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Ann Thorac Surg 1997;64:954-957
© 1997 The Society of Thoracic Surgeons

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Original Article: General Thoracic

Transsternal Closure of Bronchopleural Fistula After Pneumonectomy

Departments of Thoracic Surgery and Pulmonology, St Antonius Hospital, Nieuwegein, the Netherlands

	Abstract

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Background. Bronchopeural fistula after pneumonectomy, with associated empyema, has no standard therapy. The transsternal, transpericardial approach was used in all patients presenting with a large fistula.

Methods. From 1974 through 1995, 55 patients underwent transsternal, transpericardial closure of a bronchopleural fistula. Mean age was 62.7 years (range, 33 to 78 years). Malignant disease had been the indication for pneumonectomy in 50 patients and benign lesions in 5 patients. The fistula was right-sided in 41 patients (74.5%), and the bronchial stump was less than 2 cm in 25 (45.5%). Treatment of the concomitant empyema was by closed drainage in 2 patients, by repeated needle aspiration in 17, and by open thoracostomy in 36 patients. Reamputation and closure of the stump was possible in 51 patients; in 4 a primary carinal resection was done.

Results. Three patients died within 30 days after operation (5.4%, 70% confidence interval 2.4%–10.7%). Ten patients died late during hospitalization, total hospital mortality, 23.6% (70% confidence interval 17.3% to 31.0%). Recurrent fistula symptoms were caused by a large recurrency in 6 patients (all died), by a small one in 7 (one death due to pulmonary embolism). Mean duration of hospital stay was 56 days (range, 2 to 174 days). At follow-up of 42 patients, there were no recurrent fistulas. All patients with benign lesions are alive and well. Of 37 cancer patients, 29 died, more than half due to malignancy. Risk factors for death included recurrent fistula, short interval between pneumonectomy and onset of fistula, and closing technique. Risk factors for recurrent fistula were a short bronchial stump and the nonuse of an open thoracostomy.

Conclusions. Long-term results of transsternal closure are good, but hospital mortality is high. The present treatment of patients with large postpneumonectomy bronchopleural fistula includes early open thoracostomy, improvement of nutritional status, transsternal closure using resorbable sutures, and closure of the pleural space 3 weeks later.

	Introduction

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
See also page 958

and page 959.

The development of a bronchopleural fistula after pneumonectomy is a devastating complication. When present for a few days, the associated empyema will further hamper simple treatment. Although treatment of the empyema may result in closure of a small fistula [1], in cases of larger fistulas, a more direct approach to the airway is necessary. Nonsurgical techniques, such as the application of fibrin glue, are only useful in small fistulas [2]. To close a wide open bronchial stump, a direct approach is mandatory. The adjuvant use of omental or myocutaneous flaps has been shown to be extremely helpful [1, 3].

For direct closure, the bronchus may be approached through the midline, through the homolateral pleural space, or, in cases of left-sided fistula, through the contralateral pleura. Recently, a video-assisted approach through the mediastinum was described [4].

The transpericardial approach was developed by Padhi and Lynn [5], using an anterior thoracotomy, and by Abruzzini [6] using median sternotomy. Particularly, the good results reported by Perelman and Ambatjello [7] have made us adopt this technique for the last 23 years. We report our experience since 1974 [8] with 55 patients.

	Patients and Methods

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Patients
From January 1974 through December 1995, 55 patients underwent transsternal, transpericardial closure of a postpneumonectomy bronchopleural fistula. Forty-nine patients had had their primary operation elsewhere, 6 patients in our own institution.

Mean age was 62.7 years (range, 33 to 78 years); there were 54 men and 1 woman (1.8%). Follow-up by personal contact closed January 1, 1996. Follow-up was complete for all 42 discharged patients for a mean of 54 months (range, 4.1 to 259 months). Four time frames were arbitrarily chosen: 1974 to 1979 (n = 4), 1980 to 1984 (n = 18), 1985 to 1990 (n = 19), and 1991 to 1995 (n = 14).

Data Analysis
Data from all consecutive patients who underwent transsternal transpericardial closure of bronchopleural fistula were reviewed retrospectively. Quantitative data are represented as mean ± standard deviation. Univariate comparisons between groups were calculated by the unpaired test, Fisher's exact test, ² test, or the one-way or two-way analysis of variance, as appropriate. All probabilities are two-tailed. Kaplan Meyer survival curves were used for analysis of survival times. Relative risks for factors associated with death were obtained by use of the Cox proportional hazards model. Odds ratios for factors associated with the recurrence of bronchopleural fistula were obtained using multivariate logistic regression models. Precision was indicated by means of the 95% confidence interval (CI).

Preoperative Treatment
The empyema—present in all patients—was treated by closed drainage in 2 patients (3.6%), by repeated needle aspiration in 17 (31%), or by open thoracostomy in 36 patients (65.4%). When an open thoracostomy was made, the presently preferred method, the cavity was packed with gauze pads soaked in either povidone–iodine solution or chlorhexidine daily.

Operative Technique
Either a double-lumen endotracheal tube or a long endobronchial tube allowing selective ventilation was used. After median sternotomy, the pericardium was opened. In case of a right-sided fistula, first, the residual intrapericardial right pulmonary artery was transected dorsal to the ascending aorta, facilitating exposure of the main carina. The pericardium was opened dorsally, and the main carina exposed, paying attention to the esophagus and the recurrent laryngeal nerve. When feasible, the affected bronchus was dissected completely. If dense adhesions precluded complete exposure, the bronchus was gradually transsected from anterior to posterior. After transection, the bronchus was closed. The stump was covered by a pericardial or thymic fat pad. The omentum was used in 6 patients. The residual stump was removed or treated by extensive cautery to destroy the mucosa.

If an open thoracostomy was present, it was closed 2 to 3 weeks later. Granulation tissue between skin and pleura was excised. The remnants of latissimus dorsi are mobilized, and subsequently the various layers were closed using continuous resorbable sutures.

	Results

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
The fistula was on the right side in 41 patients (74.5%). In 14 patients (25.5%) the fistula followed a completion pneumonectomy. The original pathology was malignant in 50 patients (90.9%), benign in 5 (aspergillosis in 3, tuberculosis in 1, and posttraumatic in 1). Mean age of patients with malignant pathology was 64 years (range, 43 to 78 years), of patients with benign lesions 48 years (range, 33 to 64 years) (p = 0.02).

Histologic examination revealed squamous cell carcinoma in 36 patients (72%), adenocarcinoma in 10 (20%), and other in 4 patients (8%). In 2 patients resection had been incomplete. Data for TNM classification and staging were available in 46 patients (92%): stage I, 25 patients (54%); stage II, 15 (33%); stage IIIa, 6 (13%). Three patients had received postoperative radiotherapy (4,000 cGy or more).

The interval between pneumonectomy and fistula occurrence was 1 week or less in 4 patients, 1 week to 1 month in 27 (1 with a benign lesion), between 1 and 6 months in 12, and more than 6 months in 12 patients (4 with benign lesions) (the interval was defined as short if less than 1 month). Mean period of time elapsing between fistula symptoms and midsternal closure was 3.7 months, for malignant pathology 2.4 months, and for benign lesions 3.9 years (p < 0.01).

In 46 patients the technique of bronchial closure was known: by sutures in 24 and by stapler in 22. Nutritional status of the patients was graded as good in 17 (31%) and poor in 38 (69%). Hyperalimentation was given to 32 patients: before 1985, to 7 (37%), after 1985 to 25 (69%). At bronchoscopy, the residual main bronchus was 2 cm or more in 30 patients (54.5%), less than 2 cm in 25 (45.5%), defined as a "short" stump. There was no relationship between side (right or left) and stump length. In patients with benign lesions, it was short in 20%, whereas in malignant cases it was short in 48% of the patients (not significant).

Pretreatment
Before 1985, 14 patients (70%) were treated by repeated needle aspiration (after 1985, n = 3), whereas from 1985 on, 28 patients (93%) were treated by open thoracostomy (p = 0.001). Before 1985, 8 patients were treated by open thoracostomy. Two patients were treated by repeated needle aspiration.

Transsternal closure followed various attempts at fistula closure in 15 patients, including the use of histo acryl in 1 patient. The operation was done electively in 52 patients, emergently in 3, all due to bleeding from the pulmonary artery stump. It was a primary sternotomy in 50 patients. It was defined as "complex" in 5; in 4, it followed previous bypass grafting, whereas in 1 patient it was combined with coronary artery revascularization.

Reamputation and bronchial closure was performed in 51 patients, in 44 (86.3%) the bronchus was closed by suture, in 7 (13.7%) a stapler was used. In 4, a primary carinal resection was done. Indications for carinal resection included dense adhesions in 3 patients and a positive re-resection margin in 1.

Mortality
Three patients died within 30 days after operation (5.4%, 70% CI 2.4–10.7). In 1 patient, operated on emergently, severe neurologic complications developed due to low blood pressure before and during operation, and he died (he also had a recurrent fistula). Another patient sustained intraoperative bleeding from the pulmonary artery, which was controlled using extracorporeal circulation. Two days after operation, while he was breathing spontaneously, a pneumothorax developed and he arrested. Although cardiopulmonary resuscitation was successful, the patient was found to have a flat electroencephalogram and died. A recurrent fistula developed 7 days after operation, in the third patient probably related to nodal metastases in the carina, and he died in sepsis.

Ten patients died late during hospitalization: 4 of complications related to recurrent fistula, 1 of arrest, 1 of pulmonary embolism, 1 in sepsis (but without fistula), 2 of pneumonia, and 1 patient, 3 months after operation, of hepatic metastases.

Two patients (of 4) with carinal resection died in the hospital; 2 are long-term survivors. Total hospital mortality was 23.6% (70% confidence interval, 17.3–31.0). There was no mortality in benign cases.

Morbidity
Intraoperative complications consisted of bleeding from the pulmonary artery in 3 patients (5.4%). One of them died, as mentioned above. In two others, the bleeding could be controlled without special auxiliary measures.

Postoperative complications included bleeding in the pleural space in 2 patients (3.6%), respiratory insufficiency in 14 (25.5), necessitating prolonged mechanical ventilation in 5 (9.1%). In 2 patients a temporary tracheostomy was needed. Two patients had paroxysmal atrial fibrillation. Recurrent fistula symptoms were found in 13 patients: in 6 (10.9%), caused by a large fistula (all died), in 7 it was caused by a small fistula (12.7%) (1 patient died due to a pulmonary embolism).

Duration of intensive care unit stay was 0 to 3 days for 29 patients (52.7%), 4 to 7 days in 15 (27.3%), and 8 days or longer for 11 patients (20%). Mean duration of hospital stay after midsternal closure for all patients was 56 days (range, 2 to 174 days)—for benign lesions 40 days (12 to 68 days), for malignant lesions 58 days (2 to 174 days) (p = not significant).

Follow-up
Estimated mean survival of the 55 patients was 4.0 years (±0.6 years). All 5 patients with benign lesions are alive and well, with a mean follow-up of 7.8 years (range, 0.1 to 21.6 years). Estimated mean survival of patients with malignant lesions (n = 50), inclusive of hospital death, was 3.5 years (±0.6 years), of patients with stage I, 3.9 years (±0.7 months), stage II, 2.4 years (±1.0 year), and stage IIIa, 2.1 years (±1.0 year) (not significant). There were no fistula recurrences; 2 patients had a late recurrent empyema, which in both was treated succesfully by nonsurgical therapy. Causes of late death included recurrent malignancy in 15 patients, cardiac in 5, pneumonia in 2, cachexia in 2, and unknown in 5 patients. Causes of late death differed significantly from causes of hospital death (p = 0.02). Multivariate analysis of death in all patients (Table 1) (including localization, age, pathology, stage, interval, stump length, pretreatment, nutritional status, hyperalimentation, recurrent fistula, recurrent cancer, primary operation, closure technique) showed recurrent fistula, interval (ie, a short interval), and closure technique (by stapler) to be incremental risk factors for death. Logistic regression analysis of recurrent fistula (Table 2) showed a short bronchial stump and pretreatment (ie, the nonuse of an open thoracostomy) to be incremental risk factors for recurrency. Considering only the subset of patients with malignancy (n = 50), in addition to stump length and pretreatment, year of operation (ie, before 1985) was found to be associated with recurrent fistula (p = 0.002). Logistic regression analysis of recurrent fistula in this subset showed a short stump to be an incremental risk factor for recurrency. The use of the omentum could not be correlated to outcome, probably due to small numbers.

	Comment

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

The influence of the original operation on final outcome is striking: we found a significant difference not only in in-hospital events, but also in long-term survival, between patients operated on for benign or malignant lesions. Late survival in cancer patients was mostly related to the malignant process. No mortality was encountered in patients presenting with benign disease.

As with many studies extending over a longer period of time, year of operation was associated with outcome. This correlated with pretreatment. From 1985, we almost exclusively used the Clagett and Geraci procedure [14] for the initial treatment of the empyema. We favor open thoracostomy to drain the infected pleural space, although it requires a second operation to close the chest. Rather simultaneously, we introduced hyperalimentation for patients in poor nutritional status, but this change in therapeutic strategy did not make a statistically significant difference. Multivariate and univariate analyses both showed pretreatment to be an incremental risk factor for recurrent fistula, the most important determinant for death. The value of the Clagett procedure confirms the experience of others [9]. Death was found to be related to closure technique; 6 of 7 patients who had had their bronchus stapled died. Today, we favor resorbable suture material for closing any bronchial stump [10]. Complex procedures were performed without effect on outcome. Even emergently, the midsternal approach can be done with acceptable results, obviously depending on the patient's condition.

The most important factor determining outcome was fistula recurrency. Small fistulas can be treated successfully by continuing empyema treatment or most probably, also by muscle flaps or the use of the omentum, large ones have escaped therapy in this series. Associated with year of operation and pretreatment, the most consequential correlation of recurrency was with stump length. As already indicated by other researchers [1, 9], the transpericardial approach has the best results when a long bronchial stump is present. Stamatis and colleagues [15] performed carinal resection using the midsternal approach when a short stump was present. In this series, all four carinal resections were done in short stumps, all right sided. The two deaths occurred before 1985, one probably related to a positive resection margin. The indication for carinal resection is the impossibility of closing the bronchus without tension using disease-free, viable bronchial tissue.

Hospital stay is long, not only before the operation, but also after repair. Although we found a difference in hospitalization between patients operated on for benign or malignant lesions, it is substantial for all patients. Once discharged, the patient has a closed bronchus and a closed chest. We have not found late recurrences. Long-term results were according to original pathology;we did not find a correlation between survival and cancer stage.

In conclusion, the best results are obtained by open thoracostomy treatment of the empyema, followed by transsternal closure. When a long stump is present, standard reamputation followed by closure with (absorbable) sutures should be performed, followed by chest closure 3 weeks later. In case of a short stump, a carinal resection is probably the best therapeutic option, buttressing the anastomosis with the greater omentum.

	Acknowledgments

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
This study was supported by a grant from the Dr Sander Schaepkens van Riempst Research Foundation.

	Footnotes

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 
Presented at the Thirty-third Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Feb 3–5, 1997.

Address reprint requests to Dr Brutel de la Riviere, Department of Thoracic Surgery, St Antonius Hospital, PO B 2500, 3430 EM Nieuwegein, the Netherlands.

	References

Top Footnotes Abstract Introduction Patients and Methods Results Comment Acknowledgments References

 

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