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Ann Thorac Surg 2001;72:1887-1891
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Heart-lung transplantation for Eisenmenger syndrome: early and long-term results

^a Department of Cardiothoracic Transplantation, Papworth Hospital, Cambridge, United Kingdom

Accepted for publication July 6, 2001.

* Address reprint requests to Mr Wallwork, Department of Cardiothoracic Transplantation, Papworth Hospital, Papworth Everard, Cambridge CB3 8RE, UK
e-mail: john.wallwork{at}papworth-tr.anglox.nhs.uk

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Background. Heart-lung transplantation (HLT) for Eisenmenger syndrome (ES) provides superior early and intermediate survival when compared with other forms of transplantation. The early risk factors and long-term outcome of HLT for ES are less well defined.

Methods. We analyzed 263 patients who had undergone HLT at our institution during more than 15 years. Fifty-one consecutive patients with ES who underwent HLT, 33 (65%) of which had simple anatomy, were compared with 212 cases having HLT for other indications (non-ES).

Results. Female sex and previous thoracotomy were more prevalent in the ES group. Patients with ES had greater postoperative blood loss and returned more frequently to the operating room for control of bleeding. There were 8 (16%) early deaths in the ES group compared with 27 (13%) in non-ES (p = 0.65). One-, 5-, and 10-year survival rates for ES were 72.6%, 51.3%, and 27.6%, respectively, compared with non-ES of 74.1%, 48.1%, and 26.0%, respectively, and there was no difference in survival overall (p = 0.54). Among ES patients, previous thoracotomy was a risk factor for hospital death. A subgroup analysis based on simple versus complex type of ES did not show statistically significant differences in terms of postoperative course or early or late survival.

Conclusions. Heart-lung transplantation is a successful procedure for ES. Despite a greater frequency of risk factors and a more difficult operative course, early and late outcome with HLT is comparable to non-ES recipients.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Patients with Eisenmenger syndrome (ES) have a poor prognosis, with relatively few surviving into mid-adulthood [1] and those with advanced disease having markedly reduced functional capacity. Intrathoracic organ transplantation is the only treatment that can improve their quality of life and potentially prolong survival. For the individual patient, however, optimal timing of the operation is difficult as survival on the waiting list can be prolonged, especially when compared with the results of transplantation. Thus, transplantation is often performed for quality-of-life issues rather than survival per se, which is in distinct contrast to patients with diseases such as cystic fibrosis or primary pulmonary hypertension. Recent longitudinal studies, however, demonstrated that patients with complex cardiac anatomy have earlier clinical deterioration and significantly shorter survival than patients with simple defects [1, 2]. In addition, it has been reported that previous operation to correct or palliate the congenital defect adds to the operative risk [3], raising the issue of optimal use of scarce donor organs, especially when heart-lung transplantation is required.

The question of which transplant procedure to perform has been the subject of much debate and is compounded by different organ allocation policies around the world. Heart-lung transplantation (HLT) is our procedure of choice for all patients with ES regardless of the underlying cardiac defect; however, bilateral and single-lung transplantation, with or without repair of the cardiac defect, have been advocated to maximize the use of the limited donor organ supply [3–5]. A single-institution analysis of HLT versus bilateral-lung transplantation concluded that the two procedures are closely comparable in terms of early and medium-term survival [5], whereas the International Society for Heart and Lung Transplantation/United Network for Organ Sharing Joint Thoracic Registry showed that for patients with ES, HLT is superior to lung transplantation, the largest benefits being seen in patients with ventricular septal defect and those with multiple congenital anomalies [6]. The aim of this study was therefore to determine the outcome of HLT in patients with ES, based on a large single-center experience.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
A retrospective study of HLT was performed comparing the outcome of patients with ES with those receiving transplants for other indications. There have been no cases of bilateral-lung transplantation or single-lung transplantation for ES in our institution. The records of all patients who underwent HLT at Papworth Hospital between July 1984 and August 1999 were reviewed. Fifty-one patients with the clinical and operative diagnosis of ES were identified. A group formed by all 212 non-Eisenmenger syndrome (non-ES) cases undergoing HLT during the same interval was used for comparison. Eisenmenger syndrome patients were listed predominantly on the basis of poor quality of life. Details of recipient selection criteria remained similar throughout the period of study and basically conformed to the guidelines subsequently formulated by the International Society for Heart and Lung Transplantation working party [7]. Simple anatomy was defined as a pulmonary to systemic communication at atrial, ventricular, or ductus arteriosus level in the absence of other anomalies. All other cases were classified as complex anatomy.

Operative procedure
The donor and recipient operations were performed with techniques previously described [8]. Particular attention was paid to the management of the donor organs [9, 10]. Since 1991 a routine donor management protocol was instituted based on a hemodynamic (Swan-Ganz catheter) assessment of all donor hearts, with optimization against predetermined physiologic targets. Flexible bronchoscopy was performed routinely to assess the donor airways and remove any retained secretions. After sternotomy, with the pleural cavities opened, the ventilation was adjusted to eliminate atelectasis and fully expand the lungs. The lungs were preserved using a single-flush technique with 20 mL/kg of cold blood perfusate, preceded by prostacyclin infusion directly into the pulmonary artery. The composition of the perfusate for a 70-kg donor was donor blood (400 mL), citrate/phosphate/dextrose chelating agent (56 mL), 20% albumin (180 mL), 20% mannitol (90 mL), Ringer’s solution (600 mL), and heparin (9,000 IU). At the time of tracheal stapling the lungs were inflated just enough to ensure that there was no residual collapse. Cold normal saline solution was used for storage during the journey back to Papworth Hospital.

Immunosuppression and follow-up
All patients had induction of immune suppression with rabbit antithymocyte immunoglobulin followed by maintenance on triple, cyclosporin-based therapy. They were followed up for life in the transplant outpatients department at Papworth Hospital.

Statistical analysis
The prevalence of previous thoracotomy, reexploration for bleeding, and 30-day survival in the two groups was compared using Pearson’s chi-square test. Comparison of continuous variables including recipient age at transplantation, cardiopulmonary bypass time, and blood loss were made using Student’s t test and confirmed using the Mann-Whitney U test. Actuarial survival was estimated with the Kaplan-Meier method and analyzed using the log-rank test. A two-sided p value of less than 0.05 was considered statistically significant.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
The demographic characteristics and operative variables of the two groups are listed in Table 1. The cardiac anatomy of the ES patients is shown in Table 2. Patients with ES had similar age to non-ES at the time of transplantation (34.1 versus 32.8 years, p = 0.47). In the ES group, female sex (69% versus 46%, p = 0.005) and previous cardiothoracic operation (24% versus 11%, p = 0.012) were more prevalent.

View larger version (16K): [in this window] [in a new window]   Fig 1. Kaplan-Meier survival curves after heart-lung transplantation for patients with Eisenmenger syndrome (ES), patients without Eisenmenger syndrome (non-ES), and patients on the International Society for Heart and Lung Transplantation (ISHLT) registry. There was no statistically significant difference among the groups (log rank test).

Even though median blood loss did not appear to be significantly different among ES patients with and without previous operation (2.6 versus 1.9 L, p = 0.29), the former were more likely to return to the operating room for control of bleeding (64% versus 24%, p = 0.027). The same was not true for the patients undergoing HLT for other indications (return to operating room rate 19%, irrespective of previous chest operation). There was a trend toward higher 30-day mortality in ES patients reopened for bleeding compared with ES patients who did not experience this complication (25% versus 6.3%, p = 0.086).

To evaluate the influence of our early experience and the introduction of standardized donor management protocols in 1991, we performed a time period analysis (1984 to 1990 versus 1991 to 1999). There was no difference in outcomes between these time periods in terms of return to operating room or 30-day or overall survival.

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
For many decades physicians caring for patients with ES have been frustrated by their inability to offer more than inadequate palliation. Even those cases followed up until recently in centers specializing in congenital heart disease had a life expectancy that rarely exceeded 40 years [1]. With the development of HLT, the outlook for these patients changed significantly, although with time it has been increasingly recognized that the benefits of transplantation for this group of patients are largely confined to improvements in quality of life rather than survival. The shortage of donor organs limits the application of this therapy to many patients who might benefit, and within this context there are ongoing controversies surrounding patient selection and best use of donor organs. The results of this analysis show that, in spite of a more difficult postoperative course, ES patients overall have short-term and long-term outcomes similar to those of patients undergoing HLT for other indications.

Together with our earlier assessment of outcome while on the waiting list, the weight of evidence suggests that ES patients have a longer natural history and a smaller risk of dying while waiting for transplantation compared with other indications [11–13]. Two recent series, however, analyzed the prognosis of ES on the basis of type of anatomy [1, 2]. Daliento and colleagues [1], in a three-center experience of 188 patients with ES (of which only 8 received transplants), reported that 60 patients (32%) with complex anatomy had earlier clinical deterioration (at 18.6 versus 26.7 years for simple anatomy) and shorter survival (25.8 versus 32.5 years). Overall, the risk factors for early death were right ventricular dysfunction, age at onset of symptoms, and complex cardiac anatomy. Cantor and associates [2] reported on a single-center series of 109 patients (9 underwent transplantation). Those patients with simple cardiac anatomy (61%) had a mean survival exceeding 40 years, in contrast to less than 30 years for those with complex anatomy. Collectively, these studies show that within the ES group, complex cardiac anatomy is a significant risk factor for earlier death. Our series supports these findings, showing that patients with complex anatomy undergo transplantation at a younger age.

The ES patients in our study had a more eventful postoperative course in terms of bleeding necessitating reexploration. This is not an unexpected finding, as we are aware of the significant risks for bleeding imposed by coagulopathy, intense intrathoracic collateral vessel formation, previous operations in some cases, and the obligatory need for cardiopulmonary bypass for HLT. Reoperation for bleeding is clinically significant and appeared to affect hospital survival in our study (the same is true in fact for nontransplantation cardiac procedures [14]). The most frequent causes of perioperative death were bleeding related and donor organ failure. Donor organ failure, however, rarely occurred outside the context of significant bleeding, in which the resulting hemodynamic instability and need for fluid resuscitation in the immediate postoperative period have significant negative impacts on immediate graft function.

In terms of long-term survival the International Society for Heart and Lung Transplantation Registry reports 1- and 12-year survivals for HLT of 61% and 21%, respectively, with a survival half-life of 2.8 years and a conditional half-life for those surviving the first year of 8.6 years [15]. We are encouraged to see that in both our ES and non-ES patients we were able to achieve at least equally good results. In common with all forms and indications for lung transplantation, obliterative bronchiolitis was the major factor determining long-term graft outcome. In contrast, cardiac allograft vasculopathy was uncommon (4%) and always occurred in the context of advanced obliterative bronchiolitis.

In addition to the survival advantages for ES patients with HLT, they also have an improved quality of life. The Stanford group, who in 1986 published their early experience with HLT for ES, have emphasized the marked functional improvement that is associated with the procedure [3]. Subsequent formal quality-of-life analyses by our group [16] and others [17] objectively confirmed these early clinical observations. Quality of life remains well preserved when lung function is maintained. Deterioration in lung function in the longer term usually represents the onset of bronchiolitis obliterans syndrome. In our series of HLT, only 36% of patients remained free of bronchiolitis obliterans syndrome at 5 years [18], and it is not until the advanced stage of bronchiolitis obliterans syndrome is reached that quality of life is significantly affected.

With the advent of single-lung transplantation and bilateral-lung transplantation, a number of centers adopted them as the procedures of choice for simple ES, with or without repair of the cardiac defect [4, 5]. The popularity of these operations increased after the demonstration that in patients with pulmonary hypertension right ventricular dysfunction improves postoperatively with reduction in the pulmonary resistance [19]. Subsequently however, single-lung transplantation has been largely abandoned for the treatment of severe pulmonary hypertension of any cause, because of the potential for inducing severe reperfusion injury and significant ventilation-perfusion mismatch problems in the immediate postoperative period, postoperative dynamic obstruction of the right ventricular outflow tract (which can range from trivial to fatal) [20, 21], and limited symptomatic improvement in the longer term [4]. In addition, repairing of the underlying cardiac defect in patients with ES is seldom straightforward, and may require deep hypothermia and circulatory arrest [4].

In general these studies have relatively small numbers of ES patients, amalgamated with other cases of pulmonary hypertension, and undergoing a variety of operations. More evidence in favor of one procedure or another can be gathered from long-term survival analyses, which have now shown that the biggest benefit for ES resulting from ventricular communication comes from HLT [6]. Nevertheless, the concept of maximizing donor organ usage is beyond dispute. With the existing evidence, however, we believe that bilateral-lung transplantation for ES should only be performed for uncomplicated cases of atrial septal defect or patent ductus arteriosus in dedicated centers. The procedure of choice for ES patients with ventricular septal defect, complex anatomy, or significant left or right ventricular dysfunction remains HLT. We do, however, recognize the dichotomy of opinion in this area because of the very real issue of donor organ availability.

In conclusion, the results of this series show that ES patients treated with HLT achieve the expected long-term survival for the procedure. Bleeding-related morbidity is significant in the postoperative period, particularly in patients who have undergone previous surgical procedures. Continued evaluation of the outcome of all the transplant surgical options used to treat this group of patients is necessary to more accurately define the optimal procedure in terms of individual patient outcome versus most effective use of donor organs. It is our recommendation, however, that whatever surgical procedure is preferred, this group of patients is optimally treated in a center with considerable transplantation experience, and furthermore, for those patients requiring HLT, they should only be treated in a center with extensive experience with this operation.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments References

 
Doctors Stoica and Satchithananda are supported by grants from the Garfield Weston Research Trust.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments 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): Serban C. Stoica Steven S. Tsui John Wallwork Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Stoica, S. C. Articles by Wallwork, J. Search for Related Content PubMed PubMed Citation Articles by Stoica, S. C. Articles by Wallwork, J. Related Collections Lung - transplantation Related Article