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Imaging of Severe Acute Respiratory Syndrome in Hong Kong

¹ Department of Diagnostic Radiology and Organ Imaging, Prince of Wales Hospital, Chinese University of Hong Kong, 30-32 Ngan Shing St., Shatin, Hong Kong Special Administrative Region, Republic of China.
² Department of Medicine and Therapeutics, Prince of Wales Hospital, Chinese University of Hong Kong, Shatin, Hong Kong Special Administrative Region, Republic of China.
³ Department of Surgery, Prince of Wales Hospital, Chinese University of Hong Kong, Shatin, Hong Kong Special Administrative Region, Republic of China.

Received April 25, 2003; accepted after revision April 30, 2003.

Address correspondence to G. E. Antonio (gregantonio{at}cuhk.edu.hk).

An epidemic of severe acute respiratory syndrome (SARS) began in mid March 2003 in Hong Kong, China. This epidemic soon spread throughout the territory and to the rest of the world. By the end of April 2003, 26 countries and 4288 patients have been affected, and new cases are being reported daily [1]. At our institution, we have, at the time of this writing, treated over 300 SARS patients and obtained in excess of 3000 chest radiographs and over 100 CT scans of the thorax. We present the radiographic and CT appearances of SARS in Hong Kong. The imaging appearances of SARS may be different in other settings or regions. We hope this review adds to the collective knowledge of this disease.

SARS is characterized by high infectivity and severe morbidity [2], both of which have resulted in quarantine measures and significant changes in international travel. This infection is defined by the United States Centers for Disease Control and Prevention (CDC) [3] using the following three criteria: measured temperature greater than 100.4°F (38°C); one or more clinical findings of respiratory illness (e.g., cough, shortness of breath, difficulty breathing, or hypoxia); and travel within 10 days of onset of symptoms to an area with documented or suspected community transmission of SARS or close contact with a person suspected of having SARS within 10 days of onset of symptoms.

A Coronavirus has been implicated as the causative agent. However, as yet, no rapid laboratory test is available that has a high degree of accuracy. Abnormal findings on chest radiography have been used as part of the case definition [3] and considered an important component of clinical management by the World Health Organization and the CDC.

Radiographic Findings

At presentation, most patients (78.3%) [2, 4] have air-space opacification on chest radiographs [5]. For patients who have normal findings on chest radiography at presentation, the follow-up findings become abnormal after an average of 3 days. The periphery and lower zones of the lung are preferentially affected [2, 4]. Relevant negative findings on radiography are the lack of cavitation, calcification, a reticular or nodular pattern of opacification, lymphadenopathy, or pleural effusion [5].

Progressive radiographs may follow one of four patterns [5]. In type 1, the radiographic appearance deteriorates for a week followed by improvement (in 70.3% of patients) (Figs. 1A, 1B, 1C, 1D). In type 2, the appearance fluctuates with at least one intervening period of significant improvement followed by deterioration and later recovery (in 17.4% of patients) (Figs. 2A, 2B, 2C, 2D, 2E). In type 3, the appearance remains relatively static for 10 days followed by improvement (7.2%). Type 4 involves progressive deterioration leading to death [5] (Figs. 3A, 3B, 3C, 3D).

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —Type 1 progression shown on serial chest radiographs of 38-year-old woman with 2-day history of fever and chills. Frontal chest radiograph obtained at presentation shows ill-defined air-space opacity in periphery of right lower zone.

View larger version (158K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —Type 1 progression shown on serial chest radiographs of 38-year-old woman with 2-day history of fever and chills. Frontal chest radiograph obtained on day 2 shows increase in extent of pulmonary opacity in right lower zone.

View larger version (124K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —Type 1 progression shown on serial chest radiographs of 38-year-old woman with 2-day history of fever and chills. Frontal chest radiograph obtained on day 7 shows further radiographic progression with additional ill-defined air-space opacity in left lower zone.

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —Type 1 progression shown on serial chest radiographs of 38-year-old woman with 2-day history of fever and chills. Frontal chest radiograph obtained on day 12 shows resolution of pulmonary opacities in both lower zones.

View larger version (133K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —Type 2 progression shown on serial chest radiographs of 37-year-old man with 1-day history of high fever and cough. Frontal chest radiograph obtained at presentation shows subtle increased opacity in periphery of right lower zone.

View larger version (139K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —Type 2 progression shown on serial chest radiographs of 37-year-old man with 1-day history of high fever and cough. Frontal chest radiograph obtained on day 3 shows confluent air-space opacity in periphery of right lower zone that is more obvious than on previous radiograph (A).

View larger version (140K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —Type 2 progression shown on serial chest radiographs of 37-year-old man with 1-day history of high fever and cough. Frontal chest radiograph obtained on day 5 shows worsening of airspace opacities in right lower zone and involvement of left lower zone.

View larger version (151K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D. —Type 2 progression shown on serial chest radiographs of 37-year-old man with 1-day history of high fever and cough. Frontal chest radiograph obtained on day 12 shows resolution of bilateral lower zone pulmonary opacities.

View larger version (136K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2E. —Type 2 progression shown on serial chest radiographs of 37-year-old man with 1-day history of high fever and cough. Frontal chest radiograph obtained on day 16 shows reappearance of multifocal ill-defined air-space opacities in mid and lower zones of both lungs. Subsequent follow-up radiograph obtained at discharge (not shown) revealed resolution of pulmonary opacities.

View larger version (132K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —Type 4 progression shown on serial chest radiographs of 83-year-old woman with 3-day history of fever, chills, and rigor. Frontal chest radiograph obtained at presentation shows area of ill-defined air-space opacity in right middle lobe obscuring part of right heart border.

View larger version (135K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —Type 4 progression shown on serial chest radiographs of 83-year-old woman with 3-day history of fever, chills, and rigor. Frontal chest radiograph obtained on day 2 shows increased area of pulmonary opacities in right lower zone. Subtle air-space opacities appear in perihilar regions of both upper zones.

View larger version (115K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —Type 4 progression shown on serial chest radiographs of 83-year-old woman with 3-day history of fever, chills, and rigor. Frontal chest radiograph obtained on day 5 shows progressive patchy areas of pulmonary opacities in both lungs.

View larger version (130K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3D. —Type 4 progression shown on serial chest radiographs of 83-year-old woman with 3-day history of fever, chills, and rigor. Frontal chest radiograph obtained on day 10 shows further radiographic progression with adult respiratory distress syndrome—type of confluent opacification. Patient died 1 day after last radiograph.

For most patients (74.6%) [2, 4, 5], deterioration shown on radiography takes the form of multifocal unilateral or bilateral opacification. In the patients who are most affected by SARS, confluent consolidation is seen, a picture compatible with adult respiratory distress syndrome, which is associated with a grave prognosis. The postmortem examinations at our institution [2] have shown diffuse alveolar damage with some areas of pulmonary edema and hyaline membrane formation reminiscent of adult respiratory distress syndrome and some areas of the organizing phase of alveolar damage.

The radiographic findings of SARS are indistinguishable from other causes of atypical pneumonia such as Mycoplasma and Chlamydia organisms and viral species [6].

CT Findings

In view of the absence of lymphadenopathy or pleural abnormalities, we perform only high-resolution CT (1-mm thickness, 6-mm gap) at our institution. High-resolution CT is also performed only on patients with signs and symptoms fitting the CDC criteria for SARS but with normal findings on chest radiography.

Our initial experience [7] has shown that early in the disease, the lower lobes of the lungs are preferentially affected. In the more severely affected patients, lesions extend to the upper lobes or become bilateral or both. Lesions usually begin in the periphery of the lungs but may progress to incorporate the central or perihilar regions.

The lesions are either areas of ground-glass opacification (Figs. 4A, 4B) or consolidation [2, 4, 8] (Fig. 5) or a mixture of both (Fig. 6). In the areas of ground-glass opacification, thickening of the intralobular interstitium (Fig. 7) or interlobular septa may be present [7]. If marked septal thickening occurs, a crazy paving appearance results (Fig. 8A). Cavitation, calcification, a reticular or nodular pattern of opacification, lymphadenopathy, or pleural effusion are not features of this disease. None of the findings on high-resolution CT are specific, including the crazy paving pattern that is seen in almost all diseases affecting the lungs [9]. However, coupled with the clinical findings, the list of differentials is reduced to atypical pneumonia, acute extrinsic allergic alveolitis, bronchiolitis obliterans with organizing pneumonia, and chronic eosinophilic pneumonia.

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —High-resolution CT scans show ground-glass opacification in two patients. CT scan of 33-year-old man shows large area of ground-glass opacification. Note that underlying pulmonary vasculature (arrow) is not obscured.

View larger version (98K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —High-resolution CT scans show ground-glass opacification in two patients. CT scan of 51-year-old woman shows multiple small areas of ground-glass opacification.

View larger version (125K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5. —High-resolution CT scan of 52-year-old woman shows consolidation. Vascular architecture is obscured and air bronchograms are seen.

View larger version (199K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6. —High-resolution CT scan of 61-year-old man shows mixed ground-glass and consolidated opacification. Air bronchogram (arrow) runs through center of consolidation (vascular architecture obscured). Note ground-glass opacification present at edges of consolidation.

View larger version (159K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7. —High-resolution CT scan of 56-year-old man shows thickened interlobular septa and intralobular interstitium superimposed on ground-glass opacification.

View larger version (144K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8A. —High-resolution CT scans and radiograph of 27-year-old woman with strong clinical suspicion of severe acute respiratory syndrome. CT scan shows crazy paving pattern (arrow) with markedly thickened interlobular septa superimposed on ground-glass opacification.

We also have found on follow-up radiographs that abnormalities seen on high-resolution CT scans may precede those on the radiographs by 2 days [7]. In patients who are strongly suspected of having SARS but have normal findings on chest radiography, the lesions seen on high-resolution CT tend to be paraspinal—hidden by the cardiac or mediastinal structures or located in the posterior costophrenic angle. The CT findings are also a blind spot for frontal radiographs (Figs. 8B and 8C).

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8B. —High-resolution CT scans and radiograph of 27-year-old woman with strong clinical suspicion of severe acute respiratory syndrome. Chest radiograph shows no obvious abnormality.

View larger version (101K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8C. —High-resolution CT scans and radiograph of 27-year-old woman with strong clinical suspicion of severe acute respiratory syndrome. CT scan obtained within 24 hr of initial CT scan shows left paraspinal opacity in left upper lobe posterior segment behind aortic arch.

Conclusion

Imaging helps to confirm or rule out lung involvement, making it an important triage tool and a monitor for the progression of an epidemic such as SARS. However, the radiographic and CT appearances of SARS are nonspecific, and clinical information is indispensable in helping to determine the diagnosis.

Our current imaging protocol is as follows: Patients who have symptoms and signs consistent with SARS and abnormalities found on chest radiographs are followed-up with serial radiography. No CT scan is required for diagnosis. Next, patients who have symptoms and signs consistent with SARS and normal findings on chest radiography undergo high-resolution CT to confirm this diagnosis and subsequently undergo serial radiography for follow-up. Finally, patients who have minor symptoms and signs that do not fulfill the definition of SARS do not undergo high-resolution CT.

References

1. World Health Organization Web site. Cumulative number of reported probable cases of severe acute respiratory syndrome (SARS). Available at: www.who.int/csr/sarscountry/2003_04_23/en/. Accessed November 1, 2002–April 23, 2003
2. Lee N, Hui D, Wu A, et al. A major outbreak of severe acute respiratory syndrome in Hong Kong. N Engl J Med Web site. Available at: http://content.nejm.org/cgi/reprint/NEJMoa030685v2.pdf. Accessed April 7, 2003
3. Centers for Disease Control and Prevention Web site. 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
4. Tsang KW, Ho PL, Ooi GC, et al. A cluster of cases of severe acute respiratory syndrome in Hong Kong. N Engl J Med Web site. Available at: http://content.nejm.org/cgi/reprint/NEJMoa030666v2.pdf. Accessed March 31, 2003
5. Wong KT, Antonio GE, Hui DSC, et al. Radiographic appearances and pattern of progression of severe acute respiratory syndrome (SARS): a study of 138 patients. Radiology (in press)
6. Kim EA, Lee KS, Primack SL, et al. Viral pneumonias in adults: radiologic and pathologic findings. RadioGraphics2002; 22[suppl]:137S –149S
7. Wong KT, Antonio GE, Hui DSC, et al. Thin-section CT of severe acute respiratory syndrome: evaluation of 73 patients exposed to or with the disease. Radiology 2003 (in press)
8. Wong KT, Antonio GE, Hui DSC, et al. Radiological appearances of severe acute respiratory syndrome. J Hong Kong Coll Radiologists 2003;6:4 –6
9. Johkoh T, Itoh H, Müller NL, et al. Crazy-paving appearance at thin-section CT: spectrum of disease and pathologic findings. Radiology 1999;211 : 155–160[Abstract/Free Full Text]

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