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J Thorac Cardiovasc Surg 2007;134:1477-1484
© 2007 The American Association for Thoracic Surgery

General Thoracic Surgery

Feasibility of multimodality therapy including extended resections in stage IVA thymoma

James Huang, MDa, Nabil P. Rizk, MDa,*, William D. Travis, MDb, Venkatraman E. Seshan, PhDc, Manjit S. Bains, MDa, Joseph Dycoco, BAa, Robert J. Downey, MDa, Raja M. Flores, MDa, Bernard J. Park, MDa, Valerie W. Rusch, MDa

a Thoracic Service, Department of Surgery, Memorial Sloan–Kettering Cancer Center, New York, NY
b Department of Pathology, Memorial Sloan–Kettering Cancer Center, New York, NY
c Biostatistics Service, Department of Epidemiology–Biostatistics, Memorial Sloan–Kettering Cancer Center, New York, NY.

Read at the Eighty-seventh Annual Meeting of The American Association for Thoracic Surgery, Washington, DC, May 5-9, 2007.

Received for publication April 25, 2007; revisions received July 20, 2007; accepted for publication July 26, 2007.

* Address for reprints: Nabil P. Rizk, MD, Thoracic Service, Department of Surgery, Memorial Sloan–Kettering Cancer Center, 1275 York Ave, New York, NY 10021. (Email: rizkn{at}mskcc.org).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Discussion
 References
 
Objective: Extended resections for advanced-stage thymomas are not commonly performed because of the potential morbidity in the face of unclear survival or palliative benefit. We reviewed our experience with multimodality treatment for Masaoka stage IVA thymomas for feasibility and outcomes.

Methods: We conducted a retrospective review of a single-institution surgical database. Data included patient demographics, preoperative staging and treatment, perioperative events, pathologic findings, and postoperative outcomes.

Results: During the period from 1996 to 2006, 18 patients who had Masaoka stage IVA thymoma underwent surgical resection. All patients received preoperative chemotherapy. Four patients with extensive pleural involvement underwent concomitant extrapleural pneumonectomy and postoperative hemithoracic radiation. Complete resection was achieved in 12 (67%) patients. There was no operative mortality. With a median follow-up of 32.2 months (range 1.4–129.9 months), 3-year, 5-year, and 10-year survivals were 91%, 78%, and 65%, respectively, and median survival has not yet been reached.

Conclusion: Multimodality therapy including extended surgical resection can be performed in select patients with stage IVA thymoma with low morbidity and mortality and can result in excellent long-term survival.

Abbreviations and Acronyms CP = carboplatin and paclitaxel; EP = cisplatin and etoposide; EPP = extrapleural pneumonectomy; PAC = cisplatin, doxorubicin, and cyclophosphamide; RECIST = Response Evaluation Criteria In Solid Tumors; SSDI = Social Security Death Index; VIP = etoposide, ifosfamide, cisplatin


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Discussion
 References
 

Figure 2
Dr Rizk


GoSurgery is considered the mainstay of treatment for thymoma. The prognosis in thymoma has been consistently established to correspond to the completeness of resection and the Masaoka stage of the tumor.1-5Go Masaoka stage IVA describes locally advanced disease with pleural or pericardial metastases without distant metastases. The treatment of advanced thymoma is unclear inasmuch as complete resection may be difficult to attain and no standardized approach to multimodality treatment has been developed. The literature on stage IVA thymoma has been limited owing to its rarity, and series often span several decades, reflecting older histologic classification schemes, therapeutic agents, or surgical techniques.

In stage IVA thymoma, metastatic disease confined to the chest still allows the potential for complete resection of all disease. Extensive resections including extrapleural pneumonectomy (EPP) and resection of the superior vena cava for various thoracic malignant tumors including thymoma have been reported.6-13Go Several reports suggest that multimodality therapy in advanced thymoma may improve outcomes by potentially increasing resectability and reducing recurrences.14-19Go The purpose of this study was to determine the feasibility and outcome of multimodality therapy and extended resections in a contemporary series of consecutive patients with Masaoka stage IVA thymoma.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Discussion
 References
 
Collection of Clinical Data
We undertook a retrospective review of all patients undergoing resection for thymic epithelial tumors at Memorial Sloan–Kettering Cancer Center between January 1996 and December 2006. The Institutional Review Board granted approval for this study on August 30, 2005. Patients who had undergone prior resection and patients with a diagnosis of thymic carcinoma only or thymic carcinoid were excluded from the analysis. During this time period, 107 patients underwent surgery for the diagnosis of thymoma or well-differentiated thymic carcinoma. Of these, 18 patients had stage IVA thymoma with pleural dissemination and were included in this analysis. Patient records were reviewed for demographic information, treatment details, adverse events, and outcomes.

Pathologic Classification
Microscopic sections from these patients were re-reviewed by one pathologist (W.T.) to confirm the diagnosis of thymoma without prior knowledge of clinical data. Histologic type was classified according to the 2004 revision of the World Health Organization classification of thymic epithelial tumors.20Go Resection status was determined from the operative notes and the pathology reports. R0 and R1 resections were collectively considered as complete macroscopic resections. Incomplete resections were defined as those resections in which gross tumor was left behind (R2 resections).

Disease Assessment, Adverse Events, and Follow-up
Response to preoperative therapy was graded according to the RECIST criteria (Response Evaluation Criteria In Solid Tumors). Partial response was defined as a 30% decrease and progressive disease as a 20% increase in the longest diameter of target lesions.21Go Perioperative adverse events and adverse events arising from adjuvant radiation therapy were identified from the medical record and graded according to the "Common Terminology Criteria for Adverse Events" version 3.0.22Go A significant proportion of patients received their chemotherapy outside of this institution and, therefore, data regarding these treatment-related adverse events were not uniformly available. Dates of death were obtained from the medical record and from the Social Security Death Index (SSDI). Surviving patients were censored at the last update of the SSDI on January 24, 2007. Recurrences were dated from the first postoperative radiographic study that demonstrated recurrent disease. Although there was no strict routine for postoperative follow-up, the most common approach was to obtain serial computed tomographic scans of the chest, generally at 6-month intervals. Patients with no evidence of disease were censored at the date of the most recent radiographic study demonstrating absence of disease.

Statistical Analysis
Survival analysis was performed by the Kaplan–Meier method and was calculated from the date of surgery to the date of death or to the last update of the SSDI. Disease-free survival was determined in only those patients who had undergone complete macroscopic resections and was calculated from the date of surgery to the date of the first radiographic study demonstrating recurrent disease or most recent study demonstrating absence of disease.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Discussion
 References
 
Clinical and Pathologic Data
From January 1996 to December 2006, 18 patients with stage IVA thymoma underwent multimodality therapy including surgery. Patient characteristics are shown in Table 1. The median age was 43.5 years (range 26–74 years). Ten patients were female. The majority of patients were white. The most common presentations were pain or dyspnea, although many patients were free of symptoms. None of the patients had any significant cardiac, pulmonary, or renal disease, but 1 patient had insulin-dependent diabetes. There were no cases of myasthenia gravis at diagnosis, although this disease developed postoperatively in 1 patient, and 1 patient had systemic lupus erythematosus. The histologic classification of the tumors was distributed primarily among the B subtypes with half of the patients demonstrating a component of B3 thymoma.


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  		TABLE 1 Patient characteristics (n = 18 patients)
 
Preoperative Treatment
All 18 patients received preoperative chemotherapy with a platinum-based regimen. Treatment details are noted in Table 2. The majority (n = 10) underwent treatment with PAC (cisplatin, doxorubicin, and cyclophosphamide). Three patients each received VIP (etoposide, ifosfamide, cisplatin), CP (carboplatin and paclitaxel), and 2 were treated with PE (cisplatin and etoposide). One patient taking CP received concurrent radiation. Three patients who failed to respond to initial chemotherapy received additional alternative systemic therapy. There were 12 partial responses and no complete responses, for an overall response rate to chemotherapy of 67%.


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  		TABLE 2 Patient treatment
 
Surgical Management
The surgical management, perioperative treatment, and outcomes are shown schematically in Figure 1. The most common approach used either a hemi-clamshell (n = 8) incision or full clamshell (n = 3) to provide adequate exposure of the mediastinum and pleural space (Table 2). In 2 cases, the clamshell incision was extended with a partial sternotomy for better exposure of the mediastinum and diaphragm. In 3 cases requiring a thymectomy with en bloc EPP, a median sternotomy was performed to mobilize the thymus followed immediately by a posterolateral thoracotomy to resect the lung and pleura. Pleural and parenchymal involvement was most frequently managed with pleurectomy and wedge resections of involved lung. Extensive pleural involvement necessitated EPP in 4 patients, lobectomy in 2 patients, and pneumonectomy and parietal pleurectomy in 1 patient. Local infiltration also necessitated resection of the superior vena cava or innominate vein in 3 patients and chest wall resection in 2 patients. In patients with disease involving the diaphragm, this was resected and the diaphragm either repaired primarily or reconstructed with prosthetic material. Complete macroscopic resection of all tumor was achieved in 12 (67%) patients. Resections were incomplete in the remaining 6 patients. Four of these had near-total resections, in which all of the tumor was removed but minimal residual disease was left behind on either the great vessels or the phrenic nerve. The other 2 incomplete resections left the gross tumor behind owing to tumor invading the heart in 1 case and inaccessible bilateral disease in the other.


Figure 1
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  		Figure 1. Schema showing the preoperative and postoperative treatment, the operations performed, and the outcomes in the 18 patients undergoing surgery for stage IVA thymoma. RT, Radiation; NED, alive, no evidence of disease; AWD, alive with disease; DOD, dead of disease. *One patient also received concurrent induction radiation. **One patient received concurrent chemoradiation postoperatively.

 
Postoperative Treatment
The 4 patients who underwent EPP received adjuvant hemithoracic radiation (4500–5400 cGy). Three additional patients were treated with postoperative mediastinal radiation to the tumor bed alone (3000–5400c Gy). Five patients were treated with additional postoperative chemotherapy. (Table 2) Three patients had postoperative instillation of intrapleural brachytherapy with P32 (10–15 mCi) via an intrapleural catheter placed at the time of the operation.

Immediate and Long-term Outcomes
There were no operative deaths and the 30-day mortality was 0%. The median length of hospital stay was 9 days (range 5–17 days). Perioperative adverse events occurred in 7 (39%) of the 18 patients and are noted in Table 3. The most common events were pulmonary (n = 7), followed by gastrointestinal (n = 2). One patient required vocal cord injection for a temporary laryngeal nerve dysfunction, and 1 patient who had been receiving high-dose corticosteroids required rewiring of an unstable sternum. There was one major complication of an intraoperative cardiac arrest of unknown etiology in a patient who was successfully resuscitated and subsequently discharged from the hospital in 9 days with no sequelae. Adjuvant radiation therapy was well tolerated, with adverse events limited to only grade 1 or 2 skin reactions, nausea, and esophagitis. One long-term adverse event was noted in a long-term survivor (112 months)—radiation-induced breast cancer, which developed 8 years after postoperative hemithoracic radiation.


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  		TABLE 3 Perioperative adverse events *
 
Disease-free and Overall Survival
Among the 12 patients who had a complete macroscopic resection, recurrences developed in 3 patients who had all undergone pleurectomies (5, 65, and 95 months postoperatively). Of the patients with recurrences, all of which were pleura-based, 1 died of disease at 73 months, 1 who had postoperative chemotherapy and intrapleural brachytherapy had 2 re-resections and is alive with disease at 77 months, and 1 who had postoperative radiation is alive with disease at 117 months. One patient with an initially incomplete resection underwent re-resection of the residual disease 3 months postoperatively with a complete macroscopic resection and remains alive with disease at 108 months.

At the time of latest follow-up, 3 of the 18 patients had died at 29, 42, and 73 months. Four patients have survived more than 9 years. The longest survival in this series is 11 years and the patient is free of disease. The overall survival of these patients was 91% at 3 years, 78% at 5 years, and 65% at 10 years (Figure 2). Median survival has not yet been reached. Median follow-up was 32.2 months (range 1.4–129.9 months). Disease-free survival was 90% at 3 and 5 years and 34% at 10 years, with a median disease-free survival of 95 months. The median follow-up for disease status was 22.8 months (range 0.2–108.7 months) (Figure 2).


Figure 2
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  		Figure 2. Overall and disease-free survival.

 

   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
References
 
There are few studies in the literature examining the management of stage IVA thymoma. For thymomas with intrathoracic metastases, the optimal treatment strategy remains undefined. Previous series often have not classified their tumors according to the current World Health Organization histologic scheme and frequently consider stages III and IV together collectively as advanced disease. Series that include patients with stage IV disease may span multiple decades and do not always distinguish between resections for pleural recurrences versus thymomas with pleural involvement at diagnosis. Surgery is considered the mainstay of treatment, but few reports have gone into detail regarding the surgical approaches to advanced thymomas with pleural involvement. In Masaoka’s original report, patients with stage IV disease (including IVA and IVB) had a 5-year survival of 50% and a 10-year survival of 0%.3Go Since then, several series have observed a wide range of survivals for stage IVA disease (Table 4). Our previous series included a smaller number of patients (n = 9) with stage IVA thymomas treated less uniformly over a period of 44 years (1949 to 1993).1Go This earlier experience suggested that multimodality treatment and complete resection were important in achieving long-term survival. We now present a larger contemporary series of patients who had Masaoka stage IVA thymoma at diagnosis, treated more uniformly with multimodality treatment including extended resections with low morbidity, no mortality, and excellent long-term survival.


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  		TABLE 4 Survival of patients with stage IVA thymoma
 
Complete resections can be difficult to achieve in the face of a large mediastinal mass with associated pleural disease. Resectability rates of stage IVA thymomas have been reported to range from 0% to 42% without preoperative therapy.3,17,18Go Induction therapy for advanced thymomas, including stages III and IV, has been advocated by several authors with good clinical response rates and improved resectability rates in the range of 70%.17,19Go Despite the heterogeneity of chemotherapy regimens in our series, all were platinum based. Three patients who failed to respond to initial chemotherapy underwent a second line of treatment, and overall we observed a clinical response rate of 67%, emphasizing that thymomas are sensitive to platinum-based chemotherapy. In a series of 21 stage III and IVA thymomas receiving induction therapy with PAC plus prednisone, Kim and associates15Go reported a complete resection rate of 76%. We obtained comparable results in our series with a 67% complete resection rate in our group of stage IVA thymomas.

We consider an aggressive approach toward surgical resection to be warranted. The management of thymoma with pleural involvement depends on whether the pleural disease is limited or extensive. Our experience suggests that disease limited to scattered pleural metastases can be managed by resection of individual pleural lesions and concomitant pulmonary resections as needed. There are no data regarding the use of complete parietal pleurectomy for these patients. Unlike malignant pleural mesothelioma, in which the disease intrinsically involves the entire pleural surface, metastatic thymoma may be a more limited pleural disease process. In the majority of patients, a hemi-clamshell approach provides optimal exposure of the mediastinum as well as the pleural space.23,24Go

In patients with extensive and confluent pleural disease, an extended resection with EPP is required for complete resection. A median sternotomy followed immediately by en bloc EPP via a posterolateral thoracotomy usually provides the best exposure. Compared with the largest published experience with EPP, our series had less morbidity and no mortality.25Go Our results are comparable with a previously reported small series of EPP for thymoma and add to the literature that suggests aggressive approaches with extended resections are feasible with low morbidity and mortality.26,27Go This may relate to the generally young age and good overall health of patients with thymoma.

High-dose hemithoracic radiation has been shown to be feasible after EPP for mesothelioma and reduces local recurrence rates.28,29Go The absence of the lung in the chest allows delivery of higher doses of radiation without incurring additional toxicity. Drawing from this experience, we have treated all 4 patients who underwent EPP with hemithoracic radiation at a median dose of 5040 cGy. Three other patients received adjuvant mediastinal radiation, 2 in the setting of microscopic diseased margins. There was no major immediate radiotherapy-related toxicity. However, a radiation-induced second malignant tumor in 1 long-term survivor (breast cancer arising on the irradiated side 8 years postoperatively) serves as a cautionary note that all of these patients should be kept under life-long follow-up. The role of adjuvant radiation after pleurectomy and the role of adjuvant chemotherapy remain unclear. Currently no data have been reported regarding the feasibility and efficacy of adjuvant chemotherapy in this setting.

In conclusion, multimodality therapy of stage IVA thymoma incorporating extended resections is feasible and safe with low morbidity and mortality and offers the potential for long-term survival. However, by definition, any retrospective single-institution surgical series will include small numbers of patients who never underwent an operation because induction therapy failed. In addition, there is a need to develop more uniform treatment regimens for this challenging patient population. Our data suggest that prospective multicenter trials in this patient population are warranted to confirm and extend our experience.


Earn CME credits at http://cme.ctsnetjournals.org

 


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Discussion
 References
 

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J. Huang, N. P. Rizk, W. D. Travis, G. J. Riely, B. J. Park, M. S. Bains, J. Dycoco, R. M. Flores, R. J. Downey, and V. W. Rusch
Comparison of patterns of relapse in thymic carcinoma and thymoma
J. Thorac. Cardiovasc. Surg., July 1, 2009; 138(1): 26 - 31.
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Discussion
J. Thorac. Cardiovasc. Surg., July 1, 2009; 138(1): 31 - 31.
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S. Tomaszek, D. A. Wigle, S. Keshavjee, and S. Fischer
Thymomas: Review of Current Clinical Practice
Ann. Thorac. Surg., June 1, 2009; 87(6): 1973 - 1980.
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J. Huang, G. J. Riely, K. E. Rosenzweig, and V. W. Rusch
Multimodality Therapy for Locally Advanced Thymomas: State of the Art or Investigational Therapy?
Ann. Thorac. Surg., February 1, 2008; 85(2): 365 - 367.
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