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Ann Thorac Surg 2009;87:869-873. doi:10.1016/j.athoracsur.2008.12.003
© 2009 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Open Window Thoracostomy for Pleural Empyema Complicating Partial Lung Resection

Fabio Massera, MDa,*, Mario Robustellini, MDa, Claudio Della Pona, MDa, Gerolamo Rossi, MDa, Adriano Rizzi, MDb, Gaetano Rocco, MD, FRCS (Ed)c

a Division of General Thoracic Surgery, "E. Morelli" Regional Hospital, Sondalo, Italy
b Division of General Thoracic Surgery, Humanitas Gavazzeni Hospital, Bergamo, Italy
c Department of Thoracic Surgery and Oncology, National Cancer Institute, Pascale Foundation, Naples, Italy

Accepted for publication December 1, 2008.

* Address correspondence to Dr Massera, Viale Curtatone 24, Novara, 28100, Italy (Email: fabiomassera{at}tiscalinet.it).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
Background: Although an open-window thoracostomy (OWT) represents the ideal method for drainage of postpneumonectomy empyema, several controversies exist concerning its application to pleural empyema complicating pulmonary resections less than pneumonectomy.

Methods: Between January 1993 and December 2003, 19 patients (16 male and 3 female) were treated for a pleural empyema complicating partial lung resection. The median age was 62 years (range, 17 to 79). Five patients (26%) had a bronchopleural fistula.

Results: In 2 patients (10%), successful control of the infection was achieved with the OWT. In 10 patients (56%), the OWT was closed by obliteration of pleural cavity with antibiotic solution (2 patients) or intrathoracic muscle transposition (8 patients). OWT closure was successfully performed in all of 5 patients with postoperative pleural empyema due to bronchopleural fistula. Prolonged chest drainage was not successful in any patient with late onset postoperative pleural empyema. Univariate analysis revealed that previous left pulmonary resections (p < 0.05) and timing of OWT (p < 0.001) were significant predictors of empyema healing after pulmonary resections smaller than pneumonectomy.

Conclusions: Immediate OWT is a significant predictor of empyema healing after partial lung resection. Smaller pleural cavities appeared to increase the likelihood of healing. Prolonged chest tube drainage failed to control the infection in late onset of postoperative pleural empyema due to entrapped lung.


   Introduction
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 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Pleural empyema may complicate lung resections in 2% to 8% of cases [1, 2]. Despite a threefold decreased likelihood of an empyema after subtotal lung resections compared with pneumonectomy, the overall mortality can reach a surprisingly high 26% rate [3]. The open window thoracostomy (OWT) represents the ideal method for drainage of the pleural cavity to control the septic symptoms in these patients [3], especially in the presence of bronchopleural fistula, as demonstrated in the majority of patients with postpneumonectomy empyema [4].

However, several controversies exist concerning the resort to OWT for pleural empyema complicating pulmonary resections less than pneumonectomy [5]. We have reviewed our experience concerning the management of pleural empyema complicating partial lung resection with OWT in a 10-year period.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Between January 1993 and December 2003, 50 consecutive patients were treated for a postoperative pleural empyema. Primary operations included 31 pneumonectomies, 15 lobectomies, and 4 segmentectomies. Only patients with an empyema after pulmonary resection less than pneumonectomy were included in this study.

This retrospective study was approved by the Institutional Review Board at the "E. Morelli" Regional Hospital on November 26, 2003, and written informed consent was obtained from each patient entered in the study.

Of a total of 19 patients, 9 (47%) had this complication after 978 pulmonary resections less than pneumonectomy (47 segmentectomies, 827 lobectomies, and 104 bilobectomies) performed at the "E. Morelli" Regional Hospital in the same period, accounting for an overall institutional postoperative empyema incidence of 0.9% and a nil mortality. Conversely, the remaining 10 patients (53%) had been referred from outside institutions.

In this series, there were 16 men and 3 women with a median age of 62 years (range, 17 to 79). Five patients (26.3%) had undergone a bilobectomy. A resection of the lower parenchymal areas was performed in 5 patients whereas upper resection was required in 14 (73.6%). For the purpose of this study, we have classified as "upper" resections the following pulmonary resections: right and left upper lobectomies, right upper bilobectomy, and middle lobectomy. The inclusion of the latter into the upper category was justified by the usually common venous drainage with the upper lobe. "Lower" resections included right and left lower lobectomies and right lower bilobectomies.

Fourteen patients (73.6%) underwent a right-sided pulmonary resection. Histology showed a bronchogenic carcinoma in 10 patients and a benign condition in 9. Among lung cancer patients, a squamous cell carcinoma was found in 7 patients, a carcinoid in 2, and an adenocarcinoma in 1. Stage I disease was found in 9 patients, and stage III in 1 patient. No residual neoplastic tissue was observed. A preventative surgical procedure to decrease residual pleural space after partial lung resection was not performed. No patients had undergone either chemotherapy or radiotherapy. Among benign disease patients, multidrug-resistant Mycobacterium disease was found in 5 patients, aspergillosis in 3, and infected bulla in 1.

The median time between pulmonary resection and pleural empyema was 6 months (range, 12 days to 132 months). If an arbitrary 3 month cut off is used to distinguish between early (within 3 months of surgery) and late onset of empyema after surgery, 7 patients presented with an early onset (median 1 month) and 12 with a late onset (median 12 months) of postoperative pleural empyema. Independently to onset of empyema after surgery, Staphylococcus, Pseudomonas, and anaerobic species were the organisms most frequently isolated from postoperative pleural empyema.

Overall, 5 of 19 patients (26.3%) presented with a bronchopleural fistula (BPF) due to bronchial stump dehiscence.

After diagnosis of postoperative pleural empyema, the treatment of the pleural cavity was performed by chest tube drainage or by immediate resection of two to three rib segments (generally not more than 10 cm in length) and by suturing the skin flaps to the empyema cavity (Fig 1) [6]. According to chest computed tomography, the OWT is planned in the most dependent portion of the empyema cavity (Fig 2).


Figure 1
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  		Fig 1. Window thoracostomy fashioning of "Mercedes-Benz symbol" [6].

 

Figure 2
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  		Fig 2. Chest computed tomography image showing the most depending portion of the empyema cavity after upper right lobectomy.

 
The selected method of empyema management was decided according to the presence of a BPF. If a bronchial stump dehiscence was noted, the pleural cavity was treated with an OWT. At the time of OWT, the bronchial stump was dissected free and closed by directly hand-sewn primary repair reinforced with intercostal muscle flaps. Conversely, postoperative empyema without BPF was managed with prolonged chest tube drainage. In no instances was either an endoscopic treatment of the BPF or a completion pneumonectomy attempted. The success of the treatment was defined by obliteration of pleural cavity after OWT or by the uneventful removal of the chest tube.

Statistics
Given this limited series, only a univariate analysis was performed to determine which factors were associated with the healing of pleural empyema complicating partial lung resection. Unpaired Student's t test was used to compare continuous variables, and Pearson's {chi}2 test was used to assess differences between categorical variables. Data are presented as median values. Statistical significance was accepted for p values less than or equal to 0.05. Finally, a survival analysis was performed to better understand the outcome of the patients with previous lung cancer. Survival was calculated from the date of empyema treatment. The statistical analysis was performed with StatView for Windows software system version 4.5 (Abacus Concepts, Berkeley, CA).


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
The pleural empyema complicating partial lung resection was treated with immediate creation of OWT in 5 patients (26.4%) and with chest drainage in 14 (73.6%). Local control of the infection was satisfactory in all of the 5 patients treated by OWT. The postoperative mortality was nil. After a median time of 5 months (range, 3 to 9), the chest wall was closed. The obliteration of the pleural cavity was achieved with an antibiotic solution in 2 patients (40%) and with intrathoracic transposition of the pectoralis major muscle in 3 (60%).

Conversely, only 2 (14.2%) of the 14 patients treated by chest drainage had a successful outcome. In the remaining 12 patients, the control of the infection was unsatisfactory. Indeed, after a median time of 2 months (range, 1 to 228), an OWT was planned. The creation of an open drainage was delayed in the patients referred from an outside institution. One patient died in the postoperative period of sepsis-related multiorgan failure. However, the delayed creation of OWT was effective in obtaining adequate drainage of the empyema cavity. Nevertheless, the surgical closure was performed after obliteration of pleural cavity with intrathoracic pectoralis major muscle transposition in only 5 patients. Impediments to OWT closure were unavailability of the patient to follow-up (n = 3), tumor recurrence (n = 2), and refusal of further operation (n = 1).

Seven variables were considered for the univariate analysis. The results are shown in Table 1. The significant predictors of higher likelihood of definitive healing of the empyema were the left side of the previous pulmonary resection (p < 0.05) and the immediate creation of the OWT (p < 0.001). The analysis showed an increased probability of empyema healing in males compared with females (44% versus 0%), in patients with previous segmentectomy compared with lobectomy (50% versus 33%), in previous lower compared with upper resection (40% versus 36%), in previous infectious disease (44% versus 30%), and in patients with early onset of pleural empyema after surgery (43% versus 33%). However, these differences were not statistically significant.


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  		Table 1 Predictors of Successful Outcome in 19 Patients With Pleural Empyema Complicating Partial Lung Resection
 
All 5 patients with BPF underwent successful treatment of pleural empyema owing to the immediate creation of OWT (p < 0.001). In fact, longer empyema healing time was related to the timing of OWT. The median time between diagnosis and resolution of pleural empyema was 5 months (range, 1 to 9) for patients treated by immediate OWT, and 8 months (range, 5 to 14) for patients treated by delayed OWT (p < 0.05).

After a median follow-up of 26 months (range, 9 to 109), neither pleural empyema nor BPF recurred in 9 of the 10 patients (90%) with a closed OWT. A recurrent pleural empyema was observed in 1 patient treated by intrathoracic muscle transposition caused by partial necrosis of the muscular flap. A new OWT was fashioned and maintained because the patient declined further surgery. Another 2 patients died of tumor recurrence 24 and 32 months after the OWT, respectively.

The overall survival for patients with previous surgically treated bronchogenic carcinoma was 41% at 5 years. The median survival time was 67 months and 5 months, respectively, for patients with healed and persistent postoperative pleural empyema. Actuarial 5-year survival rates of 7 patients with healed postoperative pleural empyema were 35% for stage I and 40% for stage III. Actuarial 5-year survival rates of 2 patients with persistent OWT were 50% for stage I and 0% for stage III.


   Comment
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
The management strategy for pleural empyema complicating partial lung resection should be focused on the treatment of persistent pleural space and on the closure of BPF other than on the control of infectious disease [7]. Although closed chest tube drainage may be adequate for most patients with pleural empyema [5], nonsurgical treatment modalities with or without intrapleural administration of fibrinolytic agents are ineffective once the empyema is associated with an entrapped lung, as in the cases of late postoperative pleural empyema, or a BPF [8]. In these situations, Lemmer and collegues [3] reported a less than 15% cure rate for patients treated by chest tube drainage alone, yielding 26% of the associated mortality rate.

Treatment of Postresectional Pleural Empyema Due to Entrapped Lung
Although most postoperative pleural empyema occur early after surgery, they can appear at a later date [9]. In our study, an empyema developed in 63% of the patients more than 3 months after subtotal lung resection. The late onset of postoperative pleural empyema is probably due to hematogenous spread of bacteria to the pleura from the lung or from other parts of the body [9].

In contrast to chronic parapneumonic empyema, the surgical release of the entrapped lung (ie, decortication) is rarely indicated because it does not resolve the problem of the residual infected postresectional space for lack of compliance of the residual lobes [10].

Because postoperative residual space may develop more frequently after upper than lower pulmonary resections [11], Hopkins and coworkers [12] suggested the applications of thoracoplasty to the postoperative pleural empyema, reporting a 68% successful obliteration of the pleural cavity. However, a more than 15% postoperative mortality rate [12], and a poor postoperative quality of life reduce its application [13].

Because OWT is effective in obtaining adequate debridement of postpneumonectomy empyema with an acceptable 7% mortality rate [14], Regnard and collegues [15] performed OWT in 16 patients with pleural empyema complicating partial lung resection, and achieved a 85% success rate and nil mortality. Despite that, few others reports have been published about the management of pleural empyema complicating pulmonary resection less than pneumonectomy with OWT [16, 17].

Our current series reinforces the usefulness of open drainage. For as many as 90% of the patients, OWT was effective in obtaining adequate debridement of the empyema cavity. Left side of the previous pulmonary resection and immediate creation of OWT have been proved to be significant predictors of adequate pleural debridement. Although not reaching statistical significance, an increased likelihood of definitive empyema healing has been observed for patients presenting with segmentectomy, lower pulmonary resection, and infectious disease. In these patients, the reduced size of pleural cavity might have contributed to the successful outcome.

To minimize the surgical discomfort of the open drainage, a video-assisted thoracoscopic pleural debridement has been described for the treatment of pleural empyema [18]. However, as more than 60% of the patients had a late onset of pleural empyema after surgery, the narrow and twisting pleural cavity may made thoracoscopic debridement difficult and insufficient [19].

Treatment of Postresectional Pleural Empyema Due to BPF
Since a less than 35% success rate has been reported [20], transbronchial closure of the bronchial stump should be addressed to high-risk surgical patients alone [20]. In 1983, Pairolero and associates [21] suggested a modified Clagett procedure with an immediate muscle transposition to close a postthoracotomy BPF complicating a pleural empyema. In that experience, a 73% successful result was facilitated by the immediate creation of an OWT, as the bronchial stump was easily identified from the surrounding fibrosis and the viability of the muscle flaps was still preserved [21].

In our experience, the closure of BPF by hand-sewn primary repair of the bronchial stump and reinforcement with intercostal muscle flaps was effective in all cases. Furthermore, an immediate OWT was related to a faster resolution of the postoperative pleural empyema. In this setting, the time elapsed between diagnosis and resolution of pleural empyema was 5 months after immediate OWT and 8 months after delayed OWT. Although completion pneumonectomy has been referred as possible treatment of BPF after lobectomy [22], the highest mortality rate (33%) [22] and the hindrance of future resections make unfeasible its application in the treatment of pleural empyema.

Healing of Postresectional Pleural Empyema After OWT
Although the residual pleural space after subtotal lung resection is smaller than after pneumonectomy, and the incidence of BPF after partial lung resection is lower than after pneumonectomy, the process of obliteration of pleural space after OWT alone may take as long as 2 years [23]. Indeed, several authors [15, 21] have suggested the need for further surgery to obliterate the pleural space.

The timing of attempted closure is usually dictated by conditions of the pleural cavity and the prognosis of the patient [16]. When the pleural cavity is clean, as characterized by healthy granulation tissue without gross exudates, the cavity can be closed [7]. In the absence of recurrent cancer, OWT closure should be taken into consideration in view of the improved quality of life offered to the patient [24].

In actual experience, the successful closure of OWT was achieved in 67% patients after lung cancer surgery. Recurrent cancer was a common cause of failure to obtain OWT closure. However, no difference was noted between actual and expected survival rates in patients with either closed or persistent OWT.

If no BPF is noted, the pleural cavity may be filled with antibiotics as per the Clagett postpneumonectomy procedure [25]. Instead, when a persistent BPF is present, an intrathoracic muscle and omental flap transposition may be used to close the bronchial or parenchimal dehiscence and to obliterate the pleural cavity [15, 16]. In accordance with Nomori and coworkers [26], we used the intercostal muscles for the bronchial stump and saved the latissimus dorsi and pectoralis major muscles for the obliteration of the residual space. We have preferred these muscles to omentum because of the risk of laparotomy-related complications [27].

The surgical procedure of OWT closure achieves optimal results in 64% to 85% of patients (Table 2). In our experience, a successful closure has been observed in 9 of 10 patients (90%), with a high success rate (100%) after Clagett's procedure.


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  		Table 2 Results of Open Window Thoracostomy Closure in Patients With Pleural Empyema Complicating Partial Lung Resection
 
In conclusion, nonsurgical treatment modalities may be adequate for most patients in whom postoperative pleural empyema has not associated with entrapped lung, as observed in the late onset of empyema after surgery, or BPF. In late postoperative pleural empyema with or without concurrent BPF, an immediate OWT with bronchial stump reinforcement achieves successful results and shortens the process of obliteration of pleural space. In patients with previously treated lung cancer and good performance status, OWT closure might be scheduled in the absence of disease recurrence regardless of stage-related prognosis. When the pleural cavity shows healthy granulation tissue and no BPF, Clagett's procedure is safe and effective to obliterate the pleural cavity also after subtotal pulmonary resections. Obliteration by muscle flap transposition can be reserved for patients with persistent or recurrent bronchial stump or parenchymal fistulas.


   References
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 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

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