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Ann Thorac Surg 2006;82:288-292
© 2006 The Society of Thoracic Surgeons


Original article: General thoracic

Predictors of Successful Closure of Open Window Thoracostomy for Postpneumonectomy Empyema

Fabio Massera, MD a , * , Mario Robustellini, MD a , Claudio Della Pona, MD a , Gerolamo Rossi, MD a , Adriano Rizzi, MD b , 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 Division of General Thoracic Surgery, National Cancer Institute, Pascale Foundation, Naples, Italy

Accepted for publication November 28, 2005.

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


    Abstract
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BACKGROUND: Although the open window thoracostomy (OWT) represents the ideal method for drainage of postpneumonectomy empyema (PPE), several controversies exist concerning its closure.

METHODS: Between January 1993 and December 2003, an OWT was created in 31 patients (29 male and 2 female) with PPE. The median age was 61 years (range, 32 to 76). In 26 patients (84%) a bronchial stump fistula developed. The OWT closure was correlated with characteristics of PPE and the timing of OWT.

RESULTS: In 15 patients (48%), the OWT could be closed by obliteration of pleural cavity with antibiotic solution (3 patients) or intrathoracic muscle transposition (12 patients). A successful closure was observed in 13 of the 15 patients (87%). All patients closed by Clagett's procedure remained empyema free. Recurrent cancer (n = 4), poor functional status (n = 3), refusal of further operation (n = 2), and persistent tuberculous empyema (n = 2) were common causes of failure of OWT closure. Univariate analysis revealed that the timing of empyema development after surgery (p = 0.02) and the timing of OWT (p = 0.03) were significant predictors of thoracostomy closure.

CONCLUSIONS: Late onset of PPE and immediate OWT creation are significant predictors of OWT closure. Smaller dimensions of the pleural cavity appeared to increase the likelihood of closure. When the pleural cavity shows healthy granulation tissue and no bronchopleural fistula, the Clagett's procedure is safe and effective to obliterate the pleural cavity. Obliteration by muscle flap transposition can be reserved for patients with persistent or recurrent bronchopleural fistula.


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Pleural empyema complicating lung resections occurs in 2% to 16% of the cases and may yield a 40% increase of the associated perioperative mortality rate [1, 2].

The open window thoracostomy (OWT) represents the ideal method for drainage of the pleural cavity to control the septic symptoms in patients with post–pulmonary resection empyema [3–5], especially in the presence of bronchopleural fistula (BPF) as in most patients with postpneumonectomy empyema (PPE) [6]. At a later date, the pleural cavity can be filled with antibiotics [3, 7] or with viable tissue [8, 9] and the OWT closed. However, several controversies exist concerning the closure of OWT [7–9].

We have reviewed our records concerning the management of PPE with OWT, focusing on the indications for and the timing of OWT closure.


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Between January 1993 and December 2003, 48 consecutive patients with post–pulmonary resection empyema underwent OWT. The OWT was performed by resecting two to three rib segments (generally not more than 10 cm in length) and by suturing the skin flaps to the empyema cavity. Primary operations included 31 pneumonectomies, 13 lobectomies, and 4 segmentectomies. Only pneumonectomy patients 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; written informed consent was obtained from each patient.

There were 29 men and 2 women with a median age of 61 years (range, 32 to 76). Nineteen patients (61%) had undergone a right pneumonectomy. Histology had shown a bronchogenic carcinoma in 20 patients, a bronchial hamartoma in 1, and a destroyed lung from infectious disease in 10. Among lung cancer patients, a squamous cell carcinoma was found in 15 patients, an adenocarcinoma in 3, and other cell types in 2. Stage I disease was found in 7 patients, stage II in 2, and stage III in 11. Seven patients had undergone either chemotherapy (n = 3) or radiotherapy (n = 4), in a neoadjuvant (n = 2) or adjuvant (n = 5) setting.

The median time between pneumonectomy and PPE was 1 month (range, 10 days to 132 months). Of the 31 pneumonectomy patients, 24 presented with an early PPE occurring less than 3 months after pulmonary resection (median, 1 months) and 7 with a late PPE (median, 55 months).

After diagnosis of PPE, 6 patients (19.4%) underwent immediate OWT. This group included all PPEs recorded at the "E. Morelli" Regional Hospital during the same 10-year period, during which a total of 246 pneumonectomies were performed with a PPE incidence of 2.4% and a PPE mortality rate of 16.6%.

Conversely, the remaining 25 patients (80.6%) underwent delayed OWT after prolonged chest tube drainage. The median time between tube drainage and OWT was 9 months (range, 1 to 198). The delayed creation of the OWT was decided according to a "cautious PPE management protocol" followed in 19 patients referred from outside institutions and in 6 originally treated at the "E. Morelli" Regional Hospital in Sondalo before 1993. This approach was dictated by different institutional management strategies and not by concurrent major patient comorbidities.

Twenty-six of 31 patients (84%) had a bronchial stump fistula (BPF). Of these patients, 3 (12%) were treated with an immediate OWT. At the time of OWT, the bronchial stump was dissected free and closed with adsorbable suture and then reinforced with intrathoracic transposition of intercostal (2 patients) and serratus anterior muscles (1 patient). In remaining 23 patients (88%), the bronchial stump was not closed because it could not be identified from the surrounding dense fibrotic tissue.

After daily packing, the definitive obliteration of pleural cavity was performed by filling it with antibiotics [3, 7] or by muscle flap transposition (namely, pectoralis major, serratus anterior, or latissimus dorsi) [8, 9]. The closure of the thoracostomy was performed by direct approximation of the musculocutaneous edges [3].

The timing of attempted closure was dictated by the absence of recurrent disease, the overall patient condition, and the healing progress of the pleural cavity. Stage-related prognosis was not considered a factor in the decision-making process.

The selected method of obliteration of the pleural cavity, and chest wall closure was decided according to the cleanliness of pleural cavity and the presence of a BPF. If a closed BPF and healthy granulation tissue were noted, the pleural cavity was filled with antibiotics as per the procedure originally described by Clagett and Geraci [3]. Conversely, the intrathoracic transposition of extrathoracic muscles was used to close an active BPF and to obliterate the residual pleural space. The muscles used for the obliteration of the residual space were chosen by taking into account the damage caused to them by previous operations.

In no instances was an endoscopic treatment of the BPF attempted.

Univariate analysis was performed to determine which factors were associated with OWT closure. 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 value 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 thoracostomy. The statistical analysis was performed with StatView for Windows software system, version 4.5 (Abacus Concepts, Berkeley, California).


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Of the 31 pneumonectomy patients, 15 (48%) underwent closure of the OWT. The chest wall was closed after obliteration of pleural cavity with antibiotic solution in 3 patients (20%) and with intrathoracic muscle transposition in 12 (80%). The pectoralis major muscle was used in 11 of the 12 patients (92%), and pectoralis major plus serratus anterior in 1. In no instance was a tailored thoracoplasty performed.

The postoperative mortality rate for patients undergoing the Clagett's procedure was nil (p = 0.29). Conversely, 1 (8.3%) of the 12 patients undergoing pleural cavity obliteration by muscle flap transposition died of myocardial infarction in the postoperative period.

Although in 9 of the remaining 16 patients the OWT was effective in obtaining adequate drainage of the empyema cavity, the surgical closure was not performed owing to tumor recurrence (n = 4), refusal of further operation (n = 2), poor functional status (n = 2), and cachexia (n = 1). In 6 cases, persistent tuberculous empyema (n = 2) and loss of the patient to follow-up (n = 4) were an impediment to OWT closure. One additional patient died in the OWT postoperative period owing to sepsis-related multiorgan failure.

Seven variables were considered for the univariate analysis. The results are shown in Table 1. The significant predictors of higher likelihood of definitive OWT closure were the late onset of PPE after surgery (p = 0.02), and the immediate creation of the OWT (p = 0.03). The analysis also showed an increased probability of OWT closure in female patients (50% versus 48%), in patients with previous left pneumonectomy (58% versus 42%), with previous infectious disease (50% versus 45%), and in patients undergoing adjuvant chemoradiation therapy (57% versus 46%). However, these differences were not statistically significant.


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Table 1. Predictors of Open Window Thoracostomy Closure of 31 Patients
 
In addition, longer PPE healing time was related to the timing of OWT. Indeed, the median time between diagnosis and resolution of PPE was 3 months (range, 3 to 4) in patients treated by immediate OWT, and 38 months (range, 13 to 97) in patients treated by delayed OWT (p = 0.02).

After a median follow-up of 66 months (range, 5 to 103), neither PPE nor BPF recurred in 13 of the 15 patients (87%) with a closed OWT. All patients closed by Clagett procedure remained empyema free. Conversely, 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 patient died of tumor recurrence 9 months after the OWT.

The overall survival for patients with previous surgically treated bronchogenic carcinoma was 30% at 5 years. The median survival time was 56 months and 12 months for patients with closed and persistent OWTs, respectively. Actuarial 5-year survival rates of 9 patients with closed OWT were 35% for stage I, 100% for stage II, and 40% for stage III. Actuarial 5-year survival rates of 11 patients with persistent OWT were 50% and 0% for stages I and III, respectively.


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Timing of OWT Creation and Closure
Although most PPEs occur early after surgery, they can appear at a later date [10]. In our study, 22% of the patients developed an empyema more than 3 months after pneumonectomy.

In more than 80% of PPE, OWT is effective in obtaining adequate drainage of the empyema cavity [3–6]. As the process of obliteration of pleural space after OWT alone may take up to 2 years [11], several authors [7–9] have suggested the need for further surgery to obliterate the pleural space.

The timing of attempted closure is usually dictated by conditions of pleural cavity and prognosis of the patient [8]. When the pleural space is clean, as characterized by healthy granulation tissue without gross exudate, the cavity can be closed [12]. In our experience, late PPE and immediate OWT have been proved to be significant predictors of OWT closure.

Although not reaching statistical significance, an increased likelihood of OWT closure has been also observed in female patients and in patients presenting with infectious disease, left pneumonectomy, and chemoradiation therapy. In these patients, the reduced size of the pleural cavity might have contributed to the successful closure.

In the event of PPE with BPF, the latter can be closed at the time of the creation of the OWT by hand-sewn primary repair of the bronchial stump and reinforcement with chest wall muscles [7, 12]. However, the closure of BPF at the time of OWT was only achieved in 11.5% of the cases.. After prolonged treatment of PPE with tube drainage, the unsatisfactory control of the infection and the deteriorated patient condition may complicate the closure of BPF at the time of OWT [4]. Indeed, the dissection of the bronchial stump from the surrounding fibrotic tissue was considered hazardous in most of the patients [12]. Furthermore, in these severely ill patients, the poor vascularization of the chest wall muscles increases the incidence of necrosis of the transposed flaps [13].

Accordingly, BPF closure is facilitated by the immediate creation of an OWT, as the bronchial stump can be easily identified from the surrounding fibrosis and the viability of the muscle flaps may still be preserved [14]. Furthermore, in our patients, an immediate OWT was related to a faster resolution of the PPE. In this setting, the time elapsed between performing and closing of OWT was 3 months and 11 months after immediate and delayed OWT, respectively.

The arguments against operative closure of OWT within 2 years of PPE in lung cancer patients are the acceptable probability of spontaneous resolution and the risk of recurrent disease [15]. In this setting, Garcia-Juste and colleagues [8] recommended waiting no less than 6 months between performing and closing the OWT.

In our experience, the successful closure of OWT was achieved in the 45% of 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. As a consequence, we believe that in the absence of recurrent disease, OWT closure should be taken into consideration, especially if the Clagett's procedure can be performed, in view of the improved quality of life offered to the patient. Muscle flap transposition also remains a viable option since the only recurrence of pleural empyema was due to surgical complications, such as flap necrosis.

Methods of OWT Closure
In our opinion, the selected method of OWT closure is based on the presence of a persistent BPF. If no BPF is noted, the pleural cavity may be filled with antibiotics as per the Clagett procedure [3, 5]. Instead, when a persistent BPF is present, an intrathoracic muscle flap transposition may be used to close the bronchial stump and to obliterate the pleural cavity [8, 9]. In accordance with Nomori and associates [16], we used the intercostal and serratus anterior 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 muscle to omentum because of the risk of laparatomy-related complications [17].

The efficacy of intrathoracic muscle transposition depends on the muscle damage caused by previous operations and on the location of the space to be filled [9]. The intrathoracic transposition of previously divided latissimum dorsi and serratus anterior muscles is generally contraindicated [13]. When the primary operation was done through a standard posterolateral thoracotomy, the pectoralis major muscle is harvested to close a BPF and to fill the upper half of the pleural space. The remaining cavity is usually obliterated by the combination of granulation tissue and diaphragmatic elevation [3].

The routine use of a muscle-sparing thoracotomy (namely, in the auscultatory triangle) may allow for further utilization of the undivided chest wall muscles. In addition, the rectus abdominis flap may also be used [16]. However, when a pleural space is judged too large to be filled by muscle flap transposition, a tailored thoracoplasty becomes a viable option [8]. In our clinical practice, we have not used any endoscopic techniques to treat postpneumonectomy BPF [18].

When these principles are respected, the surgical procedure of OWT closure achieves optimal results in more than 70% of patients (Table 2). In our experience, a successful closure has been observed in 13 of 15 patients (87%) with a high success rate (100%) after Clagett's procedure.


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Table 2. Results of Open Window Thoracostomy Closure
 
In conclusion, successful treatment of PPE is based on the creation of an OWT. 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. An immediate OWT with bronchial stump reinforcement shortens the process of obliteration of the pleural space. When the pleural cavity shows healthy granulation tissue and no BPF, the Clagett's procedure is safe and effective to obliterate the pleural cavity. Obliteration by muscle flap transposition can be reserved for patients with persistent or recurrent BPFs.


    Interactive eLearning Activities
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http://learning.ctsnet.org

The Joint Council on Thoracic Surgery Education was pleased to introduce a series of unique eLearning activities to CTSNet users at the AATS annual meeting in Philadelphia. Sponsored by several cardiothoracic surgical groups, this exciting new educational tool contains narrated videos of actual surgical procedures followed by a series of questions and an evaluation to earn Continuing Medical Education credit.

Diagnosis and Management of Complications of Mitral Valve Repair

Off-Pump Coronary Artery Bypass

OPCAB Debriefing

Pediatric Cardiopulmonary Bypass Emergency Situations

Experience these new educational tools today and provide us with your feedback. Go to: http://learning.ctsnet.org .

William E. Baumgartner, Chair

Joint Council on Thoracic Surgery Education

Sponsored By:

American Association for Thoracic Surgery The Society of Thoracic Surgeons European Association for Cardio-Thoracic Surgery Children's Memorial Hospital


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  1. Nagasaki F, Flehinger BJ, Martini N. Complications of surgery in the treatment of carcinoma of the lung Chest 1982;82:25-29.[Abstract/Free Full Text]
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  3. Clagett OT, Geraci JE. A procedure for the management of postpneumonectomy empyema J Thorac Cardiovasc Surg 1963;45:141-145.[Medline]
  4. Lemmer JH, Botham MJ, Orringer MB. Modern management of adult thoracic empyema J Thorac Cardiovasc Surg 1985;90:849-855.[Abstract]
  5. Shamji FM, Ginsberg RJ, Cooper JD, et al. Open window thoracostomy in the management of postpneumonectomy empyema with or without bronchopleural fistula J Thorac Cardiovasc Surg 1983;86:818-822.[Abstract]
  6. Goldstraw P. Treatment of postpneumonectomy empyemathe case of fenestration. Thorax 1979;34:740-745.[Abstract/Free Full Text]
  7. Pairolero PC, Arnold PG, Trastek VF, Kay PP. Postpneumonectomy empyema. A role of intrathoracic muscle transposition J Thorac Cardiovasc Surg 1990;99:958-968.[Abstract]
  8. Garcia-Yuste M, Ramos G, Duque JL, et al. Open-window thoracostomy and thoracomyoplasty to manage chronic pleural empyema Ann Thorac Surg 1998;65:818-822.[Abstract/Free Full Text]
  9. Regnard JF, Alifano M, Puyo P, Fares E, Magdeleinat P, Levasseur P. Open window thoracostomy followed by intrathoracic flap transposition in the treatment of empyema complicating pulmonary resection J Thorac Cardiovasc Surg 2000;120:270-275.[Abstract/Free Full Text]
  10. Schueckler OJ, Rodriguez MI, Takita H. Delayed postpneumonectomy empyema J Cardiovasc Surg 1995;36:515-517.[Medline]
  11. Weissberg D, Refaely Y. Empyema and bronchopleural fistulaexperience with OWT. Chest 1982;82:447-450.[Abstract/Free Full Text]
  12. Deschamps C, Pairolero PC, Allen MS, Trastek VF. Management of postpneumonectomy empyema and bronchopleural fistula Chest Surg Clin North Am 1996;6:519-527.[Medline]
  13. Mathes SJ, Nahai F. Reconstructive sugery. principles, anatomy and technique. New York: Churchill Livingstone; 1997.
  14. Schneiter D, Cassina P, Korom S, et al. Accelerated treatment for early and late postpneumonectomy empyema Ann Thorac Surg 2001;72:1668-1672.[Abstract/Free Full Text]
  15. Postmus PE, Kerstjens JM, deBoer WJ, Homan van der Heide JN, Koeter GH. Treatment of postpneumonectomy pleural empyema by open-window thoracostomy Eur Resp J 1989;2:853-855.[Abstract]
  16. Nomori H, Horio H, Kobayashi R, Hasegawa T. Intrathoracic transposition of the musculocutaneous flap in treating empyema Thorac Cardiovasc Surg 1994;43:171-175.
  17. Scott-Hultman C, Carlson GW, Losken A, et al. Utility of the omentum in the reconstruction of complex extraperitoneal wounds and defectsdonor site complications in 135 patients from 1975 to 2000. Ann Surg 2002;235:786-795.
  18. Hollaus PH, Lax F, Janakiev D, et al. Endoscopic treatment of postoperative bronchopleural fistulaexperience with 45 cases. Ann Thorac Surg 1998;66:923-927.[Abstract/Free Full Text]



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