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Original Report |
1 Department of Radiology, Vancouver General Hospital, University of British
Columbia, 899 W. 12th Ave., Vancouver, BC V5Z 1M9, Canada.
2 Department of Hematology, Vancouver General Hospital, University of British
Columbia, Vancouver, BC V5Z 1M9, Canada.
Received December 13, 2002;
accepted after revision January 30, 2003.
Address correspondence to N. L. Müller.
Abstract
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CONCLUSION. Radiologic findings of influenza virus pneumonia in immunocompromised patients consist of patchy or confluent consolidation and nodular opacities on chest radiography and ground-glass attenuation, consolidation, centrilobular nodules, and branching linear opacities on high-resolution CT.
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To our knowledge, the radiographic and high-resolution CT findings of influenza pneumonia in immunosuppressed patients who have hematologic malignancies have not been previously described. The aim of our study was to describe the radiographic and high-resolution CT findings of confirmed influenza virus pneumonia in four immunocompromised patients with hematologic malignancies.
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The four patients in our study population were two women and two men whose ages ranged from 25 to 62 years (mean, 38 years; median, 32 years). All patients had hematologic malignancies: two patients had acute lymphoblastic leukemia, one had multiple myeloma, and one had acute myelogenous leukemia. Two of the patients had received an allogeneic bone marrow transplant before the onset of the influenza infection.
All four patients presented with cough, and three had significant fever (> 38°C [> 100.4°F]). The only afebrile patient was on high-dose corticosteroids. Only one of the patients had dyspnea, and only one had a normal WBC. Three of the four had significant leukopenia (WBC < 1.0 x 103/L).
Type A influenza virus pneumonia was confirmed in all patients by findings of a direct fluorescent antibody against influenza virus in bronchoalveolar lavage fluid. In the bone marrow transplant recipients, the infection was diagnosed 1 week after the transplantation procedure (i.e., during the preengraftment period) in one patient and 75 days after the transplantation procedure (i.e., during the early postengraftment period) in the other patient. Chest radiographs and high-resolution CT scans of the chest were obtained the day before bronchoalveolar lavage was performed. Three patients (one, a bone marrow transplant recipient) received antiviral therapy (amantidine hydrochloride), and all three showed clinical improvement. Radiographic follow-up was performed immediately after bronchoalveolar lavage and up to 25 days later. One patient had follow-up high-resolution CT (HiSpeed Advantage scanner and Advantage workstation, General Electric Medical Systems, Milwaukee, WI) performed 8 days and another, 4 months after the bronchoalveolar lavage.
Our CT protocol consisted of obtaining 1-mm-thick high-resolution CT scans at 10-mm intervals that were then reconstructed using a high spatial frequency algorithm. The entire thorax was scanned with the supine patient asked to suspend inspiration. Scans were obtained with both the lung window (window width, 1000–1500 H; level, –700 H) and mediastinal window (window width, 450 H; level, 35 H) settings. The CT scans and chest radiographs were reviewed by two observers who reached a decision about the pattern and distribution of the findings by consensus.
The reviewers assessed the presence, distribution, and predominance of the imaging findings on chest radiographs and CT scans. The chest radiographs were assessed particularly for the presence and distribution of parenchymal consolidation, ground-glass opacities, and large and small nodules. Large nodules were defined as discrete opacities larger than 1 cm and small nodules, as 1 cm or smaller. The overall distribution of findings was assessed. Distribution of abnormalities was also assessed as being predominantly in the upper, middle, or lower lung zones and as being in either the central or peripheral lung regions. High-resolution CT scans were assessed for the presence of ground-glass opacifications, consolidation, large and small nodules, centrilobular nodular and branching linear opacities (i.e., tree-in-bud pattern), and septal thickening. The presence of zonal (upper, middle, or lower and central or peripheral) and lateral (unilateral or bilateral) predominance was also assessed. For the CT scans, consolidation was defined as an area of opacification that obscured the underlying vessels; in contrast, ground-glass opacity was defined as a hazy increase in lung attenuation with no obscuration of underlying vessels. The presence of a halo of ground-glass attenuation around the nodules and the presence of pleural effusions and mediastinal lymphadenopathy were also evaluated.
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All three patients who underwent high-resolution CT exhibited ground-glass opacities, consolidation, nodules, and a tree-in-bud pattern. In two of the three patients in whom ground-glass opacities were identified, it was the predominant finding (Fig. 1A, 1B). In all patients, ground-glass opacities were patchy; in two of the three, the opacities were bilateral, and in one, the opacities were unilateral. The ground-glass opacities showed upper lobe predominance in two patients and lower lobe predominance in another. Small areas of consolidation were seen in all three patients and were bilateral (two patients) or unilateral (one patient). The consolidation involved mainly the upper lobes in two patients and the lower lobes in one patient.
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Centrilobular nodules measuring 2–9 mm in diameter were seen on high-resolution CT scans in all three patients who had CT scans and were the predominant finding in one patient (Fig. 2A, 2B, 2C). The nodules were associated with areas of ground-glass attenuation in all the patients and were bilateral in two patients and unilateral in one. The centrilobular nodules were asymmetric in distribution and involved mainly the upper (two patients) or lower (one patient) lobes. The tree-in-bud pattern seen in the three patients who underwent CT was limited to small areas of the parenchyma and was asymmetric and bilateral in distribution (Fig. 2A, 2B, 2C).
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Nodules ranging from 1 to 3 cm in diameter were present in one patient. A surrounding halo of ground-glass attenuation was noted in one of these large nodules. None of the nodules in this or any other patient had evidence of cavitation.
In two patients, minimal septal thickening was noted adjacent to areas of consolidation. A small amount of pleural effusion was identified in two patients, one of whom had bilateral effusion. None of the patients had mediastinal lymphadenopathy.
On high-resolution CT scans, the extent of the disease and patterns of abnormality were more evident than on the radiographs. In two patients with only patchy consolidation evident on the radiographs, high-resolution CT scans showed ground-glass opacities, centrilobular nodules, branching linear opacities (tree-in-bud pattern), and consolidation. Minimal septal thickening (one patient) and small pleural effusions (two patients) were identifiable only on CT scans.
In three patients, radiologic improvement was noted at follow-up. In the remaining patient, follow-up radiography showed progression of the disease, and follow-up CT performed 8 days later showed more extensive areas of consolidation and multiple centrilobular nodules.
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The radiographic findings of influenza virus pneumonia in immunocompetent patients are well known. These changes are nonspecific and most commonly consist of segmental areas of consolidation that may be homogeneous or patchy and unilateral or bilateral. Serial radiographs show poorly defined, patchy areas of air-space consolidation with a 1–2 cm diameter that rapidly becomes confluent. Pleural effusion is rare. The radiologic abnormalities usually resolve in approximately 3 weeks. Kim et al. [7] reported the radiographic findings of influenza virus pneumonia in two immunocompetent patients as consisting of poorly defined bilateral nodules and reticular areas of increased opacity that progressed to diffuse consolidation.
Information about the radiographic findings of influenza pneumonia in immunocompromised patients is limited. Leung et al. [8] in their study of 59 cases of pulmonary infection in bone marrow transplant recipients included one case of influenza virus B pneumonia, a patient whose chest radiograph showed 20–30 nodules with diameters of 6–10 mm in the middle and lower zones of both lungs with no other associated findings. In a retrospective study of the radiographic findings of viral infection in 21 lung transplant recipients, the authors reported that one patient with influenza virus pneumonia showed bilateral homogeneous opacities that progressed to show patterns associated with acute respiratory distress syndrome, whereas the other patient had only minimal abnormalities [9]. In our study, the radiographic findings consisted mainly of unilateral or bilateral patchy areas of consolidation with or without associated poorly defined nodular opacities.
Kim et al. [7] evaluated the high-resolution CT findings of influenza virus pneumonia in two immunocompetent patients and reported that both lungs had areas of multi-focal peribronchovascular or subpleural consolidation. In one patient, some areas of consolidation had lobular distribution and were associated with air-space nodules. Small centrilobular nodules representing alveolar hemorrhage were also seen. The other patient showed diffuse ground-glass opacities with irregular linear areas of increased attenuation. Tanaka et al. [10] reported the high-resolution CT findings of influenza virus pneumonia in an immunocompetent patient as consisting of bilateral areas of ground-glass attenuation with a lobular distribution.
In our study, the predominant high-resolution CT findings in the three patients who had scans available were ground-glass opacities in two patients and centrilobular nodules and branching linear opacities (tree-in-bud pattern) in one. A lobular distribution of the ground-glass opacities was evident in one patient. On CT, all three patients had small patchy areas of consolidation; in one patient, these areas had a lobular distribution. The ground-glass opacities were all associated with patchy areas of air-space consolidation and centrilobular nodules. All cases of air-space consolidation were patchy in distribution.
The radiographic and high-resolution CT findings of influenza pneumonia seen in our study are similar to those described for other infections, including bacterial pneumonia, mycoplasmal pneumonia, and chlamydial pneumonia [10]. However, centrilobular nodular and linear opacities (i.e., the tree-in-bud pattern) seen on high-resolution CT scans in our patients are signs that are suggestive of pulmonary infection. A tree-in-bud pattern is seen much more commonly in viral, bacterial, and mycoplasmal bronchiolitis and pneumonia than in noninfectious pulmonary opacities [11].
One of our patients had 1- to 3-cm nodules with hazy margins; one of the nodules was surrounded by a CT halo of ground-glass opacification. The CT halo sign has been described as a characteristic feature of hemorrhagic nodules in immunocompromised patients. The sign has been reported in patients with cytomegalovirus, angioinvasive pulmonary aspergillosis, and herpes simplex virus or Candida pneumonias. McGuinness et al. [12] in their study of cytomegalovirus pneumonia in 21 AIDS patients found large nodules or masses ranging from 1 to 3 cm in diameter in 12 patients; in four patients, the nodules were the predominant abnormality.
Our study has two major limitations. First, the small number of patients does not allow us to make generalized statements about the range of potential abnormalities. Second, no correlation with pathologic findings was possible because it was a retrospective study.
In conclusion, the findings of our study are that the radiographic findings of influenza A virus pneumonia in patients with hematologic malignancies consist of bilateral or unilateral patchy areas of consolidation associated with nodular opacities and that the CT findings consist of ground-glass opacities, patchy consolidation, centrilobular nodules, and branching linear opacities, also known as the tree-in-bud pattern. These findings are not unique to this particular infection; similar radiologic changes are seen in patients with other viral and bacterial pneumonias.
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