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Ann Thorac Surg 2005;80:37-43
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Seven-Year Clinical Experience With the Extracardiac Pedicled Pericardial Fontan Operation

Minoo N. Kavarana, MDa,*, Sebastian Pagni, MDa, Michael R. Recto, MDb, Walter L. Sobczyk, MDb, Thomas Yeh, Jr, MD, PhDc, Michael Mitchell, MDa, Erle H. Austin, III, MDa

a Division of Thoracic and Cardiovascular Surgery, Kosair Children’s Hospital, University of Louisville, Louisville, Kentucky
b Division of Pediatric Cardiology, Kosair Children’s Hospital, University of Louisville, Louisville, Kentucky
c Department of Cardiothoracic Surgery, The University of Texas Southwestern Medical Center, Dallas, Texas

Accepted for publication January 10, 2005.

* Address reprint requests to Dr Kavarana, Division of Thoracic and Cardiovascular Surgery, 201 Abraham Flexner Way, Suite 1200, Louisville, KY40201 (Email: mkavarana{at}att.net).

Presented at the Fifty-first Annual Meeting of the Southern Thoracic Surgical Association, Cancun, Mexico, Nov 2–4, 2004.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
BACKGROUND: Although improved perioperative outcomes with growth potential of the extracardiac pedicled pericardial Fontan (EPPF) operation have been suggested, no advantage has been demonstrated.

METHODS: We retrospectively reviewed our institutional experience of 54 consecutive patients undergoing EPPF between June 1996 and August 2003. Clinical and echocardiographic follow-up was obtained yearly with a mean follow-up of 2.8 ± 2.0 years.

RESULTS: There were 29 males, median age 3.3 years (2–6.8). Median cardiopulmonary bypass time was 79 min (39–295). Fibrillatory arrest was used briefly in 9 patients, of which 6 were for fenestration. One Fontan required takedown (1.8%) and there was 1 death (1.8%) from Candida mediastinitis. Median intensive care unit stay, hospital length of stay, and chest tube drainage were 4 days, 12 days, and 8 days, respectively. Arrhythmias occurred in 7 patients. Three (5.6%) of these had preexisting Holter abnormalities requiring permanent pacemaker implantation. Freedom from thromboembolic events, reoperation, and death at 2.8 years after discharge were 96.2%, 98.1%, and 100%, respectively. All patients were New York Heart Association class I-II, with median oxygen saturation of 94 %. Only 5 patients (9.4%) had mild self-restricted activities. Echocardiographic evaluation revealed excellent ventricular function and flow dynamics.

CONCLUSIONS: At midterm follow-up this technique yields outcomes as good as the other Fontan techniques and with further follow-up may prove to be superior. However, at this point no clear advantage has been demonstrated. The low rate of complications and potential for growth are appealing features of this procedure.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Discussion
 References
 
As early Fontan patients are reaching adulthood, the long-term outcomes of this palliative operation are not ideal. Several modifications to the original atriopulmonary connection introduced in 1971 [1] have been proposed in order to decrease postoperative morbidity [2–4].

DeLeval and colleagues [5] introduced the "cavopulmonary anastomosis" also known as the intracardiac or "lateral tunnel" technique. This modification provided more laminar and efficient flow; but required the use of cardioplegic or fibrillatory arrest, intracardiac manipulation, and atrial incisions. In 1988 [6, 7], prosthetic extracardiac conduits were introduced in an attempt to decrease the incidence of late atrial arrhythmias. Decreasing cardiopulmonary bypass time and the avoidance of myocardial ischemia or fibrillation have resulted in better preservation of ventricular and pulmonary vascular function, lower Fontan circuit pressures, lower postoperative morbidity, and lower incidence of atrial arrhythmias [8]. The disadvantages of this technique revolve largely around the potential for thromboembolism and infection associated with the use of prosthetic material and a fixed (or even decreased) luminal conduit diameter over time [9, 10].

In an attempt to further decrease the morbidity associated with extracardiac conduits, Gundry and colleagues in 1997 [11] reintroduced the use of a pedicled pericardial tube first reported by Hvass and colleagues in 1992 [12] to construct an extracardiac lateral tunnel and complete the cavopulmonary connection. Although both the intracardiac lateral tunnel and the extracardiac conduit are widely accepted as standard "Fontan" operations, the extracardiac pedicled pericardial Fontan (EPPF) may offer the greatest potential for optimizing both early and late results. The objective of our study was to assess operative, early postoperative, and midterm results using this technique.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Discussion
 References
 
Study Population
We retrospectively reviewed consecutive patients with univentricular physiology undergoing

EPPF between June 1996 and August 2003 at Kosair Children’s Hospital, University of Louisville. An EPPF was defined as an extracardiac conduit fashioned from a native lateral pericardial pedicle to construct the total cavopulmonary connection. The Institutional Review Board of the Kosair Children’s Hospital, University of Louisville, approved the study. Fifty-four extracardiac Fontan operations were performed using viable ipsilateral pericardium. There were 29 males and 25 females, with a median age at operation of 3.3 years (2–6.8) and a median weight of 13.5 kg (9.4–26.3 kg). Primary anatomic diagnoses are shown in Table 1. All patients underwent prior operations, which are summarized in Table 2. All patients had bidirectional Glenn shunts prior to the EPPF operation and underwent preoperative echocardiography and catheterization. Median cardiopulmonary bypass (CPB) time was 79 min (39–295). Fibrillatory arrest was used in 9 patients to complete additional procedures. These include fenestrations in 6 patients (11.3%), atrial septectomy (n = 5), and pulmonary valve closure (n = 2). Fenestrations were required in patients with high Fontan conduit pressure (> 17 mm Hg), low arterial blood pressures (systolic blood pressure < 80), and suboptimal hemodynamics after CPB wean (Table 3). Median fibrillatory arrest time was 16 minutes (2–41 minutes). Perioperative complications were defined as occurring within 30 days of surgery or during the same admission. Major morbidity was defined as readmission to the intensive care unit [ICU] (excluding brief readmission solely for sedation for minor procedures), intubation longer than 48 hours, and need for reoperation or reintervention. Prolonged chest tube drainage (> 14 days) was considered separately.


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  		Table 1. Anatomic Diagnosis
 

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  		Table 2. Previous Procedures
 

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  		Table 3. Perioperative Outcome Variables: Comparison of Fenestrated Versus Nonfenestrated Patients
 
Operative Technique
All patients underwent intraoperative continuous neurologic monitoring using electroencephalogram, transcranial Doppler, and near-infrared oximetry as described previously [13]. Operations were performed by median sternotomy using CPB with mild hypothermia (32–34°C). The operative technique is described in Figure 1A and 1B. Cardioplegic or fibrillatory arrest was not used unless additional procedures, ie, fenestration, atrial septectomy, or oversewing of the pulmonary valve were required. The aorta and systemic atrium were cannulated in a standard fashion. An ipsilateral pericardial flap was prepared in situ, preserving the posterior pericardial connection with its vasculature, protecting the phrenic nerve. In four patients, the superior aspect of the flap was deficient. In these cases narrowing of the final conduit was avoided by adding a small piece of bovine pericardium sufficient to make up for the deficiency. After CPB was instituted, the posterolateral aspect of the right atrium (RA) was sutured to the adjacent pericardium from the inferior surface of the right pulmonary artery (RPA) to the inferior vena cava (IVC). The RA-IVC junction was clamped and the anterolateral aspect of the IVC was incised below the clamp leaving the back wall intact. The IVC flow was then controlled with pump suction. The divided front wall was sutured to the undivided back wall closing the cavoatrial junction permitting removal of the clamp. The inferior edge of the pericardial flap was sutured to the divided edge of the IVC opening using 5–0 interrupted polypropylene suture (Ethicon Inc, Somerville, NJ). Next, the inferior aspect of the RPA was opened from the pericardial reflection to just beneath the aorta with venous return controlled with cardiotomy suction. The superior edge of the pericardial flap was sutured to the anterior lip of the right pulmonary arteriotomy to complete the tunnel superiorly, using interrupted 5–0 polypropylene sutures. Both superior and inferior tunnel anastomoses were sized using Hegar dilators to assure a diameter equal to or slightly greater than the IVC (median size, 14 mm; range, 12–18 mm). Excess pericardium was trimmed in an effort to achieve a final conduit of uniform diameter. The tunnel was completed anteriorly using continuous 5–0 polypropylene bringing the free edge of the pericardial flap to the RA wall using epicardial bites and avoiding the area of the sinoatrial (SA) node.



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  		Fig 1. Operative techniques. (A) The pericardial pedicle is fashioned and the anterior wall of the right atrium is sutured to the backwall of the ipsilateral pericardial flap. (B) The completed EPPF. (EPPF = extracardiac pedicled pericardial Fontan; IVC = inferior vena cava; LPA = left pulmonary artery; RPA = right pulmonary artery; SVC = superior vena cava.)

 
After weaning from CPB, the operation was assessed by directly measuring pressures in the IVC, the pericardial conduit, the RPA, and the left atrium. Intraoperative transesophageal echocardiography (TEE) was used to evaluate myocardial and valve function and to assure laminar flow in the pericardial conduit. Fenestration was selectively performed if conduit pressures were elevated (> 17 mm Hg) or if hemodynamics were suboptimal after weaning from CPB. In these cases CPB was resumed and the anterior free edge of the flap was separated from the RA by loosening the snared untied sutures. A 1–2 cm patch of Gore-Tex (W L Gore & Associates, Flagstaff, AZ) with a 4 mm fenestration was then sutured to a circular opening created in the RA free wall during a brief period of fibrillation. Cross-clamp with cardioplegic arrest was used in one patient in whom air emboli was detected by transcranial Doppler. All patients were weaned from CPB on low dose dopamine (3–5 mcg/kg/min) and milrinone (0.25–0.5 mcg/kg/min). Postoperative management goals were early extubation, placement on angiotensin-converting enzyme inhibitors, and chest-tube retention until drainage was less than 100 cc per day. All patients were anticoagulated with warfarin to a target international normalized ratio of 2 to 3. Warfarin anticoagulation was arbitrarily maintained for one year. A catheterization is performed at one year to rule out obstruction or thromboembolism after which warfarin is discontinued and the patient is maintained on aspirin.

Data Analysis
Data were collected by retrospective review of the patient’s hospital and office records. Data were expressed as mean ± standard deviation and median (range). Dichotomous variables were compared using Fisher’s exact test or the {chi}2 test. Differences were considered significant when the p value was 0.05 or less. Clinical and echocardiographic follow-up were obtained yearly with a mean of 2.8 ± 2.0 years.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Discussion
 References
 
Postoperative Complications
There was 1 perioperative death (1.8%) from fulminant Candida mediastinitis. This patient developed heparin-induced thrombocytopenia, underwent multiple reexplorations with extracorporeal membrane oxygenation (ECMO) for shock, accounted for an ICU stay of 55 days, and ultimately succumbed to fungal sepsis. Major complications occurred in 11 patients (20.7%) and included the need for reoperation (n = 6) and reintubation (n = 1). Patients were reoperated on for bleeding (n = 3), mediastinitis (n = 1), ECMO (n = 1), and low output syndrome requiring takedown of the EPPF with conversion to bidirectional Glenn (n = 1). The patient who died of fungal sepsis accounted for the ECMO, mediastinitis, and two of the three reexplorations for bleeding. The median ICU and hospital length of stay was 4 (2–55) days and 12 (5–55) days, respectively. Prolonged pleural effusions (> 14 days) occurred in 7 patients (13.2%) and chylothorax in one. The median chest tube duration was 8 (3–55) days. Nine patients (16.9%) required reinsertion of a chest tube. Prolonged effusions were the single predictor of prolonged hospital stay (p < 0.05). Hospital stay was a median of 16 days (8–40 days) for patients with chest tube drainage more than 7 days (45.2%) as opposed to 8 days (5–20 days) for patients with less than 7 days of drainage (53.8%).

Transient junctional rhythm occurred in 4 patients. All of these patients were on high dose inotropes, had prolonged median CPB time (159.5 min [133–295 min]), and required fenestrations. One patient had postoperative bleeding and one had cerebral infarcts from air embolism [14].

Three patients had permanent pacemakers (PPM) placed at the time of EPPF for varying degrees of heart block determined at preoperative Holter and/or electrophysiology studies. Two required dual chamber PPM for second-degree atrioventricular block and complete heart block, respectively, while one required an atrial PPM for junctional bradycardia. At midterm follow-up 48 patients were in normal sinus rhythm, one patient had a junctional (ectopic atrial) rhythm, and another had sinus node dysfunction. One patient developed progressive subaortic stenosis (gradient 68 mm Hg) eighteen months post-Fontan and required a subaortic myectomy, which resulted in immediate heart block and placement of a PPM.

Forty-nine patients (92.4%) were extubated within 24-hours. Four patients required ventilatory support for more than 24 hours. The majority of patients were weaned off inotropes by postoperative day three (Table 4).


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  		Table 4. Early Postoperative Outcome Variables
 
Follow-Up Data
Median follow-up was 2.8 years (0.2–7 years) and follow-up was 100% complete. At follow-up, patients had a median oxygen saturation of 94% (77%–99%) and 5 patients (9.4%) had mild self-restricted activities. Exercise tolerance was evaluated subjectively by the cardiologist and quantified as mild indicating no symptoms with daily routine activities but exemption from competitive sports.

Freedom from arrhythmias, thromboembolic events, reoperation, and death at 2.8 years after discharge was 96.2%, 96.2%, 98.1%, and 100%, respectively. Angiographic (Fig 2) and/or echocardiographic serial evaluations showed normal ventricular function in all patients. All but one late postoperative echocardiogram showed patent tunnels with no increased velocities at anastomotic sites and no evidence of narrowing or obstruction or dilatation (Figs 3A and 3B). Late complications (> 6 months) were observed in four patients (Table 5). All but one were treated medically.



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  		Fig 2. Extracardiac pedicled pericardial Fontan (EPPF) conduit on cardiac catheterization. (IVC = inferior vena cava;SVC = superior vena cava.)

 


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  		Fig 3. (A) Apical "four-chamber" view of the extracardiac pedicled pericardial Fontan (EPPF) in a patient born with pulmonary atresia and an intact ventricular septum: a cross-sectional cut of the conduit. (B) Subcostal saggital view of the EPPF in a patient born with pulmonary atresia and an intact ventricular septum: the entire length of the conduit is seen from this view. (IVC = inferior vena cava; LA = left atrium; LV = left ventricular.)

 

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  		Table 5. Late Postoperative Outcome Variables: Late Interventions
 
Three of 9 (33.3%) patients who had undergone postoperative catheterizations had fenestration closures. One had a fenestration performed for protein losing enteropathy. One patient (1.8%) had a late embolic cerebrovascular accident. This patient was off warfarin at the time and presented 7 months post-EPPF with transient left-sided weakness and was found by magnetic resonance imaging (MRI) and angiography to have saccular aneurysms in the left internal carotid. Recovery was complete; the patient was placed back on warfarin and remains asymptomatic with no neurologic deficits at 46 months of follow-up.

One patient was discovered to have thrombosis of the EPPF 18 months postoperatively. He was not on warfarin at the time and was treated empirically with diuretics and anticoagulants due to the presence of periazygos collaterals and is currently asymptomatic.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Discussion
 References
 
Since its inception in 1971 [1], results of the Fontan operation have steadily improved [15]. Improvements in surgical technique in both extracardiac conduit and lateral tunnel Fontan operations, fenestrations, and advances in ICU care have resulted in decreased pleural effusions, shorter length of stay, and decreased mortality [16]. Nevertheless, survivors are still developing arrhythmias, conduit stenoses, infections, and thromboembolism [17–19, 20–23]. For these reasons we have chosen to perform the EPPF modification.

By definition, the palliative Fontan circulation has abnormal hemodynamics that can result in poor early and delayed clinical outcomes [15, 24]. To improve these outcomes several modifications to the original atriopulmonary connection procedure have been described, which have evolved to the present total cavopulmonary connections [5, 25, 26].

The concept of the lateral intraatrial tunnel introduced by de Leval and colleagues [5] and it’s successful clinical application by the Boston Children’s Group [15] derived a near widespread acceptance of the technique. However, several drawbacks remained such as the need for cardiac arrest, atrial suture lines, and hemodynamic and thromboembolic issues related to the intraatrial baffle. The extracardiac lateral tunnel technique was introduced in search of a simpler operation with better hemodynamics [6–8]. Although the initial operation was described using cardioplegia, cooling, and circulatory arrest [6], the operation has been simplified and is presently performed by many with a short period of CPB, and by some without it [27]. The classic extracardiac Fontan operation requires use of prosthetic material that lacks growth potential and has a fixed diameter, which could potentially limit its use in small children. Amodeo and colleagues [9] reported a decrease in diameter of 20 extracardiac tubes screened by MRI. There was an average of 18% reduction in luminal area with a maximal reduction of 32% within the first 6 months.

The conceptual appeal for using autologous viable pericardium is its potential for growth. Pericardium as a graft substitute has been routinely used in congenital cardiac surgery. The free surface of the pericardium is nonthrombogenic [12] and rarely dilates unless there is excessive internal pressure. As a vascularized pedicle, pericardial tissue should theoretically grow with the heart and mediastinal structures as it does normally. Guyton and colleagues [28] reported satisfactory growth of pedicled pericardial flaps used to patch atrial walls in dogs. Growth of viable pericardium has been shown in humans after flaps used to enlarge pulmonary artery branch stenosis [29]. The first successful use of viable ipsilateral pericardium to complete a lateral extracardiac Fontan connection demonstrated no echocardiographic evidence of thrombus formation or collapse of the tube and laminar flow in all tubes [12]. Gundry and colleagues [11] described the construction of an extracardiac lateral tunnel utilizing viable autologous pericardium. The results showed a decreased overall morbidity and a reproducible technique, although detailed follow-up was not described.

Unlike Gundry we employed normothermic or mildly hypothermic (34°C) CPB and moved the upper anastomosis medially. We use interrupted sutures at the IVC and pulmonary artery connections and attempt to close all the depressions and other irregularities in the posterior wall of the tunnel to minimize turbulence and energy dissipation. Recent reports have shown evidence that by staging palliative procedures at an early age, performing ancillary intracardiac procedures during the Glenn anastomosis, using short times of CPB without cardioplegia, and avoiding intraatrial suture lines, early postoperative outcomes are much improved [8]. We have followed these principles in our EPPF procedures. The use of prosthetic material is not necessary unless a fenestration or conduit augmentation is required.

Lemler and colleagues [30] demonstrated that fenestrations significantly reduced chest-tube drainage and hospital length of stay. It has also been shown that fenestration is associated with its own set of complications including thromboembolic phenomena with neurologic sequelae [31, 32]. We selectively fenestrated patients and, as seen in other series of extracardiac conduits, the improved hemodynamics have made routine fenestration unnecessary [33]. Furthermore, a fenestration can be created percutaneously in the cardiac catheterization laboratory [34].

A recent study of 100 extracardiac Fontans showed that postoperative infections of the blood and respiratory tract predicted an increased rate of effusions with an infection rate of 16% [10]. The avoidance of prosthetic material with the EPPF may result in a lower infection rate (1.8%). Our early perioperative complication rate compares favorably with reported data using the extracardiac conduit techniques [10].

Experimental data showed that a lateral tunnel produces more turbulence and dissipation of energy from the lateral conduit when compared with extracardiac conduits [35]. Careful smoothening of the posterior wall, tailoring the tunnel as a tube using a Hegar dilator, seems to improve the flow characteristics of the tunnel.

The patient with an obstructed EPPF presented with dilated chest wall veins and on catheterization demonstrated occlusion of the conduit. He had developed abundant collaterals and no further intervention was required. This occurrence was noted early in our experience before intraoperative TEE was used to document laminar flow and was most likely due to a technical error affecting flow through the conduit. Our risk of thromboembolic complications (3.6%) compares favorably with the 2.3% to 25% risk of thromboembolism described after different types of Fontan operations [20–22, 31]. Most of them require use of prosthetic material or intraatrial communication with risk of obstruction, thrombosis, or paradoxical emboli. An additional benefit of the EPPF is the maintenance of tunnel size and growth potential. Our echocardiographic and angiographic data showed no evidence of narrowing, obstruction, or dilatation. However, this is difficult to quantify because the data are only representative of the early phase of the study.

Concerns with this technique include the availability and quality of pericardium after reoperative surgery, which we found partially deficient in four patients who required augmentation. None of these patients developed obstruction or thromboembolism. We made a conscious effort during previous operations to preserve pericardium on the appropriate side. If very little viable pericardium is present an extracardiac Fontan using a Gore-Tex tube is performed. Phrenic nerve injury resulting in hemidiaphragmatic paralysis has been associated with an increased morbidity [36]. Although we had 0% incidence in this series it remains an important concern and we recommend that the phrenic nerve and its accompanying blood supply be clearly identified prior to performing the posterior tunnel suture line and that the use of cautery be minimized during lateral mobilization. Another theoretic concern is external compression of the tunnel or tunnel compression of the right-sided pulmonary veins. To date, these concerns have not manifested clinically. The relatively short-term follow-up prevents a true evaluation of the arrhythmia or thromboembolic potential with this technique and clearly longer follow-up is required.

Our data show that construction of an EPPF connection is a relatively simple technique, is safe, is reproducible, and has similar CPB times to other extracardiac Fontan conduits [8, 10]. This technique yields early outcomes as good as the lateral tunnel Fontan and other extracardiac Fontans and further follow-up is required to demonstrate clear advantage. Early and midterm evaluations have been encouraging due to the low incidence of arrhythmias and absence of obstruction within the extracardiac lateral tunnel. Long-term follow-up with serial echocardiography, angiography, or MRI will be essential and is ongoing to demonstrate continued growth of the conduit.


   Discussion
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
References
 
DR IRVING L. KRON (Charlottesville, VA): One of the issues I think that we have seen using lateral tunnels, and this has that potential, are dilation of the conduit. Have you looked for that, in other words, late inefficiency of the conduit? Is there evidence of dilation of any of these?

DR KAVARANA: We have looked at echocardiograms at midterm and we haven’t found any dilation. There is an echocardiogram that I can show, which demonstrates how we follow up these patients typically.

(Slide) This is an apical four-chamber view of the tunnel, and this is a patient that had pulmonary atresia with an intact ventricular septum, and you can see a cross-sectional view of the tunnel there. We have followed them up, but we don’t have long-term follow-up. I think that is essential and that needs to be done.

DR JOHN H. CALHOON (San Antonio, TX): Dr Kavarana, I enjoyed your presentation. It was very well presented. Do you have any cause for why the one thrombosed? One would think that using autologous tissue that thrombosis would be a low likelihood. And a second question is, what is your anticoagulation? I don’t remember hearing what your anticoagulation regimen was, if any.

DR KAVARANA: We were very concerned after we had this patient thrombose after a Fontan conduit, and since then we make sure that we augment the patch if there is a lack of pericardial tissue. We now have patients on warfarin for one year. After one year they get a cath. If the cath shows no evidence of obstruction or thrombosis, then they get converted to aspirin.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 

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