Current issues and trends in Respiratory therapy
Value of Bedside Lung Ultrasound in Severe and Critical COVID-19 Pneumonia
Shuangshuang Kong, Jing Wang, Yuman Li, Ying Tian, Cheng Yu, Danqing Zhang, Hong Li, Li Zhang, Xueqin Pang, and Mingxing Xie
BACKGROUND: Lung ultrasound (LUS) is an effective imaging modality that can differentiate
pathological lung from non-diseased lung. We aimed to explore the value of bedside LUS in
patients with severe and critical coronavirus disease 2019 (COVID-19)-associated lung injury.
METHODS: Sixty-three severe and 33 critical hospitalized subjects with COVID-19 were en-
rolled in this study. Bedside LUS was performed in all subjects; chest computed tomography
was performed on the same day as bedside LUS in 23 cases. The LUS protocol consisted of 12
scanning zones. LUS score based on B-lines and lung consolidation was evaluated. RESULTS:
The most common abnormality of LUS was the various forms of B-lines, detected in 93 (96.9%)
subjects; as the second most frequent abnormality, 80 (83.3%) subjects exhibited lung consolida-
tion, mainly located in the posterior lung region. Twenty-four (25.0%) subjects had pleural line
abnormalities, and 16 (16.7%) had pleural effusion; 78 (81.3%) subjects had 6 2 abnormal LUS
patterns, and 93 (96.9%) had bilateral lung involvement. The proportion of bilateral or unilat-
eral lung consolidation and pleural effusion in the critical COVID-19 group were higher than
that in the severe group (P < .05). The lung consolidation of critical subjects showed a marked increase in most lung areas, including bilateral lateral lung, posterior lung, and left anterior-in-
ferior lung area. The median (interquartile range) LUS scores of critical cases were higher than
those of severe cases: left: 14 (12–17) vs 7 (5–12); right: 14 (10–16) vs 8 (3–12); bilateral: 28 (23–
31) vs 15 (8–22) (P < .001 for all). There was a good correlation between the LUS score and the chest computed tomography score (r 5 0.887, P < .001). CONCLUSIONS: The most common abnormal LUS pattern in subjects with severe and critical COVID-19 pneumonia was B-lines, fol-
lowed by lung consolidation. Bedside LUS can provide important information for pulmonary involve-
ment in patients with COVID-19. Key words: lung; ultrasound; diagnostic imaging; COVID-19; pneumonia; computed tomography. [Respir Care 2021;66(6):920–927. © 2021 Daedalus Enterprises]
Introduction
The coronavirus disease 2019 (COVID-19) caused by
severe acute respiratory syndrome coronavirus 2 (SARS-
CoV-2) has spread worldwide, resulting in lung and other
multiple organ damage and seriously threatening human
life and health.1-4 Severe and critical COVID-19 patients
may have hypoxemia or respiratory failure, as well as shock
or multiple organ failure, which require mechanical ventila-
tion and monitoring. Chest computed tomography (CT) has
The authors are affiliated with the Department of Ultrasound, Union
Hospital, Tongji Medical College, Huazhong University of Science and
Technology, Wuhan, China. The authors are also affiliated with the
Hubei Province Key Laboratory of Molecular Imaging, Wuhan, China.
Drs Kong, Wang, Li, and Tian are co-first authors.
This work was supported by the National Natural Science Foundation of
China (Grant Nos. 81771851, 81727805, 81922033). The authors have
disclosed no conflicts of interest.
Supplementary material related to this paper is available at http://www.
rcjournal.com.
Correspondence: Mingxing Xie MD PhD, Department of Ultrasound,
Union Hospital, Tongji Medical College, Huazhong University of
Science and Technology, 1277# Jiefang Ave, Wuhan 430022, China.
E-mail: [email protected].
DOI: 10.4187/respcare.08382
920 RESPIRATORY CARE � JUNE 2021 VOL 66 NO 6
been recommended for the diagnosis of COVID-19,5,6 but
it is limited when there is no bedside CT capability due to
the high risk of transporting patients with COVID-19.7
Lung ultrasound (LUS) identifies ultrasonic artifacts origi-
nating from the pleural line and can accurately differentiate
pathological lung from non-diseased lung.8 LUS has the
advantages of being fast, noninvasive, convenient (ie, bed-
side availability),8-11 and safe with no radiation exposure,
all of which are especially suitable for the evaluation and
serial observation of patients with severe and critical
COVID-19.
The purposes of this study were to summarize the char-
acteristics of LUS in patients with severe and critical
COVID-19 in isolation wards, and to provide a reliable
method to assess COVID-19–associated lung injury.
Methods
Subjects
We included 96 adult subjects who were diagnosed with
severe or critical COVID-19 between January 25 and March
20, 2020, in the west branch of Union Hospital, Tongji
Medical College, Huazhong University of Science and
Technology. COVID-19 was confirmed in these 96 subjects
with nucleic acid testing for the diagnosis of SARS-CoV-2
infection, referring to the diagnostic criteria from the National
Health Commission of the People’s Republic of China guide-
lines for COVID-19.12 Of these subjects, 63 with severe
COVID-19 were included on the basis of exhibiting any of
the following: dyspnea, breathing frequency $ 30 brea- ths/min, SpO2 # 93% at rest, PaO2=FIO2 # 300 mm Hg, and lung infiltrates > 50% within 24–48 h. Thirty-three subjects with critical COVID-19 had respiratory failure requiring inva-
sive mechanical ventilation, shock, or multisystem organ failure.
Clinical data for the present analysis were obtained from
the medical record system of our hospital, which included
clinical findings, medical history, and pathophysiologic
findings such as vital signs and laboratory test results. This
study was approved by the ethics committee of Union
Hospital, Tongji Medical College of Huazhong University
of Science and Technology, and informed consent was
waived for this retrospective study.
LUS Image Acquisition and Score
Bedside LUS scans were ordered for subjects with severe
and critical COVID-19 who presented with dyspnea after oxy-
gen therapy through nasal cannula or mask. LUS was per-
formed by 2 experienced sonographers who had completed
LUS training (SK and YT). The images were assessed by
these physicians (SK and YT), and they reached consensus on
their findings. All subjects underwent bedside LUS examina-
tions on the first day of hospitalization and before mechanical
ventilation with the M9 Doppler ultrasonic diagnostic appara-
tus (Mindray Biomed Electronics, Shenzhen, China) with
1.0–5.0 MHz transducer or the GE LOGIQ E9 (GE
Healthcare, Milwaukee, Wisconsin) with 1.0–6.0 MHz trans-
ducer. For each hemithorax, 6 regions were scanned: anterior,
lateral, and posterior regions were delimited by anatomical
landmarks of anterior and posterior axillary lines. Each area
was divided in half, including superior and inferior region.13-15
In each subject, anterior and lateral lung regions were scanned
with the subject in the supine position, and the posterior
region was scanned with the subject in a lateral or sitting posi-
tion. All adjacent intercostal spaces must be explored parallel
and perpendicular to ribs. For each explored region, the worst
finding and the LUS score were recorded according to the fol-
lowing rating: the presence of lung sliding with A-lines or < 3 isolated B-lines, 0; multiple well-separated B-lines, 1; multi-
ple coalescent B-lines, 2; and consolidation, 3.15,16 The cumu-
lative LUS score corresponded to the sum of each region
score, with totals ranging from 0 to 36.
Chest CT Assessment and Simplified Score
Twenty-three of 96 subjects with COVID-19, including 2
critically ill subjects and 21 severely ill subjects, underwent
thin-section chest CT scans on the same day as LUS exami-
nations. CT scans were performed during full inspiration and
expiration, with a section collimation of 0.5 mm. All subjects
were scanned in a helical CT scanner (SOMATOM Force,
Siemens Healthineers, Erlangen, Germany) in the supine
position. Major CT findings, including ground-glass opac-
ities and consolidations, were recorded.5,17 To quantify the
extent of pulmonary abnormalities, a CT score was assigned
QUICK LOOK
Current knowledge
The coronavirus disease 2019 (COVID-19) can result
in serious lung damage and complications. The high
risk of transporting patients with COVID-19 limits
chest computed tomography for critical patients. It is
necessary to explore a different imaging tool, such as
lung ultrasound (LUS), to evaluate associated lung
involvement in pneumonia due to COVID-19.
What this paper contributes to our knowledge
The most common abnormal LUS pattern was B-lines,
followed by lung consolidation in severe and critical
pneumonia due to COVID-19. A strong correlation
between LUS score and computed tomography score
was observed, suggesting that bedside LUS is a reliable
method to assess COVID-19-associated lung injury.
BEDSIDE LUNG ULTRASOUND IN COVID-19
RESPIRATORY CARE � JUNE 2021 VOL 66 NO 6 921
for each lobe of bilateral lung: absent, 0; < 5% of lobe, 1; 5– 25% of lobe, 2; 26–49% of lobe, 3; 50–75% of lobe, 4; and
76–100% of lobe, 5.18 The CT score was calculated by sum-
ming the scores from all 5 lung lobes, with totals ranging
from 0 to 25.
Statistical Analyses
Statistical analyses were performed with SPSS 25.0
(IBM, Armonk, New York). Continuous normally distrib-
uted data are expressed as mean 6 SD, and non-normally distributed data are expressed as median (interquartile
range [IQR]). Comparison between severe and critical
groups was performed with the 2-sample t test or the Mann- Whitney test for continuous variables. Categorical variables
are expressed as percentage (%) and were compared using
the chi-square test or the Fisher exact test. Correlations
between LUS score and CT score and clinical data were
evaluated with the Spearman correlation coefficient. A 2-
tailed P value < .05 was considered statistically significant.
Results
Clinical Characteristics
The clinical characteristics of subjects with severe and
critical COVID-19 are summarized in Table 1. Forty-five
subjects were male, and 51 were female, with ages ranging
from 32 to 97 y (mean 65 6 13 y). The most common clini- cal symptoms were fever and cough. Compared with sub-
jects with severe COVID-19, critically ill subjects were
more likely to be older and had lower SpO2, lower lympho-
cyte count, higher levels of oxygen flow, and higher levels
of D-dimer and B-type natriuretic peptide, as well as higher
incidence of ARDS, acute kidney injury, acute heart injury,
deep vein thrombosis, septic shock, pneumothorax, and mor-
tality. There were no significant differences in gender, body
mass index, body temperature, smokers, C-reactive protein,
erythrocyte sedimentation rate, alanine aminotransferase, se-
rum creatinine, clinical symptoms, and comorbidities
between subjects with severe or critical COVID-19.
LUS Features
The median (IQR) time from the onset of the disease to
LUS measurement in severe and critical subjects was 7 (6–
10) d. All 96 subjects with COVID-19 had LUS abnormal-
ities, which mainly manifested as patterns of B-lines (93 of
96, 96.9%) and different extent of consolidations (80 of 96,
83.3%). In addition, 24 of 96 (25.0%) subjects had a thick-
ened and irregular pleural line. Pleural effusion was found
in 16 of 96 (16.7%) subjects, including 11 cases with a
small amount of effusion and 5 with a large amount of effu-
sion. Of the 96 subjects, 78 (81.3%) had $ 2 abnormal
LUS patterns, while 14 (14.6%) had all abnormal LUS pat-
terns. The LUS characteristics of all 96 subjects with severe
and critical COVID-19 are shown in the supplementary
materials (available at http://www.rcjournal.com). The
LUS features are presented in Figure 1.
The distribution of common LUS features, including B-
lines and consolidation in all lung regions of subjects with
severe and critical COVID-19, are described in Table 2. The
incidences of consolidation in the bilateral lateral lung, pos-
terior lung area, and left anterior-inferior lung of the crit-
ically ill group were higher than those of the severe group
(P < .05 for all). The proportions of B-lines in the left infe- rior-lateral lung (P ¼ .02) and right posterior-superior lung area (P ¼ .005) of the group with severe COVID-19 were higher than those of the group with critical COVID-19.
In addition, 93 (96.9%) subjects had bilateral lung
involvement. The distribution of LUS abnormalities in uni-
lateral or bilateral lung are shown in Table 3. Compared with
the group with severe COVID-19, the group with critical
COVID-19 had a higher proportion of bilateral or unilateral
lung consolidation and pleural effusion (P < .05 for all). Eleven (11.5%) cases underwent serial bedside LUS mea-
surement, and 2 cases progressed from the severe to criti-
cal stage (see the supplementary materials at http://www.
rcjournal.com). One case was a 71-y-old woman with clini-
cally diagnosed severe COVID-19 infection. A bedside LUS
performed on admission showed abnormal B-lines pattern in
all lung regions with no consolidations. On day 30, the subject
suffered from respiratory failure, with an inability to maintain
SpO2 > 90% on high-flow oxygen via mask. When a ventila- tor was needed, the repeat bedside LUS revealed subpleural
consolidations in bilateral lateral and posterior lung regions.
The other confirmed case was a 76-y-old man who was admit-
ted with symptoms of fever (up to 38.7�C), cough, fatigue, and dyspnea. Bedside LUS examination showed multiple B-
lines and right pleural effusion, and no consolidation was
observed. After 28 d of treatment, the subject’s condition had
not improved. A repeat LUS demonstrated increased pleural
effusion, and consolidations had appeared in all lung areas.
LUS and Chest CT Score
The median (IQR) left, right, and bilateral LUS scores
of critical COVID-19 cases were higher than those of
severe COVID-19 cases: left: 14 (12–17) vs 7 (5–12);
right: 14 (10–16) vs 8 (3–12); bilateral: 28 (23–31) vs 15
(8–22) (P < .001 for all) (Fig. 2). In this study, 23 subjects with COVID-19 underwent chest CT scan, with a median
(IQR) CT score of 9 (5–14) and a median (IQR) LUS
score of 12 (8–22). There was a good correlation between
the LUS and CT scores (r ¼ 0.887, P < .001) (Fig. 3A). The clinical and LUS characteristics of these 23 subjects
with COVID-19 are shown in the supplementary materials
(available at http://www.rcjournal.com).
BEDSIDE LUNG ULTRASOUND IN COVID-19
922 RESPIRATORY CARE � JUNE 2021 VOL 66 NO 6
LUS Score and Clinical Data
LUS score had a weak correlation with oxygen flow (r ¼ 0.363, P ¼ .003) and SpO2 (r ¼ –0.340, P ¼ .001) (Fig. 3B, C). However, LUS score was not associated with breathing
frequency (r ¼ 0.244, P ¼ .056).
Discussion
Our results indicate that fever and cough were the most
common clinical symptoms in subjects with severe and criti-
cal COVID-19, which is consistent with prior studies.2,3
Subjects with COVID-19 were also likely to have numerous
Table 1. Clinical Characteristics of Subjects With Severe and Critical COVID-19
Total Severe COVID–19 Critical COVID–19 P
Subjects, n (male/female) 96 (45/51) 63 (25/38) 33 (20/13) .057
Age, y 65.4 6 12.7 63.4 6 12.2 69.2 6 12.7 .031
Body mass index, kg/m2 24.2 6 2.8 24.5 6 3.1 23.8 6 1.9 .29
Body temperature, �C 38.0 (37.5–38.9) 38.0 (37.6–38.8) 38.0 (37.3–39.0) .71 Breathing frequency, breaths/min 20 (19–25) 20 (19–22) 24 (21–27) < .001
Oxygen flow, L/min 5 (3–10) 4 (3–6) 10 (6–40) < .001
SpO2 , % 91 (89–92) 91 (90–92) 89 (88–90) < .001
Smokers 5 (5.2) 2 (3.2) 3 (9.1) .34
Clinical symptoms
Fever 77 (80.2) 51 (81.0) 26 (78.8) .79
Cough 63 (65.6) 43 (68.3) 20 (6.6) .50
Expectoration 28 (29.2) 16 (25.4) 12 (36.4) .35
Dyspnea 23 (24.0) 18 (28.6) 5 (15.2) .21
Shortness of breath 37 (38.5) 22 (34.9) 15 (45.5) .38
Chills 10 (10.4) 7 (11.1) 3 (9.1) > .99
Chest tightness 31 (32.3) 21 (33.3) 10 (30.3) .82
Fatigue 27 (28.1) 20 (31.7) 7 (21.2) .34
Poor appetite 17 (17.7) 12 (19.0) 5 (15.2) .78
Dizzy 7 (7.3) 5 (7.9) 2 (6.1) > .99
Diarrhea 17 (17.7) 14 (22.2) 3 (9.1) .16
Vomit 5 (5.2) 4 (6.3) 1 (3.0) .66
Muscle soreness 13 (13.5) 11 (17.5) 2 (6.1) .21
Laboratory results
Lymphocyte count, �109/L 0.80 (0.55–1.27) 1.00 (0.59–1.40) 0.70 (0.52–1.08) .039 C-reactive protein, mg/L 2.9 (5.2–68.6) 15.1 (4.2–66.8) 37.3 (9.1–71.1) .63
Erythrocyte sedimentation rate, mm/h 49.0 (28.5–76.0) 46.0 (25.0–79.0) 53.0 (38.0–70.0) .40
Alanine aminotransferase, U/L 32.5 (22.8–51.0) 60.0 (21.5–47.5) 33.0 (26.0–64.0) .25
Serum creatinine, mmol/L 65.0 (54.4–80.7) 12.1 (54.0–79.0) 69.0 (55.0–85.0) .41
B-type natriuretic peptide, pg/mL 65.4 (24.0–146.9) 48.4 (14.1–120.1) 108.1 (50.4–263.8) .007
D-dimers, mg/mL 2.2 (0.9–4.8) 1.6 (0.6–4.0) 3.9 (2.1–7.1) < .001
Comorbidities
Cardiovascular disease 51 (53.1) 29 (46.0) 22 (66.7) .08
Diabetes 10 (10.4) 7 (11.1) 3 (9.1) > .99
COPD 7 (7.3) 4 (6.3) 3 (9.1) .69
Pulmonary tuberculosis 2 (2.1) 0 2 (6.1) .12
Malignant tumor 8 (8.3) 5 (7.9) 3 (9.1) > .99
Complications
ARDS 19 (19.8) 2 (6.1) 17 (27.0) < .001
Acute kidney injury 3 (3.1) 0 3 (4.8) .038
Acute heart injury 5 (5.2) 1 (3.0) 4 (6.3) .046
Deep vein thrombosis 21 (21.9) 7 (21.2) 14 (22.2) .001
Septic shock 8 (8.3) 0 8 (12.7) < .001
Pneumothorax 3 (3.1) 0 3 (4.8) .038
Prognosis
Discharge 85 (88.5) 63 (100) 22 (66.7) < .001
Death 11 (11.8) 0 11 (33.3) < .001
Data are presented as n (%), median (interquartile range), or mean 6 SD.
BEDSIDE LUNG ULTRASOUND IN COVID-19
RESPIRATORY CARE � JUNE 2021 VOL 66 NO 6 923
changes in laboratory findings, underlying comorbidities,
and complications, which are also in keeping with previous
studies.2-4 Compared with subjects with severe COVID-19,
critical subjects had lymphopenia, high levels of D-dimer,
higher incidence of complications, and higher mortality.
These findings are similar to those previously observed
A B C
D E F
Fig. 1. Lung ultrasound (LUS) features of subjects with COVID-19. A and B: Multiple hyperechoic B-lines (red arrows) arise from the thickened
and irregular pleural line (white arrows). C: Small consolidation is visualized as local subpleural hypoechoic with irregular boundary. D and E: Air bronchograms (white arrows) are identified by a linear hyperechoic within lung consolidations (red arrows). F: Pleural effusion is observed in the posterior lower lung region.
Table 2. B-Lines and Consolidation in All Lung Regions of Subjects With Severe and Critical COVID-19
Multiple B-Lines Consolidation
Severe
(n ¼ 63) Critical
(n ¼ 33) P Severe
(n ¼ 63) Critical
(n ¼ 33) P
L1 Left anterior-superior lung 32 (50.8) 17 (51.5) > .99 10 (15.9) 10 (30.3) .12
L2 Left anterior-inferior lung 31 (49.2) 18 (54.5) .67 10 (15.9) 13 (39.4) .01
L3 Left superior-lateral lung 33 (52.4) 16 (48.5) .83 13 (2.6) 15 (45.5) .02
L4 Left inferior-lateral lung 32 (50.8) 8 (24.2) .02 18 (28.6) 23 (69.7) < .001
L5 Left posterior-superior lung 19 (30.2) 5 (15.2) .14 30 (47.6) 28 (84.8) < .001
L6 Left posterior-inferior lung 18 (28.6) 4 (12.1) .08 31 (49.2) 29 (87.9) < .001
R1 Right anterior-superior lung 34 (54.0) 21 (63.6) .39 5 (7.9) 8 (24.2) .055
R2 Right anterior-inferior lung 36 (57.1) 19 (57.6) > .99 9 (14.3) 9 (27.3) .17
R3 Right superior-lateral lung 32 (50.8) 10 (30.3) .08 16 (25.4) 20 (6.6) < .001
R4 Right inferior-lateral lung 24 (38.1) 9 (27.3) .37 21 (33.3) 23 (69.7) .001
R5 Right posterior-superior lung 20 (31.7) 2 (6.1) .005 31 (49.2) 31 (93.9) < .001
R6 Right posterior-inferior lung 17 (27.0) 3 (9.1) .06 28 (44.4) 30 (9.9) < .001
Data are presented as n (%).
BEDSIDE LUNG ULTRASOUND IN COVID-19
924 RESPIRATORY CARE � JUNE 2021 VOL 66 NO 6
between ICU and non-ICU subjects with COVID-19.2,4 The
differences in the characteristics of inflammatory markers,
complications, and prognosis between the critical and severe
groups may indicate that critically ill patients are more seri-
ously injured.
In this study, all subjects with severe and critical
COVID-19 had abnormal LUS findings, including B-lines,
consolidations, abnormal pleural lines, and pleural effu-
sions. Fourteen (14.6%) of the 96 subjects had all abnormal
LUS patterns. The different degrees of lung injury and
imbalance of air-liquid ratio results in multiple sonogra-
phic features. In 78 (81.3%) cases, various manifestations
appeared in different lung regions, indicating that varying
degrees of lung involvement can occur at the same time.
In our cohort, the most frequent LUS abnormality was
multiple B-lines, which was detected in 93 (96.9%) subjects.
B-lines are known as ultrasonic artifacts and present as
hyperechoic vertical lines arising from the pleural line and
spreading up to the edge of the screen, relating to the abnor-
mal interlobular septa or alveoli edema.19-21 Various patterns
of B-lines are observed in the inflammatory exudation of
pulmonary interstitium or alveoli. Multiple well-spaced B-
lines and coalescent B-lines reflect pulmonary interstitial
and alveolar edema, respectively. In addition, the second
most common LUS pattern was consolidation, noted in 80
0
5
10
15
20
0
5
10
15
20
0
10
20
30
40
Le ft
LU S
s co
re
R ig
ht L
U S
s co
re
B ila
te ra
l L U
S s
co re
Severe Critical Severe Critical Severe Critical
A B C
Fig. 2. Comparisons of left (A), right (B), and bilateral (C) LUS score between severe and critical COVID-19 cases. P <.001 for each. LUS ¼ lung ultrasound.
0 0
10
10
20
20
30
30
40
LU S
s co
re
r = 0.887 P < .001
0 0
10
20
20
40
30
60
40
0
10
20
30
40
LU S
s co
re
LU S
s co
re
r = 0.363 P = .003
r = −0.340 P = .001
Oxygen flow (L/min)CT score Oxygen saturation (%) 84 86 88 90 92 94
A B C
Fig. 3. Correlations between lung ultrasound (LUS) score and computed tomography (CT) score (A), oxygen flow (B), and oxygen saturation (C).
Table 3. LUS Signs and Scores of Subjects With Severe and Critical
COVID-19
Severe
(n ¼ 63) Critical
(n ¼ 33) P
Left lung
Abnormal pleural line 12 (19.0) 6 (18.2) > .99
Multiple B-lines 59 (93.7) 28 (84.8) .27
Consolidation 39 (61.9) 29 (87.9) .004
Pleural effusion 3 (4.8) 9 (27.3) .003
LUS score 7 (5–12) 14 (12–17) < .001
Right lung
Abnormal pleural line 13 (2.6) 7 (21.2) > .99
Multiple B-lines 57 (9.5) 29 (87.9) .73
Consolidation 40 (63.5) 33 (100.0) < .001
Pleural effusion 3 (4.8) 11 (33.3) < .001
LUS score 8 (3–12) 14 (10–16) < .001
Bilateral lung
Abnormal pleural line 6 (9.5) 4 (12.1) .73
Multiple B-lines 54 (85.7) 27 (81.8) .77
Consolidation 31 (49.2) 30 (9.9) < .001
Pleural effusion 2 (3.1) 8 (24.2) .003
LUS score 15 (8–22) 28 (22–31) < .001
Data are presented as n (%) or median (interquartile range).
LUS ¼ lung ultrasound
BEDSIDE LUNG ULTRASOUND IN COVID-19
RESPIRATORY CARE � JUNE 2021 VOL 66 NO 6 925
(83.3%) subjects with COVID-19 who had various extent of
consolidation, which is caused by loss of air in alveoli, filling
with exudates or even collapsing progressively. The propor-
tion of consolidation in this cohort was higher than that
reported in previous studies.22-24 This discrepancy might be
due to our study population of subjects with severe and criti-
cal COVID-19. Our findings indicate that lung pathology
may evolve to consolidation as the disease progresses to the
severe or critical stages.
The ultrasonic sign of a small consolidation is a local sub-
pleural hypoechoic signal, while a large consolidation has a
characteristic hepatization. Air bronchogram presented with
penetration of gas through the bronchus into consolidation
during inspiration.25 There was no gas between the subpleural
lung consolidation and chest wall, thus providing a good
acoustic window for LUS examination of subjects with
COVID-19. Moreover, we observed that 12 (12.6%) subjects
displayed pleural effusions, which was caused by the accu-
mulation of exudate in the chest with the progress of pneumo-
nia. Until now, limited pathological reports from postmortem
biopsies showed pulmonary edema, diffuse alveolar dam-
age, desquamation of pneumocytes, and hyaline mem-
brane formation in subjects with severe COVID-19.26
The LUS findings of subjects with severe and critical
COVID-19 in this study are in accordance with other
recent pathological results.
In our study, 93 (96.9%) subjects had bilateral lung
involvement. The incidence of bilateral or unilateral lung
consolidation and pleural effusion in the group with critical
COVID-19 was higher than that in the severe group. These
results indicate that lung consolidation and pleural effusion
are more likely to exist in critically ill patients with COVID-
19. The consolidation in critically ill subjects showed a
marked increase in prevalence in most lung regions, including
bilateral lateral lung, bilateral posterior lung area, and left an-
terior-inferior lung. In these regions, the proportion of B-lines
in the left inferior-lateral and right posterior-superior lung
region of the critically ill group was lower than that in the
group with severe COVID-19. These findings might be due
to the progress of the disease, as the ultrasonic signs evolved
from B-lines to consolidation, even with pleural effusion.
In the 11 subjects who had repeat LUS, 2 progressed from
the severe stage to the critical stage; this was accompanied by
changes in the LUS patterns. In these 2 subjects, the major
change of LUS abnormalities at follow-up was the progression
of consolidation. This finding indicates that lung pathology
could develop to consolidation with lesion progression, and
different LUS features may correlate with the severity of the
lung injury in subjects with COVID-19. The changes of LUS
features on repeated LUS suggests that bedside LUS may be a
useful follow-up tool for the serial assessment of lung involve-
ment in subjects with confirmed COVID-19.
The LUS score depends mainly on the involved lung
regions and ultrasonic features, such as B-lines and
consolidation, which can quantify the extent of lung
lesions. In our cohort, the LUS scores of critical COVID-19
cases were higher than those of severe cases. These results
suggest more severe lung injury in critically ill patients, and
the LUS score may reflect the progression of lung lesions.
In addition, we noted a weaker correlation between LUS
score and oxygen flow and oxygen saturation in this study,
which may also indicate that LUS reflects the degree of dis-
ease to some extent. Previous studies have reported good
correlation between the total number of B-lines score and
the high-resolution CT simplified score in subjects with in-
terstitial lung disease.27 Similarly, there was also a strong
correlation between the LUS score and the chest CT score,
which was used as a semi-quantitative approach to assess
the extent and severity of infectious lung disease.27,28 Our
results demonstrate the value of LUS for the assessment of
COVID-19 compared to the use of chest CT, which had
been recommended as the first-line imaging test for identi-
fying pneumonia. In addition, CT imaging studies have
reported that early-stage lung lesions in subjects with
COVID-19 are mainly located peripherally and subpleur-
ally, and the distribution diffuses with the progress of the
disease.17 Because lung ultrasonic signs originate from the
pleura line, the characteristics of subpleural region involve-
ment can improve the accuracy of the LUS examination in
patients with COVID-19.
Our data indicate that lung consolidations are mainly
located in the posterior lung regions, followed by the lateral
and anterior areas, which may be related to the gravity
effect in supine position. It is worth noting that patients
with COVID-19 often take the original supine position for
bedside LUS examinations, and the dorsal lung region had
a greater tendency to be involved with consolidation.
Therefore, patients with COVID-19 need to be assisted in
prone or lateral decubitus positions to fully expose the chest
wall and expand the scope of the scan, which helps compre-
hensively assess the extent of lung injury.
There are several limitations in this study. First, this was
a retrospective analysis, so extrapolation of our results
could be affected by local bias; a prospective study using
LUS would have greater scientific value. Second, because
our center was a designated hospital to treat severe and crit-
ically ill patients with COVID-19 pneumonia in China, we
could not obtain data from milder cases of COVID-19.
Accordingly, our findings may not be applicable to the
entire COVID-19 population. Third, this is a single-center
study and is limited by the small sample size in our hospi-
tal. Therefore, multicenter studies with larger sample sizes
are needed to confirm our findings. Fourth, it is difficult to
detect central lung lesions with LUS without pleural
involvement. Fifth, ultrasonic detection is limited by subcu-
taneous emphysema and the occlusion of scapula.29 Finally,
the good correlation of LUS scores with CT scores noted in
our study may not be generalizable to the larger population
BEDSIDE LUNG ULTRASOUND IN COVID-19
926 RESPIRATORY CARE � JUNE 2021 VOL 66 NO 6
because we only had chest CT information for a small sub-
set of subjects.
Conclusions
Subjects with severe and critical COVID-19 had typical
LUS features, mainly consisting of B-lines and consolidation.
A strong correlation between LUS score and CT score was
observed, suggesting that bedside LUS is a reliable method to
assess and monitor lung injury associated with COVID-19.
REFERENCES
1. Gralinski LE, Menachery VD. Return of the coronavirus: 2019-nCoV.
Viruses 2020;12(2):135.
2. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, et al. Clinical features
of patients infected with 2019 novel coronavirus in Wuhan. Lancet
2020;395(10223):497-506.
3. Chen N, Zhou M, Dong X, Qu J, Gong F, Han Y, et al.
Epidemiological and clinical characteristics of 99 cases of 2019 novel
coronavirus pneumonia in Wuhan, China: a descriptive study. Lancet
2020;395(10223):507-513.
4. Wang D, Hu B, Hu C, Zhu F, Liu X, Zhang J, et al. Clinical characteris-
tics of 138 hospitalized patients with 2019 novel coronavirus-infected
pneumonia in Wuhan, China. JAMA 2020;323(11):1061-1069.
5. Li B, Li X, Wang Y, Han Y, Wang Y, Wang C, et al. Diagnostic value
and key features of computed tomography in coronavirus disease
2019. Emerg Microbes Infect 2020;9(1):787-793.
6. Xu X, Yu C, Qu J, Zhang L, Jiang S, Huang D, et al. Imaging and clin-
ical features of patients with 2019 novel coronavirus SARS-CoV-2.
Eur J Nucl Med Mol Imaging 2020;47(5):1275-1280.
7. Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, et al. Clinical course and risk
factors for mortality of adult inpatients with COVID-19 in Wuhan,
China: a retrospective cohort study. Lancet 2020;395(10229):1054-1062.
8. Gillman LM, Kirkpatrick AW. Portable bedside ultrasound: the visual
stethoscope of the 21st century. Scand J Trauma Resusc Emerg Med
2012;20:18.
9. Islam M, Levitus M, Eisen L, Shiloh AL, Fein D. Lung ultrasound for
the diagnosis and management of acute respiratory failure. Lung
2020;198(1):1-11.
10. Lichtenstein DA. Ultrasound in the management of thoracic disease.
Crit Care Med 2007;35(5 Suppl):S250-S261.
11. Volpicelli G, Elbarbary M, Blaivas M, Lichtenstein DA, Mathis G,
Kirkpatrick AW, et al. International evidence-based recommendations for
point-of-care lung ultrasound. Intensive Care Med 2012;38(4):577-591.
12. National Health Commission of the People’s Republic of China.
Chinese Management Guideline for COVID-19 (Trial Version
3.0). 2020 Available at: http://www.nhc.gov.cn/xcs/yqfkdt/202001/
f492c9153ea9437bb587ce2ffcbee1fa.shtml. Accessed January 23,
2020. 13. Soummer A, Perbet S, Brisson H, Arbelot C, Constantin JM, Lu Q, et al.
Ultrasound assessment of lung aeration loss during a successful weaning
trial predicts postextubation distress. Crit Care Med 2012;40(7):2064-
2072.
14. Bouhemad B, Dransart-Rayé O, Mojoli F, Mongodi S. Lung ultra-
sound for diagnosis and monitoring of ventilator-associated pneumo-
nia. Ann Transl Med 2018;6(21):418.
15. Caltabeloti F, Monsel A, Arbelot C, Brisson H, Lu Q, Gu WJ, et al.
Early fluid loading in acute respiratory distress syndrome with septic
shock deteriorates lung aeration without impairing arterial oxygen-
ation: a lung ultrasound observational study. Crit Care 2014;18(3)R91.
16. Wang G, Ji X, Xu Y, Xiang X. Lung ultrasound: a promising tool to
monitor ventilator-associated pneumonia in critically ill patients. Crit
Care 2016;20(1):320.
17. Shi H, Han X, Jiang N, Cao Y, Alwalid O, Gu J, et al. Radiological
findings from 81 patients with COVID-19 pneumonia in Wuhan,
China: a descriptive study. Lancet Infect Dis 2020;20(4):425-434.
18. Chang YC, Yu CJ, Chang SC, Galvin JR, Liu HM, Hsiao CH, et al.
Pulmonary sequelae in convalescent patients after severe acute
respiratory syndrome: evaluation with thin-section CT. Radiology
2005;236(3):1067-1075.
19. Dietrich CF, Mathis G, Blaivas M, Volpicelli G, Seibel A, Wastl D, et al.
Lung B-line artefacts and their use. J Thorac Dis 2016;8(6):1356-1365.
20. Chiumello D, Mongodi S, Algieri I, Vergani GL, Orlando A, Via G,
et al. Assessment of lung aeration and recruitment by ct scan and ultra-
sound in acute respiratory distress syndrome patients. Crit Care Med
2018;46(11):1761-1768.
21. Ji L, Li Y, Cao C, Lv Q, Xie M. Serial bedside lung ultrasonography
in a critically ill COVID-19 patient. QJM 2020;113(7):491-493.
22. Lomoro P, Verde F, Zerboni F, Simonetti I, Borghi C, Fachinetti C,
et al. COVID-19 pneumonia manifestations at the admission on chest
ultrasound, radiographs, and CT: single-center study and comprehen-
sive radiologic literature review. Eur J Radiol Open 2020;7:100231.
23. Xing C, Li Q, Du H, Kang W, Lian J, Yuan L. Lung ultrasound findings
in patients with COVID-19 pneumonia. Crit Care 2020;24(1):174.
24. Lu W, Zhang S, Chen B, Chen J, Xian J, Lin Y, et al. A clinical study
of noninvasive assessment of lung lesions in patients with coronavi-
rus disease-19 (COVID-19) by bedside ultrasound. Ultraschall Med
2020;41(3):300-307.
25. Lichtenstein D, Mezière G, Seitz J. The dynamic air bronchogram. A
lung ultrasound sign of alveolar consolidation ruling out atelectasis.
Chest 2009;135(6):1421-1425.
26. Xu Z, Shi L, Wang Y, Zhang J, Huang L, Zhang C, et al. Pathological
findings of COVID-19 associated with acute respiratory distress syn-
drome. Lancet Respir Med 2020;8(4):420-422.
27. Man MA, Dantes E, Domokos Hancu B, Bondor CI, Ruscovan A,
Parau A, et al. Correlation between transthoracic lung ultrasound score
and hrct features in patients with interstitial lung diseases. J Clin Med
2019;8(8):1199.
28. Wangkaew S, Euathrongchit J, Wattanawittawas P, Kasitanon N.
Correlation of delta high-resolution computed tomography (HRCT)
score with delta clinical variables in early systemic sclerosis (SSc)
patients. Quant Imaging Med Surg 2016;6(4):381-390.
29. Reissig A, Copetti R. Lung ultrasound in community-acquired pneumo-
nia and in interstitial lung diseases. Respiration 2014;87(3):179-189.
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