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* From the Division of Transplantation Medicine (Drs. Nunley and Dauber, and Mr. Grgurich) and the Department of Cardiothoracic Surgery (Dr. Keenan), University of Pittsburgh, Pittsburgh, PA.
Correspondence to: David R. Nunley, MD, Critical Care Medicine, University of Pittsburgh Medical Center, 612 Scaife Hall, 3550 Terrace Street, Pittsburgh, PA 15261; e-mail: DDDNunley{at}aol.com
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Abstract |
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Design: Retrospective review.
Setting: University medical center transplant service.
Patients: All recipients (n = 392) of single-lung, double-lung, and heart-lung transplantation between May 1984 and April 1997.
Results: Of the 392 transplant recipients,
empyema was documented in 14 patients (3.6%) at a mean time (± SD)
of 46 days after transplantation (range, 14 to 167 days). Of these 14
recipients with empyema, 4 recipients (28.6%) died of infectious
complications related to empyema. Empyema was seen secondary to
Gram-positive, Gram-negative, and saprophytic organisms; however, there
was no predominance of a particular organism recovered from the
empyemic fluid (
2 = 0.53; p = 0.75). The development
of empyema was not related to whether the transplant was performed
secondary to a septic or nonseptic lung disorder
(2 = 1.06; p = 0.67), nor was it related to the type
of transplant procedure performed (ie, single-lung,
double-lung, or heart-lung allografts; 2 = 4.39;
p = 0.30).
Conclusion: Empyema, a relatively uncommon complication of lung transplantation, is not related to the type of allograft received or to whether the recipient had a septic or a nonseptic lung disorder. If empyema does occur, the mortality associated with this infection is substantial.
Key Words: cystic fibrosis • empyema • heart-lung transplantation • pleura
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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Sixty-eight transplant procedures were performed for patients with septic lung diseases, such as cystic fibrosis (CF), bronchiectasis, or dysmotile cilia syndromes. Of these 68 procedures, 62 procedures were DLTXs, 2 procedures were HLTXs, and the remaining 4 procedures were lobar transplants. Sixty-five of these 68 recipients had at least one sputum culture obtained prior to transplantation. All of the 60 recipients with CF had Pseudomonas spp isolated from the sputum cultures. Of the six recipients with bronchiectasis, the pretransplant sputum cultures revealed Pseudomonas spp in three recipients, and Escherichia coli was found in a fourth recipient. Of the two recipients with dysmotile cilia syndromes, one recipient had Pseudomonas aeruginosa recovered from the sputum, and no predominant organism was identified in the other recipient.
Three hundred twenty-four procedures were performed for nonseptic lung diseases, including emphysema, silicosis, sarcoidosis, pulmonary fibrosis, Eisenmenger's syndrome, and primary pulmonary hypertension (PPH). Seventy-nine of these procedures were HLTXs, 60 were DLTXs, and the remaining 185 were single-lung transplants (SLTXs). Due to the nonpurulence of their respiratory secretions, pretransplant sputum cultures were not performed on transplant recipients with nonseptic lung diseases.
Immediately following transplantation, routine immunosuppression with standard regimens consisted of cyclosporine A or tacrolimus with azathioprine and corticosteroids (initially IV methylprednisolone and later oral prednisone). All of the recipients received empiric IV antimicrobial therapy, and the initial doses were administered intraoperatively. Recipients with septic lung disorders received 10 to 14 days of empiric systemic antimicrobial therapy employing two antibiotics with extended activity against Pseudomonas. Recipients with nonseptic lung disorders received 7 to 10 days of empiric systemic antimicrobial therapy employing two antibiotics that included coverage for Gram-positive organisms (synthetic penicillin or clindamycin), as well as Gram-negative organisms (third-generation cephalosporin). The antibiotic therapy was not altered unless the pretransplant sputum cultures or the cultures taken from the explanted lungs identified a specific organism that required additional coverage.
Drainage of the pleural space was routinely performed following the transplant procedure. If the drainage procedure was uncomplicated, the thoracostomy tubes were removed within the first 7 days following surgery at the discretion of the surgical staff. The subsequent sampling of the pleural space was performed using a thoracentesis or a tube thoracostomy for evidence of pleural fluid on chest radiography associated with clinical features including, but not limited to, fever, elevated WBC count, respiratory compromise, and hemodynamic parameters consistent with sepsis. Empyema was defined as the recovery of grossly purulent material from the pleural space.
Statistical Analysis
All data are expressed as mean (± SD) unless otherwise stated.
The 2 test was employed for comparisons
between nominal variables utilizing 2 x 2 or 2 x 3 contingency
tables. A significant difference was determined at p < 0.05.
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Results |
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In 12 of the 14 transplant recipients with empyema, the organism(s)
responsible for infection in the pleural space were identified (Table 1
). The cultures from two recipients revealed more than one organism.
Saprophytic and atypical organisms as well as Gram-positive and
Gram-negative organisms were identified as causative agents. There was
no difference in the prevalence of Gram-positive, Gram-negative, or
saprophytic organisms (2 = 0.53;
p = 0.75). Of the 68 recipients who received transplants for septic
lung disorders, only 1 (1.5%) developed empyema. This recipient
received a transplant for end-stage lung disease secondary to CF;
however, despite the recovery of purulent material from the pleural
space, no organism was cultured. The empyema in this recipient was
identified and drained on POD 60; on POD 121, the recipient died from a
contiguous pneumonia secondary to P aeruginosa and
Alcaligenes xylosoxidans. Of the remaining 324 recipients
who received transplants for nonseptic lung disorders, empyema occurred
in 13 recipients (4.0%). There was no difference in the prevalence of
empyema in those recipients who received transplants for septic or
nonseptic lung disorders (2 = 1.06;
p = 0.67).
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2 = 4.39; p = 0.30). |
Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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The surgical manipulation of the recipient's native lungs and pleural space during a transplant procedure might be expected to result in seeding of the pleura with potential pathogens. This has been a significant concern when considering transplantation for patients with septic lung disease. To decrease the likelihood of this complication and to decrease the chance of bacteremia (a complication also resulting from manipulation during surgery), preoperative and/or intraoperative antibiotics are often given. Despite this concern and these precautions, only one of our recipients with septic lung disease (CF with a documented Pseudomonas infection) developed empyema after transplantation (at POD 60), which is well beyond the operative period when an infection resulting from seeding of the pleura would be expected. Although there have been anecdotal reports concerning CF lung transplant recipients with empyema involving organisms that had been harbored in the airway prior to transplantation,8 9 10 we are unaware of any reports finding a greater prevalence of empyema in these recipients. Indeed, in our series, when comparing the recipients with septic lung disorders to the recipients with nonseptic lung disorders, the prevalence of empyema did not differ. However, it should be noted that the extended use of perioperative prophylactic antibiotics in recipients with septic lung disorders could have affected these results.
Our experience indicates that there is no prevalent type of organism isolated from Gram-positive, Gram-negative, or saprophytic pleural fluid. This finding is not unexpected, considering the inability to demonstrate an increase in the prevalence of empyema in recipients with septic disorders who were colonized with Gram-negative organisms at the time of the transplant procedure. In addition (despite the anecdotal reports previously described), our finding that empyema did not occur until a mean of 6 weeks following transplant surgery suggests that the development of empyema is not necessarily related to flora infecting or colonizing the native lungs. Thus, it is possible that the development of empyema in these recipients is related to significant immunosuppression in association with events that occur following surgery. Possible events include surgical wound or bronchial anastomosis infection, arterial or venous cannulation, or maneuvers that may traumatize the airway, such as bronchoscopy or mechanical ventilation. Further investigation into these possibilities should be considered. It should be underscored, however, that three of the four deaths attributed to empyema did involve an overwhelming infection with Gram-negative organisms, and the fourth death was associated with a saprophytic infection. No deaths were recorded in recipients with empyema resulting from Gram-positive organisms.
The Toronto experience previously detailed by Herridge et al4 identified empyema as a complication seen exclusively in DLTX recipients. It was suggested that this finding may have been the result of the exposure and manipulation of two pleural spaces in the immunocompromised recipient, thus effectively doubling the surface area available for potential contamination. Our data reveal no difference in the prevalence of empyema when comparing SLTX, DLTX, or HLTX procedures, again suggesting that the development of empyema may not be related to operative or immediate postoperative occurrences, but rather to events that occur later. Again, the choice and duration of prophylactic antibiotic therapy as well as variations in the use of immunosuppressive agents may account for some of these differences.
In summary, our experience suggests that empyema is a complication seen following a small number of transplant procedures; however, when empyema does occur, the associated mortality is relatively high. Empyema usually occurs within the first 6 months following transplant surgery and generally not during the immediate postoperative period. There appears to be no difference in the prevalence of empyema between recipients receiving transplants for septic and nonseptic lung disorders, nor is there a difference when the graft types are compared. Although it is well documented that empyema can develop secondary to Gram-negative organisms that were harbored before transplantation in recipients with septic lung diseases, our data suggest that there is no predominant organism isolated from the empyemic fluid. Other factors that might influence the development of empyema in lung transplant recipients should be considered and investigated.
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Footnotes |
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Received for publication August 11, 1998. Accepted for publication November 30, 1998.
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References |
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This article has been cited by other articles:
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  E. M. Marom, S. M. Palmer, J. J. Erasmus, J. E. Herndon, C. Zhang, and H. P. McAdams Pleural Effusions in Lung Transplant Recipients: Image-guided Small-Bore Catheter Drainage Radiology, July 1, 2003; 228(1): 241 - 245. [Abstract] [Full Text] [PDF]
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