Ann Thorac Surg 2002;73:1076-1081
© 2002 The Society of Thoracic Surgeons
Original article: general thoracic
Primary thymic carcinoma
Hung-Chang Liu, MDa,e,
Wen-Hu Hsu, MD*e,
Yu-Jen Chen, MDc,d,
Yu-Jan Chan, MDb,d,
Yu-Chung Wu, MDe,d,
Biing-Shium Huang, MDe,d,
Min-Hsiung Huang, MDe,d
a Divisions of Thoracic Surgery, Taipei, Taiwan
b Pathology, Taipei, Taiwan
c Oncology, Mackay Memorial Hospital and Taipei Veterans General Hospital, Taipei, Taiwan
d Divisions of Surgery, Taipei Medical University, Taipei, Taiwan
e Yang-Ming University, Taipei, Taiwan
Accepted for publication December 4, 2001.
* Address reprint requests to Dr Hsu, Division of Thoracic Surgery, Taipei Veterans General Hospital, #201, Sec 2, Shei-Pai Rd, Taipei 112, Taiwan
e-mail: hcliu23{at}hotmail.com
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Abstract
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Background. Thymic carcinoma is a malignancy of the anterior mediastinum, always with poor prognosis. Up to the present, very few articles have discussed and evaluated either the clinical or pathologic features or treatments of this tumor. Therefore, we are in a position to analyze our research data to support our belief as follows.
Methods. From January 1977 until December 1997, we received 614 patients who were diagnosed with anterior mediastinal tumors. Of the 614 patients, 38 patients (6.2%) were diagnosed with thymic carcinoma, including 26 men and 12 women. Data were collected from clinical records and personal interviews with the patients. Classification of these patients’ tumor stages was based on the Masaoka staging system.
Results. We proceeded with surgery for 15 of the 38 patients to remove their tumors. Complete resection was done in 8 of these 15 patients (21.0%), whereas debulking was done in the other 7 (18.4%) patients. The mean survival time of all the patients in this study (excluding 3 patients who were lost to follow-up) was 53.0 months, with a median of 24.1 months. The overall cumulative survival rate was 38.6% at 3 years and 27.5% at 5 years. The data in this research show that tumor grading (p = 0.01), resectability (p = 0.02), and stage (p = 0.04) have statistically significant influence on patients’ survival.
Conclusions. The grade, stage, and resectability of the tumor are decisive factors of the effectiveness of either surgery or chemo/radiotherapies in the treatment of thymic carcinoma.
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Introduction
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Among anterior mediastinal tumors, thymic carcinoma is relatively rare. For most physicians, the clinicopathologic behaviors of thymic carcinoma are often confused with thymoma because of its heterogeneous histology and rarity. Thymic carcinoma has a different histology from thymoma. However, it is often difficult to differentiate them. Thymic carcinoma was first classified by Levine and Rosai [1], who included it as a type II malignant thymoma. Although the characteristics of thymic carcinoma have been sporadically reported, very few large series have discussed its treatments and prognosis in detail. We retrospectively reviewed 38 consecutive patients who were diagnosed with thymic carcinoma by either tumor resection or biopsy. In this article, these patients’ clinical behaviors, histologic entities, prognostic factors, treatments, and survival conditions are analyzed and discussed.
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Material and methods
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From January 1977 until December 1997, we managed 614 patients who had received anterior mediastinal surgery. Thirty-eight patients were diagnosed as thymic carcinoma according to the 1978 criteria of Snover and associates [4]. After the confirmation of the mediastinal abnormality, all 38 patients received surgical interventions followed with or without chemotherapy, radiotherapy, or both chemotherapy and radiotherapy.
We would like to clarify that, in this study, all equivocal cases between thymoma and thymic carcinoma were excluded. In the pathologic confirmation of thymic carcinoma, it must be proven to have a malignant cytology. All of our patients’ pathologic diagnoses were conducted by our pathologists, all of whom had at least 5 years of pathologic experience. To classify and make a comparison of the types of surgeries, we decided that: (1) tumor resection must be completely done, grossly and microscopically; (2) debulking surgery means that the tumor has been removed as much as possible, usually at least more than two-thirds of the tumor; and (3) the other cases were delegated in the biopsy group, including cases of partial resection.
As to the surgical approach of the tumors, it is rather complex. Basically, it depends on the tumor location and invasiveness, individual factors (eg, previous chest surgery or infection history), and performance status. For operable cases, median sternotomy is usually a favorable option among the surgeons, except when the tumors are suspected to have invaded the pulmonary trunk, in which case, thoracotomy would be performed (Fig 1).
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Fig 1. Surgical approaches for debated stage III cases. (A) The tumor invades the major central vessels with more than half of circumferential encasement and pericardial effusion. The case received Chamberlin open biopsy. (B) The tumor, located at the left side, with partial invasion to the left pulmonary trunk in roentgenography, is considered operable before operation. However, if, after thoracotomy, the tumor invades the pulmonary trunk and aorta, the resection becomes impossible. Then, biopsy is to be done. (C) Although the tumor, located at the right side, invades the mediastinal vital structure, sternotomy is done for resection of the tumor.
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We outline the stages of the tumors according to the Masaoka system [2] (Table 1).
In this study, tumor grading was based on cell differentiation, which was modified from Suster and Rosai’s classification system [3]. Carcinoid tumors, well-differentiated (keratinizing) squamous cell carcinoma, and mucoepidermoid carcinoma were delegated to low-grade tumors, and all other types were classified as high-grade tumors.
Twenty-seven out of the first 35 survived patients (77.1%) received postoperative radiotherapy with tumor doses from 4,000 to 6,500 cGy. Thirteen out of those 35 patients received cisplatin-based postoperative chemotherapy with regimens, including fluorouracil, leukovorin, etoposide, bleomycin, endoxan, mitomycin, tamoxifen, and interferon. Among the 35 studied patients, 10 of them received both postoperative radiotherapy and chemotherapy.
For this research, the statistical analysis and survival comparisons were done by the SPSS/PC+ Advanced Statistics 7.0 software package for microcomputer data management and analysis developed in 1995 by SPSS Inc (SPSS, Inc, Chicago, IL). Survival analysis is estimated with the Kaplan-Meier methods. The survival period of time is calculated beginning with the date of thoracotomy or when definite diagnosis was established. Category variables are compared for survival differences by log-rank test, and the difference in survival time is considered significant if the p value was less than 0.05.
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Results
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Our patient group included 26 men and 12 women. Their ages ranged from 28 to 80 years, with an average of 55 years. Of the 38 patients, 20 patients were still alive at the end of our research period and 3 patients were lost track of during the follow-up period. One of those 3 patients (stage II with complete tumor resection) moved to another city and we failed to locate the other 2 patients (both stage IVb) 5.1 months and 15 months after surgery. All these 3 patients were excluded in the subsequent survival analysis.
The cytologic classifications of the tumors were 20 epidermoid carcinoma, eight poorly differentiated carcinoma, five carcinoid tumors, one clear cell carcinoma, one small cell carcinoma, one adenocarcinoma, one neuroendocrine carcinoma, and one mucoepidermoid carcinoma. Three (7.9%) out of the 38 patients with thymic carcinoma were diagnosed to have myasthenia gravis. The clinical features of these patients are listed in Table 2.
Staging
Among the 38 patients, 1 patient had stage I cancer, 2 had stage II, 13 had stage III, 13 had stage IVa, and 9 had stage IVb cancer. Figure 2
shows the cumulative survival curve of the patients according to the modified Masaoka staging system. Neither surgical mortality nor morbidity was found in these patients. The tumor sizes of the patients ranged from 4.0 to 15.0 cm, with an average of 7.0 cm. In 17 patients, the tumors were located on the right side; in 13 patients, the tumors were located on the left side; the tumor locations were unidentifiable in 8 patients (due to undistinguishable distribution of the tumor on either side of the thorax from roentgenography and surgerys). All of the stage III operable patients, receiving tumor resection or debulking and adjuvant therapy, were still alive at the time of the last follow-up (Table 3).
The median survival times for stage IVa and IVb disease were 23.3 and 14.0 months, respectively. Stage III and stage IV shows significant difference in survival (p = 0.04), whereas IVa and IVb do not (Fig 2).
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Fig 2. Cumulative (Cum) survival time for different stages of thymic cancer. Stage III (n = 13) and stage IV (n = 13 for a, n = 7 for b) have significant difference, but no difference is found between stages IVa and IVb.
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Grading
Figure 3
shows the survival curve for different tumor grades. Among the 35 patients, 23 patients had low-grade tumors and 12 patients had high-grade tumors. Tumor grades influenced the prognosis of the patients, with statistical significance (p = 0.01). All patients with carcinoid tumors were alive after surgery, no matter with resection or not (Table 4).
The median survival time for low- and high-grade tumors was 41.1 and 17.3 months, respectively.
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Fig 3. Cumulative (Cum) survival time according to tumor grading, which is of statistical significance for the grading of the tumor histology.
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Operability
Eight of the 38 patients had complete resection of the tumor and 7 patients received debulking surgery (Table 5),
whereas 23 patients received either partial resection or open biopsy (either because the tumor was too large to be resected or because there were multiple seedings of the tumors). The patients were tracked for 1 to 141 months of follow-up, with an average of 24.8 months. The overall median and average survival time of our patients was 24.1 and 53.0 months, respectively (Fig 4).
The 3-year and 5-year survival rate of our patients was 38.6% and 27.5%, respectively.
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Fig 4. Cumulative (Cum) survival curves of 35 patients with thymic carcinoma. The median survival time was 24.1 months.
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Tumor resection has a significantly positive effect for patients, although the successful resection rate was not high (21.0%). The median survival time for patients with complete resection of the tumor is 35.0 months. Resectability has a statistical significance for the prognosis (Fig 5).
In contrast, debulking surgery does not prolong the survival period of the patients. In the incomplete resection group, the median survival time for debulking surgery and biopsy is 25 and 17.4 months, respectively.
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Fig 5. Cumulative (Cum) survival time according to type of surgery in patients with thymic carcinoma. Complete resection (n = 7) had statistical significance, but there was no difference between debulking surgery (n = 7) and biopsy (n = 21).
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On the other hand, adjuvant chemotherapy and radiotherapy for patients receiving partial resection or biopsy show that neither radiotherapy nor chemotherapy benefits the patients. There were a total of 35 patients observed for survival analysis. Twenty-one out of these 35 patients received biopsy. Their breakdowns are as follows: (1) 4 out of the 21 patients who received biopsy refused any form of treatment (neither chemotherapy nor radiotherapy). Their median survival time was 4.1 months. (2) Six out of the 21 patients who received biopsy accepted only radiotherapy. Their median survival time was 14.0 months. (3) Three out of the 21 patients who received biopsy accepted only chemotherapy. Their median survival time was 21.4 months. (4) Eight out of the 21 patients who received biopsy accepted both chemotherapy and radiotherapy. Their median survival time was 17.3 months.
The median disease-free interval of our patients after the first treatment was 17.2 months. Fifteen patients died at the end of this study. Three patients died of complication of adjuvant therapy. Two of these 3 died of radiation pneumonitis during the therapeutic period. The other patient died of heart failure, caused by the pericardial effusion, after chemotherapy. Twelve patients (80%) died of tumor metastasis. Two of these 12 patients expired during the follow-up period. One had a myocardial infarction 15 months after a series of treatments for the tumor, while the other patient suffered from traumatic intracranial hemorrhage and eventually died 35 months after tumor resection. The sites of patients with distant metastasis are listed in Table 6.
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Comment
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There are few articles that have dealt with thymic carcinoma. Snover and associates [4] were the first ones to classify the kinds of thymic carcinomas. Traditionally, thymic carcinoma was reported with only nine major variants because of its different histology: squamous cell, lymphoepithelioma-like, undifferentiated, small cell/neuroendocrine, basaloid, mucoepidermoid, clear cell, sarcomatoid, and mixed undifferentiated-small carcinomas [3–5]. However, another two rare subtypes of thymic carcinoma have been discovered. One is thymic adenocarcinoma and the other is thymic carcinoid tumor. From articles published, there have only been two in English that discussed thymic adenocarcinomas [6, 7]. Malignant transformation and differentiation from cystic lesion in the thymus were thought to be the common cause of thymic adenocarcinoma. Whether thymic carcinoid tumor belongs to thymic carcinoma or neuroendocrine tumor is still controversial. However, for this research, we included thymic carcinoid tumors in thymic carcinoma because several previous articles [8, 9, 26] had also provided strong evidence to support that thymic carcinoid tumor was one of thymic carcinomas. Thus, there are currently 11 variants for thymic carcinoma.
As for thymic tumorigenesis, the concept of the multipotential stem cell has been presented [4, 8, 10, 11]. It describes that no matter what kind of thymic carcinoma it is, it is from the same precursor cell. The concept was interpreted by the evidence of the coexistence of two or more mixed histologies with clear-cut areas of transition between either component within the same tumor mass. One kind of multipotential stem cell appeared to have diverse transformation during carcinogenesis. Through a series of events, biphasic differentiation or dedifferentiation, it develops later into two separated but related categories of tumors. Usually, thymic carcinoma can be classified into nonendocrine carcinoma and endocrine carcinoma.
A definite preoperative diagnosis of a mediastinal tumor is difficult. It is unlike any luminal tumor (bronchogenic or alimentogenic) can be approached by endoscopic instruments. In contrast, the mediastinal tumor is located in a completely shielded body cavity, the anterior mediastinum. Unless the tumor is large enough, it is difficult to be detected clinically and preoperatively. That is why the mediastinal tumor is often diagnosed in an advanced stage. In addition, when a tumor is large enough for biopsy, the precise origin of the tumor is difficult to be clearly determined. Thymic carcinoma is difficult to be microscopically distinguished from lymphoma, sarcoma, seminoma, or embryonic carcinoma. However, with the improvement of immunohistochemical techniques, a mediastinal tumor can be diagnosed, with more accuracy, to be of thymic origin before operation. Thymic carcinoma is immunoreactive to epithelial membrane antigen, neuron-specific enolase, CD5, synaptophysin, and cytokeratin, but is not reactive to 
-fetoprotein, ß-human chorioembryonic gonadotropin, placental alkaline phosphatase, or common leukocyte antigen [9, 12, 13].
The paraneoplastic syndrome of thymic carcinoma rarely has been reported. Thymic carcinoid associated with Cushing’s syndrome has been reported because of the production of adrenocorticotropic hormone [17, 18]. Myasthenia gravis is one of the paraneoplastic syndromes of thymoma [15]. It is widely known to specialists that about 30% of patients with thymoma have concurrent myasthenia gravis. Based on this study, 7.8% of patients with thymic carcinoma were associated with myasthenia gravis. All were squamous cell carcinoma. Verley and Hollmann [16] once reported four cases of type IV thymoma with concomitant myasthenia gravis. Marino and associates [17] presented a case of thymic carcinoma with myasthenia gravis. The frequency of thymic carcinoma with myasthenia gravis is less than that of thymoma. Two (40%) of our patients with thymic carcinoid were found to have symptoms of cutaneous and gastrointestinal manifestations of carcinoid syndrome. This condition had not been found in any previous reports.
The prognosis of thymic carcinoma is worse than that of thymoma. The overall 3- and 5-year survival rates in our study were 38.6% and 27%, respectively. The median survival time was 24.1 months. This result is better than that in the report of Wick and associates [8], similar to that of Hsu’s report [9], but worse than that in the report of Blumberg and associates [19]. Regarding the survival time of thymic carcinoma, one recent report by Chung’s collection [27] has included 13 articles about the survival rate of thymic carcinoma. The average median survival time of these articles is 24 months. In these articles, because of the different stages in which the patients were diagnosed, the survival rates reported by the authors varied. Furthermore, the main concept of the result signifies that early diagnosis and complete resection of the tumor are the best treatment for the patients. According to different histology, our patients with carcinoid tumors have the top survival rate, whereas those with squamous cell carcinoma and mucoepidermoid carcinoma have the second highest. Most of the patients with other thymic carcinomas die within 3 years. Tumor grades significantly influence the survival time.
Clinically, compression to the mediastinal vital structures and invasiveness of the tumors on computed tomography are both more severe in thymic carcinoma than in thymoma [8, 17]. Most (92.1%) patients with thymic carcinoma are diagnosed at an advanced stage (stage III or IV). Pleura, innominate vein, pericardium, and lung are most commonly invaded by tumors. Locoregional lymph node invasion is always found in patients with thymic carcinoma.
Treatment for thymic carcinoma has rarely been mentioned because of the limited number of the cases. Complete resection (21.0%) of the thymic carcinoma is not very often done in our cases. Debulking surgery was done in 18.4% of our patients. Other patients were managed by partial resection or biopsy, either because resection was impossible in advanced stages or because of the patient’s poor physiologic condition. Surgical resection shows effective results. Delayed diagnosis with advanced stage in most of our patients is the main cause of their poor survival rate. Debulking surgery has not yet been proved beneficial for patients. For carcinoid and stage III resectable cases, aggressive management of patients helped to enhance their chances of survival. The radiotherapy for malignant thymoma has been acknowledged and documented before [20–23]. Thus, routine postoperative radiotherapy became a reasonable treatment modality for thymic carcinoma. Of the unresectable patients, those who received radiotherapy could only have a better mean survival time than those without (23.8 to 7.2 months). Chemotherapy with cisplatin-based regimen produces similar results (24.1 to 8.5 months). However, because of limited numbers of cases and combined treatments, this study could not prove the effectiveness of either therapy. Even though this study does not confirm the effect of adjuvant therapy, it is still commonly recommended that aggressive chemotherapy or radiotherapy should be given for advanced and unresectable patients [24, 25].
Thymic carcinoma is a cancer with wide heterogeneity. Its invasiveness and prognosis are quite different from that of the thymoma. Surgical resection of the tumor is still the best treatment. Debulking surgery or chemo/radiotherapy could not be proven to be of significant effect to thymic carcinoma. [14]
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Top
Abstract
Introduction
