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Eur J Cardiothorac Surg 2000;17:550-556
© 2000 Elsevier Science NL

Long-term results of sleeve lobectomy for lung cancer

Division of Thoracic Surgery, Centre de Pneumologie de l'Hôpital Laval, 2725 Chemin Sainte-Foy, Sainte-Foy, Québec, Canada G1V 4G5

Corresponding author. Tel.: +1-418-656-4747; fax: +1-418-656-4762

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 
Objective: Sleeve lobectomy is a lung saving procedure indicated for central tumors for which the alternative is a pneumonectomy. Current controversies relate to the safety of the procedure and adequacy as a cancer operation. The aim of the study is to analyze long-term survival after sleeve lobectomy, particularly in relation with nodal status and histological type. The incidence and patterns of recurrences were reviewed. Methods: From 1972 to 1998, 184 patients (male 152, female 32) underwent sleeve resection for lung cancer. The mean age was 60±10 years (11–78 years), and the indications for operation were a central tumor (79%), peripheral tumor with nodal involvement (13%) and compromised pulmonary function (8%). The histological type was predominantly squamous (n=125, 68%), followed by non-squamous (n=50, 27%) and carcinoid tumors (n=9, 5%). Resection was complete in 161 patients (87%). Results: The operative mortality was 1.6% (n=3). Follow-up was complete for the remaining 181 patients (mean, 5.7 years; range, 1 month–26 years). The survival at 5 and 10 years of all patients was 52 and 33%, respectively. Theses rates for patients with N0 status (n=97) were 63 and 48%, and 48 and 27% for those with N1 status (n=68; N0 vs. N1, P<0.05). An 8% survival rate was observed with N2 status (n=19) at 5 years, with no survivors after 7 years of follow-up. The 5 and 10 year survival was 56 and 34% for squamous carcinoma vs. 33 and 22% for non-squamous carcinoma (P<0.05). These rates were 58 and 38% for complete resection vs. 11 and 6% for incomplete resection at 5 and 10 years, respectively (P<0.05). Local recurrences occurred in 22% of cases, and the prevalence was statistically different between patients with N0 disease (14%) and N1 disease (23%; P=0.03), but not between N1 and N2 disease (42%; P=0.2). When local and distant recurrence were pooled together, the differences were highly significant between N0 (22%) and N1 (41%) disease (P=0.007), and between N0 and N2 (63%) disease (P=0.0002), but not between N1 and N2 disease (P=0.09). Conclusion: Sleeve lobectomy is a safe and effective therapy for patients with resectable lung cancer. The presence of N1 and N2 disease, or of non-squamous carcinoma significantly worsen the prognosis.

Key Words: Sleeve lobectomy • Bronchoplastic resection • Lung neoplasms • Survival • Recurrence

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 
Bronchoplastic procedures were originally designed for cancer patients unable to tolerate pneumonectomy, or for the treatment of uncommon benign endobronchial lesions, such as adenomas or strictures. Indeed, the first case of sleeve lobectomy reported by Price Thomas in 1947 [1] was carried out for a carcinoid tumor located in the right main bronchus. In 1952, Allison [2] performed the first bronchoplastic procedure for lung cancer, and since then, many reports [3–7] have suggested that sleeve resection should be done more electively because it accomplishes tumor and nodal clearance similar to that of pneumonectomy. In addition, the survival after sleeve resection is at least equal to that reported after pneumonectomy, with the added advantage of an improved quality of life and lower incidence of long-term detrimental respiratory sequelae.

In the current literature, the 5 and 10 year survival figures after sleeve lobectomy done for lung cancer vary quite widely dependent on cancer stage and nodal status [3,6,8]. Because of these conflicting results, we reviewed our experience with these procedures done over a 25 year interval. The purposes of this review were to look at operative mortality and morbidity as they relate to modern thoracic surgery, to determine the adequacy of cancer clearance in relation with the incidence of local recurrences and ultimately to analyze long-term survival figures.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 
From January 1972 to July 1998, 184 patients underwent sleeve resection as a primary treatment for bronchogenic tumors. There were 152 men and 32 women, and the mean age at the time of operation was 60±10 years (range, 11–78 years). Bronchoplastic procedures were usually done by choice in patients who would have been able to tolerate pneumonectomy, but in whom the lesion could be completely resected by a lesser operative procedure (n=145). In this group, the indications for operation included patients with endobronchial tumors originating from a lobar bronchus and extending into the main bronchus (n=71), extraluminal extension to the outer wall of the main bronchus undetected by bronchoscopic examination (n=25), unsuspected involvement of the bronchial margins diagnosed by frozen section (n=49), and peripheral tumors with nodal involvement (n=24). In all of these individuals, the tumor could not have been removed by conventional lobectomy because the line of resection would have either transected the tumor or provided an inadequate margin. In 15 additional patients with severe respiratory impairment, the bronchoplasty was done as a compromise to pneumonectomy.

Mediastinoscopy, with random node sampling at three different levels, was done in nearly every case (160/184). In 24 patients, mediastinoscopy was not done because the diagnosis was that of a carcinoid tumor, or simply because the diagnosis of lung cancer had not been confirmed preoperatively. Induction chemotherapy was used in three patients with N2 disease documented at mediastinoscopy.

2.1. Operative procedure
Although the initial finding that identified a possible candidate for sleeve resection was the bronchoscopic appearance of the tumor extending from a lobar orifice to the adjacent main bronchus, the final decision was always made at the time of thoracotomy. The procedures were considered complete when all gross carcinoma were removed, and when both resection margins and the highest node were free of the tumor.

The majority of sleeve resections were done for tumors involving the origin of either upper lobe (n=152, 83%; Table 1). In 17 patients, the middle lobe had to be taken in continuity with the right upper lobe because of tumor growth across the fissure, or because of nodal disease around the bronchus intermedius. Nine patients had a lower lobe sleeve resection, and in four patients, a small tumor located in the main bronchus could be resected without sacrificing any of the distal lung. Four patients required a concomitant sleeve resection of the pulmonary artery (double sleeve resection). Frozen section analyses of lymph nodes were routinely used during operation, and if a patient was found to have surgical N1 or N2 disease, radical lymphadenectomy was carried out.

2.2. Follow-up
Patients were observed from the date of operation to the time of death, or end of observation (July 1998), whichever came first. No patients were lost to follow-up. The mean follow-up time was 2071 days and the maximum follow-up time was 9559 days.

A local recurrence was defined as tumor growth within the ipsilateral hemithorax or mediastinum, or both. For patients who died, the cause of death and the site of first recurrence were determined from clinical records, death certificates, or from information provided by family physicians or by relatives of the patient. Each death was classified as being due to: (1), lung cancer, including second primary lesions and operative deaths; (2), causes unrelated to lung cancer; or (3), unknown causes.

The sites of first recurrences were classified as being: (1), local; (2), distant; (3), local and distant; (4), unknown sites; or (5), second primary defined according to the criteria of Martini and Melamed [9] as a tumor of different histological type, or a tumor of similar histological type if it occurred more than 2 years after the first operation or if its origin could be traced to a carcinoma in situ.

Operative mortality was defined as a death occurring within 30 days of the operation, or a death directly related to the procedure even if it occurred more than 30 days after the operation.

2.3. Statistical analysis
The results are presented as means±SD for continuous variables, and as percentages for categorical data. The Chi-square test was used to compare these proportions. A P-value of 0.05 was considered significant. The life-table method for longitudinal data was obtained using the Kaplan–Meier method and all causes of death were included. Differences between survival curves were obtained by computing the confidence limits on the life-table values. The data were analyzed using the SAS statistical package (SAS Institute, Inc, Corey, NC).

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 
3.1. Histopathology and stage of disease
There were 125 patients (68%) with squamous cell carcinoma (Table 2), 50 patients with non-squamous carcinomas (adenocarcinoma, 19; large cell carcinoma, 20; mixed cell type, 11), and nine patients with typical carcinoid tumors.

3.2. Operative morbidity and mortality
Three deaths occurred after operation, resulting in a hospital mortality of 1.6%. Two of the three deaths were the result of infectious complications in the reimplanted lung, while the third operative death was due to a pulmonary embolus.

Non-fatal complications were seen in 26 additional patients, and these are listed in Table 3. Late anastomotic strictures developed in four patients, all after right upper lobe sleeve resection. These complications were treated by the endoscopic removal of granulomas in two patients and dilatation of the stricture in one patient. Completion pneumonectomy was required in the remaining patient. Including the two patients with early bronchopleural fistula, both managed conservatively, six patients (3.2%) had complications related to the anastomosis.

View larger version (49K): [in this window] [in a new window]   Fig. 1. Life-table analysis showing the percentage of all patients remaining alive after sleeve resection of bronchogenic carcinoma.

View larger version (55K): [in this window] [in a new window]   Fig. 2. Life-table analysis by nodal status showing the percentage of all patients remaining alive after sleeve resection of bronchogenic carcinoma. Significant differences in survival were noted between N0, N1 and N2 patients.

For squamous carcinomas, the 5 and 10 year survival was 56±5 and 34±5%, and 33±8 and 22±7% for non-squamous carcinomas (Fig. 3). The curves differ significantly (P0.05) after 2 years of follow-up. All patients with carcinoid tumors survived 10 or more years after operation. No significant difference in survival was observed between patients with right- or left-sided sleeve resections (Fig. 4). Only 11% of patients with incomplete resection survived 5 years.

View larger version (44K): [in this window] [in a new window]   Fig. 3. Life-table analysis by histological type showing the percentage of all patients remaining alive after sleeve resection of bronchogenic carcinoma. Significant differences were noted between the two groups.

View larger version (53K): [in this window] [in a new window]   Fig. 4. Life-table analysis by side of operation showing the percentage of all patients remaining alive after sleeve resection of bronchogenic carcinoma.

Local recurrence occurred in 22% of patients, and the distribution was significantly different between patients with N0 (14%) and patients with N1 disease (23%) (P=0.03; Table 4). In comparison, eight of 19 patients (42%) with N2 disease had a local recurrence (N0 vs. N2, P=0.005). When local and distant recurrence are pooled together, the recurrence rates were 22, 41 and 63% for N0, N1 and N2 groups, respectively, (N0 vs. N1, P=0.007; N0 vs. N2, P=0.0002; N1 vs. N2, P=0.09). The first site of recurrence for the entire group was mostly locoregional (locoregional, 41/61, 67%; distant, 20/61, 33%). The most common site of distant metastases was the brain (n=9).

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 
Sleeve lobectomy can be used as an alternative to pneumonectomy in carefully selected patients with bronchogenic carcinoma. It preserves the functional lung, and it has been previously shown that the reimplanted lobe(s) contribute significantly to postoperative lung function [5,7]. In addition, it may allow a second procedure to be done in patients who develop a second primary, the incidence of which has increased in recent years [11].

Sleeve resection is a technically more demanding procedure than standard lobectomy, and the bronchial anastomosis can give rise to specific complications not seen after conventional lobectomies. This is one of the reasons why bronchoplastic operations must have a low operative morbidity and mortality, as well as provide adequate survival in order to be recognized as valid cancer operations.

In a collective review of 1915 patients submitted to bronchoplastic procedures over a period of 12 years (1980–1992), Tedder and colleagues [12] reported a 30 day mortality of 5.5%, with a range of 0–11% [7,13,14]. The causes of death were mainly respiratory or cardiac related events. In the current series, the operative mortality of 1.6% is similar to that of more recent reports [5,8,13], and compares favorably with the 6% 30 day operative mortality reported by the Lung Cancer Study Group after pneumonectomy [15].

Persistent atelectasis is one of the most common morbidities reported after bronchoplasty [12,16], as it relates to the interruption of the ciliary epithelium and lymphatics, partial denervation of the reimplanted lobe(s), or anastomotic edema. In this series, atelectasis occurred in 10% of patients, but in the majority of cases, the problem was minor and could be solved by the bronchoscopic removal of the retained mucus.

In the review of Tedder and colleagues [12], anastomotic complications included bronchopleural fistula in 3% of patients and late stricture in 4.8% of cases. In the present series, these problems occurred in 1.1 and 2.2% of patients, respectively. This favorable outcome is likely to be the result of careful construction of the anastomosis, and the use of resorbable suture material.

In their review, Tedder and colleagues [12] report overall 5 year survival figures of 40% when sleeve lobectomy is done for bronchogenic carcinoma. In the absence of nodal involvement (N0 status), these rates can reach up to 60%. Our overall survival figures of 52 and 33% at 5 and 10 years are similar to figures recently reported by other institutions. In 1999, Suen and associates [17] reported an overall 37% 5 year survival in 58 patients, while this was 42% in the Gaissert and colleagues series [5] of 72 patients, and 46% in the series of Van Schil et al. [6] (Table 5). Older series include those of Watanabe and associates [4] (5 year survival, 45%; n=79), Maggi and associates [16] (5 year survival, 40.8%; n=69), and Naruke and associates [13] (41%; n=91). In general, survival figures after sleeve resection are comparable with those seen after conventional lobectomy, but much better than those reported after pneumonectomy [18].

In contrast to our previous report [21], we now find a significant difference in the long-term survival between patients with N0 and N1 disease. In their series of 145 patients, Van Schil and colleagues [6] showed by multivariate analysis that nodal status was the most significant factor related to long-term survival, both N1 and N2 disease having a definite negative impact. Our results are similar to these, although patients with N1 status can still expect a survival of equal or better to that reported after pneumonectomy for similar stage tumors [22,23]. For patients with N2 disease, the difference in survival at 5 years between our series (8%) and that of Van Schil [6] (31%) might be explained by the unsettled controversy in determining whether central nodes, especially in the right lung, are to be included in station 10 or 4 of the nodal maps, and whether these nodes are hilar or mediastinal. If one groups the patients with pN1 and pN2 status together, the survival at 5 and 10 years after operation is quite similar between the current series and that of other series [5,6,13].

The issue of local tumor recurrence after sleeve resection has been extensively investigated. In their review, Tedder [12] and colleagues reported local recurrence rates of 12.5%, ranging between 5 and 51% [14,16], while Faber and colleagues [3] observed local recurrence rates of 9% in 101 patients, and Gaissert and associates [5] had a local recurrence rate of 14% in 69 patients. In many of these papers, local recurrences are not clearly defined, some authors considering only tumor at the suture line as a local recurrence, while others include nodal disease or disease at pulmonary sites which are remote from the initial resection. For the purpose of clarity, we included all patients with recurrent disease within the ipsilateral hemithorax as having a local recurrence. By using this definition, our results correlate with the experience of other groups [6,24]. Despite meticulous operative evaluation through the liberal use of frozen sections, there were nine instances of truly anastomotic recurrences. The majority of these occurred in patients with incomplete resections based on positive resection margins, and it is of interest to note that some of these individuals had negative frozen sections, but turned out to have positive margins at the final microscopic analysis obtained 3 days after operation. This would support the reluctance that some surgeons have to completely rely on frozen sections for final decision making.

Overall, the incidence of cancer recurrence is similar or even less after sleeve resection to what is reported after conventional resection for stage 1 and 2 carcinomas of the lung [22,25]. However, the patterns of failure are slightly different. After complete resection of early stage lung cancer, first recurrences tend to be distant for patients with N0 status, and local for patients with N1 status [25]. Immerman and colleagues [25] reported that after the complete resection of non-small cell stage 1 and 2 lung cancers, the site of first relapse was local in 18% of patients and distant in 26%. In our series, the site of first relapse is more often locoregional, even for patients with N0 status. This pattern of recurrence in patients with N0 or N1 disease is different from that reported by Van Schil and colleagues [6] where distant metastases were the main cause of death.

	5. Conclusion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 
Sleeve lobectomy is a valuable alternative to pneumonectomy, with excellent short- and long-term survival results. The operative mortality is low and the radical nature of lung cancer treatment is not jeopardized. Bronchoplasty with node dissection achieves the same surgical margins as pneumonectomy and the long-term results are strongly influenced by nodal status.

	Footnotes

 
Presented at the 13th Annual Meeting of the European Association for Cardio-thoracic Surgery, Glasgow, Scotland, UK, September 5–8, 1999.

	Appendix A Conference discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 
Dr P. Van Schil (Antwerp, Belgium): I have three questions. In contrast to earlier reports from our institution, you presently found a significant difference between N0 and N1 disease. Is this due to longer follow-up time, and did you look at the causes of death in relation to nodal involvement?

Secondly, do you advocate adjuvant therapy in N1 or N2 disease after sleeve resection?

Thirdly, the group from Paris, from Professors Levasseur and Icard, recently proposed to initiate a prospective randomized trial between sleeve lobectomy and pneumonectomy in N1 disease for patients who can tolerate a pneumonectomy. What is your opinion about this kind of study?

Dr Tronc: First of all, yes, we found a difference between N0 and N1 with longer follow-up, exactly. For the second question, we do radiotherapy for all patients with N2 status studied at mediastinoscopy or thoracotomy. For N1, this is not always the case. For the third question, if I understand it, pneumonectomy for patients who are not able to tolerate a sleeve lobectomy?

Dr Van Schil: Yes. Due to the controversial results of N1 disease, they propose to initiate, a prospective study with patients randomized between sleeve lobectomy and pneumonectomy when N1 disease is found during the operation.

Dr Tronc: I think the results of sleeve lobectomy are good enough and in this series perhaps not needed.

Dr K. Al Kattan (Riyadh, Saudi Arabia): I noted there is a big difference in the 10 and 5 year survival, and we always deal with lung cancer so that after 5 years the cause of death related to cancer becomes much less. Have you analyzed the cause of death in the patients who had a 10 year survival?

Dr Tronc: Most of the patients died from cancer in this series, of course, and my opinion is, what is cause of death after 5 or 10 years? We don't exactly analyze the question.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 5. Conclusion Appendix A Conference discussion References

 

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