Although the incidence of malignant primary mediastinal

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1 Surgery for Invasive Primary Mediastinal Tumors Emile A. Bacha, MD, Alain R. Chapelier, MD, PhD, Paolo Macchiarini, MD, Elie Fadel, MD, and Philippe G. Dartevelle, MD Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, Centre Chirurgical Marie-Lannelongue, Paris-Sud University, Le Plessis-Robinson, France Background. There have been few reports on results after extended radical resection for primary mediastinal tumors invading neighboring organs. Methods. A retrospective analysis of 89 patients who underwent total or subtotal resection of a primary mediastinal tumor with resection of at least part of an adjacent structure between 1979 and 1995 was performed. Clinical data were collected from the medical records. Results. There were 35 invasive thymomas, 12 thymic carcinomas, 17 germ cell tumors, 16 lymphomas, 3 neurogenic tumors, 3 thyroid carcinomas, 2 radiationinduced sarcomas, and 1 mediastinal mesothelioma. The tumor was located in the anterior mediastinum in 74% of patients. Residual masses after chemotherapy were excised in 14 patients with germ cell tumor and 8 with lymphoma. A median sternotomy was the most frequently used approach (79% of patients). Total resection was achieved in 79% and significantly improved survival (p < 0.01). Adjacent resected structures included 38 phrenic nerves, 21 superior venae cavae, 16 upper lobes, and 13 innominate veins, in 5 patients, a pneumonectomy was required. The complication rate was 17% and the mortality rate, 6%. With follow-up available for 86 patients, the overall 5-year survival rate was 69% for patients with thymoma, 42% for patients with thymic carcinoma, 48% for patients with germ cell tumor, and 83% for patients with lymphoma. Conclusions. Malignant mediastinal tumors can be safely resected even if they have invaded other mediastinal structures. Complete resection is important to achieve satisfactory long-term survival. A median sternotomy is an excellent approach, and a preoperative diagnosis by biopsy is desirable. Residual masses after chemotherapy for lymphoma or germ cell tumor should be resected. Extensive resection without a preoperative diagnosis is not indicated. (Ann Thorac Surg 1998;66:234 9) 1998 by The Society of Thoracic Surgeons Although the incidence of malignant primary mediastinal tumors seems to be increasing over the last decades [1, 2], these tumors remain a relatively uncommon finding. Recent advances in radiographic techniques and immunohistochemistry have led to more accurate preoperative delineation and histologic diagnoses [2]. However, when an invasive mediastinal tumor is present, the surgeon s decision to resect the mass along with involved neighboring structures must be weighed against the morbidity of such a procedure. In addition, the potential long-term survival benefit must be considered. Several authors [1 4] have reviewed their experience with mediastinal tumors, but little information is available on the immediate and long-term survival of patients undergoing additional resection of invaded structures. Survival after radical removal of infiltrating thymomas, for example, has been shown to be affected positively [5, 6]. Consequently, we reviewed our 16-year experience with extended radical resection of invasive mediastinal tumors to determine whether short- and long-term results justify this type of surgical intervention. The modalities, techniques, and limits of such procedures will be discussed. Accepted for publication Feb 12, Address reprint requests to Dr Dartevelle, Centre Chirurgical Marie- Lannelongue, 133 Avenue de la R esistance, Le Plessis-Robinson, France. Material and Methods From November 1979 to December 1995, 89 patients with invasive primary mediastinal tumors underwent tumor resection at our institution. Only those patients who were found to have macroscopic tumor invasion of one or several mediastinal structures at the time of operation and required resection of at least part of a neighboring structure were included in this study. Patients who underwent biopsies or limited debulking procedures only or patients who had metastatic disease of the mediastinum, direct extension of lung malignancy into the mediastinum, esophageal, tracheal, or cardiac malignancies, or extrathoracic metastases were excluded. Medical records were reviewed for demographic data, clinical presentation, diagnostic investigations, operative procedure, location, tumor invasion as determined by the surgeon, histologic diagnosis, postoperative morbidity and mortality, and long-term follow-up. For the purpose of this study, we divided the mediastinum into three segments: anterior, middle, and posterior [7]. Clinical staging included history and physical examination, biochemical profile including tumor markers, posteroanterior and lateral chest roentgenograms, chest and abdominal computed tomographic scans, bronchoscopy, and upper venography by bilateral simultaneous upper extremity injection when there was a suggestion of compression of the venous system by The Society of Thoracic Surgeons /98/$19.00 Published by Elsevier Science Inc PII S (98)

2 Ann Thorac Surg BACHA ET AL 1998;66:234 9 SURGERY FOR INVASIVE MEDIASTINAL TUMORS 235 Clinical data, adjuvant therapy, and outcome are addressed separately for each group of patients. Survival analysis was performed by the method of Kaplan and Meier [8], and comparisons of survival were done by log-rank analysis. Significance was defined as a p value of less than Results Histology There were 35 invasive thymomas, including three recurrences from previously resected thymomas. Invasiveness was evaluated according to the modified classification of Masaoka and colleagues [9]: 2 patients had stage IIa tumor (invasion of mediastinal pleura and surrounding fatty tissue), 23 had stage III tumor (invasion into mediastinal structures, ie, lung, pericardium, or great vessels), and 10 had stage IVa (metastasis confined to the intrathoracic cavity). Twelve patients had a carcinoma arising from the anterior mediastinum: 6 were in stage III and 6, stage IVa. There were 7 undifferentiated carcinomas, 2 small cell carcinomas, 2 carcinoid tumors, and 1 adenocarcinoma. Seventeen patients (19%) had germ cell tumors (5 embryonal carcinomas, 3 yolk sac tumors, 3 choriocarcinomas, 3 seminomas, 2 mixed germ cell tumors, and 1 malignant teratoma). Sixteen patients (18%) had mediastinal lymphomas (11 non-hodgkin s large B-cell lymphomas, 4 scleronodular Hodgkin s lymphomas, and 1 lymphoblastic lymphoma). The remaining tumors included 3 invasive neurogenic tumors, 3 thyroid tumors arising in the mediastinum, 2 radiation-induced sarcomas, and 1 mesothelioma arising from the mediastinal pleura. Symptoms and Demographic Data Symptoms were present at the time of diagnosis in 73% of the 89 patients. Main presenting symptoms are listed in Table 1. The youngest patient was 2.5 years old and the oldest, 83 years old. Average age was 42 years. There were 33 female and 56 male patients. Anatomic Location The majority of tumors were located in the anterior mediastinum (66 patients), followed by the middle mediastinum (20 patients). Thymomas were the most common lesion in the anterior mediastinum. Preoperative and Postoperative Chemotherapy and Radiation Therapy For thymic neoplasms, irradiation was used as postoperative adjuvant therapy in 85% of patients with thymomas and 58% of those with thymic carcinomas. Postoperative chemotherapy was used in 67% of patients with thymic carcinomas. Sixteen of the 17 patients with a malignant germ cell tumor had elevated serum levels of -fetoprotein, -human chorionic gonadotropin, or both on presentation. Three patients, all seen in the very early part of the Table 1. Symptoms and Clinical Presentation Symptom Thymoma Germ Cell Tumor Lymphoma Other Total a Asymptomatic (17) (CXR) Chest pain (19) SVC (16) syndrome Respiratory (15) symptoms b Myasthenia (12) gravis Weight loss (5) Fever (5) Phrenic nerve (3) Dysphonia (3) Tracheal (2) Gynecomastia (2) Pericardial (2) effusion Thrombosis of upper extremity (1) a Numbers in parentheses are percentages. b These include cough, bronchitis, and dyspnea. CXR routine chest roentgenogram; SVC superior vena cava. series, did not have preoperative chemotherapy. Fourteen patients received cisplatin-based combination chemotherapy preoperatively. This resulted in normalization of tumor markers in 8 patients. In the 6 patients without marker normalization, preoperative chemotherapy was considered a failure; they underwent operation and received chemotherapy postoperatively. Five patients had no residual viable tumor cells left in the specimen. Ten patients underwent postoperative chemotherapy. Eight patients with lymphoma underwent preoperative chemotherapy and resection of a residual mass. Six had no residual malignant cells; the remaining 2 patients and the 8 other patients in this group (who had not had a preoperative diagnosis of lymphoma) were given chemotherapy postoperatively. Complications of chemotherapy and radiation therapy included bone marrow aplasia in 5 patients, interstitial pneumonitis in 3, fatal systemic mastocytosis in 2, and pericarditis, myocarditis, and secondary malignancy in 1 patient each. Surgical Approach A median sternotomy was used in 70 patients (79%). A left thoracotomy was added in 2 patients and a right thoracotomy, in 1 patient. A thoracotomy was used in 14 patients. The clamshell incision (bilateral anterior thoracotomy with transverse sternotomy) was chosen for 3 patients with large chemoresistant germ cell tumors. A bilateral thoracotomy was performed in 1 patient and a cervicomanubriotomy, in 1 patient.

3 236 BACHA ET AL Ann Thorac Surg SURGERY FOR INVASIVE MEDIASTINAL TUMORS 1998;66:234 9 Table 2. Resection of Additional Structures Resection Thymoma Germ Cell Tumor Lymphoma Other Total Extent Radical Subtotal Of pulmonary structures Phrenic nerve Pulmonary wedge Pleura Lobectomy Pneumonectomy Of vascular structures SVC 11 a b Innominate vein c Partial PA resection 1 d 0 1 e 0 2 Other Pericardium Bony chest wall 1 f g 6 Diaphragm (part) a One SVC was not replaced. b These patients were the subject of a previous report [10]. c The innominate vein was resected and not replaced. d This comprised PA resection and reanastomosis. e This comprised partial wall resection and patch repair. f This was an internal hemicleidectomy. g The manubrium (two radiation-induced sarcomas invading the chest wall, one thyroid cancer, and one neurogenic tumor) and posterior ribs (one neurogenic tumor) were involved. PA pulmonary artery; SVC superior vena cava. Resection of Adjacent Structures In the majority of patients (79%), total removal of the tumor by radical excision was achieved (Table 2). The pericardium was the most frequently excised structure, and pulmonary tissue, including 16 upper lobes and five lungs, was resected along with the tumor in 68 patients (76%). Thirty-six patients (40%) underwent resection of vascular structures, including superior vena cava (SVC) replacement in 21 patients [10] and innominate vein resection in 13, all of which were performed without replacement. All SVC grafts but one were patent on the first postoperative venogram at 3 months. The failure occurred in a patient with prior SVC thrombosis extending into the subclavian veins [10]. There was one late graft occlusion after 15 months after insertion of a central venous catheter through the graft for an exploratory laparotomy. Surgical Complications Fifteen patients (17%) experienced complications. Sternal wound infections developed in 3 patients. Two patients, both with myasthenia gravis, required intubation for longer than 4 days, and 2 others sustained postoperative hemorrhage requiring reoperation (both after pneumonectomy). One patient each had early SVC graft occlusion, late SVC graft occlusion, phrenic nerve palsy, bilateral recurrent nerve palsy, left recurrent nerve palsy, and atrial fibrillation. One patient had development of left pulmonary artery thrombosis after pulmonary artery resection and reanastomosis. This necessitated a completion pneumonectomy. One patient had mediastinitis because of tracheal necrosis after an extensive operation with prosthetic replacement of the SVC for a third recurrence of thyroid cancer. This patient was successfully treated by omentopexy and tracheostomy. Surgical Mortality Five patients (6%) died in the immediate postoperative period. One patient with thymoma and massive tumor invasion had subtotal resection of the tumor along with a pneumonectomy. Another patient with thymoma and severe myasthenia gravis underwent resection of a phrenic nerve and the left innominate vein and an atypical pulmonary resection. Both patients died of respiratory causes. Two patients with giant germ-cell tumors (3.7 and 3.2 kg) and severe preoperative compression of the left lung and great vessels in 1, and of the Fig 1. Kaplan-Meier estimate of survival by histologic diagnosis.

4 Ann Thorac Surg BACHA ET AL 1998;66:234 9 SURGERY FOR INVASIVE MEDIASTINAL TUMORS 237 Fig 2. Kaplan-Meier estimate of survival by extent of resection (p 0.01). heart in the other died on postoperative days 4 and 10. The cause of death was thought to be reperfusion edema after reestablishment of flow to the pulmonary parenchyma and myocardium. Both had undergone preoperative chemotherapy and radiation therapy. One patient with a large thyroid carcinoma invading the upper mediastinum underwent total thyroidectomy, SVC replacement, left upper lobectomy, and resection of invaded manubrium. He died on postoperative day 30 of a perforated sigmoid diverticulitis. Long-Term Survival Follow-up was available for 86 patients (97%) and extended from 3 months to 15 years. Median follow-up was 29 months with an average of 44 months. The overall actuarial 5-year survival rate for all patients was 63%. Five-year survival on the basis of histologic diagnosis is depicted in Figure 1. The 5-year survival rate for patients with thymoma was 69%; it was 42% for patients with thymic carcinoma, 48% for those with germ cell tumors, and 83% for those with lymphoma. Recurrence was documented in 4 patients with invasive thymoma, 9 patients with thymic carcinoma, 3 patients with germ cell tumor, 3 patients with lymphoma, 2 patients with radiation-induced sarcoma, and 1 patient with thyroid carcinoma. Survival by extent of surgical resection is shown in Figure 2. Comment This large series focused specifically on patients with malignant mediastinal tumors invading adjacent organs or structures and requiring at least partial resection thereof. Our overall survival rate of 63% at 5 years compares favorably with rates published in earlier series [1, 3]. This can partially be explained by recent advances in neoadjuvant and adjuvant therapies and by the higher number of less aggressive thymomas in our series. As demonstrated by the significantly better survival of patients with complete resection, we concur with most other series showing that completeness of surgical resection is beneficial [1, 5, 11, 12]. Technical Aspects Median sternotomy is the optimal approach to anterior mediastinal tumors, even in the presence of pulmonary involvement. Upper lobectomy or bilobectomy as well as main pulmonary artery resection or repair by pericardial patch can be performed through this approach. Indeed, we used a median sternotomy approach in about three quarters of our patients. Alternatively, an axillary anterolateral thoracotomy, with transverse sternotomy if needed, can also be used. A posterolateral thoracotomy is chosen mainly for posterior tumors. Mediastinal tumors are best excised from left to right. Technical problems can often be encountered at the level of the right brachiocephalic vein and the right pulmonary pedicle. Here, resection can be conducted from the intrapericardial side of the right pulmonary pedicle to free the right extremity of the tumor, which often invades the pericardium at the origin of the pulmonary pedicle. Invasion of the superior pulmonary vein is best approached intrapericardially, allowing a standard lobectomy in a posterior to anterior fashion, with sacrifice of the phrenic nerve if needed. Absolute contraindications to resection of mediastinal masses are invasion of the myocardium, great vessels, or a long tracheal segment. In our series, the most commonly invaded structure was the pericardium, followed by the lung, phrenic nerve, and SVC. One important pitfall in large pericardial resections is the potential for rotation of the heart through the defect into one of the thoracic cavities, especially when a pneumonectomy is performed. A Vicryl (Ethicon, Somerville, NJ) mesh should always be placed to reconstruct large pericardial resections. The lung was involved in 55% of our patients. The majority of these cases consisted of invasion of the anterior segments of the upper lobes or lingula and can be dealt with by a wedge resection using a stapler. If possible, pneumonectomy should be avoided, particularly in patients with poor respiratory function. In our series, 5 patients underwent pleuropneumonectomy for stage IVa thymomas with two postoperative hemorrhages and one death. In our opinion, only massive invasion of the pulmonary hilum or extensive subpleural and pulmonary thymoma metastases can justify a pneumonectomy. Total SVC replacement is indicated when a clinical SVC syndrome is present and the vein is extensively invaded or occluded by the tumor, thus making local reconstruction of the vein by lateral suture or pericardial patch unfeasible [10]. Intraoperative management includes intravascular fluid expansion, use of vasoconstrictive agents to keep a high cerebral perfusion pressure, and systemic heparinization. The left brachiocephalic vein is ligated first; resection is then carried out while the mass is rotated around the SVC right brachiocephalic vein axis. Resection of the SVC is done last to minimize clamping time. If only the left brachiocephalic vein is invaded by tumor, it can safely be resected without replacement. In our experience, a ringed polytetrafluoroethylene graft at least 12 mm in diameter is needed and ideally is placed between the right brachiocephalic vein

5 238 BACHA ET AL Ann Thorac Surg SURGERY FOR INVASIVE MEDIASTINAL TUMORS 1998;66:234 9 and the SVC right atrial junction. After intraoperative systemic heparinization, patients are placed on a heparin sodium drip, keeping the partial thromboplastin time 1.5 times normal. Oral warfarin sodium is then started and overlapped with heparin. Warfarin is stopped after 6 months, at which time aspirin is started. Reconstruction of the SVC is contraindicated in the presence of extensive thrombosis invading the subclavian veins. In fact, extensive thrombosis is associated with a high risk of postoperative thromboembolism, and the only patient in our series with postoperative thrombosis had had extensive SVC thrombosis preoperatively. Another contraindication to SVC reconstruction is widespread collateral venous circulation. The venous flow available to the graft decreases, thus increasing the likelihood of thrombosis [13]. In such a situation, it is preferable to simply ligate the SVC. Because the right phrenic nerve is often sacrificed, left phrenic nerve invasion also represents a formal contraindication to SVC replacement. In general, phrenic nerve function must always be preserved on at least one side, especially if pulmonary resection is planned [14]. Thymic Neoplasms On the basis of our experience and that of others [5, 6, 12], there is little doubt that radical excision is the standard of care for invasive thymomas. Debulking procedures have survival rates similar to those of biopsy alone [15]. Our 5- and 10-year survival rates have improved from 50% to 63% and 35% to 50%, respectively [16]. Predictably, patients with thymic carcinomas had the worst survival (42% at 5 years) and a high recurrence rate (75%). Postoperative irradiation has become a mainstay of therapy for all invasive thymomas in our practice as well as in others [15]. Germ Cell Tumors Since the advent of cisplatin-based chemotherapy, the role of operation as primary treatment of invasive germ cell tumors has been more limited [17 19]. In this historical series, preoperative chemotherapy was underused in the early period. Marker normalization after chemotherapy has been associated with improved survival [20]. This is analogous to our series where, after the exclusion of both postoperative deaths, patients with marker normalization had an improved survival compared with those without such normalization. Resection of residual masses after chemotherapy has been advocated [17, 18, 20 22]. Fourteen patients underwent resection of residual masses that were invading adjacent structures. In 5 patients, the specimen consisted of only necrotic cells with no tumor. This subgroup of patients had a median survival of 45 months, which was offset by two deaths at 36 months postoperatively from postchemotherapy systemic mastocytosis. The remaining 3 patients are alive and disease free. Our experience, like the experiences of others [21, 22], suggests that aggressive surgical intervention to resect residual masses, ideally after marker normalization, is indicated (three SVC replacements in our series). It serves as a means to direct additional therapeutic measures if tumor is found and to eliminate any residual active tumor cells. Indeed, the residual tumor frequently contains malignant cells that are resistant to chemotherapy [22], as in 9 patients in this series. Also, if viable carcinoma is found in the specimen, patients can receive further chemotherapy under a salvage regimen, because the relapse rate is high [23]. Lymphomas Intensive combination chemotherapy is the primary treatment modality for mediastinal lymphomas, and the role of surgical intervention is mostly confined to diagnostic biopsies and resection of residual masses after chemotherapy [24]. Resection of such masses serves a triple purpose: it establishes the need of further chemotherapy, eliminates any nidus of residual tumor, and eliminates the need of additional radiotherapy in completely resected residual masses. All 8 patients who underwent chemotherapy as the primary treatment modality are currently alive and disease free. Only 1 had relapse at 2 months. Two patients had residual tumor in the resected specimen: they underwent postoperative chemotherapy. On the basis of these results, we think that resectional procedures for residual masses are indicated. Eight patients underwent complete resection after a frozen section biopsy was initially incorrectly interpreted as not being lymphoma. Until better frozen section biopsy techniques become available, we believe that aggressive surgical intervention, in particular phrenic nerve resection, is not indicated when lymphoma is a potential diagnosis. Conclusions We conclude that malignant mediastinal tumors can safely be resected even if they have invaded other mediastinal structures, such as the lung or the SVC. Complete resection is important to achieve satisfactory long-term survival. Median sternotomy is an excellent approach, even in cases of pulmonary involvement. Postoperative mortality is associated with pneumonectomies and large bulky tumors. A preoperative diagnosis by biopsy is highly desirable, especially in young patients at risk for lymphoma, for whom frozen section biopsies are of only limited value. Residual masses on computed tomography after chemotherapy for lymphoma or germ cell tumor should be resected. Ideally germ cell tumors should be resected when tumor markers have normalized. Extensive resection without a preoperative diagnosis is not indicated. References 1. Adkins RB Jr, Maples MD, Hainsworth JD. Primary malignant mediastinal tumors. 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