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Ann Thorac Surg 2011;92:666-672. doi:10.1016/j.athoracsur.2011.04.024
© 2011 The Society of Thoracic Surgeons
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Original Articles: Pediatric Cardiac

Early Outcomes of Primary Sutureless Repair of the Pulmonary Veins

Anthony Azakie, MDa,b,c,*, Michael J. Lavrsen, MDd, Natalie C. Johnson, BSa,b, Anil Sapru, MDa,c

a UCSF Benioff Children's Hospital, University of California-San Francisco, San Francisco, California
b Department of Surgery, University of California-San Francisco, San Francisco, California
c Department of Pediatrics, University of California-San Francisco, San Francisco, California
d Department of Surgery, Oregon Health Sciences University, Portland, Oregon

Accepted for publication April 1, 2011.

* Address correspondence to Dr Azakie, 513 Parnassus Ave, Rm S-549, Box 0117, San Francisco, CA 94143 (Email: tony.azakie{at}ucsfmedctr.org).

Presented at the Forty-seventh Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2011.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 
Background: The "sutureless" repair technique has improved outcomes for post-repair pulmonary vein (PV) stenosis. The purpose of this study is to determine the early outcomes of primary sutureless repair of pulmonary venoocclusive disease in infants with congenital PV stenosis-hypoplasia or PVs at high risk for progressive stenosis.

Methods: This is a retrospective review of infants who had primary sutureless repair of the PVs from October 2002 to April 2010.

Results: Twenty-five infants had primary sutureless repair of the PVs. Eighteen infants had total anomalous pulmonary venous return; 14 with obstruction, 10 with heterotaxy syndrome, and 9 with univentricular anatomy. Seven infants had congenital PV stenosis. There were 24 perioperative survivors (96%; 95% confidence interval [CI], 75% to 99%) and 2 late deaths from extracardiac causes. Follow-up was available on 21 out of 22 survivors at a median duration of 34 months (range, 9 to 100 months). Persistence-recurrence of PV stenosis occurred in 3 veins (3%) of 2 infants (8%). On follow-up echocardiography, right ventricular systolic pressure was normal in 13 out of 14 infants with a biventricular heart and 60% of systemic blood pressure in 1 infant. Kaplan-Meier 1-year cumulative survival was 88% (95% CI, 66% to 96%). Kaplan-Meier cumulative disease-free survival was 96% (95% CI, 75% to 99%) at 30 days and 84% (95% CI, 58% to 95%) at 1 year. By Cox proportional hazards, age, univentricular anatomy, and atrial isomerism-heterotaxy syndrome were not associated with an increased risk of death or persistence-recurrence. One-year disease-free survival was lower in infants with prematurity (p = 0.0055) and low birth weight (p = 0.0011).

Conclusions: Primary sutureless repair is a feasible, safe, and relatively effective method of addressing congenital PV stenosis and (or) high-risk PVs, particularly in infants with single ventricle anatomy and (or) heterotaxy syndrome.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Discussion
 References
 
Pulmonary vein stenosis (PVS) continues to be a difficult clinical problem in children. It occurs as a congenital lesion or can be acquired, particularly after repair of total anomalous pulmonary venous drainage [1, 2]. The strategies that have historically been used to address PVS in the pediatric population, including patch venoplasty, balloon dilation, vein stenting, or anastomotic revision, have met with failure, high morbidity, and mortality. The "sutureless" repair technique has been relatively effective in treating post-repair PVS, which develops in approximately 5% to 15% of cases where total anomalous pulmonary venous return (TAPVR) is corrected using standard techniques [3, 4]. There may be an increased likelihood of progressive PVS in patients with infracardiac type TAPVR, or those with associated pulmonary vein hypoplasia or stenosis. The consequences of relentless or progressive PVS are highly morbid and potentially fatal. As a result, we have used primary sutureless repair of the pulmonary veins in neonates and infants with congenital PVS or those with TAPVR with associated atrial isomerism-heterotaxy syndrome, infracardiac or mixed type drainage patterns, or pulmonary vein hypoplasia or stenosis.

Reports on the use of the sutureless technique as a primary procedure for the repair of pulmonary veins are limited [5, 6]. In the current study, we report early outcomes for primary sutureless repair of pulmonary venoocclusive disease in patients with high-risk lesions.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 References
 
Patient Population
The pediatric cardiac surgery database at the University of California, San Francisco was queried for all infants having repair of anomalous pulmonary venous drainage from October 2002 to April 2010. Neonates and infants having primary sutureless repair of the pulmonary veins were identified and were retrospectively reviewed. Demographic, operative and postoperative, and echocardiographic data were prospectively collected and retrospectively analyzed. Follow-up characteristics were collected from in-hospital charts and the records of ambulatory clinic visits. Additional follow-up information was obtained from outpatient cardiology offices. Survival information was also obtained and verified by querying public databases. Permission to perform the study was obtained from the Committee on Human Research at the University of California San Francisco and, due to its retrospective nature, need for patient consent was waived.

Surgical Technique
The operative techniques are illustrated in Figure 1 .


Figure 1
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  		Fig 1. Operative techniques. (A) In situ pericardial marsupialization for right-sided pulmonary vein stenosis. A similar approach is used for left-sided pulmonary vein stenosis (not illustrated). (B) Atrial cuff to posterior pericardial anastomosis. See text for details. (Ao = aorta; IVC = inferior vena cava; LA = left atrium; PA = pulmonary artery; PV = pulmonary vein; RA = right atrium; SVC = superior vena cava.)

 
Atrial Cuff to Posterior Pericardial Anastomosis
The sutureless repair was generally performed using standard cardiopulmonary bypass with prolonged cooling into deep hypothermia. Under circulatory arrest, in the setting of TAPVR the venous confluence was opened and longitudinal incisions were carried into each pulmonary venous tributary up to the pleuropericardial junction. Abnormal, obstructive, or fibrotic pulmonary venous tissue was excised as necessary. An incision was made along the posterior wall of the atrium and this was then sutured with fine polypropylene suture to the posterior pericardium and mediastinal adventitia. No direct suturing into the pulmonary venous channels was performed. There were no cases of hemorrhage into the posterior mediastinum or pleural spaces. Intrapleural hilar reapproximation was not necessary [7].

In Situ Pericardial Flap Repair
For infants with single ventricle and mixed TAPVR or those with biventricular anatomy and congenital PVS, sutureless pericardial marsupialization techniques were applied. The veins were incised longitudinally, excess pathologic or fibrotic tissue was excised, and in situ pericardial flaps were sewn as described by Lacour-Gayet and colleagues [8, 9] and Najim and colleagues [10]. The phrenic nerve was mobilized in all cases. There were no cases of postoperative phrenic nerve palsy necessitating diaphragm plication.

Statistical Analysis
Data are expressed as frequencies, means with standard deviations, or medians with ranges. Cumulative survival data are reported using the Kaplan-Meier method. Comparisons of cumulative survival were made by the log-rank test for equality of survival functions. A Cox proportional hazards analysis was fitted with time to death or recurrence of PVS and Cox proportional hazards regression analysis was performed to assess the effects of clinically significant covariates including age at operation, single ventricle anatomy-physiology, atrial isomerism-heterotaxy syndrome, low birth weight, prematurity, and severity of preoperative pulmonary venous obstruction. Analysis was carried out using STATA 11 software package (Stata Corp, College Station, TX). A p value of 0.05 was empirically set as statistically significant.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 References
 
Patient Characteristics
Twenty-five neonates or infants had primary sutureless repair of the pulmonary veins at a median age of 18 days (range, 1 day to 6 months) and median weight of 3.6 kg (range, 2.5 to 6.3 kg). Seven out of 25 (28%) were premature or had a gestational age less than 37 weeks. Eighteen infants had TAPVR, 14 with obstruction. Ten infants had atrial isomerism-heterotaxy syndrome, 9 of whom had single ventricle anatomy or physiology. Seven infants had primary sutureless repair for normally draining veins that were congenitally stenotic or hypoplastic. Anatomic details are summarized in Table 1.


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  		Table 1 Demographic, Diagnostic, and Preoperative Data
 
Operative Details
At the time of primary sutureless repair, 5 infants had associated systemic to pulmonary arterial shunting, 3 infants had bidirectional cavopulmonary anastomosis, 2 infants had atrioventricular valve repair, and another 2 infants had pulmonary artery banding. Extracorporeal life support was initiated at the end of the procedure in 5 neonates who had right atrial isomerism (RAI)-heterotaxy syndrome, repair of TAPVR with insertion of a Blalock-Taussig shunt so as to protect from sudden death due to potential severe atrial tachyarrhythmias, supraventricular tachycardia, or pulmonary hypertensive crises. Operative details are summarized in Table 2.


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  		Table 2 Perioperative Data
 
Perioperative Mortality, Survival, and Follow-Up
A flow diagram of the cohort of patients who had primary sutureless repair of the pulmonary veins is shown in Figure 2 . Postoperative outcomes, complications, and hospitalization details are summarized in Table 3. There were 24 out of 25 perioperative survivors. Cumulative survival at 30 days was 96% (95% confidence interval [CI], 75% to 99%). The only early death occurred in an infant who had RAI-heterotaxy syndrome, TAPVR, and single ventricle who succumbed to refractory sepsis. There were 2 late deaths, both after a general surgical procedure 3 to 4 months after the original repair. One patient was lost to follow-up. Long-term follow-up was available on 21 out of 22 survivors with a median duration of 34 months (range, 9 to 100 months). The Kaplan-Meier 1-year cumulative survival was 88% (95% CI, 66% to 96%), as shown in Figure 3 .


Figure 2
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  		Fig 2. Flow diagram of the cohort of patients having primary sutureless repair of the pulmonary veins from October 2002 to April 2010. (NYHA = New York Heart Association; PVS = pulmonary vein stenosis; TAPVR = total anomalous pulmonary venous return.)

 

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  		Table 3 Postoperative Outcomes Data
 

Figure 3
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  		Fig 3. Kaplan-Meier cumulative survival. The 95% confidence interval (CI) is shown. The numbers of subjects at risk are below the horizontal axis.

 
On follow-up echocardiography, right ventricular systolic pressure was normal in 13 of 14 infants with biventricular anatomy. In the remaining 1 patient with biventricular anatomy, right ventricular systolic pressure was estimated to be 60% of systemic blood pressure. Persistence or recurrence of PVS was present in 3 veins (3%) among 2 patients (8%) at follow-up. One infant with congenital PVS and pulmonary vein hypoplasia had incomplete relief of obstruction in the left lower pulmonary vein, possibly due to compression between the descending thoracic aorta and heart. There was no reintervention and at 3 years postoperative, the patient is clinically well, active, and asymptomatic. Another infant with congenital PVS, pulmonary orificial fibrosis, and intraparenchymal stenosis and hypoplasia developed progressive PVS in 2 veins after the original repair and required reoperation at 10 months postoperatively.

The Kaplan-Meier disease-free survival was 96% (95% CI, 75% to 99%) at 30 days and 84% (95% CI, 58% to 95%) at 1 year. The cumulative disease-free survival overall and among patients categorized on the basis of low birth weight, prematurity, and heterotaxy syndrome is presented in Figure 4 (A, B, C, and D). One year cumulative disease-free survival was lower in patients with low birth weight (50% vs 95%, p = 0.0011) and prematurity (63% vs 94%, p = 0.0055). One-year cumulative survival and disease-free survival were also slightly lower in patients with atrial isomerism-heterotaxy syndrome, but this trend did not reach statistical significance (80% vs 93%, p = 0.346 and 75% vs 90%, p = 0.935).


Figure 4
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  		Fig 4. Kaplan-Meier cumulative disease-free survival. The 95% confidence interval (CI) is shown. The numbers of subjects at risk are below the horizontal axis. Overall disease-free survival is shown in (A). Survival curves are stratified by low birth weight (Bwt; B), p = 0.0011, prematurity (C), p = 0.0055, and atrial isomerism-heterotaxy syndrome (D), p = 0.935.

 
Although the sample size (n = 25) and number of outcomes measured were low, a Cox proportional hazard analysis was performed to test for the effect of other clinically significant covariates on disease-free survival. Age, single ventricle anatomy, and atrial isomerism-heterotaxy syndrome were not associated with an increased risk of death or persistent-recurrent pulmonary venous obstruction (p = 0.7865, p = 0.3420, and p = 0.9352, respectively).


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 References
 
Recently, the indications for sutureless repair of the pulmonary veins as a primary operation have been extended for infants who have congenital PVS or those at risk for developing PVS after repair of TAPVR [5, 6, 11]. The primary sutureless repair seems to be safe and effective. We have selectively applied these techniques as the first line therapeutic option in infants with congenital PVS or pulmonary vein hypoplasia. The operation has also been used prophylactically in patients at high risk for developing post-repair PVS, including those with RAI, single ventricle anatomy, and TAPVR or those with infracardiac type TAPVR with so-called "inverted Christmas tree" pattern, or those with mixed pattern TAPVR. The 1-year cumulative survival was 88% and was lower in infants with low birth weight or prematurity, but not in infants operated at a younger age or with single ventricle anatomy or RAI-heterotaxy syndrome.

Survival Outcomes for Complex TAPVR
Survival after standard repair of TAPVR is negatively impacted in the setting of single ventricle physiology with associated atrial isomerism-heterotaxy syndrome, severe preoperative pulmonary venous obstruction, and younger age. A review from the Children's Hospital of Philadelphia for infants with single ventricle and TAPVR showed that the early mortality was 53% with a 5-year survival of only 19% [12]. In a more recent analysis, Lodge and colleagues [13] reported improvements in early survival but intermediate survival was still approximately 50%. Younger age at first operation was an independent risk factor for adverse outcome and may have been a marker for severity of disease or associated cardiac conditions. In contrast, age was not a risk factor for adverse outcome in the current series.

Similar to the recent Children's Hospital of Philadelphia report, heterotaxy was not a risk factor for adverse outcome in our series. While we did not find an increased risk of adverse outcomes in infants with heterotaxy syndromes, a number of studies have shown high mortality rates for repair of TAPVR in the setting of RAI, especially if severe pulmonary venous obstruction or pulmonary atresia were present. Hashmi and colleagues [14] reported on outcomes in neonates and infants with RAI. The mortality rate for patients who had the first cardiovascular operation in the neonatal period was 75% versus 51% for those with later first cardiovascular operation. The surgical mortality for patients who had pulmonary vein repair was 95%.

A recent report by Yun and colleagues [11] showed that the contemporary management of RAI with TAPVR continues to have high mortality, but results are improving. The authors report the use of primary sutureless repair for management of pulmonary venous obstruction and an associated improvement in survival. The same group recently reported on primary sutureless repair in infants with mixed TAPVR and concluded that the technique was safe and effective, with improving trends in survival and reintervention rates. The survival benefit in the primary sutureless era is probably due to a number of factors, including improvements in perioperative management of shunted single ventricle physiology and possibly improvements in surgical technique. In our experience, 10 patients had atrial isomerism-heterotaxy syndrome with 80% survival at last follow-up. We have selectively used prophylactic extracorporeal life support after repair of obstructed TAPVR in the setting of single ventricle physiology necessitating systemic to pulmonary arterial shunting in order to help neutralize potentially life-threatening events, such as pulmonary hypertensive crises or supraventricular tachyarrhythmias, in the postoperative period. We, like others, cannot infer that the improving early survival rates are due solely to application of the primary sutureless operation [5]. However, it is possible that the use of primary sutureless repair of the pulmonary veins in this patient cohort may have an early survival advantage by protecting against early subclinical PVS, which may develop after repair using conventional techniques.

Honjo and colleagues [5] recently reported their early to midterm outcomes with primary sutureless repair for infants with mixed TAPVR, where they found that the technique was safe with no mortality and no need for early reintervention. The authors note that anomalous right upper pulmonary veins to the superior vena cava may remain unrepaired and that this physiology is well tolerated in the postoperative period. Our strategy is to divert and repair anomalous right upper pulmonary veins, particularly in the setting of single ventricle anatomy and heterotaxy syndrome, using in situ pericardial marsupialization sutureless techniques. We have had no complications with this approach.

Both prematurity and low birth weight (2 strongly related conditions) were associated with lower 1-year disease-free survival. In a recent multiinstitutional analysis, the Society of Thoracic Surgeons Congenital Heart Database reported that low birth weight continues to be an independent risk factor for adverse outcome after reparative or palliative neonatal cardiac surgery [15]. Lower weight babies had significantly higher mortality for specific operations including repair of TAPVR. Of note, there seems to be a relationship between the development of PVS or pulmonary vein mal-development and prematurity. The etiology is unclear but may be related to intimal proliferation in the setting of bronchopulmonary dysplasia [16].

In our series, 2 patients had persistent-recurrent disease. Both had congenital PVS as the primary lesion. Despite the absence of retrocardiac adhesions, we have aggressively incised the veins into the hilum in this patient subgroup, without any adverse bleeding events into the pleural or posterior mediastinal spaces, and completed the repair using sutureless pericardial marsupialization [2]. Progressive PVS after repair of TAPVR may be due to an exuberant healing response or technical issues. This may be the case in patients who have different forms of repair for congenital PVS. However, in this patient subpopulation the progression in PVS may be due to a primary developmental abnormality. Primary sutureless repair may be effective for repair in infants with discrete congenital PVS. Those with pulmonary vein hypoplasia or disease that extends into the intraparenchymal region despite aggressive management pose a significant challenge, particularly if the process is a biologically preprogrammed event.

In conclusion, sutureless repair techniques were selectively applied as the primary treatment option in infants with congenital PVS or pulmonary vein hypoplasia, and used prophylactically in infants with TAPVR at high risk for developing post-repair PVS. Primary sutureless repair is feasible, safe, and relatively effective with very good early survival and freedom from reintervention. The techniques are particularly effective in infants with single ventricle anatomy and (or) atrial isomerism-heterotaxy syndrome. Infants with prematurity and (or) low birth weight may have lower disease-free survival that pose an important future challenge.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
References
 
DR PETER MANNING (Cincinnati, OH): Just a quick technical question. You said you were relatively surprised by the lack of bleeding complications given no previous dissection and consequently the lack of pericardial adhesions. How much posterior dissection did you do in these cases before opening the confluence of veins? Also, because some of these kids were total veins cases, what did you do with the vertical vein? Did you dissect that out or leave it alone?

DR AZAKIE: The approach for all patients with biventricular hearts or single ventricle anatomy was to identify the central and anterior portion of the confluence, make an incision in it, carry that right up to the pleuropericardial junction and then use the "atrial cuff" technique.

If the child had single ventricle anatomy or physiology, we did not dissect or ligate the draining vein. If a biventricular heart was present, then only in a very few selected cases did we perform a minimal dissection. The draining vein was ligated and left it in situ; it was not divided. We usually just leave it alone.

DR MANNING: Yes, I think the group from Toronto presented a similar series at the AATS [American Association for Thoracic Surgery] meeting and they don't do anything to the vertical vein.

We learned it the hard way. We dissected a vertical vein in an infradiaphragmatic total veins case, and just by dissecting that plane we created a space for bleeding to occur. We ended up having to bail on the sutureless technique and go to a more traditional repair. So I think that a key issue in these kids who don't have the adhesions is to limit your dissection and just open up the confluence and leave it at that.

DR AZAKIE: I might add, if the patients had any orificial disease, then we generally did a partial excision of the abnormal tissue. Near the draining vein one can take larger bites if necessary.

I think there was a slight difference between our patient population and the Toronto population. In their most recent report the technique was applied selectively in patients with simple total anomalous pulmonary venous return. We selectively used the sutureless technique in patients who had known congenital pulmonary vein stenosis or who we thought were at risk for developing progressive pulmonary vein stenosis.

DR PEDRO DEL NIDO (Boston, MA): Tony, this is an outstanding technical result and I congratulate you.

The one thing that you should elaborate on, if I understand what you're proposing, is whether this is really a prophylactic measure in patients who you suspect are at risk. I noted your average patient age was about 18 days and only some presented with obstructed anomalous pulmonary venous return.

One, tell me what the parameters were that made you decide to perform this procedure. Were they intraoperative, or did you decide this preoperatively on the basis of some imaging study?

Two, also, what is the basis for doing this? In other words, do you have a comparison group? Because you're always going to be held at a slightly higher standard when you're proposing a new paradigm. I'm not saying I disagree; in fact, I think it's a good idea. But what's the basis by which you're improving the outcomes, or at least you think you're improving the outcomes?

DR AZAKIE: With regards to the first question, that is, how did we select patients for a prophylactic operation, the decision to do so was not based on a comparison group. We do not have a concurrent comparison group nor a baseline group of patients in which we operated on in a previous era and found that the results were unfavorable in terms of survival or development of subsequent pulmonary vein stenosis. It was based on previous experience of other groups and published reports by and from other groups.

It has been shown that neonates with TAPVR and right atrial isomerism, with or without pulmonary atresia, were at very high risk for death. And those who didn't have obstructed total veins with pulmonary atresia, in other words, those who didn't need shunted single ventricle physiology in the setting of total veins, did have significant mortality hazard as well as an important incidence or recurrence of pulmonary vein stenosis. So based on the experience from other groups, we felt that patients who had right atrial isomerism or heterotaxy syndrome were an important group where the development of pulmonary vein stenosis was an important concern. And I think other groups from Paris, Denver, and Michigan have shown that.

DR DEL NIDO: Right. So you're using the literature historical controls for the heterotaxy group.

DR AZAKIE: Yes, that's correct.

DR DEL NIDO: What about the patients who just had anomalous pulmonary venous return; how did you make the decision to apply this approach? Was it purely intraoperative or did you do something special preoperatively to help you make that decision?

DR AZAKIE: We made the decision preoperatively to include those who had heterotaxy syndrome or single ventricle anatomy. And the third pattern was the infracardiac Christmas tree patterns where we thought, and that again was based on past experience in the literature, that those patients were prone to developing progressive or recurrent stenosis.

The intraoperative decision to proceed with this approach was made when we felt that a vein appeared hypoplastic or fibrotic, or there was some orificial stenosis that we didn't see on echo. So then with regards to improving early mortality outcomes, I'm not entirely sure that we can say that primary sutureless repair in and of itself is responsible for reducing early hazard of mortality, particularly in the high-risk groups. I think it's a combination of things, including improved management of infants with shunted single ventricle physiology as well as the application of prophylactic ECLS [extracorporeal life support] to prevent sudden death from pulmonary hypertensive crisis or SVT [supraventricular tachycardia], to which many of the right isomerism patients are prone. Primary sutureless repair may however minimize the likelihood of early or midterm recurrent venous obstruction and the associated morbidity and mortality.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 

  1. Devaney EJ, Chang AC, Ohye RG, Bove EL. Management of congenital and acquired pulmonary vein stenosis Ann Thorac Surg 2006;81:992-996.[Abstract/Free Full Text]
  2. Devaney EJ, Ohye RG, Bove EL. Pulmonary vein stenosis following repair of total anomalous pulmonary venous connection Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 2006:515.
  3. Caldarone CA, Najm HK, Kadletz M, et al. Relentless pulmonary vein stenosis after repair of total anomalous pulmonary venous drainage Ann Thorac Surg 1998;66:1514-1520.[Abstract/Free Full Text]
  4. Lacour-Gayet F. Surgery for pulmonary venous obstruction after repair of total anomalous pulmonary venous return Semin Thorac Cardiovasc Surg Pediatr Card Surg Annu 2006:4550.
  5. Honjo O, Atlin CR, Hamilton BC, et al. Primary sutureless repair for infants with mixed total anomalous pulmonary venous drainage Ann Thorac Surg 2010;90:862-868.[Abstract/Free Full Text]
  6. Yun TJ, Coles JG, Konstantinov IE, et al. Conventional and sutureless techniques for management of the pulmonary veins: Evolution of indications from postrepair pulmonary vein stenosis to primary pulmonary vein anomalies J Thorac Cardiovasc Surg 2005;129:167-174.[Abstract/Free Full Text]
  7. Konstantinov IE. Primary sutureless repair of total anomalous pulmonary venous connection: the value of intrapleural hilar reapproximation J Thorac Cardiovasc Surg 2006;132:729-730.[Free Full Text]
  8. Lacour-Gayet F, Rey C, Planche C. Pulmonary vein stenosis. Description of a sutureless surgical procedure using the pericardium in situ. Arch Mal Coeur Vaiss 1996;89:633-636[Article in French].[Medline]
  9. Lacour-Gayet F, Zoghbi J, Serraf AE, et al. Surgical management of progressive pulmonary venous obstruction after repair of total anomalous pulmonary venous connection J Thorac Cardiovasc Surg 1999;117:679-687.[Abstract/Free Full Text]
  10. Najm HK, Caldarone CA, Smallhorn J, Coles JG. A sutureless technique for the relief of pulmonary vein stenosis with the use of in situ pericardium J Thorac Cardiovasc Surg 1998;115:468-470.[Free Full Text]
  11. Yun TJ, Al-Radi OO, Adatia I, et al. Contemporary management of right atrial isomerism: effect of evolving therapeutic strategies J Thorac Cardiovasc Surg 2006;131:1108-1113.[Abstract/Free Full Text]
  12. Gaynor JW, Collins MH, Rychik J, Gaughan JP, Spray TL. Long-term outcome of infants with single ventricle and total anomalous pulmonary venous connection J Thorac Cardiovasc Surg 1999;117:506-514.[Abstract/Free Full Text]
  13. Lodge AJ, Rychik J, Nicolson SC, Ittenbach RF, Spray TL, Gaynor JW. Improving outcomes in functional single ventricle and total anomalous pulmonary venous connection Ann Thorac Surg 2004;78:1688-1695.[Abstract/Free Full Text]
  14. Hashmi A, Abu-Sulaiman R, McCrindle BW, Smallhorn JF, Williams WG, Freedom RM. Management and outcomes of right atrial isomerism: a 26-year experience J Am Coll Cardiol 1998;31:1120-1126.[Medline]
  15. Curzon CL, Milford-Beland S, Li JS, et al. Cardiac surgery in infants with low birth weight is associated with increased mortality: analysis of the Society of Thoracic Surgeons Congenital Heart Database J Thorac Cardiovasc Surg 2008;135:546-551.[Abstract/Free Full Text]
  16. Drossner DM, Kim DW, Maher KO, Mahle WT. Pulmonary vein stenosis: prematurity and associated conditions Pediatrics 2008;122:e656-e661.[Abstract/Free Full Text]



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