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Ann Thorac Surg 2001;71:1833-1838
© 2001 The Society of Thoracic Surgeons

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Original article: cardiovascular

The paradox of survival results after heart transplantation for cardiomyopathy caused by Trypanosoma cruzi

^a Brazilian Society of Cardiology, São Paulo, Brazil

Accepted for publication February 20, 2001.

Address reprint requests to Dr Bocchi, Heart Institute (Incor), University of São Paulo Medical School, Brazil, Rua Oscar Freire 2077 apto 161, São Paulo, Brazil, CEP 05409-011
e-mail: dcledimar{at}incor.usp.br

	Abstract

Top Footnotes Abstract Introduction Material and methods Results Comment References

 
Background. Donor supply limits heart transplantation (HT) and relative priority should be given to cases with greater chances of success. The objectives of this multicenter study were (1) to determine the survival rate after heart transplantation for patients with Chagas’ heart disease (ChHD) in comparison with other causes; and (2) to identify the causes of death specifically due to reactivation of the Trypanosoma cruzi infection.

Methods. We studied 720 patients who had undergone orthotopic heart transplantation and were followed in 16 heart transplantation centers. The etiology was idiopathic dilated cardiomyopathy in 407 patients, ischemic cardiomyopathy in 196 patients, and ChHD in 117 patients.

Results. Follow-up was 2.87 ± 3.05 years (from 1 month to 13.85 years). Survival of ischemic recipients at 1, 4, 8, and 12 years was 59%, 44%, 34%, and 22%, respectively; for idiopathic dilated cardiomyopathy it was 69%, 57%, 40%, and 32%; and for ChHD it was 71%, 57%, 55%, and 46% (p < 0.027). In ischemic recipients the most frequent causes of death were infection (15.3%), acute graft failure (13.3%), and graft coronary artery disease/sudden death (7.7%). In idiopathic dilated cardiomyopathy the causes were infection (11.1%), rejection (9.6%), and acute graft failure (9.1%). In ChHD the causes were infection (10.3%), rejection (10.3%), and neoplasm (4.3%). In ChHD, reactivation of the cruzi infection was the cause of death in 2 patients.

Conclusions. The survival results after heart transplantation are paradoxical according to the usually high expected death rates for Chagas’ disease. Heart transplantation for ChHD should be regarded as a valuable treatment option.

	Introduction

Top Footnotes Abstract Introduction Material and methods Results Comment References

 
Orthotopic heart transplantation has become an accepted treatment for end-stage heart failure in underdeveloped countries [1]. The limited donor supply restricts transplantation activity in all countries and relative priority should be given to patients with greater chances of survival. Chagas’ disease is endemic in almost all Latin American countries, where it is one of the leading causes of death, affecting almost 20 million people [2]. The heart is the most commonly affected organ, responsible for up to 18% of the cases of refractory heart failure seen in Brazil [3]. Chagas’ disease is a systemic chronic infection with evidence that persistent Trypanosoma cruzi may have a role in the pathogenesis of chronic Chagas’ heart disease [4]. The recommendation for heart transplantation in the treatment of Chagas’ heart disease is controversial, in that chronic infection is a contraindication for this operation and for necessary immunosuppressive therapy. In fact, reactivation of the Trypanosoma cruzi infection was diagnosed after heart transplantation, but showed acceptable survival in studies conducted on a limited number of subjects [5–10]. Furthermore, a higher incidence of neoplasm was described in an initial experience [9]. The impact of these findings on a larger number of patients was not clarified, however.

The objectives of this multicenter study were (1) to determine the survival of heart transplantation in the treatment of Chagas’ heart disease in comparison with other indications for transplantation; (2) to identify causes of death in an attempt to determine which features contribute to our current results; and (3) to determine whether reactivation of the T. cruzi infection is a cause of death.

	Material and methods

Top Footnotes Abstract Introduction Material and methods Results Comment References

 
Population
We studied a cohort of 792 patients that underwent orthotopic heart transplantation in 16 centers in Brazil from June 1984 to April 1999 inclusive. The mean age was 42 ± 16 years; 632 of these patients were men. The etiology was idiopathic dilated cardiomyopathy in 407 patients, ischemic cardiopathy in 196 patients, Chagas’ heart disease in 117 patients, valvular disease in 29 patients, congenital anomalies in 14 patients, peripartum cardiomyopathy in 12 patients, hypertrophy cardiomyopathy in 7 patients, restrictive in 5 patients, alcoholic in 4 patients, and drugs in 1 patient. Six patients had retransplantation. The mean age for chagasic recipients was 39 ± 11 years, for idiopathic dilated cardiomyopathy it was 40 ± 15 years, and for ischemic etiology it was 51 ± 9 years. Ischemic recipients were older than idiopathic dilated cardiomyopathy and chagasic recipients (p < 0.05). The mean number of heart transplants performed by each center was 54 ± 57 (range, 1 to 207). The diagnostic criteria for chronic Chagas’ heart disease were a combination of epidemiologic data, positive serologic tests for anti-Trypanosoma cruzi (complement fixation and indirect immunofluorescence), no evidence of other cause for cardiomyopathy, and characteristic findings of chagasic cardiomyopathy in postmortem studies. Complement-fixation tests (Machado-Guerrero) were considered positive when the reaction was observed in a serum dilution equal to or greater than 1:8 and when indirect immunofluorescence was equal to or greater than 1:32 in at least two different assays. Criteria and contraindications for patient selection for transplantation among the Chagas’ disease patients were similar to those used for nonchagasic patients, except in the case of the chagasic megaesophagus or megacolon, which was considered a contraindication for heart transplantation [11].

Surgical procedure and immunosuppressive therapy
Most orthotopic heart transplantations were performed as described by Shumway and Lower [12]. Recently, the bicaval technique has been used in some centers regardless of the etiology [13]. Therapy using cyclosporine was the cornerstone of chronic immunosuppressive therapy. Immunosuppressive treatment was comparable in all etiologies and evolved during the period of the study to reducing immunosuppressive drugs without causing rejection. Intravenous methylprednisolone was used in the postoperative period followed by oral prednisone, except in one center. Azathioprine was given before and after operation. Cyclosporine dosages were adjusted according to blood cyclosporine levels, serum creatinine levels, toxicity, drug intolerance, and cases of rejection, reactivation of Chagas’ disease, or infection. Rejection was monitored through endomyocardial biopsy. In some centers echocardiography or implanted epicardial electrodes with telemetry monitoring or gallium-67 myocardial scintigraphy were used for screening for rejection. Rejections were treated when biopsies were graded III or higher by the International Society for Heart Transplantation Standardized Grading System criteria; when moderate or severe rejection presented according to the Stanford criteria; and when there was no evidence of Chagas’ disease reactivation [14, 15]. Rejections were treated in a uniform manner and were usually treated with an increased dose of steroids, either intravenous methylprednisolone or a short course of oral prednisone. Steroid-resistant rejection was treated with a polyclonal antithymocyte globulin or monoclonal antibody OKT3.

Trypanosoma infection and treatment
The diagnosis of reactivation of Chagas’ disease was considered when the parasite was detected in blood or tissues surrounded by inflammation, in association with symptoms or signs attributable to infection by T cruzi. Episodes of Chagas’ disease reactivation were successfully treated with benznidazole or allopurinol. Prophylactic benznidazole for T cruzi infection was not used routinely.

Study design and data analysis
This investigation, conducted under the auspices of the Brazilian Society of Cardiology, studied the outcome of all heart transplants performed in Brazil from June 1984 to April 1999 inclusive. The data were obtained from each of 16 centers that participated in the First Guidelines Group for Heart Transplantation of the Brazilian Society of Cardiology (see Appendix). All patients were closely and prospectively followed by each center involved in the transplants. Patients with different etiologies of heart failure had the routine follow-up and protocol after heart transplantation in their respective centers. Patients were seen regularly in the outpatient department of each center every 3 or 6 months. The study involved all transplant teams in Brazil. Sudden death was classified as death within 1 hour of the onset of acute symptoms in nonhospitalized patients without previous diagnosis of coronary artery disease, rejection, or reactivation of the T. cruzi infection.

The Kaplan-Meier method was used retrospectively to estimate the survival of all patients with idiopathic dilated cardiomyopathy, ischemic cardiomyopathy or chagasic heart disease. Patients with retransplantation and congenital disease were excluded. Survival was compared using the log-rank test. A significance level of 0.05 was adopted. Causes of death were expressed as percentages of the total population at risk for each group. The ² test was used to compare the causes of death among the idiopathic, ischemic, and chagasic etiologies. When the expected frequencies were too low Fisher’s exact test was used instead. Fisher’s exact test was also performed to compare causes of death between etiologies. To exclude the possibility of Chagas’ disease, patients were concentrated in a few institutions. Linear regression was used to analyze the correlation between the number of transplants in each center and the percentage of chagasic etiology.

	Results

Top Footnotes Abstract Introduction Material and methods Results Comment References

 
Survival
The mean overall follow-up period was 2.87 ± 3.05 years (range, 1 to 13.85 years). Survival for the entire group, excluding retransplantation (778 patients) and congenital etiology at 1, 6 months, 1, 2, 4, 6, 8, 10, and 12 years after heart transplantation, was 81% (standard error 2%), 72% (2%), 66% (2%), 61% (2%), 54% (2%), 47% (2%), 40% (2%), 32% (3%), and 27% (4%), respectively. The survival probability of patients submitted to heart transplantation for ischemic etiology at 1, 6 months, 1, 2, 4, 6, 8, 10, and 12 years was 77%, 66%, 59%, 54%, 44%, 36%, 34%, 26%, and 22%, respectively; for idiopathic dilated cardiomyopathy survival was 85%, 73%, 69%, 64%, 57%, 51%, 40%, 32%, and 32%; and for chagasic etiology survival was 83%, 76%, 71%, 62%, 57%, 55%, 55%, 46%, and 46% (Fig 1). The survival rate of patients who underwent transplants for the treatment of Chagas’ heart disease was better in comparison with the total group survival (p < 0.03). Survival of chagasic recipients was significantly better in comparison with idiopathic and ischemic cardiomyopathy (p < 0.027). Survival of chagasic recipients was better than patients with ischemic cardiomyopathy in both short- and long-term follow-up. However, survival of chagasic and idiopathic dilated cardiomyopathy recipients was comparable in short-term follow-up (until 3 years). It was better for chagasic recipients at long-term follow-up (> 3 years); however, the small number of chagasic recipients at risk after 8 years is one limitation of these results.

View larger version (14K): [in this window] [in a new window]   Fig 1. Comparison of estimated survival using the Kaplan-Meier method after primary heart transplantation for the treatment of ischemic (Ischemic), idiopathic dilated cardiomyopathy (IDC), and chagasic etiology (chagasic) (p < 0.027).

Causes of death
The causes of death for the entire group were infection in 23%, acute graft failure in 19%, rejection in 18%, sudden death in 7.3%, graft coronary vascular disease in 6%, indeterminate in 6%, hemorrhagic disorders in the immediate postoperative period in 5%, cerebral stroke in 4%, neoplasm in 3.7%, hyperacute rejection in 2.9%, infective endocarditis in 1%, pulmonary thromboembolism in 0.7%, suicide in 0.7%, atrioventricular block in 0.7%, hepatic failure in 0.7%, tricuspid insufficiency in 0.5%, cardiac restrictive syndrome in 0.5%, accident in 0.2%, technical surgical limitations in 0.3%, dissecting aneurysm of the aorta in 0.3%, mesenteric ischemia in 0.3%, and reactivation of the T cruzi infection with myocarditis and meningoencephalitis in 0.3%. Neoplasm was not documented in any women.

Table 1 shows the causes of death (350 deaths) according to etiology. Reactivation of the T cruzi infection was a rare cause of death. Graft coronary artery disease/sudden death and acute graft failure were infrequent causes of death in chagasic patients in comparison with other etiologies. Neoplasia was more frequent in chagasic patients. Infection, acute graft failure, and hemorrhagic disorder were more frequent in patients with ischemic cardiomyopathy. Rejection rate was lower in patients with ischemic cardiomyopathy.

	Comment

Top Footnotes Abstract Introduction Material and methods Results Comment References

Our higher early mortality for all etiologies may be influenced by several factors. The most prominent are the number of procedures per transplantation center, and the unreliable quality of donors. In complex surgical procedures such as heart transplantation there is an association between a low volume of procedures and an increased risk of death for patients who undergo the procedure. We had many centers that performed less than nine transplants per year, for whom a higher mortality rate was expected in comparison with those that performed nine or more procedures [16]. Our results did not corroborate this previous report, however. Some controversial results also were reported regarding the influence of etiology on survival after heart transplantation [17]. The primary cause of death in our experience was infection. This corroborates most reports, except multiple organ failure cited in one report and coronary graft artery disease in another [16, 18, 19]. Rejection was the second cause of death in idiopathic dilated cardiomyopathy and chagasic cardiomyopathy and corroborates other reports. In our results acute graft failure was the most important cause of death in idiopathic dilated cardiomyopathy and the second cause in patients with ischemic cardiomyopathy. This is in contrast with most reports but in agreement with one study [18].

Acute graft failure and functional status of the transplanted heart, especially the right ventricular function, is primarily related to donor selection and preoperative status of the donor heart, pulmonary vascular disease, recipient selection, the quality of graft preservation, surgical techniques, and immunologic complications [20]. One possible explanation for the high percentage of acute graft failure could be the use of marginal donors in our country due to both the lack and poor care of potential donors. Social, economic, and ethical considerations may vary in different countries, and notable differences in practice have been documented in heart transplantation [21]. Exclusion criteria for selection of recipients was the same for all causes of heart disease and included elevated pulmonary vascular resistance and other systemic diseases [1, 11].

The survival rate of idiopathic dilated cardiomyopathy and ischemic cardiomyopathic recipients was lower than that described in developed countries and in the 1999 International Society for Heart and Lung Transplantation Report [17, 18, 22–24]. Survival after heart transplantation for Chagas’ heart disease is comparable to survival reported by single centers and by the International Society for Heart and Lung Transplantation Report for other etiologies [16–18, 22–24]. The first report of long-term survival after heart transplantation for the treatment of Chagas’ heart disease was published by Bocchi and colleagues in 1993 [10]. Few reports have been published since 1993 describing the results of heart transplantation for the treatment of chagasic recipients and all studies were done on a small number of patients [5, 7, 8]. Some publications included a respective survival curve with limited clinical conclusions based on the small number of patients at risk [5, 7]. Our report includes a sufficient and significant number of patients to suggest a clinical indication of heart transplantation for Chagas’ disease.

The main reason explaining the better long-term survival rate after heart transplantation for Chagas’ heart disease in comparison with other causes is the low incidence of graft coronary artery disease and sudden death in chagasic recipients. Data from one recent study also suggested a lower incidence of graft coronary artery disease in chagasic recipients (Bacal F, Thesis. 1999, Asymptomatic allograft vasculopathy after heart transplantation, São Paulo University). Graft coronary artery disease has been described as the major cause of late death after heart transplantation [18]. Possible factors associated with this low incidence of graft coronary artery disease should be investigated. The contribution of a high incidence of malignant neoplasm in mortality was probably offset by a lower incidence of acute graft failure and a low incidence of graft coronary artery disease/sudden death in chagasic patients. Our high incidence of malignant neoplasia corroborates a previous report [9]. Multiple factors such as reactivation of T cruzi infection, benzonidazole treatment, and immunologic disorders associated with T cruzi infection could influence the high incidence of neoplasm [9]. The reasons for the lower incidence of acute graft failure as a cause of death are not known. The high incidence and frequent predominance of right ventricular dysfunction before transplantation in chagasic recipients in comparison with other etiologies could lead to lower pulmonary vascular resistance and, consequently, a reduced incidence of right ventricular graft failure.

The better results for chagasic recipients were obtained despite that these patients had less income and were more socioeconomically deprived. In general, more socioeconomically deprived patients are less likely to be referred for complex procedures because of worse results [25]. Furthermore, idiopathic dilated cardiomyopathy and ischemic cardiomyopathic recipients were older than chagasic recipients [26].

In summary, survival using the same transplantation protocol after heart transplantation is better for chagasic recipients as compared with ischemic cardiomyopathic recipients for short- and long-term follow-up. Chagasic survival is comparable to idiopathic cardiomyopathy for short- and medium-term survival and better for long-term follow-up. However, the small number of patients at risk in long-term follow-up limits a definitive conclusion in comparison with idiopathic dilated cardiomyopathy. This survival result is a paradox because of the usually generally higher accepted risk factors for death for chagasic recipients, due to infection, and greater social deprivation. Heart transplantation for the treatment of Chagas’ heart disease should be regarded worthwhile in underdeveloped countries.

	Footnotes

Top Footnotes Abstract Introduction Material and methods Results Comment References

 
^* A list of the participants of the First Guidelines Group For Heart Transplantation of the Brazilian Society of Cardiology appears in the Appendix.

	Appendix

 
Participants of the First Guidelines Group for Heart Transplantation of the Brazilian Society of Cardiology
Writing coordinator: Edimar Alcides Bocchi; Writing committee: Edimar Alcides Bocchi, Alfredo Fiorelli, Luis Felipe Moreira, Fernando Bacal; Clinical coordinator: Edimar Alcides Bocchi; Surgical coordinator: Alfredo Fiorelli.

Participants: Edimar Alcides Bocchi, Alfredo Fiorelli, Estela Azeka, Danton Rocha Loures, Marcelo Biscegli Jatene, Maria Elenita Sampaio Favarato, Maria da Consolação V. Moreira, Hélio M. Magalhães, Solange Bordignon, Ana Augusta Maria Pereira, Cláudia Regina Haponczuk de Lemos, Leda Maria Muniz, Siliva Foresti, Fernando Bacal, Maria Gerbásia de Lima, Ricardo Manrique, Maria de Lourdes Higuchi, Paulo Brofman, Deuzeny Tenório, João David de Souza, Antonio Carlos de Carvalho, Márcia Marcelino de Souza, Dirceu Rodrigues de Almeida, Carlos Ernesto Starling, Luís Fernando Camargo, Valéria Bezerra de Carvalho, José Henrique Vila, Cláudio Pereira da Cunha, Guilherme Veiga Guimarães, Nadine Clausell, Glória Heloise Perez, Dirceu Carrara, Noedir Stolf, Luís Felipe Moreira, Maurício Scanavacca, José Dario Frota-Filho, Bayard Gontijo-Filho, Guaracy F. Teixeira-Filho, Domingos Marcolino Braile, Ivo Abrhão Nesralla, José Pedro da Silva, José Teles de Mendonça, Jerônimo Antonio Fortunato, Jarbas Dinkhuysen, Marcondes T. Neves-Junior, Orlando Petrucci-Junior, Cícera Isabel C. de Oliveira, Lídia Lucas Lima, João Nelson Rodrigues Branco, Iseu de Santo Elias Affonso Costa, Glauco Lobo-Filho, José Wanderly Neto, Carlos Roberto Moraes.

Data collection: Dirceu Carrara, Maria de Lourdes Ribeiro; Statistician: MSc Mariana Curi.

	References

Top Footnotes Abstract Introduction Material and methods Results Comment References

 

1. Bocchi E.A., Bellotti G., Moreira L.F.P., et al. Mid-term results of heart transplantation, cardiomyoplasty, and medical treatment of refractory heart failure caused by idiopathic dilated cardiomyopathy. J Heart Lung Transplant 1996;15:736-745.[Medline]
2. World Health Organization Expert Committee. Chagas’ disease. In: World Health Organization Expert Committee. World Health Organization technical report series 697. Geneva: WHO, 1984:50–5.
3. Bocchi E.A. Situação atual das indicações e resultados do tratamento cirúrgico da insuficiência cardíaca. Arq Bras Cardiol 1994;63:523-530.[Medline]
4. Bellotti G., Bocchi E.A., Moraes A.V., et al. In vivo detection of Trypanosoma cruzi antigens in hearts of patients with chronic Chagas’ heart disease. Heart J 1996;131:301-307.
5. Bocchi E.A., Bellotti G., Mocelin A., et al. Heart transplantation for chronic Chagas’ heart disease. Ann Thorac Surg 1996;61:1727-1733.[Abstract/Free Full Text]
6. Stolf N.A., Higushi L., Bocchi E.A., et al. Heart transplantation in patients with Chagas’ disease cardiomyopathy. J Heart Transplant 1987;6:307-312.[Medline]
7. Carvalho V.B., Souza E.F.L., Vila J.H.A., et al. Transplantation in Chagas’ disease: 10 years after the initial experience. Circulation 1996;94:1815-1817.[Abstract/Free Full Text]
8. Almeida D.R., Carvalho A.C.C., Branco J.N., et al. Chagas disease reactivation after heart transplantation: efficacy of allopurinol treatment. J Heart Lung Transplant 1996;15:988-992.[Medline]
9. Bocchi E.A., Higuchi M.L., Vieira M.C., et al. Higher incidence of malignant neoplasms after heart transplantation for treatment for chronic Chagas’ heart disease. J Heart Lung Transpl 1998;17:399-405.[Medline]
10. Bocchi E.A., Bellotti G., Uip D.E., et al. Long-term follow-up after heart transplantation in Chagas’ disease. Transplantation Proc 1993;25:1329-1330.[Medline]
11. Guidelines for heart transplantation of the Brazilian Society of Cardiology. Arq Bras Cardiol 1999;73:1–57.
12. Shumway N.E., Lower R.R. Transplantation of the heart. Adv Surg 1966;2:265-284.[Medline]
13. Deleuze P.H., Benvenuti C., Mazzucotelli P., et al. Orthotopic cardiac transplantation with direct caval anastomosis: is it the optimal procedure. J Thorac Cardiovasc Surg 1995;109:731-737.[Abstract/Free Full Text]
14. Billingham M.E., Cary N.R.B., Hamond M.E., et al. A working formulation for the standardization of nomenclature in the diagnosis of heart and lung rejection: Heart Rejection Study. J Heart Transplant 1990;9:587-593.[Medline]
15. Billingham M.E. Endomyocardial biopsy diagnosis of acute rejection in cardiac allografts. Prog Cardiovasc Dis 1990;33:11-18.[Medline]
16. Hosenpud J.D., Breen T.J., Edwards E.B., Daily O.P., Hunsicker L.G. The effect of transplant center volume on cardiac transplant outcome: a report of the United network for Organ Sharing Registry. JAMA 1994;271:1844-1849.[Abstract]
17. Walley V.M., Masters R.G., Boone A.S., et al. Analysis of death after heart transplantation: the University of Otawa Heart Institute Experience. J Heart Lung Transplant 1993;12:790-801.[Medline]
18. Cabrol C, Nataf P, Pavie A, Bors V, et al. Heart transplantation in 1992: the La Pitie experience. Transplant Proc 1993;1992:25:2220–1.
19. Fraund S., Pething K., Franke U., et al. Ten year survival after heart transplantation: palliative procedure or successful long term treatment?. Heart 1999;82:47-51.[Abstract/Free Full Text]
20. Bittner H.B., Chen E.P., Biswas S.S., Trigt P.V., Davis R.D. Right ventricular dysfunction after cardiac transplantation: primarily related to status of donor heart. Ann Thorac Surg 1999;68:1605-1611.[Abstract/Free Full Text]
21. Anyanwu A.C., Rogers C.A., Murday A.J. Variation in cardiac transplantation: comparisons between the United Kingdom and United States. J Heart Lung Transplant 1999;18:297-303.[Medline]
22. Pasic M., Loebe M., Hummel M., et al. Heart transplantation. a single-center experience. Ann Thorac Surg 1999;62:1685-1690.[Abstract/Free Full Text]
23. Robbins R.C., Barlow C.W., Oyer P.E., et al. Thirty years of cardiac transplantation at Stanford University. J Thoracic Cardiovasc Surg 1999;117:939-951.[Abstract/Free Full Text]
24. 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: Sixteenth Official Report –1999. J Heart Lung Transplant 1999;18:611-626.[Medline]
25. Pell J.P., Pell A.C.H., Norrie J., Ford I., Cobbe S.M. Effect of socioeconomic deprivation on waiting time for cardiac surgery: retrospective cohort study. BMJ 2000;320:15-18.[Abstract/Free Full Text]
26. Bourge C.R., Kirklin J.K., Naftel D.C. Predicting outcome after heart transplantation: lessons from the cardiac transplant research database. Curr Opin Cardiol 1997;12:136-145.[Medline]

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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): Edimar Alcides Bocchi Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Bocchi, E. A. Articles by Fiorelli, A. Search for Related Content PubMed PubMed Citation Articles by Bocchi, E. A. Articles by Fiorelli, A. Related Collections Transplantation - heart