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Ann Thorac Surg 2005;80:2046-2050
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Sleeve Lobectomy Versus Pneumonectomy: Tumor Characteristics and Comparative Analysis of Feasibility and Results

Patrick Bagan, MD, Pascal Berna, MD, Joao Carlos Das Neves Pereira, MD, PhD, Françoise Le Pimpec Barthes, MD, Christophe Foucault, MD, Antoine Dujon, MD, Marc Riquet, MD *

Department of Thoracic Surgery, Georges Pompidou European Hospital, Paris V University, Paris, France

Accepted for publication June 3, 2005.

* Address correspondence to Dr Riquet, Service de Chirurgie Thoracique, Hôpital Européen Georges Pompidou, 20-40 rue Leblanc, 75908 Paris, France (Email: marc.riquet{at}hop.egp.ap-hop-paris.fr).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: Sleeve lobectomy (SL) seems to have better results than pneumonectomy. Some authors propose to extend its indications. The aim of this study was to compare postoperative results, locoregional recurrence, and survival after sleeve lobectomy and pneumonectomy in focusing on right upper lobe cancer.

METHODS: From 1984 to 2002, 973 lung resections were performed for T1, T2, and bronchial T3 right upper lobe non-small cell lung cancer. There were 756 lobectomies (L group), 151 pneumonectomies (RP group), and 66 sleeve lobectomies (SL group). The RP group was further divided with regard to intrapulmonary lymph node involvement. Pneumonectomy 1 (RP1) was a group of N0, intralobar N1, and skip metastasis involvement (N0-N2). Pneumonectomy 2 (RP2) was a group of extralobar N1 and nonskip metastasis involvement (N1-N2). Postoperative results were compared among SL, L, and RP groups. Survival was compared between the two homogeneous groups for oncologic chracteristics (SL, RP1).

RESULTS: Statistical comparison of 5-year actuarial survival showed a significant difference favoring SL (SL: 72.5%/ RP1: 53.2%; p = 0.0025). Postoperative mortality was higher after RP (L: 2.9% / SL: 4.5%/ RP: 12.6 %). Significant factors limiting SL were tumor size, extralobar N1, and main bronchus involvement (p = 0.000026, 0.0002, and 0.005, respectively).

CONCLUSIONS: Immediate and long-term survival appears better after sleeve lobectomy than right pneumonectomy for comparable stages of right upper lobe cancer. For frequency to increase by systematic attempt at SL, limited by large tumors and extralobar N1 involvement, the only way should be after favorable response to induction chemotherapy.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Bronchial sleeve lobectomy (SL) was first introduced by Price-Thomas [1] in 1947 as a means of parenchymal-sparing surgery. Several surgeons [2–7] promoted SL as an alternative to pneumonectomy for patients with non-small cell lung cancer (NSCLC). Recent reports [8, 9] suggested that SL even improved the quality of life and long-term survival when compared with pneumonectomy, regardless of underlying pulmonary function [10]. Right upper sleeve lobectomy is the most frequently performed bronchoplastic procedure (average frequency 70% [11, 12]) and right pneumonectomy is the most high-risk procedure [13]. The objectives of this retrospective study were to compare postoperative results, locoregional recurrence, and survival after sleeve resection, and pneumonectomy for comparable disease stages in focusing on right upper lobe (RUL) NSCLC. Pathologic characteristics that limited bronchoplastic operation were also analyzed in order to look for a potential strategy likely to extend the performance of this procedure.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Patients
Between 1984 and 2002, 3,428 consecutive patients underwent curative complete lung resection for NSCLC at the Georges Pompidou Hospital and at the Bois-Guillaume Surgical center. The number of all bronchoplastic procedures performed during the study period was 118 (3.4%). During this period, 1,187 patients underwent pulmonary resection for a centrally located and/or a bronchial right upper lobe cancer. Preoperative workup included bronchoscopy, thoracoabdominal and cerebral computed tomographic (CT) scan, pulmonary function tests, and lung perfusion scintigraphy. Mediastinoscopy was performed only to rule out N3 disease and to confirm clinical N2 disease on CT scan in view of neoadjuvant therapy. Patients who had preoperative neoadjuvant therapy (n = 173) or who had palliative surgery with positive margin (n = 41) section were also excluded from the study. The remaining 973 patients had T1 (n = 353), T2 (n = 580), and bronchial T3 (n = 40) NSCLC. The surgical procedure was right upper lobectomy in 77.7% of cases (L group: n = 756 patients), right pneumonectomy in 15.5% of cases (RP group: n = 151 patients), and right upper sleeve lobectomy in 6.78% of cases (SL group: n = 66). All patients underwent a curative oncologic resection associated with a complete mediastinal lymphadenectomy. Specific indication for sleeve resection was the involvement of the right upper bronchus by endobronchial tumor (n = 53) or by tumoral lymph nodes with an associated lateral vascular resection (n = 13). Pneumonectomies were performed when right upper lobe NSCLC extended to the proximal main bronchus and/or to the proximal pulmonary artery (n = 118) and when tumoral lymph nodes precluded a fissural approach (n = 33). Characteristics of this population are depicted in Table 1.


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  		Table 1. Clinical Characteristics of the Study Population
 
Methods
We reviewed pathologic findings, postoperative course, and long-term survival of these patients. The RP group was further divided with regard to intrapulmonary lymph node involvement. The RP1 was a group of patients whose intrapulmonary N involvement was negative or only intralobar (12, 13, 14 [14]), not precluding a fissural approach (n = 65). There were 40 N0 patients, 11 intralobar N1 patients, and 14 skip metastasis (N0-N2) patients. The RP2 was a group of important intrapulmonary lymph node involvement (n = 86) including extralobar N1 involvement (10, 11 [14]) and N2 patients with intrapulmonary lymph node involvement precluding intrafissural dissection: extralobar N1 (n = 32) and N1-N2 patients (n = 54). The SL group was compared with L and RP groups in terms of postoperative morbimortality. The SL group was also compared with RP groups in terms of bronchial involvement, lymph node metastasis, tumor size, long-term survival, and cause of death (systemic metastasis, local recurrence, and others).

Our Institutional Review Board approved this study and follow-up information was obtained from hospital case records, a questionnaire completed by the local chest physician or general practitioner, or from death certificates. Zero-time was considered as the date of surgery. Univariate analysis was conducted among the three populations. Actuarial survival curves were calculated by the Kaplan-Meier method; statistical comparisons were made using the log-rank test. All data analyses were conducted with a two-sided test: a p value less than 0.05 was considered as statistically significant. Standard error of the mean software was used for calculation [15].


   Results
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 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
Patient Characteristics
Regarding the clinical characteristics of the patient population presented in Table 1, no statistical differences were observed between the SL and RP groups concerning age and respiratory function tests. Comparing SL with the most similar group with regard to fissural involvement (RP1 group), pneumonectomy was significantly more often performed in patients with larger tumor size (p = 0.0000003) and main bronchus involvement (p = 0.005) precluded parenchymal-sparing surgery (Table 2).


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  		Table 2. Pathologic Comparison Between SL Group, RP1, and RP2 Groups
 
Postoperative Results and Survival
Postoperative complications occurred in 28.8% of patients after sleeve resection, in 29.9% after right pneumonectomy (p = 0.88), and in 26.5% after right upper lobectomy (p = 0.6). Operative mortality was more frequently observed after right pneumonectomy (12.6 vs 4.5%), which approached significativity (p = 0.07). A significant difference was observed between right pneumonectomy and lobectomy (12.6 vs 2.9 %, p = 0.00008).

The overall 5-year actuarial survival for patients with right upper lobe NSCLC who underwent sleeve lobectomy was 72.5%, whereas overall 5-year survival was 53.2% in the RP1 group. Statistical comparison showed a significant difference favoring sleeve lobectomy (Fig 1).



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  		Fig 1. Survival curves of SL (1), RP1 (2), and RP2 (3) groups. Statistically significant differences were observed (log-rank test; 1/2 p = 0.0025; 1/3 p = 0.000019).

 
During follow-up, 15 (22.7%) patients died from NSCLC in the SL group and 22 (34.8%) in the RP1 group (p = 0.0025). We observed no statistical difference in terms of locoregional recurrence among the three groups. Death from widespread recurrent cancer was more frequently observed after pneumonectomy, especially in the RP2 group with advanced stage disease. Cause of death and sites of recurrences are detailed in Table 3.


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  		Table 3. Comparative Details on Locoregional Recurrence and Long-Term Survival
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
Initially performed in case of compromised pulmonary function [1–6], sleeve resection was progressively adopted by most thoracic surgeons. Concerns about its oncologic validity were solved by data progressively supporting its use in patients whatever the pulmonary function [8, 16, 17]. In our comparative study, pulmonary function tests were similar in the SL and RP groups, confirming that during the study period, sleeve lobectomy was not only restricted to patients with compromised lung function who would not have tolerated pneumonectomy.

Sleeve lobectomy is a safe procedure with few operative morbidities [11, 12, 16, 17]. Recent studies demonstrate that this procedure is also safe and efficient after neoadjuvant therapy [18–20]. In our study, the rates of complication between the SL group and the P group were similar but operative mortality was worse after right pneumonectomy. This supports the significant benefit on postoperative course reported by some authors [8, 16]. In a meta-analysis, Ferguson and Lehman [9] report that the weighted mean operative mortality is 4.1% (confidence interval [CI], 2.3% to 5.9%) after sleeve lobectomy and 6.0% (CI, 1% to 11%) after pneumonectomy (p = 0.3). Deslauriers and colleagues [8] report an operative mortality four times more important after pneumonectomy (5.3% vs 1.3%, p = 0.036). In our study, operative mortality is as high as the highest rate reported by Ferguson and Lehman [9] in a meta-analysis concerning sleeve resection and pneumonectomy, whatever the side and tumor location within the lung. This is mainly due to the gravity of the right pneumonectomy itself [13], which represents the whole group of our patients.

Most studies comparing sleeve lobectomy and pneumonectomy [9, 10, 16, 17] demonstrate that long-term survival after bronchoplastic resection is not compromised by the procedure. Van Shil and colleagues [21] stress long-term survival after sleeve lobectomy in relation to nodal involvement and believe that N1 disease does not exclude sleeve resection but that adjuvant therapy should be considered. Ferguson and Lehman [9] report better prognoses after sleeve lobectomy in stage I patients. Deslauriers and colleagues [8] report a significant better survival after sleeve lobectomy in stage I and in stage II but not in stage III patients, which was only reported by Okada and colleagues [10].

According to Deslauriers and colleagues [8], long-term survival is better in stage II patients. This can be explained by the heterogeneity of N1 lymph node involvement. Patients with extralobar N1 disease have a significantly worse prognosis than patients with intralobar N1 disease [22, 23]. Difference in 5-year survival observed by Deslauriers and colleagues [8] between sleeve lobectomy and pneumonectomy in stage II (N1) patients (50% vs 34%) is similar to that observed by Riquet and colleagues [22] between intralobar and extralobar N1 patients (53.6% vs 38.5%). In fact, extralobar N1 is commonly the cause of pneumonectomy. In a multicentric retrospective study, Dujon and colleagues [24], reviewing 924 patients with N1 disease, demonstrated that pneumonectomy was indicated by local technical possibilities in 65.2% of cases, that lobectomy was performed in 22.1% of cases because of occult intralobar N1 disease, and that the type of resection (lobectomy or pneumonectomy in case of N1) could be chosen by the surgeon in only 12.7% of cases. Also, by contrast with other comparative studies [8–10, 16, 17], we subdivided pneumonectomy not with regard to the nodal status but only with regard to fissural dissection and theoric ability to perform right upper sleeve lobectomy. Comparison between the two most homogeneous groups (SL and RP1), with regard to a fissural approach, effectively did not demonstrate any difference in the matter of lymph node involvement but disclosed a significant difference in terms of tumor size and main bronchus involvement; in the RP1 group; mean tumor size was significantly larger and tumors more frequently largely involved the main bronchus.

These data, to our knowledge never reported in comparative studies, focus on the pathologic T (pT) when considering the size of the tumor as the main factor limiting the technical possibility of sleeve lobectomy performance in N0 or intralobar N1 disease. Patients with early stage disease undergoing a lung-saving procedure have better long-term survival than patients undergoing pneumonectomy, which tends to favor this procedure to avoid short and long-term deleterious effects inherent to a right pneumonectomy. Effectively, staging between SL and RP1 is not different (Table 2) but 5-year survival is significantly better in the SL group than in the RP1 group (Fig 1).

Although preferable to pneumonectomy, sleeve resection is performed in a small proportion of cases. Studies in which these data are available report a proportion of sleeve lobectomies ranging from 3% to 4% of all resections [2, 11, 25]. These retrospective studies compare different diseases in terms of side intrapulmonary tumor location, tumor size, and lymph node involvement. The rate we observed in our series (3.4%) is within the range of that which is commonly reported and increases up to 7% when only the right upper lobe is considered. This increase is, of course, artificial because of the greatest frequency of right upper sleeve resections. Martin-Ucar and colleagues [26] have implemented a policy of parenchymal-sparing surgery for tumors involving the main stem bronchus and observed that the rate of pneumonectomies decreased significantly with increasing experience with parenchymal-sparing surgery. Improvement of surgical skill and technique may allow performing more sleeve resections in difficult situations. However, our analysis lets us consider that the rate could not dramatically increase because of the resection limitation due not only to tumoral N1 but also large-sized tumors at the level of the lobar root. Only induction therapy could be helpful by clearing the fissural approach.

In summary, sleeve lobectomy for right upper lobe non-small cell lung cancer appears safer than right pneumonectomy. Better postoperative and long-term results favor the tendency promoting performance of bronchoplastic operations. However, the frequency of sleeve lobectomy remains low due to N1 involvement and tumor size. It could be improved by a systematic attempt at sleeve lobectomy, particularly after neoadjuvant chemotherapy, for large-sized tumors. The latter configuration should be evaluated by further multi-institutional studies comparing a bronchoplastic procedure with a pneumonectomy after induction therapy.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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