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Eur J Cardiothorac Surg 2006;30:923-929
© 2006 Elsevier Science NL

Clinical outcome of patients 20 years after Fontan operation — effect of fenestration on late morbidity

Masamichi Onoa,*, Dietmar Boethigb, Heidi Goerlera, Melanie Langea, Mechthild Westhoff-Bleckc, Thomas Breymanna

a Division of Thoracic and Cardiovascular Surgery, Hannover Medical School, Hannover, Germany
b Division of Pediatric Cardiology and Intensive Care Medicine, Hannover Medical School, Hannover, Germany
c Division of Cardiology, Hannover Medical School, Hannover, Germany

Received 27 March 2006; received in revised form 6 August 2006; accepted 14 August 2006.

* Corresponding author. Address: Division of Thoracic and Cardiovascular Surgery, Hannover Medical School, Carl-Neuberg-Str. 1, 30625 Hannover, Germany. Tel.: +49 511 532 9397; fax: +49 511 532 9832. (Email: Ono.Masamichi{at}MH-Hannover.DE).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objective: The Fontan operation has been proposed as definitive palliation for an increasing variety of hearts with complex univentricular anatomy, but late morbidity after Fontan operation is still a matter of concern. This retrospective study evaluates the late outcome in patients with Fontan circulation. Methods: We included 121 consecutive patients that underwent Fontan operation between 1984 and 2004. Modifications of the Fontan operation included atriopulmonary anastomosis (APA; n = 28), total cavopulmonary connection (TCPC; n = 63), and fenestrated TCPC (f-TCPC; n = 30). Mean age was 5.8 ± 5.5 years. Post operative mortality, morbidity, hemodynamics, and somatic development were analyzed. Results: Actuarial survival was 87% at 20 years after Fontan operation. There were 10 early deaths, 5 late deaths, and 2 takedowns followed by successful conversion and heart transplantation. Among 108 early-survivors with Fontan circulation, 19 underwent reoperation, including 3 conversions of APA to TCPC. Freedom from reoperation was 76% at 20 years. Freedom from intervention was 34% at 20 years. Freedom from tachyarrhythmia or pacemaker implantation was 23% and 77%, respectively at 20 years. Heterotaxy and atrioventricular valve anomaly were risk factors for late failure and tachyarrhythmias. Patients with fenestrated TCPC had reduced incidence of late tachyarrhythmias, and patients with APA who developed collaterals showed low incidence of late tachyarrythmia. Postoperative sinus node dysfunction or tachyarrhythmias was associated with significantly lower cardiac index. Somatic development was gradually compensated after Fontan operation. Weight normalized completely 15 years postoperatively. Conclusions: Long-term survival after Fontan procedure is encouraging, but late morbidity remains suboptimal. During follow-up, emerging complications should be managed by surgical and interventional procedures. Fenestration in Fontan circulation provided better cardiac output and lower incidence of late tachyarrhythmias, suggesting a benefit of fenestration for late outcome.

Key Words: Fontan procedure • Fenestration • Tachyarrhythmia


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
The Fontan operation was first performed in patients with tricuspid atresia as a functional repair [1]. Modifications of the Fontan procedure and staging with bidirectional cavopulmonary shunt have extended the indications for this operation now applied to a wide range of congenital heart defects unsuitable for biventricular repair [2,3]. Furthermore, creation of fenestration in Fontan pathway reduces early mortality and morbidity even in high-risk patients for Fontan completion [4]. Despite the improvements in surgical techniques that reduce perioperative mortality [5–7], late deterioration in functional status can be observed with longer duration of follow-up [8–10]. Late morbidity is mainly defined by pathway obstruction [11], atrial arrhythmia [12–14], and cyanosis because of systemic venous collateralization [15], thrombus formation [16], protein-losing enteropathy [17], and pulmonary arteriovenous malformations [18]. Postoperative morbidity with the need of hospitalization also includes surgical and catheter-based re-interventions. Somatic growth failure was documented after Fontan operation [19].

The reason why these various morbidities occur in time-dependent manner after Fontan operation is still unclear. Francis Fontan himself [8] stated that this operation has a palliative nature in itself. A recent study demonstrated the evidence of progression of pulmonary vascular disease [20] in patients with failing Fontan circulation. Neurohormonal abnormalities [21,22] and pulmonary endothelial dysfunction [23] are also reported in patients late after Fontan operation. These findings suggest underlying mechanisms in the pulmonary circulation that induce late morbidities after Fontan operation.

In this retrospective study, we evaluated late mortality, late morbidity, postoperative hemodynamics, and somatic development during long-term follow-up after Fontan-type operations.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 Appendix A
 References
 
2.1 Patients
Between 1984 and 2004, 121 patients with functionally univentricular hearts underwent Fontan-type procedures at our institution. Patients’ characteristics are shown in Table 1 . Balloon atrial septostomy has been performed in 11 patients. In our institute, bidirectional Glenn shunts were introduced in 1989 and performed in high-risk patients for Fontan operation. Since 1997, bidirectional Glenn shunts has been performed in all patients prior to Fontan completion. Mean age at the time of bidirectional Glenn shunt was 1.8 ± 1.5 years, and mean period prior to Fontan completion was 1.3 ± 0.6 years.


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  		Table 1. Patients characteristics (n = 12l)
 
Mean age at Fontan operation was 5.8 ± 5.5 years, ranging from 0.6 to 32 years. There were 20 patients who underwent Fontan procedure at the age of 10 or older. Seventeen of 20 patients were operated before 1994. The main cause was late referral from other institutions. Modifications of the Fontan operation included atriopulmonary anastomosis (APA; n = 28), total cavopulmonary connection (TCPC; n = 63), and fenestrated TCPC (f-TCPC; n = 30). Concomitant procedures were tricuspid valve closure in six patients, mitral valve closure in two, atrioventricular valve plasty in two, left ventricular outflow tract obstruction relief in seven, repair of total anomalous pulmonary venous return in one, and pulmonary artery reconstruction in three patients.

2.2 Surgical procedures
APA was performed by connection of the atrial appendage to the main pulmonary artery. In three patients, a homograft was inserted between the atrial appendage and main pulmonary artery, and in the others APA was performed by direct anastomosis. TCPC was performed as lateral tunnel technique, described by de Leval et al. [2]. As for the material for atrial patch, pericardium or Gore-tex patches were used. Fenestrations were created using a 4 mm diameter punch. Only one patient underwent extracardiac TCPC using a Gore-tex tube graft.

2.3 Data collection and analysis
Pre- and postoperative data were collected from patients’ records of Hannover Medical School. For patients followed elsewhere, data were collected by fax transmission. Postoperative hemodynamic data were collected from cardiac catheterization reports. Somatic development after Fontan procedure was investigated using weight and height gain related to standardized percentiles. These parameters were evaluated preoperatively and 1, 2, 5, 7, 10, 12, and 15 years postoperatively, and expressed in percentiles. Late mortality and late morbidity was evaluated using the Kaplan–Meier method.

2.4 Statistical analysis
Values are expressed as mean ± standard deviation. Data were analyzed using SPSS statistical software (SPSS Inc., Chicago, IL). Estimated actuarial survival and freedom from late morbidities were determined by the Kaplan–Meier method and analyzed with the log-rank test. Multivariate risk analysis was performed with Cox regression test. A value of p < 0.05 was considered to be statistically significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 Appendix A
 References
 
3.1 Mortality and late Fontan failure
Ten patients died within the first 30 postoperative days (early death): causes of death were low output syndrome in eight, intractable atrial tachycardia in one and intrapulmonary bleeding in one. There were five late deaths: one patient died 1 month after operation because of sepsis and massive pleural effusion. Two patients died of low output syndrome 2 and 5 months after the operation. Two patients with heterotaxy syndrome died 29 and 66 months postoperatively because of multi-organ failure and sudden death at home. Two patients underwent Fontan takedown 4 and 30 months after Fontan operation, both of them are alive and doing well: in one patient extra-cardiac TCPC was performed 6 years after takedown, in the other received heart transplantation 6 years after takedown. Overall survival in Fontan circulation was 87% at 20 years after Fontan operation (Fig. 1A). Actuarial survival in patients with APA was 75% at 10 years, which was significantly lower than that of TCPC (90%) and f-TCPC (90%) (p = 0.04) (Fig. 1B).


Figure 1
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  		Fig. 1. Estimated probability of survival after Fontan procedure. Survival curves are demonstrated for all patients (A) and in each type of Fontan procedure (B). APA, atrio pulmonary anastomosis; TCPC, total cavopulmonary connection; f-TCPC, fenestrated total cavopulmonary connection.

 
3.2 Late morbidities
Focusing on the late events and risk analysis, postoperative long-term morbidity was evaluated using 108 patients who survived more than 6 months in Fontan circulation (excluding 10 early deaths and 3 hospital deaths). The follow-up period was 10.9 ± 5.2 years. At the time of their last visit, 100 patients were in NYHA class I and 8 were in NYHA class II.

3.2.1 Reoperations
Nineteen patients (16%) underwent reoperations, including conversion from APA to TCPC in three, pericardectomy in six, relief of left ventricular outflow tract obstruction in three, pulmonary artery reconstruction in two, tricuspid valve closure in two, homograft explantation between atrial appendage and pulmonary artery in one, aortic valve replacement in one, and atrial patch revision in two. All patients survived reoperations. Overall freedom from reoperation was 76% at 20 years. Freedom from reoperation at 10 years was 67% in APA, 86% in TCPC, and 92% in f-TCPC. The differences were not statistically significant between the types of Fontan procedure (Fig. 2A).


Figure 2
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  		Fig. 2. Estimated probabilities of freedom from reoperation (A), intervention (B), tachyarrhythmia (C), and pacemaker implantation (D) in each type of Fontan procedure. APA, atrio pulmonary anastomosis; TCPC, total cavopulmonary connection; f-TCPC, fenestrated total cavopulmonary connection.

 
3.2.2 Catheter interventions
Thirty-four patients (31%) required the following catheter interventions: 16 catheter ablations, 11 fenestration closures, 9 veno-venous collateral closures, 8 arterio-venous collateral closures, 6 balloon dilatations of pulmonary artery, 2 stent implantations in the pulmonary artery, 1 fenestration creation, and 1 closure of persistent left superior vena cava. Freedom from intervention was 34% at 20 years. Freedom from intervention at 10 years was 63% in APA, 77% in TCPC, and 49% in f-TCPC. The differences were not statistically significant between the types of Fontan procedure (Fig. 2B).

3.2.3 Tachyarrhythmia
Tachyarrhythmia occurred in 40 patients, atrial flutter or fibrillation in 15, supraventricular tachycardia in 26, and ventricular fibrillation in 4. Two patients required Implantable Cardioverter Defibrillation (ICD) implantation. Freedom from tachyarrhythmia after Fontan operation was 23% at 20 years. Freedom from tachyarrhythmia at 10 years was 76% in APA, 66% in TCPC, and 90% in f-TCPC. Patients who underwent fenestrated TCPC showed lower incidence of late tachyarrhythmia (Fig. 2C). Interestingly, among 21 late survivors in APA, patients who developed collateral formation had a low incidence of tachyarrhythmia (1 of 6), compared with those who did not (10 of 15) (Fig. 3 ). This difference is statistically significant (p = 0.03). In long-term follow up, patients with collateral formation showed lower mean pulmonary artery pressure (10.5 ± 2.8 mmHg) and smaller inferior vena cava diameter (1.7 ± 0.3 cm) than those without collateral formation (12.2 ± 2.7 mmHg and 2.1 ± 0.4 cm), but these values were not significantly different (p = 0.24 and p = 0.19, respectively).


Figure 3
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  		Fig. 3. Estimated probabilities of freedom from tachyarrhythmia in patients with atriopulmonary anastomosis.

 
3.2.4 Bradyarrhythmia
Bradyarrhythmia occurred in 27 patients, 20 of which underwent pacemaker implantation. Freedom from pacemaker implantation was 80% at 10 years and 77% at 20 years. Freedom from pacemaker implantation at 10 years was 76% in APA, 82% in TCPC, and 89% in f-TCPC. There was no significant difference between the types of Fontan procedure (Fig. 2D).

3.3 Other morbidities or observations
Thromboembolic complications occurred in 11 patients, 3 patients developed protein losing enteropathy. Pulmonary arteriovenous malformations occurred in 2 patients. Collateral formation occurred in 21 cases including arterio-venous collaterals in 18 and veno-venous collaterals in 15 patients.

3.4 Risk factor analysis for late failure and late morbidities
Univariate and multivariate analysis have been performed to find risk factors for late Fontan failure and late morbidity. Univariate analysis showed that heterotaxy was a risk factor for late Fontan failure and late tachyarrhythmia. Atrioventricular regurgitation was a risk factor for late Fontan failure and late intervention. Palliative procedures, perioperative variables, or age at Fontan operation were not risk factors for late mortality or late morbidity (Table 2 ).


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  		Table 2. Risk factor analyses for late Fontan failure and morbidities (n = 108)
 
3.5 Postoperative hemodynamics
Postoperative hemodynamics were evaluated by cardiac catheterization in 89 patients for 200 times at our institute. Mean follow-up after Fontan completion was 66.0 ± 40.0 (6–184) months. Arterial oxygen saturation (SaO2), Cardiac Index (CI), mean pulmonary artery pressure (mPAP), and end-diastolic pressure of the systemic ventricle (SVEDP) were evaluated in each type of Fontan procedure. In patients after fenestrated TCPC, SaO2 was significantly lower compared with APA and TCPA, but CI was significantly higher than that of other procedures. Average mPAP and SVEDP were not significantly different between the types of procedure.

Univariate analysis showed that previous postoperative sinus node dysfunction and tachyarrhythmia were risk factors for a lower cardiac index. Patients who received coarctation repair and pulmonary artery banding were also at risk for higher mean pulmonary artery pressure after Fontan completion (Table 3 ).


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  		Table 3. Post-operative hemodynamics (n = 89)
 
3.6 Somatic development
Before undergoing the Fontan procedure, the patients ranged between the 20th and 30th percentile. After the Fontan procedure, somatic development was compensated concerning both weight and height gain. Weight normalized completely 15 years after Fontan operation (Fig. 4A), but height did not reach average normal level even 15 years postoperatively (Fig. 4B).


Figure 4
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  		Fig. 4. Somatic development after Fontan procedure. Weight (A) and height (B) gain pre Fontan and post Fontan operation. Parameters are shown in percentiles (normal; 50%) before and 1, 2, 5, 7, 10, 12, 15 years after Fontan operation. Data are expressed as mean ± standard error.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
Appendix A
 References
 
After 20 years of follow-up, the number of late deaths is limited and survival is satisfactory, but there is a relevant late morbidity to be observed after Fontan procedure. Considerable late morbidities have been demonstrated clearly for the atriopulmonary types of Fontan circulation. After introduction of the modifications of the Fontan procedure, the incidence of morbidities has tended to decrease, but this remains to be defined for more recent modifications.

The main findings of this study are: patients after fenestrated TCPC showed significantly lower incidence of late tachyarrhythmias, and patients after atriopulmonary anastomosis that developed collaterals showed lower mean pulmonary artery pressures, smaller venous pathway diameters, and a significantly lower incidence of late tachyarrhythmias than those who did not develop collaterals. Furthermore, patients that underwent fenestrated TCPC demonstrated a higher cardiac index than other types of Fontan procedure, and patients who developed late tachyarrhythmias showed a significantly lower cardiac index. These results demonstrate the importance of prepulmonary venous decompression by increased fenestration shunting particularly under exercise load to prevent late onset of tachyarrhythmias. A possible explanation for lower incidence of late tachyarrhythmias of fenestrated patients could be: an adequate shunt volume into the systemic ventricle, which bypasses the pulmonary circulation, contributes to maintain cardiac output, and prevents the heart from dilatation by avoiding extensive prepulmonary venous load under exercise.

These findings also implicate the latent progression of pulmonary vascular disease after Fontan operation. As it is difficult to access pulmonary vascular resistance after Fontan procedure directly, Mitchell et al. [20] demonstrated the evidence of progression of pulmonary vascular disease in patients with heart transplantation after Fontan failure. Although it seems experimentally [24] and clinically [2] proven that pulsatility is not necessary for pulmonary circulation in Fontan circuit and sinus rhythm is important for maintaining systemic ventricular function, long term nonpulsatile flow of pulmonary circulation itself induces neurohormonal abnormality [21,22] causing pulmonary vascular remodeling late after cavopulmonary shunt. These changes may progress very slowly, but are likely to have unavoidable impact on Fontan circulation several years postoperatively leading to late complications.

The concept of baffle fenestration of the Fontan operation was introduced by Bridges et al. [4] to decrease operative mortality for high-risk Fontan candidates. Nowadays, this modification has been widely accepted and contributed to improve short-term outcome even in standard-risk patients [7]. However, long-term effects of baffle fenestration are not clear. The necessity, proper timing, and clinical benefit of fenestration closure remain unknown. Goff et al. [25] described improved oxygenation and reduced need for anticongestive medication, but an increase in use of antiarrhythmics during a mean follow-up of 3.4 years after fenestration closure.

In this study, similar to the previous reports [12–14], tachyarrhythmia continues to develop with time in patients with atriopulmonary anastomosis and nonfenestrated TCPC. In this context, fenestration closure, which establishes complete separation of pulmonary and systemic circulation, may contribute to late tachyarrhythmias, even when this procedure is performed several years after Fontan operation. Because of the beneficial long-term effect of fenestration, the indication for fenestration closure should be reconsidered at least for some cohort of patients with single ventricle physiology after Fontan completion despite the risk of thoromboembolism. As for somatic development after Fontan operation, there is no significant difference between fenestrated TCPC and the other procedures.

As for bidirectional Glenn shunt, it was introduced in 1989 and was performed for selected patients until 1997, then it has been routinely performed before Fontan completion. Among 31 patients, there were no hospital deaths at the time of Fontan procedure, but 2 patients died 78 and 180 days after Fontan completion because of cardiac dysfunction, which made no statistical difference for late mortality. In our overall risk analysis, bidirectional Glenn shunt showed no beneficial effect on late morbidity. Explanation may be the increased preoperative risks for Fontan procedure in this cohort. The beneficial effects of this shunt on late morbidity should be addressed using case matched studies in future.

The limitation of this study analysis is that this study is hypothesis-generating only and that significances do not mean that a difference was proven.

In summary, long-term survival after Fontan procedure is satisfactory, but late morbidity remains suboptimal. During the follow-up, cumulative occurrence of late complications can and should be managed by surgical and medical interventions. Fenestration in Fontan circuit provided better cardiac output and lower incidence of late tachyarrhythmia, suggesting a benefit of fenestration for late outcome.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
References
 
Conference discussion

Dr R. Jonas (Washington, DC, USA): Can you tell us how you defined collaterals, and whether you quantitated the hemodynamic impact of those collaterals? That's one question.

Also, do you think it's important that the fenestration remain patent long term or is it simply an early effect? And if you think long-term patency is important, how did you measure that? What are your thoughts about device closure of a fenestration?

Dr Ono: A fenestrated Fontan was done in 30 patients. There were about 60 patients in our study group. It is not so gross number.

About 10 patients, the fenestration is closed spontaneously, or it was catheter closure in 5 or 6 patients. These patients also did not develop the late tachyarrhythmias until now. Though we analyze the efficacy or the hemodynamic change of effect of closure of fenestration, but it's not significantly different in our small number of our study.

In my opinion, though, I think Goff et al., had reported long-term results after catheter closure after fenestration in Circulation 2000. They said that the hemodynamics change significantly because of saturation, but though small risk of medication for antiarrhythmic drugs. So I think after closure of fenestration that these risks for tachyarrhythmias for late phase may occur after long term after Fontan circulation.

Dr Jonas: What about the collaterals?

Dr Vouhe (Paris, France): Yes, what about the collaterals? What is your definition of collaterals?

Dr Ono: Collaterals were defined by cardiac catheterization.

Dr Vouhe: Yes, but how do you quantify the collateral circulation?

Dr Ono: These are cardiac catheterization results, no? That defines the collateral formation. This is our definition, not clear for me.

Dr G. Ziemer (Tuebingen, Germany): Actually, I’ve operated about 80% of these patients when I was in Hannover, so, Richard, I may answer you.

We did not have the occlusion devices available in the early ’90s when we started the fenestrations. It obviously was invented in Boston, and I picked it up right away. We started with smaller holes and hoped that they would close on their own. Therefore we usually used the 2.8 punch in the beginning, and only in larger patients, who in the early ’90s were not too many anymore, as we operated then already our Fontan candidates before 3 years of age.

What I would be interested in, Dr Ono, is the impact of the Glenn stage. We had the feeling at the beginning that those patients who got the Glenn in the staging process, did worse by means of tachyarrhythmias early postoperatively. So do you have an idea whether late postoperatively there is a difference between those patients who had a Glenn stage and who did not have a Glenn stage as far as rhythm problems are concerned?

Dr Ono: Our bidirectional Glenn shunt had no effect, or a beneficial effect, for late tachyarrhythmia. But fenestration had a significantly lower incidence for late tachyarrhythmia.


   Acknowledgments
 
This study was supported in parts by Grant from The Uehara Memorial Foundation and The Mochida Memorial Foundation for Medical and Pharmaceutical Research. The authors thank Dr Hikaru Matsuda, Professor emeritus, Osaka University Graduate School of medicine, for his arrangement of this research work.


   Footnotes
 
\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 

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S. Kim, O. Al-Radi, M. K. Friedberg, C. A. Caldarone, J. G. Coles, E. Oechslin, W. G. Williams, and G. S. Van Arsdell
Superior vena cava to pulmonary artery anastomosis as an adjunct to biventricular repair: 38-year follow-up.
Ann. Thorac. Surg., May 1, 2009; 87(5): 1475 - 1482.
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F. Kerendi, Z. B. Kramer, W. T. Mahle, B. E. Kogon, K. R. Kanter, and P. M. Kirshbom
Perioperative risks and outcomes of atrioventricular valve surgery in conjunction with Fontan procedure.
Ann. Thorac. Surg., May 1, 2009; 87(5): 1484 - 1488.
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 CirculationHome page
P. Khairy, S. M. Fernandes, J. E. Mayer Jr, J. K. Triedman, E. P. Walsh, J. E. Lock, and M. J. Landzberg
Long-Term Survival, Modes of Death, and Predictors of Mortality in Patients With Fontan Surgery
Circulation, January 1, 2008; 117(1): 85 - 92.
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 J. Thorac. Cardiovasc. Surg.Home page
M. Ono, D. Boethig, H. Goerler, M. Lange, M. Westhoff-Bleck, and T. Breymann
Somatic development long after the Fontan operation: factors influencing catch-up growth.
J. Thorac. Cardiovasc. Surg., November 1, 2007; 134(5): 1199 - 1206.
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 Eur. J. Cardiothorac. Surg.Home page
I. Adachi, T. Yagihara, K. Kagisaki, I. Hagino, T. Ishizaka, J. Kobayashi, S. Kitamura, and H. Uemura
Preoperative small pulmonary artery did not affect the midterm results of Fontan operation
Eur. J. Cardiothorac. Surg., July 1, 2007; 32(1): 156 - 162.
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