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DOI:10.2214/AJR.05.0128
AJR 2006; 186:1288-1293
© American Roentgen Ray Society

Clinical Observations

Adenovirus Pneumonia in Adults: Radiographic and High-Resolution CT Findings in Five Patients

Semin Chong1, Kyung Soo Lee1, Tae Sung Kim1, Myung Jin Chung1, Man Pyo Chung2 and Joungho Han3

1 Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50, Ilwon-dong, Kangnam-gu, Seoul 135-710, Korea.
2 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 135-710, Korea.
3 Department of Pathology, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul 135-710, Korea.

Received January 26, 2005; accepted after revision April 18, 2005.

 
Address correspondence to K. S. Lee (kyungs.lee{at}samsung.com).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of this study was to describe the radiographic and high-resolution CT (HRCT) findings of adenovirus pneumonia in five patients.

CONCLUSION. Adenovirus pneumonia in adults appears as bilateral patchy parenchymal opacities on chest radiographs and as bilateral ground-glass opacities with a random distribution with or without consolidation on HRCT images. These findings, however, are not specific for adenovirus pneumonia.

Keywords: CT • high-resolution CT • infectious diseases • lung • lung diseases • pneumonia • radiography


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Viral pneumonia in adults may be classified into two clinical groups: so-called atypical pneumonia, in otherwise healthy hosts, and viral pneumonia, in immunocompromised hosts [1]. With adenoviral respiratory tract infection, immunocompromised patients are more prone to pneumonia and more prone to develop adult respiratory distress syndrome than immunocompetent patients [2]. Pathologically, the lungs in adenovirus pneumonia usually show patchy areas of hemorrhagic consolidation, are mixed with areas of overinflation or atelectasis, and contain necrotic changes with diffuse alveolar damage [3]. In mild forms, findings of interstitial inflammatory cell infiltration may predominate, and nuclear inclusion bodies, most prominent in alveolar lining cells, may be identified in infected cells [4, 5].

In adults with adenovirus pneumonia, mainly in immunocompromised patients, chest radiographs show bilateral or unilateral parenchymal opacities [6]. However, to the best of our knowledge, only a few reports have included the CT findings of adenovirus pneumonia in adults [6, 7]. The purpose of the present study was to describe the radiographic and high-resolution CT (HRCT) findings of histopathologically confirmed adenovirus pneumonia in five adults.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
We reviewed retrospectively chest radiographs and HRCT scans of five patients with adenovirus pneumonia. Patients (male-female ratio, 1:4; age range, 35-76 years; mean age, 52.6 years) were identified by reviewing complete medical record archives at the Division of Pulmonary and Critical Care Medicine at our institution. In four patients, diagnoses were made using lung biopsy specimens obtained by videotape-assisted thoracoscopic surgery (VATS). The specimens were evaluated using H and E and immunohistochemical stains. Immunohistochemical staining was accomplished by incubating undigested 5-mm tissue sections with a 1:400 dilution of monoclonal mouse antiadenovirus solution recognizing serotypes 1-41 (MAb Set, Chemicon) for 30 min at room temperature [8]. In the remaining patient, the diagnosis was confirmed by a positive viral culture for adenovirus in bronchoalveolar lavage (BAL) fluid. In that patient, the transbronchial biopsy specimen also showed cytopathologic changes characteristic of adenovirus. Bacterial cultures or viral cultures for cytomegalovirus, influenza virus, parainfluenza virus, herpes simplex virus, or respiratory syncytial virus using BAL fluid were negative in all patients. One patient with adenovirus pneumonia, who also had Pneumocystis carinii identified in BAL fluid, was excluded from this study.

Two patients had acute myelogenous leukemia and one had non-Hodgkin's lymphoma. These three patients had received an allogeneic bone marrow transplant (n = 2; 4 and 11 months before, respectively) or an allogeneic peripheral blood stem cell transplant (12 months before) before the onset of the adenovirus infection. The other two patients were immunocompetent without underlying disease. Thus, our study population comprised three immunocompromised patients and two immunocompetent patients. Patients presented with fever (n = 5), dyspnea (n = 5), cough (n = 2), sputum (n = 1), and hemoptysis (n = 1). At presentation, three patients had a normal WBC; one, leukopenia (1.9 x 103/µL); and another, leukocytosis (14.9 x 103/µL). Antiviral therapy (ribavirin in two, cidofovir in two, and ganciclovir in one) was administered to all patients. Four patients died of the infection (mean survival after diagnosis, 55 days; range, 14-173 days). One immunocompetent patient recovered completely from the infection over a follow-up period of 3 months.


Figure 1
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  		Fig. 1A —35-year-old woman with non-Hodgkin's lymphoma who developed adenovirus pneumonia 1 year after allogeneic peripheral blood stem cell transplantation. Anteroposterior chest radiograph shows patchy opacities (arrows) in both lungs. Also note endotracheal intubation tube and central venous line.

 


Figure 2
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  		Fig. 1B —35-year-old woman with non-Hodgkin's lymphoma who developed adenovirus pneumonia 1 year after allogeneic peripheral blood stem cell transplantation. High-resolution (1.0-mm collimation) CT scans obtained at level of great vessels (B) and right inferior pulmonary vein (C) show extensive and patchy ground-glass opacities (arrows) associated with interlobular septal thickening (arrowheads) and intralobular linear opacities in both upper lobes, forming so-called crazy paving appearance. Also note small amount of left pleural effusion.

 


Figure 3
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  		Fig. 1C —35-year-old woman with non-Hodgkin's lymphoma who developed adenovirus pneumonia 1 year after allogeneic peripheral blood stem cell transplantation. High-resolution (1.0-mm collimation) CT scans obtained at level of great vessels (B) and right inferior pulmonary vein (C) show extensive and patchy ground-glass opacities (arrows) associated with interlobular septal thickening (arrowheads) and intralobular linear opacities in both upper lobes, forming so-called crazy paving appearance. Also note small amount of left pleural effusion.

 


Figure 4
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  		Fig. 1D —35-year-old woman with non-Hodgkin's lymphoma who developed adenovirus pneumonia 1 year after allogeneic peripheral blood stem cell transplantation. Photomicrograph of pathologic specimen obtained by videotape-assisted thoracoscopic surgery biopsy shows intraalveolar fibrinous exudate forming hyaline membrane (arrows) and interstitial fibroblastic proliferation (arrowheads), suggestive of mixed exudative and proliferative phase of diffuse alveolar damage. (H and E, x100)

 
Chest radiographs and HRCT scans of the thorax were obtained on the same day. The time interval between radiologic examinations and a pathologic or microbiologic diagnosis was 2-7 days (mean, 4.4 ± 2.1 [SD] days). Posteroanterior chest radiographs were obtained using a computed radiography system (FCR 9501, Fuji) with the following parameters: 120 kVp; nominal focus, 0.6 or 1.2 mm; film-focus distance, 183 cm; oscillating grid, 12:1; and exposure, photo-timed.

Two chest radiologists (with 15 and 2 years of experience in thoracic imaging, respectively) reviewed the chest radiographs and HRCT scans together, and decisions concerning findings were reached by consensus. The observers assessed the presence and distribution of parenchymal opacities, nodules, and reticulation on chest radiographs. An opacity was defined as a circumscribed area that appears more nearly white than its surroundings without a discrete border. A nodule was defined as a circular opacity with a discrete border. Reticulation was defined as a collection of innumerable small linear opacities that together produce an appearance resembling a net [9]. For analysis purposes, each lung was divided into upper and lower zones. Lesions were considered to be located in the upper lung zone when located cephalad to the hilum, in the lower lung zone when located caudad to the hilum, or random when located in both zones.


Figure 5
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  		Fig. 1E —35-year-old woman with non-Hodgkin's lymphoma who developed adenovirus pneumonia 1 year after allogeneic peripheral blood stem cell transplantation. Photomicrograph of pathologic specimen shows alveolar lining cell with intranuclear inclusions, which are surrounded by halo (arrows). (H and E, x1,000)

 


Figure 6
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  		Fig. 1F —35-year-old woman with non-Hodgkin's lymphoma who developed adenovirus pneumonia 1 year after allogeneic peripheral blood stem cell transplantation. Photomicrograph of pathologic specimen after immunohistochemical staining for adenovirus shows poorly demarcated smudges (arrowheads) within nucleus, indicating positivity for adenovirus infection. (x400)

 
HRCT scans of the chest were obtained using 1-mm collimation at 10-mm intervals without IV contrast medium injection. All CT data were reconstructed using a high-spatial-frequency algorithm. CT scans were obtained using commercially available CT scanners (HiSpeed Advantage, LightSpeed QXi, or LightSpeed Ultra, GE Healthcare). Scan data were displayed directly on four monitors with 1,536 x 2,048 image matrices, 8-bit viewable gray-scale, and 60-foot-Lamberts luminescence of a PACS (PathSpeed, GE Healthcare). Scans were obtained using both mediastinal window (window width, 400 H; window level, 20 H) and lung window (window width, 1,500 H; window level, -700 H) settings.

We assessed the presence and distribution of lung parenchymal abnormalities and the presence of pleural effusion and of mediastinal or hilar lymphadenopathy. HRCT scans were assessed particularly for the presence and distribution of parenchymal abnormalities including ground-glass opacity, consolidation, small nodules (< 10 mm in diameter), nodules (10-30 mm in diameter), interlobular septal thickening, intralobular lines, and bronchial dilatation. Consolidation was defined as an area of opacification that obscured the underlying vessels; ground-glass opacity was defined as a hazy increase in lung attenuation with no obscuration of the underlying vessels. Septal thickening was defined as abnormal widening of an interlobular septum or septa. Intralobular lines were defined as intralobular networks. The distribution of the patterns on CT scans was categorized as unilateral or bilateral. The anatomic distribution of parenchymal abnormalities was classified as subpleural, central, or random in the transaxial plane; upper, lower, or random in the longitudinal plane; and peribronchovascular or random.

In four patients, in whom pathologic specimens were obtained using VATS at the area of parenchymal opacity (ground-glass opacity or mixed area of ground-glass opacity and consolidation) on CT scans, CT-pathologic correlation was performed. In one of the four patients, the crazy paving appearance (ground-glass opacity with superimposed interlobular septal thickening and intralobular lines) was detected at the site of biopsy.


Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The most common radiographic finding was parenchymal opacity (n = 5), which was bilateral (n = 4) or unilateral (n = 1) and patchy (n = 5) in distribution (Figs. 1A, 1B, 1C, 1D, 1E, 1F, 2A, 2B, and 2C). The parenchymal opacity involved both upper and lower lung zones in all patients. One patient had ill-defined small nodules in the unilateral lower lung zone associated with parenchymal opacities. No patient showed reticulation.


Figure 7
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  		Fig. 2A —76-year-old woman with history of fever and dyspnea who developed adenovirus pneumonia. Chest radiograph shows patchy areas of parenchymal opacities (arrows) in both lungs.

 

Figure 8
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  		Fig. 2B —76-year-old woman with history of fever and dyspnea who developed adenovirus pneumonia. High-resolution (1.0-mm collimation) CT scans obtained at subcarinal level (B) and at level of left basal trunk (C) show patchy subpleural ground-glass opacities (arrows) in both lungs, associated with consolidative areas (arrowheads).

 

Figure 9
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  		Fig. 2C —76-year-old woman with history of fever and dyspnea who developed adenovirus pneumonia. High-resolution (1.0-mm collimation) CT scans obtained at subcarinal level (B) and at level of left basal trunk (C) show patchy subpleural ground-glass opacities (arrows) in both lungs, associated with consolidative areas (arrowheads).

 
The HRCT findings included ground-glass opacity (n = 5), consolidation (n = 3), small nodules (n = 1), interlobular septal thickening (n = 1), bronchial dilatation (n = 1), and pleural effusion (n = 3) (Figs. 1A, 1B, 1C, 1D, 1E, 1F, 2A, 2B, and 2C). Ground-glass opacity (n = 5), which was bilateral in all patients, showed a mainly random distribution in both the transaxial (n = 4) and longitudinal (n = 4) planes (Figs. 1A, 1B, 1C, 1D, 1E, 1F, 3A, and 3B). Consolidation (n = 3), which was bilateral (n = 2) or unilateral (n = 1) (Figs. 3A and 3B), showed upper lung zone (n = 2) or random (n = 1) distribution in the longitudinal plane and random (n = 2) or subpleural (n = 1) distribution in the transaxial plane (Figs. 2A, 2B, and 2C). Small nodules, which were seen in one patient and which were associated with ground-glass opacity, involved unilaterally the lower lung zone and were located in the centrilobular areas. Interlobular septal thickenings (n = 1) and intralobular lines (n = 1), bilaterally associated with ground-glass opacities, formed a crazy paving pattern (Figs. 1A, 1B, 1C, 1D, 1E, and 1F and Table 1). Mild bronchial dilatation (n = 1) was associated with areas of consolidation and ground-glass opacity. Small amounts of pleural effusion were identified in three patients: bilateral in two and unilateral in one (Figs. 1A, 1B, 1C, 1D, 1E, and 1F). None had mediastinal or hilar lymphadenopathy.


Figure 10
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  		Fig. 3A —36-year-old woman with acute myelogenous leukemia who developed adenovirus pneumonia 4 months after allogeneic bone marrow transplantation. A, High-resolution (1.0-mm collimation) CT scan obtained at level of great vessels in thoracic inlet shows subpleural consolidation (arrow) in right upper lobe and patchy ground-glass opacities (arrowheads) in both lungs.

 

Figure 11
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  		Fig. 3B —36-year-old woman with acute myelogenous leukemia who developed adenovirus pneumonia 4 months after allogeneic bone marrow transplantation. B, CT scan obtained at level of aortic arch shows patchy ground-glass opacities (arrowheads) with random distribution in both lungs.

 

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  		TABLE 1: Patterns and Distribution of High-Resolution CT Findings in Five Patients with Adenovirus Pneumonia

 

In three immunocompromised patients, the main patterns of abnormalities were parenchymal opacity on chest radiography and ground-glass opacity on HRCT. In two immunocompetent patients, they were also opacity and ground-glass opacity, respectively.

On CT-pathologic correlation (n = 4), parenchymal opacities observed on HRCT corresponded histopathologically to the areas of interstitial fibroblastic proliferation with inflammatory cell infiltration and to intraalveolar fibrinous exudates containing hemosiderin-laden macrophages and forming hyaline membranes, suggestive of the late exudative or proliferative phase of diffuse alveolar damage (Fig. 1D). In one patient, intraalveolar hemorrhage was associated with diffuse alveolar damage findings. The histopathologic findings of specimens obtained from crazy paving appearance were not different from those of ground-glass opacity without crazy paving appearance. H and E staining showed cytopathologic changes characteristic of adenovirus, discrete dense eosinophilic or basophilic-amphophilic "smudgy" intranuclear inclusions. Immunohistochemical staining showed positivity for adenovirus (Figs. 1E and 1F).


Discussion
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
In adults, adenovirus pneumonia occurs commonly in immunocompromised hosts including patients who have received organ and bone marrow transplants [10, 11], whereas in healthy individuals it is rare [7]. Our study population comprised five adults, either immunocompromised (n = 3) or immunocompetent (n = 2).

Few studies on the CT findings of adenovirus pneumonia have been reported in the literature [6]. In our study, three immunocompromised patients who underwent bone marrow or peripheral stem cell transplantation due to leukemia or lymphoma showed extensive ground-glass opacities with (n = 2) or without (n = 1) consolidation on HRCT. In a case study of adenovirus pneumonia in an immunocompetent adult, Motallebi et al. [7] reported that adenovirus pneumonia presented with patchy ground-glass opacities on HRCT. In our series, two immunocompetent adults presented with ground-glass opacities with or without consolidation on HRCT. Although the number of patients was small, no differences in radiologic findings were evident between immunocompromised and immunocompetent patients; both groups had parenchymal opacities on chest radiography and ground-glass opacities with or without consolidation on HRCT. Adenovirus is one of the viral entities associated with obliterative bronchiolitis or Swyer-James syndrome in children and obliterative bronchiolitis in transplant recipients [2, 5, 12].

Extensive or diffuse ground-glass opacity on HRCT, with an associated extensive differential diagnosis, is known to represent either interstitial or alveolar disease [13]. According to the clinical symptom duration of lung disease and the immune status of the patient, differential diagnoses in patients with these ground-glass opacities are variable. An acute disease process with ground-glass opacity in a patient with AIDS or in an organ transplant recipient is suggestive of P. carinii, cytomegalovirus, or herpes simplex virus pneumonia [14]. In an immunocompetent adult, on the other hand, acute lung disease with ground-glass opacity is suggestive of pulmonary hemorrhage; pulmonary edema; acute eosinophilic pneumonia; or atypical pneumonias caused by Mycoplasma pneumoniae, influenza virus, or varicella-zoster virus [15].

In recent studies of adult viral pneumonia caused by cytomegalovirus or influenza virus [1], ground-glass opacity was the most common findings on HRCT with no zonal predominance, although consolidation may be associated. Ground-glass opacity corresponds histopathologically to areas of acute diffuse alveolar damage comprising interstitial lymphocyte infiltration, intraalveolar hemorrhage, edema and fibrin, type II cell hyperplasia, and hyaline membrane formation [1, 7]. Similarly in our series, ground-glass opacities observed on HRCT were histopathologically correlated with interstitial fibroblastic proliferation with inflammatory cell infiltration and with intraalveolar fibrinous exudates containing hemosiderin-laden macrophages and forming hyaline membrane, suggestive of the late exudative or proliferative phase of diffuse alveolar damage.

The crazy paving pattern composed of scattered or diffuse ground-glass opacities with superimposed interlobular septal thickening and intralobular lines on HRCT had a variety of potential causes, which include P. carinii pneumonia, mucinous bronchioloalveolar carcinoma, pulmonary alveolar proteinosis, nonspecific interstitial pneumonia, exogenous lipoid pneumonia, adult respiratory distress syndrome, and pulmonary hemorrhage syndromes [16]. In the present study, one patient had a crazy paving pattern on HRCT (Figs. 1A, 1B, 1C, 1D, 1E, and 1F) and histopathology showed interstitial pneumonia with fibrous thickening and intraalveolar hemorrhage with hemosiderin-laden macrophages in the lung specimen obtained by VATS biopsy. We propose this crazy paving pattern might be an HRCT finding of diffuse alveolar damage caused by adenovirus pneumonia.

Our study has several limitations. Its first and major limitation is that the sample size was small, which was mainly due to the difficult early detection of adenoviral infection. Second, obtaining positive viral culture results for adenovirus pneumonia is problematic because adenovirus shows slow growth; thus, its identification is difficult. Four of our five patients failed to produce a positive viral culture result. Therefore, adenovirus pneumonia was diagnosed on the basis of the presence of positive intranuclear inclusion bodies and a background of diffuse alveolar damage by H and E staining and positive immunohistochemical staining for adenovirus. Third, a positive immunohistochemical study is probably not sufficient for a confident diagnosis of adenoviral infection in the absence of a clinical setting of acute-onset pneumonia or a background of the histopathologic changes of diffuse alveolar damage. However, this immunohistochemical staining method has been described as having potential for early detection and to be useful for confirming a diagnosis of adenovirus infections, including adenovirus pneumonia [4, 8].

In conclusion, adenovirus pneumonia manifested usually as bilateral parenchymal opacities on chest radiographs and as extensive or diffuse bilateral ground-glass opacities with or without consolidation on HRCT scans. These findings are not specific for adenovirus infection; however, in immunocompromised or immunocompetent patients suspected of having an acute lower respiratory infection with clinical manifestations of dyspnea and fever, the possibility of adenovirus pneumonia should be included when extensive or diffuse bilateral ground-glass opacities are associated with areas of consolidation on HRCT.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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