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Zhou et al.
CT Features of COVID-19 Pneumonia
Cardiopulmonary Imaging
Original Research CT Features of Coronavirus
Disease 2019 (COVID-19)
Pneumonia in 62 Patients in
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Wuhan, China
Shuchang Zhou1 OBJECTIVE. The purpose of this study was to investigate 62 subjects in Wuhan, China,
Yujin Wang with laboratory-confirmed coronavirus disease (COVID-19) pneumonia and describe the CT
Tingting Zhu features of this epidemic disease.
Liming Xia MATERIALS AND METHODS. A retrospective study of 62 consecutive patients with
laboratory-confirmed COVID-19 pneumonia was performed. CT images and clinical data
Zhou S, Wang Y, Zhu T, Xia L were reviewed. Two thoracic radiologists evaluated the distribution and CT signs of the le-
sions and also scored the extent of involvement of the CT signs. The Mann-Whitney U test
was used to compare lesion distribution and CT scores. The chi-square test was used to com-
pare the CT signs of early-phase versus advanced-phase COVID-19 pneumonia.
RESULTS. A total of 62 patients (39 men and 23 women; mean [± SD] age, 52.8 ± 12.2
years; range, 30–77 years) with COVID-19 pneumonia were evaluated. Twenty-four of 30 pa-
tients who underwent routine blood tests (80.0%) had a decreased lymphocyte count. Of 27 pa-
tients who had their erythrocyte sedimentation rate and high-sensitivity C-reactive protein level
assessed, 18 (66.7%) had an increased erythrocyte sedimentation rate, and all 27 (100.0%) had
an elevated high-sensitivity C-reactive protein level. Multiple lesions were seen on the initial CT
scan of 52 of 62 patients (83.9%). Forty-eight of 62 patients (77.4%) had predominantly periph-
eral distribution of lesions. The mean CT score for the upper zone (3.0 ± 3.4) was significantly
lower than that for the middle (4.5 ± 3.8) and lower (4.5 ± 3.7) zones (p = 0.022 and p = 0.020,
respectively), and there was no significant difference in the mean CT score of the middle and
lower zones (p = 1.00). The mean CT score for the anterior area (4.4 ± 4.1) was significantly
lower than that for the posterior area (7.7 ± 6.3) (p = 0.003). CT findings for the patients were
as follows: 25 patients (40.3%) had ground-glass opacities (GGO), 21 (33.9%), consolidation; 39
(62.9%), GGO plus a reticular pattern; 34 (54.8%), vacuolar sign; 28 (45.2%), microvascular di-
lation sign; 35 (56.5%), fibrotic streaks; 21 (33.9%), a subpleural line; and 33 (53.2%), a subpleu-
ral transparent line. With regard to bronchial changes seen on CT, 45 patients (72.6%) had air
bronchogram, and 11 (17.7%) had bronchus distortion. In terms of pleural changes, CT showed
that 30 patients (48.4%) had pleural thickening, 35 (56.5%) had pleural retraction sign, and six
(9.7%) had pleural effusion. Compared with early-phase disease (≤ 7 days after the onset of
symptoms), advanced-phase disease (8–14 days after the onset of symptoms) was characterized
by significantly increased frequencies of GGO plus a reticular pattern, vacuolar sign, fibrotic
streaks, a subpleural line, a subpleural transparent line, air bronchogram, bronchus distortion,
and pleural effusion; however, GGO significantly decreased in advanced-phase disease.
CONCLUSION. CT examination of patients with COVID-19 pneumonia showed a
Keywords: coronavirus disease 2019, COVID-19, CT, mixed and diverse pattern with both lung parenchyma and the interstitium involved. Identi-
pneumonia fication of GGO and a single lesion on the initial CT scan suggested early-phase disease. CT
doi.org/10.2214/AJR.20.22975
signs of aggravation and repair coexisted in advanced-phase disease. Lesions presented with a
characteristic multifocal distribution in the middle and lower lung regions and in the posterior
Received February 16, 2020; accepted without revision lung area. A decreased lymphocyte count and an increased high-sensitivity C-reactive protein
February 19, 2020. level were the most common laboratory findings.
1
All authors: Department of Radiology, Tongji Hospital,
Tongji Medical College, Huazhong University of Science
ince late December of 2019, an ing to the initial investigation, most cases
S
and Technology, 1095 Jiefang Rd, Qiaokou District,
Wuhan, Hubei 430030, China. Address correspondence explosion in the number of cases were thought to originate from the Huanan
to Y. Wang (wangyujin8303@163.com). of a new acute viral respiratory Seafood Wholesale Market in Wuhan [1]. At
disease (coronavirus disease the time of the writing of this article, the vi-
AJR 2020; 214:1287–1294 [COVID-19]) caused by a novel coronavirus rus is rapidly spreading to many other cities
(severe acute respiratory syndrome coronavi- in China and even to other countries around
ISSN-L 0361–803X/20/2146–1287
rus 2 [SARS-CoV-2]) has been reported in the world. Although SARS-CoV-2 is a mem-
© American Roentgen Ray Society the city of Wuhan in central China. Accord- ber of the coronavirus family of viruses, it is
more distant from SARS coronavirus spectively reviewed the CT images on a PACS nally, bilateral lungs were divided into 12 zones
(SARS-CoV) and Middle East respiratory workstation (Synapses, Fujifilm) with multipla- altogether. The degree of involvement in each lung
syndrome coronavirus, is considered to be a nar reconstruction tools and reached a decision zone was scored as follows [6–8]: a score of 0 de-
new type of betacoronavirus that infects hu- in consensus. The images were viewed in lung noted no involvement; 1, < 25% involvement; 2,
mans [2], and on the basis of the current epi- window settings (width, 1000–1500 HU; level, 25% to less than 50% involvement; 3, 50% to less
demic, is more infectious than SARS-CoV. 700 to −550 HU) and mediastinal window set- than 75% involvement; and 4, ≥ 75% involvement.
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As of 8:00 p.m. on February 17, 2020, a total tings (width, 300–350 HU; level, 30–40 HU). Scores were recorded and summed for each lung
of 68,595 confirmed cases of COVID-19 and The predominant patterns seen on CT imag- zone, with a maximum possible score of 48.
1667 deaths were reported. In the present es were classified into three major categories:
study, we identified 62 patients in Wuhan, lung, bronchial, and pleural changes. Each major Statistical Analysis
China, who had laboratory-confirmed category was divided into subcategories. Lung Data were recorded using spreadsheet soft-
COVID-19 pneumonia and described the CT changes were classified into the following eight ware (Excel 2010, Microsoft) and were analyzed
features of this pneumonia. subcategories: ground-glass opacities (GGO; in- using statistical software (SPSS, version 22.0,
creased attenuation without obscuration of the IBM). Continuous variables were expressed as
Materials and Methods underlying lung vessels) [3], consolidation (ho- mean (± SD) values. The Kolmogorov-Smirnov
The ethics committee at Huazhong University mogeneous increased intensity of lung parenchy- test was used for the normal distribution test,
of Science and Technology waived the need for in- ma with obscuration of the underlying vessels), and continuous variables were compared using
formed consent for this retrospective study. GGO plus a reticular pattern (a reticular shad- the Mann-Whitney U test. The frequency of CT
We retrospectively reviewed 118 patients seen ow on the background of GGO and thickening of signs was expressed as the number (percentage)
with suspected COVID-19 pneumonia from Janu- the interlobular septum and interlobular septum, of occurrences and was compared for cases of
ary 16 to January 30, 2020. All patients had ab- showing paving stone sign) [4], vacuolar sign (a early- versus advanced-phase disease using the
normal CT findings that suggested pneumonia as vacuole-like transparent shadow of < 5 mm in chi-square test or the Fisher exact test. Differenc-
the diagnosis. A patient with suspected COVID-19 length observed in the lesion), microvascular di- es for which p < 0.05 were considered statistical-
pneumonia was defined as a patient with pneumo- lation sign (dilated small vessels in the lesion), fi- ly significant.
nia who met at least three of the following five cri- brotic streaks (an irregular strip shadow), a sub-
teria: fever, a low or normal WBC count or low pleural line (an arc-shaped linear shadow 2–5 cm Results
lymphocyte count, exclusion of other respiratory in length appearing parallel to the chest wall), or Clinical Characteristics
virus species on the basis of laboratory findings, a subpleural transparent line (a thin and transpar- A total of 62 patients (mean age, 52.8 ±
no relief in symptoms noted after receipt of empir- ent line lying between the lesions and the viscer- 12.2 years; range, 30–77 years) with COV-
ical antimicrobial or antiinfluenza treatment for 3 al layer of pleura). Bronchial changes were classi- ID-19 pneumonia were included in the study.
days, and in particular, an epidemiologic link to fied into two subcategories: air bronchogram (an Thirty-nine of the 62 patients (62.9%) were
the Huanan Seafood Wholesale Market or a his- air-filled image of bronchus in lung lesions) and men (mean age, 54.1 ± 11.8 years; range,
tory of contact with other patients with COVID-19 bronchus distortion. Pleural changes were clas- 30–77 years), and 23 (37.1%) were women
pneumonia. A total of 62 patients were confirmed sified into three subcategories: thickening of the (mean age, 50.7 ± 12.8 years; range, 30–73
to have COVID-19 nucleic acid on the basis of pleura, pleural retraction sign (lesions present years). All patients had symptoms at onset of
positive findings for respiratory samples tested close to the visceral pleura and pull pleura), or the disease, with fever noted in 54 patients
using real-time reverse-transcription–polymerase pleural effusion. Distribution of the lung lesions (87.1%), coughing and sputum in 28 patients
chain reaction. Two of the researchers recorded was classified as predominantly peripheral (in- (45.2%), fatigue in 14 patients (22.6%), short-
clinical data, including symptoms, date of onset volving mainly the peripheral region comprising ness of breath in 15 patients (24.2%), mus-
of symptoms, laboratory examination results, and one-third of the lung), central (involving mainly cle pain in 20 patients (32.3%), and gastro-
information regarding other accompanying condi- the central region comprising two-thirds of the intestinal symptoms, including abdominal
tions or diseases. lung), or peripheral plus central (involving both pain and diarrhea, in nine patients (14.5%).
the peripheral and central regions) [5]. Because Routine blood tests were performed for 30
CT Scanning Protocol no cases of lymphadenopathy and pneumothorax patients. Six patients (20.0%) had leukope-
MDCT was performed using either of the follow- were found, those two signs will not be described nia, 24 (80.0%) had a decreased lympho-
ing CT scanners: the 16-MDCT LightSpeed scan- in the present study. cyte count, and 15 (50.0%) had a decreased
ner (GE Healthcare) or the uCT 760 scanner (Unit- The extent of involvement on thin-section CT percentage of lymphocytes. The erythrocyte
ed Imaging). The parameters used for the scanning images was also assessed by the two radiologists. sedimentation rate and high-sensitivity C-re-
protocol were as follows: patient in the supine po- Each side of the lung was divided (from top to bot- active protein (hs-CRP) level were evaluated
sition; end inspiratory acquisition; tube voltage, tom) into three zones: the upper zone (above the in 27 patients. Of these patients, 18 (66.7%)
100–120 kV; tube current–exposure time product, carina), the middle zone (from the carina to the had an increased erythrocyte sedimenta-
200–300 mAs; pitch, 1.375 and 0.9125; and sec- inferior pulmonary vein), and the lower zone (be- tion rate, and all 27 (100.0%) had an elevat-
tion thickness after reconstruction, 1.25 mm. Un- low the inferior pulmonary vein). Each zone was ed hs-CRP level. Four patients had a history
enhanced CT scans were obtained for all patients. then divided into two areas: the anterior area (the of hypertension, four had diabetes, one had
area before the vertical line of the midpoint of the cerebral infarction, one had chronic kidney
Image Viewing and Evaluation diaphragm in the sagittal position) and the poste- disease, and two were pregnant. Table 1 sum-
Two experienced radiologists with 13 and 9 rior area (the area after the vertical line of the mid- marizes the demographic and clinical char-
years of experience in thoracic radiology retro- point of the diaphragm in the sagittal position). Fi- acteristics of the patients.
TABLE 1: Demographic and Clinical TABLE 2: Distribution and CT Score for Parenchymal Abnormalities in 62
Characteristics of Patients Patients With Coronavirus Disease 2019 Pneumonia
With Coronavirus Disease
2019 Pneumonia Category and Subcategory No. (%) of Patients CT Score, Mean ± SD p
Lesion distribution 0.008a
Characteristic Value
Peripheral 48 (77.4)
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TABLE 3: CT Features of C
oronavirus TABLE 4: CT Features of Coronavirus Disease 2019 Pneumonia in Patients
Disease 2019 Pneumonia With Early- and Advanced-Phase Disease
No. (%) of Early-Phase Advanced-Phase Chi-Square Test
Patients CT Feature Disease (n = 40) Disease (n = 22) Statistic p
CT Feature (n = 62)
Lung change
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by an incompletely filled alveolar cluster in was accompanied by repair changes. There tion and epidemiology of 2019 novel coronavirus:
the exudative lung parenchyma. The micro- was no significant difference between early- implications for virus origins and receptor bind-
vascular dilation sign probably indicated in- phase disease versus advanced-phase disease ing. Lancet 2020; 395:565–574
creased blood supply to the inflammatory in terms of consolidation, the microvascular 3. Joynt GM, Antonio GE, Lam P, et al. Late-stage
area. Air bronchogram was formed by bron- dilation sign, thickening of pleura, and the adult respiratory distress syndrome caused by se-
chus containing air in consolidation. GGO pleural retraction sign. vere acute respiratory syndrome: abnormal findings
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plus a reticular pattern represented thicken- The present study has two limitations. First, at thin-section CT. Radiology 2004; 230:339–346
ing of the interlobular septum resulting from because the course of COVID-19 pneumonia 4. Wong KT, Antonio GE, Hui DS, et al. Thin-sec-
the GGO, which ultimately evolved into the is short, changes seen on CT over its entire tion CT of severe acute respiratory syndrome:
subpleural line. Fibrotic streaks indicated lo- course have not been completely tracked and evaluation of 73 patients exposed to or with the
cal inflammatory absorption and residual fi- described for all patients. Second, there is not disease. Radiology 2003; 228:395–400
brosis, and bronchus distortion suggested that enough pathologic data on these patients for a 5. Ajlan AM, Ahyad RA, Jamjoom LG, Alharthy A,
the local inflammation absorbed and retract- comparative study to be performed. Madani TA. Middle East respiratory syndrome
ed the bronchus inside or surrounded it. The In conclusion, CT findings for patients coronavirus (MERS-CoV) infection: chest CT
pleura were often involved and were charac- with COVID-19 pneumonia showed that the findings. AJR 2014; 203:782–787
terized by thickening and retraction resulting disease has a mixed and diverse pattern, with 6. Ooi GC, Khong PL, Müller NL, et al. Severe acute
from the inflammatory reaction. both lung parenchyma and interstitium in- respiratory syndrome: temporal lung changes at
In early-phase COVID-19 pneumonia (≤ 7 volved. The presence of GGO and a single thin-section CT in 30 patients. Radiology 2004;
days after the onset of symptoms), bron- lesion at the onset of COVID-19 pneumonia 230:836–844
chus distortion (10.0%) and pleural effu- suggested that the disease was in its early 7. Chang YC, Yu CJ, Chang SC, et al. Pulmonary
sion (2.5%) were relatively rare compared phase. CT signs of aggravation and repair co- sequelae in convalescent patients after severe
with other signs (frequency, 27.5–62.5%). existed in examinations of patients with ad- acute respiratory syndrome: evaluation with thin-
In advanced-phase disease (8–14 days after vanced-phase disease. Pleural effusion might section CT. Radiology 2005; 236:1067–1075
the onset of symptoms), GGO plus a retic- occur in the advanced phase. Multifocality 8. Chung M, Bernheim A, Mei X, et al. CT imaging
ular pattern (86.4%), vacuolar sign (81.8%), as well as primary distribution of lesions in features of 2019 novel coronavirus (2019-nCoV).
air bronchogram (81.8%), fibrotic streaks the middle and lower zones and the posteri- Radiology 2020 Feb 24 [Epub ahead of print]
(90.9%), and the subpleural transparent or area of the lungs were rather characteris- 9. Wan Y, Shang J, Graham R, Baric RS, Li F. Receptor
line (72.7%) were relatively more common tic manifestations. A decreased lymphocyte recognition by novel coronavirus from Wuhan: an
than other signs (frequency, 22.7–59.1%). count and an elevated hs-CRP level were the analysis based on decade-long structural studies of
Compared with early-phase disease, ad- most common laboratory findings. SARS. J Virol 2020 Jan 29 [Epub ahead of print]]
vanced-phase disease was associated with 10. Harmer D, Gilbert M, Borman R, Clark KL.
a significantly increased frequency of GGO Acknowledgment Quantitative mRNA expression profiling of ACE
plus a reticular pattern, vacuolar sign, fibrot- We thank Zujun Hou for assistance in re- 2, a novel homologue of angiotensin converting
ic streaks, air bronchogram, bronchus distor- vising this manuscript. enzyme. FEBS Lett 2002; 532:107–110
tion, a subpleural line, a subpleural transpar- 11. Chen N, Zhou M, Dong X, et al. Epidemiological
ent line, and pleural effusion, but GGO was References and clinical characteristics of 99 cases of 2019
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gested that GGO was a relatively early sign patients infected with 2019 novel coronavirus in descriptive study. Lancet 2020; 395:507–513
in the course of the disease and that in the ad- Wuhan, China. Lancet 2020; 395:497–506 [Erra- 12. Koo HJ, Lim S, Choe J, Choi SH, Sung H, Do KH.
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(Figures start on next page)
A B
C D E
Fig. 1—Distribution of lesions in five patients with coronavirus disease 2019 pneumonia.
A, 30-year-old man. CT image obtained on day 2 after onset of symptoms shows single lesion that developed in inferior lobe of right lung.
B, 49-year-old man. CT image obtained on day 7 after onset of symptoms shows multiple lesions involving multiple lobes of bilateral lungs.
C, 38-year-old man. CT image obtained on day 5 after onset of symptoms shows peripheral distribution of patchy ground-glass opacities plus reticular pattern with
vacuole inside.
D, 46-year-old woman. CT image obtained on day 9 after onset of symptoms shows peripheral plus central distribution of ground-glass opacities, partial consolidation,
and fibrosis streak.
E, 38-year-old woman. CT image obtained on day 7 after onset of symptoms shows posterior area with more serious involvement than anterior area.
A B C
Fig. 2—CT features indicating changes in lungs caused by coronavirus disease 2019 pneumonia in eight patients.
A, 52-year-old woman. CT image obtained on day 4 after onset of symptoms shows multiple ground-glass opacities (box) in inferior lobe of left lung.
B, 55-year-old man. CT image obtained on day 8 after onset of symptoms shows area of consolidation (box) with ground-glass opacities surrounded (arrow) in lingual
segment of upper lobe of left lung. Air bronchogram can be seen inside consolidation.
C, 32-year-old woman. CT image obtained on day 5 after onset of symptoms shows ground-glass opacities plus reticular pattern (box) in peripheral area of inferior lobe of
right lung.
(Fig. 2 continues on next page)
D E F
Fig. 2 (continued)—CT features indicating changes in
lungs caused by coronavirus disease 2019 pneumonia
in eight patients.
D, 57-year-old woman. CT image obtained on day 7
after onset of symptoms shows vacuolar sign (arrow).
E, 55-year-old man. CT image obtained on day 7 after
onset of symptoms shows microvascular dilation sign
(arrow) in ground-glass opacities.
F, 57-year-old woman. CT image obtained on day 10
after onset of symptoms shows fibrotic streaks (box)
in inferior lobe of left lung.
G, 39-year-old man. CT image obtained on day 14
after onset of symptoms shows subpleural line
(arrow) in right lung.
H, 45-year-old man. CT image obtained on day 12 after
onset of symptoms shows subpleural transparent line
(arrows) below left pleura.
G H
A B C
Fig. 3—CT features indicating bronchial changes caused by coronavirus disease 2019 pneumonia.
A, 41-year-old man. CT image obtained on day 7 after onset of symptoms shows air bronchogram (arrow) in patchy ground-glass opacities with partial consolidation in
inferior lobe of right lung.
B, 55-year-old man. CT image obtained on day 16 after onset of symptoms shows air bronchogram (arrow) in consolidation in lingual segment of upper lobe of left lung.
C, 57-year-old woman. CT image obtained on day 16 after onset of symptoms shows bronchus distortion (arrow) in ground-glass opacities.