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Ann Thorac Surg 1997;64:1593-1598
© 1997 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Results of Re-resection for Recurrent Thymomas

Department of Thoracic and Vascular Surgery, Marie Lannelongue Hospital, Le Plessis Robinson, France

	Abstract

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Background. The treatment of recurrent thymomas remains controversial.

Patients. The place for re-resection was retrospectively studied in 28 consecutive patients operated on during the last 40 years. The initial Masaoka staging of the thymoma was stage I, 4; stage II, 8; stage III, 11; and stage IVa, 3. Postoperatively, 14 have had radiation therapy, 1 chemotherapy, and 13 no adjuvant treatment. Seven patients had development of recurrences, 15 had pleuropulmonary metastases, 5 had both, and 1 had thoracotomy scar recurrence. Nineteen patients had a complete resection and 9 an incomplete one.

Results. Most local recurrences appeared after resection of stage I or II thymomas. On the other hand, in patients with stage III or IV thymomas pleural or pulmonary metastases mainly developed. No local recurrence occurred in patients who initially received postoperative radiation therapy. Five-year and 10-year survival rates were 51% and 43%, respectively, for the overall population. Among the 19 patients with complete resection, only 3 patients had a subsequent recurrence; 1 of them could be reoperated on and is still alive and free of disease.

Conclusions. Thymoma recurrences often appear as a locoregional rather than a hematogenous spread. Re-resection can be recommended in selected patients.

	Introduction

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
See also page 1598.

Thymoma is an infrequent malignant disease; it grows slowly, and long-term follow-up is needed to study recurrences. Recurrences occur in 10% to 30% of patients after complete thymoma resections and may have a slow progress even in the absence of treatment [1–6]. As a result, the treatment of recurrences and its results are not well known due to a lack of sufficient number of patients in published series [7, 8].

Most recurrences occur in the intrathoracic cavity and seem resectable. Surgical resection is considered the gold standard for thymomas; surgical re-resection, in case of recurrence, has been advised by several surgical teams [2, 7, 8], although others [9, 10] considered chemotherapy as the treatment of choice. In our experience, chemotherapy was not effective in thymomas; as a result, we decided to reoperate on all intrathoracic resectable recurrent thymomas.

The aim of this study was to evaluate the results of re-resections and to analyze the specific pattern of spread of this slow-growing tumor.

	Material and Methods

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
In a 40-year period (1956 to 1995), in the Department of Thoracic Surgery of Marie Lannelongue Hospital, 28 patients were reoperated on for intrathoracic recurrences after presumably complete thymoma resections. These resections represented 10% of the 285 completely resected thymomas during the same period and about two-thirds of the recurrences observed after complete thymoma resections. Patients reoperated on after adjuvant treatment with radiotherapy, chemotherapy, or both for initially unresectable thymomas have been excluded, as well as those with recurrences after thymic carcinomas. In fact, these tumors have a far worse prognosis in our experience and in the literature [11–14] than thymomas. There were 16 male and 12 female patients with a mean age of 50 years (range, 30 to 72 years). Sixteen patients (57%) had myasthenia gravis (6 women and 10 men) and one had a polymyosite.

First Surgical Procedure
All but 3 patients were previously operated on in our institution. Mean age at first operation was 42 years (range, 24 to 59 years). Thirteen patients had a full median sternotomy, 8 an anterolateral thoracotomy, and 7 a lateral thoracotomy.

At the time of the first surgical procedure 22 thymomas (85%) were invasive and 3 of them had synchronous pleural metastases. Thymoma resections were enlarged to adjacent structures in 19 patients. Three patients required an associated lung resection (2 wedge resections, 1 pneumonectomy), 17 a pleurectomy, 10 a pericardial resection, 2 a phrenic nerve resection, and 1 a vena caval resection. According to the Masaoka staging system there were 4 stage I (15%), 8 stage II (30%), 11 stage III (43%), and 3 stage IVa (12%) tumors. The tumors of 2 patients initially operated on elsewhere could not be classified according to the Masaoka staging. In comparison, the distribution by Masaoka staging in our overall experience was as follows: stage I, 44%; stage II, 23%; stage III, 27%; and stage IVa, 6%. At the beginning of our experience, an associated thymectomy was not routinely performed in nonmyasthenic patients; however, this thymectomy has been performed in the 13 patients operated on by sternotomy and in 4 patients operated on by anterolateral thoracotomy.

For the 26 patients with complete data, tumors were classified according to the Verley-Hollmann histologic classification [15]. There were no spindle and oval cell thymomas (type 1), 4 lymphocyte rich thymomas (type 2) (16%), 19 differentiated epithelial rich thymomas (type 3) (73%), and 3 undifferentiated epithelial rich thymomas (type 4) (12%). In comparison, the histologic types of the overall population of thymomas operated on in our department was type 1, 22%; type 2, 25%; type 3, 45%; and type 4, 8% [2].

Postoperative morbidity was 33% including pneumonia and tracheal intubation for more than 3 days in 11% and 26%, respectively. Eighty-five percent of morbid events occurred in myasthenic patients.

Thirteen patients had no postoperative treatment, 14 had mediastinal radiation therapy (in 1 case combined with chemotherapy), and 1 patient had chemotherapy. Table 1 shows the adjuvant treatment performed according to Masaoka staging.

Patients considered for re-resection had recurrences confined to the intrathoracic cavity. Only 2 patients had an associated extrathoracic metastasis: 1 patient had a synchronous liver metastasis and another a brain metastasis. Both were considered before the thoracic operation as curable by surgical resection in case of complete intrathoracic recurrence resections.

Only 1 patient had preoperative chemotherapy without any response. The re-resection was performed through a median sternotomy in 1 patient, through a lateral thoracotomy in 21, through an anterolateral thoracotomy in 5, and through an anterior bithoracotomy with split sternotomy in 1 patient.

Seven patients had local recurrences, 15 had pleural, pulmonary, or pericardial "metastases," 5 had both local and metastatic recurrences, and 1 had a thoracotomy scar recurrence. The 2 patients with associated distant metastases (liver, brain) had pleural and pulmonary metastases.

These patients underwent the re-resection of a mediastinal mass in 7 cases, pleural, pericardial, or pulmonary metastasectomies in 12 cases, both mediastinal resections and metastatectomies in 4 cases, and a parietal resection in 1 case. Four patients only had a biopsy for unpredictable carcinosis in 3 cases or an unresectable tumor in 1 case.

Eleven patients required lung wedge resections, 6 phrenic nerve resections, 5 diaphragmatic resections, 10 pericardial, and 3 superior vena caval system resections. Unfortunately, the 2 patients with an associated extrathoracic recurrence did not have a further surgical resection as we initially planned. The patient with a hepatic metastasis was referred to a specialized medicosurgical team and underwent hepatic chemoembolization before the surgical resection because of a poor general condition; he died 6 months later of hepatic complications. The patient with a brain metastasis had a carcinosis discovered at the thoracotomy; as a result, no further radical treatment was attempted.

Finally, 19 patients had a complete resection of the recurrence and 9 an incomplete one.

Postoperatively, 16 patients had radiation therapy, 2 chemotherapy, and 3 both. Seven patients did not have postoperative treatment (3 postoperative deaths, 1 thoracotomy scar recurrence, 3 severe myasthenia gravis).

Complete follow-up data were obtained for all but 1 patient until their deaths or the completion of the study. One patient was lost to follow-up after a 63-month disease-free follow-up. The mean follow-up since the re-resection was 60 months (range, 3 to 234 months).

Statistical Analysis
Percentage comparisons were made by the corrected ² test. Survival and disease-free survival were calculated by the actuarial method derived from the method of Kaplan and Meier [16] and compared by the log-rank test. Significance was defined as a p value less than 0.05.

	Results

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Three patients died during the postoperative course (11%). All of them had myasthenia gravis. One patient died of sudden death related to respiratory failure, another of pneumonia, and the last of hemoptysis due to a bronchoarterial fistula after an associated lung resection.

The overall morbidity rate was 33% and the morbidity rate among myasthenic patients was 60%. Nine patients, all myasthenic, had at least one postoperative complication. Among these 9 patients, 3 had a pneumonia, 7 a respiratory failure requiring a tracheal intubation, 1 a pulmonary embolism, and the last 1 a myocardial infarction.

Twelve patients died during the follow-up; 2 of unrelated diseases, 2 of myasthenia gravis, and 8 of tumor growth. The overall actuarial survival rates were 51% and 43% at 5 and 10 years, respectively. The survival rates after complete resection were 64% and 53% at 5 and 10 years, respectively (median survival, 53 months). Survival seems better after complete resection than after incomplete resection, but the difference is not significant (p = 0.08) (Fig 1).

View larger version (19K): [in this window] [in a new window]   Fig 1. . Actuarial survival according to the completeness of the re-resection.

Among the 9 patients who had an incomplete resection, all but 2 died. One surviving patient was operated on only 6 months ago, and the second survivor is still alive 42 months after a biopsy for carcinosis. One of these patients was also reoperated on for a thoracotomy scar recurrence 6 months after the re-resection.

Figure 2 shows the actuarial survival curves according to the type of recurrence. No significant difference was observed between local, metastatic, or both recurrences.

View larger version (16K): [in this window] [in a new window]   Fig 2. . Actuarial survival according to the type of recurrence.

	Comment

Top Footnotes Abstract Introduction Material and Methods Results Comment References

As thymoma is an infrequent tumor, the treatment of these recurrences is not well known. In our experience, in contrast with some recent series of literature [9, 10, 17–20], chemotherapy was not very effective in thymomas, even if some patients with unresectable thymoma may survive a long time after medical therapy or sometimes without treatment.

Furthermore, in our experience, most recurrences occurred in the intrathoracic cavity and seemed resectable, with only 2 patients with concomitant extrathoracic metastasis. These recurrences often appeared as a locoregional spread.

Given these facts, we decided to reoperate on all patients with resectable recurrences. As some authors have pointed out, this series clearly demonstrates that recurrences can occur in most stages of the disease and in most histologic types [1–6]. However, recurrences occurred mainly in stage III or IV thymomas and in epithelial-rich histologic types (type 3 or 4). In this series, recurrences occurred up to 306 months after the initial operation; as a result, long-term follow-up is needed in this disease. Nevertheless, high-grade malignant thymomas generally recurred sooner than low-grade malignant thymomas, as we previously demonstrated in our overall population of resected thymomas [2].

Most of our patients had pleural pericardial or pulmonary "metastases," but 7 patients had local recurrences and 5 patients had both local recurrences and pleuropulmonary metastases.

Among the seven local recurrences, two of them undoubtedly occurred in the thymus left in place during the first surgical procedure. The discovery of eight small thymomas by systematic specimen analysis of 258 associated thymectomies in our overall experience of thymoma resections explains this type of recurrence. The five other local recurrences occurred in patients with localized tumors (mainly stage I or II) who did not receive postoperative mediastinal radiation therapy (see Table 3). These recurrences probably developed in microscopic tumoral residues, left in place despite an apparent complete resection. In fact there is a risk of missing a microscopic capsular invasion despite a meticulous specimen analysis as suggested by Wilkins and associates [21]. As a result, the aggressiveness of the disease could be underestimated and consequently a decision could be made to give no adjuvant treatment. We must notice that no local recurrence was observed in patients who received postoperative radiation therapy; probably some tumoral residues may be cured by adjuvant radiation therapy.

On the other hand, pleural, pericardial, and pulmonary "metastases" mainly occurred in stage III or IV thymomas. These patients generally received adjuvant mediastinal radiation therapy, which may prevent mediastinal recurrence but obviously cannot prevent pleural or pulmonary metastases.

In addition, we noticed that most metastatic recurrences were located on the pleura or on the pericardium rather than in the pulmonary parenchyma and were often located in the costodiaphragmatic recess. This spread may suggest a locoregional rather than a hematogenous spread. We also noticed that all intrathoracic metastatic recurrences occurred into the intrathoracic cavity where the thymoma was located or in the intrathoracic cavity previously opened during the first surgical procedure.

Given these facts, these metastases may correspond to "malignant implants" related to a thymoma capsule disruption secondary to the tumor growth or sometimes to the surgical resection. This hypothesis is supported by the occurrence of scar recurrences (muscles) in this short series of 28 patients. This locoregional spread also explains why most thymomas with synchronous metastases have metastases confined to the intrathoracic cavity (stage IVa) and why these patients may have a good outcome after surgical resection alone or combined with adjuvant therapy [3, 8].

In some other patients, however, hematogenous metastases also developed as we observed in 2 patients of this series (liver and brain metastases).

Given these facts, as previously suggested, we recommend in thymoma resections an associated thymectomy even in the absence of myasthenia gravis, postoperative radiation therapy in all invasive thymomas, and care during the dissection to avoid disruption of the capsule, with en bloc resection of all invaded structures.

However, in the literature, the indication of postoperative radiation therapy after thymoma resections remains controversial [2, 3, 6, 22, 23]. In our previous experience with mediastinal radiation therapy, we did not demonstrate a significant difference between irradiated and nonirradiated patients when a complete resection was performed. We only observed a trend toward better disease-free survival in case of postoperative radiation therapy. On the other hand, Uematsu and associates [24] advise prophylactic entire hemithorax irradiation with a significant decrease of intrathoracic relapses in comparison with only mediastinal irradiation. This approach should be considered in the future.

Postoperative morbidity and mortality were quite high in this series, especially in myasthenic patients. However, this retrospective study included patients over a 40-year period and undoubtedly nowadays myasthenia gravis is better taken into account in the postoperative course than 20 years ago. The 11% mortality rate contrasts with the 1.4% mortality rate in our overall series of thymoma resections [2]. Nevertheless, re-resection for thymoma recurrences should be considered a major surgical procedure in myasthenic patients.

These patients represent a selected group of patients with resectable recurrences confined to the intrathoracic cavity. However, they represent about two thirds of recurrent thymomas in our experience.

The actuarial survival curves after re-resection show 5-year and 10-year survival rates of 51% and 43%, respectively, for the overall population, and 64% and 53% in complete resections. These results, especially for a malignant disease, are encouraging but no group control is available to consider surgical re-resection as the treatment of choice in recurrent thymomas. In fact some patients with incomplete resection or biopsy may survive several years with chemotherapy or without treatment. One of our patients with a diffuse carcinosis is still alive 42 months after a biopsy. This series confirms that these tumors often have an indolent natural history, and as a result that the best therapeutic approach is difficult to determine.

However, we should point out that a subsequent recurrence developed in only 3 patients among the 19 who had a complete re-resection; 1 of these patients was reoperated on a second time and is still alive without recurrence 46 months after the second resection.

Maggi and colleagues [8] also emphasized the effectiveness of surgical re-resection in recurrent thymomas, with a 5-year survival rate of 71% in a series of 12 patients; in comparison, the 5-year survival of 11 patients treated by radiation and chemotherapy during the same period was 40.8%.

The same team [6] in a second article recently identified two significant prognostic factors in a multivariate analysis: total resection of the recurrent tumor and the presence of a local recurrence rather than intrathoracic metastases. They also recommend re-resection in recurrent thymomas. They also noticed that most recurrent thymomas were confined to the intrathoracic cavity and that no local recurrence occurred in patients with stage I tumor who received postoperative radiation therapy.

In contrast, we did not observe a better survival in patients with local recurrences than in those with pleuropulmonary metastases. This difference may be due to the small sample of patients with local recurrences and to a more aggressive surgical approach in metastatic recurrences.

On the other hand, Loehrer and associates [9], in a multicenter study, demonstrated the effectiveness of chemotherapy in 30 patients with metastatic or recurrent thymomas with a 50% response rate (3 complete and 12 partial responses), a median duration of 11.8 months, and a time to treatment failure of 18 months. The median survival of these patients was 37.7 months (range, 2 to 91 months). We have to notice that this series considered patients with a different prognosis (patients with stage IVa and patients with recurrent thymomas), and that 2 of the 4 long-term survivors eventually required the resection of a tumoral residue. Giaccone and colleagues [10], in a multicenter study, had similar results. These results are leading us to combine chemotherapy and re-resection in recurrent thymomas, and we are starting a French prospective multicentric phase II study with the Gustave Roussy Cancer Institute to better define the effectiveness of chemotherapy (etoposide, ifosfamide, and cisplatin regimens) in recurrent thymomas but also in marginally resectable or stage IV thymomas and the benefits of such treatment in terms of recurrences and survival.

Finally, considering the particular spread of thymoma and the encouraging results of the aggressive surgical approach, re-resection should be recommended in resectable recurrent thymomas. This could be easily recommended in local recurrences but also in intrathoracic metastases if we consider these metastases as a locoregional spread with malignant implants. However, the progress of the new regimens of chemotherapy is leading us to combine the surgical resection with neoadjuvant chemotherapy.

The benefits of these multimodality therapies will probably remain difficult to determine considering the rarity, the heterogeneity, and the indolent natural history of this particular malignant tumor.

	Footnotes

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 
Presented at the Thirty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Feb 3–5, 1997.

Address reprint requests to Dr Regnard, Marie Lannelongue Hospital, 133 Ave de la Résistance, 92350 Le Plessis Robinson, France.

	References

Top Footnotes Abstract Introduction Material and Methods Results Comment References

 

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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 Author home page(s): Jean-François Regnard Pierre Magdeleinat Lionel Guibert Lorenzo Spaggiari Philippe Levasseur Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Regnard, J.-F. Articles by Levasseur, P. Search for Related Content PubMed PubMed Citation Articles by Regnard, J.-F. Articles by Levasseur, P. Related Collections Related Article