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Ann Thorac Surg 2000;70:367-371
© 2000 The Society of Thoracic Surgeons


Original articles: general thoracic

Bronchial and bronchovascular sleeve resection for treatment of central lung tumors

Henning F. Lausberg, MDa, Thomas P. Graeter, MDa, Olaf Wendler, MDa, Stefanos Demertzis, MD, PhDa, Dieter Ukena, MD, PhDb, Hans-Joachim Schäfers, MD, PhDa

a Departments of Thoracic and Cardiovascular Surgery, University Hospitals Homburg, Homburg/Saar, Germany
b Departments of Pneumology and Internal Medicine, University Hospitals Homburg, Homburg/Saar, Germany

Address reprint requests to Dr Schäfers, Department of Thoracic and Cardiovascular Surgery, University Hospitals Homburg, Kirrberger Str 1, 66421 Homburg/Saar, Germany
e-mail: chhjsc{at}med-rz.uni-saarland.de

Presented at the Thirty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 31–Feb 2, 2000.


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. To improve postoperative pulmonary reserve, we have employed parenchyma-sparing resections for central lung tumors irrespective of pulmonary function. The results of lobectomy, pneumonectomy, and sleeve resection were analyzed retrospectively.

Methods. From October 1995 to June 1999, 422 typical lung resections were performed for lung cancer. Of these, 301 were lobectomies (group I), 81 were sleeve resections (group II), and 40 were pneumonectomies (group III).

Results. Operative mortality was 2% in group I, 1.2% in group II, and 7.5% in group III (group I and II vs group III, p < 0.03). Mean time of intubation was 1.0 ± 4.1 days in group I, 0.9 ± 1.3 days in group II, and 3.6 ± 11.2 days in group III (groups I and II vs group III, p < 0.01). The incidence of bronchial complications was 1.3% in group I, none in group II, and 7.5% in group III (group I and II vs group III, p < 0.001). After 2 years, survival was 64% in group I, 61.9% in group II, and 56.1% in group III (p = NS). Freedom from local disease recurrence was 92.1% in group I, 95.7% in group II, and 90.9% in group III after 2 years (p = NS).

Conclusions. Sleeve resection is a useful surgical option for the treatment of central lung tumors, thus avoiding pneumonectomy with its associated risks. Morbidity, early mortality, long-term survival, and recurrence of disease after sleeve resection are similar to those seen after lobectomy.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Since the first introduction of sleeve resection for a bronchial adenoma in 1947 by Price-Thomas [1], this procedure has become a therapeutic option also for the treatment of bronchogenic carcinoma [29]. Currently, parenchyma-sparing resection is most often performed in patients with impaired preoperative lung function who would not be able to tolerate a pneumonectomy [35, 1013]. Because it is considered a more complex procedure and a relevant incidence of bronchial complications has been reported [9], it has not been applied widely. In addition, the oncologic success of parenchyma-sparing resection has been the subject of controversial discussion [7, 13]. Previous results regarding bronchial healing in lung transplantation [14, 15] led us to hypothesize that preservation of lung parenchyma should be feasible with a low incidence of bronchial complications and lead to reduction in morbidity and mortality compared with pneumonectomy. We have thus performed sleeve resection for the treatment of central bronchial malignancies regardless of pulmonary function whenever possible according to histopathology at quick sections.

The purpose of this study was to review our experience with this approach retrospectively, analyzing morbidity, mortality, and disease-free survival in comparison with lobectomy and pneumonectomy.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
We retrospectively reviewed our experience of typical lung resections for bronchogenic carcinoma from October 1995 to June 1999, ie, lobectomies, sleeve resections, and pneumonectomies.

Preoperatively, all patients underwent the same diagnostic and staging procedures. Specimens for cytological and histological examination were obtained via bronchoscopy. Chest roentgenogram and computed tomography (CT) of brain, chest, and abdomen were performed for noninvasive preoperative staging. Bone scintigram and abdominal ultrasound were obtained in every patient. Every patient underwent pulmonary function tests and calculation of the predicted postoperative lung function to assess the surgical risk. A cervical mediastinoscopy with histopathological examination of the mediastinal lymph nodes was performed in every patient for suspected N2 or N3 stage based on CT scan.

Intraoperatively, particular care was taken to limit peribronchial dissection to the necessary degree and maintain short distal and proximal bronchial stumps. The anastomosis was performed in end-to-end fashion with absorbable monofilament sutures in interrupted technique (PDS; Ethicon Inc, Hamburg, Germany). A careful lymphadenectomy was performed in every patient.

Whenever possible, the patients were extubated in the operating room. Criteria for mechanical ventilation and extubation were similar in all groups. Reasons for continuing mechanical ventilation were either inadequate respiratory function or hypothermia. Postoperatively, all patients were transferred to our intensive care unit (ICU) and were treated by aggressive physiotherapy to achieve adequate drainage of bronchial secretions. Early mobilization of the patient was started as soon as possible, usually on the day of surgery.

Whenever necessary, bronchial drainage was supported by flexible bronchoscopy or insertion of a transtracheal catheter to improve coughing. Patients after sleeve resections were treated by inhalation of racemic epinephrine to minimize mucosal edema. Intravenous application of heparin (200 U/kg body weight per day) was started 4 hours postoperatively as a standard therapeutic regimen in those patients and continued for 5 days. On the fifth postoperative day, a routine flexible bronchoscopy was performed to assess healing of the bronchial anastomosis. Further bronchoscopic examinations were done as indicated by abnormal physical examination, chest roentgenogram, or pulmonary function studies. Bronchial complications were defined as any dehiscence or stenosis of the bronchial stump/anastomosis that required treatment.

Based on the operative specimens, all patients were staged postoperatively according to the TNM classification of the American Joint Committee for Cancer Staging and End Results Reporting [16].

The operative morbidity or speed of recovery from the procedure was assessed using the duration of mechanical ventilation as an indicator. Also, time of ICU stay and time of hospitalization were recorded. Operative mortality was defined as lethal complication within 30 days after surgery or any death in a patient who never left the hospital.

Follow-up data were obtained from follow-up examinations or by direct contact with the referring physicians. Local recurrence of disease was defined as appearance of tumor of the original histological type at any site within the same hemithorax or mediastinum.

Survival and recurrence of disease were estimated according to the Kaplan-Meier method with the date of surgery as a starting point. The curves of survival and recurrence of disease were analyzed for similarity by the Mantel-Haenszel logrank test (Prizm 3.0; GraphPad Software Inc, San Diego, CA). The comparison of the demographic data and tumor stages were performed using the contingency table and {chi}2 test. All other data were compared using the analysis of variance test (SigmaStat 2.0; Jandel Scientific/SPSS Inc, Chicago, IL). Values of p less than 0.05 were considered statistically significant.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
From October 1995 to June 1999, 422 typical lung resections were performed for bronchial malignancies in our institution. All patients were analyzed. The patients were retrospectively divided into three groups according to the surgical procedure. A lobectomy was performed in 301 (71.6%) patients (group I, lob), 81 (19.2%) patients were treated with sleeve resection (group II, slr), and 40 (9.5%) patients underwent pneumonectomy (group II, pne). Of the parenchyma-sparing operations, 48 were bronchoplastic and four angioplastic procedures; 29 patients underwent a bronchovascular sleeve resection. Most frequently, a sleeve resection of either upper lobe was performed (left upper lobe, n = 25; right upper lobe, n = 33).

There were no significant differences concerning mean age and gender ratio between the groups (group I: male-to-female ratio 3.4:1, mean age 62.1 ± 10.1 years; group II: male-to-female ratio 2.4:1, mean age 59.4 ± 12.3 years; group III; male-to-female ratio 4.7:1, mean age 59.8 ± 11.2 years, p = NS for age and gender).

The most frequent histologic tumor types were squamous cell carcinoma and adenocarcinoma in all three groups (p = NS). Preoperative pulmonary function tests (PFT) showed no significant differences among the groups (Table 1).


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Table 1. Results of Pulmonary Function Tests

 
The postoperative staging of patients in group I showed stage I disease in about 60% of cases. Significantly different, most patients in group II and III were staged either as stage II or III A (group I vs group II, p < 0.001; group I vs group III, p < 0.01). There were no significant differences between group II and III with respect to tumor stage (Fig 1).



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Fig 1. Postoperative staging. The distribution of tumor stages in the three patient groups are shown. The proportion of stage I in group I (lobectomy) is significantly higher than in groups II and III. There is no difference in tumor stage between group II (sleeve resection) and group III (pneumonectomy) (see text).

 
In group I, operative mortality was 2% (n = 6). Four patients died from sepsis and multiorgan failure and the remaining 2 suffered from cardiac complications. In group II, 1 patient died from sepsis and multiorgan failure 10 days after surgery resulting in an operative mortality of 1.2%. In group III, 3 patients (7.5%) died in hospital from sepsis and multiorgan failure. Thus, operative mortality was significantly higher after pneumonectomy compared with the two other groups (p < 0.03). There was no significant difference between groups I and II.

The time of mechanical ventilation was identical in both groups I and II, with a mean of approximately 1 day (p = NS; Table 2), while patients in group III showed a significantly longer time of ventilation (p < 0.01; Table 2). A similar duration of ICU stay (Table 2) was seen after lobectomy and sleeve resection (p = NS), while it was significantly increased after pneumonectomy (p < 0.05). Total hospital stay was also prolonged in group III, although this was not statistically significant (Table 2).


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Table 2. Indicators of Postoperative Morbidity

 
In group I, 4 patients (1.3%) showed limited dehiscence of the bronchial stump as documented by bronchoscopy. All patients were treated successfully by bronchoscopic application of fibrin glue and pleural drainage. In group II, no patient developed stenosis or dehiscence. In group III, bronchial dehiscence was observed in 3 patients resulting in a complication rate of 7.5%. All patients were reexplored surgically and the bronchus closed with muscle flaps. Thus, there was no significant difference between group I and II. Patients in group III, however, suffered from bronchial complications significantly more frequently than patients in both other groups (p < 0.001).

When comparing postoperative pulmonary function, significant differences are noticed. As expected, patients after pneumonectomy showed significantly impaired spirometric data in comparison with both other groups (p < 0.05; Table 1). There was no difference between groups I and II (Table 1).

Follow-up ranged from 1 to 44 months with a mean of 20 months. Fifty-five patients (13%) were lost to follow-up. Survival rates after 2 years were 64% in group I, 61.9% in group II, and 56.1% in group III (p = NS; Fig 2).



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Fig 2. Survival analysis according to surgical procedure (Kaplan-Meier method).

 
Freedom from local recurrence after a follow-up of 2 years was 92.9% in group I, 95.7% in group II, and 90.9% in group III (p = NS; Fig 3).



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Fig 3. Analysis of freedom from recurrent disease according to surgical procedure (Kaplan-Meier method).

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Traditionally, sleeve resection was applied as a surgical option for the treatment of central lung tumors in patients with impaired pulmonary function in order to avoid the associated risks of pneumonectomy. An issue of major concern has been the incidence of healing disorders of the bronchial anastomosis with remarkable morbidity [2, 5, 9]. This experience has restricted a wider application of sleeve resections.

Theoretically, the preservation of functional lung tissue should provide an increased pulmonary reserve. Therefore, it only seems reasonable to assume that this physiologic advantage should result in decreased operative morbidity and mortality in comparison with pneumonectomy, if a low incidence of bronchial complications can be achieved. Some other groups have similarly assumed a potential advantage of sleeve resection and performed this procedure more liberally recently [3, 1719]. The generally positive results led us to the decision to use this technique also for patients with normal pulmonary function. Additionally, our previous results in clinical lung transplantation have shown that a low incidence of bronchial complications can be achieved [14, 15].

Compared with other series [4, 6, 8, 9, 11, 17, 19], our proportion of patients who underwent either pneumonectomies or sleeve resection is somewhat larger in relation to the overall patients after typical lung resection. In a coal mining region with a high incidence of pulmonary disease, our center has become a referral center especially for patients with central lung tumors. Our approach has been to perform sleeve resection whenever technically possible with the resection margins regardless of pulmonary function and/or nodal disease. Thus, for us, even N2 stage is not a contraindication to sleeve resection for those patients who underwent preoperative adjuvant therapy or will be radiated postoperatively.

Our current results confirm the hypothesis with respect to early morbidity and mortality [3, 17, 19]. Bronchial complications can be limited using surgical technique as well as perioperative management principles applied in lung transplantation [14, 15]. Using this protocol, a low incidence of bronchial complications can be achieved, a fact that has been reported by others [10, 17, 19].

With the low bronchial morbidity, postoperative effects of increased pulmonary reserve may have facilitated postoperative rehabilitation and decreased morbidity. The significantly shorter duration of mechanical ventilation and ICU stay in comparison with pneumonectomy confirm the physiological advantage of an increased pulmonary reserve. Similarly, the low operative mortality in our series most likely is due to increased pulmonary reserve in comparison with those after pneumonectomy [20]. Interestingly, there was no significant survival benefit after 2 years, possibly due to the low numbers in groups II and III.

One of the major concerns against the wide use of parenchyma-saving operations has been the questionable oncologic success after these procedures. With respect to local recurrence of disease, our experience has shown no difference between sleeve resection and pneumonectomy. Still, few of our patients have entered the fourth postoperative year, which does not provide reliable 3-year survival data. However, so far, no disadvantage regarding local recurrence of either surgical approach could be noted.

In conclusion, bronchoplastic procedures appear to be adequate cancer operations for central lung tumors. With careful surgical technique and postoperative care, operative mortality and morbidity comparable with standard lobe resections can be achieved. There has been no evidence of increased risk of local recurrence. Sleeve resection appears as a competent and useful surgical alternative for treatment of central lung cancer, thus avoiding the "disease" pneumonectomy.


    Footnotes
 
This article has been selected for the open discussion forum on the STS Web site: http://www.sts.org/section/atsdiscussion/


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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  5. Krüger M., Uschinsky K., Hässler K., Engelmann C. Postoperative complications after bronchoplastic procedures in the treatment of bronchial malignancies. Eur J Cardiothorac Surg 1998;14:46-53.[Abstract/Free Full Text]
  6. Maggi G., Casadio C., Pischedda F., Cianci R., Ruffini E., Filosso P. Bronchoplastic and angioplastic techniques in the treatment of bronchogenic carcinoma. Ann Thor Surg 1993;55:1501-1507.[Abstract/Free Full Text]
  7. Rendina E.A., Venuta F., Ciriaco P., Ricci C. Bronchovascular sleeve resection. Technique, perioperative management, prevention, and treatment of complications. J Thorac Cardiovasc Surg 1993;106:73-79.[Abstract]
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  9. Tedder M., Anstadt M.P., Tedder S.D., Lowe J.E. Current morbidity, mortality, and survival after bronchoplastic procedures for malignancies. Ann Thorac Surg 1992;54:387-391.[Abstract/Free Full Text]
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  11. Naruke T. Bronchoplastic and bronchovascular procedures of the tracheobronchial tree in the management of primary lung cancer. Chest 1989;96(Suppl 1):53-56.
  12. Frist W.H., Mathisen D.J., Hilgenberg A.D., Grillo H.C. Bronchial sleeve resection with and without pulmonary resection. J Thorac Cardiovasc Surg 1987;93:350-357.[Abstract]
  13. VanSchil P.E., Brutel de la Riviere A., Knaepen P.J., van Swieten H.A., Defauw J.J., van den Bosch J.M. TNM staging and long term follow-up after sleeve resection for bronchogenic tumor. Ann Thorac Surg 1991;52:1096-1101.[Abstract/Free Full Text]
  14. Schäfers H.J., Haydock D.A., Cooper J.D. The prevalence and management of bronchial anastomotic complications in lung transplantation. J Thorac Cardiovasc Surg 1991;101:1044-1052.[Abstract]
  15. Schäfers H.J., Haverich A., Wagner T.O.F., Wahlers T., Alken A., Borst H.G. Decreased incidence of bronchial complications following lung transplantation. Eur J Cardiothorac Surg 1992;6:174-179.[Abstract/Free Full Text]
  16. Mountain C.F. Revisions in the International System for Staging Lung Cancer. Chest 1997;111:1710-1717.[Medline]
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