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Severe Acute Respiratory Syndrome: Spectrum of High-Resolution CT Findings and Temporal Progression of the Disease

¹ Department of Diagnostic Radiology and Organ Imaging, United Christian Hospital, 130 Hip Wo St., Kwun Tong, Hong Kong.
² Department of Medicine, Respiratory Division, United Christian Hospital, Kwun Tong, Hong Kong.

Received May 27, 2003; accepted after revision July 2, 2003.

 
Address correspondence to J. Y. H. Hui (jhuiyh{at}yahoo.com.hk).

Introduction

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Severe acute respiratory syndrome (SARS) is an emerging infection that is caused by a novel coronavirus [1–3]. Since its first outbreak in the Guandong province in southern China in November 2002, until now, 8,046 people have been infected [4]. The global case number is still growing every day. In Hong Kong, more than 1,722 individuals have been infected, with 193 patients admitted to our hospital as a result of an outbreak in a high-rise housing development.

The radiology department plays a pivotal role in the diagnosis and management of SARS [5, 6]. Although chest radiography remains the most commonly used imaging modality in the investigation and treatment of patients with SARS, subtle changes such as ground-glass opacities, which are readily identifiable on high-resolution CT, are easily overlooked [7, 8]. Previous reports on SARS are mainly limited to findings on chest radiographs [9–11]. High-resolution CT helps to provide a more objective and better understanding of the pathogenesis of the disease by allowing a cross-sectional study of the pulmonary parenchymal abnormalities induced by the virus. Moreover, the natural history of SARS can be shown on serial examinations. Histologic examination of the pulmonary parenchyma obtained through transbronchial, video-assisted thoracoscopic or open-lung biopsies in patients with SARS is limited because of the high risk of infection associated with these procedures. The major advantage of high-resolution CT over histologic examination is its ability to assess the entire lung rather than relying on a small biopsy specimen. We report the radiologic manifestation of the disease with special emphasis on the high-resolution CT findings and its temporal progression.

Subjects and Methods

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The patients reported in this article were those with SARS Coronavirus pneumonia confirmed microbiologically by reverse transcriptase polymerase chain reaction or serology [2]. Under our current investigation protocol, chest radiography remains the primary imaging modality for patients with suspected SARS. If the chest radiograph reveals changes compatible with pneumonia, further imaging is not required for diagnosis, and treatment is immediately instituted. Serial chest radiographs are obtained to monitor treatment progress. In contrast to the recommendation of the Centers for Disease Control and Prevention on diagnosis and evaluation of patients with suspected SARS [12], in our hospital a patient with negative findings on chest radiography will be subjected to high-resolution CT and if the findings are negative, SARS is less likely and the patient would be kept under observation. Follow-up high-resolution CT would be performed if there is a discrepancy between the clinical and radiographic findings or suspicion of any reversible complications that may contribute to respiratory compromise.

All scans were obtained with a helical CT scanner (HiSpeed Advantage, General Electric Medical Systems, Milwaukee, WI). One-millimeter-thick transverse sections were obtained from the lung apices through the bases at 10-mm increments with the patients in the supine position during suspended inspiration. Because the coronavirus is highly contagious, in order to achieve better infection control, high-resolution CT was not performed on patients who were undergoing intubation in the intensive care unit. Moreover, to decrease the contamination of our CT suite, expiratory high-resolution CT scans, which are useful in the evaluation of obstructive components in interstitial lung diseases, were also omitted. Images were reconstructed using a high-spatial-frequency algorithm. The CT images were reviewed in cine formats at a computer workstation (CT Advantage workstation 3.1, General Electric Medical Systems) (Microsoft, Redmond, WA). Patients who underwent serial high-resolution CT and those who were confirmed to have SARS due to coronavirus by positive findings of a nasopharyngeal aspirate, stool, or urine reverse transcriptase polymerase chain reaction or serologic testing [2] constitute our study population. The clinical and radiologic data were analyzed.

Clinical and Radiologic Manifestations

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According to our present knowledge of SARS, the disease can be divided into two stages [7, 13–15].

Viral Replicative Phase
During the first week of the illness, most patients with SARS experienced flulike symptoms, with fever being the most consistent one on presentation. Early diagnosis at this stage is important so that contact tracing and proper infection control measures can be implemented. Treatment with an antiviral agent, such as ribavirin and a protease inhibitor (treatment effectiveness not established yet), can be given immediately, to decrease the viral load.

Rapid diagnostic tests for SARS, including reverse transcriptase polymerase chain reaction and serologic testing, are still in the developmental phase and cannot be used to exclude SARS and are not useful for screening. The use of high-resolution CT compensates for these deficiencies and can facilitate an early diagnosis of SARS by revealing pneumonic changes that can be hidden on a chest radiograph with normal findings [15]. Although patients with SARS can have completely normal findings on high-resolution CT on presentation, most patients have abnormal findings on high-resolution CT that appear as relatively well-defined areas of ground-glass opacity (Fig. 1A, 1B, 1C, 1D) or consolidation (Fig. 2A, 2B, 2C, 2D). The lesions may involve a single lobe, one lung (Fig. 3A, 3B, 3C, 3D, 3E, 3F), or both lungs (Fig. 4A, 4B). The lower lobes and the peripheral lungs are more commonly involved [8, 10, 11, 16–18].

View larger version (151K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A. —42-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, and myalgia. High-resolution CT scan obtained on day 3 from onset of symptoms shows well-defined lobular ground-glass opacity (arrow) in subpleural area of anteromedial basal segment of lower lobe. She developed fever and diarrhea on day 8.

View larger version (135K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B. —42-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, and myalgia. High-resolution CT scan obtained on day 12 shows that original lesion has resolved (arrow). Patchy ill-defined areas of peribronchial and subpleural consolidations are found in adjacent lung (not shown). Bronchial wall thickening (arrowheads) is also observed.

View larger version (104K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C. —42-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, and myalgia. High-resolution CT scans obtained on day 15 show ill-defined nodular areas of ground-glass opacities in upper lobes (arrows) and consolidations in lower lobes.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1D. —42-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, and myalgia. Progressive resolution of parenchymal changes is seen in follow-up high-resolution CT scans obtained on day 19 showing residual parenchymal bands that may represent atelectasis or scarring. Patient was discharged on day 33.

View larger version (149K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A. —36-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented early on day 1 with fever, malaise, and diarrhea. High-resolution CT scan obtained on same day shows small consolidation in anterobasal segment of right lower lobe (arrow).

View larger version (143K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B. —36-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented early on day 1 with fever, malaise, and diarrhea. Repeated high-resolution CT scan obtained on day 2 shows that lesion has enlarged slightly (arrow). Patient's symptoms improved in first week, but she developed fever again on day 10.

View larger version (151K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C. —36-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented early on day 1 with fever, malaise, and diarrhea. High-resolution CT scan obtained on day 13 shows that original lesion has resolved (arrow). Pleural-based consolidation and air bronchograms are observed in adjacent pulmonary parenchyma. Changes were confined to right lower lobe throughout course of her illness. Remains of the lungs are clear.

View larger version (131K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2D. —36-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented early on day 1 with fever, malaise, and diarrhea. Parenchyma bands (arrows) are seen in subpleural area of right lower lobe on day 21. Follow-up high-resolution CT scan (not shown) obtained on day 27 showed completely normal findings. The patient was discharged on day 31.

View larger version (150K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A. —30-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever and throat discomfort. High-resolution CT scan obtained on day 3 from onset of symptoms shows small lobular consolidations (arrow) in anterior segment of right upper lobe.

View larger version (136K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B. —30-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever and throat discomfort. High-resolution CT scan obtained on same day as A at different level shows another consolidation (arrow) in posterobasal segment of right lower lobe. She developed fever again on day 11 with progressively worsening chest radiography findings (not shown).

View larger version (157K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C. —30-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever and throat discomfort. High-resolution CT scan obtained on day 12 shows consolidation in right lower lobe in predominantly peribronchial distribution. Ground-glass opacification and thickening of interlobular septa and intralobular interstitium (arrow) are seen anteriorly. Small pleural effusion is also observed. Patient's condition deteriorated, with arterial oxygen saturation of 96% in room air.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3D. —30-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever and throat discomfort. High-resolution CT scans obtained on day 15 show patchy ground-glass changes and consolidations involving both lungs.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3E. —30-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever and throat discomfort. Small pneumomediastinum is shown on high-resolution CT scan in prevertebral (arrow), retrosternal, and paratracheal spaces on day 20. Patient's condition improved gradually, and she was sent home on day 27.

View larger version (101K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3F. —30-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever and throat discomfort. Follow-up high-resolution CT scans obtained on day 31 reveal minimal subtle ground-glass opacities (arrows).

View larger version (97K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4A. —36-year-old man with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, rigors, myalgia, and cough. High-resolution CT scans obtained on day 4 from onset of symptoms show multiple nodular ground-glass opacities in both lungs distributed peripherally. He developed recurrent fever, diarrhea, and shortness of breath on day 7.

View larger version (107K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4B. —36-year-old man with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, rigors, myalgia, and cough. Follow-up high-resolution CT scans obtained on day 34 show ground-glass changes, consolidations in peribronchial distribution in both lungs, and extensive pneumomediastinum and subcutaneous emphysema. Patient's condition was stabilized, but he was still in hospital at time of writing (day 71).

Immunopathologic Damage
Although some patients may recover spontaneously from the first stage of the disease, to our knowledge the actual percentage of these patients is not known at present. As the disease progresses into the second week, most patients develop fever again, with cough and shortness of breath. Symptoms are usually much more severe and the patient's condition may deteriorate rapidly. A shifting pattern of air-space consolidation has been shown on serial chest radiographs [14], and there is an overall worsening of the radiologic picture coupled with clinical deterioration. Resolution of the original lesion on serial high-resolution CT followed by the appearance of new lesions in the adjacent lungs [14] may be seen (Fig. 5A, 5B). In contrast to the well-defined lesions in the viral replicative phase, these new lesions are more ill defined (Fig. 6A, 6B, 6C) but still appear to involve the lower lobes and posterior lungs preferentially [10, 11, 16]. The changes are most intense in the initially involved lobe, whereas the lung that was not involved in the first phase is also affected, although often to a lesser extent. Sometimes a clear gradient (involvement of the upper lobes to a lesser extent than the lower lobes due to differential blood flows to different parts of the lungs) (Fig. 7A, 7B, 7C) can be observed if a follow-up scan is performed at the correct moment. A clinical picture compatible with acute interstitial pneumonia or acute respiratory distress syndrome caused by coronavirus with different disease severity is therefore produced. Patients with clinically less severe lung damage are considered to have acute lung injury, whereas the ones with more severe hypoxemia are considered to have acute respiratory distress syndrome.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5A. —23-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, rigors, myalgia, and sore throat. Her fever subsided on day 3. High-resolution CT scan obtained on day 4 from onset of symptoms shows ground-glass opacity with superimposed reticular pattern producing crazy paving appearance (arrow) in anterior segment of left upper lobe.

View larger version (119K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5B. —23-year-old woman with severe acute respiratory syndrome coronavirus pneumonia who presented with fever, chills, rigors, myalgia, and sore throat. Her fever subsided on day 3. Follow-up high-resolution CT scan obtained on day 12 shows that previously seen lesion (not shown) has resolved. Subtle ill-defined ground-glass changes are seen involving entire left upper lobe. Patient was discharged on day 25.

View larger version (142K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6A. —32-year-old man with severe acute respiratory syndrome coronavirus pneumonia who is also hepatitis B carrier. He presented with fever and myalgia. Chest radiograph with apparently normal findings was obtained on admission (day 5 from onset of symptoms). High-resolution CT scan obtained on day 5 shows consolidation in posterobasal segment of left lower lobe with air bronchograms. His condition was stable during first week, but he developed fever and desaturation on day 9 and was admitted to intensive care unit for close monitoring.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6B. —32-year-old man with severe acute respiratory syndrome coronavirus pneumonia who is also hepatitis B carrier. He presented with fever and myalgia. Chest radiograph with apparently normal findings was obtained on admission (day 5 from onset of symptoms). Follow-up high-resolution CT scans obtained on day 21 show extensive ground-glass opacities and consolidations in both lungs. Air-space consolidations with air bronchograms (solid arrow) are seen predominantly in posterior location in lower lungs and areas of ground-glass attenuation are found anteriorly in upper lungs. Extensive pneumomediastinum with trapping of air along bronchovascular sheath (open arrow) is noted. There is also small right pleural effusion (arrowhead). He was recieving intubation on day 24 but ventilation was successfully discontinued 4 days later.

View larger version (103K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 6C. —32-year-old man with severe acute respiratory syndrome coronavirus pneumonia who is also hepatitis B carrier. He presented with fever and myalgia. Chest radiograph with apparently normal findings was obtained on admission (day 5 from onset of symptoms). High-resolution CT scans obtained on day 45 show progressive resolution of pneumomediastinum, ground-glass changes, and consolidations. Ground-glass opacities in centrilobular distribution (arrows) are seen in upper lobes. Intralobular honeycombing and bronchiolectasis with septal lines (arrowheads) are found in lung bases. Patient was discharged on day 52.

View larger version (147K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7A. —31-year-old woman with severe acute respiratory syndrome coronavirus pneumonia. She presented with fever, myalgia, cough, and malaise. On admission (day 3), posteroanterior chest radiograph shows air-space opacity in right lower zone. Initial high-resolution CT was not performed. Patient's fever subsided soon after admission, but she developed recurrent fever with shortness of breath on day 11.

View larger version (106K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7B. —31-year-old woman with severe acute respiratory syndrome coronavirus pneumonia. She presented with fever, myalgia, cough, and malaise. High-resolution CT scans obtained on day 21 show extensive consolidations and ground-glass opacities that are denser in dependent, posterior lung zone with relative sparing of anterior and upper lung fields. Thickened interlobular septa and intralobular interstitium are also seen. Patient was admitted to intensive care unit on day 26 because of persistent desaturation despite 100% oxygen therapy.

View larger version (97K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 7C. —31-year-old woman with severe acute respiratory syndrome coronavirus pneumonia. She presented with fever, myalgia, cough, and malaise. Follow-up high-resolution CT scans obtained on day 31 reveal extensive pneumomediastinum with secondary subcutaneous emphysema and left pneumothorax. Chest drain (arrow) has been inserted into left pleural cavity. There is partial resolution of ground-glass changes and consolidations. Patient's condition further deteriorated on day 32 with development of large right pneumothorax. Patient was intubated but died on day 55 as result of uncontrolled sepsis and respiratory failure.

Patients who began with having a larger lesion or multifocal or bilateral lung involvement in the early phase were associated with more severe disease and a more prolonged course of the illness (Fig. 8A, 8B, 8C). Multifocal ground-glass opacities and consolidations are the predominant high-resolution CT changes detected in the second stage in patients with SARS. Although these changes are nonspecific, they are in fact the most common radiologic pattern occurring in patients with bronchiolitis obliterans with organizing pneumonia [19, 20] and acute respiratory distress syndrome as a result of diffuse alveolar damage [21–25]. The rapid clinical improvement and resolution of the radiologic changes in some of our patients treated with steroids (Figs. 1A, 1B, 1C, 1D and 2A, 2B, 2C, 2D) are consistent with the hypothesis that bronchiolitis obliterans with organizing pneumonia–like changes were responsible for the radiologic pattern [17]. Moreover, patients with the organizing pneumonia type of acute respiratory distress syndrome were found to respond relatively favorably to steroid treatment, as judged from results of serial arterial blood gas analyses and radiography [26].

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8A. —47-year-old man with severe acute respiratory syndrome coronavirus pneumonia. He was admitted on day 4 with fever, chills, rigors, and myalgia. Posteroanterior chest radiograph shows air-space opacifications (arrows) in right middle and lower zones. Initial high-resolution CT was not performed. Patient developed fever again with shortness of breath on day 8 and had been admitted to intensive care unit on day 11 for close monitoring because of persistent desaturation.

View larger version (108K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8B. —47-year-old man with severe acute respiratory syndrome coronavirus pneumonia. He was admitted on day 4 with fever, chills, rigors, and myalgia. High-resolution CT scans obtained on day 23 show patchy ground-glass opacities in upper lobes and consolidations in upper and lower lobes. There is extensive pneumomediastinum.

View larger version (109K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 8C. —47-year-old man with severe acute respiratory syndrome coronavirus pneumonia. He was admitted on day 4 with fever, chills, rigors, and myalgia. Follow-up high-resolution CT scans obtained on day 51 show persistent pneumomediastinum. Partial resolution of ground-glass opacities and consolidations is observed. Traction bronchiectasis (arrows) is seen in subsegmental airways. Intralobular honeycombing and bronchiolectasis with septal lines are found in both lung bases. Note small right pleural effusion. Patient's condition improved gradually, and he was discharged on day 56.

After the acute phase of the immunopathologic damage, some patients have a relatively uncomplicated course with rapid resolution of the symptoms, especially with steroid therapy. Radiologically, there is a progressive decrease in the extent of ground-glass opacity and consolidation. A substantial proportion (12%) of these patients developed spontaneous pneumomediastinum [14] unrelated to the use of positive end-expiratory pressure ventilation. This occurred most commonly as the ground-glass opacities and consolidations began to resolve and is probably the result of peribronchiolar abscess formation leading to interstitial pulmonary emphysema, which tracks back along vessels and bronchi to the mediastinum. Subcutaneous emphysema and pneumothorax may develop as a result of the pneumomediastinum.

A few patients may progress to fibrosis with persistent ground-glass opacities, bronchiectasis, bronchiolectasis, honeycombing, and architectural distortion (Fig. 9A, 9B). About 20% of patients with persistent desaturation refractory to oxygen therapy require ventilatory support [14]. The whole clinical picture may be further complicated by infections, such as hospital-acquired pneumonias, which are common during a stay in the intensive care unit, making a definite radiologic diagnosis in these patients difficult.

View larger version (122K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 9A. —34-year-old man with severe acute respiratory syndrome coronavirus pneumonia. He presented with fever, cough, and malaise. Posteroanterior chest radiograph on admission (day 3 from onset of symptoms) shows air-space opacification (arrow) in left middle zone. Initial high-resolution CT was therefore not performed. Patient developed high fever and desaturation on day 7 and was admitted to intensive care unit.

View larger version (113K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 9B. —34-year-old man with severe acute respiratory syndrome coronavirus pneumonia. He presented with fever, cough, and malaise. High-resolution CT scans obtained on day 20 show diffuse ground-glass attenuation and consolidations (arrows) associated with traction bronchiectasis and bronchiolectasis. Honeycomb changes (arrowheads) are found in subpleural area of left and right lower lobes posteriorly. Architectural distortion is observed from displacement of bronchi and pulling back of major fissures. There is no pneumomediastinum. Patient also had cardiomegaly with pulmonary arterial hypertension. Pulmonary trunk measured 33.6 mm in diameter. Follow-up high-resolution CT scans obtained on days 28 and 32 (not shown) did not show much change in extent of disease. He was intubated on day 42 because of respiratory failure and died on day 56 because of uncontrolled sepsis.

The major limitation of our report is that, because of the highly contagious nature of this virus and the desire to avoid cross infection, high-resolution CT was not performed on those patients who were undergoing intubation in the intensive care unit; therefore, the full spectrum of the disease may not be appreciated. Autopsy in patients with SARS shows diffuse alveolar damage in varying phases of organization [3, 11, 27]. However, it is likely that those patients admitted to the intensive care unit will have a more severe form of ground-glass opacities or consolidations, manifesting as multifocal lesions or bilateral lung involvement.

Conclusion

Top Introduction Subjects and Methods Clinical and Radiologic... Conclusion References

 
SARS is an emerging infection that is highly contagious. The disease can be divided into two stages. During the initial viral replicative phase, most patients will have abnormal findings on high-resolution CT that appear as relatively well-defined areas of ground-glass opacity or consolidation located mainly in the lower lobes and peripheral lungs. The immunopathologic stage is more prolonged and varied, depending on the host response. This is reflected by a spectrum of ground-glass changes and consolidations with varying disease severity resembling bronchiolitis obliterans organizing pneumonia and acute respiratory distress syndrome.

References

Top Introduction Subjects and Methods Clinical and Radiologic... Conclusion References

 

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