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Eur J Cardiothorac Surg 1999;16:418-423
© 1999 Elsevier Science NL

Closure of the bronchial stump by manual suture and incidence of bronchopleural fistula in a series of 209 pneumonectomies for lung cancer

Clinic Thoracic and Cardio-Vascular Surgery, Hôpital G. & R. Laënnec, 44093 Nantes Cedex 1, France

Corresponding author. Tel.: +33-2-40-16-51-04; fax: +33-2-40-16-51-35

	Abstract

Top Abstract 1. Introduction 2. Material and methods 3. Results 4. Discussion Appendix A. Statistical Analysis... References

 
Objective: Bronchopleural fistula after pneumonectomy is a very serious complication, occurring in 1–4% of cases, regardless of the bronchial stump closure technique adopted. The objective of this study was to report a bronchial stump closure technique in pneumonectomy by manual suture (polypropylene running suture) and to study the incidence of bronchopleural fistula. Methods: Between January 1988 and December 1997, 209 patients (186 men and 23 women, mean age=60.5 years) were operated by the same operator. The indication for surgery was lung cancer in all cases. Results: The incidence of bronchopleural fistula was 2.4%; four fistulas during the first postoperative month and another occurred at 6 months; four were located on the left side and one was situated on the right. The bronchial stump was covered in only two of these five cases; 40% died of this complication. Neoadjuvant treatment (chemotherapy and/or radiotherapy) was found to increase the risk of development of bronchopleural fistula (40% vs. 7.2%) and this difference was statistically significant (P=0.046). Conclusions: Manual closure of the bronchial stump by running suture, performed on an open bronchus, is a reliable technique with a low incidence of bronchopleural fistula. Those results could be further improved by systematically covering the right and the left bronchial stumps.

Key Words: Pneumonectomy • Bronchopleural fistula • Bronchial suture • Manual suture

	1. Introduction

Top Abstract 1. Introduction 2. Material and methods 3. Results 4. Discussion Appendix A. Statistical Analysis... References

 
In 1933, Graham [1] reported the first pneumonectomy performed in man. In 1942, Rienhoff [2] established the histological basis for healing of the bronchial stump. In 1945 Sweet [3] proposed a bronchial stump suture technique by longitudinal suture of the mucosa onto the bronchial cartilage, while, in 1949, Overholt [4] defined a second manual closure technique with transverse suture of the cartilage onto itself after application of the mucosa. Early in the 1960, Amosov [5] published the first series of patients operated with bronchial suture by automatic stapling.

From then on, two methods of bronchial suture were available to thoracic surgeons: manual suture (by running or interrupted suture) and mechanical suture. Each technique has its supporters, but neither has clearly demonstrated its superiority in pneumonectomy in terms of reduction of the incidence of bronchopleural fistula (BPF). In 1999, post-pneumonectomy BPF, a factor of morbidity and mortality aggravating the prognosis, still remains a topical problem.

The current incidence of post-pneumonectomy BPF is between 1 and 4% [6]. The objective of this study was to analyse the incidence of BPF and the factors affecting this incidence by collecting a consecutive series of 209 patients in the same institution, undergoing pneumonectomy performed by the same operator (Professor J.L. Michaud), according to a uniform operative technique comprising manual bronchial suture.

	2. Material and methods

Top Abstract 1. Introduction 2. Material and methods 3. Results 4. Discussion Appendix A. Statistical Analysis... References

 
2.1. Study population
Of the 723 consecutive pneumonectomies performed by the same technique in the Department of Thoracic and Cardiovascular Surgery of the Nantes University Hospital between 1st January 1988 and 31st December 1997, 209 were performed by the same operator (Professor J.L. Michaud). This homogeneous series consisted of 186 men and 23 women with a mean age of 60.5±10.5 years (range: 25–82). The characteristics of this retrospective series are shown in Table 1.

After possible release of the lung, the pleura, lung and mediastinum were inspected; in the case of a suspected neoplastic pleural effusion, frozen section examination of the pleural fluid was requested to determine the subsequent surgical procedure. Pneumonectomy was performed by dissection, control, section on clamp and suture by nonabsorbable monofilament running suture of the vascular pedicles; depending on local possibilities, the pulmonary veins and/or artery were controlled in an extrapericardial or intrapericardial position. In all cases, mediastinal dissection of all draining lymph node chains was performed; infracarenal lymph node dissection was completed after resection of the operative specimen by avoiding major devitalisation of the bronchial stump.

Control of the bronchus was performed and a clamp was positioned away from the carena and bronchial section was performed proximal to this clamp. Bronchial secretions were immediately aspirated and samples in the case of superinfection. Bronchial section was performed as close as possible to the carena by resection of an anterior segment of cartilage, thereby creating a posterior flap of bronchial mucosa, according to the technique described by Brewer [7], to reduce tension on the suture line (Fig. 1A). Guided frozen section examination of the bronchial resection margins was not systematically requested. A clamp was never applied to this stump to avoid damaging its blood supply.

View larger version (63K): [in this window] [in a new window]   Fig. 1. Bronchial suture technique used. (A) Section of the bronchial stump with mucosal flap. (B) Closure by running suture after application of the cartilage onto the mucosa.

Resection of the carena was associated with pneumonectomy in five cases of tumours of the main bronchus situated less than 10 mm from the carena. Following resection of the carena, anastomosis of the main bronchus to the trachea was performed with Prolene^® 3/0 in the cartilaginous zone and 4/0 in the mucosal zone. Usual reinforcement by adjacent mediastinal tissues or by a posterior pericardial free flap fixed by non-transfixing sutures was performed.

2.3. Postoperative management
The patient was usually extubated on the table after return to the dorsal supine position. Exsufflation of air was performed by direct punction of the chest, if the postoperative X-ray showed mediastinal deviation; air pressure in pneumonectomy space was not measured. This procedure did not change perioperative prophylactic antibiotherapy protocol. Stay in the intensive care unit was performed for the most debilitated patients or in the case of a difficult operation. The other patients, after spending several hours in the recovery ward, returned to their rooms.

Postoperative physiotherapy systematically was performed daily. Bronchoscopy was only done if BPF was suspected or/if an atelectasie appeared on the chest X-ray.

Prophylaxis of thromboembolic disease was systematically performed by elastic stocking on the lower limbs and by injections of calcium heparin or, more often, low molecular weight heparin. Regular surveillance of filling of the pneumonectomy cavity and the position of the mediastinum was performed by chest X-rays in the vertical position. The patient was discharged from the department after the 10th postoperative day.

2.4. Data collection and patient follow-up
The information necessary for the study was extracted from the operation reports and various letters concerning hospitalisations and outpatient visits. Follow-up was considered to be complete as the patient was systematically referred to the department for any early or late postoperative surgical complications.

2.5. Assessment criteria and statistical analysis
The main assessment criterion of reliability of the surgical technique described was the incidence of BPF, defined as any disruption, regardless of the size, situated on the bronchial stump suture line and visualised by endoscopic examination. Postoperative empyema (or pyothorax) without BPF demonstrated on endoscopy was excluded. The other assessment criteria were the usual criteria of morbidity and mortality associated with the surgical procedure.

Statistical analysis was performed with SAS software version 6.12, SAS Institute Inc. Continuous variables were expressed in terms of their mean accompanied by the standard deviation and range between parenthesises. Risk factors correlated with an increased incidence of BPF were investigated by univariate analysis; multivariate analysis was not performed due to the small number of cases of BPF. The analysis was performed according to the hypothesis of independence of the samples corresponding to each solution. A possible correlation between two qualitative variables was investigated by the Chi-square test or the Fisher exact test, when sample sizes were too small to satisfy the validity conditions of the Chi-square test. A statistical test was considered significant for P less than 5% (P=0.05).

	3. Results

Top Abstract 1. Introduction 2. Material and methods 3. Results 4. Discussion Appendix A. Statistical Analysis... References

 
3.1. Incidence and risk factors of BPF
Five BPF occurred in 208 patients surviving after the operation (one intraoperative death), i.e. a BPF rate of 2.4%. The mean time to development was 43.2±77.0 days PO (1–180 days) with four early BPF (80%) (before the 3rd month PO), including two very early BPF (before the 48th h PO) and only one (20%) late BPF (after the 3rd month PO). These five cases are described in Table 2. Two patients had no risk factors for BPF. Among these five BPF, four were on the left. The bronchial suture was covered in two cases, including the right pneumonectomy. The bronchial resection margins were not invaded in any of the five cases, but were very inflammatory in one case. The only two very early BPF were treated by reoperation. In these two cases a longitudinal tear located on the membranous part of the stump was viewed. A new manual suture, reinforced by pericardial flap was performed in these two cases. Unfortunately, one patient, who developed multiorgan failure rapidly died. The other three patients were conservatively managed by drainage with chest tube associated with antibiotic therapy. The drain was remained in situ for 2 weeks a least and no lavage was performed. One patient died 3 days after the onset of this treatment by violent pneumonia of remaining lung. On the whole three patients recovered and two died (40%).

3.2. Other results
Recovery of free tumour fragments after bronchial section was performed during the operation in six cases (2.9%); frozen section examination of the bronchial resection margins was requested in seven cases (3.3%).

The operative mortality (at 30 days) was 4.3% (nine patients) including one intraoperative death due to injury to the pulmonary artery invaded by a squamous cell carcinoma (stage IIIB) in a 77-year-old patient, three cases of pulmonary embolism, three cases of respiratory decompensation, and the two BPF already indicated.

Postoperative complications are shown in Table 3. The postoperative morbidity was 28.7 %, (60 patients with 71 complications).

	4. Discussion

Top Abstract 1. Introduction 2. Material and methods 3. Results 4. Discussion Appendix A. Statistical Analysis... References

 
4.1. Various bronchial stump closure techniques have been proposed in pneumonectomy
The main surgical procedures are defined by four technical modalities [8]: the suture line (transverse [3] versus longitudinal [4]), the suture technique (manual versus mechanical), the clamping technique (open stump technique versus closed stump technique) and cover or no cover of the stump (pleuralisation, flap or tissue adhesive).

Transverse suture [3], applying the cartilage onto the bronchial mucosa, appears preferable as it allows harmonious suture. It also allows creation of a mucosal flap according to the technical procedure described by Brewer [7], the procedure used in all patients of this series and in all patients operated on by our team. Naruke [9] used a combination of these two suture techniques in his bronchial stump closure technique. Manual suture can be performed by interrupted sutures [3,9–11]; but, we prefer a running suture which, despite its theoretically ischaemic nature, allows better distribution of tensions and a better watertight seal of the stump compared to interrupted sutures. The suture material used varies considerably from one author to another: absorbable [10,11] or nonabsorbable suture material [9,12], monofilament [10,12] or braided [9,11], we have opted for Polypropylene (Prolene^®) because of its excellent qualities.

Mechanical suture and manual suture on the clamp [12,13] are so-called ‘closed bronchus’ techniques. Their main advantage is to reduce contamination of the surgical field by bronchial secretions. Manual suture, recommended by most authors [3,9–11] including ourselves, has the advantage of being an ‘open bronchus’ technique, allowing inspection of the bronchial mucosa, aspiration of bronchial secretions, and, in some cases, recovery of tumour fragments released during section of the main bronchus on the clamp, as in six cases in our study. It also facilitates assessment of the length and quality of the bronchial stump while suturing.

The majority of authors [7,9,11,14] have recommended cover of the right bronchial stump, while the left stump naturally buries itself underneath the aorta. In our experience, we have covered 38.8% of our stumps by using exclusively natural materials (pleura, azygos vein, pericardium). Nevertheless, the development of four of the five BPF after left pneumonectomy indicates the need for systematic cover of the bronchial stump on either side.

4.2. Incidence and risk factors for BPF
Table 4 shows the incidence of BPF reported in the largest series of pneumonectomies; this incidence is reported in relation to the suture technique, the distribution between left and right pneumonectomies and the proportion of indications for infectious disease. Sarsam [10] did not observe any BPF in a series of 332 pneumonectomies using Jack's technique [17] with tracheal suture without a bronchial stump. Our BPF rate of 2.4% was among the lowest of the published series.

We just demonstrated the role of Neoadjuvant therapy in our study; this could be due to a lack of statistical power (probability of demonstrating a difference), due to the low incidence of BPF.

In conclusion, like Wright [11], we believe that manual closure of the bronchial stump after pneumonectomy is at least as good if not better than closure by stapling. Mechanical suture is certainly a simple and rapid technique [8,20], but we consider manual suture to be the technique of choice. It is a reliable technique, which can be used regardless of the quality of the bronchus and regardless of the disease; it is easily reproducible and can be taught to trainee surgeons [11,12]. Its low cost (10 times less expensive than mechanical suture) makes it a widely used universal technique.

	Acknowledgments

 
We heartily thank Dr C. Vergnes, from the Department of Medical Information of Montpellier University Hospital for his collaboration in statistical analysis of this study. We gratefully acknowledge the technical assistance of G. Vaire.

	Appendix A. Statistical Analysis of risk factors for BPF

Top Abstract 1. Introduction 2. Material and methods 3. Results 4. Discussion Appendix A. Statistical Analysis... References

 
Table 5.

	References

Top Abstract 1. Introduction 2. Material and methods 3. Results 4. Discussion Appendix A. Statistical Analysis... References

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4. Overholt R.J. General considerations pertaining to all resections. In: Overholt R.J., Langer L., eds. The technique of pulmonary resection. Springfield, IL: Charles C. Thomas, 1949:24-68.
5. Amosov N.M., Berezovsky K.K. Pulmonary resection with mechanical suture. J Thorac Cardiovasc Surg 1961;41:325-335.
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