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Ann Thorac Surg 2008;85:1039-1043. doi:10.1016/j.athoracsur.2007.10.096
© 2008 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

Decortication After Lung Transplantation

Daniel J. Boffa, MDa, David P. Mason, MDa,*, Jang W. Su, MDa, Sudish C. Murthy, MD, PhDa, Jingyuan Feng, MSb, Ann M. McNeill, RNa, Marie M. Budev, DOc, Atul C. Mehta, MDc, Gösta B. Pettersson, MD, PhDa

a Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, Cleveland, Ohio
b Department of Quantitative Health Sciences, Cleveland Clinic, Cleveland, Ohio
c Department of Pulmonary, Allergy, and Critical Care Medicine, Cleveland Clinic, Cleveland, Ohio

Accepted for publication October 30, 2007.

* Address correspondence to Dr Mason, Department of Thoracic and Cardiovascular Surgery, Cleveland Clinic, 9500 Euclid Avenue/Desk F24, Cleveland, OH 44195 (Email: masond2{at}ccf.org).


    Abstract
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Compromise of a pulmonary allograft by restrictive or infectious pleural-space pathology may be amenable to surgical intervention; however, the role of decortication in this patient population has not yet been substantiated. To address this issue, indications and outcomes of decortication after lung transplantation were examined at our institution.

Methods: From February 1990 to December 2006, 553 patients underwent lung transplantation; postoperative decortications were performed 27 times in 24 patients (4.3%).

Results: Indications for decortication included presumed empyema (15), loculated effusion (7), hemothorax (3), and fibrothorax (2). Decortication was performed at a median of 81 days after transplantation (range, 12 days to 7.8 years). Complete lung reexpansion was achieved after 19 of 27 decortications (70%). Infection was cleared from the pleural space in 9 of 15 empyema patients (64%). Survivals at 1, 3, 6, and 12 months after decortication were 85%, 73%, 65%, and 60%, respectively. Operative mortality (30-day or in-hospital) was 23%, and median length of stay was 19 days.

Conclusions: Decortication may alleviate the compromise of a transplanted lung by restrictive or infectious pleural-space disease, but operative risk is substantial.


    Introduction
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Accumulation of fluid and debris in the pleural space is common after lung transplantation and may impair allograft function [1–3]. Percutaneous management strategies, which use a variety of catheters and thoracostomy tubes, have been described previously [4]. Presumably, affected patients who fail less invasive approaches could benefit from surgical intervention; however, the published experience of decortication after lung transplantation is limited to a few case reports [1]. Obliterated tissue planes and the fragility of the transplanted lung pose technical challenges that make decortication less predictable in this patient population. To clarify the role of decortication, indications and outcomes of decortication after lung transplantation were examined within the experience of our single institution.


    Patients and Methods
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Patients
From February 1990 to December 2006, 553 patients underwent single or double lung transplantation for end-stage lung disease at Cleveland Clinic. Data were extracted from the Unified Transplant Registry and supplemental review of medical records, both of which were approved for use in research by the Institutional Review Board, with patient consent waived. Evacuation of hemothorax or drainage of simple pleural effusion was excluded. Decortication was performed in 24 of 553 patients a total of 27 times (4.3%). In two patients, the contralateral pleural space was decorticated during a separate hospitalization. Neither imaging studies nor clinical picture suggested pathology in the contralateral hemithorax at the time of the first decortication. One patient underwent repeat decortication during the same admission because of a refractory empyema. The etiologies of end-stage lung disease were chronic obstructive pulmonary disease (COPD) in seven patients, cystic fibrosis in six, interstitial pulmonary fibrosis in six, pulmonary hypertension in two, pulmonary atresia in one, alpha-1 antitrypsin deficiency in one, and bronchiolitis obliterans in one. Highest grade of transbronchial biopsies performed on patients undergoing decortication was A0 in ten patients, grade A1 in three, grade A2 in nine, and grade A3 in one. One patient underwent biopsy before numeric grading was established by the Lung Rejection Study Group [5].

Yearly follow-ups were obtained for all patients, most of whom received all postoperative care at Cleveland Clinic. Mean follow-up of patient survival after decortication was 1.4 ± 1.5 years; 35 patient-years of data were available for analyses.

Endpoints
Primary endpoint was all-cause mortality. Procedures considered in mortality tabulations included 24 primary decortications as well as two reoperative decortications of contralateral lungs. Reoperation for refractory empyema during the same admission was not included in mortality calculations. Secondary endpoints were lung expansion and clearance of infection. Lung expansion was determined by the surgeon at the time of operation and confirmed by chest radiography. Clearance of infection was judged by clinical evaluation and freedom from reoperation.

Data Analysis
Survival curves were estimated by the Kaplan-Meier method; resulting curves were compared using the log-rank test. A p value less than 0.05 was considered statistically significant.

Decortication
Surgical approaches to the pleural space were through posterolateral thoracotomy (22), video-assisted thoracic surgery (VATS; 3), redo clamshell (1), or sternotomy (1). One patient underwent Clagett window at the time of decortication through a posterolateral thoracotomy [6]. Technical goals of the procedure were clearance of all fluid and debris and expansion of the allograft. An open approach was performed when the surgeon believed a minimally invasive technique could not achieve these goals. Indications for surgery included pleural thickening with signs of lung entrapment documented by computed tomographic (CT) scan and loculations not considered amenable to percutaneous drainage or tube thoracostomy. The most common approach was posterolateral thoracotomy, commencing through the fifth interspace with the creation of an extrapleural dissection. The lung was freed up in its entirety: medially to the mediastinum, superiorly to the apex, inferiorly to the diaphragm, and posteriorly to the hilum. Careful parietal and visceral decortication was continued using a combination of sharp and blunt techniques until the lung was maximally reexpanded (Fig 1). No further attempts were made to obliterate the residual pleural space (such as pleural tenting) in patients whose lungs failed to reexpand in the operating room.


Figure 1
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Fig 1. Operative decortication technique. (A) Illustration of a pulmonary decortication demonstrating the cortex (thick arrow) and underlying normal lung (thin arrow). (B) Photo of a posttransplant decortication demonstrating removal of cortex (thick arrow) from underlying transplanted lung (thin arrow).

 

    Results
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Indications for Decortication
The most common indication for decortication was suspected empyema (15), defined as a purulent pleural space infection. Other indications included loculated effusion (7), hemothorax (3), and fibrothorax (2). Of note, three of four empyemas identified within five weeks of transplant were associated with bronchopleural fistulas.

Timing of Operation
The interval between lung transplantation and decortication ranged from 12 days to 7.8 years (median 81 days). Median interval between transplant and VATS decortication was 25 days, while the interval between transplant and open decortication was 82 days. During this latter interval, more conservative attempts were made to manage the pleural space: thoracentesis (10), tube thoracostomy (7), and fibrinolysis (3).

Lung Reexpansion
Decortication resulted in complete reexpansion of the transplanted lung in 19 of 27 procedures (70%; Table 1). Complete lung reexpansion was more likely in patients undergoing decortication in the early postoperative period. Complete lung reexpansion was observed in 78% (11 of 14) of patients undergoing decortication within 90 days of transplant, compared with 58% (7 of 12) of patients decorticated beyond 90 days.


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Table 1 Decortication Patients
 
Clearance of Infection
Hospital mortality among the empyema patients was 36% (5 of 14), including one patient who twice underwent decortication for empyema. Decortication effectively cleared the infection in the remaining nine patients (64%).

Complications
Median length of stay was 19 days (range, 3 to 102 days). Operative mortality (30-day or in-hospital) for 26 primary decortications (one patient had the same lung decorticated twice) was 23% (6 of 26). Causes of death included sepsis in three patients and multisystem organ failure, brain abscess, and respiratory failure in one patient each. Morbidities included renal failure in 15 patients and new-onset atrial fibrillation in four patients.

Survival
Survivals at 1, 3, 6, and 12 months after decortication were 85%, 73%, 65%, and 60%, respectively. Survival at 3 years was 56% (Fig 2A). Patients undergoing decortication within 90 days of lung transplant had significantly better long-term survival than patients whose interval was greater than 90 days (p = 0.03, log-rank test; Fig 2B).


Figure 2
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Fig 2. Survival after decortication. Kaplan-Meier survival curves of (A) all patients after decortication of a transplanted lung, and (B) patients undergoing decortication within 90 days of transplant (top solid line) or more than 90 days after transplant (bottom solid line). Confidence intervals are shown as dashed lines. The number of patients at risk for death is indicated at several time points along each curve.

 

    Comment
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 
Most pleural complications after lung transplantation can be managed nonoperatively. However, complex and infected fluid collections, as well as fibrothorax, may require surgical intervention [3].

Principal Findings
Indications for decortication
Empyema was the most common indication for decortication in this series. Management options become more invasive as the empyema becomes more organized, ranging from thoracentesis, tube thoracostomy, and fibrinolytics, to VATS and open decortication [7–9]. Patients in this series represent fibrinopurulent and chronic organizing phases typically refractory to nonoperative interventions [10]. Earlier detection of pleural space infections, closer to the time of lung transplant, may reduce the magnitude of secondary procedures as well as the sobering mortality (29% to 36%) [11].

Although VATS has been used to manage loculated effusions and other complex pleural space diseases, only three of our patients were successfully managed with this technique [12]. Pleural symphysis, dense loculations, and fusion of the cortex to the underlying lung precluded a less invasive approach in the current series. Perhaps surgical intervention earlier in the time course would allow more patients to be managed by VATS.

Fibrothorax was the least common indication for decortication. Surgery was performed for two patients whose restrictive scarring was possibly a manifestation of prior episodes of rejection or subclinical infection [13, 14].

Timing of operation
The interval between lung transplant and decortication was highly variable, with many procedures taking place beyond what we would consider the "initial" postoperative period. Delayed presentation of pleural disease is likely multifactorial. Pleural effusions have been shown to present in a delayed fashion after cardiac surgery, particularly coronary artery bypass grafting (CABG), most likely a result of perioperative inflammatory conditions [15]. In one series, pleural surgery was necessary a median of 132 days after CABG [16]. Similar operative conditions may contribute to postoperative pleural effusions after lung transplantation. In addition, allograft infection or rejection at any time after transplant may induce parapneumonic effusion that can rapidly become organized if not adequately addressed.

Lung reexpansion
Decortication has been used to reexpand entrapped lungs in a variety of clinical settings [17]. We found decortication after lung transplantation successfully achieved complete lung reexpansion in the majority of patients. While the small study population precluded identifying predictors of lung reexpansion, two observations relating to chronicity were made. First, patients who underwent decortication within three months of transplant were more likely to achieve lung reexpansion than patients whose transplant to decortication interval exceeded three months. Second, fibrothorax, a process thought to represent the endpoint of a chronic inflammatory process, was not amenable to decortication in this series. The duration of lung entrapment generally leads to more mature pleural fibrosis and tissue ingrowth into the underlying lung parenchyma [18]. As postoperative visits become less frequent, a pleural process may go unchecked, leading to lung entrapment. Early intervention prior to maturation might prevent the need for decortication.

Clearance of infection
Pleural space infection was controlled in most patients, with redo decortication required only once. Mortality, however, was high in this subset of patients, highlighting the importance of intervention prior to the organization of pleural space infections.

Survival
Even though decortication carried high operative mortality and extended length of hospital stay, short- and long-term survivals were reasonable.

Limitations
This represents a small, retrospective study from a single center of heterogeneous pleural space processes selected for decortication. Choice and timing of intervention was surgeon dependent, subjective, and individually made. It is our hope, however, that our experience with decortication after lung transplantation can help guide other surgeons faced with this difficult problem.

Conclusions
Decortication after lung transplantation, albeit technically demanding, is feasible and largely effective. Patients must be carefully selected and potential benefits weighed against high operative mortality.


    References
 Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Backhus LM, Sievers EM, Schenkel FA, et al. Pleural space problems after living lobar transplantation J Heart Lung Transplant 2005;24:2086-2090.[Medline]
  2. Ferrer J, Roldan J, Roman A, et al. Acute and chronic pleural complications in lung transplantation J Heart Lung Transplant 2003;22:1217-1225.[Medline]
  3. Herridge MS, de Hoyos AL, Chaparro C, Winton TL, Kesten S, Maurer JR. Pleural complications in lung transplant recipients J Thorac Cardiovasc Surg 1995;110:22-26.[Abstract/Free Full Text]
  4. Marom EM, Palmer SM, Erasmus JJ, Herndon JE, Zhang C, McAdams HP. Pleural effusions in lung transplant recipients: image-guided small-bore catheter drainage Radiology 2003;228:241-245.[Abstract/Free Full Text]
  5. Yousem SA, Berry GJ, Cagle PT, et al. Revision of the 1990 working formulation for the classification of pulmonary allograft rejection: Lung Rejection Study Group J Heart Lung Transplant 1996;15(1 pt 1):1-15.[Medline]
  6. Clagett OT, Geraci JE. A procedure for the management of postpneumonectomy empyema J Thorac Cardiovasc Surg 1963;45:141-145.[Medline]
  7. Katariya K, Thurer RJ. Surgical management of empyema Clin Chest Med 1998;19:395-406.[Medline]
  8. Thurer RJ. Decortication in thoracic empyema. Indications and surgical technique. Chest Surg Clin N Am 1996;6:461-490.[Medline]
  9. Moran JF. Surgical management of pleural space infections Semin Respir Infect 1988;3:383-394.[Medline]
  10. Bouros D, Schiza S, Patsourakis G, Chalkiadakis G, Panagou P, Siafakas NM. Intrapleural streptokinase versus urokinase in the treatment of complicated parapneumonic effusions: a prospective, double-blind study Am J Respir Crit Care Med 1997;155:291-295.[Abstract]
  11. Nunley DR, Grgurich WF, Keenan RJ, Dauber JH. Empyema complicating successful lung transplantation Chest 1999;115:1312-1315.[Medline]
  12. Striffeler H, Gugger M, Im Hof V, Cerny A, Furrer M, Ris HB. Video-assisted thoracoscopic surgery for fibrinopurulent pleural empyema in 67 patients Ann Thorac Surg 1998;65:319-323.[Abstract/Free Full Text]
  13. Nieminen MM, Antila P, Markkula H, Karvonen J. Effect of decortication in fibrothorax on pulmonary function Respiration 1985;48:94-96.[Medline]
  14. Uyama T, Sakiyama S, Tanida N, et al. Pleural-changes in the lung allograft during acute rejection Transpl Int 1994;7(suppl 1):S399-S401.[Medline]
  15. Heidecker J, Sahn SA. The spectrum of pleural effusions after coronary artery bypass grafting surgery Clin Chest Med 2006;27:267-283.[Medline]
  16. Lee YC, Vaz MA, Ely KA, et al. Symptomatic persistent post-coronary artery bypass graft pleural effusions requiring operative treatment: clinical and histologic features Chest 2001;119:795-800.[Medline]
  17. Doelken P, Sahn SA. Trapped lung Semin Respir Crit Care Med 2001;22:631-636.[Medline]
  18. Huggins JT, Sahn SA. Causes and management of pleural fibrosis Respirology 2004;9:441-447.[Medline]



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