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Ann Thorac Surg 1995;59:804-811
© 1995 The Society of Thoracic Surgeons

Heart Transplantation in Children and Young Adults: Early and Intermediate-Term Results

Departments of Surgery and Pediatrics, University of Colorado, Denver, Colorado

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
The purpose of this article is to report our short- and intermediate-term follow-up of cardiac transplantation for congenital heart disease and cardiomyopathy in children (age greater than 6 months), adolescents, and young adults. Thirty patients (ages 8 months to 24 years) with end-stage heart failure have undergone cardiac transplantation in our program: 12 (40%) for postoperative end-stage heart failure, 9 (30%) as primary treatment for congenital heart disease, 5 (17%) for dilated cardiomyopathy, and 4 (13%) for restrictive/hypertrophic cardiomyopathy. Nineteen patients (63%) had undergone prior operations; 4 patients received transplants for failed Fontan procedures. Induction therapy with antithymocyte therapy was used routinely, and long-term immunosuppression was by cyclosporine and azathioprine alone. Rejection surveillance/diagnosis was based on echocardiographic criteria. Posttransplantation follow-up ranges from 3 to 78 months. Operative mortality was 3.3% (1/30). No patients have been diagnosed with either accelerated allograft atherosclerosis or posttransplantation lymphoproliferative disease. We conclude that cardiac transplantation may be performed with excellent early and intermediate-term results.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 811.

Cardiac transplantation in infants with hypoplastic left heart syndrome and other forms of severe congenital heart disease (CHD) is an accepted therapy with excellent early and long-term results. However, the results of cardiac transplantation in children (age greater than 6 months), adolescents, and young adults generally do not compare favorably. Such patients frequently have complex anatomy, have undergone multiple prior palliative procedures, and may have increased pulmonary vascular resistance. Such factors significantly increase the operative mortality rate associated with cardiac transplantation; operative mortality rates as high as 25% have been reported recently [1].

The cumulative experience of our pediatric transplant program entails a total of 58 heart transplants in 58 recipients. The focus of this report is on those recipients greater than 6 months of age. Our purpose is to report our short- and intermediate-term follow-up of cardiac transplantation for CHD and cardiomyopathy in children, adolescents, and young adults (ages 8 months to 24 years). Our results indicate that at least in early follow-up, cardiac transplantation may be performed in these patients with a low operative mortality rate, excellent posttransplantation survival, and a low incidence of accelerated allograft atherosclerosis and posttransplantation lymphoproliferative disease.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Thirty children (age greater than 6 months) and young adults with end-stage heart failure secondary to cardiomyopathy or CHD have undergone orthotopic cardiac transplantation in our program. Patients with CHD underwent transplantation if (1) they suffered from end-stage heart failure after palliative or corrective cardiac surgical procedures or (2) surgical correction of their CHD was thought either to be impossible or to carry an unacceptably high operative mortality rate.

Pretransplantation Evaluation
All patients underwent cardiac catheterization with angiography to define accurately the patient's anatomy. All patients underwent a careful evaluation to exclude irreversible and significant dysfunction of all organ systems (renal, pulmonary, hepatic, neurologic, and immunologic evaluations). The pretransplantation evaluation particularly focused on pulmonary vascular resistance index (PVRI). A PVRI greater than 5 Wood units was considered a strong relative contraindication to orthotopic cardiac transplantation. If PVRI was determined to be greater than or equal to 4 Wood units during the pretransplantation evaluation, an attempt was made in the cardiac catheterization laboratory to lower PVRI pharmacologically using oxygen, inhaled nitric oxide, milrinone or sodium nitroprusside. If PVRI was lowered effectively to less than or equal to 4 Wood units by pharmacologic manipulation with any of the above agents alone or in combination, patients were considered appropriate candidates and the effective pharmacologic agent was employed in the perioperative transplant period to modulate pulmonary vascular resistance.

Surgical Procedure
Oximetric pulmonary arterial thermodilution catheters (Abbot Laboratories, Chicago, IL) were used perioperatively in all recipients continuously to monitor mixed venous oxygen saturation and pulmonary arterial pressure. A specific effort was made to keep the allograft ischemic time less than 4 hours. Donor hearts were procured in the standard manner using Roe's cardioplegia solution. The procurement and the recipient surgical teams were in frequent telephone communication to accurately coordinate the arrival of the donor heart with explantation of the recipient's heart. In recipients in whom extensive reconstruction was required, extra donor tissue was procured with the heart, if possible, such as extra length of vena cava, innominate vein, or pulmonary arteries.

Immunosuppression
The perioperative immunosuppression regimen consisted of a continuous intravenous cyclosporine infusion (0.1 mg • kg^-1 • h^-1), azathioprine (2 mg/kg orally or intravenously), and methylprednisolone (125 mg intravenously three times daily for 24 hours). An additional dose of methylprednisolone (30 mg/kg) was administered to the patient in the operating room just before reperfusion of the transplanted heart. Beginning on the first posttransplantation day, unless contraindicated by possible infection, induction therapy using antithymocyte serum (DCI Laboratories, Nashville, TN) (0.5 mL/kg) was given for either 3 or 5 days as part of a prospective, randomized study. Cyclosporine levels were measured using the whole blood radioimmunoassay technique. The target cyclosporine blood level was 250 to 350 ng/mL for the first 3 months after transplantation, 250 to 300 ng/mL for months 3 to 6 after transplantation, 150 to 200 ng/mL for months 6 to 12 after transplantation, and 100 to 150 ng/mL thereafter. Beyond 24 hours after transplantation, immunosuppression was maintained with cyclosporine and azathioprine alone.

Diagnosis of Rejection
All patients were followed up by frequent, serial two-dimensional echocardiography with Doppler/color flow mapping in surveillance for rejection. As previously described, the echocardiographic diagnosis of rejection was based primarily on impaired indices of systolic and diastolic function, increased posterior left ventricular wall thickness, and left ventricular mass [2]. Endomyocardial biopsy was rarely performed, and reserved for situations in which the diagnosis of rejection of unclear from echocardiography.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Between May 1988 and September 1994, 15 male and 15 female patients with end-stage heart failure have undergone orthotopic cardiac transplantation in our program. There have been no retransplant procedures. As shown in Figure 1, the number of cardiac transplantations performed annually has increased during the recent years of this experience. Recipient ages ranged from 8 months to 24 years (Fig 2).

View larger version (14K): [in this window] [in a new window]   Fig 1. . Number of cardiac transplantations performed in the University of Colorado Pediatric Heart Transplant Program annually in children (age greater than 6 months), adolescents, and young adults. No patients have undergone retransplantation.

View larger version (13K): [in this window] [in a new window]   Fig 2. . Number of transplant recipients by age group.

View larger version (29K): [in this window] [in a new window]   Fig 3. . Indications for cardiac transplantation.

View larger version (46K): [in this window] [in a new window]   Fig 4. . Reconstruction of an absent interatrial septum. A sheet of thin-walled Gore-Tex material was sewn to the back wall of the common atrium. The atrial septum of the donor heart then was sewn to the Gore-Tex material.

View larger version (28K): [in this window] [in a new window]   Fig 5. . Reconstruction of the main pulmonary arteries using the donor pulmonary artery. The donor main pulmonary arteries are procured out to the hilum of the donor lung. End-to-end anastomoses then are performed with the recipient pulmonary arteries.

View larger version (23K): [in this window] [in a new window]   Fig 6. . If insufficient donor pulmonary artery is available the recipient pulmonary artery may be reconstructed with a synthetic tube graft.

View larger version (27K): [in this window] [in a new window]   Fig 7. . Particularly if both donor lungs are procured for transplantation, the recipient pulmonary arteries may be reconstructed using a synthetic tube graft.

View larger version (24K): [in this window] [in a new window]   Fig 8. . Reconstruction of bilateral superior venae cavae without an innominate vein in a patient who previously had undergone bilateral classic Glenn shunts. An end-to-end anastomosis was performed between the donor and recipient superior venae cavae. The blood flow of the left superior vena cava then was channeled to the allograft via a synthetic tube graft.

View larger version (62K): [in this window] [in a new window]   Fig 9. . Reconstruction in a recipient who had only a left superior vena cava that was unroofed in the left atrium. The recipient's heart was explanted, leaving enough lateral left atrial wall to fold it over into the left atrium, which was virtually a common atrium, creating a channel to direct the flow of blood into the right atrium. The chamber size of the left atrium then was augmented by sewing a pericardial patch to a ridge of tissue that was the vestigial atrial septum.

Although the majority of patients have undergone transplantation within the past 2 years, survival during follow-up has been excellent. As shown in Figure 10, there have been no deaths in posttransplantation follow-up. The frequency of rejection has been approximately two episodes per patient (range, zero to eight), although 3 patients have experienced severe, chronic rejection. One patient required mechanical support with an intraaortic balloon pump during an episode of severe acute rejection 3 years after transplantation, which was aborted successfully with steroids and cytolytic therapy. The first-line treatment of acute rejection was pulse steroids. Steroid-refractory rejection was treated with antithymocyte serum, ATGam (Upjohn, Kalamazoo, MI), or OKT3. Rejection that was refractory to these measures or in patients with frequent episodes of rejection despite augmented immunosuppression was treated with total lymphoid irradiation (TLI). Eight patients have been treated with TLI, using a treatment protocol of 800 Gy; 4 patients received 1,300 Gy because of particularly refractory rejection. Total lymphoid irradiation was effective in all patients, and all patients have been weaned successfully to standard immunosuppression of cyclosporine and azathioprine. Only one episode of mild rejection has occurred after completion of TLI.

View larger version (11K): [in this window] [in a new window]   Fig 10. . Survival after transplantation. The numbers in parentheses represent the number of patients followed up at that length of time. There has been one operative death (3.3%) and no deaths in posttransplantation follow-up.

No patients have been diagnosed with posttransplantation lymphoproliferative disease. However, 3 patients have converted from negative to positive Epstein-Barr virus serology. These patients have been managed with lower levels of immunosuppression and 6 months of high-dose (20 mg • kg^-1 • day^-1) oral acyclovir therapy.

All recipients have undergone annual cardiac catheterization and coronary angiography. No patients have been found to have coronary arterial disease.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Data from the International Heart and Lung Transplantation Registry demonstrate that the number of adult cardiac transplant recipients has been stable since 1990, while the number of pediatric recipients has continued to grow [3]. It is estimated that between 10% and 20% of children with heart disease will undergo cardiac transplantation [4]. Although the reported results of cardiac transplantation in infants with hypoplastic left heart syndrome are excellent, the results in children and adolescents generally have been reported to be less favorable [1, 5–9]. There are several factors that may compromise the results in the latter group of patients. First, the operative procedure may be complicated by multiple prior palliative procedures or by congenital abnormalities of pulmonary or systemic venous return [10, 11]. Second, patients with congenital heart disease are prone to the development of pulmonary vascular disease and pulmonary hypertension [12, 13]. Third, the diagnosis and treatment of rejection may be very difficult in pediatric patients. Because of these issues, we reviewed our own experience with heart transplantation in children and young adults.

Operative techniques to accomplish transplantation in patients with CHD despite complex anatomy and prior operations have been described [11]. Nonetheless, such anatomic complexities may require intraoperative innovation and add to the allograft ischemic time; both of these factors may compromise results. These factors may contribute to the fact that most authors have reported better short- and long-term survival data for pediatric recipients whose indication for transplantation was cardiomyopathy rather than complex congenital heart disease [5]. In the present series, 19 of 30 recipients (63%) had undergone at least one prior operative procedure, and 10 of 30 (33%) had undergone more than one procedure. We strongly advocate a precise angiographic demonstration of the surgical anatomy, including delineation of any prior procedures, before initiating the operative transplant procedure to conduct an efficient surgical procedure. Arterial and venous reconstruction usually may be accomplished with use of autologous tissue procured from the donor. Our policy continues to be to limit allograft ischemic time to less than 4 hours, although the Loma Linda University experience suggests that longer ischemic times are tolerable in pediatric heart transplantation [14].

The most frequently reported cause of operative death in pediatric cardiac transplantation is acute allograft failure secondary to increased pulmonary vascular resistance. The inherent nature of congenital heart disease makes these recipients particularly prone to the development of pulmonary vascular disease. The pretransplantation evaluation in our institution includes a careful study of pulmonary artery pressure and PVRI. Successful pediatric cardiac transplantation in the setting of a PVRI greater than 6 Wood units has been reported [12, 13]. Nonetheless, the philosophy of our program has been to avoid cardiac transplantation if PVRI remains greater than approximately 4 Wood units despite pharmacologic manipulation during the pretransplantation evaluation. This focus on PVRI is maintained in the perioperative period where pulmonary arterial pressure is monitored continuously and pharmacologically controlled. It is our impression that strict pharmacologic control of PVRI in the perioperative period contributes significantly to our low operative mortality rate.

There are few reports in the literature of successful cardiac transplantation in children supported before transplantation with mechanical circulatory assistance [6]. One 5-year-old boy in the present series underwent successful transplantation after being supported for 30 hours with a left ventricular assist device for postcardiotomy cardiac failure. Other centers have reported significant mortality rates among children supported by extracorporeal membrane oxygenation before undergoing heart transplantation [9]. The single death in the present series occurred in a 13-year-old girl who had undergone several prior operations and was supported with extracorporeal membrane oxygenation for 18 hours for postcardiotomy cardiac failure. While on extracorporeal membrane oxygenation she exhibited significant pulmonary dysfunction and died intraoperatively of acute allograft failure that was thought to be secondary to high pulmonary vascular resistance refractory to milrinone, sodium nitroprusside, and inhaled nitric oxide.

The standard perioperative immunosuppressive protocol in the present series included cyclosporine, azathioprine, methylprednisolone, and induction therapy with antithymocyte serum. Antithymocyte serum, a rabbit polyclonal anti-T cell antibody, has efficacy both in the treatment of acute rejection and for induction therapy [15]. Despite the routine use of induction therapy, no patients experienced serious infection. A low incidence of infection after pediatric heart transplantation also has been reported by others [16]. The only serious infection in this series, fungal endocarditis, was transmitted from the donor via the allograft. Antithymocyte serum was not administered to that patient, and the infection was controlled successfully with perioperative amphotericin B and long-term fluconazole therapy.

Rejection consistently is reported to be the most common cause of death in long-term follow-up of pediatric transplant recipients [17, 18]. The incidence of rejection in the present series appears to be comparable with that reported by others, despite avoidance of long-term steroids. However, rejection has been a vexing problem in posttransplantation follow-up. In 8 patients, TLI was an effective adjunct in the treatment of refractory rejection. In pediatric heart transplant recipients, TLI previously has been shown to control refractory acute rejection effectively as well as virtually to eliminate the incidence of rejection in up to 2-year follow-up [19]. In the present series, post-TLI follow-up is relatively short, but only 1 patient has had a single post-TLI episode of mild rejection.

Accelerated allograft coronary artery disease (CAD) remains the Achilles' heel of cardiac transplantation. The incidence of CAD in adult cardiac transplant recipients has been reported to be 50% to 60% at 5 years after transplantation [20]. The incidence of CAD among pediatric heart transplant recipients has been reported to be as low as 2% [21] and as high as 43% at 3 years after transplantation [22]. Although the etiology of CAD remains unclear, there is evidence to suggest that immunologically mediated mechanisms are involved. In some series of pediatric heart transplants, an increased incidence of CAD was associated with rejection frequency [23]. However, other authors have found no association of CAD with either rejection frequency [22, 24] or cytomegalovirus infection [22].

Whether the particular chronic immunosuppression regimen influences the incidence of CAD is unclear. Addonizio and associates [21] reported a significant reduction in CAD from 18% in historical controls using immunosuppression with cyclosporine and azathioprine alone to 2% with use of triple-drug immunosuppression. However, other authors have reported significantly higher rates of CAD despite triple-drug immunosuppression; Pahl and colleagues [23] reported an incidence of 28% and Braunlin and co-workers [22] reported an incidence of 23%, 33%, and 43% at 1, 2, and 3 years after transplantation, respectively. Despite relatively short follow-up, the incidence of CAD in the present series appears to be low: no patients have been identified to have CAD on routine annual coronary arteriography. The incidence of CAD in the present series appears to be low despite avoidance of chronic triple-drug immunosuppression. This finding is consistent with that of Radley-Smith and Yacoub [24], who reported an incidence of CAD of only 3% despite using an immunosuppressive regimen of cyclosporine and azathioprine alone.

Epstein-Barr virus infection commonly is believed to contribute to the development of posttransplantation lymphoproliferative disease. This is of particular concern in pediatric transplant recipients because Epstein-Barr virus infection is so common among children. Acknowledging only short-term follow-up, no cases of posttransplantation lymphoproliferative disease have been identified in the present series. Bernstein and associates [25] reported that the actuarial adjusted risk for pediatric heart transplant recipients was 7% at 2 years, 12% at 3 years, and 15% at 4 to 5 years. In most series, the reported incidence has been approximately the same as in adult heart transplant recipients, ranging from 3% to 11% [1, 7, 16, 17]. Nonetheless, Armitage and colleagues [26] did report an increased incidence of posttransplantation lymphoproliferative disease among pediatric recipients; recipients older than 18 years of age had an incidence of only 3.5%, but those less than 18 years of age had an incidence of 9.7%. These data confirm the need for continued surveillance for lymphoproliferative disease in the present series.

In summary, the results of this series demonstrate that cardiac transplantation may be performed in children, adolescents, and young adults with CHD and cardiomyopathy with a low operative mortality rate. The incidence of both accelerated allograft CAD and posttransplantation lymphoproliferative disease appears to be low in short- and intermediate-term follow-up. Survival during this same follow-up period has been excellent. In this limited experience, TLI appears to be an effective adjunct in the treatment of refractory rejection. We conclude that cardiac transplantation may be performed with excellent early and intermediate-term results in young patients with end-stage heart disease.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Forty-first Annual Meeting of the Southern Thoracic Surgical Association, Marco Island, FL, Nov 10--12, 1994.

Address reprint requests to Dr Fullerton, Division of Cardiothoracic Surgery, University of Colorado Health Sciences Center, Box C-310, 4200 E Ninth Ave, Denver, CO 80262.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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11. Chartrand C. Pediatric cardiac transplantation despite atrial and venous return anomalies. Ann Thorac Surg 1991;52: 716–21.[Abstract]
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13. Addonizio LJ, Hsu DT, Fuzesi L, Smith CR, Rose EA. Optimal timing of pediatric heart transplantation. Circulation 1989;80(Suppl 3):84–9.
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17. Baum D, Bernstein D, Starnes VA, et al. Pediatric heart transplantation at Stanford: results of a 15-year experience. Pediatrics 1991;88:203–14.[Abstract/Free Full Text]
18. Addonizio LJ, Hsu DT, Smith CR, Gersony WM, Rose EA. Late complications in pediatric cardiac transplant recipients. Circulation 1990;82(Suppl 4):295–301.
19. Kirklin JK, George JF, McGiffin DC, Naftel DC, Salter MM, Bourge RC. Total lymphoid irradiation: is there a role in pediatric heart transplantation? J Heart Lung Transplant 1993;12:S293–300.[Medline]
20. Uretsky BF, Murali S, Reddy S, et al. Development of coronary artery disease in cardiac transplant patients receiving immunosuppressive therapy. Circulation 1987;76:827–34.[Abstract/Free Full Text]
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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): David A. Fullerton David N. Campbell Stephen D. Jones James Jaggers Mary M. Wollmering Frederick L. Grover Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Fullerton, D. A. Articles by Boucek, M. M. Search for Related Content PubMed PubMed Citation Articles by Fullerton, D. A. Articles by Boucek, M. M. Related Collections Related Article