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1 Department of Radiology, Taipei Medical University–Municipal Wan Fang
Hospital, 111 Hsing-Long Rd., Section 3, Taipei 116, Taiwan, Republic of
China.
2 Department of Radiology, School of Medicine, Taipei Medical University, 250
Wu-Hsing St., Taipei 110, Taiwan, Republic of China.
3 Department of Internal Medicine, Taipei Medical University–Municipal Wan
Fang Hospital, Taipei 116, Taiwan, Republic of China.
Received July 28, 2003;
accepted after revision November 6, 2003.
Address correspondence to W. P. Chan
(wingchan{at}tmu.edu.tw).
Abstract
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MATERIALS AND METHODS. We retrospectively reviewed the initial radiograph and a series of follow-up chest radiographs in 26 patients who had symptoms and signs consistent with SARS. Twenty-five patients completed the full course of radiographs in the hospital. The initial radiographic features and the distribution of parenchymal, mediastinal, and pleural abnormalities for each patient were evaluated. Follow-up radiographic findings were correlated with clinical outcomes for these patients.
RESULTS. Initial chest radiographs showed abnormalities in 23 (88%) of 26 subjects. Eighteen patients (69%) had air-space consolidation, two (8%) had ground-glass attenuation, one (4%) had nodules, and two (8%) had mixed consolidation and nodules. Four patients (15%) had pleural effusion. Younger patients and those with normal initial radiographic findings or unifocal lung lesions had better outcomes.
CONCLUSION. The initial predominant radiographic feature of SARS was air-space consolidation in the lateral and lower lung zones. Progressive deterioration to diffuse unilateral or bilateral consolidation in the series of follow-up chest radiographs is associated with a poor prognosis.
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SARS is a form of lung injury characterized by epithelial cell proliferation and an increase in macrophages in the lung [3]. Clinically, the disease is characterized by fever (> 38°C), nonproductive cough, progressive dyspnea, lymphopenia, and rapidly progressive lung changes on chest radiographs [4]. Current evidence suggests that a novel Coronavirus is associated with SARS [5].
Chest radiography has a crucial role in the diagnosis and monitoring of disease progression in the treatment of patients with SARS [6]. The purpose of our study was to evaluate the radiographic appearance of these patients and correlate these findings with the clinical outcomes.
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Frontal chest radiographs were obtained at initial clinical presentation and once a day during treatment. All initial chest radiographs were obtained after the onset of fever. All radiographic examinations were performed with computed radiography equipment (MU125M, Shimadzu) by using a standardized technique (70 kV, 2 mAs, 100-cm film-focus distance for the anteroposterior view, broad tube focus). The images were assessed using a PACS (picture archiving and communication system) viewer with a 2,560 x 2,048 pixel monitor (MGD 521 MK II, Barco).
Two radiologists interpreted all chest radiographs without knowing the clinical progress of the patients, and a consensus was reached. The observers evaluated the patterns and the distribution of the pulmonary parenchymal, mediastinal, and pleural abnormalities on each chest radiograph in all subjects. The patterns of parenchymal change were classified as air-space consolidation, ground-glass attenuation, nodules, and reticulation. Air-space consolidation was defined as homogeneous opacification of the parenchyma with the underlying vessels obscured. Ground-glass attenuation was defined as a diffuse increase in density that reduced the clarity of the pulmonary vessels but did not efface their outlines entirely [8]. Nodules were defined as focal round opacities.
The anatomic distribution was noted to be medial if the abnormality predominantly involved the medial half of the zone and lateral if it predominantly involved the lateral half. Abnormalities were classified as being distributed predominantly in the upper, middle, or lower lung zones, either unilaterally or bilaterally. The hilum, the paratracheal space, and the aortopulmonary window were evaluated for lymph node enlargement, and the pleural spaces were assessed for the presence of pleural effusion.
Twenty-five patients completed the hospital course of radiographs. The 26th patient was transferred to another hospital. The follow-up chest radiographs were evaluated for the relationship between the radiographic patterns and the clinical outcome of the disease. The peak time of the worst findings on chest radiography (showing the most opacity and the most lung involvement), the pattern of the initial chest radiograph, the appearance of the last chest radiograph, and the number of days in the hospital were included in the analysis. We identified pulmonary fibrosis on the last chest radiographs if reticular opacities or honeycombing appeared in the affected lung that had not been seen on the initial chest radiographs.
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Pleural effusions were found in four patients (15%) (Fig. 3), and three patients had associated air-space consolidation on the same side. Neither cavitation nor lymphadenopathy was noted on initial or follow-up chest radiographs.
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The right lung was involved in 17 (74%) of 23 patients and the left lung in 14 (61%). Involvement of the lateral lung parenchyma (12/23, 52%) was more common than a mixed medial and lateral pattern (9/23, 39%) or a medial pattern (2/23, 9%). Multifocal involvement (12/23, 52%) and unifocal involvement (11/23, 48%) were equally common. Unilateral disease (15/23, 65%) was more common than bilateral disease. Lower lung zone involvement (11/23, 48%) was more common than abnormalities in the upper (4/23, 17%), middle (1/23, 4%), or mixed lung zones (7/23, 30%).
Follow-Up Radiographs
The patterns on follow-up chest radiographs were the same as those on the
initial chest radiographs, except that one patient had a changed pattern from
air-space consolidation to ill-defined nodules. The three patients who
initially had normal findings on chest radiographs developed air-space
consolidations 3 days after the onset of symptoms (Fig.
4A,
4B).
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Clinical Outcome and Radiographic Patterns
Of the 25 patients who completed the hospital course of radiographs, 18
completely recovered and seven died. Younger patients and those with an
initially normal radiograph or a unifocal lung lesion had a better outcome
(Table 1).
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In the recovery group, the worst chest radiographs developed at a mean of day 3 (range, day 1–8), and the mean hospital stay was 12 days. The last chest radiographs before discharge were normal for 11 patients (61%), and five (28%) had minimal airspace consolidation or ground-glass attenuation. Two patients developed pulmonary fibrosis. In all patients who died, the worst chest radiographs were seen on the last day, and their mean hospital stay was 6 days. The last chest radiographs showed unilateral consolidation in two patients (29%) and diffuse bilateral consolidation compatible with the radiographic features of acute respiratory distress syndrome in five patients (71%).
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From recent reports [4, 6, 9, 10], the primary radiographic appearance of SARS is air-space consolidation, predominantly in the peripheral and lower lung zones; similar findings were observed in our study. One of our patients showed multiple bilateral nodules on the initial and follow-up chest radiographs. Pleural effusions have been uncommon in previous series [4, 6, 11], but we identified them in four of our patients (15%).
SARS is a form of lung injury characterized by epithelial cell proliferation and an increase in macrophages in the lung. Patients who have had SARS less than 10 days show hyaline membrane formation, pneumocyte proliferation, and edema. Diffuse alveolar damage is seen after 10 days. The diffuse alveolar damage typically goes through an exudative phase followed by a proliferative phase [3]. Pulmonary edema with hyaline membrane formation appears early in the phase of alveolar damage and then cellular fibromyxoid exudates appear in air spaces [12]. These findings may be identical to the rapidly progressing bilateral ground-glass opacities or consolidations observed in some of our patients as well as patients in other series [6, 9, 10] that are consistent with SARS.
The radiographic appearances of SARS are nonspecific and may be indistinguishable from those of bacterial bronchopneumonia or viral infections, and they share CT features with other conditions that result in subpleural air-space disease, such as bronchiolitis obliterans organizing pneumonia and acute interstitial pneumonia [4]. In later stages, particularly with diffuse involvement of the lungs, the radiographic appearance is similar to that of acute respiratory distress syndrome [4, 6, 9, 10].
Wong et al. [6] reported four patterns of radiographic progression in SARS; type 1 pattern (initial radiographic deterioration to peak level, followed by radiographic improvement with a maximum difference in overall mean lung involvement > 25%) was the most commonly observed, and type 4 pattern (progressive radiographic deterioration) seemed to be associated with poor prognosis. In our study, most patients in the recovery group showed the type 1 pattern, and all patients in the group who died showed the type 4 pattern. The type 2 pattern (fluctuating radiographic changes) and type 3 pattern (static radiographic appearance) were less common.
Antonio et al. [13] reported that fibrosis (detected on CT) occurred in more than half (62%) of their discharged SARS patients. In our recovery group, the last chest radiographs before discharge were normal in 11 patients (61%), and two patients (11%) showed fibrosis. It is possible that CT is more sensitive in detecting lung parenchymal change or that a longer follow-up period is needed.
Our study has some limitations. First, the two patients with pulmonary fibrosis were not evaluated on high-resolution CT. A frontal radiograph alone may not be accurate for identification of pulmonary fibrosis. Second, the pleural effusions were not evaluated pathologically and chemically. Three of the four patients with pleural effusion were older than 80; therefore, we cannot exclude the possibility that combined bacterial infection or heart disease induced the pleural effusion.
In summary, the initial radiographic feature of SARS was air-space consolidation, predominantly in the peripheral and the lower lung zones. The presence of a pleural effusion does not exclude SARS. The clinical outcome was better in younger patients and patients with initially normal lungs or a unifocal lung lesion.
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