Received: 22 September 2020 | Revised: 21 January 2021 | Accepted: 12 February 2021

DOI: 10.1002/ppul.25325

ORIGINAL ARTICLE: COVID 19

Quantitative assessment of COVID‐19 pneumonia in

neonates using lung ultrasound score

Wei Li MD1 | Manli Fu MD, PhD1 | Chao Qian MD1 | Xin Liu MD2 |
Lingkong Zeng MD, PhD2 | Xuehua Peng MD, PhD3 | Yue Hong MD1 |
Huan Zhou MD1 | Li Yuan MD, PhD1

1
Department of Medical Ultrasonics, Wuhan
Children's Hospital (Wuhan Maternal and Abstract
Child Healthcare Hospital), Tongji Medical
Background: Lung ultrasound (LUS) and lung ultrasound score (LUSS) have been
College, Huazhong University of Science and
Technology, Wuhan, China successfully used to diagnose neonatal pneumonia, assess the lesion distribution,
2
Department of Neonatology, Wuhan and quantify the aeration loss. The present study design determines the diagnostic
Children's Hospital (Wuhan Maternal and
Child Healthcare Hospital), Tongji Medical
value of LUSS in the semi‐quantitative assessment of pneumonia in coronavirus
College, Huazhong University of Science and disease 2019 (COVID‐19) neonates.
Technology, Wuhan, China
Methods: Eleven COVID‐19 neonates born to mothers with COVID‐19 infection
3
Department of Radiology, Wuhan Children's
Hospital (Wuhan Maternal and Child and 11 age‐ and gender‐matched controls were retrospectively studied. LUSS was
Healthcare Hospital), Tongji Medical College, acquired by assessing the lesions and aeration loss in 12 lung regions per subject.
Huazhong University of Science and
Technology, Wuhan, China Results: Most of the COVID‐19 newborns presented with mild and atypical symp-
toms, mainly involving respiratory and digestive systems. In the COVID‐19 group, a
Correspondence
total of 132 regions of the lung were examined, 83 regions (62.8%) of which were
Li Yuan, MD, Phd, Department of Medical
Ultrasonics, Wuhan Children's Hospital detected abnormalities by LUS. Compared with controls, COVID‐19 neonates
(Wuhan Maternal and Child Healthcare
showed sparse or confluent B‐lines (83 regions), disappearing A‐lines (83 regions),
Hospital), Tongji Medical College, Huazhong
University of Science and Technology, No. abnormal pleural lines (29 regions), and subpleural consolidations (2 regions). The
100, Hongkong Rd, 430016 Wuhan, China.
LUSS was significantly higher in the COVID‐19 group. In total, 49 regions (37%)
Email: yuanli1206@163.com
were normal, 73 regions (55%) scored 1, and 10 regions (8%) scored 2 by LUSS. All
Funding information the lesions were bilateral, with multiple regions involved. The majority of the lesions
Science and Technology Department of Hubei were located in the bilateral inferior and posterior regions. LUS detected abnorm-
Province, Grant/Award Number:
2019CFC892; Health Commission of Hubei alities in three COVID‐19 neonates with normal radiological performance. The
Province, Grant/Award Number: intra‐observer and inter‐observer reproducibility of LUSS was excellent.
WJ2019Q002; Science Foundation Project of
Hubei Pediatric Union, Grant/Award Number: Conclusions: LUS is a noninvasive, convenient, and sensitive method to assess
HBPASF‐2019‐04 neonatal COVID‐19 pneumonia, and can be used as an alternative to the use of
diagnostic radiography. LUSS provides valuable semi‐quantitative information on
the lesion distribution and severity.

KEYWORDS
COVID‐19, lung ultrasound, neonate, pneumonia

Wei Li and Manli Fu contributed equally to this study.

Pediatric Pulmonology. 2021;56:1419–1426. wileyonlinelibrary.com/journal/ppul © 2021 Wiley Periodicals LLC | 1419

1420 | LI ET AL.

1 | INTRODUCTION SARS‐CoV‐2 real‐time reverse transcription‐polymerase chain

reaction (RT‐PCR) tests (Novel Coronavirus PCR Fluorescence
The outbreak of coronavirus disease 2019 (COVID‐19) has become a Diagnostic Kit; BGI) were conducted using nasopharyngeal swab
pandemic and is severely affecting public health worldwide. The samples. SARS‐CoV‐2 serological antibodies (immunoglobulin M
epidemic is geographically focused in the city of Wuhan, Hubei, [IgM] and IgG) test was detected by magnetic particle chemilumi-
mainland China from January to March 2020. As increasing of new nescence (Yahuilong). All the neonates underwent influenza virus
infections in Wuhan, the number of pregnant women with COVID‐19 tests. Chest X‐ray or CT scan was performed at admission.
had been on the rise. The neonates born to mothers with COVID‐19 The inclusion criteria were: neonates born to mothers with
were quarantined immediately after birth, some of whom were se- COVID‐19; neonates testing positive for SARS‐CoV‐2 real‐time
vere acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) posi- RT‐PCR, or for virus‐specific IgM. The exclusion criteria were neo-
1
tive and developed COVID‐19 pneumonia. Chest computed nates with transient tachypnea of the newborn, with bacterial
tomography (CT) scan is an important diagnostic tool for COVID‐19, pneumonia, with positive influenza virus test, and with concomitant
with specific imaging findings in the pediatric population.2 However, congenital anomalies.
radiation safety concern for the neonates is essential.
Lung ultrasound (LUS) examination is convenient, nonionizing,
and widely used in the assessment or monitoring of patients with 2.2 | LUS and LUSS
infective pneumonia and dyspnea. COVID‐19 lung lesions in children
begin from and are mainly located in the peripheral thoracic area, LUS images were acquired by one doctor with over 5‐year experi-
and most pediatric patients are in the early stage of the disease. ence within 3 days after admission. Pacifier could be used in some
Therefore, LUS has the advantage of detecting COVID‐19 pneumo- uncooperative neonates. LUS was performed in the supine, prone,
nia lesions, and especially becomes essential for COVID‐19 neonates. and decubitus position, using a portable ultrasound system (Mindray
A lung ultrasound score (LUSS)3 is helpful to semi‐quantitatively M9) and a linear array probe with a frequency of 4–12 MHz (L12‐4s).
evaluate regional lung aeration, and has been successfully used in Lung aeration loss can be estimated using a validated score
various pulmonary disease assessments. called the Lung Ultrasound Score. As previously recommended,3 the
The morbidity of COVID‐19 in the pediatric population was low. chest wall was divided into 12 regions (6 regions per hemithorax,
Our hospital was the exclusive children's hospital in Wuhan for Figure 1). We delineated the anterior and posterior axillary lines as
treating COVID‐19. Data regarding the lung lesion distribution and practical landmarks that defined the anterior, lateral, and posterior
aeration loss of COVID‐19 neonates using LUS are rare. Therefore, areas of both lungs, and delineated the nipple line defining the upper
the present study aimed to investigate the ultrasonic features, lung and lower halves. One video clip was obtained for each region. Each
lesion distribution, the severity of aeration loss of neonatal region of interest was extensively examined.
COVID‐19 pneumonia using semi‐quantitative LUSS method. A semi‐quantitative LUSS was proposed for identifying four
progressive stages of lung aeration loss, assigning a score from 0 to
3. See Table 1 and Figure 2 for a detailed description of LUSS.
2 | METHODS LUSS was independently assessed by two experienced reviewers
for inter‐observer reproducibility. Intra‐observer analysis was per-
2.1 | Study population and clinical information formed using the recorded loops 4 weeks after the initial reading was
conducted.
We searched the medical database and retrospectively surveyed all
neonates born to mothers with COVID‐19 (n = 60) in Wuhan
Children's Hospital from January 31 to March 31, 2020. Eleven 2.3 | Statistical analysis
neonates (three males, 3.8 ± 5.2 days) with confirmed SARS‐CoV‐2
infection (COVID‐19 group), as well as 11 age‐ and gender‐matched Statistical analysis was performed using SPSS Version 23.0 (IBM
controls (control group) at the same time, were recruited in this Corp.) and MedCalc Version 16.2.1 (MedCalc Software). Continuous
single‐center retrospective study. The systematic LUS images of the variables were expressed as mean ± standard deviations. Variances
subjects in two groups were properly achieved. were compared through F test. Continuous variables were compared
This study was approved by the Ethics Committee of Wuhan via the independent sample t test. Categorical variables were com-
Children's Hospital (Approval No. 2020R111‐E01). The guardians of pared through the χ2 test.
the neonates agreed to participate in this study. The diagnosis and The inter‐ and intra‐observer reproducibility of LUSS was as-
management of a neonate with or at risk of COVID‐19 were in ac- sessed using Bland–Altman plot, coefficient of variation, Pearson's
cordance with guidelines provided by the National Health Commis- correlation, and intra‐class correlation coefficient (ICC). The coeffi-
sion and the Chinese Perinatal‐Neonatal SARS‐CoV‐2 Committee.4 cient of variation was defined as the standard deviation of differ-
Demographic, epidemiologic, and clinical features were obtained ences between two readings in the percentage of the mean. p < .05
from the Electronic Health Records Sharing System. In addition, were considered statistically significant.
LI ET AL. | 1421

F I G U R E 1 Neonates were placed in supine position (A), lateral position (B), and prone position (C), and the bilateral lungs were divided into
12 lung regions using the anterior axillary line, posterior axillary line, and nipple line [Color figure can be viewed at wileyonlinelibrary.com]

3 | RESULTS 3.2 | LUS and LUSS

3.1 | Clinical information In the COVID‐19 group, there were a total of 132 regions
reviewed and 83 regions (62.8%) with detected abnormities. Each
Demographic characteristics and clinical features of the COVID‐19 patient showed lesions in bilateral lungs and multiple regions.
group and control group were described in Table 2. There were no There were maximal 10 regions, average 7.5 regions involved
differences in demographic characteristics between the two groups. among 12 regions per subject. The majority of detectable ultra-
In the COVID‐19 group, two babies born preterm and nine babies sonic findings were sparse or confluent B‐lines in the non-
born at term. Most of the neonates initially experienced atypical and consolidated regions (83 regions, 62.8%), including sparse
mild symptoms, that is, shortness of breath, vomiting, bucking, and (73 regions, 55.3%) B‐lines and confluent B‐lines (10 regions,
lethargy. Two babies showed low‐grade fever, with the others nor- 7.6%); disappearing A‐lines (83 regions, 62.8%); irregular and
mal. There were two asymptomatic newborns. Radiographic findings interrupted pleural lines (29 regions, 21.9%), small subpleural
commonly showed peripheral ground‐glass opacities (GGO) and consolidations (2 regions, 1.5%), and no pleural effusion in pa-
patch shadows, with nonspecific findings in three babies. Most of the tients. Forty‐nine regions (37%) were normal and scored 0, 73
babies showed elevated creatine kinase myocardial band (CK‐MB) regions (55%) scored 1, 10 regions (8%) scored 2, and no regions
(83.5 ± 39.5 U/L, reference range 24 U/L), with normal echocardio- scored 3. The global LUSS was higher in the COVID‐19 group
graphic results. There were five (45%) neonates with SARS‐CoV‐2 by than that in the control group. The regions with higher scores
nasopharyngeal swabs testing positive, and six neonates with SARS‐ were primarily located in bilateral inferior and posterior regions
CoV‐2 IgM positive. The serum IgM and IgG levels in the COVID‐19 (regions L4, L5, L6, R3, R4, R5, and R6) (Table 3 and Figure 3). LUS
group were 29.5 ± 27.7 AU/ml and 73.9 ± 31.7 AU/ml, respectively. detected abnormalities in 3 COVID‐19 neonates with normal
radiographic imaging.

TABLE 1 Lung Ultrasound Scoring System

3.3 | Intra‐ and inter‐observer reproducibility
Score Ultrasonographic findings of LUSS
Score 0—normal aeration A‐lines presence—max 2 B‐lines
Bland–Alterman plot revealed that the LUSS derived by two readings
Score 1—moderate loss of ≥ 3 well‐spaced B‐lines
aeration
from intra‐ and inter‐observers, were highly consistent (Figure 4).
Both the intra‐ and inter‐observer reproducibility were excellent,
Score 2—severe loss of aeration Confluent B‐lines
with ICCs of 0.930 and 0.854, respectively. Intra‐observer re-
Score 3—complete loss of Tissue‐like pattern producibility of LUSS slightly better than that of inter‐observer
aeration
(Table 4).
1422 | LI ET AL.

F I G U R E 2 Lung ultrasound scoring system (A–D figures displayed ultrasound images of neonates with COVID‐19 pneumonia. Because
there were no COVID‐19 neonates scored 3, so E and F figures displayed ultrasound images of other neonatal pneumonia for demonstration).
(A) Score 0: normal aeration, normal pleural line (triangle), and A‐lines (arrow). (B) Score 1: moderate loss of aeration and ≥3 well‐spaced B‐lines
(arrow). (C) Score 2: severe loss of aeration and confluent B‐lines (arrow). (D) Score 2: severe loss of aeration, confluent B‐lines (arrow), and
small subpleural consolidation (triangle) with interrupted pleural line. (E) Score 3: lung consolidation (arrow) with air‐bronchograms (triangle)
and pleural effusion (star). (F) Score 3: lung consolidation (arrow) with fluid‐bronchograms (triangle) and pleural effusion (star). COVID‐19,
coronavirus disease 2019 [Color figure can be viewed at wileyonlinelibrary.com]

4 | DI SCUSSION pneumonia in 33 neonates born to mothers with COVID‐19. The

clinical data in the present study demonstrated a similar scene, and
The SARS‐CoV‐2 particles enter the airways and lungs, and could most of the COVID‐19 neonates showed mild symptoms, mainly in-
reach the bronchioles and alveoli. Therefore, the lesions are mostly volving respiratory and digestive systems. Meanwhile, transient mild
located in the terminal alveoli and subpleural.5 The pathologic find- myocardial injury may exist in the majority of patients, due to rapid
6
ings of COVID‐19 showed diffuse lesions of the alveoli with mucus CK‐MB recovery and normal cardiac function. However, asympto-
exudation, which caused consolidation of the lung. Infants and chil- matic patients are not uncommon in the pediatric population, some
dren are also considered to be susceptible to SARS‐CoV‐2 infection, of whom show radiologic findings of pneumonia.8 Therefore, it is
and mainly infected from family cluster outbreaks in China.7 Com- important for us to be able to recognize the pediatric COVID‐19
pared with infected adults, infected children experience differently, patients, using medical imaging modalities.9
and most of them appear to bear milder clinical course. Our collea- CT should be a primary diagnostic tool for COVID‐19, with dif-
gue has reported1 that three neonates were identified the COVID‐19 ferent features in the pediatric population when compared to adults.
LI ET AL. | 1423

TABLE 2 Demographic characteristics and clinical features T A B L E 3 Comparison of regional lung ultrasound score between
the COVID‐19 group and the control group
COVID‐19 Control
Variables group (n = 11) group (n = 11) p Lung COVID‐19 Control
region group (n = 11) group (n = 11) P
Males (%) 3 (27.3%) 3 (27.2%) .647
L1 0.18 ± 0.40 0.09 ± 0.30 .557
Age (days) 3.8 ± 5.2 3.5 ± 4.7 .848
L2 0.45 ± 0.50 0.18 ± 0.41 .187
Wt (g) 3050 ± 609 3240 ± 477 .761
L3 0.09 ± 0.30 0 .341
Ht (cm) 50.0 ± 2.0 49.1 ± 2.3 .979
L4 1.00 ± 0.00 0.18 ± 0.41* .000
HR (bpma) 136.4 ± 8.0 136.7 ± 11.0 .356
L5 1.18 ± 0.41 0.27 ± 0.47* .000
R (bpmb) 41.2 ± 7.4 40.3 ± 4.0 .133
L6 1.00 ± 0.63 0.36 ± 0.51* .017
T (°C) 36.5 ± 0.4 36.5 ± 0.5 .687
R1 0.09 ± 0.30 0 .341
RBC (109/L) 3.8 ± 0.6 4.7 ± 1.0* .008
R2 0.36 ± 0.51 0.18 ± 0.41 .362
WBC (1012/L) 9.6 ± 3.7 10.2 ± 2.6 .177
R3 0.64 ± 0.51 0.09 ± 0.30* .007
LYM (109/L) 3.3 ± 1.6 4.5 ± 1.4 .632
R4 0.91 ± 0.30 0.09 ± 0.30* .000
NEU (109/L) 3.6 ± 0.6 5.5 ± 2.5 .849
R5 1.18 ± 0.60 0.27 ± 0.47* .000
hsCPR (mg/L) 1.1 ± 1.0 1.5 ± 0.8 .605
R6 1.27 ± 0.47 0.55 ± 0.52* .003
Note: Variables are expressed as means ± SD.
Abbreviations: HR, heart rate; hsCPR, hypersensitive C‐reactive protein; All regions 8.40 ± 1.70 2.30 ± 1.40* 1.9 × 10−8
Ht, height; LYM, lymphocyte count; NEU, neutrophil count; R, frequency
Note: Variables are expressed as means ± SD.
of respiratory; RBC, red blood cell count; T, temperature; WBC, white
*p < .05 is statistically significant.
blood cell count; Wt, weight.
a
Beats per minute.
b
Breaths per minute.
of chest radiograms and significantly decreased the mean radiation
*p < .05 is statistically significant.
dose.14 In fact, LUS exam during the COVID‐19 outbreak should be
Most children recover in the early stage, and very few of them progress as focused as necessary to obtain diagnostic views,10 but should also
into the advanced and critical stages. Hence, subpleural lesions with be adequate to avoid return to the isolation ward. Each exam should
localized inflammatory infiltration, along with no signs of pleural effu- be tailored to the indication and planned in advance.
sion or lymphadenopathy, are easily detected in most pediatric patients In the current study, LUS presented most lung regions involved,
on chest CT.2,9 Meanwhile, compared to adults, the lesions distribution with the lesions being identified as bilateral and diffuse. Lesions dis-
is less extensive and some atypical GGO appear in children. In the tribution suggested that bilateral inferior and posterior regions were
current investigation, chest CT or X‐ray demonstrated similar non- mostly involved, which were similar to previous CT findings5,9 and the
specific or mild changes in neonates. The peripheral distribution of le- lesion distribution on radiographic images in the present study.
sions makes ultrasound detection relatively easier.10 Abnormalities in B‐lines and A‐lines were the most common signs,
LUS cannot create direct imaging of the pulmonary parenchyma, covering all of the infected regions. There may be a few B‐lines in the
but can be used for the diagnosis through utilizing artifacts produced by lung fields of normal neonates at the age of 3–7 days. The abnormal
different pathological changes. The state of aeration of lung par- visibility of B‐lines, usually accompanied with the disappearance of A‐
enchyma is a measure of its “air/fluid ratio.” This ratio determines the lines, represents fluid accumulation at the alveolar level and lobular
characteristics of the image produced by LUS. All LUS findings de- space, decreased air/liquid ratio, and pulmonary function impairment in
scribed in adults are alike in neonates and children, in both normal and varying degrees. Pulmonary edema, which is a typical sign in neonatal
pathological conditions.11 Given the small size of the neonates' chest, a patients detected by LUS, has been previously reported as one of the
linear probe allows the best visualization of the lungs in most cases, major pathological findings in patients with COVID‐19 pneumonia.6
irrespective of the depth of the main target of the examination. A When confluent B‐lines spread throughout the lung field, the ultra-
number of studies have described the benefits of LUS in the diagnosis sound shows a compact B‐line pattern representing severe pulmonary
of transient tachypnea of the newborn, respiratory distress syndrome, edema, which was not observed in our study due to mildly symptomatic
bronchiolitis in neonates. Compared with chest X‐ray, LUS is valuable in neonatal patients.15 LUS shows a high sensitivity and specificity to
detecting pediatric pneumonia with excellent sensitivity and specificity, detect lung edema throughout B‐line appearance, however, it is chal-
especially companied with lung consolidation.12 However, it can reduce lenging to identify the etiology of edema, that is, cardiogenic, ne-
13
38.8% chest X‐ray usage in the pediatric population. phrogenic, or pneumonia.16 We propose that it could be combined with
Considering children's higher radio‐sensitivity and free radiation other clinical and ultrasonic assessments to give a comprehensive
of this technique, neonates may benefit from LUS. Launching a LUS in judgment of the situation. Subpleural consolidation is another typical
the neonatal intensive care unit (NICU) roughly halved the number sign in neonatal COVID‐19. It indicates that the lung tissue becomes
1424 | LI ET AL.

F I G U R E 3 Comparison of LUSS in different

lung regions between the COVID‐19 group and
the control group. COVID‐19, coronavirus
disease 2019; LUSS, lung ultrasound score [Color
figure can be viewed at wileyonlinelibrary.com]

F I G U R E 4 Bland–Altman plot showing the intra‐observer and inter‐observer agreement on LUSS. LUSS, lung ultrasound score [Color figure
can be viewed at wileyonlinelibrary.com]

non‐aerated, resulting in tissue‐like echotexture. If residual gas or liquid in CT image, and the other was undetectable in X‐ray image. In the
in the bronchi is visible, air bronchogram or fluid bronchogram can be meantime, the abnormal LUS findings detected in patients with normal
presented. In our study, we only observed two small subpleural con- radiography made us believe that LUS is a sensitive diagnostic tool of
solidations, one of which was consistent with a small subpleural nodule neonatal COVID‐19 pneumonia. According to previous research

TABLE 4 Intra‐ and inter‐observer reproducibility of LUSS

Intra‐observer Inter‐observer
CV (%) R (Pearson's) ICC (95% CI) CV (%) R (Pearson's) ICC (95% CI)

LUSS 8.5% 0.931* 0.930 (0.765–0.981) 13.0% 0.844* 0.854 (0.543–0.959)

Abbreviation: LUSS, lung ultrasound score.

*p < .05 is statistically significant.
LI ET AL. | 1425

regarding LUS application in the COVID‐19 pediatric population, when CO N FLI CT O F I N TER E S TS
compared with the gold standard of chest CT, chest X‐ray displays false‐ The authors declare that there are no conflict of interests.
negative results for pulmonary involvement in 75%, whereas for LUS it
is 16.7%.10 Furthermore, LUS findings are more sensitive than chest X‐ A U T H OR C O N T R I B U T I ON S
ray in pediatric patients with COVID‐19 infection, especially in the early Wei Li, Manli Fu, and Li Yuan contributed to the study design, analysis,
stage of the disease and in mild cases.17 interpretation of the results, and draft of the manuscript. Chao Qian and
Since LUS detects the artifacts generated by the accumulation of Yue Hong contributed to the ultrasound image reading and scoring.
fluid, we could rank the artifacts according to the air/liquid ratio and Lingkong Zeng, Huan Zhou, and Xin Liu contributed to the data collec-
create a score reflecting lung aeration. LUSS, a three‐stage classifi- tion, analysis, and interpretation of the results. Xuehua Peng contributed
cation system, could comprehensively and semi‐quantitatively reflect to the radiographic reading and interpretation of the results. All authors
the lung aeration function and disease severity. LUSS is well corre- critically revised the manuscript and approved the final version.
lated with indices of oxygenation in both term and preterm neo-
nates,18 guiding surfactant therapy and weaning ventilator DATA A VAILABILITY STA TEMENT
support. 19
LUSS could assess global and regional lung aeration, and The data that support the findings of this study titled “Quantitative
well correlated with CT quantitative analysis indices20 in ARDS. In assessment of COVID‐19 pneumonia in neonates using lung ultra-
the present study, the global LUSS was obviously higher in the sound score” are available from the corresponding author upon
COVID‐19 group, in consistent with patients' symptoms. Patients reasonable request.
with two lowest scores were asymptomatic. Two patients, in whom
regions scored 2 were more than three regions, presented with ob- OR C ID
vious shortness of breath and digestive symptoms, along with posi- Huan Zhou http://orcid.org/0000-0003-1299-5263
tive chest radiographic findings. The regional score also reflected
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