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Eur J Cardiothorac Surg 1998;14:1-6
© 1998 Elsevier Science NL

Clinical experience with heart transplantation in infants¹

^a Department of Cardiovascular Surgery, Justus-Liebig-University, D-35385 Giessen, Germany
^b Department of Pediatric Cardiology; Justus-Liebig-University, D-35385 Giessen, Germany
^c Department of Anesthesiology and Intensive Care Medicine, Justus-Liebig-University, D-35385 Giessen, Germany
^d Department of Pathology, Justus-Liebig-University, D-35385 Giessen, Germany

Received 26 November 1997; received in revised form 9 March 1998; accepted 15 April 1998.

Corresponding author. Tel.: +49 40 47172440; fax: +49 40 47174931; e-mail: dapper@uke.uni-hamburg.de

	Abstract

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Objective: Orthotopic heart transplantation has become an accepted therapeutic concept for adult patients with endstage heart disease. In newborns and infants this procedure is still a matter of discussion because of unknown long-term results and the lack of donor organs. Methods: Since March 1988 we have performed 40 orthotopic heart transplantation in 39 infants who were from 1 to 280 days of age. Indications for transplantation included hypoplastic left-heart syndrome (n=28), dilative cardiomyopathy (n=4), endocardial fibroelastosis (n=4) and other complex structural anomalies (n=3). The mean waiting period for transplantation was 53 days. A donor–recipient weight ratio up to 4.0 was accepted. Profound hypothermic circulatory arrest was used for graft implantation in all those patients who required extensive aortic arch reconstruction (71%). The initial immunomodulation was based on Cyclosporine, Azathioprine and Prednisolone. Patients who underwent transplantation during the first 6 weeks of life received a chronic single-drug therapy with Cyclosporine after 1 year. Results: There were six peri-operative deaths caused by drug-resistant right-heart failure in three cases, humoral rejection (n=1), CMV infection (n=1) and multi organ failure (n=1). One infant died late, due to rejection. The actuarial survival rate for the entire group is now 82%. There is a remarkable influence of increasing experience. Whereas six of 15 infants who had heart transplantation between 1988 and 1993 died early post-operatively (survival rate: 60%), only one late death occurred among 24 recipients in the period from 1994 to April 1997 (survival rate: 96%). Episodes of rejection occurred once or several times in about half of the patients in this series (48%). All surviving children are living at home in excellent condition. Conclusions: Heart transplantation during early infancy is a rational and durable therapy for heart diseases with irreversible myocardial failure or severe structural anomalies. The intermediate-term results have been encouraging in many centers, but more data must be accumulated to determine the sequelae of chronic immunosuppression. The lack of donor organs remains one of the major problems in pediatric heart transplantation.

Key Words: Heart transplantation • Infants • Rejection • Somatic development • Long-term results

	Introduction

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Orthotopic heart transplantation has become an accepted therapeutic concept for adult patients with endstage heart disease. In newborns and small infants this procedure is still a matter of controversial discussion because of unknown long-term results and the lack of donor organs. Since the first successful neonatal heart transplantation in Loma Linda by L. Bailey and colleagues in 1985 [1], transplantation activities in children and particularly in infants have clearly increased. More than 34 000 heart transplantation have been performed world-wide until 1996 [2], about 10% in children, with a 5-year survival rate of 70% [3]. Bailey and co-workers even report survival rates of 80–84% after heart transplantation in infants and neonates [4].

The question has now changed from: `should we perform heart transplantation in very young children?' to `when and for which indications is heart transplantation necessary or helpful in this age group?'. In Giessen, Germany we started a pediatric heart transplantation program in June 1988 [5]. Until today, the majority of our patients are infants and therefore this study is dealing especially with this group of patients younger than 1 year of age at the time of transplantation. Certainly, the predominant indications in this age group are congenital cardiac malformations, such as hypoplastic left-heart syndrome and endocardial fibroelastosis in infants, whereas progressive dilative cardiomyopathy is the main indication for transplantation in older children [2]. Further rare indications in our experience are other complex cardiac malformations, cardiac tumors and structural myocardial diseases.

In our experience we have seen a remarkable difference between children operated upon at the age of 1 year and older, and infants younger than 12 months of age at the time of transplantation. Heart transplantation in older children is comparable to heart transplantation in adults, as far as the technical concepts of surgery and the post-operative medical treatment and the long-term outcome are concerned. On the other hand, infants undergoing heart transplantation in the first weeks or months of their life show special pre- and post-transplant problems, but usually a much more favorable long-term follow-up concerning rejection episodes and the need of immunosuppressive drugs [4].

	Materials and methods

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Patients
Sixty infants were accepted for heart transplantation. Sixteen patients died due to shortage of donor organs before transplantation during the waiting time. Main causes of deaths were myocardial failure (n=10), sepsis/infection (n=5) and other reasons (n=1). Another five patients were rejected from the waiting list. Forty heart transplantation were performed in 39 patients from June 1988 to April 1997. Indications for transplantation in the infant group were hypoplastic left-heart syndrome (n=29), endocardial fibroelastosis (n=4), dilative cardiomyopathy (n=4) and other complex cardiac malformations (n=3).

Mean age at transplantation was 89 days (range 2–280 days), mean waiting time 53 days (range 1–233 days). Mean body weight of the recipient was 4.1 kg (range 2.7–7.0).

Peri- and post-operative management
Peri-operative management was identical for children and infants. Prior to surgery, 2 mg/kg Azathioprine® and 5 mg Cyclosporin A® were administered orally. Immediately before declamping the aorta, 10 mg/kg Prednisolone® were given. In the absence of renal failure or severe circulatory problems we started a continuous intravenous infusion of Cyclosporin A® (about 1–2 mg/kg per day) immediately after transplantation, in order to achieve and to maintain a serum level of about 250 ng/ml. Additional intravenous medication consisted of Azathioprine at a dosage of 1 mg/kg per day and Prednisolone at a dosage of 3 mg/kg per day. Prednisolone was rapidly tapered and withdrawn 3–6 weeks after operation. In infants transplanted during the neonatal period, Azathioprine is withdrawn 12 months after transplantation. Cyclosporin A target blood level 1 year after transplantation was 100 ng/ml. In routine cases we never use ATG®, ALG® or OKT 3®.

For prophylaxis and treatment of post-operative pulmonary hypertension we prefer Prostaglandin E1®, hyperventilation and alkalosis and since 1 year we have noticed convincing effects after applying NO-inhalation.

For rejection-surveillance we changed our philosophy during the last years. Since we lost one child 3 months after a successful heart transplantation and after an uncomplicated follow-up period as a result of an endomyocardial biopsy, which was followed by a pulmonary embolism, we nowadays concentrate our diagnosis of rejection in small infants and children mainly on clinical impression, ECG and echocardiographic findings. Echocardiographic signs of rejection were increasing myocardial edema, pericardial effusions, reduced, reduced systolic function and changes in diastolic function estimated by mitral valve flow measurements. ECG findings were mainly dysrhythmias and changes in frequency. Changes in volume were not helpful in the small infants in our experience. Biopsies are only carried out in severe and unclear episodes of suspected rejections.

Operative technique
The operative techniques for procurement and transplantation differed depending on the underlying disease or malformation. Only four donor hearts could be harvested in our hospital. The other 36 were procured remotely. Therefore the time of ischemia ranged from 80 to 360 min (mean 225 min). After aortic clamping, the hearts were perfused and stored in cold Bretschneider-HTK solution for transport. Aortic-arch reconstruction in infants with hypoplastic left heart was carried out in deep hypothermia and circulatory arrest. Mean duration of hypothermic circulatory arrest was 35 min (range 17–52 min).

	Results

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Forty heart transplantations were performed in 39 infants. One patient with hypoplastic left heart was retransplanted within 24 h due to primary graft failure. He remained on extracorporeal circulation for 10 h until retransplantion was possible.

Seven patients died after transplantation. There were six early hospital deaths (rejection=2, right-ventricular failure=3, infection=1, multisystem organ failure=1) and one late death (rejection) on day 391 after transplantation. Overall survival in our infant group was 33 of 39 patients (85%). Probability of survival after 3 years was 80% ( Fig. 1 ). Only one patient died in the later course on day 391 due to rejection. The mean observation period of our infants is now 773 days (range 19–3187 days). The influence of increasing experience is an important factor in survival rates. Patients transplanted from 1988 to 1993 (n=15) have a survival probability of 60%. Patients transplanted from 1994 to 1997 however have a survival probability of 93% ( Fig. 1). This clearly demonstrates the influence of increasing operative and peri-operative experience on the results after heart transplantation in our patients.

View larger version (28K): [in this window] [in a new window]   Fig. 1. Probability of survival in 39 infants after heart transplantation.

Rejection episodes occurred mainly within the first month after transplantation ( Fig. 2 ). There was a total of 30 rejection episodes in 19 patients (48%). Twenty patients never had any rejection episode, as far as we know from non-invasive monitoring. The vast majority of the rejection episodes were diagnosed within the first month after transplantation (n=21). Only one episode occurred in the late course after transplantation, on day 391. Grading of rejection was performed using the modified IUC-Classifikation proposed by Kemnitz classifying acute rejection from A-0 to A-5. Grades A-4 and A-5 were considered for therapy. We observed two lethal rejections, one of them was a severe humoral rejection diagnosed by endomyocardial biopsy. The other was an acute rejection due to discontinuation of immunosuppressive therapy more than 1 year after transplantation. Until now, there is no evidence of chronic rejection in terms of graft vasculopathy. Routine monitoring is based on heart catheterization with selective coronarography and endomyocardial biopsy every 1–2 years after transplantation. In all patients, coronary artery morphology is quite normal until now, in the long-term follow-up. Neither circumscribed stenosis nor generalized narrowing of the coronary arteries could be detected by coronary angiography. However, angiography is not very sensitive in detection of these changes, and the sensitivity may be even lower in very small children, with small coronary arteries. Other diagnostic tools such as intravascular ultrasound are not feasible in this age group.

View larger version (37K): [in this window] [in a new window]   Fig. 2. Frequency of rejection after heart transplantation in 39 infants.

View larger version (16K): [in this window] [in a new window]   Fig. 3. Calculated glomerular filtration rate (cGFR) in 39 infants following heart transplantation.

View larger version (32K): [in this window] [in a new window]   Fig. 4. Development of body weight and body height in infants and children after heart transplantation. The group of 39 infants is represented on the left side of each graph.

	Discussion

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Mortality during waiting time is a major problem in patients listed for heart transplantation. Up to 49% of patients accepted for transplantation die on the waiting list [9]. In our infant patient group, pre-transplant mortality was about 25%. The majority died of untreatable myocardial failure and infections. Considering the complex hemodynamic situation in patients with hypoplastic left heart with ductus-dependent systemic circulation, improvement in survival pre-transplant is not possible. Some patients however can be offered other palliative procedures as for example the Norwood operation [10] [11]. However there are contraindications or severe risk factors, for example right-ventricular dysfunction or severe tricuspid insufficiency, which make these patients better candidates for transplantation. Other patients with cardiomyopathy do not have any alternative treatment option.

Diagnosis of rejection in small infants remains difficult. Endomyocardial biopsy is extremely invasive in infants and in our opinion it is not a routine procedure, as in adults. Even in adults, complications following myocardial biopsies are reported, with a frequency of 3% [12]. The frequency of lethal rejections in children following heart transplantation ranges between 3% [6] and 21% [13]. In our series we had two lethal rejections in 39 patients [5%]. Therefore in our experience clinical and echocardiographic parameters as well as the ECG allow a reliable monitoring of rejection so that invasive monitoring is not necessary in routine cases.

Renal impairment is a well-known complication in organ transplantation. The few data concerning Cyclosporine toxicity in children [4] [14] [15] are encouraging. Nephrotoxicity seems less prominent in infants compared to adolescents or adults. Our results also demonstrate only a slight impairment in renal function. Serum creatinine was normal in all infants and therefore not suitable for monitoring renal function in order to detect early compromise in renal function. We therefore use the calculated GFR reported by Schwartz et al. [16]. GFR was reduced to a mean value of 80–90 ml/min per m² within the first year after transplantation and remained constant throughout the long-term course, until now. No further deterioration of renal function could be detected until now and probably renal function will remain stable.

Somatic development in infants and children after organ transplantation may be impaired, due to immunosuppression. Experience with renal and liver transplantation in children show a reduction in growth in association with steroids [17] [18] [19] [20] [21]. The Loma Linda group were not able to find a significant growth and development reduction in infants following heart transplantation [22] [23]. This is comparable to the experience in our infant patient group without any chronic steroid medication. Body weight and body length develop within the normal limits.

In conclusion, heart transplantation in infants can be performed with good peri- and post-operative results. The probability of survival is excellent in infants receiving a transplant. Quality of life in our experience is better compared to other palliative procedures. Nevertheless, about 25% of infants die awaiting a transplant. The major limiting factor for the future will still be the lack of donor organs. Therefore a selective approach concerning transplantation or for example Norwood operation is necessary. Criteria for this decision in hypoplastic left heart are, in our opinion, right-ventricular function, function of the tricuspid valve and psychosocial determinants.

	Footnotes

 
Presented at the 11th Annual Meeting of the European Association for Cardio-thoracic Surgery, Copenhagen, Denmark, September 28 – October 1, 1997.

	Appendix A. Conference discussion

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Dr L. Hamilton (Newcastle Upon Tyne, UK): With specific reference to the neonates with hypoplastic left heart, how do you manage them in terms of their pulmonary vasculature while you are waiting for a donor heart?

Dr Dapper: As this malformation is ductus-dependent, they are under the medication of Prostaglandin E1. We must keep the ductus open. This is one point. The other point is that we must try to achieve a balance between the systemic and the pulmonary circulation. In the first days of life there is an increased pulmonary vascular resistance, and the systemic circulation is not deteriorated, but with a longer time after birth the pulmonary vascular resistance decreases, and with this change the systemic circulation deteriorates. And so we have to try to keep the pulmonary vascular resistance high. That means in some cases we have to treat the patients with PEEP ventilation. And the other method is the principle not to give oxygen. That is the most common mistake. These babies don't need oxygen. On the contrary, we have to keep them on an acidotic level of pH so that the pulmonary vascular resistance increases. On the other hand, there must be a good shunt between the right and the left atrium, so that in some of these cases a balloonatrioseptostomy (Rashkind) is necessary. But, on the other hand, a shunt which is too large is the reason for pulmonary hyperperfusion. Therefore, patients who have very large ASD can't wait too long for a donor. In those cases with pulmonary hypertension there is an indication for a Norwood procedure.

Dr D. Mazzitelli (Munich, Germany): I have two questions about the post-operative course. How did you achieve induction of immunosuppression, and did you have technical problems with biopsy in such small children?

Dr Dapper: The immunosuppressive management was started pre-operatively. Prior to surgery 2 mg/kg of Azathioprine and 5 mg of Cyclosporine A are administered orally just when the baby is going into the Op theater. Immediately before declamping, 10 mg/kg of Prednisolone is given. In the absence of renal failure post-operatively or severe circulatory problems, we start an intravenous infusion of Cyclosporine A immediately after the transplantation in order to achieve and to maintain a level of about 250 ng/ml, a serum level of 250 ng/ml, and then additional intravenous medication consists of Azathioprine at the dosage of 1 mg/kg per day and Prednisolone at the dosage of 3 mg/kg per day. Prednisolone in all these children is rapidly tapered, diminished, and withdrawn 3–6 weeks after transplantation. The babies don't get cortisone/Prednisolone after this time. In infants transplanted during the neonatal period, that means 6–8 weeks after birth, Azathioprine is also withdrawn 12 months after transplantation, though there is a monotherapy with Cyclosporine A. And for the long time, Cyclosporine target blood-level 1 year after transplantation is about 100 ng/ml serum level. Also, in routine cases we never use ATG or OKT3.

Dr M.J. Elliott (London, UK): I think your results, particularly reflecting the post-operative therapy, are excellent, and I certainly have a lot to learn from them. I'm very grateful to you for bringing them to our attention. Do you think when you are presenting data about transplantation in hypoplastic left-heart syndrome there is a place for reporting it on an `intention-to-treat' basis as the starting point for your actuarial survival curve rather than the procedure itself? There is a natural tendency to compare the outcome of a Norwood with a transplant, and although you stated quite clearly that some patients died on the waiting list, it is quite difficult for us to work out how that fits into understanding your strategy of care. Unless you report an intention to treat on the basis of transplantation rather than an intention to treat on the basis of a Norwood, it makes it very difficult to interpret the outcome of your policy rather than the outcome of the particular operation itself.

Dr Dapper: If I have understood correctly, you want to know what is the indication for transplantation or the indication for a Norwood procedure in this case?

Dr M.J. Elliott: No, not at all. It's a matter of how you present your results. You have presented very beautiful results of transplantation, and I think you indicate that your unit has a preference for transplantation for hypoplastic left-heart syndrome. If that's true, then the starting point for your actuarial survival curve for the hypoplasts ought to be at the moment of intention to treat rather than the procedure itself, because otherwise you ignore the attrition rate from your results for that particular diagnosis.

Dr Dapper: I don't understand.

Dr Monro: He means that those infants that died while waiting for a heart should be included in your overall mortality. Is that right?

Dr Elliott: In the actuarial survival.

Dr Monro: Could you perhaps explain to us what your protocol is? I mean do you do all transplants and very rarely Norwoods or are you doing half and half? What is your program?

Dr Dapper: We know that not for all babies is there a source for donor organs. And so we have established some criteria for these patients with hypoplastic left-heart syndrome for doing transplantation or for doing the Norwood procedure. In the meantime we have also done about 20 Norwood procedures with a mortality of four patients. Some criteria I can collect are a very, very tiny hypoplastic ascending aorta, what is, in our view, not so suited for a Norwood procedure. Another criterion would be insufficiency of the atrioventricular valve. This is a case for transplantation because the Norwood procedure is not favorable. It's considered to have a bad outcome. Another criterion would be social reasons. For example, we have patients coming from other countries who are living in bad conditions, for example, fugitives and so on, and this is no condition to do a transplantation because the long-term therapy would not be assured. Those are some criteria which help us. And naturally we must ask the parents of the patients. It is explained to all patients that there are two methods of therapy and they have to decide together with us which of the two is the best in this case for the baby. But I have to remark, I have shown that we have lost babies on the waiting list, but when you see the literature also from Loma Linda, this point is clear that there is a loss of patients during waiting a donor organ, and what I want to show is only the results of the surgical therapy and also the medical therapy after transplantation. We know that there is a quarter of patients dying on the waiting list. It's no problem. I have shown it.

Dr C.A. Thuys (Melbourne, Australia): Given that everyone suffers from the problem of lack of donor availability, what is your maximum acceptable ischemic time and what donor storage solution are you using?

Dr Dapper: The maximum ischemic time is 6 hours and 35 minutes and the mean ischemic time is 244 minutes. The storage solution is Bretschneider solution.

	References

Top Abstract Introduction Materials and methods Results Discussion Appendix A. Conference... References

 

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This Article Abstract Full Text (PDF) 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): Friedhelm Dapper Johannes Kroll Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Dapper, F. Articles by Schranz, D. Search for Related Content PubMed PubMed Citation Articles by Dapper, F. Articles by Schranz, D.