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Thin-Section CT of Severe Acute Respiratory Syndrome: Evaluation of 73 Patients Exposed to or with the Disease¹

¹ From the Departments of Diagnostic Radiology and Organ Imaging (K.T.W., G.E.A., E.H.Y.Y., A.T.A.), Medicine and Therapeutics (D.S.C.H., N.L., A.W., C.B.L., J.J.Y.S.), Accident and Emergency Medicine (T.H.R., P.C.), and Surgery (S.S.C.C.), Prince of Wales Hospital, Chinese University of Hong Kong, 30-32 Ngan Shing St, Shatin, Hong Kong SAR. Received April 7, 2003; revision requested April 14; revision received April 16; accepted April 17. Address correspondence to K.T.W. (e-mail: wongkatakjeffrey@hotmail.com).

	ABSTRACT

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PURPOSE: To retrospectively analyze the thin-section computed tomographic (CT) features in patients with severe acute respiratory syndrome (SARS) at the authors’ institution.

MATERIALS AND METHODS: From March 11, 2003, to April 2, 2003, 74 patients with symptoms and signs suggestive of SARS underwent CT of the thorax; all underwent thin-section CT except for one patient who underwent conventional CT. Group 1 (n = 23) patients had symptoms of SARS in keeping with criteria from the Centers for Disease Control and Prevention and a positive chest radiograph. Group 2 (n = 17) patients had a high clinical suspicion of SARS but a normal radiograph. Group 3 (n = 34) patients had minor symptoms and a normal chest radiograph. The thin-section CT images were analyzed for ground-glass opacification or consolidation, lesion size in each lung segment, peripheral or central location, interstitial thickening, and other abnormalities.

RESULTS: Thin-section CT scans were abnormal only for patients in groups 1 and 2. The patient with only conventional CT scans was in group 3; scans for group 3 patients were normal. Affected segments were predominantly in the lower lobes (91 of 149 affected segments). Common findings included ground-glass opacification, sometimes with consolidation, and interlobular septal and intralobular interstitial thickening. The size of each lesion and the total number of segments involved were smaller in group 2 patients. A majority of patients in group 1 (14 of 23) had mixed central and peripheral lesions. In group 2, however, peripheral lesions were more common (10 of 17). In both groups, a purely central lesion was uncommon (one of 23 in group 1 and two of 17 in group 2).

CONCLUSION: Common thin-section CT features of SARS are ground-glass opacification and lower lobe and peripheral distribution.

© RSNA, 2003

Index terms: Lung, CT, 69.12118 • Pneumonia, acute interstitial, 69.21 • Severe acute respiratory syndrome

	INTRODUCTION

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Editor’s Note: Although 25 patients included in this report were also included in a report published online by the New England Journal of Medicine (www.nejm.org; April 7, 2003), the analysis of the specific thin-section computed tomographic findings for these 25 patients and for all others included in the Radiology report has been performed in much greater detail. —Anthony V. Proto, MD, Editor

In mid-March 2003, there was an outbreak of atypical pneumonia in one of the wards at our institution in Hong Kong, China. The disease initially affected mainly medical personnel, thus raising alarm that this might be an unusual form of infection. Within 1 week, the number of infected individuals soared and included inpatients and patient relatives, in addition to medical personnel. Cases were beginning to appear in other countries in the region, Europe, North America, and Australia. By the end of the 2nd week, quarantine measures and international travel were substantially altered due to the rapidly rising number of cases. This infection was termed severe acute respiratory syndrome (SARS) and is of unknown etiology, although a coronavirus has been implicated (1). Clinically, the syndrome is defined by the Centers for Disease Control and Prevention (CDC) by three criteria (2): (a) a high fever of more than 38°C and (b) one or more clinical findings of respiratory illness (eg, cough, shortness of breath, difficulty breathing, hypoxia, or radiographic findings of either pneumonia or acute respiratory distress syndrome) and (c) travel within 10 days of onset of symptoms to an area with documented or suspected community transmission of SARS, or close contact within 10 days of onset of symptoms with either a person with a respiratory illness who traveled to a SARS area or a person known to be a suspect SARS case (close contact is defined as having cared for, having lived with, or having had direct contact with respiratory secretions and/or body fluids of a patient suspected of having SARS).

Since there is no single test that can be used to diagnose the condition with a reasonable degree of accuracy and reliability, the diagnosis must be based on clinical appearance in combination with imaging features. Chest radiography is one of the major diagnostic components according to World Health Organization and CDC guidelines (3,4). The purpose of our study was to analyze retrospectively the thin-section computed tomographic (CT) features in patients with SARS at our institution.

	MATERIALS AND METHODS

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Patients and CT Imaging
Our institutional review board approved this retrospective study; informed consent was not required.

From March 11, 2003, to April 2, 2003, 74 patients underwent CT scanning (Highspeed Advantage; GE Medical Systems, Milwaukee, Wis) of the thorax. The average age of the 22 male and 52 female patients was 34.7 years (range, 2–82 years). Initially, because we were faced with an unknown disease affecting mainly medical personnel working in the same ward, the first 50 patients underwent both conventional CT of the entire thorax (7-mm section thickness, pitch of 1.5, 120 kV, 180 mA) and thin-section CT of the thorax to better evaluate the lungs (1-mm section thickness with 6-mm gap, supine position, scanning during inspiration, 1 second per scan, 120 kV, 140 mA). On the basis of our findings in these first 50 patients, we performed only thin-section CT in subsequent patients. In one patient (a 2-year-old boy), only conventional CT was performed because the boy was unable to hold his breath.

The patients were sorted into three groups. Group 1 (n = 23) included patients who had symptoms and signs consistent with what is now defined as SARS and abnormalities on their chest radiographs consistent with pneumonia or acute respiratory distress syndrome. Because SARS is a new entity and thus we had no previous literature to refer to for guidance, we performed CT in these patients—despite their positive chest radiographs—to look for any additional findings. CT was performed an average of 3.3 days (range, same day to 13 days) after admission in this group. Group 2 (n = 17) included patients in whom there was a strong suspicion of SARS but who had a normal chest radiograph. All had a history of contact with a person without a respiratory illness who traveled to a SARS area or a person known to be a suspect SARS case, high fever (higher than 38°C), respiratory symptom(s), and leukopenia. CT was performed an average of 0.8 days (range, same day to 5 days) after admission in this group. Group 3 (n = 34) included medical personnel or patients who had minor symptoms such as cough or low-grade fever, a normal chest radiograph, and a low suspicion for SARS. They underwent CT because they had a history of contact with other personnel or patients with a diagnosis of SARS. CT was performed an average of 1.4 days (range, same day to 6 days) after admission in this group.

Review of CT Images
All CT images were reviewed by three radiologists (A.T.A., K.T.W., G.E.A.) using a viewing console. Decisions were reached by consensus. Each segment of the lung was reviewed for opacification, and the lesion size was described as small (diameter, <1 cm), medium (diameter, 1 to <3 cm), large (diameter, 3 cm to <50% of the segment), or segmental (50%–100% of the segment). The location of the lesion was defined as peripheral if it was in the outer one-third of the lung; otherwise, it was defined as central.

Ground-glass opacification was defined as increased lung parenchymal attenuation that did not obscure the underlying vascular architecture (5). Consolidation was defined as opacification in which the underlying vasculature was obscured (5). Each lesion was magnified and examined for intralobular, interlobular septal, or peri-bronchovascular interstitial thickening. Attention was also paid to the presence of nodules or masses, cavitation or calcification, bronchiolar or bronchial dilatation, and emphysema. Any other abnormalities seen were noted.

Follow-up Chest Radiography in Group 2
Follow-up chest radiographs, obtained daily in the patients in group 2 (all of whom had normal initial radiographs), were reviewed by three radiologists (K.T.W., E.H.Y.Y., G.E.A.). Decisions were reached by consensus. The radiographs were reviewed separately from the CT scans and were evaluated for development of areas of opacification.

	RESULTS

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The 40 patients in groups 1 and 2 (all of whom underwent thin-section CT) consisted of 13 male and 27 female patients. Their ages ranged from 2 to 82 years of age with a mean of 37.2 years (mean of 39.6 years for patients in group 1 and 33.9 years for patients in group 2). The patients in groups 1 and 2 were considered to have SARS or were strongly suspected of having SARS on the basis of CDC criteria. The 34 patients in group 3 were ultimately considered not to have SARS, since they did not fulfill the CDC criteria. The CT scans in these patients were normal, including the scans in one patient who underwent only conventional CT and the 33 patients who underwent thin-section CT.

Sites Involved and Frequency
Although all segments of the lung can be involved, affected segments were predominantly in the lower lobes (91 of 149 affected segments, 61.1%) (Table 1, Fig 1). The number of patients with lower lobe involvement (30 of 40 patients) was also greater than the number with involvement in other lobes (14 of 40 had upper lobe involvement) (Table 2). Patients in group 2 had a higher percentage of lower lobe involvement than did those in group 1.

View larger version (110K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Transverse thin-section CT scan of lower lobes shows involvement in multiple segments. Lesions show opacification, are of various sizes, and are distributed in a peripheral manner.

Size of Lesions
There was a difference between the sizes of the lesions in group 1 and those in group 2 (Table 3). A higher proportion of large lesions (>3 cm) was seen in group 1 (68 of 115, 59%) compared with group 2 (eight of 34, 24%).

View larger version (166K): [in this window] [in a new window] [Download PPT slide]   Figure 2. Transverse thin-section CT scan shows ground-glass opacification of lesion. Underlying vascular architecture (arrowhead) is clearly visible. The bronchi are dilated.

View larger version (158K): [in this window] [in a new window] [Download PPT slide]   Figure 3. Transverse thin-section CT scan shows mixed ground-glass opacification and consolidation. Air bronchogram (arrow) is present in the center of the consolidation.

View larger version (135K): [in this window] [in a new window] [Download PPT slide]   Figure 4. Transverse thin-section CT scan shows ground-glass opacification and thickened interlobular septa (arrow) and intralobular interstitium (crazy-paving pattern).

Two patients had apical fibrosis and a calcified nodule, findings that are suggestive of old tuberculosis infection. One patient (a 76-year-old man) had bilateral pleural effusions and cardiomegaly, which are suggestive of congestive cardiac failure. One patient (an 82-year-old woman) had enlarged lymph nodes, which appeared matted, and another patient (a 60-year-old woman) had a 1.8-cm irregular nodule in the left upper lobe and a 4-mm nodule in the right upper lobe. These two patients will undergo further evaluation.

Follow-up Chest Radiography in Group 2
Follow-up chest radiography of patients in group 2 showed abnormalities (areas of opacification) in 12 patients (71%) and normal findings in the other five (29%). The radiographic abnormalities developed an average of 2.0 days (range, same day to 5 days) after CT. The five patients with no subsequent radiographic abnormalities were followed up for an average of 3.4 days (range, 2–6 days) after CT.

	DISCUSSION

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SARS is a newly described infection of unknown etiology. A coronavirus has been implicated as the causative agent (4). Our initial experience has shown some frequent findings at thin-section CT. In terms of distribution, the lower lobes are preferentially affected (average of 5.0 segments for group 1 and 2.0 for group 2), especially in the early stages (assuming the group 2 patients to be in an earlier stage of infection than the group 1 patients). The patients with more advanced cases show more bilateral involvement (61% in group 1). The lesions tend to be peripheral and smaller (76% were smaller than 3 cm in group 2) in the less severely affected lungs, also suggesting that we are scanning patients with an earlier stage of the disease. In patients with more advanced cases, there is involvement of the central, perihilar regions by larger (>3 cm) lesions. The majority of the lesions contained an area of ground-glass opacification with or without consolidation. Other findings include intralobular thickening, interlobular septal thickening, a crazy-paving pattern, and bronchiectasis. None of the CT features of this syndrome were themselves specific or diagnostic. The crazy-paving pattern, once thought to be characteristic of alveolar proteinosis, has been shown to occur in many other diseases, such as usual interstitial pneumonia, infection, pulmonary edema, adult respiratory distress syndrome, bronchiolitis obliterans organizing pneumonia (BOOP), and hemorrhage and as a result of irradiation (6). Some of these diagnoses could be excluded by correlating the clinical history with the distribution of opacification. Thus, our differential diagnosis in terms of CT findings included other causes of atypical pneumonia, BOOP, chronic eosinophilic pneumonia, and acute extrinsic allergic alveolitis.

Atypical pneumonia is frequently caused by Mycoplasma species, influenza virus, or Chlamydia species. Tanaka et al (7) described a central pattern of ground-glass opacification and consolidation in these types of atypical pneumonia. This appearance may then progress to centrilobular, acinar shadows and air-space consolidation with a lobular distribution. We have not found these to be major features of SARS in our series.

Bronchiolitis obliterans is an inflammatory disease of the bronchioles and alveolar ducts that results in destruction of the airways and scarring. This condition combined with an organizing pneumonia is termed BOOP. The CT findings of BOOP are well recognized (8–10) and are similar to those of SARS. These similarities include the lower lobe and peripheral distribution, a mixture of ground-glass opacification and consolidation, interstitial or septal thickening, and bronchiectasis. Nodules were not present in the patients with SARS in our series but are relatively common (31.6%) in patients with BOOP (11). Patients with BOOP also demonstrate lymphadenopathy (13%) (12) and pleural effusion (20%) (12), of which we saw only one case each in our patients with SARS.

Chronic eosinophilic pneumonia shares many of the features of BOOP and thus SARS. In a recent thin-section CT study of BOOP and chronic eosinophilic pneumonia (11), both diseases showed a high prevalence of consolidation (86.8% and 74.4%, respectively) aside from ground-glass opacification. In a report by Jederlinic et al (13), chronic eosinophilic pneumonia has been shown to have middle and upper zone predominance, which is different from the lower zone predominance in SARS.

Acute allergic extrinsic alveolitis is an abnormal immunologic reaction to inhaled allergens, which produces an alveolar inflammation, ground-glass opacification, and consolidation. However, its distribution is predominantly in the middle zone (sparing the lower lobes), and centrilobular nodules may be present (14).

During this outbreak of SARS, our initial 50 patients underwent both conventional CT (7-mm section thickness, pitch of 1.5) and thin-section CT (1-mm section thickness, 6-mm gap). Both examinations were performed because we were faced with an unknown disease and we wanted to rule out other findings such as lymphadenopathy and pleural effusion. Because we did not observe these findings in the initial 50 patients, we changed the protocol to include only thin-section CT of the thorax.

In retrospect, the 34 patients in group 3, who had minor symptoms and a normal chest radiograph, would not have been scanned if we strictly adhered to the definition subsequently released by the CDC. These patients—some of whom were inpatients but most of whom were medical personnel and all of whom had a history of contact with a person without a respiratory illness who traveled to a SARS area or a person known to be a suspect SARS case—were scanned at a time when we were faced with an unknown disease and were experiencing a high level of anxiety. Although we now consider CT unnecessary for such patients, these CT findings did help us as we began learning about this disease.

Our current imaging protocol is the following: (a) Patients with symptoms and signs consistent with SARS and with abnormalities on chest radiographs are followed up with serial radiography. CT scanning is not required for diagnosis. (b) Patients with symptoms and signs consistent with SARS and with a normal chest radiograph undergo thin-section CT to confirm the diagnosis. They subsequently undergo serial radiography for follow-up. (c) Patients with minor symptoms and signs that do not match the definition of SARS do not undergo thin-section CT.

There are limitations to our study. First, on the basis of the number of patients studied, the full range of disease distribution and appearance may not have been demonstrated. Second, we have no proof, histologic or biochemical, that the patients had been infected with the same causative agent. At this writing, the causative agent has not been definitively isolated and a definitive test has not yet been developed for diagnosis.

In summary, the CT features of SARS are predominantly ground-glass opacification, lower lobe predominance, and peripheral distribution.

	FOOTNOTES

 
See also the other article by Wong et al in this issue.

Abbreviations: BOOP = bronchiolitis obliterans organizing pneumonia, CDC = Centers for Disease Control and Prevention, SARS = severe acute respiratory syndrome

Author contributions: Guarantor of integrity of entire study, A.T.A.; study concepts, A.T.A., K.T.W., G.E.A.; study design, K.T.W., G.E.A., D.S.C.H., P.C., S.S.C.C.; literature research, K.T.W., G.E.A.; clinical studies, D.S.C.H., N.L., A.W., C.B.L., T.H.R., P.C., S.S.C.C., J.J.Y.S.; data acquisition, A.T.A., K.T.W., G.E.A., N.L., E.H.Y.Y., A.W., T.H.R., C.B.L.; data analysis/interpretation, G.E.A., A.T.A., K.T.W.; statistical analysis, G.E.A., K.T.W.; manuscript preparation and definition of intellectual content, G.E.A., A.T.A., K.T.W.; manuscript editing, A.T.A., K.T.W., J.J.Y.S., S.S.C.C.; manuscript revision/review and final version approval, A.T.A., K.T.W., G.E.A.

	REFERENCES

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3. World Health Organization. Preliminary clinical description of severe acute respiratory syndrome. Available at: www.who.int/csr/sars/clinical/en/ 2003. Accessed March 21.
4. Centers for Disease Control and Prevention. Diagnosis/evaluation for SARS. Available at: www.cdc.gov/ncidod/sars/diagnosis.htm 2003. Accessed April 7.
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