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Ann Thorac Surg 2001;72:1668-1672
© 2001 The Society of Thoracic Surgeons


Original article: general thoracic

Accelerated treatment for early and late postpneumonectomy empyema

Didier Schneiter, MDa, Paulo Cassina, MDa, Stephan Korom, MDa, Ilhan Inci, MDa, Mohammad Al-Abdullatief, MDa, André Dutly, MDa, Peter Kestenholz, MDa, Walter Weder, MD*a

a Division of Thoracic Surgery, Department of Surgery, University Hospital, Zurich, Switzerland

* Address reprint requests to Prof Dr Weder, Division of Thoracic Surgery, Department of Surgery, University Hospital, CH-8091 Zurich, Switzerland
e-mail: walter.weder{at}chi.usz.ch

Presented at the Poster Session of the Thirty-seventh Annual Meeting of The Society of Thoracic Surgeons, New Orleans, LA, Jan 29–31, 2001.


    Abstract
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Postpneumonectomy empyema is a rare but serious complication of pneumonectomy. Despite use of various therapeutic approaches and techniques during the last five decades, successful therapy remains difficult and is often associated with high morbidity and prolonged hospitalization.

Methods. We evaluated a concept for accelerated treatment, which consists of radical debridement of the pleural cavity and packing with wet dressings of povidone-iodine. This was repeated in the operating theater every second day, until the chest cavity was macroscopically clean. If present, bronchial stump insufficiency was closed and secured by omentopexy. Finally, the pleural space was obliterated with antibiotic solution.

Results. Twenty patients, 13 with early postpneumonectomy empyema (10 to 89 days; mean, 37 days) and 7 with late postpneumonectomy empyema (124 to 7,200 days; mean, 1,126 days) were treated. Fifteen patients presented with bronchopleural fistula (11 right, 4 left), which developed after chemotherapy (n = 6) or after radiotherapy (n = 3) (unknown cause in 4 patients). Six patients were referred after previously unsuccessful surgical attempts. Pleural cultures were positive in 17 cases for one or several bacteria including fungoides (n = 2). The average number of interventions was 3.5 (3 to 5). The chest was definitively closed in all patients within 8 days. Mean hospitalization time was 17 days (7 to 35 days). During the same hospitalization, 2 patients needed reoperation because of an undetected bronchopleural fistula. Postpneumonectomy empyema was successfully treated in all patients. There was no in-hospital or 3-month postoperative mortality.

Conclusions. Repeated surgical debridement combined with closure of bronchopleural fistula and antimicrobial therapy enables successful treatment of early and late postpneumonectomy empyema within a short period and is a well-tolerated concept.


    Introduction
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Postpneumonectomy empyema (PPE) is a rare but serious complication with an incidence of 5% to 10%. Seventy-five percent of PPEs occur within the first 3 months of pneumonectomy [1], but it may appear even years after the procedure. In up to 80% of patients, PPE is associated with bronchial stump insufficiency (BSI) [2]. Successful management of PPE with or without BSI continues to be a challenge.

Nearly 40 years ago, Clagett and Geraci [3] introduced a two-stage procedure for treatment of PPE. This procedure combined an open pleural drainage (thoracostomy) with repetitive irrigation of the infected cavity with an antibiotic solution. The procedure has been successful, but resulted in prolonged hospitalization and significant morbidity. Pairolero and associates [4] modified the "Clagett procedure" with initial bronchial stump closure, reinforced with intrathoracic muscle transposition. This proved effective in 84% of cases; however, surgical reinterventions were numerous and the hospitalization time long.

To find a well-tolerated, successful, and accelerated treatment concept for both early and late PPE, with or without BSI, we have further modified the procedure.


    Patients and methods
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Patients
From March 1995 until July 2000, 20 consecutive patients with acute and chronic PPE were treated at our institution. Six of them were referred after one or several unsuccessful surgical attempts from elsewhere (Table 1). One patient had five surgical interventions for empyema after lobectomy for bronchiectasis within 7 years until completion pneumonectomy was performed in 1976. Since then, she had had multiple unsuccessful treatment attempts for chronic empyema. In 1995, she was referred to our institution with an empyema, harboring multiresistant Pseudomonas species, and suffering from a thoracic wall abscess with multiple transthoracic fistulas.


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Table 1. Details of Surgical Interventions in Other Institutions Before the New Concept

 
There were 3 women and 17 men with a mean age of 61 years (range, 34 to 70 years). Eleven patients underwent right pneumonectomy (10 bronchial carcinoma, 1 tuberculosis), 4 were treated with right pleuropneumonectomy (all of them had malignant pleural mesothelioma), and 5 had left pneumonectomy (3 bronchial carcinoma, 2 benign disease; Table 2). Of all patients with PPE, 11 had neoadjuvant (n = 5) or adjuvant (n = 8), either chemotherapy (n = 6) or radiotherapy (n = 3) individually or in combination (n = 2; Table 2).


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Table 2. Details of Patients With Postpneumonectomy Empyema

 
Thirteen patients presented with early PPE defined by an onset of less than 3 months after pneumonectomy (10 to 89 days; mean, 37 days) and 7 with late PPE (124 to 7,200 days; mean, 1,126 days).

Bronchial stump insufficiency was diagnosed in 15 (12 right, 3 left) of the 20 patients (75%). Eight of them had either chemotherapy (n = 6) or radiotherapy (n = 3) individually or in combination (Table 2). The onset of BSI was less than a month (10 to 25 days) in 6 patients, and more than a month (36 to 690 days) in 9 patients after pneumonectomy.

Patients usually presented with the clinical signs of acute or chronic infection including malaise, fever, anorexia, and purulent expectoration, mainly associated with BSI. None of them displayed a full sepsis syndrome with multiorgan failure.

Every patient underwent preoperative or intraoperative fiberoptic bronchoscopy to evaluate the presence of a potential BSI, and chest computed tomography for optimal preoperative planning (Fig 1).



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Fig 1. Computed tomographic image showing an example of chronic empyema. The right chest cavity with thickened pleural layer has shrunken. (* = bronchopleura fistula.)

 
The diagnosis of empyema was made on the basis of the macroscopic appearance of the intrathoracic fluid and the microbiologic findings (microscopy and cultures) in the purulent pleural fluid. Bacteriology of the pleural cavity was positive in 17 patients for one or several microorganisms including fungi (n = 2).

Appropriate systemic antibiotic treatment was initiated preoperatively, in general with tazobactam/piperacillin (Tazobac, Wyeth-Lederle, Zug, Switzerland) or according to the microbiologic findings.

Before surgery 11 of the 20 patients were treated with a closed chest tube drainage for 1 or 2 days. The remaining 9 patients were operated on without preoperative drainage.

The patients were discharged after wound healing and normalization of the inflammatory parameters in the blood tests (white blood cell counts, C-reactive protein).

Operative technique
All 20 patients with PPE were treated in the following way: patients were intubated endotracheally, or with a double-lumen endotracheal tube if a BSI was present, and placed in an anterolateral decubitus position. The previous thoracotomy (generally an anterolateral incision) was reopened, and a radical debridement of the pleural cavity by partial pleurectomy and curettage of all necrotic and fibrous infected tissue was performed and followed with irrigation. The presence of minor BSI was confirmed by flooding the chest cavity with saline and observing escaping air bubbles from the mediastinum. If present, the BSI was closed through various techniques and secured by omentopexy in all but 2 patients (in whom a mediastinal fat patch was used).

If possible, the BSI was closed directly with interrupted sutures using polydioxanone suture (PDS) 4-0 or 3-0 (Ethicon, Johnson & Johnson, Somerville, NJ).

In the rare case of a long stump, the bronchus was closed proximally with a stapler and shortened. In the occasion of a necrotic stump or an open bronchus fixed in the mediastinal plane however, direct closure was not possible. In these cases, the opening was closed with an omental pedicle used as a patch. The pedicle was placed on the stump without tension to cover the opening and fixed with interrupted 4-0 PDS sutures, achieving airtight closure (Fig 2). Laparotomy was performed after the thoracic procedure, subsequent to a change of gloves and gowns and redisinfection of the chest and abdominal region. To expose the omentum, a short upper midline incision was performed, and the omentum was freed from the transverse colon and mesocolon. It was then dissected from the stomach along the greater curvature. Pediculated on the right gastroepiploic artery, it was placed in the pleural cavity through an incision in the diaphragm, and fixed with interrupted sutures at the bronchial wall. In addition, the omentum was fixed to the mediastinum with several sutures.



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Fig 2. Omental flap being used as a patch.

 
At the end of every programmed surgical intervention, until definitive closure could be risked, the pleural cavity was packed with dressings soaked with povidone-iodine solution (diluted 20:1), avoiding a mediastinal shift through overstuffing. By temporarily packing the cavity, the omentum was brought in gentle approximation to the mediastinum, thus supporting the pedicle until definite adherence to the intrathoracic structures had occurred. One chest tube with continuous suction of 5 cm H2O was placed and the thoracotomy closed. The patient was extubated and transferred to the intensive care unit.

Every 48 hours, the antiseptic packing was changed and the surgical debridement repeated in the operating room under general anesthesia until the chest cavity was macroscopically clean.

Patients with a BSI were intubated with a double-lumen endotracheal tube, the others with a conventional tube. Finally, the pleural space was obliterated with an antibiotic solution and the thoracotomy definitively closed.

The instilled antibiotic solution contained 0.3 g of netilmicin, 2.2 g of ampicillin/clavulanic acid, and 1 g of vancomycin per liter of saline. If necessary, additional antibiotic agents or fungicides (0.4 g of fluconazole or 0.05 g of itraconazole) were added to the solution according to the microbiologic cultures.

Parenteral antibiotic treatment started preoperatively was continued.


    Results
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
The mean number of interventions per patient, including reopening of the thoracotomy, transposition of the omentum, debridements, changing of wet dressings, and definitive closure of the chest wall, was 3.5 (3 to 5). In all patients, the chest was definitively closed within 8 days. Three patients developed wound infection, which required local treatment without reopening of the chest. The mean hospitalization time was 17 days (7 to 35 days).

During the initial hospitalization, 2 patients needed reoperation because of an undetected pinhole BSI in the first procedure. Both had a bronchoscopy, and the bronchial stump was checked intraoperatively. They had omentopexy during the second intervention and were discharged within 25 and 30 days.

In 8 patients, BSI was closed directly with interrupted sutures. In 2 patients, the bronchus stump was shortened and stapled. Omentum transposition was performed in 13 of the 15 patients with BSI. In 11 patients, the omentum served as protection after closure of the fistula. In 3 patients, it was used to occlude a wide-open bronchial stump, as direct closure of the BSI was not possible. The presence of BSI did not influence the number of interventions. We did not observe any intraabdominal complications, wound infections, or hernias associated with the laparotomy. In 2 patients, a mediastinal fat patch was used to secure the BSI. Both of them had early pleural fistula with a not heavily infected chest and ample pericardial fat.

The follow-up time ranged from 6 to 60 months (mean, 30 months). There was no in-hospital or 3-month postoperative mortality, nor did we observe any recurrences. Three patients died postoperatively, unrelated to PPE. Two patients succumbed to tumor progression.

The third patient died of graft failure after unilateral lung transplantation. In this case, PPE with BSI were the sequelae of a completion pneumonectomy performed to treat a persisting parenchymal leak, after volume reduction surgery of the autologous, emphysematous lung.


    Comment
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
The development of empyema after pneumonectomy is a devastating complication, especially if associated with BSI. Earlier reported attempts with a two-step procedure described by Pairolero and colleagues [4] had a success rate of 84%, and a mortality of 13%. They needed up to 19 operative interventions (mean 5), however, until definitive closure could be achieved. In our study, we introduce an accelerated treatment regimen for PPE. Thoracotomy, radical debridement, local application of antiseptics, and repetitive scheduled debridement under general anesthesia in the operating theater lead to a rapid and thorough consolidation of this serious complication with a 100% success rate and no mortality within the first 3 postoperative months.

Postoperative BSI as an important causative factor of PPE has become less prevalent with advances in surgical technique. This includes bronchial closure without tension, avoiding a long bronchial stump with excessive peribronchial dissection [5], and covering the stump with mediastinal fat or an intercostal or diaphragmatic muscle flap. Despite all these surgical measures and advances in antimicrobial therapy and perioperative management during the last five decades, the incidence of empyema after pneumonectomy or completion pneumonectomy has stagnated at 5% to 10%.

Major risk factors for PPE are right pneumonectomy, completion pneumonectomy [6, 7], immunosuppression, and neoadjuvant or adjuvant therapy [8]. The reported perioperative mortality ranges from 12% [4] to 40% [1] and is therefore a threat to the patient.

The main cause of deaths in the presence of BSI is pneumonia caused by aspiration, especially in early PPE. In late PPE, stump fistulas are generally small and often partly covered by fibrotic tissue, decreasing the risk of severe aspiration [9]. The prophylactic administration of antibiotics for a longer postoperative period to prevent empyema has been postulated; however, reports on penetration of antibiotics into the postpneumonectomy cavity remain fragmentary [10].

Empyema of the thoracic cavity, after pneumonectomy, comprises a unique infectious entity. As an evacuated, noncollapsible space, filled with bradytrophic tissue after the procedure, it serves as an ideal bed for possible contamination. Treatment of PPE follows the established rules for managing any abscess, and consists of adequate drainage, a parenteral antibiotic regimen, removal of necrotic tissue (ie, debridement), occlusion of fistula, and obliteration of the remaining cavity. Closed chest tube thoracostomy is recommended as a first step in acute situations, but complete drainage of the cavity can only be achieved by thoracotomy.

Choice of the appropriate procedure depends on the duration of the empyema, its clinical severity, and the pathogenicity of the predominant microbiologic strain. Several authors have developed concepts to cope with PPE in regard to its clinical appearance. Early infection has been successfully treated by Gharagozloo and associates [5], who advocated the use of a continuous intrathoracic irrigation system with antibiotic solution; however, these favorable results in such highly selective cohorts have not been reproduced by other groups.

In more advanced empyema, the approach of choice in many centers is based on the procedures described by Clagett and Geraci [3] and modified by Pairolero and coworkers [4]. First, debridement, closure of BSI, and open drainage are undertaken. Second, the pleural space is cleansed and eventually obliterated by daily dressing changes through the thoracostomy. Third—providing that the cavity has been successfully sterilized—the thoracostomy is closed in a second operative procedure. This method, however, achieves only an 80% success rate. It furthermore includes a significant morbidity because of prolonged hospitalization and disabling dressing changes under suboptimal circumstances.

This has prompted us to establish a concept of repeated debridement in the operating theater to optimize and quicken the containment of the empyematous condition. Initially tailored for late and chronic PPE, because of our excellent results we extended this concept to early empyemas as well. In this latter group, the numbers of interventions were low, with usually only one programmed rethoracotomy before definitive closure.

There are several ways to manage a BSI. A fresh, vital stump can occasionally be directly closed by interrupted sutures or stapler and reinforced with a transposed muscle flap or an omental or mediastinal fat patch.

A long bronchial stump can be dissected up to the carina, and shortened to allow a direct suture or stapled sealing, and again reinforced by well-vascularized tissue.

For patients with older fistulas, or after bronchial resection near the carina, direct closure without tension is generally not possible. Here we favor the use of an omental pedicle as a patch. A muscle may also be used to close the opening. The omentum is suitable because of its extendibility and good adherence to an inflammatory area, its well-documented ability of neovascularization, and its immunologic properties. Omental transposition causes neither a functional nor aesthetic loss, in contrast to various muscle transposition procedures.

We were initially hesitant to access a second cavity after treating empyema of the chest. Nevertheless, adhering to a strict code of glove and gown change before performing laparotomy, and under systemic administration of antibiotics, we never encountered any infectious abdominal complications postoperatively.

Using our concept, the chest could be closed definitely in all 20 patients within 8 days without recurrence of empyema or BSI. All but 1 patient (after lung transplantation) were discharged after a mean hospital stay of 17 days. It is noteworthy that accelerated treatment did not increase morbidity. We saw no deaths related to our procedure within the first 3 months postoperatively. Reviewing the literature, in which mortality rates of up to 9% to 13% [4, 11] are being reported after surgical treatment of PPE, we attribute our mortality results to the consequence of performing these steps in a sequential and standardized fashion, treating each revision as an independent operative step in which maximum gain in surgical debridement is paramount.

Aside from these convincing results, there are additional advantages of accelerated PPE management. Between debridements, which take place in the operating theater, there are no painful dressing changes on the ward. Because the chest is closed and is water- and airtight, respiratory mechanics are not impaired, and mediastinal shift does not occur. Patients also remain mobile and profit from physiotherapy. Our procedure greatly improves independent bodily hygiene and spares patients the burden of an open chest wound.

In some of our cases, it might have been possible to have achieved successful healing whereby fewer surgical interventions would have been sufficient. Given the fact, however, that the operation was very well tolerated in all our patients, and that a failure could be a major drawback, we decided to adhere to the initiated regimen.

Taking into account that more than 50% of patients suffering from PPE in our study had been treated in adjuvant or neoadjuvant protocols, and considering the current trend to operate on bronchial carcinoma and mesothelioma after neoadjuvant therapy, the incidence of PPE will most likely not decrease in the near future.


    Acknowledgments
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 
Supported by the Sonnenwiese-Stiftung.


    References
 Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Shamji F.M., Ginsberg R.J., Cooper J.D., 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]
  2. Wain J.C. Management of late postpneumonectomy empyema and bronchopleural fistula. Chest Surg Clinic 1996;6:529-541.
  3. Clagett O.T., Geraci J.E. A procedure for the management of postpneumonectomy empyema. J Thorac Cardiovasc Surg 1963;45:141-145.
  4. Pairolero P.C., Arnold P.G., Trastek V.F., Melant N.B., Kay P.P. Postpneumonectomy empyema. The role of intrathoracic muscle transposition. J Thorac Cardiovasc Surg 1990;99:958-968.[Abstract]
  5. Gharagozloo F., Trachiotis G., Wolfe A., DuBree K.J., Cox J.L. Pleural space irrigation and modified Clagett procedure for the treatment of early postpneumonectomy empyema. J Thorac Cardiovasc Surg 1998;116:943-948.[Abstract/Free Full Text]
  6. Asamura H., Naruke T., Tsuchiya R., Goya T., Kondo H., Suemasu K. Bronchopleural fistula associated with lung cancer operations. J Thorac Cardiovasc Surg 1992;104:1456-1464.[Abstract]
  7. Wright C.D., Wain J.C., Mathisen D.J., Grillo H.C. Postpneumonectomy bronchopleural fistula after sutured bronchial closure: incidence, risk factors and management. J Thorac Cardiovasc Surg 1996;112:1367-1371.[Abstract/Free Full Text]
  8. Frytak S., Lee R.E., Pairolero P.C., Arnold P.G., Shaw J.N. Necrotic lung and bronchopleural fistula as complications of therapy in lung cancer. Cancer Invest 1988;6:139-143.[Medline]
  9. Hollaus P.H., Lax F., El-Nashef B.B., Hauck H.H., Lucciarini P., Pridun N.S. Natural history of bronchopleural fistula after pneumonectomy; a review of 96 cases. Ann Thorac Surg 1997;63:1391-1397.[Abstract/Free Full Text]
  10. Padberg W.M., Jager E., Buhr J., Zimmermann T. Ciprofloxacin levels in pleural fluid and serum during systemic administration after pneumonectomy. Zentralbl Chir 2000;125:450-453.[Medline]
  11. Pukas J.D., Mathisen D.J., Grillo H.C., et al. Treatment strategies for bronchopleural fistula. J Thorac Cardiovasc Surg 1995;109:989-995.[Abstract]



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