Congenital pulmonary vein (PV) stenosis with anatomically
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1 Pulmonary Vein Stenosis With Normal Connection: Associated Cardiac Abnormalities and Variable Outcome John P. Breinholt, BS, John A. Hawkins, MD, LuAnn Minich, MD, Lloyd Y. Tani, MD, Garth S. Orsmond, MD, Saskia Ritter, MD, and Robert E. Shaddy, MD Departments of Pediatrics and Surgery, Primary Children s Medical Center and University of Utah, Salt Lake City, Utah Background. Pulmonary vein (PV) stenosis with anatomically normal connection is considered rare, unresponsive to treatment, progressive, and usually fatal. Methods. We reviewed the records of 13 children with this diagnosis at our center since Results. The number of stenosed PVs ranged from all PVs (n 5); three PVs (n 1); two PVs (n 5); and one PV (n 2). All patients had associated congenital cardiac abnormalities. Operation on PV stenosis was attempted in 7 patients (54%), 2 of whom have done and 5 of whom have not. Two patients underwent heart transplantation for inoperable associated cardiac lesions. Significantly more patients with three or four stenosed PVs died (83%) compared with patients with one or two stenosed PVs (0%). Conclusions. (1) Pulmonary vein stenosis with anatomically normal connection is associated with other congenital cardiac abnormalities, (2) presentation and outcome are contingent on the number of stenosed PVs, (3) surgical palliation may be helpful in some patients, and (4) heart transplantation for inoperable associated cardiac abnormalities may be an option in patients with only one or two stenosed PVs. (Ann Thorac Surg 1999;68:164 8) 1999 by The Society of Thoracic Surgeons Congenital pulmonary vein (PV) stenosis with anatomically normal connection is rare and generally leads to progressive pulmonary hypertension and cardiac failure in infancy. Traditionally, this has been thought to be a lesion that is essentially unresponsive to treatment and usually associated with high mortality. The purposes of this study were to determine the associated cardiac abnormalities, the results of surgical intervention, and the varied presentations and outcomes of PV stenosis with anatomically normal PV connection. Material and Methods We evaluated the medical records, echocardiograms, and catheterization reports of children diagnosed with PV stenosis with anatomically normal PV connection at Primary Children s Medical Center between June 1990 and June We excluded all patients with anomalous PV return. We determined demographic variables, associated cardiac anomalies, types and outcomes of operations, and overall outcomes in all patients. In addition, the initial echocardiograms in those patients not diagnosed with PV stenosis at presentation were reviewed. Accepted for publication Jan 14, Address reprint requests to Dr Shaddy, Division of Pediatric Cardiology, Primary Children s Medical Center, Suite 1500, 100 North Medical Dr, Salt Lake City, UT 84113; pcrshadd@ihc.com. Imaging Complete two-dimensional and Doppler echocardiograms were performed on all patients at the time of presentation and for at least one follow-up evaluation. All four PVs were identified with color Doppler techniques. If a mosaic-colored jet was seen, flow was considered to be turbulent, and pulsed and continuous wave Doppler was performed with attention to intercept angle, wall filters, and velocity scale. Pulmonary veins were considered obstructed if the Doppler pattern showed nonphasic flow or velocities greater than 1.6 m/s [1, 2]. Cardiac catheterization diagnosis of PV stenosis was based on angiographic evidence of stenosis from the levophase of pulmonary arterial injections and significant pressure gradients between the pulmonary capillary wedge pressure and the left atrial pressure (or left ventricular end-diastolic pressure when the left atrium could not be entered). Operative Procedures All patients who underwent operative correction of PV stenosis and associated defects underwent standard hypothermic cardiopulmonary bypass with bicaval cannulation. Moderate and profound hypothermia was used. Circulatory arrest was used only for brief periods of time to optimize visualization of the PVs. Standard blood potassium cardioplegic arrest was used. The operative technique for relief of PV stenosis varied according to the anatomic situation. For localized stenosis at the orifice of a PV, we excised the stenotic ring as 1999 by The Society of Thoracic Surgeons /99/$20.00 Published by Elsevier Science Inc PII S (99)
2 Ann Thorac Surg BREINHOLT ET AL 1999;68:164 8 PULMONARY VEIN STENOSIS WITH NORMAL CONNECTION 165 previously described [3]. We then reestablished endothelial cell integrity by anastomosing the PV endothelium to the atrial endocardium using interrupted polypropylene sutures. For long segment stenosis, or stenosis proximal to the PV ostia, we used a pericardial [4]. Comparisons between groups were made using a Mann-Whitney U test, or Fisher s exact test. All data are expressed as mean standard deviation. Differences were considered statistically significant for p Results Thirteen children satisfied our inclusion criteria. The age of the patients at diagnosis ranged from 2 months to 17 years (median age, 4 months). Five of the patients were girls and 8 were boys. Diagnosis was made by echocardiography (and confirmed by catheterization) in 11 cases and by catheterization in 2 patients whose prior echocardiograms were noncontributory. All patients had associated congenital cardiac abnormalities, some of whom had more than one abnormality. The number of PVs involved was variable. Table 1 addresses the demographics, associated lesions, and affected pulmonary veins. The progression of the disease also varied. Those patients with three or four stenosed PVs presented with symptoms earlier ( months old, median age 4 months) than those with one or two stenosed PVs (37 73 months old, median age 9 months) ( p 0.05). Pulmonary vein stenosis was a component of the initial cardiac assessment in only 3 patients (23%), and therefore was not identified until subsequent evaluation in 10 patients (77%) months after their initial presentation with associated cardiac lesions and symptoms. Review of initial echocardiograms in those patients not diagnosed on initial presentation showed normal color Doppler flow patterns in the PVs of all patients without evidence of obstruction. In 3 cases, the patient initially exhibited stenosis in a limited number of PVs that later involved additional veins (three initial PVs to four PVs involved, one initial PV to two PVs, and two initial PVs to four PVs). In 4 patients with four affected PVs, one side had significantly more stenosis than the other side. The child with three stenosed PVs had more severe stenosis in the right PVs as compared with the single left PV affected. In all 4 patients with two affected PVs, the two PVs drained from the same lung. Pulmonary Vein Surgery Patients Surgical repair of stenosed PVs was attempted in 7 patients (54%) simultaneous with intracardiac repair of associated anomalies. Surgery technique noted in Table 1. All 7 patients exhibited laminar flow by postoperative echocardiography. Two patients have shown symptomatic improvement since operation, both of whom had discrete stenosis at the orifice of the stenosed PV and underwent excision of the stenotic ring. At 3 years after operation, the child with one affected PV exhibited normal pulsed and color Doppler echocardiographic flow in the repaired right upper PV without signs of obstruction or pulmonary hypertension. At 4 years after operation, the child with stenosis of the common orifice of the two left PVs exhibited normal, low-velocity phasic flow from the repaired PVs by echocardiography. Four children with four stenosed PVs received surgical palliation resulting in poor outcomes. In these patients, only the one or two most severely affected PVs were attempted to be repaired surgically. The decision of which veins would be surgically corrected was made intraoperatively when the pulmonary veins could be visually inspected. Some individual pulmonary veins were believed to be inoperable and were not repaired when the degree of stenosis involved too long a segment or was too severe. Within 1 to 2 months, 3 of these patients manifested increasing stenosis by echocardiography, and the remaining child exhibited significant obstruction within 5 months. Three of these children died 1, 3, and 5 months after operation, and the fourth patient has severe stenosis with recurrent respiratory infections. No Pulmonary Vein Surgery Patients No PV operation was performed in 6 patients (46%). Two patients received heart transplants because of a right ventricle dominant atrioventricular septal defect with valvar pulmonary stenosis in one patient and a severe Ebstein s anomaly with dilated left ventricular cardiomyopathy in the other. Intraoperative inspection of the PVs revealed a virtually atretic left lower PV in 1 patient, and stenotic left PVs (the upper vein was nearly atretic with a less than 1-mm lumen; the lower vein measured about 3.5 mm) in the other patient (Table 1, patients 12 and 11, respectively). No repair of the stenosed PVs remaining with the heart transplant recipient was attempted. Both have done at 6 and 11 months after transplantation with mean pulmonary artery pressures of 22 mm Hg and 20 mm Hg, respectively. Two patients, 1 with three stenosed PVs and 1 with four stenosed PVs, died of progressive pulmonary hypertension at 3 and 6 months after diagnosis of PV stenosis, respectively. The 2 remaining unoperated patients, each with two stenosed PVs, remain stable with moderate to severe pulmonary hypertension and echocardiographic evidence of increasing stenosis. Pathology Autopsies were performed on 2 patients (Table 1, patients 1 and 2) who underwent operation to repair stenosed PVs. After considerable dissection, gross inspection of the PVs of patient 1, who had four affected PVs and repair of the right PVs, revealed an orifice of about 0.5 mm in the one left PV that could be found. One right PV was found that easily admitted a probe and was considered to measure at least a few millimeters in diameter without evidence of obstruction. Pulmonary congestion in this patient was greater in the left lung than the right lung. Inspection of the PVs of patient 2, who also had four affected PVs and repair of the right PVs, revealed a partially patent left upper PV (1 mm) and a left lower PV that was nearly completely stenosed ( 1 mm) at the entrance into the left atrium. Beyond the opening,
3 166 BREINHOLT ET AL Ann Thorac Surg PULMONARY VEIN STENOSIS WITH NORMAL CONNECTION 1999;68:164 8 Table 1. Comparison of Patients With Stenosis of 3 or 4 Pulmonary Veins and Patients With Stenosis of 1 or 2 Pulmonary Veins Patient Sex Number of Stenosed PVs Age at Associated Lesions Operations Pulmonary Vein Surgery Type Outcome Follow-Up Since Time to Death After 3 or 4 PVs Stenosed 1 F 4 2 AVSD Repair of AVSD and right PVs 2 M 4 4 AVSD Repair of AVSD and right PVs Deceased 1 Deceased 8 3 M 4 3 ASD, PDA None Deceased 8 4 M 4 2 Cor triatriatum, ASD Repair of cor triatriatum, ASD, and right PVs 5 M 4 6 AVSD Repair of AVSD and left and right PVs 6 M 3 5 Valvar AS, PDA Aortic valvotomy with aortic root enlargement Deceased 5 Severe PV stenosis 24 Deceased 8 Mean SD N or 2 PVs Stenosed 7 F ASD None Alive with pulmonary vascular disease 8 M 2 8 ASD, polysplenism Repair of ASD and left PV 9 F 2 9 Tetralogy of Fallot, PDA 10 M 2 18 Pulmonary atresia, intact ventricular septum, PDA 11 M 2 5 Ebstein s anomaly, VSD, PDA 12 F 1 3 Unbalanced AVSD, Subaortic stenosis Blalock-Taussig shunt Staged repair of pulmonary atresia and left PV transplant transplant 13 F 1 13 ASD, VSD Repair of ASD, VSD, and right PV Alive with increasing right PV stenosis Alive with moderate pulmonary hypertension Mean SD N 7 7 AS aortic stenosis; ASD atrial septal defect; AVSD atrioventricular septal defect; PDA patent ductus arteriosus; PV pulmonary vein; VSD ventricular septal defect.
4 Ann Thorac Surg BREINHOLT ET AL 1999;68:164 8 PULMONARY VEIN STENOSIS WITH NORMAL CONNECTION 167 however, the branches were considered patent. The right upper PV was stenotic at its orifice and barely patent enough to admit a probe. The right lower PV was also stenotic where the two branches entered the left atrium. Both orifices measured less than 1 mm in diameter. Mortality and Morbidity Mortality was related to the number of stenosed PVs. Significantly more patients with three or four stenosed PVs died (83%) at months after initial presentation compared with patients with one or two stenosed PVs (0%) with follow-up of months ( p 0.05). Morbidity may have also been related to the number of stenosed PVs. The 1 surviving patient with four stenosed PVs has progressive stenosis, pulmonary hypertension, and recurrent respiratory infections. Of the patients with one or two stenosed PVs, 2 have done after surgical intervention, 2 have done after heart transplantation, and 3 have moderate to severe pulmonary hypertension. Comment In this study, we have demonstrated that PV stenosis with anatomically normal connection is usually associated with other cardiac anomalies and has a variable presentation and outcome. Although the precise incidence of this disease is unknown, it is thought to be rare. Previous descriptions of this disease have often focused around autopsy findings, possibly representing a particularly severe end of this disease spectrum. Many different types of PV stenosis have been described, ranging from hypoplasia of individual PVs to intimal constriction at the venoatrial junction [4, 5]. Any number of PVs may be involved. In our study, not surprisingly, the number of stenosed PVs affected presentation and outcome. Thus, those with only one or two stenosed PVs presented later and had better outcomes than those with three or four stenosed PVs. Associated Cardiac Lesions We report a high incidence of associated cardiac lesions with PV stenosis. Previous reports have reported an incidence of associated cardiac defects ranging from 30% to 80% [4 6]. One report describes a high incidence of PV stenosis associated with d-transposition of the great arteries [7], although we did not observe this association in our series. We did, however, find a relatively high incidence of septal defects in our series, which is comparable with previous reports [6, 8]. Our data would suggest a very strong association with all types of congenital heart disease and thus would advocate for a very careful echocardiographic examination of all PVs at the time of presentation of other cardiac lesions. Nearly all patients had associated lesions that resulted in left to right shunts. It is possible that some turbulence in the PVs could be attributed to the shunt, and that subsequent repair of the defect could result in some resolution of turbulence. However, the degree of turbulence and velocity profile in those patients with PV stenosis was significantly greater when compared with patients with left to right shunts and no PV stenosis. It is intriguing that most patients were not diagnosed with PV stenosis at the time of presentation, and that review of their echocardiograms from the time of presentation failed to demonstrate any evidence of PV stenosis that was readily apparent on subsequent echocardiograms. The reason for this either relates to the insensitivity of color Doppler echocardiography for diagnosing this entity, or, more likely, the progressive nature of this disease that is initially quite mild in infancy and then progresses over time. Surgical Outcome The treatment of PV stenosis has generally been unrewarding. Early reports of attempted surgical repair demonstrated relentless progression of the disease despite initial improvement, leading some investigators to recommend against operating, particularly if more than two PVs are involved [3, 9]. More recently, short-term success has been reported in the surgical treatment of a few patients with one congenitally stenosed PV, although progression is still of concern [8]. In our series, attempted repair of PV stenosis was undertaken in 54% of the patients at the time that other intracardiac repairs were being performed. Two patients in particular seemed to have had a beneficial effect from this operation in that the one or two affected PVs appear to be only mildly stenosed by follow-up echocardiography, and the patients are asymptomatic without evidence of pulmonary hypertension 3 and 4 years postoperatively. As suggested in earlier reports, these patients probably represent a mild form of this disease, and thus may be amenable to attempted surgical palliation. Similar to operation, attempts at transvenous balloon dilation of PV stenosis has met with poor long-term results [6, 10]. Likewise, experience with intravascular stenting of PV stenosis has been limited and has met with poor long-term success [11]. Transplantation The role of heart transplantation in patients with PV stenosis as part of their inoperable cardiac disease is unknown. Our 2 patients who received transplants are doing with only mildly elevated pulmonary artery pressures. Longer follow-up will be necessary to determine the natural history of PV stenosis after transplantation. Certainly, even if the PV stenosis is unilateral as it is in our patients, there are significant concerns about progressive PV stenosis and resultant pulmonary hypertension in these patients. However, heart transplantation has been successfully performed in a patient with functionally one lung [12], thus suggesting that transplantation may be a viable alternative in selected patients with otherwise inoperable congenital heart disease and unilateral stenosis of PVs. Lung transplantation has also met with some success in a limited number of patients, but with unknown long-term outcome [13]. Previous reports have described this disease as almost invariably fatal [4, 5]. In our series, 8 of 13 (62%) of our patients are alive months after presentation. The most likely explanation for this is that the patients in our
5 168 BREINHOLT ET AL Ann Thorac Surg PULMONARY VEIN STENOSIS WITH NORMAL CONNECTION 1999;68:164 8 series represent a less severe manifestation of PV stenosis than previous series. Clearly, outcome is directly related to the number of PVs involved. Previous studies have described more patients with involvement of three or four PVs, compared with our incidence of 54% [4, 5]. The increased incidence of less severe forms of PV stenosis with fewer affected PVs in our series compared with others is probably related to improved diagnostic accuracy of milder forms of the disease. We speculate that the use of newer diagnostic modalities such as color and transesophageal Doppler echocardiography may allow earlier diagnosis of less severe forms of this disease. Thus, patients may be diagnosed in the current era with less severe forms of PV stenosis, the natural history of which may be better than previously thought. We conclude that PV stenosis with anatomically normal connection is commonly associated with other congenital cardiac abnormalities. and outcome are largely contingent on the number of stenosed PVs. Surgical palliation, including heart transplantation for otherwise inoperable associated cardiac lesions, may be helpful in selected patients with only one or two stenosed PVs. References 1. Vick GW, Murphy DJ, Ludimorsky A, et al. Pulmonary venous and systemic ventricular inflow obstruction in patients with congenital heart disease: detection by combined two-dimensional and Doppler echocardiography. J Am Coll Cardiol 1987;9: Smallhorn JF, Pauperio H, Benson L, Freedom RM, Rowe RD. Pulsed Doppler assessment of pulmonary vein obstruction. Am J 1985;110: Victor S, Nayak VM. Deringing procedure for congenital pulmonary vein stenosis. Tex Inst J 1995;22: Bini RA, Cleveland DC, Ceballos R, Bargeron LM, Pacifico AD, Kirklin JW. Congenital pulmonary vein stenosis. Am J Cardiol 1984;54: Fong LV, Anderson RH, Park SC, Zuberbuhler JR. Morphologic features of stenosis of the pulmonary veins. Am J Cardiol 1988;62: Driscoll DJ, Hesslein PS, Mullins CE. Congenital stenosis of individual pulmonary veins: clinical spectrum and unsuccessful treatment of transvenous balloon dilation. Am J Cardiol 1982;49: Vogel M, Ash J, Rowe RD, Trusler GA, Rabinovitch M. Congenital unilateral pulmonary vein stenosis complicating transposition of the great arteries. Am J Cardiol 1984;54: Van Son JAM, Danielson GK, Puga FJ, Edwards WD, Driscoll DJ. Repair of congenital and acquired pulmonary vein stenosis. Ann Thorac Surg 1995;60: Sade RM, Freed MD, Matthews EC, Castañeda AR. Stenosis of individual pulmonary veins. Review of the literature and report of a surgical case. J Thorac Cardiovasc Surg 1974;67: Lock JE, Bass JL, Castaneda-Zuniga W, Fuhrman BP, Rashkind WJ, Lucas RV. Dilation of congenital or operative narrowings of venous channels. Circulation 1984; 70: Mendelsohn AM, Bove EL, Lupinetti FM, et al. Intraoperative and percutaneous stenting of congenital pulmonary artery and vein stenosis. Circulation 1993;88(Part 2): Shah AS, Michler RE. Successful heart transplantation with acquired pulmonary artery atresia. Ann Thorac Surg 1995;59: Mendeloff EN, Spray TL, Huddleston CB, Bridges ND, Canter CB, Mallory GB. Lung transplantation for congenital pulmonary vein stenosis. Ann Thorac Surg 1995;60:903 6.
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