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Eur J Cardiothorac Surg 2000;18:519-523
© 2000 Elsevier Science NL

Analysis of risk factors in bronchopleural fistula after pulmonary resection for primary lung cancer

Makoto Sonobe, Masatsugu Nakagawa, Masutaro Ichinose, Naoyuki Ikegami, Miyuki Nagasawa, Toru Shindo

Department of Thoracic Surgery, Tenri Hospital, Mishima-cho 200, Tenri City, Nara 632-8552, Japan

Received 11 February 2000; received in revised form 23 June 2000; accepted 18 July 2000.

Corresponding author. Tel.: +81-743-63-5611; fax: +81-743-62-5576
e-mail: mysonobe{at}d5.dion.ne.jp


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 
Objectives: Despite the advances in surgical technology, bronchopleural fistulas (BPFs) still occur and are often fatal. We studied the risk factors for BPF formation after lung cancer operation to clarify the indication of preventive bronchial stump coverage. In addition, the reliability of our methods of bronchial closure was evaluated. Methods: We reviewed 557 consecutive bronchial stumps, corresponding to 547 patients without any coverage in pulmonary resection for lung cancer between 1989 and 1998. According to nine variables, stumps that made dehiscence were compared with uneventful ones using contingency table analysis. The incidence of BPFs according to each method of bronchial closure was calculated. Results: BPFs developed in ten patients (1.8%). Compared with the lobar bronchus (LB), the main bronchus (MB; P<0.01; odds ratio, 23.0) and the intermediate bronchus (IB; P=0.03; odds ratio, 10.7) carried a high risk. Previous ipsilateral thoracotomy (P<0.01; odds ratio, 37.9) and preoperative chemotherapy and/or radiotherapy (P=0.02; odds ratio, 13.2) increased the risk. The incidence of BPFs with manual suture, stapling devices only, reinforcement suture at the distal side of staplers, or reinforcement suture at the proximal side of staplers was 1.8, 5.0, 1.9 and 1.0%, respectively. Conclusions: The main and intermediate bronchial stumps, and the stumps in cases with previous ipsilateral thoracotomy or receiving induction therapy are prone to BPFs. Preventive coverage should be considered for these stumps. Our methods for reinforcement of stapled stumps are thought to be reliable.

Key Words: Lung cancer • Surgery • Complication • Bronchopleural fistula


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 References
 
Recent advances in perioperative management, antibiotics and surgical materials, including mechanical staplers, have decreased the operative risk of pulmonary resection. However, bronchopleural fistula (BPF) can still occur in some instances, the occurrence often being lethal. Therefore, we studied the risk factors for BPF formation after lobectomy, bilobectomy or pneumonectomy for primary lung cancer in order to clarify the indication of preventive coverage of the bronchial stumps. In addition, we evaluated the reliability of our methods of bronchial closure.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 References
 
We reviewed the clinical and pathological data on 590 consecutive patients with primary lung cancer who underwent lobectomy, bilobectomy or pneumonectomy without any type of tracheal or bronchial plasty at our department between 1989 and 1998. Standard resection of the entire lobe or lung where the tumor existed and systematic hilar and ipsilateral mediastinal lymphnode dissection were performed where possible. In aged patients or patients with limited cardiopulmonary reserves, less extensive lymphnode sampling was performed. All patients received postoperative chest roentgenography to confirm the expansion of the residual lung. When the residual lung was not adequately expanded, the endotracheal tube was extubated after bronchial toilet with bronchofiberscopy. Perioperative prophylactic antibiotic therapy was routine in all patients.

The pathological T- and N-factors of the tumors were classified according to the International System for Staging Lung Cancer [1]. The location of the bronchial stump was classified by: main bronchus (MB); intermediate bronchus (IB); or lobar bronchus (LB). The lymphnode dissection was defined as ‘systematic dissection’ or ‘sampling’.

Historically, we have performed four methods of bronchial stump closure. In method A, the bronchial stump is manually sutured in the fashion of Sweet's method. In method B, the stump is closed with a surgical stapler only. In method C, the stump is closed with a surgical stapler and is reinforced by several simple interrupted stitches with absorbable sutures at intervals of 2–3 mm at the distal side of the stapler line (Fig. 1) , as Kaplan et al. [2] reported. In method D, the stump is closed with a surgical stapler and each edge of the stump is sutured with a horizontal mattress stitch using a pair of 7x3x0.5 mm pledgets made of absorbable polyglycolic acid felt (Medifit® felt, manufactured by JMS Ltd., Hiroshima, Japan), and several simple interrupted stitches at intervals of 2–3 mm are placed between the sides of the stump (Fig. 2a,b) . This is a modified method reported by Sato and co-workers [3]. From 1989 to 1991, method A was mainly employed and method B was occasionally used. Method C was applied during 1991–1995. Since 1995, we have mainly used method D. After 1991, method A was used in cases with an insufficient margin of the bronchial stump. The principal surgical stapler used was a Premium Multifire TA 30–4.8 stapler® manufactured by United States Surgical Company (Norwalk, CT). In each method, an intraoperative pressure-proof test was performed with a pressure of 30 cmH2O. In several cases, we detected small air leakages, for which horizontal mattress stitches were added using a pair of pledgets.



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  		Fig. 1. Diagram of method C for bronchial closure. After the bronchus is closed with a stapler and transected distal to the stapler line, simple interrupted stitches at intervals of 2–3 mm are placed between both ends just distal to the stapler line.

 


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  		Fig. 2. Diagram of method D for bronchial closure. (a) After the bronchus is closed with a stapler and transected distal to the stapler line, a horizontal mattress stitch with a pair of pledgets is placed on each end just proximal to the stapler line. (b) Then, simple interrupted stitches at intervals of 2–3 mm are placed between both ends just proximal to the stapler line.

 
Coverage of bronchial stumps had been performed preferentially before 1994, and has been routinely performed since 1995 for cases with concurrent pulmonary infection, preoperative chemotherapy or radiotherapy, or impaired renal function. The 44 stumps in 43 patients that received preventive coverage did not develop BPF and were excluded from this study.

The factors in relation to BPF were studied on patients whose bronchial stumps did not receive any type of coverage. BPF was diagnosed from the clinical course, chest X-ray film or chest drainage, and was confirmed by bronchography or bronchofiberscopy examination. Variables included in the analysis were location of bronchial stumps, history of previous ipsilateral thoracotomy, preoperative chemotherapy and/or radiotherapy, types of bronchial closure methods described above, T-factor, N-factor, degree of lymphnode dissection, presence or absence of residual malignant cells at the stump, and association with diabetes mellitus. Three factors that were specific to the stump, i.e. location of the bronchial stumps, types of bronchial closure methods described above, and the presence or absence of residual malignant cells at the stump, were analyzed by the stumps and not by patients. Differences in binary and ordinal variables were tested with the Chi-square test or Fisher's exact test. The results were considered significant when the P value was less than 0.05.


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 References
 
This study included 547 patients, consisting of 174 females and 373 males. Their ages ranged from 31 to 83 years, with an average of 65.3 years. The tumor histology and the mode of pulmonary resection are shown in Table 1. Ten patients had two bronchial stumps after bilobectomy, and the number of bronchial stumps included was 557. Forty patients underwent pneumonectomy, including five cases of completion pneumonectomy. Forty-one patients received bilobectomy. Four hundred and sixty-six patients underwent lobectomy, including one left upper lobectomy after left explanatory thoracotomy, one right middle lobectomy after right upper lobectomy, one right middle lobectomy after right lower lobectomy, and one right lower lobectomy after thoracic esophagectomy. Twelve patients received induction therapy. Nine of them received chemotherapy, two received irradiation and one received concurrent chemo-radiotherapy.


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  		Table 1. Tumor histology and operation procedures

 
BPFs occurred in ten patients (1.8%). Five BPFs occurred in the MB, with an incidence of 12.5%. Of these five cases, three BPFs developed after right pneumonectomy, including one right completion pneumonectomy, and two BPFs developed after left pneumonectomy, including one left completion pneumonectomy. Two BPFs were found in the IB, with an incidence of 6.3%. One of them occurred after a right middle lobectomy after a previous right lower lobectomy. Three BPFs were found in the LB, with an incidence of 0.6%; all of them occurred in left upper bronchial stumps. In the ten cases of BPF, four female and six male patients were included. Their ages ranged from 52 to 79 years, with an average of 67.0 years. None of them ventilated prior the to development of BPFs and their stumps showed no leakage in the intraoperative pressure-proof test. The onset of ten BPFs ranged from 5 to 481 days after surgery, and five of them developed within 20 days after surgery. Two patients died of BPF-related complications (mortality, 20%). Four patients were treated by wrapping the bronchial stumps with the pedicled greater omental flap. Two patients with BPF of the left upper bronchus were treated by wrapping with the pedicled left pectoralis major muscle. One patient with BPF of the left MB underwent resection of the broken stump and re-suturing through the transsternal approach. One patient without infection was observed with no surgical interventions because of her poor general condition.

The incidence of BPF formation with method C (1.9%) was as low as that with method A (1.8%). It was lowest with method D (1.0%), although no statistical significance was observed (Tables 2 and 3). Besides, in methods A, B and C, BPFs developed frequently in proximal larger bronchi, while in method D, BPFs occurred only in the left upper bronchi (Table 2).


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  		Table 2. Location of bronchial stump according to the method for bronchial closurea

 

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  		Table 3. Analysis of risk factors for BPFs

 
The statistical analyses on the investigated factors are presented in Table 3. The incidence of BPFs was higher in the MB (P<0.01; odds ratio, 23.0) and IB (P=0.03; odds ratio, 10.7) compared with the LB. Cases with previous ipsilateral thoracotomies had a significantly higher incidence of BPFs (P<0.01; odds ratio, 37.9). Cases with preoperative chemotherapy and/or radiotherapy also had a statistically higher incidence of BPFs (P=0.02; odds ratio, 13.2). The T-factor, N-factor, extent of lymph node dissection, residual malignant cells in the bronchial stumps, and association of diabetes mellitus did not influence the incidence of the development of BPFs.


   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
References
 
In lung cancer surgery, BPF is caused by incomplete bronchial closure, impediment of wound healing at the stump, or destruction of the stump by residual carcinomatous tissue. In spite of a low rate of about 3% or less [2,4–9], BPF is still a critical complication with a mortality of 12.5–71.2% [2,4,6,7,10–16]. Besides, BPF in pulmonary resection with tracheo-bronchial plasty and/or induction chemo-radiotherapy for advanced stage lung cancer is an important problem [17,18]. Therefore, we analyzed the risk factors for BPF formation in our cases of pulmonary resection for primary lung cancer, and evaluated our methods of bronchial closure that were performed over the last 10 years.

Regarding the location of bronchial stumps, the rate of BPF formation in the MB and IB was significantly higher than that in the LB, as reported [5–8,12,14]. Bronchial stumps in the MB and IB are thought to receive a lower blood supply from the surrounding mediastinal tissue and pulmonary circulation compared with those in the LB, because these stumps usually face the intrathoracic dead space, especially in the right MB [3,12]. This condition may lead to a higher incidence of BPFs. Therefore, some kind of preventive coverage should be considered. We have routinely performed wrapping of the stump in the right MB using a pedicled intercostal muscle since 1997, and no BPF has been observed. For the left MB, we have attempted to cut the bronchus near the carina so that the stump could be retracted and buried in the mediastinal tissue.

Our study revealed that previous ipsilateral thoracotomy and preoperative chemotherapy and/or radiotherapy were risk factors for BPF, as reported [17–20]. Under the deteriorated condition of patients, the vascularity to the bronchial stump is thought to be poor. In addition, chemotherapy and radiotherapy can directly interfere with the bronchial healing. Considering other reports about preventive coverage [19,21,22], after 1995, we routinely performed bronchial stump coverage using a pedicled intercostal muscle flap in cases with previous ipsilateral thoracotomy or induction therapy without encountering BPF formation to date. Coverage of the stumps in these cases is recommended for safe pulmonary resection.

We were not able to show that T-factor, N-factor, extent of lymphnode dissection, residual carcinomatous tissue in the stump, or diabetes mellitus were significant risk factors for BPF. These factors can damage the peribronchial blood circulation and potentially contribute to BPF formation [4,6,10–12]. Protective and careful handling of the bronchial stump during operation and perioperative management of patients may be important to reduce the disadvantages of these factors.

Our result of BPF formation with method A (1.8%) is not inferior to the reported series of hand-sewn closures, ranging from 0 to 17.6% [3,5,8,11–13,23]. The coverage of stumps in all cases might further reduce the BPF formation, but it seems an extreme procedure considering the incidence of BPF in our series. Stapling devices have been matched for manual suture in the rate of BPF formation in the large-sized reported series (0.8–5.4% in the large series [3,6,10,13]), and they have the advantages of uniformity, rapid closing and protection of the intrathoracic space from contamination with the transection of the bronchus after closing its proximal side. Thus, we have attempted to further reduce the incidence of BPF with stapling devices.

In our data, method C (reinforcement of the distal side) has provided an incidence of BPF (1.9%) as low as that of method A. However, three BPFs were found at the side end of stumps. Therefore, we designed method D to reinforce both sides of the stumps, adhere the bronchial mucosa closely over a larger area and cover the latent cutting of the bronchial wall by staples. With the introduction of method D, the incidence of BPF remained at only 1.0%, and Uchida and Wada [9] reported a similar reinforcement method at the proximal side with a low incidence of BPF (0.7%). Method D has potential to be a safer method for bronchial closure.

However, two BPFs developed in left upper bronchial stumps closed with method D. The re-operation for BPF revealed a tear of the bronchial wall at the staple line by the strong tension of bending bronchial cartilages. Takizawa et al. [24] reported a high rate of pressure-proof test failure after closing the left upper bronchus with stapling devices. This may suggest that the bronchial cartilages of the left upper bronchus induce structurally high tension with closure. The direction of stapling should be noted in order to avoid bending the bronchial cartilage unnecessarily, and the reinforcement method remains to be investigated for prevention of BPFs at the left upper bronchial stumps.

In closing, the stumps of the MB and IB had a higher risk of BPFs. Cases with previous ipsilateral thoracotomy or induction therapy were also at high risk of BPFs. Coverage of stumps for these cases should be considered. With method D for bronchial closure, the incidence of BPF formation was satisfactorily low.


   Acknowledgments
 
No traders or manufacturers supported this study.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 References
 

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