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ardiac Autotransplantation for Primaryardiac Tumorsichael J. Reardon, MD, S. Chris Malaisrie, MD, Jon-Cecil Walkes, MD,ra A. Vaporciyan, MD, David C. Rice, MD, W. Roy Smythe, MD,lement A. DeFelice, MD, and Zbigniew J. Wojciechowski, MDethodist DeBakey Heart Center, The Methodist Hospital; Division of Cardiothoracic Surgery, Michael E. DeBakey Department

f Surgery, Baylor College of Medicine; Department of Thoracic and Cardiovascular Surgery, M.D. Anderson Cancer Center,

ouston; and Department of Surgery, Scott & White Hospital, Texas A&M University, Temple, Texas

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Background. Complete tumor resection is the optimalreatment of cardiac tumors. Anatomic accessibilitynd proximity to vital structures complicates resectionf tumors involving the left heart. The results oftandard resection and resection with orthotopic heartransplantation are dismal. We, therefore, reviewedur series of patients with complex left-sided primaryardiac tumors who underwent tumor resection withardiac autotransplantation.

Methods. Since April 1998, 11 consecutive patients withomplex left atrial or left ventricular intracavitary cardiacumors underwent 12 resections using cardiac autotrans-lantation—cardiac explantation, ex vivo tumor resec-

ion with cardiac reconstruction, and cardiac reimplanta-ion. Demographics, tumor histology, operative data, and

ortality were analyzed. Follow-up was complete in allatients.Results. Complete resection by cardiac autotransplan-

ation was used in 7 patients with left atrial sarcoma, 1

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ddress correspondence to Dr Reardon, 6560 Fannin St, Suite 1002,ouston, TX 77030; e-mail: mreardon@tmh.tmc.edu.

2006 by The Society of Thoracic Surgeonsublished by Elsevier Inc

atient with left ventricular sarcoma, 2 patients with lefttrial paraganglioma, and 1 patient with a complex gianteft atrial myxoma. Eight patients had previous resectionf their cardiac tumor, and 1 patient had a repeat auto-ransplantation for recurrent disease. There were noperative deaths. Median overall survival was 18.5onths in patients with sarcomas. All patients with

enign tumors are alive without evidence of recurrence.Conclusions. Cardiac autotransplantation is a feasible

echnique for resection of complex left-sided cardiacumors. Recurrent disease after previous resections cane safely treated with this technique. Operative mortalitynd overall survival seems favorable in this series ofatients. Benefits of this technique include improvedccessibility and ability to perform a complete tumoresection with reliable cardiac reconstruction.

(Ann Thorac Surg 2006;82:645–50)

© 2006 by The Society of Thoracic Surgeons

rimary cardiac tumors are uncommon clinical entitieswith an incidence of 0.0017% to 0.03% [1, 2]. The

ajority of these tumors are benign atrial myxomas,hich can be successfully managed by surgical excision

3]. Malignant cardiac tumors, however, continue toresent a difficult therapeutic challenge, especially those

umors involving the left heart. Surgical resection is oftenecessary to alleviate the severe symptoms associatedith these tumors, but is, nevertheless, associated withoor long-term prognosis [4]. Because of the rarity ofrimary cardiac malignancies, therapeutic concepts andethods of surgical resection have not been

tandardized.To overcome the technical challenges of complete

esection of left-sided tumors with accurate cardiac re-onstruction, we have used a technique of cardiac ex-lantation, ex vivo tumor resection with cardiac recon-truction, and cardiac reimplantation— cardiacutotransplantation. Including our first successful caseublished in 1999 [5], we have performed this technique

ccepted for publication Feb 27, 2006.

n 11 consecutive patients with presumed left atrial orntracavitary left ventricular primary cardiac malignantumors. We sought to evaluate the feasibility of thispproach for primary resection and resection for recur-ent disease.

atients and Methods

atientsrom 1998 to the present, 11 patients with complex

eft-sided cardiac tumors underwent 12 operations usingardiac autotransplantation. Eight patients had malig-ant tumors and 3 had benign tumors (Table 1). All casesere performed by a single surgeon (M.J.R.) at either Theethodist DeBakey Heart Center (10 operations) or the.D. Anderson Cancer Center (2 operations). Demo-

raphics, tumor histology, operative data, and mortalityere analyzed. Follow-up was complete in all 11 patients.

ndividual informed consent was obtained to perform therocedure, and consent for research authorization wasbtained at the time of admission from each patient. Inddition, formal internal review board approval was

btained for this retrospective study.

0003-4975/06/$32.00doi:10.1016/j.athoracsur.2006.02.086

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urgeryhe technique of cardiac autotransplantation—cardiacxplantation, ex vivo tumor resection with cardiac recon-truction, and cardiac reimplantation—has been de-cribed previously [5]. Surgical approach was through aedian sternotomy for all cases. Cardiopulmonary by-

ass was established using most commonly bicaval ve-ous cannulation (Table 2). Mild systemic hypothermiaas used. Cold-blood hyperkalemic cardioplegic solu-

ion was given using antegrade delivery at a dose of 10L/kg, and a 200-mL dose of warm reperfusion car-

ioplegic solution was given just before removal of theortic cross-clamp. Cardiac explantation was performedy dividing, in sequence, the superior vena cava, inferiorena cava, the great vessels, and the left atrium. Thexplanted heart was placed in a container of iced salineolution for static hypothermia, and no further preserva-ion solution was administered. Tumor resection waserformed ex vivo, and the left atrium was reconstructedith bovine pericardium. Patients were routinely weaned

rom cardiopulmonary bypass on moderate inotropicupport with no intraaortic balloon pump or other car-iac assist devices.

djuvant Chemotherapyatients with cardiac sarcomas underwent adjuvant che-otherapy consisting of Adriamycin (75 mg/m2) and

fosfamide (106 mg/m2) in four to five divided doses. Allatients completed their planned dose except for the 2atients who expired of metastatic disease at 2 and 3onths.

tatistical Analysisurvival distributions were graphically displayed using

he Kaplan–Meier method. Overall survival was calcu-ated from the date of surgery to the date of death or theate of last follow-up. Data analysis was performed using

he Statistical Package for Social Sciences (SPSS version1.5.2.1, SPSS Inc, Chicago, IL).

esults

emographicsleven patients underwent cardiac autotransplantation

or resection of their left-sided cardiac tumor (Table 3)

able 1. Histologic Diagnosis of Left-Sided Cardiac Tumors

istologic Diagnosis n � 11

alignantMalignant fibrous histiocytoma 5Osteosarcoma 1Leiomyosarcoma 1Unspecified malignancy 1

enignParaganglioma 2Myxoma 1

5–7]. One patient underwent repeat cardiac autotrans-I

lantation for recurrent disease, for a total of 12 opera-ions. The average age at the time of operation was 40ears, and 63% were male (Table 4). The most prominentymptom at presentation was congestive heart failureanifested by fatigue and dyspnea (9 of 11 patients).

hree patients presented with rapid progression of theiryspnea on exertion to hypotension during a period ofeveral days. Other presenting symptoms included chestain, cough, and fever. One patient was asymptomaticnd was found to have a ventricular tumor on an annualchocardiogram performed for known mitral regurgita-ion. There were no episodes of embolic phenomenon,eart block, or other arrhythmias. The main diagnosticodality was echocardiography. Echocardiography was

sed in all patients, and cardiac catheterization withoronary arteriogram was performed to exclude the pres-nce of coronary artery involvement.Seven patients came with an established diagnosis of

arcoma from their previous tumor resection. One pa-ient had the presumptive diagnosis of radiation-ssociated sarcoma after therapy for a lymphoma. Thisatient was followed with serial echocardiograms foritral regurgitation and was found to have a cardiac

arcoma of the left ventricular outflow tract at the time ofurgery. No patient with benign cardiac tumors had aissue diagnosis before surgery. The very large left atrial

ass in 1 patient (Fig 1) was thought to be suspicious forarcoma, but at surgery proved to be a giant myxoma.ne patient had a large posterior left atrial mass byagnetic resonance imaging (Fig 2), and 1 patient had a

arge tumor blush on cardiac catheterization (Fig 3); bothumors were suspicious for malignancy but proved to bearagangliomas at the time of operation.

erioperative Dataor patients with primary cardiac malignancies, the

ength of intubation after surgery ranged from 2 hours to1 days, with the 2 patients requiring lung resectionsntubated for 7 and 11 days (Table 4). If these 2 patientsre excluded, the length of intubation ranged from 2 to 24ours (average, 16 hours). Similarly, if these 2 patientsre excluded, intensive care unit stay ranged from 24 to6 hours (average, 64 hours). For all patients, there wereo reexplorations for bleeding, and no episodes of newenal insufficiency or atrial fibrillation occurred. Theength of hospital stay for all patients ranged from 7 to 22ays (average, 14 days), with the patients requiring lungesections being discharged at 15 and 22 days. All pa-ients were discharged to home.

able 2. Cannulation Technique

enous Arterial n � 12

icaval Ascending aorta 8VC/femoral vein Ascending aorta 3

nnominate/femoral vein Femoral artery 1

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perative Mortality and Survivalhere was no in-hospital or 30-day mortality. Four pa-

ients are currently alive. Follow-up ranges 4 months to 5ears, with a median overall survival of 18.5 months (Fig). The patient requiring a repeat cardiac autotransplan-ation for recurrence 5 years after his initial cardiacutotransplantation survived an additional 11 months.ll patients with benign cardiac tumors are currently freef disease with good functional status.

omment

uch progress has been made since the first resectionf a left atrial myxoma using cardiopulmonary bypassy Craafoord in 1954 [8]. Major series report that

able 3. Patient Population Undergoing Cardiac Autotranspla

Casea Age Sex Site Histo

1b 20 M LA appendage MFH2 36 M LA posterior wall MFH3c 57 F LA septum and dome leiomyos4d 23 M LA dome MFH5 57 F LA dome MFH6 31 F LV PM papillary osteosar7 40 M LA left SPV undiffere

sarcom8 45 M LA septum myxoma9 26 M LA posterior wall paragang0 63 M LA dome paragang1 41 M LA right SPV MFH

2 46 F LA posterior wall MFH

Case 2 and 11 are the same patient who underwent repeat cardiac autoteported in [6]. d Previously reported in [7].

VC � inferior vena cava reconstruction; IVS � interventricular septuistiocytoma; MVR � mitral valve replacement; PM � posteromed

superior vena cava reconstruction.

able 4. Demographics and Perioperative Data of Patients W

ariable Benign (n � 3)

ge (range; y) 45 (22–63)exMale 3Female 0

revious resection 0dditional procedures 0ump time in minutes (range) 168 (131–228)lamp time in minutes (range) 120 (83–171)protinin 2ransfusions in units (range) 1.3 (0–2)ours of intubation (range) 12 (0.5–24)ays in intensive care (range) 3 (1–4)ays in hospital (range) 9 (7–13)

One patient underwent two autotransplantation procedures for recurrent sar

pproximately 75% of the primary cardiac tumors areenign and 25% malignant [9 –14]. Of the malignant

umors, 75% are sarcomas. The presentation of patientsith a primary cardiac tumor depends on tumor size,

ocation, and tissue type. Signs and symptoms can beevere, including hypotension and congestive heartailure from intracardiac obstruction, stroke and pe-ipheral arterial occlusion from systemic embolizationf tumor fragments, heart block from infiltration of thetrioventricular node, and various constitutionalymptoms. Experience with definitive chemoradiother-py is limited and often fails to relieve symptoms ormprove survival. In the series by Putnam and col-eagues [4], complete surgical resection provided bet-er relief of symptoms and improved overall survival

on

PreviousResection Other Procedures

Survival(months) Status

yes MVR 3 deadyes 67 dead

ma yes IVC 9 deadyes 18 deadyes MVR, RUL wedge 2 deadno MVR, IVS resection 21 alive

ed yes 20 alive

no 17 alivea no 15 alivea no 12 alive

yes SVC, rightpneumonectomy

11 dead

yes 12 alive

lantation for recurrence. b Previously reported in [5]. c Previously

LA � left atrium; LV � left ventricle; MFH � malignant fibrousRUL � right upper lobe; SPV � superior pulmonary vein; SVC

eft-Sided Cardiac Tumors

Malignant (n � 9) Total (n � 12)

39 (23–57) 40

5a 8a

4 48 85 5

200 (139–287) 192127 (95–164) 126

9 115 (2–8) 4

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han nonoperative therapy, and remains the standardherapy for cardiac tumors

Malignant tumors continue to present a therapeutichallenge as incomplete resections universally resultn rapid local tumor recurrence [15, 16]. In patientsith left heart tumors the challenge of complete sur-ical resection is magnified by the more posterior and

naccessible location as well as the association withther intracardiac structures. Surgical options for re-ection of left atrial tumors include radical resectionssing left atrial approaches through the interatrialroove or transseptally through the right atrium. Thesepproaches are adequate for typical benign tumors ofhe left atrium, but often do not provide the exposureecessary for complete removal and accurate cardiaceconstruction for malignant tumors. For left ventricu-ar tumors, surgical resection can be accomplishedhrough a transaortic valve approach, a ventriculot-my, or a transmitral valve approach. In patients with

ig 1. Large left atrial tumor on echocardiogram thought suspiciousor sarcoma.

ig 2. Magnetic resonance image of large posterior left atrial mass. F

ery large tumors, exposure through the mitral valveay not be adequate with the heart in situ. The need

or papillary muscle resection, interventricular septalesection, and mitral valve replacement further ham-ers resection through these approaches.Orthotopic heart transplantation [17] and combined

eart-lung transplantation [18] have been previouslyescribed in small series of patients. The limited ex-erience of these techniques emphasizes the impor-

ance of complete tumor resection for malignancieshat would otherwise be considered unresectable. Ben-fits of this radical resection are control of local recur-ence and prevention of systemic metastasis. The lim-ted donor availability and long waiting period,owever, often precludes this approach in patients

ig 3. Coronary arteriogram showing large tumor blush off the cir-umflex coronary artery.

ig 4. Overall survival of patients after cardiac autotransplantation.

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resenting with heart failure in need of prompt treat-ent. In addition, the effects of posttransplant immu-

osuppression on residual malignant cells remainnknown.Cardiac autotransplantation is a well-described tech-

ique with a novel application for the resection ofalignant cardiac tumors. Historically, animal re-

earch with cardiac autotransplantation was an inte-ral part of the development of cardiac transplanta-ion, showing that the heart could survive afterisconnection from the nervous and lymphatic systems

19 –21]. First performed clinically in humans to treatrinzmetal’s angina [22, 23], this technique was soonbandoned because of the high mortality and persis-ent coronary ischemia. Cardiac autotransplantationor nontumor indications has also been reported in thereatment of atrial fibrillation combined with mitralalve disease [24], long QT syndrome [25], and theepair of a giant left atrium [26]. The first attemptedbut unsuccessful) cardiac autotransplantation re-orted in the English literature for the resection of aardiac tumor was by Cooley and associates in 198527]. The first successful case of cardiac autotransplan-ation for the resection of a large benign myxoma waseported by Scheld and coworkers in 1987 [28], and haseen reported by other authors in subsequent caseeports [29, 30]. In an earlier report in 1999 [5], weescribed the first successful case of cardiac autotrans-lantation for the treatment of a primary cardiac ma-

ignant tumor.No operative mortality has occurred in this current

eries of cardiac autotransplantation. The poor survivalssociated with these tumors continues to be second-ry to systemic recurrence, despite improved localontrol. Review of the literature concerning standardesection for primary cardiac sarcomas reveals a me-ian survival of 11 months [4]. Survival after orthotopiceart transplant appears slightly improved, with aeported mean survival of 12 months [31]. The medianurvival of 18.5 months from the time of operation inur series of cardiac autotransplantation comparesavorably with these reports, especially consideringhat the majority (7 of 8 patients) were treated forecurrent tumors. Because some tumors can only beompletely resected by cardiac explantation, cardiacutotransplantation may be an alternative strategy torthotopic heart transplantation in patients with oth-rwise unresectable tumors.In conclusion, cardiac autotransplantation is a feasible

echnique for resection of complex left-sided cardiacumors. Recurrent disease after previous resections cane safely treated with this technique. Operative mortalitynd overall survival seems favorable in this series ofatients. Benefits of this technique include improvedccessibility and the ability to perform a complete tumoresection with reliable cardiac reconstruction. Survivalfter cardiac autotransplantation compares favorablyith survival reported after standard resection and or-

hotopic heart transplantation.

eferences

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4. Troise G, Brunelli F, Cirillo M, et al. Cardiac autotransplan-tation for the treatment of permanent atrial fibrillationcombined with mitral valve disease. Heart Surg Forum2003;6:138–42.

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8. Scheld HH, Nestle HW, Kling D, Stertmann WA, Lange-bartels H, Hehrlein FW. Resection of a heart tumor usingautotransplantation. Thorac Cardiovasc Surg 1988;36:40 –3.

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Inst J 1985;12:171–6. Cardiol 2000;15:121–5.

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