The association of lung ultrasound images with COVID‐19 infection in an emergency room cohort

Abstract

Lung ultrasound could facilitate the triage of patients with suspected COVID‐19 infection admitted to the emergency room. We developed a predictive model for COVID‐19 diagnosis based on lung ultrasound and clinical features. We used ultrasound to image the lung bilaterally at two anterior sites, one and two hands below each clavicle, and a posterolateral site that was the posterior transverse continuation from the lower anterior site. We studied 100 patients, 31 of whom had a COVID‐19 positive reverse transcriptase polymerase chain reaction. A positive test was independently associated with: quick sequential organ failure assessment score ≥ 1; ≥ 3 B‐lines at the upper site; consolidation and thickened pleura at the lower site; and thickened pleura line at the posterolateral site. The model discrimination was an area (95%CI) under the receiver operating characteristic curve of 0.82 (0.75‐0.90). The characteristics (95%CI) of the model’s diagnostic threshold, applied to the population from which it was derived, were: sensitivity, 97% (83–100%); specificity, 62% (50–74%); positive predictive value, 54% (41–98%); and negative predictive value, 98% (88–99%). This model may facilitate triage of patients with suspected COVID‐19 infection admitted to the emergency room.

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The association of lung ultrasound images with COVID-19 infection in an emergency room cohort
S. Bar,1 A. Lecourtois,2 M. Diouf,3 E. Goldberg,4 C. Bourbon, 5 E. Arnaud,5 L. Domisse,5 H. Dupont6 and P.
Gosset5
1 Anaesthetist, 4 Resident, 6 Professor, Anaesthesiology and Critical Care Department, 2 Resident, 5 Doctor
of Medicine, Emergency Medicine Department, 3 Biostatistician, Amiens University Hospital, Amiens,
France
Keywords: lung ultrasound, COVID-19, triage.
Short title: Lung ultrasound to diagnose COVID-19
Correspondence to: S. Bar
Email: stephane.bar.sb@gmail.com
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Summary
Lung ultrasound could facilitate the triage of patients with suspected COVID-19 infection admitted to the
emergency room. We developed a predictive model for COVID-19 diagnosis based on lung ultrasound and
clinical features. We used ultrasound to image the lung bilaterally at two anterior sites, one and two
hands below each clavicle, and a posterolateral site that was the posterior transverse continuation from
the lower anterior site. We studied 100 patients, 31 of whom had a COVID-19 positive reverse
transcriptase polymerase chain reaction. A positive test was independently associated with: quick
sequential organ failure assessment score ≥ 1; ≥ 3 B-lines at the upper site; consolidation and thickened
pleura at the lower site; and thickened pleura line at the posterolateral site. The model discrimination was
an area (95%CI) under the receiver operating characteristic curve of 0.82 (0.75-0.90). The characteristics
(95%CI) of the model’s diagnostic threshold, applied to the population from which it was derived, were:
sensitivity, 97% (83–100%); specificity, 62% (50–74%); positive predictive value, 54% (41–98%); and
negative predictive value, 98% (88–99%). This model may facilitate triage of patients with suspected
COVID-19 infection admitted to the emergency room.
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Introduction
The current coronavirus disease 2019 (COVID-19) pandemic is caused by the severe acute respiratory
syndrome coronavirus 2 strain (SARS-CoV-2), with many patients admitted to the emergency room with
suspected COVID-19 infection [1]. The results of RNA reverse transcriptase polymerase chain reaction (RT-
CR) diagnostic oropharyngeal swabs may be unavailable for 48 h after collection [2]. This delay can lead to
unnecessary isolation of many patients that may exceed a hospital’s resources.
Lung ultrasound can contribute to the diagnosis of acute respiratory failure in the emergency
room, for instance the ‘bedside lung ultrasound in emergency’ (BLUE) protocol [3]. Lung ultrasonographic
characteristics of COVID-19 disease have been recently described [4]. Lung ultrasound could facilitate
rapid, simple and reliable triage of patients with suspected COVID-19 infection admitted to the emergency
room and may inform prognosis [5].
We aimed to develop a model for COVID-19 diagnosis in patients presenting to the emergency
room with possible infection, based on the association of lung ultrasound and clinical features with
positive viral swabs. Our secondary objectives were to study the associations between these and
admission to the intensive care unit, respiratory complications, and mortality.
Methods
The University Medical Centre review board approved this prospectively registered observational study,
which we conducted from March to April 2020 and that we report as standard [6]. Participants gave
informed consent. We studied adults admitted to the emergency room whose lungs were imaged with
ultrasound by the emergency physician for suspected COVID-19 infection as part of the BLUE protocol and
who had a SARS-CoV-2 RT-PCR test [3].
We did not study pregnant women or patients unable to give informed consent or patients with
suspected or proven chronic interstitial lung disease. We did not analyse patients whose ultrasound scans
were poor due to an acoustic barrier, for instance pneumothorax or subcutaneous emphysema.
We used a convex array transducer and ultrasound system (C5-2s™ and TE7, Mindray™;
Shenzhen, China) to identify abnormality consistent with possible COVID-19 disease: thickening of the
pleural line with irregularity; B-lines in a variety of patterns, including focal, multifocal, and confluent; and
consolidation in a variety of patterns (Fig. 1a) [4, 7, 8]. The ‘bedside lung ultrasound in emergency’ (BLUE)
protocol interrogates the lung bilaterally at upper and lower anterior sites and at a posterolateral site (Fig.
1b) [9]. We only counted the number of B-lines at the upper and lower sites as they are present in around
25% of healthy subjects elsewhere [8, 10]. The number of B-lines was counted in a short-axis scan
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between two ribs. Two experts who had performed at least 50 lung ultrasound scans interpreted stored
images, unaware of patients’ SARS-CoV-2 RT-PCR status (SB, PG) [11].
We recorded patients’ characteristics, including age, sex, BMI, medical history and medications.
We also recorded heart rate, mean arterial pressure and pulsed oxygen saturation. We calculated the
quick sequential organ failure assessment (qSOFA) score and the Glasgow coma scale, respiratory rate and
systolic arterial pressure [12]. We measured lymphocyte count, C-reactive protein and the ratio of arterial
oxygen partial pressure to inspired fraction oxygen (PaO2/FIO2). The primary outcome was the SARS-CoV-2
RT-PCR result, which we defined as negative if COVID-19 was not detected by two RT-PCRs [13]. The
secondary outcomes were admission to intensive care, respiratory complications (acute respiratory
distress syndrome (ARDS), pulmonary embolism and secondary bacterial infection), and mortality 14 days
after inclusion, recorded by one investigator (AL) who was not informed of lung ultrasound results or
COVID-19 status.
We calculated that we would need 100 patients to have a 80% power to demonstrate an
ultrasound diagnostic accuracy of 18% and 12% for sensitivity and specificity, assuming their true values
to be 50%, at an alpha threshold of 5%, if 30% of patients presenting to the emergency room with
suspected COVID19 had SARS-CoV-2 detected by up to two RT-PCR. We used the Agostino-Pearson test
for normality of data distribution. We used Student's t-test, Mann-Whitney test, chi-square test or Fisher
test, as appropriate. We used logistic regression to model the associations of lung ultrasound and clinical
features with admission to intensive care, respiratory complications and mortality. We constructed a
multivariate logistic model with ultrasound variables that associated with outcome (p < 0.05), constrained
by elastic net penalisation, with the L2 ridge parameter α set to 0.9 and the optimal L1 Lasso parameter λ
determined by 10-fold cross-validation [14, 15]. In this multivariate logistic model, we categorised the
number of B-lines ≥ 3 and < 3 in accordance with the international definition of interstitial syndrome [7].
We used the area under the receiver operating characteristic curve and the highest Youden index to
define model discrimination and diagnostic threshold, respectively. Interobserver agreement between the
two experts concerning qualitative ultrasound signs (signs present or absent) was evaluated using a Kappa
concordance coefficient and agreement on quantitative evaluations (number of B-lines detected at the
upper and lower sites) using an intraclass correlation coefficient. We used R for analyses (Core Team®,
2017, Vienna, Austria).
Results
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We included 100 adults of whom 31 had a positive SARS-CoV-2 RT-PCR (Table 1 and Fig. 2). The qSOFA
score (≥ 1) and four ultrasound signs were independently associated with a positive test (Table 2). The
area (95%CI) under the receiver operating characteristic curve for the multivariate equation was 0.82
(0.75-0.90). The optimal model value for diagnosis was -1.35, recursively characterised (95%CI) in the
derivation population by: sensitivity, 97% (83-100%); specificity, 62% (50-74%); positive predictive value,
54% (41-98%); and negative predictive value, 98% (88-99%).
Nine patients (29%) with a positive SARS-CoV-2 RT-PCR developed ARDS, 6 (19%) developed a
secondary bacterial infection and none developed a pulmonary embolism. The odds ratio (95%CI) for
subsequent ARDS in patients with COVID-19 was independently associated with three variables: > 3 upper
site B-lines, 1.7 (1.3-2.3), p = 0.001; > 3 lower site B-lines, 1.0 (1.0-1.1), p = 0.03; and PaO2/FIO2 ratio, 1.00
(1.00-1.01), p = 0.006. The same variables were associated with admission to the ICU, OR (95%CI): 1.6
(1.2-2.1), p = 0.003; 1.0 (1.0-1.1), p = 0.016; and 1.00 (1.00-1.01], p = 0.02, respectively. No associations
were found between other respiratory complications and lung ultrasound variables.
Six patients (19 %) with a positive SARS-CoV-2 RT-PCR died during the study period. Mortality was
not associated with lung ultrasound variables. The interobserver agreement was good, with a Kappa
concordance coefficient of 0.89 (95% CI [0.67-1.00]). The intraclass correlation coefficient for the
agreement on quantitative evaluations was 0.92 (95% CI [0.81-0.97]).
Discussion
We found that a combination of clinical features and lung ultrasound signs were independently associated
with positive SARS-CoV-2 RT-PCR. Subsequent development of adult respiratory distress syndrome and
ICU admission were also associated with lung ultrasound signs.
Chest computed tomography (CT) imaging has been strongly recommended because it is very
sensitive for detecting early disease [16]. The early stages of COVID-19 infection are characterised by
bilateral ground glass opacification, accompanied by interlobular thickening and consolidation,
predominantly in the peripheral and subpleural middle and lower lobes [17, 18]. However, the
transportation of potentially infectious and unstable patients for CT limits its use [4].
Lung ultrasound has several advantages compared with CT. It is non-irradiating and noninvasive. It
can be learned quickly and its use in the emergency room has generated great interest [7, 19–23]. The
decontamination of the equipment is straightforward [24]. The abnormalities observed on CT are
accompanied by ultrasound signs, which include B-lines that become more extensive with disease
progression, accompanied by pleural thickening and subpleural consolidation [25, 26].
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The signs associated with COVID-19 diagnosis in our model are consistent with other studies [4,
25]. The most common sign was thickening of the pleural line in the inferior and posterolateral sites,
which is indicative of pneumonia or ARDS [7]. Consolidation is common to bacterial pneumonitis and did
not independently associate with COVID-19 diagnosis [7]. Occasional B-lines may indicate chronic changes
and are common to a number of diseases, but at least three lines indicate interstitial syndrome and
greater numbers are associated with disease severity and higher mortality [4, 5, 7, 8, 10, 26–28]. The
qSOFA score is a simplified version of the SOFA score that aims to identify patients more likely to suffer
serious outcomes after infection [12]. Few patients with COVID-19 are haemodynamically compromised,
which may limit its utility [29, 30].
Our study had several limitations. The first was the interpretation of B-lines in the upper chest, as
a diffuse and heterogeneous distribution of B-lines with thickening of the pleura also occurs with chronic
interstitial lung disease, whom we excluded from the study [31]. Lung ultrasound can distinguish between
cardiogenic and non-cardiogenic pulmonary oedema, particularly through careful examination of the
pleura [32, 33]. Lung ultrasound signs are not particularly specific for infections, although the bilateral
distribution of changes in COVID-19 can help differentiate it from influenza and bacterial pneumonias [7,
34, 35]. The performance of our model will be limited in part by the sensitivity of the SARS-CoV-2 RT-PCR
test, which misdiagnoses one quarter of COVID-19 patients as negative, a rate that we tried to reduce by
performing two tests on each patient. It is possible that the performance of a model might be improved
by imaging with ultrasound more lung areas, but any improvement might not justify the additional time
[3, 5, 31, 36].
In conclusion, the association of BLUE protocol lung ultrasound signs and qSOFA with COVID-19
diagnosis could facilitate more effective triage of patients presenting to emergency departments with
suspected COVID-19 infection. This model should be tested on an independent cohort.
Acknowledgements
We retrospectively registered this study, 29 April 2020 (Clinicaltrials.gov, NCT04368338). No competing
interests declared.
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Table 1 Characteristics of 100 patients presenting to the emergency room with possible COVID-19
infection. Values are mean (SD), numbers (proportion) or median (IQR [range]).
SARS-CoV-2 RT-PCR
Characteristic
Positive (n = 31)
Negative (n = 69)
p value
Age; y
66.8 (16.3)
68.7 (16.4)
0.98
Females
20 (65%)
39 (56%)
0.60
BMI; kg.m-2
30.0 (3.19)
26.4 (3.98)
0.06
Medical history
High blood pressure
21 (68%)
36 (52%)
0.22
Coronary heart disease
2 (6%)
13 (19%)
0.19
Smoking
2 (6%)
21 (30%)
0.01
Peripheral arterial disease
2 (6%)
4 (6%)
0.74
Stroke
7 (23%)
9 (13%)
0.36
Diabetes
3 (10%)
7 (10%)
0.77
Dyslipidaemia
10 (32%)
21 (30%)
0.96
Medication
ACE inhibitor
5 (16%)
11 (16%)
0.79
Angiotensin receptor blocker
8 (26%)
10 (15%)
0.28
NSAID
0
1 (1%)
0.68
qSOFA score
1 (0-1 [0-2])
0 (0-1 [0-1])
0.003
Heart rate; min-1
97 (80-115 [70-127])
88 (80-105 [67-134])
0.22
Mean arterial pressure; mmHg
96.0 (12.9)
97.5 (17.4)
0.68
Oxygen saturation; %
95 (93-98 [85-100])
97 (93-99 [82-100])
0.22
Lymphocyte count; 109.l-1
1.5 (1.0-2.1 [0.6-3.6])
2.0 (1.8-2.2 [0.6-3.9])
0.01
C-reactive protein; mg.l-1
118 (71-151 [14-327])
42 (12-125 [0-29])
0.005
PaO2/FiO2
298 (119)
338 (105)
0.12
Chest ultrasound sites
Upper and lower anterior
B lines
6 (2-10 [0-30])
3 (1-7 [0-16])
0.04
Confluent B-lines
3 (10%)
0
0.04
Thickened pleural line
24 (77%)
26 (38%)
< 0.001
Consolidation
17 (54%)
11 (16%)
< 0.001
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Posterolateral
Confluent B-lines
10 (32%)
8 (12%)
0.03
Thickened pleural line
24 (77%)
26 (38%)
< 0.001
Consolidation
18 (58%)
23 (33)
0.04
ACE, angiotensin-converting-enzyme; BLUE, bedside lung ultrasound in emergency; NSAID, nonsteroidal
anti-inflammatory drug; PaO2/FiO2, arterial oxygen partial pressure to fractional inspired oxygen; qSOFA,
quick sequential organ failure assessment; SARS-CoV RT-PCR, severe acute respiratory syndrome
coronavirus 2 reverse transcription polymerase chain reaction
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Table 2 Lung ultrasound characteristics and qSOFA score independently associated with COVID-19.
Variables
Coefficients
Odds ratio (95%CI)
Intercept
-1.95
qSOFA score > 1
0.05
1.05 (1.01-1.10)
Chest ultrasound site findings
Upper sites B lines ≥ 3
0.42
1.52 (1.31-1.79)
Lower sites thickened pleura
0.55
1.73 (1.49-1.98)
Lower sites consolidation
0.87
2.39 (2.07-2.69)
Posterolateral sites thickened pleura
0.68
1.97 (1.72-2.22)
qSOFA, quick sequential organ failure assessment
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Figure 1a Lower anterior chest subpleural consolidation associated with thickened pleura.
Figure 1b The ‘bedside lung ultrasound in emergency’ (BLUE) protocol interrogates three points in each
hemithorax. The two anterior sites are under one (upper) and two (lower) hands placed below each
clavicle. The posterolateral site is the posterior transverse continuation from the lower anterior site,
interrogated as posterior as possible in the supine patient.
Figure 2 Study flow chart detailing complications in case of positive RT-PCR and other aetiologies in case
of negative RT-PCR.
ARDS, acute respiratory distress syndrome; ER, emergency room; ICU, intensive care unit; RT-PCR, reverse
transcription polymerase chain reaction.
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