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Ann Thorac Surg 2005;79:1834-1839
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Adjuvant Radiation of Stage III Thymoma: Is It Necessary?

Abeel A. Mangi, MD, John C. Wain, MD, Dean M. Donahue, MD, Hermes C. Grillo, MD, Douglas J. Mathisen, MD, Cameron D. Wright, MD*

General Thoracic Surgical Unit, Department of Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts

Accepted for publication December 28, 2004.

* Address reprint requests to Dr Wright, Blake 1570, Massachusetts General Hospital, 55 Fruit St, Boston, MA02114 (E-mail: wright.cameron{at}mgh.harvard.edu).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: The criteria for administration of adjuvant radiation therapy after thymoma resection remains controversial, and it is unclear whether patients with Masaoka stage III thymoma benefit from adjuvant radiation. The goal of this report was to determine whether or not this group benefits from radiation therapy in disease-specific survival and disease-free survival.

METHODS: Case records of the Massachusetts General Hospital were retrospectively reviewed from 1972 to 2004. One hundred and seventy-nine patients underwent resection for thymoma, of which 45 had stage III disease.

RESULTS: Forty-five stage III patients underwent resection and in 36 it was complete. Thirty-eight stage III patients received radiation therapy. Baseline prognostic factors between radiated and nonradiated groups were similar. The addition of adjuvant radiotherapy did not alter local or distant recurrence rates in patients with stage III thymoma. Disease-specific survival at 10 years in stage III patients who did not receive radiation was 75% (95% confidence interval, 32% to 100%) and in patients who did receive radiation therapy it was 79% (95% confidence interval, 64% to 94%) (p = 0.21). The most common site of relapse was the pleura.

CONCLUSIONS: Most patients who have stage III thymoma undergo complete resection. Some patients enjoy prolonged disease-free survival without adjuvant radiation after resection of stage III thymoma. Radiation does not seem to prevent pleural recurrences when given after resection of stage III thymomas. The use of routine adjuvant radiation after a complete resection of stage III thymoma needs to be re-addressed. There may be a role for the use of chemotherapy to reduce pleural recurrences.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Thymoma is a difficult condition to study because of its rarity, indolent natural history, and high mortality due to unrelated causes [1–3]. The 5-year survival rate for thymoma approximates 60% and has not changed over the past 3 decades [4–9] despite advances in operative management, radiotherapy, and chemotherapy. Surgery remains the mainstay of clinical management. Generally accepted 5-year and 10-year overall survival rates for stage III thymoma are 60% to 80% and 50% to 75%, respectively [10, 11].

There is no consensus statement nor randomized trial data to support the use of adjuvant radiation therapy in the care of patients with stage III thymoma. The current standard of care appears to involve adjuvant radiation for the majority of stage III patients, but the criteria for administering adjuvant radiation therapy to patients with stage III thymoma vary from institution to institution and are controversial. Currently, postoperative radiation is offered either to all thymoma patients [5, 12–14], to those with invasive features on pathologic examination of the specimen, or to patients with tumors greater than 5 cm in size [6]. It may be that patients who do not require radiation will receive it, unnecessarily subjecting them to the risks of that modality.

The aim of this study was to investigate whether or not the addition of adjuvant radiotherapy confers an advantage in local control or survival in patients undergoing operation for stage III thymoma, and to discuss the judicious use of adjuvant and neoadjuvant therapy in this patient population.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
After approval from the Institutional Review Board, the surgical logs and pathology files at the Massachusetts General Hospital were retrospectively reviewed between 1972 and 2004. One hundred and seventy-nine patients underwent thymoma resection; of these, 45 had stage III disease, which forms the basis for this report. Hospital and office medical records were reviewed, and demographic and tumor-related data entered into a computerized database. Patient follow-up was obtained by review of hospital and office records; telephone interviews with patients, family members, or physicians; and written questionnaires from the Department of Vital Statistics. Two surgeons reviewed surgical notes and pathology reports, and patients were staged using the Masaoka classification scheme [15].

Patients were referred for radiation therapy if microscopic positive margins were found on final pathologic examination, if there was gross evidence of residual tumor at the time of operation, if a patient was referred to a radiation oncologist carrying the label of "stage III disease," or based on the clinical intuition of the treating surgeon and the surgeon’s belief of how the operation "went." Thirty-eight patients received radiation therapy (median, 4,550 Gy; standard error, 188 Gy; range, 3,000 to 6,100 Gy). Survival was calculated from the date of operation. Treatment-related deaths (postoperative or radiation related) were counted as death from thymoma. Time to recurrence (disease-free survival), time until death from thymoma (disease-specific survival) and time until death from any cause (overall survival) were recorded for all patients. Disease-specific survival was censored if patients died from nonthymoma-related causes. In this series of 45 patients, the mean follow-up was 94 months, which ranged from 2 to 268 months. Two patients were lost to follow-up at 2 and 12 months after operation. Follow-up was complete in 96% of the patients at 10 years. The Kaplan-Meier method was used to estimate the time to relapse or death. The log rank test was used to compare survival between groups. The two-group chi2 test was used to test the distribution of categorical variables, and the Fischer exact test was used when appropriate.


   Results
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 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
The mean age at diagnosis was 58 years (range, 18 to 21 years). Twenty-eight patients (62%) were female. Thirteen patients (36%) had myasthenia gravis. Thirty-eight patients (84%) received adjuvant radiation therapy, which was administered according to previously published protocols [10]. There were no significant demographic differences between radiated and nonradiated patients (Table 1).


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  		Table 1. Tumor Characteristics
 
Surgery was offered as initial treatment to all patients. Thymoma resection was performed through a median sternotomy and involved total thymectomy with en bloc resection of involved structures in all patients. Thirty-six patients with stage III disease underwent complete resection with negative microscopic margins. Nine patients were not amenable to complete resection; of these, 6 had large tumors (> 10 cm) involving unresectable structures. The World Health Organization pathology in the unresectable patients was B1 in 1 patient, B2 in 1, and B3 in 7. Radiation was administered after operation for incomplete resections and generally based on the belief that it was needed in stage III thymomas. Completeness of resection did not influence locoregional recurrence (p = 0.33) or death from thymoma (p = 0.37). Based on the World Health Organization histologic classification, the distribution of tumor types was as follows: A-1, AB-1, B1-3, B2-8, B3-28, and C-4. There were no significant differences in the World Health Organization histologic type, types of structures invaded, number of large tumors (> 10 cm) or resection status between patients undergoing radiation therapy and those not undergoing radiation therapy (Table 1).

There were 14 recurrences in patients with stage III thymoma. Of the 38 patients that received radiation therapy, 12 recurred (recurrence rate, 32%), and of the 7 patients that did not receive radiation therapy, two recurred (recurrence rate, 29%). This difference did not reach statistical significance, suggesting that the choice of adjuvant therapy did not influence outcome (p = 0.87). Recurrences were either pleural or distant. Of the 12 patients with pleural recurrences, 10 had undergone radiation therapy and 2 had not. The mean time to recurrence was 40 ± 23 months in the group receiving radiation therapy and 87 plusmn; 10 months in the group not receiving radiation. This difference was statistically significant (p = 0.033). Time to death after detection and treatment of recurrent disease (median, 31 months) in both groups was not statistically significant. Three patients had distant metastases (bone, brain, liver) develop during a median of 26 months after initial therapy. These 3 patients had undergone radiation therapy after initial operation. Survival after detection of distant disease was only 5 months.

The addition of radiation therapy did not alter overall survival at 10 years, which was –54% with radiation therapy (RT) (95% confidence interval [CI], 36% to 71%), and 43% without RT (95% CI, 6% to 80%) (p = 0.41). Disease-free survival at 10 years was 64% with RT (95% CI, 44% to 83%), and 60% without RT (95% CI, 17% to 100%) (p = 0.21). Disease-specific survival at 10 years was 79% in the group receiving RT (95% CI, 64% to 94%), and 75% in the group not receiving RT (95% CI, 32% to 100%) (p = 0.21) (Fig 1). A repeat analysis was performed that excluded the 9 patients who had incomplete resections, and again there was no difference in disease-specific survival at 10 years (75% without RT and 82% with RT; p = 0.40). There was 1 radiation-related death due to radiation pneumonitis.



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  		Fig 1. Influence of radiation therapy on disease-specific survival in stage III patients. The numbers of patients at risk at selected time intervals are seen at the bottom of the survival curve. (RT = radiation therapy.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
The most important determinants of long-term survival in thymoma are completeness of resection [11], Masaoka stage [15], and the World Health Organization histologic classification [16–20]. The prognostic importance of these determinants has been verified in several large studies. Despite the evenly balanced prognostic factors in our two treatment groups, we could not demonstrate an advantage to adjuvant RT in stage III thymoma. Most centers consider the addition of postoperative radiation therapy as the standard of care for stage III thymoma patients, and would recommend the routine referral of these patients for adjuvant radiation therapy [10, 21]. The basis for this recommendation is unclear.

Radiation therapy to the chest is not benign. Several reports of late consequences such as hematopoietic malignancies, esophageal malignancies, dysmotility and strictures, or radiation pneumonitis and chronic pulmonary fibrosis [22–30] have emerged. In addition, a recent study has detailed a variety of late postradiation injuries to the heart that include entities such as restrictive cardiomyopathy, cardiac valve fibrosis, conduction defects (manifested by monotonous heart rate, persistent tachycardia, and blunted hemodynamic responses to exercise), pericardial effusions, reduced peak oxygen uptake during exercise (an independent predictor of premature death), and accelerated coronary artery disease [31]. Given the potential for serious consequences from radiation therapy, a policy of selective radiation therapy for patients with stage III thymoma should be considered. A consensus on this subject is made difficult by the indolent natural history of this disease, and by the large numbers of patient deaths from unrelated causes. These reasons also make a prospective randomized study investigating the possible benefits of radiation therapy as unlikely to ever be undertaken.

In order to ascertain the role of radiation therapy in the management of stage III thymoma, we reviewed seven articles in which at least 10 stage III patients were studied and in which patients both received and did not receive adjuvant radiation therapy after complete resection. We then compared the two groups. Six of the seven authors (Table 2) [6, 11, 32–35] were unable to demonstrate any advantage to adjuvant radiation therapy in terms of either local control or survival. Local recurrence rates ranged from 19% to 31% after radiation (median, 22%) and from 4% to 45% without radiation (median, 23%). These differences did not reach statistical significance, except in the study by Ruffini and colleagues [34] who demonstrated a significant advantage to not receiving adjuvant radiation (p = 0.02). Curran and colleagues [7] reported local recurrences in 8 of 18 stage III patients not receiving radiation therapy, as opposed to zero recurrences in the only stage III patient receiving radiation, and they recommended routine adjuvant radiation therapy on the basis of this observation. However, it should be noted that statistical analyses were not possible due to the single patient in the no-radiation arm, and that all-cause mortality in stage III thymoma was much higher than that generally reported in the literature (5-year survival rate of 53% compared with 5-year survival >90%).


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  		Table 2. Review of the Literature Discussing Adjuvant Radiation Therapy for Thymoma
 
In our study, disease-specific survival at 10 years was 79% in the group receiving radiation and 75% in the group not receiving radiation (p = 0.21) (Fig 1). Patients receiving radiation had a recurrence rate of 32%, and those not receiving radiation had a recurrence rate of 29%, similar to those reported in the literature. This difference did not reach statistical significance. Because the recurrence rate is not influenced by the addition of radiation therapy, and because the majority of patients with stage III disease can safely undergo complete resection (complete resection rate, 80% in this series), it is difficult to recommend the routine use of postoperative radiation for patients with stage III disease who undergo complete resection. Radiation therapy has a role for patients who could not possibly have a complete resection, and it may have a role for patients whose surgeon suspected a close margin. Such a paradigm has been established and followed for most intrathoracic neoplasms [36], but is difficult to prove in our small group of patients. Stage III patients may also benefit from a cisplatin-based course of adjuvant chemotherapy because most recurrences are pleural rather than mediastinal.

One group of patients that may benefit from neoadjuvant therapy is the group who displays clear evidence of invasion of adjacent structures by bulky tumors on preoperative imaging. Neoadjuvant radiation therapy as outlined by Myojin and colleagues [10] may be of benefit in downsizing the tumor and enhancing resectability, although there is scant data from other reports to support the use of radiation therapy in this setting. The decision to proceed with a neoadjuvant regimen needs to be undertaken by the treating physician on a case-by-case basis. If review of the preoperative imaging does not remove doubts about resectability, computed tomographic-guided core needle biopsy, an anterior mediastinotomy, and open biopsy or video-assisted thoracoscopic examination of the chest should be undertaken for diagnosis. Care must be taken at that time not to disturb tumor planes in order to prevent widespread pleural dissemination. If pleural disease is present, or if tumor planes are disrupted at the time of operation, there may be a benefit to intrapleural administration of platinum-based chemotherapeutic agents that have been reported to be useful in thymic tumors with pleural spread [37]. We do not favor routine video-assisted thoracoscopic biopsy of advanced thymomas for fear of causing pleural dissemination. We find the video-assisted approach most useful to document stage IVA pleural disease.

A neoadjuvant chemotherapy strategy for patients with stage III thymoma that appears to hold promise has recently been described by Venuta and colleagues [38]. This group has prospectively described a regimen of induction chemotherapy including cisplatin (50 mg/m2), adriblastin (50 mg/m2), and cyclophosphamide (500 mg/m2) administered three times every 3 weeks in which treatment was made by protocol. Ninety-three percent of patients successfully completed therapy. One patient demonstrated complete remission (7%), 2 had a complete response (13%), 8 had partial responses (53%), and 5 had stable disease (33%). Twenty percent of patients were downstaged to stage II, and 67% of patients initially believed to be unresectable were rendered resectable by the administration of neoadjuvant chemotherapy. Unresectable patients and resected patients were referred for chemoradiation therapy. The administration of neoadjuvant chemotherapy improved 10-year survival from 71% (no induction therapy) to 90%, but this did not reach statistical significance. Therefore a combined neoadjuvant approach with both chemotherapy and radiation therapy probably deserves further analysis in a prospective fashion and may be best undertaken in a multicenter investigation given the rarity of this disease.

There are several limitations of our study. First, the retrospective nature of this consecutive case series for treatment was not made by protocol. Second, there may have been case selection bias in which patients with larger, more aggressive tumors were stratified to receive radiation based on subjective criteria (such as the in situ appearance of the tumor), based on how the surgeon felt about the procedure (surgeon’s bias), and based on the patient’s willingness to undergo the procedure and the patient’s ability to tolerate radiation. However, major prognostic factors such as histologic type, invasiveness, completeness of resection, and tumor size were distributed evenly between the two groups. Third, as this study spans almost 30 years, an element of time selection bias may also influence the results due to improvements in surgical and anesthetic technique, postoperative care, radiation therapy, and management of myasthenia gravis, which favors patients who were treated more recently. Finally, the sample size is small, and the inability to demonstrate a survival advantage may represent an inability to reject the null hypothesis (type II error). However, the observations made in this study are in concordance with those reported in the literature.

In summary, in the hands of experienced surgeons, stage III thymoma is largely amenable to complete resection. Regardless of tumor size, histology, or invasiveness, there is a questionable role for routine adjuvant radiation therapy after complete resection as it has little influence on local control and long-term disease-specific survival. If treated in this way, patients can be followed-up by serial computed tomographic scans and can be spared the potential sequelae of mediastinal irradiation. There may be a role for neoadjuvant chemotherapy treatment of large and obviously invasive clinical stage III tumors, or both, or the adjuvant treatment of resected stage III tumors with chemotherapy given that the most common site of relapse is the pleura.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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