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Ann Thorac Surg 2002;74:851-859
© 2002 The Society of Thoracic Surgeons
a Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, Hôpital Marie-Lannelongue, Paris-Sud University, Le Plessis Robinson, France
* Address reprint requests to Dr Fadel, Department of Thoracic and Vascular Surgery and Heart-Lung Transplantation, Hôpital Marie-Lannelongue (Paris-Sud University), 133 Avenue de la Resistance, 92350 Le Plessis Robinson, France
e-mail: fadel{at}ccml.com
Presented at the Thirty-eighth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2002.
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Abstract |
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 Top Abstract IntroductionPatients and methodsResultsCommentDiscussionReferences |
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Methods. Between January 1981 and June 2001, 169 patients underwent sleeve lobectomy for non-small-cell lung cancer (n = 139) or carcinoid tumor (n = 30), including 61 with a preoperative contraindication to pneumonectomy. Mean age was 59 ± 14 years (range, 19 to 82 years). Vascular sleeve resection was performed in 11 patients. The remaining bronchial stump contained microscopic disease in 7 patients.
Results. Major bronchial anastomotic complications occurred in 6 (3.6%) patients: one was fatal postoperatively, three required reoperation, and two were managed conservatively. In the non-small-cell lung cancer group, operative mortality was 2.9% (4 of 139), and overall 5-year and 10-year survival rates were 52% and 28%, respectively. Six patients experienced local recurrence after complete resection. By multivariate analysis, two factors significantly and independently influenced survival: nodal status (N0 or N1 versus N2; p = 0.01) and microscopic invasion of the bronchial stump (p = 0.02). In the carcinoid tumor group, there were no operative deaths, and overall 5-year and 10-year survival rates were 100% and 92%, respectively.
Conclusions. Sleeve lobectomy achieves local tumor control and is associated with low mortality and bronchial anastomotic complication rates. Long-term survival is excellent for carcinoid tumors. For patients with non-small-cell lung cancer, N2 disease or incomplete resection is associated with a worse prognosis; outcome is not affected by presence of a preoperative contraindication to pneumonectomy.
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Introduction |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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Since the first report by Price-Thomas [2], sleeve lobectomy has been widely used to treat patients with central bronchogenic cancer [3–7]. However, bronchial anastomotic complications and operative mortality rates show considerable variation across studies, perhaps because of differences in surgical technique [8, 9]. Also, few studies report long-term survival rates after sleeve lobectomy for non-small-cell lung cancer (NSCLC), and in some studies, low-grade malignant tumors were added to the NSCLC group, modifying the results [7, 10, 11]. The two objectives of this study were to report our 20-year single-center experience with sleeve lobectomy for bronchogenic cancer, describing the surgical technique and separately reporting results in patients with NSCLC and low-grade tumors, and to investigate factors that might affect long-term survival.
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Patients and methods |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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Two thirds of the 169 sleeve lobectomies were performed in or after January 1992. For the last decade, sleeve lobectomy has been the procedure of choice, when technically feasible, for lung cancer resection even in patients without contraindications to pneumonectomy. During this study, 4,463 lung resections (908 pneumonectomies) were performed in our department. Sleeve lobectomy represented 6% of the total cases of surgical resections for lung cancer during the last year.
Preoperative evaluation
Tumor spread and functional status were evaluated preoperatively. Physical examination, chest roentgenography, spirometry, arterial blood gases, and quantitative ventilation and perfusion scans were performed routinely to evaluate functional status. Patients at high risk for heart disease were screened by echocardiography, thallium stress testing, and, in some cases, selective coronary arteriography. Tumor spread to the airway was evaluated by fiberoptic bronchoscopy, which plays a key role in selecting patients for sleeve lobectomy; patients who have submucosal invasion or extrinsic compression of a lobar orifice with a positive elective biopsy are good candidates for sleeve lobectomy. A bronchoscopic biopsy was collected routinely unless a hypervascular lesion was noted. Mediastinal nodal status was investigated by computed tomography and, in our more recent experience, by positron emission tomography. In patients with NSCLC, mediastinoscopy was performed when computed tomography showed mediastinal nodes larger than 1.5 cm in diameter or when positron emission tomography showed mediastinal fixation; mediastinoscopy was not used in patients with carcinoid tumor. Investigations for extrathoracic metastases were performed routinely. A pulmonary angiogram was performed when the tumor was adherent to the main pulmonary artery in a patient whose preoperative functional test results contraindicated pneumonectomy. In patients at high risk, a right heart catheterization was performed before and after balloon occlusion of the relevant pulmonary artery to detect pulmonary hypertension, precluding pneumonectomy.
Surgical technique
Single-lung ventilation was established through a double-lumen endotracheal tube. A posterolateral thoracotomy was performed in the fifth intercostal space. On the right, for upper sleeve lobectomy, the arch of the azygos vein was divided, allowing excellent exposure of the main bronchus. No irreversible procedures were performed until resectability was confirmed. First, the lobar branches of the pulmonary artery and the lobar vein were dissected to permit an assessment of tumor spread and resectability. Then, the lobar and main bronchi were dissected. Care was taken to preserve as much as possible of the bronchial vascular supply in the remaining lobes during mediastinal lymph node dissection. The hilar, carinal, paratracheal, esophageal, and inferior pulmonary ligament lymph nodes were routinely dissected. Circumferential bronchial resection was performed with a knife to obtain straight margins distant from the tumor. Specimens of the resection margins were taken for frozen-section examination to ensure complete resection.
Bronchial anastomosis was started using a short continuous running 4-0 polydioxanone suture (PDS, Ethicon, Inc., Somerville, NJ) lying on one third of the cartilaginous airway wall. The remaining cartilaginous and membranous walls were anastomosed using interrupted 3-0 or 4-0 polyglactin suture (Vicryl, Ethicon) tied at completion of the anastomosis. The knots were placed outside the lumen. The suture line was checked for air leaks by inflating the lung after immersing the anastomosis in fluid.
Fourteen patients had an upper lobe tumor in the right lung that extended within 5 to 10 mm from the carina. In these patients, the main bronchus was transected at the level of the carina (Fig 1) and the anastomosis was performed between the tracheobronchial bifurcation and the bronchus intermedius. Because closing the main bronchus ostium at the level of the carina produces excessive suture tension, the sleeve lobectomy performed in these 14 patients can be considered an alternative to sleeve pneumonectomy.
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Tumor resection was considered complete when the resection margins were free of disease. Postoperatively, the TNM classification system was used for staging [12].
The tumor was central in 151 patients (89%) and peripheral with nodal involvement in 18 patients (11%). The decision to perform sleeve lobectomy was based on the preoperative bronchoscopic evaluation in 76 patients (45%) and was made during the operation in 93 patients, of whom 59 (of 169; 35%) had previously unsuspected tumoral or nodal extension to the main bronchus and 34 (of 169; 20%) had bronchial margin involvement by frozen-section examination. Table 1 shows the location of the tumors.
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In 61 patients, pneumonectomy was contraindicated preoperatively because of a predicted postoperative forced expiratory volume in 1 s less than 40%, a high pulmonary artery pressure, or severe coronary artery disease. In 35 of these patients, preoperative bronchoscopy and computed tomographic scan showed that a standard lobectomy could not be performed because the tumor had spread to the adjacent main bronchus. In the other 108 patients (64%), sleeve lobectomy was performed electively.
Type of resection
Table 1 shows the types of lung resection and bronchial reconstruction. Upper sleeve lobectomy was the most common procedure. In 16 patients, the tumor invaded the main bronchus and the bronchus intermedius on the right or the lower bronchus on the left. The upper lobe was preserved, and the upper bronchus was anastomosed with the main bronchus. In 11 patients, the bronchogenic tumor invaded both the main bronchus and the pulmonary artery, and consequently, vascular sleeve resection was performed. This double-sleeve resection procedure was used significantly more often among patients who underwent left upper sleeve lobectomy (p = 0.004).
Patients were followed up by routine chest roentgenograms and chest computed tomographic scans. Fiberoptic bronchoscopy was performed routinely after the anastomosis in the operating room, before hospital discharge, 1 month after discharge, and when atelectasis or a persistent air leak indicated a need to look for anastomotic complications. Two patients with NSCLC and 1 patient with a carcinoid tumor were lost to follow-up more than 5 years after the sleeve resection. Follow-up data were obtained by direct contact with patients, relatives, or referring physicians. Survival was counted as the time from operation to death, dropout, or study completion.
Operative mortality was defined as death within 30 days of the operation or death directly related to the surgical procedure. Findings from local follow-up investigations were used to categorize recurrences as local (tumor growth within the anastomosed area and in the ipsilateral hemithorax in patients without a positive tumoral resection margin), mediastinal, or distant.
Statistical analysis
All results are expressed as the mean ± standard error. Categorical data were calculated as percentages and compared using the 
2 test. Survival rates were calculated by life-table analysis. Kaplan-Meier curves were plotted and compared using the log-rank test for univariate analysis. The results of the multivariate analysis of independent prognostic factors, which included nodal status and incomplete resection, were assessed by using the Cox proportional hazards stepwise model, using StatView V (Abacus Concepts, Berkeley, CA). Differences were considered significant when p was less than 0.05.
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Results |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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Sleeve lobectomy for carcinoid tumors (n = 30)
Of these 30 patients with low-grade malignancies, 25 had typical carcinoid tumor (grade I neuroendocrine tumor) and 5 had atypical carcinoid tumor (grade II neuroendocrine tumor). Twenty-two patients had stage I (15 IA and 7 IB) and 8 had stage II (8 IIB) disease. Twenty-six patients (87%) were N0 and 4 (13%) were N1. Fourteen (47%) patients had T1, 12 (40%) T2, and 4 (13%) T3 disease. Resection was complete in all 30 patients with carcinoid tumor.
Operative morbidity and mortality
Types of postoperative complications are listed in Table 2.
Overall operative mortality and morbidity rates were 2.4% and 12.4%, respectively. Overall operative morbidity was significantly higher in the compromised patients (p < 0.001), whereas operative mortality was not. Major bronchial anastomotic complications occurred in 3.6% of patients, with no significant difference between the compromised and noncompromised groups.
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Sleeve lobectomy for carcinoid tumors
There were no perioperative deaths. A single patient had a bronchial anastomotic stenosis, which became symptomatic 3 months after the right upper lobe sleeve resection. Repeated endoscopic dilatation failed, and completion pneumonectomy was required because of irreversible parenchymal damage. This patient was alive and free of disease more than 10 years later.
Survival
Sleeve lobectomy for non-small-cell lung cancer
In the NSCLC group, median survival was 66 months, and 5-year and 10-year survival rates were 52% and 28%, respectively (Fig 2). Mean and median follow-up in survivors was 42 and 28 months, respectively (range, 1 to 188 months). Table 3
lists all potential prognostic factors investigated in this study. The 5-year and 10-year survival rates were 55% and 39%, respectively, in patients with N0 disease and 68% and 19%, respectively, in patients with N1 disease. These two curves were similar, whereas the patients with N2 disease (n = 24) had a significantly worse curve with no survivors at 5 years (Fig 3).
Figure 4
shows survival according to TNM stage. The 5-year and 10-year survival rates were 55% and 36%, respectively, in patients with stage I disease and 62% and 37%, respectively, in patients with stage II disease. There was no significant difference between these two stages. None of the patients with stage III disease were alive 10 years after the sleeve lobectomy, and the 5-year survival rate was 21%. Neither a preoperative contraindication to pneumonectomy nor pulmonary artery sleeve resection significantly influenced survival.
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During follow-up, 55 of the 128 remaining patients died. Among them, 36 (65%) died of recurrent lung cancer. The first site of recurrence was local in 6, mediastinal in 15, and distant in 15. Eight (15%) other patients died of a second primary cancer; 5 of them had a different histology, and in the 3 remaining patients, the lung cancer developed in the contralateral lung more than 5 years after the sleeve lobectomy. The remaining 11 patients died of another disease with no documented lung cancer relapse.
Death by local tumor growth was significantly more common among the patients with incomplete resection (2 of 7 versus 6 of 132; p = 0.008). Among the patients with complete resection, fatal locoregional (both local and mediastinal) recurrence was seen in 11% (7 of 63) of patients with N0 disease, 12% (6 of 49) of those with N1 disease, and 40% (8 of 20) of those with N2 disease. The locoregional recurrence rate was significantly higher in patients with N2 disease (p = 0.001).
Sleeve lobectomy for carcinoid tumors
During follow-up, 1 patient died after 78 months from a myocardial infarction. The remaining 29 patients were alive without evidence of recurrence at the end of the study. Mean and median follow-up in survivors was 64 and 54 months, respectively (range, 4 to 180 months), and overall 5-year and 10-year survival rates were 100% and 92%, respectively (Fig 5).
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Comment |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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Bronchial sleeve resection preserves the functional lung parenchyma. The reimplanted parenchyma has been shown to contribute significantly to postoperative lung function [6]. A 1992 collective review of 1,915 bronchoplastic procedures performed during a 12-year period in patients with bronchogenic tumors found that sleeve lobectomy was followed by similar morbidity and mortality as compared with pneumonectomy but was associated with better lung function preservation [3]. Operative mortality was 5.5%, as compared with 2.4% in the present study. In recent series, operative mortality has ranged from 0% to 5.2% [4, 6, 9, 11, 17], which is similar to the range after standard lobectomy [18] and lower than after standard pneumonectomy [9, 19]. In the present series, although the operative morbidity rate was significantly lower in noncompromised patients, compromised patients did not have increased rates of operative mortality or bronchial anastomotic complications.
Preservation of the bronchial blood supply, creation of a tension-free bronchial anastomosis, and improved suture materials [1, 20] have resulted in better bronchial healing, thereby significantly reducing the incidence of bronchial anastomotic complications [7, 8, 14, 21]. Bronchial anastomotic complications were seen in 3.6% of our patients, which is similar to the rate in recent series [4, 9, 11, 17] and lower than the 10% rate in the review by Tedder and colleagues [3]. The most severe postoperative complication after sleeve lobectomy is bronchovascular fistula, which manifests as potentially fatal hemoptysis [3]. To prevent this complication, we routinely separate the pulmonary artery from the bronchial anastomosis by a pleural flap. When hemoptysis occurs in a patient who has had sleeve resection, a bronchovascular fistula should be suspected immediately and bronchoscopy performed on an emergency basis. In one of the two cases in our study, the fistula was identified early and repeat surgery was performed promptly. Completion pneumonectomy was not feasible because the bronchial anastomosis had been performed between the bronchus intermedius and the carina. Sleeve pneumonectomy was performed successfully. The rates of bronchopleural fistula and bronchial anastomotic dehiscence were lower than those reported by Tedder and colleagues [3] and similar to those in recent series [4, 9, 11, 17].
The main concern raised by the use of sleeve lobectomy to treat bronchogenic malignancy is the risk of local recurrence. Suture line recurrence may be related to lung preservation at the expense of adequate bronchial margins [3]. Therefore, Paulson and colleagues [22] recommended that the bronchial resection margins be at least 1.5 cm away from the tumor. The incidence of local recurrence has ranged from 5% to 51% [23, 24]. This wide variation is probably ascribable to the absence in most studies of a definition of local recurrence. In the present study, local recurrence was defined as tumor relapse after complete resection, located at the bronchial anastomosis or in the ipsilateral lung. Local recurrence occurred in 6 patients (5%). In addition, 2 patients with a positive bronchial stump died of local tumor development. Among the 139 patients with NSCLC, 21 died of local or mediastinal recurrence, resulting in a locoregional recurrence rate of 15%, which is similar to that reported by others [9, 11, 16] and lower than the 26% intrathoracic recurrence rate reported after complete standard NSCLC resection [25]. In a recent study comparing sleeve lobectomy with pneumonectomy for NSCLC, Okada and colleagues [9] found that the local recurrence rate was lower after bronchoplastic procedures.
Long-term survival rates after sleeve lobectomy for NSCLC were comparable with those after conventional resections in the review performed by Tedder and colleagues [3]. More recently, studies comparing sleeve lobectomy with pneumonectomy reported similar [4] or significantly longer survival [9] in patients treated with sleeve resection. Van Schil [16] reported that the most significant determinant of long-term survival after sleeve lobectomy was nodal status, with significantly shorter survival in patients with N2 disease as compared with those with N1 or N0 disease. In keeping with a study by Voyt-Moykopf and colleagues [15], none of our patients with N2 disease were alive 5 years after the sleeve lobectomy. It has been shown that N2 disease is highly predictive of distant recurrences [11]. In keeping with this, the main cause of death in our patients with N2 disease was distant relapse. This, together with the fact that complete lymph node dissection was performed in all our patients, suggests that pneumonectomy may not increase survival as compared with sleeve resection in these patients. In our study and in that reported by Mehran and colleagues [7], there were no significant differences in survival between N0 and N1 disease. Others, however, have found a significantly lower survival rate in patients with N1 than N0 disease [16], leading to controversy about the use of sleeve resection in noncompromised patients with N1 disease. Our results do not suggest that pneumonectomy in N1 disease may improve long-term survival.
Pneumonectomy limits pulmonary reserve, increases pulmonary artery pressure, and leads to greater long-term cardiopulmonary disability and worse quality of life than does lobectomy [9]. Also, pneumonectomy has been reported to increase the risk of cardiopulmonary death [9]. Thus, pneumonectomy can be viewed as a procedure that should be avoided. Moreover, development of a second primary lung tumor requiring further operation is not uncommon [7]. These data have led us and others [9, 11] to increase use of sleeve lobectomy. Thus, we agree with Faber [5] that sleeve resection is the procedure of choice whenever it is technically feasible, even in patients who could tolerate pneumonectomy.
In conclusion, sleeve lobectomy is a valid parenchyma-sparing procedure for bronchogenic tumor resection. It can be used as an alternative to pneumonectomy and even to sleeve right pneumonectomy in selected patients. Sleeve lobectomy achieves local tumor control and is associated with low rates of mortality and bronchial anastomotic complications. Long-term survival is excellent in patients with carcinoid tumors. In those patients with NSCLC, the main adverse prognostic factors are N2 disease and incomplete resection; the outcome is not affected by the presence of preoperative contraindications to pneumonectomy. Sleeve lobectomy, when technically feasible, should be the standard procedure for resecting all bronchogenic tumors.
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Discussion |
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TopAbstractIntroductionPatients and methodsResultsCommentDiscussionReferences |
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DR FADEL: Yes. This is a good suggestion. However, preoperative biopsy on the future site of anastomosis is not possible to perform, because the location of anastomosis is not predictable preoperatively. We routinely do frozen section specimens in the operating room, so we always are guided by this frozen section specimen on the bronchial margins.
DR PAUL E. VAN SCHIL (Edegem, Belgium): I enjoyed your presentation.
I have three questions for you. First of all, regarding N2 disease, you had a fairly high incidence of patients with N2 disease. Did you perform a routine mediastinoscopy before a sleeve resection, and, if not, would you change your strategy now?
DR FADEL: Thank you. We only did mediastinoscopy when on preoperative computed tomographic scan there was a mediastinal lymph node larger than 1.5 cm diameter; we do not perform mediastinoscopy routinely. Maybe a routine positron emission tomographic scan will help to decrease the number of operated N2 disease.
DR VAN SCHIL: I noticed that you had a very good survival in patients with N1 disease, much higher than usually reported. For example, in our series of 145 sleeve resections, which was reported some years ago, we had a rather poor prognosis in N1 disease (Ann Thorac Surg 1996;61:1087–91).
DR FADEL: We had similar results in N1 and N0 with carinal resection.
DR VAN SCHIL: Lastly, did you look at the incidence or the prevalence of a second primary lung cancer after sleeve resection?
DR FADEL: Yes. We had 8 cases of a second lung cancer, in the contralateral lung.
DR VAN SCHIL: And did those patients have another operation?
DR FADEL: Four of them had a second operation.
DR VAN SCHIL: Thank you.
DR RICHARD I. WHYTE (Stanford, CA): I have a couple of quick questions. First of all, you had a number of patients who had induction chemotherapy. Did you find that increased or was associated with an increased risk of complications?
Second, you mentioned 1 patient who had a bronchovascular fistula. Do you do anything to separate the bronchial and vascular suture lines?
DR FADEL: Induction chemotherapy was used in only 3 patients with N2 disease in this series. Only 1 of them experienced postoperative complications. In the beginning of our experience, patients with N2 disease were more frequently managed by pneumonectomy. We try now to perform a sleeve lobectomy even in N2 disease because for these patients the major cause of death is metastasis and not local recurrence. For the second question, we always separate the bronchial anastomosis from the artery with a pleural flap. We do not think that it brings a blood supply, but it is a barrier between the anastomosis and the pulmonary artery.
DR YOUNGICK LEE (Ridgewood, NJ): I have a question for you. The 7 patients you found with microscope involvement, what did you do with these patients?
DR FADEL: Unfortunately those patients could not tolerate pneumonectomy, so they had adjuvant treatment with radiation therapy and chemotherapy. Two of them died of local recurrence. But it is not really a local recurrence. It is a local growth of the remaining tumor. Concerning the 2 other patients, 1 died of bronchovascular fistula and 1 died postoperatively of pneumonia. So, there are 3 remaining patients who are still alive without recurrence.
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