 consecutive patients undergoing a modified Fontan procedure, we found and coil occluded significant collaterals in 43 patients (46%) at cardiac catheterization either before or after the Fontan procedure. Others have found a similar incidence of systemic-to-pulmonary collateral arteries in this patient population. Triedman and associates [3] reported a 65% incidence of collaterals in children after a bidirectional Glenn anastomosis and a 30% incidence after a modified Fontan procedure. Salim and associates [4] found that 59% of children had collaterals after a bidirectional Glenn, and Bridges and colleagues [5] found that 20% of children after a Fontan had collaterals. Furthermore, Spicer and colleagues reported as many as 84% of catheterizations of children before a Fontan procedure showed collateral vessels, although they judged only half of them to be significant [8]. Clearly, when sought for, there is a significant proportion of children undergoing a Fontan procedure in whom these collaterals can be demonstrated.

The etiology of these enlarged collateral arteries is unknown. One can speculate that it is the result of chronic hypoxemia and thus an adaptive mechanism to deliver more total pulmonary blood flow. The presence of abnormal systemic-to-pulmonary collateral arteries has also been reported in children with cyanotic heart disease other than that requiring a Fontan procedure [13, 14]. If indeed chronic hypoxemia is the stimulus for development of these collaterals, then one would expect a higher incidence in older children, as was reported by Ichikawa and colleagues [9]. However, the present study not only failed to confirm this association, but interestingly found a significant correlation between younger age and the need for occlusion of collaterals preoperatively.

Triedman and others reported a higher incidence of collaterals in children who had a previous Blalock-Taussig shunt [3]. This current study, however, did not find evidence to confirm this relationship. Similarly, we found no correlation between the development of collaterals and the time interval between Glenn and Fontan, previous coarctation repair or pulmonary artery banding, or previous Norwood procedure.

In this study, all significant collaterals, once found, were coil occluded at the time of cardiac catheterization. We reasoned that these vessels create an increased left-to-right shunt due to extra pulmonary blood flow. This is usually reasonably well tolerated in children after a bidirectional Glenn anastomosis and can even result in higher systemic arterial oxygen saturations due to augmented pulmonary blood flow [4]. However, after a Fontan procedure, this excessive pulmonary blood flow can result in elevated pulmonary arterial and left atrial pressures with subsequent heart failure or respiratory failure. In a very carefully performed quantitative study looking retrospectively at angiograms in children after a bidirectional Glenn or Fontan procedure, Triedman and associates [3] calculated the value of the average estimated total cross-sectional area of the collaterals in 54 cardiac catheterizations at 10.7 ± 7.2 mm2. This compares with a calculated cross-sectional area of 12.6 mm2 for a 4.0-mm modified Blalock-Taussig shunt and 9.6 mm2 for a 3.5-mm modified Blalock-Taussig shunt. Certainly, under normal circumstances, one would not knowingly leave a functioning modified Blalock-Taussig shunt patent after a Fontan procedure. This reasoning, in part, is the basis for our policy to aggressively control these collaterals before the Fontan procedure.

Clinically, this increased left-to-right shunt from systemic-to-pulmonary collaterals is important. Collaterals have been shown to result in prolonged chest tube drainage after the Fontan procedure [7] with effusions lasting twice as long compared with children who did not have collaterals [8]. In this study, children with significant collaterals had a significantly longer hospital stay (14.9 ± 15.4 vs 9.5 ± 9.0 days, coils vs no coils) presumably related to more prolonged chest tube drainage and pleural effusions. If one looks only at the group of children who required occlusion of collaterals postoperatively, all parameters examined (duration of postoperative ventilation, duration of inotropic support, ICU stay, and hospital stay) were significantly longer when compared with children who did not need collaterals occluded postoperatively (Fig 2; Table 3).

Excessive pulmonary blood flow due to systemic-to-pulmonary collaterals has also been shown to adversely affect patient survival after the Fontan procedure [9]. In this study, two of the three perioperative deaths were directly related to excessive pulmonary blood flow due to collaterals. It is our contention that the relatively low operative mortality in this series (3%) is partially related to our policy of aggressively identifying and controlling systemic-to-pulmonary collateral arteries in the preoperative period, as has been advocated by others [5, 7–9].

Eight of the operative survivors in this series developed significant heart failure and either died or underwent cardiac transplantation. All 8 of these patients required postoperative coil occlusion of a mean of eight collateral vessels (range 1 to 21 vessels/patient). Hsu and associates have previously reported that 3 of 9 patients undergoing cardiac transplantation after a Fontan procedure had aortopulmonary collateral channels, and 2 of these patients developed significant hemodynamic compromise requiring coil occlusion of these collaterals within 2 weeks of transplantation [14]. One can only speculate that the chronic burden of a large left-to-right shunt from persistent systemic-to-pulmonary collaterals can, with time, result in eventual myocardial dysfunction, particularly in a child with single-ventricle physiology.

There are potential weaknesses in this current report due to its nonrandomized nature. Although we attributed the low operative mortality in part to aggressive control of systemic-to-pulmonary collaterals preoperatively, we cannot be sure that these patients would have done well anyway without occlusion of collaterals. Supporting our conclusion, however, are reports showing more chronic pleural effusions [7, 8] and higher mortality [9] in patients with collaterals that were not controlled preoperatively. Additionally, the fact that two of the three perioperative deaths in this series were related to collaterals lends crdence to our hypothesis.

Another potential flaw in this study is the absence of routine cardiac catheterization after the Fontan procedre. Because cardiac catheterization was performed only when clinically indicated, we do not know the true incidence of systemic-to-pulmonary collaterals after the Fontan procedure in this study. However, the observed incidence of 20% in this series compares with previous reports of a 20% to 30% incidence of collaterals in cardiac catheterizations performed after the Fontan procedure [3, 5].

Finally, we contend that the need for coil occlusion of significant systemic-to-pulmonary collaterals after the Fontan procedure is a marker for poor outcome because 8 of 18 operative survivors who required postoperative coils developed end-stage heart failure. This conclusion may be the consequence of our institutional bias to search for and control collaterals if present in patients who have hemodynamic difficulties after the Fontan procedure. It is difficult to refute the argument that the causal relationship in this setting may be reversed; ie, arguing that if a patient is not doing well postoperatively, he must have collaterals, and thus, searching for them, rather than concluding that if a patient has significant collaterals postoperatively, this predisposes to a poor outcome. Although this question cannot be answered definitively without a prospective randomized trial, it is certainly our experience as well as that of others [7, 8, 14] that these patients improve hemodynamically after control of these collaterals.

In summary, in this study, we found that significant systemic-to-pulmonary collaterals are common (46%) in patients undergoing a Fontan procedure. These collaterals can be identified preoperatively or postoperatively and can result in hemodynamic compromise. A policy of aggressive search for and control of these collaterals brings acceptable results with the Fontan procedure. Finally, the need for coil occlusion of collaterals after the Fontan procedure is associated with prolonged ventilation, duration of inotropic support, ICU stay, and hospitalization, and may be a marker for an eventually unfavorable outcome.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. Gentles T.L., Mayer J.E., Gauvreau K., et al. Fontan operation in five hundred consecutive patients. J Thorac Cardiovasc Surg 1997;114:376-391.[Abstract/Free Full Text]
  2. Rothman A., Tong A.D. Percutaneous coil embolization of superfluous vascular connections in patients with congenital heart disease. Am Heart J 1993;126:206-213.[Medline]
  3. Triedman J.K., Bridges N.D., Mayer J.E., Lock J.E. Prevalence and risk factors for aortopulmonary collateral vessels after Fontan and bidirectional Glenn procedures. J Am Coll Cardiol 1993;22:207-215.[Abstract]
  4. Salim M.A., Case C.L., Sade R.M., Watson D.C., Alpert B.S., DiSessa T.G. Pulmonary/systemic flow ratio in children after cavopulmonary anastomosis. J Am Coll Cardiol 1995;25:735-738.[Abstract]
  5. Bridges N.D., Lock J.E., Mayer J.E., Burnett J., Castaneda A.R. Cardiac catheterization and test occlusion of the interatrial communication after the fenestrated Fontan operation. J Am Coll Cardiol 1995;25:1712-1717.[Abstract]
  6. Geggel R.L. Update on the modified Fontan procedure. Curr Opinion Cardiol 1997;12:51-62.[Medline]
  7. Lamberti J.J., Mainwaring R.D., Spicer R.L., Uzark K.C., Moore J.W. Factors influencing perioperative morbidity during palliation of the univentricular heart. Ann Thorac Surg 1995;60:S550-S553.
  8. Spicer R.L., Uzark K.C., Moore J.W., Mainwaring R.D., Lamberti J.J. Aortopulmonary collateral vessels and prolonged pleural effusions after modified Fontan procedures. Am Heart J 1996;131:1164-1168.[Medline]
  9. Ichikawa H., Yagihara T., Kishimoto H., et al. Extent of aortopulmonary collateral blood flow as a risk factor for Fontan operations. Ann Thorac Surg 1995;59:433-437.[Abstract/Free Full Text]
  10. Gianturco C., Anderson J.H., Wallace S. Mechanical devices for arterial occlusion. Circulation 1975;124:428-435.
  11. De Leval M.R., Kilner P., Gewillig M., Bull C. Total cavopulmonary connection. J Thorac Cardiovasc Surg 1988;96:682-695.[Abstract]
  12. Jonas R.A., Castaneda A.R. Modified Fontan procedure. J Cardiac Surg 1988;3:91-96.[Medline]
  13. Redington A.N., Rigby M.L. Novel uses of the Rashkind ductal umbrella in adults and children with congenital heart disease. Br Heart J 1993;69:47-51.[Abstract/Free Full Text]
  14. Hsu D.T., Quaegebeur J.M., Michler R.E., et al. Heart transplantation in children with congenital heart disease. J Am Coll Cardiol 1995;26:743-749.[Abstract]



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