DOI: 10.1148/radiol.2361040460
(Radiology 2005;236:326-331.)
© RSNA, 2005
Pulmonary Cryptococcosis: CT Findings in Immunocompetent Patients1
Rebecca M. Lindell, MD,
Thomas E. Hartman, MD,
Hassan F. Nadrous, MD and
Jay H. Ryu, MD
1 From the Departments of Radiology (R.M.L., T.E.H.) and Pulmonary and Critical Care Medicine (H.F.N., J.H.R.), Mayo Clinic Rochester, 200 First St SW, Rochester, MN 55905. Received March 22, 2004; revision requested June 2; revision received August 2; accepted August 20.
Address correspondence to R.M.L. (e-mail: lindell.rebecca{at}mayo.edu).
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ABSTRACT
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PURPOSE: To evaluate retrospectively the computed tomographic (CT) findings in immunocompetent patients with pulmonary cryptococcosis.
MATERIALS AND METHODS: Institutional review board approval was obtained with a waiver of informed consent, and the study complied with requirements of the Health Insurance Portability and Accountability Act. Chest CT scans of 10 immunocompetent patients with clinically proved pulmonary cryptococcosis were retrospectively reviewed by four reviewers in consensus. Criterion for diagnosis of pulmonary cryptococcosis was (a) the histopathologic presence of the organism at lung biopsy or (b) a positive culture of a respiratory specimen or positive serum cryptococcal antigen test with clinical or radiographic evidence of active pulmonary infection. Patients included six women and four men ranging in age from 46 to 73 years (mean, 59 years). Scans were evaluated for nodules, masses, areas of ground-glass attenuation or of hazy increased attenuation, areas of consolidation, areas of cavitation, pleural effusions, linear opacities, septal thickening, lymphadenopathy, extent of parenchymal involvement, and distribution.
RESULTS: The most common CT finding was pulmonary nodules (n = 9). Multiple nodules (n = 7) were more common than solitary nodules (n = 2). Nodules most commonly occupied less than 10% of the pulmonary parenchyma (n = 7), measured less than 10 mm in diameter (n = 7), and had middle and upper lung predominance (n = 6). The majority of the nodules were well defined with smooth margins (n = 7). Multiple nodules were usually bilaterally distributed (n = 5). Masses (n = 2), lymphadenopathy (n = 2), areas of consolidation (n = 2), areas of hazy increased attenuation (n = 1), pleural effusion (n = 1), and areas of cavitation (n = 1) were uncommon.
CONCLUSION: CT most commonly demonstrated pulmonary nodules in immunocompetent patients with pulmonary cryptococcosis. The nodules were most often multiple, small, well defined, and smoothly marginated with middle and upper lung predominance.
© RSNA, 2005
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INTRODUCTION
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Cryptococcus neoformans is a thin-walled, nonmycelial, budding encapsulated yeast (1,2). It is found worldwide, particularly in soil contaminated with pigeon excreta and decayed wood (1,2). Human infection occurs via inhalation of cryptococcal particles into the lungs, although pneumonia is relatively uncommon in infected individuals (1). In fact, central nervous system infection after hematogenous dissemination is more common than pneumonia (1). Cryptococcal infections most commonly occur in immunocompromised hosts, such as those with acquired immunodeficiency syndrome, transplant-related immunosuppression, or hematologic malignancies (2). Immunocompetent individuals are infected less commonly (3,4). For instance, in 1999 Aberg et al (5) reported findings in 52 patients with pulmonary cryptococcosis who were seen during a 10-year period. Eighteen (35%) of these 52 patients were immunocompetent.
Computed tomographic (CT) findings in immunocompromised patients with pulmonary cryptococcosis have been reported (6–8). Researchers in one study examined CT appearances of pulmonary cryptococcosis in a population that included, but did not distinguish between, immunocompetent and immunocompromised patients (8). Investigators in other studies have reported the chest radiographic appearances of pulmonary cryptococcosis (9–12). Khoury et al (13) examined and compared the radiographic features of pulmonary cryptococcosis in immunocompetent and immunocompromised patients. To our knowledge, no study has concentrated on the CT appearance of pulmonary cryptococcosis in immunocompetent patients. Hence, the purpose of this study was to evaluate retrospectively the thoracic CT findings in immunocompetent patients with pulmonary cryptococcosis.
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MATERIALS AND METHODS
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Patients
After institutional review board approval was obtained with a waiver of informed consent, patients with cryptococcal infections diagnosed from 1976 to 2002 were identified through a computer-assisted search of medical records. Our study was compliant with requirements of the Health Insurance Portability and Accountability Act. A total of 143 patients were identified. Patients with human immunodeficiency virus infection and transplant recipients were excluded. One author (H.F.N.) reviewed the medical records and excluded 101 patients who had other immunocompromising conditions or who were receiving immunosuppressive therapy. Of the remaining 42 immunocompetent patients, 37 had pulmonary involvement with cryptococcal infection, whereas the other five had isolated skin (n = 2), bone (n = 2), or urinary tract (n = 1) infection. Two of the 37 immunocompetent patients were excluded due to chronic underlying lung disease.
Of the qualifying 35 immunocompetent patients with pulmonary cryptococcosis, 10 had chest CT scans available for retrospective review. These patients included six women and four men; their mean age was 59 years ± 8.7 (standard deviation) (range, 46–73 years). Nine of the patients had isolated pulmonary infection, and one had a suspected cerebral cryptococcoma in addition to pulmonary involvement.
In seven of 10 patients, the CT scan was obtained 1–9 days before the date of diagnosis. In the other three patients, the diagnosis had been established at an outside institution. In one patient, the CT scan had been obtained at our institution between 2 and 3 months after the diagnosis was established at an outside institution and was compared with a CT scan obtained elsewhere less than 1 month before the diagnosis. In a second patient, a CT scan had been obtained at our institution 5 months after the diagnosis was determined at an outside institution and was compared with two CT scans obtained elsewhere 1 day and 2 months before the diagnosis. In the third patient, a CT scan had been obtained between 6 and 7 months after the diagnosis was established at an outside institution and was compared with a CT scan obtained elsewhere the same day that the diagnosis was established.
The scans from outside institutions were not available for our study, but the reported changes between examinations were considered. Criteria for diagnosis of pulmonary cryptococcosis were defined in an earlier study (3). Inclusion in the final study group required a definite diagnosis of pulmonary cryptococcosis as defined by either (a) histopathologic presence of the organism at lung biopsy (n = 4) or (b) a positive culture of a respiratory specimen (n = 7) or positive serum cryptococcal antigen test with clinical or radiographic evidence of active pulmonary infection (n = 1). One patient satisfied both criteria, with histopathologic presence of Cryptococcus and positive cultures. Four patients had no symptoms before undergoing chest CT at our institution. The duration of symptoms in the other patients before they underwent chest CT at our institution were as follows: 2 weeks (n = 1), 1–2 months (n = 2), 1 year (n = 2), and 6 years (n = 1).
CT Scanning
In 10 of the qualifying patients, nine underwent routine nonenhanced chest CT and one underwent routine chest CT with intravenous contrast material enhancement. Three patients later underwent solitary nodule CT enhancement studies. Two patients also underwent high-resolution CT.
Chest CT scans were obtained with a variety of CT systems (HiSpeed Advantage, HiSpeed CT/i, Light Speed QX/i, and Light Speed Ultra; GE Medical Systems, Milwaukee, Wis). Specific parameters are given in the Table. Transverse high-resolution CT scans were obtained with the HiSpeed Advantage scanner at the following settings: peak tube voltage, 140 kVp; tube current, 200 mA; rotation time, 2.0 seconds; section thickness, 1.00 mm; detector configuration, single detector row with 1.00-mm collimation; and table increment per rotation, 10 mm. Routine chest CT scans were obtained from the lung apices through the bases. Solitary nodule CT enhancement evaluations were performed at the discretion of the radiologist at the time CT was originally performed, according to a previously published protocol (14). If a nodule enhanced less than 15 HU, it was considered benign.
CT Interpretation
CT scans were retrospectively reviewed on printed film. Two radiologists (R.M.L. and T.E.H., who had 6 and 15 years of experience with chest CT, respectively) and two pulmonologists (H.F.N. and J.H.R., who had 6 and 20 years of experience with chest CT, respectively) reviewed the scans and arrived at decisions in consensus. Original scan reports were not used unless there was information in regard to comparisons with scans obtained at outside institutions, as mentioned earlier. Scans were evaluated for nodules, masses, areas of ground-glass attenuation or hazy increased attenuation, areas of consolidation, pleural effusions, lymphadenopathy, linear opacities, and septal thickening. The bilaterality, symmetry, and distribution of abnormalities were noted.
Cephalocaudal predominance referred to the location of the majority of the abnormalities, that is, in the upper, middle, or lower lungs. The upper lungs were defined as areas that included the lung parenchyma and extended above the level of the inferior edge of the aortic arch. The middle lungs were defined as areas that extended from the level of the inferior edge of the aortic arch to the level of the superior edge of the inferior pulmonary veins as they enter the left atrium. The lower lungs were defined as areas that included the parenchyma and extended below the level of the superior edge of the inferior pulmonary veins as they enter the left atrium. If there was no cephalocaudal predominance of the abnormalities, they were categorized as diffuse.
The transaxial distribution of the abnormalities was also identified. If a majority of the abnormalities were adjacent to the visceral pleura, they were described as subpleurally predominant. If a majority of the abnormalities were adjacent to the hila, they were described as centrally predominant. If the abnormalities occurred along interlobular septa and bronchovascular bundles and subpleurally, they were described as perilymphatic. If they were neither centrally nor subpleurally predominant, they were categorized as random. The extent of an abnormality was visually quantified according to percentage of the total pulmonary parenchyma it occupied (<10%, 10%–40%, or >40%).
Nodules were defined as round or oval opacities that were less than 3 cm in greatest diameter. If these opacities were 3 cm or larger in diameter, they were referred to as masses. The nodules were characterized as well or ill defined, and the margins, as smooth or irregular. If a rim of ground-glass attenuation or hazy increased attenuation surrounded a nodule, it was said to have a halo sign. Nodules were categorized into three size groups (<6 mm, 6–10 mm, and >10 to 29 mm), on the basis of the size of the majority of the nodules. On high-resolution CT scans, hazy opacities through which normal pulmonary architecture could be visualized were defined as areas of ground-glass attenuation. A similar appearance on routine chest CT scans was referred to as areas of hazy increased attenuation. Areas of consolidation were defined as parenchymal nonnodular opacities that obscured underlying pulmonary architecture and that often included air bronchograms. Cavitation of nodules or masses was noted. Lymphadenopathy was determined when the short-axis diameter exceeded 1 cm.
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RESULTS
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Nodules
CT demonstrated pulmonary nodules in nine patients. Nodules were solitary in two patients and multiple in seven. The two solitary pulmonary nodules were well defined with smooth margins and less than 6 mm in diameter. Both occurred in the upper lobe of the right lung. In the seven patients with multiple nodules, the nodules were well defined with smooth margins in five patients (Fig 1) and ill defined with irregular margins in two patients (Fig 1). No nodules had a halo sign. In one patient, some of the nodules were cavitated (Fig 2). The diameter ranges of the multiple pulmonary nodules were less than 6 mm in three patients, 6–10 mm in three, and more than 10 mm in one, and their distributions were bilateral and asymmetric in three patients, bilateral and symmetric in two, and unilateral in two. The cephalocaudal predominance of the multiple nodules was categorized as follows: middle, three patients; upper, two patients; and diffuse, two patients. In the seven patients with multiple nodules, nodules were randomly distributed in five and subpleurally predominant in two. Multiple nodules occupied less than 10% of the parenchyma in five patients and 10%–40% of the parenchyma in two.
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Figure 1a. (a) Transverse CT scan in 46-year-old woman shows several nodules in the lung bases (7-mm-thick section). Most of the nodules have smooth margins. (b) Transverse CT scan in 47-year-old man demonstrates multiple ill-defined irregularly marginated nodules in the upper lobes (arrows) (5-mm-thick section).
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Figure 1b. (a) Transverse CT scan in 46-year-old woman shows several nodules in the lung bases (7-mm-thick section). Most of the nodules have smooth margins. (b) Transverse CT scan in 47-year-old man demonstrates multiple ill-defined irregularly marginated nodules in the upper lobes (arrows) (5-mm-thick section).
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Figure 2a. Transverse CT scan in 51-year-old woman (7-mm-thick section). (a) Scan obtained at level of the bronchus of the upper lobe in the right lung shows several nodules (thin arrows), one of which is cavitated (thick arrow). (b) Scan shows cavitated mass in the apex in the right lung (arrow). Solid and cavitated nodules are seen in the apex in the left lung.
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Figure 2b. Transverse CT scan in 51-year-old woman (7-mm-thick section). (a) Scan obtained at level of the bronchus of the upper lobe in the right lung shows several nodules (thin arrows), one of which is cavitated (thick arrow). (b) Scan shows cavitated mass in the apex in the right lung (arrow). Solid and cavitated nodules are seen in the apex in the left lung.
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Masses
CT demonstrated pulmonary masses in two patients. One patient had an irregular cavitated mass in the apex of the right lung, in addition to multiple bilateral cavitated nodules (Fig 2). The second patient had no pulmonary nodules but had a hilar mass in the left lung or lymphadenopathy with endoluminal extension into the bronchus of the upper lobe in the left lung and postobstructive lingular consolidation (Fig 3).
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Figure 3a. Contrast-enhanced transverse CT scan in 55-year-old man (5-mm-thick section). (a) Scan shows low-attenuating mass or lymphadenopathy in the hilum in the left lung (white arrow). The mass had an endoluminal component (black arrow), which protruded into the bronchus of the upper lobe in the left lung. (b) Scan shows postobstructive consolidation (arrow) of the lingula distal to the mass.
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Figure 3b. Contrast-enhanced transverse CT scan in 55-year-old man (5-mm-thick section). (a) Scan shows low-attenuating mass or lymphadenopathy in the hilum in the left lung (white arrow). The mass had an endoluminal component (black arrow), which protruded into the bronchus of the upper lobe in the left lung. (b) Scan shows postobstructive consolidation (arrow) of the lingula distal to the mass.
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Areas of Consolidation and of Ground-Glass or Hazy Increased Attenuation and Pleural Effusions
Two patients had areas of consolidation. One had postobstructive lingular consolidation from a hilar mass in the left lung or lymphadenopathy. The second patient also had areas of hazy increased attenuation and small bilateral pleural effusions (Fig 4), and this was the only patient with such findings. The areas of hazy increased attenuation and of consolidation were bilateral and asymmetric with lower lung predominance and occupied more than 40% of the lung parenchyma. The areas of hazy increased attenuation were associated with interstitial opacities, and the areas of consolidation were subpleurally predominant. Of the two patients who underwent high-resolution CT, neither had areas of ground-glass attenuation.
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Figure 4. Transverse CT scan obtained through the lung bases in 62-year-old man shows small bilateral pleural effusions (*) and small areas of hazy increased attenuation (5-mm-thick section).
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Lymph Nodes
Two patients had lymphadenopathy. As mentioned before, the patient with the postobstructive lingular consolidation had a hilar mass in the left lung or lymphadenopathy. According to the report, another patient had hilar lymphadenopathy of the right lung on a scan obtained elsewhere at the time of the original diagnosis. This scan was not available to us, and the lymphadenopathy was not present by the time we performed CT, which was 6 months after the original diagnosis. No other patients had lymphadenopathy.
Linear Opacities and Septal Thickening
The only patient with linear opacities and intralobular septal thickening was the one with interstitial opacities associated with areas of hazy increased attenuation, areas of consolidation, and small bilateral pleural effusions.
Solitary Nodule CT Enhancement Evaluation
Three patients underwent solitary nodule CT enhancement evaluation. In these patients, nodules showed enhancement of 26, 33, and 50 HU. All of these were false-positive enhancement studies.
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DISCUSSION
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To our knowledge, this study is the first to examine the CT findings of pulmonary cryptococcosis in immunocompetent patients. Although pulmonary cryptococcosis is uncommon in immunocompetent patients (3–5), it is important for the radiologist to be familiar with the CT appearance of this disease to expedite the diagnosis.
Khoury et al (13) examined radiographic findings of pulmonary cryptococcosis in immunocompetent patients and, as in our study, found that pulmonary nodules were the most common radiographic finding. They reported that solitary nodules (five of nine patients) were more common than multiple nodules (three of nine patients). In our study, however, more patients had multiple nodules (seven of 10, compared with two of 10 for solitary nodules). This disparity could be due to the better sensitivity of CT, compared with radiography, for demonstration of pulmonary nodules (15). No areas of consolidation, pleural effusions, lymphadenopathy, or areas of cavitation were detected with radiography in the immunocompetent patients examined in the study of Khoury et al; these findings are similar to those in our study, with low incidence of areas of consolidation, lymphadenopathy, pleural effusions, and areas of cavitation.
In addition, Khoury et al (13) compared chest radiographic findings of immunocompetent and immunocompromised patients and found a wider variety of radiographic abnormalities among the immunocompromised patients. Specifically, areas of consolidation, lymphadenopathy, and pleural effusions occurred only in the immunocompromised patients. Comparison of findings in our study with those in prior studies of CT for pulmonary cryptococcosis yields similar results. For example, Sider and Westcott (6) examined CT scans of 10 patients with acquired immunodeficiency syndrome and pulmonary cryptococcosis and reported parenchymal opacities (n = 7), interstitial opacities (n = 5), segmental alveolar opacities (n = 5), multiple ill-defined spiculated nodules (n = 3), lymphadenopathy (n = 1), and small bilateral pleural effusions (n = 1). The patients with acquired immunodeficiency syndrome had a lower incidence of nodules (three of 10 vs nine of 10 in our study) and a higher incidence of other pulmonary parenchymal abnormalities than did our immunocompetent patients. The incidence of pleural effusion and of lymphadenopathy at CT was similarly low in their study and in ours.
Lacomis et al (7) also reported a wider variety of imaging findings and a lower incidence of pulmonary nodules in 46 patients, only one of whom was immunocompetent. In contrast to our study findings, the most common finding in their study was an area of consolidation (n = 30). As in the patients with acquired immunodeficiency syndrome examined by Sider and Westcott (6), the incidence of pulmonary nodules was lower than it was in our immunocompetent population (24 [52%] of 46 patients vs nine [90%] of 10). Pleural effusions (n = 19) and lymphadenopathy (n = 9) occurred more commonly, however, in the study of Lacomis et al than they did in our study or that of Sider and Westcott.
Zinck et al (8) looked at the CT and pathologic findings of pulmonary cryptococcosis in a group that included seven immunocompromised and four immunocompetent patients. Their findings were not distinguished according to immune status and, therefore, resulted in limitation of the comparison with our study findings. As in our study, however, the most common CT findings were pulmonary nodules (n = 10), though nodules were less frequently multiple (n = 5). Additionally, masses (n = 4) occurred more commonly than they did in our study. The nodules in our study were most often smaller than 10 mm in diameter, whereas those in the study of Zinck et al were usually 6–20 mm in diameter. In that study, none of the nodules were cavitated. Similar to the findings about nodule margins in our study, nodule margins varied but were most commonly smooth (n = 5). The incidence of consolidation (n = 2), pleural effusion (n = 1), lymphadenopathy (n = 1), or areas of ground-glass attenuation (n = 1) was similarly low. Unlike findings in our study, nodule halo signs (n = 3) were seen.
The main limitation of our study was the small number of patients. The size of our series reflects the rarity of pulmonary cryptococcosis in immunocompetent patients (1,3,4). Another limitation was the lack of uniformity in scanning technique, a function of the fact that ours was a retrospective study. The rarity of this infection necessitated that data be collected over a large number of years. In the normal evolution of our radiology department, scanners and protocols changed over time. In addition, different practices had different standard protocols and different scanners were used, which also contributed to the lack of uniformity. Although minor, a third limitation was the use of high-resolution CT in a few cases. Lack of use of high-resolution CT in the other patients limited the sensitivity of the study.
In conclusion, the most common CT findings in immunocompetent patients with pulmonary cryptococcosis were pulmonary nodules. The nodules were most often multiple, smaller than 10 mm in diameter, and well defined with smooth margins. Nodules most commonly involved less than 10% of the parenchyma and were distributed in the middle and upper lungs. Multiple nodules were most commonly bilateral. Masses, areas of consolidation, cases of lymphadenopathy, pleural effusions, and areas of cavitation occurred infrequently.
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FOOTNOTES
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Authors stated no financial relationship to disclose.
Author contributions: Guarantor of integrity of entire study, R.M.L.; study concepts and design, all authors; literature research, R.M.L., H.F.N., J.H.R.; clinical studies, H.F.N., R.M.L.; data acquisition, R.M.L., H.F.N.; data analysis/interpretation, all authors; statistical analysis, R.M.L.; manuscript preparation, editing, revision/review, and final version approval, all authors; manuscript definition of intellectual content, R.M.L.
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ABSTRACT
INTRODUCTION
