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Fungal Empyema Thoracis^*

An Emerging Clinical Entity

^* From the Departments of Internal Medicine (Drs. Ko, Chen, Hsueh, Yang) and Laboratory Medicine (Dr. Luh), National Taiwan University Hospital, Taipei, Taiwan.

Correspondence to: Pan-Chyr Yang, MD, PhD, FCCP, Department of Internal Medicine, National Taiwan University Hospital, 7, Chung-Shan South Rd, Taipei 100, Taiwan; e-mail: pcyang{at}ha.mc.ntu.edu.tw

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Study objectives: To analyze the clinical spectra, pathogenesis, treatment, outcome, and prognostic factors of fungal empyema thoracis.

Design: The medical records of patients with positive fungal cultures from pleural effusions were retrospectively analyzed.

Setting: A university-based tertiary care hospital in Taipei, Taiwan.

Patients and methods: From January 1990 through December 1997, patients diagnosed with fungal empyema were included in this study. The criteria for diagnosis of fungal empyema thoracis were as follows: (1) isolation of a fungal species from the pleural effusion; (2) significant signs of infection, such as fever (body temperature > 38.3°C) and leukocytosis (white blood cell > 10,000/µL); and (3) isolation of the same mold species from pleural effusion on more than one occasion, or from pleural effusion and other specimens such as blood, sputum, or surgical wounds that showed evidence of tissue invasion.

Results: Sixty-seven patients with fungal empyema thoracis were included. Their mean age was 54 years (range, 2 weeks to 93 years), and 64% (43 patients) were men. Fifty-seven patients (85%) had various underlying diseases, and 18 (27%) had more than one immunocompromising condition. A total of 73 fungal isolates were recovered from pleural effusion; the most commonly encountered were Candida species (47 isolates, 64%), Torulopsis glabrata (13 isolates, 18%), and Aspergillus species (9 isolates, 12%). Candida albicans (28 isolates) was the most common Candida species, followed by Candida tropicalis (13 isolates). Six patients (9%) had two fungal strains isolated, and 16 (24%) had concomitant bacterial empyema thoracis. Eighteen patients (27%) had concurrent fungemia. Most (56 patients, 84%) cases of fungal empyema thoracis were nosocomial, and many case (43 patients, 64%) were acquired in ICUs. Abdominal disease (20 patients, 30%), especially previous abdominal surgery and GI perforation (12% and 10%, respectively), was the most common cause of fungal empyema thoracis, followed by bronchopulmonary infection (15 patients, 22%) and chest surgery (12 patients, 18%). Forty-nine patients (73%) received systemic antifungal therapy, and 38 (57%) underwent closed drainage therapy. Eleven patients (16%) underwent pleural irrigation with normal saline solution, povidone-iodine solution, or antifungal agents. Six patients (9%) finally received decortication. All patients receiving surgery or pleural irrigation with antifungal agents survived. Despite the aforementioned management, the crude mortality was high (73%). Multivariate analysis showed a significantly increased risk of death in immunocompromised patients (relative risk, 1.58; p < 0.005) and those with respiratory failure (relative risk, 2.31; p < 0.001). Systemic antifungal therapy was associated with a significantly lower risk of death (relative risk, 0.69; p < 0.05).

Conclusion: These data imply an increasing incidence of fungal empyema thoracis in recent years and the necessity for aggressive treatment of patients with this disease.

Key Words: empyema thoracis • fungal infection

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
The occurrence of fungal infection is rising rapidly worldwide.^{1 2 3 4} Data from the Centers for Disease Control and Prevention reveal that, between 1980 and 1990, Candida species emerged as the sixth most common nosocomial pathogen (7.2%).⁵ The increase in the rate of fungal infections has been attributed mainly to the increasing use of broad-spectrum antibiotics, intravascular devices, and hyperalimentation, as well as to the ever-increasing number of critically ill or immunocompromised patients in hospital populations.^{2 6 7 8 9 10 11}

The increasing incidence of fungal infection is also a serious problem in Taiwan. From 1980 to 1994, a 27-fold increase in bloodstream infections caused by Candida species was observed at National Taiwan University Hospital (NTUH).¹² In 1994, nosocomial candidemia was seen in 2.53 per 1,000 discharges and accounted for 16.2% of all nosocomial bloodstream infections at this hospital.¹²

The most common sites of fungal nosocomial infections at NTUH are the bloodstream, urinary tract, and bronchopulmonary system.¹² The diagnosis of bronchopulmonary infection caused by fungi is difficult to confirm: because fungi isolated from sputum may represent either pathogens or saprophytes, invasive diagnostic procedures such as bronchoscopy or lung biopsy are usually necessary. Recently, we found that fungal empyema thoracis is also increasing in incidence at NTUH. This entity has become a serious clinical problem with high mortality and deserves early and aggressive treatment.

Most previous studies of fungal infections concerned invasive and systemic infections in cancer patients.² To the best of our knowledge, there have been no large-scale studies of thoracic empyema caused by fungal species; only a few case reports are available in the literature.^{13 14} Therefore, in this study, we reviewed the clinical features of patients with culture-positive fungal empyema thoracis to determine the clinical spectra, pathogenesis, treatment, outcome, and prognostic factors of this disease.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
The medical records of patients with culture-positive fungal empyema thoracis treated at NTUH during the period of January 1990 through December 1997 were analyzed. NTUH, a major teaching hospital in northern Taiwan, had 1,200 beds before 1991 and 1,500 beds as of 1991.

Patients with fungal empyema were first selected from the hospital register at the Mycology Laboratory, and the case records were analyzed. Diagnosis of fungal empyema thoracis required that the following criteria be met: (1) isolation of a fungal species from the pleural effusion belonging to the exudate category, according to the criteria of Light et al¹⁵ ; (2) significant signs of infection, such as fever (body temperature > 38.3°C) and leukocytosis (white blood cell > 10,000/µL); and (3) isolation of the same mold species from pleural effusion on more than one occasion, or from pleural effusion and other specimens such as blood, sputum, or surgical wounds that showed evidence of tissue invasion. Fungi isolated from prior tube thoracostomy for preexisting pneumothorax or bacterial empyema were assumed to be colonized within chest tubes, unless infection persisted without antifungal therapy.

The following data were collected for each patient: age and sex; predisposing factors, including underlying diseases and associated medical conditions; prior use of invasive devices or surgical interventions; antimicrobial agents administered; clinical symptoms; peripheral WBC and differential cell counts; characteristics (appearance, cell counts, differential cell counts, total protein concentration, glucose concentration, lactic dehydrogenase concentration) of the pleural effusion; strains of pathogens isolated from cultures of the pleural effusion; regimen and duration of antifungal therapy; use of intrapleural irrigation with normal saline solution and/or povidone-iodine solution and/or antifungal agents; use of intrapleural fibrinolytic therapy; invasive drainage procedures or surgery; duration of hospitalization; and outcome.

The pathogenesis of fungal empyema thoracis was evaluated on the basis of the history and clinical picture described in the medical records. Fungal empyema thoracis developing 48 h after admission was regarded as hospital-acquired. Patients were considered to have pneumonia before the development of empyema if there was radiographic evidence of a parenchymal infiltrate adjacent to the empyema thoracis and/or the initial clinical manifestations included fever and apparent productive cough with purulent sputum. Granulocytopenia was defined as an absolute neutrophil count < 1,000/µL in peripheral blood.

Pleural fluid specimens were collected by thoracentesis under aseptic conditions or during tube thoracotomy. The specimens were examined microscopically and cultured for bacteria, mycobacteria, and fungi. For isolation of fungi, the specimens were inoculated onto Sabouraud dextrose agar plates (BBL Microbiology Systems; Cockeysville, MD). Cornmeal agar (BBL Microbiology Systems) slide cultures were used to identify molds. Yeasts were identified to the species level by standard methods, and their identity was confirmed with the API ID 32C system (bioMerieux; Marcy-I’Etoile, France).¹⁶ Identification of molds was based on the gross colony morphology and microscopic pictures. With regard to the determination of the fungal species Glabrata, we choose the genus Torulopsis instead of Candida as some taxonomists suggested.¹⁶

Most patients received standard tube thoracotomy or an indwelling pigtail catheter for continuous closed drainage, unless the scarcity of effusion or the clinical condition (eg, bleeding diathesis) did not allow invasive procedures. Patients received intrapleural streptokinase instillation, open drainage, or decortication if there was radiographic or sonographic evidence of loculation of pleural effusion with poor drainage and the clinical condition suggested persistent inflammation or poorly controlled lung abscess.

Differences in survival among subgroups were analyzed by ² test, or Fisher’s Exact Test when necessary. A forward stepwise logistic regression model was run, with significance levels for entry or retention in the model both set at p = 0.05; only variables that were significantly associated with survival in the univariate analysis were included in the multivariate model.

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Clinical Characteristics
From January 1990 through December 1997, 111 patients at NTUH had positive fungal cultures from pleural effusions. Of these, 44 patients were excluded because of at least one of the following conditions: (1) the pleural effusion was transudate; (2) the patient had no symptoms or signs associated with infection; (3) mold fungus was isolated from pleural effusion only once, and no other specimen yielded the same species; or (4) the fungus was isolated from a prior tubal thoracotomy, and the patient did well without antifungal therapy. The specimens from these 44 patients were presumed to represent contamination or colonization.

Of the 67 cases included in the analysis, there was only 1 case annually in 1990 and 1991, whereas there were 6 in 1992 and 7 in 1993. However, there were > 10 cases annually from 1994 through 1997: 15 in 1994, 13 in 1995, 11 in 1996, and 13 in 1997.

The demographic and clinical features of the 67 patients are summarized in Table 1 . The majority of the patients were male (64%). Twenty-eight patients (42%) were > 65 years old. Fifty-six cases (84%) of fungal empyema thoracis were nosocomial, most of which were acquired in the ICU (43 cases, 64%). Sixty of the 67 patients (90%) had underlying diseases or associated medical conditions. Fifty-three patients (79%) had compromised immunity caused by (in order of decreasing frequency) malignancy, diabetes mellitus, long-term steroid use, liver cirrhosis, organ transplantation, uremia, alcoholism, or AIDS. Among the 33 patients (49%) with malignancies, abdominal and hematologic malignancies were the most common; 8 patients (12%) had malignant pleural effusions. Four patients were transplant recipients: 2 renal, 1 heart, and 1 bone marrow transplantation.

The most common manifestations among the 67 patients were fever (76%), leukocytosis (67%), and dyspnea (60%). Fourteen patients (21%) had shock as an initial presentation. The peripheral WBC count was > 20,000/µL in 28 patients (42%). Five patients (7%) had fungal empyema thoracis during the granulocytopenia stage after chemotherapy.

Thirty-one patients (41%) had loculated effusions on radiography or ultrasonography. The majority of the pleural effusion specimens appeared yellowish and turbid (51%). Only 9 patients (13%) expressed frank pus. The mean total protein (3.5 g/dL) and lactate dehydrogenase (3,198 U/L) concentrations in the exudates were high, and the mean glucose concentration (27 mg/dL) was low. Thirty-one patients (69%) had neutrophil predominance in pleural effusions.

Microbiology
Of the 123 fungal isolates recovered from the 111 specimens of pleural effusion, 50 were considered to represent contamination or colonization, and 73 were considered clinically significant (Table 2 ). Six of the 67 patients with fungal empyema thoracis had more than one fungal strain isolated. Of the 73 clinically significant fungal isolates, 47 (64%) were Candida species, including C albicans (28 isolates, 38%) and C tropicalis (13 isolates, 18%). Torulopsis glabrata (13 isolates, 18%) was the second most common fungi encountered, followed by Aspergillus species (9 isolates, 12%) and Cryptococcus species (3 isolates, 4%).

Treatment and Outcome
The treatment modalities and outcomes of these 67 patients are summarized in Table 3 . The median hospital stay of the patients was 50 days (mean, 66 days; range, 8 to 297 days). Forty-nine patients (73%) died, 43 (88%) of whom had compromised immunity. Forty-nine patients (73%) received systemic antifungal therapy with amphotericin B (12%), fluconazole (33%), or both (28%). All patients who did not receive antifungal therapy died, except for one who underwent surgical intervention. In most cases in which antifungal therapy was not given, fungi grew from the pleural effusion after the patients died. All 13 patients with T glabrata and all 6 patients with more than one fungal strain isolated from the pleural effusion died. Of the 44 patients (66%) who underwent drainage (closed, 38; surgical, 6), 29 (66%) died, whereas 20 of the 23 patients (87%) without drainage died.

Table 4 summarizes clinical, epidemiologic, microbiologic, and laboratory variables studied, as well as their relative influence on mortality. Patients with compromised immunity (relative risk [RR], 1.58; 95% confidence interval [CI], 1.03 to 2.42), underlying malignancy (RR, 2.66; 95% CI, 1.09 to 6.25), antecedent broad-spectrum antibiotic use (RR, 2.08; 45% CI, 1.06 to 4.11), respiratory failure (RR, 2.31; 95% CI, 1.28 to 4.15), T glabrata, or more than one fungal isolate had higher risks of mortality than those without these conditions. Patients with systemic antifungal therapy (RR, 0.69; 95% CI, 0.55 to 0.87) or pleural drainage (RR, 0.71; 95% CI, 0.52 to 0.97) were less likely to die than those who did not undergo these procedures.

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Our findings point to an increasing incidence of fungal empyema thoracis at our hospital in recent years. In fact, because we used strict criteria to define fungal empyema thoracis and excluded patients who had transient and self-limited fungal empyema thoracis without significant signs of infection, the frequency of fungal empyema thoracis may have been underestimated. In our study, 84% of fungal empyema thoracis episodes were acquired in the hospital, most often in ICUs. The overall mortality was up to 73%. This supports the notion that nosocomial fungal infections now represent a very important cause of morbidity and mortality.¹⁷

Candida species are the most common pathogens in fungal empyema thoracis; empyema thoracis caused by other filamentous fungi is rare, and only sporadic cases have been reported.¹⁸ Candida empyema thoracis has been reported as a complication of operation,¹⁹ gastropleural fistula,²⁰ and spontaneous esophageal rupture.²¹ Aspergillus empyema thoracis is uncommon and is caused by rupture of an aspergilloma cavity or as a complication of a preexisting chronic empyema.²² Pleural cryptococcosis has been reported to be associated with HIV infection,^{23 24} liver cirrhosis,²⁵ and Bruton’s agammaglobulinemia.²⁶

Candida and Torulopsis species accounted for 82% of the fungal isolates from pleural effusion, with C albicans representing 60% of all Candida species isolates in our study. These findings are consistent with the data from the Centers for Disease Control and Prevention’s National Nosocomial Infection Surveillance, which showed Candida and Torulopsis species to account for 80% of fungal isolates associated with nosocomial infections in the 1980s.^{27 28}

A number of factors have been reported to predispose patients to fungal infection. Impaired T-cell function because of factors such as high-dose glucocorticoid therapy, chemotherapy, or AIDS, as well as depressed neutrophil number or function from causes such as hematologic malignancies and chemotherapy, may increase the risk of fungal infection.²⁹ The use of multiple broad-spectrum antimicrobial agents in critically ill patients may alter the normal flora in the GI tract and precipitate fungal infection, and is another important factor in the increasing occurrence of fungal infection; disruption of the normal GI flora may allow overgrowth of Candida species, which can then translocate from the GI tract to the bloodstream.⁹ In addition, because Candida species commonly colonize the skin, any break in the epithelial barrier could act as a portal for invasion. Thus, the increasing use of hyperalimentation and invasive devices, including central vascular catheters, urinary catheters, and chest tubes, also contributes to the development of fungal infections.¹⁰ Because of drainage tube insertion and damage to the normal mucosal barrier, chest and abdominal surgery can also put patients at risk for fungal infection.¹¹

In our series, most episodes of fungal empyema thoracis occurred in men and were hospital-acquired. Many of the patients (60%) had received broad-spectrum antibiotics; had compromised immunity or malignancies, especially abdominal and hematologic malignancies; and/or had a history of recent surgery or intra-abdominal infection. Surprisingly, intra-abdominal diseases (30%) were the major cause of fungal empyema thoracis in our series. Subdiaphragmatic infection may extend to the lung or pleural space by way of lymphatics, directly through the diaphragm or a defect in it, or by way of the bloodstream.¹⁰

The development of fungal empyema thoracis immediately after thoracotomy in 12 patients (18%) may have been caused by direct inoculation during the procedure, wound infection, or inoculation via drainage tubes.³⁰ In the nine patients with lung abscess, fungal empyema was most likely caused by rupture of the abscesses. The route of fungal empyema thoracis in patients with esophageal rupture, seen in three patients in our study, has been reported to be direct involvement via fungal mediastinitis.¹⁹ Repeated thoracentesis and previous tube thoracotomy may also precede fungal empyema thoracis, owing to imperfectly aseptic procedures.³¹ Five patients with systemic fungal infection apparently had empyema thoracis via hematogenous spread.³²

The crude mortality of fungal empyema in our study was high (73%), and most patients who died had severe underlying diseases combined with bacterial infection. Those patients without systemic antifungal therapy or pleural drainage also had poor outcomes. Most patients who did not receive antifungal agents died before the culture results became available. Early administration of antifungal agents and pleural drainage might be helpful in improving the outcome, although the lack of strict criteria for empiric use of antifungals in this study precludes us from drawing a conclusion regarding this issue. For rapid diagnosis of fungal empyema thoracis, serologic tests or polymerase chain reaction-based assays may be useful.^{33 34}

A high proportion of our patients had severe bacterial infections, including bacteremia (28%) and coexisting bacterial empyema thoracis (24%). However, there was no significant correlation between combined bacteremia or bacterial empyema thoracis and survival.

The species of fungus and number of fungal species isolated seemed to affect the risk of death. All 13 patients with T glabrata and all six patients with more than one fungal strain isolated from pleural effusion died. T glabrata has the least susceptibility to fluconazole,³⁵ and this factor may have contributed to the high mortality in our series. The presence of more than one fungal isolate might indicate more compromised immunity or more severe intrapleural infection.

Patients with compromised immunity, underlying malignancy, antecedent broad-spectrum antibiotic use, concomitant respiratory failure, and/or more than one fungal isolate had elevated risks of mortality. However, only compromised immunity and respiratory failure were significantly associated with outcome in multivariate logistic regression analysis.

In conclusion, the incidence of fungal empyema thoracis at our hospital has increased in recent years. Patients with fungal empyema thoracis often had concurrent severe underlying diseases, such as malignancies, or were receiving immunosuppressive medications. The major causes of fungal empyema included abdominal infection, bronchopulmonary infection, surgical intervention, and repeated thoracentesis. Fungal empyema thoracis is associated with high mortality, and early diagnosis and antifungal therapy may improve the outcome.

	Footnotes

 
Abbreviations: CI = confidence interval; NTUH = National Taiwan University Hospital; RR = relative risk

Received for publication July 13, 1999. Accepted for publication February 11, 2000.

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TOP Abstract Introduction Materials and Methods Results Discussion References

 

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This Article Abstract Full Text (PDF) Free Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Article Archive Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (8) Citing Articles via Google Scholar Google Scholar Articles by Ko, S.-C. Articles by Yang, P.-C. Search for Related Content PubMed PubMed Citation Articles by Ko, S.-C. Articles by Yang, P.-C.