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Ann Thorac Surg 2000;70:1202-1206
© 2000 The Society of Thoracic Surgeons


Original articles: general thoracic

Morbidity and mortality after 94 extrapleural pneumonectomies for empyema

Yuji Shiraishi, MDa, Yutsuki Nakajima, MDa, Akira Koyama, MDa, Keiichiro Takasuna, MDa, Naoya Katsuragi, MDa, Satoko Yoshida, MDa

a Section of Chest Surgery, Fukujuji Hospital, Tokyo, Japan

Address reprint requests to Dr Shiraishi, Section of Chest Surgery, Fukujuji Hospital, 3–1-24 Matsuyama, Kiyose, Tokyo, 204–8522 Japan;
e-mail: yujishi{at}mvb.biglobe.ne.jp

Presented at the Thirty-sixth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 31–Feb 2, 2000.


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Extrapleural pneumonectomy is still indicated in some patients with empyema. We examined morbidity and mortality after this high-risk operation.

Methods. Between 1979 and 1998, 94 (92 chronic, 2 postsurgical) patients with empyema underwent extrapleural pneumonectomy. There were 79 men and 15 women (mean age, 59 years). Eighty-eight patients had a history of tuberculosis, and 53 had undergone a therapeutic pneumothorax. The right side was operated on in 50 patients and left in 44.

Results. Operative mortality was 8.5%. Fifteen major complications (1 esophageal perforation, 9 empyemas, and 5 bronchopleural fistulas) occurred in 13 patients. Eight patients required reexploration for hemorrhage. Reexploration was a risk factor for empyema. Bronchopleural fistulas occurred only on the right side. Eighty-nine percent of the 86 operative survivors were free of empyemas at 5 years. Overall 5-year survival was 83%, and survival was better in patients without than in those with empyema.

Conclusions. Extrapleural pneumonectomy for empyema has acceptable morbidity and mortality. Postoperative empyema affects prognosis. Covering a bronchial stump with muscle is recommended, especially when the operation is performed on the right side.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Empyema remains challenging for thoracic surgeons, particularly when it occurs in a patient with a destroyed lung [1, 2]. Most empyemas are sequelae of active or previous tuberculosis; therefore, the underlying lung has been severely damaged and the empyema is often calcified. A badly damaged lung cannot expand to the degree that it fills up the pleural cavity, even if decortication is completely accomplished. Moreover, the respiratory problems caused by the destroyed lung necessitate resection of the lung. Therefore, complete removal of the empyema and the destroyed lung (ie, extrapleural pneumonectomy) is sometimes required. This procedure is not usually recommended, however, because of its technical complexity and high morbidity and mortality [3, 4]. Some researchers recommend pneumonectomy through an empyema [3], decortication [4], and thoracomyoplasty [5] to reduce postoperative complications, but there is a high rate of postpneumonectomy empyema after pneumonectomy through an empyema [3]. Decortication leaves the destroyed lung intact and uses the lung as a "natural prosthesis" [4]. This is not always feasible, however. For the past 20 years, we have performed extrapleural pneumonectomy in selected patients to completely resect the empyema and the destroyed lung. This study was undertaken to investigate morbidity and mortality after this high-risk operation.


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
We retrospectively analyzed 94 patients (79 men, 15 women; mean age, 59 years [range, 31 to 73 years]) who underwent extrapleural pneumonectomy for empyema at Fukujuji Hospital between 1979 and 1998. Eighty-eight patients had a history of pulmonary tuberculosis or tuberculous pleurisy, and 53 had undergone a therapeutic pneumothorax. Ninety-two patients had chronic empyema, and the remaining 2 patients had postsurgical empyemas resulting from the failure of previous operations performed to treat empyema. One patient had undergone a right lower lobectomy and decortication, and the other, a decortication of the left lung.

Preoperative assessment
The preoperative workup included chest roentgenogram, computed tomography, pulmonary function tests, arterial blood gas analysis, and quantitative perfusion scan. Whenever feasible, bronchoscopy was used to rule out intrabronchial disease and coexisting malignancy. Thoracentesis was performed to find the organism responsible for the empyema. Of the 92 patients with chronic empyema, 24 had no organisms in the empyema space, 18 had pyogenic bacilli, 26 had Mycobacterium tuberculosis (tuberculous), 4 had mycobacterium other than tuberculosis, and 11 had Aspergillus species. In the remaining 9, the empyema space was filled with necrotic substance that had been gathering volume chronically (expansive type). As a preoperative treatment, a chest tube was placed in 25 patients, and an open-window thoracostomy was performed in 14 patients. Forty-seven patients, including those with tuberculosis or mycobacterium other than tuberculosis were treated preoperatively with antituberculosis drugs. From two to four drugs chosen from isoniazid, rifampin, ethambutol, streptomycin, and kanamycin were administered initially. The drug regimens were then adjusted depending on the result of susceptibility testing. The average length of preoperative chemotherapy was 4.7 months (range, 0.3 to 30.9 months).

Indications
The indications for extrapleural pneumonectomy were: (1) the empyema space extended from the apex down to the diaphragm; (2) the underlying lung was destroyed and received less than 10% of the total lung perfusion; (3) decortication did not allow reexpansion of the underlying lung; and (4) the patient had sufficient pulmonary reserve to tolerate a pneumonectomy. Preoperative pulmonary function tests showed that the mean percent of vital capacity was 53.3% ± 12.6% (range, 18.2% to 83.2%) and the average forced expiratory volume in 1 second/vital capacity was 76.8% ± 9.2% (range, 53.7% to 98.1%). Arterial blood gases revealed that the mean arterial oxygen tension was 79.4 ± 9.9 mm Hg (range, 55.2 to 101.9 mm Hg) and the average arterial carbon dioxide tension was 39.4 ± 5.7 mm Hg (range, 22.4 to 64.3 mm Hg).

Operative technique
Before routine use of the double-lumen endotracheal tube, the patient was placed in the prone position to prevent intraoperative spillage of infected material into the contralateral bronchus [6]. We now routinely use the double-lumen endotracheal tube, however, and we perform the operation with the patient in the lateral decubitus position. The posterolateral thoracotomy is made, and the fifth or sixth rib is usually removed. The extrapleural plane is sought, and dissection advances extrapleurally toward the apex, the hilum, and the diaphragm. Care must be taken not to enter the empyema cavity, although it is often difficult to keep the empyema intact throughout the dissection. In patients with the expansive type of empyema, the empyema space is intentionally opened to reduce its bulk. Also, in patients in whom the dissection is especially difficult, the empyema is opened to determine its extent. We liberally use electrocautery and bipolar scissors (PowerStar Bipolar Scissors; Ethicon Inc, Somerville, NJ) during dissection to reduce blood loss. In most cases, a supplementary opening located in the eighth or ninth intercostal space is necessary to facilitate the separation of the parietal peel from over the diaphragm. Pulmonary arteries and veins are severed as in a usual pneumonectomy. The bronchus is divided and closed with sutures or staples. In recent cases, the bronchial stump has been wrapped with the latissimus dorsi muscle. Meticulous hemostasis is again achieved using electrocautery and an argon beam coagulator. The pleural cavity is irrigated with a large amount (more than 10 L) of saline and povidone iodine, and then the chest is drained. In the past, the postpneumonectomy space was irrigated with antibiotic solutions for several days postoperatively, but this irrigation is no longer routinely done.

Follow-up
Follow-up data were obtained from outpatient or hospital charts, or by direct contact with patients or relatives. Follow-up was completed on June 30, 1999, ranging from 0 to 18.8 years (mean, 9.1 ± 5.7 years).

Statistical analysis
Whenever possible, the data were presented as mean ± standard deviation. A {chi}2 test was used for univariate analysis of any correlation between the risk factors and the prevalence of complications. Operative mortality included all deaths clearly related to the operation, regardless of the postoperative interval. Survival and freedom curves were calculated with the Kaplan-Meier method, and differences in curves were analyzed using the log-rank test. A p value less than 0.05 was considered to be statistically significant.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The right side was operated on in 50 patients and the left side in 44. Operating time ranged between 1.9 and 12.2 hours (mean, 5.3 ± 2.6 hours). The average intraoperative blood loss was 3,182 ± 2,693 mL (range, 500 to 15,700 mL). Extrapleural dissection was completed without empyema rupture in 20 patients. In 8 patients, the empyema was inadvertently entered, but only a small amount of the infected material spilled (minor contamination). In 21, the empyema was inadvertently entered, and the pleural cavity was contaminated with the infected material (gross contamination). In 31, the empyema was intentionally opened. In the remaining 14 patients, open-window thoracostomy had been performed before the operation.

There was one intraoperative death. In this patient, the right atrium was torn during dissection and could not be repaired. Four patients died within 30 days of the operation, and another 3 patients died after 30 days. Operative mortality was 8.5% (Table 1). The causes of death were pulmonary embolism in 2 patients, multiple organ failure in 2, arrhythmia in 1, interstitial pneumonia in 1, and heart failure in 1 patient.


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Table 1. Postoperative Complications

 
Eight patients required reexploration to control postoperative hemorrhage. Fifteen major postoperative complications occurred in 13 patients, including 1 esophageal perforation, 5 bronchopleural fistulas, and 9 postoperative empyemas (Table 1). Esophageal perforation occurred in a patient with an esophageal diverticulum, which must have been inadvertently injured during dissection. Bronchopleural fistula occurred in 5 patients undergoing the operation on the right side. In 3 of these 5 patients, the fistulas were not associated with an empyema. These fistulas were successfully treated with extrathoracic muscle transposition in 2 patients and with omentopexy in 1 patient. In the remaining 2 patients, the fistulas were associated with an empyema, and were eventually treated with omentopexy. Seven patients developed a postoperative empyema in the absence of a bronchopleural fistula. Of these, 3 patients died before the space was sterilized. The remaining 4 patients were successfully treated with chest tube drainage and irrigation.

Reexploration was identified as a risk factor for the development of postoperative empyema (p < 0.001) (Table 2). Four of the 8 patients who underwent reexploration developed empyema compared with 5 of the 85 who did not undergo reexploration. The incidence of postoperative empyema was slightly lower in patients who had undergone either chest tube drainage or open-window thoracostomy than in patients without preoperative drainage. Empyema did not occur in patients without contamination during dissection, and 7 of the 9 empyemas that did occur were either in patients in whom the space was intentionally opened or in those with gross contamination. These differences, however, were not statistically significant.


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Table 2. Risk Factors for Postoperative Empyemaa

 
Late empyema occurred in 3 patients, 16 to 44 months postoperatively. Two patients were treated with thoracomyoplasty, and one with open-window thoracostomy. Eighty-nine percent of the 86 operative survivors were free of empyema at 5 years (Fig 1). Overall 1- and 5-year survival was 92% and 83%, respectively (Fig 2). Five-year survival was significantly (p < 0.001) better in patients without postoperative empyema (88%) than in patients with empyema (50%) (Fig 3).



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Fig 1. Kaplan-Meier curve of freedom from empyema for the 86 operative survivors.

 


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Fig 2. Overall Kaplan-Meier survival curve for 94 patients undergoing an extrapleural pneumonectomy.

 


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Fig 3. Kaplan-Meier survival curves for patients without postoperative empyema (Empyema(-), n = 82) and patients with empyema (Empyema(+), n = 12) (p < 0.001, log-rank).

 

    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Empyema is an old problem, but it remains challenging for thoracic surgeons. Its prevalence has declined since the introduction of antibiotic therapy for inflammatory pulmonary and pleural disease [7]. In Japan, however, there are still many patients with empyemas, especially those with chronic empyemas that are sequelae of pulmonary or pleural tuberculosis. Because our hospital started as a tuberculosis sanitarium, we have seen various patients with chronic empyemas, the majority of whom have been successfully treated with decortication, muscle transposition, thoracoplasty, or a combination of these procedures. However, not all patients with an empyema and a destroyed lung can be treated with these lung-preserving procedures because concomitant resection of the underlying lung is sometimes necessary. Therefore, extrapleural pneumonectomy is still indicated in patients who must have a resection of both the empyema and the underlying lung.

Extrapleural pneumonectomy has been used for empyema along with destroyed lung since the era of tuberculosis [1, 2, 8]. However, this procedure is associated with a high incidence of postoperative problems. In the report of Okano and Walkup [1], postoperative empyema developed in 17 of 30 patients undergoing extrapleural pneumonectomy, and 9 were demonstrated to have a bronchopleural fistula. Langston and coworkers [2] also reported that pleural disease extensive enough to require extrapleural pneumonectomy had 21.9% mortality and a 17% empyema rate. In a recent report, the greatest incidence of postoperative complications after pneumonectomy for destroyed lung was observed in patients with a preoperative empyema [9]. Extrapleural pneumonectomy for a destroyed lung is also technically demanding. According to Halezeroglu and coworkers [9], extrapleural dissection was attempted at the beginning of the operation, but it could only be achieved throughout the operation in 9.3% of patients.

It has been suggested, therefore, that extrapleural pneumonectomy should be performed only when absolutely necessary and only in a carefully selected group of patients [10]. In its place, several alternative procedures, such as, pneumonectomy through an empyema [3], decortication [4], and thoracomyoplasty [5], have been advocated to decrease the incidence of postoperative complications. However, pneumonectomy through an empyema results in a high rate (45.7%) of postoperative empyema [3, 11]. Decortication and thoracomyoplasty obliterate the empyema space, but leave the destroyed lung, which cannot cure the respiratory morbidity caused by the underlying lung. The main purpose of decortication in this indication is to use the native lung as a "natural prosthesis" to fill the pleural space and thus avoid extrapleural pneumonectomy [4]. Despite these unfavorable reports of extrapleural pneumonectomy, when there has been no other option, we have performed this radical operation in selected patients with an empyema and a destroyed lung. Drastic measures have been adopted on the basis of our 40 years of experience in treating empyema. We do not agree with Massard and coworkers [4] that extrapleural pneumonectomy might be the choice of an inexperienced surgeon who is unaware of the possibilities of a careful decortication.

It was more than 30 years ago that Langston and coworkers [2] reported 21.9% mortality after pleuropneumonectomy for pleural tuberculosis. Since then, there have been few articles on extrapleural pneumonectomy for empyema and a destroyed lung. In one recent report [9], 60-day mortality was 14.8% when pneumonectomy for a destroyed lung was performed in patients with preoperative empyema. According to a report on pneumonectomy through an empyema, operative mortality was 5.4% [11]. When pneumonectomy is performed for chronic lung infections, operative mortality ranges from 2.4% to 7.6% [9, 1214]. An operative mortality of 8.5% in our study is comparable to that in these reports on pneumonectomy for chronic pulmonary infection.

Postoperative empyema is one of the most serious complications after extrapleural pneumonectomy. There are several possible risk factors for postoperative empyema. In our study, the only significant risk factor for postoperative empyema was reexploration for hemorrhage, which makes the pleural cavity more vulnerable to infection, and, thus, should be prevented with meticulous hemostasis before the chest is closed. Preoperative drainage has been thought to increase the incidence of postoperative empyema. Langston and coworkers [2] reported that complications after pneumonectomy were more likely to occur in patients who had had drainage used as a preliminary measure and who still had a sinus tract at the time of the operation. On the other hand, in our study, preoperative chest tube drainage and open-window thoracostomy slightly decreased the prevalence of postoperative empyema. As some investigators have reported [1, 12, 13], the incidence of postoperative empyema tended to increase when the pleural cavity was contaminated with infected material intraoperatively and when the empyema was intentionally opened. The rate of empyema in our study, however, is still lower than that seen in other studies. In the study of Okano and Walkup [1], 66.7% of patients who had operative contamination developed postoperative empyema. A high incidence of empyema in cases of gross intraoperative pleural spillage has also been reported after pneumonectomy for chronic infection [12, 13]. In addition, the incidence of postoperative empyema was 45.7% in patients who had pneumonectomy through an empyema [3]. Once the empyema has been entered, we routinely irrigate the pleural cavity with a large amount of saline and povidone iodine, until a Gram stain and an acid-fast stain of the pleural fluid were negative. This painstaking intraoperative irrigation reduces the incidence of postoperative empyema.

Bronchopleural fistula can be a major postoperative complication, but our study had a lower incidence of this complication (5.4%) than some other studies. Halezeroglu and co-workers [9] reported that 22.2% of patients with a preoperative empyema developed a bronchopleural fistula after pneumonectomy. When pneumonectomy is performed for chronic lung infection, the prevalence of bronchopleural fistula ranges from 5.6% to 23% [1214]. In our study, bronchopleural fistulas occurred only in patients who were operated on the right side. The development of bronchopleural fistula predominantly in the right-sided operation has also been seen after pneumonectomy for lung cancer [15] and mycobacterioses [16]. The reason for this may be that there is no natural coverage available for the bronchial stump on the right side. We now liberally reinforce the bronchial stump with the latissimus dorsi during a right-sided operation [17]. On the left side, we cover the stump with a muscle flap to protect it from intraoperative contamination.

Langston and co-workers [2] demonstrated that patients who survived the extrapleural pneumonectomy had a good chance for an ultimately satisfactory outcome. In their report, the immediate mortality increased to 36%, with a 28.5% instance of empyema in the survivors. Our results are consistent with the results of their study. The operative mortality was 8.5%, and 89% of the operative survivors were free from empyema 5 years after the operation. Therefore, we suggest that, when necessary, extrapleural pneumonectomy should still be used to treat patients without other options.

In summary, when extrapleural pneumonectomy for empyema is performed in selected patients, it has a fairly acceptable morbidity and mortality. Postoperative empyema leads to a poor prognosis and should be prevented. The reinforcement of the bronchial stump with muscle flaps is advocated, especially on the right side.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Okano T., Walkup H.E. Some problems in extrapleural pneumonectomy for tuberculous empyema and destroyed lung. J Thorac Surg 1958;35:523-531.
  2. Langston H.T., Barker W.L., Graham A.A. Pleural tuberculosis. J Thorac Cardiovasc Surg 1967;54:511-519.[Medline]
  3. Odell J.A., Henderson B.J. Pneumonectomy through an empyema. J Thorac Cardiovasc Surg 1985;89:423-427.[Abstract]
  4. Massard G., Rougé C., Wihlm J.M., et al. Decortication is a valuable option for late empyema after collapse therapy. Ann Thorac Surg 1995;60:888-895.[Abstract/Free Full Text]
  5. Yuste M.G., Ramos G., Duque J.L., et al. Open-window thoracostomy, and thoracomyoplasty to manage chronic pleural empyema. Ann Thorac Surg 1998;65:818-822.[Abstract/Free Full Text]
  6. Conlan A.A., Moyes D.G., Schutz J., Scoccianti M., Abramor E., Levy H. Pulmonary resection in the prone position for suppurative lung disease in children. J Thorac Cardiovasc Surg 1986;92:890-893.[Abstract]
  7. Katariya K., Thurer R.J. Surgical management of empyema. Clin Chest Med 1998;19:395-406.[Medline]
  8. Sarot I.A. Extrapleural pneumonectomy and pleurectomy in pulmonary tuberculosis. Thorax 1949;4:173-223.
  9. Halezeroglu S., Keles M., Uysal A., et al. Factors affecting postoperative morbidity and mortality in destroyed lung. Ann Thorac Surg 1997;64:1635-1638.[Abstract/Free Full Text]
  10. Mouroux J., Maalouf J., Padovani B., Rotomondo C., Richelme H. Surgical management of pleuropulmonary tuberculosis. J Thorac Cardiovasc Surg 1996;111:662-670.[Abstract/Free Full Text]
  11. Odell J.A., Buckels N.J. Techniques of pneumonectomy. Chest Surg Clin N Am 1999;9:369-378.[Medline]
  12. Conlan A.A., Lukanich J.M., Shutz J., Hurwitz S.S. Elective pneumonectomy for benign lung disease. J Thorac Cardiovasc Surg 1995;110:1118-1124.[Abstract/Free Full Text]
  13. Massard G., Dabbagh A., Wihlm J.M., et al. Pneumonectomy for chronic infection is a high-risk procedure. Ann Thorac Surg 1996;62:1033-1038.[Abstract/Free Full Text]
  14. Reed C.E. Pneumonectomy for chronic infection. Ann Thorac Surg 1995;59:408-411.[Abstract/Free Full Text]
  15. Klemperer J., Ginsberg R.J. Morbidity and mortality after pneumonectomy. Chest Surg Clin N Am 1999;9:515-525.[Medline]
  16. Pomerantz M., Madsen L., Goble M., Iseman M. Surgical management of resistant mycobacterial tuberculosis and other mycobacterial pulmonary infections. Ann Thorac Surg 1991;52:1108-1112.[Abstract]
  17. Pairolero P.C., Arnold P.G., Piehler J.M. Intrathoracic transposition of extrathoracic skeletal muscle. J Thorac Cardiovasc Surg 1983;86:809-817.[Abstract]

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