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(Chest. 2006;129:333-340.)
© 2006 American College of Chest Physicians

Pulmonary Cryptococcosis*

Comparison of Clinical and Radiographic Characteristics in Immunocompetent and Immunocompromised Patients

Wei-Chou Chang, MD{dagger}; Ching Tzao, MD, PhD{dagger}; Hsian-He Hsu, MD; Shih-Chun Lee, MD; Kun-Lun Huang, MD, PhD; Ho-Jui Tung, PhD and Cheng-Yu Chen, MD

* From the Department of Radiology (Drs. Chang, Hsu, and Chen), the Department of Surgery (Drs. Tzao and Lee), Division of Thoracic Surgery, the Department of Internal Medicine (Dr. Huang), Division of Pulmonary and Critical Care Medicine, Tir-Service General Hospital, and the Department of Humanity and Social Studies (Dr. Tung), National Defense Medical Center, Taipei, Taiwan, Republic of China. {dagger} Drs. Chang and Tzao contributed equally to this work.

Correspondence to: Ching Tzao, MD, PhD, Division of Thoracic Surgery, Department of Surgery, Tri-Service General Hospital, 325, Section 2, Cheng Gong Rd, Nei-Hu, Taipei 114, Taiwan, Republic of China; e-mail: tzao{at}yahoo.com

Abstract

Study objectives: We compared the clinical characteristics and imaging findings between immunocompetent and immunocompromised patients in whom pulmonary cryptococcosis had been diagnosed to define the role of serum cryptococcal antigen (sCRAG) and radiographs during a follow-up period of up to 1 year.

Design: Retrospective cohort study.

Setting: University hospital.

Patients: The clinical records, chest radiographs, and CT scan findings of 13 immunocompetent and 16 immunocompromised patients with a diagnosis based on cerebrospinal fluid (CSF) culture, sCRAG titers, and cytologic or histologic confirmation of the presence of pulmonary cryptococcosis were reviewed during the course of the study. Two thoracic radiologists reviewed chest radiographs and CT scans for morphologic characteristics and the distribution of parenchymal abnormalities, and a final reading was reached by consensus. The correlation between serial radiographs and sCRAG titers was examined in 9 immunocompetent and 10 immunocompromised patients.

Measurements: Serum or CSF cryptococcal antigen.

Results: The most common clinical symptom was cough, which was present in 24 patients (82.8%). Pulmonary nodules were the most frequent radiologic abnormality. Cavitation within nodules and parenchymal consolidation were significantly less common in immunocompetent patients compared to immunocompromised patients (p = 0.02 and p = 0.05, respectively). Immunocompromised patients tended to have a larger extent of pulmonary involvement than immunocompetent patients, the changes seen on their serial radiographs were more variable, and their corresponding sCRAG titers were higher (> 1:256). In the immunocompetent patients, the radiographic characteristics of lesions usually improved with a corresponding decrease in sCRAG titers over time.

Conclusions: Our study suggests that pulmonary cryptococcosis usually follows a benign clinical course in immunocompetent patients. Immunocompromised patients often undergo an evolution to cavitary lesions that represent a more aggressive disease nature. Serial radiographic changes and changes in sCRAG titers reliably reflect disease progression and the response to therapy.

Key Words: cryptococcosis • immunology • infection • radiology • serum cryptococcal antigen

Cryptococcosis is a fungal infection that can result in pulmonary involvement after the inhalation of Cryptococcus neoformans spores.12345 The fungus most commonly infects patients with AIDS and other causes of reduced immunity, and less frequently occurs in immunocompetent patients. The respiratory tract is thought to be the entry site and is the organ most frequently involved when cryptococcal infection develops.1236 Depending on a patient’s immune status, spores may remain dormant in the lung or may undergo hematogenous spread to any organ system.

Descriptions of pulmonary cryptococcosis commonly focus on patients with immunodeficiencies.6789 Comparisons between immunocompetent and immunocompromised patients have been limited to clinical and radiologic differences at the time of presentation.101112 Furthermore, extant studies have not addressed the role of serum cryptococcal antigen (sCRAG) in relation to radiographic changes during follow-up to predict the outcome of treatment. We conducted this study to compare clinical features and initial CT scan findings in patients with pulmonary cryptococcosis who were immunocompetent and immunocompromised. We also sought to correlate sCRAG titers with radiographic changes during a 1-year follow-up period in both groups of patients.

Materials and Methods

Patients and Diagnostic Criteria
From January 1987 to January 2004, 29 patients with a diagnosis of pulmonary cryptococcosis at hospital discharge were retrospectively reviewed at our institution. The medical records of all patients were analyzed for demographic data, host immune status, presenting symptoms, sCRAG titers, treatment, follow-up, and outcomes. The diagnosis was established based on the cytologic or histologic identification of C neoformans obtained by percutaneous biopsy (16 patients), open biopsy or resection (5 patients), BAL (5 patients), or transbronchial biopsy (1 patient). The remaining two patients received diagnoses based on an elevated cryptococcal antigen titer in their pleural fluid combined with a culture from cerebrospinal fluid in one patient and from a blood sample in the other patients, revealing the presence of C neoformans. Patients were excluded from our review if another pathogen was isolated from the lung. All cryptococcal antigen titers in serum, cerebrospinal fluid, and pleural fluid were measured by means of a commercially available latex agglutination test (Crypto-LA test, enzyme-linked immunosorbent assay; Fumouze; Levallois-Perret, France).

Image Acquisition and Evaluation
Chest radiography was limited to a standard posteroanterior projection. The CT scans were performed with either of two scanners (Somatom DRH scanner; Siemens; Iselin, NJ; or Somatom Plus 4 scanner; Siemens; Erlangen, Germany). Scan increments varied from 5 to 10 mm, depending on the region to be studied. Additional high-resolution CT scans were obtained with 2-mm collimation and a high-spatial-frequency reconstruction algorithm at selected levels in six patients. IV contrast material was administered in 21 patients. The images were examined with window settings appropriate for the assessment of the lung parenchyma (window level, –500 to –700 Hounsfield units [HU]; window width, 1,000 to 1,500 HU) and mediastinum (window level, 30 to 50 HU; window width, 350 to 500 HU).

All radiologic studies were reviewed retrospectively by two radiologists (H.H.H. and W.C.C.) who were unaware of any clinical data. A final reading was reached by consensus. The chest radiographs were reviewed, and the number, size, border characteristics, and location of pulmonary nodules (those ≤ 3.0 cm in diameter) or masses (those > 3.0 cm in diameter) were recorded. The presence, location, and extent of airspace opacifications were evaluated. The distribution of each pattern was classified as being either predominantly in the upper, middle, or lower lung zone, and as being predominantly central, peripheral, or random. Associated findings, such as the presence of cavitation, mediastinal or hilar masses, and pleural effusion, were also recorded.

CT scans of the chest were reviewed for lesion characteristics and associated findings using the same evaluation criteria as for the chest radiographs. CT scans were also assessed for ground-glass opacities, airspace consolidation, a CT halo sign (a halo of ground-glass opacity surrounding a nodule or mass), central low attenuation, and mediastinal or hilar adenopathy (defined as a lymph node > 10 mm in size on the short-axis diameter). Any other abnormalities were noted. Patterns of CT scan abnormalities, clinical features, and outcomes were compared between the immunocompromised group (n = 16) and the immunocompetent group (n = 13).

Follow-up Studies
Nine immunocompetent and 10 immunocompromised patients had serial serologic tests and radiographic evaluations at 3, 6, and 12 months after the initial CT scans were performed. Follow-up CT scans were also available in four of our patients to correlate with the changes in plain chest radiographs. Complete resolution was defined as the disappearance of radiographic evidence of pulmonary abnormalities, while deterioration was defined as progressive radiographic worsening of pulmonary abnormalities. Partial resolution was defined as a decrease in the size and extent of the pulmonary abnormalities compared to the previous chest radiographs. A stable condition was defined as no change when compared with previous imaging findings.

Statistical Analysis
The Pearson {chi}2 test or Fisher exact test was employed to compare different patterns of CT scan abnormalities between the immunocompetent and immunocompromised patients. A significant difference was considered to be present for p values < 0.05.

Results

Demographics and Clinical Data
Patient demographic and clinical information is summarized in Table 1 . Our patients ranged in age from 17 to 79 years (mean age, 47 years). Twenty patients were male and 9 were female. Thirteen patients had no comorbidity, and 16 patients were considered to be immunocompromised with at least one predisposing condition, including underlying malignancy in 8 patients, use of immunosuppressive drugs in 5 patients, severe diabetes mellitus in 4 patients, cirrhosis secondary to hepatitis B or C in 4 patients, cirrhosis secondary to alcoholism in 2 patients, and aplastic anemia in 1 patient. None of the patients included in this study had AIDS at the time of diagnosis of pulmonary cryptococcosis. Mean age, duration of hospitalization, the incidence of CNS involvement, and the likelihood of cryptococcal dissemination to other organs were significantly different between the two groups (p < 0.05). Cough was the most common presenting symptom, occurring in 9 immunocompetent patients (69%) and 15 immunocompromised patients (94%), followed by fever (8% vs 50% of patients, respectively), chest pain (8% vs 44% of patients, respectively), shortness of breath (8% vs 38% of patients, respectively), and headache (8% vs 31% of patients, respectively). Four patients were asymptomatic, all of whom were immunocompetent. Seven immunocompetent patients, including those four asymptomatic individuals, were treated conservatively. All of the immunocompromised patients were symptomatic and were treated by antifungal agents (n = 13) or by surgical intervention (n = 3). Four of 16 immunocompromised patients (25.0%) died of cryptococcal fungemia (1 patient) or their underlying diseases (3 patients); none of the immunocompetent patients died of pulmonary cryptococcosis.


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  		Table 1.. Demographics and Clinical Information of Patients With Pulmonary Cryptococcosis*

 
Radiologic Features
The pulmonary abnormalities seen on the initial CT scans are summarized in Table 2 . The most common radiologic finding was one or more nodules/masses. These lesions were 7 to 20 mm in diameter in 14 patients, 20 to 30 mm in 3 patients, and > 30 mm in 4 patients. Most of the nodules had poorly defined margins, with peripheral predominance in 12 patients. The second most common finding was patchy airspace consolidation. It was present alone in 9 patients and as part of a mixed pattern in 8 patients. These pulmonary lesions usually had no predominance in a specific lung zone. A pattern of diffuse innumerable reticular nodules, ranging from 1 to 3 mm in size, was seen in only one immunocompromised patient. Other associated findings included cavitation (n = 15; 52%), areas of ground-glass opacity (n = 5; 17%), CT scan halo sign (n = 2; 7%), mediastinal lymphadenopathy (n = 2; 7%), and pleural effusion (n = 3; 10%).


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  		Table 2.. Patterns and Distribution of Pulmonary Abnormalities of Initial CT Scans*

 
The comparisons of CT scan abnormalities between the two groups of patients are summarized in Table 3 . The proportion of patients with pulmonary nodules and airspace consolidation in the immunocompetent group was not significantly different from that of the immunocompromised patients. The presence of cavitations within nodules or airspace consolidation was significantly less frequent in immunocompetent patients than in immunocompromised patients (2 vs 10, respectively [p = 0.02]; 0 vs 5, respectively [p = 0.05]). Areas of ground-glass attenuation were observed in five patients (two immunocompetent patients and three immunocompromised patients), and were bilateral and random in distribution. Mediastinal lymphadenopathy was observed only in two patients (7%), including one immunocompetent patient and one immunocompromised patient. The frequencies of ground-glass attenuation and mediastinal lymphadenopathy were also not significantly different between the immunocompromised and immunocompetent groups. Isolated pleural effusions were observed in three immunocompromised patients (10%).


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  		Table 3.. Comparison of CT Scan Findings Between Immunocompetent and Immunocompromised Patients*

 
Follow-up Studies
The mean duration of follow-up for the 9 immunocompetent patients was 14.3 months (range, 12.5 to 19.7 months) and was 30.9 months (range 2.1 to 44.8 months) for the 10 immunocompromised patients. Changes in sCRAG titers and chest radiographic findings in a total of 19 patients are summarized in Table 4 . Five of nine immunocompetent patients (patients 1 to 5) were treated conservatively, and the remaining four patients (patients 6 to 9) received 3 months of antifungal treatment with oral fluconazole (400 mg/d). In the immunocompromised group, seven patients (patients 10 to 16) received at least 6 months of therapy with oral fluconazole, whereas the other three patients (patients 17 to 19) were treated with IV amphotericin B (1 mg/kg/d) for 8 weeks to a cumulative dose of up to 2 g, followed by oral fluconazole for another 3 months.


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  		Table 4.. Nineteen Patients Who Received Serial Serologic and Radiographic Surveillance Studies During 1 Year of Follow-up*

 
Of the immunocompetent patients at their 3-month follow-up evaluation, three patients showed partial resolution of pulmonary abnormalities with a decrease in sCRAG titer, the conditions of five patients remained unchanged, and 1 patient showed radiographic deterioration. At the 6-month follow-up evaluation, seven patients showed radiographic improvement and two patients remained radiographically stable with a decrease in sCRAG titers. At the time of the evaluations, which were performed ≥ 1 year after the initial infection, the radiographs in all nine of the immunocompetent patients showed significant resolution of pulmonary abnormalities with a parallel decrease in sCRAG titers.

In the immunocompromised group, no patient had radiographic improvement after 3 months of follow-up, while six patients remained stable and four patients showed deterioration of their condition. The sCRAG titer changes were variable. At the 6-month follow-up evaluation, only one patient had radiographic improvement, five patients showed deterioration, and three patients remained stable. One patient who died of multiple organ failure had a diffuse reticulonodular pattern seen on chest radiographs that had been performed shortly before death. At the 1-year follow-up evaluation, 3 of 10 patients (30%) showed radiographic improvement with a reduction in sCRAG titers, 5 patients showed no radiographic changes with fluctuating sCRAG titers, and the remaining patient showed continued deterioration of radiographic abnormalities. A comparison of the levels of sCRAG titers between the immunocompetent and immunocompromised patients is shown in Figure 1 .


Figure 1
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  		Figure 1.. Comparison of sCRAG titer changes between treated and nontreated immunocompetent and immunocompromised patients at different follow-up intervals.

 
Discussion

We performed this study in view of the lack of comparisons in patients with pulmonary cryptococcosis with regard to their immune status. Our main observations are that immunocompromised patients develop a greater extent of pulmonary abnormalities than do immunocompetent patients. The changes in immunocompromised patients are often characterized by cavitation and are associated with higher corresponding sCRAG titers than in immunocompetent patients.

In asymptomatic immunocompetent patients, cryptococcal pneumonia is sometimes diagnosed incidentally on routine chest radiographs.113 In our series, only four patients were asymptomatic at the time of diagnosis. Similar to previous reports, the most frequent symptoms in our immunocompromised patients included cough and fever (94% and 50%, respectively). Chest pain, shortness of breath, and headache were also found in immunocompromised patients in our series and in those in previously published reports.123 Among the clinical presenting symptoms, headache has been reported to be a prominent sign that usually implies an increased risk of central venous system involvement.214 Our findings support the these results.

Khoury et al11 first described differences in the radiographic features of pulmonary cryptococcosis comparing immunocompromised and immunocompetent patients. Their study focused on plain chest radiographs. We included CT scan studies in this report with results similar to those of others.9101115 The most common finding on the CT scan was pulmonary nodules, which were present alone or with other pulmonary abnormalities in 21 patients (72%). Zinck et al12 have described CT scan findings of pulmonary cryptococcosis in 11 patients (7 immunocompromised patients and 4 immunocompetent patients) but did not perform a valid statistical comparison between the two groups. We found that pulmonary cavitation was a significantly more common radiologic finding in immunocompromised patients than in immunocompetent ones. Although cavitation in nodules and masses has been previously described1112 as a radiographic feature limited to immunosuppressed patients, two immunocompetent patients in this study also had this finding. It is believed that cavitation indicates a long-term localized pulmonary abnormality,916 suggesting that patients with cavitary pulmonary lesions may experience a more severe cryptococcal infection that requires a more aggressive antifungal therapy.

sCRAG is often used to diagnose cryptococcal infection and to monitor disease activity.171819 Some studies5192021 have focused on the utility of sCRAG titers in patients with AIDS and have concluded that high titers suggest invasive disease. However, this correlation is less certain in patients who do not have AIDS.152223 In the study by Aberg et al,15 only 39% of patients, all of whom were immunocompromised, had positive sCRAG results. Nunez et al22 and Nadrous et al23 postulated that a positive result might reflect an increased risk of more severe localized disease or dissemination. As cited above, previous reports lacked sufficient follow-up data and comparative studies between immunocompetent and immunocompromised patients to address the role of sCRAG titers and radiographs in predicting the course of disease activity or progression. In contrast, our study suggests that immunocompromised patients tend to have more aggressive disease than do immunocompetent patients, as evidenced by higher sCRAG titers in the former group, especially when the titers exceed 1:4,096.

Our study had several limitations. First, this was a retrospective study with a small number of patients collected over a long period of time. Patients in whom pulmonary cryptococcosis has been diagnosed and those who have been treated more recently may have a better prognosis, because progress in imaging technology and improvements in radiographic-guided biopsy methods may permit an earlier diagnosis and thus better outcomes. New antifungal drugs cause less severe side effects, thus potentially resulting in additional bias in the outcomes. It is difficult to clearly identify an immunocompetent or an immunocompromised host, and we had to define immunosuppression by clinical history alone. Unlike in the United States and other Western countries, where cryptococcosis is most commonly diagnosed in AIDS patients,24 no AIDS patients were included in this study, probably because the prevalence of AIDS is much lower in our country.25 This fact suggests that our results perhaps should not be generalized to the worldwide population.

In conclusion, we have demonstrated that immunocompromised patients usually have more extensive pulmonary involvement and higher titers of sCRAG than do immunocompetent patients in the setting of cryptococcal infection. This indicates that immunocompromised patients tend to have more advanced cryptococcal infections compared to immunocompetent patients. Serial radiographic changes and changes in sCRAG titers reliably reflect disease progression and response to therapy.

Acknowledgements

The authors thank Professor Mark K. Ferguson at the University of Chicago Hospitals for his review of this manuscript.

Footnotes

Abbreviations: HU = Hounsfield units; sCRAG = serum cryptococcal antigen

This research was supported by the Research Foundation of Tri-Service General Hospital (grant No. TSGH-C91-22), Taipei, Taiwan, Republic of China.

Received for publication December 15, 2004. Accepted for publication June 13, 2005.

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