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Eur J Cardiothorac Surg 2007;31:765-770. doi:10.1016/j.ejcts.2007.01.064
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

Case-control study between extrapleural pneumonectomy and radical pleurectomy/decortication for pathological N2 malignant pleural mesothelioma

Antonio E. Martin-Ucar, Apostolos Nakas, John G. Edwards, David A. Waller*

Department of Thoracic Surgery, Glenfield Hospital, Leicester, United Kingdom

Received 19 September 2006; received in revised form 25 December 2006; accepted 15 January 2007.

* Corresponding author. Address: Department of Thoracic Surgery, University Hospitals Leicester NHS Trust, Glenfield Hospital, Groby Road, Leicester LE3 9QP, United Kingdom. Tel.: +44 116 256 3959; fax: +44 116 236 7768. (Email: david.waller{at}uhl-tr.nhs.uk).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Objective: To compare the outcomes of extrapleural pneumonectomy (EPP) and radical pleurectomy/decortication (P/D) for N2 malignant pleural mesothelioma (MM). Patients and methods: In a retrospective case-control study we analysed the results of the 57 patients [49 male and 8 female, median age 59 (range 14–70) years] who underwent radical surgery for MM found to have pathological N2 disease over a 7-year-period. EPP was performed on 45 and P/D on 12 patients. Prognostic factors, postoperative course, pathological data and postoperative survival were analysed. Results: Those in the P/D group were significantly older (median age 62 vs 58 years, p = 0.03) than in the EPP group. There was no difference in postoperative hospital stay (p = 0.1) nor T stage (p = 0.7) between the groups. There were no significant differences in the proportion of patients undergoing some adjuvant therapy in each group (p = 0.2). Mean survival from diagnosis was 15 months in the EPP group and 16 months for those who underwent P/D (p = 0.4). Conclusions: Preservation of the lung during radical surgery for N2 MM does not compromise survival even in an older group population. We therefore now have ceased to perform EPP in cases of N2 disease and we make every effort to accurately stage patients with mediastinoscopy to identify them.

Key Words: Malignant mesothelioma • Extrapleural pneumonectomy • Decortication • Pleurectomy


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Discussion
 Appendix A
 References
 
Despite the increasing interest in radical surgery for malignant mesothelioma (MM), there is no consensus regarding whether extrapleural pneumonectomy (EPP) should be offered to patients with N2 disease. Positive N2 or extrapleural nodes confer a worse prognosis than either N0 or N1 status [1–3] but this is not a universal finding [4,5]. Because of the lack of proven benefit of staging procedures in prospective studies the protocol for preoperative staging varies between units. Some groups do perform universal preoperative mediastinoscopy [6] and even more extended surgical staging procedures have been proposed incorporating laparoscopy and peritoneal lavage cytology [7]. However, some perform mediastinoscopy to exclude positivity in contralateral nodes only and still offer EPP if ipsilateral mediastinal lymph node metastasis is present. Only recently we have found that the size of mediastinal nodes does not correlate with the presence of metastasis [8] and we now advocate video-assisted mediastinoscopy in all current cases being considered for EPP, but that was not our routine practice in the past.

An alternative operation, radical pleurectomy and decortication (P/D) has been proposed as the appropriate surgical procedure for early stage MM, with EPP reserved for more bulky disease [3]. P/D involves excision of the entire parietal and visceral pleura, including resection and reconstruction of the pericardium and diaphragm [9]. In the experience of Rusch, survival was greater for the group of patients undergoing P/D than for EPP, which was probably a reflection of stage [3]. The main advantages of this approach are the preservation of the lung and may be a reduction of the possible complications inherent to EPP. Sugarbaker and colleagues reported their results of P/D in patients probably not medically fit to undergo EPP [10]. As the morbidity/mortality of EPP is high [11,12] and the prognosis for patients with N2 disease following EPP is poor, we aimed to assess whether P/D is a suitable alternative to EPP in patients with N2 malignant pleural mesothelioma.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Discussion
 Appendix A
 References
 
Over a 7-year-period (August 1999–May 2006) a retrospective review of a single surgeon's practice identified 57 patients [49 male and 8 female, median age 59 (range 14–70) years] who had undergone radical surgery for MM with N2 pathological stage. Forty-five patients had undergone EPP and 12 had P/D. Patients in the P/D group were significantly older then in the EPP group (p = 0.03). Operative side and gender distribution were similar in the two groups (Table 1 ).


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  		Table 1 Demographics of the groups
 
2.1 Preoperative assessment
A diagnosis of malignant mesothelioma was made by percutaneous core, thoracoscopic or open pleural biopsy in all cases, confirmed with an appropriate panel of immunohistochemical stains. Patients with a diagnosis of sarcomatoid mesothelioma did not undergo further evaluation for radical surgery, but this was not contraindicated in those who had received a previous pleurodesis. All patients underwent contrast enhanced thoracic computed tomography (CT) to assess local tumour invasion, mediastinal lymph nodes and contralateral pleural involvement. Contrast enhanced magnetic resonance imaging [13] was used to evaluate invasion into the mediastinum or across the diaphragm. The majority of these patients belong to the era when we did not universally employ cervical mediastionscopy as staging [6]. Preoperative echocardiography was employed in all patients under assessment for radical surgery to mainly exclude right-sided heart dysfunction. Extrapleural pneumonectomy was offered to patients who were deemed resectable and medically operable. Those with pathological involvement of mediastinal N2 nodes on mediastinoscopy (n = 4) were offered radical pleurectomy, as were those who had resectable disease but who were judged not fit for EPP (n = 5), patients who declined EPP (n = 2), and unable to completely excised the tumour at thoracotomy (n = 1).

2.2 Operative techniques
EPP was performed with standard techniques, resecting the lung, pericardium and diaphragm en-bloc, with reconstruction of the diaphragm with a Gore-Tex Dual Mesh patch (W.L. Gore & Associates, Inc.) and the pericardium with a non-absorbable mesh patch. Radical P/D was performed via a posterolateral thoracotomy through the sixth intercostal space. We do not excise the rib to achieve more exposure. The dissection of the extrapleural plane is performed as for EPP normally dissecting the apical region first, with care not to injury the great vessels. The internal thoracic vessels are routinely ligated and divided. In the right side care is taken to avoid injury to the azygos vein and in the left to avoid injury to aorta and hemiazygos. The risk to damage the oesophagus is minimized by the insertion of a bougie at surgery. The pericardium in contact with the mediastinal pleura is excised, but the plane of dissection carried onto the lung at the hilar pleural reflection. A complete visceral pleurectomy is performed, continuing dissection down and including the fissures (Fig. 1 ). Once the lung is fully decorticated, the diaphragm is excised as for an EPP, although, if possible, attempts are made to preserve as much of the diaphragmatic muscle as possible. The central tendon is almost always excised. With radical P/D, it may be possible to deliver the pleurae, pericardium and diaphragm en bloc (Fig. 2 ). Reconstruction of the diaphragm and pericardium is performed as for EPP. Two or three 32F intercostal drains are placed to the apex and base of the pleural cavity. Application of a fibrin-based glue (Tisseel, Baxter, Newbury, UK) may assist with the control of any parenchymal air leak. Both EPP and P/D patients receive a thoracic epidural catheter routinely and are observed on the Thoracic High Dependency Unit as they are all extubated in the operating room.


Figure 1
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  		Fig. 1. Pleurectomy/Decortication via a right thoracotomy, showing dissection of the visceral pleura from the lung.

 

Figure 2
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  		Fig. 2. (a and b) Pathological specimens following P/D. The specimens are shown with paper towel in the pleural space. The visceral pleural cortex which has been removed from the oblique fissure is clearly seen in (a).

 
2.3 Statistical methods
Clinicopathological [14], surgical, oncological and follow-up data were entered prospectively into a database. Statistical analysis was performed using the SPSS software system (SPSS for Windows Version 11.0, SPSS Inc., Chicago, USA). Differences between groups were analysed with the Chi squared and Fisher's Exact test for qualitative and Students t-test for quantitative data. Survival curves were estimated using the Kaplan–Meier method and the log-rank test was used to assess the statistical significance of differences between groups. Patients dying in the postoperative period were not censored and therefore operative deaths were included in the survival analyses.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Discussion
 Appendix A
 References
 
3.1 Patients
Those in the P/D groups were older than in the EPP group (median (range) 61 (53–72) vs 58 (39–70) years, p = 0.03). Positron emission tomography (PET) was not offered routinely in this study and was only used as preoperative staging in five patients. No patients during the study period were deemed inoperable based on PET data alone. Preoperative mediastinal staging by video-assisted mediastinoscopy was performed in 16 and 9 patients in the EPP and P/D groups respectively (p = 0.5). Mediastinoscopy was positive in four patients, who subsequently underwent P/D. Five patients who underwent P/D had a negative mediastinoscopy, and it was not performed in three cases.

3.2 Other therapeutic modalities
Chemo and/or radiotherapy were given to patients according to their Oncologist decision, who also decided on the timing of therapies and regimes. Any additional therapy was received by 23 patients in the EPP and nine patients in the P/D group (p = 0.2). There were no significant differences in the proportion of patients receiving any chemotherapy between the groups. There were however, more patients receiving adjuvant chemotherapy in the P/D group. Regimes varied between the units offering the treatment, but the use of platin-based agents was mostly universal in these series (Table 2 ). There was a trend towards receiving radiotherapy in the P/D group (67 vs 38%, p = 0.1). Postoperative radical hemithorax irradiation was only received by patients in the EPP group but no P/D patients, due to concerns regarding radiation pneumonitis. These P/D patients did undergo irradiation of the wound and intercostal tube sites when provided.


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  		Table 2 The distribution of pathological data according to the operative groups
 
3.3 Operative results
Operative mortality was 4 (8.9%) and 1 (8.3%) in the EPP and P/D groups respectively. Causes of death after EPP included pleural sepsis following oesophageal perforation, bronchopneumonia following bronchopleural fistula after right EPP, pulmonary embolism 21 days after surgery, and myocardial infarction 2 days postoperative. Mortality after P/D occurred in a 67-year-old man who died 24 days after surgery of a pulmonary embolism. Macroscopic complete resection (R0 and R1) was reported in 91% of the EPP group and 83% of the P/D group (p = 0.8). The majority of patients were UICC Stage III: there were no differences in either the T stage between the groups (Table 2) with most of them being T3–T4.

Cell type distribution did not differ significantly with the majority of patients presenting epithelioid differentiation (Table 2).

3.4 Postoperative course
No patients in the P/D group required admission to the Intensive Therapy Unit, whereas eight did in the EPP group. We have previously published the range, incidence and predictors of postoperative morbidities in our series of EPP [10] and those encountered in the EPP and P/D groups are presented in Table 3 . The morbidity rate in the EPP group was 64% (29 out of 45). Six (50%) of the P/D group experienced morbidity, but in four of these patients this was a persistent air leak. All patients after P/D presented a postoperative air leak on day one. The median duration of the intercostal drainage after P/D was 10 (range 6–33) days. Four of these patients were discharged home with an intercostal drain in situ with a one-way valve system. Postoperative hospital stay was median 14 (range 6–184) days in the EPP and 10.5 (7–28) in the P/D groups (p = 0.1).


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  		Table 3 Incidence of in-hospital postoperative morbidities amongst the N2 EPP (n = 42) and P/D (n = 30) groups
 
3.5 Survival
Overall mean survival for the whole cohort of 57 patients was 15 (95% confidence interval 10–16) months. One-year survival rates were 54% (SE 7) and 18%, respectively. These figures were 15 months, 53% in the EPP group versus 16 months, 55% in the P/D group (p = 0.4, Fig. 3 ).


Figure 3
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  		Fig. 3. Kaplan–Meier plot showing the difference in survival between patients with N2 status following EPP and radical pleurectomy/decortication, which narrowly missed statistical significance in the Log Rank test (p = 0.06).

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Discussion
Appendix A
 References
 
These two groups of patients are contemporary, the first P/D and the first EPP being undertaken within six weeks of each other. We found that P/D is a feasible alternative to EPP in a number of different scenarios. The morbidity of P/D was lower. Specifically, we did not see in the EPP group the morbidities specific to (extrapleural) pneumonectomy, such as atrial fibrillation, mediastinal shift, bronchopleural fistula and post pneumonectomy empyema. This was, however, at the expense of a prolonged air leak in some patients, which was responsible for the lack of difference in hospital stay between groups. We did not assess formerly the quality of life following P/D or EPP, which should receive attention in future trials. However, any preservation of lung function in the P/D group is likely to have a positive impact on the quality of life.

With regard to pathological data, there were no differences in the histological cell type, no differences in the T stage and the rate of complete macroscopic resection was equally high in both groups.

There are several reason why the survival in the P/D group might be expected to be less than for EPP. The indications for P/D are diverse and this is a heterogeneous group as a result. Some patients had N2 disease detected at mediastinoscopy, some had unresectable disease at thoracotomy, some were medically unfit for EPP. The patients in the P/D group were older and displayed what might be accepted as negative prognostic factors in this disease.

An additional reason to expect survival following EPP to be better than P/D is that EPP did enable postoperative radical radiotherapy to be administered. In the P/D group, radiotherapy was restricted to the wound and drain sites. Chemotherapy was administered to an equal proportion of patients in both groups, although adjuvant more so in the P/D group. This raises the question of whether patients were fitter to receive postoperative chemotherapy after P/D than after EPP.

As our data suggests that by performing P/D in N2 malignant mesothelioma we do not compromise outcomes compared to EPP, and given that staging of nodal status by PET has been shown to have a sensitivity of only 11% in MM [15], we advocate that preoperative video-assisted mediastinoscopy is the staging modality of choice. In MM, mediastinoscopy was found to have a sensitivity of 80% and specificity of 100% [7]. We have shown previously that the proportion of involved nodes, rather than the anatomical location, is of importance [1] and therefore biopsy of multiple stations is required. We propose that the potential role of P/D in patients who are staged N2 positive and are fit for thoracotomy should be examined in future trials. Furthermore, our findings justify the use of mediastinoscopy to select those for EPP and suggest that accurate mediastinal staging should be incorporated into surgical trial protocols. In addition, systematic lymph node dissection should be performed in those patients undergoing thoracotomy for MM to allow further assessment of the powerful negative prognostic influence of N2 nodal status in future studies.

We acknowledge the limitations of our report. It is the result of a non-randomised study, the group population undergoing P/D is small, and we have not physiological or quality of life data of the effects of preserving the lung.

In summary, as we have not found any survival advantage of EPP over P/D in N2 patients, we now have ceased to offer EPP to this group. Moreover, we now aim to accurately stage every candidate for radical surgery with a cervical mediastinoscopy.


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

Dr M. Dusmet (London, United Kingdom): With a 7% mortality for a palliative procedure with relatively short survival, I would challenge you that until you’ve proven that quality of life is quite significantly better with your radical procedure, we should still be preferring simple procedures, like talc pleurodesis, for this patient population that has a median survival of, give or take, around a year.

Dr Edwards: I agree with that comment in that further studies are required looking at quality of life, but we have shown and other groups have shown that there are symptomatic benefits to be gained by palliative debulking surgery, and we have found that if we can remove as much tumour as possible, then the results may be better, but, of course, yes, it requires a randomized trial to show that. The point of this paper was to demonstrate that the patients who have N2 positive disease have a very poor survival, and therefore we should not be operating by extrapleural pneumonectomy in these patients.

Dr A. Turna (Istanbul, Turkey): I would like to know how you describe R0 resection in the pleurectomy/decortication group.

Dr Edwards: In terms of the operative technique, the technique of extrapleural dissection is the same. Our pathologists look at up to 20 blocks in different areas of the circumferential plane, and they look at the diaphragm and they look at the pericardium as well. In terms of the surface of the lung, it is more difficult, but certainly we are able to gain complete macroscopic clearance, and I think that is the most important indicator of resection. I agree it is difficult to say that these patients are R0 compared to R1, but I think it's the R1 versus R2 that is what we as surgeons can influence, and that is the same for extrapleural pneumonectomy as well.

Dr H. Batirel (Istanbul, Turkey): Which lymph node stations are accessible with mediastinoscopy?

I wonder if there were any patients with internal mammary or diaphragmatic lymph node metastases? Second, was there any difference between the T stages of the tumours between the pleurectomy/decortication and EPP group?

Dr Edwards: To deal with your second question first, there was no difference in the T stage. The only difference in staging indicated was, of course, the N stage, and there were some patients with node-negative disease in the pleurectomy/decortication group.

In terms of your first question and mediastinoscopy, I refer you to our previous paper where we demonstrated the scatter of lymph node metastases. We performed standard video-assisted mediastinoscopy. We directed our dissection at the right and left pretracheal and paratracheal lymph nodes and also took station 7 lymph nodes as a matter of routine. We did not perform extended mediastinoscopy, and, of course, it is not possible to stage the internal mammary and subdiaphragmatic nodes by that technique.

Dr M. Zielinski (Zakopane, Poland): Maybe I’m wrong, but I thought that you obtained positive results on mediastinoscopy in several patients, and nevertheless you did a big operation, EPP or pleurectomy/decortication. What was the mediastinoscopy for? If you obtained positive results, I see little sense in referring the patient for a huge and purely palliative operation.

And the same with regard to my second question, was it reasonable to perform a purely palliative pleurectomy/decortication and resect the pericardium and the diaphragm? Is talc pleurodesis not the better solution in such palliative cases?

Dr Edwards: I agree with your first comments. We do not perform extrapleural pneumonectomy in patients who we know have N2 positive disease. The patients who had mediastinoscopy, there were 4 patients who had positive mediastinoscopy out of the mediastinoscopies we had performed, and they underwent radical pleurectomy/decortication. In terms of randomized controlled trials, of course there is no evidence yet to suggest that radical pleurectomy/decortication is better than talc. That should be the question in a future randomized trial.

Dr R. Schmid (Bern, Switzerland): Nice and somehow surprising results.

I have two questions. First, don’t you think you should eliminate the ‘radical’ for your pleurectomy/decortication? I don’t think it's really radical because it's more like a debulking.

Second, you showed the survival curves. Did you differentiate between the histological types, and would you perform this operation for all three histological types?

Dr Edwards: We certainly do not perform extrapleural pneumonectomy knowingly in patients who have nonepithelioid mesothelioma. In terms of radical pleurectomy/decortication, the intention of surgery is to remove all macroscopic disease, and we aim for complete macroscopic resection. That should be the gold standard for palliative surgery, because the best chances of palliation are to remove all visible disease. We did not see a great deal of morbidity in view of respiratory failure from taking the pericardium or the diaphragm, and therefore this would be our preferred approach for patients who are fit for thoracotomy.

Dr Schmid: And the histological types?

Dr Edwards: The histological types, again, for radical pleurectomy/decortication, there were some patients who had nonepithelioid tumours, but our numbers are not great in that area.


   Footnotes
 
\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.


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

  1. Edwards JG, Stewart DJ, Martin-Ucar A, Muller S, Richards C, Waller DA. The pattern of lymph node involvement influences outcome after extrapleural pneumonectomy for malignant mesothelioma. J Thorac Cardiovasc Surg 2006;131(5):981-987.[Abstract/Free Full Text]
  2. Sugarbaker DJ, Flores RM, Jaklitsch MT, Richards WG, Strauss GM, Corson JM, DeCamp Jr. MM, Swanson SJ, Bueno R, Lukanich JM, Baldini EH, Mentzer SJ. Resection margins, extrapleural nodal status, and cell type determine postoperative long-term survival in trimodality therapy of malignant pleural mesothelioma: results in 183 patients. J Thorac Cardiovasc Surg 1999;117(1):54-63.[Abstract/Free Full Text]
  3. Rusch VW, Venkatraman E. The importance of surgical staging in the treatment of malignant pleural mesothelioma. J Thorac Cardiovasc Surg 1996;111(4):815-825.[Abstract/Free Full Text]
  4. Aziz T, Jilaihawi A, Prakash D. The management of malignant pleural mesothelioma; single centre experience in 10 years. Eur J Cardiothorac Surg 2002;22(2):298-305.[Abstract/Free Full Text]
  5. Tammilehto L, Kivisaari L, Salminen US, Maasilta P, Mattson K. Evaluation of the clinical TNM staging system for malignant pleural mesothelioma: an assessment in 88 patients. Lung Cancer 1995;12(1–2):25-34.[CrossRef][Medline]
  6. Schouwink JH, Kool LS, Rutgers EJ, Zoetmulder FA, van Zandwijk N, v d Vijver MJ, Baas P. The value of chest computer tomography and cervical mediastinoscopy in the preoperative assessment of patients with malignant pleural mesothelioma. Ann Thorac Surg 2003;75(6):1715-1718.[Abstract/Free Full Text]
  7. Rice DC, Erasmus JJ, Stevens CW, Vaporciyan AA, Wu JS, Tsao AS, Walsh GL, Swisher SG, Hofstetter WL, Ordonez NG, Smythe WR. Extended surgical staging for potentially resectable malignant pleural mesothelioma. Ann Thorac Surg 2005;80(6):1988-1992.[Abstract/Free Full Text]
  8. Pilling JE, Stewart DJ, Martin-Ucar AE, Muller S, O’Byrne KJ, Waller DA. The case for routine cervical mediastinoscopy prior to radical surgery for malignant pleural mesothelioma. Eur J Cardiothorac Surg 2004;25(4):497-501.[Abstract/Free Full Text]
  9. Rusch VW. Pleurectomy/decortication in the setting of multimodality treatment for diffuse malignant pleural mesothelioma. Sem Thorac Cardiovasc Surg 1997;9(4):367-372.[Medline]
  10. Richards WG, Zellos L, Bueno R, Jaklitsch MT, Janne PA, Chirieac LR, Yeap BY, Dekkers RJ, Hartigan PM, Capalbo L, Sugarbaker DJ. Phase I–II study of pleurectomy/decortication and intraoperaive intracavity hyperthermic cisplatin lavage for mesothelioma. J Clin Oncol 2006;24(10):1561-1566.[Abstract/Free Full Text]
  11. Stewart DJ, Martin-Ucar AE, Edwards JG, West K, Waller DA. Extra-pleural pneumonectomy for malignant pleural mesothelioma: the risks of induction chemotherapy, right-sided procedures and prolonged operations. Eur J Cardiothorac Surg 2005;27(3):373-378.[Abstract/Free Full Text]
  12. Sugarbaker DJ, Jaklitsch MT, Bueno R, Richards W, Lukanich J, Mentzer SJ, Colson Y, Linden P, Chang M, Capalbo L, Oldread E, Neragi-Miandoab S, Swanson SJ, Zellos LS. Prevention, early detection, and management of complications after 328 consecutive extrapleural pneumonectomies. J Thorac Cardiovasc Surg 2004;128(1):138-146.[Abstract/Free Full Text]
  13. Stewart D, Waller DA, Edwards JG, Jeyapalan K, Entwisle JJ. Is there a role for pre-operative contrast enhanced magnetic resonance imaging for radical surgery in malignant pleural mesothelioma?. Eur J Cardiothorac Surg 2003;24(6):1019-1024.[Abstract/Free Full Text]
  14. Edwards JG, Abrams KR, Leverment JN, Spyt TJ, Waller DA, O’Byrne KJ. Prognostic factors for malignant mesothelioma in 142 patients: validation of CALGB and EORTC prognostic scoring systems. Thorax 2000;55(9):731-735.[Abstract/Free Full Text]
  15. Flores RM, Akhurst T, Gonen M, Larson SM, Rusch VW. Positron emission tomography defines metastatic disease but not locoregional disease in patients with malignant pleural mesothelioma. J Thorac Cardiovasc Surg 2003;126(1):11-16.[Abstract/Free Full Text]



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