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Eur J Cardiothorac Surg 2007;31:181-185. doi:10.1016/j.ejcts.2006.11.008
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

Induction chemotherapy does not increase the operative risk of pneumonectomy!

Ziad Mansour, Evgenia A. Kochetkova, Xavier Ducrocq, Mircea-Dan Vasilescu, Guillaume Maxant, Alexis Buggenhout, Jean-Marie Wihlm, Gilbert Massard*

Service de Chirurgie Thoracique, Hôpitaux Universitaires de Strasbourg, 67091 Strasbourg, France

Received 27 July 2006; received in revised form 27 October 2006; accepted 7 November 2006.

* Corresponding author. Tel.: +33 3 88 11 62 02; fax: +33 3 88 11 60 77. (Email: Gilbert.Massard{at}chru-strasbourg.fr).


   Abstract
Top
 Abstract
1. Introduction
 2. Patients and methods
 3. Results
 4. Comment
 References
 
Background: There is an ongoing debate whether induction therapy increases post-operative mortality and morbidity, especially when performing pneumonectomy. We therefore reviewed a consecutive series of patients having undergone pneumonectomy in a single center. Methods: The charts of 298 patients operated on between January 1999 and July 2005 were reviewed. Patients were divided into two groups: group 1 included those who received induction chemotherapy (60 patients, 20.1%), and group 2 included those who underwent surgery alone (238 patients, 79.9%). Endpoints were operative mortality at 30 and at 90 days, and major complications such as empyema, bronchial fistula and acute respiratory distress syndrome. Statistical analyses were performed using SPSS 11.0 software. Results: Demographic data were similar for both groups when considering side of operation, comorbidity and weaning from tobacco; patients were older in group 2 (61.83 ± 9.58 years vs 57.75 ± 8.94 years; p = 0.003) and there were more female patients in group 2 (17.2% vs 5.0%; p = 0.010). Post-operative mortality at 30 days was 6.7% in group 1 and 5.5% in group 2 (p = 0.458), and 11.7% for group 1 and 10.9% in group 2 at 90 days (p = 0.512). Incidence of empyema was 1.7% in group 1 and 2.1% in group 2 (p = 0.652); incidence of bronchopleural fistulas was 1.7% in group 1 and 5.5% in group 2 (p = 0.188); incidence of acute respiratory distress syndrome was 3.3% in group 1 and 3.4% in group 2 (p = 0.675). Conclusion: In opposition to previous reports, induction chemotherapy did not significantly jeopardize post-operative outcome following pneumonectomy in our experience.

Key Words: Pneumonectomy • Chemotherapy • Surgery • Complications


   1. Introduction
Top
 Abstract
 1. Introduction
2. Patients and methods
 3. Results
 4. Comment
 References
 
Whether induction chemotherapy (IC) interferes with post-operative outcome is still a matter of debate. Many recent reports have treated this subject; however, most of them included patient populations having undergone all types of pulmonary resection and have analyzed all the subsets together on a whole. Pooling together these studies, we got the impression of a possible increase of complications in patients undergoing pneumonectomy. One of the mile-stone papers in the recent literature is the report by Martin et al. [1], although its conclusions are somehow ambiguous. The authors conclude on the one hand that pulmonary resection after neoadjuvant chemotherapy is associated with an acceptable overall morbidity and mortality; on the other hand, they alerted that pneumonectomy on the right side is associated with a mortality rate of 23.9% at 3 months, whereas there was no mortality following left pneumonectomy. Several other reports demonstrated an adverse effect of IC onto any type of pulmonary resection [2–6]. They reported mortality rates for pneumonectomy after IC ranging from 0 to 43%, and an increased incidence of broncho-pleural fistulae (BPF) ranging from 6 to 15%. The controversy is fed by some other studies relating more favorable results [7–11]. In the latter reports, mortality rates of pneumonectomies after IC ranged from 0 to 7.2%; the incidence of BPF ranged from 0 to 8%. A final subset of reports took a neutral position [12,13]. Given this contradictory information, we decided to review operative mortality and specific morbidity (empyema, bronchial fistula, acute respiratory distress syndrome (ARDS)) following pneumonectomy at our unit, and to compare outcome of patients having received induction chemotherapy to those having undergone surgery alone.


   2. Patients and methods
Top
 Abstract
 1. Introduction
 2. Patients and methods
3. Results
 4. Comment
 References
 
2.1 Collection of data
Three hundred and six patients underwent a pneumonectomy between January 1999 and July 2005. Their charts were retrospectively reviewed. Requested data were complete in all but eight cases; the latter were excluded from the study. The remaining 298 charts were screened for patients’ demographics and post-operative results. Demographic data included age, sex, smoking habits, pulmonary function tests, pre-operative co-morbidities (coronary artery disease, diabetes), pre-operative chemotherapy, side of pneumonectomy, and post-operative pathological staging. A patient was considered as suffering from chronic obstructive pulmonary disease (COPD) when forced vital capacity (FVC) in 1 s (FEV1) was less than 80% of predicted and/or when FEV1/FVC was less than 70%. Mortality was assessed at 30 days and 90 days post-operatively according to the recommendations of Doddoli et al. [6]. Post-operative complications were listed regardless if they occurred during the initial hospital stay or if they led to a readmission.

The whole cohort was divided into two groups: group 1 included those who received induction chemotherapy (n = 60, 20.1%) and group 2 included those who underwent surgery alone (n = 238, 79.9%). IC consisted typically of three cycles of a platinum-based drug (cisplatin or carboplatin) associated with vinorelbine (n = 24), or gemcitabine (n = 14), or taxotere (n = 12) or other associations depending on the referring oncological department.

Endpoints of the study were mortality at 30 days and at 90 days, and procedure specific complications such as empyema, bronchopleural fistula (BPF) and post-pneumonectomy pulmonary edema (ARDS)

2.2 Operative details
Patients were operated on by one of the department's three senior thoracic surgeons through a muscle-sparing antero-lateral or axillary thoracotomy, or a non-muscle-sparing postero-lateral thoracotomy. Thoracic epidural analgesia was used liberally. Complete lymph node resection was performed in all patients; on the right side, it included upper mediastinal nodes (levels 2, 4, and 10), subcarinal nodes (levels 7 and 8) and pulmonary ligament (level 9); on the left side we dissected the para-aortic nodes (levels 5 and 6), sub-aortic nodes down to the left tracheobronchial angle (levels 10 and 4), subcarinal nodes and pulmonary ligament (level 9). The bronchial suture was preferentially made with a stapling device. We routinely covered the bronchial stump following right sided pneumonectomy, regardless whether the patient received IC or not; our preferred technique is a pericardial and thymic fat pad placed below the superior vena cava. The chest was systematically drained with a single tube connected to a balanced drainage system and kept in place for 48 h. Patients stayed in the high dependency unit for at least 48 h before being transferred to the ward.

Post-operative monitoring included physical examination repeated 2–3 times per day and registration of vital signs; chest radiogram, white blood cell count and CRP level were repeated every 48 h during in-hospital stay to detect early signs of empyema or BPF. Fiberoptic bronchoscopy and thoracentesis were used liberally to promote early diagnosis of complications.

Post-operative radiation therapy was given in case of N2 disease (excepted microscopic N2) or incomplete resection.

2.3 Statistics
Demographic data and results of both groups were compared using SPSS 11.0 for windows software (SPSS Inc, Chicago, IL.). Pearson's Chi-square test or Fisher's exact test when needed were used to compare proportions, Student's t-test was used to compare means. Data were reported as mean ± standard deviation or as proportions. A p value less than 0.05 was considered significant.


   3. Results
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
4. Comment
 References
 
3.1 Patient population
Two hundred and ninety-eight consecutive patients underwent pneumonectomy for non-small cell lung cancer at the thoracic surgery department in Strasbourg university hospital between January 1999 and July 2005.

Sixty patients (20.1%) have undergone pre-operative chemotherapy before pneumonectomy (group 1), of whom only eight were included in a prospective chemotherapy trial (six in IFCT 0002, and two in IFCT 01–01). Six of these 60 patients further underwent sequential pre-operative radiation therapy because of presumed chest wall invasion; the field of irradiation did not include the mediastinum.

Two hundred and thirty-eight patients (79.9%) underwent pneumonectomy without pre-operative chemotherapy (group 2), of whom only one received preoperative radiation therapy.

Group 1 included younger patients and less female patients than group 2; there were more patients with diabetes in group 2 (Table 1 ). Demographic comparison of right and left pneumonectomies, and right pneumonectomy with or without IC failed to demonstrate any difference.


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  		Table 1. Demographics
 
3.2 Rough results
In group 1, four patients died until post-operative day 30 (6.7%) and compared to 13 patients in group 2 (5.5%). Ninety-day mortality concerned seven patients (11.7%) in group 1, and 26 patients (10.9%) in group 2. Empyema was observed in a single patient in group 1 (1.7%) and in five patients in group 2 (2.1%). BPF occurred in one patient in group 1 (1.7%) and in 13 patients (5.5%) in group 2. ARDS occurred in two patients in group 1 (3.3%) and in eight patients (3.4%) in group 2. There was no significant difference for any of these variables between the two groups (Table 2 ).


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  		Table 2. Results depending on the IC status
 
3.3 Impact of side of pneumonectomy
Mortality and morbidity rates according to the side of operation are shown in Table 3 ; except for BPF (8.4% on the right side, vs 1.8% on the left side; p = 0.008), there was no significant difference for any of these variables. Table 4 further describes morbidity and mortality according to IC status and side of pneumonectomy. Thirty-day mortality and prevalence of BPF were significantly increased following right pneumonectomy in patients having undergone surgery alone (group 2), whereas outcomes of right and left pneumonectomies were similar in patients having undergone IC (group 1).


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  		Table 3. Results depending on the side of operation
 

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  		Table 4. Results depending on the IC status and the side of operation
 

   4. Comment
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Comment
References
 
The present study fails to demonstrate any significant increase of mortality or morbidity following pneumonectomy after IC. We did not confirm an increased risk of right pneumonectomy following IC. On the contrary, results were improved. However, we cannot rule out that perhaps patients in the ‘surgery alone group’ had a slightly increased risk: mean age of the latter group was 4 years older; 1113% of patients suffered from diabetes, to be compared to 555% only in the IC group. Nevertheless, our results fit into a contradictory panorama set by the contemporary literature; some studies argue in favor of an increased risk, whereas others deny any influence of induction chemotherapy onto postoperative outcome.

Actually, there are several questions to discuss. First, which is the global risk of pneumonectomy. Second, does the side of operation influence outcome? Third, can we still justify pneumonectomy following induction chemotherapy? Forth, is it reasonable to undertake induction chemotherapy when pneumonectomy is anticipated?

The answers are not straight forward when we refer to the available literature. Most of the studies dealing with IC analyze series of operated patients regardless of the type of resection, and pool together exploratory thoracotomy, wedge resection, lobectomy, bilobectomy, pneumonectomy, with or without extended resection of the chestwall. We reviewed these articles in order to extract only data relative to pneumonectomy.

We would like to express a preliminary remark regarding definition of post-operative mortality. The studies reported by Martin et al. [1] and Doddoli et al. [6] showed that 30-day mortality might not be the most accurate indicator, given that mortality at 90 days is almost twice as high. The present study disclosed similar results (Table 5 ).


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  		Table 5. Overall mortality rates at post-operative days 30 and 90, detailed to the operated side
 
It is a classic believe shared by most thoracic surgeons that mortality is higher following right pneumonectomy, regardless whether IC has been given or not. However, this conception is challenged by two recent reports. Bernard et al. [15] reviewed a cohort of 639 pneumonectomies, of whom 63 had IC; right pneumonectomy was associated with increased post-operative mortality in univariate analysis, but not in multivariate analysis. Further, Licker et al. [16] reported 193 consecutive pneumonectomies without IC, and found that the side of pneumonectomy did not affect mortality. Accordingly, the side of pneumonectomy had no impact on mortality in the present series in either group (Table 3). However, like most reports, we found an increased rate of BPF following right pneumonectomy on a whole, and in patients who underwent surgery alone. Surprisingly, in the subset of patients who received IC, the prevalence of BPF was similar on either side (Table 4).

The report by Martin et al. [1] is a milestone in the history of pneumonectomy, and this operation is differently considered since its publication. The frightening 90-day-mortality rate of 23.9% following right pneumonectomy could in part be explained by the use of mitomycin-based chemotherapies and by the fact that chemotherapy was often performed outside of the specialized institution; however, it then remains also surprising that there was no mortality following left pneumonectomy. Nevertheless, this report triggered some reconsideration of pneumonectomy as a routine procedure, the danger being that operable patients could be denied for surgery.

Several other publications raised admonitions against IC, concluding that it increased post-operative complications (Table 6 ). Fowler et al. [2] reported a mortality rate of 43% among only seven pneumonectomized patients after 5-FU, cisplatin and etoposide IC. Roberts et al. [3] in 2001 compared all types of resection with or without IC (34 vs 67 patients). Although there was no increased mortality, there was 3–4-fold increase of major or life threatening complications in IC patients. Doddoli et al. [4] described 9% mortality and a 15% rate of BPF in 33 pneumonectomies after IC. They completed their survey in 2005 [6], and reported a 12% mortality rate and a 6% rate of BPF following 100 pneumonectomies after IC. Matsubara et al. [5] accordingly concluded that ‘extended resection’ or pneumonectomy are at increased risk after IC.


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  		Table 6. Selected reports concerning pneumonectomies after induction chemotherapy
 
This negative view of IC is counter-argumented by other reports concluding that there is no adverse impact of IC onto post-operative outcome (Table 6). Siegenthaler et al. [7] observed a 0% mortality rate with no BPF in eight pneumonectomies after IC, and when comparing with 28 pneumonectomies performed without IC, they found a statistically significant lower morbidity. Stamatis et al. [8] reported 7.2% mortality and an 8% BPF rate in 125 pneumonectomies for locally advanced tumors having received IC with cisplatin and etoposide or paclitaxel. Van Schil et al. [9] described 69 pneumonectomies included in the EORTC 08941 trial, operated on after objective response to platinum-based IC; there was a 7.2% mortality rate at 30 days. Perrot et al. [10] in 2005 described a 3.7% mortality rate with no BPF in 27 pneumonectomies after IC. Darling et al. [14] studied 187 pneumonectomies. While concluding to an increased mortality and an increased risk of BPF following right lung resections, there was no increased risk among the 31 patients who received IC. Vaprociyan et al. [17] also concluded that IC does not increase post-operative mortality when compared to immediate surgery in a series comprising 261 pneumonectomies. The only criticism we can address to the latter studies is that they limited evaluation of operative mortality to a 30-day period.

Pooling together the different series discussed above, and our results as well, we may conclude that there is no evidence for an increased mortality of pneumonectomy following IC, even if performed on the right side. We cannot conclude whether the risk of bronchopleural fistula is increased, and whether the risk for BPF is higher on the right side.

A final question concerns IC itself. While there is an increasing amount of studies demonstrating a slight survival advantage in patients receiving a combined modality treatment adding surgery and neo-adjuvant or adjuvant chemotherapy, it is yet unclear which timing of chemotherapy is optimal. IC offers some theoretic advantages over adjuvant chemotherapy: the response to chemotherapy can be monitored objectively, and compliance to treatment is higher. We do not agree that IC jeopardizes post-operative outcome. This leads however to questionable conclusions and strategies.

Bueno et al. [18] were the first to point out improved cancer-free survival in all types of resection when IC achieved a down-staging from N2 to N0. Consequently, many colleagues concluded that if (1) only downstaging offers an advantage in terms of survival and (2) if pneumonectomy carries an increased risk of post-operative death, patients should be reevaluated with redo mediastinoscopy, and surgery should be limited to patients with proven downstaging. Recent publications demonstrate the feasibility of redo mediastinoscopy, which seems to be safe and relatively effective in experienced hands. Mateu-Navarro et al. [19] evaluated remediastinoscopy after IC in non-small cell lung cancer in 24 patients, and found residual extra-capsular disease or N3 disease in 12 patients (50%), in whom they avoided an ‘unnecessary’ thoracothomy; the remaining 12 patients underwent thoracotomy, and five had a residual N2 disease. They conclude to a sensitivity of 70%, a specificity of 100%, and an accuracy of 80%. Van Schil et al. [20] reported similar data: 11 ‘unnecessary’ thoracotomies were avoided among 27 patients (40.7%); eight out of the remaining 16 patients who underwent thoracotomy were with residual N2 disease. They described a sensitivity of 73%, a specificity of 100%, and an accuracy of 85%.

However, from a methodologic point of view, it seems unfair to deny surgery to patients who are not downstaged: a phase 2 study does only allow to conclude on treatment toxicity, but in no way to survival data. Once again, the very few phase 3 studies published in peer-reviewed journals remain controversial: whereas some studies showed a tremendous survival advantage with IC in stage IIIA [21–23], the largest published series by Depierre et al. demonstrated a survival benefit limited to stages I and II [24].

We conclude that our data suggest that the potential adverse effect of induction chemotherapy on post-operative mortality following pneumonectomy may have been overestimated, and that available data do not allow to conclude whether IC increases or not the risk for bronchopleural fistula. Hence, pneumonectomy may be justified in selected patients cared for in specialized institutions.


   References
Top
 Abstract
 1. Introduction
 2. Patients and methods
 3. Results
 4. Comment
 References
 

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