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\begin{document}

\title{Our Italian Experience Using Lung Ultrasound for Identification, Grading
and Serial Follow-up of Severity of Lung Involvement for Management of
Patients with COVID-19}



\author[1]{Luigi Vetrugno}%
\author[1]{Tiziana Bove}%
\author[1]{Daniele Orso}%
\author[2]{Federico Barbariol}%
\author[2]{Flavio Bassi}%
\author[3]{Enrico Boero}%
\author[4]{Giovanni Ferrari}%
\author[5]{Robert Kong}%
\author[6]{Daniel A. Lichtenstein}%
\affil[1]{Department of Medicine, University of Udine, Italy}%
\affil[2]{University-Hospital of Udine, Italy}%
\affil[3]{Anesthesia and Intensive Care, San Giovanni Bosco Hospital, Torino, Italy}%
\affil[4]{SC Pneumologia ad Indirizzo Semi Intensivo, Azienda Ospedaliera Ordine Mauriziano}%
\affil[5]{Cardiac Anaesthesia \& Intensive Care, Brighton \& Sussex University Hospital, Brighton BN2 5BE United Kingdom}%
\affil[6]{Medical Intensive Care Unit, Hospital Ambroise Paré (AP-HP), Paris-West university, 9 avenue Charles de Gaulle, F-92100, Boulogne (Paris-West), France.}%


\vspace{-1em}



  
  \date{June 18, 2024}


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\selectlanguage{english}
\begin{abstract}
Lung ultrasound (LU) has rapidly become a tool for assessment of
patients stricken by the novel coronavirus 2019 (COVID-19). Over the
past two and a half months (January, February and first half of March
2020) we have used this modality for identification of lung involvement
along with pulmonary severity in patients with suspected or documented
COVID-19 infection. Use of LU has helped us in clinical decision making
and reduced the use of both chest x-rays and computed tomography (CT).%
\end{abstract}%



\sloppy


Published
in~\href{https://onlinelibrary.wiley.com/journal/15408175}{Echocardiography}.
DOI forthcoming.

\par\null

\section*{Authors' contributions}

{\label{800070}}

LV and DO concept, design and drafting the manuscript. TB, FB, EB, FB,
GF critical revision of the manuscript for important intellectual
content. RK and DL critical review and editing the manuscript. All
authors read and approved the final manuscript.

\par\null

\section*{Lung ultrasound}

{\label{266811}}

During this ongoing battle against the novel COVID-19, LU has quickly
been recognized as a tool for diagnosis and monitoring of lung
involvement severity (1).

A normal LU demonstrates what are termed A lines. These are a repetition
of the pleural line at the same distance from skin to the pleural line.
This is indicative of air below the pleural line, corresponding to the
parietal pleura. Lines may be complete or partial (Figure 1, Movie 1).

Demonstration of B lines are described as hyperechoic laser-like
artifacts that resemble a ``comet tail'' (Figure 2). These arise from
the pleural line and move in concert with a sliding lung. The A lines
are generally not present. B1 lines are associated with an interstitial
syndrome and diminished lung aeration. B2 lines are confluent lines
appearing as a ``white lung'' (called also glass-rockets), equivalent to
computed tomography (CT) ground-glass opacities. This suggests a more
severe loss of lung aeration (Movies 2 and 3).

Lung consolidations (C) are associated with hepatization of lung
parenchyma with or without air bronchograms, and suggest major loss of
lung aeration (atelectasis vs. pneumonia) (Movie 4).

We have not identified an ultrasound appearance that would be
pathognomonic of COVID-19 (4).

\section*{Lung ultrasound score}

{\label{748617}}

The lung ultrasound score (LUS) has been shown to be a useful tool in
intensive care (ICU) patients with adult respiratory distress syndrome
(ARDS). We feel this has been of value in assessing severity of lung
involvement with COVID-19 (2-3).

One may perform a topographic analysis of the underlying lung regions
daily without moving the patient. A scan of the three different areas of
the thorax: anterior, lateral, and posterior, and then superior and
inferior segments are performed. Thus, six specific regions for each
lung are defined and categorized by one of four different aeration
patterns.

A point scoring system is employed by region and ultrasound pattern as:
A = 0 point, B1 = 1 point, B2 = 2 points, C = 3 points. Thus, a LUS of 0
is normal, and 36 would be the worst.

LUS score can be used to follow the clinical patient trajectory in which
an increased score means decreased lung aeration, while on the contrary,
a decrease in score means an increase in lung aeration limiting the need
of chest x-ray and CT scan (4).

An experienced sonographer can do this examination within 5 minutes,
while brief training and about 25 supervised exams seem to be sufficient
to achieve a basic ability to perform the study (5). A prior study
showed the impact of LU to affect clinical decisions in up to 50\% of
intensive care unit patients (6).

\section*{Clinical context}

{\label{668239}}

Although a patient's clinical context allows for an improved pre-test
estimate of COVID-19 lung involvement, it appears that LU may serve as a
bedside tool to improve evaluation of lung involvement, and also reduce
the use of chest x-rays and CT (7). In addition, several intensive care
units following central venous line positioning with ultrasound, have
not been routinely obtaining post insertion chest x-rays (8-9).

While the ability of a chest x-ray to discriminate a bacterial pneumonia
from a non-bacterial infection is no more than 60\% (10), LU has a
higher sensitivity (80\%) (11). Specific comparison studies in
critically ill patients regarding viral pneumonia, however, are few
(12).

\section*{Conclusion}

{\label{897334}}

During this pandemic we have used LU in patients suspected or diagnosed
with COVID-19. Application of LUS has allowed for identification of
patients with lung involvement and severity. In addition, serial studies
help us follow for progression or regression of disease.

With the application of LU we have had a noted reduction in use of chest
x-rays and CT scans during this pandemic, helping make care and
management of our patients a little more efficient.

\par\null

\section*{REFERENCES}

{\label{307361}}

\begin{enumerate}
\tightlist
\item
  Peng QY, Wang XT, Zhang LN, Chinese Critical Care Ultrasound Study
  Group (CCUSG). Finding of lung ultrasonography of novel coronavirus
  pneumonia during the 2019-2020 epidemic. Intensive Care Med 2020 Mar
  12. doi: 10.1007/s00134-020-05996-6.
\item
  Man MA, Dantes E, Domokos Hancu B, Bondor CI, Ruscovan A, Parau A,
  Motoc NS, Marc M. Correlation between transthoracic lung ultrasound
  score and HRCT features in patients with interstitial lung diseases. J
  Clin Med 2019; 8 (8). pii: E1199. doi: 10.3390/jcm8081199.
\item
  Zhao Z, Jiang L, Xi X, Jiang Q, Zhu B, Wang M, Xing J, Zhang D.
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\item
  Bouhemad B, Mongodi S, Via Gabriele, Rouquette I. Ultrasound for
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\item
  Rouby JJ, Arbelot C, Gao Y, et al. Training for Lung Ultrasound Score
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  2018. {[}Epub ahead of print{]}.
\item
  Xirouchaki N, Kondili E, Prinianakis G, et al. Impact of lung
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  Intensive Care Med 2014;40:57-65.
\item
  Brogi E, Bignami E, Sidoti A, Shawae M, Gargani L, Vetrugno L, et al.
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  x-rays in the intensive care unit? Cardiovasc Ultrasound 2017; 15:23.
  doi: 10.1186/s12947-017-0113-8.
\item
  Smit JM, Haaksma ME, Lim EHT, Steenvoorden TS, Blans MJ, Bosch. FH et
  al. Ultrasound to detect central venous catheter placement associated
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\item
  Vetrugno L, Bove T, Orso D, Flabio B, Boero E, Ferrari G. Lung
  ultrasound and COVID-19 ``pattern'': not all that glitters today is
  gold tomorrow. J Ultrasound in Med. (Accepted for publication)
\item
  Courtoy I, Lande AE, Turner RB. Accuracy of radiographic
  differentiation of bacterial from nonbacterial pneumonia. Clin Pediatr
  (Phila) 1989; 28(6): 261-264.
\item
  Berce V, Tomazin M, Gorenjak M, Berce T, Lovren\selectlanguage{polish}č\selectlanguage{english}i\selectlanguage{polish}č \selectlanguage{english}B. The usefulness
  of lung ultrasound for the aetiological diagnosis of
  community-acquired pneumonia in children. Sci Rep 2019; 9(1): 17957.
\item
  Testa A, Soldati G, Copetti R, Giannuzzi R, Portale G, Gentiloni
  Silveri N. Early recognition of the 2009 pandemic influenza A (H1N1)
  pneumonia by chest ultrasound. Crit Care 2012; 16(1): R30.
\end{enumerate}

\section*{}

{\label{193378}}

\section*{Figures}

{\label{193378}}\par\null\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure1/Figure1}
\caption{{Lung ultrasound of normal aerated lung. A lines are visible: they are a
repetition of the pleural line at the same distance from skin to pleural
line. This indicates the presence of air below the pleural line (which
corresponds to the parietal pleura). A lines can be complete or partial
(as in this image);
{\label{850490}}%
}}
\end{center}
\end{figure}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Figure2/Figure2}
\caption{{Lung ultrasound of interstitial syndrome, characterized by the presence
of three or more B lines between two ribs. B lines are hyperechoic
laser-like artifacts that resemble a comet tail, arise from the pleural
line and move in concert with lung sliding. A lines are wiped out.
{\label{971017}}%
}}
\end{center}
\end{figure}

\par\null

\section*{Supplemental information}

{\label{569542}}

Movie1: Anterior region with A lines.

\textbf{Hosted file}

\verb`1-movie.avi`  available at \url{https://authorea.com/users/5588/articles/438105-our-italian-experience-using-lung-ultrasound-for-identification-grading-and-serial-follow-up-of-severity-of-lung-involvement-for-management-of-patients-with-covid-19}

\par\null

Movie 2: Posterior region with coalescent B lines.

\textbf{Hosted file}

\verb`2-movie.avi`  available at \url{https://authorea.com/users/5588/articles/438105-our-italian-experience-using-lung-ultrasound-for-identification-grading-and-serial-follow-up-of-severity-of-lung-involvement-for-management-of-patients-with-covid-19}

\par\null

Movie 3: A thickened and disrupted pleural line with B lines.

\textbf{Hosted file}

\verb`3-movie.avi`  available at \url{https://authorea.com/users/5588/articles/438105-our-italian-experience-using-lung-ultrasound-for-identification-grading-and-serial-follow-up-of-severity-of-lung-involvement-for-management-of-patients-with-covid-19}

\par\null

Movie 4: A subpleural consolidation disappearing with inspiration.

\textbf{Hosted file}

\verb`4-movie.avi`  available at \url{https://authorea.com/users/5588/articles/438105-our-italian-experience-using-lung-ultrasound-for-identification-grading-and-serial-follow-up-of-severity-of-lung-involvement-for-management-of-patients-with-covid-19}

\selectlanguage{english}
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\end{document}

