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Sleeve Resections for Squamous Cell Carcinoma of the Lung
ORIGINAL ARTICLE
Original Article
Sleeve Resections for Squamous Cell Carcinoma of the Lung Suat Gezer, MD a,∗ , Gürhan Öz, MD b , Göktürk Fındık, MD b , Hasan Türüt, MD b , Tamer Altınok, MD b , Mehmet Sırmalı, MD b , Erkmen Gülhan, MD b , ˙ ˘ ¸ kıran, MD c , Sadi Kaya, MD b and Irfan Yetkin Agac Tas¸tepe, MD b a Düzce University, Faculty of Medicine, Clinic of Thoracic Surgery, Düzce, Turkey Atatürk Chest Diseases and Thoracic Surgery Training and Research Hospital, Clinic of Thoracic Surgery, Ankara, Turkey c Atatürk Chest Diseases and Thoracic Surgery Training and Research Hospital, Department of Pathology, Ankara, Turkey
b
Background: Sleeve resection is an advanced technique that was developed as an alternative to pneumonectomy. This study evaluated our cases of sleeve resection for squamous cell carcinoma of the lung and compared the outcomes with the literature reports. Methods: In total, 26 bronchial, 5 bronchovascular, and 3 vascular sleeve lobectomies were performed between January 2000 and July 2005 in our clinic. Age, gender, operations, postoperative diagnosis and staging, and postoperative morbidity and mortality were evaluated. Results: Sleeve resections were performed in 34 patients. All patients were male, with a mean age of 59.4 years. The operations consisted of 16 right upper, 14 left upper, and 1 left lower sleeve lobectomies and 3 superior sleeve bilobectomies. The most common postoperative pathological staging group was stage IIb (32.3%). Operative mortality was 5.9% (n = 2). Postoperative morbidity was 20.5% (n = 7), including 4 prolonged air leaks plus empyema, 1 prolonged air leak, 1 postoperative bleeding needing revision, and 1 severe bronchostenosis; of these, 6 had persistent atelectasis. The local tumour recurrence rate was 11.7% (n = 4). The median survival time and 5-year survival were 36 months and 42%, respectively. Conclusions: Sleeve resection proved to be good therapy for lung cancer and has a lower morbidity and mortality than standard pneumonectomies and results in better lung function and quality of life. The anastomosis-related complications are experience-related technical complications and training thoracic surgeons to perform SRs at experienced centres will reduce the morbidity associated with SRs. (Heart, Lung and Circulation 2010;19:549–554) © 2010 Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand. Published by Elsevier Inc. All rights reserved. Keywords. Pulmonary malignancy; Sleeve resection of lung; Parenchyma sparing operation; Sleeve lobectomy
Introduction
S
leeve resections (SR) were designed to treat patients with rare endobronchial lesions, such as tumours or strictures, in patients who could not tolerate a pneumonectomy. Price Thomas performed the first sleeve lobectomy for a carcinoid tumour located in the right main bronchus in 1947 [1]. Allison performed the first sleeve lobectomy for lung cancer in 1952 [2]. Subsequently, many publications have reported that SR enables a tumour resection rate similar to that of pneumonectomy and they proposed that SRs be performed more widely [3–6]. Additionally, they pointed out the significant contribution of the
Received 28 April 2009; received in revised form 9 February 2010; accepted 21 February 2010 ∗
Corresponding author at: Düzce Üniversitesi Tıp Fakültesi, ˘ Cerrahisi AD, 81620 Konuralp, Düzce, Turkey. Gögüs Tel.: +90 380 5421390. E-mail address: [email protected] (S. Gezer).
re-implanted lung to postoperative respiratory function [6]. Sleeve resections can be classified as follows: 1. Sleeve lobectomies a. bronchial sleeve lobectomy b. vascular sleeve lobectomy c. bronchovascular sleeve lobectomy 2. Sleeve bronchial resections 3. Tracheal sleeve pneumonectomies This study evaluated the results of sleeve lobectomies for squamous cell carcinoma of the lung that we performed over a 5.5-year period.
Materials and Methods In total, 34 patients underwent sleeve lobectomies for squamous cell carcinoma of the lung at Atatürk Chest Diseases and Thoracic Surgery Training and Research
© 2010 Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand. Published by Elsevier Inc. All rights reserved.
1443-9506/04/$36.00 doi:10.1016/j.hlc.2010.02.026
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Gezer et al. ‘Sleeve Resections of the Lung’
Heart, Lung and Circulation 2010;19:549–554
Figure 1. Chest X-ray (a) and thoracic computed tomography (b and c) of patient with squamous cell carcinoma invading entrance of left upper lobe bronchus and pulmonary artery.
Hospital, Ankara, Turkey, between January 2000 and July 2005. Preoperatively, all of the patients underwent radiological investigations, including a chest X-ray and thoracic computed tomography (CT) (Fig. 1). Fibre-optic bronchoscopy (FOB) was used to obtain diagnostic biopsies and to evaluate the feasibility of SR. The patients in whom a classical lobectomy was not feasible, but complete disease resection was possible with a SR, based on the results of thoracic CT and FOB, underwent SR. The patients’ respiratory sufficiency for the resection was evaluated by measuring the forced expiratory volume in 1 s (FEV1 ) and diffusing capacity of the lung for carbon monoxide (DLCO). For patients with borderline FEV1 and DLCO measures, the maximum oxygen consumption during exercise (VO2max ) and postoperative FEV1 were measured. Additionally, all patients were assessed with a complete blood count, analyses of blood chemistry and coagulation parameters, and a complete urinalysis. Cardiac status was assessed routinely with an electrocardiogram (ECG) and a cardiology consultation was requested for the patients older than 55 years or with any suspected pathology. All patients underwent an anesthesia clinic evaluation preoperatively. The patients who were selected for a sleeve resection were taken to the operating room and underwent a posterolateral thoracotomy. All bronchial sleeve resections were circumferential and the anastomoses were performed in an end-to-end manner. The vascular sleeve resections were circumferential or tangential, according to the vessel involvement, and end-to-end anastomoses were performed after circumferential resections and vessel repair after tangential resections. The bronchial anastomosis was performed with a continuous suture on the membranous side and with interrupted sutures on the cartilaginous side, using 3-0 absorbable (polydioxanone or polyglactin) sutures. Vascular anastomoses or repairs were performed with continuous 5-0 polypropylene sutures (Fig. 2). Following completion of the anastomosis, the lung
was inflated and the saline-covered bronchus observed for any evidence of air leaks under 30–40 cm H2 O airway pressure and sutures were added if any air leak was observed. The anastomosis line was covered with a pedicle flap, consisting of thymic remnant, pericardial fat tissue, pleura, or intercostal muscle. After closing the thoracotomy, FOB through the endotracheal tube or rigid bronchoscope was performed to check the anastomotic line and to perform bronchial cleaning. All patients were followed in the intensive care unit for 24 h. All patients used expectorants and incentive spirometry and had chest physiotherapy to prevent secretion retention. The patients who developed secretion retention and atelectasis despite this therapy underwent FOB for bronchial cleaning. Additionally, those patients who did not undergo a FOB for another reason underwent FOB to check the anastomotic line 7 days postoperatively. The patients with no complications were discharged 7 days postoperatively. After discharge, the patients were followed in the outpatient clinic for 20 days postoperatively and then once every 3 months for the rest of the first year and twice a year subsequently. Patient records were re-evaluated for age, gender, type of operation, histopathological results and stage, adjuvant and neoadjuvant therapies, postoperative complications, and survival. Patient survival was analysed using the Kaplan–Meier method. Our data were compared with published results.
Results During a 5.5-year period, 34 patients underwent a SR for squamous cell carcinoma of the lung. All of the patients were male with a mean age of 59.4 (41–74) years. The procedures included 26 bronchial sleeve lobectomies, 5 bronchovascular sleeve lobectomies, and 3 vascular sleeve lobectomies.
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Table 1. Postoperative Staging of Primary Lung Cancer Patients. Stage IA IB IIA IIB IIB IIIA IIIA IIIA
TNM
Patient Number
Ratio (%)
T1N0M0 T2N0M0 T1N1M0 T2N1M0 T3N0M0 T2N2M0 T3N1M0 T3N2M0
3 10 2 10 1 3 3 2
8.8 29.4 5.9 29.4 2.9 8.8 8.8 5.9
Total
Figure 2. (Same patient) Intraoperative view of bronchovascular sleeve lobectomy of left upper lobe: (a) pulmonary artery invaded by the tumour, (b) clamping of proximal and distal part of invasion, (c) segmental resection of invaded part of pulmonary artery, (d) beginning of end-to-end anastomosis of pulmonary artery, (e) anastomosis of pulmonary artery, (f) anastomosed pulmonary artery, and (g) endobronchial lesion invading the entrance of upper lobe bronchus in resected lobe.
In all patients, a preoperative histopathological diagnosis was made after FOB. Eight patients had a preoperative mediastinoscopy. Metastasis to mediastinal lymph nodes was diagnosed in one patient and this patient underwent surgery after neoadjuvant chemotherapy. Additionally, one patient received neoadjuvant chemotherapy based on the preoperative CT findings and was operated on after evaluating the mediastinal lymph node clearance at mediastinoscopy. The other six patients were found to be free of N2 disease at mediastinoscopy and underwent SR. The location of the sleeve lobectomy was the right upper lobe in 16 patients, left upper lobe in 14 patients, bilobectomy of the right upper and middle lobes in 3, and left lower lobe in 1.
34
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The postoperative histopathological examinations confirmed squamous cell carcinoma. The most common stage was IIb (32.3%; Table 1). Although we routinely made frozen examinations of the bronchial surgical margins, the postoperative histopathological examinations detected tumour-positive bronchial surgical margins in four patients. Those patients could not have undergone an alternative procedure, because two had insufficient respiratory capacity for pneumonectomy and two refused a second operation and were referred for radiotherapy. Postoperatively, eight patients underwent radiotherapy, one had chemotherapy, and two had chemoradiotherapy as adjuvant treatment. Postoperatively, seven patients (20.5%) developed complications (Table 2). Secretion retention and atelectasis was the most common complication. All of the complications, except the bronchial stenosis, improved with treatment and did not cause any permanent morbidity or mortality. The patient with bronchostenosis refused a second operation. One patient died 10 days postoperatively of acute renal failure and one, 24 days postoperatively due to cerebral thromboembolism. Thus, the 30-day postoperative mortality was 5.9% (n = 2). In the long-term, one patient died 3 years postoperatively due to myocardial infarction and eight patients died of the disease progression at a median of 21 months postoperatively (four local tumour recurrences and four distant metastases). The long-term mortality was 26.4% (n = 9). By the Kaplan–Meier method, the median survival time was 36 months and the 5-year survival was 42% (Graph 1).
Discussion Sleeve resections require more experience than a classical lobectomy. The bronchial and vascular anastomosis may cause complications that are not seen in classical lobectomies. Thus, bronchoplasty and angioplasty operations should also have low morbidity and mortality ratios to constitute a suitable treatment method. The reported operative mortality is summarised in Table 3 and is between 1.6 and 5.5%. This is better than the 6% operative mortality after pneumonectomy, reported by the Lung Cancer Study Group [3,5,7–12]. Bagan et al. compared sleeve lobectomy and pneumonectomy and reported a 4.5% operative mortality for sleeve lobectomy
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Table 2. Postoperative Morbidities. Complications
Patient Number
Secretion retention and atelectasis Prolonged air leak + empyema Prolonged air leak (without empyema) Haemorrhagic drainage that needed revision Stenosis on bronchial anastomotic line due to extended granulation and fibrosis
Ratio (%)
6 4 1 1 1
17.6 11.7 2.9 2.9 2.9
Table 3. The Literature about Operative (30-Day) Mortality and 5-Year Survival after Bronchoplastic Procedures. First Author (reference)
Year
Tedder (meta-analysis) Van Schil Tronc Ferguson (meta-analysis) Deslauriers Bagan Rea
1992 1996 2000 2003 2004 2005 2008
Number of Patients 1915 145 184 860 184 66 199
Graph 1. Survival (Kaplan–Meier method).
versus 12.6% for pneumonectomy [10]. The respective rates were 4.1% versus 6.0% in Ferguson and Lehman’s meta-analysis [11] and 1.3% versus 5.3% in Deslauriers et al. [12]. Our operative mortality was 5.9%. Additionally, these deaths were not related to the operations directly: one was due to acute renal failure and the other to cerebral thromboembolism. Nevertheless, the reported operative mortality and our results are better than for pneumonectomy. The five-year survival after sleeve lobectomy for lung cancer is generally between 39.7 and 52% (Table 3). Exceptionally, Bagan et al. reported a rate of 72.5% [10]. Some other published five-year survivals are 45, 42, and 40% in 79, 72, and 69 patients, respectively [4,6,13]. In our study, the five-year survival was 42% (Graph 1), consistent with these literature reports. Many studies comparing sleeve lobectomy and pneumonectomy have shown that sleeve lobectomy has no negative effects on long-term survival [6,11,14,15]. Furthermore, Ferguson and Lehman found a better prognosis after sleeve lobectomy in stage I patients [11]. Both Deslauriers et al. [12] and Okada et al. [14] reported a significantly
30-Day Mortality (%) 5.5 4.8 1.6 4.1 1.6 4.5 4.5
5-Year Survival (%) 40 46 52 51.4 52 72.5 39.7
better prognosis after sleeve lobectomy in stages I and II patients. Takeda et al. did not report any difference in the five-year survival of stages I and II patients after sleeve lobectomy or pneumonectomy, but the overall five-year survival of the sleeve lobectomy group was better than that of the pneumonectomy group (54% vs. 33%) [16]. Some other reported five-year survivals after sleeve lobectomy and pneumonectomy were 72.5% versus 53.2% and 39% versus 27% [10,17]. Local tumour recurrence after SR has been widely investigated, but there is no consistent definition of “local recurrence” in the published studies. While some authors define local recurrence as recurrence in the suture line, others define it as recurrence in the same lung [6–8]. Reported local tumour recurrence rates are 14.0, 12.5, and 11.6% [4–6]. We observed tumour recurrence in the same lung in 4 patients (11.7%). One of the four local recurrence patients had a tumour-positive bronchial surgical margin. Despite some unsuccessful results, frozen section examination should be routinely made in TSP operations for the safety of the bronchial surgical margins like other bronchial cancer operations. Secretion retention and persistent atelectasis are the most common complications of SRs [5,7,13]. These problems are related to the deterioration of the ciliary epithelium and lymphatics and partial denervation of the re-implanted lung or anastomotic oedema [5]. In our study, we experienced this complication in six patients, despite aggressive therapy that included expectorants, incentive spirometry, and chest physiotherapy. A lack of patient compliance was the leading cause of this complication and all recovered with secretion clearance via FOB. Although bronchial anastomotic complications are important complications of SRs, preservation of the bronchial blood supply, creation of a tension-free bronchial anastomosis, and improved suture materials have resulted in better bronchial healing, significantly reducing the incidence of bronchial anastomotic complications [18]. Tedder et al. examined 1915 patients and reported bronchopleural fistulas in 3.5% and late strictures in 4.8% [7]. The respective rates were 1.1 and 2.2% in
a study of 184 patients [5]. Another study of 199 patients observed bronchopleural fistulas in 1% and bronchial stenosis in 10% [8]. We observed no bronchopleural fistula. We experienced stenosis of the anastomotic line and complete obstruction of the main bronchus after a sleeve lobectomy of the right upper lobe in one patient (2.9%). We offered a pneumonectomy, but the patient refused the second operation. Despite the resulting autopneumonectomy, he did not develop respiratory distress, because his respiratory capacity was good. The outcomes of vascular sleeve lobectomies are also good. Rendina et al. experienced only one complication, which was thrombosis in the pulmonary artery in their series in which they performed SR and reconstruction of the pulmonary artery in 52 patients; they did not observe any mortality and reported that their morbidity, mortality, and functional results were not different from those reported for standard lobectomies [19]. For 33 vascular sleeve lobectomy patients, the results of Shrager et al. did not differ from standard lobectomies [20]. Additionally, Rea et al. found that angioplasty procedures in SRs were not a risk factor for postoperative morbidity in their study in which they performed angioplasty procedures in 39 of 199 SR patients [8]. In our series, we performed SR and reconstruction of the pulmonary artery in eight patients and did not experience any angioplasty-related complication. Pneumonectomy reduces the quality of life by restricting the lung reserve, increasing the pressure in the pulmonary artery, and causing more serious heart failure than lobectomy [11]. Additionally, pneumonectomy is associated with complications that include postpneumonectomy lung oedema, adult respiratory distress syndrome, and post-pneumonectomy syndrome [21]. Moreover, pneumonectomy increases the risk of cardiopulmonary death [11]. Thus, pneumonectomy should be avoided whenever possible anatomically. Furthermore, the survival after SR is at least equal to that after pneumonectomy and SR causes fewer respiratory sequelae and enables a better quality of life [5]. Additionally, SR allows a second operation in cases that develop a second primary lung cancer. In conclusion, SR is an alternative to pneumonectomy. Since 1947, the published outcomes indicate that SR is good therapy for both malignant and benign diseases of the lungs and has a better postoperative morbidity, mortality, and lung function and quality of life than pneumonectomy. At present, when a pneumonectomy is considered a disease condition itself, surgeons should be encouraged to perform SRs. We think that anastomosisrelated complications, which are the most important complications of SRs, are experience-related technical complications and training thoracic surgeons to perform SRs at experienced institutes will reduce the morbidity associated with SRs.
References [1] Price Thomas C. Conservative resection of bronchial tree. J R Coll Surg Edinburgh 1955;1:169–86.
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[2] Jones PH. Lobectomy and bronchial anastomosis in the surgery of bronchial carcinoma. Ann R Coll Surg Engl 1959 Jul;25:20–38. [3] Van Schil PE, Brutel de la Riviere A, Knaepen PJ, van Swieten HA, Reher SW, Goossens DJ, Vanderschueren RG, van den Bosch JM. Long-term survival after bronchial sleeve resection: univariate and multivariate analyses. Ann Thorac Surg 1996;61:1087–91. [4] Watanabe Y, Shimizu J, Oda M, Hayashi Y, Watanabe S, Yazaki U, Iwa T. Results in 104 patients undergoing bronchoplastic procedures for bronchial lesions. Ann Thorac Surg 1990;50:607–14. [5] Tronc F, Gregoire J, Rouleau J, Deslauriers J. Long-term results of sleeve lobectomy for lung cancer. Eur J Cardiothorac Surg 2000;17:550–6. [6] Gaissert HA, Mathisen DJ, Moncure AC, Hilgenberg AD, Grillo HC, Wain JC. Survival and function after sleeve lobectomy for lung cancer. J Thorac Cardiovasc Surg 1996;111:948–53. [7] Tedder M, Anstadt MP, Tedder SD, Lowe JE. Current morbidity, mortality, and survival after bronchoplastic procedures for malignancy. Ann Thorac Surg 1992;54:387–91. [8] Rea F, Marulli G, Schiavon M, Zuin A, Hamad AM, Rizzardi G, Perissinotto E, Sartori F. A quarter of century experience with sleeve lobectomy for non-small cell lung cancer. Eur J Cardiothorac Surg 2008;34:488–92. [9] Ginsberg RJ, Hill LD, Eagan RT, Thomas P, Mountain CF, Deslauriers J, Fry WA, Butz RO, Goldberg M, Waters PF. Modern 30 day operative mortality for surgical resections in lung cancer. J Thorac Cardiovasc Surg 1983;86:654–8. [10] Bagan P, Berna P, Pereira JC, Le Pimpec Barthes F, Foucault C, Dujon A, Riquet M. Sleeve lobectomy versus pneumonectomy: tumor characteristics and comparative analysis of feasibility and results. Ann Thorac Surg 2005;80:2046–50. [11] Ferguson MK, Lehman AG. Sleeve lobectomy or pneumonectomy: optimal management strategy using decision analysis techniques. Ann Thorac Surg 2003;76:1782–8. [12] Deslauriers J, Grégoire J, Jacques LF, Piraux M, Guojin L, Lacasse Y. Sleeve lobectomy versus pneumonectomy for lung cancer: a comparative analysis of survival and sites or recurrences. Ann Thorac Surg 2004;77:1152–6. [13] Maggi G, Casadio C, Pischedda F, Cianci R, Ruffini E, Filosso P. Bronchoplastic and angioplasty techniques in the treatment of bronchogenic carcinoma. Ann Thorac Surg 1993;55: 1501–7. [14] Okada M, Yamagishi H, Satake S, Matsuoka H, Miyamoto Y, Yoshimura M, Tsubota N. Survival related to lymph node involvement in lung cancer after sleeve lobectomy compared with pneumonectomy. J Thorac Cardiovasc Surg 2000;119:814–9. [15] Yoshino I, Yokoyama H, Yano T, Ueda T, Takai E, Mizutani K, Asoh H, Ichinose Y. Comparison of the surgical results of lobectomy with bronchoplasty and pneumonectomy for lung cancer. J Surg Oncol 1997;64:32–5. [16] Takeda S, Maeda H, Koma M, Matsubara Y, Sawabata N, Inoue M, Tokunaga T, Ohta M. Comparison of surgical results after pneumonectomy and sleeve lobectomy for non-small cell lung cancer. Trends over time and 20-year institutional experience. Eur J Cardiothorac Surg 2006;29:276–80. [17] Ludwig C, Stoelben E, Olschewski M, Hasse J. Comparison of morbidity, 30-day mortality, and long-term survival after pneumonectomy and sleeve lobectomy for non-small cell lung carcinoma. Ann Thorac Surg 2005;79:968–73. [18] Fadel E, Yildizeli B, Chapelier AR, Dicenta I, Mussot S, Dartevelle PG. Sleeve lobectomy for bronchogenic cancers: factors affecting survival. Ann Thorac Surg 2002;74:851–9.
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[19] Rendina EA, Venuta F, De Giacomo T, Ciccone AM, Moretti M, Ruvolo G, Coloni GF. Sleeve resection and prosthetic reconstruction of the pulmonary artery for lung cancer. Ann Thorac Surg 1999;68:995–1002. [20] Shrager JB, Lambright ES, McGrath CM, Wahl PM, Deeb ME, Friedberg JS, Kaiser LR. Lobectomy with tangential
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pulmonary artery resection without regard to pulmonary function. Ann Thorac Surg 2000;70:234–9. [21] Ferguson MK, Karrison T. Does pneumonectomy for lung cancer adversely influence long-term survival? J Thorac Cardiovasc Surg 2000;119:440–8.
Original Article
Sleeve Resections for Squamous Cell Carcinoma of the Lung Suat Gezer, MD a,∗ , Gürhan Öz, MD b , Göktürk Fındık, MD b , Hasan Türüt, MD b , Tamer Altınok, MD b , Mehmet Sırmalı, MD b , Erkmen Gülhan, MD b , ˙ ˘ ¸ kıran, MD c , Sadi Kaya, MD b and Irfan Yetkin Agac Tas¸tepe, MD b a Düzce University, Faculty of Medicine, Clinic of Thoracic Surgery, Düzce, Turkey Atatürk Chest Diseases and Thoracic Surgery Training and Research Hospital, Clinic of Thoracic Surgery, Ankara, Turkey c Atatürk Chest Diseases and Thoracic Surgery Training and Research Hospital, Department of Pathology, Ankara, Turkey
b
Background: Sleeve resection is an advanced technique that was developed as an alternative to pneumonectomy. This study evaluated our cases of sleeve resection for squamous cell carcinoma of the lung and compared the outcomes with the literature reports. Methods: In total, 26 bronchial, 5 bronchovascular, and 3 vascular sleeve lobectomies were performed between January 2000 and July 2005 in our clinic. Age, gender, operations, postoperative diagnosis and staging, and postoperative morbidity and mortality were evaluated. Results: Sleeve resections were performed in 34 patients. All patients were male, with a mean age of 59.4 years. The operations consisted of 16 right upper, 14 left upper, and 1 left lower sleeve lobectomies and 3 superior sleeve bilobectomies. The most common postoperative pathological staging group was stage IIb (32.3%). Operative mortality was 5.9% (n = 2). Postoperative morbidity was 20.5% (n = 7), including 4 prolonged air leaks plus empyema, 1 prolonged air leak, 1 postoperative bleeding needing revision, and 1 severe bronchostenosis; of these, 6 had persistent atelectasis. The local tumour recurrence rate was 11.7% (n = 4). The median survival time and 5-year survival were 36 months and 42%, respectively. Conclusions: Sleeve resection proved to be good therapy for lung cancer and has a lower morbidity and mortality than standard pneumonectomies and results in better lung function and quality of life. The anastomosis-related complications are experience-related technical complications and training thoracic surgeons to perform SRs at experienced centres will reduce the morbidity associated with SRs. (Heart, Lung and Circulation 2010;19:549–554) © 2010 Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand. Published by Elsevier Inc. All rights reserved. Keywords. Pulmonary malignancy; Sleeve resection of lung; Parenchyma sparing operation; Sleeve lobectomy
Introduction
S
leeve resections (SR) were designed to treat patients with rare endobronchial lesions, such as tumours or strictures, in patients who could not tolerate a pneumonectomy. Price Thomas performed the first sleeve lobectomy for a carcinoid tumour located in the right main bronchus in 1947 [1]. Allison performed the first sleeve lobectomy for lung cancer in 1952 [2]. Subsequently, many publications have reported that SR enables a tumour resection rate similar to that of pneumonectomy and they proposed that SRs be performed more widely [3–6]. Additionally, they pointed out the significant contribution of the
Received 28 April 2009; received in revised form 9 February 2010; accepted 21 February 2010 ∗
Corresponding author at: Düzce Üniversitesi Tıp Fakültesi, ˘ Cerrahisi AD, 81620 Konuralp, Düzce, Turkey. Gögüs Tel.: +90 380 5421390. E-mail address: [email protected] (S. Gezer).
re-implanted lung to postoperative respiratory function [6]. Sleeve resections can be classified as follows: 1. Sleeve lobectomies a. bronchial sleeve lobectomy b. vascular sleeve lobectomy c. bronchovascular sleeve lobectomy 2. Sleeve bronchial resections 3. Tracheal sleeve pneumonectomies This study evaluated the results of sleeve lobectomies for squamous cell carcinoma of the lung that we performed over a 5.5-year period.
Materials and Methods In total, 34 patients underwent sleeve lobectomies for squamous cell carcinoma of the lung at Atatürk Chest Diseases and Thoracic Surgery Training and Research
© 2010 Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand. Published by Elsevier Inc. All rights reserved.
1443-9506/04/$36.00 doi:10.1016/j.hlc.2010.02.026
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Gezer et al. ‘Sleeve Resections of the Lung’
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Figure 1. Chest X-ray (a) and thoracic computed tomography (b and c) of patient with squamous cell carcinoma invading entrance of left upper lobe bronchus and pulmonary artery.
Hospital, Ankara, Turkey, between January 2000 and July 2005. Preoperatively, all of the patients underwent radiological investigations, including a chest X-ray and thoracic computed tomography (CT) (Fig. 1). Fibre-optic bronchoscopy (FOB) was used to obtain diagnostic biopsies and to evaluate the feasibility of SR. The patients in whom a classical lobectomy was not feasible, but complete disease resection was possible with a SR, based on the results of thoracic CT and FOB, underwent SR. The patients’ respiratory sufficiency for the resection was evaluated by measuring the forced expiratory volume in 1 s (FEV1 ) and diffusing capacity of the lung for carbon monoxide (DLCO). For patients with borderline FEV1 and DLCO measures, the maximum oxygen consumption during exercise (VO2max ) and postoperative FEV1 were measured. Additionally, all patients were assessed with a complete blood count, analyses of blood chemistry and coagulation parameters, and a complete urinalysis. Cardiac status was assessed routinely with an electrocardiogram (ECG) and a cardiology consultation was requested for the patients older than 55 years or with any suspected pathology. All patients underwent an anesthesia clinic evaluation preoperatively. The patients who were selected for a sleeve resection were taken to the operating room and underwent a posterolateral thoracotomy. All bronchial sleeve resections were circumferential and the anastomoses were performed in an end-to-end manner. The vascular sleeve resections were circumferential or tangential, according to the vessel involvement, and end-to-end anastomoses were performed after circumferential resections and vessel repair after tangential resections. The bronchial anastomosis was performed with a continuous suture on the membranous side and with interrupted sutures on the cartilaginous side, using 3-0 absorbable (polydioxanone or polyglactin) sutures. Vascular anastomoses or repairs were performed with continuous 5-0 polypropylene sutures (Fig. 2). Following completion of the anastomosis, the lung
was inflated and the saline-covered bronchus observed for any evidence of air leaks under 30–40 cm H2 O airway pressure and sutures were added if any air leak was observed. The anastomosis line was covered with a pedicle flap, consisting of thymic remnant, pericardial fat tissue, pleura, or intercostal muscle. After closing the thoracotomy, FOB through the endotracheal tube or rigid bronchoscope was performed to check the anastomotic line and to perform bronchial cleaning. All patients were followed in the intensive care unit for 24 h. All patients used expectorants and incentive spirometry and had chest physiotherapy to prevent secretion retention. The patients who developed secretion retention and atelectasis despite this therapy underwent FOB for bronchial cleaning. Additionally, those patients who did not undergo a FOB for another reason underwent FOB to check the anastomotic line 7 days postoperatively. The patients with no complications were discharged 7 days postoperatively. After discharge, the patients were followed in the outpatient clinic for 20 days postoperatively and then once every 3 months for the rest of the first year and twice a year subsequently. Patient records were re-evaluated for age, gender, type of operation, histopathological results and stage, adjuvant and neoadjuvant therapies, postoperative complications, and survival. Patient survival was analysed using the Kaplan–Meier method. Our data were compared with published results.
Results During a 5.5-year period, 34 patients underwent a SR for squamous cell carcinoma of the lung. All of the patients were male with a mean age of 59.4 (41–74) years. The procedures included 26 bronchial sleeve lobectomies, 5 bronchovascular sleeve lobectomies, and 3 vascular sleeve lobectomies.
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Table 1. Postoperative Staging of Primary Lung Cancer Patients. Stage IA IB IIA IIB IIB IIIA IIIA IIIA
TNM
Patient Number
Ratio (%)
T1N0M0 T2N0M0 T1N1M0 T2N1M0 T3N0M0 T2N2M0 T3N1M0 T3N2M0
3 10 2 10 1 3 3 2
8.8 29.4 5.9 29.4 2.9 8.8 8.8 5.9
Total
Figure 2. (Same patient) Intraoperative view of bronchovascular sleeve lobectomy of left upper lobe: (a) pulmonary artery invaded by the tumour, (b) clamping of proximal and distal part of invasion, (c) segmental resection of invaded part of pulmonary artery, (d) beginning of end-to-end anastomosis of pulmonary artery, (e) anastomosis of pulmonary artery, (f) anastomosed pulmonary artery, and (g) endobronchial lesion invading the entrance of upper lobe bronchus in resected lobe.
In all patients, a preoperative histopathological diagnosis was made after FOB. Eight patients had a preoperative mediastinoscopy. Metastasis to mediastinal lymph nodes was diagnosed in one patient and this patient underwent surgery after neoadjuvant chemotherapy. Additionally, one patient received neoadjuvant chemotherapy based on the preoperative CT findings and was operated on after evaluating the mediastinal lymph node clearance at mediastinoscopy. The other six patients were found to be free of N2 disease at mediastinoscopy and underwent SR. The location of the sleeve lobectomy was the right upper lobe in 16 patients, left upper lobe in 14 patients, bilobectomy of the right upper and middle lobes in 3, and left lower lobe in 1.
34
100
The postoperative histopathological examinations confirmed squamous cell carcinoma. The most common stage was IIb (32.3%; Table 1). Although we routinely made frozen examinations of the bronchial surgical margins, the postoperative histopathological examinations detected tumour-positive bronchial surgical margins in four patients. Those patients could not have undergone an alternative procedure, because two had insufficient respiratory capacity for pneumonectomy and two refused a second operation and were referred for radiotherapy. Postoperatively, eight patients underwent radiotherapy, one had chemotherapy, and two had chemoradiotherapy as adjuvant treatment. Postoperatively, seven patients (20.5%) developed complications (Table 2). Secretion retention and atelectasis was the most common complication. All of the complications, except the bronchial stenosis, improved with treatment and did not cause any permanent morbidity or mortality. The patient with bronchostenosis refused a second operation. One patient died 10 days postoperatively of acute renal failure and one, 24 days postoperatively due to cerebral thromboembolism. Thus, the 30-day postoperative mortality was 5.9% (n = 2). In the long-term, one patient died 3 years postoperatively due to myocardial infarction and eight patients died of the disease progression at a median of 21 months postoperatively (four local tumour recurrences and four distant metastases). The long-term mortality was 26.4% (n = 9). By the Kaplan–Meier method, the median survival time was 36 months and the 5-year survival was 42% (Graph 1).
Discussion Sleeve resections require more experience than a classical lobectomy. The bronchial and vascular anastomosis may cause complications that are not seen in classical lobectomies. Thus, bronchoplasty and angioplasty operations should also have low morbidity and mortality ratios to constitute a suitable treatment method. The reported operative mortality is summarised in Table 3 and is between 1.6 and 5.5%. This is better than the 6% operative mortality after pneumonectomy, reported by the Lung Cancer Study Group [3,5,7–12]. Bagan et al. compared sleeve lobectomy and pneumonectomy and reported a 4.5% operative mortality for sleeve lobectomy
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Table 2. Postoperative Morbidities. Complications
Patient Number
Secretion retention and atelectasis Prolonged air leak + empyema Prolonged air leak (without empyema) Haemorrhagic drainage that needed revision Stenosis on bronchial anastomotic line due to extended granulation and fibrosis
Ratio (%)
6 4 1 1 1
17.6 11.7 2.9 2.9 2.9
Table 3. The Literature about Operative (30-Day) Mortality and 5-Year Survival after Bronchoplastic Procedures. First Author (reference)
Year
Tedder (meta-analysis) Van Schil Tronc Ferguson (meta-analysis) Deslauriers Bagan Rea
1992 1996 2000 2003 2004 2005 2008
Number of Patients 1915 145 184 860 184 66 199
Graph 1. Survival (Kaplan–Meier method).
versus 12.6% for pneumonectomy [10]. The respective rates were 4.1% versus 6.0% in Ferguson and Lehman’s meta-analysis [11] and 1.3% versus 5.3% in Deslauriers et al. [12]. Our operative mortality was 5.9%. Additionally, these deaths were not related to the operations directly: one was due to acute renal failure and the other to cerebral thromboembolism. Nevertheless, the reported operative mortality and our results are better than for pneumonectomy. The five-year survival after sleeve lobectomy for lung cancer is generally between 39.7 and 52% (Table 3). Exceptionally, Bagan et al. reported a rate of 72.5% [10]. Some other published five-year survivals are 45, 42, and 40% in 79, 72, and 69 patients, respectively [4,6,13]. In our study, the five-year survival was 42% (Graph 1), consistent with these literature reports. Many studies comparing sleeve lobectomy and pneumonectomy have shown that sleeve lobectomy has no negative effects on long-term survival [6,11,14,15]. Furthermore, Ferguson and Lehman found a better prognosis after sleeve lobectomy in stage I patients [11]. Both Deslauriers et al. [12] and Okada et al. [14] reported a significantly
30-Day Mortality (%) 5.5 4.8 1.6 4.1 1.6 4.5 4.5
5-Year Survival (%) 40 46 52 51.4 52 72.5 39.7
better prognosis after sleeve lobectomy in stages I and II patients. Takeda et al. did not report any difference in the five-year survival of stages I and II patients after sleeve lobectomy or pneumonectomy, but the overall five-year survival of the sleeve lobectomy group was better than that of the pneumonectomy group (54% vs. 33%) [16]. Some other reported five-year survivals after sleeve lobectomy and pneumonectomy were 72.5% versus 53.2% and 39% versus 27% [10,17]. Local tumour recurrence after SR has been widely investigated, but there is no consistent definition of “local recurrence” in the published studies. While some authors define local recurrence as recurrence in the suture line, others define it as recurrence in the same lung [6–8]. Reported local tumour recurrence rates are 14.0, 12.5, and 11.6% [4–6]. We observed tumour recurrence in the same lung in 4 patients (11.7%). One of the four local recurrence patients had a tumour-positive bronchial surgical margin. Despite some unsuccessful results, frozen section examination should be routinely made in TSP operations for the safety of the bronchial surgical margins like other bronchial cancer operations. Secretion retention and persistent atelectasis are the most common complications of SRs [5,7,13]. These problems are related to the deterioration of the ciliary epithelium and lymphatics and partial denervation of the re-implanted lung or anastomotic oedema [5]. In our study, we experienced this complication in six patients, despite aggressive therapy that included expectorants, incentive spirometry, and chest physiotherapy. A lack of patient compliance was the leading cause of this complication and all recovered with secretion clearance via FOB. Although bronchial anastomotic complications are important complications of SRs, preservation of the bronchial blood supply, creation of a tension-free bronchial anastomosis, and improved suture materials have resulted in better bronchial healing, significantly reducing the incidence of bronchial anastomotic complications [18]. Tedder et al. examined 1915 patients and reported bronchopleural fistulas in 3.5% and late strictures in 4.8% [7]. The respective rates were 1.1 and 2.2% in
a study of 184 patients [5]. Another study of 199 patients observed bronchopleural fistulas in 1% and bronchial stenosis in 10% [8]. We observed no bronchopleural fistula. We experienced stenosis of the anastomotic line and complete obstruction of the main bronchus after a sleeve lobectomy of the right upper lobe in one patient (2.9%). We offered a pneumonectomy, but the patient refused the second operation. Despite the resulting autopneumonectomy, he did not develop respiratory distress, because his respiratory capacity was good. The outcomes of vascular sleeve lobectomies are also good. Rendina et al. experienced only one complication, which was thrombosis in the pulmonary artery in their series in which they performed SR and reconstruction of the pulmonary artery in 52 patients; they did not observe any mortality and reported that their morbidity, mortality, and functional results were not different from those reported for standard lobectomies [19]. For 33 vascular sleeve lobectomy patients, the results of Shrager et al. did not differ from standard lobectomies [20]. Additionally, Rea et al. found that angioplasty procedures in SRs were not a risk factor for postoperative morbidity in their study in which they performed angioplasty procedures in 39 of 199 SR patients [8]. In our series, we performed SR and reconstruction of the pulmonary artery in eight patients and did not experience any angioplasty-related complication. Pneumonectomy reduces the quality of life by restricting the lung reserve, increasing the pressure in the pulmonary artery, and causing more serious heart failure than lobectomy [11]. Additionally, pneumonectomy is associated with complications that include postpneumonectomy lung oedema, adult respiratory distress syndrome, and post-pneumonectomy syndrome [21]. Moreover, pneumonectomy increases the risk of cardiopulmonary death [11]. Thus, pneumonectomy should be avoided whenever possible anatomically. Furthermore, the survival after SR is at least equal to that after pneumonectomy and SR causes fewer respiratory sequelae and enables a better quality of life [5]. Additionally, SR allows a second operation in cases that develop a second primary lung cancer. In conclusion, SR is an alternative to pneumonectomy. Since 1947, the published outcomes indicate that SR is good therapy for both malignant and benign diseases of the lungs and has a better postoperative morbidity, mortality, and lung function and quality of life than pneumonectomy. At present, when a pneumonectomy is considered a disease condition itself, surgeons should be encouraged to perform SRs. We think that anastomosisrelated complications, which are the most important complications of SRs, are experience-related technical complications and training thoracic surgeons to perform SRs at experienced institutes will reduce the morbidity associated with SRs.
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