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Ann Thorac Surg 2005;79:1147-1152
© 2005 The Society of Thoracic Surgeons
Department of Thoracic and Cardiovascular Surgery, University Hospitals, University of Saarland, Homburg/Saar, Germany
Accepted for publication September 3, 2004.
* Address reprint requests to Dr Lausberg, Department of Thoracic and Cardiovascular Surgery, University Hospitals, University of Saarland, 66421 Homburg/Saar, Germany (E-mail: henning.lausberg{at}uniklinik-saarland.de).
Presented at the Fortieth Annual Meeting of The Society of Thoracic Surgeons, San Antonio, TX, Jan 26–28, 2004.
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Abstract |
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METHODS: We retrospectively analyzed all patients who underwent bronchial sleeve resection (group I, n = 104), bronchovascular sleeve resection (group II, n = 67), and pneumonectomy (group III, n = 63) for central lung cancer in our institution.
RESULTS: The groups were comparable regarding demographics and tumor, node, and metastasis (TNM) stage. Early mortality was 1.9% in group I, 1.5% in group II, and 6.3% in group III (p = 0.19). The rate of bronchial complications was 0.96% in group I, 0% in group II, and 7.9% in group III (p = 0.006). Five-year survival was 46.1% in group I, 42.9% in group II, and 30.4% in group III (p = 0.16). Freedom from local recurrence of disease (5 years) was 83.8% in group I, 84.2% in group II, and 88.7% in group III (p = 0.56).
CONCLUSIONS: Bronchovascular sleeve resections are as safe as bronchial sleeve resections for the treatment of central lung cancer. Both procedures have comparable early and long-term results, which are similar to those of pneumonectomy. It appears reasonable to apply bronchovascular sleeve resections more liberally.
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Introduction |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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Whenever central lung tumors involve not only the airway but also the central vascular structures, in particular the pulmonary artery, bronchovascular sleeve resection remains as the only alternative to pneumonectomy. In view of the traditionally high perioperative mortality of this form of parenchyma-sparing resection [12] pneumonectomy is still the preferred approach for most surgeons. In addition, the long-term oncologic success of bronchovascular sleeve resections has been the subject of concern. Encouraged by the positive short and long-term results of bronchial sleeve resection [9–11] we have extended our systematic approach of parenchyma-sparing surgery also to bronchogenic carcinoma involving the central pulmonary arteries. Whenever distal resection margins were macroscopically and microscopically free of tumor, the distal parenchyma was preserved utilizing the standard techniques [13] of bronchovascular sleeve resection.
We retrospectively analyzed our experience with bronchovascular sleeve resections regarding morbidity, mortality, and disease-free survival. We compared the patients to those undergoing bronchial sleeve resections and pneumonectomy during the same interval.
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Patients and Methods |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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The surgical technique included primary exploration of the hilar structures followed by a complete dissection of the fissure(s). When the distal parenchyma was free of tumor and/or invasive growth of lymph nodes, a sleeve resection was performed. Frozen sections of the resected bronchi and/or pulmonary artery were taken to ensure resection margins of at least 1 cm. The technique of bronchial sleeve resection has been described previously [14]. In the presence of involvement of the proximal pulmonary artery either by malignant tissue (tumor or invasive growth of lymph nodes), heparin (5,000 IU) was given intravenously and the pulmonary artery clamped proximally. The superior pulmonary vein was ligated, and the inferior pulmonary vein or the distal part of the pulmonary artery were occluded with a vascular clamp. Resection of the tumor-bearing lobe was performed en bloc with the involved portion of the pulmonary artery. The artery was reconstructed by implantation of a pericardial patch after tangential resection or end-to-end anastomosis (Prolene 5-0, Ethicon Inc, Hamburg, Germany) after segmental resection. In all patients the bronchial anastomosis (interrupted PDS 4-0, Ethicon Inc) was created first followed by vascular reconstruction. Following pneumonectomy, closure of the bronchial stump was performed with interrupted PDS 3-0 sutures (Ethicon Inc, Hamburg, Germany). In earlier patients, the bronchial stump was not covered routinely. In the recent patients, the bronchial stump was covered with pericardium or mediastinal tissue. In all patients, a radical mediastinal lymphadenectomy was included.
Patients were extubated in the operating room whenever possible. Mechanical ventilation was continued for hemodynamic instability or inadequate respiratory status or hypothermia of 35.5°C or less. Our postoperative treatment used for all patients undergoing parenchyma-sparing procedures has been previously described [15]. All patients underwent routine bronchoscopy one week postoperatively if they had undergone any form of parenchyma-sparing procedure. Based on the operative specimens, all patients were staged according to the tumor, node, metastasis (TNM) classification of the American Joint Committee for Cancer Staging and End Results Reporting [16].
The duration of mechanical ventilation was used as a global indicator of operative morbidity. In addition, the duration of intensive care unit (ICU) stay and hospitalization were recorded. Surgical mortality was defined as any death occurring within 30 days after surgery or any death in a patient who never left the hospital. Episodes of respiratory infections were defined as any symptomatic infection of the airways requiring antibiotic treatment. Furthermore the need for therapeutic fiberoptic bronchoscopy due to mucus retention was documented. Both factors were used as indicators for the operative morbidity. Follow-up data were obtained from follow-up examination or direct contact with the referring physicians. Local recurrence of disease was defined as appearance of a tumor of the original type as judged by histopathology at any site within the same hemithorax.
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 local recurrence of disease were compared using the Mantel-Haenszel log-rank test (Prism 3.0, GraphPad Software Inc, San Diego, CA). The comparison of the demographic data and tumor stages was performed using the contingency table and 
2 test. All other data were compared using the analysis of variance test (SigmaStat 2.0, SPSS Inc, Chicago, IL). The p values of less than 0.05 were considered statistically significant.
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Results |
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Group III had a significantly higher proportion of patients in stage IIIB in comparison with group I (p = 0.029; Table 2). All other tumor stages were comparable between the groups. Approximately half of the patients had stage II disease in the three groups. The higher proportion of patients in group III in more advanced tumor stages were due to either T4 extension (stage IIIB) or ipsilateral pulmonary metastasis (M1 PUL; stage IV). No patient had N3 lymph node involvement.
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The duration of mechanical ventilation after pneumonectomy was significantly longer than after bronchial sleeve resection (3.2 ± 10.9 vs 0.73 ± 0.86 days, p = 0.029). Groups I and II, and II and III did not differ significantly (Table 3). There were no significant differences between the groups regarding ICU and hospital stay (Table 3). The incidences of respiratory infections and the need for invasive mucus clearance were significantly higher after pneumonectomy (Table 3).
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Follow-up ranged from 11 to 97 months with a mean follow-up of 46 months (cumulative follow-up: 10,446 patient-months). Some patients were lost to follow-up between 3 and 5 years postoperatively. Follow-up was complete in 94 patients in group I (90.4%), 62 patients in group II (92.5%), and 56 patients in group III (88.9%).
Overall five-year survival was 46.1% in group I, 42.9% in group II, and 30.4% in group III (p = 0.16, Fig 1). Five-year survival for stage II disease was 50.5% in group I, 36.7% in group II, and 46.3% in group III (p = 0.7). Freedom from local recurrence of disease at 5 years was 83.8% in group I, 84.2% in group II, and 88.7% in group III (p = 0.56; Fig 2).
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Comment |
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TopAbstractIntroductionPatients and MethodsResultsCommentDISCUSSIONReferences |
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Pneumonectomy has been the standard surgical approach in patients with central lung cancer. This extensive pulmonary resection has offered curative treatment in a large proportion of cases. This procedure, however, is associated with a significantly higher morbidity and mortality compared to lobectomy [1, 2]. Long-term complications are the development of pulmonary hypertension or respiratory failure.
Parenchyma-sparing bronchial and bronchovascular sleeve resections were primarily intended to offer a surgical alternative to those individuals who would not tolerate a pneumonectomy due to impairment of their pulmonary reserve. Initial reports indicated that this form of resection was associated with an increased mortality and morbidity associated with the bronchial and vascular anastomosis [12, 21]. There has been additional concern of a possibly higher risk of tumor recurrence with consecutive limitations of survival [7, 22].
Several series have been published in recent years indicating that bronchial sleeve resection applied irrespective of pulmonary function was associated with a mortality risk lower than that of pneumonectomy, and in most instances was comparable to standard lobe resection [9, 10, 15]. The incidence of bronchial anastomotic complications has consistently been lower than that of pneumonectomy [9, 10, 15]. The published 5-year survival and tumor recurrence data have not been inferior to those after pneumonectomy. A recent metaanalysis on parenchyma-sparing resections versus pneumonectomy in stages I and II lung cancer revealed a significant advantage in quality-adjusted life years for sleeve resections [23].
While the use of bronchial sleeve resections is thus gaining wider acceptance, concern continues regarding the routine application of bronchovascular sleeve resections for the treatment of central lung cancer involving the pulmonary artery. In a series of 37 sleeve resections of the pulmonary artery, Vogt-Moykopf and colleagues [12, 24] reported acceptable long-term results but an operative mortality of up to 14%. Major complications of the vascular anastomosis have been described [12, 24]. With the impression that angioplasty was not a safe procedure, apparently many surgeons have been reluctant to employ this technique. Only recently has it become apparent that angioplastic resections could be performed with favorable early results [13, 25]. In addition, lessons learned from lung transplantation not only pointed out potential pitfalls of the vascular anastomosis but also showed ways to avoid them [25–27].
Our current results indicate that not only bronchial but also bronchovascular sleeve resections for the treatment of central lung tumors can be performed with a low perioperative risk. Most importantly, the long-term data regarding survival and tumor recurrence are identical to those of bronchial sleeve resection and pneumonectomy in our patient population. Thus, we believe that this surgical option does not compromise oncologic success. A definite conclusion regarding oncologic results is, however, hampered by the relatively limited number of individuals in our study. In a recent metaanalysis an increased risk of local tumor recurrence was found after sleeve lobectomy compared to pneumonectomy. Interestingly, this increase in tumor recurrence did not affect long-term survival [23]. It is unclear whether routine application of adjuvant radiotherapy for all parenchyma-sparing operations could be of benefit.
It may be argued that a relatively high proportion of our patients treated surgically were in more advanced tumor stages; ie, IIIB and IV. In all instances stage IIIB was defined by mediastinal involvement or metastasis within the tumor-bearing lobe, which was found intraoperatively. In view of the promising results in resection tumors of T4 stage, we attempt to resect these tumors whenever possible without incurring major morbidity. In view of other results [28–30] this appears justified in selected patients. All patients with an unequivocal preoperative T4 stage are considered as candidates for neoadjuvant protocols.
In only 6 of 234 patients (2.6%) was stage IV disease diagnosed intraoperatively. In all instances, the tumor stage was determined by a single metastasis in the nontumor-bearing lobe, which had not been diagnosed preoperatively. All patients had preoperatively expressed a definite wish in favor of resection.
We thus conclude that bronchovascular sleeve resections are as safe as bronchial sleeve resections for the treatment of central lung cancer. Both procedures have comparable early and long-term results, which are similar to those of pneumonectomy. It appears reasonable to also apply bronchovascular sleeve resections more liberally.
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DISCUSSION |
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What can Dr Lausberg tell us about incomplete resections? Were there any cases done in this time period that were excluded from the paper because of positive margins? It seems unusual in a population of patients with advanced central tumors that there were not resections that resulted in microscopic or gross positive margins. Twenty-six of the reported patients, or about 10%, are stage IIIb due to T4 local invasion, and this would seem to put many at risk for an incomplete resection. Next, the authors have not specifically looked at patient outcomes with regard to the vascular anastomosis or reconstruction. This is a complication of the vascular sleeve resection that is difficult to detect unless one looks for it specifically. It won’t change the chest x-ray, it won’t change spirometry, and when bronchovascular sleeve is applied to patients who had physiologically tolerated pneumonectomy, they might also be expected to tolerate the insult of vascular thrombosis at the arterioplasty site. The authors should present whatever information they have with regard to vascular patency. Finally, systemic recurrence is not addressed, and it should be. In these central tumors, this will be the greatest hazard to the patients with regard to risk of cancer death. It would be worthwhile to report this, and it would be reassuring to see that the rate of distant failure in all three groups was comparable. What additional treatment for local or distant recurrence has been required: completion pneumonectomy, adjuvant radiation therapy, or adjuvant chemotherapy? I commend you on your results and for your presentation.
DR PAUL VAN SCHIL (Edegem, Antwerp, Belgium): I enjoyed your presentation very much. It would be interesting to know how many of your patients had induction therapy, especially before undergoing a bronchovascular sleeve resection. Did you encounter any technical difficulties in these patients? As known from recent literature, dissection of the pulmonary artery can be very tedious after induction or neoadjuvant therapy, especially chemoradiotherapy.
DR PETER C. PAIROLERO (Rochester, MN): Did you know that you were going to do a bronchovascular sleeve resection before you were inside the chest? If so, what type of imaging studies were done to indicate that this procedure would be necessary?
DR REX STANBRIDGE (London, UK): In this complex series of cases you would obviously have quite a narrow margin of resection from the tumor. What minimum margin of resection were you aiming for?
DR LAUSBERG: Thank you very much for these comments. I would like to answer Dr Meyers’ questions first: There were 11 patients who were incompletely resected who were shown to be stage R1, and, of course, they had adjuvant therapy postoperatively. No, we did not see any vascular problems, but we did not systematically look for those, for example, by angiography. It is a very interesting comment. Clinically no patient had any symptoms suggestive for a complication of the vascular anastomosis. The incidence of completion pneumonectomy of either bronchial or bronchovascular sleeve resection was between 7% and 8% in the long term.
Next I would like to comment on Dr van Schil’s remarks. About 10% of patients had preoperative downstaging for N2 disease before either bronchial and bronchovascular sleeve resections. Of course, dissecting in an irradiated field is more difficult, but using the standard technique we are comfortable to do the anastomoses. I remember two cases in the past in which the patients had to be placed on cardiopulmonary bypass because of tears in the central pulmonary artery. Both patients could be resected successfully.
Dr Pairolero, we try to perform a sleeve resection whenever possible. If we can achieve a resection margin of at least one centimeter in the absence of tumor or invasive lymph nodes in the distal parenchyma we do a parenchyma-sparing operation. I believe this should also answer Dr Stanbridge’s question. Again, thank you very much.
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This article has been cited by other articles:
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  Z. Ma, A. Dong, J. Fan, and H. Cheng Does sleeve lobectomy concomitant with or without pulmonary artery reconstruction (double sleeve) have favorable results for non-small cell lung cancer compared with pneumonectomy? A meta-analysis Eur. J. Cardiothorac. Surg., July 1, 2007; 32(1): 20 - 28. [Abstract] [Full Text] [PDF]
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= group I; 
= group II; 
= group III.