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Published online before print May 20, 2003, 10.1148/radiol.2282030593

(Radiology 2003;228:401.)

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© RSNA, 2003

Thoracic Imaging

Severe Acute Respiratory Syndrome: Radiographic Appearances and Pattern of Progression in 138 Patients1

K. T. Wong, FRCR, Gregory E. Antonio, FRANZCR, David S. C. Hui, MD, Nelson Lee, MD, Edmund H. Y. Yuen, FRCR, Alan Wu, MD, C. B. Leung, MD, T. H. Rainer, MD, Peter Cameron, MD, Sydney S. C. Chung, MD, Joseph J. Y. Sung, MD and Anil T. Ahuja, FRCR

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 15, 2003; revision requested April 17; revision received April 22; accepted April 29. Address correspondence to K.T.W. (e-mail: wongkatakjeffrey@hotmail.com).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
PURPOSE: To retrospectively evaluate the radiographic appearances and pattern of progression of severe acute respiratory syndrome (SARS).

MATERIALS AND METHODS: Chest radiographs obtained at clinical presentation and during treatment in 138 patients with confirmed SARS (66 men, 72 women; mean age, 39 years; age range, 20–83 years) were assessed. Radiographic appearances of pulmonary parenchymal abnormality, distribution, and extent of involvement on initial chest radiographs were documented. Recognizable patterns of radiographic progression were determined by comparing the overall mean percentage of lung involvement for each patient on serial radiographs.

RESULTS: Initial chest radiographs were abnormal in 108 of 138 (78.3%) patients and showed air-space opacity. Lower lung zone (70 of 108, 64.8%) and right lung (82 of 108, 75.9%) were more commonly involved. In most patients, peripheral lung involvement was more common (81 of 108, 75.0%). Unifocal involvement (59 of 108, 54.6%) was more common than multifocal or bilateral involvement. No cavitation, lymphadenopathy, or pleural effusion was demonstrated. Four patterns of radiographic progression were recognized: type 1 (initial radiographic deterioration to peak level followed by radiographic improvement) in 97 of 138 patients (70.3%), type 2 (fluctuating radiographic changes) in 24 patients (17.4%), type 3 (static radiographic appearance) in 10 patients (7.3%), and type 4 (progressive radiographic deterioration) in seven patients (5.1%). Initial focal air-space opacity in 44 of 59 patients (74.6%) progressed to unilateral multifocal or bilateral involvement during treatment.

CONCLUSION: Predominant peripheral location; common progression pattern from unilateral focal air-space opacity to unilateral multifocal or bilateral involvement during treatment; and lack of cavitation, lymphadenopathy, and pleural effusion are the more distinctive radiographic findings of SARS.

© RSNA, 2003

Index terms: Lung, radiography, 68.11 • Pneumonia, acute interstitial, 68.21 • Severe acute respiratory syndrome


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Editor’s Note: Although the 138 patients described 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 radiographic findings for these patients in the Radiology report has been performed in much greater detail.

—Anthony V. Proto, MD, Editor

In early March 2003, there was an outbreak of atypical pneumonia in Hong Kong. The World Health Organization (WHO) defined the illness as severe acute respiratory syndrome (SARS). At the time of writing this article, there have been 1,059 reported cases in Hong Kong and more than 2,890 cases worldwide (1), including 32 deaths in Hong Kong related to the illness.

At our institution, over 200 confirmed cases of SARS have been treated (2). Imaging plays a crucial role in diagnosis and in monitoring of disease progress during medical treatment. From our experience, the radiographic appearances of SARS at the time of initial presentation are variable, ranging from normal to widespread opacification. In addition, patients show different radiologic progression during treatment.

Because the role of imaging is central to the diagnosis and the care of the patients, radiographers and radiologists should be aware of the radiographic appearances of this disease and the infection-control guidelines to prevent transmission of the disease. The purpose of our study was to retrospectively evaluate the radiographic appearances and patterns of progression in patients with SARS.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
DISCUSSION
 REFERENCES
 
Subjects
Between March 11 and 25, 2003, 138 subjects (66 men, 72 women; mean age, 39 years; age range 20–83 years) were identified as being secondary (history of direct contact with index case at our institution) or tertiary (history of direct contact with secondary cases) cases of SARS at our institution. There were 66 men and 72 women, with a mean age of 39 years, age range of 20–83 years. Sixty-nine of the 138 were health care workers and an additional 16 were medical students who were present for clinical teaching in the index ward (Table 1). The remaining 53 were inpatients in the same medical ward or those who had visited their relatives in that ward. The diagnosis of SARS was based on WHO diagnostic criteria (3). This retrospective study was approved by our Institutional Review Board; patient informed consent was not required.


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  		TABLE 1. Profile of 138 Subjects with SARS

 
Chest Radiography and Evaluation
Frontal chest radiographs were obtained at initial clinical presentation and during treatment. The initial chest radiograph was obtained an average of 2.5 days (range, 0–10 days) after onset of fever. Only frontal chest radiographs were obtained (posteroanterior for subjects who could stand, anteroposterior for those who could not). All radiographic examinations were performed with computed radiography equipment (Mobilett Plus; Siemens, Erlangen, Germany) by using a standardized technique (75 kV, 4 mAs, 180-cm film-focus distance for posteroanterior; 70 kV, 4 mAs, 100-cm film-focus distance for anteroposterior; broad tube focus for both). The images were assessed by using a picture archiving and communication system viewer with a 2,048 x 2,048-pixel monitor (Magicview version VA22E; Siemens).

The frontal chest radiographs obtained at clinical presentation and at follow-up during treatment were retrospectively reviewed in consensus by three radiologists (K.T.W., G.E.A., H.Y.Y.) who were unaware of the clinical progress of the subjects. Each lung was divided into three zones: upper, middle, and lower. Each zone spanned one-third of the craniocaudal distance of the lung on the frontal radiograph and was evaluated separately.

The observers assessed the presence, appearances, distribution, and size of lung parenchymal abnormalities on each chest radiograph in all subjects. The appearances were categorized as follows: air-space shadow, reticular shadow, nodular shadow, or mass. The anatomic distribution was noted to be central if the abnormality predominantly involved the medial half of the zone and peripheral if it predominantly involved the lateral half. The size of the lesion was assessed by visually estimating the percentage area occupied in each zone on each side to determine the overall mean percentage of involvement by averaging the percentage involvement of the six lung zones. Associated findings, in particular the presence of cavitation, lymphadenopathy, and pleural effusion, were also assessed.

Serial frontal chest radiographs obtained during treatment were also retrospectively reviewed by the same radiologists in consensus. All subjects included in this study underwent serial follow-up chest radiography for at least 14 days (unless deceased). For each follow-up radiograph, the extent of lung parenchymal involvement was assessed by using the same method as for the radiograph obtained at initial clinical presentation. Follow-up radiographs were obtained daily during the hospital stay. All subjects were given a combination of ribavirin (Derbin BLC, United Kingdom) (an antiviral agent, administered orally; initial dose of 2.4 g followed by 1.2 g three times daily) and corticosteroid (prednisolone; Clonmel Healthcare, Ireland) (0.5–1.0 mg per kilogram of body weight per day; ) for treatment. The steroid methylprednisolone (Solu-medrol; Pharmacia Upjohn, Belgium) was administered intravenously in pulsed fashion (0.5 g for three consecutive days) to 107 subjects whose clinical condition so indicated.

Data Analysis
The radiographic patterns at the time of clinical presentation in all 138 subjects, as assessed on initial chest radiographs, were analyzed and categorized as normal or unifocal, unilateral multifocal, or bilateral multifocal abnormalities. The distribution of lung parenchymal involvement in terms of central or peripheral involvement and the zones involved were noted. We determined if there were recognizable patterns of radiographic progression by comparing the overall percentage of lung involvement for each subject on serial radiographs.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Appearances of Abnormalities at Presentation
Chest radiographs obtained at presentation were abnormal in 108 of 138 subjects (78.3%). The radiographic pattern observed in all 108 subjects was air-space opacities with ill-defined margins. None of these lesions showed a reticular or nodular pattern or a mass. There was no evidence of cavitation in the area of air-space consolidation, lymphadenopathy, or pleural effusion (except in one subject with concomitant congestive cardiac failure who had a small pleural effusion) on any chest radiograph at initial presentation. Chest radiographs obtained at presentation were normal in 30 of 138 subjects (21.7%).

Distribution of Abnormalities at Presentation
The location and appearance of lung opacities on initial radiographs are shown in Tables 2 and 3, respectively. The right lung (82 of 108 subjects, 75.9%) was involved in more subjects than the left (67 of 108, 62.0%). The disease showed a predilection for the lower zone (70 of 108, 64.8%). Involvement of peripheral lung parenchyma (81 of 108, 75.0%) (Fig 1) was more common than a mixed peripheral and central pattern (14 of 108, 13.0%) or a central pattern (13 of 108, 12.0%) at the time of presentation. Unifocal involvement (59 of 108, 54.6%) was slightly more common than multifocal involvement (49 of 108, 45.4%). Bilateral disease was present in 41 (38.0%) subjects. At presentation, the overall mean lung involvement was 4.7% (range, 0.8%–63.3%).


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  		TABLE 2. Location of Lung Opacities on Initial Radiographs in 108 Subjects

 

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  		TABLE 3. Appearance of Lung Opacities on Initial Radiographs in 108 Subjects

 


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  		Figure 1. Frontal chest radiograph in a 23-year-old man with SARS shows a focal ill-defined air-space opacity predominantly involving the periphery of right lower zone. Note lack of cavitation, lymphadenopathy, and pleural effusion.

 
Radiographic Progression
Of the 30 subjects with an initial normal chest radiograph, 29 showed evidence of air-space opacities on subsequent follow-up chest radiographs after an average of 3.1 days (range, 1–7 days). The remaining subject had normal-appearing follow-up radiographs, but signs and symptoms were strongly suggestive of SARS and the diagnosis was made with the aid of thin-section computed tomography (CT) of thorax. Thus, of the total of 138 subjects, all but one showed air-space opacity, either initially (n = 108) or subsequently (n = 29) on radiographs.

At review of follow-up radiographs, we were able to identify four patterns of radiographic progression (Table 4, Fig 2): type 1, initial radiographic deterioration to peak level, followed by radiographic improvement, with maximum difference in overall mean lung involvement greater than 25%; type 2, fluctuating radiographic changes with at least two radiographic peaks and an intervening trough, which differed by more than 25% for overall mean lung involvement; type 3, static radiographic changes with no discernible radiographic peak or change in overall mean lung involvement of less than 25% for more than 10 days; and type 4, progressive radiographic deterioration.


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  		TABLE 4. Patterns of Radiographic Progression of SARS in 138 Subjects

 


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  		Figure 2. Schematic depicts the four patterns of radiographic progression determined from serial chest radiographs. See Table 4 for time to peak(s).

 
The type 1 pattern was the most commonly observed (97 of 138, 70.3%), with radiographic deterioration to a peak (mean time from onset of fever to peak, 8.6 days ± 3.1 [SD]; range, 2–17 days) followed by radiographic improvement (Fig 3). Twenty-four of 138 subjects (17.4%) had the type 2 pattern, with two distinct radiographic peaks at 6.3 days ± 3.0 and 13.5 days ± 3.7. Ten subjects (7.3%) had the static type 3 radiographic appearances for most of the time during treatment. Among seven subjects with Type 4 pattern, radiographs showed progressive deterioration until the lungs became completely consolidated or the subject died. Six died during the study period, and one remains critically ill at the time of this writing, requiring intensive care and assisted ventilation.



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  		Figure 3a. Serial radiographic appearances in a 23-year-old woman with SARS, type 1 pattern. (a) Frontal chest radiograph obtained at clinical presentation shows unilateral focal air-space opacity in the right middle zone. (b) Follow-up frontal chest radiograph obtained 5 days later shows progression of radiographic changes, with multifocal bilateral air-space opacities in both lungs. (c) Subsequent follow-up chest radiograph obtained after another 7 days shows radiographic improvement in extent of pulmonary parenchymal air-space opacities after successful medical therapy with a combination of oral ribavirin and corticosteroids.

 


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  		Figure 3b. Serial radiographic appearances in a 23-year-old woman with SARS, type 1 pattern. (a) Frontal chest radiograph obtained at clinical presentation shows unilateral focal air-space opacity in the right middle zone. (b) Follow-up frontal chest radiograph obtained 5 days later shows progression of radiographic changes, with multifocal bilateral air-space opacities in both lungs. (c) Subsequent follow-up chest radiograph obtained after another 7 days shows radiographic improvement in extent of pulmonary parenchymal air-space opacities after successful medical therapy with a combination of oral ribavirin and corticosteroids.

 


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  		Figure 3c. Serial radiographic appearances in a 23-year-old woman with SARS, type 1 pattern. (a) Frontal chest radiograph obtained at clinical presentation shows unilateral focal air-space opacity in the right middle zone. (b) Follow-up frontal chest radiograph obtained 5 days later shows progression of radiographic changes, with multifocal bilateral air-space opacities in both lungs. (c) Subsequent follow-up chest radiograph obtained after another 7 days shows radiographic improvement in extent of pulmonary parenchymal air-space opacities after successful medical therapy with a combination of oral ribavirin and corticosteroids.

 
Of the 59 subjects with unilateral focal air-space opacity on initial radiographs, 44 (74.6%) progressed to unilateral multifocal (n = 10) or bilateral multifocal (n = 34) air-space opacities during hospitalization. In fifteen (25.4%), the opacity remained unilateral focal in terms of lung involvement.

Confluent air-space opacities diffusely involving both lungs, compatible with acute respiratory distress syndrome, were observed in 11 of 138 subjects (8.0%) during the course of the disease (Fig 4); this occurred almost exclusively in subjects with poor clinical outcome (six died and five required prolonged assisted ventilation at the end of the study period).



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  		Figure 4. Frontal chest radiograph in a 76-year-old man with SARS who was undergoing medical treatment shows diffuse confluent air-space opacities involving both lungs and normal heart size. These findings are compatible with radiologic features of acute respiratory distress syndrome.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
REFERENCES
 
SARS was recognized as a global health hazard in March 2003. At our institution it initially affected mainly health care professionals but soon spread to involve inpatients, outpatients and their contacts. With the convenience of air travel, the disease has now spread to all parts of the world, with patients appearing in other parts of Asia, Europe, North America, and Australia. In view of the worldwide increase in number of confirmed cases, the WHO issued a global alert for the first time in more than a decade (1). The disease is highly infectious and, at the time of this writing, only preliminary data have been reported on the causative agent of SARS. A coronavirus has been implicated as the causative agent (4). It is suspected that infection is transmitted by means of droplets and, possibly, fomites; hence, both respiratory and contact infection-control precautions are important for the protection of health care workers, as recommended by the Centers for Disease Control and Prevention (5).

On the basis of our results, air-space opacification is the pattern seen on chest radiographs in patients with SARS. All but one of 138 subjects showed air-space opacification of varying extent and distribution at some stage of the disease. In one subject, the initial and early-progress radiographs were normal and the diagnosis was made with the aid of thin-section CT of thorax. The CT scans in this subject showed a small (approximately 2-cm) area of ground-glass opacification with intralobular interstitial and interlobular septal thickening in the posterior costophrenic recess of the right lung. We have recently reported the thin-section CT findings in patients with SARS (6).

The peripheral location of air-space opacification was another common radiographic feature of SARS in our study. The opacities occupied a peripheral or mixed peripheral and central location in 88% of subjects. Important absent findings included the lack of cavitation, lymphadenopathy, or pleural effusion.

The radiographic appearance of peripheral air-space opacities in SARS is indistinguishable from other causes of atypical pneumonia, such as Mycoplasma, Chlamydia, and Legionella (7,8), and overlap with other types of viral pneumonia in adults (9). Since imaging alone cannot help differentiate SARS from other diseases, the clinical manifestation is indispensable for diagnosis. The presence of characteristic clinical features, including high fever (temperature > 38°C), chills, rigor, myalgia, and laboratory findings such as leukopenia and thrombocytopenia in patients with recent exposure, are very suggestive of SARS. The presence of an air-space opacity on chest radiographs has been as helpful in confirmation of the diagnosis.

Radiographic progression to unilateral multifocal or bilateral involvement occurred in most subjects with unilateral focal air-space opacity on the initial chest radiograph obtained during treatment with a combination of an antiviral agent and corticosteroids. We found that only a small percentage (7.2%) of subjects with SARS showed a static radiographic appearance (type 3 pattern) for most of the time during treatment. On the other hand, progressive radiographic deterioration despite medical treatment seems to be associated with poor prognosis, with all deaths in our series occurring in patients with the type 4 pattern.

There are some limitations to our early study: (a) The subjects in this study were a heterogeneous group, and we have not taken into account the severity of clinical symptoms and clinical outcome. (b) Visual estimation of the percentage of lung involvement may appear to be subjective; however, in our opinion this appears to be the most practical method in real life, in an epidemic crisis in which it is not possible to design detailed computer-based models at short notice. (c) A frontal radiograph alone may not be accurate in helping identify central versus peripheral lesions; however, in patients who underwent thin-section CT, this localization proved to be accurate (6). (d) This report does not deal with clinical and radiologic comparison, particularly the timing and type of treatment regimen and the timing of the radiographic response. It also does not include evaluation of any outcome indicators. Such an evaluation requires detailed clinical, immunologic, and statistical analyses, which may be possible when more data and experience become available.

In conclusion, SARS has become a global health hazard and its high infectivity is alarming. Imaging plays an important role in the diagnosis and monitoring of response to therapy. The predominant peripheral location; common progression pattern from unilateral focal air-space opacity to unilateral multifocal or bilateral involvement during treatment; and lack of cavitation, lymphadenopathy, and pleural effusion are the more distinctive radiographic findings of this potentially lethal disease.


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

Abbreviations: SARS = severe acute respiratory syndrome, WHO = World Health Organization

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


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 

  1. World Health Organization. Cumulative number of reported cases (SARS) from 1 February to 27 March 2003. Available at: www.who.int/csr/sarscountry/2003_04_11. Accessed April 12 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 [serial online]. April 14 2003. Available at: nejm.org/earlyrelease/sars.asp.
  3. World Health Organization. Case definitions for surveillance of severe acute respiratory syndrome (SARS). Available at: www.who.int/csr/sars/casedefinition/en/. Accessed April 12 2003.
  4. Update: outbreak of severe acute respiratory syndrome—worldwide, 2003. MMWR Morb Mortal Wkly Rep 2003; 52:241-248.[Medline]
  5. Centers for Disease Control and Prevention. Updated interim domestic infection control guidance in the health care and community setting for patients with suspected SARS. Available at: www.cdc.gov/ncidod/sars/infectioncontrol.htm. Accessed April 4 2003.
  6. 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 (in press).
  7. Goodman LR, Goren RA, Teptick SK. The radiographic evaluation of pulmonary infection. Med Clin North Am 1980; 64:553-574.[Medline]
  8. Macfarlane JT, Miller AC, Roderick Smith WH, Morris AH, Rose DH. Comparative radiographic features of community acquired Legionnaires disease, pneumococcal pneumonia, mycoplasma pneumonia, and psittacosis. Thorax 1984; 39:28-33.[Abstract]
  9. Kim EA, Lee KS, Primack SL, et al. Viral pneumonias in adults: radiologic and pathologic findings. RadioGraphics 2002; 22(spec issue):137S-149S.



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C.-L. Liu, Y.-T. Lu, M.-J. Peng, P.-J. Chen, R.-L. Lin, C.-L. Wu, and H.-T. Kuo
Clinical and Laboratory Features of Severe Acute Respiratory Syndrome Vis-A-Vis Onset of Fever
Chest, August 1, 2004; 126(2): 509 - 517.
[Abstract] [Full Text] [PDF]

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 Int J EpidemiolHome page
U. D Parashar and L. J Anderson
Severe acute respiratory syndrome: review and lessons of the 2003 outbreak
Int. J. Epidemiol., August 1, 2004; 33(4): 628 - 634.
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 ChestHome page
H.-H. Hsu, C. Tzao, C.-P. Wu, W.-C. Chang, C.-L. Tsai, H.-J. Tung, and C.-Y. Chen
Correlation of High-Resolution CT, Symptoms, and Pulmonary Function in Patients During Recovery From Severe Acute Respiratory Syndrome
Chest, July 1, 2004; 126(1): 149 - 158.
[Abstract] [Full Text] [PDF]

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 Postgrad. Med. J.Home page
D S C Hui, M C H Chan, A K Wu, and P C Ng
Severe acute respiratory syndrome (SARS): epidemiology and clinical features
Postgrad. Med. J., July 1, 2004; 80(945): 373 - 381.
[Abstract] [Full Text] [PDF]

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 Am. J. Roentgenol.Home page
Y.-L. Wan, H.-P. Kuo, Y.-H. Tsai, Y.-K. Wu, C.-H. Wang, C.-Y. Liu, K.-C. Kao, and S.-F. Ko
Eight Cases of Severe Acute Respiratory Syndrome Presenting as Round Pneumonia
Am. J. Roentgenol., June 1, 2004; 182(6): 1567 - 1570.
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 Am. J. Roentgenol.Home page
S.-C. Hsieh, W. P. Chan, J. C.-W. Chien, W.-S. Lee, M.-S. Yao, W.-M. Choi, C.-Y. Chen, and C. Yu
Radiographic Appearance and Clinical Outcome Correlates in 26 Patients with Severe Acute Respiratory Syndrome
Am. J. Roentgenol., May 1, 2004; 182(5): 1119 - 1122.
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 J. Clin. Pathol.Home page
G M-K Tse, K-F To, P K-S Chan, A W I Lo, K-C Ng, A Wu, N Lee, H-C Wong, S-M Mak, K-F Chan, et al.
Pulmonary pathological features in coronavirus associated severe acute respiratory syndrome (SARS)
J. Clin. Pathol., March 1, 2004; 57(3): 260 - 265.
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 RadioGraphicsHome page
N. S. Paul, H. Roberts, J. Butany, T. Chung, W. Gold, S. Mehta, E. Konen, A. Rao, Y. Provost, H. H. Hong, et al.
Radiologic Pattern of Disease in Patients with Severe Acute Respiratory Syndrome: The Toronto Experience
RadioGraphics, March 1, 2004; 24(2): 553 - 563.
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 RadiologyHome page
G. M. Joynt, G. E. Antonio, P. Lam, K. T. Wong, T. Li, C. D. Gomersall, and A. T. Ahuja
Late-Stage Adult Respiratory Distress Syndrome Caused by Severe Acute Respiratory Syndrome: Abnormal Findings at Thin-Section CT
Radiology, February 1, 2004; 230(2): 339 - 346.
[Abstract] [Full Text] [PDF]

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 Am. J. Roentgenol.Home page
N. L. Muller, G. C. Ooi, P. L. Khong, L. J. Zhou, K. W. T. Tsang, and S. Nicolaou
High-Resolution CT Findings of Severe Acute Respiratory Syndrome at Presentation and After Admission
Am. J. Roentgenol., January 1, 2004; 182(1): 39 - 44.
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 Am. J. Roentgenol.Home page
R. Bitar, W. J. Weiser, M. Avendano, P. Derkach, D. E. Low, and D. Muradali
Chest Radiographic Manifestations of Severe Acute Respiratory Syndrome in Health Care Workers: The Toronto Experience
Am. J. Roentgenol., January 1, 2004; 182(1): 45 - 48.
[Abstract] [Full Text] [PDF]

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 Am. J. Roentgenol.Home page
H. A. Parmar, T. C. C. Lim, J. S.-K. Goh, J. T. Tan, Y. Y. Sitoh, and F. Hui
Providing Optimal Radiology Service in the Severe Acute Respiratory Syndrome Outbreak: Use of Mobile CT
Am. J. Roentgenol., January 1, 2004; 182(1): 57 - 60.
[Abstract] [Full Text] [PDF]

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 NEJMHome page
J. S.M. Peiris, K. Y. Yuen, A. D.M.E. Osterhaus, and K. Stohr
The Severe Acute Respiratory Syndrome
N. Engl. J. Med., December 18, 2003; 349(25): 2431 - 2441.
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 QJMHome page
D.A. Groneberg, L. Zhang, T. Welte, P. Zabel, and K.F. Chung
Severe acute respiratory syndrome: global initiatives for disease diagnosis
QJM, November 1, 2003; 96(11): 845 - 852.
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 RadiologyHome page
C. G. C. Ooi, P. L. Khong, J. C. M. Ho, B. Lam, W. M. Wong, W. C. Yiu, P. C. Wong, C. F. Wong, K. N. Lai, and K. W. T. Tsang
Severe Acute Respiratory Syndrome: Radiographic Evaluation and Clinical Outcome Measures
Radiology, November 1, 2003; 229(2): 500 - 506.
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 ThoraxHome page
N L Muller and J M FitzGerald
Severe acute respiratory syndrome (SARS)
Thorax, November 1, 2003; 58(11): 919 - 919.
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 RadiologyHome page
C. G. C. Ooi, P. L. Khong, B. Lam, J. C. M. Ho, W. C. Yiu, W.-M. Wong, T. Wang, P. L. Ho, P. C. Wong, R. H. Chan, et al.
Severe Acute Respiratory Syndrome: Relationship between Radiologic and Clinical Parameters
Radiology, November 1, 2003; 229(2): 492 - 499.
[Abstract] [Full Text] [PDF]

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 JWatch GastroenterologyHome page
Radiographic Appearance of SARS
Journal Watch Gastroenterology, September 30, 2003; 2003(930): 12 - 12.
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 RadiologyHome page
C.C. T. Lim, J. S. K. Goh, H. Parmar, Y. Y. Sitoh, J. T. Tan, and F. Hui
CT and Picture Archiving and Communication Systems: Radiology Response to the SARS Outbreak [letter]
Radiology, September 1, 2003; 228(3): 901 - 901.
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