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1 Department of Radiology, Vancouver General Hospital, University of British
Columbia, 899 W 12th Ave., Vancouver, BC V5Z 1M9, Canada.
2 Department of Diagnostic Radiology, The University of Hong Kong, Queen Mary
Hospital, Hong Kong SAR, China.
3 Department of Medicine, The University of Hong Kong, Queen Mary Hospital, Hong
Kong SAR, China.
Received May 30, 2003;
accepted after revision July 23, 2003.
Address correspondence to N. L. Müller.
Abstract
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MATERIALS AND METHODS. We reviewed the HRCT findings at presentation (n = 12) and after hospital admission (n = 25) of 29 patients with SARS and compared the HRCT findings with the radiographic findings. HRCT scans were obtained using 1-mm (n = 28) or 2-mm (n = 1) collimation. The radiographs and HRCT scans were reviewed independently by two observers who reached a decision by consensus.
RESULTS. All patients had abnormal findings on HRCT at presentation. Eight of these 12 patients had normal findings on radiographs. The predominant HRCT findings at presentation consisted of unilateral (n = 6) or bilateral (n = 2) ground-glass opacities or focal unilateral (n = 2) or bilateral (n = 2) areas of consolidation. All patients showed progression of disease on follow-up. The predominant HRCT findings on follow-up CT scans consisted of unilateral (n = 2) or bilateral ground-glass opacities (n = 13), unilateral (n = 2) or bilateral consolidation (n = 5), or a mixed bilateral pattern of ground-glass attenuation, consolidation, and reticulation (n = 3). Reticulation with associated architectural distortion and mild traction bronchiectasis was present in eight patients.
CONCLUSION. HRCT can show parenchymal abnormalities in patients with SARS who have normal findings on radiographs at presentation. Follow-up CT scans obtained in hospitalized patients show findings consistent with fibrosis in a small percentage of patients.
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SARS was first reported in southern China in November 2002 and rapidly spread throughout the world [4]. The clinical manifestations typically consist of fever with measured temperature greater than 100.4°F (> 38°C), nonproductive cough, and progressive dyspnea [5]. Most patients have lymphopenia and elevated serum liver transaminase levels [6, 7]. The radiographic manifestations at presentation include unilateral and bilateral areas of consolidation and ground-glass opacities [6, 8, 9]. Preliminary studies have shown that high-resolution CT (HRCT) may show parenchymal abnormalities in patients with SARS who have normal findings on radiographs [9, 10]. Limited information is available, however, on the abnormal findings on radiography and HRCT seen in the follow-up of patients with SARS. The aim of this study was to review the HRCT findings at presentation and on follow-up in patients with SARS and to compare the HRCT findings with radiographic findings.
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Chest radiographs were obtained using conventional radiography (26 patients) or computed radiography (three patients) in the anteroposterior projection performed at bedside. HRCT was performed on a HiSpeed Advantage scanner (General Electric Medical Systems, Milwaukee, WI) (26 patients), an Asteion Multi scanner (Toshiba, Tokyo, Japan) (two patients), and a Sensation 16-detector CT scanner (Siemens, Erlangen, Germany) (one patient). The scans were obtained at end inspiration using 1-mm collimation at 10-mm intervals through the chest (27 patients), 2-mm collimation at 10-mm intervals (one patient), and 1-mm collimation helical CT through the chest (one patient). The images were obtained on lung (window width, 1,000–1,500 H; level, –700 H) and mediastinal (window width, 350 H; level, 35–40 H) settings.
Two experienced radiologists reviewed the radiographs obtained within the same day as the HRCT scans and, subsequently, the CT scans, independently and in random order, and reached a decision by consensus. The radiographs and HRCT scans were assessed for the presence and distribution of abnormalities.
The radiographs and HRCT scans were assessed for the presence of ground-glass opacities, consolidation, nodular opacities, septal lines, and reticular opacities and for the presence of associated hilar, mediastinal, or pleural abnormalities. Ground-glass opacities were defined as hazy areas of increased opacity or attenuation without obscuration of the underlying vessels. Consolidation was defined as homogeneous opacification of the parenchyma with obscuration of the underlying vessels. Nodular opacities were defined as focal round opacities. Reticular opacities were defined as linear opacities forming a meshlike pattern. The predominant patterns of abnormality on HRCT were classified into consolidation, ground-glass opacities, reticular opacities, or mixed. Ground-glass opacities were further subclassified into ground-glass opacities on their own or those associated with smooth interlobular septal thickening; smooth intralobular lines; and irregular lines associated with irregular interfaces, architectural distortion, or traction bronchiectasis. A mixed pattern denoted a combination of ground-glass opacities, consolidation, and reticulation.
The distribution was categorized as focal, patchy, and diffuse. Focal was defined as a single focus of abnormality, patchy as more than one focus, and diffuse if bilateral and involving the equivalent of the volume of one or both lungs. Predominant distribution was also assessed as being in the upper, middle, or lower lung zones, in random, central, or peripheral (outer third of the lungs) location.
The site of involvement on chest radiographs was defined as predominantly in the upper (above the level of the anterior end of the second rib), middle (between the second and fourth anterior ribs), and lower (below the level of the anterior end of the fourth rib) lung zones.
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None of the 12 patients had nodular opacities, hilar or mediastinal lymphadenopathy, or pleural effusion evident on HRCT. Eight of the 12 patients who underwent HRCT at presentation had chest radiographs interpreted prospectively and retrospectively as normal (Fig. 1A, 1B, 1C, 1D), three had ground-glass opacities, and one had focal consolidation visible on the radiograph. Follow-up radiographs, available in seven of these eight patients, showed development of unilateral or bilateral ground-glass opacities or consolidation within 24–48 hr after hospital admission.
Follow-up HRCT scans were available in 25 patients and were obtained 2–27 days (median, 9 days) after hospital admission. All follow-up HRCT scans were abnormal. The predominant abnormalities consisted of unilateral (n = 2) or bilateral (n = 13) ground-glass opacities or unilateral (n = 2) or bilateral (n = 5) consolidation and a mixed pattern (n = 3) (Fig. 2A, 2B). Fourteen of the 15 patients with predominant ground-glass opacities had associated findings, including smooth thickening of the interlobular septa (n = 6), smooth thickening of the interlobular septa and smooth intralobular lines (n = 3), or a combination of irregular lines and mild traction bronchiectasis (n = 5) (Figs. 3A, 3B and 4A, 4B, 4C). Three patients had a mixed pattern comprising coarse parenchymal bands; ground-glass opacities; reticulation; broad, bandlike areas of consolidation; and traction bronchiectasis.
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The abnormalities were bilateral in 23 of the 25 patients, had a predominately subpleural distribution in 15 patients, had a random distribution in two, had peribronchial distribution in one, and were diffuse in the remaining seven patients. Other findings seen on follow-up HRCT included pneumothorax (n = 2), pneumomediastinum (n = 3), and small pleural effusions (n = 2) (Fig. 5). None of the patients had nodular opacities or hilar or mediastinal lymphadenopathy evident on follow-up HRCT.
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The findings of chest radiographs obtained concurrent with the follow-up HRCT scans in 25 patients were all abnormal. The predominant abnormalities on follow-up radiographs consisted of single or multiple areas of consolidation (n = 23), unilateral ground-glass opacities (n = 1), or a combination of focal consolidation and bilateral reticular opacities (n = 1). The abnormalities involved mainly the upper and midlung zones in four patients, the middle and lower lung zones in 11 patients, the lower lung zones in seven, and all zones to a similar extent in three patients. The extent of abnormalities on the radiographs obtained after hospital admission in all 25 patients was greater than that at presentation.
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Müller et al. [11] reviewed the radiographic findings at presentation in 12 patients with SARS. The most common radiographic finding was unilateral or bilateral ground-glass opacities or focal unilateral or bilateral areas of consolidation. One patient had a normal radiograph. Helical CT or HRCT scans were obtained in five patients. CT scans in all patients were abnormal, including the one in the patient with a normal radiograph. The CT findings consisted of bilateral ground-glass opacities, focal areas of consolidation, or both. HRCT findings at presentation in one of the patients from Vancouver and four from Hong Kong in our study were part of the study by Müller et al.
Wong et al. [9] reviewed the HRCT findings at presentation in 73 patients exposed to or with SARS. The study included three groups of patients: group 1, patients with symptoms of SARS and abnormal radiograph (n = 23); group 2, patients with a high clinical suspicion of SARS and a normal radiograph (n = 17); and group 3, patients with minor symptoms and normal radiograph (n = 34). The 34 patients in the latter group were ultimately considered not to have SARS. HRCT scans were abnormal only in the first two groups of patients. The most common findings on HRCT in these patients were ground-glass attenuation, sometimes with associated areas of consolidation and interlobular septal and intralobular interstitial thickening. Affected segments were predominantly in the lower lobes (91/149 affected segments). Most patients in group 1 (14/23) had mixed central and peripheral lesions. In group 2, however, peripheral lesions were more common (10/17). In both groups, a purely central distribution was uncommon (one of 23 in group 1 and two of 17 in group 2).
The HRCT findings at presentation in our patients were similar to those described by Wong et al. [9]. The main abnormalities consisted of unilateral or bilateral consolidation and bilateral ground-glass opacities. Septal thickening and smooth intralobular lines were seen in some patients. Eight of our patients with SARS had normal radiographs and abnormal HRCT scans at presentation. Follow-up radiographs available in seven of these patients showed development of unilateral or bilateral ground-glass opacities or consolidation within 24–48 hr after hospital admission.
The unilateral and bilateral areas of consolidation in patients with SARS are similar to those seen in a variety of bacterial, fungal, and viral pneumonias [12]. The findings in patients with SARS in our study differ, however, from those described in other viral pneumonias by the absence of centrilobular nodular opacities. Centrilobular nodules and branching centrilobular opacities resulting in a tree-in-bud pattern are commonly seen in patients with various forms of infectious bronchiolitis and in patients with bacterial, viral, and mycoplasma pneumonia [12–14]. Reittner et al. [12] reviewed the HRCT findings in 114 patients with different types of pneumonia. In that study, seven (78%) of nine patients with viral pneumonia had centrilobular nodules. Septal thickening was seen at presentation in three patients (33%) with viral pneumonia in the study by Reittner et al. and in three (25%) of 12 patients with SARS in our study.
Most patients with SARS show progression of disease after hospital admission. Follow-up radiographs in seven patients with initially normal radiographs in our study showed that these patients developed unilateral or bilateral ground-glass opacities or consolidation within 24–48 hr after hospital admission. Wong et al. [15] reviewed the radiographic appearances at presentation and the pattern of progression in 138 patients with SARS. They observed predominant peripheral distribution of abnormalities and common progression pattern from unilateral focal air-space opacity to unilateral multifocal or bilateral involvement during treatment. Ninety-seven (70%) of 138 patients showed initial radiographic deterioration to peak level followed by radiographic improvement, 24 patients (17%) showed fluctuating radiographic changes, 10 patients (7%) had static radiographic appearance, and seven (5%) had progressive radiographic deterioration [15].
The predominant findings on follow-up HRCT in our study consisted of bilateral ground-glass opacities and unilateral or bilateral consolidation. Superimposed septal lines and reticulation were seen in the scans of some patients. A mixed pattern was also noted in the second week after admission in some patients who had a combination of ground-glass opacities, bandlike areas of consolidation, and reticular opacities. Eight patients developed a reticular pattern with associated irregular interfaces and mild traction bronchiectasis superimposed on ground-glass opacities. These findings suggest fibrosis [16]. However, further follow-up in these patients will be required to determine whether these changes are reversible. Five (20%) of 25 patients developed superimposed complications, including pneumomediastinum, pneumothorax, and small pleural effusions.
SARS is highly infectious. Proper infection-control measures must be taken to minimize the risk of cross-infection to other patients and personnel [17, 18]. Whenever possible, these patients should be assessed outside the main radiology department. Radiography in these patients is routinely performed using a portable technique at bedside. However, in most centers, CT scanners are available only in the main radiology department. Therefore, although HRCT can be helpful in the assessment of patients with SARS, we believe that its use should be limited to patients with high clinical suspicion of SARS and normal or only questionable abnormalities on radiography and to patients with suspected complications.
Our study has several limitations. It is retrospective and includes a small number of cases. Almost all the patients in the study required hospitalization. Therefore, the analysis is biased toward patients with severe SARS who required further evaluation because of poor response to therapy or development of complications such as pneumomediastinum and pneumothorax.
We conclude that the most common HRCT manifestations of SARS are unilateral or bilateral ground-glass opacities or focal unilateral or bilateral areas of consolidation. HRCT may show parenchymal disease, predominantly ground-glass opacification, in patients with normal radiographs. In hospitalized patients, the abnormalities tend to progress to more extensive ground-glass opacities and bilateral consolidation. A small percentage of patients may develop superimposed complications such as pneumothorax and pneumomediastinum or show reticulation and traction bronchiectasis consistent with fibrosis.
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