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Ann Thorac Surg 2009;88:952-957. doi:10.1016/j.athoracsur.2009.05.019
© 2009 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Multimodality Therapy for Patients With Invasive Thymoma Disseminated Into the Pleural Cavity: The Potential Role of Extrapleural Pneumonectomy

Yoshinori Ishikawa, MDa,b, Haruhisa Matsuguma, MDa,*, Rie Nakahara, MDa, Haruko Suzuki, MDa,b, Akiko Ui, MDa, Tetsuro Kondo, MDc, Yukari Kamiyama, MDc, Seiji Igarashi, MDd, Kiyoshi Mori, MDc, Tetsuro Kodama, MDc, Kohei Yokoi, MDa,b

a Division of Thoracic Surgery, Tochigi Cancer Center, Utsunomiya, Tochigi, Japan
c Division of Thoracic Diseases, Tochigi Cancer Center, Utsunomiya, Tochigi, Japan
d Division of Pathology, Tochigi Cancer Center, Utsunomiya, Tochigi, Japan
b Division of Thoracic Surgery, Nagoya University Graduate School of Medicine, Nagoya, Aichi, Japan

Accepted for publication May 8, 2009.

* Address correspondence to Dr Matsuguma, Division of Thoracic Surgery, Tochigi Cancer Center, 4-9-13 Yohnan, Utsunomiya, Tochigi, 320–0834, Japan (Email: hmatsugu{at}tcc.pref.tochigi.lg.jp).


   Abstract
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 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: The optimal treatment method for thymoma with pleural dissemination remains controversial. We analyzed our experience with a multimodality approach and evaluated the role of extrapleural pneumonectomy (EPP) in the treatment of disseminated thymoma.

Methods: Multimodality therapy was used to treat 11 consecutive patients with invasive thymoma disseminated into the pleural cavity. Disease was stage IVa in 9 and stage IVb disease with lymph node metastasis in 2. Our treatment strategy for those patients was induction chemotherapy with cisplatin, doxorubicin, and methylprednisolone (CAMP therapy), followed by thymectomy combined with resection of the visible disseminated nodules and postoperative radiotherapy. EPP was applied for 4 patients who had chemoresistant tumors or pleural refractory recurrence.

Results: Eight patients underwent induction chemotherapy. The response rate to CAMP was 85%. Thymectomy with or without the resection of disseminated pleural tumors was performed in 7 patients and EPP in 3. Postoperative radiotherapy was administered in 6. All patients except 1 with EPP had recurrence: pleural recurrence in 7, lung in 1, and multiple organs in 2. Nine patients were retreated with chemotherapy, radiotherapy, pulmonary metastasectomy, or pleurectomy. One underwent EPP for pleural recurrence. Consequently, among the 7 patients without EPP, only 1 was alive without disease and 4 were alive with pleural recurrence. In contrast, 3 of the 4 patients with EPP had no local failure and were alive without recurrence.

Conclusions: In multimodality therapy for thymoma with pleural dissemination, EPP offers good local control and may lead to cure.


   Introduction
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 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Thymoma is an epithelial tumor originating from the thymus that grows relatively slowly and generally responds to surgical resection, chemotherapy, and radiotherapy [1]. For patients with stage I or II thymoma, primary resection is recommended. For patients with stage III thymoma, multimodality treatment, including chemotherapy, radiotherapy, and resection, is often applied for cure [2–4]. On the other hand, for patients with stage IVb thymoma who have distant or lymph node metastasis, or both, the main goal of treatment is not cure but disease control using chemotherapy [5, 6]. Between these stages, treatment for patients with stage IVa thymoma, defined as a tumor with pleural or pericardial dissemination, remains controversial because complete resection is generally considered difficult. In recent years, however, some surgeons have attempted complete surgical resection in multimodality therapy [2, 4, 7].

Two types of operation have been reported for pleural dissemination of invasive thymoma: resection of visible disseminated nodules as far as possible and extrapleural pneumonectomy (EPP), aiming at the resection of visible and invisible disseminated tumor cells. The former technique has been more frequently selected, but the latter has been rarely implemented. To elucidate the role of EPP for invasive thymoma with dissemination into the pleural cavity in multimodality therapy, we retrospectively analyzed our experiences.


   Patients and Methods
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 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Between February 1988 and April 2006, 49 consecutive patients with thymoma were treated at Tochigi Cancer Center. Tumor stages were 15 at stage I, 11 at stage II, 7 at stage III, 11 at stage IVa, and 5 at stage IVb. Pleural disseminations were present in 9 with stage IVa disease and 3 with stage IVb disease. The remaining 2 patients with stage IVa disease had pericardial dissemination. Of the 3 patients with stage IVb disease and pleural dissemination, 2 had lymph node metastasis in the anterior mediastinum or ipsilateral axilla, and 1 had contralateral multiple pulmonary metastases. We analyzed the 11 patients with pleural dissemination, excluding the patient with pulmonary metastases. The Tochigi Cancer Center Institutional review board approved this retrospective analysis and waived the requirement of patient consent for the study. Staging was based on the Masaoka staging system [8]. According to the World Health Organization (WHO) classification [9], 7 tumors were categorized as type B2, 3 type B3, and 1 type B3+ thymic squamous cell carcinoma, respectively. In the last case, because the histology of the pleural disseminations was not thymic carcinoma but type B3 thymoma, we included this case in the study. The patients' characteristics are summarized in Table 1.


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  		Table 1 Patient Characteristics, Treatments, and Outcomes
 
Therapeutic Strategy
Our basic therapeutic strategy for patients with thymoma and pleural disseminated was as follows:
1 Patients were treated with induction chemotherapy. The chemotherapy regimen consisted of cisplatin, doxorubicin, and methylprednisolone (CAMP) [5]. Surgical resection was attempted after four cycles of chemotherapy.
2 The usual surgical procedure was thymectomy with resection of the visible disseminated nodules in the pleural cavity. In some patients with unforeseen pleural disseminations found during the operation, adjuvant chemotherapy was administered after thymectomy.
3 Radiation therapy was applied if the tumor was incompletely resected or likely to remain. The radiation field in most patients included the area where the tumor was deemed likely to remain. We did not perform hemithoracic radiotherapy postoperatively.
4 Exceptionally, EPP was performed in selected patients whose cardiopulmonary function was sufficient to undergo pneumonectomy and in whom concomitant resection of the mediastinal mass in conjunction with EPP was determined to be able to be safely completed. Additional disease conditions included recurrent pleural dissemination after standard surgery (patients 1 and 9) or the failure of induction chemotherapy (patients 5 and 11).

The patients were followed up every 1 to 3 months for 2 years after completion of the multimodality therapy and every 6 months thereafter. All patients were followed up until December 2008, and the median follow-up period for surviving patients was 112 months. We retrospectively reviewed the medical records of 11 patients with thymoma disseminating into the pleural cavity to clarify the outcome of our multimodality therapy, especially focusing on the role of EPP.

The patients were evaluated with computed tomography (CT) for response after induction chemotherapy and completion of the multimodality treatment. Complete remission (CR) was defined as the complete disappearance of all objective evidence of disease on CT for at least 4 weeks. Partial remission (PR) was defined as a decrease of at least 50% in the sum of the product of the perpendicular diameter of measurable lesions for at least 4 weeks. Disease progression was defined as an increase of at least 25% in tumor size or new lesions. All other circumstances were classified as no change (NC).

Statistical Analysis
Survival was measured from the first day of treatment at our hospital for thymoma accompanied by pleural dissemination until death from any cause or the last date of follow-up. Local recurrence-free survival was measured from the date of resection until local recurrence or death from any cause or the last date of follow-up. Survival and local recurrence-free survival curves were calculated using the Kaplan-Meier method, and differences in local recurrence-free survival were determined by the log-rank test. Statistical analysis was conducted using StatView 5.0 software (SAS Institute Inc, Cary, NC).


   Results
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 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
The clinical courses of the 11 patients, none of whom had myasthenia gravis, are reported in Tables 1 and 2 Go and Figure 1. All but 1 patient had pleural dissemination at the first presentation. Patient 9 had pleural recurrence 4 years after thymectomy and came to our hospital after two resections for pleural dissemination.


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  		Table 2 Treatments After Surgical Resection, Recurrences, and Outcomes
 

Figure 1
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  		Fig 1. Clinical courses of all patients with pleural dissemination. (C = chemotherapy; DOD = died of disease; EPP = extrapleural pneumonectomy; M = pulmonary metastasectomy; P = pleurectomy; R = radiotherapy; T = thymectomy.)

 
Induction chemotherapy was performed in 8 patients: CAMP therapy was applied in 7 patients, and a regimen including cisplatin, doxorubicin, cyclophosphamide, and etoposide (PACE) was administered in patient 5. CHOP, consisting of cyclophosphamide, doxorubicin, vincristine, and prednisone, was used in patient 3 after acute renal failure caused by tumor lysis syndrome during CAMP therapy [10]. Patient 11 received carboplatin and gemcitabine before CAMP therapy. Among the patients with induction chemotherapy, 6 had a partial response and 2 showed no change, and the response rate was 75%. The response rate to CAMP therapy was 85%.

Surgical resection was performed in 10 patients in the initial multimodality therapy: 7 underwent thymectomy with or without resection of the visible pleural tumors, 2 underwent EPP as the initial operation, and 1 had EPP for recurrent pleural dissemination after two resections of pleural dissemination at a previous hospital. Adjuvant chemotherapy was administered to 5 patients.

Six patients received postsurgical radiotherapy. The radiation field was the mediastinal tumor bed in patients 2 and 6 because pleural dissemination had disappeared after induction chemotherapy. In addition to the mediastinum, the whole left pleural surface in patient 3, more than half of the left pleural surface and left axilla in patient 5, and the lower third of the right hemithorax in patient 10 were irradiated. Only the lower third of the left hemithorax was irradiated in patient 8.

Patient 6 was not treated surgically because CT after induction therapy documented the tumor had invaded the main pulmonary artery. The patient was treated with radiotherapy.

Recurrence developed in 10 patients, consisting of pleural recurrence in 7, pulmonary metastasis in 1, and metastases to multiple organs in 2. Treatment for recurrence was mostly chemotherapy and radiotherapy. Surgical resections were EPP in 1 patient, pleurectomy in 2, and pulmonary metastasectomy in 1. Among the 10 patients who had recurrence after initial treatment, patients 2 and 3 died during chemotherapy for recurrence. Patient 2 received chemotherapy consisting of cisplatin, vinblastine, and bleomycin for recurrent pericardial tumors, and died 13 months after the initiation of treatment due to bleomycin-induced pneumonitis. Patient 3 received CHOP therapy for pleural recurrence. Fulminant rhabdomyolysis occurred on the day 7 of the second course of chemotherapy, and the patient died of acute renal failure 18 months after the diagnosis of primary tumor [10].

Four EPP cases are detailed:

• Patient 1: A 40-year-old man underwent thymectomy with combined resection of the pericardium for invasive thymoma with pleural dissemination, which persisted because of numerous miliary nodules. The patient received four cycles of CAMP adjuvant chemotherapy. Pleural recurrence developed 5 years after the operation, and left EPP was performed. The patient's postoperative course was uneventful, and he was alive without recurrence at 188 months after EPP.
• Patient 5: A 63-year-old woman who had invasive thymoma with pleural dissemination and axillary lymph node metastasis received PACE therapy at a previous hospital. Because the chemotherapy had no effect, the patient was referred to our hospital (Fig 2) and underwent left EPP and excision of axillary lymph node metastasis. Her postoperative course was uneventful. Pulmonary metastasis developed 1 year after EPP. She received four courses of CAMP therapy and then underwent wedge resection of the right upper lobe of the lung. The patient was alive without recurrence at 157 months after EPP.
• Patient 9: A 24-year-old man with recurrent disseminated thymoma in the pleural cavity was referred to Tochigi Cancer Center. The patient had undergone thymectomy at age 15 years and recurrent pleural nodules were twice removed at ages 19 and 22 at another hospital. He received four courses of CAMP therapy, resulting in partial response, and underwent left EPP at 25 years old with postoperative chemotherapy; however, pleural recurrence and abdominal lymph node, bone, and liver metastases developed 2 years after EPP. The patient died of disease at age 31.
• Patient 11: A 47-year-old woman was diagnosed with a left lung cancer with pleural dissemination at another hospital. Carboplatin and gemcitabine therapy was performed, without response. The needle biopsy specimen was reexamined and the diagnosis was changed to invasive thymoma. Thereafter, the patient received CAMP therapy, but the tumor did not respond and she underwent left EPP. The patient's postoperative course was uneventful, and she was alive without recurrence 31 months after the operation.


Figure 2
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  		Fig 2. Chest computed tomography scan shows multiple pleural nodules in the left thorax in patient 5. This patient also had an ipsilateral axillary lymph node metastasis.

 
The surgical approach for EPP was posterolateral thoracotomy in patients 1, 9, and 11 and median sternotomy combined with continuous anterior thoracotomy in patient 5.

The 8 patients without EPP in the initial multimodality therapy had pleural recurrence, and after retreatment with chemotherapy and radiotherapy, 1 patient was alive without disease, 4 were alive with pleural recurrence, and 2 died during chemotherapy for recurrence. In contrast, 3 of the 4 patients with EPP had no local failure and were alive without recurrence at 31, 157, and 188 months after their operations (Fig 1 and 4).

Figure 3 shows the overall survival curve of the 11 patients with thymoma with pleural dissemination. Overall survival rates were 81% at 5 years and 70% at 10 years. Figure 4 shows the local recurrence-free survival curves of 10 patients who underwent operations according to the procedure. Local recurrence-free survival was 75% at both 5 and 10 years for the EPP group, and 16% and 0%, respectively, for the non-EPP group (p = 0.06).


Figure 3
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  		Fig 3. Survival curve of the 11 patients with disseminated thymoma and pleural dissemination. Overall survival was 81% at 5 years and 70% at 10 years.

 

Figure 4
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  		Fig 4. Local recurrence-free survival curves of 10 patients who underwent surgical resection according to the operative procedures. The 5- and 10-year local recurrence-free survival rates were both 75% for the EPP group, and 16% and 0%, respectively, for the non-EPP group (p = 0.06).

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Although surgical resection is considered the mainstay of therapy for thymoma, the standard treatment for stage IVa thymoma with pleural dissemination has not been established. This is partly because the proportion of patients with this stage of thymoma is small, and complete resection is usually difficult to achieve. Masaoka and colleagues [8] created a classification in 1981 that is now widely used. They analyzed 96 patients with thymoma, but only 8 patients were classified with having stage IVa disease. The 5- and 10-year survival rates for this stage were reported to be 50% and 0%, respectively.

Although Wilkins and colleagues [11] recommended the excision of all pleural disseminated tumors, it is usually impossible to remove numerous pleural tumors, unless EPP is performed; therefore, radiation or chemotherapy, or both, are the treatments of choice for stage IVa thymoma. Ichinose and colleagues [12] treated 8 patients with thymoma and pleural dissemination mainly by radiotherapy. Only 2 of these patients underwent operations. The 5-year survival rate was 87.5%, and the authors suggested that radiotherapy should play a primary role in the treatment of this disease condition.

In 1993 Rea and colleagues [13] reported the results of induction chemotherapy for advanced thymoma patients, including stage IVa disease, to improve resectability. They used therapy consisting of cisplatin, doxorubicin, vincristine, and cyclophosphamide; the response rate was 100% and the complete remission rate was 43%.

To improve local control for these patients, multimodality therapy, which usually includes induction chemotherapy, surgical resection, adjuvant chemotherapy, and radiotherapy, has been developed [2, 5, 14]. Although different chemotherapy regimens were used and different proportions of stage IVa patients were included, survival rates were higher than previously documented outcomes. These results warrant the use of multimodality therapy for stage IVa thymoma.

The surgical procedure in multimodality therapy remains to be determined. Two surgical techniques are used for invasive thymoma that has disseminated into the pleural cavity: resection of visible disseminated nodules as far as possible, and EPP, aimed at resecting visible and invisible disseminated tumor cells. The former operation is used frequently, but EPP is rarely implemented. EPP for stage IVa thymoma was suggested as a curative operation by Bergh and colleagues [15] in 1978. Since then, more than 10 EPP procedures for thymoma have been documented as case reports (Table 3) [12, 16–18]. Although the follow-up periods were relatively short and publication bias may have affected the results, all patients were reported to be alive without recurrence at publication.


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  		Table 3 Published Cases of EPP for Thymoma With Pleural Dissemination in English Literature
 
Two retrospective studies dealing with surgical treatment, including EPP for stage IVa thymoma, have recently been published. Wright [19] reported 5 patients, including a long-term survivor without recurrence after an operation for pleural recurrence, and advocated that EPP can be performed safely and improve survival in selected patients. Huang and colleagues [7] reported 18 patients with stage IVa thymoma treated with multimodality therapy. Among them, 4 patients underwent EPP to achieve complete resection. High-dose hemithoracic radiotherapy was also initiated after EPP. They reported 3 of the 4 patients were alive without recurrence.

In our hospital, thymectomy with resection of pleural nodules in multimodality therapy was the treatment strategy for disseminated thymoma; however, after we experienced a long-term disease-free survivor (patient 1) who underwent EPP for recurrent pleural dissemination, we applied EPP for selected patients who had recurrent pleural dissemination after multiple resections and in whom the tumor had failed to respond to induction chemotherapy. As a result, 3 of the 4 patients treated with EPP were alive without recurrence, and 2 survived for more than 10 years after EPP. Although multimodality therapy using CAMP therapy was able to prolong survival even after recurrence, EPP was associated with long-term disease-free survival. We considered that EPP was able to provide complete resection of invisible disseminated tumor cells and improve local control compared with other surgical procedures.

Although we did not encounter any operative deaths, EPP is thought to be a more invasive operation compared with lung-preserving operations, and patient selection is essential. A sufficient cardiopulmonary function is essential when applying EPP. In primary disseminated cases, complicated resection of the mediastinal mass, such as the combined resection of great vessels, in addition to EPP seems to be intolerable. In addition to these, two good indications for EPP are considered to be thymoma with extensive and confluent pleural dissemination that can be completely resected only by EPP, as in the Huang series, and chemoresistant disseminated thymoma, which is considered a less controllable disease if it recurs postoperatively. For these candidates, we consider that EPP may become a treatment of choice at the first attempt to resect these tumors. Needless to say, patients with myasthenia gravis are not good candidates for EPP. As experience of EPP for thymoma with pleural dissemination is limited, a prospective multicenter study is needed to elucidate the role of EPP in the treatment of thymoma.

In conclusion, our retrospective study revealed that multimodality therapy, including chemotherapy, surgical resection, and radiotherapy, prolonged survival of patients with thymoma and pleural dissemination. Furthermore, EPP as part of multimodality therapy for selected patients showed a possibility of improving local control, leading to cure. A prospective multicenter study is warranted to establish a treatment strategy that includes EPP for stage IVa thymoma.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Block MI. ThymomaIn: Pearson F, Cooper J, Deslauriers J, et al. editors. Thoracic surgery. 63. Philadelphia: Churchill Livingstone; 2002. pp. 1688-16962nd ed.
  2. Kim ES, Putnam JB, Komaki R, et al. Phase II study of a multidisciplinary approach with induction chemotherapy, followed by surgical resection, radiation therapy, and consolidation chemotherapy for unresectable malignant thymomas: final report Lung Cancer 2004;44:369-379.[Medline]
  3. Venuta F, Rendina EA, Longo F, et al. Long-term outcome after multimodality treatment for stage III thymic tumors Ann Thorac Surg 2003;76:1866-1872.[Abstract/Free Full Text]
  4. Shin DM, Walsh GL, Komaki R, et al. A multidisciplinary approach to therapy for unresectable malignant thymoma Ann Intern Med 1998;129:100-104.[Medline]
  5. Yokoi K, Matsuguma H, Nakahara R, et al. Multidisciplinary treatment for advanced invasive thymoma with cisplatin, doxorubicin, and methylprednisolone J Thorac Oncol 2007;2:73-78.[Medline]
  6. Evans TL, Lynch TJ. Role of chemotherapy in the management of advanced thymic tumors Semin Thorac Cardiovasc Surg 2005;17:41-50.[Medline]
  7. Huang J, Rizk NP, Travis WD, et al. Feasibility of multimodality therapy including extended resections in stage IVA thymoma J Thorac Cardiovasc Surg 2007;134:1477-1483.[Abstract/Free Full Text]
  8. Masaoka A, Monden Y, Nakahara K, et al. Follow-up study of thymomas with special reference to their clinical stages Cancer 1981;48:2485-2492.[Medline]
  9. Rosai J, Sobin L. Histological typing of tumours of the thymus. International histological classification of tumours. 2nd ed.. New York: Springer; 1999.
  10. Yokoi K, Miyazawa N, Kano Y, et al. Tumor lysis syndrome in invasive thymoma with peripheral blood T-cell lymphocytosis Am J Clin Oncol 1997;20:86-89.[Medline]
  11. Wilkins Jr. EW, Grillo HC, Scannell JG, et al. J. Maxwell Chamberlain Memorial Paper. Role of staging in prognosis and management of thymoma. Ann Thorac Surg 1991;51:888-892.[Abstract/Free Full Text]
  12. Ichinose Y, Ohta M, Yano T, et al. Treatment of invasive thymoma with pleural dissemination J Surg Oncol 1993;54:180-183.[Medline]
  13. Rea F, Sartori F, Loy M, et al. Chemotherapy and operation for invasive thymoma J Thorac Cardiovasc Surg 1993;106:543-549.[Abstract]
  14. Venuta F, Rendina EA, Pescarmona EO, et al. Multimodality treatment of thymoma: a prospective study Ann Thorac Surg 1997;64:1585-1591.[Abstract/Free Full Text]
  15. Bergh NP, Gatzinsky P, Larsson S, et al. Tumors of the thymus and thymic region: I. Clinicopathological studies on thymomas Ann Thorac Surg 1978;25:91-98.[Abstract/Free Full Text]
  16. Higashiyama M, Doi O, Kodama K, et al. Intrathoracic chemothermotherapy following panpleuropneumonectomy for pleural dissemination of invasive thymoma Chest 1994;105:1884-1885.[Medline]
  17. Nakahashi H, Maeo S, Osaki T, et al. Complete excision and panpleuropneumonectomy resulting in long-term survival for a teenager with invasive thymoma: report of a case Surg Today 1992;22:558-560.[Medline]
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