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Ann Thorac Surg 2001;72:1662-1667
© 2001 The Society of Thoracic Surgeons
a Department of Thoracic Surgery, Hospital Universitario Reina Sofía, Córdoba, Spain
Accepted for publication July 16, 2001.
* Address reprint requests to Dr Algar, Servicio de Cirugía Torácica, Hospital Universitario Reina Sofía, Avda Menéndez Pidal s/n, 14004 Córdoba, Spain
e-mail: med015662{at}nacom.es
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Abstract |
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Methods. We reviewed 242 consecutive patients undergoing pneumonectomy for lung cancer. The bronchial stump was covered with autologous tissue in 178 patients (74%). Perioperative data were recorded to identify risk factors of BPF by univariate and multivariate analyses.
Results. Overall morbidity and mortality rates were 59% and 5.4%, respectively. The incidence of BPF was 5.4%. By univariate analysis, patients with chronic obstructive pulmonary disease (COPD; p = 0.017), hyperglycemia (p = 0.003), hypoalbuminemia (p = 0.017), previous steroid therapy (p < 0.001), poor predicted postpneumonectomy forced expiratory volume in 1 second (FEV1; p = 0.012), long bronchial stumps (p < 0.001), and mechanical ventilation (p = 0.015), were related with higher risk of BPF. In the multiple logistic regression model, the independent risk factors of BPF were the bronchial stump coverage and length, side of pneumonectomy, predicted postpneumonectomy FEV1, COPD, and mechanical ventilation.
Conclusions. Bronchial stump coverage is highly recommended in all cases to minimize the risks of BPF. A shorter length of the bronchial stump and early extubation may prevent the development of BPF. Careful attention must be paid to those patients with COPD and poor predicted postpneumonectomy FEV1.
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Introduction |
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Recently, it has been emphasized that the bronchial stump coverage with autologous tissue decreases the incidence of BPF [6], however, the actual role of this procedure in preventing the BPF development has not been clearly defined in multivariate analyses.
The objectives of this study were to assess the incidence of early (30 days) postpneumonectomy BPF in a 12-year single center experience; to analyze different techniques of bronchial closure and coverage; and to determine risk factors for BPF development based on a multivariate analysis, with special focus on the impact of bronchial stump coverage in preventing this complication.
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Material and methods |
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Antibiotic and thromboembolic prophylaxis were used routinely and most patients started pulmonary rehabilitation exercises before the operation. Thirty-four individuals (14%) underwent mediastinal exploration (mediastinoscopy or mediastinotomy) before the lung resection because the computed tomography scan revealed the presence of nodal disease. Thirty-two individuals (13%) underwent neoadjuvant therapy with chemotherapy or radiation therapy for biopsy-proved N2 disease or T3.
Surgical treatment
All patients were operated on by the same surgical team through a standard posterolateral thoracotomy and air exclusion of the lung to be resected. The bronchial closure was performed with staplers (Ethicon, Endo-Surgery, Inc, Cincinnati, OH; and Autosuture USSC, Norwalk, CT) in 233 patients (96%) and manually with interrupted 4-0 sutures of polypropylene (Prolene, Ethicon, Somerville, NJ) in 9 (4%) because of the tumor’s proximity to the carina. In all cases, the bronchial closure was performed according to the Sweet technique [9]. The bronchial stump was covered with autologous tissue in 178 cases (74%)—in 88% of right pneumonectomies and 64% of left pneumonectomies. This coverage was performed more frequently in those cases more likely to develop a BPF (right pneumonectomies, older patients, those who had previously taken immunosuppressive drugs); however, the final decision of whether to cover the bronchus was made by the operating surgeon. Several tissues were used to cover the bronchial stump: intercostal muscle in 80 cases, mediastinal fat pad in 64, parietal pleura in 15, phrenic pedicle in 10, acygos vein in 6, and other tissues in 3. In all cases, a systematic lymph node resection was performed.
Extended resections were needed in 46 tumors involving the chest wall (4.5%), parietal pleura (2.5%), pericardium (4.5%), diaphragm (0.4%), and other mediastinal structures (7%). In 3 patients (1.2%) a completion pneumonectomy was performed.
Staging
Patients were staged postoperatively according to the TNM staging system [10]. Ninety patients were in stage I, 65 in stage II, 70 in stage IIIa, and 11 in IIIb. In 6 patients receiving neoadjuvant therapy, no viable tumor cells were found after pulmonary resection; therefore, a surgical staging was not possible in such cases.
Postoperative management
An early extubation was achieved after pneumonectomy in 96 patients (39.7%), and 146 cases (60.3%) were under mechanical ventilation for several hours after the operation. Bronchoscopies were done if BPF was suspected or mucus retention with atelectasis of the remaining lung was noted. Late fistulas secondary to postpneumonectomy empyema were excluded from the analysis.
Bronchial stump length was estimated by measuring the bronchial length in a chest roentgenogram from the main carina to the stapled suture line. In manually sutured bronchi, the airway transsection was performed at the level of the main carina. The mean bronchial stump length in stapled bronchi was 10.9 ± 5.4 mm (0 to 30 mm).
Data collection and analysis
Several preoperative, intraoperative, and postoperative variables were recorded retrospectively including general demographic data, patient comorbidity, functional status, tumor characteristics and stage, neoadjuvant therapy, type of surgical procedure, postoperative complications, and mortality within 30 days after pneumonectomy. In the univariate analysis, Pearson’s 
2 test and Fisher’s exact test were used to assess differences between discrete variables, and unpaired Student’s t test was used to compare means between two quantitative variables. Data are presented as mean ± standard deviation. Differences were considered significant with p less than 0.05.
Those variables with p less than 0.25 in the univariate analysis were included in the multivariate analysis. A forward and backward stepwise logistic regression analysis was used to determine the effect of independent risk factors for BPF development. The final model included factors that remained significant with a p value less than 0.10. The statistical analysis was performed with SPSS 7.5 for Windows software system (SPSS Inc, Chicago, IL).
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Results |
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A BPF developed within 1 patient who had left pneumonectomy with the bronchus stapled within 24 hours postoperatively and required resuturing of the bronchial stump with an additional intercostal pedicled flap. The rest of the BPF patients were treated with the insertion of a pleural drainage alone (1 patient), or followed by an open window thoracostomy (11 patients).
Univariate analysis
Eleven preoperative variables and eight intraoperative variables were considered for the univariate analysis. The results are provided in Table 3. Preoperative factors associated with higher risk of BPF development were patients with chronic obstructive pulmonary disease (COPD) (p = 0.017), hyperglycemia (p = 0.003), hypoalbuminemia (p = 0.017), preoperative steroid therapy (p < 0.001), and low predicted postpneumonectomy FEV1 (p = 0.012). Intraoperative variables associated with BPF development were bronchial stump length (p < 0.001) and need for postoperative mechanical ventilation (p = 0.015). Despite the higher incidence of BPF in right pneumonectomies (8.6% versus 3.4%), sutured bronchi (11.1% versus 5.2%), and those bronchial stumps without coverage (9.4% versus 3.9%), these differences were not significant. However, when those BPF appearing within 10 postoperative days were considered, we observed only 2 BPF cases of 178 pneumonectomies with bronchial stump coverage (1.1%) (p = 0.018).
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Comment |
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In our series, the incidence of BPF was within the range of that reported in other large series. Thirteen of 242 patients undergoing pneumonectomy developed BPF (5.4%) with an associated mortality rate of 30.8% in this subgroup of patients.
Several factors have been reported to be associated with the development of BPF, but few investigations have assessed the actual impact of such factors in a multivariate analysis. Some reports [1, 12] suggest that pneumonectomy, residual tumor in the bronchial stump, preoperative radiation therapy, diabetes mellitus, and mechanical ventilation are the major factors associated with the development of BPF. Also, the preoperative status of the patient may play a role. Thus, it is well known the relationship between age, diabetes mellitus, malnutrition and prolonged steroid therapy and the risk of BPF [1, 3, 12]. In our experience, the age of the patient has not been related to BPF development, but those patients with hyperglycemia, hypoalbuminemia, or those undergoing prolonged preoperative steroid therapy had higher risk of BPF. Furthermore, other factors such as COPD and the poor predicted postpneumonectomy FEV1 have also been related to the incidence of BPF.
The influence of the neoadjuvant therapy is controversial. Although previous reports have demonstrated a higher incidence of BPF in patients receiving preoperative chemotherapy or radiotherapy [1, 4, 13], other investigators did not find such a relationship [5, 12]. Probably, the coverage of the bronchial stump performed in these latter reports might have contributed to the low incidence of BPF in those series [5, 12]. In our experience, the neoadjuvant therapy with chemotherapy and radiation therapy did not increase the risk of BPF, but also the bronchial stump was covered in all of these cases.
When we analyzed the role of preoperative variables in the development of BPF by a multivariate analysis, only the coexistence of COPD and the estimated FEV1 postpneumonectomy proved to be independent risk factors. It is possible that the chronic inflammation of the bronchial mucosa in these patients might have contributed to the impaired healing after the lung resection.
It seems logical that the development of BPF is associated with some intraoperative factors. Undoubtedly the risk of BPF is higher after pneumonectomy than after lesser pulmonary resections [1]. Most authors, including us, have found a higher incidence of BPF after right than after left pneumonectomy [1, 4, 5, 14], probably because of the better protection provided by the mediastinal tissue for the left bronchial stump and the more devascularization produced around the right bronchial stump during lymph node dissection, because this bronchus more commonly is irrigated by only one bronchial artery. We have not observed a relationship between the type of pneumonectomy (standard, extended, or completion pneumonectomy) and the incidence of BPF; however, other authors have reported higher risks of BPF in those cases of completion pneumonectomy [1, 4, 15].
The surgical technique of bronchial closure has been studied extensively. The stapled and sutured techniques have their supporters and detractors, but none of these techniques has a proven superiority in reducing the incidence of BPF. Around a 4% rate of BPF has been reported for both the hand-suture technique [1, 3, 5, 13, 16] and mechanical stapling [4, 16, 17]. We prefer the stapled technique for the bronchial closure because of its simplicity and safety. Although we observed a higher incidence of BPF in manually sutured bronchi than in stapled bronchi, the small number of sutured bronchi did not allow us to draw firm conclusions about the benefits of the stapled technique.
Some factors such as the bronchial stump length and its coverage with autologous tissue have been suggested as factors influencing the BPF onset. It is well known that the higher incidence of BPF in longer bronchial stumps is a likely consequence of mucus accumulation leading to a higher risk of infection and impaired healing of the bronchus. Nevertheless, few reports have analyzed this issue consistently. We observed a higher rate of BPF in longer bronchial stumps, being an independent risk factor for BPF development.
The benefits of the coverage of the bronchial stump in preventing the BPF is controversial. Most authors support the bronchial stump coverage for right pneumonectomies, because the left bronchial stump remains more protected within the mediastinal structures [1, 18]. However, other investigations advocate the need of similar coverage for left pneumonectomies as well, mainly in cases of patients at potential risk [5, 6, 13]. In our series, most of patients underwent bronchial stump coverage with an incidence of BPF of 3.9% as opposed to 9.4% in those patients without coverage. No previous reports have analyzed consistently the impact of the bronchial coverage in the development of BPF comparing left and right pneumonectomies. In our study, the influence of the bronchial stump coverage resulted significant in the multivariate analysis, whereas in the univariate analysis nonsignificant p values were obtained. Probably, this discrepancy is related to the relationship of the side of coverage. When the influence of the side of pneumonectomy was eliminated in the multivariate analysis, the actual role of the bronchial coverage in preventing the BPF was demonstrated irrespective of the side of pneumonectomy. In the univariate analysis, the influence of the bronchial coverage was biased by the side of operation and therefore, the results were not significant. The results of the multivariate analysis in the present series suggest that bronchial stump coverage is advisable in all cases, irrespective of the side of pneumonectomy.
A great variety of tissues have been used to cover the bronchial stump, but all authors agree with the need for tissue vascularized enough to promote an early healing of the bronchus. For this purpose, the parietal pleura, intercostal muscle, pericardium, phrenic pedicle, and other adjacent tissues have been used [5, 6, 19]. In our experience, the intercostal muscle has been used the most frequently with excellent results (2 BPF of 80 stumps covered; 2.5%), similar to those reported by other authors [6], whereas in 64 patients the bronchial stump was covered with mediastinal fat pad and a BPF appeared in 4.7% of cases.
The need for postoperative mechanical ventilation has been reported to be a risk factor for BPF development [5, 12]; however, some investigations [13] did not support this hypothesis. Wright and coworkers [5] in a series of 256 pneumonectomies, observed a BPF incidence of 19.3% in those cases requiring postoperative mechanical ventilation. Furthermore, De Perrot and coworkers [12] reported a high rate of BPF (43%) in pneumonectomies under prolonged mechanical ventilation. Our results agree with the results in these investigations, with a higher incidence of BPF in those patients undergoing postoperative mechanical ventilation. This factor was found to be an independent predictor of BPF development in the multivariate analysis, as demonstrated previously by other investigations [12]. Based on these results, the early extubation of these patients may be advisable to prevent early BPF onset.
In conclusion, because BPF is a severe complication after pneumonectomy and is associated with high rates of mortality, reducing the potential risks for BPF development is of paramount importance. Based on previous reports and the present series, careful attention must be paid to those patients with significant risk factors (COPD, poor functional status, hyperglycemia, previous steroid therapy, and hypoalbuminemia). Bronchial stump coverage with autologous tissue and the early extubation of the patient are factors that were found to prevent the development of an early postpneumonectomy BPF.
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