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J Thorac Cardiovasc Surg 2007;133:640-647
© 2007 The American Association for Thoracic Surgery

Surgery for Congenital Heart Disease

Pulmonary valve cusp augmentation with autologous pericardium may improve early outcome for tetralogy of Fallot

Petros Anagnostopoulos, MDa, Anthony Azakie, MDa, Shobha Natarajan, MDb, Nelson Alphonso, MDa, Michael M. Brook, MDb, Tom R. Karl, MDa,*

a Division of Pediatric Cardiac Surgery, Pediatric Heart Center, University of California at San Francisco Children’s Hospital, San Francisco, Calif
b Division of Pediatric Cardiology, Pediatric Heart Center, University of California at San Francisco Children’s Hospital, San Francisco, Calif.

Read at the Eighty-sixth Annual Meeting of The American Association for Thoracic Surgery, Philadelphia, Pa, April 29-May 3, 2006.

Received for publication April 21, 2006; revisions received September 23, 2006; accepted for publication October 9, 2006.

* Address for reprints: Tom R. Karl, MD, UCSF Department of Surgery, Division of Pediatric Cardiothoracic Surgery, 513 Parnassus Avenue, Suite S-549, Box 0117, San Francisco, CA 94143-0117. (Email: karlt{at}surgery.ucsf.edu).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Objectives: The transannular patch used to relieve right ventricular outflow tract obstruction in children with tetralogy of Fallot may result in pulmonary insufficiency. We hypothesized that pulmonary valve cusp augmentation with pericardium would decrease pulmonary insufficiency and improve the early outcome for transatrial–transpulmonary tetralogy of Fallot repair requiring transannular patch.

Methods: Since November 2001, 41 patients with tetralogy of Fallot and 2 patients with isolated pulmonary valve stenosis had relief of right ventricular outflow tract obstruction with either a transannular patch plus pulmonary valve cusp augmentation (n = 18) or a transannular patch alone (n = 25). Data were retrospectively collected.

Results: The median age (5.3 vs 3.2 months; P = .09) and weight (6.4 vs 5.2 kg; P = .3) were similar for the cusp augmentation and transannular patch groups, respectively. The diameter of the pulmonary valve annulus (6.4 vs 6.0 mm; P = .57) and the McGoon index (1.47 vs 1.69, P = .75) were also similar. The mean aortic clamp time (48 ± 18 minutes vs 52 ± 19 minutes; P = .46) and median cardiopulmonary bypass time (89 vs 91 minutes; P = .9) did not differ. One patient with a transannular patch died of multiorgan system failure. Patients with a pulmonary valve cusp augmentation had a shorter duration of intubation (1 vs 3 days; P < .001) and intensive care unit stay (2 vs 8 days; P < .001). Thirteen patients with a transannular patch and 1 patient with a pulmonary valve cusp augmentation required inotropic support for more than 72 hours (P = .001). Discharge echocardiograms demonstrated moderate or severe pulmonary insufficiency in 5 patients with a pulmonary valve cusp augmentation and in 21 patients with a transannular patch (P < .001). At 7.5 months, 3 patients (17%) with a pulmonary valve cusp augmentation had progression of pulmonary insufficiency.

Conclusions: Augmentation of a pulmonary valve cusp reduces the incidence of clinically significant postoperative pulmonary insufficiency. This technique may improve the early outcome for children with tetralogy of Fallot requiring a transannular patch.

Abbreviations and Acronyms ICU = intensive care unit; PI = pulmonary insufficiency; RVOT = right ventricular outflow tract; TOF = tetralogy of Fallot; UCSF = University of California at San Francisco


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 
The combination of a ventriculotomy and free pulmonary insufficiency (PI), both associated with the transannular patch, is implicated in the deterioration of right ventricular function and the development of arrhythmias after tetralogy of Fallot (TOF) repair. In the current era, in which the immediate outcome of TOF repair is expected to be excellent irrespective of surgical technique and timing of the repair, the goal of the surgical treatment of TOF should be the avoidance of long-term complications and a low probability of early and late reoperations. At the University of California at San Francisco (UCSF), since November of 2001, we have used the transatrial–transpulmonary approach for repair of TOF to avoid an extensive right ventriculotomy.1,2Go In the subset of patients who did not have adequate relief of the right ventricular outflow tract (RVOT) obstruction with complete sparing of the pulmonary valve, we extended the pulmonary artery incision for approximately 10 to 15 mm onto the right ventricular free wall. To further decrease the degree of postoperative PI, we used the technique of augmentation of the native pulmonary valve tissue with autologous pericardium, originally described by Sung and associates.3Go We hypothesized that it would lead to an improved early outcome for transatrial–transpulmonary TOF repair.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
Patient Population
The Committee on Human Research at UCSF approved the study.

The study population consisted of all patients with TOF (n = 41) or isolated pulmonary valve stenosis (n = 2) who underwent transatrial–transpulmonary repair at UCSF Children’s Hospital between November 2001 and August 2005 and required division of the pulmonary valve annulus for adequate relief of RVOT obstruction. Patients with TOF who had repair without division of the pulmonary annulus (pulmonary valve–sparing operation) were excluded, as were those with discontinuous pulmonary arteries, pulmonary atresia and ventricular septal defect, atrioventricular septal defect, and absent pulmonary valve syndrome. Eighteen patients had pulmonary valve cusp augmentation with an autologous pericardial patch according to the technique described by Sung and associates.3Go During the same period of time, 25 patients underwent repair with a transannular patch and were used as controls. The patients were not randomized, and each of the 2 primary surgeons in the study used both techniques. There was not a clearly defined indication for one procedure or the other.

Operative Details
The operative technique is outlined in Figure 1. A patch of autologous pericardium was harvested and treated with 0.2% glutaraldehyde for 10 minutes. Cardiopulmonary bypass was established through bicaval and aortic cannulation. Systemic to pulmonary artery shunts, if present, were ligated after the beginning of cardiopulmonary bypass. Moderate hypothermia was used (28°C-32°C). The heart was arrested with antegrade cold blood cardioplegia. The right atrium was opened longitudinally, and the left heart was vented through the foramen ovale. A longitudinal incision was made in the main pulmonary artery and extended to the annulus of the pulmonary valve. The valve was inspected. If there was significant commissural fusion or tethering of the leaflets to the pulmonary artery wall, these were sharply divided. Excision of the parietal extension of the infundibular septum was performed through the tricuspid valve. Hegar dilators were then passed through the tricuspid valve toward the main pulmonary artery. If the diameter of the annulus was more than 2 standard deviations (z score < –2) below the normal predicted annulus diameter for the patient’s weight, the pulmonary annulus was divided.4Go In the majority of cases the pulmonary valve was bicuspid with location of the commissures at the 3 and 9 o’clock positions. An incision was made in the middle of the anterior cusp and then extended to the right ventricular free wall for approximately 10 to 15 mm. When the pulmonary valve commissures were located at the 6 and 12 o’clock positions or the commissures were anterior and posterior but located off the midline, we divided the pulmonary valve at or near the anterior commissure to preserve as much valve tissue as possible, as described by Sung and associates.3Go The division of the remaining obstructing muscular and fibrous bands was performed through the ventriculotomy. The ventricular septal defect was closed through the tricuspid valve. The foramen ovale was closed with a temporary purse string suture, the heart was de-aired, and the aortic clamp was removed.


Figure 1
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  		Figure 1. A, Pulmonary cusp augmentation repair technique. A transannular incision has been created according to calibration of the RVOT diameter (see text). The incision divides the anterior pulmonary valve leaflet, although the exact location will vary with the valve orientation and morphology. B, Pulmonary cusp augmentation repair technique. A triangular patch of glutaraldehyde-preserved autologous pericardium is sutured to the epicardial edge of the RVOT incision and to the divided edges of the valve leaflet. The leaflet dimensions are based on the caliber of a normal pulmonary valve diameter and should provide sufficient free edge diameter to ensure coaptation with the native valve remnant. C, Pulmonary cusp augmentation repair technique. A second larger oval patch of the same material is sutured to the epicardial aspect of the RVOT incision and to the edges of the pulmonary arteriotomy, creating a sinus anterior to the reconstructed leaflet. PA, Pulmonary artery; PV, pulmonary valve; RVOT, right ventricular outflow tract.

 
Reconstruction of the RVOT was then performed. In patients who underwent RVOT reconstruction with a transannular patch, the RVOT and pulmonary arteriotomy were closed with an appropriately sized single pericardial or polytetrafluoroethylene (Gore-Tex, WL Gore and Associates, Flagstaff, Ariz) patch. In patients who underwent the transannular patch plus reconstruction with the pulmonary valve cusp augmentation technique, a triangular glutaraldehyde-treated autologous pericardial patch was sutured in the endocardium from the most inferior aspect of the right ventriculotomy all the way up to the hinge point of the anterior cusp and then along the divided edge of the valve on either side. When the anterior cusp was small or the anterior commissure was located at the 12 o’clock position, the patch was anchored to the main pulmonary artery. In patients in whom the commissure was eccentric, the patch was sewn to the main pulmonary artery on 1 side and to the free edge of the leaflet on the other side. Then a second patch was used to close the RVOT and the pulmonary arteriotomy, thus recreating a sinus over the augmented valve leaflet.

Clinical Data
The medical records of all patients were reviewed. We recorded demographic data, previous operations, catheterization procedures, and associated comorbidities, including genetic syndromes. For each patient we gathered data on the operative repair including cardiopulmonary bypass time, aortic clamp time, description of the RVOT management, and additional surgical procedures performed. The postoperative course was then reviewed. The date of extubation, the date of discharge from the intensive care unit (ICU), and the date of discharge from the hospital were used to calculate days intubated, days in the ICU, and days hospitalized. All of the complications were recorded. Finally, the condition during the last clinic visit of the patients with a pulmonary valve cusp augmentation was recorded. Late complications, follow-up interventions, and reoperations were noted.

Echocardiographic Data
All preoperative and postoperative echocardiograms and echocardiographic reports were reviewed. The preoperative pulmonary valve annulus was measured in a modified parasternal long-axis view. The branch pulmonary artery diameter was measured in the parasternal short-axis plane, and the McGoon index was calculated. Tricuspid regurgitation was graded as follows: 0 = none; 1 = trivial; 2 = mild; 3 = moderate; 4 = severe. PI severity was graded in a similar fashion. Patients with mild or less insufficiency were grouped and compared with those with moderate or severe insufficiency. For the patients who underwent pulmonary valve cusp augmentation with autologous pericardium, we reviewed the follow-up echocardiogram to investigate whether there was progression in the degree of PI.

Statistical Analysis
Variables with a normal distribution are expressed as the mean ± standard deviation. Variables without a normal distribution are expressed as median and range. Differences were examined for significance by univariate analysis (Student t test, chi-square test, Fisher exact test, or Mann–Whitney U test as appropriate). All data were analyzed with Statistica 6.0 (StatSoft Inc, Tulsa, Okla).


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
Patient characteristics and preoperative transthoracic echocardiographic data are shown in Tables 1 and 2, Go respectively.


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  		TABLE 1 Patient characteristics
 

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  		TABLE 2 Preoperative transthoracic echocardiographic data
 
Mean aortic clamp time (48 ± 18 minutes vs 52 ± 19 minutes for transannular patch; P = .46) and median cardiopulmonary bypass time (89 minutes vs 91 minutes for transannular patch; P = .9) were similar in the 2 groups. One patient with a transannular patch died. The patient was a 34-week gestational age twin baby boy who never left the hospital after birth and underwent operation at 6 weeks of age. Postoperatively he required extracorporeal membrane oxygenation twice for persistent low cardiac output from right ventricular diastolic dysfunction and intractable atrial tachyarrhythmias. Persistent large output bilateral chylothoraces and acute renal failure developed in the boy, which were treated with peritoneal dialysis. After a brief period of improvement, Staphylococcus epidermidis endocarditis developed that led to multiorgan system failure. He died on postoperative day 86.

The postoperative course and discharge data in the 2 groups of patients are shown in Table 3.


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  		TABLE 3 Postoperative clinical and transthoracic echocardiographic data
 
Of the 18 patients who underwent pulmonary valve cusp augmentation, 1 was lost to follow-up. Two patients required reintervention. One patient presented to the hospital 3 months postoperatively with a delayed pericardial effusion and required a pericardial window. The cause of this effusion was unclear. The second patient was symptomatic with persistent subvalvar pulmonary stenosis. She underwent operative RVOT muscle bundle resection 2 years after her original repair. This patient had moderate PI at discharge, and the degree of PI did not change during follow-up. At a median follow-up of 7.5 months (range 0-29 months), 6 of the 17 patients (35.3%) had moderate or severe PI at follow-up. Three patients (17%) who underwent pulmonary valve cusp augmentation had progression of PI when compared with the degree of PI at discharge.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
There is a current trend for complete repair of TOF in early infancy. This strategy was first applied in neonates with unacceptable oxygen saturations5-7Go and has been adopted by some centers as the preferred approach even the for minimally cyanotic neonates.8,9Go Although primary neonatal repair can be accomplished with excellent early results, it can lead to routine use of a large ventriculotomy and repair with a transannular patch in up to 70% of patients. In fact, this operation is remarkably similar to the technique described by Lillehei in which ventriculotomy is used for VSD closure in up to 96% of patients.10Go

The use of a transannular patch may result in free PI, which causes right ventricular dilation that in turn compresses the left ventricle. The functional reserve and myocardial contractility of the right (and possibly left) ventricle decrease. These changes can be detected in experimental models as early as 3 months after the onset of PI.11Go This physiology is well tolerated in the majority of patients for a prolonged period of time,12-14Go but some will eventually experience decreased exercise tolerance and progressive right ventricular dilation and failure.15,16Go The exercise performance and the degree of right ventricular failure correlate with the severity of PI.17,18Go The chronic volume load to the right ventricle after TOF repair leads to dilation of the ventricle and predisposes the patient to late life-threatening ventricular arrhythmias and sudden death.15,19Go

Several groups have described strategies to limit the size of the right ventriculotomy and reduce the incidence of PI. Valved homografts and xenografts were proposed as the most anatomic and physiologic way to resolve RVOT obstruction, but all will eventually need replacement because of patient growth and conduit deterioration.20Go The use of a monocusp valve created from pericardium, xenograft valve cusps, fascia lata, autologous pulmonary artery wall, or polytetrafluoroethylene has been shown to decrease short-term PI.21-23Go However, even the monocusp has limited durability. Gundry and associates21Go reported that by 24 months only 14% of their patients with a homograft monocusp-bearing transannular patch had a competent valve despite excellent short-term function. Similarly, in a report from the University of Indiana most of the patients had deterioration of the polytetrafluoroethylene monocusp valve function by 3 years, even though the valve function was still better compared with the free PI experienced by the patients with a transannular patch.22Go Other groups have abandoned the monocusp because they did not think that it provided a significant advantage for the patient.24Go

The Northwestern University group recommends avoidance of a transannular patch with preservation of the annulus of the pulmonary valve.24Go They perform transatrial closure of the ventricular septal defect, extensive commissurotomy, transpulmonary, and transatrial RVOT muscle resection, and, when needed, augmentation of the infundibulum with a separate patch that does not cross the annulus. They accept a right ventricular to left ventricular systolic pressure ratio of 0.7, because their main goal is to preserve the annulus, more so than the valve cusps, explaining the 36% incidence of PI at midterm follow-up. Only 2 of 73 patients who met their criteria required reoperation for residual stenosis at a mean follow-up of approximately 3 years.24Go In the subgroup of patients who do not have adequate RVOT relief through transatrial and transpulmonary muscle bundle resection, it is not clear that patching of the outflow with preservation of the annulus will offer an advantage in the long run over transannular patching. D’Udekem and associates25Go reviewed 191 patients who had TOF repair between 1964 and 1984 and concluded that a transannular patch does not result in a worse late functional outcome than patching of an incision limited to the right ventricle.

TOF can be reliably repaired through a transatrial and transpulmonary approach.1,2,26,27Go This approach differs from the transventricular TOF repair in that the right ventricular incision, if needed, extends just enough to relieve the obstruction of the outflow tract. There is a suggestion that this approach results in a lesser degree of PI, lower incidence of arrhythmias, and better overall right ventricular performance.1,28Go

In our unit since November of 2001, we have used the transatrial–transpulmonary approach for TOF repair, following the policy set forth by Dr Mee at Royal Children’s Hospital, Melbourne. Neonates with an unacceptable level of hemoglobin saturation and/or hypercyanotic spells may be palliated with a modified Blalock–Taussig shunt. Although there is documented morbidity and interval mortality with this approach,29Go there are centers that report excellent outcome and a risk of palliation that approaches 0% with the use of this strategy.1,24Go The pros and cons of this approach have been extensively discussed elsewhere and are beyond the scope of the present study. We do make an effort to complete the repair without division of the annulus, although our target right to left ventricular systolic pressure ratio is less than 0.6. If this is not possible we perform a limited ventriculotomy, which is reconstructed with a transannular patch. Since the description of the pulmonary cusp augmentation technique by Sung and associates3Go in 2003, we have adopted this technique for patients requiring a transannular patch. This technique preserves the native hinge mechanism of the valve cusps, especially when the pulmonary valve is bicuspid and the commissures are located in the 3 and 9 o’clock positions. The use of native valve tissue also offers the theoretic potential of growth. The pulmonary valve cusp augmentation technique effectively reduces the degree of postoperative PI. Of 18 patients who had relief of RVOT obstruction with the use of the pulmonary valve cusp augmentation technique, 5 (27%) had moderate or severe PI at discharge. In contrast, 84% of the patients with transannular patch reconstruction had clinically significant PI at discharge. In the series published by Sung and associates,3Go all 18 patients had absent or mild PI at discharge. It is not clear whether the higher incidence of PI in our series is because of technical reasons (ie, a learning curve) or because the patients in Sung’s series were older (mean age 13.8 months).

The pulmonary neocusp technique can be used in the majority of patients with TOF and pulmonary stenosis who require division of the pulmonary valve annulus for relief of RVOT obstruction. In our experience it cannot be applied only in a certain subgroup of patients who have a small pulmonary annulus with hypoplastic inadequate native pulmonary valve tissue. In this group of patients the transatrial–transpulmonary repair with a minimal right ventriculotomy and closure of the RVOT with a simple transannular patch is our preferred technique.

The acute change from a pressure-loaded to a volume-loaded right ventricle in addition to the right ventriculotomy after a transannular patch reconstruction can adversely affect the performance of the right ventricle in the immediate postoperative period.21,30Go Our patients who underwent pulmonary valve cusp augmentation had a far better postoperative course when compared with the patients with a transannular patch reconstruction. They stayed intubated for a shorter period of time, required less inotropic support, had fewer persistent pleural effusions and chylothoraces, and had fewer postoperative supraventricular arrhythmias. Turrentine and associates,22Go using a polytetrafluoroethylene monocusp valve for RVOT reconstruction, effectively decreased the degree of PI compared with their patients who received a nonvalved transannular patch. They also found a significant difference in ICU use and a trend toward better survival in favor of the patients with a monocusp. In contrast, a study from Toronto failed to show any advantage in the postoperative course of patients who had a monocusp valve creation as part of their TOF repair. In this study, however, the degree of postoperative PI was similar in the patients who had a monocusp valve constructed and the patients who underwent transannular patch reconstruction.31Go

Seventeen percent of our patients had progression of PI on short-term follow-up (median 7.5 months). In Sung and colleagues’3Go series, 2 of the 18 patients also had progression of PI at the 10-month follow-up. We will continue to follow these patients to determine whether this reconstruction is durable or not.

The limitations of the study include its retrospective nonrandomized nature. Although there are no demographic, clinical, and echocardiographic parameters that differed between the 2 groups, it is possible there is selection bias that influenced the results of this study. In addition, although there is a considerable overlap in the use of the 2 techniques in our institution, the majority of the patients who had pulmonary neocusp reconstruction underwent operation after the introduction of the technique by Sung and associates in 2002.3Go It is possible that part of the improvement in clinical outcome may reflect this time discrepancy. Also, as mentioned above, we have no data on the long-term outcome for these patients or for the durability of the repair, both of which we will assess over time.

Despite all of the limitations of our study, the augmentation of the pulmonary valve cusp with autologous pericardium is simple, does not significantly prolong the operation, reduces the degree of PI in the immediate postoperative period, and improves the early outcome after transatrial–transpulmonary TOF repair requiring a transannular patch. When technically feasible, it has become our preferred technique for RVOT reconstruction in patients with TOF and in patients with pulmonary stenosis who require surgical intervention.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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