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J Thorac Cardiovasc Surg 2008;135:620-626
© 2008 The American Association for Thoracic Surgery
General Thoracic Surgery |
a Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, NY
b Biostatistics Service, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, NY
c Department of Pathology, Memorial Sloan-Kettering Cancer Center, New York, NY
d Department of Cardiothoracic Surgery, New York University Medical Center, New York, NY
e Department of Pathology, University of Hawaii, Honolulu, Hawaii
Received for publication May 3, 2007; revisions received September 13, 2007; accepted for publication October 22, 2007. * Address for reprints: Raja M. Flores, MD, Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, Room C-879, New York, NY 10021. (Email: floresr{at}mskcc.org).
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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Methods: Patients with malignant pleural mesothelioma who underwent extrapleural pneumonectomy or pleurectomy/decortication at 3 institutions were identified. Survival and prognostic factors were analyzed by the Kaplan–Meier method, log-rank test, and Cox proportional hazards analysis.
Results: From 1990 to 2006, 663 consecutive patients (538 men and 125 women) underwent resection. The median age was 63 years (range, 26–93 years). The operative mortality was 7% for extrapleural pneumonectomy (n = 27/385) and 4% for pleurectomy/decortication (n = 13/278). Significant survival differences were seen for American Joint Committee on Cancer stages 1 to 4 (P < .001), epithelioid versus non-epithelioid histology (P < .001), extrapleural pneumonectomy versus pleurectomy/decortication (P < .001), multimodality therapy versus surgery alone (P < .001), and gender (P < .001). Multivariate analysis demonstrated a hazard rate of 1.4 for extrapleural pneumonectomy (P < .001) controlling for stage, histology, gender, and multimodality therapy.
Conclusion: Patients who underwent pleurectomy/decortication had a better survival than those who underwent extrapleural pneumonectomy; however, the reasons are multifactorial and subject to selection bias. At present, the choice of resection should be tailored to the extent of disease, patient comorbidities, and type of multimodality therapy planned.
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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The role of surgical resection, especially extrapleural pneumonectomy (EPP), in the management of malignant pleural mesothelioma (MPM) is controversial. EPP usually involves an en bloc resection of lung, pleura, pericardium, and diaphragm, whereas pleurectomy/decortication (P/D) involves resection of the parietal and visceral pleurae, pericardium, and diaphragm when necessary, but spares the lung. The goal of surgery is to remove all gross disease, but a complete resection (R0) with surgery alone is theoretically unattainable because of the inability to eradicate residual microscopic disease regardless of whether an EPP or P/D is performed. Therefore, treatment has focused on surgery in combination with radiation and/or chemotherapy in a multimodality setting.
The majority of studies have included exclusively either P/D or EPP in conjunction with preoperative or postoperative chemotherapy, intrathoracic chemotherapy, postoperative external beam radiotherapy, intensity-modulated radiation therapy, intraoperative radiotherapy, brachytherapy, photodynamic therapy, and a number of other novel adjuvants.1-11
However, the decision to perform either EPP or P/D in multimodality studies is based predominantly on surgeon bias rather than scientific data.
Several studies have chosen end points, such as time to progression and patterns of recurrence, to justify the preferred procedure because the numbers are too small to demonstrate statistically significant differences in survival.12-14 However, these end points are fraught with inaccuracy because the follow-up practices, definitions of progression of disease, and ways of documenting recurrence vary greatly. Thus, rates of progression-free survival may differ considerably from overall survival. Therefore, this study was undertaken to investigate the outcomes of EPP and P/D with overall survival as the primary end point.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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Pathologic stage was based on the pathologist's evaluation of the resected specimen and the surgeon's intraoperative findings. All patients were followed until the date of death or the date of last follow-up if still alive. Dates of death were verified through the Social Security Death Index and personal telephone communications.
Treatment selection was based primarily on the tumor stage, patients' overall medical condition, and requirements of several prospective clinical trials performed during this time period. Operative intervention was recommended to patients with tumor localized to the hemithorax by computed tomography scan and adequate cardiopulmonary function testing. Routine mediastinoscopy and magnetic resonance imaging were not performed. Positron emission tomography has only recently been used for clinical staging. EPP was defined as an en bloc resection of the pleura, lung, ipsilateral diaphragm, and pericardium. P/D removed tumor with the parietal and visceral pleurae and pericardium and/or diaphragm when necessary without removing the entire underlying lung. In patients not participating in protocols that mandated either EPP or P/D, the decision to perform an EPP or P/D was based on intraoperative findings, tumor stage, patients' medical condition, and surgeons' intraoperative judgment about which procedure would permit resection of all gross tumor. The decision to perform chemotherapy or radiation was based on enrollment in a clinical trial. The total radiation dose and method of administration was dependent on whether an EPP or a P/D had been performed.16,17 When a patient could not participate in a clinical trial, therapy was administered according to protocol guidelines.
Statistical Methods
Comparison of proportions of prognostic variables in EPP and P/D were assessed by the Pearson chi-square test. Operative mortality included all patients who died within 30 days of surgery or during the same hospitalization. Survival was calculated from the date of surgery until the date of death or the date of last follow-up. Survival and prognostic factors were analyzed by the Kaplan–Meier method, and the log-rank test was used to assess statistical significance. A Cox proportional hazard analysis was used to assess the joint influences of predictors on survival. Insignificant variables were then excluded from the analysis using a stepwise procedure, thus yielding the final model. The Stata 8 (Stata Corp, College Station, Tex) statistical package was used.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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Table 1. P/D had a significantly greater proportion of patients who were several years older with early stage tumors, whereas patients undergoing EPP were more likely to receive multimodality therapy, have a higher proportion of epithelioid tumors, and have a greater frequency of asbestos exposure. Postoperative complications recorded according to the Common Terminology Criteria for Adverse Events version 3.0 grading system are outlined in Table E2. It was not surprising that the most common adverse events among patients undergoing EPP were atrial arrhythmias and respiratory complications. Severe or life-threatening (grades 3–5) respiratory complications occurred in 10% of patients undergoing EPP. Serious respiratory complications were less frequent after P/D, occurring in 6.4% of patients, but were still the most common adverse event. Patterns of recurrence are outlined in
Table 2.
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Figures 1 and 2). Female gender (P < .001) and multimodality treatment (P < .001) were significantly associated with improved survival. History of asbestos exposure demonstrated a slightly improved survival for patients without asbestos exposure (P = .06). Laterality and surgeon were not significant.
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Figure 3), even when operative deaths were excluded. An analysis of surgical procedure in relationship to American Joint Committee on Cancer tumor stage was performed to identify differences in survival in favor of EPP versus P/D. There was no statistical difference in survival by procedure at any individual tumor stage (
Figures 4–7). Only 14 patients underwent EPP with stage IV disease (usually T4 tumors) with a median survival of 4 months.
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Table 3).
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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These changes have led to wide variations and considerable controversy in the use of EPP or P/D for resection of MPM. Controversy over EPP and P/D focuses on their relative merits with respect to operative risk, ability to remove all gross tumor, and options for adjuvant therapy. Proponents of EPP believe that it more frequently allows a complete removal of all gross tumor (R0/R1 resection), with increasingly acceptable rates of morbidity and mortality, and facilitates the administration of postoperative high-dose hemithoracic radiation, which in turns provides excellent local control.6 Proponents of P/D believe that it provides adequate cytoreduction, especially for patients with earlier stage tumors, is associated with a lower morbidity and mortality than EPP, and is an effective part of a multimodality treatment program in conjunction with therapies such as photodynamic therapy, intrapleural or systemic chemotherapy, and intensity-modulated radiation therapy.1,2,4-6,10,11
Our results in this study reflect all of the pros and cons and the controversies surrounding the use of EPP and P/D. In a patient population who are typical for MPM (given age, gender, tumor stage, and histology), our decision to perform an EPP or P/D was based on a combination of factors, including patient operative risk, technical ability to remove all gross disease, and participation in a series of clinical trials that mandated performing either one operation or the other. Although our study is retrospective, it benefits from being multicenter and including a larger number of patients than other surgical series, and therefore has a greater statistical power to identify potential survival differences between EPP and P/D. Our results confirm previous smaller studies with respect to the lower mortality of P/D, differences in postoperative adverse events, and patterns of relapse. Patients who undergo EPP and adjuvant therapy, particularly high-dose hemithoracic radiation, relapse predominantly in distant sites, whereas after P/D disease progression occurs predominantly locally in the ipsilateral hemithorax.1,2,4-6,16 Any clinician who treats patients with MPM is well aware of these differences in disease progression that lead to notable differences in patient symptoms during the latter phases of their disease. Local disease progression after P/D leads to death from worsening restrictive lung disease, intractable chest pain, and respiratory failure. Distant disease progression, usually after EPP, manifests most frequently with dyspnea from a contralateral pleural effusion, ascites, or both.
The relative impact of EPP and P/D on overall survival is less clear. The results of our univariate analyses suggesting a strong survival benefit for P/D become only marginally significant (hazard ratio = 1.4) when considered in a multivariable analysis that accounts for other important variables, such as tumor stage, histology, gender, and multimodality treatment. This emphasizes the importance of considering surgical data within the context of known prognostic factors. Viewed from the most nihilistic perspective, these results could be interpreted as indicating that neither approach to resection influences overall survival that is primarily dependent on tumor histology, stage, nonsurgical therapy, and various still undefined biological factors. Previous series and clinical trials argue against this perspective,1-3,6 but ultimately this question may be answered by a randomized clinical trial currently under way in the United Kingdom that addresses the survival benefit of EPP relative to nonsurgical therapy. Viewed from another perspective, our results could be interpreted as emphasizing the lack of truly effective systemic therapy for MPM. For instance, patients who underwent EPP who receive adjuvant hemithoracic radiation have a low risk of local recurrence but currently have no available systemic therapy that significantly reduces the risk of distant metastases.1,2,6,14 No matter what the efficacy of EPP or P/D in removing gross tumor, the lack of highly effective adjuvant therapy for both of these operations leads to similar results in terms of overall survival. By contrast, locally advanced ovarian cancer, which is currently managed with a combination of vigorous surgical cytoreduction and adjuvant chemotherapy, is potentially curable, not only because of the proven benefits of resection but also because of the effectiveness of current chemotherapy for that disease.
Our study suffers from a lack of comorbidity data. Although patients undergoing EPP are more likely to have less comorbid disease than those undergoing P/D, this bias would tend to falsely inflate survival results in the EPP group. Selection bias plays a large role in determining who receives EPP or P/D on the basis of intraoperative findings. There are probably unmeasurable differences in the extent of disease not accounted for in the staging system that may make the tumor stage in patients undergoing EPP even more advanced within the same stage, thus falsely favoring survival in the P/D group. In addition, the ability of patients to undergo adjuvant therapy is biased based on their postoperative functional status, which, per se, would account for the differences in survival between patients undergoing multimodality therapy versus patients undergoing surgery alone. This finding would tend to favor EPP because 69% of patients receiving EPP underwent multimodality therapy compared with 58% of patients receiving P/D. Regardless of controlling for all known biases, the data by its retrospective nature are limited and the influence of unknown confounding variables cannot be accounted for short of a randomized trial.
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Conclusions |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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Figure E1 |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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Table E1 |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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AJCC, American Joint Committee on Cancer; EPP, extrapleural pneumonectomy; P/D, pleurectomy/decortication.
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Table E2 |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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EPP, Extrapleural pneumonectomy; P/D, pleurectomy/decortication.
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Footnotes |
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Dr Pass reports consulting fees from GlaxoSmithKline and Astra Zeneca.
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsFigure E1Table E1Table E2References |
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A. Nakas, D. S. Trousse, A. E. Martin-Ucar, and D. A. Waller Open lung-sparing surgery for malignant pleural mesothelioma: the benefits of a radical approach within multimodality therapy Eur J Cardiothorac Surg, October 1, 2008; 34(4): 886 - 891. [Abstract] [Full Text] [PDF]
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