Patients with Eisenmenger syndrome (ES) have a poor
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1 Heart-Lung Transplantation for Eisenmenger Syndrome: Early and Long-Term Results Serban C. Stoica, AFRCSEd, Keith D. McNeil, FRACP, Kostas Perreas, FRCS, Linda D. Sharples, PhD, Duwarakan K. Satchithananda, MRCP, Steven S. Tsui, FRCS, Stephen R. Large, FRCS, and John Wallwork, FRCS Department of Cardiothoracic Transplantation, Papworth Hospital, Cambridge, United Kingdom Patients with Eisenmenger syndrome (ES) have a poor prognosis, with relatively few surviving into midadulthood [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. Accepted for publication July 6, Address reprint requests to Mr Wallwork, Department of Cardiothoracic Transplantation, Papworth Hospital, Papworth Everard, Cambridge CB3 8RE, UK; john.wallwork@papworth-tr.anglox.nhs.uk. 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. (Ann Thorac Surg 2001;72: ) 2001 by The Society of Thoracic Surgeons 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 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 diagno by The Society of Thoracic Surgeons /01/$20.00 Published by Elsevier Science Inc PII S (01)
2 1888 STOICA ET AL Ann Thorac Surg HEART-LUNG TRANSPLANT FOR EISENMENGER 2001;72: Table 1. Patient Demographics and Operative Variables a Group ES Non-ES p Value No. of patients (absolute values) Age at transplant (y) Female sex 69% 46% Previous thoracic operation 24% 11% Ischemic time (min) Cardiopulmonary bypass time (min) Blood loss (ml) Return to operating room for blood loss 33% 19% 0.03 a Values are presented as the mean standard deviation or percentages. ES Eisenmenger syndrome patients. sis 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 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. There was no statistically significant difference in allograft ischemic times and cardiopulmonary bypass times between ES and non-es patients. Patients with ES had greater postoperative blood loss (2.1 versus 1.5 L for non-es, p 0.01) and were more likely to require reexploration for bleeding (33% versus 19%, p 0.03). There were 8 (16%) deaths within 30 days in the ES group compared with 27 (13%) in non-es patients (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. The survival halflife for the ES curve was 5.1 years, and the conditional half-life for those surviving the first year was 8.8 years (Fig 1). There was no difference in overall survival be- Table 2. Type of Cardiac Anatomy Simple VSD 16 PDA 8 VSD PDA 5 ASD 4 Subtotal 33 Complex TGA 5 AV canal 4 Univentricular heart 3 Truncus arteriosus 3 Pulmonary atresia 1 Tetralogy of Fallot 1 Ao-P window 1 Subtotal 18 Ao-P aorto-pulmonary; ASD atrial septal defect; AV atrioventricular; PDA persistent ductus arteriosus; TGA transposition of the great arteries; VSD ventricular septal defect.
3 Ann Thorac Surg STOICA ET AL 2001;72: HEART-LUNG TRANSPLANT FOR EISENMENGER 1889 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). tween ES patients and non-es patients (p 0.54). The causes of early and late deaths are listed in Table 3. A subgroup analysis based on simple versus complex type of ES anatomy did not show statistically significant differences in terms of postoperative course or early or late survival. The ES patients with complex anatomy were younger at the time of transplantation (average, 28.6 versus 37.0 years, p 0.003) and were more likely to have undergone previous operation (39% versus 15%, p 0.085). 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 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 threecenter 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 Table 3. Cause of Death for Eisenmenger Syndrome Patients Cause ES Simple ES Complex Total (%) a Early Bleeding related (6) Donor organ failure (6) Infection bacterial (2) Cerebrovascular (2) Total (16) Late Obliterative bronchiolitis (16) Cardiac vasculopathy (4) Infection bacterial (4) Infection viral (4) Infection fungal (4) Acute rejection (4) Other (8) Total (44) a The denominator for percentages is the entire ES cohort of 51 patients. ES Eisenmenger syndrome patients, with simple or complex cardiac anatomy.
4 1890 STOICA ET AL Ann Thorac Surg HEART-LUNG TRANSPLANT FOR EISENMENGER 2001;72: 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 longterm 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. Doctors Stoica and Satchithananda are supported by grants from the Garfield Weston Research Trust. References 1. Daliento L, Somerville J, Presbitero P, et al. Eisenmenger syndrome. Factors relating to deterioration and death. Eur Heart J 1998;19: Cantor WJ, Harrison DA, Moussadji JS, et al. Determinants of survival and length of survival in adults with Eisenmenger syndrome. Am J Cardiol 1999;84: McGregor CGA, Jamieson SW, Baldwin JC, et al. Combined heart-lung transplantation for end-stage Eisenmenger syndrome. J Thorac Cardiovasc Surg 1986;91: Bando K, Armitage JM, Paradis IL, et al. Indications for and results of single, bilateral and heart-lung transplantation for pulmonary hypertension. J Thorac Cardiovasc Surg 1994; 108: Ueno T, Smith JA, Snell GI, et al. Bilateral sequential single lung transplantation for pulmonary hypertension and Eisenmenger syndrome. Ann Thorac Surg 2000;69: Waddell TK, Bennett LE, Kennedy R, Todd TRJ, Keshavjee S. Lung or heart-lung transplantation for Eisenmenger s syndrome: analysis of the ISHLT/UNOS Joint Thoracic Registry [Abstract]. J Heart Lung Transplant 2000;19: Maurer JR, Frost AE, Estenne M, Higenbottam T, Glanville AR. International guidelines for the selection of lung transplant candidates. The International Society for Heart and
5 Ann Thorac Surg STOICA ET AL 2001;72: HEART-LUNG TRANSPLANT FOR EISENMENGER 1891 Lung Transplantation, the American Thoracic Society, the American Society of Transplant Physicians, the European Respiratory Society. J Heart Lung Transplant 1998;17: Kendall SW, Wallwork J. Heart-lung transplantation: indications and technique. Semin Thorac Cardiovasc Surg 1992; 4: Potter CDO, Wheeldon DR, Wallwork J. Functional assessment and management of heart donors: a rationale for characterization and a guide to therapy. J Heart Lung Transplant 1995;14: Parry A, Higgins R, Wheeldon R, Bethune D, Wallwork J. The contribution of donor management and modified cold blood lung perfusate to post-transplant lung function. J Heart Lung Transplant 1999;18: D Armini AM, Callegari G, Vitulo P, et al. Risk factors for early death in patients awaiting heart-lung or heart transplantation. Transplantation 1998;66: Hopkins WE, Ochoa LL, Richardson GW, Trulock EP. Comparison of the hemodynamics and survival of adults with severe primary pulmonary hypertension or Eisenmenger syndrome. J Heart Lung Transplant 1996;15: Sharples LD, Belcher C, Dennis C, Higenbottam T, Wallwork J. Who waits longest for heart and lung transplantation? J Heart Lung Transplant 1994;13: Moulton MJ, Creswell LL, Mackey ME, Cox JL, Rosenbloom M. Reexploration for bleeding is a risk factor for adverse outcomes after cardiac operations. J Thorac Cardiovasc Surg 1996;111: Hosenpud JD, Bennett LE, Keck BM, Fiol B, Boucek MM, Novick RJ. The Registry of the International Society for Heart and Lung Transplantation: Sixteenth Official Report J Heart Lung Transplant 1999;18: Caine N, Sharples LD, Dennis C, Higenbottam TW, Wallwork J. Measurement of health-related quality of life before and after heart-lung transplantation. J Heart Lung Transplant 1996;15: O Brien BJ, Banner NR, Gibson S, Yacoub MH. The Nottingham Health Profile as a measure of quality of life following combined heart and lung transplantation. J Epidemiol Community Health 1988;42: Heng D, Sharples LD, McNeil K, Stewart S, Wreghitt T, Wallwork J. Bronchiolitis obliterans syndrome: incidence, natural history, prognosis, and risk factors. J Heart Lung Transplant 1998;17: Pasque MK, Trulock EP, Cooper JD, et al. Single lung transplantation for pulmonary hypertension. Single institution experience in 34 patients. Circulation 1995;92: Aeba R, Griffith BP, Hardesty RL, Kormos RL, Armitage JM. Isolated lung transplantation for patients with Eisenmenger s syndrome. Circulation 1993;88: Kroshus TJ, Kshettry VR, Hertz MI, Everett JE, Bolman RM. Suicide right ventricle after lung transplantation for Eisenmenger syndrome. Ann Thorac Surg 1995;59: INVITED COMMENTARY Combined heart-lung (H-L) transplantation is the least commonly performed solid organ transplant procedure in the world, and perhaps the least understood. This procedure, which was introduced in 1981 at the dawn of the era of lung transplantation was only performed 90 times in 1999 according to the seventeenth report of the International Society for Heart and Lung Transplantation (ISHLT)[1]. This is the nadir reached from a peak of 237 H-L transplants reported to the ISHLT in This is due in part to the realization that isolated lung transplantation can offer equivalent survival and physiologic recovery for many diseases previously treated with H-L transplantation such as cystic fibrosis and primary pulmonary hypertension. In such situations, utilization of the heart for isolated cardiac transplantation appears morally and ethically appropriate. The decrease is also due to the misconception that H-L transplantation is particularly morbid with poor outcomes. Experienced groups, such as the authors, have shown that excellent one-year survival of 73% to 74% can be achieved for Eisenmenger and non-eisenmenger patients. Results such as this are comparable to ISHLT data for isolated lung transplantation for pulmonary hypertension. Furthermore, data from a review of the International Society for Heart and Lung Transplantation/ United Network for Organ Sharing (ISHLT/UNOS) Joint Thoracic Registry presented at the Twentieth Annual Meeting of the ISHLT in Osaka, Japan showed that H-L is superior than isolated lung transplantation and cardiac repair for Eisenmenger s syndrome [2]. Univariate and multivariate analysis revealed that survival following H-L was particularly advantageous in patients with ventricular septal defects and multiple complex congenital anomalies confirming smaller single center reports. Unfortunately, part of the reason for the decrease in H-L transplantation is the current UNOS allocation system that unfairly disadvantages patients waiting for H-L. The current system, implemented in 1999, shows preference for patients in hospitals awaiting isolated cardiac transplantation. Current discussions at the UNOS thoracic organ committee are seeking to increase the number of organs allocated to status 1A patients in an effort to decrease waiting list mortality. The aim is altruistic, but may further disadvantage those patients whose best option for long term survival is H-L transplantation. It is critically important that policymakers do not unintentionally disadvantage this group of patients, and thereby deny them the procedure most likely to result in their survival. John V. Conte, MD Division of Cardiac Surgery Johns Hopkins Medical Institutions Blalock N Wolfe St Baltimore, MD jcontecsurg.jhmi.edu. References 1. Hosenpud JD, Bennett LE, Keck BM, et al. The registry of the International Society of Heart and Lung Transplantation: seventeenth official report J Heart Lung Transplant 2000;19: Waddell TK, Bennett LE, Kennedy R, et al. Lung or heart-lung transplantation for Eisenmenger s syndrome: analysis of the ISHLT/UNOS joint thoracic registry [Abstract]. J Heart Lung Transplant 2000;19: by The Society of Thoracic Surgeons /01/$20.00 Published by Elsevier Science Inc PII S (01)
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