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The Sound of Air - Point-Of-care Lung Ultrasound in Perioperative Medicine

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The Sound of Air - Point-Of-care Lung Ultrasound in Perioperative Medicine

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© © All Rights Reserved
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Can J Anesth/J Can Anesth

https://doi.org/10.1007/s12630-018-1062-x

REVIEW ARTICLE/BRIEF REVIEW

The sound of air: point-of-care lung ultrasound in perioperative


medicine
Le bruit de l’air : échographie pulmonaire au point d’intervention
en médecine périopératoire
Alberto Goffi, MD . Richelle Kruisselbrink, MD . Giovanni Volpicelli, MD

Received: 19 September 2017 / Revised: 4 December 2017 / Accepted: 7 January 2018


! Canadian Anesthesiologists’ Society 2018

Abstract and chest radiography for the diagnosis and monitoring of


Purpose Lung ultrasound (LUS) has emerged as an many pulmonary and pleural conditions. In this article, we
effective and accurate goal-directed diagnostic tool that review the principles of LUS image acquisition and
can be applied in real time for the bedside assessment of interpretation, summarizing key terms and sonographic
patients with respiratory symptoms and signs. Lung findings.
ultrasound has definite and easily recognized findings Principal findings Although LUS is easy to learn,
and has been shown to outperform physical examination adequate training and performance in an organized
fashion are crucial to its clinical effectiveness and to
prevent harm. Therefore, we review normal LUS findings
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s12630-018-1062-x) contains supple- and propose step-wise approaches to the most common
mentary material, which is available to authorized users. LUS diagnoses, such as pneumothorax, pleural effusion,
interstitial syndrome, and lung consolidation. We highlight
A. Goffi, MD potential pitfalls to avoid and review a recently published
Interdepartmental Division of Critical Care Medicine, University
of Toronto, Toronto, ON, Canada practical algorithm for LUS use in clinical practice.
Conclusions Because of the unique physical properties of
A. Goffi, MD the lungs, only a careful and systematic analysis of both
Division of Respirology (Critical Care), Department of artifacts and anatomical images allows accurate
Medicine, University Health Network, Toronto, ON, Canada
interpretation of sonographic findings. Future studies
A. Goffi, MD exploring the use of software for automatic
Department of Medicine, University of Toronto, Toronto, ON, interpretation, quantitative methods for the assessment of
Canada interstitial syndrome, and continuous monitoring devices
A. Goffi, MD (&) may further simplify and expand the use of this technique at
Toronto Western Hospital, 399 Bathurst Street, 2nd Floor the bedside in acute medicine and the perioperative setting.
McLaughlin Rm 411-H, Toronto, ON M5T 2S8, Canada
e-mail: [email protected] Résumé
R. Kruisselbrink, MD Objectif L’échographie pulmonaire s’est avérée un outil
Department of Anesthesia, University Health Network, Toronto, diagnostique efficace et précis qui peut être appliqué en
ON, Canada temps réel au chevet des patients pour l’évaluation de
signes et symptômes respiratoires. L’échographie
R. Kruisselbrink, MD
Department of Anesthesia, University of Toronto, Toronto, ON, pulmonaire permet des constatations claires et facilement
Canada reconnaissables qui surpassent les résultats de l’examen
physique et de la radiographie du poumon pour le
G. Volpicelli, MD diagnostic et le suivi de nombreuses conditions
Department of Emergency Medicine, San Luigi Gonzaga
University Hospital, Orbassano, Turin, Italy pulmonaires et pleurales. Dans cet article, nous passons

123
A. Goffi et al.

en revue les principes de l’acquisition et de l’interprétation principles of LUS image acquisition and interpretation,
de l’échographie pulmonaire, et résumons les principaux summarizing key terms and sonographic findings and
termes et constatations permises par l’échographie. presenting step-wise approaches to frequent LUS
Constatations principales L’apprentissage de diagnoses. We highlight potential pitfalls to avoid and
l’échographie pulmonaire est aisé, mais une formation review a recently published systematic algorithm for LUS
adéquate et sa réalisation structurée sont les clés de use in clinical practice.
l’efficacité clinique et de la prévention d’un préjudice pour
le patient. Nous examinons donc les constatations d’une
échographie normale et proposons une évaluation par Physical principles of ultrasound
étapes des diagnostics échographiques les plus fréquents,
notamment le pneumothorax, l’épanchement pleural, le In the human body, ultrasound waves propagate in straight
syndrome interstitiel et la consolidation pulmonaire. Nous lines until they encounter a boundary between tissues of
soulignons les écueils éventuels à éviter et analysons un different acoustic impedance. At these boundaries, some
algorithme pratique récemment publié pour l’utilisation de waves are reflected back to the transducer (allowing image
l’échographie pulmonaire en pratique clinique. generation in relation to distance/time from the boundary
Conclusions Compte tenu des caractéristiques physiques and intensity of the reflection), while some travel further
uniques des poumons, seule une analyse soigneuse et until they reach another tissue boundary and are reflected,
systématique des artefacts et des images anatomiques or are completely absorbed by tissues. Two main
permet une interprétation exacte des constatations interactions therefore affect ultrasound image generation:
échographiques. De futures études explorant l’utilisation reflection and attenuation.
de logiciels pour une interprétation automatique, les The intensity of reflection that occurs at a tissue
méthodes quantitatives d’évaluation d’un syndrome interface (e.g., air-fluid; fluid-muscles; air-muscles) is
interstitiel, ainsi que pour les dispositifs de surveillance directly proportional to the difference in acoustic
continue pourront encore simplifier et étendre l’utilisation impedance of the tissues. The degree of attenuation (i.e.,
de cette technique au chevet des patients dans le cadre des gradual loss of intensity due to absorption and scattering)
soins aigus et périopératoires. depends on the conducting medium, with the greatest
attenuation occurring in air and bone. Thus, in normally
aerated lung tissue, ultrasound waves are nearly completely
reflected at the interface between the visceral pleura and
Do we need lung ultrasound? lung tissue, with the few waves traversing the interface
being absorbed almost immediately.
Since its original description 20 years ago,1 lung ultrasound For decades, these physics principles discouraged
(LUS) has emerged as an indispensable goal-directed attempts to use ultrasonography to study the lung.
diagnostic tool that can be applied in real time at the Nevertheless, in the past 20 years many have shown that
bedside for the assessment of patients with respiratory ultrasound can be used for evaluation of the pulmonary
symptoms and signs.2,3 Advantages are striking, as LUS parenchyma.1,6-8,16,17
has been shown to be easy to learn, accurate, and
reproducible because of definite and easily recognized
findings.3-5 In comparative studies, LUS has been shown to Normal lung ultrasound findings
outperform physical examination and chest radiography for
the diagnosis and monitoring of many pulmonary and Because of the unique physical properties of the lungs,
pleural conditions.3,6-14 Availability of new ultrasound their sonographic examination requires systematic analysis
devices, extremely portable but at the same time capable of of both non-anatomical (i.e., artifacts) and anatomical (e.g.,
excellent image quality, has further facilitated the use of visualization of the pleural space and lung parenchyma in
LUS in non-traditional scenarios such as the operating the presence of effusion and consolidation) images.3,4 In
room, emergency department, intensive care unit, pre- normal lungs, when an ultrasound transducer is placed
hospital setting, and other perioperative scenarios. sagittally on the chest wall over any intercostal space
Like other ultrasound applications, LUS performance projecting over aerated lung (e.g., 2nd to 7th), the following
and interpretation are operator dependent.15 Adequate structures and artifacts can be identified: 1) subcutaneous
training and performance in an organized fashion are tissues and intercostal muscles (anatomical image); 2)
crucial to reduce operator dependency, ensure its clinical superior and inferior ribs with posterior acoustic shadowing
effectiveness, and prevent harm from misdiagnosis (falsely (artifact due to near complete reflection of the ultrasound
positive or negative).4 In this article, we review the beam at the calcified bone cortex); 3) a hyperechoic

123
Lung ultrasound in perioperative medicine

homogenous horizontal line at the interface between the (parietal pleura), with lung sliding representing air
pleura and aerated lung tissue, called the pleural line movement during respiration and lung pulse the
(artifact due to near complete reflection of the ultrasound transmission of cardiac contractions through the lung
beam at the aerated lung); 4) hyperechoic horizontal lines (Fig. 1; Video, available as Electronic Supplementary
below the pleural line, regularly spaced at multiples of the Material [ESM]; Online Tutorial at http://pie.med.
distance between the probe and the pleural line, called A utoronto.ca/POCUS/POCUS_content/lungUS.html).
lines (reverberation artifacts generated from the strong In the posterolateral and supradiaphragmatic regions of
reflectivity of the pleural line, with each ultrasound beam normal lung, when a low frequency transducer (typically 5-
travelling several times between the probe and pleura). 2 MHz) is placed at the 8th-9th /9th-10th intercostal spaces,
Moreover, in most lungs, short vertical artifacts (formerly mid-axillary line, in a cephalocaudal orientation and
called Z lines) originating from and moving with the directed posteriorly, the following structures and artifacts
pleural line can be identified. They are thought to represent can be identified: 1) subcutaneous tissues and intercostal
areas of focal increased lung density (i.e., interlobular muscles (anatomical image) and the pleural line (artifact as
septa, microatelectasis) and considered pathologic only explained above); 2) a hyperechoic homogenous curved
when visible on the whole image, from the pleural line to line between the lung and abdomen, representing the
the end of the screen without fading, and present in large diaphragm (anatomical image); 3) abdominal organs: liver/
numbers.18,19 Finally, two normal dynamic LUS findings spleen and potentially kidney (anatomical image); 4) the
can be recognized: lung sliding and lung pulse. These vertebral column with posterior acoustic shadowing
findings are generated by the movement of the lung surface (artifact as explained above). Note that the vertebral
(visceral pleura) with respect to the innermost chest wall column is not visualized above the diaphragm because of

Fig. 1 Normal lung ultrasound findings: anterior and lateral chest. In artifacts (formerly called Z lines) originating from and moving with
normal lungs, when a transducer is placed sagittally on the chest wall the pleural line; 6) two dynamic LUS findings: lung sliding and lung
over any intercostal space projecting over aerated lung (e.g., 2nd to pulse, generated by the movement of the lung surface (visceral
7th), the following structures and artifacts may be identified: 1) pleura) with respect to the innermost chest wall (parietal pleura).
subcutaneous tissues and intercostal muscles; 2) ribs with posterior (Please refer to the article text for a detailed explanation of normal
acoustic shadowing; 3) hyperechoic horizontal pleural line at the anterolateral lung ultrasound findings as well as the Video available
interface between pleura and aerated lung tissue; 4) hyperechoic as Electronic Supplementary Material and Online Tutorial: http://pie.
horizontal A line artifacts below the pleural line at multiples of the med.utoronto.ca/POCUS/POCUS_content/lungUS.html). Images
distance between the probe and the pleural line; 5) short vertical adapted with permission from http://pie.med.utoronto.ca/POCUS

123
A. Goffi et al.

the presence of air causing near complete reflection of the dependent part of the thorax. Therefore, the supine
ultrasound beam. This is referred to as a negative spine position is ideal for pneumothorax detection, where the
sign. In addition, the curtain sign should be observed. At least dependent part of the thorax can be identified
full inspiration, the descent of the lung and diaphragm around the 2nd to 4th intercostal space between the
obscures the liver/spleen previously seen to the right of the parasternal and mid-clavicular lines, an area readily
image and with expiration these organs reappear (Fig. 2; accessible for ultrasound imaging. If the semi-sitting
Video, available as ESM; Online Tutorial at http://pie.med. position is used (e.g., patients in respiratory distress), the
utoronto.ca/POCUS/POCUS_content/lungUS.html). apical regions of the thorax become the least dependent.
Four of the most common and well-studied indications The presence of the clavicles makes this area less
for LUS are the assessments of pneumothorax, pleural accessible for imaging, thus increasing the possibility of
effusion, interstitial syndrome, and alveolar syndrome. We missing a small pneumothorax.4,13,20-22
present step-wise approaches to these conditions below.
Step 2
PROBE SELECTION
Visualization of the pleural line is key. Therefore,
Pneumothorax
although the pleural line is seen with both low- and high-
frequency probes, a high-frequency (typically 13-6
How to… (Fig. 3 and Table; Video, available as ESM;
MHz) linear probe is preferred because of the higher
Online Tutorial at http://pie.med.utoronto.ca/POCUS/
resolution. Nevertheless, in complex scenarios where
POCUS_content/lungUS.html).
several differential diagnoses are considered and a
Step 1 ‘‘whole-body’’ examination is needed, the use of a
PATIENT POSITION low-frequency probe (convex or microconvex, with
Except for rare occasions (e.g., loculated frequency ranging between 5 and 2 MHz) should be
pneumothorax), pleural air collects in the least

Fig. 2 Normal lung ultrasound findings: supradiaphragmatic area. In image and with expiration these organs reappear. 5) Also, a
the posterolateral and supradiaphragmatic regions of normal lung, ‘‘negative’’ spine sign should be observed (bottom right panel B):
when a low-frequency transducer is placed at the 8th-9th /9th-10th in a normally aerated lung the vertebral column is not visualized
intercostal spaces, in a cephalocaudal orientation and directed above the diaphragm because of the presence of air causing near
posteriorly, the following structures and artifacts can be identified: complete reflection of the ultrasound beam. (Please refer to the article
1) hyperechoic homogenous curved line of the diaphragm between text for a detailed explanation of normal supradiaphragmatic lung
the lung artifacts cephalad and abdomen caudad; 2) abdominal ultrasound findings as well as the Video available as Electronic
organs: liver/spleen and potentially kidney; 3) vertebral column with Supplementary Material and Online Tutorial: http://pie.med.utoronto.
posterior acoustic shadowing. 4) The curtain sign should be observed ca/POCUS/POCUS_content/lungUS.html). Images adapted with
(top right panel A): at full inspiration, the descent of the lung and permission from http://pie.med.utoronto.ca/POCUS
diaphragm obscures the liver/spleen previously seen to the right of the

123
Lung ultrasound in perioperative medicine

Fig. 3 Step-by-step approach to lung ultrasound for the diagnosis of Supplementary Material and Online Tutorial: http://pie.med.utoronto.
pneumothorax. Please see the corresponding article text for detailed ca/POCUS/POCUS_content/lungUS.html. Images adapted with per-
explanations of each step as well as the Video available as Electronic mission from http://pie.med.utoronto.ca/POCUS

considered as the first choice. Depth, focus, and gain Step 4


should be adjusted to optimize pleural line visualization. IMAGE INTERPRETATION
The three most useful findings when suspecting a
Step 3
pneumothorax are lung sliding, lung pulse, and vertical
IMAGE ACQUISITION
artifacts. In the case of a pneumothorax, the visceral
The probe should be placed on the anterior chest wall in
pleura is separated from the parietal pleura by intra-
a cephalocaudal orientation to allow visualization of at
pleural air; even a tiny amount of intra-pleural air is
least two ribs with the pleural line between. This
enough to reflect and attenuate all ultrasound waves at the
minimizes the risk of mistaking the rib border for a
level of the parietal pleura. Thus, all underlying lung
non-moving pleural line. The pleural line should be
movements (lung sliding and pulse) and vertical artifacts
visualized at multiple interspaces (2nd to 4th) and from
originating at the surface of the visceral pleura are not
medial to lateral in the presumed least dependent zone of
detectable. In the absence of both pleural movements and
the thorax. Comparison with findings on the contralateral
vertical artifacts, a pneumothorax is highly likely, though
side may facilitate interpretation.

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A. Goffi et al.

Table Key findings and pitfalls in the performance and interpretation of lung ultrasound
Main sonographic findings Pitfalls

PNEUMOTHORAX Absence of lung sliding False- Failure to insonate least dependent zones of thorax
Absence of lung pulse negative Absence of lung point with complete PTX
results
Absence of vertical artifacts Misinterpretation of ‘‘E lines’’ (vertical artifacts
Presence of A lines originating in the subcutaneous tissues in the
context of subcutaneous emphysema) for vertical
± Identification of lung point (only in non-complete
artifacts originating from the pleural line
PTX)
Presence of lung sliding, pulse, and/or vertical
artifacts in the least dependent zones of thorax in
the context of loculated PTX
Small left PTX in the paracardiac area
(misinterpretation of internal thoracic artery
pulsation as a lung pulse)
Misinterpretation of internal thoracic artery pulsation
as a lung pulse
On M-mode, misinterpretation of operator movement
as lung sliding or pulse
Failure to identify lung pulse in the context of severe
bradycardia
False- Absence of lung sliding in conditions where visceral
positive pleura does not slide against parietal pleura (e.g.,
results apnea, inflammatory adherences, over-inflation,
severe bullous disease, decrease in lung
compliance, pleural symphysis, endobronchial
intubation)
Absence of lung pulse when lung aeration is
significantly increased (e.g., bullous disease, over-
inflation/-distension)
Absence of lung sliding, pulse, and vertical artifacts
due to improper position of transducer over rib
Misinterpretation of pericardial movement
(paracardiac area), diaphragm (supradiaphragmatic
area), adhesions, or transition point between
normal lung and lung bulla as lung point
PLEURAL Presence of anechoic (fluid) collection between the False- Failure to insonate most dependent zone of thorax
EFFUSION parietal and visceral pleura negative due to either inadequate depth or failure to
results visualize the spine when patients are in supine or
semi-sitting position
Absent (negative) curtain sign Failure to examine patients in the semi-sitting
Positive spine sign position (may miss small effusions)
Hyperechoic regions of collapsed lung and possibly Failure to identify loculated collections
respiratory movements within these regions (i.e., Failure to differentiate complex hyperechoic
sinusoid sign) collections (e.g., organized hematoma in the
pleural cavity) from lung consolidation
Transudates are mostly anechoic and exudates and False- Failure to differentiate between pleural fluid ABOVE
hemorrhages often contain internal echoes within positive the diaphragm and peritoneal fluid BELOW the
the anechoic effusion; however, significant overlap results diaphragm
is present Absent curtain sign due to other conditions (e.g.,
hemidiaphragmatic paresis, consolidation without
effusion)

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Lung ultrasound in perioperative medicine

Table continued
Main sonographic findings Pitfalls

INTERSTITIAL Absence of A lines False- High positive end-expiratory pressure


SYNDROME Presence of C 3 B lines/intercostal space negative Absence of B lines due to improper position of
results transducer over rib
B line definition: discrete, laser-like, vertical,
hyperechoic artifact that arises from the pleural Absence of B lines due to improper angulation of
line, extends to the bottom of the screen without transducer: transducer must be perpendicular to the
fading, and moves synchronously with lung sliding pleural line for visualization of artifacts (with any
[3] scan either A or B lines should be visualized)
B line density: absolute number of B lines correlates Misinterpretation of B lines as non-pathologic short
with severity/loss of lung aeration: vertical artifacts due to inadequate depth or
B1 pattern: moderate loss of aeration, associated with inadequate far field gain
presence of C 3 well-defined spaced B lines/ Failure to systematically explore the entire chest and
intercostal space to identify focal areas of interstitial syndrome
B2 pattern: severe loss of aeration, associated with False- Misinterpretation of short vertical artifacts as marker
multiple coalescent B lines/intercostal space17,44 positive of increased lung density
Other associated findings: results Misinterpretation of B lines in dependent areas as
B line distribution sign of lung pathology
Gravity-dependent vs -independent pattern Elderly patients (higher number of B lines without
pathology)
Changes in lung sliding and pulse
Misinterpretation of ‘‘E lines’’ (vertical artifacts
Pleural line and subpleural abnormalities
originating in the subcutaneous tissues in the
context of subcutaneous emphysema) for vertical
artifacts originating from the pleural line
ALVEOLAR Poorly echogenic or tissue-like image (hepatisation), False- Failure to systematically explore the entire chest and
SYNDROME originating from the pleural line negative to identify focal areas of alveolar syndrome
Interior border of consolidated lung tissue abutting results Failure to use alternative diagnostic modalities in
aerated lung appears shredded and irregular (shred patients with a high pre-test probability and
sign) negative LUS scan (LUS will not identify
Presence of fluid or air bronchograms consolidations that do not abut the pleural line)
Other associated findings: False- Misinterpretation of liver mirror artifact as marker of
positive increased lung density
Shape
results
Margin
Distribution
Vascularization pattern on Doppler imaging
Only conditions that reach the pleural line can be
identified on LUS
LUS = lung ultrasound; PTX = pneumothorax

not definite. Certain conditions (e.g., severe chronic and vertical artifacts) are more important to ‘‘rule out’’
obstructive pulmonary disease, lung overdistension) can than ‘‘rule in’’ a pneumothorax.7 The presence of any one
generate similar findings and potentially cause false- of them can exclude a pneumothorax in a particular area
positive results. Other conditions generate one of the of insonation. On the other hand, a ‘‘positive’’ finding
findings, but not the others. For example, apnea, airway with a high specificity for confirming a pneumothorax is
obstruction, and endobronchial intubation all result in the lung point.24 A lung point can be visualized in a non-
absent lung sliding. Nevertheless, since the pleural layers complete pneumothorax when the beam insonates the
are still in physical contact, lung pulse and vertical transition between the intra-pleural air and expanded lung
artifacts are still present.23 Unsurprisingly, the absence of adhering to the parietal pleura without interposed air. The
lung sliding alone has very poor specificity for ultrasound image displays the absence of lung sliding,
pneumothorax, with a positive predictive value of only pulse, and vertical artifacts on one side of the image and
22%. Therefore, the three findings (lung pulse, sliding, the presence of any/all of these findings on the other side

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A. Goffi et al.

Fig. 4 Step-by-step approach to lung ultrasound for the diagnosis of Supplementary Material and Online Tutorial: http://pie.med.utoronto.
pleural effusion. Please see the corresponding article text for detailed ca/POCUS/POCUS_content/lungUS.html. Images adapted with per-
explanations of each step as well as the Video available as Electronic mission from http://pie.med.utoronto.ca/POCUS

(Fig. 3 and Video, available as ESM). In a supine patient investigations (e.g., chest radiography or computed
with suspected pneumothorax, the lung point is identified tomography), as the findings may represent a false-
by rotating the probe transversely over an intercostal positive result (Table).
space and sliding laterally and posteriorly. If a lung point
is not found, one possibility is circumferential detachment
of the lung (i.e., complete pneumothorax), a clinical The evidence
emergency that should be treated immediately in case of
hemodynamic and respiratory compromise. In When performed by expert users and the clinical suspicion
stable patients, absence of a lung point does not allow a is high, the diagnostic accuracy of LUS for pneumothorax
definitive diagnosis and should prompt further is superior to chest radiography. In particular, LUS

123
Lung ultrasound in perioperative medicine

Fig. 5 Step-by-step approach to lung ultrasound for the diagnosis of Electronic Supplementary Material and Online Tutorial: http://pie.
interstitial syndrome. Please see the corresponding article text for med.utoronto.ca/POCUS/POCUS_content/lungUS.html. Images
detailed explanations of each step as well as the Video available as adapted with permission from http://pie.med.utoronto.ca/POCUS

sensitivity [79%; 95% confidence interval (CI), 68 to 89%] excellent.13 Note that most of these data are from trauma
has been shown to be significantly higher than supine chest and post-procedural studies and may overestimate the
radiography [40% (95% CI, 29 to 50%)], whereas LUS diagnostic performance of LUS in other settings (e.g.,
specificity [98% (95% CI, 97 to 99%)] and radiography inability to lie supine; pre-existent lung conditions such as
specificity [99% (95% CI, 98 to 100%)] are equally bullous disease and emphysema).

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A. Goffi et al.

Fig. 6 Step-by-step approach to lung ultrasound for the diagnosis of Electronic Supplementary Material and Online Tutorial: http://pie.
alveolar syndrome. Please see the corresponding article text for med.utoronto.ca/POCUS/POCUS_content/lungUS.html. Images
detailed explanations of each step as well as the Video available as adapted with permission from http://pie.med.utoronto.ca/POCUS

Pleural effusion most dependent area is the posterior costophrenic angle.


For small effusions, the semi-sitting position maximizes
How to… (Fig. 4 and Table; Video, available as ESM; the effect of gravity and thereby the sensitivity of the
Online Tutorial at http://pie.med.utoronto.ca/POCUS/ scan. Loculated effusions, by contrast, are usually
POCUS_content/lungUS.html). unaffected by patient positioning.
Step 1 Step 2
PATIENT POSITION PROBE SELECTION
Non-loculated pleural fluid distributes to the most In the supine or semi-sitting position, insonation of the
gravitationally dependent region of the thorax. When posterior costophrenic angle is achieved from the mid-
patients are in the supine or semi-sitting position, the axillary line. A low-frequency (5-1 MHz) microarray,

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Lung ultrasound in perioperative medicine

phased array, or curvilinear probe is required for The evidence


sufficient depth penetration.
A meta-analysis including over 1,500 subjects found LUS
Step 3
to be highly sensitive and specific for the diagnosis of
IMAGE ACQUISITION
pleural effusion with superior diagnostic accuracy to chest
The probe should be placed at the 8th-9th /9th-10th
radiography: LUS sensitivity 94% (95% CI, 88 to 97%)
intercostal spaces, mid-axillary line, in a cephalocaudal
and specificity 98% (95% CI, 92 to 100%) compared with
orientation with slight counterclockwise rotation to
chest radiography sensitivity 51% (95% CI, 33 to 68%) and
allow the beam to penetrate an intercostal space. The
specificity 91% (95% CI, 68 to 98%).29 The evidence is
probe should be directed posteriorly towards the
also supportive of using LUS to guide thoracentesis,
vertebral column to ensure visualization of the most
suggesting a lower complication rate, especially regarding
gravity-dependent portion of the pleural space. The
the occurrence of pneumothorax.30,31
image should display the lung artifact and diaphragm to
the left with the liver/spleen, vertebral column, and
potentially the kidney to the right. Visualization of the B lines and interstitial syndrome
spine and kidney provides confirmation that the beam is
interrogating the most dependent region of the thoracic When the lung tissue increases in density, whether
cavity ensuring that small effusions will not be missed.25 because of increased lung weight (e.g., increased
The probe should be held still while the patient inspires extravascular lung water, deposition of collagen and
to assess for the curtain sign. Should pleural fluid be fibrotic tissue, accumulation of blood, lipids, pus, or
seen, the probe is angled anteriorly and slid cranially to proteins) or lung de-aeration (i.e., atelectasis), it no
evaluate its full extent. longer acts as a strong homogenous acoustic reflector but
Step 4 rather behaves as a heterogeneous surface, characterized
IMAGE INTERPRETATION by areas where acoustic impedance is similar to soft
Pleural effusions create several distinct findings at the tissue intercalated with areas where residual air still
costophrenic angle. First, pleural fluid creates an causes a strong acoustic interface.19 On LUS this
anechoic region above the diaphragm between the increased tissue-air ratio is associated with the
visceral and parietal pleura, the region formerly appearance of sonographic artifacts called B lines,
occupied by the lung. Within the fluid, one may see defined as ‘‘laser-like, vertical, hyperechoic artifacts
hyperechoic regions of collapsed lung and possibly that arise from the pleural line, extend to the bottom
respiratory movements within these regions (i.e., of the screen without fading, and move synchronously
sinusoid sign).3 Second, the curtain sign is absent: the with lung sliding’’.1,3,7 B lines are extremely dynamic,
lung artifacts and diaphragm do not descend with with their appearance and resolution detectable in real
inspiration and the abdominal organs remain visible time as lung density changes.14,32,33 They appear very
throughout. Third, a spine sign is present. Due to the early in the course of interstitial involvement in lung
presence of fluid, the spine is visualized above as well as diseases, even before radiographic changes or evidence
below the diaphragm because the fluid conducts the of gas exchange deterioration.1,34,35
ultrasound beam deeper. With regard to distinguishing How to… (Fig. 5 and Table; Video, available as ESM;
between types of pleural effusions (i.e., transudates, Online Tutorial at http://pie.med.utoronto.ca/POCUS/
exudates, hemothoraces, or empyemas), LUS is limited. POCUS_content/lungUS.html).
While transudates are mostly anechoic and exudates and Step 1
hemorrhages often contain internal echoes within the PATIENT POSITION AND PROTOCOL
anechoic effusion, there is significant overlap and B lines can be affected by gravity and their distribution
thoracentesis is usually required for a definitive with respect to gravity is important in distinguishing
diagnosis.3 Quantitative assessments of effusion size their etiology; thus, it is essential to consider and
have been described26; however, the patient’s respiratory document patient position when performing and
status rather than absolute effusion volume is usually the interpreting LUS in patients with these findings.4,5,7
deciding factor regarding clinical management (e.g., Several scanning protocols have been described, all of
drainage). Finally, LUS should always be considered to which systematically insonate the entire chest
guide thoracentesis; either static (ultrasound-assisted) or bilaterally.3,4,7,17,36 Eight-zone or abbreviated six-zone
dynamic (ultrasound-guided) techniques may be protocols limited to the anterior and lateral chest have
used.27,28

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A. Goffi et al.

been shown to be useful in the emergency department The evidence


population and in critically ill patients with acute severe
respiratory failure.6-8 A 28-zone protocol in the anterior Since the first publication correlating B lines and diseases
and lateral chest has been used in an ambulatory affecting lung interstitium,1 B lines have been consistently
population of patients with chronic heart failure for found to be useful and accurate in the diagnosis and
monitoring interstitial syndrome.37 In the examination of monitoring of several lung conditions including
patients with pulmonary fibrosis, a scanning protocol inflammatory diseases such as acute respiratory distress
that includes the posterior chest is mandatory.38 Finally, syndrome (ARDS),16 lung contusion,46 lung infections,47,48
when the assessment of interstitial syndrome is and connective-tissue disorders/lung fibrosis.49 Further,
combined with the assessment of alveolar syndrome several observational studies and a recent meta-analysis
for monitoring of lung aeration in critically ill patients, a suggest higher accuracy of LUS for the diagnosis of heart
protocol including posterior zones of the chest is failure than routine clinical workup, including chest
recommended17 (see below). radiography and natriuretic peptides.6,8,9,50,51 Repeated
LUS examinations allow monitoring of changes in lung
Step 2
aeration and/or extravascular lung water as a result of
PROBE SELECTION
interventions such as dialysis,14,52 heart failure
Although high-frequency (13-6 MHz) transducers can be
treatment,32,53 changes in positive pressure
used, low-frequency probes (5-1 MHz) are preferred as
ventilation,17,44,45 and whole lung lavage.33 B lines may
the increased depth penetration allows better
also have a prognostic role in heart failure and end-stage
visualization of the vertical extent of B lines and
renal disease.54-56
avoids misclassification of short vertical artifacts.
Step 3
Alveolar syndrome
IMAGE ACQUISITION
As described for pneumothorax, the probe should be
When the lung density increases extensively and the tissue-
held over an intercostal space in a cephalocaudal
air ratio is extremely high (with complete or near-complete
orientation to allow visualization of at least two ribs
disappearance of alveolar air), LUS in the affected area
and the pleural line in between. Gain should be adjusted
will reveal an anatomical tissue-like pattern that has been
to maximize contrast and visualization of the pleural line
termed alveolar syndrome. There are multiple possible
and B lines, if present. The entire chest should be
etiologies of alveolar syndrome including infective
systematically insonated bilaterally using the correct
consolidations, atelectasis, pulmonary infarcts, tumours,
scanning protocol adapted to clinical setting, clinical
and contusions.
question, and patient condition and status.
How to… (Fig. 6; and Table; Video, available as ESM;
Step 4 Online Tutorial at http://pie.med.utoronto.ca/POCUS/
IMAGE INTERPRETATION POCUS_content/lungUS.html).
Three or more B lines in an intercostal space represent a
Step 1
positive region of increased lung density (interstitial
PATIENT POSITION
syndrome).3 The absolute number of B lines correlates
Except for specific conditions (e.g., dynamic changes in
with the severity of the disease and loss of lung
consolidation patterns in the context of prone positioning
aeration.14,39-43 Moderate loss of aeration is associated
for ARDS),57,58 patient position is less crucial for the
with the presence of C three well-defined spaced B
assessment of alveolar syndrome compared with
lines/intercostal space (B1 pattern), while severe loss of
pneumothorax, pleural effusion, and interstitial
lung aeration displays multiple coalescent B lines/
syndrome. Therefore, either supine or semi-sitting
intercostal space (B2 pattern).17,44,45 Although very
positions can be used. Since lung consolidations are
sensitive for increased lung density, B lines lack
often located in the dependent (posterior) zones of the
specificity and have a broad differential diagnosis.19
chest, it can be useful to slightly rotate the patient to the
The clinical context and specific sonographic findings
contralateral side to facilitate insonation of dorsal areas.
(e.g., B line distribution, B line density, gravity-
dependent vs -independent pattern, associated changes Step 2
in lung sliding and pulse, associated pleural line and PROBE SELECTION
subpleural abnormalities, presence of fluid or air Alveolar syndrome can be seen with both low- and high-
bronchograms) can be sought to narrow the differential frequency probes although one type may be preferable
diagnosis and increase specificity.4,6,16,22 depending on the size of the consolidation. For large

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Lung ultrasound in perioperative medicine

consolidations, low-frequency (5-1 MHz) transducers operating characteristic curves (0.901-0.978).


are recommended, since they facilitate better evaluation Nevertheless, one should be cautious in using LUS to
of the extension of the condition,3 whereas for small rule out pneumonia as one of the largest studies of patients
peripheral consolidations and in children, high- with suspected pneumonia (n = 362) found the number of
frequency (13-6 MHz) transducers allow better false-negative results to be significant (7.9%).11 For the
delineation and characterization. diagnosis of pulmonary embolism, another potential
etiology of alveolar syndrome, LUS may show peripheral
Step 3
infarcts, but alone does not have adequate accuracy when
IMAGE ACQUISITION
compared with CT [sensitivity 85% (95% CI, 78 to 90%),
As previously described for interstitial syndrome,
specificity 83% (73 to 90%)].67 Nevertheless, LUS still
assessment for alveolar syndrome should involve
represents a valid alternative diagnostic tool when CT
systematic insonation of the entire chest bilaterally.
cannot be performed or is contraindicated.60 Moreover, an
Nevertheless, if a particular region is clinically
integrated multiorgan approach using focused cardiac,
suspicious (e.g., auscultatory finding, area of pain), the
lung, and venous ultrasonography has been shown to
sonographic assessment may start with that region and
achieve significantly higher diagnostic accuracy for
then progress to the entire lung.3
pulmonary embolism (sensitivity 90%, specificity
Step 4 86.2%).68
IMAGE INTERPRETATION
On LUS, an area affected by alveolar syndrome appears
Putting it all together
as a poorly echogenic or tissue-like image (hepatisation)
arising from the pleural line.3,4 Note that only conditions
In our recently published algorithm4 (Fig. 7), we suggested
reaching the pleural line can be identified on LUS. When
an approach that highlights four key steps in the
alveolar syndrome is present but does not abut the pleural
performance and interpretation of LUS examinations.69
line, LUS can be misleading and give the false impression
The algorithm begins with the indication for the scan.
that alveolar syndrome is absent.4,11 Like interstitial
Since LUS is a useful tool for both diagnostic6,7,70-72 and
syndrome, alveolar syndrome is a non-specific
monitoring purposes,17,56,57 we suggest that it be
sonographic finding in many different lung conditions;
considered in the diagnostic approach to every patient
thus, it is essential to integrate relevant clinical
presenting with unexplained respiratory symptoms or signs
information and other sonographic findings to narrow
or with unclear chest radiography findings.4,6,72 After
the differential diagnosis. Shape, margin, distribution,
formulation of the initial diagnostic hypothesis, optimal
vascularization pattern on Doppler imaging, and presence
image acquisition requires choosing the most appropriate
of air and fluid bronchograms have been shown to assist
patient position, probe, and scanning protocol to maximize
in identifying the etiology.11,59-63
diagnostic accuracy for the suspected pathology. It also
requires careful attention to the ultrasound settings
The evidence (especially gain, depth, and focus adjustments), probe
location and angulation, and final image quality to avoid
Lung ultrasound has been shown to be accurate for the the risk of misinterpretation of findings due to inadequate
diagnosis of alveolar syndrome when compared with acquisition. We suggest initiating the third step,
clinical examination and chest radiography. In a study of interpretation of LUS findings, with assessment of the
patients presenting to the emergency department with pleural line. At this interface, three different patterns can
respiratory symptoms and undergoing computed be observed: 1) A line pattern (marker of normally aerated
tomography (CT), LUS detected alveolar syndrome in 81 lung or intrapleural air); 2) anechoic pattern (indicating the
of the 87 patients with lung consolidation on CT presence of pleural effusion); 3) B line or consolidation
(sensitivity 82.8%; specificity 95.5%). Compared with pattern (marker of increased lung density). An A line
chest radiography, LUS had greater sensitivity (81.4% vs pattern can be associated with the presence or absence of
64.3%) but similar specificity (94.2% vs 90%) for lung pleural line movements (lung sliding and/or pulse) and
consolidation.64 For particular etiologies of alveolar vertical artifacts. Absence of all of these findings is highly
syndrome, the evidence varies. For example, for the suggestive of pneumothorax, while identification of even
diagnosis of pneumonia, systematic reviews and meta- one of them immediately rules out pneumothorax. An A
analyses65,66 found LUS sensitivity and specificity to range line pattern associated with pleural line movements
between 85-93% and 72-93%, respectively, with excellent indicates normal lung density immediately below the
pooled diagnostic odds ratios (151.2-173.6) and receiver- visceral pleura; this is seen in normal lung but also in

123
A. Goffi et al.

pathologies not necessarily visible on LUS (e.g., lung posteriorly, or only in part of these zones, when clinically
overinflation, pathologies not reaching the pleural line, indicated.3,4,17 Ultrasound findings can vary at different
early stages of lung disease, pulmonary vascular diseases). locations (e.g., pleural effusion at the level of supra-
As previously discussed, identification of an anechoic diaphragmatic regions and B lines in the anterior, non-
pattern indicates fluid beneath the pleural line while a B dependent zones) and integration of findings from all zones
line pattern or lung consolidation is suggestive of increased is essential in the generation of an ultrasonographic
lung density.3,16,73-76 The process of acquisition and differential diagnosis. Further, consideration of other
interpretation should always be repeated in multiple point-of-care applications (e.g., focused cardiac
zones of the chest, in a systematic approach that ultrasound, vascular ultrasound, diaphragmatic and
insonates the lungs bilaterally, anteriorly, laterally, and abdominal ultrasound) can be made when needed (e.g.,

123
Lung ultrasound in perioperative medicine

b Fig. 7 Clinical algorithm for the performance and interpretation of arthroscopy. Immediately following block insertion, the
lung ultrasound. Please see the corresponding article text for a patient reports shortness of breath and chest pain. There
detailed step-wise explanation of each step of the algorithm. In this
algorithm four key steps in the performance and interpretation of LUS are distant breath sounds on the left side. On LUS, lung
examinations are described. 1) INDICATION for the scan. We sliding, lung pulse, and vertical artifacts are all absent
suggest considering LUS in the diagnostic approach to every patient over the anterior left hemithorax and a lung point is
presenting with unexplained respiratory symptoms or signs or with detected more laterally. Together with the clinical
unclear chest radiography findings. 2) ACQUISITION. After
formulation of the initial diagnostic hypothesis, optimal image history and examination, these sonographic findings are
acquisition requires choosing the most appropriate patient position, decisive for the diagnosis of a large left pneumothorax
probe, scanning protocol, and settings (especially gain, depth, and and a pigtail catheter should be inserted for drainage.
focus adjustments), probe location, and angulation. 3)
INTERPRETATION. We suggest initiating interpretation with Patient 2
assessment of the pleural line. Three different patterns can be You have been called to the trauma bay to assist with the
observed: A) A line pattern (i.e., normally aerated lung or intrapleural
management of a 25-yr-old multisystem trauma victim.
air); B) anechoic pattern (i.e., pleural effusion); C) B line or
consolidation pattern (i.e., increased lung density). Ultrasound He was intubated at the scene by paramedics. On
findings can vary at different locations and integration of findings physical examination, there is decreased air entry on the
from all zones is essential in the generation of an ultrasonographic right side. A right-sided subclavian line has been
differential diagnosis. 4) MEDICAL DECISION-MAKING. Lung
inserted. On LUS, lung sliding is not identified but
ultrasound is only one piece of the diagnostic puzzle, and the
sonographic findings must be integrated with the clinical context and both lung pulse and several vertical artifacts can be seen
results of other available tests. ABG = arterial blood gas; ARDS = on the anterior right hemithorax. Left endobronchial
acute respiratory distress syndrome; COPD = chronic obstructive intubation is suspected and the endotracheal tube is
pulmonary disease; ECG = electrocardiogram; ILDs = interstitial lung
withdrawn a few centimetres. New LUS post-
diseases; PEEP = positive end-expiratory pressure; LUS = lung
ultrasound; PTX = pneumothorax. Image reproduced with permission endotracheal tube withdrawal shows reappearance of
from Wolters Kluwer: Kruisselbrink R, Chan V, Cibinel GA, lung sliding on the right, confirming the diagnostic
Abrahamson S, Goffi A. I-AIM (indication, acquisition, hypothesis.
interpretation, medical decision-making) framework for point-of-
care lung ultrasound. Anesthesiology 2017; 127: 568-82.4 Patient 3
Promotional and commercial use of the material in print, digital, or You are working in the intensive care unit. A 39-yr-old
mobile device format is prohibited without the permission from the
publisher Wolters Kluver. Please contact healthpermissions@
patient with out-of-hospital cardiac arrest has developed
wolterskluver.com for further information severe ARDS. A chest radiograph shows diffuse bilateral
airspace disease. Lung ultrasound confirms the presence
of severe diffuse bilateral interstitial syndrome but also
examination of the left ventricle in the context of finding shows bilateral dense consolidations with dynamic air
homogenous, gravity-dependent, bilateral B line artifacts in bronchograms. A lung recruitment maneuver is
the pulmonary parenchyma, likely secondary to cardiac attempted and the positive end-expiratory pressure is
dysfunction; or examination of the veins of lower increased to 20 cmH2O. Oxygenation and lung
extremities in the context of dyspnea and normal lung compliance significantly improve and repeated LUS
examination/small peripheral consolidations, in a patient shows near complete resolution of the dependent
with risk factors for pulmonary edema/deep vein consolidations.
thrombosis). Finally, for medical decision-making,
remember that LUS is only one piece of the diagnostic
puzzle, and the sonographic findings must be integrated Conclusion
with the clinical context and results of other available
tests.4 Since the original publication demonstrating a role for LUS
in the evaluation of the pulmonary parenchyma, many
Three patients studies have shown its utility in multiple respiratory
conditions. Because of the unique physical properties of
Having reviewed the principles of LUS image acquisition the lungs, only a careful and systematic analysis of both
and interpretation, we can now apply LUS to three patients artifacts and anatomical images allows accurate
with dyspnea and/or respiratory failure. interpretation of sonographic findings. Future studies
exploring the use of software for automatic interpretation,
Patient 1 quantitative methods for the assessment of interstitial
You have just performed a left supraclavicular brachial syndrome, and continuous monitoring devices may further
plexus block for a patient scheduled to undergo left wrist

123
A. Goffi et al.

simplify and expand the use of this technique at the bedside extravascular lung water. J Am Soc Echocardiogr 2006; 19:
in acute medicine and the perioperative setting. 356-63.
13. Alrajab S, Youssef AM, Akkus NI, Caldito G. Pleural
ultrasonography versus chest radiography for the diagnosis of
Acknowledgements We would like to thank Jean YiChun Lin, pneumothorax: review of the literature and meta-analysis. Crit
Gordon Tait, and Massimiliano Meineri from the Toronto General Care 2013; 17: R208.
Hospital Department of Anesthesia Perioperative Interactive 14. Noble VE, Murray AF, Capp R, Sylvia-Reardon MH, Steele DJ,
Education (http://pie.med.utoronto.ca/index.htm) for the generous Liteplo A. Ultrasound assessment for extravascular lung water in
sharing of their educational material. patients undergoing hemodialysis. Time course for resolution.
Chest 2009; 135: 1433-9.
Research support Support was provided solely from institutional 15. Brandli L. Benefits of protocol-driven ultrasound exams. Radiol
(University Health Network, Toronto, Canada) and departmental Manag 2007; 29: 56-9.
sources (Department of Anesthesia, University of Toronto and 16. Copetti R, Soldati G, Copetti P. Chest sonography: a useful tool
Interdepartmental Division of Critical Care Medicine, University of to differentiate acute cardiogenic pulmonary edema from acute
Toronto, Toronto, ON, Canada). respiratory distress syndrome. Cardiovasc Ultrasound 2008; 6:
16.
Competing interests None declared. 17. Bouhemad B, Brisson H, Le-Guen M, Arbelot C, Lu Q, Rouby JJ.
Bedside ultrasound assessment of positive end-expiratory
Editorial responsibility This submission was handled by Dr. pressure-induced lung recruitment. Am J Respir Crit Care Med
Steven Backman, Associate Editor, Canadian Journal of Anesthesia. 2011; 183: 341-7.
18. Soldati G, Demi M. The use of lung ultrasound images for the
differential diagnosis of pulmonary and cardiac interstitial
pathology. J Ultrasound 2017; 20: 91-6.
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