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Ann Thorac Surg 1995;60:908-913
© 1995 The Society of Thoracic Surgeons
Thoracic Service, Department of Surgery, and Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, New York
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Abstract |
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Methods. A retrospective analysis of patients operated on for thymoma between 1949 and 1993 at Memorial Sloan-Kettering Cancer Center was performed. Clinical data were collected from chart review. Only patients with a pathology report confirming the diagnosis of thymoma were included in this analysis. Kaplan-Meier survival curves were generated and comparisons of survival analyzed by log rank test. Multivariate analysis was performed by the Cox proportional hazards model.
Results. One hundred eighteen patients with thymoma underwent operation. There were 86 complete resections (73%), 18 partial resections (15%), and 14 biopsies (12%). By Masaoka staging, 25 patients were stage I (21%), 41 stage II (35%), 43 stage III (36%), and 9 stage IVa (8%). Overall survival was 77% at 5 years and 55% at 10 years. Tumor recurred in 25 (29%) of 86 completely resected thymomas. Stage of disease (p = 0.03) was the only independent prognostic factor affecting recurrence. By multivariate analysis, stage (p = 0.003), tumor size (p = 0.0001), histology (p = 0.004), and extent of surgical resection (p = 0.0006) were independent predictors of long-term survival.
Conclusions. Patients with stage I disease require no further therapy after complete surgical resection. Neoadjuvant therapy should be considered for patients with large tumors and invasive disease.
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Introduction |
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Thymomas are uncommon neoplasms that are derived from the epithelial cells of the thymus [1]. These tumors often have a peculiar, indolent natural history with recurrences noted as long as 10 years after surgical resection. Attempts at predicting the evolution of this disease by histopathologic examination alone have proved frustrating. Several authors have commented on the fact that many invasive thymomas have cytoarchitectural features similar to those of encapsulated (benign) thymomas [2, 3]. These are referred to as type I malignant thymomas and distinguished from the cytologically malignant neoplasms, known as type II malignant thymomas or thymic carcinomas. The existence of intermediate or hybrid cases has also been commented on [4].
Previous studies have demonstrated that the presence of mediastinal invasion negatively affects survival whereas complete resection of tumor appears to translate into improved survival. In this study, we have performed a multivariate analysis of prognostic factors in 118 patients surgically treated for thymoma to define which factors independently predict prognosis.
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Patients and Methods |
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Final pathologic staging was performed by the Masaoka staging system [6]. Stage I was defined as patients with encapsulated thymomas; stage II, invasion into surrounding fatty tissue or mediastinal pleura or microscopic invasion of the thymic capsule; stage III, invasion into mediastinal structures (ie, lung, pericardium, or great vessels); stage IVa, metastasis confined to the intrathoracic cavity; and stage IVb, distant metastasis.
Sixty-two patients were female and 56 were male. The median age of all patients was 54 years, with a range of 15 to 81 years. Eighty-five patients (72%) presented with clinical symptoms or signs, including cough (22%), dyspnea (24%), chest pain (24%), and superior vena caval syndrome (5%). Patients also presented with associated autoimmune findings of myasthenia gravis (10%), red cell aplasia (3%), hypogammaglobulinemia (3%), systemic lupus erythematosus (3%), a positive antinuclear antibody (1%), and 1 case of limbic encephalitis [7]. In addition, 12 patients had a second malignancy: soft tissue sarcoma (3), breast carcinoma (2), colon carcinoma (1), gallbladder carcinoma (1), lymphoma (1), malignant melanoma (1), lung carcinoma (1), thyroid carcinoma (1), and uterine corpus carcinoma (1).
Preoperative diagnostic studies included chest radiograph in all patients, computed tomographic scan in 47 patients, and a diagnostic tumor biopsy in 48 patients. A mediastinal mass was present in 102 patients, with 80% being localized to the anterior mediastinum. Thirteen patients were noted to have a lung mass, and 3 patients had only a pleural effusion. Preoperative biopsy was performed in 48 patients by open biopsy (n = 26) and fine-needle biopsy (n = 22). A tissue diagnosis of thymoma was confirmed in 32 of 48 patients for an overall accuracy rate of 67%. Diagnosis was accurate by fine-needle biopsy in 59% of patients (n = 13) compared with 81% of patients (n = 21) with open biopsy.
Operative approach was median sternotomy in 50% of patients and anterolateral thoracotomy in 48%, with 2% of patients approached by bilateral anterolateral thoracotomy with a transverse sternotomy (``clamshell''). At operation, 79 patients (67%) had mediastinal invasion. The most common sites of tumor invasion were pleura (61%), pericardium (57%), great vessels (33%), phrenic nerve (27%), and lung (23%). Staging by Masaoka classification identified 25 stage I patients (21%), 41 stage II (35%), 43 stage III (36%), and 9 stage IVa (8%).
In addition to operation, the majority of patients were treated with adjuvant radiation therapy, chemotherapy, or both. Sixty-four patients (54%) received external beam radiation therapy with a median dose of 45 Gy and a range of 5.23 to 116 Gy. Thirty-eight patients (32%) received chemotherapy, with the most common agents being cisplatin, cyclophosphamide, and doxorubicin.
Survival analysis was performed by the method of Kaplan and Meier [8], comparisons of survival by log-rank analysis [9], and multivariate analysis by the Cox proportional hazards model [10]. Significance was defined as a p value less than 0.05.
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Results |
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Recurrence: Incidence and Patterns of Failure
Of 86 patients who had complete resection, 25 patients (29%) had a recurrence. Seventeen had local recurrence in the mediastinum, 5 patients had distant recurrence, and 3 patients had both local and distant recurrence. Overall recurrence rates at 5 and 10 years were 35% and 40%, with a range of 4 months to 11 years. The sites of local recurrence were lung (n = 15), diaphragm (n = 3), pleura (n = 1), heart (n = 1), carotid artery (n = 1), and aorta (n = 1). Distant recurrences were to liver (n = 3), clavicle (n = 1), ribs (n = 1), vertebrae (n = 1), and bone (n = 1).
Epidemiologic and Clinical Features
Survival was not dependent on age, sex, or presence of symptoms. Patients with myasthenia gravis had a 5-year survival of 84%, which did not differ (p = 0.32) from that of patients without myasthenia, who had a 74% 5-year survival. Patients (n = 9) with signs or symptoms of red cell aplasia, hypogammaglobulinemia, or systemic lupus erythematosus had a decreased survival (p = 0.02). Five- and 10-year survival for these patients was 57% and 24%, respectively, as compared with unaffected patients, who had a 78% 5-year and 57% 10-year survival.
Histologic Type
A definite histologic classification was able to be determined in 106 thymomas: There were 43 thymic carcinomas, 19 mixed lymphoepithelial thymomas, 15 predominantly lymphocytic thymomas, 5 predominantly epithelial thymomas, and 24 spindle cell thymomas. Of these, 78 patients had a complete resection. Spindle and predominantly lymphocytic thymomas had the lowest recurrence rates, with no recurrences at 5 years for lymphocytic type and a 5% recurrence for spindle cell thymomas. Mixed thymomas had a recurrence rate of 35%. Predominantly epithelial thymomas and thymic carcinomas had the highest (p = 0.0001) recurrence rates at 5 years: 50% for epithelial and 65% for thymic carcinomas.
Patient survival was also dependent on tumor histology. Survival was greatest for patients with spindle cell and predominantly lymphocytic thymomas, with respective 10-year survivals of 90% and 80%. Patients with mixed thymomas and thymic carcinomas had a 65% and 60% survival, respectively at 6 years. Survival of patients with predominantly epithelial thymomas was the worst (p = 0.04), with only 40% alive at 6 years (Fig 1
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Survival rates of all 118 patients stratified by Masaoka staging system were also significantly different (p = 0.002). Stage I thymomas had an excellent prognosis, with 95% of patients surviving 5 years and 86% at 10 years. Thymomas with capsular or pleural invasion (stage II) had a 70% 5-year survival rate, and thymomas with mediastinal invasion (stage III) had a 5-year survival of 50%. Despite an extraordinary high recurrence rate (80%), the 9 patients with stage IVa thymomas (thymoma with intrathoracic metastasis) had a 5-year survival rate of 100% (Fig 3).
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). Eighty-six patients (73%) underwent complete resection. An additional 18 patients (15%) underwent a debulking procedure or partial resection. In 14 patients (12%) a simple biopsy was performed. Patients who underwent complete resection survived significantly longer (p = 0.0002) than those who had partial resection or biopsy. Survival in patients with complete resection was 80% and 70% at 5 and 10 years, respectively. Survival at 5 and 10 years for partial resection was 70% and 28%, and for biopsy was 38% and 24%. No significant (p = 0.14) difference in survival was observed for those patients having a partial resection compared with those patients having a biopsy (Fig 4).
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Effect of Recurrence on Overall Survival
Of 86 patients with complete resection, survival of patients with recurrence (n = 25) was 65% at 5 years, which was significantly less (p = 0.05) when compared with patients (n = 61) with no recurrence (90% 5-year survival). However, patients with local recurrence (n = 17) had similar (p = 0.2) 5-year survival (80%) when compared with patients with no recurrence. Distant recurrence (n = 8) was associated with a decreased (p = 0.007) survival compared with patients who had local or no recurrence. The median time to recurrence was 3.8 years for local and 3.4 years for distant recurrence (p = 0.3).
Operation for Recurrence
Of the 25 patients with complete resection who had recurrence, treatment in 13 patients consisted of primarily surgical resection, with addition of radiation in 4 and radiation plus chemotherapy in 6 patients. Recurrence in these patients was primarily local (n = 12), with one distant recurrence. In the remaining 12 patients, recurrence was treated nonsurgically with radiation, chemotherapy, or both (radiation [n = 3], chemotherapy [n = 5], radiation plus chemotherapy [n = 4]). In these patients, there were 5 local, 4 distant, and 3 local and distant recurrences. Initial stage of patients with surgically re-resection was comparable (stage I [n = 2], stage II [n = 3], stage III [n = 6], stage IV [n = 2]) with that of patients without resection (stage II [n = 3], stage III [n = 6], stage IV [n = 3]), as was the initial disease-free interval (3.6 versus 2.3 years; p = 0.5). Surgical resection of recurrent thymoma was associated with a greater survival (p = 0.001), with 85% 5-year survival as compared with a 45% 5-year survival for patients without resection. In addition, 5-year survival (85%) of patients with resected recurrent thymomas was comparable (p = 0.5) with survival (90%) of patients with complete resection in whom recurrence did not develop (Fig 5). In addition, patients with surgical re-resection had a 90% 2-year survival from the time of recurrence compared with 30% survival of those without resection (p = 0.0004).
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Unresectable Thymoma: Effect of Chemotherapy and Radiation Therapy
Patients with unresectable (partial resection + biopsy) stage III thymomas (n = 19) received combinations of chemotherapy and radiation therapy. Eight patients were given both chemotherapy and radiation, 6 received radiation alone, 3 had chemotherapy alone, and 2 patients received neither chemotherapy nor radiation. Patients treated with radiation (n = 14) had a similar (p = 0.3) 2-year survival of 62% as compared with 58% for 5 nonirradiated patients. Patients receiving chemotherapy (n = 11) had a 5-year survival of 56%, which was no different (p = 0.25) than the 58% survival of 8 not treated with chemotherapy. In addition, 8 patients treated with radiation and chemotherapy had a 5-year survival of 62%, which was no different (p = 0.72) than the 50% 5-year survival of all other patients with unresected stage III disease (n = 11).
Treatment of Stage IV Thymomas
Although patients with stage IV thymomas (n = 9) had a high recurrence rate (80% at 5 years), survival was remarkably high (100% at 5 years). Aggressive multimodality therapy was used. Seven patients had complete resections, with 1 patient undergoing two re-resections and 1 patient operated on 6 times. Chemotherapy was administered to 7 patients and consisted of two or more drugs in 6 cases, including cisplatin, doxorubicin, and cyclophosphamide. Radiation was given to 8 patients, with a range of 20 to 116 Gy. Eight patients were alive at last follow-up, and there were 5 survivors past 6 years. Of these long-term survivors, 1 patient survived 9.8 years with aggressive chemotherapy and radiation after biopsy. Of the 2 longest survivors, 1 patient was alive with disease at 10.1 years after undergoing three surgical resections, 70 Gy of radiation, and combination chemotherapy. The second patient was also alive with disease at 19.9 years after six surgical resections and 40 Gy of radiation.
Multivariate Analysis of Survival and Local Recurrence
Recurrence was solely dependent on stage of disease (p = 0.03). Significant independent predictors of survival were histology (p = 0.004), tumor size (p = 0.0001), stage of disease (p = 0.003), and extent of surgical resection (p = 0.0006).
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Comment |
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TopFootnotesAbstractIntroductionPatients and MethodsResultsCommentReferences |
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The fact that local recurrence did not affect 5-year survival may be accounted for by the aggressive surgical approach taken in these patients. The majority of local recurrences were treated with surgical resection. Resection of recurrence resulted in a favorable 5-year survival, which was similar to that of patients with complete resection who did not have recurrence. In contrast, medical treatment of recurrence resulted in a significantly reduced survival of 45% at 5 years. One recent study [11], reported by Kirschner, also confirmed that long-term survival is possible with resection of recurrent thymoma.
Of epidemiologic and clinical factors analyzed, excluding myasthenia gravis, the presence of autoimmune disease (systemic lupus erythematosus, red cell aplasia, hypogammaglobulinemia) was associated with a decreased survival as compared with unaffected patients. Similar poor survival of these patients has been demonstrated by other studies [13, 14]. In our series, survival of patients with myasthenia gravis was no different than that of patients without myasthenia gravis. Earlier series [13] showed decreased survival of myasthenics, which has been attributed to increased perioperative mortality. More recently, multiple studies have documented that myasthenia is not an adverse prognostic factor [14–17]. Survival was also independent of age, sex, and presence of symptoms.
Of tumor characteristics, survival was related to histology and stage of disease by both univariate and multivariate analysis. Patients with spindle cell thymomas had the greatest survival, with 90% surviving 10 years, and patients with predominantly epithelial thymomas had the worst prognosis, with only 40% alive at 6 years. Other series have also confirmed a reduced survival of patients with predominantly epithelial thymoma [13, 14, 18–20]. In our series, there were 43 patients with thymic carcinoma. Survival of these patients was 65% at 5 years, which compares favorably with the 34% 5-year survival reported by other investigators [21]. The difference in survival is probably related to differences in stage and resectability. In the series reported by Hsu and associates [21], 19 of 20 patients (95%) presented with stage III and IV disease and only 7 of 20 patients (35%) underwent complete resection. In contrast, our patients presented earlier with 3 stage I, 15 stage II, 20 stage III, and 5 stage IV tumors. In addition, complete resection was accomplished in 29 of 43 patients (67%). Although thymic carcinomas have been described as more aggressive tumors, prior reports of a poor outcome in these patients are probably the result of advanced stage at time of presentation and low resectability rates.
By multivariate analysis, survival was also significantly affected by stage of disease, with stage I patients having a favorable prognosis of 95% survival at 5 years and 86% 10-year survival. Similar to other series [14, 15, 19, 22, 23], the presence of mediastinal invasion (stage III disease) was associated with decreased survival. In contrast to these studies, patients with stage IV disease in our series had a remarkably high survival of 100% at 5 years, although there were only 9 patients. The favorable survival for stage IV patients may be the result of aggressive multimodality treatment of these patients. Seven had complete resection, 2 had multiple resections, 2 received radiation, 1 had chemotherapy, and 6 patients received a combination of radiation and chemotherapy.
Tumor size was also a significant independent prognostic variable, with large thymomas (>11 cm) having a worse survival as compared with 84% 5-year survival of smaller tumors. Similar results have been reported by others [15, 23]. In the UCLA experience, large thymomas (>15 cm) had approximately a 50% survival at 10 years as compared with 100% survival of small tumors (<5 cm).
The extent of surgical resection was also a significant independent predictor of survival. Patients who underwent complete surgical resection had a greater 5- and 10-year survival, as compared with partial resection or biopsy. However, there was no difference in long-term survival for patients undergoing partial resection compared with biopsy, indicating a lack of efficacy for surgical debulking, which has been shown by others [24]. The favorable prognosis of patients who had complete resection was not the result of these patients having earlier stage disease. Patients with malignant thymomas (stage II, III, and IVa) also benefited from surgical resection. Excluding 25 patients with benign thymomas (stage I), there were 93 patients with malignant thymomas. Sixty-one of these patients underwent complete resection, 14 had partial resection, and 18 had biopsy. Five-year survival of patients with complete resection was greater than that of those with partial resection or biopsy. In other series, complete resection of stage III disease also afforded improved survival [19].
Although radiation has been reported as a potentially useful adjuvant for treatment of invasive thymoma, we did not see a reduction in recurrence or an improvement in survival with adjuvant radiation. In a recent Japanese study a promising trend (p = 0.12) toward improved survival was reported in 17 patients receiving postoperative radiation after complete resection as compared with 5 patients not receiving adjuvant therapy [25]. Other studies have also shown marginal benefit for radiation [26, 27]. In 19 patients, radiation and chemotherapy were used as a primary treatment modality for patients with unresectable stage III disease; however, we could not determine any survival benefit for patients receiving these adjuvants as compared to untreated patients. In recent studies, radiation has failed to demonstrate clinical efficacy as a primary therapy [28] for treatment of thymoma. In a report from M.D. Anderson, patients who responded to chemotherapy had improved survival compared with nonresponders [29]. Although we were unable to demonstrate a statistical benefit for radiation or chemotherapy, 3 of 5 patients achieving long-term survival (>6 years) with stage IV disease received adjuvant radiation and chemotherapy after complete surgical resection. In addition, 1 stage IV patient who received only radiation and chemotherapy without surgical resection achieved long-term survival for 10 years.
More recent studies have suggested that preoperative chemotherapy may potentially benefit patients with invasive thymoma. The study by Rea and associates [30] demonstrated an overall response rate to chemotherapy (doxorubicin, cyclophosphamide, vincristine, and cisplatin) of 100% in 16 patients with stage III and IVa thymoma. All underwent resection and most received postoperative radiation therapy. The 3-year survival was 70% for those 16 patients.
Based on the experience reported here, our current recommendations on the management of thymoma are as follows: (1) Small (<5 cm) tumors that appear encapsulated should be resected and, if pathologically stage I, require no further treatment. (2) Tumors greater than 5 cm or those that appear invasive by computed tomography have a high local recurrence rate and a decreased survival. These patients should therefore be considered for neoadjuvant protocols that include chemotherapy.
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Address reprint requests to Dr Burt, Thoracic Service, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021.
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M. de Perrot, M.-A. Brundler, C. Girardet, and A. Spiliopoulos Spontaneous hemorrhage of thymus and thymoma in adults Eur. J. Cardiothorac. Surg., December 1, 1999; 16(6): 674 - 676. [Abstract] [Full Text] [PDF]
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C. R. Thomas, C. D. Wright, and P. J. Loehrer Thymoma: State of the Art J. Clin. Oncol., July 1, 1999; 17(7): 2280 - 2280. [Abstract] [Full Text] [PDF]
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M. Okumura, S. Miyoshi, Y. Takeuchi, H.-E. Yoon, M. Minami, S.-I. Takeda, Y. Fujii, K. Nakahara, and H. Matsuda Results Of Surgical Treatment Of Thymomas With Special Reference To The Involved Organs J. Thorac. Cardiovasc. Surg., March 1, 1999; 117(3): 605 - 611. [Abstract] [Full Text]
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W. I. Awad, P. J. Symmans, and J. E. Dussek Recurrence of stage I thymoma 32 years after total excision Ann. Thorac. Surg., December 1, 1998; 66(6): 2106 - 2108. [Abstract] [Full Text] [PDF]
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E. A. Bacha, A. R. Chapelier, P. Macchiarini, E. Fadel, and P. G. Dartevelle Surgery for invasive primary mediastinal tumors Ann. Thorac. Surg., July 1, 1998; 66(1): 234 - 239. [Abstract] [Full Text] [PDF]
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D. Blumberg, M. E. Burt, M. S. Bains, R. J. Downey, N. Martini, V. Rusch, and R. J. Ginsberg Thymic Carcinoma: Current Staging Does Not Predict Prognosis J. Thorac. Cardiovasc. Surg., February 1, 1998; 115(2): 303 - 309. [Abstract] [Full Text] [PDF]
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J.-F. Regnard, F. Zinzindohoue, P. Magdeleinat, L. Guibert, L. Spaggiari, and P. Levasseur Results of Re-resection for Recurrent Thymomas Ann. Thorac. Surg., December 1, 1997; 64(6): 1593 - 1598. [Abstract] [Full Text]
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K. V. Arom and R. W. Emery Minimally Invasive Mitral Operations Ann. Thorac. Surg., April 1, 1997; 63(4): 1219 - 1220. [Full Text]
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E. Ruffini, M. Mancuso, A. Oliaro, C. Casadio, A. Cavallo, R. Cianci, P. L. Filosso, M. Molinatti, C. Porrello, N. Cappello, et al. RECURRENCE OF THYMOMA: ANALYSIS OF CLINICOPATHOLOGIC FEATURES, TREATMENT, AND OUTCOME J. Thorac. Cardiovasc. Surg., January 1, 1997; 113(1): 55 - 63. [Abstract] [Full Text]
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