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214 Bronchopleural ﬁstula after pneumonectomy and lobectomy

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CHEST CLOSURE

Drains are inserted; and after careful hemostasis, the sternum is closed in routine fashion with interrupted stainless steel wires.

Endoscopic treatment of small ﬁstulae

In some cases of very small ﬁstulae, the patient remains well, and management can be expectant with close follow-up. A more satisfactory method of dealing with this problem is bronchoscopic closure. This method is worth attempting in cases of small ﬁstulae, ﬁstulae in very ill patients who would not tolerate reoperation, and ﬁstulae developing later in the postoperative recovery period when the formation of a more ﬁbrous thorax makes signiﬁcant aspiration less likely. Many methods have been reported with varying success, including insertion of decalciﬁed autologous bone, application of local irritants (caustic soda), or adhesion with ﬁbrin glue. The basis of most methods is induction of inﬂammation and formation of scar tissue to close the hole. Multiple applications may be necessary, and reported success ranges from closure rates of 35% to over 60%.

Bronchopleural ﬁstula after lobectomy

closed in routine fashion with layers of polyglycolic acid sutures.

OUTCOME

The overall mortality in patients with bronchopleural ﬁstula after pneumonectomy is high. In most cases the cause of death is aspiration pneumonia. The mortality tends to be highest in those developing ﬁstulae early in the postoperative phase. This fact is probably due to the ﬂuidity of the space contents and the higher risk of signiﬁcant aspiration. Reported mortality after operative intervention to reclose a ﬁstula is between 20% and 30%. In those patients surviving, however, recurrent ﬁstulae are rare, and the late prognosis is determined by the stage of the malignancy. Recurrent ﬁstula formation seems to be a uniformly fatal event. Finally, one should remember that, in cases of malignancy in which postoperative histological analysis has identiﬁed stage III disease, the medium-term prognosis is poor, even in patients who do not experience the complication of bronchopleural ﬁstula. Therefore, before performing major reintervention in patients who present later with more chronic symptoms, one should consider a more conservative approach, with an attempt at bronchoscopic closure of the ﬁstula and permanent intercostal drainage for the empyema space.

As stated earlier, ﬁstula formation after lobectomy is rare in our experience. In the reported series of lung resections for carcinoma or infection, the two situations in which postlobectomy bronchopleural ﬁstulae are encountered are after sleeve lobectomy and bilobectomy (middle and lower) in high-risk patients, with an incidence of 6% and 11%, respectively.

Often the patient is asymptomatic, but a chest radiograph reveals a pneumothorax and ﬂuid level. The consequences of ﬁstula formation after lobectomy are less signiﬁcant than those after pneumonectomy as long as the residual lobe is viable. If the remaining lobe is not expandable, then a complete pneumonectomy is the only option, and the mortality approaches that with ﬁstula formation after pneumonectomy.

The initial management is insertion of an intercostal drain with an underwater seal. This maneuver may be all that is necessary if the remaining lobe is able to expand and obliterate the space. When simple drainage for a week is unsuccessful, the thoracotomy should be re-explored. The empyema cavity is débrided, and a decortication of the remaining lung is performed. The bronchial stump is amputated and reclosed with interrupted 4/0 polypropylene sutures. The expanded lobe should seal the closure and obliterate any residual space so that muscle buttressing of the closure is unnecessary. Apical and basal intercostal drains are placed, and the chest is

FURTHER READING

Deschamps C, Bernard A, Nichols FC 3rd, Allen MS, Miller DL, Trastek VF,

Jenkins GD, Pairolero PC. Empyema and bronchopleural ﬁstula after pneumonectomy: factors affecting incidence. Annals of Thoracic Surgery 2001; 72: 243–7.

Deschamps C, Pairolero PC, Allen MS, Trastek VF. Management of

postpneumonectomy empyema and bronchopleural ﬁstula. Chest Surgery Clinics of North America 1996; 6: 519–27.

Lois M, Noppen M. Bronchopleural ﬁstulas: an overview of the problem

with special focus on endoscopic management. Chest 2005; 128: 3955–65.

Perelman MI, Rymko LP. Management of empyemas: the problem of

associated bronchopleural ﬁstula. In: Thoracic Surgery: Surgical Management of Pleural Disease, eds. Deslauriers J, Lacquet L. In: International Trends in General Thoracic Surgery, Vol 6, CV Mosby, St Louis 1991: 301.

Puskas JD, Mathisen DJ, Grillo HC

bronchopleural ﬁstula. Journal of Thoracic and Cardiovascular Surgery 1995; 109: 989.

Sirbu H, Busch T, Aleksic I, Schreiner W, Oster O, Dalichau H.

Bronchopleural ﬁstula in the surgery of non-small cell lung cancer: incidence, risk factors, and management. Annals of Thoracic and Cardiovascular Surgery 2001; 7: 330–6.

Sonobe M, Nakagawa M, Ichinose M, Ikegami N, Nagasawa M, Shindo T.

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

Cardiothoracic Surgery 2000; 18: 519–23.

et al. Treatment strategies for

Postpneumonectomy empyema

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PETER H. HOLLAUS

Consultant, General and Thoracic Surgeon, Department of Thoracic Surgery, Pulmologisched Zentrum Wien, Vienna, Austria

PRINCIPLES AND JUSTIFICATION

Postpneumonectomy emphema (PPE) associated with bronchopleural ﬁstula (BPF) is the most dreaded complication in thoracic surgery. The reported incidence ranges from 2–13%, reaching its peak in the second and third postoperative weeks and declining rapidly thereafter. However, PPE has been reported even 35 years after operation.

PPE is associated with a bronchopleural ﬁstula in approximately 40% of all cases and occurs in our experience in the membranous part of the main bronchus in the majority of cases. Its size ranges from 1 mm to total stump dehiscence.

Mortality ranges from 20–70%, the most common cause of death being aspiration pneumonia with subsequent adult respiratory distress syndrome (ARDS).

The predominant causative organism is Staphylococcus aureus. Whether infection starts intrathoracically and leads to perforation of the bronchial stump, or primary breakdown of the bronchial stump allows secondary invasion of the thorax from the bronchial system, is not clearly established. Both pathophysiological mechanisms seem to play a role. Especially in late PPE, hematogenous spread to the postpneumonectomy space is assumed to cause infection.

The reasons why and when PPE occurs remain unclear. Risk factors for BPF have been investigated intensively. Smith et al showed that the pneumonectomy stump heals by second intention in 50% of cases. Thus, poor local blood supply together with overzealous dissection may be responsible.

Advanced age (>70 years), preoperative irradiation, diabetes, malnutrition, malignant invasion of the bronchial stump, male sex, right-sided resections, and completion pneumonectomy are proven risk factors for PPE associated with BPF. The presence of tumor cells in the stump normally is a result of nonradical resection in early BPF. In late ﬁstulas

local recurrence leads to bronchial stump breakdown either by itself or via irradiation damage.

While malignant cells, irradiation damage, diabetes, and malnutrition deﬁnitely lead to impaired wound healing, these problems are only relevant in a minority of patients. The remaining “risk factors” offer no pathophysiological explanation for the formation of BPF. Technical ﬂaws may be responsible for very early ﬁstulas. Some authors postulate that a long bronchial stump forms a blindsac in which secretions are pooled and become infected if the patient is not capable of removing retentions by coughing. However, this theory has never been challenged by any study and is not proven. Additionally, it does not offer an explanation for the predominance of the right side and of male sex, two proven risk factors for BPF. Some authors even prefer a long stump because it offers more therapeutic options if BPF occurs. Lymphadenectomy is thought to enhance the risk of BPF but does not explain sex and side differences either. Again, statistical conﬁrmation is missing.

BPF mostly occurs after pneumonectomy. Although a high TNM stage has been reported to promote ﬁstula occurrence, it is more probable that the real problem is pneumonectomy itself, which is carried out more often in advanced tumors and, therefore, leads to accumulation of high TNM stages in a selected group compared to patients with lesser resections. Postoperative ventilation also has been accused of promoting ﬁstula formation. However, aspiration pneumonia may be the initial symptom of bronchopleural ﬁstula, which is already present when the patient is referred to the intensive care unit (ICU). Diagnosis of BPF follows later on and may be misinterpreted as a consequence of ventilation.

The sequelae of BPF are aspiration pneumonia, empyema and, in the rare case of total bronchial stump insufﬁciency, massive air loss with respiratory insufﬁciency. Aspiration remains the main cause of death if a ﬁstula occurs in the early

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postoperative period and does not depend on ﬁstula size. Patients still suffer from ventilation/perfusion mismatch and mucous congestion in the remaining lung caused by the procedure and anesthesia. Due to pain, their ability to cough is reduced. If pneumonia occurs in this time, ARDS is nearly inevitable and even results of mechanical ventilation are disastrous. Therefore, the interval between operation and onset of BPF is the most important factor that inﬂuences clinical course and outcome. The incidence of aspiration pneumonia reaches its peak during the ﬁrst two postoperative weeks, until the patient is free of pain and has regained his or her capability to cough, and drops dramatically after the ninetieth postoperative day, when the formation of ﬁbrothorax is completed. Fibrothorax with its multiple small ﬂuid compartments seems to offer an effective protection against ﬁstula formation and aspiration in the late postoperative period. Mortality sharply declines as soon as the risk of aspiration diminishes.

In late ﬁstulas empyema becomes the main problem to deal with. If adequate treatment is delayed, the patient develops sepsis.

With special regard to prognosis and postoperative time BPF can be classiﬁed as:

1 Early ﬁstulas, occurring during the ﬁrst two postoperative

weeks with a maximum risk of aspiration pneumonia and, thus, highest mortality.

2 Fistulas occurring between 2 weeks and 3 months after

operation. Mortality resulting from aspiration pneumonia is declining due to the patient’s postoperative recovery. In this period the patient is already discharged from hospital and may fail to seek adequate treatment. Mortality is still high, though decreasing.

3 Late ﬁstulas occurring later than 3 months after operation.

The formation of ﬁbrothorax is completed, and the main problem of BPF becomes empyema of the postpneumonectomy space with sepsis. The mortality is low. The most dangerous postoperative complications comprise ﬁstula or empyema recurrence and persisting infection.

PREOPERATIVE ASSESSMENT AND PREPARATION

The following symptoms occur in cases of bronchopleural ﬁstula: subcutaneous emphysema, dyspnea, fever, fetid breath, serosanguineous expectoration, and productive cough. Lying on the healthy side may lead to cough and expectoration, because in this position the bronchial stump becomes situated under the ﬂuid level in the postpneumonectomy space. Very rarely, patients feel non-neuritic pain in the empty thoracic cavity. In some cases sudden onset of pneumonia is the only sign of bronchopleural ﬁstula and heralds an ominous prognosis.

Clinical symptoms (drop of oxygenation, dyspnea) may be misdiagnosed as pulmonary edema, and diuretics are applied, while the patient is literally drowning in ﬂuid aspirated from the postpneumonectomy space. In cases of late empyema patients complain about fatigue, weight loss, fever, and productive cough. Late PPEs are frequently overlooked until empyema necessitatis occurs.

C-reactive protein (CRP) and white blood count (WBC) rise dramatically and may be the ﬁrst sign of beginning postpneumonectomy empyema, before clinical symptoms appear. In this early phase aspiration of the pneumonectomy space may yield positive bacterial cultures or a positive gram stain and establishes the diagnosis, but as many as 20% of cases will prove sterile, even when frank pus is drained, probably as a result of previous antibiotic treatment.

In case of an early bronchopleural ﬁstula chest X-ray shows a drop in the ﬂuid level in the postpneumonectomy space. In late empyema multiple ﬂuid levels are visible radiologically after the thoracic cavity had been obliterated in previous ﬁlms. A computerized tomography (CT) scan provides important diagnostic information on intrathoracic topography in late ﬁstulas or isolated postpneumonectomy empyema. The persistence of air bubbles within the thoracic cavity suggests empyema if clinical symptoms are present. Although big ﬁstulas may be visible, CT is not useful for ﬁstula diagnosis itself.

Often symptoms are rather nonspeciﬁc, and a high grade of suspicion is necessary to make the correct diagnosis. If there is any doubt, diagnostic chest tube drainage is justiﬁed. If air escapes through the drain, BPF is evident. When pus is evacuated and no air bubbling is visible, a concomitant BPF must be ruled out endoscopically, because the ﬁstula may be covered with ﬁbrin or debris which prevent air leakage temporarily.

Bronchoscopy is performed under general anesthesia with jet ventilation and a rigid bronchoscope. Endoscopic visualization allows assessment of ﬁstula size, identiﬁcation of local tumor recurrence, and collection of intrabronchial cultures. If a very small ﬁstula is suspected but not visible, indirect diagnosis is achieved by contrast media instilled via the bronchial stump during endoscopy and radiological examination (ﬁstulography). If malignancy is suspected, biopsies should be taken to conﬁrm the diagnosis.

Broad spectrum antibiotics are given parenterally. Debilitated patients require adequate nutrition in terms of calories, protein, and micronutrients.

ANESTHESIA

All operations are performed under general anesthesia with single-lung ventilation via a double-lumen endotracheal tube to avoid air loss through the leakage and further aspiration from the postpneumonectomy space.

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OPERATION

Primary treatment

Immediate thoracic drainage must be performed if PPE is suspected. The goal of primary treatment is to prevent aspiration and sepsis originating from empyema. Both goals can be achieved by chest tube drainage.

Until a chest tube is inserted, the patient is turned on the operated side to prevent aspiration. The drain must be placed cranial to the thoracotomy scar to avoid intraabdominal damage. For early PPE, the procedure is carried out under local anesthesia.

In late PPE a thick ﬁbrous layer covers the inner surface of the postpneumonectomy space. Due to scarring, the topography of the inner organs may have changed dramatically making chest tube drainage a dangerous intervention. CT scan provides excellent information on the intrathoracic topography. Rib resection and drain insertion under general anesthesia should be considered in selected cases. Further management depends on whether a ﬁstula is present and the patient’s general condition.

Sterilization of the pleural space can only be achieved if a concomitant ﬁstula of the bronchial stump is closed. Fistula treatment options are bronchoscopic sealing with ﬁbin glue and surgical procedures. While surgery remains the primary option, patients in a bad general condition or suffering from metastatic disease may undergo bronchoscopic treatment if their ﬁstula is smaller than 3 mm. If the pleural space is loculated, sepsis may progress despite chest tube drainage. Immediate open window drainage (i.e. fenestration) allows evacuation of empyema, debridement of the postpneumonectomy space, and control of sepsis.

ate start of antibiotic instillation after surgery. After pneumonectomy, the diaphragm moves upwards. To avoid opening of the abdominal cavity by mistake, secondary thoracotomy should be performed through the original incision or cranially to it. At the beginning of the procedure the thoracic cavity is thoroughly debrided, and bacteriological cultures are taken. After rinsing of the postpneumonectomy space with saline, the bronchial stump is dissected. On the right side the azygous vein is ligated to gain better access to the stump. On the left side the bronchial stump retracts deeply into the mediastinum and is much more difﬁcult to approach.

If the ﬁstula is not visible, the thoracic cavity is ﬁlled with water and the patient ventilated under 40 cmH2O positive end-expiratory pressure (PEEP), to locate the ﬁstula. If possible, the stump is refreshed and closed with interrupted sutures (PDS, 3.0 or 4.0). A covering ﬂap (muscle or omentum) is sutured circumferentially around the stump with interrupted sutures (Vicryl 3.0, 4.0), regardless of whether the ﬁstula had been previously closed. At the end of the operation the thoracic cavity is again ﬁlled with saline and the endobronchial pressure increased to 40 cm PEEP to assure air tightness.

After irrigation of the entire hemithorax with saline, one or two chest drains are inserted at the most caudal point of the thoracic cavity. Due to the natural organizing process of obliteration after successful empyema eradication, surgical reduction of the postpneumonectomy space should only be considered in cases of ﬁstula or empyema recurrence or in empyemas recalcitrant to conservative measures.

Postpneumonectomy empyema with bronchopleural ﬁstula

Deﬁnitive treatment

The basic goals of operative treatment are debridement of the postpneumonectomy space, closure of the ﬁstula, and sufﬁcient drainage of the thoracic cavity. In our experience obliteration of the postpneumonectomy space is not mandatory and should be reserved for recalcitrant cases. Late PPE is more difﬁcult to treat, because the empyema cavity is thickwalled and the bronchial stump is covered by extensive ﬁbrosis, making dissection of the ﬁstula impossible. Although numerous methods are available to close a BPF, the initial operative steps remain the same, no matter how a ﬁstula is closed.

Surgical principles of ﬁstula repair

In our experience waiting until the mediastinum is ﬁxed is not necessary. We prefer immediate operation and immedi-

If a ﬁstula smaller than 3 mm is present, bronchoscopic closure by submucosal injection of ﬁbrin glue should be considered, especially in patients whose condition is too bad to tolerate surgical intervention. Several tries may be necessary until ﬁstula closure is achieved. Bigger ﬁstulas require surgery.

If the patient is ﬁt enough for surgery, immediate operation should be performed, before aspiration occurs. Several different techniques of closure of the bronchial stump have been described; and to date, no option has proven to be superior to the others. Thus, the use of a particular operation depends on the surgeon’s preference.

SIMPLE RE-RESECTION OF THE BRONCHIAL STUMP AND CLOSURE WITH INTERRUPTED SUTURES

This method may be used if the intervention takes place very early, before empyema has occurred. If intrathoracic infection is manifest, the closed stump should be covered.

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The bronchial stump is approached via the original

divided to gain better access to the bronchial stump. On the left side mobilization of the bronchial stump may be difﬁcult due to the fact that it is retracted deeply into the mediastinum. The stump is then isolated from adjacent tissues and reamputated.

thoracotomy. On the right side the azygos vein is

Muscle ﬂap closure of the bronchopleural ﬁstula

Virtually every muscle ﬂap long enough to allow intrathoracic transposition can be used. The most popular techniques comprise the m. pectoralis major, the m. latissmus dorsi, the m. serratus anterior, the diaphragm, and the intercostal muscle.

Only very rarely is the stump long enough to

1b,c

tion, the stump is closed with interrupted sutures (Vicryl, PDS). If the stump is too short to allow re-amputation, ﬁstula closure is technically impossible, or empyema has already occurred, coverage with viable tissue is indicated.

Muscle ﬂaps also can be used from the m. rectus abdominis and the m. erector spinae.

PRINCIPLES OF MUSCLE FLAP CLOSURE

The survival of a muscle ﬂap depends on the preservation of the vascular pedicle contained in its base. Therefore, precise anatomical knowledge of the supplying arteries is crucial. The

allow the use of a stapling device. After amputa-

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vascular pedicle must be identiﬁed during operation so that damage of the vessels is avoided.

To avoid tension, extrathoracic muscle ﬂaps require a route of entry into the thoracic cavity which is facilitated by an additional minithoracotomy combined with rib resection over a length of 5–10 cm. The choice of the rib to be resected depends on which ﬂap is chosen and on the location of the vascular pedicle after completed mobilization of the muscle. The opening for the ﬂap must be big enough to prevent kinking or compression. The ﬂaps are ﬁxed circumferentially around the bronchial stump with interrupted sutures.

Azygos vein

Pulmonary artery

Superior pulmonary vein

INTRATHORACIC MUSCLE FLAPS

The advantage of intrathoracic ﬂaps lies in the fact that no functional impairment of the upper extremity occurs.

DIAPHRAGMATIC MUSCLE FLAP

Except for the rare case of diaphragmatic resection, the diaphragm is always available and is never damaged by thoracotomy. Technically, it is the easiest way to close a BPF with a muscle ﬂap. To approach the diaphragm, an additional thoracotomy two intercostal spaces below the original incision is useful.

The basis of the ﬂap lies at the base of the

of the phrenic artery. The diaphragm is elevated with tension sutures and excised with electrocautery. On the right side care has to be taken not to damage the underlying surface of the liver.

mediastinum thus preserving branches

Inferior pulmonary vein

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The diaphragmatic incision is closed during ﬂap

sutures are removed.

excision with interrupted sutures, before tension

The ﬂap is bent upwards and ﬁxed

interrupted sutures.

around the bronchial stump with

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Operation 221

The lateral margins of the ﬂap are sutured to the mediastinum.

THE INTERCOSTAL MUSCLE FLAP

The advantage of the intercostal muscle lies in the fact that it can reach every position within the thorax, and it has a multiplicity of uses (except in cases of thoracic wall resection). Although ossiﬁcation originating from the periosteum, which is attached to the ﬂap, was reported, this development does not hamper ﬂap function. The pleura covering the intercostal muscle provides an epithelial surface at the site of the tracheal or bronchial repair and should therefore be left in place. When the intercostal muscle is used, the preparation of the ﬂap is the initial procedure because the

rib spreader might damage the neurovascular bundle of the muscle.

Which intercostal space for the ﬂap is chosen depends on the local situation resulting from rib resection, shrinkage of the chest cavity, and reduction of the intercostal spaces due to scarring.

After rib resection, the neurovascular bundle may be damaged, endangering the function of the muscle. If the muscle adjacent to the primary thoracotomy scar is used, it must be considered that scarring of adjacent structures reduces the mobility of the ﬂap.