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(Chest. 2000;117:1031-1037.)
© 2000 American College of Chest Physicians

Pleural Effusion and Pneumothorax in Hospitalized Patients With HIV Infection*

The Pulmonary Complications, ICU Support, and Prognostic Factors of Hospitalized Patients With HIV (PIP) Study

Bekele Afessa, MD, FCCP

* From the Department of Internal Medicine, Division of Pulmonary and Critical Care, University of Florida Health Science Center, Jacksonville, FL.

Correspondence to: Bekele Afessa, MD, FCCP, Division of Pulmonary and Critical Care Medicine, Department of Medicine, Mayo Clinic, 200 First St SW, Rochester, MN 55905.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objectives: To describe the incidence, causes, and impact of pleural effusion and pneumothorax in hospitalized patients with HIV infection.

Design: Prospective, observational.

Setting: A university-affiliated medical center.

Methods: During a 3-year period, 599 HIV-infected patients with a total of 1,225 consecutive hospital admissions were followed. A total of 1,097 hospital admissions were included. Patients’ medical records, chest radiographs, and computerized laboratory values were reviewed.

Results: Pleural effusions developed in 160 hospital admissions (14.6%). The effusions were right sided (56%), left sided (29%), and bilateral (15%). Their sizes were small (65%), moderate (23%), large (9%), and massive (4%). The associated conditions were infectious: bacterial pneumonia (n = 50), pulmonary tuberculosis (n = 10), Pneumocystis carinii pneumonia (PCP; n = 5), and empyema (n = 2); and noninfectious: renal failure (n = 15), hypoalbuminemia (n = 12), malignancy (n = 9), pancreatitis (n = 7), hepatic cirrhosis (n = 5), congestive heart failure (n = 4), atelectasis (n = 3), pulmonary embolism (n = 3), trauma (n = 1), and surgery (n = 1). Pneumothorax developed in 13 hospital admissions (1.2%). The conditions associated with pneumothorax were iatrogenic (n = 4), bacterial pneumonia (n = 3), PCP (n = 2), positive pressure ventilation for PCP (n = 2), pulmonary Mycobacterium avium complex (n = 1), and trauma (n = 1). The in-hospital mortality of hospital admissions with pleural effusion was 10.0% compared to 5.4% of those without pleural effusion (p = 0.0407). The in-hospital mortality of hospital admissions with pneumothorax was 30.8% compared to 5.8% of those without pneumothorax (p = 0.0060).

Conclusions: Pleural effusions occur in 14.6% of hospital admissions in our patient population with HIV infection. Bacterial pneumonia is the condition most commonly associated with pleural effusion. Pneumothorax, seen in 1.2% of hospital admissions with HIV infection, is associated with poor outcome.

Key Words: AIDS • bacterial pneumonia • empyema • HIV infection • pleural effusion • Pneumocystis carinii pneumonia • pneumothorax


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The number of patients with HIV infection has been increasing worldwide. Pulmonary complications, which have remained common in these patients, and nonpulmonary diseases can lead to pleural effusion and pneumothorax. The incidence of pleural effusion in hospitalized patients with HIV infection ranges from 1.7 to 27%.1 2 The conditions associated with pleural effusion vary from place to place and according to differences in exposure category. Although most studies have shown that bacterial pneumonia is the most common cause of pleural effusion in HIV-infected patients,1 2 Kaposi’s sarcoma was a more common cause of pleural effusion than bacterial pneumonia in one study.3 Bacterial pneumonia and pulmonary tuberculosis can cause spontaneous pneumothorax in patients with HIV infection.4 5 However, the majority of the spontaneous pneumothoraces in HIV-infected patients are associated with Pneumocystis carinii pneumonia (PCP).6 7 8

The development of pneumothorax in patients with HIV infection, especially in the setting of PCP and mechanical ventilation, is associated with poor outcome.9 10 However, the impact of pleural effusion on patient outcome has not been well studied. The Pulmonary Complications, ICU Support, and Prognostic Factors of Hospitalized Patients With HIV (PIP) Study is a single-center, prospective, observational study that was designed to describe the types of pulmonary complications and the role of critical care support and to determine the prognostic factors of hospitalized HIV-infected adults. This article describes the prevalence of pleural effusion and pneumothorax, as well as the conditions associated with them, and their impact on outcome of hospitalized patients with HIV infection.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
This prospective, observational study was performed at the University Medical Center, Jacksonville, FL, during the 3-year period from April 1995 through March 1998. The University Medical Center is a 528-bed, teaching, inner-city hospital affiliated with the University of Florida. The Institutional Review Board of the hospital waived the need for informed consent. A total of 1,225 consecutive hospital admissions of 599 adults with HIV infection were noted during the study period. After excluding 128 hospital admissions of patients who did not have chest radiograph during their hospital stay, 1,097 hospital admissions were included in this study.

Patients’ medical records and their computerized laboratory values were reviewed. The data collected included demographics, risk factor for HIV infection, the presence of congestive heart failure (CHF), liver failure and renal failure, WBC count and differential, serum albumin, serum protein, serum lactate dehydrogenase (LDH), and CD4+ lymphocyte count. The APACHE (acute physiology and chronic health evaluation) II score was calculated for each hospital admission.11 The microbiological and histologic findings of sputum, bronchoscopic specimen, lung biopsy, and pleural tissue were reviewed. If pleural fluid was obtained, the cell count, WBC differential, protein, LDH, cytology, and microbiology results were noted. Exudative pleural effusion was defined by the presence of at least one of Light’s three criteria: pleural fluid/serum protein ratio > 0.5, pleural fluid/serum LDH ratio > 0.6, and pleural fluid LDH greater than two-thirds the upper limit of normal for serum LDH.12

The investigator, a pulmonologist, reviewed all chest radiographs. The presence of pleural effusion and pneumothorax was noted. For the most part, the method of Joseph et al2 was followed to assess the size of and conditions associated with the pleural effusion. The size of the pleural effusion on chest radiograph was considered small if the costophrenic angle was blunted, moderate if the lower zone was completely opaque, large if the lower and middle zones were opaque, and massive if all three zones were opaque.

A parapneumonic effusion was diagnosed based on the presence of the following: (1) new or worsening infiltrate on chest radiograph; (2) temperature > 38.0°C (100.4°F) or < 36.0°C (96.8°F); (3) leukocyte count > 12,000 cells/µL or < 4,000 cells/µL or bandemia > 10%; and (4) sputum Gram stain or culture showing a bacterial organism in a purulent sputum, or quantitative culture of BAL showing bacteria >= 104 colony-forming units/mL, or the isolation of a likely pathogen from blood or pleural fluid, or urine positive for Legionella pneumophila antigen. Purulent sputum was identified by the presence of WBC > 25/low power field and epithelial cells < 10/low power field. Empyema was diagnosed when pus was aspirated from the pleural space, or if the pleural fluid culture was positive for a pathogen. Nocardiosis was diagnosed with the recovery of the organism from sputum or BAL. PCP was diagnosed if the organism was identified in sputum, BAL, or lung tissue. Tuberculous effusion was diagnosed if the organism was isolated from the pleural fluid or tissue. Tuberculous pneumonia was diagnosed by the isolation of the organism from respiratory tract specimen or lung tissue. Kaposi’s sarcoma was diagnosed by pathologic results or bronchoscopic findings, atelectasis when there were compatible chest radiographic findings, CHF when the effusion improved with treatment in the appropriate clinical setting, and hypoalbuminemia when serum albumin was <= 1.8 g/dL and no other cause for effusion was found.

The length of hospital stay, ICU admission status, and mortality were noted.

StatView 5.0 computer software (SAS Institute; Cary, NC) was used for statistical analyses. Multiple hospital admissions of the same patient were analyzed independently of each other. All means are expressed with their standard deviations. Comparisons between groups were made using multiple logistic regression analysis, Student’s t test, Mann-Whitney U test, {chi}2, and Fisher’s Exact Test. The continuity-corrected p values were used for {chi}2 analysis. The p values < 0.05 were considered significant.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
A total of 160 of 1,097 hospital admissions (14.6%) had pleural effusion on chest radiograph. The differences in age, gender, race, exposure category for HIV, APACHE II score, serum albumin level, and CD4+ lymphocyte count between hospital admissions with and without pleural effusion are listed in Table 1 . The APACHE II predicted mortality rate was 29% for hospital admissions with pleural effusion, compared to 23% for hospital admissions without pleural effusion (p = 0.0001). Twenty-one percent of the hospital admissions with the risk factor of injection drug use had pleural effusion, compared to 7% of the hospital admissions with the risk factor of heterosexual contact (p = 0.0001) and 10% of the hospital admissions with the risk factor of homosexuality (p = 0.0097). Of the 160 effusions, 89 were right sided (56%), 47 were left sided (29%), and 24 were bilateral (15%). In addition, 104 of the effusions were small (65%), 36 were moderate (23%), 14 were large (9%), and 6 were massive (4%). The conditions associated with the pleural effusions are listed in Table 2 . Pleural effusions were present in 52 of 111 hospital admissions (47%) with bacterial pneumonia, 5 of 85 hospital admissions (6%) with PCP, and 10 of 40 hospital admissions (25%) with pulmonary tuberculosis. Pleural fluid analysis results, available in 11 hospital admissions of 11 different patients, suggested exudate in all 11. Mycobacterium tuberculosis was isolated from the pleural effusion of three patients. The WBC counts in the pleural fluid of the patients with pleural M tuberculosis were 640, 1,028, and 1,220/µL; neutrophils were 73, 3, and 72%; lymphocytes were 12, 92, and 14%; and macrophages were 15, 5, and 14%, respectively.


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  		Table 1.. Differences in Demographics, Exposure Categories, Serum Albumin, CD4+ Lymphocyte Count, and APACHE II Score Between Hospital Admissions of Patients With and Without Pleural Effusion*

 

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  		Table 2.. Conditions Associated With Pleural Effusion in Hospitalized Patients With HIV

 
The length of hospital stay of hospital admissions with pleural effusion was 7.6 ± 8.2 days (median, 5 days), compared to 6.4 ± 6.4 days (median, 4 days) of hospital admissions without pleural effusion (p = 0.0064). Twenty-three of 160 hospital admissions (14%) with pleural effusion were admitted to ICU, compared to 106 of 937 hospital admissions (11%) without pleural effusion (p = 0.3277). The in-hospital mortality rate was 10.0% for hospital admissions with pleural effusion, compared to 5.4% for hospital admissions without pleural effusion (p = 0.0407). Multiple logistic regression analysis showed that higher severity of illness, assessed by APACHE II predicted mortality rate, correlated with increasing observed in-hospital mortality (odds ratio [OR], 1.06; 95% confidence interval [CI], 1.04 to 1.07). However, the presence of pleural effusion was not an independent risk factor for increased mortality (OR, 1.5; 95% CI, 0.8 to 2.8).

Pneumothorax developed in 13 different patients of the 1,097 hospital admissions (1.2%). Pleural effusion was present in 6 of 13 patients with pneumothorax. The mean age of these 13 patients was 34.1 ± 5.8 years; 8 patients were male and 5 were female; 9 patients were African American and 4 were white. The risk factors for HIV infection were injection drug use in three patients, homosexuality in two patients, commercial sex work in one patient, and unidentified in seven patients. Their CD4+ lymphocyte count was 93 ± 143/µL (median, 35/µL). Their APACHE II score was 17.8 ± 9.3 (median, 16) and predicted mortality was 30%. Eight of the pneumothoraces were left sided, three were right sided, and two were bilateral. The most common condition associated with the development of pneumothorax was iatrogenic: central line placement (n = 2), thoracentesis (n = 1), and surgery (n = 1). The other conditions associated with pneumothorax were bacterial pneumonia (n = 3), positive pressure mechanical ventilation for PCP (n = 2), PCP without positive pressure ventilation (n = 2), pulmonary Mycobacterium avium complex (n = 1), and chest trauma (n = 1). Two patients had bilateral pneumothoraces, and both had PCP. The incidence of pneumothorax in hospital admissions with PCP was 4.7%. Chest tube drainage was required in seven patients for pneumothorax and in two patients for empyema. After the failure of chest tube drainage, surgical pleurodesis was required in one patient with PCP-associated pneumothorax. The median length of hospital stay for hospital admissions with pneumothorax was 9 days, compared to 5 days for hospital admissions without pneumothorax (p = 0.0029). Seven of 13 hospital admissions (54%) with pneumothorax were admitted to the ICU, compared to 122 of 1,084 hospital admissions (11%) without pneumothorax (p < 0.0001). The in-hospital mortality rate of hospital admissions with pneumothorax was 30.8%, compared to 5.8% of hospital admissions without pneumothorax (p = 0.0060). Multiple logistic regression analysis showed that both the presence of pneumothorax (OR, 7.5; 95% CI, 1.8 to 30.7) and APACHE II predicted mortality (OR, 1.06; 95% CI, 1.04 to 1.07) were independently associated with in-hospital mortality.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This study describes the incidence of pleural effusion and pneumothorax in 1,097 consecutive hospital admissions of patients with HIV infection. Pleural effusions were noted in 14.6% of the hospital admissions. The reported incidence of pleural effusion among hospitalized patients with HIV infection has varied from study to study. In a series of 4,511 HIV-seropositive patients hospitalized in a hospital in New York City, the prevalence of pleural effusion was 1.7%.1 In another study of 222 hospitalized patients with AIDS, pleural effusions occurred in 27%.2 Two other studies have shown the prevalence of pleural effusion to be 7.2% and 8.5%, respectively, among hospitalized patients with HIV infection.13 14

The reasons for these differences are not clear. The variations in the study designs, geographic locations, and patient characteristics may partly explain them. Similar to the study by Joseph et al,2 no significant differences were found in age and sex between patients with and without pleural effusion in the PIP study. However, the prevalence of pleural effusion was higher in patients with the risk factor of injection drug use, compared to homosexuality and heterosexual contact in the PIP study. Contrary to the study by Joseph et al,2 the CD4+ lymphocyte count of patients with pleural effusion was higher, compared to the CD4+ lymphocyte count of patients without pleural effusion in the PIP study. Despite the higher CD4+ lymphocyte count, the lower serum albumin level and higher APACHE II score indicate the overall higher disease severity in the patients with pleural effusion. Differences in severity of illness may be partly responsible for variations in the incidence of pleural effusion among different studies.

Eighty-eight percent of the pleural effusions were either small or moderate in size in the PIP study. This result is similar to previous findings: 17 of 21 effusions in the study by Venkatram et al13 and 50 of 59 pleural effusions in the study by Joseph et al2 were either small or moderate in size. Diagnostic thoracentesis is performed in 24 to 38% of hospitalized patients with HIV infection.1 2 Pleural fluid analysis was done only in 7% of the patients with pleural effusion in the PIP study, suggesting a less aggressive diagnostic approach.

Several investigators have examined the conditions associated with pleural effusion in patients with HIV infection. These conditions may vary according to geographic location and the predominant risk factor for HIV infection of the study population. Bacterial pneumonia is the most common condition associated with pleural effusions in HIV-infected patients in the United States.1 2 However, Kaposi’s sarcoma was the cause of the pleural effusion in 52% of 62 patients in one study from Paris.3 In HIV-infected patients from underdeveloped countries, tuberculosis is the most common cause of pleural effusion.15 Bacterial pneumonia was the most common identified condition associated with pleural effusion in the PIP study. This is not surprising, because bacterial respiratory infections are very common in patients with HIV.16 17 18 The incidence of parapneumonic effusion is also higher in HIV-positive patients, compared to HIV-negative patients with community-acquired pneumonia.19

Tuberculous pleurisy is more common in AIDS than in non-AIDS patients with tuberculosis.20 Among patients with M tuberculosis and HIV coinfection, patients with pleural effusion have higher CD4+ lymphocyte counts than do patients without pleural effusion.21 In the PIP study, M tuberculosis was isolated from the pleural fluid in three, and from the sputum or BAL in seven other patient admissions with pleural effusion. In the study by Frye et al,20 the mean WBC count of tuberculous pleural effusions in HIV-infected patients was 4,000 cells/µL with lymphocytic predominance. Another study has shown the WBC count in tuberculous pleural effusion to range from 20 to 16,250 cells/µL, with a median of 720 cells/µL.22 In the PIP study, the WBC count in pleural fluid ranged from 640 to 1,220/µL, and only one of the three patients had lymphocytic predominance. However, because only three patients had documented M tuberculosis in the pleural fluid, no conclusion can be made.

Although P carinii is a frequent cause of pneumonia in patients with HIV infection, it rarely causes pleural effusion. PCP was reported to be associated with 15% of pleural effusions in patients with HIV infection in one study.2 However, the presence of the organism in the pleural fluid was not confirmed in that study.2 Only a few cases of confirmed pleural involvement by P carinii have been reported in the literature.23 24 25 26 27 In the PIP study, pleural effusion was present in 6% of hospital admissions with PCP, and PCP was associated with 3% of the 160 pleural effusions. However, the presence of P carinii was confirmed in none of the pleural effusions.

Malignancy was associated with 9 of 160 pleural effusions in the PIP study. Because homosexuality was not a common risk factor in the patient population, Kaposi’s sarcoma was associated with only two of the pleural effusions. Kaposi’s sarcoma is one of the most frequent causes of pleural effusion in patients with HIV infection. It occurs predominantly in the homosexual risk category.28 29 About half of the patients with pulmonary Kaposi’s sarcoma have pleural effusion.30 31 Non-Hodgkin’s lymphoma is the second most common neoplasm associated with HIV infection.32 In a study of 38 patients with HIV and non-Hodgkin’s lymphoma involving the chest, pleural effusion was detected in 44% of the patients by chest radiography and in 68% of the patients by CT scan.33

Although infection and neoplasm are the two most frequent causes of pleural effusions in patients with HIV infection, other etiologies should be considered. In the study by Joseph et al,2 the most common noninfectious cause of pleural effusion in hospitalized patients with AIDS was hypoalbuminemia. Patients with pleural effusion had lower serum albumin level than did patients without pleural effusion in the PIP study. In addition to hypoalbuminemia, the PIP study also confirmed the association of renal failure, pancreatitis, hepatic cirrhosis, CHF, and atelectasis with pleural effusion in patients with HIV infection.

One retrospective review showed the incidence of pneumothorax to be 9% in HIV-infected patients with PCP, compared to 0% in HIV-infected patients without PCP.7 Among patients with PCP, injection drug users are more likely to develop pneumothorax.34 Pneumothorax was found in 13 of 1,097 patient admissions (1.2%) in the PIP study; 4 were associated with PCP with or without positive pressure ventilation. Most of the spontaneous pneumothoraces in patients with HIV infection occur in the context of PCP.8 Subpleural necrosis with bleb formation and bullous changes have been observed in patients with PCP-associated pneumothoraces.35 In a previous study of 1,000 HIV-infected patients followed during a 9-year period, 20 developed spontaneous pneumothoraces; 19 were associated with PCP.6 In a recently reported series of 1,360 cases of AIDS-related PCP, 67 patients (4.9%) developed pneumothorax: 44% were spontaneous, 30% developed during mechanical ventilation, and 26% were iatrogenic.10 Bacterial pneumonia was associated with three of the pneumothoraces in the PIP study. Although PCP has been found to be the most frequent cause of pneumothorax in HIV-infected patients, bacterial pneumonia was more common than PCP in a study of 100 pneumothoraces among 98 patients, 80% of whom were injection drug users.4 Pulmonary tuberculosis has also been associated with the development of pneumothorax in HIV-infected patients.4 5 However, none of the pneumothoraces was associated with pulmonary tuberculosis in the PIP study. Although most of the pneumothoraces in HIV-infected patients resolve with tube thoracostomy alone, chemical and surgical pleurodesis may be needed in some patients.8 36 37 38 39 40 41 42

The impact of pleural effusion and pneumothorax on the length of hospital stay and mortality of patients with HIV infection has not been well studied. Logistic regression models consisting of the severity of illness assessed by APACHE II predicted mortality and the presence of pleural effusion or pneumothorax were used to determine the impact of pleural effusion and pneumothorax on outcome in the PIP study. The PIP study showed that pleural effusion was not an independent risk factor for increased in-hospital mortality. This is not surprising, because the overall severity of the underlying disease measured by the APACHE II prognostic system is the main determinant of outcome. HIV-infected patients who develop pneumothorax have a poor outcome.9 10 Although the number of patients with pneumothorax was small, the PIP study confirmed that the development of pneumothorax is an independent risk factor for increased in-hospital mortality.

The PIP study has several weaknesses. Although the study was prospective, it was purely observational. No uniform diagnostic or therapeutic plans were followed in the management of the patients. The investigator’s unblinded reviewing of chest radiographs may have introduced biases into the study. Thoracentesis was performed in only 7% of the hospital admissions with pleural effusion, thereby leading to underestimation of the incidence of transudates and leaving the etiology of the effusion uncertain in many patients. Even when the conditions associated with pleural effusion were listed, the cause-effect relationships were not clearly established. Moreover, because the study was limited to only one medical center, the findings may not apply to other patient populations.

In summary, this study describes the incidence and associated conditions of pleural effusion and pneumothorax in hospitalized patients with HIV infection. Although pleural effusion was seen in 14.6% of hospital admissions, most of the effusions were small and did not require any specific intervention. Bacterial pneumonia was the most common condition associated with pleural effusion. Pneumothorax developed in 1.2% of the hospital admissions and in 4.7% of the hospital admissions with PCP.


   Acknowledgements
 
The author thanks Dr. David Armbruster for review of the manuscript.


   Footnotes
 
Abbreviations: APACHE = acute physiology and chronic health evaluation; CHF = congestive heart failure; CI = confidence interval; LDH = lactate dehydrogenase; OR = odds ratio; PCP = Pneumocystis carinii pneumonia; PIP = Pulmonary Complications, ICU Support, and Prognostic Factors of Hospitalized Patients With HIV

Received for publication July 28, 1999. Accepted for publication November 19, 1999.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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