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Severe Acute Respiratory Syndrome: Radiographic and CT Findings

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 Special Administrative Region, Republic of China.

Received April 28, 2003; accepted after revision April 30, 2003.

Address correspondence to N. L. Müller (nmuller{at}vanhosp.bc.ca).

Abstract

OBJECTIVE. We review the radiographic and CT findings in the lungs of 12 patients with severe acute respiratory syndrome (SARS) in an effort to describe the most common radiologic findings for this disease.

CONCLUSION. The most common radiographic findings of SARS patients at presentation are unilateral or bilateral ground-glass opacities or focal unilateral or bilateral areas of consolidation. In hospitalized SARS patients, the abnormalities tend to progress to bilateral air-space consolidation. CT may reveal parenchymal disease in patients whose radiographs show normal results.

Severe acute respiratory syndrome (SARS) is an atypical pneumonia first reported in southern China in November 2002 that has spread rapidly to many countries throughout the world [1]. As of April 24, 2003, 26 countries had reported a cumulative total of 4439 cases of SARS, 263 of which had resulted in death [2]. The overwhelming majority of cases have occurred in China and in the Hong Kong Special Administrative Region. A new pathogen—a member of the Coronavirus family that has not been previously seen in humans—has been identified in patients with SARS [3]. Genetic characterization of the virus has shown it to be only distantly related to previously known coronaviruses [4].

The clinical manifestations typically consist of fever exceeding 100.4°F (> 38°C), nonproductive cough, and progressive dyspnea [5]. Most SARS patients have lymphopenia and elevated levels of serum liver transaminases [6, 7]. Preliminary reports indicate that the radiographic manifestations include focal and patchy interstitial opacities, ground-glass opacities, and unilateral and bilateral areas of consolidation [6, 8, 9]. In this article, we review the radiographic and CT findings in 12 patients with SARS.

Subjects and Methods

The study included all four patients with a clinical diagnosis of SARS in Vancouver, BC, Canada, and eight patients from Hong Kong. The patients included six men and six women ranging in age from 24 to 82 years (median age, 44 years). All 12 patients fulfilled the clinical criteria for diagnosis of SARS established by the United States Centers for Disease Control and Prevention [5] (Appendix 1). All patients had temperatures exceeding 100.4°F (> 38°C) and one or more clinical symptoms of respiratory illness (cough, shortness of breath, difficulty breathing, or hypoxia), and all had lived in an area in which community transmission of SARS has been documented (n = 8), had traveled to such an area (n = 3), or had come into close contact with a person known to have SARS (n = 1). All 12 patients had lymphopenia (absolute lymphocyte count, < 1.0 x 10³/L). Eleven of the 12 patients had elevated levels of serum liver transaminases (aspartate aminotransferase and alanine aminotransferase).

Initial chest radiographs were obtained using conventional radiography (n = 9), computed radiography (n = 2), or digital radiography (n = 1). Ten patients had only anteroposterior-projection radiographs that had been obtained bedside, and two patients had posteroanterior- and lateral-projection radiographs. Follow-up radiographs obtained within 24 hr of hospital admission were available for 10 patients.

CT scans were available for five patients. In four patients, CT scans had been obtained at admission, and in one patient, within 24 hr after admission. Because the CT scans were obtained in different institutions, the types of scanners and protocols used varied. In four patients, CT scans were obtained using 1.0- to 1.5-mm collimation at 10-mm intervals through the chest; the scans were reconstructed with an edge-enhancing algorithm (high-resolution CT). In one patient, the scans were obtained using 5-mm collimation and a multidetector CT (MDCT) scanner.

Two experienced radiologists reviewed the radiographs and CT scans independently and reached a decision on the final interpretations by consensus. The radiographic and CT findings were classified as consisting of ground-glass opacities, consolidation, a reticular pattern, or nodular opacities. Ground-glass opacities were defined as hazy areas of increased opacity or attenuation with the view of the underlying vessels unobscured. Consolidation was defined as homogeneous opacification of the parenchyma with the underlying vessels obscured. Nodular opacities were defined as focal round opacities.

Results

The predominant radiographic findings in the patients at presentation were unilateral or bilateral ground-glass opacities (n = 5) (Figs. 1A, 1B and 2A, 2B), focal unilateral or bilateral areas of consolidation (n = 5) (Fig. 3), and diffuse small nodular opacities (n = 1) (Figs. 4A, 4B, 4C). In one patient, the findings of the chest radiograph obtained at admission were normal. Radiographs showed that two patients with consolidation also had ground-glass opacities, and one patient whose radiograph showed predominantly ground-glass opacities also had poorly defined small nodular opacities visible on the radiograph. The remaining patients only had one pattern of abnormality identified on the radiograph. Of the seven patients with findings of ground-glass opacities, three had extensive and fairly symmetric bilateral opacities, one had bilateral and asymmetric opacities, two had unilateral opacities, and one had opacities only in the lower lobes of both lungs. The areas of consolidation involved mainly the upper lung zones in two patients, the lower zones in two patients, and the middle lung zones in one patient.

View larger version (129K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —29-year-old woman with severe acute respiratory syndrome. Chest radiograph obtained at hospital admission shows ill-defined hazy increased density (i.e., ground-glass opacity) in right middle lung zone.

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —29-year-old woman with severe acute respiratory syndrome. Chest radiograph obtained 24 hr after A shows dense focal consolidation.

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —24-year-old woman with severe acute respiratory syndrome. Chest radiograph obtained at hospital admission shows faint patchy ground-glass opacities in lower lobes.

View larger version (130K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —24-year-old woman with severe acute respiratory syndrome. Chest radiograph obtained 24 hr after A reveals bilateral patchy areas of consolidation.

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3. —Chest radiograph obtained in 44-year-old woman with severe acute respiratory syndrome reveals patchy bilateral areas of consolidation.

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —64-year-old man with severe acute respiratory syndrome. Chest radiograph obtained at admission with patient supine reveals diffuse small nodular opacities throughout both lungs. Patient was immediately intubated for assisted ventilation.

View larger version (161K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —64-year-old man with severe acute respiratory syndrome. Repeated radiograph (B) and magnified radiographic image (C) of right lower lobe show nodular opacities more clearly than does A.

View larger version (139K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4C. —64-year-old man with severe acute respiratory syndrome. Repeated radiograph (B) and magnified radiographic image (C) of right lower lobe show nodular opacities more clearly than does A.

In the one patient whose chest radiograph showed normal findings, high-resolution CT showed patchy bilateral areas of ground-glass attenuation and focal consolidation in the superior segment of the left lower lobe (Figs. 5A, 5B). Three of the patients who underwent high-resolution or MDCT of the chest had bilateral ground-glass opacities identified on their radiographs; the radiograph of one of these patients had prospectively been interpreted as showing normal findings. In all three patients, CT revealed extensive bilateral areas of ground-glass attenuation (Figs. 6A, 6B, 6C); two patients also had foci of consolidation. The areas of consolidation were found mainly in the posterior regions of the lungs. In two of these patients, sharp demarcation between the areas of involved and uninvolved parenchyma (geographic pattern) was seen on CT scans (Figs. 6A, 6B, 6C). One of the patients who underwent high-resolution CT had focal consolidation in the right lower lobe visible on the admission radiograph. CT revealed focal consolidation and surrounding ground-glass attenuation in the right lower lobe.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —27-year-old man with severe acute respiratory syndrome. Chest radiograph acquired at hospital admission shows no obvious abnormality.

View larger version (72K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —27-year-old man with severe acute respiratory syndrome. High-resolution CT scan obtained on same day as A shows focal area of consolidation in superior segment of left lower lobe with adjacent ground-glass opacification. Subpleural ground-glass opacification is also present in contralateral lung.

View larger version (123K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6A. —48-year-old man with severe acute respiratory syndrome. Chest radiograph obtained 12 hr after hospital admission shows subtle bilateral ground-glass opacities, with relative sparing of left upper lobe. Radiographic findings were similar to those seen on radiograph obtained just before hospital admission.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6B. —48-year-old man with severe acute respiratory syndrome. High-resolution CT scans obtained at level of distal trachea (B) and bronchus intermedius (C) on same day as chest radiograph reveals extensive bilateral ground-glass opacities. Sharp demarcation between normal and abnormal parenchyma is visible.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6C. —48-year-old man with severe acute respiratory syndrome. High-resolution CT scans obtained at level of distal trachea (B) and bronchus intermedius (C) on same day as chest radiograph reveals extensive bilateral ground-glass opacities. Sharp demarcation between normal and abnormal parenchyma is visible.

Eight of the 10 patients who were hospitalized and had follow-up chest radiographs obtained within 24 hr of presentation showed progression of the disease. In all these patients, follow-up radiographs showed extensive unilateral (n = 2) or bilateral areas of consolidation (n = 6) regardless of the pattern seen on the initial radiograph (Figs. 1A, 1B, 2A, 2B, and 7A, 7B). One patient who had extensive ground-glass opacities at presentation and the patient who had diffuse small nodular opacities at presentation showed no change in the radiographic findings on a follow-up radiograph obtained the day after hospital admission.

View larger version (117K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7A. —64-year-old woman with severe acute respiratory syndrome. Chest radiograph obtained at admission shows area of consolidation in right perihilar region and ground-glass opacities in right middle and lower lung zones.

View larger version (110K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7B. —64-year-old woman with severe acute respiratory syndrome. Chest radiograph obtained 1 day after A reveals extensive consolidation in right lung and focal consolidation in left lung.

One of the 12 patients had small bilateral pleural effusions that were only evident on high-resolution CT. None had evidence of hilar or mediastinal lymph node enlargement at admission or on radiography or CT performed within 24 hr of admission.

Discussion

SARS usually begins with a prodrome of fever (> 100.4°F [> 38.0°C]), often associated with chills and rigors [8]. Other symptoms include headache, malaise, and myalgia. After 3–7 days, a lower respiratory phase of the disease begins with the onset of a dry, nonproductive cough or dyspnea that may progress to hypoxemia [8]. A preliminary report from the United States Centers for Disease Control and Prevention [8] emphasized that the findings on chest radiographs may be normal during the febrile prodrome and throughout the course of illness. However, the report stated that in a substantial proportion of patients, the respiratory phase is characterized by "focal interstitial infiltrates progressing to more generalized, patchy, interstitial infiltrates." Areas of consolidation were described as being present in the late stages of SARS [8].

Lee et al. [6] reviewed the clinical, laboratory, and radiologic features of 138 patients in whom SARS was suspected during an outbreak in a hospital in Hong Kong. The most common symptoms included fever (in 100% of patients); chills, rigors, or both (73%); myalgia (61%); cough (57%); and headache (56%). Thirty-two patients (23%) were admitted to the intensive care unit; five patients died. At the onset of fever, 108 (78%) of the 138 patients had abnormal chest radiographs, all of which were interpreted as showing air-space consolidation. The consolidation was unilateral and focal in 59 (55%) and was unilateral and multifocal or bilateral in 49 (45%) of the 108 patients. The authors noted a predominantly peripheral distribution of the consolidation and the absence of associated cavitation, pleural effusion, or hilar lymphadenopathy [6].

Poutanen et al. [7] collected epidemiologic, clinical, and diagnostic data from the first 10 cases of SARS identified in Canada. The most common presenting symptoms were fever and nonproductive cough (in 100% of patients), dyspnea (80%), and malaise (70%). The authors reported that all patients had abnormal findings on radiographs but did not provide a detailed description of the radiologic findings.

Our findings suggest that the most common initial radiographic and CT manifestation of SARS is the presence of hazy areas of increased density (ground-glass opacities) that do not obscure the underlying vessel margins. Ground-glass opacities are a nonspecific finding that can be seen in patients with interstitial lung disease or mild air-space disease, or both [10, 11]. We also found that CT may show parenchymal abnormalities in patients with apparently normal radiographs and may confirm the presence of abnormalities in patients with subtle or questionable radiographic findings. In hospitalized patients, the abnormalities tend to progress to bilateral air-space consolidation.

The autopsy findings reported for two patients who died of SARS during the outbreak of the disease in a Hong Kong hospital were diffuse alveolar damage and a scanty amount of lymphocytic inflammatory interstitial infiltrate [6]. The histologic features varied by lung region and included the early phase and the organizing phase of alveolar damage. The early phase was characterized by pulmonary edema with hyaline membrane formation and the organizing phase, by cellular fibromyxoid organizing air-space exudates [6]. These findings are identical to those of acute respiratory distress syndrome. The radiographic and CT findings of bilateral ground-glass opacification or consolidation and the rapid progression seen in some of our patients are consistent with acute respiratory distress syndrome. The focal or multifocal areas of consolidation seen on images obtained in most of our patients the day after hospital admission and images obtained in most reported patients with SARS are indistinguishable from those obtained in patients with other viral or bacterial bronchopneumonias [6].

Our study has several limitations: It is retrospective and includes only a small number of cases. Almost all of the patients in our study required hospitalization. Therefore, our analysis is biased toward patients with severe SARS. Because most of these patients were quite ill, the radiographs were all obtained in anteroposterior projections at the bedside.

We conclude that the most common radiographic manifestations of SARS are unilateral or bilateral ground-glass opacities or focal unilateral or bilateral areas of consolidation. In hospitalized patients, the abnormalities tend to progress to bilateral air-space consolidation. CT may reveal parenchymal disease in patients whose radiographs appear to be normal. Because SARS is highly contagious, use of CT should be limited to patients with high clinical suspicion of the disease and normal findings or only questionable abnormalities on radiography.

Acknowledgments

We thank H. S. Lam, Kwong Wah Hospital, Hong Kong, China; Peter Cooperberg, St. Paul's Hospital, Vancouver, BC, Canada; and Will Siu, Royal Columbian Hospital, Vancouver, BC, Canada.

Radiographic and CT Findings in SARS Patients

References

1. World Health Organization. Acute respiratory syndrome in China: update 3—disease outbreak reported. Available at: www.who.int/csr/don/2003_2_20/en/. Accessed February 20, 2003
2. World Health Organization. Severe acute respiratory syndrome (SARS): update 38—multi-country outbreak. Available at: www.who.int/csr/don/2003_04_24a/en/. Accessed April 24, 2003
3. World Health Organization. Unprecedented collaboration pinpoints new Coronavirus as cause of SARS. Available at: www.who.int/en/. Accessed April 23, 2003
4. Drosten C, Günther S, Preiser W, et al. Identification of a novel Coronavirus in patients with severe acute respiratory syndrome. (preprint electronic publication) N Engl J Med Web site. Available at: content.nejm.org/cgi/reprint/NEJMoa030781v3. Accessed April 16, 2003
5. United States Centers for Disease Control and Prevention. Updated interim U. S. case definition of severe acute respiratory syndrome (SARS). Available at: www.cdc.gov/ncidod/sars/casedefinition.htm. Accessed April 20, 2003
6. Lee N, Hui D, Wu A, et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. (preprint electronic publication) N Engl J Med Web site. Available at: content.nejm.org/cgi/reprint/NEJMoa030685v2. Accessed April 14, 2003
7. Poutanen SM, Low DE, Henry B, et al. Identification of severe acute respiratory syndrome in Canada. (preprint electronic publication) N Engl J Med web site. Available at: content.nejm.org/cgi/reprint/NEJMoa030685v2. Accessed April 10, 2003
8. United States Centers for Disease Control and Prevention. Preliminary clinical description of severe acute respiratory syndrome. Available at: www.cdc.gov/mmwr/preview/mmwrhtml/mm5212a5.htm. Accessed March 21, 2003
9. Nicolaou S, Al-Nakshabandi NA, Müller NL. SARS: imaging of severe acute respiratory syndrome. AJR2003; 180:1247 –1249[Free Full Text]
10. Remy-Jardin M, Remy J, Giraud F, et al. Computed tomography assessment of ground-glass opacity: semiology and significance. J Thorac Imag 1993;8:249 –264[Medline]
11. Leung AN, Miller RR, Müller NL. Parenchymal opacification in chronic infiltrative lung diseases: CT—pathologic correlation. Radiology1993; 188:209 –214[Abstract/Free Full Text]

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