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J Thorac Cardiovasc Surg 1994;107:990-1000
© 1994 Mosby, Inc.
CARDIAC AND PULMONARY TRANSPLANTATION |
St. Louis, Mo.
Address for reprints: Thomas L. Spray, MD, St. Louis Children's Hospital, 400 South Kingshighway, Suite 5W24, St. Louis, MO 63110.
Abstract
From July 1990 to April 1993, 36 lung transplantations in 33 patients were performed in our pediatric transplant program (0.25 to 23 years, mean age 10.3 years). Eight children had been continuously supported with a ventilator for 3 days to 4.5 years before transplantation and three were supported by extracorporeal membrane oxygenation. Indications for lung transplantation in this pediatric population included the following: cystic fibrosis (n = 13), pulmonary hypertension, and associated congenital heart disease (n = 10), pulmonary atresia, ventricular septal defect and nonconfluent pulmonary arteries (n = 3), pulmonary fibrosis (n = 6), and acute respiratory distress syndrome (n = 1). Three children underwent retransplantation for acute graft failure (n = 2) or chronic rejection (n = 1). Pulmonary fibrosis was related to complications of treatment of acute myelogenous leukemia with bone marrow transplantation in two children and to bronchiolitis obliterans, bronchopulmonary dysplasia, interstitial pneumonitis, and Langerhans cell histiocytosis in four others. Thirteen children underwent lung transplantation and concomitant cardiac repair. Bilateral lung transplantation, ventricular septal defect closure and pulmonary homograft reconstruction of the right ventricular outflow tract to the transplanted lungs was performed in three children by means of a new technique that avoids the need for combined heart-lung transplantation. Two patients had ventricular septal defect closure and single lung transplant for Eisenmenger's syndrome, two had ligation of a patent ductus arteriosus and transplantation, three additional children underwent atrial septal defect closure and lung transplantation, and two underwent lung transplantation for congenital pulmonary vein stenosis. Eight early deaths and three late deaths occurred (actuarial 1-year survival 62%). Lung transplantation in children has been associated with acceptable early results, although modification of the adult implantation technique has been necessary. Lung transplantation and repair of complex congenital heart defects is possible; heart-lung transplantation may only be required for patients with severe left heart dysfunction and associated pulmonary vascular disease. Bronchiolitis obliterans remains a major concern for long-term graft function in pediatric lung transplant recipients. (J THORACCARDIOVASCSURG1994;107:990-1000)
Although the majority of the lung transplantations performed during development of clinical lung transplantation were in adult patients, improvement in the surgical techniques and results with adult lung transplantation for end-stage pulmonary disease has resulted in application of lung transplantation to pediatric patients. 
1 Because pediatric patients have different forms of end-stage pulmonary vascular disease and fibrotic pulmonary diseases compared with those of adults, they represent a distinctly different group of recipients for lung transplantation. We report our experience in lung transplantation at St. Louis Children's Hospital with emphasis on the unusual indications for lung transplantation in the pediatric patient, the necessary modifications of the transplantation technique, and the early results.
PATIENTS AND METHODS
From July 1990 through April 1993, 36 lung transplantations were performed in 33 patients at St. Louis Children's Hospital at Washington University. The patient age ranged from 3 months to 23 years with a mean age of 10.3 years. Twenty-five of the transplant procedures were done with the bilateral sequential technique, six were single lung transplantations, one was a lobar transplantation, and three were redo bilateral transplantations (two performed with the bilateral sequential technique and one with an en bloc double lung technique). One child underwent heart transplantation and left single lung transplantation with right pulmonary artery reconstruction. The average waiting time for donor lungs was 4 months, with a range of 3 days to 19 months. Follow-up has been 0.5 to 30 months with a mean of 12.7 months in the total group.
Twenty-three lung transplantations were performed in children whose primary indication for transplantation was respiratory failure from intrinsic pulmonary parenchymal disorders (Table I). Thirteen patients underwent lung transplantation for cystic fibrosis, six for pulmonary fibrosis, one for respiratory distress syndrome requiring extracorporeal membrane oxygenation support, and three children required redo bilateral transplantation (two for acute graft failure and one for chronic rejection).
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An additional 13 lung transplant procedures were performed with concomitant cardiac repair for various indications (Table II). Three children underwent bilateral sequential lung transplantation and cardiac repair for pulmonary atresia and ventricular septal defect (VSD) associated with nonconfluent pulmonary arteries and multiple aortopulmonary bronchial collateral vessels who did not respond to palliative procedures. One older patient underwent inlet VSD closure and right single lung transplantation for Eisenmenger's syndrome, and one patient underwent outlet VSD closure, right ventricular outflow tract enlargement, patent ductus arteriosus ligation, and right single lung transplantation for Eisenmenger's syndrome. Two additional children underwent patent ductus arteriosus ligation and bilateral sequential lung transplantation for pulmonary hypertension, and three underwent atrial septal defect closure and single or double lung transplantation for pulmonary hypertension. Two children at 3 and 17 months of age underwent bilateral sequential lung transplantation for congenital pulmonary vein stenosis that was not amenable to surgical reconstruction and was associated with severe pulmonary hypertension and cardiac failure. One additional child underwent heart transplantation and left single lung transplantation with reconstruction of the right pulmonary artery after failed repair of tetralogy of Fallot, with pulmonary hypertension and biventricular failure.
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1,2 Several modifications of the adult technique, however, have been necessary to account for the size variation of children and the higher incidence of cardiac defects and pulmonary vascular disease. The thin and tenuous nature of omentum in malnourished and small pediatric patients has led to abandonment of its use for bronchial wrapping, and we have used pericardial pedicles taken down at the time of opening the pericardium for wrapping the bronchial anastomoses in the majority of our patients. 3 In the most recent four transplant procedures, we have not used any bronchial wrap. Bronchial anastomoses in children are performed in an end-to-end fashion with absorbable suture material in hopes of preventing residual foreign body in the airway and maximizing growth potential. Telescoping bronchial anastomoses are not used unless donor and recipient size discrepancy is severe. 3-5
The majority of children who undergo pediatric lung transplantation are supported by cardiopulmonary bypass for the procedure. Of the 36 lung transplantations, 35 were performed with the use of cardiopulmonary bypass. One 12-year-old child underwent bilateral sequential lung transplantation for cystic fibrosis without the use of cardiopulmonary bypass. The use of cardiopulmonary bypass eliminates the need for double lumen endotracheal tubes or bronchial blockers, which may be cumbersome or unavailable for use in small children or young adults. In addition, the placement of the patient with cystic fibrosis on cardiopulmonary bypass early in the procedure permits removal of both infected lungs and stapling of the bronchi with irrigation of the blind trachea with antibiotic solution before implantation of the donor lungs. This technique prevents spill-over contamination of purulent secretions into the newly transplanted lung, as can occur in the sequential lung implantation technique without the use of bypass. Cardiopulmonary bypass also permits dissection in the hilum in patients with hyperinflation and poor pulmonary compliance, which improves the exposure and ease of dissection. We have used a bilateral transverse thoracotomy incision with sternal transection, which provides excellent exposure for takedown of pleural adhesions and access to the heart for repair of congenital cardiac defects. 2 Because the femoral artery and vein are often small or have been previously sacrificed during catheterization or previous vascular access, we have used direct aortic and right atrial cannulation through the bilateral transverse thoracotomy in most instances for lung transplantation with or without concomitant cardiac repair.
Three patients who had pulmonary atresia with ventricular septal defect and aortopulmonary bronchial collaterals underwent bilateral sequential lung transplantation and cardiac repair (Figs. 1 to 3). With the patient supported by cardiopulmonary bypass and under cardioplegic arrest, a right ventriculotomy was performed and the VSD closed with a Dacron patch. The largest available pulmonary homograft that would fit in the chest cavity was then sutured to the right ventricular incision and augmented with a polytetrafluoroethylene (PTFE) gusset. Bilateral sequential lung transplantation was then performed, and the donor pulmonary arteries brought behind the superior venae cavae to the midline where they were approximated. The homograft was then anastomosed to the new pulmonary artery confluence to complete the repair. Separate pulmonary venous anastomoses and bronchial anastomoses were performed as in the standard technique for bilateral sequential lung transplantation. 1 In all three patients in whom this technique was used, the donor heart was not offered for transplantation and was provided to a separate recipient at another institution. The operative procedure was performed under cardioplegic arrest except for the PTFE augmentation of the right ventricular outflow tract, with an average crossclamp time of 90 minutes for bilateral lung implantation and cardiac repair.
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RESULTS
Overall survival of the 33 patients at a mean follow-up of 12.7 months was 67% (22 of the 33 patients). Analysis of survival according to the indication for transplantation (Table III) shows excellent survival in patients with pulmonary fibrosis as an indication for lung transplantation, with all six children surviving the hospitalization and no late deaths at the time this article was written. Seventy-seven percent of the patients with cystic fibrosis survived the hospitalization, with one late death and a current survival of 69%. The children with pulmonary hypertension associated with congenital heart disease had an 80% hospital survival, with two late deaths (60% late survival). None of the retransplant procedures were successful, with mortality caused by sepsis or graft failure in all three individuals. Increased immunosuppression had been given before the retransplant procedure in hopes of reversing initial graft failure or bronchiolitis obliterans. Analysis of the causes of mortality in the 11 patients who died after transplantation(Table IV) showed sepsis or acute graft failure to be the most common cause of early mortality with hemorrhage, persistent pulmonary hypertension and graft failure, and right ventricular pseudoaneurysm occurring in isolated cases. Two children had lymphoproliferative disorder at 2 months after transplantation, and both died despite decreased immunosuppressive therapy. In both cases, Epstein-Barr virus exposure was reported. One patient died of progressive bronchiolitis obliterans 8 months after successful bilateral sequential lung transplantation for cystic fibrosis. This child was listed for retransplantation but died before donor lungs were available.
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One 5-year-old boy with pulmonary fibrosis was supported continuously with a ventilator from 6 months of age to the time of bilateral sequential lung transplantation and was weaned from ventilator support and oxygen supplementation within 1 week after the procedure; he has subsequently done well.
As might be expected in a complicated group of pediatric patients over a wide age and weight range, bronchial complications were common. Of 63 bronchial anastomoses at risk, eight (12.5%) developed some complication. Two bronchial anastomoses became disrupted, one with active Aspergillus invasion requiring transplant pneumonectomy. Three additional bronchial anastomoses developed stenosis at the suture line necessitating implantation of silicone rubber stents (Fig. 5). Two additional bronchial anastomoses developed a combination of malacia and stenosis and, in one patient, malacia of the native bronchus proximal to the anastomosis was present, which was treated with a Gianturco wire stent and with a silicone rubber stent at the anastomotic suture line. One additional anastomosis developed a partial dehiscence with mediastinal cavity formation which gradually healed without complication. In all patients with stents, the stent adequately relieved the stenosis or malacia. In one patient, the silicone rubber stent was removed 6 months after implantation with good healing of the anastomosis and no evidence of restenosis.
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Of the 22 surviving patients after lung transplantation, 21 (95%) were ambulatory and had no ventilatory support with marked improvement in exercise tolerance and pulmonary function from the pretransplantation status. As noted in Table V, the vital capacity and forced expiratory vital capacity in 1 second in the patients with bilateral and single lung transplantation are not significantly different in this small group of children.
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DISCUSSION
Combined heart and lung transplantation has been performed in pediatric recipients in several centers although relatively few reported series of pediatric pulmonary transplantation have been reported. 6-12 Métras and associates 6 from the Montreal/Marseille Lung Transplant Program have reported a large series of pediatric recipients who underwent pulmonary transplantation for cystic fibrosis. Results in this group of children were excellent, with 80% early and late survival at a follow-up of up to 2 years after transplantation. The authors did not note a significantly increased prevalence of rejection or infection in the pediatric recipients compared with that in adult transplant recipients.
The Pittsburgh group of Armitage, Kormos, and Flicker reported a small population of pediatric pulmonary and cardiopulmonary recipients in whom FK 506 and azathioprine with low-dose steroids have been used for immunosuppression with an excellent 80% hospital survival and no reported late deaths. 12 The follow-up ranged from 6 months to 6 years, although the majority of cases of lung transplantation had less than 2 years of follow-up. Complications, including phrenic nerve palsy, bronchial stenosis, posttransplantation lymphoproliferative disease, and frequent viral infections, including Epstein-Barr virus, Coxsackie virus, and cytomegalovirus, were noted.
A comparison of adult and pediatric lung transplant recipients reported to the St. Louis International Lung Transplant Registry by April of 1993 has shown comparable early survival in the pediatric and adult groups. 13 An analysis of the indications for transplantation shows that adult patients undergo lung transplantation primarily for emphysema, which is a disease not seen in children. 
1-Antitrypsin deficiency with emphysema and chronic obstructive pulmonary disease comprise approximately 42% of the indications for performance of all lung transplants in adults. Cystic fibrosis, however, is becoming an increasingly frequent indication for lung transplantation and is the largest single indication for transplantation in the pediatric group. Results with lung transplantation for cystic fibrosis have not been noted to be significantly different than for transplantation for other indications, suggesting that problems of sepsis inherent in patients with cystic fibrosis do not seriously affect the chance for early and late survival. 13
Although only early and intermediate results are available at the present time on pediatric lung transplantation, comparison of the reported transplant results with the few reported series of pediatric heart-lung transplantation suggests that the two techniques are comparable. 8-11
Although it was hoped that bronchiolitis obliterans would be less frequent in patients who undergo transplantation by the bilateral sequential technique as opposed to the en bloc heart-lung transplant technique, it is now evident that the prevalence of bronchiolitis obliterans is not significantly different with the use of these two techniques. 6,14-16 Bronchiolitis obliterans remains a significant complication of both single and bilateral sequential lung transplantation and affects 25% to 40% of survivors. 6 Children may represent a particularly vulnerable group for the development of this complication because rejection and viral challenges may be more frequent in children than in adults. It is not clear whether any immune advantage exists in infants and young children compared with adults with respect to lung transplantation, as has been suggested in infants who undergo heart transplantation. 17 To date, only a few infant lung transplantations have been performed. 18,19 Two of our 33 children had rapidly progressive bronchiolitis obliterans at 6 months and 11 months after the transplant procedure.
The indication for combined heart-lung transplantation rather than lung transplantation remains unclear. Early results with cardiac repair and single or bilateral lung transplantation in patients with pulmonary hypertension and associated congenital heart disease have been acceptable, and an increasing number of adults with intracardiac defects have undergone repair with either single or bilateral lung transplantation techniques. 20-22 The technique of lung transplantation and cardiac repair has been extended to those children with more complex congenital defects necessitating elaborate repairs, such as pulmonary atresia with VSD and lack of central pulmonary arteries, and patients with atrioventricular canal defects and pulmonary hypertension. The pulmonary artery pressures early after transplantation and measurements of cardiac function have been encouraging in these patients; however, the long-term effects of correction of congenital heart defects on ventricular function and compliance are currently unknown. 22 If the encouraging early results are maintained, then it is possible that expansion of lung transplantation and cardiac repair to complex congenital heart malformations associated with pulmonary vascular disease may be possible. The advantage of cardiac repair and lung transplantation is the maximum use of scarce donor organs with the potential availability of the donor heart for use in an additional recipient. Although the domino procedure has been used with en bloc heart-lung transplantation in patients with cystic fibrosis, this procedure would not be available to patients with associated congenital heart disease and, therefore, an increased use of scarce donor organs would be the result of lung transplantation and cardiac repair. 23 The technical aspects of lung transplantation and heart-lung transplantation are comparable. Combined heart and lung transplantation, however, will continue to have a major place in the transplantation armamentarium and may be the best option for children with significant left ventricular dysfunction. In addition, potential risks of complex congenital heart repairs, which may be added to the risks of lung transplantation, do exist, and the long-term durability of the repair of the congenital cardiac defect must also be anticipated. The effects of long-standing pulmonary hypertension and cyanosis on myocardial function must also be considered before the decision for preservation of the recipient's own heart and cardiac repair. It is not known whether the pulmonary vascular resistance of a transplanted lung is low enough to consider complex univentricular cardiac repair such as the Fontan procedure with associated lung implantation. 24 Heart-lung bloc availability may ultimately be the primary determinant of whether combined heart and lung transplantation supplants cardiac repair and lung transplantation for more complex forms of congenital heart disease.
Because of the smaller size of children, it was hoped that waiting times for donor lungs for pediatric patients would be significantly shorter than those for adults; however, it is clear that the average waiting time for pediatric donor lungs is increasing and significant mortality has occurred in children awaiting lung transplantation. The fact that some adults are small because of chronic illness and that small lungs can be used in significantly larger adults because of the capacity of the lung to expand to fill the pleural cavity, has limited the number of organs available for pediatric patients. In addition, there are relatively fewer pediatric donors, and large lungs from adult patients may not be suitable for use in pediatric recipients. All of these factors make the use of lung transplantation for salvage of patients with acute pulmonary disease an unlikely prospect. Although we have noted some survival in patients who required significant ventilatory support and extracorporeal membrane oxygenation before transplantation, the limited life expectancy of patients on extracorporeal membrane oxygenation and the increasing waiting time required for lung availability are major concerns.
The significant shortage of donor lungs, the increasingly long waiting times, and the increasing number of potential recipients make single lung transplantation techniques attractive. Single lung transplantation will rapidly result in a drop of pulmonary pressure to normal levels in patients with pulmonary hypertension; however, the postoperative period may be unstable because the entire cardiac output is delivered to the transplanted lung. Concomitant cardiac repairs may add to the early postoperative hemodynamic problems. There has been concern that bronchiolitis obliterans may be seen more frequently in patients who undergo lung transplantation for pulmonary hypertension and that cardiovascular collapse might occur more readily if significant bronchiolitis obliterans or major rejection episodes occur in the single lung transplant that receives the entire cardiac output as opposed to bilateral lung transplants in which the perfusion may be more evenly distributed. 27 In spite of these theoretic objections to single lung transplantation for pulmonary hypertension or Eisenmenger's syndrome, the reported results to the International Lung Transplant Registry show similar 1-year actuarial survival for single or bilateral lung transplantation for this diagnosis and in some large series the prevalence of bronchiolitis obliterans has not been noted to be significantly different. 13,28
Lung transplantation in children can be performed with acceptable early results that are comparable with the results of heart-lung transplantation for which longer follow-up is available. Whether lung or heart-lung transplantation is the preferred technique in children, it is apparent that children represent a particularly difficult group of recipients. Careful patient selection coupled with attention to multiple medical conditions relating to the underlying disease process are required for optimal results.
Appendix: DISCUSSION
Dr. Dominique R. Metras (Marseille, France).
Since 1988 in our Children's Hospital in Marseille, a member of the Marseille-Montreal Lung Transplant Program, we have performed 30 lung transplantations in children from 6 to 16 years of age. Most patients underwent transplantation for cystic fibrosis, and most patients received a double lung transplant. Three patients underwent retransplantation for obliterative bronchiolitis.
In the double lung group, in the last 14 cases, sequential single lung transplantation has been performed, including small patients under 10 years of age. Airway anastomosis has always been done without wrapping, contrary to Dr. Spray's position; and, in the last 28 anastomoses at risk, only one needed a temporary silicone rubber stenting. We therefore concluded that a simple end-to-end anastomosis was adequate for children with a generally uneventful healing.
No patient died in the intraoperative period. The total hospital mortality was 13.3%, including two cases after retransplantation. The other patients were alive and well after 2 years.
In the double lung group, we had two hospital deaths at 1 month and 2 months, and probability of survival was 81% at 1 year, 62% at 2 years, and 44% thereafter. Presently, 66% of the patients are alive. We conclude that double lung transplantation is a reasonable option in cystic fibrosis in children.
Nine children underwent transplantation under so-called emergency conditions and were admitted in the intensive care unit with intravenous inotropic support; seven patients were supported with a ventilator from 1 to 21 days before the transplantation. The comparison of the patients in an emergency situation with those in a nonemergency situation showed a similar difficult postoperative course, length of stay in the intensive care unit, infections, rejections, and late prevalence of obliterative bronchiolitis. Survival was also similar in these two groups. These findings supported the concept that the need for artificial ventilation in cystic fibrosis (usually a terminal condition) may not be, per se, a contraindication as is usually advocated, provided there is not yet other organ failure.
I have two questions for Dr. Spray. First of all I would like to know what would be your current attitude with this group of dramatically ill young patients, and the second question concerns the choice between heart-lung transplantation and doublelung transplantation in small children with parenchymal disease. Would you consider it safer to perform heart-lung transplantation to perform a tracheal anastomosis or would you perform a double lung transplantation with a greater risk of airway complications?
Dr. Spray.
Clearly the Montreal-Marseille group has an extensive experience in pediatric transplantation of the lung. I would make three comments. The first is that I am not sure the bronchial wrap is necessary. Early in our experience we used pericardial pedicles as wraps, believing that if a bronchial disruption occurred less risk of erosion into the pulmonary artery would be present. I am not sure that is necessary, and in our recent experience we have not used any bronchial wrapping. I am somewhat concerned that the wrap may interfere with blood supply to the bronchus and that may increase the prevalence of bronchial complications, as you suggest.
Second, the problem of what to do with the ill infant who requires ventilatory support is, I think, a significant one. I was surprised early in this experience of pediatric patients, even with those who were 3 months of age, that the waiting time was long, the average waiting time being 4 months. Many of the patients who had ventilatory support at the time of the transplantation had been listed for transplantation well before they were in serious condition. In fact, our most severely ill patient, who received lungs literally within hours of her expected death, had been listed for 19 months and barely met the criteria for transplantation at the time she was placed on the list. So, over the time it took her to get lungs, her condition deteriorated so badly that she was in extremis at the time of the transplantation. I believe this is a major concern now because of the allocation system of lungs for transplantation in this country. We have no way of highlighting patients, if you will, who are extremely ill and have been waiting for a significant period of time. I think this is a major problem. Clearly, the results can be good with transplantation in these ill children if you can get them to the operating room early enough. We have had one patient who literally died on the way to the operating room before the lungs could be received. He had such high ventilatory support that, during transportation to the operating room, cardiac arrest occurred and he could not be resuscitated.
Footnotes
From the Departments of Surgery a and Pediatrics, b Washington University School of Medicine, St. Louis Children's Hospital, 400 South Kingshighway, Suite 5W24, St. Louis, MO 63110. 
Read at the Seventy-third Annual Meeting of The American Association for Thoracic Surgery, Chicago, Ill, April 25-28, 1993.
References
This article has been cited by other articles:
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  S. C. Sweet Pediatric Lung Transplantation Proceedings of the ATS, January 15, 2009; 6(1): 122 - 127. [Abstract] [Full Text] [PDF]
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 G.B. Mallory and T.L. Spray Paediatric lung transplantation Eur. Respir. J., November 1, 2004; 24(5): 839 - 845. [Abstract] [Full Text] [PDF]
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 M. J. Siegel, E. Y. Lee, S. C. Sweet, and C. Hildebolt CT of Posttransplantation Lymphoproliferative Disorder in Pediatric Recipients of Lung Allograft Am. J. Roentgenol., October 1, 2003; 181(4): 1125 - 1131. [Abstract] [Full Text] [PDF]
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 P. J. Pickhardt, M. J. Siegel, R. J. Hayashi, and M. Kelly Posttransplantation Lymphoproliferative Disorder in Children: Clinical, Histopathologic, and Imaging Features Radiology, October 1, 2000; 217(1): 16 - 25. [Abstract] [Full Text]
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 A. H. COHEN, S. C. SWEET, E. MENDELOFF, G. B. MALLORY Jr., C. B. HUDDLESTON, M. KRAUS, M. KELLY, R. HAYASHI, and M. R. DEBAUN High Incidence of Posttransplant Lymphoproliferative Disease in Pediatric Patients with Cystic Fibrosis Am. J. Respir. Crit. Care Med., April 1, 2000; 161(4): 1252 - 1255. [Abstract] [Full Text]
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 J.-P. A. Couetil, M. J. Tolan, D. F. Loulmet, A. Guinvarch, P. G. Chevalier, A. Achkar, P. Birmbaum, and A. F. Carpentier PULMONARY BIPARTITIONING AND LOBAR TRANSPLANTATION: A NEW APPROACH TO DONOR ORGAN SHORTAGE J. Thorac. Cardiovasc. Surg., March 1, 1997; 113(3): 529 - 537. [Abstract] [Full Text]
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 N. D. Bridges, G. B. Mallory Jr, C. B. Huddleston, C. E. Canter, S. C. Sweet, and T. L. Spray Lung Transplantation in Children and Young Adults With Cardiovascular Disease Ann. Thorac. Surg., April 1, 1995; 59(4): 813 - 820. [Abstract] [Full Text]
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