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Eur J Cardiothorac Surg 2008;33:307-313. doi:10.1016/j.ejcts.2007.09.044
Copyright © 2008, European Association for Cardio-thoracic Surgery. Published by Elsevier. All rights reserved.
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Malignant pleural mesothelioma: clinicopathologic and survival characteristics in a consecutive series of 394 patients

Piero Borasioa, Alfredo Berrutib, Andrea Billéa, Paolo Lausia, Matteo Giaj Levrac, Roberto Giardinoa, Francesco Ardissonea,*

a University of Turin, Department of Clinical & Biological Sciences, Thoracic Surgery Unit, Italy
b University of Turin, Department of Clinical & Biological Sciences, Medical Oncology Unit, Italy
c University of Turin, Department of Clinical & Biological Sciences, Pulmonary Oncology Unit, Italy

Received 4 June 2007; received in revised form 29 August 2007; accepted 3 September 2007.

* Corresponding author. Address: University of Turin, Department of Clinical & Biological Sciences, Thoracic Surgery Unit, San Luigi Hospital, 10043 Orbassano, Torino, Italy. Tel.: +39 011 9026575; fax: +39 011 9026529. (Email: francesco.ardissone{at}unito.it).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objective: Treatment of malignant pleural mesothelioma (MPM) remains disappointing, although recent reports suggest that multimodality therapy including surgery may provide a significant survival benefit. The aims of this single institution study were: to investigate clinicopathologic characteristics and potential prognostic factors in MPM patients, and to ascertain whether surgery followed by adjuvant therapy had an independent prognostic role. Methods: Retrospective review of a prospectively compiled computerized database of all patients with MPM evaluated between 1989 and 2003. Kaplan–Meier method, log-rank test, and Cox model were used in the statistical analysis. Results: There were 394 patients: 270 men (68.5%), 124 women, median age 64 (range 28–93). Twenty-seven patients (6.8%) underwent surgical resection (extrapleural pneumonectomy 15, pleurectomy/decortication 12), followed by adjuvant therapy. As of March 2006, 381 patients (96.7%) had died (median survival, 11.7 months; range 0.03–117.9). Median follow-up of 13 surviving patients (3.3%) was 45.2 months (range 28.7–126.5). Overall survival at 2 years was 18.8%. Multimodality therapy including surgery yielded a median survival of 14.5 months and a 2-year survival rate of 29.6%. Using univariate analysis, age (p = 0.009), chest pain (p = 0.01), weight loss (p = 0.001), performance status (p = 0.0001), platelet count (p = 0.008), histology (p = 0.0001), macroscopic appearance of pleural surface (non-specific inflammation, tumor-like thickening, or nodules; p = 0.0001), visceral pleura involvement (p = 0.0001), degree of involvement of pleural cavity (less than or more than one third of the cavity; p = 0.0001), and multimodality therapy (p < 0.01) were found to be significant prognostic factors. At multivariate analysis, performance status, platelet count, histology, and degree of involvement of pleural cavity remained independently associated with survival, whereas multimodality therapy failed to enter the model. Conclusions: Significant predictors of survival include performance status, platelet count, histology, and degree of involvement of pleural cavity. Within the confines of this retrospective study and the small number of patients undergoing multimodality therapy, the role of surgery in the treatment of MPM remains unclear. Further investigation is warranted to determine the optimal treatment strategy in this disease.

Key Words: Malignant pleural mesothelioma • Treatment • Prognosis


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Malignant pleural mesothelioma (MPM) is a relatively rare tumor, with a growing incidence over the last decades [1]. Owing to its highly aggressive behavior, there have been repeated efforts to identify more accurate prognostic factors [2] and staging systems [3], and to investigate novel treatment regimens [4].

One area of major debate in the treatment of MPM is the role of multimodality therapy (i.e., combined surgery, chemotherapy, and/or radiotherapy), although several reports suggest that it may provide long-term survival benefits in selected patients [5,6].

The current single institution study was performed in order to investigate clinicopathologic characteristics and potential prognostic factors in patients with MPM, and to ascertain whether surgery followed by adjuvant therapy had an independent prognostic role.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 Appendix A
 References
 
2.1 Data retrieval
A database analysis of our thoracic surgery unit registry was conducted to identify all patients with pathologically confirmed MPM who underwent evaluation between January 1989 and December 2003. Data were collected retrospectively from hospital records and from a prospectively compiled computerized database, which had been established by the unit in 1997. Clinical records were analyzed for sex, age, documented exposure to asbestos, history of smoking, interval from time of symptom onset to diagnosis, history of weight loss, presence of chest pain, performance status (Karnofsky scale), platelet count, site of disease, tumor cell type, method of diagnosis, macroscopic features of pleural surfaces, treatment modalities, and long-term survival.

2.2 Methods
Three tumor cell types were identified: epithelial, biphasic, and sarcomatous. Immunohistochemical examination was carried out in addition to morphological examination in 73% of the cases. In 21% of the cases, specimens were reassessed by a regional panel of reference pathologists in order to confirm diagnosis and histologic typing.

Thoracoscopy was performed in the operating room. Following local anesthesia and removal of the fluid, a rigid thoracoscope was used to obtain pleural specimens. If the macroscopic aspect of the pleura was evocative of a malignant lesion and the lung was judged able to re-expand, sterile talc (4 g) was insufflated. Systemic sedation and analgesia were provided as necessary. In the absence of pleural fluid on imaging studies, open pleural biopsy was performed via a minithoracotomy incision under general anesthesia.

In patients undergoing thoracoscopic or open pleural biopsy, macroscopic features of pleural surfaces were noted and classified according to the criteria outlined by Boutin and co-workers [7] as follows:

macroscopic appearance of pleural surface: non-specific inflammation, tumor-like thickening, and nodules (±thickening);
visceral pleura involvement: absent or present;
degree of involvement of pleural cavity: not assessable (non-specific inflammation), localized (≤1/3 of the cavity), and diffuse (>1/3 of the cavity).

Since June 1999, identification of potential candidates to multimodality therapy followed the criteria outlined by Sugarbaker and co-workers [5] for assessment of medical suitability and surgical resectability, with minor modifications. Patients with histologically confirmed non sarcomatous MPM, under the age of 70 years, with a Karnofsky performance status of 80% or greater, and normal liver and renal function tests, were evaluated with pulmonary function testing, quantitative ventilation-perfusion scanning, echocardiography, and computed tomographic (CT) scanning of the chest and abdomen. Additional imaging studies were performed as clinically indicated. Patients were considered suitable candidates for multimodality therapy if the predicted postoperative forced expiratory volume in 1 s was at least 1 l, and echocardiography showed a grossly normal cardiac function and an ejection fraction of >45%, with an estimated normal pulmonary artery pressure. Surgical resectability was defined by tumor confined to one hemithorax without evidence of metastatic disease, or invasion of the chest wall (preservation of extrapleural fat planes, absence of extrapleural soft tissue masses, and absence of rib displacement or infiltration) or mediastinum (normal CT attenuation values of mediastinal content), or transdiaphragmatic extension (smooth diaphragmatic undersurface). At surgery, the decision to perform a pleurectomy/decortication (P/D) as opposed to an extrapleural pneumonectomy (EPP) was based on the extent of visceral pleural involvement. P/D was performed for early stage disease in patients who had minimal or circumscribed visceral pleural tumor. EPP was carried out in patients with a confluent sheet of visceral pleural tumor involving the lung parenchyma with obliteration of the pleural space. Systematic mediastinal lymph node dissection or sampling was performed in all cases. Postoperatively, patients undergoing P/D received adjuvant chemotherapy. The combination of chemotherapy consisted of carboplatin (at an area under (plasma concentration time) the curve of 6) and paclitaxel (200 mg/m2) for four cycles administered 3 weeks apart, beginning 1–2 months after surgery. Following EPP, adjuvant chemoradiation was carried out according to the scheme of Sugarbaker and co-workers [5]. From 1 to 2 months after surgery, patients received two cycles of carboplatin (at an area under [plasma concentration time] the curve of 6) and paclitaxel (200 mg/m2), administered 3 weeks apart. Radiation therapy was then given with concurrent weekly paclitaxel, 60 mg/m2. Linear accelerators (4–10 MV) were used to deliver a dose of approximately 30 Gy to the hemithorax and 40 Gy to the mediastinum. Subsequent boosts were given to areas of gross residual disease, positive resection margins, or lymph nodes. The total maximum dose was 50–55 Gy. Two additional cycles of carboplatin and paclitaxel were administered, beginning 1 month after completion of radiation therapy.

2.3 Follow-up
Survival was measured from the date of diagnosis. All of the patients were followed up until death or for a minimum period of 2 years.

2.4 Statistical analysis
All potential prognostic indices were measured at the time of diagnosis and evaluated as categorical variables. Survival curves were computed according to the method of Kaplan–Meier. Survival comparison between groups of patients (n = 394) was performed by means of the log-rank test. Factors that significantly affected survival in univariate analysis (p < 0.10) were tested for their independent role in multivariate analysis using the Cox proportional hazards model. The stepwise backward procedure based on the likelihood ratio was used to assess the significance of covariates included in the model. Hazard ratios and 95% confidence intervals were calculated. A p value <0.05 was considered statistically significant. All analyses were conducted using the SPSS (SPSS Inc., USA) software package.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 Appendix A
 References
 
3.1 Patient's demographic and clinical data
Three hundred and ninety-four consecutive patients with pathologically confirmed MPM were assessed in a single institution between January 1989 and December 2003. Their demographic and clinical characteristics are presented in Table 1 . Median age was 64 (range 28–93) years. A routine chest radiograph incidentally revealed pleural effusion in the absence of chest symptoms in 14 patients (3.6%). Unusual clinical presentation included spontaneous pneumothorax in seven patients (1.8%). In patients with advanced age, comorbidity or poor performance status, the diagnosis of MPM was established by means of pleural fluid cytology (n = 19) or needle biopsy (n = 7). On the other hand, thoracoscopy confirmed its primary role in achieving a definitive diagnosis of MPM. However, nine patients (9/304 = 2.9%) underwent open pleural biopsy after a previous false negative thoracoscopic biopsy. In a small number of patients undergoing thoracoscopic or open pleural biopsy (15/368 = 4.1%), pleural surface showed a non-specific pseudoinflammatory aspect with scattered areas of minimal thickening, hyper-vascularization or lymphangitic aspect. Twenty-nine patients were considered to be candidates for multimodality therapy. Staging laparoscopy was performed in 17 of them (58.6%), and one patient had multiple peritoneal metastases. At subsequent thoracotomy under the same anesthetic, one additional patient was found to have unresectable tumor due to mediastinal invasion, 15 patients underwent extrapleural pneumonectomy, and 12 patients underwent pleurectomy/decortication. Complete resection of gross disease was accomplished in 22 patients (81.5%), while five patients (18.5%) had microscopically positive resection margins. According to the IMIG staging system [3], postoperative stage was I, II, III, and IV in 5, 4, 15, and 3 patients, respectively. There were 13 lymph node-negative patients, three N1 (all stage III), and 11 N2 (nine stage III and two stage IV). The final histologic subtype was epithelial in 22 cases, biphasic in five. One patient who underwent extrapleural pneumonectomy died postoperatively. Cause of death was respiratory distress syndrome. EPP-related morbidity occurred in nine patients and included (some patients had multiple complications) atrial fibrillation (four patients), respiratory failure (three patients), bleeding requiring blood transfusions (three patients), ileus (two patients), pneumonia and vocal cord paralysis (one patient each). P/D-related morbidity occurred in four patients and included bleeding requiring blood transfusions (two patients), atrial fibrillation (one patient), and retained secretions (one patient). Adjuvant chemotherapy in the 26 surviving patients was in general well tolerated. The most relevant toxicity was hematologic: grade 2–3 leucopenia in six patients, and grade 2–3 thrombocytopenia in two patients. As for non-hematologic toxicity, grade 2–3 nausea and vomiting was observed in one patient, and grade 2 neuropathy in one patient. The addition of radiation therapy did not consistently increase the overall toxicity since only two patients developed grade 2 radiation-related esophagitis. Two patients did not receive the two planned post-radiation chemotherapy courses due to patient refusal and low performance status, respectively. One-week treatment delay was performed in three patients due to toxicity.


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  		Table 1 Demographic and clinical data of the study population (n = 394)
 
3.2 Survival data
At the conclusion of this study in March 2006, 381 patients (96.7%) had died (median survival, 11.7 months; range 0.03–117.9). Median follow-up of 13 surviving patients (3.3%) was 45.2 months (range 28.7–126.5) (Fig. 1 ).


Figure 1
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  		Fig. 1. Kaplan–Meier survival curve of the entire study population (n = 394). The median survival time was 11.9 months (95% CI 10.5–13.2); 1-year and 2-year survival rates were 49.7% and 18.8%, respectively.

 
3.3 Univariate analysis
The results of the univariate analysis for each of the variables studied in this series are displayed in Table 2 . Factors that individually predicted worse prognosis were advanced age (≥70 years), presence of chest pain, history of weight loss (≥5%), poor performance status (Karnofsky scale < 80), high platelet count (≥400,000 mm3), non epithelial cell type, macroscopic appearance of pleural surface (nodules and/or tumor-like thickening), presence of visceral pleura involvement, extended degree of involvement of pleural cavity (>1/3 of the cavity), and not having undergone combined surgery and adjuvant therapy. Median survival time and 2-year survival rate were 14.6 months (95% CI 12.9–16.2) and 23.6%, respectively, in patients with epithelial cell type (n = 246), and 8.7 months (95% CI 6.1–10.4) and 11.9%, respectively, in patients with biphasic cell type (n = 84). The patients with sarcomatous cell type (n = 36) had a significantly worse prognosis: median survival time 4.5 months (95% CI 2.3–5.8), 2-year survival rate 0% (Fig. 2 ). Median survival time and 2-year survival rate were 11.8 months (95% CI 10.5–13.2) and 18%, 14.5 months (95% CI 10.8–18.1) and 29.6%, respectively, in patients undergoing diagnostic procedure only (n = 367), and in patients undergoing surgical resection with adjuvant therapy (n = 27) (Fig. 3 ). The remaining parameters failed to be significantly associated with survival in the univariate analysis.


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  		Table 2 Univariate survival analysis (n = 394)
 

Figure 2
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  		Fig. 2. Kaplan–Meier survival curves according to tumor cell type (n = 366). Cell type could not be determined in 28 patients.

 

Figure 3
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  		Fig. 3. Kaplan–Meier survival curves according to management (n = 394).

 
3.4 Multivariate analysis
The multivariate analysis was limited to patients (n = 203) in whom information on all variables was available. Accordingly, factors independently associated with decreased survival included: poor performance status, high platelet count, non-epithelial cell type, and diffuse involvement of pleural cavity (Table 3 ). The greatest hazard ratios of death were observed for sarcomatous cell type (3.78 times more in respect to patients with epithelial cell type) and diffuse involvement of pleural cavity (2.73 times as opposed to patients with pseudoinflammatory aspect of pleural surface or localized degree of involvement of pleural cavity). The following variables: advanced age, presence of chest pain, history of weight loss, macroscopic appearance of pleural surface, presence of visceral pleura involvement, and management modalities did not enter the model.


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  		Table 3 Multivariate survival analysis (n = 203)
 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
Appendix A
 References
 
Malignant pleural mesothelioma is distinctively characterised by a highly aggressive clinical behavior and a relative unresponsiveness to conventional treatments. In an effort to control symptoms and prolong survival of MPM patients, several multimodality treatment regimens, combining the so called maximal cytoreductive surgery, chemotherapy, and/or radiation therapy, have been implemented, either in an adjuvant [4–6] or neoadjuvant setting [8,9]. From these studies, it appears that multimodality therapies may provide a survival improvement in selected patients.

Our series confirms the main clinicopathologic characteristics of MPM patients. The majority were males in their sixties, with a documented history of exposure to asbestos, and smokers; they presented with chest pain and were in a poor performance status. At thoracoscopy or open pleural biopsy, pleural surfaces appeared diffusely involved by neoplastic nodules or thickenings. The most common tumor histologic type was epithelial. Only a small number of patients were deemed suitable to undergo multimodality therapy. On the whole, the prognosis of our series was dismal: overall median survival 11.9 months (95% CI 10.5–13.2), 2-year survival rate 18.8%.

Three recent, large studies have focused on the identification and evaluation of potential prognostic factors for survival in MPM patients [2,10,11] (Table 4 ).


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  		Table 4 Independent prognostic factors in MPM patients
 
Our data reveal the individual effect on survival of the following patient-related prognostic factors: age, presence of chest pain, history of weight loss, performance status, and platelet count. Among them, however, only patient performance status and platelet count were confirmed as independent prognostic factors in the multivariate analysis when adjusting for tumor characteristics. Conflicting data have been reported on the importance of many potential patient-related prognostic factors in MPM patients. However, the prognostic significance of performance status has been validated by most analyses [13].

Among the tumor-related prognostic factors in our MPM patients, the most important was tumor cell type, although several notable studies provided contradictory data [14,15]. Indeed, current routine pathologic study still focuses on morphological parameters, and does not evaluate the recently explored biological factors that may contribute to the diagnostic and prognostic evaluation of MPM.

As in other solid tumors, also in MPM patients, anatomic staging is of paramount importance for prognostic information and therapeutic decision-making. However, the eminently surgical–pathologic character of proposed staging systems underlines the limited ability of imaging techniques in assessing the locoregional disease extent accurately. On the other hand, there is little previous information regarding the potential prognostic significance of macroscopic features of pleural surfaces. Our results are in agreement with the study of Boutin and co-workers [7] in which macroscopic appearance of pleural surface, visceral pleura involvement, and degree of involvement of the pleural cavity were found to be of prognostic importance in the univariate model, and at times in the multivariate one. Prospective studies are required to validate the significance of macroscopic features of pleural surfaces as a prognostic factor.

Treatment of MPM remains largely disappointing [16]. Most patients in our study had serious disease with limited life expectancy. The survival data underscore the fact that, at present, limited therapeutic options exist for patients with MPM. However, a small number of patients (27/394 = 6.8%) did undergo multimodality treatment. In univariate analysis, these patients showed a significant survival advantage. However, after adjusting for other patient- and tumor-related prognostic factors, surgical resection and adjuvant therapy were not found to be an independent prognostic parameter. These data suggest that surgical approach may select a patient population already destined to have a good prognosis even without treatment. Indeed, the survival benefit of multimodality therapies seems to apply only to highly selected groups of patients: patients with epithelial cell type MPM, negative surgical resection margins, and negative extrapleural lymph nodes, according to Sugarbaker and co-workers [5], and patients with IMIG stage I and II, according to Rusch and co-workers [6]. Several authors have raised critical remarks on the quality of surgical literature on MPM [17–19]. Small patient groups, selection bias, lead-time bias, lack of internal control groups, variability in treatment regimens, relative inadequacy of long-term follow-up, and lack of quality of life evaluation are all issues which hinder the interpretation of the published literature on surgical and multimodality treatment of MPM.

This study has several limitations. First, the retrospective design and the extended period of data collection, during which treatment was not uniformly established, could have introduced biased information. Second, the small sample size of several groups of patients under study limits the power of our statistical analysis.

In conclusion, we can summarize our current findings as follows:

(1) Malignant pleural mesothelioma continues to represent a therapeutic challenge to the thoracic surgeon.
(2) Significant predictors of survival include performance status, platelet count, histology, and degree of involvement of pleural cavity.
(3) The retrospective design of this study and the small number of patients undergoing multimodality therapy make it hard to decipher the role of surgical resection and adjuvant therapy in the treatment of MPM.
(4) Prospective randomized studies comparing multimodality therapy to other treatment regimens as well as evaluating quality of life issues are warranted to determine the optimal treatment strategy in this disease.


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

Dr S. Cassivi (Rochester, MN): The low numbers of patients in your study make it such that your study is not powered to find a difference between surgically resected patients and those not undergoing surgery. I have a hard time, therefore, accepting the title of your presentation. With all due respect, with only 27 patients, it would be difficult to show a benefit or lack of benefit for surgery. It is a very small number of patients on which to base such a provocative title.

Dr Billé: In fact one of the main limitations of our study is the small number of several groups of patients. More specifically, the small number of patients who underwent surgical treatment does not allow us to say anything definite about surgical treatment. Most likely, surgical treatment applied only to selected patients.

Dr Cassivi: Just to clarify this, your title is: ‘Surgical resection is not an independent prognostic parameter with malignant pleural mesothelioma’. I don’t think you can say that with a low numbers of patients in your study.

Dr Billé: As a matter of fact, at multivariate analyses after adjusting for other patients – and tumor related prognostic factor, surgical resection followed by adjuvant therapy did not enter the model. Multimodality therapy showed a significant survival benefit on univariate analyses only. Most likely, the small number of patients undergoing multimodality therapy may explain why surgery confers no significant survival benefit at multivariant analyses.

Dr D.E. Wood (Seattle, WA): I guess I am confused because your survival curves showed a significant difference between treatment but then you are saying that you are considering this a negative study at least for surgical intervention, because of a lack of a difference in the multivariant analyses. I guess when one looks at how we deliver a message in a paper, it sounds like your conclusion is that surgery doesn’t add survival benefit for a mesothelioma. I don’t really think that is what you mean to have as your conclusion, nor is your paper constructed to adequately address that issue, so I would argue that the title and the conclusion end up delivering a potentially incorrect and even dangerous message. Our colleagues outside of thoracic surgery may try to use this conclusion as an excuse for excluding thoracic surgeons in the management of mesothelioma.

Dr Billé: The small number of patients undergoing multimodality therapy can probably explain why surgery confers no significant survival benefit at multivariate analyses. The message is that randomized controlled trials are eagerly needed in order to confirm the survival advantage of multimodality therapy

Dr T.W. Rice (Cleveland, OH): I would not implicitly trust your multivariable analyses, just because you don’t find a difference doesn’t mean one doesn’t exist. And a further problem is that very few people have undergone surgery. Rather than assuming that surgery isn’t a factor, you could examine the data to see if significant variables are being missed. You could resample your data many times, a bootstrap analyses, to make sure the variables show up in all the resampling. It may also identify significant ‘lurking’ variables by looking at all these resamplings. Resection may be important. You have to go one step beyond multivariable analyses.

Another way to solve the problem is to look at the 27 patients who had a resection and match those patients to 27 identical patients who did not have a resection, propensity matches.

I think your paper would be much more powerful if you bootstrap the multivariable analyses and make sure these factors come up in the 1000 resamplings and try to add propensity matching to the analyses. Then you are more likely to make pertinent conclusions. Just because surgery does not come up in the analyses, maybe that there are too few people with surgery in your group. You have to be a little bit more careful. I would not throw away your work, but I would improve the analyses.

Dr P. Pafko (Prague, Czech Republic): Extrapleural pneumonectomy is a complicated procedure, my question is in which percentage of your patients is the operation finished as RO, R1 and R2?

Dr Billé: Complete resection of gross disease was carried out in 22 patients, while five patients had microscopically positive resection margins.


   Acknowledgments
 
We would like to thank Susanna Cappia BscD for her valuable help with the pathologic study.


   Footnotes
 
\#9734; Presented at the 15th European Conference on General Thoracic Surgery, Leuven, Belgium, June 3–6, 2007.


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

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  6. Rusch VW, Rosenzweig K, Venkatraman E, Leon L, Raben A, Harrison L, Bains MS, Downey RJ, Ginsberg RJ. A phase II trial of surgical resection and adjuvant high-dose hemithoracic radiation for malignant pleural mesothelioma. J Thorac Cardiovasc Surg 2001;122:788-795.[Abstract/Free Full Text]
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