Ann Thorac Surg 2006;82:1245-1251
© 2006 The Society of Thoracic Surgeons
Original Articles: Cardiovascular
Improving Results of the Fontan Procedure in Patients With Heterotaxy Syndrome
Soo-Jin Kim, MDa,
Woong-Han Kim, MD, PhDb,*,
Hong Gook Lim, MDa,
Chang-Ha Lee, MDa,
Jae Young Lee, MDa
a Department of Pediatric Cardiology and Cardiovascular Surgery, Sejong General Hospital, Bucheon, Korea
b Department of Thoracic and Cardiovascular Surgery, Clinical Research Institute, Seoul National University, College of Medicine, Seoul National University Children's Hospital, Seoul, Korea
Accepted for publication April 24, 2006.
* Address correspondence to Dr Woong-Han Kim, Department of Thoracic & Cardiovascular Surgery, Clinical Research Institute, Seoul National University, College of Medicine, Seoul National University Children's Hospital, 28 Yongon-Dong, Jongno-Gu, Seoul, 110-744 Korea (Email: woonghan{at}snu.ac.kr).
| Pediatric cardiac surgery:
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Abstract
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BACKGROUND: The Fontan operation in patients with heterotaxy syndrome has been associated with a poor prognosis. We studied whether the outcome of those patients with heterotaxy syndrome improved compared with those who did not have the syndrome after an extracardiac Fontan operation.
METHODS: A retrospective review was performed on 185 patients who had undergone an extracardiac Fontan operation between 1996 and 2005.
RESULTS: Sixty-two of the patients had heterotaxy syndrome (33.5%). Forty-one had right isomerism and 21 had left isomerism. Heterotaxy syndrome was commonly associated with a morphologic right ventricle (59.7%), a common atrioventricular valve (72.6%), an interrupted inferior vena cava (25.8%), a separate hepatic vein (30.6%), and extracardiac pulmonary venous drainage (16.1%). The hospital mortality rate was higher in the heterotaxy syndrome than nonheterotaxy (4.8% vs 2.4%; p = 0.05). Eight-year survivals were 91.9 ± 3.2% in the nonheterotaxy group and 89.3 ± 4.2 % in the heterotaxy group (p = 0.39). At 8 years, freedom from reoperation was 90.2 ± 3.2% in the nonheterotaxy group and 78.5 ± 6.2% in the heterotaxy group (p = 0.15). The outcomes (other than those of arrhythmia) were no different between the two groups. The incidences of early and late postoperative arrhythmia were 29.0% and 25.4%, respectively, in heterotaxy patients, and 15.4% and 10.8% in nonheterotaxy patients (p < 0.05). Bradyarrhythmia was found to be more common. During follow-up, atrioventricular valve regurgitation of more than mild was more common in heterotaxy patients (33.9% vs 18.9%; p = 0.05).
CONCLUSIONS: Midterm outcomes after an extracardiac Fontan operation in heterotaxy and nonheterotaxy patients are similar, except arrhythmia and atrioventricular valve regurgitation.
The natural history of patients with a complex congenital cardiac malformation associated heterotaxy and atrial isomerism is poor. And the Fontan procedure remains the preferred palliative procedure for these patients. However, mortality rates remain high for patients with heterotaxy syndrome [1–5]. Factors that have historically been associated with increased operative risk include abnormalities of the systemic venous connection (eg, an interrupted inferior vena cava [IVC] or a bilateral superior vena cava), partial or total anomalous pulmonary venous connection (APVC), a common atrioventricular valve that is incompetent, and a morphologic right ventricle supporting the systemic circulation [6, 7]. In addition, sinus node and conduction system abnormalities are found in virtually all patients with heterotaxy syndrome and may increase the risk of early or late postoperative arrhythmia.
The purpose of this study was to determine and compare the early and midterm outcomes for the extracardiac Fontan operation in patients with and without heterotaxy syndrome.
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Patients and Methods
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Clinical data obtained from the medical records of 62 patients with heterotaxy syndrome who received an extracardiac Fontan operation in Sejong General Hospital between August 1996 and February 2005 were reviewed. These results were compared with identical data obtained from 123 nonheterotaxy syndrome patients who also received an extracardiac Fontan operation during the same period (Table 1). This study was be approved by the Seoul National University Hospital Institutional Review Board, and the individual consent for the study was waived. Patients with heterotaxy syndrome were further classified as having either right isomerism or left isomerism based on reviews of echocardiographic and catheterization reports using the criteria proposed by Van Praagh and colleagues [8].
Right isomerism (asplenia syndrome) was suspected when a patient had a single-ventricle anatomy and one or more of the following types of cardiac defects: (1) juxtaposition of the aorta and IVC, (2) an unroofed coronary sinus, (3) a total APVC to a systemic vein, (4) a common atrioventricular canal, (5) a double-outlet right ventricle or transposition of the great vessels with a bilateral or subaortic conus, and (6) pulmonary valve stenosis or atresia.
Left isomerism (polysplenia syndrome) was suspected when a patient had a single-ventricle anatomy and one or more of the following types of cardiac defect: (1) an interrupted IVC with azygos vein continuation, (2) total or partial APVC to the right atrium, (3) a complete or partial atrioventricular canal, and (4) normally related great vessels or a double-outlet right ventricle without subaortic conus. In all patients, computed tomographic angiography or abdominal sonography, or both, were used to assess the bronchial anatomy and spleen and to confirm a clinical impression of right or left isomerism.
Surgical Technique
Of 62 patients with heterotaxy syndrome, 60 patients had received at least one operation before the Fontan operation. Initial palliative operations included: systemic-to-pulmonary artery shunts (15 patients), pulmonary artery (PA) bandings (3 patients), and PA banding and repair of aortic coarctation (1 patient). The Fontan procedure was preceded by a cavopulmonary anastomosis in 167 patients (90.3%). The single-stage Fontan operation was accomplished in 2 heterotaxy patients and 18 nonheterotaxy patients. In 16 patients with an interrupted IVC, total cavopulmonary anastomosis was performed, leaving only the hepatic veins (Kawashima operation). Before Fontan operations, 11 patients had undergone pulmonary angioplasty, 2 had undergone APVC repair, 1 had undergone a Damus-Kaye-Stansel procedure, 1 had an implantation of a permanent pacemaker, 4 had AV valve repairs, and 1 had an aortic valve replacement. The numbers of prior surgeries were not significantly different between patients with and without heterotaxy syndrome.
An expanded polytetrafluoroethylene tube conduit (Gore-Tex stretch vascular graft, W.L. Gore & Assoc, Flagstaff, AZ) was used throughout. The mean diameter of the conduits used was 18.8 ± 2.3 mm (range, 14.0 to 24.0 mm) in the entire cohort. We chose small-sized grafts (mean, 17.5 ± 2.0 mm; range, 14 to 20 mm) for previous Kawashima procedures. A fenestration was placed in 41.9% patients with a PA pressure of greater than 18 mm Hg or transpulmonary gradient of greater than 10 mm Hg, or both. The fenestration was made with a surgical Gore-Tex tube graft placed between the conduit and the systemic atrium. The fenestration size was from 3.5 mm to 8 mm (median, 4 mm). Fenestration was required less frequently in patients with left isomerism (who were more likely to have pulmonary arteriovenous fistula [PAVF] develop) than in those with right isomerism (p = 0.009), but there was no significant difference in the need for fenestration between patients with and those without heterotaxy syndrome (41.9% and 46.7%, respectively; p = 0.570).
At the time of Fontan operation, 6 patients underwent AV valve repair, 4 underwent PA angioplasty, and 1 underwent an implantation of a permanent pacemaker. Mean cardiopulmonary bypass time was 155.5 ± 57.3 minutes. Of the 185 study subjects, 63 patients (34.1%) needed aortic cross clamping for a mean 22.6 ± 28.5 minutes.
Patients were operated on through a median sternotomy with mild hypothermia and cardiopulmonary bypass. If there was no planned concomitant intracardiac procedure, the procedure was basically performed with a beating heart. If we had to make an atrial septectomy, we transected the IVC and carried out atrial septectomy under temporary ventricular fibrillation.
Perioperative Echocardiography
The degree of AVVR and ventricular function were determined by review of echocardiographic database at our institution. The echocardiography was done by 3 pediatric cardiologists who were blinded to the group. The grade of AVVR was based on the ratio of the color Doppler jet to the area of the atrium [9], and the identification of significant AVVR by echocardiography was compared with that determined at cardiac catheterization.
Diagnosis of Pulmonary Arteriovenous Fistula
Before the Fontan operation, the PAVF was evaluated with a pulmonary angiography, a lung perfusion scan, and a contrast echocardiography, and confirmation was made according to diagnostic criteria as we previously reported [10]. After the Fontan operation, we defined recovery of PAVF with the following criteria: (1) no systemic arterial desaturation of SaO2 more than 90%, and (2) no evidence of intrapulmonary right to left shunt by three diagnostic modalities.
Data are presented as means ± standard deviation or as medians with ranges, as appropriate. Estimated survival and freedom from reoperation were determined by the Kaplan-Meier method based on the product-limit estimator, and 95% confidence intervals were constructed around curves using Greenwood's formula.
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Results
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A total of 62 patients with heterotaxy syndrome (33.5%) underwent an extracardiac Fontan operation. Thirty patients (48.4%) were men and 32 (51.6%) were women. Mean age at Fontan operation was 4.6 ± 2.9 years (range, 1.7 to 12.1 years). The interval between Glenn and Fontan completion was a median of 25 months (range, 10 to 370 months), with a median of 26 months (range, 8 to 134 months) in the heterotaxy group and a median of 25 months (range, 10 to 370 months) in nonheterotaxy group. Forty-one of these 62 patients (66.1%) had asplenia syndrome or right atrial isomerism, and 21 patients (33.9%) had polysplenia syndrome or a left atrial isomerism.
Morphologies of atrioventricular valves and ventricles are described in Table 2. Right atrial isomerism and a functional single right ventricle were the most common (59.7%). There was a common atrioventricular valve in 45 patients (72.6%), and most of these patients had an unbalanced opening into the morphologic right ventricle. Right isomerism was more commonly associated with a common atrioventricular valve and a morphologic right ventricle supporting the systemic circulation than the left isomerism, although this did not reach statistical significance (p = 0.053 and p = 0.051, respectively).
Systemic and pulmonary venous anomalies are described in Table 3. Left isomerism was more commonly associated with a contralateral superior vena cava and an interrupted IVC than the right isomerism. The presence of an extracardiac pulmonary venous drainage impacting the establishment of a Fontan circulation was observed in 10 patients (16.1 %), and all had APVC of the supracardiac type.
In patients with heterotaxy syndrome, the preoperative mean PA pressure was 12.9 ± 3.3 mm Hg (range, 5.0 to 21.0 mm Hg), mean pulmonary vascular resistance was 1.5 ± 0.7 Wood units (range, 0.6 to 3.3), and the mean transpulmonary gradient was 4.8 ± 1.9 mm Hg (range, 1.0 to 10.0 mm Hg). These data were not significantly different from those of the nonheterotaxy patients.
No significant differences were observed in postoperative hemodynamic data, such as PA pressure, urine output, mechanical ventilator support, median stay in ICU, median hospital stay, median duration of the chest tube between patients with or without heterotaxy syndrome.
Mortality and Risk Factors for Death
The hospital mortality rate was 4.8% (n = 3) in patients with heterotaxy syndrome and 2.4% (n = 3) in those with nonheterotaxy (p = 0.05; 
2 test). Mortality cases are detailed in Table 4. In patients with heterotaxy syndrome, there were 3 late deaths (5.1%) with a follow-up duration of 48.4 ± 31.2 months (range, 2.9 to 102.7), and in patients with nonheterotaxy there were 4 late deaths (3.3%) with a follow-up duration of 40.2 ± 29.8 months (range, 0.3 to 105.3). In patients with heterotaxy syndrome, the 1-year and 8-year survivals were 91.5 ± 3.7% and 89.3 ± 4.2%, respectively, and in patients with nonheterotaxy syndrome the 1-year and 8-year survivals were 96.7 ± 1.7% and 91.9 ± 3.2%, respectively. No significant difference was observed between the two groups in terms of survival (p = 0.39, log rank test) (Fig 1). The 8-year survival was 90.5 ± 6.4% for left isomerism and 88.6 ± 5.4% for right isomerism (p = 0.94).
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Fig 1. Kaplan-Meier curve of cumulative survival. The dotted line indicates survival for patients with heterotaxy syndrome; the solid line indicates patients without heterotaxy syndrome.
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Univariate analysis indicated that infection during the early postoperative period (p = 0.0001), protein losing enteropathy after Fontan operation (p = 0.008), high preoperative ventricular end-diastolic pressure (p = 0.019), and high central venous pressure during the early postoperative period (p = 0.004) were significant risk factors of mortality. Multivariate analysis identified severe infection during the early postoperative period (hazard ratio, 17.502; p = 0.0001), protein losing enteropathy after the Fontan operation (hazard ratio, 5.691; p = 0.041), and high central venous pressure during the early postoperative period (hazard ratio, 10.367; p = 0.002) as risk factors of mortality (Table 5). Neither the presence of heterotaxy syndrome nor preoperative hemodynamic data were found to be significantly associated with mortality.
Reoperations
In total there were 29 reoperations in 19 patients. Sixteen reoperations in 10 patients with heterotaxy syndrome and 13 reoperations in 9 patients without heterotaxy syndrome (Table 6). Eight reoperations were conducted in 6 patients with right isomerism and 8 reoperations in 4 patients with left isomerism. Actuarial freedom from reoperation at 8 years was 78.5 ± 6.2% for patients with heterotaxy and 90.2 ± 3.2% for patients without heterotaxy (Fig 2). There was a tendency for more reoperations in patients with heterotaxy, but this did not reach significance (p = 0.15, log rank test). Actuarial freedom from reoperation at 8 years was 73.9 ± 11.3% for those with left isomerism and 82.3 ± 6.7% for those with right isomerism, which was not significant (p = 0.87, log rank test). However, there was a tendency toward more pacemaker implantations for sick sinus syndrome and toward more reoperations due to pulmonary arteriovenous fistulae in those with left isomerism.
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Fig 2. Kaplan-Meier curve of freedom from reoperation. The dotted line indicates survival for patients with heterotaxy syndrome; the solid line indicates patients without heterotaxy syndrome.
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Postoperative Arrhythmia
In heterotaxy syndrome, 18 patients (29.0%) had early postoperative arrhythmias develop. In 10 children, sinus node dysfunction was present (as characterized by relative bradycardia or the presence of a junctional rhythm), atrioventricular conduction block had developed in 3, and supraventricular arrhythmia was present in 5. During the early postoperative period, patients with heterotaxy syndrome were more likely to have early postoperative arrhythmia develop than those without heterotaxy (29.0% vs 15.4%; p = 0.03; 2 test). Moreover, patients with left isomerism were more likely to have bradyarrhythmia develop than those with right atrial isomerism (38.1% vs 12.2%; p = 0.049; 2 test). During follow-up, arrhythmia was documented in 15 of the surviving patients (25.4%) with heterotaxy syndrome and in 13 of the patients (10.8%) without, and the incidence of arrhythmia was more common in patients with heterotaxy syndrome (p = 0.012; 2 test). Of the 15 heterotaxy syndrome patients that had late arrhythmia develop, 86.7% (13 patients) had bradyarrhythmia develop, and 13.3% (2 patients) had tachyarrhythmia develop. No significant difference between right and left isomerism was observed in terms of arrhythmia incidence, but severe bradyarrhythmia requiring the implantation of a permanent pacemaker was more common in those with left isomerism (n = 5; 3 after Fontan, 2 before Fontan; 27.3%) than in those with right isomerism (n = 2; all before Fontan; 5.3%) (p = 0.030; 2 test).
Other Postoperative Complications During Follow-Up
Two patients (3.2%) with heterotaxy and 3 patients (2.4%) without heterotaxy had protein-losing enteropathy develop. Interestingly, both heterotaxy patients died and the 3 nonheterotaxy patients improved after medical treatment [11]. The incidence of thromboembolism was 9.7% in the patients with heterotaxy syndrome and 6.5% in the patients without (p = 0.763).
Before the Fontan operation, 13 heterotaxy patients (21.0%) had a PAVF develop, but no nonheterotaxy patient had this condition develop. The incidence of PAVF before Fontan completion was more common in those with left isomerism than in those with right isomerism (52.4% and 4.9%, respectively; p = 0.001).
Most patients (69.2%; 9 of 13) recovered, but 4 patients (30.8%; 4 of 13) with left isomerism had persistent hypoxia over a mean follow-up of 50.6 ± 30.7 months (range, 1.4 to 102.7) after the Fontan operation. Of these, two underwent reoperation to provide an even distribution of hepatic blood flow to both lungs, requiring the division of the previous conduit between hepatic veins and the pulmonary artery and anastomosis between hepatic veins and the azygous vein.
Atrioventricular Valve and Ventricular Function
Figure 3
shows change in the grades of atrioventricular valve regurgitation. A significant decrease in the degree of regurgitation from 0.77 ± 0.74 to 0.62 ± 0.62 occurred after the Fontan operation in the nonheterotaxy syndrome patients (p = 0.023), and a slight decrease from 0.97 ± 0.82 to 0.84 ± 0.59 occurred in the heterotaxy syndrome patients (total p = 0.164; in left isomerism, p = 0.357; in right isomerism, p = 0.305). However, in those patients without heterotaxy, a significant increase in atrioventricular valve regurgitation grades was observed; from 0.62 ± 0.62 to 0.87 ± 0.78 (p = 0.0001) during a follow-up of 28.5 ± 26.1 months (range, 0.2 to 99.9) after the Fontan operation, and correspondingly in heterotaxy syndrome patients from 0.84 ± 0.59 to 1.15 ± 0.63 (p = 0.0001) during a follow-up of 35.9 ± 29.0 months (range, 0.1 to 98.3). At the most recent follow-up, 19 heterotaxy patients (33.9%) had at least mild atrioventricular valve regurgitation, and 22 nonheterotaxy patients (18.9%) (p = 0.05).
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Fig 3. Atrioventricular valve regurgitation grades before and after Fontan operation. (AVVR = atrioventricular valve regurgitation; Last F/U = mean grades of AVVR at last follow-up; PreFontan = mean grades of AVVR before Fontan operation; PostFontan = mean grades of AVVR immediately after Fontan operation.) (A) Open box represents nonheterotaxy; closed box represents heterotaxy. (B) Open box represents left isomerism; closed box represents right isomerism.
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Echocardiographic evaluations showed a qualitatively depressed ventricular function in 5 patients (8.9%) with heterotaxy syndrome (1 with left isomerism and 4 with right isomerism) and in 14 patients (12.1%) without heterotaxy syndrome. The remaining patients had a good qualitative ventricular function.
New York Heart Association's Functional Class at Last Follow-up
Follow-up information on functional status was available for 54 patients (96.4%) with heterotaxy; 94.4% (51 of 54) met the criteria for the New York Heart Association's functional class I, and 5.6% (3 of 54) met the criteria for functional class II. In 113 patients (97.4%) without heterotaxy syndrome, 92.9% (105 of 113) were in class I, 6.2% (7 of 113) were in class II, and 0.9% (1 of 113) were in class III.
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Comment
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Despite the improved outcome of the Fontan operation, previous reports on the overall outcome of children with heterotaxy syndrome have generally shown a poor prognosis [1–5]. Mortality of the Fontan operation in heterotaxy syndrome has been reported to range from 0% to 69%, although an improvement over time has been noted [3, 5, 12–14]. According to our recent experience of 62 patients with heterotaxy syndrome, in-hospital mortality for the extracardiac Fontan operation was 4.8%, and late mortality 5.1%, over a mean follow-up of 48.4 months. In the present study, the in-hospital mortality of patients with heterotaxy syndrome was found to be higher than that of those without (2.4% vs 4.8%; p = 0.05). However, Kaplan-Meier survival at 8-years was 89.3% for patients with heterotaxy syndrome, which was comparable with that of those without (91.9%; p < 0.05; log rank test). Risk factors for death identified by multivariate analysis included perioperative infection, protein losing enteropathy, and a high central venous pressure after Fontan operation.
Of the many associated malformations found in heterotaxy syndrome with a univentricular heart, an APVC is considered to be the important risk factor in terms of mortality. To deal with this problem, the extracardiac Fontan procedure is an option for direction of IVC or hepatic venous drainage to the pulmonary arteries [15]; moreover, this modification can produce marked improvements [13, 14]. Our patient population is noteworthy because of a relatively large number of heterotaxy syndrome patients (33.5%) that were treated by extracardiac Fontan.
Despite the good results quoted by recent studies, the incidence of early postoperative arrhythmia remains high (at up to 47%), as is the incidence of late postoperative arrhythmia, with freedom from late bradyarrhythmia and tachyarrhythmia at 78% and 70%, respectively [14]. The types of Fontan modifications used in previous studies vary: classic Glenn procedure; atriopulmonary connection; lateral tunneling procedure; and extracardiac Fontan operation. One study [16] indicated that extracardiac Fontan modifications effectively preserve sinus node function. In our current study, early postoperative arrhythmia and late arrhythmia incidences were relatively low (ie, 29.0% and 25.4%, respectively), as compared with previous reports. In particular, the incidence of tachyarrhythmia was rare in the present study. Although no clear cause and effect relationship can be proven from the data obtained during this retrospective study, our study suggests that extracardiac Fontan modification reduces the incidence of postoperative arrhythmia and especially of tachyarrhythmia. However, early postoperative arrhythmia and late arrhythmia were found to be more common in patients with heterotaxy syndrome. In particular, 86.7% of arrhythmias were bradyarrhythmia in those with heterotaxy, and severe bradyarrhythmia requiring permanent pacemaker implantation was more common in those with left isomerism (p = 0.030).
The importance of treating concomitant malformations before or at the time of the Fontan operation has been frequently emphasized [7, 13, 14]. It has been reported that the risk factors of the Fontan operation in this group are atrioventricular valve regurgitation, hypoplastic pulmonary arteries, and a mean pulmonary artery pressure of greater than 15 mm Hg [7]. We tried to correct associated malformations aggressively and to reduce risk factors before and at the time of Fontan operations. Thus we performed atrioventricular valve repair in 23 patients, pulmonary artery angioplasty in 45, total anomalous venous drainage repair in 3, and implantation of a permanent pacemaker in 5 for sinus node dysfunction before and at the time of the Fontan operations.
Pulmonary arteriovenous fistula is a risk factor of mortality and morbidity in heterotaxy syndrome, and especially in cases with left isomerism with an interrupted IVC. We previously reported that 70% had PAVF develop subclinically or clinically after bidirectional cavopulmonary anastomosis in all patients with functional single ventricles [10]. In the present study, 21.0% had clinical PAVF develop after bidirectional cavopulmonary anastomosis, and most of these recovered after Fontan completion. However, 4 patients did not completely recover, because putatively, hepatic blood flow did not provide a balanced distribution to both lung beds, and showed persistent PAVF despite Fontan completion. Two patients with severe hypoxia underwent takedown of a previous hepatic vein-pulmonary artery conduit and of a hepatic vein-azygos vein anastomosis.
Progressive deteriorations in atrioventricular valve competency and systemic ventricular function were observed in some patients after the Fontan operation. This may have been caused by a functional single right ventricle and a common atrioventricular valve or tricuspid valve, or both, supporting the systemic circulation. Close follow-up of these patients may be needed.
Reoperations were more frequent in those with heterotaxy during follow-up. These included revision for conduit stenosis, atrioventricular valve repair, hepatic vein inclusion for residual right-to-left shunt, permanent pacemaker implantation, and rerouting of hepatic flow for persistent PAVF.
In conclusion, the extracardiac Fontan operation can now be performed in patients with heterotaxy syndrome with good early results. However, the Fontan operation in those with heterotaxy syndrome may yet be associated with long-term morbidity.
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References
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Abstract
Introduction
