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1 Department of Radiology, University of Paraná, Paraná,
Brazil.
2 Department of Radiology, University of Rio de Janeiro, Rio de Janeiro,
Brazil.
3 Department of Internal Medicine, University of Paraná, Paraná,
Brazil.
4 Department of Radiology, Vancouver General Hospital, 899 W 12th Ave.,
Vancouver, BC V5Z 1M9, Canada.
Received August 11, 2003;
accepted after revision November 6, 2003.
Address correspondence to N. L. Müller.
Abstract
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MATERIALS AND METHODS. The study included 20 consecutive patients who developed respiratory syncytial virus pneumonia after bone marrow transplantation and who had high-resolution CT of the chest performed within 24 hr after the onset of symptoms. The CT scans were reviewed by two chest radiologists who assessed the pattern and distribution of findings.
RESULTS. Bone marrow transplantation was performed on 12 male and eight female patients ranging from 3 to 48 years old (mean age, 25 years) for treatment of various forms of leukemia (n = 12), severe aplastic anemia (n = 6), Fanconi's syndrome (n = 1), and paroxysmal nocturnal hemoglobinuria (n = 1). Sixteen patients (80%) had abnormal CT findings. The predominant patterns of abnormality on high-resolution CT scans were small centrilobular nodules (10/20, 50%), air-space consolidation (7/20, 35%), ground-glass opacities (6/20, 30%), and bronchial wall thickening (6/20, 30%). The abnormalities were distributed in the central and peripheral areas of the lungs in nine cases, only in the periphery in five cases, and only in the central regions in two cases. The abnormalities were bilateral and asymmetric in distribution in 13 patients, bilateral and symmetric in two patients, and unilateral in one patient.
CONCLUSION. The most common high-resolution CT findings in patients with respiratory syncytial virus pneumonia after bone marrow transplantation consist of small centrilobular nodules and multifocal areas of consolidation and ground-glass opacities in a bilateral asymmetric distribution.
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Viral infection accounts for a significant proportion of pulmonary complications seen in patients with bone marrow transplants. The most commonly identified organism is cytomegalovirus. However, evidence is accumulating that other viruses including respiratory syncytial virus, influenza virus, parainfluenza virus, adenovirus, and picornaviruses also play an important role in the development of respiratory diseases in recipients of bone marrow transplants [2]. Infection with these viruses may account for a large proportion of patient pneumonias previously classified as idiopathic [2].
Respiratory syncytial virus is now recognized as one of the causes of life-threatening pneumonia in some subsets of immunocompromised patients, most notably transplant recipients and patients with hematologic malignancies [3–7]. Limited information is available, however, regarding the high-resolution CT findings of respiratory syncytial virus pneumonia in patients with bone marrow transplants.
The aim of this study was to review the high-resolution CT findings in 20 patients diagnosed with respiratory syncytial virus pneumonia after allogeneic bone marrow transplantation.
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The high-resolution CT was performed at end inspiration using 1-mm collimation at 10-mm intervals (Somaton ART, Siemens). Images were obtained at lung (width, 1,500 H; level, –700 H) and mediastinal (width, 400 H; level, 20 H) window settings. Two chest radiologists analyzed the high-resolution CT scans and reached final decisions by consensus. These CT findings were assessed: distribution of the lesions (central or peripheral, unilateral or bilateral, symmetric or asymmetric, and upper vs middle vs lower zone distribution), pattern of abnormality (ground-glass and air-space opacities, bronchial dilatation, bronchial wall thickening, tree-in-bud opacities, reticular opacities, large or small nodules, mosaic attenuation, and perfusion), lymph node enlargement, pleural effusions, and any other lung abnormalities. Criteria for these findings were those defined in the Fleischner Society's glossary of terms [9].
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All patients underwent allogeneic bone marrow transplantation. The time elapsed between bone marrow transplantation and the diagnosis of respiratory syncytial virus infection ranged from 1 to 103 days (median, 10 days; average, 28 days). Twelve patients (60%) had the viral infection while they had neutropenia (1–18 days after bone marrow transplantation; mean, 7 days; median, 5 days), and eight patients (40%) had the infection after recovery of their normal WBC (33–103 days after bone marrow transplantation; mean, 61 days; median, 60 days). Graft-versus-host disease was histologically proven in five cases (25%). All patients were treated with aerosolized ribavirin. Sixteen patients (80%) recovered and four (20%) died. The time interval between start of therapy and clinical and radiologic resolution of pneumonia ranged from 7 to 15 days.
Sixteen patients (80%) had parenchymal abnormalities evident on high-resolution CT, and four patients (20%) had normal findings on CT scans. Abnormalities included small centrilobular nodules (n = 10, 50%) air-space opacities (n = 7, 35%), ground-glass opacities (n = 6, 30%), bronchial wall thickening (n = 6, 30%), tree-in-bud opacities (n = 4, 20%), large nodules (n = 2, 10%) and bronchial dilatation (n = 1, 5%). The centrilobular nodules ranged from 1 to 5 mm in diameter (Fig. 1A, 1B). Five of the 10 patients with centrilobular nodules also had centrilobular branching nodular and linear opacities resulting in a tree-in-bud pattern (Fig. 2). The areas of air-space consolidation (Fig. 3A, 3B) and ground-glass attenuation (Fig. 1A, 1B) were multifocal. The two patients who presented with large nodules had multiple lesions, ranging from 10 to 20 mm in diameter, distributed mainly in the periphery of the lower lobes (Fig. 4A, 4B).
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The parenchymal abnormalities were distributed in both the central and peripheral zones of the lungs in nine patients, only in the periphery in five patients, and only in the central regions in two patients. The lower zone of the lungs was involved in 12 patients, the upper zone in eight patients, and the middle zone in six patients. The lung lesions were bilateral and asymmetric in 13 patients, bilateral and symmetric in two patients, and unilateral in one patient with abnormal CT.
The high-resolution CT findings in the five patients who had graft-versus-host disease were similar to those in the remaining patients. One of these patients had normal findings on CT. In the other four cases, the findings included ground-glass attenuation (n = 2, 50%), air-space opacities (n = 2, 50%), small centrilobular nodules (n = 1, 25%), bronchial wall thickening (n = 1, 25%), and large nodules (n = 1, 25%).
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The neutropenic phase occurs immediately after transplantation and is characterized by profound neutropenia lasting 2–3 weeks. Pulmonary complications in the neutropenic phase include fungal infections, particularly invasive aspergillosis, respiratory syncytial virus infection, diffuse alveolar hemorrhage, pulmonary edema, and drug toxicity.
The early phase occurs up to approximately 100 days after bone marrow transplantation, during which time patients show a gradual recovery of neutrophils and a lessening of immune impairment. The two most common pathogens to cause pulmonary complications during this phase are cytomegalovirus and respiratory syncytial virus.
The late phase begins approximately 100 days after bone marrow transplantation when the patient's immune status has returned to normal. Pulmonary complications typically encountered in the late phase include obliterative bronchiolitis, organizing pneumonia, and chronic graft-versus-host disease [10]. In our study, 12 cases (60%) of respiratory syncytial virus pneumonia occurred during the neutropenic phase after bone marrow transplantation (mean, 7 days; range, 1–18 days) and eight (40%) occurred during the early phase (mean, 61 days; range, 33–103 days).
Respiratory viral infections in bone marrow transplant recipients can result in serious morbidity and significant mortality. Several studies have shown an incidence of between 2.7% and 6.3%, and mortality rates between 19% and 78% [12–15]. Whimbey and Ghosh [16] evaluated the role of community respiratory viral infections in hospitalized adult bone marrow transplant recipients and found an incidence of respiratory syncytial virus pneumonia of 9.2% and a mortality rate of 60%. Harrington et al. [17] studied an outbreak of respiratory syncytial virus infection that occurred in a bone marrow transplantation center in 1990. They concluded that respiratory syncytial virus infection in marrow transplant patients is a serious and life-threatening infection with a high mortality rate if pneumonia develops, with preengraftment patients appearing to be more likely to develop pneumonia. These authors reported an incidence of respiratory syncytial virus pneumonia of 9% and a mortality rate of 78%. In our study, respiratory syncytial virus pneumonia had a fatal course in four patients (20%). Early diagnosis of respiratory syncytial virus pneumonia is important because patients often respond to prompt therapy [18–22].
Our study shows that the main patterns of abnormality on high-resolution CT consist of small centrilobular nodules, focal areas of consolidation, and ground-glass opacities. The abnormalities are usually bilateral and asymmetric in distribution. These findings are nonspecific, being similar to those of other infections described in bone marrow transplant patients [23, 24]. Areas of consolidation and ground-glass opacities may also be seen in a variety of noninfectious complications including pulmonary edema, drug reaction, and pulmonary hemorrhage [1, 10, 11]. However, asymmetric bilateral centrilobular nodular opacities are seen much more commonly in pulmonary infections than in noninfectious complications [24, 25]. The findings in respiratory syncytial virus pneumonia seen in patients after bone marrow transplantation are comparable to those described by Ko et al. [8] in 10 patients with respiratory syncytial virus infection after lung transplantation. The main abnormalities in their study consisted of ground-glass opacities seen in seven of 10 patients, air-space consolidation seen in five, and centrilobular nodular and branching linear opacities (tree-in-bud) pattern seen in four patients.
In summary, our study shows that respiratory syncytial virus pneumonia is an infection that usually occurs in the first 100 days after bone marrow transplantation, most commonly during the neutropenic phase. The high-resolution CT manifestations usually consist of an asymmetric bilateral distribution pattern of small centrilobular nodules, multifocal ground-glass opacities, and air-space consolidation.
Acknowledgments
We thank Ricardo Pasquini, Carlos de Medeiros, and the staff at the bone
marrow transplant unit at the Federal University of Paraná.
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