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Ann Thorac Surg 1998;66:923-927
© 1998 The Society of Thoracic Surgeons


Original articles: General Thoracic

Endoscopic treatment of postoperative bronchopleural fistula: experience with 45 cases

Peter H. Hollaus, MDa, Franz Lax, MD, PhDa, Dan Janakiev, MDa, Paolo Lucciarini, MDa, Elfi Katz, MDa, Alois Kreuzer, MDa, Nestor S. Pridun, MDa

a Department of Thoracic Surgery, Pulmologisches Zentrum, Vienna, Austria

Accepted for publication April 14, 1998.

Address reprint requests to Dr Hollaus, Department of Thoracic Surgery, Pulmologisches Zentrum, Vienna, Sanatoriumstraße 2, A-1145 Vienna, Austria
e-mail: (Peter.Hollaus{at}pul.magwien.gv.at)


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. The value of bronchoscopic sealing of bronchopleural fistulas was studied retrospectively.

Methods. The cases of 45 patients seen between 1983 and 1996 with bronchopleural fistula after pneumonectomy (40 patients) or lobectomy (5 patients) were reviewed. Age, underlying disease, side, fistula size (millimeters) at initial bronchoscopy, survival (days) after endoscopic treatment, mode and number of endoscopic interventions, interval (days) between operation and fistula occurrence, and pathologic TNM stage in the case of malignancy were recorded. On the basis of the therapeutic outcome (cure, death, chronic empyema with closed fistula, or chronic empyema with open fistula) and the modality (successful sealing or bronchoscopic failure with subsequent surgical intervention), various groups were assessed and compared.

Results. Of 29 patients (64%) treated only endoscopically, 9 were cured. Seven patients had fistula closure, but persistent chronic empyema necessitated permanent drainage. In another 7 patients, the fistula remained open and also was controlled by permanent drainage. Six patients in this group died. The overall rate of fistula closure was 35.6% (16 patients), and recurrence occurred in 2 patients. Sixteen patients (35.6%) required surgical intervention because of increasing fistula size (8 patients), sepsis with refractory empyema (7), and fecal empyema (1 patient). Two patients in the surgical group died. Small fistulas (<3 mm) responded particularly well to primary endoscopic treatment.

Conclusions. Bronchoscopic treatment of bronchopleural fistula appears an efficient alternative, especially when surgical intervention cannot be done because of the physical condition of the patient.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Postoperative bronchopleural fistula (BPF) is a serious complication in thoracic surgery and a therapeutic challenge. Many patients are seen in life-threatening condition and cannot undergo any surgical procedure. Emergency chest tube drainage remains the initial method of choice for control of tension pneumothorax and aspiration. On the other hand, surgical options such as open window drainage (OWD) or thoracoplasty are rather mutilating and disabling for an already compromised patient. Endoscopic fistula closure is a favorable alternative, as it may avoid major surgical interventions. The purpose of this retrospective study was to determine the clinical efficacy of primary bronchoscopic sealing in BPF and possibly to identify patients who may profit by avoidance of aggressive surgical intervention.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Forty-five male patients aged 43 to 73 years old (median age, 60.29 years) seen between 1983 and 1996 were treated bronchoscopically, and their hospital charts were retrospectively reviewed. The preceding operative procedures included 39 pneumonectomies, 1 secondary pneumonectomy, and 5 lobectomies. Closure of the bronchial stump was achieved with mechanical staplers in all patients. Routine postoperative ventilation was not employed.

Data taken from hospital charts included age, underlying disease, side, fistula size (millimeters) at initial bronchoscopy, survival (days) after endoscopic treatment, mode and number of endoscopic interventions, interval (days) between operation and fistula occurrence, and pathologic TNM stage in the case of malignancy. If persistent air leak occurred on the first postoperative day, the interval was defined as 1 day. Fistulas measuring 1 mm or less were defined as minifistulas. Fistulas occurring less than 30 days after operation were classified as early fistulas. On the basis of the therapeutic outcome (cure, death, chronic empyema with closed fistula, or chronic empyema with open fistula) and the modality (successful bronchoscopic closure or bronchoscopic failure with subsequent surgical intervention), various groups were assessed and compared in terms of fistula size, interval between operation and fistula occurrence, and number of endoscopic interventions. Follow-up ranged from 7 to 4,075 days (mean follow-up, 779.16 days).

Fistula diagnosis
Postoperative BPF was suspected in the case of persistent air leak of more than 8 days after operation despite treatment with continuous positive airway pressure mask and suction. Clinical symptoms leading to the diagnosis of fistula were dyspnea, fever, cough, hemoptysis, and fetid breath. Presence of BPF and fistula size were determined by direct bronchoscopic visualization or bronchography [1]. Measurement of fistula size was performed with a scaled catheter inserted through the bronchoscope.

Treatment
If BPF was suspected, immediate pleural drainage was performed, and specimens for bacterial cultures were obtained. Fistula size and localization were evaluated bronchoscopically. Patients with fistulas smaller than 8 mm and no life-threatening sepsis originating from empyema were considered suitable for primary bronchoscopic treatment.

All procedures were performed under general anesthesia with a rigid bronchoscope with jet ventilation. Before treatment, the fistula channel was deepithelialized with a cytology brush, high-frequency diathermy, or a laser. Visible leaks smaller than 3 mm were treated exclusively with fibrin sealant (Tissucol; Immuno, Vienna, Austria). Until 1995, fibrin was simply injected into the fistula channel. Since 1996, we have injected fibrin into the submucosa rather than intraluminally. In these patients, the two components of fibrin glue were injected consecutively. Fistulas bigger than 3 mm were treated with fibrin and spongy calf bone [2], as a pure fibrin clot of this size can dislocate into the pleural cavity or be aspirated to the contralateral lung. The bone, being soft and elastic, was shaped to correspond to the fistula form and sprayed with fibrin after insertion. The intervention was considered successful when air leakage stopped. Fistulas larger than 8 mm were not considered suitable for endoscopic treatment because, in our experience, openings of that size cannot be blocked successfully. Thus, this group was excluded from the analysis.

If fistula closure was achieved, rinsing of the pleural cavity with antibiotic solution according to culture sensitivity was initiated. Bronchoscopic follow-up was done routinely once a week. If fibrin or other material used for occlusion was expectorated, immediate bronchoscopy was performed to reclose the fistula. Specimens for bacteriologic cultures were obtained twice a week from the chest tube drainage. After three negative cultures, empyema was considered eradicated. The chest tube was then removed if no signs of persistent fistula were detectable by air bubbles or incomplete radiologic lung expansion.

Endoscopic treatment was discontinued when local infection was adequately controlled by pleural drainage, resulting in a drainage volume of less than 30 mL every 24 hours. Unsuccessful fistula closure was not an indication for prolongation of treatment. These patients were discharged with permanent drainage.

Surgical intervention was considered when fistula size increased during endoscopic treatment, fecal empyema developed, or there was progression to systemic sepsis. These patients were treated by OWD or, if possible, with thoracoplasty, depending on their general physical condition.

All patients who died during treatment underwent postmortem examination. Causes of death were recorded.

Statistical analysis
All data were entered in a personal computer (Compaq-PC, IBM compatible, Windows 95, Pentium) and evaluated by a statistical program (SPSS for Windows, version 6.1). Evaluation of data was performed by crosstabulation and correlation. The applied significance level was 0.05.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Forty-one patients (91.1%) had non–small cell lung carcinoma and 1 patient (2.2%), small cell lung carcinoma. Fourteen patients were in stage I, 13 in stage II, 14 in stage IIIA. One patient was referred from another hospital, and tumor stage was not recorded. No fistula was caused by tumor recurrence. In the remaining 3 patients, the underlying disease was destroyed lung in 2 (4.4%) and pulmonary atresia in 1 patient (2.2%). The ratio of right side to left side was 29:16. Fistula size was recorded for 41 patients and ranged from 1 to 8 mm (mean size, 2.35 mm); there were 21 minifistulas. The interval between operation and fistula occurrence ranged from 4 to 932 days (mean interval, 96.44 days).

Twenty-nine patients (64%) were treated endoscopically (Table 1). Nine of them were cured. The diagnosis in these 9 patients was non–small cell lung cancer in 8 and septic lung disease in 1, and the BPF developed after pneumonectomy in 5 and after lobectomy in 4. Fistula closure was successful in 7 patients, but persisting chronic empyema made permanent drainage necessary. In another 7 patients, fistula closure failed, and they also were discharged with permanent drainage. These 14 BPFs occurred after pneumonectomy. There was no direct procedure-related mortality. Six of these 29 patients died, all of whom had postpneumonectomy. Causes of death were aspiration pneumonia in 4 patients, cardiac arrest in 1 patient, and sepsis originating from empyema in 1. It is noteworthy that since 1991, only 1 patient treated endoscopically has died.


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Table 1. Results of Bronchoscopic Treatment in 29 Patientsa

 
Operative intervention became necessary in 16 patients (35.6%) (15 after pneumonectomy and 1 after lower lobectomy) (Table 2). The underlying disease was septic lung disease in 7 patients, pulmonary atresia with Addison’s disease in 1, non–small cell lung cancer in 13, and small cell lung cancer in 1. Reasons for surgical treatment were fecal empyema in 1, increase in fistula size during treatment in 8, and sepsis resulting from empyema in 7. Eleven patients (24.4%) underwent thoracoplasty. Two of them died, 1 of cardiac arrest, and 1 of aspiration pneumonia with adult respiratory distress syndrome. There was no fistula recurrence after thoracoplasty. In 5 patients (11.1%), sepsis was controlled by OWD.


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Table 2. Results of Surgical Treatment Necessitated by Bronchoscopic Failure in 16 Patientsa

 
Seventeen patients (37.8%) died after discharge during follow-up, 9 of them of tumor progression (survival range, 143 to 1,349 days; mean survival, 531.44 days). Two patients, who were treated endoscopically, had fistula recurrence, for a recurrence rate of 12.2% (2/16 successful closures). The first of these patients (BPF after lobectomy) was readmitted 5 days after discharge. He underwent partial thoracoplasty and subsequently died of adult respiratory distress syndrome. The second patient (BPF after pneumonectomy) had recurrence 2 months after discharge. He was not a candidate for surgical intervention and died of aspiration pneumonia. Two patients treated by OWD died of pneumonia, and 1 died of respiratory insufficiency. The survival of patients with OWD was 42 to 829 days (mean survival, 332.67 days). One patient, discharged with chronic empyema and open fistula, died of cardiac insufficiency. Of the remaining 3 patients who died, 2 had been discharged with an open fistula and 1 with a closed fistula, all with permanent drainage. They died of pneumonia.

Survival of patients dying of nonneoplastic causes was 42 to 2,344 days (mean survival, 860.88 days). Patients discharged with permanent drainage survived for 158 to 2,344 days (mean survival, 1177.8 days).

The average number of endoscopic interventions irrespective of outcome was 2.47 (range 1 to 7). Size, interval, and number of therapeutic interventions showed no significant differences between the surgical and endoscopic groups (p > 0.05). Although there was a marked tendency for more frequent cure of small and early fistulas compared with bigger and later ones, size and interval had no significant relevance on course of therapy (p = 0.057). The dominance of the right side was significant (p < 0.05).


    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 
Bronchopleural fistula represents the most serious postoperative complication in thoracic surgery. Especially for patients in whom the fistula develops when they are not in the hospital, the correct diagnosis is frequently delayed. The immediate sequelae are respiratory insufficiency, aspiration pneumonia, empyema, or a combination of these. Therefore, these patients are often seen in an advanced state of sepsis originating from empyema or pneumonia.

In empyema with BPF, pleural rinsing is contraindicated because of the danger of aspiration. Only aggressive surgical methods, such as OWD or thoracoplasty, are successful therapeutic modalities. Though necessary in a considerable number of patients, both these procedures are rather mutilating, and thoracoplasty creates a long-term pain problem. They should be considered the last resort. We do not use the Clagett procedure because the rate of success, especially in patients with mixed empyemas, is only about 20% [3], and the overall rate of recurrence is 40% [4]. In accordance with Pairolero and colleagues [5] and Goldstraw and Wong [6, 7], we trust in the natural organizing process of obliteration of the thoracic cavity, which can be expected if the causative infection is eradicated. Therefore we refrain from surgical reduction of the postpneumonectomy space except in the case of thoracoplasty.

Although aware of alternative methods of treatment (OWD, thoracoplasty, muscular flaps, and omental transposition), we try to optimize an algorithm of fistula management by primary minimal intervention and concomitant achievement of low mortality. The quality of life of patients undergoing thoracoplasty or OWD is hardly acceptable. Therefore, we avoid these procedures if possible.

Few successful results of bronchoscopic closure of BPF with fibrin glue have been reported to date [812]. The authors agree on the high therapeutic value of this technique. It is minimally invasive and is tolerated by all patients, especially when their physical condition is too poor for surgical intervention.

Employing the concept of early bronchoscopy and single or repeated fibrin application combined with adequate pleural drainage, we discharged 37 patients from the hospital. Eight patients died in the hospital, 5 of them of multiple-organ failure as a result of aspiration pneumonia, present at admission. In this small group, sepsis progressed from pneumonia irrespective of pleural drainage, bronchial sealing, or both.

Our hospital mortality rate of 17.8% lies in the low range reported (20% to 70%). Most patients who died were in the group treated only endoscopically. They were in poor physical condition when first seen and were not surgical candidates. In our experience, the disastrous course of pneumonia in patients with fistula, especially after pneumonectomy, cannot be positively influenced by any therapeutic intervention on the fistula itself [14].

Small fistulas (<3 mm) can be successfully treated with fibrin alone. Submucosal injection of the fibrin glue prevents expectoration of the clot and is better than local instillation. If the latter is performed, it is useful to avoid powerful ventilation at the sealing site for some minutes, thus allowing time for clot formation. It is remarkable that submucosal injection resulted in complete cure in 4 consecutive patients.

Bigger fistulas are difficult to treat. In most instances we employed decalcified spongy calf bone. Although temporary fistula closure can be easily accomplished, permanent fistula closure remains a rarity; the bone can be coughed up as late as 2 weeks after intervention, thus making early discharge impossible. However, even temporary occlusion facilitates adequate empyema treatment, improving the patient’s condition and making an eventual operation feasible. Most authors agree that fistulas bigger than 8 mm are not suitable for endoscopic therapy [1012]. Patients who were cured bronchoscopically needed one to three fibrin applications and one to three bone insertions. This experience is confirmed by others [11, 12], who also needed an average of three interventions per patient. Cure after a single endoscopic intervention is possible but is not the rule. Several attempts are necessary.

Duration of treatment can be limited by the patient, who sometimes prefers thoracoplasty to a long hospital stay and repeat bronchoscopies, even if complete cure seems possible. On the other hand, we have had patients who refused surgical intervention. We believe that the quality of life with permanent drainage is comparable to that with a colostomy. The drainage tube is changed every 2 weeks, and the small bottle (volume of 30 mL) is worn easily and is changed daily. We think permanent drainage, which leaves the patient fully mobile without disfigurement or pain, is a worthwhile alternative to thoracoplasty or OWD.

During endoscopic treatment, two main reasons make surgical intervention likely. First, conservative therapy for empyema can simply fail, as occurred in 8 of the 16 patients who required operation. Eradication of germs in the postpneumonectomy space by pleural rinsing remains a problem, as seen in patients with isolated postpneumonectomy empyema without demonstrable BPF. The second reason for surgical intervention is persistent BPF. A single bronchoscopy allows assessment of the actual condition without providing information about the course of fistula dynamics. Only serial bronchoscopy will help determine the response of the fistula size to treatment. An enlarging BPF during endoscopic treatment makes surgical intervention likely.

Statistical analysis did not show a significant influence of fistula size and interval between operation and fistula occurrence on therapeutic outcome. This result might be attributable to the small number of patients. However, the clinical experience showed us that smaller and early fistulas have a better chance for bronchoscopic cure. The reasons seem clear: small size means easier closure, and early fistula occurrence implies a quick diagnosis and early empyema therapy before local infection has covered the entire hemithorax.

In conclusion, bronchoscopic treatment is a minimally invasive, efficient method to close small BPFs and is a valuable alternative to repeat thoracotomy in patients in whom surgical closure is not feasible because of their poor general physical condition. Hospital mortality and recurrence rates are low. Even if eradication of concomitant empyema fails, successful fistula closure is possible. Although bigger fistulas can be permanently closed with spongy calf bone, only temporary fistula closure is achieved in most instances. This allows the surgeon to treat empyema and prepare the patient for eventual surgical intervention. Permanent drainage in persisting empyema or fistula is an acceptable alternative to thoracoplasty or OWD, as it offers a good quality of life without mutilation and chronic pain [13].


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

  1. McManigle J.E., Fletcher G.L., Tenholder M.F. Bronchoscopy in the management of bronchopleural fistula. Chest 1990;97:1235-1238.[Free Full Text]
  2. Pridun N., Redl H., Schlag G. Ein neues biologisches Implantat zum Verschluß bronchopleuraler Fisteln. Z Herz Thorax Gefaßchir 1987;1(Suppl 1):60-62.
  3. Miller J.I., Jr Postsurgical empyemas. In: Shields T.W., ed. General thoracic surgery, 4th ed. Baltimore: Williams & Wilkins, 1994:694-700.
  4. Stafford E.G., Clagett O.T. Postpneumonectomy empyema. Neomycin instillation and definitive closure. J Thorac Cardiovasc Surg 1972;63:771-777.[Medline]
  5. Pairolero P.C., Phillip G.A., Trastek V.F., Meland N.B., Kay P.P. Postpneumonectomy empyema. The role of intrathoracic muscle transposition. J Thorac Cardiovasc Surg 1990;99:958-968.[Abstract]
  6. Goldstraw P. Treatment of postpneumonectomy empyema: the case for fenestration. Thorax 1979;34:740-745.[Abstract/Free Full Text]
  7. Wong P.S., Goldstraw P. Post-pneumonectomy empyema. Eur J Cardiothorac Surg 1994;8:345-350.[Abstract]
  8. Roksvaag H., Skalleber L., Nordberg C., Solheim K., Hoivik B. Endoscopic closure of bronchial fistula. Thorax 1983;38:696-697.[Free Full Text]
  9. Onotera R.T., Unruh H.W. Closure of a post-pneumonectomy bronchopleural fistula with fibrin sealant (Tisseel®). Thorax 1988;43:1015-1016.[Abstract/Free Full Text]
  10. Torre M., Chiesa G., Ravini M., Vercelloni M., Belloni P.A. Endoscopic gluing of bronchopleural fistula. Ann Thorac Surg 1987;43:295-297.[Abstract]
  11. Torre M., Quaini E., Ravini M., Nerli F.P., Maioli M. Endoscopic gluing of bronchopleural fistula. Ann Thorac Surg 1994;58:901-902.[Medline]
  12. Jessen C., Sharma P. Use of fibrin glue in thoracic surgery. Ann Thorac Surg 1985;39:521-524.[Abstract]
  13. Glover W.T., Chavis T.V., Daniel T.M., Kron I.L., Spotnitz W.D. Fibrin glue application through the flexible fiberoptic bronchoscope. Closure of bronchopleural fistulas. J Thorac Cardiovasc Surg 1987;93:471-472.
  14. Hollaus P.H., Lax F., El-Nashef B.B., Hauck H.H., Lucciarini P., Pridun N.S. Natural history of bronchopleural fistula after pneumonectomy: a review of 96 cases. Ann Thorac Surg 1997;63:1391-1397.[Abstract/Free Full Text]



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