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J Thorac Cardiovasc Surg 1994;107:615-0620
© 1994 Mosby, Inc.

General Thoracic Surgery

Thymic carcinomaTen years' experience in twenty patients

Taichung, Taiwan, Republic of China

From the Division of Thoracic Surgery, Department of Surgery, Taichung Veterans General Hospital, Taichung, Taiwan, Republic of China.

Received for publication April 20, 1993. Accepted for publication July 7, 1993. Address for reprints: Chung-Ping Hsu, MD, Division of Thoracic Surgery, Department of Surgery, Taichung Veterans General Hospital, #160, Sec. 3, Taichung-Kang Road, Taichung, Taiwan, Republic of China.

Abstract

Thymic carcinoma is a rare neoplasm with extremely poor prognosis. To evaluate the outcome of treatment in thymic carcinoma, we reviewed a 10-year (1982 to 1992) experience with 20 consecutive patients in Taichung Veterans General Hospital. There were 9 men and 11 women: ages ranged from 34 to 70 years old (mean 51.4 years). None of these patients had concomitant myasthenia gravis. All of the patients received surgical intervention, and the diagnosis was made by pathologic study. Postoperative staging was made according to the modified Masaoka staging system. None of our patients were in stage I. One patient (5%) had stage II disease, 12 (60%) stage III, and 7 (35%) stage IV. The pathologic subtypes of thymic carcinoma included eight squamous cell carcinomas, seven undifferentiated carcinomas, one lymphoepithelioma-like carcinoma, one clear-cell carcinoma, 1 mucoepidermoid carcinoma, and two carcinoid tumors. Curative resection could be done in seven patients (35%). The overall cumulative survival was 45.9% at 3 years and 34.4% at 5 years. The median survival times for patients with complete and incomplete resection were 39.0 months and 14.3 months, respectively (p = 0.1752). The median survival times of patients with postoperative radiotherapy and without postoperative radiotherapy were 39.3 months and 15.0 months, respectively (p = 0.0738). The median survival times of patients with squamous cell carcinoma and undifferentiated carcinoma were 25.4 months and 11.3 months, respectively (p = 0.1464). Our data show that complete resection, postoperative radiotherapy, and squamous cell carcinoma do not indicate a significantly favorable result, even though they result in longer median survival times. Yet a positive trend of favorable outcome in patients who received postoperative radiotherapy is ambiguously shown. (J THORAC CARDIOVASC SURG 1994;107:615-20)

Thymic carcinoma is a relatively rarely seen neoplasm, with distinct pathologic and clinical characteristics. Levine and Rosai ¹ included these tumors in the group of so-called type II malignant thymomas. It was Snover, Levine, and Rosai ² who in 1982 named these tumors thymic carcinoma. That group also suggested that a thymic carcinoma should fulfill the following criteria: (1) anterior mediastinal location and (2) absence of another primary tumor. The largest single hospital series in this field came from Wick and associates, ³ who reported 20 thymic carcinomas over a 75-year period. Thymic carcinoma has a dismal prognosis as compared with that of thymoma, because most of these tumors have locoregional invasion when diagnosed.

We report 20 consecutive cases of thymic carcinoma in a 10-year period at Taichung Veterans General Hospital. All of these patients were diagnosed according to the pathologic study, either by tumor resection or biopsy. The prognosis was analyzed according to different cell types, and the occurrence of locoregional tumor invasion and sites of recurrence were described.

PATIENTS AND METHODS

From October 1982 to December 1992, 20 consecutive cases of thymic carcinoma were treated. There were 9 men and 11 women whose ages ranged from 34 to 70 years old (mean 51.4 years). At the end of this study, 8 patients were still alive, 2 patients were lost to follow-up, and 10 patients were dead. None of these patients had concomitant myasthenia gravis, but one patient was seen in whom lymphoma developed before the diagnosis of thymic carcinoid. All of the patients received surgical intervention, and the diagnosis was made by pathologic study. Postoperative staging was done according to the modified staging system of Masaoka and associates ⁴ (Table I). Table II lists the stages, pathologic subtypes, and number of complete resections in our patients. Table III lists the types of operation according to the stages of the patient. Sixteen (84.2%) of these patients received postoperative radiotherapy (tumor dose ranged from 4500 cGy to 6000 Gy). Twelve patients (60%) received chemotherapy before or after operation, or at both times. There was one surgical death as a result of postoperative respiratory failure. The cumulative survival determination and survival comparison were done by the SPSS/PC+ Advanced Statistics 4.0 software package for microcomputer data management and analysis developed in 1990 by SPSS Inc., Chicago, Illinois.

The stages of disease in our patients were as follows: 1 patient had stage II disease, 12 patients stage III; and 7 patients stage IV. The pathologic subtypes of thymic carcinoma included eight squamous-cell carcinomas, seven undifferentiated carcinomas, one lymphoepithelioma-like carcinoma, one clear-cell carcinoma, one mucoepidermoid carcinoma, and two carcinoid tumors. Curative resection could be done in seven patients (35%). The overall cumulative survival was 45.9% at 3 years and 34.4% at 5 years. One patient died on postoperative day 11 of respiratory failure; this indicates a 5% mortality rate.

Fig. 1 shows the cumulative survival curve of our patients according to the modified Masoaka staging system. There were no significant statistical differences between different stages of thymic carcinomas (p = 0.9400). The median survival times for patients with completely and incompletely resected disease were 39.0 and 14.3 months, respectively. There were no significant differences of survival probability between completely and incompletely resected cases (p = 0.1752). The median survival time of patients who received postoperative irradiation was 39.3 months. This was longer than that of those patients who did not receive postoperative irradiation (median survival time 15.0 months). However, the difference between the two groups was nonsignificant (p = 0.0738).

View larger version (17K): [in this window] [in a new window]   Fig. 1. Cumulative survival from time of diagnosis in stage III and IV thymic carcinoma.

Table IV

Table V

Table VI

There is a limited amount of experience in the management of thymic carcinoma. This is not only because thymic carcinoma is rare, but also because, in the past, the precise origin of some mediastinal tumors could not be clearly established. With the improvement of immunochemical techniques, the origin of the carcinomas mentioned herein can be attributed to thymic origin with more credence. Thymic carcinomas are immunoreactive to epithelial membrane antigen and cytokeratin, but not reactive to -fetoprotein, ß-human chorionic gonadotropin, placental alkaline phosphatase, or common leukocyte antigen. ^5-10 Sometimes, lymphoma, seminoma, sarcoma, or embryonal carcinoma are difficult to distinguish microscopically from thymic carcinoma. Now, the definitive histologic diagnosis of these tumors can be made by immunohistochemistry.

According to the classification of Levine and Rosai, ¹ thymic carcinomas are included in the group of type II malignant thymomas. Clinically, these patients frequently have more symptoms of mediastinal compression than do patients with ordinary thymomas. Invasion of the mediastinal structures is almost always present. This makes complete resection of these tumors difficult. Even though the role of "debulking" surgery is still a topic of controversy, surgical resection should be attempted whenever possible to decrease the tumor burden.

Postoperative irradiation is a reasonable treatment modality for malignant thymoma. ^11-14 However, the role of irradiation in the treatment of thymic carcinoma is unknown because of limited experience in this field. All but four of our patients (two carcinoid cancers, one patient refusal, and one surgical mortality) received postoperative radiotherapy. Even though our data do not reveal a statistical difference in survival time between the radiotherapy group and nonradiotherapy group, there is a tendency that favors postoperative radiotherapy.

The role of chemotherapy in thymic carcinoma is also unclear. ¹⁵ Twelve (60%) of our patients received chemotherapy before or after operation, or at both times. Analysis of the effect of chemotherapy is difficult in our series because too many different chemotherapeutic drugs had been used in our patients. Eight (66.7%) of these patients received a chemotherapy regimen that contained cisplatin. Among these cases, one received preoperative chemotherapy for possible downstaging of the tumors. The patient had squamous-cell carcinoma (stage IVb) and received four courses of preoperative chemotherapy (doxorubicin 40 mg, cisplatin 50 mg, vincristine 0.6 mg, and cyclophosphamide 700 mg for 3 days) and concurrent radiotherapy (4500 cGy). Then she underwent extended thymothymectomy with resection of the tumor, pericardium, and left upper lobe of lung. However, left-sided twelfth rib metastasis occurred 3 months later and the patient died 23 months after the initial operation.

At least eight subtypes of thymic carcinomas have been described. ¹⁶ Squamous-cell carcinoma and lymphoepithelioma-like carcinoma are the predominant cell types in several published articles. ¹⁷ However, the predominant cell types in our series were squamous-cell carcinoma and undifferentiated carcinoma. During the same period, we operated on 55 patients with thymic tumors, so the prevalence of thymic carcinoma overall among thymic tumors was 36.4%. This prevalence is much higher than that in the report of Wang and associates. ¹⁸

As compared with thymoma, thymic carcinoma has a more invasive tendency on computed tomographic scan examination, and most of the patients have clinical symptoms caused by tumor compression of the mediastinal vital structures. ^{3, 19} Locoregional mediastinal or lymph-node invasion is the rule. As in our series, the pleura, innominate vein, pericardium, and lung are by far the most commonly seen mediastinal structures involved by the tumor. Nineteen of our 20 patients were in stage III or IV, and complete resection could be done in only 7 (35%) of our patients. This is much lower than the figure in the thymoma group. Two of our patients were categorized into the incomplete resection group because of a microscopic tumor at the margin of the resected lung. Both of these patients received postoperative radiotherapy. One patient was still alive after 50 months, and the other one died 23 months after the operation.

It had been noted for years that the composition of thymic carcinoma is frequently heterogeneous. Different types of carcinoma had been found in a single tumor. It was suggested that this might be related to the consequence of the varied differentiation potential of the pluripotential epithelial stem cell of endodermal origin in the thymus. ² Even though the microscopic picture and clinical course of thymic carcinoma are quite different from those of thymoma, several pieces of evidence that suggest that thymic carcinoma might be derived from thymoma have been observed. ^20-22 One of our patients had an incidental finding of a concomitant microscopic island of thymoma.

The prognosis of thymic carcinoma is very poor. Wick and associates ³ reported an average survival time of 18 months in 18 of the 20 patients who died. Our 3-year and 5-year cumulative survivals were 45.9% and 34.4%, respectively. The median survival time was 25.5 months, and the longest survival period was noted in a patient with thymic carcinoid who was still alive 59 months after resection. Kuo and associates ²² reported 13 cases of thymic carcinoma during a 6-year period in the treatment of 61 thymic epithelial tumors. The most commonly seen subtype in their series was squamous-cell carcinoma, and none of their patients had myasthenia gravis. They also described a better prognosis in squamous-cell carcinoma of the thymus. Our data showed that the median survival times of patients with squamous-cell carcinoma and undifferentiated carcinoma are 25.4 months and 11.3 months, respectively (p = 0.1464).

Whether the thymic carcinoid tumor should be included under the title of thymic carcinoma is still a topic of controversy. We believe, as Wick and associates ³ suggested, that thymic carcinoid should be included as a thymic carcinoma. The traditional concept that suggests that the carcinoid tumor is derived from the neuroendocrine cell has been challenged in recent years. Sidhu ²³ and others ^{24, 25} reported that some amine precursor uptake and decarboxylation cells could be differentiated from endodermal D cells of the digestive and respiratory tract. The majority of these tumors belong to the group of atypical carcinoids. This means that thymic carcinoids are frequently metastasizing or are locoregionally invasive at diagnosis. ²⁶ Thymic carcinoid is a tumor of intermediate-grade malignancy. The time course of this tumor is long, and most of the patients will live with the disease for a long period before they die. We have had two cases of thymic carcinoid: one patient died 10 months after resection because of distant metastasis, whereas the other was still alive with the disease (left supraclavicle lymph-node metastases) 59 months after resection. Paraneoplastic syndromes have been reported sporadically. Verley and Hollmann ²⁷ reported four cases of myasthenia gravis with concomitant "type 4 thymoma." Marino and Müller-Hermelink ¹⁹ also reported a case of thymic carcinoma with concomitant myasthenia gravis. Thymic carcinoid had been reported to be associated with Cushing's syndrome because of ectopic adrenocorticotropic hormone production. ^{19, 28} None of our patients had myasthenia gravis or other paraneoplastic syndromes, but one patient in whom lymphoma developed before the diagnosis of thymic carcinoid was noted.

During the period of follow-up, there were 10 deaths in our series. The causes of death included eight tumor recurrences, one acute leukemia with sepsis, and one surgical mortality. As regards the sites of tumor recurrence, there were five mediastinal recurrences, four lung metastases, three bony metastases, three lymph-node metastases, and one liver metastasis. Five of these patients had multiple foci of tumor recurrence.

Thymic carcinoma has its unique clinical behavior, which is quite different from that of ordinary thymoma. It is more invasive, and the prognosis is poorer. Most of the patients died as a result of locoregional tumor recurrence or hematogenous spreading. We prefer to call these tumors "thymic carcinoma" rather than "type II thymoma," so as to prevent confusion with ordinary thymoma. Complete curative resection is often impossible. However, our limited experience shows that a trend of more favorable results is seen in patients who received postoperative radiotherapy. Besides this, preoperative downstaging of the tumor with sensitive chemotherapeutic agents seems to be a reasonable approach. Further accumulation of clinical experience with this disease is necessary for the establishment of a treatment protocol.

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This Article Abstract Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hsu, C.-P. Articles by Wang, P.-Y. Search for Related Content PubMed PubMed Citation Articles by Hsu, C.-P. Articles by Wang, P.-Y.