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Ann Thorac Surg 1999;68:1799-1804
© 1999 The Society of Thoracic Surgeons

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Original Articles

Important prognostic factors in patients with malignant pleural mesothelioma, managed surgically

^a Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York, USA
^b Biostatistics Service, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

Address reprint requests to Dr Rusch, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, Rm C-867, New York, NY 10021
e-mail: ruschv{at}mskcc.org

Presented at the Poster Session of the Thirty-fifth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 25–27, 1999.

	Abstract

Top Abstract Introduction Patients and methods Results Comment References

 
Background. The factors influencing outcome after resection of malignant pleural mesothelioma (MPM) are controversial. This analysis of a prospective surgical database identifies important prognostic factors.

Methods. Tumors were staged by the International Mesothelioma Interest Group staging system, and patients were followed until death. Prognostic factors were analyzed by log rank and Cox regression, and were considered significant if p was less than 0.05.

Results. From Oct 1983 to May 1998, 231 patients underwent thoracotomy, 115 had extrapleural pneumonectomy (EPP), and 59 pleurectomy/decortication (P/D). Among patients having EPP or P/D, 142 received adjuvant therapy. The median survival for stage I tumors was 29.9 months, for stage II 19 months, for stage III 10.4 months, and for stage IV 8 months. By multivariate analysis, stage, histology, gender, adjuvant therapy, but not the type of surgical resection, were significant.

Conclusions. The better survival previously reported for P/D compared with EPP is not seen in a large database with long follow-up. Stages I and II have better survival rates than generally assumed for MPM. Locally advanced T and N status, and nonepithelial histology, identify poor prognosis patients who should be considered for novel treatment regimens.

	Introduction

Top Abstract Introduction Patients and methods Results Comment References

 
In recent years, several retrospective surgical series have sought to define prognostic factors in malignant pleural mesothelioma (MPM) [1–5]. The identification of such factors is particularly important in MPM, a malignancy whose clinical behavior and biology are poorly understood and for which there is still no standard treatment. Although tumor stage and histology are consistently reported to affect overall survival, the prognostic significance of other variables such as patient gender, the type of surgical resection, and the use of adjuvant therapy remains controversial. In addition, the pattern of nodal metastases in MPM and the correlation between overall survival and the extent of nodal disease are unknown.

This analysis of prognostic factors in patients undergoing surgery for MPM is derived from a prospective database initiated in 1983. Although the type of adjuvant therapy varied because patients were entered on sequential clinical trials, the criteria for operation, the approach to surgical resection, and the methods of follow-up were uniform. During the 15 years covered by this report, patients had either a pleurectomy/decortication or extrapleural pneumonectomy performed based on the local extent of their tumor (T status) and the clinical trial being performed at that time. These circumstances permit a reliable analysis of prognostic factors in malignant mesothelioma, which in turn allows stratification of patients who are entered into clinical trials.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment References

 
All patients entered in this prospective registry had biopsy-proven MPM and underwent exploratory thoracotomy by the same surgeon (V.R.). The pathological diagnosis was based on both histology and immunohistochemistry, and when necessary, electron microscopy. Data collected in the registry included patient name, gender, age, date of operation, preoperative platelet count, type of procedure, extent of resection, tumor histology, extent of the primary tumor and presence of nodal metastases, operative morbidity and mortality, type of adjuvant therapy, date and site of first relapse, and dates of last follow-up or death with disease status.

The primary tumor was considered potentially resectable if preoperative computed tomographic (CT) scans of the chest and abdomen did not show extrathoracic disease, or clear invasion of the mediastinal organs or chest wall or extension through the diaphragm. The decision to perform an extrapleural pneumonectomy as opposed to a pleurectomy/decortication for resection was based on the extent of visceral pleural tumor at thoracotomy. Extrapleural pneumonectomy, defined as an en bloc resection of the pleura, lung, ipsilateral diaphragm, and pericardium, was performed for locally advanced disease, usually in patients with confluent visceral pleural tumor not separable from the lung and a partially or totally fused pleural space. Pleurectomy/decortication, which removes all gross tumor without removing the underlying lung, was performed in patients who had minimal visceral pleural tumor. Partial parietal pleurectomy was sometimes performed for control of a pleural effusion if the patient was found to have incompletely resectable tumor at exploration, but pleurectomy/decortication and extrapleural pneumonectomy were performed only if it was thought that all gross tumor could be removed. Complete resection was defined as no gross residual tumor. Resection was defined as incomplete if there was any visible gross tumor remaining at the completion of thoracotomy, even if this were a few scattered tumor foci less than 1 cm in size.

The International Mesothelioma Interest Group (IMIG) staging system [6] was used to determine T and N status and tumor stage. Most of the patients entered in this registry were also enrolled in clinical trials, and postoperative adjuvant therapy, if any, was determined by those protocols. Adjuvant chemotherapy was only given in the protocol setting. Patients not entered on a clinical trial usually received postoperative hemithoracic radiation. The total radiation dose and method of administration depended on whether or not a pneumonectomy was performed.

Patients who had unresectable tumor at thoracotomy were followed clinically until death. Patients who had a pleurectomy/decortication or extrapleural pneumonectomy were followed by physical exam and CT scans of the chest and abdomen every 3 months until the time of first recurrence. Additional imaging studies or biopsies were performed as necessary to document recurrent disease. Thereafter, they were also followed clinically until the time of death.

Survival probabilities were calculated by the product limit method of Kaplan and Meier. The prognostic significance of factors were tested in a univariate model by log rank statistic for categorical covariates, and by proportional hazards regression for continuous covariates. Proportional hazards regression was used to test the prognostic significance of factors in a multivariate model. The p value was considered significant when it was less than 0.05 [7–9].

	Results

Top Abstract Introduction Patients and methods Results Comment References

 
From October 1983 to May 1998, 231 consecutive patients underwent thoracotomy for possible resection of malignant mesothelioma. There were 192 men and 39 (16.8%) women, with a median age of 62 years (range 24 to 80 years). Only 5 of the women (12.8%) compared with 138 of the men (71.8%) had known asbestos exposure. Of the 231 patients who underwent surgical exploration, 174 (75%) had a complete resection via either extrapleural pneumonectomy in 115 cases (50%) or pleurectomy/decortication in 59 cases (26%). Palliative pleurectomy or exploration only were performed in 57 patents (24%). The sizeable number of patients in this category reflects a liberal policy of surgical exploration but a strict criterion of not performing an extrapleural pneumonectomy or pleurectomy/decortication unless all tumor could be resected. The median age of the patients undergoing extrapleural pneumonectomy was 61 years (range 24 to 79 years), similar to that of the entire patient group. The 30-day operative mortality was 3.5% (8/231 patients), and was 5.2% (6/115) for the patients who had an extrapleural pneumonectomy. None of the patients who had a palliative pleurectomy or exploration only died postoperatively.

In 164 of the 231 patients (71%), the histologic tumor type was epithelial, whereas it was fibrosarcomatous in 14 patients (6%), of mixed cellularity in 51 patients (22%), desmoplastic in 1 patient, and not specified in 1 patient. The preoperative platelet count, recorded in 220 patients, was elevated (> 400,000) in 60 cases and was normal in 160 patients.

According to the IMIG staging system, 21 patients had stage I (T1N0) tumors, 40 had stage II (T2N0) tumors, 102 patients had stage III (T3 or N1-2) tumors, and 68 patients had stage IV (T4 or N3 or M1) disease based on surgical and pathological staging. Of the 157 patients for whom complete information was available about nodal involvement, only 9 had nodal metastases confined to N1 sites, whereas 82 patients had N2 disease and 1 had N3 disease. The sites of lymph node involvement by lymph node stations are shown in Figure 1. These nodal stations are designated according to the lymph node mapping systems used for non-small cell lung cancer and esophageal cancer [10, 11].

View larger version (15K): [in this window] [in a new window]   Fig 1. Location of lymph node metastases by nodal station for right-sided (A) (n = 54) and left-sided (B) (n = 55) resections. The nomenclature for lymph node stations is that used for non-small cell lung cancer [10] and esophageal cancer [11]. Most patients who had lymph node metastases had more than one nodal station involved, so the number of metastatic sites exceeds the number of resections.

The univariate analyses of overall survival according to T status, N status, and stage are shown in Figures 2, 3, and 4. When analyzed across all four subsets, T status had a significant impact on overall survival (p < 0.01). Comparisons of individual T status categories (Fig 2) showed no difference in survival for T1 versus T2 (p = 0.46), but significant differences for T2 versus T3 (p = 0.02), and T3 versus T4 (p = 0.024). However, the small number of patients who had T1 tumors (n = 28) makes the comparison of the T1 and T2 subsets less reliable.

View larger version (18K): [in this window] [in a new window]   Fig 2. The relationship between tumor T status and overall survival by univariate analysis. When considered across all four categories, T status had a highly significant effect on survival (p < 0.01).

View larger version (15K): [in this window] [in a new window]   Fig 3. Univariate analysis of the relationship between the number of positive lymph nodes and overall survival. Patients who had four or more positive nodes had a significantly worse survival (p < 0.01).

View larger version (19K): [in this window] [in a new window]   Fig 4. Overall survival of all 231 patients by stage. When analyzed across all four categories, stage had a highly significant effect on survival (p < 0.01).

Tumor stage had a significant impact on overall survival (Fig 4) when analyzed across all four stage categories (p < 0.01). The median survival for stage I tumors was 29.9 months. This was not significantly different from the median survival of 19 months for stage II tumors (p = 0.163), but the small number of patents with stage I (n = 21) tumors potentially affects this comparison. The median survival for stage III tumors was 10.4 months, and for stage IV disease, 8 months. The differences in median survival times were significant for stage II versus stage III (p = 0.002), and approached significance for stage III versus stage IV (p = 0.074).

For purposes of survival analysis, the smaller numbers of tumors of mixed cellularity, fibrosarcomatous, and desmoplastic histology were grouped together and compared with tumors of pure epithelial histology. There was a highly significant difference in survival between these two histological groups in favor of the pure epithelial tumors (p < 0.01).

The use of adjuvant therapy varied in this series. Systemic chemotherapy was offered to patients who had unresectable tumors at thoracotomy. For patients who had a complete resection by extrapleural pneumonectomy or pleurectomy/decortication, the type of adjuvant therapy varied primarily according to several clinical trials performed over the duration of this registry. Of the 174 patients who had either an extrapleural pneumonectomy or pleurectomy/decortication, complete information about adjuvant therapy was available in 166 cases at the time of this analysis. Twenty-four patients received no adjuvant treatment, whereas 142 patients had adjuvant therapy, including 106 patients who had radiation without chemotherapy, 29 patients who had chemotherapy without radiation, and 7 patients who received both chemotherapy and radiation. Adjuvant therapy appeared to confer a significant survival benefit (Fig 5), although this result must be interpreted with caution because of the relatively small number of patients who did not receive any postoperative treatment and the different types of adjuvant therapy given.

View larger version (17K): [in this window] [in a new window]   Fig 5. Comparison of the overall survival rates of patients who received adjuvant therapy versus those who did not, showing that adjuvant therapy was associated with a significantly better outcome (p < 0.01).

View larger version (16K): [in this window] [in a new window]   Fig 6. Overall survival analyzed according to the type of surgical procedure performed. There was no significant difference between patients who had all gross tumor removed via extrapleural pneumonectomy versus pleurectomy/decortication.

	Comment

Top Abstract Introduction Patients and methods Results Comment References

 
The treatment of malignant pleural mesothelioma remains controversial, partly because the natural history, the role of surgical resection, and the factors influencing prognosis have not been fully defined [3, 5]. The recent development of an international staging system by the IMIG provides the means to compare clinical outcome across institutions around the world, an important issue with respect to developing treatment for this uncommon malignancy [6]. Although the staging system was developed from contemporary information about the relationship between T and N status, tumor stage, and survival [2, 12–14], it will probably require revision as additional data become available, especially regarding the patterns and prognostic importance of nodal disease. Other prognostic factors also need to be evaluated.

This series extends our prior work examining prognostic factors in malignant pleural mesothelioma. It confirms that stage I and II tumors have a much more favorable survival than was previously assumed for malignant mesothelioma, and suggests that surgical resection and adjuvant therapy may improve survival. T1 tumors and stage I disease exhibit a trend toward better survival compared with T2 and stage II. The lack of statistical significance for this difference should be reexamined as larger numbers of patients with early stage disease are treated. The median survival of 29.9 months for stage I disease, all of which were T1b tumors, appears superior to the 7-month median survival for the same stage tumors reported by Boutin and associates [14]. In addition, several prior series, in which patients did not routinely undergo surgical resection, report few or no patients surviving beyond 4 years [3, 5, 12]. Although ideally, the impact of treatment on survival would be determined through prospective randomized trials comparing specific therapies with supportive care alone, such trials are unlikely to occur given patient and physician bias and the low incidence of this disease. When considered in aggregate, the data in this and in other series suggest a survival benefit, and not merely a lead time bias, for patients with stage I and II disease who undergo surgical resection and some type of adjuvant therapy [1, 4, 15]. These data should dispel some of the nihilism about malignant mesothelioma and encourage early diagnosis and treatment.

In contrast, patients who have nonepithelial tumor histology, nodal metastases, or T3/T4 tumors have a poor prognosis even when complete surgical resection is performed. In this regard, our data parallel those from other recent series and underscore the need to identify these patients before thoracotomy. Entering such patients into clinical trials testing novel treatment strategies is appropriate. T4 tumors, and to some extent T3 tumors, can usually be identified by thoracoscopy, CT imaging, and when necessary, laparoscopy [16]. The detection of nodal metastases is more problematic. CT and magnetic resonance imaging are not useful in this regard [17]. Importantly, new data from this series suggest that superior mediastinal lymph nodes accessible to mediastinoscopy are frequently involved (Fig 1), but that approximately 25% of cases may have nodal disease confined to areas such as the peridiaphragmatic or internal mammary regions that are biopsied only at thoracotomy. Currently, the combination of CT imaging, thoracoscopy, mediastinoscopy, and occasionally laparoscopy may be the best approach to pretreatment of staging. However, 10% to 20% of patients will likely prove to have more advanced disease than anticipated despite these procedures.

The information from this series about the relationship between the number of positive lymph nodes and survival is novel and needs further validation in larger numbers of patients. If indeed this proves correct, it may be appropriate to use this as a stratification factor in clinical trials.

Our results also suggest that lymph node metastases are frequent in mesothelioma and that the pattern of lymph node involvement is very different from what occurs in non-small cell lung cancer. Specifically, metastases confined to N1 nodes appear to be uncommon, and involvement of mediastinal lymph nodes in unusual locations (eg, paravertebral, internal mammary, peridiaphragmatic) often occurs. When the IMIG staging system was developed, N1 and N2 nodal involvement were placed together into stage III disease. In the absence of further information, this stage classification remains appropriate, but the prognostic impact of N1 disease only needs further investigation.

The importance of the type of surgical resection, ie, an extrapleural pneumonectomy or a pleurectomy/decortication, has been a controversial issue for a long time because of the higher operative risk of extrapleural pneumonectomy [4, 5, 13, 18–21]. With longer follow-up in larger numbers of patients, this analysis strongly confirms our previous supposition that the type of surgical resection does not have an impact on survival. However, it must be emphasized that both of these procedures were performed only if they led to complete resection of all gross tumor. In patients who have bulky or confluent visceral pleural tumor, it is difficult to achieve a complete resection except by extrapleural pneumonectomy.

Finally, both univariate and multivariate analyses suggest that adjuvant therapy confers a survival benefit in patients who have a complete surgical resection. In this series, hemithoracic radiation was the most common form of adjuvant therapy. Although this preliminary information is encouraging, the potential benefit of various types of adjuvant therapy should be systematically explored in prospective clinical trials. The main value of this experience is to provide a benchmark against which the results of clinical trials can be judged.

In summary, our experience provides the basis of selecting patients for clinical trials. It identifies several prognostic factors such as nodal disease that warrant further investigation. Finally, it confirms the relatively favorable survival of stage I and II disease, and suggests that such patients probably benefit from surgical resection and adjuvant therapy. Unfortunately the majority of patients in this series were referred for treatment when they already had stage III disease, and therefore a relatively poor prognosis. These data should encourage early diagnosis and treatment for MPM, just as for all other cancers.

	Acknowledgments

 
We thank Melody Owens for her outstanding assistance in data management and manuscript preparation.

	References

Top Abstract Introduction Patients and methods Results Comment References

 

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