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Doff B McElhinney
Adam L Harmon
Timothy S Hall
David M Jablons
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Asian Cardiovasc Thorac Ann 2000;8:78-84
© 2000 Asia Publishing EXchange Pte Ltd

REVIEW PAPER

Management Strategies for Complex Bronchopleural Fistula

Junaid H Khan, MD, Sarah B Rahman, MD,1, Doff B McElhinney, MD, Adam L Harmon, MD,3, James P Anthony, MD,2, Timothy S Hall, MD, David M Jablons, MD

Division of Thoracic Surgery
1 Department of Medicine
2 Division of Plastic Surgery
UCSF-Mount Zion
San Francisco, California, USA
3 Division of Cardiothoracic Surgery
Washington Hospital Healthcare System
Fremont, California, USA
For reprint information contact: David M Jablons, MD Tel: 1 415 885 3887 Fax: 1 415 353 9525 Division of Thoracic Surgery, UCSF-Mount Zion, 1600 Divisadero Street, Room C-322, San Francisco, CA 94115, USA.

   Abstract
TOP
 Abstract
Introduction
 Case Reports
 Pathophysiology
 Diagnosis
 Prevention
 Surgical Treatment
 References
 
The management of complex bronchopleural fistula remains a major therapeutic challenge for the thoracic surgeon. Although the incidence of bronchopleural fistula following lung resection has decreased in recent years to 1% to 2%, when it occurs, it is associated with significant morbidity and mortality. Using illustrative cases, the epidemiology and pathophysiology of bronchopleural fistula are reviewed and operative strategies are discussed. Algorithms for the diagnosis and treatment are suggested on the basis of cases described in the literature. The best way to prevent a fistula is to rigorously follow the surgical techniques described, with minimal devascularization of the bronchus and prophylactic coverage of the stump in high-risk patients. Successful management of a fistula is combined with treatment of the associated empyema cavity. Definitive repair should be accomplished expeditiously, minimizing the number of procedures performed. When treatment is protracted, secondary complications are more likely and survival is adversely affected. The first step should be control of active infection and adequate drainage of the hemithorax, followed by timely repair of the bronchopleural fistula when possible and reinforcement of the stump with vascularized tissue. If a residual cavity is present it must also be obliterated with a pedicled muscle flap.


   Introduction
TOP
 Abstract
 Introduction
Case Reports
 Pathophysiology
 Diagnosis
 Prevention
 Surgical Treatment
 References
 
Bronchopleural fistula is a communication between a bronchus and the pleural space. The most common cause is failure of bronchial closure after partial or complete lung resection. Other etiologies include infection (necro-tizing pneumonia, coccidioidomycosis, aspergillosis), inflammatory conditions (sarcoid), and trauma (penetra-ting or blunt). Bronchopleural fistula is a rare problem, occurring in 2% of cases of lung resection (up to 10% after pneumonectomy). When it occurs, it is associated with mortality ranging from 15% to 75%, significant morbidity, and increased hospital stay for those who survive.1–7 A bronchopleural fistula can occur at any time but the peak incidence is within the first 3 weeks postoperatively. A bronchopleural fistula that occurs within the first few days after surgery should be considered a primary failure in surgical repair. In patients who have had previous irradiation, fistulas occur earlier and are associated with higher mortality.4 A bronchopleural fistula invariably results in a contaminated pleural space since there is a communication between an intubated airway and the hemithorax. A small air leak after lobectomy is common, usually due to dissection of the fissures or pleural adhesions. However, it is critical to be able to differentiate anastomotic or bronchial stump leaks from those coming from the lung parenchyma. Parenchymal leaks have a high likelihood of closure with conservative management by tube thoracostomy, whereas bronchial stump leaks usually require reoperation. Fistulas that do not resolve with conservative treatment in 7 days are a clinical challenge and will be the focus of this paper.


   Case Reports
TOP
 Abstract
 Introduction
 Case Reports
Pathophysiology
 Diagnosis
 Prevention
 Surgical Treatment
 References
 
Case 1
A 74-year-old man with diabetes and a recent 10-kg weight loss underwent right pneumonectomy and media-stinal node dissection for squamous cell carcinoma of the right upper lobe. He had an uncomplicated resection and initial postoperative course but developed a symptomatic bronchopleural fistula 17 days postoperatively. After initial stabilization, he underwent 3 separate attempts at closure of the fistula over 13 months, including bronchoscopic administration of fibrin glue, stump revision with buttressed intercostal muscle flap, and omental transposition, before presenting with a small residual fistula to our institution. At thoracotomy, the fistula could not be closed primarily because of dense fibrosis of the mediastinum and an intercostal muscle flap was used as a bronchial patch. The remaining pleural cavity was small and it was filled completely with a limited thoracoplasty and rectus abdominis muscle flap. He is doing well 3 years post-operatively.

Case 2
A 47-year-old man on steroid therapy for emphysema underwent a right pneumonectomy and mediastinal node dissection for squamous cell carcinoma of the right lower lobe after negative surgical staging. A stapling device was used to close the bronchial stump. He presented 14 days postoperatively with acute respiratory distress and copious serosanguineous sputum. He was stabilized with a tube thoracostomy and intubated for respiratory failure, then taken back to the operating room where a dehisced bronchial stump was revised primarily with interrupted sutures. The azygous vein was mobilized to cover the stump. Postoperatively, he required mechanical ventilation due to a contralateral pneumonia and developed a large air leak that progressively increased to the point where he became difficult to ventilate. He was transferred to our institution with respiratory acidosis and hypoxemia. A double-lumen endotracheal tube was placed and selective ventilation of the left side was achieved with improved gas exchange. He was started on intravenous antibiotics and a second chest tube was placed to drain a loculated pleural fluid collection. His nutrition was supplemented with a feeding tube and his steroid dose was decreased as his sepsis resolved. At reoperation 2 months after the initial surgery, the azygous patch was noted to be necrotic and primary closure of the bronchial stump was performed with pedicled intercostal muscle used to buttress the repair. The pleural cavity was filled with 2 additional intercostal muscle flaps. He did well initially but subsequently required a small Eloesser flap for drainage of a 2-cm residual pocket. He is doing well 10 months after his fistula repair.

Case 3
A 45-year-old man underwent a right middle and lower lobectomy for necrotizing pneumonia. He presented one week later with a bronchopleural fistula. There was gross contamination of the pleural space and an open drainage procedure using thoracoplasty of the 5th through 8th ribs was performed. He presented to our institution 14 months postoperatively with increasing respiratory distress, persistent drainage, and an open bronchopleural fistula through his thoracoplasty. The fistula could not be closed primarily but the hole was obliterated with a pedicled intercostal muscle flap. The residual pleural space was filled with a pedicled rectus abdominis flap. He is currently doing well 5 months postoperatively.

Case 4
A 32-year-old woman ejected during a truck accident presented with a large pneumothorax, massive subcuta-neous emphysema, multiple rib fractures, and respiratory distress. A massive air leak was noted after placement of a chest tube. Bronchoscopy confirmed the diagnosis of a left mainstem dehiscence 1-cm distal to the carina. A long single-lumen endotracheal tube was placed into the right mainstem bronchus over the bronchoscope to isolate ventilation. She underwent primary repair via a right thoracotomy and buttressing of the repair with a pedicled intercostal muscle flap. The pleural space was irrigated with antibiotic solution and closed primarily. She did well postoperatively.


   Pathophysiology
TOP
 Abstract
 Introduction
 Case Reports
 Pathophysiology
Diagnosis
 Prevention
 Surgical Treatment
 References
 
In early surgical series, a complete pneumonectomy was complicated by bronchopleural fistula in up to 28% of cases, which may have been related to the presence of bacteria at the bronchial stump, given that up to 60% of patients had positive sputum cultures at the time of resection.1 Although new antimicrobial drugs have minimized the risk of perioperative infection as a cause of bronchial stump breakdown, aggressive resection of more advanced disease, often after multimodality treatment with radiation or chemotherapy, has provided a new challenge in bronchial wound healing.

In the current era, the overall incidence of bronchopleural fistula following pulmonary resection ranges from 2% to 10%.4,6,8,9 Asamura and colleagues4 have defined several independent risk factors for the development of broncho-pleural fistula. These include a large extent of lung resection, residual or recurrent cancer at the bronchial stump, preoperative radiation, and diabetes. In addition, local factors such as empyema, pneumonia, and bron-chiectasis also impair wound healing and are implicated in fistula development. Prolonged postoperative mechani-cal ventilation or systemic infection with adult respiratory distress syndrome, as well as steroids, malnutrition, active tuberculosis, preexisting pneumonic infection, and age over 60 years are other predisposing factors.2,6,8

Technical factors thought to be associated with the development of bronchopleural fistula include devitaliza-tion and devascularization by excessive peribronchial dissection, excessively tight closure, and long bronchial stump. All of these factors contribute to poor healing of the bronchial stump or anastomotic suture line. There is controversy regarding the contribution of mediastinal node dissection and the difference between stapled and hand-sewn closure of the bronchus as risk factors.4,6,10–12 Bronchoscopic evaluation after carinal and lobar resection has demonstrated incomplete healing as late as 7 weeks postoperatively.13 Impaired mucociliary function has also been documented following bronchial anastomosis in lung transplant patients.14 Preoperatively, a single 16-Gy dose of cobalt irradiation in dogs (equivalent fractionated 36 Gy) has been associated with a 60% decrease in blood flow at the bronchial anastomosis.15 Because healing is by secondary intention, local wound conditions and healing capabilities of individual patients become more critical to a successful result.16 Our first 3 cases demonstrate typical risk factors for bronchopleural fistula development. In the first case, an elderly diabetic man with recent weight loss underwent right pneumonectomy, the second was a patient taking steroids who underwent a right pneumonectomy, and the third was a lung resection in a grossly infected field.

The pathophysiology of traumatic bronchopleural fistula is quite different. Traumatic fistula may be major or minor, a difference that is primarily determined by whether the injury is to the airway or is limited to the parenchyma. Penetrating injury (gunshot wound, knife, or fractured rib) is usually to the parenchyma and is usually self-limited. Blunt trauma is more commonly associated with major airway injury (airway injury in the neck is associated with penetrating trauma). The mechanisms for injury in blunt trauma include anteroposterior compression of the chest with lateral traction on the carina, closed glottis with increased intrathoracic pressure leading to increased airway pressure and disruption, and deceleration injury causing a shearing injury at the carina.17 As in our case 4, these patients usually have large air leaks after tube thoracostomy and must undergo immediate exploration and repair.


   Diagnosis
TOP
 Abstract
 Introduction
 Case Reports
 Pathophysiology
 Diagnosis
Prevention
 Surgical Treatment
 References
 
A history of fever and sudden onset of continuous cough with serosanguineous or purulent sputum in any patient after lung resection should raise the suspicion of a bronchopleural fistula. Though most patients eventually develop some symptoms of sepsis, the presentation can also be insidious with only malaise, anorexia and fever. At the other end of the spectrum, acute respiratory distress may occur if a large fistula allows sufficient fluid to flood the contralateral lung (as in our case 2), or if a tension pneumothorax occurs, or if a broncho-arterial fistula develops.4,5,7 The physical examination may reveal subcutaneous emphysema or decreased breath sounds if residual lung exists on the affected side. An auscultatory squeak with the Valsalva maneuver has also been noted.12 If aspiration has occurred, breath sounds may be coarse on the contralateral side and tracheal shift may occur if a large volume of air collects in the pleural space. Laboratory analysis often reveals leukocytosis. Sputum cultures may identify the causative organism. Pleural fluid obtained via thoracentesis or thoracoscopy frequently demonstrates an infection. Staphylococcus aureus and Pseudomonas aeruginosa are the most common organisms reported.18

An upright chest radiograph is the best initial screening test for the diagnosis of bronchopleural fistula. Broncho-pleural fistula should be suspected when there is: a new air-fluid level; a fall of 2 cm or more in the air-fluid level of a postpneumonectomy chest radiograph; a change in a residual airspace or new appearance of an airspace; or the return of the tracheal air column to midline in a previously shifted mediastinum. Evidence of aspiration pneumonia in the contralateral lung and subcutaneous emphysema are also suggestive findings. The location of an airspace in the presence of residual lung tissue must be differentiated between intraparenchymal (lung abscess) and intrapleural (empyema), since the two conditions are treated differently. Computed tomography can help confirm the diagnosis of bronchopleural fistula and delineate between an intrapleural and intraparenchymal process and may aid in planning any surgical treatment by demonstrating relationships to major airways.19

Bronchoscopy can help define the extent of the broncho-pleural fistula and differentiate between stump dehiscence and a distal parenchymal leak. Bronchoscopy can also help diagnose recurrent or persistent cancer at the anastomosis or closure. Bronchography was used in the past but is rarely employed today due to risk of contrast pneumonitis in the remaining lung.1 The diagnosis is usually straightforward if the presentation is early. However, an occult bronchopleural fistula (usually delayed or less extensive) manifesting as a postpneumonectomy space infection sometimes remains a diagnostic problem. Several methods are available to confirm the diagnosis. The simplest include placement of a chest tube and inspection for an air leak. Injection of methylene blue into the pleural cavity with subsequent appearance of the color in the sputum confirms the diagnosis, as does endobronchial injection of dye subsequently appearing in the pleural space.2 Ventilation nuclear scintigraphy may be helpful in a difficult case.6,20 Thoracoscopy has also been used for confirmation of the diagnosis and location of the fistula as well as a method for initial drainage of the associated empyema.6,21 Clinical suspicion remains the key to the early diagnosis of bronchopleural fistula since history, physical examination, and a plain upright chest radiograph are all that is needed to make the diagnosis in most cases.


   Prevention
TOP
 Abstract
 Introduction
 Case Reports
 Pathophysiology
 Diagnosis
 Prevention
Surgical Treatment
 References
 
The best way to manage a postoperative bronchopleural fistula is to prevent its development at the time of pulmonary resection. Since wound healing of the bronchial stump or the anastomotic suture line is the single most important factor in the development of bronchopleural fistula, strategies directed at prevention must facilitate optimal wound healing. The blood supply to the bronchial cartilage and mucosa is tenuous and easily damaged. The bronchial blood supply should be protected at all times with minimal peribronchial dissection, and minimal handling of the bronchial mucosa. All anastomoses must be without tension. The bronchial stump should be short to avoid pooling of secretions, which can contribute to subsequent infection and mucosal breakdown. A positive margin for cancer must be resected since it will un-doubtedly lead to a bronchopleural fistula. The use of a stapling device for the bronchus is controversial, insofar as the longer bronchial stump may predispose to retention of secretions, infection, and eventually recurrence of the fistula. In theory, there should be less inflammation, ischemia, and hematoma formation with the device but no study has shown a difference between the stapled and hand-sewn anastomosis in the development of broncho-pleural fistula. We prefer stapled closure when possible, with minimal peribronchial dissection.

Although nonoperative risk factors cannot always be eliminated, their effects can be minimized by preoperative preparation. Steroids can be weaned, nutritional supple-mentation started, and any contralateral pneumonia or systemic infection treated with appropriate antibiotics. The first 2 patients clearly benefited from weaning from their steroids and nutritional supplementation before definitive repair. In high-risk patients, we and others prophylactically use tissue adhesive and a pedicled vascularized flap to cover the bronchus.6


   Surgical Treatment
TOP
 Abstract
 Introduction
 Case Reports
 Pathophysiology
 Diagnosis
 Prevention
 Surgical Treatment
References
 
The general guidelines and priorities for management of bronchopleural fistulas are presented in Figures 1 to 3GoGoGo. Treatment priorities in patients with bronchopleural fistula are protection of the airway, control of infection, aggressive nutritional rehabilitation, and minimization of operative procedures. The management approach depends on whether the presentation is early or late. An early postoperative fistula diagnosed from a large air leak should be treated with immediate reexploration and revision of the bronchial stump with open drainage of the hemithorax, if significant contamination exists or the patient is septic. Unstable patients should have an immediate tube thoracostomy to prevent a tension pneumothorax and be stabilized with intravenous antibiotics before undergoing surgery (Figures 1 and 2GoGo). Direct closure is possible in nearly 80% of patients with a combination of stump resection, revision, or completion pneumonectomy, and covering of the stump with vascularized tissue. A minority of patients cannot have the fistula closed primarily and require a muscle flap to obliterate the hole.6 In high-risk patients, even when direct closure is easily achieved, we buttress the repair with an intercostal muscle flap.



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  		Figure 1. Algorithm for initial management of bronchopleural fistula. ETT = endotracheal tube, IV = intravenous.

 


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  		Figure 2. Algorithm for surgical options for management of broncho-pleural fistula.

 


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  		Figure 3. Algorithm for the management of the pleural space.

 
Mortality is related in part to the degree of contamination of the pleural space. Late-developing fistulas are more difficult to diagnose and to manage. Most of these patients unfortunately have had multiple operations and there is frequently a delay in both diagnosis and treatment, which contributes to morbidity following definitive management. Bronchopleural fistula invariably leads to a contaminated pleural space. Thus, although bronchopleural fistula and empyema are two distinct entities, their treatment in this setting is inevitably coupled.

As with any critically ill patient, airway control, ventilatory support, and hemodynamic stability must be addressed first. Patients are at risk of aspiration into the contralateral lung and should be kept in the reverse Trendelenburg position with the good lung up at all times.7,22 Intubation and positive pressure should be avoided if possible until the fistula is controlled to avoid exacerbating the air leak. A large air leak may make ventilation difficult.23,24 A double-lumen endotracheal tube or isolated contralateral mainstem bronchus intubation over a bronchoscope may be required to allow positive pressure ventilation of the remaining good lung without loss of minute ventilation through the fistula and to prevent soilage of the contra-lateral lung. Hypoxemia due to increased oxygen demand from the hypermetabolic state associated with critical illness, along with decreased oxygen delivery due to the increased arteriovenous shunting, anemia, and pneumonitis is the most common problem. Preoperative resuscitation with intravenous fluids, antibiotics, and chest drainage must be used to stabilize the critically ill patient before definitive repair of the fistula is undertaken.22 Our case 2 illustrates the importance of airway management to maximize gas exchange and the need for proper fistula control. The ventilatory difficulties in this patient were overcome by using a double-lumen endotracheal tube.

At the time of surgery, general anesthesia with spontaneous ventilation and packing of the remaining ipsilateral lung parenchyma and chest can also be used to facilitate exposure. High-frequency jet ventilation is also helpful, insofar as it delivers small tidal volumes at a high frequency and can improve alveolar mixing and gas-exchange with maintenance of mean airway pressure but reduced peak pressure.22 A thoracic epidural with local anesthetic is the ideal postoperative analgesic; however, patient-controlled analgesia is a viable option if an epidural is not available. Patient-controlled analgesia in com-bination with opiate and nonsteroidal antiinflammatory agents may help to reduce the proinflammatory cytokine cascade.25 Judicious preoperative preparation, direct visualization for the intubation, and adequate perioperative analgesia can minimize the perioperative decline in pulmonary function and improve outcome in attempting definitive repair of a bronchopleural fistula.

Traumatic bronchopleural fistulas are a special subset of all fistulas. Small distal parenchymal leaks due to penetrating trauma are usually self-limiting and resolve within 48 hours with simple chest tube drainage and lung reexpansion. Those that do not resolve spontaneously with simple chest tube drainage can often be repaired via thoracoscopy using stapling devices and newer techniques such as intrapleural and intrabronchial administration of fibrin glue.7,26,27 Blunt trauma usually results in proximal main airway injury. As case 4 illustrates, they usually present early and are not associated with a pleural space problem. The diagnosis is usually simplified due to the massive air leak after chest tube placement. These patients should be immediately explored and repaired primarily. There are 2 equally important aspects in the surgical management of all bronchopleural fistulas: closure of the fistula itself, and management of the pleural space. Although the two components are inherently integrated, we will discuss each independently for the sake of clarity.

Fistula Control
The incisions advocated for the management of proximal bronchopleural fistula include the standard ipsilateral thoracotomy, contralateral thoracotomy, and median sternotomy with transpericardial approach.3–6,28 Ipsilateral thoracotomy allows for repair of the fistula and treatment of the infected pleural cavity at the same time. The contralateral thoracotomy and sternotomy approaches have the advantage of avoiding dissection in an inflamed hilum. However, these approaches may lead to soilage of an otherwise sterile space, are limited to cases with a long bronchial stump, and usually require a second procedure to deal with the contaminated pleural cavity.

Primary repair should be done if possible, with repeat resection and revision. If revision is not technically possible, a pedicled muscle flap is sewn with interrupted sutures to the edges of the fistula to achieve an airtight seal. Muscle is used to buttress the repair in high-risk patients. Additional muscle (intercostal, pectoralis, latissimus, rectus) is placed as necessary to obliterate the cavity with or without a thoracoplasty. Any small residual cavity that persists can be managed by simple tube drainage. In case 2, the corrections initially attempted failed. Definitive repair was carried out using vascularized muscle. Azygous and pleural flaps are not well vascula-rized and often fail (as with the previous procedures with this patient). We prefer to use muscle, pericardium, and even occasionally diaphragm to buttress the repair.

Several conservative methods for closure of small (< 3 mm) or distal bronchopleural fistula have been described, including bronchoscopic and thoracoscopic application of fibrin glue and monomeric N-butyl-2-cyanoacrylate tissue adhesive.26,27 If the fistula is proximal or occurs late, conservative measures usually fail as the pleural space becomes contaminated. A large proximal fistula should be repaired primarily and the repair buttressed with vascularized tissue. A completion pneumonectomy or stump revision may be necessary. If a large fistula is distal, an initial attempt at conservative treatment is acceptable as long as the pleural space is drained sufficiently and ventilation is adequate. Definitive repair should be performed if these conservative measures do not work within 7 days. Algorithms for management are presented in Figures 1 to 3GoGoGo.

Pleural Space Control
Pleural spaces associated with bronchopleural fistula are considered infected until proven otherwise. A priority in the management of any bronchopleural fistula is to overcome active infection. Infection is controlled by intravenous antibiotics and adequate drainage of the pleural space (open or closed). Most patients are effectively drained with a tube thoracostomy. However, in cases of chronic empyema cavities, open drainage is usually necessary initially. Factors such as nutrition and physical rehabilitation should also be maximized to help combat the infection. The best approach to management of the pleural space depends on the degree of contamination. In early small fistulas with minimal contamination and low risk of aspiration, simple antibiotic irrigation and drainage (i.e., a modified Clagett procedure) is appropriate in 80% of cases.18 In the Clagett procedure, the residual cavity is irrigated with antibiotic fluid and drained until the cultures are negative, after which the residual space can be allowed to close on its own.18,29,30 Large intrathoracic defects can be obliterated with transposed muscle or by thoracoplasty. In case 4, an initial thoracoplasty failed but the patient was eventually managed successfully with a vascularized muscle flap (intercostal muscle flap) to buttress the repair of the fistula and the residual cavity was filled with a rectus flap.

Abrashanoff31 described the first use of a muscle flap to close a bronchopleural fistula in 1911. Before the advent of effective antibiotics, thoracoplasty was used extensively for tuberculosis. Thoracoplasty alone will frequently not close the fistula because of the noncompliance of the chest wall and a muscle transposition is usually required. Thoracoplasty is cosmetically disfiguring but is indicated in certain patients (especially those with large rigid cavities preventing obliteration by isolated rib removal alone) as it affords the only chance for elimination of infection in some circumstances. Thoracoplasty requires resection of thickened pleura, removal of 2 to 5 ribs (preserving the first rib) and preservation of intercostal muscle tissue for transposition.18,32–35 Today, many options are available before resorting to thoracoplasty. If only a partial lung resection was done at the first operation, a decortication can be performed to assist the remaining lung expand to help fill the cavity without the use of thoracoplasty. Different muscle groups (latissimus dorsi, pectoralis major, serratus anterior, pectoralis minor, rectus abdominis, intercostal) have been transposed successfully into the chest, as has omentum, all with varying degrees of success.35–40 Our first choice in muscle transposition is either the latissimus dorsi if it has not been divided at thoracotomy or intercostal muscle if limited muscle volume is needed. Where greater muscle mass is required, a rectus muscle and subcutaneous flap is recommended.

Infected tissue must still be debrided. Major contamination requires debridement and obliteration of the cavity with vascularized tissue and thoracoplasty, or open drainage with an Eloesser flap. Small cavities are usually amenable to a single muscle transposition, however, large spaces frequently require a combination of muscle transposition and limited thoracoplasty. An algorithm for management of the pleural space is presented in Figure 3Go.


   References
TOP
 Abstract
 Introduction
 Case Reports
 Pathophysiology
 Diagnosis
 Prevention
 Surgical Treatment
 References
 

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