(Chest. 2005;128:246-249.)
© 2005
American College of Chest Physicians
Surgical Treatment of Thoracic Empyema in HIV-Infected Patients*
Severity and Treatment Modality Is Associated With CD4 Count Status
Shamsuddin Khwaja, MD;
David H. Rosenbaum, MD;
Michelle C. Paul, BS;
Rehal A. Bhojani, BS;
Aaron S. Estrera, MD;
Michael A. Wait, MD and
J. Michael DiMaio, MD
* From the Department of Cardiovascular and Thoracic Surgery, University of Texas Southwestern Medical Center at Dallas, Dallas, TX.
Correspondence to: J. Michael DiMaio, MD, Department of Cardiovascular and Thoracic Surgery, University of Texas Southwestern Medical Center at Dallas, 5323 Harry Hines Blvd, Dallas, TX 75390-8879; e-mail: Michael.Dimaio{at}UTSouthwestern.edu
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Abstract
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Objectives: Patients infected with HIV have an increased propensity for developing thoracic empyemas secondary to their susceptibility to polymicrobial pulmonary infections. We performed an assessment of the clinical outcomes of HIV patients undergoing surgical treatment of thoracic empyemas and reviewed the microbiology of these infections.
Methods: We completed a retrospective analysis of the patients who had been referred for surgical treatment of thoracic empyemas over an 11-year period, ending in 2002. The patients were treated at a major metropolitan medical teaching facility that cares for a substantial number of HIV-positive patients.
Results: Twenty-one HIV-infected patients underwent surgical treatment of thoracic empyemas. There were no immediate deaths. Sixty-two percent of the patients had CD4 counts of < 200 cells/µL. Eight patients had postoperative complications. Six of the patients with complications had CD4 counts of < 200 cells/µL. Patients with lower CD4 counts were at risk for mycobacterial and fungal infections. Additionally, they often had complex empyemas that were not favorable for treatment by video-assisted thoracic surgery. Therefore, these patients often required surgery with lung resection, which necessitated longer periods of postoperative chest tube drainage.
Conclusions: Surgeons can obtain satisfactory operative outcomes when treating thoracic empyemas in HIV patients; however, the treatment strategy should be individualized. Patients with CD4 counts of < 200 cells/µL more commonly have complex empyemas that require surgery with open decortication and drainage. Although these patients have a higher incidence of postoperative complications, we think that HIV patients with thoracic empyemas can be safely and effectively treated with surgical techniques.
Key Words: empyema • HIV • pneumonia • video-assisted thoracic surgery
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Introduction
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Pulmonary complications in HIV-infected patients are commonly associated with high morbidity and mortality rates. The incidence of bacterial pneumonia is estimated at 5.5 per 100 patients and may be as high as 12.5 per 100 hospitalized patients.12 Risk factors for pneumonia in patients with HIV include the following: low CD4 count; IV drug abuse; prior sinusitis; and previous lower respiratory tract infections.2 Empyemas are a more frequent complication of pneumonia in patients with HIV than in those without HIV, and its incidence may be as high as 5.4%.3 The results of the surgical treatment of empyemas in these patients have only been presented in isolated case reports or small case series. We undertook a retrospective analysis of HIV-positive patients who had been treated surgically for thoracic empyemas in order (1) to characterize the patterns of empyemas in HIV-infected patients requiring surgery and (2) to assess the clinical outcomes of surgery in this group of patients with an emphasis on the subset of patients with CD4 counts of < 200 cells/µL.
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Materials and Methods
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We performed a retrospective analysis of HIV-infected patients requiring surgery for thoracic empyemas. The study was conducted predominantly at a large public hospital where approximately 5% of patients who are admitted through the emergency department are positive for HIV. One additional patient from a large metropolitan Veterans Affairs hospital was included in the analysis. We identified 21 patients through the departmental database who were admitted to the hospital between 1991 and 2002 with the dual diagnoses of HIV and empyema. We reviewed the medical records focusing specifically on the operative report, the hospital discharge summary, the laboratory results (including a review of all microbiology culture results), and outpatient follow-up results. The patients were divided into two groups based on CD4 counts of > 200 cells/µL and < 200 cells/µL. We chose this cutoff point because of the increased risk of multiple opportunistic infections when the CD4 count falls to < 200 cells/µL.4 The diagnosis of pneumonia was based on clinical presentation, radiographic findings, and the isolation of microorganisms in the sputum. Thoracic empyemas were diagnosed by the presence of persistent parapneumonic fluid on chest CT scans and/or the results of an analysis of pleural fluid. All patients were receiving treatment with antibiotics prior to surgery. The decision to perform video-assisted thoracic surgery (VATS) was based on the surgeon’s preference. This was influenced by each patient’s overall condition, their ability to tolerate single-lung ventilation, and the appearance of the empyema on imaging studies. All patients underwent complete decortication and empyema drainage. The decision to perform a resection (wedge or lobectomy) was based on the presence of lung necrosis.
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Results
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Of the 21 patients, 19 were men and 2 were women. The mean (± SD) age was 39 ± 9 years (age range, 24 to 61 years). The mean duration of the diagnosis of HIV was 3.8 ± 3.7 years (range, 0 to 10 years). The CD4 count averaged 203 cells/µL (range, 4 to 991 cells/µL). Thirteen patients presented with CD4 counts of < 200 cells/µL. The total viral RNA load averaged 132,000 copies per milliliter of plasma (range, < 400 to 419,000 copies per milliliter of plasma). A new diagnosis of HIV was made in five patients (24%) at the time of presentation with an empyema. Eleven patients (52%) were positive for hepatitis C, and an equal number admitted to a history of IV drug use. The presenting symptoms of patients are shown in Table 1
. The symptoms were similar between the two groups.
A total of 89% of the study patients underwent either thoracentesis or chest tube placement for the drainage of their pleural effusions. We were able to obtain pleural fluid for analysis in 11 of these patients (Table 2
). The results are similar between the two groups. The remaining 11% of patients were referred for surgery without prior drainage based on their medical histories and imaging study findings that were consistent with advanced empyema. One patient had undergone the instillation of streptokinase for fibrinolysis.
The indications for surgery included the presence of empyema on imaging studies with at least one of the following criteria: persistence of fever (ie, temperature, > 101°F) after conservative management (76%); multiloculated pleural fluid collections (71%); and bronchopleural fistula (9%). Eighty-five percent of patients with CD4 counts of < 200 cells/µL had persistent fever as an indication for surgery, and every patient with a bronchopleural fistula had a CD4 count of < 200 cells/µL.
The results of the surgical findings, interventions, and complications in all study patients are presented in Table 3
. A total of eight patients (38%) had complications, and six of these patients had CD4 counts of < 200 cells/µL. There were no deaths within 60 days after surgery. One patient died at a time point beyond 60 days of surgery as a result of other AIDS-related complications. This patient had a CD4 count of < 200 cells/µL. The complications included the following: prolonged mechanical ventilation (ie, > 48 h; three patients), wound drainage/infection (two patients); clotted hemothorax (one patient); persistent fever (one patient); late death (ie, > 60 days postsurgery; one patient); the need for percutaneous drainage of residual pleural fluid (one patient); cardiac arrhythmia (one patient); lung consolidation (one patient); and pulmonary embolus (one patient). Patients with CD4 counts of < 200 cells/µL had increased complication rates when compared to patients with CD4 counts of > 200 cells/µL. The group of patients with lower CD4 counts required additional percutaneous drainage, had prolonged durations of mechanical ventilation, and required tube thoracostomy for prolonged periods.
Table 4
shows the microbiologic data collected from the study patients. The most frequent pathogens were Gram-positive bacteria; however, multiple organisms were isolated in 11 of the 21 patients (65%). Four of the 21 patients (19%) had negative culture findings. One patient was presumed to have an anaerobic bacterial infection and was treated accordingly despite negative culture findings. Fifty percent of the patients had a history of Pneumocystis carinii pneumonia (PCP), while 30% of the patients had a history of tuberculosis (TB). Ninety percent of those patients with PCP had CD4 counts of < 200 cells/µL. Additionally, mycobacterial and fungal infections were associated with CD4 counts of < 200 cells/µL.
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Discussion
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Pulmonary complications in patients infected with HIV are common and are linked with high rates of morbidity and mortality. Epidemiologic data suggest that HIV-infected patients may be more susceptible to pneumonia. The prevalence of pneumococcal pneumonia in a normal host is estimated at 1 to 2.6 per 1,000 patients per year. This number is much higher in patients infected with HIV (18 to 46 per 1,000 patients per year). Patients with HIV also have a higher propensity to have pseudomonal pneumonia, PCP, and TB.12 Additionally, these individuals have an increased susceptibility to pleural infections.5 This may be related to the impaired neutrophil response and reduced recruitment of leukocytes to the lungs and airways in these patients. In experiments with CD4 knockout mice, Staphylococcus aureus injected into the pleural space resulted in a reduced neutrophil response in the pleural space, decreased bacterial clearance, and lower chemokine response.6
Pleural effusions occur in as many as 27% of hospitalized patients who are infected with HIV. Forty-two to 61% of these pleural effusions are associated with infections, while 31% are associated with bacterial pulmonary infections.78
Two studies910 have reported the incidence of empyemas to be in the range from 2.9 to 5.4%. In a study of 23 patients from the Hospital of Seville, Spain, all HIV patients with empyema were found to have a history of IV drug abuse, and in 91% this was the predominant factor leading to their infection.9 Seventy-eight percent of the patients (18 of 23 patients) were treated with chest tube drainage. The total complication rate was 39%, with 5 of the 11 complications related to the chest tubes.
In the study from the Lannec Hospital in Paris, France, nine HIV-infected patients were treated with closed chest tube drainage. There was one death in this group, and the mean (± SD) length of hospital stay averaged 25.6 ± 15 days.10 Nine additional patients underwent surgery for thoracic empyemas. A striking observation was the poor prognosis associated with empyema in the HIV group. The actuarial survival was 10 of 17 patients surviving at 12 months, and only 4 of 17 patients surviving at 36 months. In both studies from Spain and France, > 90% of the infections were secondary to community-acquired organisms.
Previously, we reported that VATS vs chest tube/streptokinase treatment of empyema in non-HIV patients was associated with a lower number of chest tube days, fewer hospital days, a higher treatment success rate, and lower overall cost.11 Therefore, we have favored early surgical drainage in patients referred to us for the treatment of empyemas, either with or without associated HIV infection.12
In our study group of HIV-infected patients, chest tube or needle drainage of the pleural fluid was attempted in 89% of the patients prior to proceeding with surgery. The two most common reasons for surgery were the persistence of fever and the presence of multiloculated pleural effusions.
Compared to the reports from France and Spain, the HIV-infected patients requiring surgery for thoracic empyemas in our group had a larger proportion of pneumonias that were secondary to organisms not commonly found in community-acquired pneumonias. Of note, Gram-positive pneumonias predominated. Observations from our study suggest that HIV-infected patients have a more virulent course of empyema and tend to have a high proportion of multiorganism infection with lung abscess. We think that this contributes to fewer HIV-infected patients undergoing successful treatment with VATS compared to our general experience with the treatment of empyema in non-HIV-infected patients.11
We can draw the following several conclusions from our current study: (1) the surgical treatment of thoracic empyemas in HIV-infected patients with CD4 counts of < 200 cells/µL is associated with a higher number of complications; (2) patients with community-acquired bacterial pneumonia and CD4 counts of > 200 cells/µL are generally more amenable to treatment with VATS; and (3) those HIV-infected patients with PCP, TB, and CD4 counts of < 200 cells/µL are at increased risk of thoracic empyema with lung abscess, often requiring thoracotomy and lung resection. We think that our data suggest that HIV-infected patients with empyema and lack of response to closed drainage can be safely and successfully treated with surgery.
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Acknowledgements
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We would like to thank Jesse Williams for his insightful suggestions and review of the manuscript.
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Footnotes
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Abbreviations: PCP = Pneumocystis carinii pneumonia; TB = tuberculosis; VATS = video-assisted thoracic surgery
Supported in part by National Institutes of Health 5T32GM08593 Training Program in Burns, Trauma and Critical Care and by the Donald W. Reynolds Cardiovascular Research Center.
Presented at CHEST 2002, the 68th Annual International Scientific meeting of the American College of Chest Physicians, San Diego, CA.
Received for publication April 27, 2004.
Accepted for publication January 7, 2005.
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References
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- Noskin, GA, Glassroth, J Bacterial pneumonia associated with HIV-1 infection. Clin Chest Med 1996;17,713-723[CrossRef][ISI][Medline]
- Hernandez, BJ, Alfageme, MI, Munoz, MJ, et al Thoracic empyema in HIV-infected patients: microbiology, management, and outcome. Chest 1998;113,732-738[Abstract/Free Full Text]
- Andreoli, T Bennett, J Carpenter, Cet al eds. Cecil essentials of medicine: HIV infection and the acquired immunodeficiency syndrome 4th ed. 1997,749-767 WB Saunders. Philadelphia, PA:
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- Mohammed, KA, Nasreen, N, Ward, MJ, et al Induction of acute pleural inflammation by Staphylococcus aureus: CD4+ T-cells play a critical role in experimental empyema. J Infect Dis 2000;181,1693-1699[CrossRef][ISI][Medline]
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Abstract
Introduction
