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Eur J Cardiothorac Surg 2008;33:251-256. doi:10.1016/j.ejcts.2007.11.023
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Exclusion of the non-functioning right ventricle in children with pulmonary atresia and intact ventricular septum

Ji-Hyuk Yanga, Tae-Gook Juna,*, Pyo Won Parka, Kiick Sunga, Wook Sung Kima, Young Tak Leea, June Huhb, I-Seok Kangb

a Department of Thoracic and Cardiovascular Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea
b Department of Pediatrics, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Republic of Korea

Received 14 September 2007; received in revised form 20 November 2007; accepted 23 November 2007.

* Corresponding author. Address: Department of Thoracic and Cardiovascular Surgery, Samsung Medical Center, lrwon-dong 50, Gangnam-gu, 135-710 Seoul, Republic of Korea. Tel.: +82 2 3410 3484; fax: +82 2 3410 0089. (Email: tg.jun{at}samsung.com).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objective A group of patients with pulmonary atresia and intact ventricular septum (PAIVS) have to undergo single ventricle repair. In these patients, the presence of the non-functioning right ventricle (RV) may lead to the aggravation of RV to coronary connections and left ventricular (LV) dysfunction. To prevent these deleterious effects, the RV was excluded surgically. Methods Between December 2000 and February 2006, 10 patients with PAIVS underwent RV exclusion in conjunction with cavo-pulmonary anastomosis (n = 6) or systemic-to-pulmonary artery shunt (n = 4). Median age at surgery was 5 months (range, 0.2–13.8). Median z-value of the tricuspid valve was –4.0 (range, –6.5 to –1.3). None had RV dependent coronary circulation. The tricuspid valve was closed directly or using a patch. Thrombotic materials were inserted into the RV cavity in eight patients. Results There was no mortality. Follow-up was completed in all patients for up to 79.1 months (median, 30.3). Seven patients underwent a Fontan procedure and the other three are waiting. Eight patients showed completely obliterated RV after exclusion. One of the two patients who had residual RV cavity underwent re-exclusion after a Fontan operation. Postoperative echocardiography revealed that LV end-diastolic dimension increased with borderline significance (p = 0.050), whereas LV end-systolic dimension showed no significant changes. During follow-up, LV showed no evidence of regional ischemia or global dysfunction, and fractional shortening significantly increased compared with the pre-exclusion value (p = 0.017). Conclusions This study demonstrates that RV exclusion may be performed safely in a selected group of patients with PAIVS. This procedure may have beneficial effects on LV systolic function, by preventing possible ischemia, and on LV diastolic function, by obliterating the non-functioning cavity and improving the geometry of the ventricular septum.

Key Words: Pulmonary atresia/surgery • Heart bypass, right • Treatment outcome • Congenital heart disease, cyanotic • Infant, newborn


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Therapeutic approaches for patients with pulmonary atresia and intact ventricular septum (PAIVS) are still challenging, especially for patients who have to undergo single ventricle repair. Commonly, these patients have a small, hypertrophied right ventricle (RV) with supra-systemic pressure and sinusoidal communication between the RV and the coronary artery [1,2]. Many authors have noticed the possible deleterious effects associated with this situation, i.e., the progression of RV-to-coronary connections and subsequent coronary artery stenosis [3–6], potential RV ‘steal’ and coronary ischemia after RV decompression [4,7], impaired left ventricular compliance [8], left ventricular hypertrophy with a prominent subaortic septal bulge [9,10], fibroelastosis of the left ventricle (LV) [10], and an impaired LV function after a Fontan procedure [11] or even after biventricular repair [12]. A surgical trial to prevent these deleterious effects was first described by Waldman and associates [13]. Toronto group also reported thromboexclusion of the RV, which included closing the tricuspid valve and filling the cavity with coils or absorbable gelatin sponge [3,14]. The authors recommended that RV exclusion is indicated in the presence of RV-to-coronary artery connections without RV dependent coronary circulation (RVDCC) [14] and that this should be performed within the first year of life [15]. However, little has been known after their report. Here, we describe the outcome of RV exclusion in selected patients with PAIVS.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 Appendix A
 References
 
2.1 Patients
Our institutional review board approved and waived individual consent for this study. Between December 2000 and February 2006, 10 patients with PAIVS underwent RV exclusion in conjunction with cavo-pulmonary anastomosis (n = 6) or systemic-to-pulmonary artery shunt (n = 4). We retrospectively reviewed medical records, cardiac catheterization, and echocardiographic data of these patients. All patients underwent cardiac catheterization and angiography preoperatively, except one patient (patient no. 8). Five of the 10 patients (50%) had RV-to-coronary artery connections, but none had evidence of RVDCC. In five patients, RV pressure was greater than left ventricular pressure. Six patients had previously undergone a palliative procedure. Median age at surgery was 5 months (range, 0.2–13.8) and median body weight was 5.8 kg (range, 2.8–10.5). Median z-value of the tricuspid valve was –4.0 (range, –6.5 to –1.3) (Table 1 ).


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  		Table 1 Preoperative patients’ characteristics and operative procedures
 
2.2 Operative techniques
After routine aorto-bicaval cardiopulmonary bypass with moderate hypothermia had been established, antegrade cold blood cardioplegia was infused. Absorbable gelatin sponge (Spongostan® standard; Johnson & Johnson Medical Ltd., Skipton, UK) was inserted into the RV cavity in eight patients, to induce thrombotic obliteration. The tricuspid valve was closed directly or with a patch (bovine pericardium in one patient, autologous pericardium in the other). The atrial septal defect was enlarged in all patients. Other procedures performed concomitantly are listed in Table 1.

2.3 Data analysis
Follow-up cardiac catheterization and angiography were performed in all patients before the next stage of surgical treatment. To evaluate the influence of RV exclusion on LV geometry and function, echocardiographic data obtained just before and after the operation were collected. These included LV-diastolic and systolic dimension, and fractional shortening by M-mode echocardiography. Differences between preoperative and postoperative data were estimated using the Wilcoxon signed rank test in SPSS (version 13.0, SPSS Inc, Chicago, IL). p-Value of less than 0.05 was considered significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 Appendix A
 References
 
3.1 Survival and staged operations
There were no early or late deaths. Patients were discharged at a median 9.5 days (range, 7–24) postoperatively. Operative complication was atrial tachyarrhythmia in one patient. Follow-up was completed in all patients for up to 79.1 months (median, 30.3). Seven patients underwent a Fontan procedure and the other three are waiting. Eight patients showed a completely obliterated RV cavity (Table 2 , Fig. 1 ). The obliteration occurred within 3 months follow-up in four patients, at 6–12 months in three patients, and at 18 months in one patient. The latter four patients, whose RV obliteration was delayed, had RV-to-coronary connections before RV exclusion. The other two patients had a remaining RV cavity even after a Fontan operation. One (patient no. 5) of these two patients had small communications between the RV and coronary artery, whose ventricular septum showed flat. The other (patient no. 2) had a large RV cavity and showed abnormal motion of the ventricular septum, which impaired diastolic function of the LV. This patient had previously undergone a modified Blalock–Taussig shunt, right ventricular outflow patch widening, and tricuspid valvotomy during the first stage of palliation. Despite a relatively good RV size (z-value = –1.3), biventricular or one-and-a-half ventricular repair were abandoned because of a poor tricuspid valve function, which had an opening of 2–3 mm, and calcification and fibrosis of the subvalvar apparatus. RV exclusion was performed with tricuspid valve closure at the time of bidirectional cavo-pulmonary shunt. Thrombotic materials were not used in this patient because the RV cavity was too large to fill. An extracardiac conduit Fontan operation with 5 mm fenestration was performed 2 years after the RV exclusion. However, this patient was found to have a large residual RV cavity, decreased LV function, and low arterial oxygen saturation during follow-up. Finally, this patient underwent RV free wall resection (as described by Sano and associates [16]) and reduction of Fontan fenestration, 3.4 years after a Fontan operation. LV function of this patient improved after re-exclusion (Fig. 2 ). Using Doppler tissue imaging assessment, which may reflect the diastolic function, E/E' decreased from 9.4 to 7.4 after re-exclusion.


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  		Table 2 Follow-up results after right ventricular exclusion
 

Figure 1
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  		Fig. 1. (a) Preoperative and (b) postoperative two-dimensional echocardiography (apical four-chamber view) taken at end-systole from the same patient (patient no. 9), who underwent right ventricular thromboexclusion and bidirectional cavo-pulmonary shunt. Note the improvement of prominent septal bulge into the left ventricular outflow tract after exclusion. White arrows indicate left ventricular septal surface.

 

Figure 2
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  		Fig. 2. (a) Preoperative two-dimensional echocardiography taken from a patient (patient no. 2) who had remaining right ventricular cavity after a Fontan operation. This patient had undergone right ventricular exclusion at the time of bidirectional cavo-pulmonary shunt. (b) Postoperative two-dimensional echocardiography taken from the same patient after re-exclusion of the right ventricle. Note the changes of septal configuration at the end-systole (left column, parasternal short axis view) and during diastole (right column, apical four-chamber view). White arrows indicate left ventricular septal surface.

 
3.2 Echocardiographic assessment
In eight of 10 patients, both pre- and post-exclusion echocardiographic parameters obtained during the same admission were available. LV end-diastolic diameter increased after RV exclusion with borderline significance (p = 0.050), whereas LV end-systolic diameter did not show significant change (Fig. 3 ). Follow-up echocardiography revealed that fractional shortening increased after RV exclusion (34.3 ± 5.7% before RV exclusion vs 39.8 ± 3.1% at the last follow-up; p = 0.017) for these eight patients (Fig. 4 ). In all 10 patients, the mean fractional shortening was 40.8 ± 3.6% and there was no evidence of regional ischemia or global dysfunction.


Figure 3
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  		Fig. 3. Acute changes of left ventricular dimension measured by M-mode echocardiography after right ventricular exclusion. Both pre- and postexclusion data obtained during the same admission were available in eight of the 10 patients. Statistical differences were estimated using Wilcoxon signed rank test. Mean ± standard deviation was depicted as a dot and error bars. Abbreviations. LVEDD: left ventricular end-diastolic dimension, LSESD: left ventricular end-systolic dimension.

 

Figure 4
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  		Fig. 4. Serial changes of fractional shortening of the left ventricle by M-mode echocardiography obtained just before and after right ventricular exclusion, and at the last follow-up (n = 8). Fractional shortening at the last follow-up increased significantly compared with pre-exclusion value (p = 0.017). Mean ± standard deviation was depicted as a dot and error bars.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
Appendix A
 References
 
Despite advances in pathophysiologic understanding and in surgical or interventional techniques, therapeutic approaches for patients with PAIVS remain challenging. Recent large multi-institutional or population-based studies [17–19] revealed that the overall survival of PAIVS patients was 57–71% at 1 year and 48–64% at 5 years, and that a successful biventricular repair could only be achieved in about 30%, although the results continue to improve. In addition, Fenton and associates [20] demonstrated a significant interim mortality rate similar to, or somewhat higher than that of hypoplastic left heart syndrome.

There must be a group of PAIVS patients who have to undergo a single ventricle repair. Commonly, these patients have a small, hypertrophied right ventricle with supra-systemic pressure and sinusoidal communications between the RV and the coronary artery [1,2]. The overall frequency of RV-to-coronary artery connections has been reported to range from 31 to 69% [17–19]. Coronary arterial anomalies are also common in this condition [1,2,4,19]. The prevalence of these findings is negatively correlated with RV size [1,19,21]. If these connections progress or persist, the RV will continue to supply desaturated blood into the coronary circulation, which is likely to result in ischemia and subsequent ventricular decompensation [3,5,22]. It has been shown that patients with RV-to-coronary connections and coronary abnormalities have a higher incidence of wall motion abnormalities (which might reflect ongoing ischemia), and that such patients are at risk of late death [5]. Hausdorf and associates [6] found a high degree of coincidence between regional wall motion abnormalities and myocardial perfusion topography resulting from persisting myocardial sinusoids. Fenton and associates [20] attributed the most common cause of interim mortality to abnormal myocardial perfusion. Others have reported myocardial abnormalities including myocardial noncompaction, disarray [22], and endocardial fibroelastosis [10]. These findings suggest that the disease is not limited to the right side, which may explain the poor prognosis of PAIVS. Akiba and associates [9] found left ventricular hypertrophy and signs of acute myocardial ischemia in all their specimens. They speculated that such disease involving the LV could be a limiting factor for long-lasting successful intervention. In addition, they also found a prominent subaortic septal bulge in seven of eight specimens. Zuberbuhler and Anderson [10] found convex bulging of the LV septal surface in 10 of 37 specimens, and Dyamenahalli and associates [19] found mild bulging in 41 (26%) patients, and moderate bulging in 11 (7%) patients from 155 angiograms. This anatomic substrate may contribute to severe obstruction of the left ventricular outflow tract after volume-unloading surgery [23]. Impairment of left ventricular function in patients with PAIVS has been observed after shunt operation [8], bidirectional cavo-pulmonary shunt, a Fontan operation [11], and even after biventricular repair [12].

Some authors believe that RV-to-coronary connections and coronary artery stenosis may progress due to high RV pressure and competitive flow [4,14,15,22], and that high pressure residual RV may impair left ventricular performance after single ventricle repair [11]. One anecdotal report concerned thrombosis in the right ventricle and perioperative brain infarction after bidirectional cavo-pulmonary shunt [24].

Surgical exclusion of the non-functioning RV to prevent the deleterious effects was first described by Waldman and associates [13]. They performed a patch closure of the tricuspid valve with or without RV plication in 10 patients without native coronary arterial stenosis [15]. Seven of the 10 survived the operation. Three of the seven survivors died during follow-up. Only two patients completed a Fontan operation. The authors advocated that the mortality can be reduced by careful selection of patients, and that the sooner (by 6 months of age) RV-to-coronary connection flow is interrupted, the better for coronary arteries and myocardium [15]. Toronto group suggested RV thromboexclusion, which includes closing the tricuspid valve with a patch and filling the cavity with coils or absorbable gelatin sponge [14]. Five of their 12 patients did not survive the operation and post-mortem examinations revealed severe myocardial ischemic damage and high-grade obstruction or interruption of the left coronary artery. The authors recommended that exclusion of the RV be indicated in the presence of RV-to-coronary artery connections without RVDCC [14]. However, follow-up results are not well provided after their initial reports with relatively high mortality. One may hesitate whether to perform the RV exclusion or not, although this has theoretical advantages. In this study, all patients survived the RV exclusion, seven of the 10 completed a Fontan operation, and the other three are waiting for a Fontan in good condition.

Our techniques of RV exclusion involve filling the RV cavity with absorbable gelatin sponge (in the last eight patients) and closing the tricuspid valve directly or with a patch. Several small pieces of gelatin sponge were sufficient to fill the cavity due to the expandable nature of this material. Because these patients usually had thick valve leaflets with a small opening, it was not difficult to close the valve by placing sutures directly on leaflets avoiding damage to the conduction system. Obliteration of the RV cavity would be easier when performed at earlier stage of palliation because the cavity would be smaller and the progression of RV-to-coronary fistula would be prevented earlier.

We did not have definite inclusion criteria of RV exclusion at the beginning. Based on our experiences recently, the following conditions are considered as candidates for RV exclusion: patients with PAIVS without an RVDCC who are unable to support total or partial pulmonary circulation despite a sizable RV cavity, or patients with PAIVS without an RVDCC who have a small RV cavity with RV-to-coronary communications. The identification of those incapable of tolerating a biventricular repair or one-and-a-half ventricular repair remains an unresolved issue, although we also prefer a biventricular repair. The proportions of definitive repair in our 10-year experiences (Fig. 5 ) were not much different from those of recent studies [17–19] with large number of patients.


Figure 5
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  		Fig. 5. A diagram showing the outcome of patients with pulmonary atresia and intact ventricular septum from the last 10-year our institutional experiences. Patients were grouped according to the initial approach (middle row). Upper row displays patients who have not reached definitive repair. Lower row displays patients who have reached definitive repair. Abbreviations. BVP: catheter-based balloon valvuloplasty; RVOT: right ventricular outflow tract widening; Shunt: modified Blalock–Taussig shunt; Others: other procedures including bidirectional cavo-pulmonary shunt (n = 1), closed valvotomy and patent ductus arteriosus banding for prematurity (n = 1), and right ventricular outflow tract widening (n = 1).

 
Postoperative increases of LV-end-diastolic dimension were of borderline significance (p = 0.050) whereas LV-end-systolic dimension did not change significantly, which encourages us to suggest that something restricting LV diastolic movement has been eliminated after operation. Fractional shortening of the LV increased immediately after RV exclusion (Fig. 4) and LV function was well maintained during follow-up regardless of staged procedures. RV exclusion might play a role in the prevention of LV dysfunction in these high-risk patients.

There are several limitations in this study. Because of the retrospective nature of this study, we could not provide complete echocardiographic parameters despite all patients having been completely followed up. We did not pay much attention to the parameters that could demonstrate the changes of LV diastolic function, especially for neonates or small infants. To compare the perioperative changes, the only available data that had been constantly measured were M-mode echocardiographic data in eight of the 10 patients. The number of patients is too small to get definite answers although we showed excellent clinical results. In addition, perioperative measurements might have been confounded by the effects of palliative procedures, which would cause either volume loading (systemic-to-pulmonary shunt) or unloading (cavo-pulmonary anastomosis) of the LV. Also, there is no reference value of echocardiographic parameters of these patients with heterogeneous single ventricle physiology at the different stage of palliation. Scarcity of this category of disease makes it difficult to perform a controlled study and to have definite indications for this procedure from the beginning of study.

In conclusion, the present study demonstrates that RV exclusion may be performed safely in a selected group of patients with PAIVS. This procedure may have beneficial effects on LV systolic function by preventing possible ischemia, and on LV diastolic function by obliterating the non-functioning cavity and improving the geometry of the ventricular septum.


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

Dr S. Sano (Okayama, Japan): If the right ventricle (RV) and the tricuspid valve (TV) are slightly hypoplastic like your case, we perform one and a half ventricular repair rather than Fontan procedure as long as the patient has no major RV-to-coronary artery communications. As long as I see from your video, the TV and the RV looks large enough to perform one and a half ventricular repair. But which is better the exercise tolerance, either the patients with Fontan or the patients with one and a half ventricular repair? I do not know which is better. Do you have any experience of one and a half ventricular repair in patients with PAIVS, and do you have any data of exercise tolerance in your patients?

Dr Yang: The first question, the identification of those incapable of tolerating total or partial biventricular repair remains an unsolved issue. This cannot be answered in this study. But our concern is that it is important to achieve good tricuspid valve inflow to make a patient a good candidate for biventricular repair. And, the proportions of definitive repair in our 10-year experiences of pulmonary atresia and intact ventricular septum (showing the same figure in the article) were not much different from those of recent studies with large number of patients.

The second question, we have two patients with one and a half ventricular repair in this patient group. As Dr Sano said, many authors have reported that the functional capacity in this patient group is not as good as we expected. In our experience, there are two other patients who underwent one and a half ventricular repair and converted to single ventricular repair.


   Footnotes
 
\#9734; Presented at the 21st Annual Meeting of the European Association for Cardio-thoracic Surgery, Geneva, Switzerland, September 16–19, 2007.


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

  1. Calder AL, Co EE, Sage, MD. Coronary arterial abnormalities in pulmonary atresia with intact ventricular septum. Am J Cardiol 1987;59:436-442.[CrossRef][Medline]
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