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Ann Thorac Surg 2004;78:1024-1030
© 2004 The Society of Thoracic Surgeons

Original article: general thoracic

Surgical management of thoracic malignancies invading the heart or great vessels

Bernard J. Park, MDa,*, Matthew Bacchetta, MDb, Manjit S. Bains, MDa, Robert J. Downey, MDa, Raja Flores, MDa, Valerie W. Rusch, MDa, Leonard N. Girardi, MDb

a Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York, USA
b Department of Cardiothoracic Surgery, Weill Medical College of Cornell University, New York, New York, USA

Accepted for publication February 10, 2004.

* Address reprint requests to Dr Park, Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, Room C-867, New York, NY 10021, USA
parkb{at}mskcc.org


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Surgical resection of thoracic malignancies involving either the heart or great vessels is uncommonly performed because of the potential morbidity and mortality for an unknown probability of significant palliation or cure. We reviewed our experience of 10 patients treated surgically, either primarily or as a component of multimodality therapy, to assess feasibility and results.

METHODS: A retrospective review of the results in 10 patients who underwent resection of thoracic malignancies that included either great vessel or the heart was conducted.

RESULTS: Histologic diagnoses included soft tissue sarcoma (n = 7), squamous cell carcinoma (n = 1), malignant thymoma (n = 1), and mediastinal teratoma (n = 1). Three patients underwent induction chemotherapy. Cardiopulmonary bypass was used in 7 patients. Structures resected included superior vena cava (n = 5), left atrium (n = 4), right atrium (n = 2), descending aorta (n = 1), and main pulmonary artery (n = 1). Concomitant anatomic pulmonary resections were performed in 3 patients. Seven patients had an R0 or R1 resection. There were no perioperative deaths. All symptomatic patients had immediate and sustained palliation of their presenting symptoms. The median length of stay was 6 days (range, 4 to 43 days). Six patients underwent postoperative systemic therapy. The overall median survival was 21.7 months (range, 3.2 to 69 months) and was 33.3 months (range, 3.7 to 69 months) for patients who had an R0 or R1 resection.

CONCLUSIONS: Resection of the heart and great vessels involved by thoracic malignancies can be performed with acceptable morbidity and mortality and results in significant palliation and, in some cases, prolonged survival.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Despite the major morbidity caused by thoracic tumors involving either the heart or the great vessels, most patients are not offered surgical resection either because of technical considerations, the potential morbidity and mortality, or concerns over a negligible impact on survival. Although a modest degree of short-term palliation may be achieved with radiation or chemotherapy, depending on the tumor histology and sensitivity to those modalities, the prognosis is typically poor. Moreover, a subgroup of such patients present with immediately life-threatening problems such as congestive heart failure, systemic embolization, or impending cardiovascular collapse. Medical palliation is generally ineffective in this setting, and an aggressive surgical approach or comfort care may be the only options.

Prior series have suggested that en bloc tumor resection and reconstruction of the superior vena cava (SVC), vertebral bodies, and pulmonary arteries invaded by bronchogenic carcinoma is technically feasible, and, in some cases, associated with survival benefit [1–3]. Few of these patients, however, were reported as facing cardiovascular collapse or other life-threatening conditions, and none required vascular or cardiac reconstruction using cardiopulmonary bypass (CPB). There have been isolated case reports of resection of locally advanced thoracic cancers using CPB that suggest there is a role for extended resection in a select group of patients [4–7].

A collaborative approach between the Thoracic Service at Memorial Sloan-Kettering Cancer Center and the Department of Cardiothoracic Surgery at the Weill Medical College of Cornell University has led to an aggressive approach in a number of these patients. We examined the outcome of 10 such patients who underwent surgical resection of thoracic malignancies invading the heart, great vessels, or both. Our results suggest that in carefully selected patients, surgical resection can be performed with acceptable surgical morbidity and mortality and an immediate improvement in hemodynamic status in patients presenting with ongoing or impending cardiovascular compromise. Some of these patients will be rendered disease-free with a resulting long-term survival benefit.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
We reviewed the records of patients whose initial thoracic surgical evaluation was at Memorial Sloan-Kettering Cancer Center between January 1, 1998, and July 1, 2001, for a known or suspected intrathoracic malignancy with evidence of invasion of a great vessel or the heart and who subsequently underwent surgical resection. Patients with bronchogenic carcinoma were excluded. All patients underwent multidisciplinary consultations with medical and surgical oncology to determine the appropriate treatment strategy. All patients had preoperative computed tomography scans with intravenous contrast that suggested great vessel or cardiac invasion (Fig 1A). Patients who had evidence of cardiac chamber invasion underwent preoperative or intraoperative transesophageal echocardiography to delineate more precisely the extent of local disease (Fig 1B). When the need for CPB for resection was determined, an inpatient transfer was arranged to The New York Presbyterian Hospital-Weill Cornell Center, where a collaborative effort and capability for CPB exists. All patients older than 40 years of age in whom the operative approach included CPB underwent left heart catheterization before surgery.



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  		Fig 1. (A) Computed tomography of the chest in a patient with a left upper lobe sarcoma with extension into the left atrium. (B) Intraoperative transesophageal echocardiogram demonstrating left atrial mass with intermittent excursion through the mitral valve.

 
The extent of resection was defined on the basis of the R classification (residual tumor) published in 1987 by the Union Internationale Contre Cancer and in 1992 by the American Joint Committee on Cancer [8–10]. R0 denotes no residual tumor; R1 indicates presence of microscopic residual tumor; and R2 signifies macroscopic residual tumor, either local-regional or distant. Decisions to offer adjuvant therapy were made on an individual basis in collaboration with the referring medical oncologists. Hospital charts and office notes were reviewed to document data on hospital stay, complications, and postoperative follow-up. When necessary, telephone contact was made to verify patient status. Median follow-up was 21.7 months and was 100% complete.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Between January 1, 1998, and July 1, 2001, 10 patients underwent surgical resection of a thoracic malignancy that invaded a great vessel, a cardiac chamber, or both. There were 5 men and 5 women with a median age 46 years (range, 22 to 65 years). Eight patients had histologic documentation of malignancy before surgery, and 4 had undergone previous explorations for diagnosis and attempts at resection (Table 1). The majority of the patients had soft tissue sarcomas (n = 7). Seven patients were symptomatic. Three had mild symptoms including chest pain, weight loss, or a nonproductive cough, whereas 4 patients had major clinical syndromes including massive hemoptysis (n = 1), SVC syndrome (n = 1), bilateral pulmonary embolism (n = 1), and distal arterial embolization (renal, cerebral; n = 1). In these patients, invasion of the heart or great vessels was evident on preoperative evaluation and imaging. All symptomatic patients underwent a single operative procedure. In the 3 asymptomatic patients, great vessel or cardiovascular invasion was discovered during an initial attempt at resection, and a second operation was performed to complete their resection with the aid of CPB. There was no evidence that any of these 3 patients suffered complications as a result of undergoing a second procedure.


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  		Table 1. Patient Characteristics

 
Details of the operative procedures performed are listed in Table 2. The majority (8 of 10) of patients underwent exploration and resection through a median sternotomy. One patient required a right hemiclamshell thoracotomy. Seven patients had great vessel involvement with tumor: 5 SVC, 1 main pulmonary artery, and 1 descending thoracic aorta. Six patients had cardiac chamber invasion: 4 left atrium (LA) and 2 right atrium. Three patients had involvement of both a great vessel and the heart: 2 with SVC and right atrium and 1 with SVC and LA. Five patients required simultaneous pulmonary resection. Three underwent anatomic resection: 2 right pneumonectomies and 1 left lower lobectomy. The remaining 2 patients underwent pulmonary wedge resections.


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  		Table 2. Operative and Hospital Stay Information

 
Cardiopulmonary bypass was required in 7 patients; 6 had cardiac chamber invasion, and 1 had involvement of the main pulmonary artery. Complete pulmonary resection or complete mobilization of the primary tumor was performed before systemic heparinization (400 U/kg) and institution of CPB. All patients were placed on CPB with bicaval venous cannulation and arterial return into the ascending aorta. Moderate systemic hypothermia (32°C) was used, except for 1 patient in whom profound hypothermic circulatory arrest (18°C) was required for complete resection of an extensive SVC and right atrial tumor. Cold-blood potassium cardioplegia was used for myocardial protection during the period of cardiac arrest, intracardiac resection, and reconstruction. One patient was identified on left heart catheterization to have hemodynamically significant two-vessel coronary artery disease, and coronary artery bypass grafting was performed with autologous reverse saphenous vein grafts. Pulmonary artery and LA reconstructions were performed with polyethylene terephthalate fiber (Dacron) patch prostheses. The median CPB time was 103 minutes (range, 65 to 145 minutes), and the median aortic cross-clamp time was 39 minutes (range, 0 to 119 minutes). One patient with SVC, innominate vein, and right atrium invasion required a short period of profound hypothermic circulatory arrest with retrograde cerebral perfusion to achieve a complete resection of tumor extending into the jugular veins.

Every patient who had SVC invasion required graft reconstruction except 1 patient who had a partial resection with primary repair. Patients with isolated SVC or innominate vein involvement (n = 2) underwent resection and reconstruction without CPB. Superior vena cava reconstructions were carried out with a clamp and sew technique. The SVC was reconstructed with a 14-mm ringed Gore-Tex graft (WL Gore, Inc, Scottsdale, AZ), and the innominate vein, with an 8-mm ringed Gore-Tex graft. The distal anastomosis between the graft and the right atrial appendage was performed first to minimize caval occlusion time. The atriocaval junction was then divided and oversewn to minimize the risk of embolization to the pulmonary circulation. Lastly, the graft to innominate or SVC was performed. Both patients had near occlusion of the SVC and tolerated the period of cross-clamping without hemodynamic compromise or evidence of cerebral edema. Three patients underwent SVC resection on CPB, and each required ringed Gore-Tex graft reconstruction.

One patient with descending aorta invasion was resected without the need for extracorporeal circulation. Aortic resection was performed using a clamp and sew technique after administration of low-dose heparin (100 U/kg). Spinal cord protection was achieved through moderate hypothermia (33°C) and spinal drainage, as previously described [11, 12]. The aorta was reconstructed with a woven Dacron tube graft (Meadox, Oakland, NJ). Aortic cross-clamp time was 18 minutes.

There were no perioperative deaths. The median requirement for packed red blood cell transfusion was 6 U (range, 3 to 12 U). Five patients were discharged from the hospital without a perioperative complication. Five patients experienced a complication requiring intervention. One patient was discharged on postoperative day eight and readmitted 5 days later with empyema. This was treated successfully with tube thoracostomy and intravenous antibiotics. Another patient who underwent left upper lobe wedge resection, LA resection, and left lower lobe lobectomy on CPB required reexploration for postoperative bleeding and coagulopathy. The postoperative course was otherwise uneventful, and the patient was discharged on the sixth postoperative day. Three patients had minor complications including postoperative atrial fibrillation, a minor transfusion reaction, and a fever of unknown origin. Postoperative neutropenia was seen in 1 patient after instillation of intrapleural mitoxantrone. This prolonged the patient's hospitalization, but did not otherwise affect the outcome. The median length of stay in the intensive care unit was 2.0 days (range, 1 to 5 days), and the median hospital stay was 6 days (range, 4 to 43 days).

The final postoperative and pathologic diagnoses are listed in Table 3. There were three cases of primary pulmonary sarcomas, one chondrosarcoma, one synovial cell sarcoma, one metastatic uterine leiomyosarcoma, one retroperitoneal leiomyosarcoma, one metastatic squamous cell carcinoma from the scalp, one malignant thymoma, and one teratoma with malignant transformation. Complete, macroscopic resection of tumor was achieved in 7 patients. One patient with a malignant thymoma had an R0 resection. Six patients had an R1 resection. Two had foci of tumor extending to the soft tissue margin, whereas the remainder had microscopic evidence of tumor at the vascular or cardiac margin (1 SVC, 2 pulmonary artery, 1 LA). Three patients with known or suspected metastatic disease underwent palliative, R2 resections. Two patients had extensive LA disease with impending cardiovascular compromise, and a third patient had bulky chest wall sarcoma invading through the SVC into the right atrium with ongoing pulmonary emboli.


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  		Table 3. Postoperative Follow-Up

 
Six patients had postoperative therapy with 3 patients undergoing adjuvant therapy consisting of either external beam radiotherapy (n = 2) or chemotherapy (n = 1). Four patients who had R1 resections received no further therapy. One patient with a metastatic sarcomatoid squamous cell carcinoma had brain metastases before adjuvant treatment began. The decision to forego additional treatment in the remaining 3 patients was made by their individual oncologists. The median survival for the entire group was 21.7 months (range, 3.2 to 69 months). Patients having either an R0 or R1 resection had a median survival of 33.3 months (range, 3.7 to 69 months). Four patients in this group died of recurrent disease (2 distant, 2 local) at a median of 18.9 months (range, 3.7 to 28.9 months) after resection. Three of the 4 had adjuvant treatment. Three patients are currently alive and have no evidence of disease after curative intent resection. None of these patients received adjuvant therapy. All 3 patients who had an R2 resection, despite receiving additional systemic therapy, were dead of disease at 3.2, 5.2, and 14.5 months postoperatively.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
Thoracic malignancies invading the heart or great vessels are rarely considered for surgical extirpation. When patients have evidence of extrathoracic disease, it is difficult to justify complex operations with the potential for prolonged convalescence and substantial morbidity and mortality, as long-term survival is limited. Patients who have locally advanced disease in the absence of distant metastasis provide an even greater therapeutic challenge. These patients are typically treated with systemic chemotherapy and radiation therapy in the hopes of achieving both a therapeutic and palliative benefit while avoiding the potential complications of surgery. For those with life-threatening events secondary to tumor invasion of major cardiovascular structures, these nonsurgical options are frequently ineffective. The published experience of extensive surgical intervention in patients with locally invasive thoracic malignancies is limited to a small number of case reports and series in the literature [4–7, 13–18]. The reported experience contains patients who had favorable natural histories and were highly selected for curative intent surgery. The results of these cases suggest that extensive surgical resection is technically feasible, but the appropriate indications for such a heroic effort are often not well delineated.

In our series, patients were selected for aggressive surgical resection after multidisciplinary evaluation by medical and surgical oncologists at our institution. All patients were required to have adequate cardiopulmonary reserve to undergo a major thoracic procedure with the probability of requiring CPB and the possibility of having a concomitant pulmonary resection. One group of patients was considered that had received systemic therapy for their primary neoplasm to best response without evidence of extrathoracic disease. Three of our patients (thymoma, gastrointestinal stromal tumor, nonseminomatous germ cell tumor) underwent multiple cycles of systemic chemotherapy that served as primary therapy and induction therapy before complete resection of their thoracic disease.

A large number of patients with tumor histologic processes for which few effective systemic or nonsurgical local modalities exist were offered surgical resection as primary therapy with the possibility for adjuvant treatment. This explains why a significant proportion of patients in the series had either a primary pulmonary or metastatic sarcoma (8 of 10). Historically, in this population of patients the most effective therapy has been surgical resection [19–21]. Although some authors have advocated the use of neoadjuvant therapy to enhance the chances of complete resection [22], overall there are few data supporting the routine use of induction therapy. Rather, as previously reported by Burt and Zakowski [23] and Regnard and colleagues [24], complete surgical resection appears to be the most important predictor of survival. On the basis of this, there have been a few case reports of extensive resection of pulmonary sarcomas using CPB [25–27].

Lastly, patients with ongoing or impending hemodynamic consequences of their malignancy were offered resection. Three patients had symptoms and signs of ongoing compromise (systemic embolization, pulmonary embolization, SVC syndrome) for which urgent resection was necessary for palliative reasons. Two patients had symptoms suggesting impending cardiovascular collapse secondary to tumor occupying a large portion of the LA. Although the overall rate of cardiac dysfunction from cardiac metastases is low (10%) [28], there have been a number of case reports of major cardiovascular sequelae of either primary or metastatic tumors involving the LA [29, 30]. The decision to offer resection was based on the presence of symptoms that precluded administration of systemic therapy and raised the possibility of cardiovascular compromise.

Great vessel reconstruction was performed in the majority of patients with prosthetic material because of extensive vessel wall invasion. Superior vena cava and innominate vein reconstructions were performed with ringed polytetrafluoroethylene grafts using the technique described by Dartevelle and colleagues [31]. No graft occlusions were noted on follow-up, and 1 patient required percutaneous balloon dilatation of an anastomotic stricture. These data are consistent with the SVC 5-year graft patency rate of 86% reported by Dartevelle and associates [1]. Cardiopulmonary bypass was used for extensive tumor invasion of the heart, alone or in conjunction with a great vessel (SVC and the main pulmonary artery). As with any patient undergoing CPB, it is important to identify significant concomitant coronary or valvular disease before surgery. In fact, one of our patients had significant two-vessel coronary disease and had successful coronary artery bypass grafting with saphenous vein grafts.

Simultaneous pulmonary resections were performed in a total of 5 patients, and 4 of these were completed while patients were on CPB. The majority of these resections were anatomic, including two pneumonectomies and one lobectomy. Only 1 patient required reexploration for postoperative hemorrhage after LA resection, left lower lobe lobectomy, and left upper lobe wedge resection. Our results with concomitant pulmonary resection compare favorably with those reported previously [32–36]. In addition, we did not find that lung resection during CPB was associated with excessive rates of bleeding or pulmonary complications as suggested by Ulicny and colleagues [36].

Our results suggest that aggressive surgical management of locally invasive thoracic malignancies is feasible and safe. The perioperative mortality was 0%, and the rate of major morbidity was only 20%. Patients can expect immediate resolution of their symptoms, and the risk of life-threatening embolization or cardiovascular collapse is eliminated. Prolonged hospitalization was uncommon. One patient had an extended hospital stay to receive intrapleural chemotherapy, unrelated to the surgical procedure. Readmission for a surgical complication was also uncommon. Only 1 patient required readmission for postoperative empyema, which was treated successfully during a short hospitalization. These results compare favorably with those reported for patients treated for primary cardiac tumors [37], as well as those undergoing concomitant cardiac and pulmonary operations [32–36].

The intermediate term results of en bloc resection of intrathoracic tumors are also encouraging. The 3 patients with extrathoracic disease who underwent palliative, R2 resections all recovered with immediate relief of symptoms and were able to receive chemotherapy subsequently. Although all ultimately died of their disease, 1 patient remained alive with disease for greater than 14 months. All had lasting palliation of their initial symptoms, and none developed recurrent tumor in the surgical resection bed. These were highly selected patients who were able to tolerate CPB and extensive resection. There are no published data that support this approach, and we would not recommend this as standard therapy for every patient. This option, however, should be at least considered in patients who have no other alternatives

In the patients resected with curative intent, complete resection of all macroscopic tumor (R0 or R1) was achieved. Three patients are currently alive and disease-free. Four patients have died since their procedure, all of their original malignancy. Two patients with left-sided cardiovascular involvement experienced cerebral metastases, and a third patient with right-sided vascular invasion had recurrent lung and pleural metastases. The fourth patient died of local recurrence at the main pulmonary artery despite adjuvant chemotherapy.

For a variety of reasons, fewer than half of patients undergoing attempted curative resection received adjuvant therapy. Of the patients receiving no further therapy, only one suffered recurrence, and this was distant (brain), whereas each of the patients who had adjuvant therapy had recurrences. Given the small numbers of patients and mixture of histologic diagnoses, no firm conclusions can be drawn regarding adjuvant therapy. Decisions regarding administration of such treatment must be individualized for each patient depending on the patient's performance status, tumor histology, and extent of resection.

Based on our results, we believe that a highly selected group of patients with cardiac chamber or great vessel invasion may derive better palliation and a potential for cure when treated with aggressive surgical resection. Complex thoracic resections that require vascular and cardiac resection and reconstruction for curative intent should only be offered to patients in whom extrathoracic sites of disease have been excluded. Those with metastatic disease should only be considered for resection if cardiovascular collapse is thought to be imminent on the basis of symptomatology and when few treatment alternatives exist. In these patients a significant improvement in quality of life and palliation can be achieved. The use of CPB is effective and associated with minimal morbidity and mortality. Concomitant anatomic pulmonary resection on CPB does not seem to increase the morbidity of the procedure. Whether a long-term survival benefit may be achieved, however, cannot be determined without comparison of the long-term results of treatment in a larger group of patients with similar histologies. The intermediate survival results in a number of patients who had complete gross tumor resection look promising.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
The authors acknowledge that some of the patients in this series were cared for by the late Dr Robert Ginsberg. The authors thank Randy Lake for his excellent assistance in manuscript preparation.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

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