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Ann Thorac Surg 2002;74:1033-1037
© 2002 The Society of Thoracic Surgeons

Original article: general thoracic

Adjuvant radiation therapy for stage II thymoma

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

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

Accepted for publication May 29, 2002.

* Address reprint requests to Dr Wright, Blake 1570, Massachusetts General Hospital, Boston, MA 02114, USA
e-mail: cdwright{at}partners.org


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. Thymoma is difficult to study because of its indolent natural history. The criteria for administration of adjuvant radiation therapy remain controversial, and it is unclear whether patients with Masaoka stage II thymoma benefit from adjuvant radiation. The goal of this report was to determine whether or not this group benefits from radiation therapy in terms of disease-specific survival and tumor recurrence.

Methods. Case records of the Massachusetts General Hospital were retrospectively reviewed from 1972 to 1999. One hundred fifty-five patients underwent resection for thymoma, of which, 49 had stage II disease. The world literature was reviewed using a Medline search (1966 to 2001), and a secondary review of referenced works was performed.

Results. Fourteen stage II patients underwent radiation therapy. Thirty-five did not receive radiation therapy. Baseline prognostic factors between radiated and nonradiated groups were similar. All patients underwent complete resection. The addition of adjuvant radiotherapy did not significantly alter local or distant recurrence rates in stage II thymoma. Disease-specific survival at 10 years in stage II patients was 100% with radiotherapy and without radiotherapy (p = 0.87). There was one recurrence in the nonradiated group at 180 months, which was outside the usual radiation portal.

Conclusions. Most stage II patients do not require adjuvant radiation therapy and can be observed after complete resection.


   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. These may include inflammatory conditions [1] and synchronous or metachronous malignancies, the incidence of which has been reported to be as high as 31% [2, 3]. The 5-year survival rate for thymoma approximates 60% and has not changed over the past three decades [4–9] despite advances in operative management, radiotherapy, and chemotherapy. Surgery and radiation therapy remain the mainstays of clinical management. Surgery is usually curative for stage I thymoma, and results in 5- and 10-year overall survival rates of over 95% and 80%, respectively [10]. Generally accepted 5- and 10-year overall survival rates for stage II thymoma are 85% and 78%, respectively [10, 11].

The criteria for administering adjuvant radiation therapy to patients with stage II thymoma remain controversial. Current recommendations range from postoperative radiation for all thymoma patients [5, 12–14], to the postoperative radiation of only patients with tumors >5 cm or with radiographic evidence of invasiveness [6]. Despite the absence of a consensus, the standard of care appears to involve radiation of the majority of stage II patients. Often, patients who may 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 terms of local control or survival in patients undergoing operation for stage II thymoma, and to draft guidelines for the judicious use of radiotherapy in this patient population.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
Patient population and follow-up
After approval from the Institutional Review Board, the surgical logs and pathology files at the Massachusetts General Hospital were retrospectively reviewed between 1972 and 1999. One hundred fifty-five patients underwent thymoma resection. Of these, 49 had stage II disease and form the basis for this report. Hospital and office medical records were reviewed, and demographic and tumor-related data were 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. Surgical notes and pathology reports were reviewed by a single surgeon, and patients were staged using the Masaoka classification scheme [15].

Fourteen 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 49 patients, the mean follow-up was 90 months, and ranged from 1 to 336 months. Follow-up was complete in 97% of cases at 5 years, 78% at 10 years, and 70% at 15 years.

Statistical methods
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 {chi}2 test was used to test the distribution of categorical variables, and Fisher’s exact test was used where appropriate. The t test and analysis of variance (ANOVA) were used to compare noncategorical variables.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
The median age at diagnosis was 56 years (range, 13 to 82 years). Twenty-seven (55%) patients were male. Sixteen patients (32.7%) had myasthenia gravis. There were no significant demographic differences between radiated and nonradiated patients.

Surgery was offered as initial treatment to all patients. Seven surgeons performed thymoma resection with total thymectomy via median sternotomy. All 49 patients with stage II disease underwent complete resection, with negative microscopic margins. Fourteen patients (29%) received adjuvant radiation therapy, which was administered according to previously published protocols [10]. Criteria for administration of radiation included invasion of mediastinal fat in seven (50%) cases, invasion of thymic capsule in two (14%) cases, and large tumors in six cases.

Based on the Mueller-Hermelink classification, 23 (47%) patients had medullary type tumors, 19 (39%) patients had cortical tumors, and 7 (14%) had well-differentiated carcinoma. There were no significant differences in Mueller-Hermelink histologic type, tumor volume, capsular or mediastinal fat invasion, or resection status between patients undergoing radiation therapy and those not undergoing radiation therapy (Table 1).


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  		Table 1. Patients With Stage II Thymoma Have Similar Histology, Tumor Volume, Invasiveness, and Resection Status

 
Recurrence rates in stage II thymoma were low, and were not influenced by adjuvant therapy. There were no recurrences among the 14 stage II patients who underwent radiation therapy (recurrence rate, 0%). There was only one pleural recurrence among the 35 stage II patients who did not receive radiation therapy (recurrence rate, 2.9%). This patient underwent complete resection of a small cortical thymoma, which extended into the mediastinal fat. There was no spillage of tumor at time of surgery. She did not receive postoperative radiation therapy, and developed a pleural recurrence 156 months after surgery. After treatment of recurrent disease, she survived an additional 32 months, and died of unrelated causes. Given the small number of recurrences, it is difficult to conclude how effective adjuvant therapy is in controlling recurrent disease in stage II thymoma.

The addition of radiation therapy did not alter overall survival (p = 0.91) or disease-free survival (p = 0.88) in stage II patients at 10 and 15 years. Disease-specific survival at 15 years was 100% in the group receiving radiation, and 84% in the group not receiving radiation (p = 0.87) (Fig 1). There were no radiation-related deaths.



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  		Fig 1. Influence of radiation therapy on disease-specific survival in stage II patients.

 

   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 Mueller-Hermelink histologic classification [16–20]. The prognostic importance of these determinants has been verified in several large studies. Unfortunately, recommendations for the appropriate use of adjuvant radiation therapy for stage II thymoma are wide ranging and controversial. Current recommendations advocate radiation of all patients with stage II thymoma [21], but the grounds for such a recommendation are unclear. As awareness of the late complications of radiation therapy to the chest is growing (such as hematopoietic malignancies, esophageal malignancies, dysmotility, and strictures; radiation pneumonitis and chronic pulmonary fibrosis; and cardiac disorders such as cardiac valve fibrosis, pericardial effusions, and accelerated coronary artery disease increase [22–30]), we feel that revisiting the issue of radiation for patients with stage II thymoma is timely and essential. A consensus is made difficult by the indolent natural history of this disease, and by the deaths of large numbers of patients due to unrelated causes, as a result of which, the use of overall survival data in earlier studies falsely lowers survival rates for thymoma, and can be circumvented by the use of disease-specific survival rates, as in this report.

We reviewed six papers in which at least 10 stage II patients were studied, and in which patients both received and did not receive adjuvant radiation therapy after complete resection, thus enabling a comparison between the two groups. Five of six papers [6, 11, 31–33] were unable to demonstrate an advantage to radiation therapy in terms of local control or survival (Table 2). The recurrence rates ranged from 19% to 31% after radiation (median 22%), and ranged from 4% to 45% (median 23%) without radiation. These differences did not reach statistical significance, except in a paper by Ruffini and associates [33], who demonstrated a significant advantage to not receiving adjuvant radiation (p = 0.02). In our study, patients receiving radiation had a recurrence rate of 0%, and those not receiving radiation had a recurrence rate of 2%, both significantly lower than those reported in the literature. A single recurrence made statistical analysis about the ability of radiation therapy to prevent recurrence difficult. However, because stage II disease is usually amenable to complete resection (all patients with stage II disease were completely resected in this series), has a very low rate of recurrence (2%), and because tumor behavior is indolent (the single recurrence came to our attention 13 years after surgery, and the patient died of unrelated causes 3 years after treatment), we do not recommend adjuvant radiation therapy as a means to prevent local recurrence for this group of patients. We believe that stage II, like stage I thymoma, is primarily a surgical disease, and patients should be followed with a serial physical and radiological examination for the remainder of their lifetimes. Curran and associates [7] are the only authors who have reported local recurrence in 8 out of 18 stage II patients not receiving radiation therapy, as opposed to zero recurrences in the only stage II patient receiving radiation. It is on the basis of this observation that they recommend adjuvant radiation therapy to all patients with stage II disease. It should be noted that statistical analyses were not possible due to the single patient in the no-radiation arm, that all-cause mortality in stage II thymoma was much higher than that generally reported in the literature (5-year survival rate of 53% compared with 5-year survival over 90%), and that they conclude that selection, physician, and time bias may have influenced the conclusions for radiation therapy in this population.


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  		Table 2. Review of the Literature Discussing Adjuvant Radiation Therapy for Stage II Thymoma

 
None of the six papers reviewed (including that of Curran and associates) [6, 7, 11, 31–33] demonstrated a correlation between adjuvant radiation therapy and an increase in overall, disease-free, or disease-specific survival. Furthermore, no study to date has undertaken a subgroup analysis of survival in stage II patients with and without radiation therapy. In this report, we were unable to document a survival advantage (overall, disease-free, or disease-specific) with the addition of radiation therapy to the surgical management of patients with stage II thymoma, therefore causing us to reiterate our belief that stage II thymoma treated by experienced surgeons is primarily a surgical disease.

There are several limitations of our study. The first is the retrospective nature of this consecutive case series, in which treatment was not by protocol. The second is that 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; and how the surgeon felt about the procedure (surgeon’s bias); and the patient’s willingness to undergo and ability to tolerate radiation. However, major prognostic factors such as histologic criteria, invasiveness, completeness of resection, and tumor volume 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, with improvements in surgical and anesthetic technique, postoperative care, radiation therapy, and management of myasthenia gravis, favoring patients who were treated later. Fourth, follow-up at 10 years was only 78% complete. However, major prognostic factors such as histology, tumor volume, invasiveness, and completeness of resection were evenly distributed (p = NS) between patients who were seen at 10-year follow-up and those that were lost to follow-up. 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 concordant with those reported in the literature, and may have reached statistical significance if the cohort were larger. However, this being an unusual disease, it is difficult to fashion a large, prospective randomized trial.

In summary, in the hands of experienced surgeons, at high-volume centers, stage II thymoma is invariably amenable to complete resection. Regardless of tumor size, histology, or invasion of mediastinal fat or thymic capsule, there may not be a need for adjuvant radiation therapy, as it has little influence on local control, and has no influence on long-term, disease-specific survival. If treated in this way, patients can be followed by serial radiographs, and can be spared the potential sequelae of mediastinal irradiation.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

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