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Ann Thorac Surg 1999;67:1557-1562
© 1999 The Society of Thoracic Surgeons


Original Articles

Favorable results after sleeve lobectomy or bronchoplasty for bronchial malignancies

Hon-Chi Suen, MBBSa, Bryan F. Meyers, MDa, Tracey Guthrie, BSNa, Mary S. Pohl, MHSa, Sudhir Sundaresan, MDa, Charles L. Roper, MDa, Joel D. Cooper, MDa, G. Alexander Patterson, MDa

a Division of Cardiothoracic Surgery, Washington University School of Medicine, Barnes-Jewish Hospital, St. Louis, Missouri, USA

Address reprint requests to Dr Patterson, Division of Cardiothoracic Surgery, Washington University School of Medicine, One Barnes-Jewish Hospital Plaza, Suite 3108, Queeny Tower, St. Louis, MO 63110

Presented at the Forty-fifth Annual Meeting of the Southern Thoracic Surgical Association, Orlando, FL, Nov 12–14, 1998.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Sleeve lobectomy and bronchoplasty are established alternatives to pneumonectomy for bronchial malignancies involving a main bronchus. However, potential bronchial anastomotic complications have deterred the general application of these types of resection. Some reports have contained a mixture of non-small cell lung cancer (NSCLC) and tumors of low-grade malignancy, making it difficult to assess the long-term results of these procedures as an alternative to pneumonectomy for lung cancer.

Methods. We retrospectively reviewed our experience with sleeve lobectomy and bronchoplasty for bronchial malignancies from January 1988 to September 1998 separating NSCLC (n = 58) from tumors of low-grade malignancy (n = 19). We compared the overall results between sleeve lobectomy and pneumonectomy (n = 142) performed for NSCLC over the same time interval.

Results. For NSCLC, after sleeve lobectomy, the operative mortality was 5.2% (3 of 58 patients) and the overall 5-year actuarial survival was 37.5%. After pneumonectomy, the operative mortality was 4.9% (7 of 142 patients) and the overall 5-year actuarial survival was 35.8%. For tumors with low-grade malignancy, there was no operative mortality after sleeve lobectomy or bronchoplasty and the 5-year actuarial survival was 100%. Major bronchial anastomotic complications occurred in 3 patients among the 77 patients who underwent sleeve resection.

Conclusions. Sleeve resection can be performed with a low risk of bronchial anastomotic complication. The long-term survival after sleeve resection for NSCLC is similar to pneumonectomy. Excellent results are obtained after sleeve resection for low-grade malignancies.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Since the pioneering work of Price-Thomas [1], D’Aubreu and MacHale [2], and Gebauer [3], bronchoplasty has become a standard procedure for benign lesions situated at favorable locations in the main bronchus. Allison [4] performed the first sleeve resection for bronchogenic carcinoma. Paulson and Shaw [5], as well as Jensik [6] and Faber [7] and their associates were credited with promoting sleeve resection as an alternative to pneumonectomy for selected patients with non-small cell lung cancer (NSCLC). Various reports have shown that long-term survival after sleeve resection for NSCLC is comparable with or better than that seen after pneumonectomy [811]. However, the increased complexity of sleeve resection as compared to pneumonectomy has led to reports with a high prevalence of bronchial anastomotic complication [7] or a high operative mortality [12]. The pathologic diagnoses in some series [13, 14] have included a mixture of NSCLC and other low-grade malignant tumors, thus skewing the results. Pneumonectomy patients, when used as a cohort for comparison, were either historic [8], chosen from a noncontemporaneous population [10], or highly selected [11]. This report reviews our results of sleeve lobectomy and bronchoplasty for bronchial malignancies at a single institution. In our analysis, patients with NSCLC were separated from those with low-grade malignancies, and the results of sleeve lobectomy for NSCLC were compared with results of pneumonectomy performed for NSCLC in the same time period.


    Material and methods
 Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
We retrospectively reviewed our experience with three types of resection for bronchial malignancies from January 1988 to September 1998: sleeve lobectomy for NSCLC, pneumonectomy for NSCLC, and sleeve lobectomy or bronchoplasty for low-grade malignancies. Types of resection were noted and the final pathologic staging was classified according to TNM classification of the American Joint Committee on Cancer Staging and End Results Reporting [15]. The operative mortality included all deaths related to operation regardless of the postoperative interval. Follow-up data were obtained from patients’ office or hospital charts or by direct contact with patients, relatives, or the referring physicians. Survival was estimated by the Kaplan-Meier method with the date of thoracotomy as the starting point. The survival of patients after sleeve lobectomy for NSCLC was compared with the survival of contemporaneous consecutive patients treated for NSCLC with pneumonectomy. Because our experience of sleeve resection for NSCLC was only a modest one, no attempt was made to separate the results according to pathologic stages. The Mantel-Haendzel pooled-relative log-rank test was used to analyze the survival curves for similarity. Fisher’s exact test was used to compare two percentages. All statistical tests were completed using Systat 7.0 software (SPSS Inc, Chicago, IL). Values of p of 0.05 or less were considered statistically significant.


    Results
 Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
From January 1988 to September 1998, 1,377 resections were performed for bronchial malignancies at the Barnes-Jewish Hospital, St. Louis, MO. Seventy-seven (5.6%) patients underwent sleeve resection; 58 (4.2%) were for NSCLC and 19 (1.4%) for low grade malignancies. One hundred forty-two (10.3%) patients underwent pneumonectomy for NSCLC.

Results of sleeve lobectomy for non-small cell lung cancer
The 58 patients who underwent sleeve lobectomy for NSCLC included 41 (70.6%) men and 17 (29.3%) women. The ages ranged from 33 to 82 years with a mean age of 63.7 years. Types of sleeve resections are listed in Table 1. Of note, among the 35 right upper lobe sleeve lobectomies, 2 required resection of the tracheal carina as well and 1 had a concomitant middle lobectomy. Among the 15 patients undergoing left upper lobe sleeve lobectomy, 1 had concomitant resection of the first three ribs for a superior sulcus tumor.


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Table 1. Types of Resection

 
After a detailed history and physical examination, all patients underwent chest roentgenogram, computed tomographic scan of the chest and upper abdomen, and bronchoscopy before operation. One patient had a preoperative pulmonary artery angiogram performed to assess suspected pulmonary artery involvement. Fifty-five of the 58 patients had mediastinoscopy before operation. The remaining 3 patients had either mediastinal lymph node dissection or sampling at the time of thoracotomy. Only one 33-year-old patient had biopsy-proven N2 disease by mediastinoscopy before operation; all others were considered N0 or N1 and M0 at the time of operation.

Three patients received preoperative neoadjuvant chemotherapy or radiotherapy, or a combination of therapies. All were initially deemed inoperable at outside institutions before referral to our center. One of these patients was treated with 8,000 cGy of irradiation over two courses, starting 1.5 years before referral.

When patients were retrospectively analyzed as to whether or not they could have tolerated pneumonectomy, 42 of the 58 patients were judged to be suitable for pneumonectomy, as determined by a forced expiratory volume in 1 second of more than 50% predicted, and the absence of significant comorbidity. Twelve patients were judged to be compromised for pneumonectomy (forced expiratory volume in 1 second, < 50% predicted, or with significant comorbidity). Pulmonary function data were not available for 4 patients.

Technique
The sleeve resection was performed through a posterolateral thoractomy in 56 of the 58 patients. Preoperative workup suggested proximal pulmonary artery or superior vena cava involvement by tumor in 2 patients who thus underwent resection (right upper lobe sleeve lobectomy and right upper lobe sleeve lobectomy with middle lobectomy) through a median sternotomy. At operation, the suspected pulmonary artery involvement was found to be inaccurate, but the superior vena cava involvement required a tangential resection of the vena cava with primary closure. Due to the proximity of the tumor to the pulmonary artery, 6 patients had concomitant tangential excision of a portion of pulmonary artery. No patient required full sleeve resection of the pulmonary artery.

Fifty-two of the 58 sleeve lobectomies included an upper lobe, and all of them had mobilization of the inferior pulmonary ligament. Fourteen patients, all of whom had right-sided sleeve lobectomies, required an inferior pericardial release to reduce tension at the bronchial anastomosis. In most patients, the bronchial anastomosis was performed with interrupted absorbablesutures (3-0 or 4-0 Vicryl or PDS; Ethicon Inc, Somerville, NJ). Sutures were tied on the outside except for the portion of the anastomosis adjacent to the pulmonary artery where knots were placed inside. Size discrepancy between the proximal and distal bronchus was usually managed by careful proportional spacing of the sutures on either side of the anastomosis. Occasionally, a corner of the main bronchial defect was closed with interrupted sutures to minimize the discrepancy. All anastomoses were wrapped with vascularized tissue for protection. A flap of parietal pleura was used most commonly. Other vascularized tissue used included pericardial fat pad, thymus, intercostal muscle, omentum, or a combination of these. In the patient who had received high-dose preoperative irradiation (8,000 cGy), we used both omentum and intercostal muscle to wrap the bronchial anastomosis.

Bronchoscopy was performed intraoperatively and before discharge to confirm the patency and viability of the bronchial anastomosis. For the first few postoperative days, the patient was positioned with the operated side up to help drainage of pulmonary secretions. Minitracheostomy and bronchoscopy were liberally performed in the early postoperative period whenever necessary for bronchial toilet.

Twenty-one patients received postoperative adjuvant chemotherapy or radiotherapy, or a combination of therapies, for T3, T4, N1, or N2 disease.

Pathology and staging
Among the 58 patients who underwent sleeve lobectomy for NSCLC, 18 (31.0%) had stage I, 28 (48.3%) had stage II, and 12 (20.7%) had stage III disease. One of the stage II patients had a synchronous contralateral stage II upper lobe cancer for which he underwent a lobectomy 1 month after his sleeve lobectomy. Twenty-six patients had N0, 25 had N1, and 7 had N2 disease.

Forty-two patients had squamous cell carcinoma, 10 had adenocarcinoma, 4 had adenosquamous carcinoma, 1 had large cell undifferentiated carcinoma, and 1 had a combined squamous cell carcinoma and non-Hodgkin’s lymphoma.

Mortality, morbidity, and survival
The operative mortality for the 58 NSCLC sleeve lobectomies was 5.2% (3 of 58 patients). One patient died from pulmonary embolism on postoperative day 8 and 1 from a myocardial infarction after discharge on postoperative day 22. The third patient was discharged from the hospital after an apparently uneventful right upper lobe sleeve lobectomy and superior segmentectomy of the right lower lobe but died from exsanguinating hemoptysis on postoperative day 32, presumably due to a bronchovascular fistula. Unfortunately, postmortem study was not available. Other complications are listed in Table 2. Of note, there were only two complications related to the bronchial anastomosis. No patient required completion pneumonectomy.


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Table 2. Operative Mortality and Morbidity

 
The length of hospital stay ranged from 3 to 19 days (mean, 8.2 days). The follow-up was complete and ranged from 8 days to 10.7 years (mean, 3.6 years). The overall 5-year actuarial survival for the entire group of NSCLC resections was 37.5% (Fig 1).



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Fig 1. Overall survival of non-small cell lung cancer patients who underwent sleeve lobectomy or pneumonectomy.

 
The actuarial survival curves of the noncompromised and compromised groups are shown in Figure 2. The compromised patients who were denied a pneumonectomy had survival after sleeve lobectomy similar to the pneumonectomy group, whereas the uncompromised group had statistically insignificant improved early and intermediate survival compared to the compromised group.



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Fig 2. Survival of compromised and noncompromised patients after sleeve lobectomy for non-small cell lung cancer and comparison with survival of patients after pneumonectomy for non-small cell lung cancer.

 
Results of pneumonectomy for non-small cell lung cancer
The 142 patients who underwent pneumonectomy for NSCLC included 81 (57%) men and 61 (43%) women. The ages ranged from 43 to 84 years with a mean age of 66.5 years. Sixty-seven patients underwent right pneumonectomy and 75 patients required left pneumonectomy.

Pathology and staging
Thirty-seven patients (26.1%) had stage I, 46 patients (32.4%) had stage II, 58 patients (40.8%) had stage III, and 1 patient (0.7%) had stage IV NSCLC.

Eighty-two patients had squamous cell carcinoma, 41 patients had adenocarcinoma, 7 patients had adenosquamous carcinoma, and 12 patients had large cell undifferentiated carcinoma. Thirty-four patients received postoperative adjuvant chemotherapy or radiotherapy, or a combination of both therapies.

Mortality, morbidity, and survival
The operative mortality after pneumonectomy for NSCLC was 4.9% (7 of 142 patients). The causes of death included respiratory failure (n = 3), stroke (n = 2), bronchopleural fistula (n = 1), and myocardial infarction (n = 1). Postoperative morbidities are listed in Table 2. Of note, the incidence of respiratory failure was higher after pneumonectomy (7%) than after sleeve lobectomy (1.7%). The length of hospital stay ranged from 4 to 58 days with a mean of 9.6 days. The follow-up was complete and ranged from 15 days to 10.1 years (mean, 3.6 years). The overall 5-year actuarial survival was 35.8% (Fig 1). Statistical comparison between sleeve lobectomy and pneumonectomy for NSCLC revealed no significant difference in overall survival (Fig 1).

Results of sleeve resection for low-grade malignancies
The 19 patients who underwent sleeve resection for low-grade malignancies included 7 (36.8%) men and 12 (73.2%) women. The ages ranged from 20 to 78 years with a mean age of 43.8 years.

Pathology and staging
Fifteen patients had grade I neuroendocrine tumor (typical carcinoid). Grade II neuroendocrine tumor (atypical carcinoid), mucoepidermoid carcinoma, pleomorphic adenoma,and squamous cell papilloma were each seen in 1 patient. Fourteen patients had stage I and 5 patients had stage II disease.

Technique
Eighteen of the 19 patients had the sleeve resection performed through a posterolateral thoracotomy. One patient underwent sleeve resection of the left main bronchus through a median sternotomy. Operative techniques for sleeve resection was almost completely identical to that used for NSCLC, except that a minimal negative bronchial resection margin was accepted in these patients. Types of sleeve resection are listed in Table 1. Of note, 8 patients (42%) had sleeve resection of the main bronchus or bronchus intermedius only, without removal of pulmonary parenchyma.

Mortality, morbidity, and survival
There was no operative mortality. Three patients had postoperative complications (Table 2). One patient had symptomatic bronchial stenosis after excision of the bifurcation of the left main bronchus. This occurred after a complicated reconstruction performed in an aggressive attempt to preserve all pulmonary parenchyma in a patient with a type I neuroendocrine tumor at the bifurcation of the left main bronchus. The bronchial stenosis persisted despite repeated bronchoscopic dilatation and finally required a sleeve resection of the left lower lobe and reanastomosis of the left upper lobe to the left main bronchus with a good long-term result. One patient had a minor suture granuloma causing an irritating cough and was cured by bronchoscopic removal of two sutures. One other patient had a postoperative dysrhythmia.

The length of hospital stay ranged from 3 to 9 days (mean, 5.8 days). The follow-up was complete and ranged from 2 months to 10.6 years (mean, 4.1 years). At the time of last follow-up, all patients were alive without evidence of recurrence and the 5-year actuarial survival was 100%.


    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
In 1992, Tedder and colleagues [16] reviewed the literature on bronchoplastic procedures for malignancy published in the previous 12 years. They meticulously analyzed the morbidity, mortality, and survival of this collective experience of 1915 bronchoplastic procedures. Comparison of our results with the collective experience summarized by Tedder was presented in Table 2.

Bronchial anastomotic complications were major features in earlier reports of sleeve resection. Completion pneumonectomy or lobectomy for anastomotic dehiscence or stenosis was common after sleeve lobectomy [7]. Our results showed that bronchial anastomosis can be performed with low morbidity and mortality. In our series of 77 sleeve lobectomies and bronchoplasties for pulmonary malignancies, there were only 3 major bronchial complications. One was a bronchovascular fistula and two were bronchial anastomotic stenoses. One stenosis occurred after a complicated reconstruction performed in an aggressive attempt to preserve all pulmonary parenchyma in a patient with type I neuroendocrine tumor at the bifurcation of the left main bronchus. This patient recovered after a redo sleeve lobectomy, which, if performed at the first operation, might have avoided the complication.

Of note, 3 patients in the NSCLC sleeve lobectomy group underwent preoperative chemotherapy or irradiation, or both therapies (up to 8,000 cGy). Fortunately, with careful technique and appropriate coverage, bronchial healing took place. The low prevalence of bronchial anastomotic complication probably explains the equally low prevalence of postoperative pneumonia, atelectasis, or empyema in our present series. With preservation of pulmonary tissue, it is logical that the incidence of respiratory failure was lower after sleeve lobectomy (1.7%) when compared with pneumonectomy (7%). Physiologically compromised patients judged not able to tolerate a pneumonectomy had long-term survival after sleeve lobectomy similar to pneumonectomy patients.

Our data support the current belief that sleeve lobectomy, when performed in selected patients with NSCLC, will produce similar overall long-term survival to that seen after pneumonectomy. Neither our data, nor that of other reports, permit a truly valid comparison of the two procedures for similar lesions. Such a comparison would require a randomized trial between the two procedures, and given the obvious lung-preserving advantages of sleeve resection, such a trial is not likely to be conducted.

In conclusion, bronchial anastomoses can be performed with a low prevalence of complications. Sleeve lobectomy or bronchoplasty should be the standard procedure when a low-grade malignant tumor involves the main bronchus. These procedures conserve pulmonary parenchyma and have excellent short- and long-term results. Sleeve lobectomy is a good alternative to pneumonectomy in patients with NSCLC involving the main bronchus. They have similar morbidity and mortality and produce similar long-term results when compared to pneumonectomy. Sleeve resection is particularly useful in patients who cannot tolerate pneumonectomy.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
This article has been selected for the open discussion on the STS Web site: http://www.sts.org/section/atsdiscussion/


    References
 Top
 Footnotes
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Price-Thomas C. Conservative resection of the bronchial tree. J R Coll Surg Edin 1955;1:169-186.
  2. D’Aubreu A.L., MacHale S.J. Bronchial "adenoma" treated by local resection and reconstruction of the left main bronchus. Br J Surg 1952;39:355-360.[Medline]
  3. Gebauer P.W. Bronchial resection and anastomosis. J Thorac Surg 1953;26:241-260.
  4. Allison P.R. Course of thoracic surgery in Groningen. Quoted by Jones PW. Ann R Coll Surg 1954;25:20-22.
  5. Paulson D.L., Shaw R.R. Preservation of lung tissue by means of bronchoplastic procedures. Am J Surg 1955;89:347-355.[Medline]
  6. Jensik R.J., Faber L.P., Milloy F.J., Amato J.J. Sleeve lobectomy for carcinoma. J Thorac Cardiovasc Surg 1972;64:400-412.[Medline]
  7. Faber L.P., Jensik R.J., Kittle C.F. Results of sleeve lobectomy for bronchogenic carcinoma in 101 patients. Ann Thorac Surg 1984;37:279-285.[Abstract]
  8. MacHale S.J. Carcinoma of the bronchus: survival following conservative resection. Thorax 1966;21:343-346.[Free Full Text]
  9. Weisel R.D., Cooper J.D., Delarue N.C., Theman T.E., Todd T.R.J., Pearson F.G. Sleeve lobectomy for carcinoma of the lung. J Thorac Cardiovasc Surg 1979;78:839-849.[Abstract]
  10. Gaissert H.A., Mathisen D.J., Moncure A.C., Hilgenberg A.D., Grillo H.C., Wain J.C. Survival and function after sleeve lobectomy for lung cancer. J Thorac Cardiovasc Surg 1996;111:948-953.[Abstract/Free Full Text]
  11. Yoshino I., Yokoyama H., Tano T., et al. Comparison of the surgical results of lobectomy with bronchoplasty and pneumonectomy for lung cancer. J Surg Oncol 1997;64:32-35.[Medline]
  12. Vogt-Moykopf I., Fritz T.H., Meyer G., Bulzerbruck H., Daskos G. Bronchoplastic and angioplastic operation in bronchial carcinoma: long-term results of a retrospective analysis from 1973 to 1983. Int Surg 1986;71:211-220.[Medline]
  13. Van Schil P.E., de la Riviere A.B., Knaepen P.J., can Swieten H.A., Defauw J.J., van den Bosch J.M. TNM staging and long-term follow-up after sleeve resection for bronchogenic tumors. Ann Thorac Surg 1991;52:1096-1101.[Abstract]
  14. Mehran R.J., Deslauriers J., Pirax M., Beaulieu M., Guimont C., Brisson J. Survival related to nodal status after sleeve resection. J Thorac Cardiovasc Surg 1994;107:576-583.[Abstract/Free Full Text]
  15. American Joint Committee on Cancer. AJCC cancer staging handbook, 5th ed. Philadelphia: Lippincott-Raven, 1998; 117–27.
  16. Tedder M., Anstadt M.P., Tedder S.D., Lowe J.E. Current morbidity, mortality, and survival after bronchoplastic procedures for malignancy. Ann Thorac Surg 1992;54:387-391.[Abstract]



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Eur. J. Cardiothorac. Surg., May 1, 2000; 17(5): 550 - 556.
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