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1 Department of Radiology, Vancouver Hospital and Health Sciences Center and
University of British Columbia, 855 W. 12th Ave., Vancouver BC V5Z 1M9,
Canada.
2 Present address: Department of Radiology, Hospital de Sant Pau, Universitat
Autónoma de Barcelona, Avda. Sant Antoni M. Claret 167, Barcelona
08025, Spain.
3 Department of Radiology, Samsung Medical Center, Sungkyunkwan University
School of Medicine, 50 Ilwon-dong, Kangnam-ku, Seoul 135-710, Korea.
Received January 27, 2003;
accepted after revision April 21, 2003.
Address correspondence to T. Franquet.
Abstract
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MATERIALS AND METHODS. The causes of immunocompromise included bone marrow (n = 25) or solid organ transplantation (n = 5) and corticosteroid therapy (n = 2). The patients included 16 men and 16 women ranging in age from 22 to 70 years (mean age, 43 years). The CT scans were retrospectively reviewed by two thoracic radiologists for the presence, appearance, and distribution of parenchymal abnormalities.
RESULTS. Bilateral abnormalities were seen in all patients. Areas of ground-glass opacification were seen in 21 (66%) of 32 patients. Ground-glass opacification was the predominant CT feature in nine cases (28%). In 19 of 32 patients, ground-glass attenuation was associated with other abnormalities. Multiple nodules were identified in 19 patients (59%). Nodules were bilateral in 15 patients and unilateral in four patients. Nodules were the only CT finding in three patients (9%). Areas of air-space consolidation were identified in 19 patients (59%). Air-space consolidation was the only CT finding in one patient (3%). Other less common CT findings included thickening of the bronchovascular bundles (n = 7) and the tree-in-bud appearance (n = 4). Pleural effusions were seen in seven patients.
CONCLUSION. The thin-section CT manifestations of Cytomegalovirus pulmonary infection usually consist of a mixture of patterns, most commonly ground-glass attenuation, areas of consolidation, and small nodules.
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McGuinness et al. [3] described the thin-section CT findings in 21 patients with AIDS and Cytomegalovirus pneumonia. The most common abnormalities consisted of ground-glass attenuation, dense consolidation, and discrete pulmonary nodules or masses. The descriptions of the manifestations of Cytomegalovirus pneumonia in immunocompromised patients without AIDS have been limited to studies that included a small number of cases. In one series of 10 patients, the predominant abnormalities were small nodules, air-space consolidation, or a combination of both [4]. In another series of 10 patients, the most common CT pattern was of ground-glass attenuation, which was seen in all patients; small nodules were present in nine patients and consolidation, in seven patients [5].
The purpose of this study was to assess the thin-section CT findings in a relatively large number of immunocompromised patients without AIDS who had proven Cytomegalovirus pneumonia.
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The time interval between CT examination and the microbiologic diagnosis ranged from 1 to 16 days (median, 3 days). In all patients, when the interval between CT and microbiologic diagnosis was longer than 48 hr, the absence of significant interval change in the pattern of parenchymal abnormalities between the dates of CT and microbiologic diagnosis was ensured with sequential chest radiographs. The patients were 16 men and 16 women, who ranged in age from 22 to 70 years (mean age, 43 years).
CT
CT was performed on a Somaton Plus 4 CT scanner (Siemens, Erlangen,
Germany), a 900 or Asteion CT scanner (Toshiba Medical Systems, Tokyo, Japan),
or a HiLight scanner (General Electric Medical Systems, Milwaukee, WI). The
scans were obtained at end inspiration using 1- or 2-mm collimation at 10- or
20-mm intervals from the apex of the lung to the diaphragm, using 120 kV and
200–320 mA. The lungs were scanned at 1000–1500 H for the window
width and level settings of –600 to – 700 H.
The CT scans were jointly reviewed by two radiologists who were aware that all patients had a proven pulmonary viral infection; final decision on the findings was reached by consensus. The CT scans were assessed for the presence, extent, and anatomic distribution of ground-glass attenuation, air-space consolidation, nodules, centrilobular branching structures (tree-in-bud), thickening of the bronchovascular bundles, and pleural effusion. Ground-glass attenuation was defined as an area of hazy increased attenuation without obscuration of underlying vascular markings. Air-space consolidation was considered present if the opacities obscured the underlying vessels. Parenchymal nodules were subcategorized according to their distribution (centrilobular, peribronchovascular, subpleural, and random), location (upper or lower lung zone), marginal characteristics (smooth or irregular), and number (single or multiple). Centrilobular nodules were defined as parenchymal opacities located in the central portion of the secondary pulmonary lobule (lobular core). Nodules were also assessed to determine whether they were surrounded by a halo of ground-glass attenuation or had associated findings, such as pleural effusion.
The anatomic distribution was regarded as predominantly peripheral if abnormalities were seen mostly in the outer third of the lung, central if most were in the inner third of the lung, peribronchial if abnormalities occurred along the bronchovascular bundles, and random otherwise. The distribution was further subclassified as lobar, segmental, and patchy or nonsegmental. Zonal predominance was divided into upper or lower. Upper lung zone predominance was considered present if most of the abnormalities were above the level of tracheal carina and lower zone predominance, if the abnormalities were below that level.
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Findings on thin-section CT showed bilateral abnormalities in all patients (Table 1). Areas of ground-glass opacification were seen in 21 (66%) of 32 patients (Fig. 1). These areas had no zonal predominance and were patchy (n = 17) or diffuse (n = 3). In one case, ground-glass opacities had a centrilobular location. Ground-glass opacification was the predominant CT feature in nine (28%) of 32 cases, but in only one patient (3%) was it the only finding seen on CT. In 19 of 32 patients, ground-glass attenuation was associated with other abnormalities, including areas of air-space consolidation (n = 12), nodules (n = 13), thickening of the bronchovascular bundles (n = 7), and the tree-in-bud pattern (n = 2).
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Multiple nodules were identified in 19 (59%) of 32 patients (Fig. 2). Nodules were bilateral in 15 patients and unilateral in four patients. In 16 cases, nodules were associated with areas of ground-glass attenuation (n = 13) and with air-space consolidation (n = 8). Nodules were the only CT finding in three patients (9%). All nodules in all cases were smaller than 10 mm in diameter. In 12 cases (63%), the nodules had irregular margins (Fig. 3), and in seven cases (37%), the nodules had a halo of ground-glass attenuation (Fig. 4). The nodules had a centrilobular (n = 10), subpleural (n = 5), or random (n = 4) distribution.
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Areas of air-space consolidation were identified in 19 patients (59%). In 16 (84%) of these 19 patients, these areas had a lobular or subsegmental distribution, whereas in three (16%) of 19 patients, they had a segmental distribution. Air-space consolidation was the predominant CT feature in six (19%) of 32 patients (Fig. 5). The consolidation involved predominantly the lower lung zones (n = 7) or was randomly distributed (n = 12) (Fig. 6). Air-space consolidation was the only CT finding in one (3%) of the 32 patients (Fig. 7A, 7B). A peripheral distribution was found in four of seven patients with predominant air-space consolidation. Other less common CT findings included thickening of the bronchovascular bundles (n = 7) and the tree-in-bud appearance (n = 4) (Fig. 8). Pleural effusions were seen in seven patients.
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Histopathologic material was available for review in all cases and was correlated with the findings on thin-section CT. Areas of ground-glass attenuation or consolidation seen on CT scans corresponded to areas of the exudative or proliferative phase of diffuse alveolar damage. The predominant histologic findings in these patients were interstitial fibroblastic proliferation and lymphocytic infiltration associated with type 2 pneumocyte hyperplasia, hyaline membrane formation, and intraalveolar exudates with or without organization. The six patients with poorly defined centrilobular nodules seen on CT had bronchiolar and peribronchiolar accumulations of macrophages, RBCs, and fibrin. In two cases, the nodules were surrounded by a halo of ground-glass attenuation. The halo in these cases consisted of a zone of less dense inflammatory reaction and hemorrhage. Diagnostic cytomegalic cells with intracytoplasmic and intranuclear inclusions were seen in all pathologic specimens. No apparent differences were found among the 25 patients with bone marrow transplants, the five patients with solid organ transplants, and the two patients being treated with long-term corticosteroids.
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The clinical features of Cytomegalovirus pneumonia include fever, nonproductive cough, dyspnea, and hypoxemia. Diagnostic criteria for cytomegalovirus pneumonia are the detection of Cytomegalovirus organisms by culture, characteristic Cytomegalic inclusion bodies in bronchoalveolar lavage and transbronchial biopsy specimens, and absence of any other pulmonary pathogen identified by bacterial, fungal, or acid-fast stains or cultures, combined with the presence of fever, respiratory symptoms, and abnormal findings seen on CT [7–9].
Chest radiography is the first imaging technique performed in the examination of an immunocompromised patient with fever. Leung et al. [10] described the radiographic findings of Cytomegalovirus pneumonia in 22 infectious episodes in 52 patients with bone marrow transplants. The most common radiographic findings consisted of parenchymal consolidation and multiple nodules smaller than 5 mm in diameter; in two cases, the findings on chest radiographs were normal. An increasing number of patients undergo CT, especially thin-section CT, if there is a high clinical suspicion for pneumonia with normal or questionable radiographic findings. The CT findings of Cytomegalovirus pneumonia have been variably described as consisting of ground-glass attenuation, consolidation, linear opacities, nodules, or masses.
The findings in AIDS patients seem to differ from those in patients without AIDS. McGuinness et al. [3] described the thin-section CT findings in 21 AIDS patients with Cytomegalovirus pneumonia. The most common abnormalities consisted of ground-glass attenuation, consolidation, and discrete pulmonary nodules or masses. These investigators reported that in AIDS, the possibility of Cytomegalovirus pneumonia should be considered, particularly in patients who had Kaposi's sarcoma and areas of dense consolidation or masslike opacities. Although consolidation is also commonly seen in patients without AIDS, it is not dense and does not result in masslike opacities.
Our results concur with those of Moon et al. [5], who showed ground-glass attenuation to be the most frequent CT pattern in Cytomegalovirus pneumonia. In our study, ground-glass attenuation was found in 21 (66%) of our 32 patients, usually associated with air-space consolidation and nodules.
In 10 patients with proven Cytomegalovirus pneumonia, Kang et al. [4] identified four different patterns on CT consisting of of multiple bilateral nodules (1–5 mm) in six patients (60%), ground-glass opacity in four (40%), air-space consolidation in four (40%), and reticular opacities in one (10%). Ground-glass opacity and nodules were seen as a part of a mixed pattern in all and in four cases (40%) respectively; air-space consolidation and nodules were the only CT finding in two patients (20%) each. In our study, 16 (84%) of 19 patients with nodules had a mixed pattern that included ground-glass opacities and air-space consolidation.
Pathologic findings of Cytomegalovirus pneumonia included areas of acute interstitial pneumonia or diffuse alveolar damage and focal inflammatory or hemorrhagic lesions [7]. Our CT findings correlated with these histopathologic findings. Patchy or diffuse areas of ground-glass opacity were present in 87% of our patients and corresponded histopathologically to areas of diffuse alveolar damage. The halo sign was found in 37% of patients presenting with a nodular pattern of disease. Previously used to describe the CT appearance of hemorrhagic nodules due to invasive aspergillosis [11], this sign has been shown to occur in association with hemorrhagic nodules of various causes [12]. In patients with Cytomegalovirus pneumonia and poorly defined nodules or nodules with an associated halo, histologic correlation showed the nodular opacities to represent focal areas of inflammation or hemorrhage.
On the basis of our results, we consider that the most helpful findings with which to diagnose Cytomegalovirus pneumonia are the combination of nodules, ground-glass opacities, and areas of air-space consolidation.
Our study has several limitations: it is retrospective and includes images obtained with different CT scanners and patients with varying intervals between the CT scan and bronchoalveolar lavage and biopsy diagnosis.
In summary, the thin-section CT findings of Cytomegalovirus pneumonia in immunocompromised patients without AIDS usually consist of a mixture of patterns, most commonly ground-glass attenuation, air-space consolidation, and multiple small nodules. Some abnormalities in Cytomegalovirus pneumonia are often difficult to recognize on radiography but can easily be seen on thin-section CT.
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