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Eur J Cardiothorac Surg 1999;15:426-432
© 1999 Elsevier Science NL

Survival and prognostic factors in patients undergoing parenchymal saving bronchoplastic operation for primary lung cancer: a series of 110 consecutive cases

Department of Thoracic Surgery, Marie Lannelongue Hospital, Le Plessis Robinson, France

Received 12 October 1998; received in revised form 13 January 1999; accepted 27 January 1999.

Corresponding author. Service de Chirurgie Thoracique et Vasculaire, Centre Chirurgical Marie Lannelongue, 133 avenue de la résistance, Le Plessis Robinson, 92350, France. Tel.: +33-1-4094-2800; fax: +33-1-4094-5582.

	Abstract

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Objective: The purpose of this study was to report our experience concerning bronchial sleeve lobectomy for treating bronchogenic cancer. Method: From 1980 to 1994, 110 patients underwent bronchial sleeve lobectomy for bronchogenic cancer. In 45 patients, preoperative investigations contraindicated pneumonectomy, whereas in 65 other patients, sleeve resection was performed without functional necessity. The most common procedures were sleeve lobectomy of the right upper lobe (64%), and of the left upper lobe (21%). Sixteen patients (15%) underwent additional arterial vascular resection. Seven patients had microscopic invasion of the bronchial margin without the possibility of further resection in six with regard to their limited respiratory function. Tumors were staged as follow: 32 stage IB (all T2 N0), 57 stage IIB (57T2 N1), and 17 stage IIIA (eight, T3N1; nine, T2N2), whereas four patients had an in situ cancer (four stage 0). Results: Operative mortality was 2.75%. The 5- and 10-year actuarial survival rates were, respectively, 39 and 22% for the entire group. The 5-year actuarial survival rates were, 60% in stage IB, 30% in stage IIB, and 27% in stage IIIA. Four factors significantly influenced survival (P<0.05): nodal stage, arterial resection, invasion of the bronchial stump and poor functional respiratory status contraindicating pneumonectomy. Conclusions: In our experience, sleeve resection for stage I provides comparable survival to that of standard resection at equal stage. However, in patients with pathologically N1 disease, who can tolerate a pneumonectomy, a randomized study is mandatory to confirm that sleeve lobectomy can be performed without the risk of decreasing long-term survival. In our study, patients who required an associated vascular resection demonstrated a poor survival.

Key Words: Pulmonary neoplasms • Surgery • Bronchial sleeve resection

	Introduction

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Sleeve lobectomy is performed to achieve complete resection of bronchial carcinoma centrally located, generally invading the origin of the upper lobar bronchus, and/or of the distal main bronchus [1] [2]. In respiratory compromised patients who cannot tolerate pneumonectomy and require a lung-sparing operation, it is the sole feasible surgical operation for cure. In other patients, it can be performed as an alternative to pneumonectomy with several advantages, i.e. decreasing post-operative morbidity and mortality, and preserving parenchyma with better long-term respiratory function [1] [2]. We present herein, our experience based on 110 sleeve lobectomies, consecutively performed in a 14-year recent period.

	Materials and methods

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From 1981 to 1995, bronchial sleeve lobectomy for primary lung cancer was performed in 110 patients in our department. Sleeve lobectomy represented approximately 3% of our total number of resections for lung cancer during this period. There were 104 men (95%) and six women (5%) with a mean age of 61 years (ranging from 41 to 78 years). Nine patients had been previously treated for an oropharyngeal cancer. Seven patients, who had previously undergone a contralateral lung resection for cancer, underwent a bronchial sleeve lobectomy. This method was the sole surgical procedure available in these patients, who were not suitable for pneumonectomy. Tumor resectability was assessed by fibroscopy and computed tomography scan, showing that in 45 patients (41%) a standard lobectomy could not be performed due to the endoluminal cancer invasion of the bronchial origin with extension towards the mucosa of the adjacent main bronchus and/or towards the distal bronchus. In 65 other patients (59%), decision making for sleeve resection was only taken during operation since dissection revealed exoluminal bronchial cancer invasion of the origin of the lobar bronchus and/or because frozen-section analysis of the bronchial section identified a positive margin. Pulmonary function tests, arterial blood gas analysis and perfusion lung scanning were always performed to completely assess the respiratory status of patients. Pneumonectomy was contraindicated when predicted post-operative forced expiratory volume in 1 second (Ppp-FEV 1) was less than 35%, or when cardiac examinations with echocardiography revealed too severe cardiac insufficiency. Finally preoperative investigations contraindicated pneumonectomy in 45 patients (41%), whereas in 65 other patients (59%), sleeve lobectomy was performed without functional necessity. Among the 45 patients with compromised function, 28 had a Ppp-FEV 1 less than 35% of the theoretical values, 13 had a Ppp-FEV 1 between 35 and 40% associated with a limited general condition and/or an altered left ventricular function, and four patients had only a poor left ventricular function. It is worth noting that these two groups were strictly equivalent in regard to other parameters: age, location of cancer, side, TNM staging. Mediastinoscopy was selectively performed in highly suspected N2 disease on high-resolution CT scan, to exclude patients with proven N2 disease for operation. Two patients in this study, underwent a mediastinoscopy, followed by a bronchoplastic lobectomy due to negative mediastinal node sampling. One patient underwent mediastinal radiotherapy with a high dosage (60 grays), for treating a tracheal cancer, 2 years before a sleeve lobectomy. This patient, who was included in another study [3], underwent a bronchial sleeve lobectomy with reinforcement of the anastomosis by an intercostal flap, and then demonstrated an uneventful recovery. Anesthesia was usually conducted with a double-lumen endotracheal tube for one-lung ventilation. When a controlled ventilation in the recovery unit was necessary, a single-lumen tube was replaced at the end of the operation. In the post-operative period, bronchoscopy was only done for specific clinical considerations, i.e. coarse wheeze with excessive secretions, atelectasis and persistent air leak at 7 days which may indicate an anastomotic dehiscence. Patients had systematically flexible endobronchial examination before discharge to check for the absence of anastomotic complications, i.e. stenosis, granuloma.

The most common procedures were upper sleeve lobectomy of the right lobe (n=70, 64%), and of the left upper lobe (n=23, 21%). Lower sleeve lobectomy were more infrequent and concerned the left inferior lobe (n=12, 11%), or the right inferior lobe (n=2). There were also two right upper and middle bilobectomies with re-implantation of the inferior lobe in the main bronchus. One patient underwent a right middle and inferior bilobectomy with resection of the origin of the upper lobe which was reimplanted into the main bronchus. Bronchoplastic resection was total and circumferential in 19 patients (17%). In 91 patients (83%) a near total resection (large wedge resection) was performed, leaving a small part of the mediastinal cartilage wall bronchus, a technical point that in our opinion, may contribute to cicatrisation, in preserving a small but important area of bronchial vascularization through adjacent mediastinal vascularized tissue. Care was taken to preserve as much as possible, the bronchial vascularization of the remaining lobes during mediastinal lymphadenectomy. After verification of the tumor free-margin of the proximal and of the distal bronchial margins of resection on frozen-section examination, the bronchial anastomosis was realized with 4-0 polydioxanone suture material(PDS, Ethicon Laboratory). In case of wedge resection, interrupted sutures were placed circumferentially and were tied up after all sutures have been positioned. In case of complete resection, a continuous running suture for cartilage–cartilage anastomosis was performed, followed by interrupted sutures for membranous–membranous anastomosis, all knots being placed outside the lumen. The inferior pulmonary ligament was always transected to enhance hilar mobility, allowing a free tension anastomosis. Sixteen patients (15%) underwent associated resection of the pulmonary artery with reconstruction. The arterial resection was total and circumferential in four cases and lateral with tangential closure in 12 cases, using 6-0 polypropylene suture material (Prolene; Ethicon laboratory). We frequently used at the beginning of our experience, a pleural flap to cover the bronchial anastomosis with hope to provide a physical barrier between the bronchus and the pulmonary artery, therefore preventing a fatal bronchovascular fistula. Due to the lack of proof of its efficacy, we currently do not realize pleural flaps. According to the TNM classification [4], four of the resected tumors were in situ-stage Tis N0 M0, 32 were stage IB (all T2N0), 57 were stage IIB (all T2 N1), and 17 were stage IIIA (8 T3 N1, 9 T2N2). Squamous cell cancer was found in 95 patients (86%), adenocarcinoma in ten (9%), mixed cell carcinoma in three, and undifferentiated large cell carcinoma in two. Tumor resection was considered as complete and radical if all gross cancer was removed, if the resection margin was free of disease, and if the highest mediastinal node was free of tumor. Local recurrence was defined as any recurrence in the ipsilateral hemithorax unless the histological type was different. All stage IIIA patients received complementary treatment: 16 patients received post-operative irradiation with a mean dose of 50 grays, and one patient both radiotherapy and chemotherapy.

Information was gathered from the files of patients followed in our institution, or was obtained from the referring pulmonary physicians. Follow-up was completed in March 1998 for all patients with a minimum follow-up for surviving patients of 2 years. Survival rates were calculated according to actuarial method derived from the Kaplan–Meier method [5], and were compared between groups with the log-rank test. A P-value less than 0.05 was considered to be significant.

	Results

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Resectability
Resection was considered as complete in 103 cases (93.6%) and incomplete in seven cases (6.4%). In six cases (four, T3N1; two T2N2), frozen section examination revealed a microscopically positive margin. Although an arterial vascular angioplastic procedure had been realized in four of these cases, a more extensive bronchial resection was anatomically not feasible, and a pneumonectomy was functionally contraindicated. All these patients having a stage IIIA disease received postoperative radiotherapy (50–60 grays). In the remaining case, the invasion of the bronchial margin was missed on frozen section examination and was secondary revealed on definitive histological examination. This patient with a T3N1 tumor denied reoperation and received adjuvant radiotherapy. It is worth noting that among the 16 patients who underwent arterial vascular angioplastic procedure, all had lymph nodes invasion, with N1 disease in 13 cases (81%) and N2 disease in three cases: there were eight, T2N1; five T3N1; three T2N2. As aforementioned, four of these 16 patients (25%) had incomplete resection with invasion of the bronchial stump on frozen section examination, without the possibility of further resection.

Mortality
Thirty-day operative mortality was 2.75% (3/110). One death was related to a bronchovascular fistula, the second to a pulmonary embolus, and the third one to a bronchopleural fistula occurring in a cirrhotic patient. Our mortality rate was not significantly higher in compromised patients (4.4%; 2/45) than in non-compromised patients (1.5%; 1/65) (P=0.7). Post-operative courses were uneventful in 61 patients (55%). Non-lethal post-operative complications occurred in 49 patients (44%), including a small bronchopleural fistula in three, an hemothorax in two, a pulmonary embolus in two, an atelectasis in eight, a ventilation exceeding 2 days in eight (max ventilation time: 10 days), an air leak exceeding 7 days in nine, a cardiac rhythmic disorder in five, and various other non-threatening medical complications in nine. Two bronchopleural fistulas healed under drainage, and the third case through a small thoracostomy. As indicated in Table 1, only post-operative atelectasis and post-operative ventilation where significantly more frequent in compromised patients than in uncompromised one's. Late complications at the site of the bronchial anastomosis occurred in four patients. It concerned two cases of granuloma at the anastomotic site, which were successfully treated with endoscopic laser excision, and two cases of anastomotic stricture which were treated with an endoluminal silicone tube stent in one instance, and necessitated a complete pneumonectomy in the other instance. No significant difference in various complications was observed, when comparing the two types of bronchoplastic procedure, i.e. complete or incomplete bronchial resection. Three out of the four patients who presented postoperative bronchopleural fistulas had undergone wrapping of their bronchial sutures with pleural flaps, as the patient who died post-operatively of bronchovascular fistula.

Eighty patients died during the follow-up, and at the completion of the study, 27 patients (24.5%) were still alive. We failed to determine the exact extent of cancer disease at the time of death in 22% of the cases. Thirty-two percent of patients died of metastases alone, 10% died of metastases combined with local recurrence, 24% died of local recurrence alone without significant difference in the distribution between the three nodal groups. Twelve percent of patients died of second primary lung cancer. The 5-year actuarial survival rate for the entire group was 39% (CI 95%, 30–48%) and the 10-year actuarial survival 22% (CI 95%, 13–30%) ( Fig. 1 ).

View larger version (16K): [in this window] [in a new window]   Fig. 1. Actuarial survival curves with reference to the entire group, to complete resection and to incomplete resection.

View larger version (16K): [in this window] [in a new window]   Fig. 2. Actuarial survival curves with reference to stage.

View larger version (13K): [in this window] [in a new window]   Fig. 3. Actuarial survival curves with reference to nodal disease.

View larger version (13K): [in this window] [in a new window]   Fig. 4. Actuarial survival curves with reference to the realization of an associated arterial resection.

View larger version (13K): [in this window] [in a new window]   Fig. 5. Actuarial survival curves with reference to the pulmonary function of patients.

	Discussion

Top Abstract Introduction Materials and methods Results Discussion References

Several procedures have been proposed to prevent bronchial dehiscence and bronchovascular fistula: pleural flaps, free pericardium flaps and muscle flaps [15]. Nowadays, we only cover the anastomosis with an intercostal muscle flap in case of previous radiotherapy. The 3.6% rate of bronchopleural fistula enregistered in our series is very similar to the 3% rate reported by Tedder et al. [9], and ranging from 0 to 6% in other reports [2,6,8–11,15). In patients presenting a small dehiscence, such as three patients in our series, the fistula may heal through prolonged drainage, sometimes with an attempt to seal the leak endoscopically with fibrin glue. Associated space problem with empyema may resolve through lavage under posture with special care to avoid any risk of aspiration through the fistula, or through tailored thoracostomy or thoracoplasty. Marked dehiscence may require, in compromised patients, an attempt of wrapping the anastomosis with a muscle flap or an omentum flap as Kawarara et al. [15] successfully reported it. In patients with good respiratory function, a completion pneumonectomy may be discussed, knowing that, it is a challenging operation in this situation, with a high risk of post-operative empyema and fistula. When studying factors leading to complications after sleeve lobectomy, Weisel et al. [10] and Deslauriers et al. [11] reported a higher incidence of bronchial fistulas in compromised patients. Despite the fact that we observed a slight increased incidence of bronchopleural fistula in this group of patients, the difference did not reach statistical significance(P=0.3). However, in our experience, compromised respiratory patients experienced significantly, more atelectasis (P<0.001) than non-compromised patients, with a trend in an increasing occurrence of prolonged air leak and in prolonged ventilation(P<0.2 and <0. 1, respectively).

Survival and prognosis factors
In our study, sleeve lobectomy provided an overall 5- and 10-year actuarial survival rates of 39 and 22%, respectively, data that are in the range of literature results, which are summarized in Table 2Table 3. Tedder et al. [9] calculated that in 1125 patients who underwent sleeve lobectomies in several institutions, the overall 5-year actuarial survival rates was 40%. Survival is mainly dependent on resectability and nodal stage. Our 5-year actuarial survival rates after complete resection were in the range of literature results (Table 2), and very similar to that calculated by Tedder et al. [9] by pooling the results of several series, with 5-year actuarial survival rates for stage I, II and III, of 63, 37 and 21%, respectively. For tumors with negative nodes (pN0 disease), sleeve lobectomy is mainly performed for central T2N0 lesions, and provided a 5-year actuarial survival of 59% in our series, a figure that is strictly comparable with results of three recent series ranging from 57 to 62%, for equal stage [6] [7] [8]. This figure is also identical to the currently accepted norm for stage IB tumors after standard lobectomy, with a 5-year actuarial survival of 59% in the recent report of Mountain [4].

First, our 1.5% mortality rate with a 1.5% rate (1/65) of bronchopleural fistula following bronchial sleeve resection in non-compromised patients, is a result that compares favorably with that of standard pneumonectomy, in our experience and in current literature, considering that the accepted norm for post-operative mortality after pneumonectomy currently ranges from 3.2 to 6.2% [12]. To make a comparison of long-term survival between the two operations, there is no comparative randomized study available to answer the question without any doubt. However, we may suggest that the 5-year actuarial survival of 30% in stage IIB (T2N1) enregistered after sleeve lobectomy in our study, which is in the range of the literature data (Table 4, is slightly lower than the 5-year actuarial survival of 39% reported by Moutain [4] for stage IIB after standard lobectomy.

Our 33% rate of 5-year actuarial survival enregistered in nine patients with pathologically N2 disease is in the range of literature results (Table 5), and is similar to what is reported after standard resection in this nodal group [4], knowing that in our series all N2 cases were pre-operatively cN0 or cN1 (clinical N0 or N1) that were later found to be pN2 on histological examination. The fact, that sleeve lobectomy provides a better quality of life than pneumonectomy in preserving lung parenchyma is quite obvious, previous studies demonstrating the normal function of the preserved lobes [18]. Since sleeve resection preserves lung parenchyma, a second cancer may sometimes be cured with a second surgical procedure, such a second cancer occuring with a rate of 12% in our series, very close to the 12.2% rate reported by Mehran et al. [6], but higher than the 7.6% rate reported by Van Schill et al. [19].

	References

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