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J Thorac Cardiovasc Surg 1994;107:576-0583
© 1994 Mosby, Inc.
General Thoracic Surgery |
Ste-Foy, Quebec, Canada
Address for reprints: Jean Deslauriers, MD, FRCS(C), 2725 Chemin Ste-Foy, Ste-Foy, Quebec, Canada, GIV 4G5.
Abstract
Sleeve lobectomy is a lung-saving procedure indicated for central tumors for which the alternative is a pneumonectomy. The relation between survival and nodal status is controversial because, in most series, the presence of N1 disease adversely affects the prognosis with few or no long-term survivors. During the period 1972 to 1992, 142 patients underwent sleeve resection for lung cancer at our institution. Mean age (±standard deviation) was 60.7 ± 9.1 years (range 11 to 78 years), and indications for operation were a central tumor in 112 patients (79%), a peripheral tumor in 18 patients (13%), and compromised pulmonary function in 12 patients (8%). Histologic type was predominantly squamous (72.5%) followed by nonsquamous (24.6%) and carcinoid tumors (2.8%). Resection was complete in 124 patients (87%) and incomplete in 18 (13%), and the operative mortality was 2.1% (n = 3). Follow-up was complete for the 139 remaining patients. Including operative deaths, survivals at 5 and 10 years for all patients were 46% (95% confidence intervals 38% to 55%) and 33% (95% confidence intervals 24% to 42%), respectively. For patients with N0 status (n = 73), 5- and 10-year survivals were 57% (95% confidence intervals 45% to 69%) and 46% (95% confidence intervals 32% to 60%); for patients with N1 status (n = 55), these rates were 46% (95% confidence intervals 32% to 60%) and 27% (95% confidence intervals 14% to 40%) (p = 0.13). No patient with N2 status (n = 14) survived 5 years. Local recurrences occurred in 23% of cases, but the prevalence was not statistically different between patients with N0 disease (16.6%) and N1 disease (23.1%) (p = 0.43). These data suggest that sleeve resection is an adequate operation for patients with resectable lung cancer and N0 N1 status. The presence of N2 disease significantly worsens the prognosis and may contraindicate the use of the procedure. (J THORAC CARDIOVASC SURG 1994;107:576-83)
Sleeve lobectomy is a lung-saving procedure indicated for central tumors for which the alternative is a pneumonectomy. It preserves otherwise normal lung tissue and enables surgical resection to be done in patients with inadequate pulmonary reserve.
The first successful bronchoplasty is credited to Price-Thomas,
1 but the first significant and comprehensive report on the use of these techniques is that of Paulson and Shaw 2 in 1955. They reviewed the case histories of 18 patients in whom sleeve resection had been done for a variety of reasons, including benign conditions, and they stressed the importance of preserving functional parenchyma in lung cancer operations. Sleeve lobectomy was then considered a compromise operation for patients whose pulmonary reserve was believed to be inadequate to permit pneumonectomy. Since then, many reports have suggested that sleeve resection accomplishes tumor and nodal clearance similar to that of pneumonectomy with the possible advantages of lower operative mortality rates, equal if not better survival rates, and improved quality of life. 3-18
In most series, the overall 5-year survival after sleeve resection carried out for lung cancer is 40% to 45% but the presence of N1 disease adversely affects the prognosis with few or no long-term survivors. This report presents a comparative survival analysis based on nodal status for 142 patients who underwent sleeve resection for lung cancer during a 20-year interval. The results indicate that there is no statistically significant difference in survival between patients with N0 and N1 status.
PATIENTS AND METHODS
General characteristics of the study population
Between January 1972 and December 1991, 142 patients underwent sleeve resection as primary treatment for bronchogenic carcinoma. There were 123 men and 19 women whose ages at the time of operation ranged from 11 to 78 years with a mean of 60.7 ± 9.1 years (mean ± standard deviation) (median age of 61 years). The first bronchoplasty was done in May 1972 and, from that date until January 1, 1980, 22 patients had a sleeve resection. The remaining 119 patients had operation during the eighties and early nineties. We now average 8 to 10 cases per year, which is approximately 5% of our total volume of resectional surgery for lung cancer.
Sleeve resection was 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 bronchoplastic procedure. In this group, indications for operation were a central tumor in 112 patients (79%) or a peripheral tumor with nodal involvement at the bronchopulmonary level (N1) in 18 patients (13%). In all of those patients, 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 12 additional patients, all of whom had 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 (120/142) for pretreatment staging of the superior mediastinum. Only 6 patients had a bronchoplasty when nodal metastasis was identified at mediastinoscopy.
Operative procedures
Although the initial finding that identified a possible candidate for sleeve resection was the bronchoscopic appearance of the tumor that extended to the lobar orifice and toward the mucosa of the adjacent main bronchus, the final decision was made at the time of thoracotomy. Operative findings such as evidence of disease along the resection line of the lobectomy, extraluminal extension of the carcinoma to the main bronchus, or presence of metastatic nodes at the hilum of the lobe to be removed were considered possible indications for sleeve resection. Procedures were considered complete if all gross carcinoma had been removed, the resection margin was free of disease, and the highest mediastinal node was free of tumor.
The majority of sleeve resections were done for central tumors involving the bronchial origin of either upper lobe (n = 124, 87%) (Table I). In 9 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. Seven patients had a lower lobe sleeve resection, and in 2 patients a tumor located in the left main bronchus could be resected without sacrificing any of the distal lung. No patient in this series required a concomitant full sleeve resection of the pulmonary artery (double sleeve resection) and no patient had preoperative radiotherapy. Resection was complete in 124 patients and incomplete in 18 patients usually because of diseased bronchial resection margins.
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Table II). The majority of resected neoplasms (72.5%) were squamous carcinomas and their prevalence was similar in the N0 group and in the N1 group. Thirty-five patients had nonsquamous carcinomas and 4 patients had a typical carcinoid tumor, all with N0 status. For the purpose of survival analysis, the squamous group was considered to include patients having pure squamous disease, whereas the nonsquamous group included all other patients, including some with a mixture of cell types.
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19 and the American Joint Committee on Cancer Staging. From 1972 to 1978 staging was done retrospectively, but for the remaining years (1978 to 1992) staging was based on complete clinical and pathologic analysis of the primary tumor (T status) and intraoperative sampling of at least the bronchopulmonary, hilar, and mediastinal (superior, posterior, and anterior mediastinum) nodal areas (N status).
Seventy-three patients (51.4%) had N0 disease and 55 (38.7%) had N1 disease, and the T status distribution shows that it is nearly identical for the two groups (
Table II). Stage distribution of the patients included in the series also shows that the majority are either in stage I (43%, 61/142) or in stage II (38.8%, 48/142) categories. Among the 31 patients with stage IIIa disease, 14 had N2 disease. Two patients had T4 tumors (stage IIIb) because of a nonmalignant exudative pleural effusion.
Follow-up
Patients were observed from the date of operation to the time of death or end of observation (July 1992), whichever came first. No patient was lost to follow-up. The potential duration of follow-up was at least 12 months for all patients under review and the mean follow-up time was 2149 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. Sites of first recurrences were classified as being (1) local, (2) distant, (3) local and distant, (4) unknown site, or (5) second primary defined as a tumor of different histologic type or a tumor of similar histologic type if it occurred more than 2 years after the first operation or if its origin could be traced to a carcinoma in situ. 20, 21
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.
Statistical analysis
Results are presented as means (±standard deviation) for continuous variables and as percentages for categoric data. The 
2 test was used to compare these proportions. The analysis of survival was based on deaths from all causes. Survival was analyzed according to the Kaplan-Meier method and differences between survival curves were compared by the log-rank test. 22, 23 Survival data are given with the 95% confidence interval (CI).
RESULTS
Operative morbidity and mortality
Three patients died (2.1% operative mortality rate) during the immediate postoperative period. Two of the three deaths were the result of infectious complications in the reimplanted lung and the third operative death was due to a pulmonary embolus.
Early nonfatal complications were seen in 16 additional patients and these are listed in Table III. Four patients had a late complication at the site of the bronchial anastomosis. Among those, 2 had granulation tissue that was successfully removed with a bronchoscope, and 2 had a fibrous stricture that was dilated in 1 but necessitated completion pneumonectomy in the other.
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Table IV. The overall rate of local recurrence was 23%, but the distribution was not significantly different between patients with N0 and patients with N1 disease (p = 0.43). When the resection was complete, 21 patients (17%) had a local recurrence. By comparison, when the resection was incomplete, 11 patients (61%) had a local recurrence (p < 0.001). Local recurrence was also more common in patients with N2 disease (p < 0.001).
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Sleeve resection of the bronchus was introduced to avoid pneumonectomy in proximal lung tumors and, in most series of bronchoplasties done for lung cancer, lesions in the hilum of the right upper lobe constitute the commonest indication for operation. The frequency of this location relates to the anatomic structure of the right main bronchus and the relatively long bronchus intermedius. The anatomic justification for sleeve resection of the upper lobes was provided by Nohl, 24 who described, in 1956, the lymphatic and vascular spread of bronchogenic carcinoma and emphasized the predictability of upper lobe lymphatic drainage. He showed that right upper lobe lesions metastasize to nodes located below the right upper lobe bronchus and seldom involve nodes located below a line drawn from the middle lobe bronchus to the apical bronchus of the lower lobe. Anatomic justification was further provided by Maeda and colleagues, 25 who reported on 47 patients who were pathologically studied to identify local tumor spread. They showed that lung cancer not only infiltrates around the primary tumor for a distance averaging 7.2 mm (range of 3 to 20 mm) but also that metastatic clusters of cancer cells are often found in the lymphatics, nodes, bronchial arterials, and nerve sheaths in the peribronchial and intrabronchial wall.
In 1981, Immerman and colleagues 26 reviewed survival and sites of recurrences in 99 patients with non-small-cell stages I and II carcinoma of the lung resected for cure from 1967 through 1975. The overall 5-year disease-free survival was 45%. In patients with stage I disease (T1 N0, T2 N0, T1 N1) the 5-year disease-free survival was 55%, and in those patients with stage II disease (T2 N1) it was 14%. Treatment was unsuccessful in 44 (44%) of the 99 patients, and the site of the first relapse was a local recurrence in 18 patients (18%) and a distant metastasis in 26 (26%). In the Ludwig Lung Cancer Study Group analysis of patterns of failure in patients with resected stage I and II non-small-cell carcinoma of the lung, 27 1012 patients were analyzed and the site of initial failure for the 426 patients with objective evidence of failure recorded. This site was intrathoracic in 231 patients (23% of patients having resection) and extrathoracic including supraclavicular nodes in 195 patients (19%). Other studies have shown similar patterns of recurrences after complete resections of early-stage lung cancer. 28-30
In a review of the literature over a 12-year period (1980 to 1992), Tedder and colleagues 18 reported that the 5-year survival of patients undergoing sleeve lobectomy for bronchogenic carcinoma was 40% (Table V). Sleeve lobectomy for stage I, II, and III disease yielded 63%, 37%, and 21% 5-year survivals, and absence of nodal involvement was associated with a 60% 5-year survival. These survival figures are comparable with those seen after conventional lobectomy but much better than the 5-year survivals reported after pneumonectomy. 31
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9 reported 5- and 10-year survivals of 71% and 48.5%, respectively, for patients with uninvolved hilar nodes. When the tumor had metastasized into the hilar nodes, the survival was significantly worse, with a 5-year survival of 17% and a 10-year survival of only 10% (p < 0.001). In 1991, Van Schill and coworkers 17 also studied the impact on survival of nodal status in 112 patients with T2 and T3 squamous cell carcinoma who had had a sleeve lobectomy between 1960 and 1989. The 5- and 10-year survivals for patients with N0 disease (n = 52) were 59% and 47%, for those with N1 disease (n = 51) 21% and 0%, and for those with N2 disease (n = 9) 44% and 0%, respectively. They raised the question as to whether patients with N1 disease should be regarded as having systemic disease and be treated accordingly with neoadjuvant therapy, but they did not specifically conclude that sleeve resection should be avoided in patients with N1 disease.
The results in the present series are concordant with those of Naruke, 15 who reported 5-year survivals of 50% for patients with N0 disease and 45.9% for patients with N1 disease, and they indicate that sleeve lobectomy should be considered in any case of lung cancer with N0 and N1 status that can be completely resected by this technique. Because the definition of complete resection is essential to this decision, intraoperative frozen section evaluation of lobar, hilar, and mediastinal nodes, and ultimately frozen section biopsy specimens of both resection margins, are a critical feature of the operation. The presence of diseased interlobar nodes between the right upper and middle lobes is not a contraindication to sleeve resection, but the middle lobe might have to be included in the bronchial sleeve.
On the basis of our results, lymph node involvement has an adverse effect on survival, but this effect is significant only in the N2 category, in which no patient survived 5 years after operation. For the 55 patients included in the N1 subset, the 5-year survival figure of 46% is not significantly different from that observed for the N0 subset (57%) and indicates that patients with N0 or N1 status can expect a survival after sleeve resection similar to that expected after conventional procedures for similar stage tumors. 26, 27, 30 The difference in survival at 10 years (N0: 46%; N1: 27%) and the difference in median survival (N0: 8.02 years; N1: 3.90 years) are greater and in keeping with the pathologic stage of disease (stage I versus stage II).
The prevalence of local recurrence of 23% is also not significantly different between these two groups and is similar to what is reported after all types of resection. 26-30 In this series, the prevalence of second primary tumors is notable at 12.2% and it is higher than that reported by Van Schill and associates 32 (7.6%). This observation illustrates one of the most important features of sleeve resection, which is to preserve otherwise normal lung tissue enabling further surgical resection to be done.
Appendix: DISCUSSION
Dr. Willard A. Fry (Evanston, Ill.).
I raise one question. You have highlighted the dismal prognosis of N2 disease, but I submit that if the disease has been eradicated with a sleeve lobectomy, palliation for those patients is probably better than otherwise. I am not sure that I would agree with the conclusion that treatment should be avoided. I would certainly hesitate to perform a right pneumonectomy on a patient who is going to have a short survival time.
Dr. Deslauriers.
The answer to that question is very personal because I seldom do palliative surgery of any kind. In my opinion, resection should always be potentially curative even if it is done as a compromise procedure. The second reason why I think bronchoplastic procedures may not be adequate for N2 disease is that, at least in theory, not as many nodes are being removed as would otherwise be removed with a pneumonectomy. Nodes are being left caudally along the bronchus intermedius, and this possibly is the reason that the failure rate is so high.
Dr. Thomas R. J. Todd (Ottawa, Ontario, Canada).
It seems to me that what we classify as an N1 lymph node is a very large nodal sump area that can extend anywhere from a lymph node that is intraparenchymal near the tumor out to a lymph node right in the hilum near the pleural reflection. In your series of patients, did you make any attempt to differentiate the level of those nodes, specifically those that might have been at the level of the main-stem bronchus or the lobar orifice versus those that were identified by the pathologist when the specimen was examined?
Dr. Deslauriers:
This was not done because it is extremely difficult, even prospectively, to identify the specific sites of N1 subsets. This identification is also difficult for the pathologist who dissects the resected lung. Dr. Van Schill from the Netherlands did look at survival related to location of N1 disease and he found no differences between patients with metastatic disease in various N1 sites.
Dr. Thomas Shields (Chicago, Ill.).
What is your opinion concerning a concomitant angioplastic procedure? Vogt-Moykopf is a very strong advocate of this procedure, particularly with the left upper lobe. The Japanese, like you, advocate doing a pneumonectomy. Is that your philosophy or do you not see this involvement very often?
Dr. Deslauriers.
We sometimes see this degree of involvement, but if the patient can tolerate a pneumonectomy, we prefer to do a pneumonectomy. The double sleeve procedure, which is a bronchial sleeve with a main artery sleeve, is a good operation but carries a significantly higher mortality rate. Vogt-Moykopf reports a 16% to 18% mortality rate with a double sleeve operation. On the left side, a pneumonectomy is well tolerated by most individuals, so we have no hesitation to carry it out whenever necessary. In a patient with compromised function, a partial resection of the pulmonary artery can be accomplished with proximal and distal clamping. The arterial wall can then be replaced with a pericardial patch. This procedure is fairly easy and is well tolerated. If there are any doubts about tumor clearance, a pneumonectomy should always be done.
Footnotes
From the Division of Thoracic Surgery,a Centre de Pneumologie de Laval; and Department of Surgery,b Laval University, Ste-Foy, Quebec, Canada 
Read at the Seventy-third Annual Meeting of The American Association for Thoracic Surgery, Chicago, Ill., April 25-28, 1993.
*Statistician, Laval University Epidemiology Research Group.
**Epidemiologist, Laval University Epidemiology Research Group.
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