Ann Thorac Surg 2006;82:645-650
© 2006 The Society of Thoracic Surgeons
Original article: Cardiovascular
Cardiac Autotransplantation for Primary Cardiac Tumors
Michael J. Reardon, MDa,c,*,
S. Chris Malaisrie, MDb,
Jon-Cecil Walkes, MDa,
Ara A. Vaporciyan, MDc,
David C. Rice, MDc,
W. Roy Smythe, MDd,
Clement A. DeFelice, MDa,
Zbigniew J. Wojciechowski, MDa
a Methodist DeBakey Heart Center, The Methodist Hospital, Houston
b Division of Cardiothoracic Surgery, Michael E. DeBakey Department of Surgery, Baylor College of Medicine, Houston
c Department of Thoracic and Cardiovascular Surgery, M.D. Anderson Cancer Center, Houston
d Department of Surgery, Scott & White Hospital, Texas A&M University, Temple, Texas
Accepted for publication February 27, 2006.
* Address correspondence to Dr Reardon, 6560 Fannin St, Suite 1002, Houston, TX 77030. (Email: mreardon{at}tmh.tmc.edu).
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Abstract
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BACKGROUND: Complete tumor resection is the optimal treatment of cardiac tumors. Anatomic accessibility and proximity to vital structures complicates resection of tumors involving the left heart. The results of standard resection and resection with orthotopic heart transplantation are dismal. We, therefore, reviewed our series of patients with complex left-sided primary cardiac tumors who underwent tumor resection with cardiac autotransplantation.
METHODS: Since April 1998, 11 consecutive patients with complex left atrial or left ventricular intracavitary cardiac tumors underwent 12 resections using cardiac autotransplantation—cardiac explantation, ex vivo tumor resection with cardiac reconstruction, and cardiac reimplantation. Demographics, tumor histology, operative data, and mortality were analyzed. Follow-up was complete in all patients.
RESULTS: Complete resection by cardiac autotransplantation was used in 7 patients with left atrial sarcoma, 1 patient with left ventricular sarcoma, 2 patients with left atrial paraganglioma, and 1 patient with a complex giant left atrial myxoma. Eight patients had previous resection of their cardiac tumor, and 1 patient had a repeat autotransplantation for recurrent disease. There were no operative deaths. Median overall survival was 18.5 months in patients with sarcomas. All patients with benign tumors are alive without evidence of recurrence.
CONCLUSIONS: Cardiac autotransplantation is a feasible technique for resection of complex left-sided cardiac tumors. Recurrent disease after previous resections can be safely treated with this technique. Operative mortality and overall survival seems favorable in this series of patients. Benefits of this technique include improved accessibility and ability to perform a complete tumor resection with reliable cardiac reconstruction.
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Introduction
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Primary cardiac tumors are uncommon clinical entities with an incidence of 0.0017% to 0.03% [1, 2]. The majority of these tumors are benign atrial myxomas, which can be successfully managed by surgical excision [3]. Malignant cardiac tumors, however, continue to present a difficult therapeutic challenge, especially those tumors involving the left heart. Surgical resection is often necessary to alleviate the severe symptoms associated with these tumors, but is, nevertheless, associated with poor long-term prognosis [4]. Because of the rarity of primary cardiac malignancies, therapeutic concepts and methods of surgical resection have not been standardized.
To overcome the technical challenges of complete resection of left-sided tumors with accurate cardiac reconstruction, we have used a technique of cardiac explantation, ex vivo tumor resection with cardiac reconstruction, and cardiac reimplantation—cardiac autotransplantation. Including our first successful case published in 1999 [5], we have performed this technique on 11 consecutive patients with presumed left atrial or intracavitary left ventricular primary cardiac malignant tumors. We sought to evaluate the feasibility of this approach for primary resection and resection for recurrent disease.
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Patients and Methods
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Patients
From 1998 to the present, 11 patients with complex left-sided cardiac tumors underwent 12 operations using cardiac autotransplantation. Eight patients had malignant tumors and 3 had benign tumors (Table 1). All cases were performed by a single surgeon (M.J.R.) at either The Methodist DeBakey Heart Center (10 operations) or the M.D. Anderson Cancer Center (2 operations). Demographics, tumor histology, operative data, and mortality were analyzed. Follow-up was complete in all 11 patients. Individual informed consent was obtained to perform the procedure, and consent for research authorization was obtained at the time of admission from each patient. In addition, formal internal review board approval was obtained for this retrospective study.
Surgery
The technique of cardiac autotransplantation—cardiac explantation, ex vivo tumor resection with cardiac reconstruction, and cardiac reimplantation—has been described previously [5]. Surgical approach was through a median sternotomy for all cases. Cardiopulmonary bypass was established using most commonly bicaval venous cannulation (Table 2). Mild systemic hypothermia was used. Cold-blood hyperkalemic cardioplegic solution was given using antegrade delivery at a dose of 10 mL/kg, and a 200-mL dose of warm reperfusion cardioplegic solution was given just before removal of the aortic cross-clamp. Cardiac explantation was performed by dividing, in sequence, the superior vena cava, inferior vena cava, the great vessels, and the left atrium. The explanted heart was placed in a container of iced saline solution for static hypothermia, and no further preservation solution was administered. Tumor resection was performed ex vivo, and the left atrium was reconstructed with bovine pericardium. Patients were routinely weaned from cardiopulmonary bypass on moderate inotropic support with no intraaortic balloon pump or other cardiac assist devices.
Adjuvant Chemotherapy
Patients with cardiac sarcomas underwent adjuvant chemotherapy consisting of Adriamycin (75 mg/m2) and ifosfamide (106 mg/m2) in four to five divided doses. All patients completed their planned dose except for the 2 patients who expired of metastatic disease at 2 and 3 months.
Statistical Analysis
Survival distributions were graphically displayed using the Kaplan–Meier method. Overall survival was calculated from the date of surgery to the date of death or the date of last follow-up. Data analysis was performed using the Statistical Package for Social Sciences (SPSS version 11.5.2.1, SPSS Inc, Chicago, IL).
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Results
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Demographics
Eleven patients underwent cardiac autotransplantation for resection of their left-sided cardiac tumor (Table 3) [5–7]. One patient underwent repeat cardiac autotransplantation for recurrent disease, for a total of 12 operations. The average age at the time of operation was 40 years, and 63% were male (Table 4). The most prominent symptom at presentation was congestive heart failure manifested by fatigue and dyspnea (9 of 11 patients). Three patients presented with rapid progression of their dyspnea on exertion to hypotension during a period of several days. Other presenting symptoms included chest pain, cough, and fever. One patient was asymptomatic and was found to have a ventricular tumor on an annual echocardiogram performed for known mitral regurgitation. There were no episodes of embolic phenomenon, heart block, or other arrhythmias. The main diagnostic modality was echocardiography. Echocardiography was used in all patients, and cardiac catheterization with coronary arteriogram was performed to exclude the presence of coronary artery involvement.
Seven patients came with an established diagnosis of sarcoma from their previous tumor resection. One patient had the presumptive diagnosis of radiation-associated sarcoma after therapy for a lymphoma. This patient was followed with serial echocardiograms for mitral regurgitation and was found to have a cardiac sarcoma of the left ventricular outflow tract at the time of surgery. No patient with benign cardiac tumors had a tissue diagnosis before surgery. The very large left atrial mass in 1 patient (Fig 1) was thought to be suspicious for sarcoma, but at surgery proved to be a giant myxoma. One patient had a large posterior left atrial mass by magnetic resonance imaging (Fig 2), and 1 patient had a large tumor blush on cardiac catheterization (Fig 3); both tumors were suspicious for malignancy but proved to be paragangliomas at the time of operation.
Perioperative Data
For patients with primary cardiac malignancies, the length of intubation after surgery ranged from 2 hours to 11 days, with the 2 patients requiring lung resections intubated for 7 and 11 days (Table 4). If these 2 patients are excluded, the length of intubation ranged from 2 to 24 hours (average, 16 hours). Similarly, if these 2 patients are excluded, intensive care unit stay ranged from 24 to 96 hours (average, 64 hours). For all patients, there were no reexplorations for bleeding, and no episodes of new renal insufficiency or atrial fibrillation occurred. The length of hospital stay for all patients ranged from 7 to 22 days (average, 14 days), with the patients requiring lung resections being discharged at 15 and 22 days. All patients were discharged to home.
Operative Mortality and Survival
There was no in-hospital or 30-day mortality. Four patients are currently alive. Follow-up ranges 4 months to 5 years, with a median overall survival of 18.5 months (Fig 4). The patient requiring a repeat cardiac autotransplantation for recurrence 5 years after his initial cardiac autotransplantation survived an additional 11 months. All patients with benign cardiac tumors are currently free of disease with good functional status.
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Comment
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Much progress has been made since the first resection of a left atrial myxoma using cardiopulmonary bypass by Craafoord in 1954 [8]. Major series report that approximately 75% of the primary cardiac tumors are benign and 25% malignant [9–14]. Of the malignant tumors, 75% are sarcomas. The presentation of patients with a primary cardiac tumor depends on tumor size, location, and tissue type. Signs and symptoms can be severe, including hypotension and congestive heart failure from intracardiac obstruction, stroke and peripheral arterial occlusion from systemic embolization of tumor fragments, heart block from infiltration of the atrioventricular node, and various constitutional symptoms. Experience with definitive chemoradiotherapy is limited and often fails to relieve symptoms or improve survival. In the series by Putnam and colleagues [4], complete surgical resection provided better relief of symptoms and improved overall survival than nonoperative therapy, and remains the standard therapy for cardiac tumors
Malignant tumors continue to present a therapeutic challenge as incomplete resections universally result in rapid local tumor recurrence [15, 16]. In patients with left heart tumors the challenge of complete surgical resection is magnified by the more posterior and inaccessible location as well as the association with other intracardiac structures. Surgical options for resection of left atrial tumors include radical resections using left atrial approaches through the interatrial groove or transseptally through the right atrium. These approaches are adequate for typical benign tumors of the left atrium, but often do not provide the exposure necessary for complete removal and accurate cardiac reconstruction for malignant tumors. For left ventricular tumors, surgical resection can be accomplished through a transaortic valve approach, a ventriculotomy, or a transmitral valve approach. In patients with very large tumors, exposure through the mitral valve may not be adequate with the heart in situ. The need for papillary muscle resection, interventricular septal resection, and mitral valve replacement further hampers resection through these approaches.
Orthotopic heart transplantation [17] and combined heart-lung transplantation [18] have been previously described in small series of patients. The limited experience of these techniques emphasizes the importance of complete tumor resection for malignancies that would otherwise be considered unresectable. Benefits of this radical resection are control of local recurrence and prevention of systemic metastasis. The limited donor availability and long waiting period, however, often precludes this approach in patients presenting with heart failure in need of prompt treatment. In addition, the effects of posttransplant immunosuppression on residual malignant cells remain unknown.
Cardiac autotransplantation is a well-described technique with a novel application for the resection of malignant cardiac tumors. Historically, animal research with cardiac autotransplantation was an integral part of the development of cardiac transplantation, showing that the heart could survive after disconnection from the nervous and lymphatic systems [19–21]. First performed clinically in humans to treat Prinzmetal's angina [22, 23], this technique was soon abandoned because of the high mortality and persistent coronary ischemia. Cardiac autotransplantation for nontumor indications has also been reported in the treatment of atrial fibrillation combined with mitral valve disease [24], long QT syndrome [25], and the repair of a giant left atrium [26]. The first attempted (but unsuccessful) cardiac autotransplantation reported in the English literature for the resection of a cardiac tumor was by Cooley and associates in 1985 [27]. The first successful case of cardiac autotransplantation for the resection of a large benign myxoma was reported by Scheld and coworkers in 1987 [28], and has been reported by other authors in subsequent case reports [29, 30]. In an earlier report in 1999 [5], we described the first successful case of cardiac autotransplantation for the treatment of a primary cardiac malignant tumor.
No operative mortality has occurred in this current series of cardiac autotransplantation. The poor survival associated with these tumors continues to be secondary to systemic recurrence, despite improved local control. Review of the literature concerning standard resection for primary cardiac sarcomas reveals a median survival of 11 months [4]. Survival after orthotopic heart transplant appears slightly improved, with a reported mean survival of 12 months [31]. The median survival of 18.5 months from the time of operation in our series of cardiac autotransplantation compares favorably with these reports, especially considering that the majority (7 of 8 patients) were treated for recurrent tumors. Because some tumors can only be completely resected by cardiac explantation, cardiac autotransplantation may be an alternative strategy to orthotopic heart transplantation in patients with otherwise unresectable tumors.
In conclusion, cardiac autotransplantation is a feasible technique for resection of complex left-sided cardiac tumors. Recurrent disease after previous resections can be safely treated with this technique. Operative mortality and overall survival seems favorable in this series of patients. Benefits of this technique include improved accessibility and the ability to perform a complete tumor resection with reliable cardiac reconstruction. Survival after cardiac autotransplantation compares favorably with survival reported after standard resection and orthotopic heart transplantation.
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Abstract
Introduction
