How to perform lung ultrasound in pregnant women with suspected COVID-19 infection

F Moro1*, D Buonsenso1*, MC Moruzzi1, R Inchingolo2, A Smargiassi2, L Demi3, AR Larici4,5, G

Scambia1,6, A Lanzone1,6, AC Testa1,6

1
Dipartimento Scienze della Salute della Donna, del Bambino e di Sanità Pubblica, Fondazione
Policlinico Universitario Agostino Gemelli, IRCCS, Rome, Italy
2
Dipartimento Scienze Mediche e Chirurgiche, Fondazione Policlinico Universitario Agostino
Gemelli, IRCCS, Rome, Italy
3
Department of Information Engineering and Computer Science, University of Trento, Trento, Italia
4
Dipartimento di Diagnostica per Immagini, Radioterapia Oncologica e Ematologia, Fondazione
Policlinico Universitario Agostino Gemelli, IRCCS, Rome, Italy
5
Dipartimento Universitario di Scienze Radiologiche ed Ematologiche, Università Cattolica del Sacro
Cuore, Rome, Italy
6
Dipartimento Scienze della Vita e Sanità pubblica. Università Cattolica del Sacro Cuore, Rome, Italy

*F.M. and D.B. contributed equally to this work

Running title: lung ultrasound in pregnancy

Keywords: lung ultrasound, pregnancy, COVID-19

Corresponding author
Dr Francesca Moro
Fondazione Policlinico Universitario A. Gemelli, IRCCS, Dipartimento Scienze della Salute della
Donna, del Bambino e di Sanità Pubblica,
L.go A. Gemelli 8, 00168 Rome, Italy
Email: morofrancy@gmail.com

This article has been accepted for publication and undergone full peer review but has not been
through the copyediting, typesetting, pagination and proofreading process which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1002/uog.22028

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Abstract

Under specific circumstances, such as during the current COVID-19 outbreak, pregnant women can
be a target for respiratory infection, and lung examination may be required as part of their clinical
evaluation, ideally avoiding exposure to radiation. We propose a practical approach for
obstetricians/gynecologists to perform lung ultrasound, showing potential applications, semiology
and practical aspects, which should be of particular importance in emergency situations, such as the
current pandemic infection of COVID-19.

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Introduction

Under specific circumstances, such as during the current COVID-19 outbreak, pregnant women can
be a target for respiratory infection, and lung examination may be required as part of their clinical
evaluation, ideally avoiding exposure to radiation1. As such, a radiation-free point-of-care diagnostic
tool, such as lung ultrasound examination, would be particularly useful for assessing the lungs of
pregnant women. It should be borne in mind that lung ultrasound examination has been traditionally
employed by non-radiologists as an adjunctive clinical instrument. Obstetricians/gynecologists
represent a category of clinicians who use ultrasound in their routine practice. From a technical point
of view, examination of the lungs soon after obstetric ultrasound evaluation could be feasible for
obstetricians and gynecologists, if only to ascertain the presence or absence of normality and
determine the need for further specialist care.
The current gold standard for the etiological diagnosis of COVID-19 infection is (real time)
reverse transcription polymerase chain reaction (rRT-PCR) analysis of respiratory tract specimens.
However, this test has a high false-negative rate due to both nasopharyngeal swab sampling error,
which often requires repeat sampling, and viral burden2. Some patients present late for testing, and
can cause spread of the disease because of delay in diagnosis. Imaging tools able to diagnose
pneumonia at an early stage are thus of fundamental importance. Currently, high-resolution computed
tomography (CT) is the main tool for primary diagnosis and evaluation of disease severity in patients
affected by COVID-19 infection3–5. However, use of ultrasound to identify specific sonographic
characteristics that are diagnostic of pneumonia infection has been reported6 (Table 1), as have the
typical ultrasound findings of COVID-19 disease in the lungs of pregnant women 7.
Here we propose, with an accompanying ‘How To’ video (Videoclip S1), a practical approach
for obstetricians/gynecologists to perform lung ultrasound, showing potential applications, semiology
and practical aspects, which should be of particular importance in emergency situations, such as the
current pandemic infection of COVID-19.

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Physical basis of lung ultrasound

Air creates a high and sudden acoustic mismatch with tissue (subcutaneous layers and muscles),
causing reflection of the ultrasound beam, and preventing direct imaging of the pulmonary
parenchyma. In a normally aerated lung, the only detectable structure is the pleura, visualized as a
highly hyperechoic horizontal line (pleural line) (Figure 1). Reflection of the ultrasound beam
determines the appearance of hyperechoic, parallel, horizontal artifacts (‘A-lines’), indicating normal
inflated peripheral lung if combined with ‘sliding’ of the pleural line (see below)8–10. This pattern is
typical of a lung that is devoid of any pathological phenomenon involving the peripheral lung
parenchyma. Indeed, since ultrasound does not penetrate air, lung ultrasound can evaluate only lung
pathology that affects the pleura. Therefore, a lung lesion that is not in contact with the pleura, for
example, a deep cancer nodule, is not detectable by lung ultrasound, which is why this technique is
not appropriate for cancer screening.
When the lung is affected by pathology that is physically comparable with soft tissue, for
example, a consolidated lung during lobar pneumonia, atelectasis or with pleural effusions, it
becomes amenable to sonographic examination, because structures (consolidations, vessels, fluid,
bronchograms) are discernible. In other pathological entities, such as interstitial lung disease, acute
respiratory distress syndrome (ARDS), pulmonary edema and pneumothorax, the lung is still aerated
but it contains a variable amount of water, cells and/or inflammation that alter the acoustic properties
of the lung and generate vertical artifacts (usually called ‘B-lines’, with several different
characteristics).

Lung ultrasound semiology

Normal lung ultrasound pattern: A-lines

When scanning a normal lung, the operator will see the subcutaneous layers and the hyperechoic
horizontal pleural line, a line that, on real-time examination, has horizontal movements synchronized
with the respiratory activity (this movement is called ‘lung sliding’)8,9. The horizontal ‘A-lines’ are
the hallmark of the normal lung (Figure 1). They are the hyperechoic, repetitive reverberations, at
regular intervals, of the pleural line. In between the A-lines, depending on the ultrasound machine,
probes and frequencies used, it is possible to see the ‘mirror’ effect of the acoustic interfaces of the

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structures of the chest wall8-10. When the probe is positioned in the intercostal space, the pleural line
and A-lines are totally visible (Figure 1a). When the probe is positioned longitudinally, the ribs with
their posterior shadowing can be identified, and between the ribs the pleural line and A-lines are
visible (Figure 1b).

Pathological lung ultrasound pattern: B-lines

When the lung loses normal aeration, but is not completely consolidated (as happens in the case of
interstitial lung disease, pulmonary fibrosis, pulmonary edema, lung deflation, lung contusion,
perilesional consolidative areas), it generates different shapes and lengths of vertical artifacts, usually
called B-lines11 (Figure 2). The genesis of these differences is not completely understood, but they
possibly reflect the different shaped and sized acoustic channels generated by altered peripheral air
space in pathological conditions6,12,13. In general, B-lines are visible and not specific to a single
pathology. However, accompanying clinical information can help to distinguish different entities. For
example, the detection of B-lines in a pregnant woman would not be associated with pulmonary
fibrosis or chronic obstructive pulmonary disease, as they are typical pathologies of advanced age.
Cardiogenic pulmonary edema is characterized by regular, laser-like, bright B-lines, particularly
evident bilaterally on the lung bases (due to the gravitational effect on cardiogenic edema) without
spared areas, and the pleural line is regular11. Conversely, in inflammatory lung disease such as viral
pneumonia (including early stages of COVID-19), the pleural line is usually irregular (blurred)
(Figure 3), thickened, and with a characteristic distribution (monofocal or multifocal, patchy or
inhomogeneous involvement, surrounded by spared areas and with no gravitational distribution)11.

Pathological lung pattern: white lung

When the density of the peripheral (subpleural) lung parenchyma is increased (but not to the extent
of that in a consolidative state), as happens in ARDS (including COVID-19-induced ARDS),
ultrasound examination shows a white area (the so-called ‘ultrasonographic white lung’) (Figure 3),
in which no horizontal reverberations (A-lines) nor separated B-lines are visible11.

Pathological lung pattern: consolidation

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During pneumonia or atelectasis, the lung is completely (or almost) collapsed. In these circumstances,
the involved area of the lung loses its air and becomes a solid organ that can be evaluated by
ultrasound in the same way as any other organ (for example, the liver). The consolidation appears as
an irregular hypoechoic area (Figure 4). In pathology such as COVID-19 pneumonia, advanced
ARDS, or bronchiolitis, the lung may present only small subpleural consolidations. In lobar
pneumonia, the consolidation is larger, liver-like and hypoechoic, and may present with dynamic,
tree-like air bronchogram, fluid bronchogram or vessels. Conversely, in the case of atelectasis, there
are static air bronchograms mainly distributed as horizontal lines14.

Pathological lung pattern: pleural effusion

Evaluation of pleural effusion is the traditional target of lung ultrasound examination. Some
obstetricians/gynecologists have experience in detecting effusion during routine clinical practice,
since some pregnancy complications and gynecological cancers can lead to the development of
effusion. In general, pleural effusion can be simple and uniformly anechoic or complicated by the
presence of hyperechoic spots due to blood, pus, fibrin and/or septa15.

Practical points

Machine, probes and settings

Lung ultrasound can be performed with any type of machine, including first-generation ultrasound
machines. Handheld ultrasound scanners, which may be preferred in an emergency situation, may
also be appropriate for this examination, having the advantage of being easier to sterilize and cover16.
Since the lung has not traditionally been considered amenable to ultrasound examination, there are
no lung-specific machines or probes. Different types of probe can be used, including linear, convex
and microconvex. In general, linear probes can be used to evaluate better details of the pleural line
and subpleural space, due to high frequencies and resolution. However, convex probes, routinely used
for gynecological and obstetric examination, can be suitable for lung examination. Similarly, there
are no lung-specific settings. However, it is fundamental to underline some technical aspects: 1) the
focus should be moved to the level corresponding to the adequately zoomed pleural line; 2) gain can

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be reduced in order to increase contrast and highlight the hyperechoic signs (A-lines, B-lines and
white lung); however, when a consolidated lung (for example, in pneumonia) is scanned, gain should
be set to that used for examination of a parenchymatous organ. In general, for specialists starting to
perform lung examination, it is advisable to use the same settings for follow-up examinations of the
same patient in order to be able to compare different images.

Patient positioning
Lung ultrasound can be considered as an ‘extension’ of the obstetric abdominal ultrasound
evaluation17. The ultrasound examiner can simply move the probe from the abdomen to the chest,
scanning the anterior and lateral areas of the thorax. The examination should cover the whole
pulmonary area, from the basal to upper zones of the thorax. Four vertical lines (right mid-axillary
line, right parasternal line, left parasternal line, left mid-axillary line) can be followed in order to
perform a systematic examination. With the patient then in a sitting or lateral position, the posterior
paravertebral surface of the thorax should be scanned, from the basal to upper zones or posterior-
axillary lines according to the patient’s position.

Conclusion

We have proposed a systematic approach for obstetricians/gynecologists to perform lung ultrasound

examination in pregnant women, describing potential applications and semiology and providing
practical points for consideration. Pathological ultrasound patterns are compared to those expected
in a normal lung, with particular emphasis on those more indicative of COVID-19 infection.

ACKNOWLEDGMENTS
We thank Mr Emerson Marinho Pinto and Dr Paola Romeo, Dipartimento Scienze della Salute della
Donna, del Bambino e di Sanità Pubblica, Fondazione Policlinico Universitario Agostino Gemelli,
Rome, Italy, for production of the video.

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References

1) Gargani L, Picano E. The risk of cumulative radiation exposure in chest imaging and the
advantage of bedside ultrasound. Crit Ultrasound J 2015; 7: 4.
2) Hao W, Li M. Clinical diagnostic value of CT imaging in COVID-19 with multiple negative
RT-PCR testing. Travel Med Infect Dis 2020; 13:101627. doi: 10.1016/j.tmaid.2020.101627.
3) Pan Y, Guan H, Zhou S, Wang Y, Li Q, Zhu T, Hu Q, Xia L. Initial CT findings and temporal
changes in patients with the novel coronavirus pneumonia (2019-nCoV): a study of 63
patients in Wuhan, China. Eur Radiol 2020. doi: 10.1007/s00330-020-06731-x.
4) Bernheim A, Mei X, Huang M, Yang Y, Fayad ZA Chest CT Findings in Coronavirus
Disease-19 (COVID-19): Relationship to Duration of Infection. Radiology 2020.
doi.org/10.1148/radiol.2020200463.
5) Zi Yue Zu, Meng Di Jiang, Peng Peng Xu, Wen Chen, Qian Qian Ni, Guang Ming Lu, Long
Jiang Zhang. Coronavirus Disease 2019 (COVID-19): A Perspective from China. Radiology
2020. doi:10.1148/radiol.2020200490.
6) Soldati G, Smargiassi A, Demi L and Inchingolo R. Artifactual Lung Ultrasonography: It Is
a Matter of Traps, Order, and Disorder. Appl. Sci 2020; 10, 1570.
7) Peng QY, Wang XT, Zhang LN; Chinese Critical Care Ultrasound Study Group (CCUSG).
Findings of lung ultrasonography of novel corona virus pneumonia during the 2019-2020
epidemic. Intensive Care Med 2020. doi: 10.1007/s00134-020-05996-6.
8) Volpicelli G. Lung sonography. J Ultrasound Med 2013; 32: 165-71.
9) Gargani L, Volpicelli G. How I do it: lung ultrasound. Cardiovasc Ultrasound 2014; 12: 25.
10) Soldati G, Demi M, Inchingolo R, Smargiassi A, Demi L. On the Physical Basis of Pulmonary
Sonographic Interstitial Syndrome. J Ultrasound Med 2016; 35: 2075-86.
11) Soldati G, Demi M, Smargiassi A, Inchingolo R, Demi L. The role of ultrasound lung artifacts
in the diagnosis of respiratory diseases. Expert Rev Respir Med 2019; 13: 163-172.
12) Demi L, van Hoeve W, van Sloun RJG, Soldati G, Demi M. Determination of a potential
quantitative measure of the state of the lung using lung ultrasound spectroscopy. Sci Rep 2017;
7:12746.

This article is protected by copyright. All rights reserved.

13) Soldati G, Smargiassi A, Inchingolo R, Sher S, Nenna R, Valente S, Inchingolo CD, Corbo
GM. Lung ultrasonography may provide an indirect estimation of lung porosity and airspace
geometry. Respiration 2014; 88: 458-68.

14) Lichtenstein D, Mezière G, Seitz J. The dynamic air bronchogram. A lung ultrasound sign of
alveolar consolidation ruling out atelectasis. Chest 2009; 135: 1421-1425.
15) Brogi E, Gargani L, Bignami E, Barbariol F, Marra A, Forfori F, Vetrugno L. Thoracic
ultrasound for pleural effusion in the intensive care unit: a narrative review from diagnosis to
treatment. Crit Care 2017; 21: 325.
16) Buonsenso D, Pata D, Chiaretti A. Covis-19 outbreak: less stethoscope, more ultrasound.
Lancet Respir Med 2020 (Accept).
17) Inchingolo R, Smargiassi A, Mormile F, Marra R, De Carolis S, Lanzone A, Valente S, Corbo
GM. Look at the lung: can chest ultrasonography be useful in pregnancy? Multidiscip Respir
Med 2014; 9: 32.

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Figure and video legends

Figure 1 Ultrasound images of normal lung. When the probe is positioned in the intercostal space
(A), the pleural line (yellow arrow) is visible with no interruption. An A-line due to the reverberation
of the pleural line is indicated by a white arrow. When the probe is positioned longitudinally (B), ribs
can be recognized (stars) with posterior shadowing, pleural line (yellow arrow) and A-lines (white
arrows).

Figure 2 Ultrasound images show hyperechoic vertical line(s) touching the bottom of the screen,
appearing as a comet (A), multiple thickened hyperechoic lines (B) or short lines arising from the
pleura (C). These lines are called “B-lines” (blue arrows). They are present in interstitial lung disease,
acute respiratory distress syndrome, pulmonary fibrosis, pulmonary edema and perilesional
consolidative areas.

Figure 3 Ultrasound images of a patient with pneumonia infection. Irregular and thickened pleural
line (yellow arrow) and a “white area” (stars) are present. Neither A-lines nor the discrete B-lines are
present.

Figure 4 Ultrasound images of patients with pneumonia infections. The lung periphery is partially
collapsed and the involved area appears as irregular hypoechoic areas (green arrows).

Figure 5 Anatomic landmarks for ultrasound assessment.

Videoclip S1 Video summarizing the basic principles of lung ultrasound, and showing images of
physiology and pathological conditions.

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Table 1 Computed tomographic and ultrasonographic features of COVID-19 pneumonia
Lung high-resolution computed tomography Lung ultrasound
Lung Findings Ground glass opacities B-lines (multifocal, discrete or confluent)
parenchyma Consolidation Sonographic interstitial syndrome
Nodules/micronodules ‘White lung’
‘Crazy paving’ Subpleural consolidation
‘Reversed halo’ sign
Distribution Subpleural Subpleural
Peribronchovascular Not applicable
Patchy/multilobar Patchy
Diffuse Diffuse
Predominantly at the lower lobes Predominantly at the lower lobes
Unilateral/bilateral Unilateral/bilateral

Pleura Smooth thickening Thickened and irregular pleural line

Pleural effusion is rare Pleural effusion is rare

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Table 2 Systematic ultrasound examination of the lung in pregnant patient with COVID-19

Procedure Instructions
1. Location Ultrasound examination should be performed at the patient’s bedside (wireless
devices are preferred in order to minimize the risk of contamination)
2. Patient positioning* Supine, prone, left- and right-sided position
3. Ultrasound equipment and Disinfection of hands and medical devices.
sterilization Appropriate personal protective equipment (PPE) should be worn.
Disinfection of the system with wipes impregnated with citric acid and dilute
solution of sodium chlorite.
Surface of ultrasound machine should be covered by adequate sheaths.
After the examination, both ultrasound machine and probe should be deeply
disinfected.
4. Scanning planes* Examination should be done assessing 14 anatomical landmarks*
5. Ultrasound parameters Pleural line (regular or irregular)
B-lines (sporadic, multiple-confluent)
White lung
Subpleural consolidations (absent, present<1cm, present >1cm)
*Figure 5

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Table 3 Lung ultrasound examination checklist

Anatomic Pleural line Vertical artifacts Subpleural consolidation

landmarks 1. regular 1. sporadic B-lines 1.absent
2. irregular and thickened 2. multiple- 2.present<1cm
confluent B-lines 3.present >1cm
3. white lung
1
2
3
4
5
6
7
8
9
10
11
12
13
14

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Table 4 Assessment of ultrasound patterns in pregnant women, including findings that might be suggestive of COVID pneumonia.

Ultrasound findings Ultrasound images Evaluation

Regular pleural line and sporadic B-lines Normal

Irregular pleural line and sporadic B-lines Suspicious for COVID-19 infection at early
stage if bilateral and patchy

Irregular pleural line and multiple B-lines Indicative of COVID-19 infection at early
stage (very indicative if bilateral and
patchy)

Irregular pleural line and white lung Severe viral pneumonia (especially if
bilateral and patchy)

Irregular pleural line and subpleural More severe viral pneumonia (especially if
consolidations bilateral and patchy)

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Accepted Article

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Accepted Article

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Accepted Article

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Accepted Article

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Accepted Article

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