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Ann Thorac Surg 2001;71:66-70
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Pediatric cardiac retransplantation: intermediate-term results

Joseph A. Dearani, MDa, Anees J. Razzouk, MDa, Steven R. Gundry, MDa, Richard E. Chinnock, MDa, Ranae L. Larsen, MDa, Michael J. del Rio, MDa, Joyce K. Johnston, RNa, Leonard L. Bailey, MDa

a Loma Linda University Medical Center and Children’s Hospital, Loma Linda, California, USA

Accepted for publication July 31, 2000.

Address reprint requests to Dr Dearani, Division of Cardiothoracic Surgery, Mayo Clinic, 200 First St, SW, Rochester, MN 55905
e-mail: jdearani{at}mayo.edu


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Cardiac retransplantation (re-CTx) in children is a controversial therapy, yet it remains the best treatment option to recipients with failing grafts. Our objective was to determine the incidence of re-CTx in a large pediatric population of recipients and evaluate the outcome of such therapy.

Methods. Between November 1985 and November 1999, 347 children underwent cardiac transplantation at the Loma Linda University Medical Center. Of these, 32 children were listed for re-CTx. Ten patients died while waiting, and 22 recipients underwent re-CTx. Median age at re-CTx was 7.1 years (range, 52 days to 20.1 years).

Results. Indications for re-CTx were allograft vasculopathy (n = 16), primary graft failure (n = 5), and acute rejection (n = 1). Two patients with primary graft failure underwent retransplantation within 24 hours of the first transplantation procedure while on extracorporeal membrane oxygenation support. Median time interval to re-CTx for the others was 7.2 years (range, 32 days to 9.4 years). Operative mortality for all cardiac re-CTx procedures was 13.6%. Causes of hospital mortality were pulmonary hypertension with graft failure (n = 2) and multiorgan failure (n = 1). Median hospital stay after re-CTx was 14.1 days (range, 6 to 45 days). There was one late death from severe rejection. Actuarial survival at 3 years for re-CTx was 81.9% ± 8.9% compared with 77.3% ± 2.6% for primary cardiac transplantation recipients (p = 0.70).

Conclusions. Elective re-CTx can be performed with acceptable mortality. Although the number of patients undergoing retransplantation in this report is small and their long-term outcome is unknown, the intermediate-term survival after re-CTx is similar to that of children undergoing primary cardiac transplantation.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
An increasing number of heart transplantations (CTx) are performed for a variety of inoperable cardiac conditions in infants and children. Some of these recipients will experience graft failure and become potential candidates for retransplantation. Indications for cardiac retransplantation (re-CTx) include: irreversible rejection, graft vasculopathy, and perioperative primary donor organ failure.

Cardiac transplantation is performed annually in approximately 300 children worldwide with good 5-year survival (70%) [1, 2]. With the longer survival of this pediatric population, the development of diffuse graft arteriosclerosis and its ischemic sequelae may develop in as many as 35% of patients [3–5]. Medical treatment has not been effective in reducing the risk of sudden death in recipients with severe graft vasculopathy. Cardiac retransplantation remains the best therapeutic option of proven benefit to those children. Consequently, graft vasculopathy is the most common indication for consideration of retransplantation.

In view of the limited organ donor supply and recent reports demonstrating poorer outcome with adult re-CTx compared with primary transplantation [6, 7], ethical, moral, and financial issues have been raised concerning the merits of re-CTx. To address these issues in the pediatric population, we retrospectively reviewed the incidence and outcome of re-CTx in a cohort of infants and children who underwent orthotopic CTx at our institution.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Patient characteristics
Between November 1985 and November 1999, 347 children underwent primary orthotopic CTx at the Loma Linda University Medical Center, Loma Linda, California. The mean age of 207 boys and 140 girls was 1.9 ± 3.9 years (range, 1.5 hours to 17.7 years); 94 patients were neonates (<30 days). Of these, 32 patients were listed for re-CTx; 10 patients died while on the waiting list, and 22 children underwent re-CTx. The mean age of 12 boys and 10 girls in the re-CTx group was 7.1 ± 1.8 years (range, 2.4 to 9.7 years).

Immunosuppressive therapy was similar in both the CTx and re-CTx groups and consisted of perioperative methylprednisolone for 48 hours and then cyclosporine and azathioprine sodium for long-term immunosuppressive therapy in the CTx group and cyclosporine and methotrexate in the re-CTx group. Polyclonal antithymocyte serum (AMR, Inc, Nashville, TN) was administered at the time of transplantation. Antithymocyte serum was given intravenously (0.5 mL/kg per day) on the day of transplantation, and the dose was repeated daily for a total of 5 days. Follow-up in the initial 6 months after transplantation in both groups consisted of biweekly visits to the outpatient transplantation clinic. The referring cardiologist and primary pediatrician provided later follow-up. Close monitoring included physical examination, electrocardiography, measurement of cyclosporine levels, and serial echocardiography. The diagnosis of graft rejection was usually based on echocardiographic and clinical criteria [8]; endomyocardial biopsy was performed selectively. Rejection episodes were defined as those that required augmentation in immunosuppressive therapy. Graft coronary arteries were evaluated by annual coronary angiography, gross and histologic examinations of explanted hearts (after re-CTx) or autopsy specimens, or a combination of angiography and pathologic examination. Graft vasculopathy was considered severe when there was luminal narrowing of more than 50%. More recently, intravascular ultrasound has been used in older children to corroborate angiographic findings.

Follow-up
Follow-up for the primary CTx group was 100% complete and averaged 05.2 ± 3.7 years (range, 1 day to 14.0 years). The mean follow-up for the re-CTx group was 2.6 ± 2.5 years (range, 4 months to 10.3 years). Follow-up data included the most recent clinic or personal physician visit, or telephone contact.

Statistical analysis
All data are presented as mean ± SD. The Kaplan-Meier log-rank method was used to calculate actuarial survival and probability of freedom from a clinical event. Statistical significance (p < 0.05) was determined using the {chi}2 test for categorical variables, the Student’s t test for normally distributed continuous variables (ischemic time; Table 2), and the Mann-Whitney test for nonparametric continuous variables (cardiopulmonary bypass time, hospital stay, and mean panel reactive antibody [PRA]; Table 2).


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  		Table 2. Perioperative Clinical Data

 

   Results
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 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Diagnoses for the CTx and re-CTx groups are shown in Table 1. Indications for re-CTx were allograft vasculopathy (n = 16), primary graft failure (n = 5), and acute rejection (n = 1). The median time interval between CTx and re-CTx was 7.2 years (range, 1 day to 9.4 years). Two patients with primary graft failure underwent retransplantation within 1 day of the first transplantation and required mechanical support with extracorporeal membrane oxygenation (ECMO) before re-CTx. Another infant presented in cardiogenic shock and severe graft rejection 1 month after CTx. He was resuscitated and placed on ECMO for 12 hours until undergoing retransplantation with another graft. One 6-year-old boy required high-dose inotropic support and hemodialysis before re-CTx, and the remaining 16 patients awaiting re-CTx were hemodynamically stable. Twenty patients underwent re-CTx at our institution, and 2 patients underwent re-CTx elsewhere. Additional procedures at the time of re-CTx included aortic arch aneurysm repair in 2 patients. Perioperative clinical characteristics are shown in Table 2. Indications for re-CTx and the time interval between CTx and re-CTx are shown in Table 3.


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  		Table 1. Diagnoses at Time of Transplantation

 

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  		Table 3. Indications for Retransplantation

 
Percent PRA was measured in all patients listed for CTx and re-CTx. The mean PRA for all re-CTx patients was 17.7% (range, 0% to 92%), and half of these patients had a PRA more than 10% (Table 2). In recent years, such patients with PRA more than 10% were given intravenous immunoglobulin at 2 g/kg every month for three doses while awaiting re-CTx. Follow-up PRA levels generally decreased; however, none of the patients was denied re-CTx because of an elevated PRA.

Human leukocyte antigen typing was performed after the transplantation procedures; prospective human leukocyte antigen matching or donor-specific lymphocyte crossmatch was not routinely done.

Patient survival and morbidity
Overall operative mortality (30-day or hospital mortality) for the re-CTx group was 13.6% (3 of 22) and for the primary CTx group was 9.0% (p = 0.9). Operative mortality for elective re-CTx was 5.2% (1 of 19). There were 3 early deaths in the re-CTx group. The 2 patients who underwent urgent re-CTx while on ECMO for acute graft failure died of pulmonary hypertension and second graft failure. The 6-year-old boy who experienced hemodynamic compromise and renal failure before re-CTx died of sepsis and multiorgan system failure 4 weeks after operation.

There was one late death 5 weeks after re-CTx because of severe rejection of the second allograft. Actuarial patient survival at 3 years after CTx and re-CTX was 77.3% ± 2.6% and 81.9% ± 8.9%, respectively (p = 0.70; Fig 1). At late follow-up, all patients were in New York Heart Association class I. Overall freedom from re-CTx in the primary CTx group at 5 and 8 years was 97.4% ± 1.0% and 88.2% ± 3.0%, respectively (Fig 2).



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  		Fig 1. Actuarial survival of 325 children who underwent primary cardiac transplantation (squares) and 22 recipients who underwent cardiac retransplantation (triangles). The number in parentheses indicates the patients at risk.

 


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  		Fig 2. Freedom from cardiac retransplantation for all children who underwent primary cardiac transplantation (n = 347).

 
Morbidity after re-CTx was minimal, and the average length of hospital stay was 18.8 ± 11.8 days (Table 2). None of the patients required exploration for bleeding after re-CTx. Although 7 patients received perioperative peritoneal dialysis for transient renal insufficiency, none of the survivors has required long-term dialysis. The mean serum creatinine level of survivors is 0.8 ± 0.2 mg/dL, and the mean glomerular filtration rate is 86.4 ± 27.1 mL · min-1 · 1.73 m-2. A 9-year-old girl, 3 weeks after re-CTx, had a sternal wound infection related to aggressive immunosuppressive therapy. She underwent debridement and rewiring of sternotomy with good recovery. The infant who underwent re-CTx after 12 hours of ECMO support for irreversible acute rejection had coarctation of the aorta. Balloon angioplasty did not improve the gradient; therefore, he underwent surgical resection of the narrowed segment of the aortic arch and is now doing well 10 years after re-CTx.

Rejection and infection
Graft rejection after CTx and re-CTx was most commonly noted during the first 3 months after transplantation. The overall incidence of treated rejection was 0.8 per patient-month. Of those surviving at least 12 months, the average number of rejection episodes in the first year was 1.8 in the CTx group and 1.6 in the re-CTx group. Actuarial freedom from graft rejection at 3 months, 1 year, 3 years, and 5 years in the CTx group was 34.4%, 30.4%, 24.3%, and 22.1%, respectively; in the re-CTx group it was 34.4%, 17.1%, 17.1%, and 17.1%, respectively. The single late death in the re-CTx group occurred 5 weeks after re-CTx and was caused by severe rejection refractory to medical treatment. There was one early death caused by sepsis that is described above. Despite augmented immunosuppression regimen in the re-CTx group, there were no late deaths related to infection.

Human leukocyte antigen matching data (class I and class II antigens) with regard to the second donor were available in 19 of 22 patients. In 16 patients (73%) there was repetition in the second donor heart of mismatched human leukocyte antigens in the first allograft. The 1-year survival in the group with repeated mismatched antigens was 82%. One patient, after re-CTx, had a positive retrospective donor-specific lymphocyte crossmatch. He was given immunoglobulin postoperatively and survived without complications.

Hospital charges
During the 1997 calendar year, the mean hospital charges for the 6 patients who underwent re-CTx was $171,000 ± $25,000 compared with $173,000 ± $20,000 for the 22 patients who underwent primary CTx during the same period (p = 0.9). These hospital charges do not include any pretransplantation (intensive care unit) charges incurred by United Network for Organ Sharing status I patients during the waiting period.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Early and late survival after CTx in children has steadily improved over the last 15 years [1, 2]. This is mostly because of advances in surgical and anesthetic techniques, new immunosuppressive agents, and better detection of graft rejection [8]. Consequently, with an increasing number of late survivors after pediatric CTx, the need for re-CTx is now being recognized. Whereas the late survival after primary CTx is similar in the adult and pediatric populations [9], recent data have indicated that the results of adult re-CTx are significantly worse when compared with primary transplantation [9–11]. The large number of patients awaiting their first CTx and the scarcity of donor organs with documented poorer outcome in the adult retransplantation literature raises the concern that it is "unfair or unethical" to allocate a donor heart to a potential recipient of a second organ. Reports of outcome for re-CTx in the pediatric population are less comprehensive. The purpose of this retrospective review was to examine the results of pediatric re-CTx and to identify a group of patients that would most benefit from retransplantation.

Cardiac retransplantation was first performed in 1977 [11], and since that time, more than 800 re-CTx procedures have been performed. Actuarial 1-year survival ranging from 55% to 75% for adult re-CTx has been reported by the Stanford [10] and Utah [11] groups, respectively. Survival rates for both were significantly lower than their respective survival for primary CTx. These findings were also noted in the registry of the International Society for Heart and Lung Transplantation (1-year survival, 58% vs 79%) [9]. Although most series of re-CTx have demonstrated poorer survival, Columbia-Presbyterian Medical Center’s 1-year and 5-year survival after re-CTx was not significantly different from their primary CTx (76% vs 66%; 60% vs 51% respectively). [12, 13]. They believe that the prognosis is better when the indication for re-CTx is identified after 30 days from the initial transplant.

Indications for re-CTx have included grafts failing from rejection, graft vasculopathy, and intraoperative donor organ failure. Of these, graft vasculopathy is the most common indication and the most serious threat to late survival after CTx [14]. Although the cause of graft arteriosclerosis is unclear and less frequent in children, it affects recipients of all ages and can occur as early as 2 months after transplantation [15]. The apparent lower incidence of graft vasculopathy in children when compared with adults (10% to 35% vs 40% to 70% at 5 years) [3, 14, 15] may be multifactorial. Fewer long-term pediatric survivors, use of younger donors, and the less frequent use of coronary angiography in the pediatric patient may each contribute to lower reported incidence of graft coronary artery disease among children. Cardiac allograft vasculopathy differs from traditional arteriosclerosis in that it is concentric, diffuse, and free of calcification, and it can affect intramyocardial vessels. Because discrete stenoses are rare, coronary angioplasty is usually ineffective. Subsequent development of myocyte hypertrophy and disarray resulting in fibrosis and scarring, progressive myocardial dysfunction, and the increased incidence of sudden death make retransplantation the only effective treatment option for children with this problem [16].

Data collected from multiple institutions in the United States identified three factors predictive of improved survival after re-CTx: longer (> 6 months) interval between transplantations, accelerated coronary artery disease causing allograft failure, and lack of preoperative mechanical support [4]. Early in our series, urgent retransplantation was performed in 2 children within 24 hours of the primary transplantation procedure. Both required ECMO support for primary graft failure and both died. Others have also shown that early re-CTx (< 30 days) is associated with a high mortality [4, 17]. We have recently reported our results for re-CTx in 12 patients who underwent re-CTx for graft vasculopathy with early survival comparable with primary transplantation [16]. The Stanford group also demonstrated better 1-year survival with re-CTx when it was performed for graft vasculopathy compared with allograft rejection (69% vs 33%) [10].

Contraindications to re-CTx are similar to primary transplantation and may include significant neurologic deficit, severe renal insufficiency or other major organ system dysfunction, pulmonary hypertension, malignancy, active infection, and noncompliance. In addition, patients needing a graft within 6 months of their initial transplantation or those requiring a mechanical assist device remain poor candidates for re-CTx. Elevated PRA has not been a significant risk factor, hence it is not a contraindication. Children undergoing re-CTx in this series exhibited a greater degree of sensitization as evidenced by a higher mean PRA (Table 1). This increased sensitization may be related to previous blood transfusions and exposure to donor-specific antigens of the first allograft. The clinical implications of higher sensitization, however, have not been important enough to necessitate preoperative donor human leukocyte antigen typing and crossmatching. In this series, like the Utah series [7], the repetition in the second allograft of mismatched human leukocyte antigens present in the first allograft did not affect survival, as has been reported in renal retransplantation [18].

It is important to note that 10 patients in this series died waiting for re-CTx. Much of this mortality occurred early in our experience with re-CTx, and was largely related to delay in relisting candidates. We have observed that the average recipient survival after a definitive diagnosis of allograft vasculopathy or the onset of cardiac symptoms relating to chronic graft rejection ranges between 90 and 120 days. Death is frequently sudden. Hence, prompt listing of the recipient for re-CTx is imperative. Current indications for relisting at our institution include (1) diffuse graft vasculopathy documented by dobutamine stress echocardiography, coronary angiography or intravascular coronary ultrasound and (2) refractory chronic graft rejection that has produced severe cardiomyopathy.

In summary, elective re-CTx in children is an effective therapy with acceptable morbidity and mortality. Although the number of patients undergoing retransplantation in this series is small and their long-term outcome is unknown, the intermediate-term survival after re-CTx is similar to that after primary CTx. The ideal candidates for re-CTx are recipients who experience severe graft vasculopathy.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Razzouk A.J., Chinnock R.E., Gundry S.R., et al. Transplantation as a primary treatment for hypoplastic left heart syndrome: intermediate-term results. Ann Thorac Surg 1996;62:1-8.[Abstract/Free Full Text]
  2. Fullerton D.A., Campbell D.N., Jones S.D., et al. Heart transplantation in children and young adults: early and intermediate-term results. Ann Thorac Surg 1995;59:804-812.[Abstract/Free Full Text]
  3. Bailey L.L., Zuppan C.W., Chinnock R.E., Johnston J.K., Razzouk A.R., Gundry S.R. Graft vasculopathy among recipients of heart transplantation during the first 12 years of life. Transplant Proc 1995;27:1921-1925.[Medline]
  4. Pahl E., Fricker F.J., Armitage J., et al. Coronary arteriosclerosis in pediatric heart transplant survivors: limitation of long-term survival. J Pediatr 1990;116:177-183.[Medline]
  5. Pahl E., Zales V.R., Fricker F.J., Addonizio L.J. Posttransplant coronary artery disease in children: a multicenter national survey. Circulation 1994;90(Part 2):II56-II60.
  6. Smith J.A., Ribakove G.H., Hunt S.A., et al. Heart retransplantation. The 25-year experience at a single institution. J Heart Lung Transplant 1995;14:832-839.[Medline]
  7. Karwande S.V., Ensley R.D., Renlund D.G., et al. Cardiac retransplantation. A viable option?. Ann Thorac Surg 1992;54:840-845.[Abstract]
  8. Chinnock R.E., Baum M.F., Larsen R., Bailey L.L. Rejection management and long-term surveillance of the pediatric heart transplant recipient: the Loma Linda experience. J Heart Lung Transplant 1993;12:S255-S264.[Medline]
  9. Hosenpud J.D., Bennett L.E., Keck B.M., Fiol B., Boucek M.M., Novick R.J. The registry of the International Society for Heart and Lung Transplantation: fifteenth official report—1998. J Heart Lung Transplant 1998;17:656-668.[Medline]
  10. Smith J.A., Ribakove G.H., Hunt S.A., et al. Heart retransplantation: the 25-year experience at a single institution. J Heart Lung Transplant 1995;14:832-839.
  11. Copeland J.G., Griepp R.B., Bieber C.P., et al. Successful retransplantation of the human heart. J Thorac Cardiovasc Surg 1977;73:242-247.[Abstract]
  12. Michler R.E., McLaughlin M.J., Chen J.M., et al. Clinical experience with cardiac retransplantation. J Thorac Cardiovasc Surg 1993;106:622-631.[Abstract]
  13. John R., Chen J.M., Weinberg A., et al. Long-term survival after cardiac retransplantation. A twenty-year single-center experience. J Thorac Cardiovasc Surg 1999;117:543-555.[Abstract/Free Full Text]
  14. Gallo P., Agozzino L., Angelini A., et al. Causes of late failure after heart transplantation: a ten-year survey. J Heart Lung Transplant 1997;16:1113-1121.[Medline]
  15. Berry G.J., Rizeq M.N., Weiss L.M., Billingham M.E. Graft coronary disease in pediatric heart and combined heart-lung transplant recipients: a study of fifteen cases. J Heart Lung Transplant 1993;12(Suppl):S309-S319.[Medline]
  16. Razzouk A.J., Chinnock R.E., Dearani J.A., Gundry S.R., Bailey L.L. Cardiac retransplantation for graft vasculopathy in children. Arch Surg 1998;133:881-885.[Abstract/Free Full Text]
  17. Bailey L.L., Zuppan C.W., Chinnock R.E., Johnston J.K., Razzouk A.R., Gundry S.R. Graft vasculopathy among recipients of heart transplantation during the first 12 years of life: the pediatric heart transplant group. Transplant Proc 1995;27:1921-1925.
  18. Almond P.S., Matas A.J., Gillingham K., et al. Risk factors for second renal allografts immunosuppressed with cyclosporine. Transplantation 1991;52:253-258.[Medline]



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