- Email: [email protected]
Heart Transplantation for End-Stage Heart Failure Due to Cardiac Sarcoidosis
Heart Transplantation for End-Stage Heart Failure Due to Cardiac Sarcoidosis D. Perkel, L.S.C. Czer, R.P. Morrissey, A. Ruzza, M. Rafiei, M. Awad, J. Patel, and J.A. Kobashigawa ABSTRACT Background. Cardiac sarcoidosis with end-stage heart failure has a poor prognosis without transplantation. The rates of sarcoid recurrence and rejection are not well established after heart transplantation. Methods. A total of 19 heart transplant recipients with sarcoid of the explanted heart were compared with a contemporaneous control group of 1,050 heart transplant recipients without cardiac sarcoidosis. Assessed outcomes included 1st-year freedom from any treated rejection, 5-year actuarial survival, 5-year freedom from cardiac allograft vasculopathy (CAV), 5-year freedom from nonfatal major adverse cardiac events (NF-MACE), and recurrence of sarcoid in the allograft or other organs. Patients with sarcoidosis were maintained on low-dose corticosteroids after transplantation. Results. There were no significant differences between the sarcoid and control groups in 1st-year freedom from any treated rejection (79% and 90%), 5-year posttransplantation survival (79% and 83%), 5-year freedom from CAV (68% and 78%), and 5-year freedom from NF-MACE (90% and 88%). Causes of death (n ¼ 5) in the sarcoid group were coccidioidomycosis, pneumonia, rejection, hemorrhage, and CAV. No patient had recurrence of sarcoidosis in the cardiac allograft. Three of 19 patients (16%) experienced recurrence of extracardiac sarcoid, with no mortality. Conclusions. Patients with cardiac sarcoidosis undergoing heart transplantation have acceptable long-term outcomes without evidence of recurrence of sarcoidosis in the allograft when maintained on low-dose corticosteroids. Progression of extracardiac sarcoid was uncommon, possibly related to immunosuppression. In patients with cardiac sarcoidosis, heart transplantation is a viable treatment modality.
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LINICAL SYNDROMES of cardiac sarcoidosis can vary from an asymptomatic state to end-stage heart failure. Cardiac sarcoidosis carries a dismal prognosis if untreated, with a 5-year survival of w 10%. With corticosteroid treatment, 5-year survival increases to 75%, but there remain a significant proportion who develop end-stage heart failure1,2. Sarcoidosis is characterized by an immune-mediated granulomatous reaction involving monocytes, lymphocytes, and cytokines. Extensive infiltration of the left ventricular walls with sarcoid granulomas causes systolic dysfunction through decreased ventricular contraction. Often, patients exhibit arrhythmias secondary to conduction system involvement that can range from first-degree AV block to complete heart block, with or without right or left bundle branch block. Ventricular tachycardia can ensue from
a reentrant rhythm involving areas of myocardial fibrosis, which may lead to sudden cardiac death3e5. The extensive degree of cardiac disease from this clinical syndrome results in significant morbidity and mortality. Patients with end-stage heart failure are at times turned down for cardiac transplantation owing to concerns about sarcoid recurrence in the cardiac allograft and failure of
From the Divisions of Cardiology (D.P., L.S.C.C., R.P.M., M.R., M.A., J.P., J.A.K.) and Cardiothoracic Surgery (A.R.), CedarsSinai Heart Institute, and the Comprehensive Transplant Center, Cedars-Sinai Medical Center, Los Angeles, California. Address reprint requests to Lawrence S. C. Czer, MD, Medical Director, Heart Transplant Program, 8700 Beverly Blvd, Los Angeles, CA 90048. E-mail: [email protected]
0041-1345/13/$esee front matter http://dx.doi.org/10.1016/j.transproceed.2013.02.116
ª 2013 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
2384
Transplantation Proceedings, 45, 2384e2386 (2013)
HEART TRANSPLANT FOR CARDIAC SARCOIDOSIS
other organs secondary to sarcoidosis. Previous analysis of ISHLT registry data suggests that in patients with cardiac sarcoidosis, heart transplantation has a survival rate similar to transplantation for other reasons.6 However, the rates of cardiac recurrence, rejection, and sarcoid progression or regression in other organs remain poorly defined. METHODS We reviewed 19 patients with cardiac sarcoidosis who had end-stage heart failure treated with orthotopic heart transplantation from January 1991 to July 2010. All patients had pathologically proven sarcoidosis after pathologic examination of the explanted heart. The control group consisted of 1,050 patients without cardiac sarcoidosis who received a heart transplant during this same time period. The surgical technique7e10 and the endomyocardial biopsy protocol11e14 were described previously. Patients were followed for 1e20 years; mean follow-up duration was 68 months. The study was approved by the Institutional Review Board. Assessed outcomes included 1-year freedom from any-treated rejection, 5-year actuarial survival, freedom from cardiac allograft vasculopathy (CAV; angiographic stenosis 30%), and 5-year freedom from nonfatal major adverse cardiac events (NFMACE). NF-MACE was defined as myocardial infarction, congestive heart failure, percutaneous cardiac intervention, need for defibrillator or pacemaker, stroke, or new peripheral vascular disease. Additional outcomes assessed were evidence of sarcoidosis in the cardiac allograft (on endomyocardial biopsy or autopsy), and the occurrence of extracardiac sarcoid.
RESULTS
The 19 heart transplant recipients with cardiac sarcoidosis ranged in age from 29 to 68 years, and 10 (53%) were male. Seven patients (37%) had hypertension, 4 (21%) diabetes mellitus type II, and 2 (11%) hyperlipidemia. Eight patients (42%) had known preoperative extracardiac sarcoidosis. Four patients (21%) had biopsy-confirmed cardiac sarcoidosis before transplant, and these patients, as well as the other 15 patients (79%), had cardiac sarcoidosis confirmed with pathologic examination of the explanted heart. Immunosuppressive regimens included prednisone in all patients, tacrolimus or cyclosporine, and mycophenolate or azathioprine. Steroids were gradually tapered down to a minimum of 5 mg/d for the sarcoidosis patients. Patients underwent endomyocardial biopsies according to a standardized regimen. In the first year following the transplant, 4 of 19 patients (21%) exhibited rejection requiring treatment, compared with 10% of the control patients, but the difference did not reach statistical significance (P ¼ .12). These episodes of rejection were treated with high-dose corticosteroids and, when there was evidence of hemodynamic compromise, anti-thymocyte globulin. First-year freedom from any treated rejection was 79% in the sarcoid group and 90% in the control group (P ¼ NS). There were no intraoperative deaths. During the course of follow-up, 5 patients died. One patient died of disseminated coccidioidomycosis 2 months after transplant. A 2nd patient died of bacterial pneumonia 5 months after transplant. A 3rd
2385
patient exhibited 3B-3R rejection and died 1 year after transplant from cellular rejection despite treatment. A 4th patient died from a mediastinal hemorrhage 4 years after transplantation. And a 5th patient died of coronary allograft vasculopathy 8 years after transplantation. The other 14 patients were alive. The 5-year survival was 79% in the sarcoid group and 83% in the control group (P ¼ NS). The development of CAV was defined as > 30% stenosis in a coronary artery seen on follow-up angiograms after transplantation. Seven of the 19 patients (32%) receiving transplants for cardiac sarcoidosis were found to have CAV compared with 22% in the control group, but the difference did not reach statistical significance (P ¼ .09). The 5-year freedom from CAV was 68% in the sarcoid group and 78% in the control group (P ¼ NS). There was no difference in 5-year freedom from NFMACE at 90% and 88% in the sarcoid and control groups respectively, (P ¼ .95). No patient had recurrence of sarcoidosis in the cardiac allograft. Two patients were found to have recurrence of pulmonary sarcoidosis, and 1 patient was found to have recurrence of hepatic sarcoidosis. No recurrences were associated with mortality. DISCUSSION
Heart transplantation is not universally considered in endstage heart failure patients with cardiac sarcoidosis, owing to concerns for sarcoid recurrence in the cardiac allograft and possible progression of disease in other organs. We reviewed the outcomes of cardiac transplantation in patients with cardiac sarcoidosis and compared the outcomes in patients without cardiac sarcoidosis who received a heart transplant during a similar time period. In our study, there was no difference seen in 5-year actuarial survival between patients who underwent heart transplantation for cardiac sarcoidosis and the control patients who underwent heart transplantation for other indications. There was also no significant difference between the sarcoid and control groups in 5-year freedom from CAV, 5-year freedom from NF-MACE, and 1st-year freedom from any treated rejection. Our results confirm an earlier retrospective study by Zaidi et al which examined outcomes for heart transplant recipients with cardiac sarcoidosis from 1987 to 2005 by analysis of the national UNOS database. That study showed the 1and 5-year survival for patients transplanted for cardiac sarcoidosis to be greater than that of the general population of heart transplant recipients.6 Patients with end-stage heart failure from sarcoidosis are often not considered for transplantation, because of concern regarding possible recurrence in the cardiac allograft. In the present study, immunosuppression with corticosteroids was maintained, and none of the patients exhibited recurrence in the cardiac allograft. There were 3 cases of extracardiac sarcoidosis recurrence in the study group, but these events did not result in mortality.
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In the literature, there are scattered case reports of sarcoid recurrence in the cardiac allograft after transplant15,16. Luk et al described a patient who exhibited sarcoid recurrence 45 months after transplantation, soon after tapering off corticosteroids16. Khan et al described a patient who developed sarcoidosis in the allograft only 1 month after tapering off corticosteroids15. The effect of corticosteroids to prevent cardiac sarcoidosis progression is not dose dependent1,2. Based on our data and scattered case reports, it appears that maintaining patients with sarcoidosis on low doses of corticosteroids for life may prevent recurrence of sarcoid in the cardiac allograft. Limitations of the present study are the small sample size of the cardiac sarcoidosis group and the retrospective analysis of the data. In conclusion, patients with cardiac sarcoidosis undergoing heart transplantation have an acceptable long-term outcome without recurrence of sarcoid in the donor heart when maintained on corticosteroids. Cardiac transplantation for patients with sarcoidosis appears to be a viable treatment modality and may be considered when indicated for advanced heart failure.
REFERENCES 1. Yazaki Y, Isobe M, Hiramitsu S, et al. Comparison of clinical features and prognosis of cardiac sarcoidosis and idiopathic dilated cardiomyopathy. Am J Cardiol. 1998;82(4):537e540. 2. Yazaki Y, Isobe M, Hiroe M, et al; Central Japan Heart Study Group. Prognostic determinants of long-term survival in Japanese patients with cardiac sarcoidosis treated with prednisone. Am J Cardiol. 2001;88(9):1006e1010. 3. Deng JC, Baughman RP, Lynch JP 3rd. Cardiac involvement in sarcoidosis. Semin Resp Crit Care Med. 2002;23(6):513e527. 4. Habersberger J, Manins V, Taylor AJ. Cardiac sarcoidosis. Intern Med J. 2008;38(4):270e277. 5. Nunes H, Freynet O, Naggara N, et al. Cardiac sarcoidosis. Semin Resp Crit Care Med. 2010;31(4):428e441.
PERKEL, CZER, MORRISSEY ET AL 6. Zaidi AR, Zaidi A, Vaitkus PT. Outcome of heart transplantation in patients with sarcoid cardiomyopathy. J Heart Lung Transplant. 2007;26(7):714e717. 7. Blanche C, Valenza M, Aleksic I, Czer LS, Trento A. Technical considerations of a new technique for orthotopic heart transplantation. Total excision of recipient’s atria with bicaval and pulmonary venous anastomoses. J Cardiovasc Surg. 1994;35(4): 283e287. 8. Blanche C, Valenza M, Czer LS, et al. Orthotopic heart transplantation with bicaval and pulmonary venous anastomoses. Ann of Thorac Surgery. 1994;58(5):1505e1509. 9. Trento A, Czer LS, Blanche C. Surgical techniques for cardiac transplantation. Semin Thorac Cardiovasc Surg. 1996;8(2):126e132. 10. Trento A, Takkenberg JM, Czer LS, et al. Clinical experience with one hundred consecutive patients undergoing orthotopic heart transplantation with bicaval and pulmonary venous anastomoses. J Thorac Cardiovasc Surg. 1996;112(6):1496e1502. discussion 1502-1503. 11. Aleksic I, Freimark D, Blanche C, Czer LS, Trento A. Does total orthotopic heart transplantation offer improved hemodynamics during cellular rejection events? Transplantat Proc. 2003;35(4):1532e1535. 12. Aleksic I, Freimark D, Blanche C, Czer LS, Trento A. Hemodynamics during humoral rejection events with total versus standard orthotopic heart transplantation. Ann Thorac Cardiovasc Surg. 2004;10(5):285e289. 13. Daneshvar DA, Czer LS, Phan A, Trento A, Schwarz ER. Heart transplantation in the elderly: why cardiac transplantation does not need to be limited to younger patients but can be safely performed in patients above 65 years of age. Ann Transplant. 2010;15(4):110e119. 14. Goland S, Czer LS, Coleman B, et al. Induction therapy with thymoglobulin after heart transplantation: impact of therapy duration on lymphocyte depletion and recovery, rejection, and cytomegalovirus infection rates. J Heart Lung Transplant. 2008;27(10): 1115e1121. 15. Khan R, Tweedie EJ, Pflugfelder PW, White JA. Cardiac sarcoid in a heart transplant recipient: detection with cardiac magnetic resonance imaging. Transplantat Proc. 2010;42(5): 1976e1978. 16. Luk A, Lee A, Ahn E, Soor GS, Ross HJ, Butany J. Cardiac sarcoidosis: recurrent disease in a heart transplant patient following pulmonary tuberculosis infection. Can J Cardiol. 2010;26(7): e273ee275.
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LINICAL SYNDROMES of cardiac sarcoidosis can vary from an asymptomatic state to end-stage heart failure. Cardiac sarcoidosis carries a dismal prognosis if untreated, with a 5-year survival of w 10%. With corticosteroid treatment, 5-year survival increases to 75%, but there remain a significant proportion who develop end-stage heart failure1,2. Sarcoidosis is characterized by an immune-mediated granulomatous reaction involving monocytes, lymphocytes, and cytokines. Extensive infiltration of the left ventricular walls with sarcoid granulomas causes systolic dysfunction through decreased ventricular contraction. Often, patients exhibit arrhythmias secondary to conduction system involvement that can range from first-degree AV block to complete heart block, with or without right or left bundle branch block. Ventricular tachycardia can ensue from
a reentrant rhythm involving areas of myocardial fibrosis, which may lead to sudden cardiac death3e5. The extensive degree of cardiac disease from this clinical syndrome results in significant morbidity and mortality. Patients with end-stage heart failure are at times turned down for cardiac transplantation owing to concerns about sarcoid recurrence in the cardiac allograft and failure of
From the Divisions of Cardiology (D.P., L.S.C.C., R.P.M., M.R., M.A., J.P., J.A.K.) and Cardiothoracic Surgery (A.R.), CedarsSinai Heart Institute, and the Comprehensive Transplant Center, Cedars-Sinai Medical Center, Los Angeles, California. Address reprint requests to Lawrence S. C. Czer, MD, Medical Director, Heart Transplant Program, 8700 Beverly Blvd, Los Angeles, CA 90048. E-mail: [email protected]
0041-1345/13/$esee front matter http://dx.doi.org/10.1016/j.transproceed.2013.02.116
ª 2013 by Elsevier Inc. All rights reserved. 360 Park Avenue South, New York, NY 10010-1710
2384
Transplantation Proceedings, 45, 2384e2386 (2013)
HEART TRANSPLANT FOR CARDIAC SARCOIDOSIS
other organs secondary to sarcoidosis. Previous analysis of ISHLT registry data suggests that in patients with cardiac sarcoidosis, heart transplantation has a survival rate similar to transplantation for other reasons.6 However, the rates of cardiac recurrence, rejection, and sarcoid progression or regression in other organs remain poorly defined. METHODS We reviewed 19 patients with cardiac sarcoidosis who had end-stage heart failure treated with orthotopic heart transplantation from January 1991 to July 2010. All patients had pathologically proven sarcoidosis after pathologic examination of the explanted heart. The control group consisted of 1,050 patients without cardiac sarcoidosis who received a heart transplant during this same time period. The surgical technique7e10 and the endomyocardial biopsy protocol11e14 were described previously. Patients were followed for 1e20 years; mean follow-up duration was 68 months. The study was approved by the Institutional Review Board. Assessed outcomes included 1-year freedom from any-treated rejection, 5-year actuarial survival, freedom from cardiac allograft vasculopathy (CAV; angiographic stenosis 30%), and 5-year freedom from nonfatal major adverse cardiac events (NFMACE). NF-MACE was defined as myocardial infarction, congestive heart failure, percutaneous cardiac intervention, need for defibrillator or pacemaker, stroke, or new peripheral vascular disease. Additional outcomes assessed were evidence of sarcoidosis in the cardiac allograft (on endomyocardial biopsy or autopsy), and the occurrence of extracardiac sarcoid.
RESULTS
The 19 heart transplant recipients with cardiac sarcoidosis ranged in age from 29 to 68 years, and 10 (53%) were male. Seven patients (37%) had hypertension, 4 (21%) diabetes mellitus type II, and 2 (11%) hyperlipidemia. Eight patients (42%) had known preoperative extracardiac sarcoidosis. Four patients (21%) had biopsy-confirmed cardiac sarcoidosis before transplant, and these patients, as well as the other 15 patients (79%), had cardiac sarcoidosis confirmed with pathologic examination of the explanted heart. Immunosuppressive regimens included prednisone in all patients, tacrolimus or cyclosporine, and mycophenolate or azathioprine. Steroids were gradually tapered down to a minimum of 5 mg/d for the sarcoidosis patients. Patients underwent endomyocardial biopsies according to a standardized regimen. In the first year following the transplant, 4 of 19 patients (21%) exhibited rejection requiring treatment, compared with 10% of the control patients, but the difference did not reach statistical significance (P ¼ .12). These episodes of rejection were treated with high-dose corticosteroids and, when there was evidence of hemodynamic compromise, anti-thymocyte globulin. First-year freedom from any treated rejection was 79% in the sarcoid group and 90% in the control group (P ¼ NS). There were no intraoperative deaths. During the course of follow-up, 5 patients died. One patient died of disseminated coccidioidomycosis 2 months after transplant. A 2nd patient died of bacterial pneumonia 5 months after transplant. A 3rd
2385
patient exhibited 3B-3R rejection and died 1 year after transplant from cellular rejection despite treatment. A 4th patient died from a mediastinal hemorrhage 4 years after transplantation. And a 5th patient died of coronary allograft vasculopathy 8 years after transplantation. The other 14 patients were alive. The 5-year survival was 79% in the sarcoid group and 83% in the control group (P ¼ NS). The development of CAV was defined as > 30% stenosis in a coronary artery seen on follow-up angiograms after transplantation. Seven of the 19 patients (32%) receiving transplants for cardiac sarcoidosis were found to have CAV compared with 22% in the control group, but the difference did not reach statistical significance (P ¼ .09). The 5-year freedom from CAV was 68% in the sarcoid group and 78% in the control group (P ¼ NS). There was no difference in 5-year freedom from NFMACE at 90% and 88% in the sarcoid and control groups respectively, (P ¼ .95). No patient had recurrence of sarcoidosis in the cardiac allograft. Two patients were found to have recurrence of pulmonary sarcoidosis, and 1 patient was found to have recurrence of hepatic sarcoidosis. No recurrences were associated with mortality. DISCUSSION
Heart transplantation is not universally considered in endstage heart failure patients with cardiac sarcoidosis, owing to concerns for sarcoid recurrence in the cardiac allograft and possible progression of disease in other organs. We reviewed the outcomes of cardiac transplantation in patients with cardiac sarcoidosis and compared the outcomes in patients without cardiac sarcoidosis who received a heart transplant during a similar time period. In our study, there was no difference seen in 5-year actuarial survival between patients who underwent heart transplantation for cardiac sarcoidosis and the control patients who underwent heart transplantation for other indications. There was also no significant difference between the sarcoid and control groups in 5-year freedom from CAV, 5-year freedom from NF-MACE, and 1st-year freedom from any treated rejection. Our results confirm an earlier retrospective study by Zaidi et al which examined outcomes for heart transplant recipients with cardiac sarcoidosis from 1987 to 2005 by analysis of the national UNOS database. That study showed the 1and 5-year survival for patients transplanted for cardiac sarcoidosis to be greater than that of the general population of heart transplant recipients.6 Patients with end-stage heart failure from sarcoidosis are often not considered for transplantation, because of concern regarding possible recurrence in the cardiac allograft. In the present study, immunosuppression with corticosteroids was maintained, and none of the patients exhibited recurrence in the cardiac allograft. There were 3 cases of extracardiac sarcoidosis recurrence in the study group, but these events did not result in mortality.
2386
In the literature, there are scattered case reports of sarcoid recurrence in the cardiac allograft after transplant15,16. Luk et al described a patient who exhibited sarcoid recurrence 45 months after transplantation, soon after tapering off corticosteroids16. Khan et al described a patient who developed sarcoidosis in the allograft only 1 month after tapering off corticosteroids15. The effect of corticosteroids to prevent cardiac sarcoidosis progression is not dose dependent1,2. Based on our data and scattered case reports, it appears that maintaining patients with sarcoidosis on low doses of corticosteroids for life may prevent recurrence of sarcoid in the cardiac allograft. Limitations of the present study are the small sample size of the cardiac sarcoidosis group and the retrospective analysis of the data. In conclusion, patients with cardiac sarcoidosis undergoing heart transplantation have an acceptable long-term outcome without recurrence of sarcoid in the donor heart when maintained on corticosteroids. Cardiac transplantation for patients with sarcoidosis appears to be a viable treatment modality and may be considered when indicated for advanced heart failure.
REFERENCES 1. Yazaki Y, Isobe M, Hiramitsu S, et al. Comparison of clinical features and prognosis of cardiac sarcoidosis and idiopathic dilated cardiomyopathy. Am J Cardiol. 1998;82(4):537e540. 2. Yazaki Y, Isobe M, Hiroe M, et al; Central Japan Heart Study Group. Prognostic determinants of long-term survival in Japanese patients with cardiac sarcoidosis treated with prednisone. Am J Cardiol. 2001;88(9):1006e1010. 3. Deng JC, Baughman RP, Lynch JP 3rd. Cardiac involvement in sarcoidosis. Semin Resp Crit Care Med. 2002;23(6):513e527. 4. Habersberger J, Manins V, Taylor AJ. Cardiac sarcoidosis. Intern Med J. 2008;38(4):270e277. 5. Nunes H, Freynet O, Naggara N, et al. Cardiac sarcoidosis. Semin Resp Crit Care Med. 2010;31(4):428e441.
PERKEL, CZER, MORRISSEY ET AL 6. Zaidi AR, Zaidi A, Vaitkus PT. Outcome of heart transplantation in patients with sarcoid cardiomyopathy. J Heart Lung Transplant. 2007;26(7):714e717. 7. Blanche C, Valenza M, Aleksic I, Czer LS, Trento A. Technical considerations of a new technique for orthotopic heart transplantation. Total excision of recipient’s atria with bicaval and pulmonary venous anastomoses. J Cardiovasc Surg. 1994;35(4): 283e287. 8. Blanche C, Valenza M, Czer LS, et al. Orthotopic heart transplantation with bicaval and pulmonary venous anastomoses. Ann of Thorac Surgery. 1994;58(5):1505e1509. 9. Trento A, Czer LS, Blanche C. Surgical techniques for cardiac transplantation. Semin Thorac Cardiovasc Surg. 1996;8(2):126e132. 10. Trento A, Takkenberg JM, Czer LS, et al. Clinical experience with one hundred consecutive patients undergoing orthotopic heart transplantation with bicaval and pulmonary venous anastomoses. J Thorac Cardiovasc Surg. 1996;112(6):1496e1502. discussion 1502-1503. 11. Aleksic I, Freimark D, Blanche C, Czer LS, Trento A. Does total orthotopic heart transplantation offer improved hemodynamics during cellular rejection events? Transplantat Proc. 2003;35(4):1532e1535. 12. Aleksic I, Freimark D, Blanche C, Czer LS, Trento A. Hemodynamics during humoral rejection events with total versus standard orthotopic heart transplantation. Ann Thorac Cardiovasc Surg. 2004;10(5):285e289. 13. Daneshvar DA, Czer LS, Phan A, Trento A, Schwarz ER. Heart transplantation in the elderly: why cardiac transplantation does not need to be limited to younger patients but can be safely performed in patients above 65 years of age. Ann Transplant. 2010;15(4):110e119. 14. Goland S, Czer LS, Coleman B, et al. Induction therapy with thymoglobulin after heart transplantation: impact of therapy duration on lymphocyte depletion and recovery, rejection, and cytomegalovirus infection rates. J Heart Lung Transplant. 2008;27(10): 1115e1121. 15. Khan R, Tweedie EJ, Pflugfelder PW, White JA. Cardiac sarcoid in a heart transplant recipient: detection with cardiac magnetic resonance imaging. Transplantat Proc. 2010;42(5): 1976e1978. 16. Luk A, Lee A, Ahn E, Soor GS, Ross HJ, Butany J. Cardiac sarcoidosis: recurrent disease in a heart transplant patient following pulmonary tuberculosis infection. Can J Cardiol. 2010;26(7): e273ee275.