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Eur J Cardiothorac Surg 2004;26:412-418
© 2004 Elsevier Science NL

Long-term survival and prognostic factors in thymic epithelial tumours

Federico Reaa*, Giuseppe Marullia, Rodolfo Girardia, Luigi Bortolottia, Adolfo Favarettob, Alessandra Galligionic, Francesco Sartoria

a Thoracic Surgery, University of Padua, via Giustiniani, 2, 35128 Padua, Italy
b Department of Oncology, University of Padua, Padua, Italy
c Department of Pathology, University of Padua, Padua, Italy

Received 22 October 2003; received in revised form 9 March 2004; accepted 21 April 2004.

* Corresponding author. Tel.: +39-049-8212237; fax: +39-049-8212249
e-mail: federico.rea{at}unipd.it


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Objective: The aim of this study is to analyze long-term survival and the prognostic significance of some factors after surgical resection of thymic epithelial tumours. Methods: We performed a retrospective analysis of clinical and histopatological data on 132 patients operated on for thymic tumours, from 1970 and 2001. Histologic diagnosis based on the new WHO classification system was made by a single patologist. A univariate and multivariate analysis of prognostic factors predicting survival was carried out. Results: There were: 108 complete resections (81.8%), 12 partial resections (9.1%) and 12 biopsies (9.1%). Overall 5, 10 and 15-year survival rate was 72, 61 and 52.5%, respectively. The Masaoka staging system showed 44 stage I, 18 stage II, 52 stage III and 18 stage IV. Histologic results were: 14 subtype A, 31 AB, 20 B1, 28 B2, 29 B3 and 10 C; the respective proportions of invasive tumour (stage II–IV) was 28.6, 58.1, 50, 75, 86.2 and 100%. There were 16 tumour recurrences (14.8%) of 108 radically resected thymomas, 10 were treated with radical re-resection. In univariate analysis, four prognostic factors were statistically significant: radical resection, Masaoka clinical staging, WHO histologic subtype and resectable tumour recurrence. In multivariate analysis, the independent factors predicting long-term survival were WHO histology and Masaoka stage. Conclusions: The WHO histologic classification seems to be the most significant prognostic factor reflecting the invasiveness of the thymic tumour. Completeness of resection and Masaoka stage I and II assure a better survival. Unresectable recurrence of thymic tumour predicted a worse prognosis.

Key Words: Thymic tumours • Prognostic factors • Masaoka stage • Surgery • WHO histologic classification


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
Thymomas are relatively common tumours of the anterior mediastinum that arise from the epithelial cells of the thymus.

The heterogeneity of the biological, oncological and histological features of thymic epithelial tumours (TETs) seems to be the main reason why researchers have difficulties in establishing some sure prognostic factors.

In fact, even if Masaoka surgical-pathologic stage is widely accepted as an important prognostic factor for TETs [1–3], the role of other factors is not clear, particularly about histology.

In the last 20 years several histological classifications have been used [4–7], creating controversies and difficulties when comparing the results of different studies [8,9].

In 1999 the World Health Organization (WHO) [10] published new histological criteria for the classification of TETs to provide a universally accepted system for all researchers.

The aim of this study is to analyse long-term survival and prognostic factors of TETs treated by surgical resection in the light of the new histological classification and the Masaoka staging system.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 Appendix A. Conference...
 References
 
We performed a retrospective analysis of clinical and histopathological data on 132 patients operated on for thymic epithelial tumours, between 1970 and 2001, at the Department of Thoracic Surgery of the University of Padua.

The surgical-pathologic staging system proposed by Masaoka and Coll [1] was used to describe the invasion of the surrounding organs (Table 1).


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  		Table 1. Clinico-pathologic staging of TETs according to Masaoka system

 
Pathologic examination, based on the WHO classification system (Table 2) [10], was performed by a single pathologist who reviewed the hematoxylin and eosin stained sections.


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  		Table 2. WHO histological classification of TETs

 
There were 68 females and 64 males, the mean age was 50 years (range 15–75 years). 40 (30.3%) patients were asymptomatic at the moment of diagnosis, while 92 (69.7%) patients presented clinical symptoms or signs, that included 23 myasthenia gravis (MG) and 11 other parathymic syndromes (4 pure red cell aplasia, 3 autoimmune thrombocytopenia, 2 hypogammaglobulinemia, 1 sclerodermia, 1 thyroiditis).

We adopted adjuvant radiotherapy in patients with stage III and IVa and adjuvant chemotherapy only in selected cases of patients with stage III and IVa not radically resected.

Since 1985, we started to use neoadjuvant chemotherapy in patients with invasive thymoma (stage III and IVa), who were considered unresectable after first staging. We judged unresectable those tumours with wide involvement of great mediastinal vessels or others major structures, using clinical and radiological criteria and in few cases even an invasive approach (VATS or anterior mediastinotomy).

The chemotherapy regimen administered (ADOC: cisplatin, doxorubicin, vincristine and cyclophosphamide) was mentioned in our previous report [11].

Follow-up for all patients was conducted until death or end of the study (January 2003), mean follow-up was 92 months (range 1–351 months).

2.1. Statistical analysis
Association between categoric variables were determined by using the {chi}2 test. The analysis of the actuarial survival rate was made by the Kaplan-Meier method. The statistical difference between the survival curves was determined using the log-rank test. The linear regression model by Pearson was employed to identify the correlation between variables. Multivariate analysis by Cox proportional hazard model was used to investigate the relative importance of different prognostic factors. A P value less than 0.05 was considered statistically significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 Appendix A. Conference...
 References
 
Operative approach was sternotomy in 69 (53%) patients, postero-lateral thoracotomy in 53 (40%), sternotomy and lateral thoracotomy in 3 (2%), cervicotomy with sternal split in 4 (3%) and cervicotomy in 3 (2%).

The operative procedures were 62 total thymectomies with the surrounding mediastinal fat, while in the invasive tumours the resection was extended to pericardium in 33 cases, to one phrenic nerve in 15 cases, to the lung in 27 cases (19 atypical resections, 6 lobectomies and 1 pneumonectomy) and to the superior vena caval system in 7 cases (6 innominate vein resections, 1 end to end anastomosis superior cava-azygos).

No intraoperative or postoperative mortality occurred; 9 (6.8%) patients had postoperative complications: 3 respiratory failure in MG, 3 pneumonia, 2 surgical wound infections and 1 post-pneumonectomy broncho-pleural fistula.

At the end of follow-up 51 (38.6%) patients had died.

The overall actuarial 5, 10 and 15-year survival rate was 72, 61 and 52.5%, respectively (Fig. 1) .



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  		Fig. 1. Overall survival in TETs.

 
Of 132 patients, 62 received adjuvant radiotherapy, while 24 patients were treated by post-operative chemotherapy.

Out of 70 patients with stage III and IVa thymoma, 32 (23 in stage III and 9 in stage IVa) were judged unresectable at the pre-operative first staging and submitted to neoadjuvant chemotherapy: 9 patients had complete remission after chemotherapy and 23 had partial remission; all underwent operation and 24 (75%) radical resections and 8 (25%) incomplete resections were performed. Overall 5 and 10-year survival rate in this group of patients was 55 and 42%, respectively.

The remaining 38 patients underwent immediate surgery and we had 22 (58%) radical resections and 16 (42%) incomplete resections. Overall 5 and 10-year survival rate in this group of patients was 55 and 39%, respectively.

The analysis of prognostic value of various factors showed a statistical significance for following:

3.1. Extent of resection
Of 132 patients operated on, 108 (81.8%) underwent radical resection, 12 (9.1%) incomplete resection (‘debulking’) and 12 (9.1%) biopsy only.

The actuarial 5 and 10-year survival rate was 82.5 and 71% for patients who had radical resection, 33 and 25% for biopsy, 16 and 9% for incomplete resection, respectively (Fig. 2) .



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  		Fig. 2. Survival by extent of surgical resection: radical resection (n=108), debulking (n=12) and biopsy (n=12).

 
Patients who underwent radical resection showed a significantly higher survival than those who received incomplete resection or biopsy (P=0.001), while we could not find statistical difference in survival between patients who underwent incomplete resection and biopsy (P=0.35).

3.2. Surgical-pathologic staging
After operation, the stratification of patients according to Masaoka staging system identified 44 (33.3%) stage I, 18 (13.6%) stage II, 52 (39.5%) stage III and 18 (13.6%) stage IVa.

The 5 and 10-year survival rate was 93 and 84% for patients with stage I disease, 93 and 82% for patients with stage II disease, 60 and 51% for patients with stage III disease, 36 and 0% for patients with stage IVa disease.

Patients in stage I and II had a good long-term survival, while stage III and IVa predicted a worse prognosis (Fig. 3) .



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  		Fig. 3. Survival according to the Masaoka staging system. In univariate analysis there were significant differences between stage I and stage III disease (P=0.0002), stage I and stage IVa disease (P=0.0001), stage II and stage III disease (P=0.01), stage II and stage IVa disease (P=0.0004). There were no significant differences between stage I and stage II disease (P=0.55), stage III and stage IVa disease (P=0.09).

 
3.3. Recurrence
Sixteen (14.8%) patients out of 108 who received a radical resection, had a recurrence. Disease-free interval ranged from 5 to 121 months (mean 36 months).

Recurrence was intrathoracic in 13 cases (3 local recurrences and 10 pleuro-pulmonary or pericardial metastases), while there were 3 distant recurrences (2 liver metastases and 1 bone metastasis).

The treatment of recurrences consisted of re-resection in 11 cases (10 radical, 1 incomplete resection), while 5 patients were treated with other therapies (2 chemotherapy only, 3 chemo-radiotherapy).

Overall 5-year survival rate in the 16 patients, from the time of recurrence, was 33%.

Radical resection of recurrent tumours was associated with better survival, in comparison with patients treated by other therapies (5-year survival: 73 and 0%, respectively. P=0.0001).

When we analysed the proportion of survival from the time of first operation, no statistical differences we found between survival of patients with complete resection without recurrence and patients with recurrence radically resected (10-year survival 71 and 69%, respectively; P=0.29. Fig. 4) .



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  		Fig. 4. Survival of patients treated by radical resection without recurrence (n=92), with recurrence surgically resected (n=11) and with recurrence treated with adjuvant therapy (n=5).

 
3.4. WHO histology
Histopathologic review, according to WHO criteria, showed 14 (10.6%) patients with subtype A tumour, 31 (23.5%) with subtype AB, 20 (15.1%) with subtype B1, 28 (21.2%) with subtype B2, 29 (22%) with subtype B3 and 10 (7.6%) with subtype C.

Overall 10-year survival rate was 100% for patients with subtype A tumour, 90% for subtype AB, 78% for subtype B1, 33% for subtype B2, 35% for subtype B3 and 0% for subtype C.

The proportion of invasive tumour (stage II–III–IV) was greater in the subtypes B2-B3 and C (83.6%; 56 of 67 patients), than in the subtypes A–AB and B1 (49.2%; 32 of 65 patients. {chi}2 test: 17.5; P=0.00003) and the relation between histology and Masaoka stage was statistically significant (P=0.0001 by linear regression).

Therefore, subtypes A–AB–B1 thymomas showed an oncological behaviour less aggressive than subtypes B2–B3–C, leading to a significantly better survival (Fig. 5) .



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  		Fig. 5. Survival according to the WHO histological classification system. In univariate analysis there were no significant differences in comparison of survival curves between patients with each combination of subtypes A, AB and B1 tumours (A vs AB: P=0.93; A vs B1: P=0.55; AB vs B1: P=0.66) and each combination of subtypes B2, B3 and C tumours (B2 vs B3: P=0.60; B2 vs C: P=0.08; B3 vs C: P=0.20). Instead, a significant difference was found in comparison between patients with subtype A and B2 (P=0.003), A and B3 (P=0.0001), A and C (P=0.0004), AB and B2 (P=0.0001), AB and B3 (P=0.0001), AB and C (P=0.0001), B1 and B2 (P=0.003), B1 and B3 (P=0.002), B1 and C (P=0.0003).

 
3.5. Multivariate analysis
Multivariate analysis was performed to assess the independent prognostic value of different factors (gender, age, MG and other parathymic syndromes, adjuvant radiotherapy, extent of resection, Masaoka stage, WHO histology and recurrence).

WHO histology (P=0.0001) and Masaoka stage (P=0.003) were identified as independent factors predicting long term survival.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
Appendix A. Conference...
 References
 
Several studies have been performed to identify prognostic factors to programme the most adequate therapeutic strategy for TETs [2,12–14].

Surgery is the best treatment in patients with early stage of TETs and leads to a good long term survival [2,12,13]. In the advanced stages, however, a multidisciplinary approach is preferable, even if the prognosis seems to depend largely on the ability to perform a radical resection.

In a study conducted on a large number of patients, Regnard and Coll [12] identified the completeness of resection as the only significant independent prognostic factor at multivariate analysis and, on the basis of their results, they proposed to include this factor in a modified clinical-pathologic staging system of thymomas.

According with Regnard and Coll, in our experience, patients who underwent radical resection had a higher 5 and 10-year survival rate (82.5 and 71%) than patients who received debulking (16 and 9%) or biopsy (33 and 25%). The role of radical resection is relevant even in cases of recurrence of TETs: recurrence, mostly intrathoracic, occurs in 10–30% of radically operated patients with thymoma [15–17]. When the recurrence is resectable, the surgical approach seems to be the best therapeutic option: in our experience patients with mediastinal or intrathoracic recurrence, who received a radical re-resection, had an excellent long term survival, comparable with patients who had a radical resection without recurrence (10-year survival: 68 and 72%, respectively, P=0.29).

Regarding the surgical-pathologic staging system proposed by Masaoka and Coll, several authors agree that it is the best prognostic factor for TETs predicting long term survival [1–3,18,19]. We confirm this thesis because in our series we found a significantly better survival in stage I and II than in stage III and IV (10-year survival rate 84, 82, 51 and 0%, respectively) with significant values in univariate and multivariate analysis.

Instead, the prognostic relevance of histology is still debatable, due to the numerous histological classifications [4–7] that contribute to confuse and make an analysis and comparison of the various results difficult.

In 1999 the WHO Consensus Committee published a new classification system regarding the criteria to distinguish the different TETs [10]: the system proposed by Marino and Muller-Hermelink [7] is the basis of this classification, that stratifies TETs into six subtypes classified with letters and numbers (A, AB, B1–3, C).

At present, few papers [18–20] tested the prognostic and clinical validity of the new WHO classification: recently, Okumura and Coll [18] reviewed 273 cases of TETs and classified them according the WHO system. Their study suggested that subtypes B2 and B3 tumours had a more malignant behaviour in terms of post-operative survival, invasiveness and tumour recurrence, compared with subtypes A, AB and B1. In this study, in multivariate analysis the Masaoka stage (P<0.001) and the WHO histology (P=0.05) were the sole independent factors predicting survival. Similar results were obtained also by Chen and Coll [19]: they found a good correlation between different histological subtypes and the risk of aggressiveness. Masaoka stage was a highly significant prognostic factor (P<0.001) and WHO histology was an independent predictive factor of survival only in stage I and II (P<0.003). Our results also confirm the clinical relevance of WHO system in predicting the aggressiveness of thymic tumours: subtypes B2, B3 and C had a more invasive oncological behaviour than subtypes A, AB and B1 and when we compared subtypes A, AB, B1 with the subtypes B2, B3, C the survival rate value reached a statistically significant difference.

In a multivariate analysis the WHO classification was identified as independent prognostic factor (P=0.0001).

Another therapeutic issue is the use of neoadjuvant therapy in order to increase the resectability of thymomas: in tumours involving the surrounding structures, a radical resection is not always possible and a multidisciplinary approach is required; however, there is no common agreement about the sequence of different therapeutic options.

Unfortunately, our study is not a prospective study and includes a long period of time: in first part of our experience we used only adjuvant therapy after surgery, since 1985 we have been using neo-adjuvant chemotherapy with ADOC regimen for patients with advanced disease, that was considered not radically resectable at the first staging. The results on 32 patients were encouraging with a remission rate of 100% (9 complete remissions and 23 partial remissions) and a complete resection performed in 24 patients (75%). If we compare this group with patients that did not receive neoadjuvant therapy, the percentage of resectability was better (75 vs 58%).

Venuta and Coll [21] report the results of a prospective study on 21 patients (8 in stage III and 13 in stage IVa) submitted to neo-adjuvant chemotherapy, followed by surgery and adjuvant radiotherapy.

They obtained a remission rate of 100% (2 complete histological remissions and 19 partial remissions) and performed 16 radical resections and 5 incomplete resections, with a very good 8-year survival rate (92 and 68% for patients in stage III and IVa, respectively).

These and other experiences [22,23] show that neoadjuvant chemotherapy could improve the resectability of TETs or, at least, make the resection easier, reducing the bulk of tumour and the vascular or mediastinal infiltration.

In conclusion, even if it is difficult to identify prognostic factors for TETs, several studies report uniform results: Masaoka stage appears to be the most significant predictor of survival, while the role of completeness of resection and histology is still not defined.

In our experience the new WHO histologic classification seems to be a reliable parameter to predict clinical behaviour and prognosis of patients affected by TETs; if this will be confirmed, a precise pre-operative histologic diagnosis will become essential to decide the most appropriate therapeutic treatment.

The main limit of this retrospective study is that it covers a wide time period, in which the surgical approaches and treatment modalities have evolved, especially in past decades. Further and broader studies will need to be made in order to verify the utility of prognostic factors in clinical practice and to improve the therapeutic strategies for patients with thymic tumours.


   Footnotes
 
Presented at the joint 17th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 11th Annual Meeting of the European Society of Thoracic Surgeons, Vienna, Austria, October 12–15, 2003.


   Appendix A. Conference discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
References
 
Dr G. DiRienzo (Bari, Italy): I have two questions. The first one is, have you been able to assess pre-operatively the histology of thymic tumors? The second question is, I know that you have a good experience in thoracoscopic resection even robotic-assisted. Is there any role for VATS surgery in Masaoka's stage I thymic tumors?

Dr Rea: Regarding the first question, this is a retrospective analysis of patients. In the majority of patients, when we did the thoracotomy, we didn't know the exact diagnosis. Maybe now that we know that the WHO classification could be important to planning the exact strategy, maybe it's very important to obtain pre-operative histology.

Regarding the second question, when I suspect the presence of thymic tumor, I never use thoracoscopy. I never use a robotic device. I just use the robotic device for hyperplasia in myasthenia gravis.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 Appendix A. Conference...
 References
 

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