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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.

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