Thoracic Ultrasound [PDF]

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Thoracic Ultrasound

ERS monograph

ERS monograph

Thoracic Ultrasound

Thoracic ultrasound is now considered an essential bedside tool in respiratory medicine. Despite this, several aspects are yet to be studied and assessed, and international consensus remains limited. With this in mind, the Guest Editors of this Monograph have selected a broad range of authors who are recognised experts, represent different specialities and use thoracic ultrasound in different settings. The result is that each chapter not only reflects expert opinion at a single site in Europe, but provides a multidisciplinary and multicentre view. Chapters include: physics and basic principles; techniques and protocols; pneumothorax; pneumonia; lung tumours; the upper abdomen; and thoracic ultrasound in newborns, infants and children.

Edited by Christian B. Laursen, Najib M. Rahman and Giovanni Volpicelli

ERS monograph 79

Print ISSN: 2312-508X Online ISSN: 2312-5098 Print ISBN: 978-1-84984-093-4 Online ISBN: 978-1-84984-094-1 March 2018 €60.00

9 781849 840934

Thoracic Ultrasound Edited by Christian B. Laursen, Najib M. Rahman and Giovanni Volpicelli Editor in Chief Robert Bals

This book is one in a series of ERS Monographs. Each individual issue provides a comprehensive overview of one specific clinical area of respiratory health, communicating information about the most advanced techniques and systems required for its investigation. It provides factual and useful scientific detail, drawing on specific case studies and looking into the diagnosis and management of individual patients. Previously published titles in this series are listed at the back of this Monograph. ERS Monographs are available online at www.erspublications.com and print copies are available from www.ersbookshop.com

Editorial Board: Antonio Anzueto (San Antonio, TX, USA), Leif Bjermer (Lund, Sweden), John R. Hurst (London, UK) and Carlos Robalo Cordeiro (Coimbra, Portugal). Managing Editor: Rachel White European Respiratory Society, 442 Glossop Road, Sheffield, S10 2PX, UK Tel: 44 114 2672860 | E-mail: [email protected] Published by European Respiratory Society ©2018 March 2018 Print ISBN: 978-1-84984-093-4 Online ISBN: 978-1-84984-094-1 Print ISSN: 2312-508X Online ISSN: 2312-5098 Typesetting by Nova Techset Private Limited Printed by Latimer Trend & Co. Ltd All material is copyright to European Respiratory Society. It may not be reproduced in any way including electronic means without the express permission of the company. Statements in the volume reflect the views of the authors, and not necessarily those of the European Respiratory Society, editors or publishers.

ERS monograph

Contents Thoracic Ultrasound

Number 79 March 2018

Preface

ix

Guest Editors

xi

Introduction

xiii

List of abbreviations

xvi

1.

1

Physics and basic principles Stephen Alerhand, Ole Graumann and Bret P. Nelson

2.

Technique and protocols Christian B. Laursen, Jesper R. Davidsen and Fergus Gleeson

3.

Chest wall and parietal pleura

14 31

Maged Hassan and Najib M. Rahman

4.

Pneumothorax Nils Petter Oveland

5.

Pleural effusion Christopher Merrick, Rachelle Asciak, Anthony Edey, Fabien Maldonado and Ioannis Psallidas

6.

Interstitial syndrome Luna Gargani

7.

Pneumonia Gebhard Mathis

8.

9.

43 64

75 87

Pulmonary embolism

102

Lung tumours

115

Giovanni Volpicelli

Christian Görg, Corinna Trenker and Andreas Schuler

10. The diaphragm Giovanni Ferrari, Søren Helbo Skaarup, Francesco Panero and John M. Wrightson

129

11. The upper abdomen Stefan Posth and Ole Graumann

12. The mediastinum Felix J.F. Herth

13. Ultrasound of the neck for airway management Michael S. Kristensen and Wendy H. Teoh

14 Focused cardiac ultrasound Gabriele Via, Anthony Dean, Gabriele Casso, Brian Bridal Løgstrup and Guido Tavazzi

15. Newborns, infants and children Francesco Raimondi, Fiorella Migliaro, Antonietta Giannattasio, Letizia Capasso, Claudia Lucia Piccolo, Margherita Trinci, Vittorio Miele and Stefania Ianniello,

148 161 172 184

206

16. Ultrasound-guided procedures

226

17 Future directions

244

John P. Corcoran, Mark Hew, Fabien Maldonado and Coenraad F.N. Koegelenberg

Christian B. Laursen, Najib M. Rahman and Giovanni Volpicelli

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Preface Robert Bals US techniques are one of the most elegant diagnostic approaches in clinical medicine. In the hands of an experienced investigator, the US machine can provide deep insight into the physiology and pathology of the body. In most cases, US application is fast, radiation-free and does not cause pain. However, the outcome of the US examination depends largely on the capabilities and experience of the investigator. The development of medical US has an interesting history, further discussed in the Guest Ediors’ Introduction [1], with the abdomen and the heart being the major targets in recent decades. US-based diagnostics have also been introduced in the respiratory field. As elsewhere, the success of this method in the respiratory field is dependent on training and practice guidance in TUS, as well as the availability of a comprehensive text book. With this latter necessity in mind, we decided to fill this critical gap by devoting an ERS Monograph to the subject. This book provides the reader with a broad and detailed overview on the various application of TUS. The initial chapters summarise the technologies and standard approaches used. Subsequent chapters focus on specific diseases and cover additional areas such as cardiac US, application in children and US use during procedures. Thanks to the hard work of the book’s Guest Editors, Christian B. Laursen, Najib M. Rahman and Giovanni Volpicelli, readers of this Monograph will benefit from a book that provides a comprehensive overview of both the background and hands-on application of US. We hope that this important publication will not only aid the respiratory physician in their day-to-day practice but will also help generate more frequent use of TUS in the field.

Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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References 1. Laursen CB, Rahman NM, Volpicelli G. Introduction. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. xiii–xv.

Disclosures: R. Bals has received grants from the German Research Ministerium and the Deutsche Forschungsgemeinschaft. He has also received personal fees from GSK, AstraZeneca, Boehringer Ingelheim and CSL Behring.

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Guest Editors Christian B. Laursen Christian B. Laursen is Associate Professor at the University of Southern Denmark (Odense, Denmark). He is a Consultant and Head of Research at the Department of Respiratory Medicine, Odense University Hospital (Odense). He qualified in medicine at the University of Southern Denmark and trained in pulmonology at Svendborg Sygehus (Svendborg, Denmark) and Odense University Hospital. He received his PhD in point-of-care ultrasonography at the University of Southern Denmark. Christian Laursen’s research interests lie particularly in clinical ultrasound, interventional pneumology, medical education and technical training. His current research focuses on the use of advanced and multiparametric ultrasound for malignancy in the chest, complex pleuropulmonary infections and interstitial lung diseases. He is one of the cofounders of an international collaborative research network in thoracic ultrasound education and training. The network currently involves the Oxford Pleural Unit at the Oxford Centre for Respiratory Medicine (Oxford, UK), Southmead Hospital (Bristol, UK), the Copenhagen Academy for Medical Education and Simulation (CAMES) (Copenhagen, Denmark), and the Department of Respiratory Medicine and Regional Centre of Technical Simulation (TechSim) (Odense, Denmark). The aim of the collaboration is to provide evidencebased educational programmes in thoracic ultrasound and related procedures. Christian Laursen chairs the Danish Society of Respiratory Medicine’s Ultrasound Committee and is Course Director of the European Respiratory Society’s course in thoracic ultrasound.

Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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Najib M. Rahman Najib M. Rahman is Associate Professor of Respiratory Medicine. He runs the Oxford Pleural Unit (Oxford, UK) and is Director of the Oxford Respiratory Trials Unit (Oxford). Having qualified in medicine from the University of Oxford (Oxford), he conducted his post graduate training in Nottingham (UK), then his specialist training in Oxford, including a DPhil in pleural disease (conducting the MIST2 study) and an MSc in clinical trials methodology. He now conducts research in clinical and translational pleural disease in Oxford, and runs randomised and observational studies in pleural infection, pneumothorax, malignant pleural effusion and ultrasound. He has authored over 90 peer reviewed publications. Giovanni Volpicelli Giovanni Volpicelli has been an emergency physician at the Emergency Department of San Luigi Gonzaga University Hospital (Torino, Italy) since 1998. In 2016, he qualified as Associate Professor of Internal Medicine. Giovanni Volpicelli was Chair of the Scientific Committee of the 1st International Consensus Conference on Lung Ultrasound. He is a member of the Scientific Committee of the 2nd International Consensus Conference on Ultrasound in Trauma, and he is a board member of the 1st International Consensus Conference on US in Medical Education. He is Editor-in-Chief of the Critical Ultrasound Journal, Academic Editor of Medicine and a member of the Editorial Boards of and reviewer for many international journals, including The New England Journal of Medicine, Annals of Internal Medicine, the American Journal of Respiratory and Critical Care Medicine, Chest, Intensive Care Medicine, Critical Care Medicine, Critical Care, Anesthesiology, and the American Journal of Emergency Medicine. He is a scientific reviewer for MORE (McMaster Online Rating of Evidence) at McMaster University (Health Information Research Unit, Hamilton, ON, Canada). Giovanni Volpicelli is a fellow of the American College of Chest Physicians (ACCP), a member of the American College of Emergency Physicians (ACEP) and a member of the Board of Directors of the World Interactive Network Focused on Critical Ultrasound (WINFOCUS). He coordinates the international program of education on lung ultrasound for WINFOCUS. Giovanni Volpicelli has authored and co-authored chapters of international books in emergency medicine and emergency ultrasound, and has 93 indexed publications in peer-reviewed international journals with 3450 citations. xii

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Introduction Christian B. Laursen1,2,3, Najib M. Rahman4,5,6 and Giovanni Volpicelli7 The sinking of RMS Titanic in 1912 led to the invention of a range of devices as a means of improving the detection of icebergs. During World War I, the technique was further developed into an active sound device using quartz for the detection of submarines. In the following decades and during World War II, the technique was further developed and named sonar (SOund Navigation And Ranging) [1]. The principles and technologies that lead to the development of sonar were also noticed amongst physicians. In 1940, Gohr and Wedekind suggested the use of reflected sound for diagnosing tumours, effusions and abscesses [2]. Dussik was the first to report the clinical use of reflected US as a medical diagnostic tool in his exploration of whether visualisation of intracranial structures and ventricular measurements was possible with US waves [3]. Despite Gohr and Wedekind’s initial suggestions and studies published by other authors, the use of TUS as a clinical tool was for many years considered to be limited to the assessment of pleural effusion [2, 4–6]. A description of the use of TUS as a tool for the assessment of horses with respiratory diseases challenged this dogma. Rantanen reported the use of TUS for the assessment and diagnosis of such conditions as lung consolidation, atelectasis, abscesses, pleural effusion, empyema and pneumothorax in horses [7]. Furthermore, Rantanen’s paper contains descriptions of vertical and horizontal reverberation artefacts as well as the concept of movement of the “pleural blades” during respiration in normal lungs, and its absence if pneumothorax is present [7]. These signs and artefacts were later to be considered key concepts in TUS [8]. The subsequent studies during the 1990s by researchers such as Targhetta and Lichtenstein lead to the birth of TUS as an essential diagnostic modality in the assessment of patients with known or suspected disease in the chest [9–14]. A milestone was reached when the first international consensus conference producing evidence-based recommendations for point-of-care LUS was published in 2012 [8]. This document achieved the great aknowledgement of becoming the most cited article of the top 50 published in Intensive Care Medicine, the journal of the European Society of Intensive Care Medicine; it was even more highly cited than other very

1 Dept of Respiratory Medicine, Odense University Hospital, Odense, Denmark. 2Centre for Thoracic Oncology, Odense University Hospital, Odense, Denmark. 3Institute for Clinical Research, SDU, Odense, Denmark. 4Oxford Centre for Respiratory Medicine, Oxford University Hospitals NHS Foundation Trust, Oxford, UK. 5Oxford Respiratory Trials Unit, Nuffield Dept of Medicine, University of Oxford, Oxford, UK. 6Oxford NIHR Biomedical Research Centre, Oxford, UK. 7Dept of Emergency Medicine, San Luigi Gonzaga University Hospital, Torino, Italy.

Correspondence: Christian B. Laursen, Dept of Respiratory Medicine, Odense University Hospital, Sdr. Boulevard 29, 5000 Odense C, Denmark. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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popular topics in critical care, such as the fluid management of shock and the new definition of acute respiratory distress syndrome [15]. The consensus analysed 320 articles published prior to 2012. The same group of experts is working on the update, analysing around 700 articles on LUS published from 2012 to the present day. This demonstrates the great importance and high impact of TUS in various communities, including, of course, respiratory medicine. We were thrilled to be asked to be guest editors of this, the very first ERS Monograph on TUS. A book solely dedicated to the subject is a clear sign that TUS is now considered to be an essential bedside tool for the modern respiratory physician. Despite this, and the fact that the number of published studies describing the clinical use of TUS is steadily increasing, several aspects are yet to be studied and assessed in robust clinical trials. In comparison with other types of clinical US (e.g. abdominal US, echocardiography) the extent of international consensus on several key aspects remains limited. Furthermore, different forms and TUS approaches have been adopted by many different specialities and societies, making a consensus process even more difficult. In the context of this Monograph, we chose to use the following definitions: • TUS: diagnostic ultrasonography of the thorax. The term chest sonography or LUS is often used synonymously in the literature [8, 16]. • Focused TUS: a focused TUS examination. • Focused ultrasonography: an ultrasonographic examination performed in a focused manner in order to answer specific and clinically relevant yes/no questions. As opposed to diagnostic ultrasonography, focused ultrasonography is believed to require less training and is less time consuming to perform [17]. An example would be FTUS examination used by an emergency physician to assess a patient with respiratory failure in an emergency department. • Diagnostic ultrasonography: defined as an US examination in which the examiner aims to identify all possible pathologic conditions in an organ or structure, including the ability to declare “normality”. In order to be able to perform diagnostic ultrasonography, dedicated training and more extensive experience are required [18]. Examples are echocardiography performed by a cardiologist or a TUS examination performed by a respiratory physician. To compensate for the lack of international consensus and different approaches used, we chose to invite a selection of authors for each chapter who were not only recognised experts but also represented different specialities, use TUS in different settings, and work at different institutions in different countries. We are very pleased that we were able to use this approach, and would like to thank all the authors for their positive attitude and collaborative efforts within the group. We hope that the result is that each chapter reflects not only the opinion of experts at a single site in Europe but a multidisciplinary and multicentre view. In summary, we hope that this ERS Monograph will facilitate increased consensus, research, implementation and evidence-based use of TUS to the benefit of the high number of patients being assessed for diseases of the thorax. This technique must surely now be regarded as essential. xiv

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References 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18.

Ainslie M. Principles of Sonar Performance Modelling. Berlin, Springer, 2010. Gohr H, Wedekind T. Der Ultraschall in der Medizin. Klin Wochenschr 1940; 19: 25. Dussik K. Uber die moglichkeit hochfrequente mechanische schwingungen als diagnostisches hilfsmittel zu verwerten. Z Neurol Psychiat 1942; 174: 153–168. Dudrick SJ, Joyner CR, Miller LD, et al. Ultrasound in the early diagnosis of pulmonary embolism. Surg Forum 1966; 17: 117–118. Miller LD, Joyner CR, Dudrick SJ, et al. Clinical use of ultrasound in the early diagnosis of pulmonary embolism. Ann Surg 1967; 166: 381–393. Joyner CR Jr, Miller LD, Dudrick SJ, et al. Reflected ultrasound in the study of diseases of the chest. Trans Am Clin Climatol Assoc 1967; 78: 28–37. Rantanen NW. Diseases of the thorax. Vet Clin North Am Equine Pract 1986; 2: 49–66. Volpicelli G, Elbarbary M, Blaivas M, et al. International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012; 38: 577–591. Targhetta R, Bourgeois JM, Balmes P. Echography of pneumothorax. Rev Mal Respir 1990; 7: 575–579. Targhetta R, Chavagneux R, Bourgeois JM, et al. Sonographic approach to diagnosing pulmonary consolidation. J Ultrasound Med 1992; 11: 667–672. Lichtenstein DA. A bedside ultrasound sign ruling out pneumothorax in the critically ill. Lung sliding. CHEST J 1995. 108: 1345. Lichtenstein D, Mézière G, Biderman P, et al. The comet-tail artifact. An ultrasound sign of alveolar-interstitial syndrome. Am J Respir Crit Care Med 1997; 156: 1640–1646. Lichtenstein D, Meziere G. A lung ultrasound sign allowing bedside distinction between pulmonary edema and COPD: the comet-tail artifact. Intensive Care Med 1998; 24: 1331–1334. Lichtenstein D, Mezière G, Biderman P, et al. The “lung point”: an ultrasound sign specific to pneumothorax. Intensive Care Med 2000; 26: 1434–1440. ICM: 50 most cited articles. www.esicm-old.org/news-article/ICM-news-50-MOST-CITED-2012-June-2015. Date last accessed: January 1, 2018. Mathis G, Sparchez Z, Volpicelli G. Chest sonography. In: Dietrich CF. EFSUMB Course Book. London, EFSUMB, 2010. Noble VE, Nelson BP. Manual of Emergency and Critical Care Ultrasound. Cambridge, Cambridge University Press, 2011. Minimal Training Requirements for the Practice of Medical Ultrasound in Europe. Appendix 11: Thoracic Ultrasound. 2008 [cited 2016 01.03.16] http://efsumb.org/guidelines/guidelines01.asp

Disclosures: C.B. Laursen has received personal fees from GE Healthcare for giving lectures at an US course organised by the company.

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List of abbreviations CEUS COPD CT CXR DUS EBUS-TBNA EUS-FNA FoCUS LUS MRI PET PoCUS TUS US

contrast-enhanced ultrasound chronic obstructive pulmonary disease computed tomography chest x-ray diaphragm ultrasound endobronchial ultrasound-guided transbronchial needle aspiration endoscopic ultrasound fine-needle aspiration focused cardiac ultrasound lung ultrasound magnetic resonance imaging positron emission tomography point-of-care ultrasound thoracic ultrasound ultrasound

| Chapter 1 Physics and basic principles Stephen Alerhand1, Ole Graumann2,3,4 and Bret P. Nelson1 The clinical benefits of LUS manifest in patients ranging from the clinically ill to those who have suffered trauma. Along with the proper hands-on technique at the bedside, the different US modalities and parameters of the US machine must be understood in order to acquire high-quality images on the screen for the physician to translate clinically. Unlike other parts of the body, the normal healthy lungs themselves are not actually visualised using bedside US, and what is depicted on the screen is not a true representation of the lung. Instead, LUS can best be described as the interpretation of US artefacts. Accordingly, the basic US principles and physics behind these artefacts must be understood in order to learn, apply and teach LUS. These tenets are reflected in both normal lung (e.g. A-lines, mirror artefact of the liver above the diaphragm) and diseased or injured lung (e.g. B-lines, pneumothorax). Cite as: Alerhand S, Graumann O, Nelson BP. Physics and basic principles. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 1–13 [https://doi.org/10.1183/2312508X.10006017].

D

ue to the poor penetration of US waves through air, LUS was traditionally considered a difficult modality to incorporate into practice. Eventually, it was realised that LUS is mostly a study of its artefacts. This concept laid the foundation for its use in diagnostic and procedural applications. Accordingly, the basic tenets of US physics must be understood in order to fully implement these techniques and interpret the acquired images. Moreover, since the structure of normal lung cannot be directly “seen” in a straightforward way as with other applications, educators must have a firm grasp on US artefacts in order to teach these concepts in a simple way that learners can appreciate. This chapter will describe several basic US concepts and principles that will be used throughout the rest of the book.

Basic physics, definitions and terminology In order to understand how the energy of an US probe is ultimately translated into a discrete picture on the screen, the fundamental qualities of the science must first be understood. This science is best encapsulated by the piezoelectric effect, which describes the conversion of electrical energy into mechanical energy. First, applied electrical voltage from the machine deforms a crystal element in the transducer to generate the initial mechanical 1

Division of Emergency Ultrasound, Dept of Emergency Medicine, Icahn School of Medicine at Mount Sinai, New York, NY, USA. Dept of Radiology, Odense University Hospital, Odense, Denmark. 3Dept of Clinical Medicine, Odense University, Odense, Denmark. 4 Dept of Clinical Medicine, Aarhus University, Aarhus, Denmark. 2

Correspondence: Bret P. Nelson, Division of Emergency Ultrasound, Dept of Emergency Medicine, Icahn School of Medicine at Mount Sinai, 1 Gustave L. Levy Place, New York, NY 10029, USA. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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pressure wave. Upon the reflection and return of these echoes to the transducer, the crystal element is deformed once again. These deformations generate an electric current that the US machine converts into an image on the screen. The distance of a given structure on the screen from the US transducer is determined by the time required for the mechanical energy of its echo to return. The greyscale representation on the screen is determined by the intensity of that returning signal, with each echo corresponding to a point on the screen. The sound waves described above consist of a series of repeating mechanical pressure waves propagating through a medium (figure 1). The peak pressure of a wave (its height when mapped out graphically) is defined as its amplitude and is measured in decibels (dB). This amplitude is a measurement of the strength of the echo returning to the US transducer as mechanical energy. The machine itself processes this information to determine the brightness of the structure on the screen. Stronger returning echoes (with higher amplitude) appear as bright white (or hyperechoic) areas on the screen, whereas weaker echoes (with lower amplitude) appear dark grey (hypoechoic) or black (anechoic) (figure 2). In between white and black, there exists a wide range on the continuum referred to as the greyscale. The velocity of the sound waves is also of critical importance for interpreting the screen images and teaching LUS. The velocity is defined as the speed of the US wave, measured in metres per second. Within any given medium through which the US wave passes, this velocity remains constant. Some media allow faster propagation than others; some examples are shown in table 1. Generally speaking, waves propagate faster when molecules are closer in relation to one another, and they propagate more slowly with decreased density of molecules. The resistance to molecular movement in a particular tissue type is referred to as its acoustic impedance. The US machine uses these different propagation speeds to determine the distance of a structure from the transducer. It accomplishes this by measuring the time taken for the wave to reach that particular structure and be reflected back to the transducer. Impedance is critically important in understanding LUS because the loss of US energy through tissue greatly determines how well it will form an image. Most structures that form good images with US have impedance values between 1.5 MRayl (water) and 1.7 MRayl (organs). In contrast, the acoustic impedance of air is 0.0004 MRayl, and for bone it is 6–8 MRayl. Since air and bone impede US wave transmission quite differently from water

Pressure Amplitude Time

0

Period Figure 1. Sound wave plotted as time versus pressure. Reproduced and modified from [1] with permission.

2

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A B

C

Figure 2. A midrange echotexture, like that of a solid organ, is shown on the left. On the right, the image of the thorax demonstrates areas that are hypoechoic (A), isoechoic (B) and hyperechoic (C) compared with the image on the left.

and organs, it is much more difficult to obtain accurate sonographic information from these structures. This will have an impact on the attenuation of US energy through these structures, as discussed later in this chapter. Having described the elements determining the screen image’s characteristics (brightness, depth), we can now turn to the visual quality of this image. This resolution is determined by the frequency of the US wave, which is defined as the number of times per second that the wave repeats. It is measured in hertz (Hz), with 1 Hz being equal to one wave-cycle per second. US waves include any frequencies above audible sound (20–20 000 Hz). Diagnostic US uses frequencies ranging from 12 to 2 MHz, with 1 MHz being equal to 1 million Hz. Waves with high frequencies generate images with high resolution. They utilise more energy and create more waves per second. These waves thus lose energy more rapidly and have less energy available to penetrate to deeper distances. In contrast, waves with low frequencies utilise less energy and create fewer waves per second. Accordingly, the images produced are of lower resolution. Since these waves lose energy less rapidly, more energy remains available to penetrate more deeply. Frequency is thus directly correlated with image resolution and indirectly correlated with tissue penetration. The strength of the returning signal also depends on the surface structure of the organ. For instance, a linear surface structure of an organ will return much of the signal directly to the transducer and therefore have a higher signal (figure 3). As described, resolution is defined as the ability of the US machine to differentiate between two closely located structures. Axial resolution refers to structures lying in a plane parallel to Table 1. Propagation speeds of US waves through different tissue media Tissue medium Aerated lung Fluid-filled structures (e.g. pleural effusion) Soft tissue (e.g. pneumonia) Bone

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Propagation speed m·s−1 330 1480 1540 4080

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a)

b)

c)

d)

Figure 3. Depiction of an emitted US beam striking and being reflected off a linear surface structure (a), compared with surface structures of varying angles and orientations (b–d).

the US wave (directly along its path), while lateral resolution refers to structures lying in a perpendicular plane to the US beam. A beam is very thin and is created by tens to hundreds of scan lines. Lateral resolution will generally be inferior. Adjusting the depth of the view on the screen, as well as the width, will indirectly adjust the focal zone of the US beam. Wavelength is defined as the distance a wave travels in a single cycle, as measured in micrometres. It fits within the following equation: velocity=frequency×wavelength. As described previously, the velocity of a wave remains constant as it propagates through a given tissue medium. Therefore, wavelength is inversely proportional to frequency. Accordingly, high-frequency waves (high-resolution images) correspond to lower wavelengths. These waves travel a shorter distance within a given cycle and thus demonstrate shallower penetration into tissue. In contrast, low-frequency waves (low-resolution images) correspond to higher wavelengths. These waves travel a greater distance within a given cycle and thus demonstrate deeper penetration into tissue. As a general rule, the depth of penetration of US in tissue is limited to 200 wavelengths. Thus, a high-frequency, short-wavelength 10 MHz transducer may penetrate only 3 cm into tissue, whereas a low-frequency 1 MHz transducer may penetrate 30 cm. The velocity, and therefore the frequency and wavelength, can also be described by its property of attenuation. This is defined as the progressive weakness of a sound wave as it travels through a given medium. This loss of energy begins upon being emitted from the transducer, all the way through the return of the echo back to the transducer. Similar to velocity, each tissue medium has a corresponding attenuation coefficient. This value is determined by several factors including: the density of molecules of the medium, the number of different interfaces encountered by the wave and the wavelength (table 2). Waves do not travel well through aerated lung due to scatter and reflection; they travel much better through tissue with increased density, such as fluid-filled or fibrotic lung. This helps to differentiate among well-aerated (i.e. healthy), fluid-filled (i.e. pulmonary oedema, pulmonary contusion) and consolidated (i.e. pneumonia) lung. With a fluid-filled lung, the fluid within the alveoli will conduct the wave rather than scatter it. The waves thus become trapped and are reflected within the alveoli to create hyperechoic vertical “B-lines” that extend from the pleural interface to the bottom of the screen and move with respiration (figure 4). The degree of fluid within the alveoli or fibrotic lung tissue corresponds to the number and size of B-lines. B-lines can also coalesce together and appear as a wide belt 4

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Table 2. Attenuation coefficients for body tissues of varying echogenicities Tissue Air Bone Muscle Liver/kidney Fat Blood Fluid

Attenuation coefficient 4500 870 350 90 60 9 6

(“lung rockets”). In newborns, wet lung will have this B-line belt appearance, which disappears when the lungs fill with air. With regard to interfaces encountered by the emitted wave, fewer interfaces will be encountered if the lung tissue is homogeneous, and thus less attenuation will occur. With more heterogeneous lung, more interfaces will be encountered and more attenuation will occur. In essence, tissue of the same type and density facilitates the transmission of sound waves. It is also of paramount importance to understand what happens to the sound waves in between their emission and subsequent return to the transducer. Reflection is defined as redirection of the sound wave, or a part of it, back to its source. If the US beam is directed at 90° to the structure being investigated, the reflection of the wave back to the transducer will be maximised. When the sound wave encounters such an interface at an oblique angle, refraction occurs. The echoes returning to the probe arrive with less-organised information than they would if having been redirected at a 90° angle. Moreover, reflection will be greater with larger differences in acoustic impedance between tissue interfaces. More energy will be lost to this reflection, and less energy therefore remains to penetrate further and visualise deeper tissue structures. In relation to LUS, air is

Figure 4. B-lines within the lung. More than three B-lines within a given lung field is indicative of increased density.

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D

*

*

*

*

*

Figure 5. Vertebral bodies (*) visible behind the window of the liver. Normally, air above the diaphragm (D) blocks their visualisation above the diaphragm. However, when fluid is present above the diaphragm, the fluid acts as a window to allow visualisation of the vertebral bodies.

not a good tissue medium for sound wave transduction, as it scatters waves in infinite directions and precludes organised feedback to the transducer. The difference in acoustic impedance between tissues thus illustrates why US waves do not allow good visualisation of structures that lie deep to air, as opposed to fluid. For instance, the “spine sign” refers to visualisation of the spine deep to the lung when the lung is filled with fluid rather than filled with air (figure 5). For suggested reading on this subject, the reader is directed to [2–4].

LUS artefacts Artefacts represent information from returning echoes that does not correspond to accurate anatomic information. Failure to recognise US artefacts can lead to misinterpretation of the images. It is therefore of utmost importance to understand these artefacts and recognise them in the proper clinical context. For further reading on this subject, the reader is directed to [5]. Acoustic shadowing

This refers to the dark shadow posterior to a structure that extends to the bottom of the screen. This occurs when the structure has a different tissue density from the tissue that immediately preceded it along the plane of the emitted beam. The greater the difference in density and attenuation between interfaced tissues, the more acoustic energy will be reflected. These surfaces are thus referred to as strong reflectors. With regard to LUS, the US probe and gel have roughly the same density as liquid. Upon reaching past the pleura, the air will scatter the US waves in infinite directions. In contrast, relatively less scattering and reflection of waves will occur with pulmonary oedema or consolidated lung (roughly liquid-dense). Reverberation

Reverberation occurs when the emitted beam bounces to and fro between two highly reflective structures. For LUS, this may appear as recurrent bright hyperechoic arcs displayed 6

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Figure 6. Reverberation artefacts, known as A-lines (arrows), extending to the bottom of the screen, spaced out at equidistant intervals from one another.

at equidistant intervals from the transducer to the bottom of the screen. These reflections between the transducer and the pleura generate “A-lines” (figure 6). A distance equal to the initial index distance between the skin and pleura separates sequential artefactual lines. In addition, the parietal and visceral pleura, which are closely apposed to one another in normal lung, will “trap” the emitted beam, which then travels repeatedly back and forth between the two surfaces. The machine displays this artefact as a hyperechoic white echo called a comet tail artefact, which will then appear as a “Z-line” (figure 7).

Refraction artefact

A refraction artefact (or edge shadowing) occurs when an emitted sound beam crosses an interface of differing tissue densities at an oblique angle. An acoustic shadow will appear posterior to the point at which the beam crossed this tissue interface and changed its direction.

Figure 7. Comet tail artefact. Although they both arise from the pleura, lung comets (arrow) do not extend all the way down to the bottom of the screen as B-lines do (see figure 4).

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Mirror imaging

Mirror imaging can produce an artefactual object when an emitted beam undergoes multiple reflections. Two objects will appear on the screen, one on each side of the strong reflector, with the deeper one being false. The mechanism for mirror imaging begins when part of the emitted beam is reflected backwards upon encountering a tissue of differing density. If this wave then encounters another object, the machine will use its amplitude to depict its presence on the screen. However, the machine will incorrectly assume that the initial emitted beam had travelled along a linear path to reach this object lying further than the index tissue. Based on the longer time that the beam travelled before the return of the echo, the machine will incorrectly duplicate the object as a false object deep to the index reflection. This artefact can be visualised when viewing the lung–diaphragm–liver interface in the sagittal plane of the midaxillary line (figure 8). Mirror imaging is very sensitive to subtle manipulation of transducer orientation, as the linear plane will be changed. Posterior acoustic enhancement

This refers to artefactual brightness deep to an anechoic structure through which low attenuation occurs. For instance, since there is low attenuation through fluid-filled structures (higher propagation speed), the beam passing through a pleural effusion will have more energy remaining with which to continue travelling deeper towards the vertebral bodies. As a result, the spine sign will be visualised on the screen (figure 5). Adjacent to the pleural effusion, for instance through the soft-tissue density of the liver, the spine may not be as well visualised because there will be less acoustic energy remaining for echoes of the spine to return with sufficient intensity. Side lobe artefact

This artefact occurs when acoustic energy emitted outside the central axis of the transducer is reflected back to the probe. The reflection is interpreted by the machine as an echo

Figure 8. US pulses (long arrow) reflected off a bright reflector such as the diaphragm encounter liver tissue (short solid arrow) and are then reflected back to the diaphragm and then to the transducer. The device calculates the extended round-trip time as an encounter with liver tissue deeper than the reflector (dotted arrow), mapping the liver tissue in this deeper, false location.

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returning from the central axis, not from the sides. It therefore creates a false representation of that structure in the central axis. Beam width artefact

A beam width artefact occurs due to the fact that the US beam is actually a few millimetres thick, as opposed to our conceptualisation that it occupies zero width. As a result, the opposing lateral sides of this thin beam may visualise tissues at points of differing echogenicity. These amplitudes will be averaged out by the machine and depicted on the screen according to that midrange value.

Probe selection Each available US transducer carries different properties and can be used to evaluate the lung. To begin with, the transducers vary in the frequency emitted. A linear transducer emits a beam with a frequency range of 6–12 MHz, a phased array probe has a range of 1–5 MHz and a curvilinear probe has a range of 2–5 MHz. As mentioned previously, higher frequencies allow high-resolution images of shallower structures, whereas lower frequencies allow lower-resolution images of deeper structures. The transducer used to evaluate the lung depends on the specific application. For instance, the linear transducer is traditionally used for visualising the pleura–lung interface to evaluate for pneumothorax (PTX) or B-lines. However, in a patient with a larger body habitus, either of the other two transducers may suffice for deeper penetration through the excess soft tissue. The piezoelectric effect described earlier manifests differently with the varying US probe shapes. To evaluate lung tissue with a linear-shaped probe, for example, the crystals at the tip of the probe are aligned along a flat plane. The US waves are emitted in a straight line, the echoes return in this same line and the machine generates a rectangular image with high lateral resolution. In contrast, with a curvilinear probe, the crystals are embedded along a curved shape. The US beams emitted from the lateral aspects of the transducer fan outwards, leading to decreased lateral resolution and a pie-shaped image on the screen.

Tenets of US technique It is best to maintain the body part to be scanned and the US screen in the same visual plane of the physician. In this way, the physician can manipulate the probe’s position and orientation while maintaining a line of sight with the structures on the screen. Once positioned, the US probe must be applied and wielded in such a way as to maximise the ability of the piezoelectric effect to produce high-quality images. To begin with, sufficient gel must be placed along the interface between the probe marker and the patient’s body. Any air residing in this interface will cause the emitted sound waves to scatter at this initial point, similar to the situation through well-aerated tissue in the lung. An appropriate technique consists of holding the probe with the first three fingers, as if holding a pencil, while using the fourth and fifth fingers for stabilisation against the patient’s body. In this way, the probe can be maintained in its position with the most ease for the ultrasonographer and with decreased probe pressure against the patient’s body. https://doi.org/10.1183/2312508X.10006017

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Lung tissue moves with respiration, and by keeping the probe still in its spot, lung tissue movement with inspiration and expiration can best be visualised.

US probe marker and image orientation The three-dimensional (3D) structures of the body being evaluated are seen on the screen as two-dimensional (2D) images. Therefore, each structure must be scanned in at least two orthogonal planes. The raised or otherwise indicated marker on the transducer corresponds to a dot or marker on the left side of the US screen. Structures in the body located on the side of the probe marker correspond to objects on the screen on the side of the dot. This enables the ultrasonographer to relate the orientation of his or her probe to the image orientation on the screen (figure 9). Another way to ensure correct probe orientation is to tap on one end of the probe with the fingers while watching for the side of the screen where this contact is visualised. The US probe, along with its emitted beam, can be oriented in the x-, y- or z-axis. To obtain a longitudinal or sagittal view, the probe is oriented along the long axis of the patient’s body with the probe marker facing cephalad, or towards the head. These cephalad structures will be seen on the left side of the screen closest to the marker. To obtain a transverse or axial view, the probe is oriented along the short axis of the patient’s body, with the probe marker facing towards the patient’s right. Structures on the patient’s right will be seen on the left side of the screen closest to the marker.

Patient positioning Different protocols for scanning have been proposed, and many authors and operators have particular preferences based on the pathology that is being evaluated. For example, scanning the anterior chest wall with the patient supine is generally sufficient for evaluating for PTX, in which the gravitationally dependent air will rise to the anterior-most part of the pleura. Conversely, a comprehensive assessment of the entire lung, especially the a)

*

b)

*

Figure 9. The probe marker on the screen (a) corresponds to the probe marker on the probe (b) (both indicated by *).

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posterior, is necessary to assess for pneumonia. This can be accomplished by using the “lawnmower technique”, which involves dividing up the lung regions into different zones as part of a standardised protocol.

US imaging modalities The US machine consists of several modalities that emit US waves differently, receive the echoes and translate that information uniquely onto the screen. Brightness or B-mode is the main modality used for diagnostic imaging of the lung. It converts the returning echoes of varying amplitudes into the greyscale visualised on the screen. It presents a 2D slice of the 3D structure being visualised. Motion or M-mode depicts the motion of a given structure in the transducer’s directed plane over time. This plane is chosen by the operator’s placement and manipulation of a vertical line through the object of interest. This line remains anchored at the top and centre of the screen, but its orientation and direction can be adjusted laterally in either the left or right direction. On the screen, the motion (or nonmotion) of the structure is plotted along the y-axis, and time in seconds is plotted along the x-axis. This scanning modality can be used to evaluate the lung for PTX, as demonstrated by the absence of visceral pleural sliding deep to the nonmoving parietal pleura (a “lung point” in B-mode and “barcode sign” in M-mode). Doppler physics allows the differentiation of reflected sound waves towards or away from the probe. Objects moving towards the transducer produce a higher reflected frequency, whereas sources moving away from the transducer produce a lower reflected frequency. These distinctions can be represented either by colour changes (colour Doppler) or by audible and graphical peaks (spectral Doppler). In the former, red and blue correspond to sound waves travelling to and away from the probe, respectively, as indicated by the legend on the side of the screen. Usually, this legend will show red at the top and blue at the bottom, with the continuum of colours in between. This means that waves moving towards the transducer (at the top of the screen) will appear red, whereas waves moving away from the transducer (at the bottom of the screen) will appear blue. This information adhering to Doppler physics is sensitive to the position and angle of the transducer relative to the direction of the waves. For instance, if the angle is at 90°, no signal will be reflected. Another Doppler modality called power Doppler is most useful for detection of low-flow states. This flow is represented on the screen by degrees or gradations of the colour red only, as it does not provide information about the direction of the flow. It averages several frames of flow over a number of cardiac cycles. It is less dependent on the angle of the transducer but is more sensitive to motion artefacts.

Mechanisms of image adjustment The US machine itself consists of several operations that can manipulate the display of the visualised structures on the screen. The focal zone is the area where the narrowest part of the US beam is focused and provides the highest lateral resolution. Some US machines allow this focus to be adjusted laterally. The focal depth can also be adjusted on some https://doi.org/10.1183/2312508X.10006017

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machines by vertically adjusting the marker located on the side of the screen. The focal zone should be placed at the level of or just below the structure you want evaluate. The depth can also be adjusted to allow visualisation of deeper structures, or to limit the depth to better visualise shallow structures. One side of the screen shows a centimetre scale for indicating depth. Adjusting the gain parameter allows adjustment of the display brightness of returning echoes. Increasing the gain will brighten the entire display field on the screen, whereas decreasing the gain will darken it. It has an equal impact on signal and noise, and does not change the amount of US energy entering the body. The gain has no effect on the resolution of images that appear on the screen. In other words, the quality of the image will remain the same. Time gain compensation allows the gain to be changed at specific depths as opposed to for the entire screen. In addition to enhancing the brightness of a certain structure to be visualised, this parameter corrects for the decreased energy that remains to reach deeper structures. These deeper structures undergo more attenuation due to their further location from the transducer, and hence a greater amount of tissue through which emitted waves

a)

b)

c)

Figure 10. Time gain compensation controls vary based on the machine manufacturer. For this device, there is a knob for near gain (a, inset: top), far gain (a, inset: middle) and overall gain (a, inset: bottom). Here we see the same image with different time gain compensation settings: a) image demonstrating good overall gain, with consistent echogenicity throughout the image; b) image showing overgain in the far field; c) image showing overgain in the near field.

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must propagate. Manipulation of the time gain compensation will enhance the brightness of these deeper structures, because otherwise they would always appear darker than their more shallow counterparts along the transducer’s imaging plane (figure 10).

Conclusion LUS can be utilised and interpreted in the medical care of a wide range of patients. In addition to understanding the basic tenets of US physics, physicians must be well acquainted with the different sonographic modalities and parameters of the US machine itself. Furthermore, it is vital to recognise that, unlike other tissues in the body, normal healthy lung is not actually visualised on the screen. Instead, the lung tissue is seen as artefacts governed by the aforementioned tenets of US physics. With a proper understanding of these tenets, LUS can thus be interpreted to great effect for both normal and diseased lung.

References 1. Ma OJ, Mateer JR, Reardon RF, et al., eds. Ma and Mateer’s Emergency Ultrasound. 3rd Edn. Maidenhead, McGraw-Hill Education, 2013; p. 31. 2. Hoskins P, Martin K, Thrush A, eds. Diagnostic Ultrasound: Physics and Equipment. Cambridge, Cambridge University Press, 2010. 3. Postema M. Fundamentals of Medical Ultrasonics. London, Soon Press, 2011. 4. Schmitz G. Ultrasound in medical diagnosis. In: Pike R, Sabatier P, eds. Scattering: Scattering and Inverse Scattering in Pure and Applied Science. London, Academic Press, 2002, pp. 162–174. 5. Feldman MK, Katyal S, Blackwood MS. US artifacts. Radiographics 2009; 29: 1179–1189.

Disclosures: None declared.

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| Chapter 2 Technique and protocols Christian B. Laursen1,2,3, Jesper R. Davidsen1,2,4 and Fergus Gleeson5 The use of a systematic approach is essential, no matter whether TUS is performed as a focused or a diagnostic examination. This chapter provides the novice in TUS with a description of the basic concepts and approach required to perform a systematic focused examination of the chest and some basic knowledge regarding a diagnostic examination of the chest. As well as training in practical US skills, inexperienced physicians should also focus on the art of integration of imaging into clinical practice. Cite as: Laursen CB, Davidsen JR, Gleeson F. Technique and protocols. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 14–30 [https://doi.org/10.1183/2312508X.10006117].

I

n order to ensure a high diagnostic accuracy of an US examination, knowledge of a number of aspects is needed: anatomy and physiology of the organ/structure assessed, US physics, functions of the US system and how to use them, scanning technique used, normal and abnormal findings, pitfalls and limitations of the examination, and integration of US findings into the clinical context. The use of a systematic approach is also essential, regardless of whether it is performed as a focused TUS (FTUS) or a diagnostic examination (TUS). The primary aim of this chapter is to provide the US novice with a description of the basic concepts and approach needed to be able to perform a systematic FTUS examination, as well as some basic knowledge regarding a diagnostic examination (TUS). The reading of this chapter does not replace theoretical and practical training, or a competency assessment prior to performing unsupervised examinations in clinical practice. The chapter will provide a brief overview of the basics of sonoanatomy of the thorax, a stepwise approach to the techniques and protocols for performing FTUS, and some of the basic differences and principles when performing TUS. Descriptions of more detailed sonoanatomy, pathology and specialised techniques are addressed in subsequent chapters in this Monograph describing specific conditions and examination techniques.

1 Dept of Respiratory Medicine, Odense University Hospital, Odense, Denmark. 2Centre for Thoracic Oncology, Odense University Hospital, Odense, Denmark. 3Institute for Clinical Research, SDU, Odense, Denmark. 4South Danish Center for Interstitial Lung Diseases (SCILS), Odense University Hospital, Odense, Denmark. 5Dept of Radiology, Churchill Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK.

Correspondence: Christian B. Laursen, Dept of Respiratory Medicine, Odense University Hospital, Søndre Boulevard 29, 5000 Odense C, Denmark. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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Basic sonoanatomy of the chest Knowledge of the basic sonoanatomy of the thorax is an essential prerequisite in the performance of FTUS. The basic two-dimensional (2D)-mode findings are described in the following sections, with more detailed and specific sonoanatomy findings of TUS given in subsequent chapters in this Monograph. The following descriptions are typical findings when the transducer is placed in a longitudinal axis over an intercostal space (ICS) (figure 1). Chest wall

Structures such as skin, s.c. tissue, muscles and connective tissue are visible just beneath the transducer. The connective tissue appears hyperechoic, and often more hyperechoic horizontal linear structures can be seen, representing connective tissue, such as muscle fascia. The two ribs aligning the ICS are visible as two hyperechoic lines with an underlying shadow (figure 2) [1, 2]. Pleura

Placed just below and between the two ribs, a hyperechoic horizontal line is seen representing the visceral and parietal pleura. Most conventional clinical US machines are not able to differentiate the two pleural surfaces from each other. The combined surfaces are termed the pleural line (figure 2) [1, 3, 4]. The “bat sign”

Since several structures as well as the pleural line may appear as a horizontal hyperechoic (white) line on the US screen, it is essential to be able to identify which of these lines represents the pleura. LICHTENSTEIN et al. [4] described how to use the “bat sign” in order to facilitate correct identification of the pleural line. The term “bat sign” is used since the two ribs adjoining an ICS (hyperechoic surface with posterior shadowing) and the pleural line resemble a bat flying towards the US screen (figure 3). Thus, the following two steps

Figure 1. A curved low-frequency transducer placed in zone L1. The orientation marker (arrow) is placed cranially to facilitate identification of the “bat sign” on the US screen.

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Figure 2. Normal sonoanatomy of the thorax. The muscles, fascia and s.c. tissue of the chest wall (CW) are placed just below the transducer. The superficial surface of the ribs (R) can be seen as hyperechoic horizontal lines with posterior shadowing (*). The visceral and parietal pleura can be seen as a hyperechoic horizontal line, the pleural line (PL), just below the ribs. The area below the pleural line (“L”) is due to artefact generation and does not represent the air-filled lung, which cannot be visualised using US.

should be performed prior to assessing the pleura line: 1) ensure that the scanning plane is vertical and the orientation marker is placed cranially (figure 1); and 2) use the “bat sign” sign to identify the pleural line (figure 3). Once this is done, the transducer can be rotated approximately 90° (depending on the angle of the ribs at the area being scanned) counterclockwise to avoid the ribs and visualise the entire pleural line in the ICS.

Assessment of the pleural line

The presence or absence of three findings is of importance when assessing the pleural line: 1) lung sliding, 2) the lung pulse and 3) B-line(s).

Figure 3. Identification of the “bat sign” is performed to identify the pleural line (PL) as being placed just below the two ribs (R). The ribs with posterior shadowing represent the bat’s wings and the pleural line represents the head of the bat.

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Lung sliding Lung sliding is seen as a horizontal movement of the pleural line in synchrony with the respiratory cycle, indicating a sliding movement of the visceral pleura against the parietal pleura [3, 5]. Lung sliding is due to the up-and-down movement of the visceral pleura in synchrony with the piston-like respiratory movement of the diaphragm [6]. Several factors may affect the magnitude of lung sliding (e.g. lung zone scanned, patient tidal volume, underlying disease and intubation) [6–8]. When air separates the two pleural layers (e.g. pneumothorax (PTX)), the movement disappears and cannot be detected with US. In such cases, the pleural line represents only the parietal pleura, which is still visible but does not slide since it is fixed to the chest wall [5, 9]. Apart from PTX, other conditions may also cause absence of lung sliding (e.g. fibrotic involvement in interstitial lung diseases, prior pleural empyema or sequelae from a prior intrathoracic operation) [6–8, 10, 11]. Lung pulse As well as lung sliding in synchrony with the respiratory cycle, the pleural line may also move in synchrony with the cardiac pulse. This movement, termed the “lung pulse”, is caused by the force of the cardiac pulsation being transmitted to the lung and hence to the visceral pleura [3, 7]. The lung pulse is not always present in healthy persons and is generally easiest to visualise in areas where the lung is in close contact with the pericardium and heart. Like lung sliding, the lung pulse indicates that the visceral and parietal pleural surfaces are juxtaposed at the location of the probe [7, 8, 12]. B-lines A B-line has been defined as a hyperechoic, laser-like, vertical reverberation artefact originating from the pleural line. B-lines are continuous from the pleural line to the bottom edge of the screen and do not fade in intensity [3, 13, 14]. Other reverberation artefacts may also originate from the pleural line, but, in contrast to B-lines, they fade out relatively quickly and do not continue to the bottom edge of the screen (figure 4) [3, 4]. If lung sliding is present, B-lines move in synchrony with the sliding [15]. B-lines are discussed in more detail in another chapter in this Monograph [16].

Figure 4. A B-line can be seen to originate at the pleural line (PL) and extends vertically to the bottom of the screen without fading. Another vertical artefact can also be seen (“Z”). However, this quickly fades when extending vertically and does thus not fulfil the criteria for a B-line. Such artefacts have been termed Z-lines by LICHTENSTEIN et al. [7].

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Lung

The normal air-filled lung cannot be visualised using conventional 2D-mode US. Due to the difference in acoustic impedance, the US signal is reflected at the surface of the lung (visceral pleura). The reflection is seen as a hyperechoic line with posterior shadowing. In persons with normal, aerated lung tissue, any structures that can be seen on the US screen below the pleural line are thus due to artefact generation [1, 3, 4]. Diaphragm and adjoining abdominal structures

Recognition and identification of the diaphragm and abdominal structures is an essential part of FTUS and TUS, as these structures serve as important anatomical landmarks when differentiating intrathoracic structures from abdominal structures. Diaphragm The superficial part of the diaphragm can be recognised as a hyperechoic “double line” located just below the ribs. The more hypoechoic area between the lines represents the muscle fibres of the diaphragm. As the diaphragm contracts, movement and thickening of the fibres can be observed [17]. The more central portion or tendinous component of the diaphragm can be visualised when using either the liver or the spleen as an acoustic window [18–21]. Liver and right kidney In healthy persons, the liver can be visualised when scanning the lower part of the thorax on the right side. Excellent images of the liver can generally be obtained when scanning in the midaxillary line. The liver is seen as a large, hyperechoic solid structure. When breathing in and out, the motion of the diaphragm causes displacement of the liver. Just below the liver, the right kidney can be visualised [22, 23]. Spleen, left kidney and stomach In healthy persons, the spleen can be visualised when scanning the lower part of the thoracic cavity on the left side. The spleen is seen as a hyperechoic solid structure. Just below the spleen, the left kidney can be visualised. It is difficult to identify the stomach when it is empty or air filled; however, it is easy to identify when filled with fluid as a hypoechoic collection of fluid. Often, small hyperechoic dots representing air bubbles are present within the fluid, and sometimes an air–fluid interface can also be seen [22, 23]. The stomach is typically seen in the lower part of the thoracic cavity on the left side.

Focused TUS The purpose of FTUS is most often to diagnose or exclude acute, potentially life-threatening conditions [22]. In comparison, the purpose of TUS is to diagnose and exclude all conditions in the chest that potentially can be visualised using sonography. Therefore, TUS often includes assessment of all areas of the pleura and lungs, which can be visualised by transthoracic scanning. TUS is often time-consuming and requires good patient cooperation, which are not always compatible with an emergency setting. When performing FTUS, usually only a limited area of the surface of the pleura and lungs is evaluated, and it can therefore be performed quickly with minimal discomfort to the critically ill patient [24, 25]. The use of FTUS has been demonstrated to have a high 18

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diagnostic accuracy for many of the common conditions seen in a variety of emergency settings [3, 10, 24, 26–34]. When used as part of whole-body ultrasonography, FTUS has been shown to help identify patients with missed life-threatening conditions, and it significantly increased the proportion of correctly diagnosed and treated patients admitted to an emergency department with respiratory symptoms [35, 36]. FTUS, alongside other forms of focused US, should be used as an integrated part of the clinical assessment of these patients. FTUS scanning protocols

Several different FTUS protocols and approaches have been described; however, no international consensus for the use of one specific protocol has been obtained [3]. Many protocols divide the thorax into a number of scanning points, areas or zones that are assessed using US, but the number of zones varies significantly for each protocol [4, 9, 12, 13, 31, 37–48]. The number of areas or zones scanned is of importance, since diagnostic criteria for some conditions (e.g. interstitial syndrome) are defined by the number of zones in which specific findings are represented. In this way, the number of areas or zones may potentially affect the diagnostic accuracy when compared with other protocols or with use in other settings [3, 24, 31, 49]. As well as the protocols describing FTUS, several other studies have described the use of FTUS principles as an integrated part of a whole-body ultrasonography approach in which several organs or structures are assessed in a given patient population or clinical setting [4, 34, 35, 50–54]. Many studies have used an eight-scanning-areas approach, as described by VOLPICELLI et al. [44], for assessing the anterior and lateral thoracic surfaces; similarly, the definition of interstitial syndrome is also based on these principles [3, 44]. However, this approach does not include assessment of the posterior thoracic surface, which is why posteriorly positioned pathology may be missed using this protocol [44]. LAURSEN et al. [35] modified the protocol to a 14-zone scanning protocol by adding assessment of the posterior surfaces using principles described previously by LICHTENSTEIN et al. [4], and this has subsequently been validated in prospective studies in a variety of settings [35, 36, 55, 56]. The use of this 14-zone FTUS approach alongside FoCUS and limited-compression ultrasonography of the deep veins has been validated for assessing patients with respiratory failure in an emergency department setting [35, 36]. Using the 14-zone approach, each hemithorax is divided into anterior, lateral and posterior surfaces, which can be further subdivided into smaller squares representing a scanning zone. Each of these scanning zones should be assessed using FTUS. Each of the scanning zones can be denoted from 1R to 7R on the right and from 1L to 7L on the left (figure 5) [35]. As described in subsequent sections, when assessing the thoracic lateral and posterior surfaces, it is of paramount importance to begin the assessment with identification of the upper abdominal structures and diaphragm. This is done in order to avoid mistaking abdominal structures as thoracic structures and vice versa (e.g. fluid in the stomach wrongly diagnosed as pleural effusion). To facilitate this approach, caudal zones (e.g. zones 3 and 5) have lower numbers than cranial zones (e.g. zones 4, 6 and 7) [35]. Predefined questions

FTUS should be performed in a focused manner in order to answer specific and clinically relevant yes/no questions [22]. The FTUS protocol aims to answer the following four predefined yes/no questions: 1) Is a PTX present? 2) Is a pleural effusion present? 3) Is interstitial syndrome present? 4) Is obvious pathology present? https://doi.org/10.1183/2312508X.10006117

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R1

L1

R2

L2

R7

L7

R4

L4

R6

L6

R3

L3

R5

L5

Figure 5. Focused TUS (FTUS) scanning zones using a 14-zone approach. The numbers of the zones denote the optimal scanning sequence. When scanning the lateral and posterior surfaces of the thorax, the examination should begin in the most caudal zones (e.g. zones 3 and 5) to ensure accurate identification of the border (diaphragm) between the chest and upper abdomen.

Several studies have documented that FTUS has a high diagnostic accuracy for conditions included as part of the predefined questions [10, 28, 35, 36, 54, 57–61]. It is, however, of importance to underline that FTUS has not been validated for a number of other conditions (e.g. pulmonary embolism, malignancy, chest wall pathology), and it has not been determined whether there is a substantial difference in diagnostic accuracy when FTUS is compared directly with TUS. Any incidental FTUS findings should therefore generally be referred to TUS performed by a trained expert. The same principles apply when reporting FTUS findings; terms such as “normal examination” should generally be avoided, since they imply the performance of TUS. FTUS reporting should be limited to answering the predefined questions: “No signs of PTX, pleural effusion or interstitial syndrome.”

General principles and preparation prior to performing FTUS Basic US principles have been addressed in the previous chapter in this Monograph [62]. A few key aspects regarding FTUS are mentioned in the following sections. Choice of transducer

A curved low-frequency transducer is generally the preferred transducer for FTUS as it has an acceptable image quality for both superficial and deep structures and can be used to answer the focused questions. In some scenarios, the use of other transducers can be considered, such as a microconvex transducer, linear transducer or phased array transducer. Microconvex transducer A microconvex transducer is an acceptable all-around transducer for FTUS. Due to its small size, it is often easier to use when the patient can only be examined in the supine position (e.g. emergency setting, intensive care unit (ICU)) or when scanning children [3, 4]. Linear transducer A linear transducer generates excellent images of superficial structures, such as ribs and the pleura, but deeper structures can be difficult to assess. It excels when the only clinically 20

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relevant question is to determine whether PTX is present, or as a supplement to a curved low-frequency transducer if doubt exists as to whether lung sliding is present or not.

Phased array transducer Due to its limited visualisation of the pleural line, a phased array transducer is generally less suitable for FTUS than most other transducers but is an acceptable alternative if no other transducers are available [3].

Choice of pre-set, scanning mode and US machine software

If a dedicated FTUS pre-set is available, then this should be used. In the absence of such a pre-set, an abdominal pre-set can be used when using a curved transducer, or a musculoskeletal pre-set when using a linear transducer. The presence or absence of US artefacts plays a pivotal role when performing FTUS. Software (e.g. harmonics, cross-beam) minimising artefacts should generally be switched off when performing FTUS [3]. Normally, the only mode needed for FTUS is B-mode.

Patient positioning

Initially, the anterior and lateral surfaces of each hemithorax are scanned with the patient in the supine position. Subsequently, the patient is asked to sit up and the zones on the posterior surface are scanned. Some patients with acute respiratory failure cannot be placed in a supine position due to severe dyspnoea. Anterior, lateral and posterior surfaces are then scanned with the patient in the sitting position. The patient position will affect the position of free air (e.g. PTX) and free fluid (e.g. simple pleural effusion) in the pleural cavities, and patient positioning is therefore of importance when assessing the patient for these two conditions. The supine position is the recommended position for assessing the presence of PTX, since the air will tend to be placed anteriorly in the chest cavity, an area that is easily assessable using FTUS. If the patient is placed in the sitting position, a small PTX can be missed if the air is located solely at the apex of the chest cavity, an area that is more difficult to assess using US [3]. In comparison, patients should be placed in the sitting position when scanning to detect a pleural effusion, in which case the fluid will tend to be in the lower posterior zones. Some critically ill patients may, however, not be able to sit up to enable assessment of the posterior zones. In this case, the posterior surfaces can be scanned either directly or indirectly (see section on Supplementary scanning techniques).

FTUS examination technique Once the machine has been prepared for the examination and the patient has been positioned in the most optimal position possible, the FTUS examination can be performed. The transducer is placed in the first of the scanning zones in the vertical plane above an ICS with the orientation marker facing cranially (figure 1). The operator then notes whether PTX, pleural effusion, multiple B-lines or other obvious pathology is present. Once this has been assessed, the transducer is moved to the next scanning zone, and this approach continues until all accessible zones have been scanned. https://doi.org/10.1183/2312508X.10006117

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Specific transducer placement and findings for each scanning zone

Each zone scanned as part of the 14-zone FTUS protocol has some special characteristics and potential pitfalls. Some of these are described for each zone. Zones R1 and L1 Transducer placement: the transducer should be placed in the second ICS a few centimetres lateral to the sternum. If the transducer is placed too far laterally, additional tissue (e.g. muscle, breast) will be present between the transducer and the pleura, possibly decreasing image quality.

Zone findings: these resemble the basic sonoanatomy pattern described previously (figure 2). Zone R2 Transducer placement: when moving the transducer from zone R1 to R2, the transducer is moved to ICS4 a few centimetres lateral to the sternum. The anatomical landmark is the lower edge of the pectoralis muscle or breast tissue. In most persons, this point corresponds to the anterior phrenicocostal sinus, and both the pleural line and the superficial part of the diaphragm can be visualised. In some patients, pericardium or mediastinal tissue will be visible instead of the pleural line. Moving the transducer a few centimetres laterally will often allow visualisation of the pleural line.

Zone findings: zone R2 findings consist of the pleural line on the left of the screen and the diaphragm and liver on the right of the screen. Zone L2 Transducer placement: when moving the transducer from zone L1 to L2, the transducer should gradually be moved caudally one ICS at a time until the pericardium and heart appear on the right side of the screen. This approach reduces the risk of misinterpreting the pericardium as the pleural line. In patients with hyperinflation of the lungs or emphysema, the lung may obscure the view of the pericardium and heart. Zone L2 findings then often resemble the findings in zone R2.

Zone findings: zone L2 findings consist of the pleural line on the left of the screen and the pericardium and heart on the right. Zone R3 Transducer placement: assessment of zone R3 should always begin with identification of the liver, right kidney and diaphragm. Most often, this can be done by placing the transducer in the midaxillary line on the lower part of the chest. Once the liver has been identified, the pleural line can be identified either by asking the patient to take a deep breath or by gradually moving the transducer to an ICS cranially until the pleural line can be visualised.

Zone findings: zone R3 findings consist of the pleural line on the left of the screen and abdominal structures on the right of the screen (figure 6). When the patient takes a deep breath, the pleural line is seen moving in from the left with “removal” of the liver due to posterior shadowing and movement of the diaphragm. This finding is also termed the “curtain sign” since it resembles a curtain being drawn, obscuring the view to the abdominal structures [63–67]. 22

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Zone L3 Transducer placement: assessment of zone L3 should also always begin with identification of the structures in the upper abdomen (e.g. spleen, left kidney) and diaphragm. Since the spleen is smaller and more posteriorly located than the liver, the transducer should be placed more posteriorly in zone L3 than when assessing zone R3. Most often, this can be done by placing the transducer in the posterior axillary line on the lower part of the chest. In the supine patient, this can be achieved by simply resting the hand with the transducer on the underlying mattress and then scanning the left side of the thorax at that point. Once the spleen and left kidney have been identified, the pleural line can be identified either by asking the patient to take a deep breath or by gradually moving the transducer to an ICS cranially until the pleural line can be visualised.

Zone findings: zone L3 findings consist of the pleural line on the left of the screen and the spleen (and left kidney) on the right of the screen. Movement of the lung during breathing also appears as the “curtain sign” on the left side. When fluid is present in the stomach, it can sometimes also be seen, even though a more posterior approach has been used. Zones R4 and L4 Transducer placement: the transducer should be placed in approximately ICS3 in the midaxillary line. This is often the area with the shortest distance between the transducer and the pleural line. When scanning zone 4, there is often a tendency to have the transducer footprint tilted in a cranial direction; in the corresponding US image, the pleural line will be angulated rather than horizontal. If this is the case, the transducer should be tilted until the pleural line is horizontally placed.

Zone findings: zone 4 findings on both sides resemble the basic pattern described previously (figure 2). Zones R5 and L5 Transducer placement: assessment of zones R5 and L5 should always begin with identification of the upper abdominal structures (e.g. liver/spleen, right/left kidney) and

Figure 6. Sonoanatomy when assessing zone R3 and the upper abdomen on the right side. The liver (Lvr), right kidney (RK) and diaphragm (D) can be visualised. The pleural line (PL) is seen in the top left corner with posterior shadowing (*). The movement of the pleural line causes the shadowing to obscure the view to the upper abdomen when the patient takes a deep breath. This is known as the “curtain sign”.

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diaphragm. This can be done by placing the transducer at the lower part of the chest at a vertical line corresponding to the tip of the scapulae (inferior angle). If the transducer is placed too medially, the distance between the transducer and the pleura will be longer, and since the surface of the pleura is no longer perpendicular to the surface of the thorax, the pleural line will often appear thickened, mimicking pathology. Once the liver has been identified, the pleural line can be identified either by asking the patient to take a deep breath or by gradually moving the transducer to an ICS cranially until the pleural line can be visualised. Zone findings: zone R5 findings consist of the pleural line on the left of the screen and the liver and upper abdominal structures on the right of the screen. Zones R6 and L6 Transducer placement: the transducer is placed in the posterior midclavicular line at a level corresponding to the middle part of the scapulae. The best images can generally be obtained by placing the transducer as close to the medial border of the scapulae as possible. An additional area of the pleura can be assessed in zone 6 if the patient is asked to place the hand of the side being scanned on the opposite shoulder, causing the scapula to move and rotate laterally.

Zone findings: these resemble the basic sonoanatomy pattern described previously (figure 2). When compared with zone 5, the distance between the ribs is shorter and the extent of lung sliding is often less pronounced. Zones R7 and L7 Transducer placement: the transducer is placed in the posterior midclavicular line at a level corresponding to the cranial part of the scapulae. The best images can generally be obtained by placing the transducer as close to the medial border of the scapulae as possible. An additional area of the pleura can be assessed in zone 7 if the patient is asked to perform the same manoeuvre as described for zone R6/L6.

Zone findings: zone 7 findings on both sides resemble the basic pattern described previously (figure 2). When compared with zone 6, additional muscle tissue is often present between the transducer and the pleural line, the distance between the ribs is often even shorter and the extent of lung sliding is often additionally decreased. In patients with small tidal volumes, lung sliding cannot always be identified in zone 7. If doubt exists as to whether lung sliding is present or absent, it is often helpful to compare the findings with zone 7 on the opposite side. Supplementary scanning techniques

Assessment of the posterior zones is not always possible (e.g. critically ill patients, trauma patients). The posterior surfaces can then be scanned either directly or indirectly. Direct assessment can be performed with the patient lying on their side, in a decubitus position, or alternatively the transducer can be inserted in between the mattress and the patient, making it possible to scan at least part of the posterior surface. The indirect approach involves use of the liver and spleen as acoustic windows in order to identify the presence of the “spine sign” [22]. 24

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“Thoracic spine sign” principle When using the liver or spleen as an acoustic window, the deeper or tendinous parts of the diaphragm can be identified. The area located above the diaphragm represents the pleural cavity and the lung. When scanning healthy persons, the area is seen as a hypoechoic area with posterior shadowing due to the air in the lung. Mirror artefacts may be present.

In patients with pathology in the lower posterior part of the pleural cavity (e.g. pleural effusion, consolidation of the lower lobe), the normal air-filled lung is replaced by fluid or tissue. Since the US signal is no longer reflected, the structures can be assessed using US, which enables visualisation of the underlying thoracic spine. The visualisation of an extended part of the thoracic spine is thus an indirect marker of pathology in the lower posterior part of the pleural cavity. This finding is known as the presence of the “V-line” or “thoracic spine sign” (figure 7), and has a high diagnostic accuracy for the diagnosis of clinically relevant pleural effusion in the supine patient [68, 69].

Identification of the thoracic spine sign in zone R3 Initially, the transducer should be placed as described for zone R3. With the transducer in the midaxillary line, an image should be obtained in which the liver is placed in the middle of the image. The depth should be increased in order to allow visualisation of the profound parts of the diaphragm and underlying spine (if visible).

The direction of the US beam is then aimed in a more posterior direction by panning the transducer. For inexperienced operators, it can be of help to look at the patient and positioning of the transducer, which is placed in the midaxillary line so that it is pointing towards the spine. When the correct image has been obtained, the liver, right kidney, diaphragm and underlying spine can be identified in the same image. The spine is typically seen as a horizontal, wavy, hyperechoic line where the individual vertebrae can often be identified. Once this image has been obtained, it can be noted whether the visualised spine below the liver and kidney can also be identified deep to the diaphragm. a)

b)

Figure 7. The “thoracic spine sign”. a) Normal findings in zone R3. The structures of the upper abdomen (liver (Lvr) and right kidney (RK)) can be used as an acoustic window to visualise the spine (blue line). Due to shadowing from the normal aerated right lung, the spine cannot be visualised in the area cranial to the liver (arrowhead). b) The vertebrae (blue lines) located below the upper abdominal organs can be as in a. The presence of pleural effusion (Eff ) allows visualisation of the vertebrae (yellow lines) cranial to the liver. The visualisation of these vertebrae is known as the presence of the “thoracic spine sign”.

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Identification of the thoracic spine sign in zone L3 Identification of the spine sign on the left side uses the same principles as described in the previous section. However, it may be more difficult to obtain an optimal view on the left side. Due to the smaller size of the spleen, the transducer is often placed more posteriorly than on the right side. If it is still not possible to obtain an adequate image, moving the transducer slightly caudally and aiming the US beam slightly cranially by tilting the transducer often improves the image.

Adaptation for the given setting

Since FTUS is used in critically ill patients in a variety of settings (e.g. pre-hospital, emergency department, ICU, operating room), it may not always be possible to perform a standardised FTUS examination. Thus, the standard protocol may sometimes be modified for the given setting. By using FTUS in a standardised and systematic approach, its clinical utility remains high, and the diagnosis and exclusion of important diagnoses, such as PTX, pleural effusion and interstitial syndrome, are often still possible.

Thoracic ultrasound In contrast to FTUS, the purpose of TUS is to perform a comprehensive ultrasonographic assessment of the lungs and adjoining anatomical structures, such as the pleural cavities, parietal pleura, thoracic wall, supra- and infraclavicular regions, diaphragm and mediastinum. TUS remains based on the same overall principles as for FTUS. Differences and aspects regarding equipment, preparation and examination technique do exist, some of which are discussed in the following sections. More specific descriptions of the technique and findings when performing TUS are discussed in subsequent chapters in this Monograph.

Equipment

Often the equipment required for performing FTUS can also be used for TUS. Dedicated high-end US machines may, however, be needed for increased image quality and supplementary scanning modes.

Choice of transducer

FTUS can often be performed using only one transducer for the examination. When performing TUS, changing between different transducers during the examination can be useful in order to obtain additional information. The interchangeable use of a curved low-frequency transducer and a high-frequency linear transducer is often an excellent combination due to optimal image quality when a given structure is assessed. The smallersized microconvex transducers excel as an alternative when the patient can only be examined in the supine position. Phased array transducers are generally less suitable but may be of use in patients with complex pleural effusions, since the characteristics of the transducer make it ideally suited for identifying septa within a pleural effusion. Due to its small footprint, a phased array transducer is also useful when assessing the mediastinum. 26

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Pre-set

Since TUS may be performed to assess a wide variety of different deep and superficial structures, the pre-set should continuously be altered whenever a new organ or anatomical structure is assessed. If no predefined TUS pre-set is available, an abdominal pre-set is often useful for deeper structures (e.g. lung, pleural effusion) and a musculoskeletal pre-set for superficial structures (e.g. chest wall, parietal pleura). Software

Supplementary software (e.g. harmonics, cross-beam) is generally useful when assessing most of the anatomical structures examined but should be turned off when assessment of artefacts is performed (e.g. B-lines). US scanning modes

2D-mode scanning is by far the most widely used mode when performing TUS. Supplementary M-mode can be used for measuring purposes (e.g. amplitude of diaphragmatic movement), and is recommended by some experts in cases where there is doubt as to whether PTX is present or not [4, 5, 70]. Colour Doppler mode assessment is a useful adjunct to the conventional B-mode scanning. Doppler mode can be used to assess vascularisation of lung parenchymal pathology, lymph nodes and vessels. Other US modes that can be used as part of more highly specialised sonography are spectral analysis, CEUS, elastography and image fusion. Examination technique

The basic TUS principles are the same as for FTUS. When performing TUS, the entire surface of the thorax, pleura and lungs is assessed, and each ICS is thoroughly examined in each zone. The use of scanning zones when performing TUS is used primarily as a tool to describe and document the position of findings, as an alternative to describing the location using other anatomical landmarks (e.g. ICS4, midaxillary line). Additionally, the use of the same scanning zones for FTUS and TUS facilitates the comparison of reports and a stepwise approach to learning FTUS/TUS, and also strengthens the multidisciplinary use of FTUS/TUS. Other areas assessed

As well as assessment of the thoracic wall, pleural cavities and lungs, the TUS examination can be supplemented with assessment of other anatomical structures and organs, such as the neck and supra- and infraclavicular regions, the diaphragm, the upper abdomen, the mediastinum and the heart. Assessment of these structures is described in later chapters in this Monograph [71–75]. Patients in which TUS reveals incidental findings in other adjoining structures (e.g. heart, upper abdomen) should generally be referred for subsequent assessment and imaging by a relevant specialist trained in diagnostic US (e.g. echocardiography, diagnostic abdominal US) of the given structure. https://doi.org/10.1183/2312508X.10006117

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Conclusion Most literature and published studies regarding FTUS and TUS have been classical diagnostic accuracy studies and, to a lesser extent, studies assessing clinical impact. The art of integrating the US examination into the clinical context is seldom discussed, even though this is probably the most difficult skill to learn. Any physician performing FTUS or TUS should be well aware of and respect the limitations of the US examination in itself and the limitations in the physician’s own skills and experience. As well as training in practical US skills, inexperienced physicians should also focus on the art of integration of imaging into clinical practice.

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Decreased sensitivity of lung ultrasound limited to the anterior chest in emergency department diagnosis of cardiogenic pulmonary edema: a retrospective analysis. Crit Ultrasound J 2010; 2: 47–52. 50. Jensen MB, Sloth E, Larsen KM, et al. Transthoracic echocardiography for cardiopulmonary monitoring in intensive care. Eur J Anaesthesiol 2004; 21: 700–707. 51. Perera P, Mailhot T, Riley D, et al. The RUSH exam: Rapid Ultrasound in SHock in the evaluation of the critically ill. Emerg Med Clin North Am 2010; 28: 29–56. https://doi.org/10.1183/2312508X.10006117

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ERS MONOGRAPH | THORACIC ULTRASOUND 52. Breitkreutz R, Price S, Steiger HV, et al. Focused echocardiographic evaluation in life support and peri-resuscitation of emergency patients: a prospective trial. Resuscitation 2010; 81: 1527–1533. 53. Janssen S, Basso F, Giordani MT, et al. Sonographic findings in the diagnosis of HIV-associated tuberculosis: image quality and inter-observer agreement in FASH vs. remote-FASH ultrasound. J Telemed Telecare 2013; 19: 491–493. 54. Volpicelli G, Lamorte A, Tullio M, et al. Point-of-care multiorgan ultrasonography for the evaluation of undifferentiated hypotension in the emergency department. Intensive Care Med 2013; 39: 1290–1298. 55. Davidsen JR, Bendstrup E, Henriksen DP, et al. Lung ultrasound has limited diagnostic value in rare cystic lung diseases: a cross-sectional study. Eur Clin Respir J 2017; 4: 1330111. 56. Davidsen JR, Laursen CB, Bendstrup E, et al. Lung ultrasound – a novel diagnostic tool to phenotype chronic lung allograft dysfunction? Ultrasound Int Open 2017; 3: E117–E119. 57. Nazerian P, Vanni S, Volpicelli G, et al. Accuracy of point-of-care multiorgan ultrasonography for the diagnosis of pulmonary embolism. Chest 2014; 145: 950–957. 58. Nazerian P, Volpicelli G, Gigli C, et al. Diagnostic performance of Wells score combined with point-of-care lung and venous ultrasound in suspected pulmonary embolism. Acad Emerg Med 2017; 24: 270–280. 59. Nazerian P, Volpicelli G, Vanni S, et al. Accuracy of lung ultrasound for the diagnosis of consolidations when compared to chest computed tomography. Am J Emerg Med 2015; 33: 620–625. 60. Nandipati KC, Allamaneni S, Kakarla R, et al. Extended focused assessment with sonography for trauma (EFAST) in the diagnosis of pneumothorax: experience at a community based level I trauma center. Injury 2011; 42: 511–514. 61. Cibinel GA, Casoli G, Elia F, et al. Diagnostic accuracy and reproducibility of pleural and lung ultrasound in discriminating cardiogenic causes of acute dyspnea in the emergency department. Intern Emerg Med 2012; 7: 65–70. 62. Alerhand S, Graumann O, Nelson BP. Physics and basic principles. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 1–13. 63. Targhetta R, Bourgeois JM, Balmes P. Echographie du pneumothorax. [Echography of pneumothorax.] Rev Mal Respir 1990; 7: 575–579. 64. Targhetta R. Ultrasonographic approach to diagnosing hydropneumothorax. Chest 1992; 101: 931–934. 65. Lin FC, Chou CW, Chang SC. Differentiating pyopneumothorax and peripheral lung abscess: chest ultrasonography. Am J Med Sci 2004; 327: 330–335. 66. Mayo PH, Doelken P. Pleural ultrasonography. Clin Chest Med 2006; 27: 215–227. 67. Lee FCY. The curtain sign in lung ultrasound. J Med Ultrasound 2017; 25: 101–104. 68. Atkinson P, Milne J, Loubani O, et al. The V-line: a sonographic aid for the confirmation of pleural fluid. Crit Ultrasound J 2012; 4: 19. 69. Dickman E, Terentiev V, Likourezos A, et al. Extension of the thoracic spine sign: a new sonographic marker of pleural effusion. J Ultrasound Med 2015; 34: 1555–1561. 70. Lichtenstein D, Mezière G, Biderman P, et al. The “lung point”: an ultrasound sign specific to pneumothorax. Intensive Care Med 2000; 26: 1434–1440. 71. Ferrari G, Helbo Skaarup S, Panero F, et al. The diaphragm. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 129–147. 72. Posth S, Graumann O. The upper abdomen. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 148–160. 73. Herth FJF. The mediastinum. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 161–171. 74. Kristensen MS, Teoh WH. Ultrasound of the neck for airway management. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 172–183. 75. Via G, Dean A, Casso G, et al. Focused cardiac ultrasound. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 184–205.

Disclosures: None declared.

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| Chapter 3 Chest wall and parietal pleura Maged Hassan1,2,3 and Najib M. Rahman1,2,4 US examination of the chest wall and parietal pleura can reveal a number of pathologies and is useful in various clinical settings. Chest wall pathologies that are identifiable during US examination include haematomas, abscesses, rib abnormalities and lymph nodes. Additionally, useful information about pleural infection and neoplasia can be gathered using US. In addition to its diagnostic potential, US provides guidance for safe execution of percutaneous sampling and/or drainage of chest wall and pleural abnormalities. Cite as: Hassan M, Rahman NM. Chest wall and parietal pleura. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 31–42 [https://doi.org/10.1183/2312508X.10006217].

P

erforming TUS for examination of the chest wall and pleura is indicated in a number of situations. In many instances, it is used to explore further and examine in more detail pleural or parietal abnormalities first seen on a chest CT scan. In other situations, TUS is used up front, particularly for evaluation of patients with localised thoracic lesions. It is the investigation of choice to first characterise palpable chest wall lesions that are picked up during clinical examination [1]. In patients with chest trauma, TUS can detect chest wall, pleural and lung injuries with high sensitivity [2]. TUS is especially valuable in delineating chest wall/pleural involvement by peripheral pulmonary masses, which has an important implication for staging. Finally, TUS is usually preferred to CT for guidance of invasive drainage and biopsy procedures due to its safety profile, live procedural ability and lower cost [3].

Technical considerations The exact technique of chest sonographic examination, as well as the physics of TUS, is covered elsewhere in this Monograph [4, 5]. Generally speaking, examination of the chest wall and parietal pleura can be achieved with a combination of low-frequency probes (range 3.5–5 MHz), a convex array (curvilinear) or phased array (sector) probe, and higher-frequency linear array probes (range 5–7.5 MHz) [6–8].

1 Oxford Centre for Respiratory Medicine, Oxford University Hospitals NHS Foundation Trust, Oxford, UK. 2Oxford Respiratory Trials Unit, Nuffield Dept of Medicine, University of Oxford, Oxford, UK. 3Chest Diseases Dept, Faculty of Medicine, Alexandria University, Alexandria, Egypt. 4Oxford NIHR Biomedical Research Centre, Oxford, UK.

Correspondence: Maged Hassan, Oxford Centre for Respiratory Medicine, Churchill Hospital, Old Road, Oxford OX3 7LE, UK. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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Chest wall anatomy and pathology are ideally appreciated with a linear probe, given the superficial position of the chest wall [9]. Some sonographers find the phased array probe useful when examining the pleura and lung in patients with narrow intercostal spaces [6]. This probe is especially useful for moving structures, such as the heart. The convex probe, however, is generally the preferred probe for pleural and peripheral lung examinations, and is particularly superior to the phased array probe during guidance of invasive procedures [10, 11]. This is because the phased array probe has a narrow footprint, which misses large parts of the superficial layer of the chest wall and consequently cannot capture a portion of the invading needle. Most of the TUS examination of the chest wall and pleura is conducted in the B-mode [7]. M-mode examination is not particularly useful except for exclusion of pneumothorax (PTX) following biopsy, given that it is a mode that captures movement. In addition to grey-scale imaging, colour Doppler is important for delineation of the vascular pattern of lesions, which is an essential component of characterisation and diagnosis. Doppler is used to identify the intercostal artery, which is necessary to minimise the risk of vascular injury during percutaneous invasive interventions [10, 12]. During TUS examination, the authors prefer to orient the scanning probe parallel to the ribs to obtain the maximum view of the pleura and to avoid the acoustic shadowing created by the ribs (figure 1b). The perpendicular probe orientation is useful mainly during examination of the acutely breathless patient in order to identify and quantify the number of intercostal comet tail artefacts, which is helpful in the diagnosis of pulmonary oedema [13]. As well as this indication, the parallel orientation should be followed during examination of the chest wall, pleura and lung to maximise the acoustic window.

a)

b)

1 2

1 2

3

3

4

4

6

6

5

Figure 1. Layers of the chest wall as seen using a high-frequency linear probe. a) Parallel orientation; b) perpendicular orientation. 1: skin; 2: s.c. fat; 3: muscles; 4: intermuscular septum; 5: outer rib cortex (with acoustic shadow seen deeper); 6: pleural band.

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Chest wall Anatomy

The chest wall is composed of four layers: the skin, s.c. fat, various layers of chest wall muscles, and ribs and intercostal muscle [14]. Very detailed anatomical images are made possible by high-frequency TUS (figure 1a). The skin appears as a thin isoechoic layer followed by s.c. fat, which is hypoechoic with interposing isoechoic fascial septa [12]. On TUS, muscles appear as generally hypoechoic with echogenic striae and dots depending on the orientation of the muscle fibres [12]. Different muscles are separated by dense fascial septa that appear hyperechoic. The outer cortex of ribs is hyperechoic, and since it causes reflection of most of the US waves, all deeper structures are obscured and only an anechoic shadow of the overlying rib (termed an acoustic shadow) is seen (figure 1b). The intercostal vessels run between intercostal muscles. They run in the middle of the space in the most medial 5 cm of their course anteriorly and posteriorly. For the rest of the course, the neurovascular bundle is hidden under the lower border of the superior rib, which makes it elusive for TUS identification. Some subjects have an aberrant course, especially in the elderly, and excluding the presence of an unprotected artery in the pleural space is essential before interventional pleural procedures (figure 2). Pathology

The majority of chest wall lesions tend to be localised [12]. TUS has the potential to uncover lesions that are too subtle to be picked up on conventional CXRs. This makes TUS the investigation of choice in patients with localised pleuritic pain or a palpable lesion [15]. The range of chest wall lesions that can be identified by TUS is summarised in table 1 [1, 7, 10]. As mentioned previously, grey-scale images should ideally be complemented with colour Doppler scanning for identification of the vascular pattern of a given lesion [12]. Soft tissue lesions Commonly identified lesions include lipomas, haematomas and lymph nodes. The combination of grey-scale findings and the colour Doppler pattern supplemented by

a)

Figure 2. Colour Doppler impulse indicating the position of the intercostal artery (arrow) just superficial to the pleura.

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Table 1. Pathological chest wall lesions identifiable by TUS Soft tissue lesions Fluid collection (e.g. haematoma, abscess) Tumours Benign (e.g. lipoma, fibroma) Malignant (e.g. sarcoma, metastasis, invasion from lung/pleura) Lymph nodes (inflammatory, infective or malignant) Bony lesions Fractures Metastatic deposits

clinical data can facilitate reaching a provisional diagnosis. A biopsy/aspiration is usually required for definitive diagnosis, and this is generally conducted with US guidance. Fluid formations usually adapt to the shape of the surrounding more rigid structures [10]. Haematomas, commonly seen in trauma patients, can have various degrees of echogenicity depending on the erythrocyte content and can exhibit denser echoes due to organisation in older lesions [1]. Chest wall abscesses show heterogeneous echoes, which makes differentiation from organising haematomas challenging, particularly because of the tendency of undrained haematomas to be complicated by infection. The presence of a capsule surrounding the abscess facilitates differentiating the lesion from an organised haematoma [1]. Thoracic lymph nodes arise in the context of various inflammatory/infective conditions, lymphoma and lymph node metastases (table 1). Each of these three categories has distinctive sonographic features [7]. Characterisation depends on the grey-scale features, as well the vascular pattern seen by Doppler [16]. Reactive lymph nodes typically appear oval or triangular, with preserved architecture and an intact capsule [6, 7]. Their size rarely exceeds 20 mm and they have central regular vascularisation [1]. Lymph node metastases appear as round to oval structures with irregular borders and occasional infiltration of surrounding tissues [6, 17]. They show a “corkscrew” pattern of vascularisation [18]. In lymphoma, lymph nodes appear rounded or sharply bordered with irregular vascularisation but without infiltration of the surrounding tissues [1, 7]. It is important to note, however, that these findings are only suggestive of the aetiology and should be considered along with the clinical data. Histopathological confirmation is warranted in most cases, as US appearances can be nonspecific [19]. Malignant infiltration of the chest wall by distinct nodules or by extension from the lung and pleura is accurately delineated by TUS [20]. Malignant space-occupying lesions commonly appear hypoechoic with occasional hyperechoic parts (figure 3). Studying the vascular pattern of a chest wall swelling can suggest malignancy if an irregular pattern is identified by colour Doppler examination [1]. Colour Doppler is valuable during the planning of biopsies from a suspected swelling, which is an attractive target for invasive sampling due to its superficial position. Infiltration of the chest wall and pleura by peripheral lung cancers has important implications for staging and subsequent treatment choice. TUS can accurately identify chest wall infiltration by demonstrating features such as fixation of the tumour during breathing, 34

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Figure 3. A hypoechoic, poorly defined, malignant s.c. nodule (arrow).

and disruption and infiltration of the parietal pleura (figure 4) [21]. It has been shown that TUS has superior sensitivity to CT in assessing chest wall involvement by lung cancer when pathological examination of surgically resected tumours is used as the gold standard [22]. Bony lesions Chest wall examination by US is usually conducted in the setting of a blunt chest wall trauma or to evaluate suspected rib deposits. Normal ribs appear as well-defined hyperechoic curved structures with an acoustic shadow seen deeper to them (figure 1a). A wide array of manifestations secondary to blunt trauma to the chest wall are identifiable by US, including rib/sternal fractures, myocardial contusion, PTX and haemothorax [2, 23, 24].

Rib fractures are more amenable to detection by TUS than by chest radiography, with a 50% increase in diagnostic sensitivity with TUS [7, 19]. Directing TUS examination to areas of maximum pain helps in delineating rib fractures [1]. Fractures are primarily diagnosed by the presence of a discontinuity (or a gap) in the outer cortex of the rib, or by the presence of a “step” if the fracture has become dislocated. Bone fragments can sometimes be visible on TUS. In nondisplaced fractures, or where there are gaps that are Needle Nee d le dle lengt length ngth ngt h

Figure 4. Peripheral lung carcinoma. Clear invasion and destruction of the pleura can be seen. Note the edge of the normal pleura (arrow).

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smaller than the lateral resolution of the TUS probe, the fissure can be identified by the presence of a reverberation artefact, known as the “chimney” phenomenon [23]. Auxiliary findings that lend support to a diagnosis of rib fracture include soft tissue haematoma, an associated pleural collection, lung contusion and PTX [2, 24]. The presence of s.c. emphysema is encountered occasionally with rib fractures, and despite being readily diagnosed clinically, its presence imposes significant limitations on full TUS examination of deeper structures due to the scattering of US waves by s.c. air (figure 5) [25]. Osteolytic rib deposits are identified as disruptions of the rib cortex, which is replaced by an inhomogeneous lesion that is invariably associated with an increase in adjacent soft tissue [7]. Colour Doppler examination may in addition reveal the presence of neovascularisation, assuming a “corkscrew” or spiral configuration [1]. In addition to its diagnostic value, TUS can be used to gauge the response to therapy in osteolytic lesions secondary to malignancies such as multiple myeloma and breast cancer. The superficial location of such structures renders them easily accessible to serial TUS to monitor changes in size or morphology of the osteolytic lesion as part of the monitoring of the tumour response. The intercostal artery does not invariably follow the classical course described in the anatomic literature but may instead follow an aberrant course in a considerable minority of cases [26]. TUS has been demonstrated to be an accurate tool at the bedside to screen for a vulnerable intercostal artery for physicians who perform thoracentesis, chest-drain insertions and TUS-guided pleural biopsies [27]. This is especially valuable in patients with increased risk of bleeding. In addition to pre-procedure planning for the intervention site, TUS can identify any procedure-related bleeding early, which expedites the process of timely management [28].

Pleura Anatomy

The pleural membrane is the deepest layer of thoracic wall that is amenable to anatomic characterisation by TUS. Aerated lung causes scattering of the US impulses, and anatomic

Needle Nee dle le lengt length ngth

Figure 5. Subcutaneous air at different layers of the chest wall (arrows). Note the two sets of reverberation artefacts, which are repetitions of the air lines.

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visualisation of lung parenchyma is only visible if air is pathologically replaced by another material. In normality, a reverberation artefact of the pleural line is seen to be repeated at equal distances equivalent to the skin–pleura distance further down the screen. The normal pleura is only 0.2–0.4 mm thick [8]. The two layers of pleura are identified as an echogenic band deeper to the intercostal muscles (figure 1) that is seen to be moving or shimmering on real-time viewing; this is the so-called “pleural slide”. The thickness of this echogenic band that represents the pleura is exaggerated by the movement of the two layers of pleura as well the movement of underlying lung and is usually found to be 2 mm [29]. Care should be taken not to mistake the pleural band for the intermuscular septum, which occasionally is encountered in subjects with thick chest walls (figure 1a). Gliding of the pleura is key for correct identification. High-definition US can delineate a two-layered membrane, which corresponds to the combination of parietal pleura and endothoracic fascia [30, 31]. An echo-free band is occasionally noted inside the pleural line, and this is thought to represent the actual pleural space [8]. The normally very thin visceral pleural is not visualised by TUS due to the fact that it is obscured by the complete reflection of sound waves off the lung interface [19, 29]. A hypoechoic layer, which corresponds to extrapleural fat, is normally seen superficial to the parietal pleura, and the thickness of this layer varies among individuals (figure 1) [6]. A thorough examination of the costal pleura is usually feasible with TUS. The diaphragmatic pleura is accessible to US examination via the transabdominal approach, and this is especially true on the right side due to the excellent sonographic window that the liver provides. Parts of the apical and mediastinal pleurae are partially assessable sonographically via the supraclavicular and parasternal approaches, respectively. It has been estimated, based on comparison between multiple CT cuts and full TUS examination, that the latter can visualise 60–70% of the pleural surface [8]. Pathology

The pleural pathology manifests either as exudation of effusion or pleural swelling [8]. Several benign and malignant processes can be seen by TUS. In addition, TUS can guide the process of sampling abnormal pleura in cases of suspected malignancy or for microbiological evaluation of nonresolving or tuberculous infection. Pleural thickening, nodularity and calcification are among the sonographic features of pleural disease. Benign disease Pleuritis can usually be identified on TUS by an abnormally rough crenulated appearance with some degree of thickening. The abnormal pleura generally looks hypoechoic with loss of the normal smooth texture. The presence of subpleural consolidation or small pleural effusions increases diagnostic certainty. Colour Doppler examination is not sensitive enough to pick up increased pleural vascularity associated with pleural inflammation [29]. CEUS, which remains an experimental technique in pleural disease, has shown promising results in identifying pleurisy, with some data suggesting sensitivity nearly comparable to that of contrast-enhanced CT in identifying enhanced pleural inflammation due to infection [32].

Long-standing inflammation leads to fibrosis of various degrees. It has been conventionally considered that thickening of 1 cm, contrast enhancement or the presence of a newly identified malignant-looking shadow [33]. The accuracy of TUS to identify pleural malignancy based on some of these CT criteria has been examined, using liver deposits as a marker of extrathoracic metastasis. When compared with final ( pathological or clinicoradiological) diagnosis, TUS had a sensitivity of 73% and specificity of 100% [21]. Mesothelioma CT is the main radiological investigation for evaluation of mesothelioma. Features such as circumferential pleural encasement of the lung, involvement of the mediastinal pleura and pleural nodules superimposed on pleural thickening favour the likelihood of mesothelioma over metastatic pleural disease [39]. However, these appearances are not specific enough to confidently exclude pleural metastasis [35]. Definitive differentiation of mesothelioma from metastatic pleural malignancy based on CT alone is not possible [7]. Using TUS, irregular, partly angular pleural thickening can be seen. Frequently, mesothelioma appears as extensive nodular growth with or without chest wall invasion. TUS is highly sensitive to chest wall and diaphragm invasion, and is superior to CT in this regard. TUS is a useful tool to direct potential biopsy sites of abnormal pleura. Pleural sliding and interventions

Sliding of the pleural membranes is a key feature used to confidently exclude the presence of PTX. In addition, the presence of sliding suggests that the lung is not tethered to the chest wall, which can be valuable information for physicians planning to perform LAT [40]. In patients requiring a pleural biopsy, lack of pleural sliding indicates probable failure of lung collapse after accessing the pleural space, which is necessary to execute LAT [41]. In this situation, input from the pre-procedure TUS can lead to conversion of the procedure from LAT to an image-guided biopsy [11]. Practitioners who are experienced with LAT can perform the procedure in the absence of any effusion by inducing PTX before the procedure. This is ideally performed after confirming the presence of lung sliding using TUS, and TUS can be used “on table” to confirm the formation of PTX during the procedure [42].

Conclusion TUS is a highly useful technique for the diagnosis and sampling of chest wall and pleural pathologies. As an increasing number of physicians are trained in TUS, it has become a central part of many diagnostic pathways in the emergency/acute setting, as well as now being an indispensable tool for specialist management of pleural disease.

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Disclosures: None declared. Support statement: Maged Hassan is a recipient of the European Respiratory Society Long-term Research Fellowship – ERS LTRF 2016-7333.

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| Chapter 4 Pneumothorax Nils Petter Oveland Pneumothorax (PTX) is common after blunt chest injury, and failure to diagnose and rapidly treat an enlarging PTX may cause patient death. The anteroposterior supine CXR is the least sensitive of all plain radiographic techniques for detecting PTX. Occult PTX (i.e. if missed on CXR) may subsequently be found by CT scans, but both of these diagnostic tools are not readily available for the patient, include a radiation hazard, and have a time delay between ordering and obtaining results. TUS is a harmless point-of-care examination to accurately diagnose PTX. The main message in this chapter is that TUS is a safe and highly accurate diagnostic tool to diagnose PTX and can be used to assess PTX progression. With the appropriate training, all clinicians can perform US examinations to detect PTX, which suggests that this technique should be used as a diagnostic adjunct to the clinical examination of patients with respiratory distress. Cite as: Oveland NP. Pneumothorax. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 43–63 [https://doi.org/10.1183/ 2312508X.10006317].

T

he topic of TUS detection of pneumothorax (PTX) can be elucidated by two clinical scenarios.

In the first scenario, you are an air ambulance doctor on call at a level 2 trauma centre. During your shift, you are dispatched to a hunting accident where a 14-year-old boy has been shot in the chest and face. When you arrive at the scene 15 min later, the patient is lying on his back on the ground complaining of general chest pain and facial discomfort around his right eye. The clinical examination, including auscultation, shows no respiratory and circulatory instability, but his chest and face have multiple gunshot wounds from the metal pellets. On the way to the hospital, you perform an in-flight TUS examination, which shows no sign of blood in the pericardium, abdomen or thorax. However, you suspect a small PTX in the left lung apex because the normal sliding movement between the two pleural layers is absent and the tip of the lung reappears on the US screen with each breath (figure 1a). Although these US signs of abnormal lung sliding and a visible lung point are subtle, your suspicion is passed on to the trauma surgeon in the emergency department. The supine CXR shows the metal pellets but no PTX (figure 1b). Subsequent CT scans confirm the chest injury caused by the gunshot: a small 5 mm-thick apical PTX (figure 1c). No chest tube is inserted, and the patient is brought to the operating room and intubated

Stavanger University Hospital, Dept of Anaesthesiology and Intensive Care, Stavanger, Norway. Correspondence: Nils Petter Oveland, Gneisveien 1 C, 4027 Stavanger, Norway. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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b) a)

c)

Figure 1. Case scenarios. a) US image of a miniscule apical pneumothorax (PTX) caused by penetrating trauma. The tip of the lung (thick arrow) has detached from the hyperechoic pleural line (thin arrow) as air interposes the parietal and visceral pleural layers (i.e. the definition of a PTX). This lung point moves to and fro along the pleural line, in a manner synchronous with respiration (visible only on video clips). b) CXR showing the multiple metal pellets from the gunshot. The PTX is not visible. c) CT confirming the small amount of intrapleural air displayed as a black pocket in the left lung apex (black arrow). The white arrow shows the lung point. Reproduced and modified from [1] with kind permission from N.P. Oveland.

prior to eye surgery. The patient is closely observed for any clinical deterioration and signs of tension PTX during surgery. In the second scenario, you are dispatched to a motorcycle accident where a 55-year-old male biker has gone off the road and hit a tree at high speed. When you arrive, the paramedics have placed the patient on a backboard, secured his neck with a collar and given him high-flow oxygen through a mask. He is anxious and complains of chest pain and dyspnoea. The clinical examination shows no chest instability, but the respiratory rate is clearly elevated (40 breaths min−1) with symmetrical breath sounds. Peripheral pulses are present and the heart rate is 136 beats min−1 with no signs of external bleeding or long-bone fractures. You perform a rapid sequence intubation, initiate positive-pressure ventilation using a portable respirator and transport the patient by helicopter to a level 2 trauma centre 15 min away. The trauma team there is notified. The initial assessment and supine CXR obtained in the emergency department do not show any thoracic injuries. The CT scan detects unstable L2 and C7 vertebral-body fractures, multiple small rib fractures, a sternum fracture and bilateral small PTXs in the anterior chest. The surgeon on call wants the patient transferred by helicopter to a level 1 trauma centre 70 min away because the vertebral fractures are unstable. You express concern for having a patient in a helicopter 44

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with bilateral PTX undergoing positive-pressure ventilation, and advocate the insertion of chest tubes, but the surgeon disagrees. Because lung auscultation in flight is impossible due to noise, you use the portable US machine to repeatedly scan the anterior chest of the patient every 10 min. The PTX is outlined on the patient’s chest with a pen by marking the US lung point sign (i.e. the edge of the PTX where the lung is still in contact with the interior chest wall). The patient is transported to the level 1 trauma centre without any progression of the PTX on either side. These scenarios show how clinicians are challenged with a diagnostic dilemma when encountering trauma patients, because a physical examination combined with an anteroposterior supine CXR is insufficient to diagnose PTX. Emergent CT scans of the chest can detect all PTX but have disadvantages, such as exposure to radiation. In addition, in settings such as pre-hospital, battlefield and remote areas, clinicians do not have access to these diagnostic modalities. Thus, an accurate mobile method for diagnosing PTX is needed. TUS meets these requirements and can be performed in almost any clinical setting. First, it is a noninvasive, radiation-free, rapid and repeatable bedside diagnostic test that has been shown to be more sensitive than, and equally specific as, supine CXR. Second, TUS can also assess PTX progression, known to be an independent factor of a patient’s later need for chest-tube insertion. This is potentially helpful in real clinical settings, as it may enable clinicians to use US to make treatment decisions.

Pneumothorax Thoracic trauma

Trauma is one of the leading causes of death worldwide (5.1 million deaths in 2010) and can be characterised as a global epidemic because it accounts for one in every 10 deaths [2]. Patients with multiple blunt injuries are far more common in civilian practice, but both penetrating and blunt trauma present significant challenges to national healthcare systems and necessitate a policy action to prevent them [3]. Chest injury is the direct cause of death in 25% of blunt trauma victims and a contributing factor in up to another 50% of trauma deaths [4], which can be explained by the large number of motor vehicle crashes and falls [2, 5]. One serious consequence of chest trauma is PTX, a potential life-threatening condition that sometimes requires immediate treatment to prevent patient death [6]. Although the origin of PTX can be spontaneous, it is trauma patients in particular who present with a respiratory instability that needs immediate diagnosis and treatment. Therefore, this chapter focuses on the basic clinical and diagnostic aspects of traumatic PTX. Cardiothoracic anatomy

The thoracic cage is a bony structure that connects the posterior vertebral column and anterior sternum via the osteocartilaginous ribs. The thorax contains the heart, lungs, great vessels and oesophagus (figure 2), and is demarcated by the diaphragm inferiorly and structures of the neck and lung apices superiorly. The aorta, pulmonary artery, pulmonary veins and vena cava occupy the mediastinum, where they connect to the base of the heart. The heart is contained within the fibrous pericardium, and its apex projects into the left thoracic cavity [7]. In the right and left hemithorax, the pleural sac surrounds each lung: the parietal layer covers the inside of the chest wall and the visceral layer encloses the lung parenchyma. During ventilation, the visceral pleura is brought into contact with the https://doi.org/10.1183/2312508X.10006317

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Figure 2. Illustration of a pneumothorax (PTX) in the right lung and detection by an US probe. PTX is caused by one of the following mechanisms: 1) air leaking from the airways ( proximal or distal conduits) or the alveolar space, 2) air communication between the pleural space and the atmosphere or 3) the presence of gas-producing organisms within the pleura. Reproduced and modified from [10] with permission.

parietal pleura, thereby reducing the pleural cavity to a closed, separate space. This space normally contains only a capillary layer of serous fluid that lubricates the apposed surfaces and reduces friction between the parietal and visceral pleura [8]. The dynamic to-and-fro sliding motion between the layers during respiration is the basis of TUS detection of PTX [9]. Definition

PTX is a common clinical condition where air is present in the pleural space (figure 2). When air separates the parietal and visceral pleural layers, the negative intrapleural pressure that keeps the lungs distended is disrupted, leading to a collapse of the elastic lung parenchyma and expansion of the thoracic cage [11]. Classification

There are different classification categories for PTX (table 1). According to aetiology, PTXs are classified as spontaneous or traumatic. A PTX is classified as primary spontaneous if no obvious precipitating factor is present and as secondary spontaneous if the patient has an underlying disease (e.g. COPD, cystic fibrosis). Traumatic PTX is either iatrogenic (i.e. caused by transthoracic or transbronchial biopsy, central venous catheterisation, pleural biopsy, thoracentesis) or noniatrogenic following a blunt or penetrating chest injury [11]. A PTX can have a wide continuum of severity, ranging from simple asymptomatic PTX caused by disruption of the pleural space to tension PTX associated with increased intrathoracic pressure [7]. The increasing use of CT to investigate thoracoabdominal trauma allows a more precise and three-dimensional evaluation of the thorax. Intrapleural 46

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Figure 3. Occult pneumothorax after blunt chest trauma. The large amount of intrapleural air anterior to the right lung was not visible on the supine CXR but was subsequently diagnosed on the CT scan images. Reproduced and modified from [1] with kind permission from N.P. Oveland.

air not seen on supine CXR is often seen on CT, and this entity is defined as occult PTX (figure 3) [12]. Epidemiology

In addition to rib fractures and pulmonary contusions, PTX is the most common chest injury found in patients with blunt trauma [13, 14]. In a population-based study from Italy, PTX was present in one in every five severely traumatised patients (i.e. an incidence of 81 per 1 million citizens per year) [6]. These results are consistent with a study of chest injuries from the regional trauma centre in Trondheim, Norway, where the most common thoracic injury was rib fracture (55%) and the most common internal thoracic injury was

Table 1. Classification of pneumothorax (PTX) Aetiology

Spontaneous Traumatic

Radiological appearance

Overt Occult

Clinical severity

Simple Tension

Primary: no underlying disease Secondary: associated underlying disease Catamenial: in menstruation due to thoracic endometriosis Iatrogenic: secondary to medical procedures or positive-pressure ventilation Noniatrogenic: secondary to blunt or penetrating chest trauma PTX diagnosed by physical examination or as seen on supine CXR PTX neither diagnosed by physical examination nor seen on supine CXR PTX with nontension physiology PTX with tension physiology resulting in cardiopulmonary collapse (hypotension and hypoxaemia)

Reproduced and modified from [1] with kind permission from N.P. Oveland.

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PTX (24%) [15]. A high incidence of extrathoracic injuries such as head trauma and musculoskeletal injuries in the extremities has also been associated with major blunt trauma [7, 15], and only a minority of patients with PTX (5%) have isolated chest injuries [4]. Furthermore, PTX is associated with greater on-scene physiological instability (i.e. low blood pressure and low oxygen saturation) compared with other chest injuries of similar severity [6]. These findings draw attention to the association between PTX and tension physiology, as well as the potential benefits of decompression procedures.

Tension PTX

If air is allowed to enter (from the lung or through the chest wall) but not exit the pleural space via a “one-way valve”-like opening, tension PTX will quickly develop. The increasing pressure deranges the cardiorespiratory capacity of the patient and makes this an insidious and life-threatening event. This condition is most often seen in pre-hospital, emergency department, trauma unit and critical care settings [16]. The instability of trauma patients with PTX [6] may be explained by the progressive accumulation of air within the pleural space, which exerts mechanical pressure on internal structures. The affected lung may then collapse, with a possible shift of the organs to the contralateral thoracic side. Such a mediastinal shift severely impairs the circulation by pinching the central venous return to the heart (figure 4) and reduces ventilation by compressing the remaining lung. Furthermore, the resulting hypotension and hypoxaemia can lead to cardiac arrest, at which point diagnostic and treatment delays are highly lethal [7, 16, 17]. Thus, PTX is a notable cause of preventable death (i.e. in ∼16% of pre-hospital trauma cases) [6, 18, 19] where simple field-friendly interventions may be lifesaving [20].

Figure 4. Tension pneumothorax on the left side. The expanding intrapleural air mass pushes the heart over the midline into the contralateral right hemithorax, impairing the lung and heart capacity. Image provided by N.P. Oveland.

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Diagnostic evaluation of PTX Clinical examination

The physical examination of the chest includes inspection (looking for signs of injury, symmetry of the thorax, abnormal breathing movements and distended neck veins), palpation (searching for s.c. emphysema, localised chest pain, crepitation, instability of the thorax and tracheal deviation), percussion (tympani or dullness) and finally auscultation ( presence of breathing sounds and lateralisation) [20]. Clinically, PTX is characterised by mild to severe signs and symptoms of chest pain (due to rib fractures), dyspnoea, tachypnoea, cyanosis, tachycardia, hypotension, contralateral tracheal deviation and ipsilateral lung hyperresonance with diminished or absent breathing sounds (figure 5) [7]. To palpate for s.c. emphysema, crepitation from rib fractures, pain and thoracic cage instability combined with measurements of pulse rate, blood pressure and arterial oxygen saturation measurements are helpful [6, 21]. In particular, s.c. emphysema is a strong clinical predictor for concurrent PTX, although this sign is often absent despite injury (i.e. not found in 85% of patients with an actual PTX [22]). Various percussion techniques have also been used to diagnose PTX in mechanically ventilated patients in the intensive care unit [23]. The most reliable part of the physical examination is auscultation of the lungs, because clinical suspicion of PTX is reinforced by diminished or absent breath sounds on the affected side [21, 24]. The diagnostic accuracy improves further if the patient complains of respiratory distress and presents an increased respiratory rate [20]; however, auscultation is often difficult due to environmental noise (e.g. during air transport or in the emergency department [25]) and because unequal breath sounds can be caused by either air (PTX) or blood (haemothorax) within the pleural cavity. Moreover, the physical examination can be misleading, and diagnoses based solely on auscultation fail to detect up to 20–30% of PTX [4, 26]. Although a large PTX can sometimes be identified [26], others may be overlooked but can become clinically relevant [12, 27]. Furthermore, the fact that a high incidence of extrathoracic injuries is associated with blunt trauma makes the diagnosis of PTX even

Respiratory distress Cyanosis Tracheal deviation Diminished breath sounds

Chest pain

Hyperresonance

Figure 5. Clinical manifestations of pneumothorax. Reproduced and modified from [1] with kind permission from N.P. Oveland.

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more challenging. Therefore, diagnostic adjuncts are needed as an extension of the physical examination. Release of air

In some trauma patients, the expedited insertion of a chest tube is necessary. If there is release of air, a characteristic hiss can be heard and used to confirm the correct diagnosis of PTX. However, this invasive procedure is only to be used in physiologically nonpermissive patients who are too unstable to await further diagnostic imaging. Chest radiography

The portable anteroposterior CXR is routinely obtained as the first radiograph in most trauma patients, and through the use of modern digital machines, these pictures are readily available for the medical team [28]. However, both lung fields must be examined carefully for the presence of PTX signs, which include a readily apparent visceral pleural line, depressed diaphragm and the deep sulcus sign (i.e. enlargement of the costophrenic angle) [29]. Furthermore, s.c. air in the soft tissue should not be overlooked, because this is a pathognomonic sign of lung and airway leakage [22]. Injured patients are often confined to the supine position (strapped to backboards) for neuroaxial protection, and the location of a PTX within the chest is directly associated with the force of gravity, the elastic recoil of the lung and the attachment of the lung to the hilar structures. The intrapleural air therefore collects anteromedially in the least-dependent pleural space [30–32]. Air trapped anteriorly and medially to the lung is particularly difficult to detect and quantify on supine CXRs, and even large air pockets may be overlooked at hospitalisation (figure 3) [33]. In one large prospective observational study of multiply injured patients, the incidence of occult PTX was 76% when the supine CXR was interpreted by the trauma team in the emergency department [22]. Most studies refer to board-certified radiologist dictations when reporting the proportions of PTX that are occult (30–55%) [27, 32, 34–37], although the time required to request and obtain the result of a CXR can be as long as 20 min [37]. Therefore, it is the initial interpretations made by the trauma team, and not the delayed dictations by the radiologist, that result in treatment decisions. The conventional supine anteroposterior CXR remains the most available but least sensitive of all plain radiographic techniques for diagnosing PTX [33] and evaluating its extension [38]. Computed tomography

A modern-generation CT scanner is an extremely valuable diagnostic tool with a high sensitivity for blunt aortic injury, great vessel injury, thoracic fractures, pulmonary contusions, haemothorax and PTX. From a multislice CT scan of the chest, coronal (figure 1), sagittal and transverse (figures 2 and 3) reconstructions of the thorax are possible, and CT imaging can therefore detect all types of PTX and provide a precise evaluation of intrapleural air [3, 28]. In fact, the awareness of occult PTXs began when intrapleural air was incidentally detected on the upper and lower parts of head and abdominal CT scans, respectively [39, 40]. At present, CT imaging is the reference diagnostic standard to safely rule out or diagnose PTX [28], although it remains disputed which patients should receive thoracic CT after blunt trauma. The value of diagnosing all occult thoracic injuries via a “whole-body” trauma scan is uncertain, because few of these additional abnormalities have demonstrated clinical importance [41]. Thus, the pendulum may have swung too far, and 50

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an emergent CT scan of the chest after obtaining a negative CXR should not be performed routinely, because this type of examination comes with a substantial cost. The radiation hazard is eminent [42–44], and the need for patient transportation to the radiology department and the time required to obtain such images can result in delayed diagnosis [37]. Indeed, timing is often critical for physiologically nonpermissive trauma patients, because CT scanning prolongs the time to lifesaving resuscitation (hence, the expression “tunnel of death”).

TUS to detect PTX A point-of-care diagnostic test

An accurate method for diagnosing PTXs is needed. Over the last two decades, PoCUS has evolved from a modality used by only a select group of medical specialities to its current position encompassing a wide range of operator backgrounds and rapidly expanding clinical applications [45]. This has in large part been due to the increasing portability and image quality of machines combined with decreased cost [46]. Physicians from different specialities have shown that they can quickly become skilled in US for diagnostic and procedural applications relevant to their medical field. TUS is a true point-of-care diagnostic test that can be performed in almost any clinical setting. It is noninvasive, radiation free, rapid and repeatable at the bedside, and has been shown to be more sensitive than, and equally specific as, supine CXR to detect PTX [36, 37, 47–52]. Equipment

The current generation of machines are impressively lightweight and utilise sophisticated processors and imaging software to provide high-quality images, including multiple modes (e.g. brightness or B-mode, motion or M-mode, Doppler). They are often laptop sized (∼3– 5 kg) or even truly pocket sized (∼0.1–0.5 kg), and importantly are designed for PoCUS use [46]. Sonographic diagnosis of PTX can be done using different machines with a variety of probes. The preferred transducers for imaging superficial structures (e.g. ribs, pleura) are linear (∼5–14 MHz), but microconvex or convex transducers (∼4–8 MHz) working at lower frequencies may also be used for imaging both superficial and deep structures [9, 53]. Both transducers fit between the ribs and can be “pushed” under the back of the supine patient to examine the posterior chest. Even a larger, low-frequency, curvilinear (∼2–5 MHz) probe may be used to look between multiple ribs. The conventional B-mode is adequate, but occasionally the M-mode setting can be helpful to distinguish movement and standstill at the pleural line [53]. The four sonographic signs of PTX

The paradox is that US imaging poorly visualises the lung parenchyma. Therefore, the conceptual basis for the US diagnosis of PTX is dynamic signs that originate from the pleural line (i.e. the adjacent two visceral and parietal pleural layers) [9, 54]. It is sufficient to combine movements and sonographic artefacts from the pleural line and study them in B-mode and M-mode to rapidly rule out or confirm PTX. The primary dynamic features are the lung sliding sign [55], B-line reverberation artefacts [56] and the pathognomonic lung point sign [57], all of which are synchronous with respiration, and finally lung pulsation transmitted from heartbeats [58]. https://doi.org/10.1183/2312508X.10006317

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Lung sliding In B-mode, lung sliding is a dynamic sign that is visible as a slight and bright sparkling/ twinkling/glittering/shimmering “to-and-fro” horizontal movement at the pleural line. The relative movement is between the lung’s surface covered by the visceral pleura towards the chest wall covered on the inside by the motionless parietal pleura. Lung sliding is more evident during active ventilation; it can be difficult to see with small tidal volumes, and may even be absent in apnoea.

Sometimes it is necessary to use M-mode scanning to evaluate subtle movements of the pleural line. If lung sliding is present, the US image has a granular appearance under the pleural line (resembling sand) and horizontal lines above the pleural line (resembling the horizon), and therefore this type of image is called the seashore pattern. Straight horizontal lines, called the stratosphere pattern, throughout the image indicate the lack of sliding (i.e. possible PTX) with air separating the pleural layers. B-lines In the normal lung, air inside the alveolar spaces hinders visualisation of the lung parenchyma, but if the interlobular septa start to fill up with fluid, this traps the US beam between elements with opposite acoustic impedance. Using B-mode, this creates a multiple reflection artefact call B-lines (i.e. a reverberation artefact) that has the visual appearance of echogenic lines or rays extending from the parietal pleura to the end of the screen without fading. The B-line artefact is dynamic, as it moves synchronously with respiration. Lung point In B-mode, this pathognomonic US sign of PTX is found by placing the US probe over the area where the collapsed lung is still in contact with the inside of the chest wall, as shown in figure 2. This location is called the lung point and is visible as two distinct patterns on the US screen: one suggestive of no lung sliding and/or B-lines where the parietal layers are separated by air (i.e. PTX), and one with normal lung sliding and/or B-lines where the pleural layers are still in contact. The lung point sign is dynamic, as lung sliding and/or B-lines intermittently replace motionless pleura during respiration.

In M-mode, the lung point appears as an interchanging seashore pattern and stratosphere pattern. Lung pulse In the absence of lung sliding, the heart may push the motionless lung and transmit vertical movements to the pleural line. In B-mode, these movements can be seen as small lung pulses synchronous with the cardiac rhythm. The heart beats transmitted through the lung can also be seen in M-mode as pulsatile seashore patterns on a motionless stratosphere background. The scanning technique

TUS detection of PTX may appear complex due to the need to recognise or exclude these four signs, but the use of a step-by-step approach (figure 6) and a flow chart for decision making (figure 7) makes the procedure straightforward. Another simplifying factor is that intrapleural air tends to accumulate in the least-dependent parts of the chest due to gravity, and with the patient in the supine position this corresponds to the anterior and lateral parts of the chest on both sides [33, 59]. These anatomical locations are almost always 52

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accessible and easy to scan in both pre- and in-hospital patients, regardless of clinical condition and body habitus. Several intercostal spaces are often scanned on each side of the chest by repeating the procedure (i.e. figure 6, steps a–c) to confirm the diagnosis of PTX. Different methodical approaches with scanning zones [9, 54] or key anatomical points [53] have been suggested, all with the common feature of covering both the anterior and lateral lung surfaces. A simple approach is to divide each lung into anterior and lateral zones demarcated by the parasternal border and anterior axillary line (i.e. anterior zone) and by the anterior axillary line and posterior axillary line (i.e. lateral zone). Furthermore, the zones can be split into upper (i.e. towards the apex/axilla) and lower (i.e. towards the diaphragm) scanning areas [54, 60].

Discussion Whether TUS is a better diagnostic test than supine CXR in injured patients with a suspected PTX is debated [61]. The British Thoracic Society (BTS) maintains their caution regarding the use of US for the detection and management of PTX because there is no evidence of improved patient outcomes [62]. The World Interactive Network Focused On Critical UltraSound (WINFOCUS) organisation argues that US is more sensitive for diagnosing PTX and is therefore an improvement on the current standard practice [60]. However, there must be a continuous focus on appropriate use and correct interpretations of US images [63]. Regardless of opinion, the use of TUS is expanding followed by growing evidence of its clinical usefulness for diagnosing PTX. The latter statement is based on the numerous publications on this diagnostic technique and recent prospective studies and reviews comparing TUS with supine CXR and CT. Spontaneous PTX

The presence of spontaneous PTX can be inferred sonographically using the same key steps as described in the section “TUS to detect PTX”, including absence of lung sliding and reverberation artefacts. These patients often present with less severe symptoms and can endure the extra time required to take a CXR in the hospital. Based on the availability of a standard erect CXR, which has increased sensitivity and specificity compared with supine CXR, the main value of TUS to date has been in the diagnosis and management of supine trauma patients [64]. Occult PTX

The body of literature that supports the use of TUS for the diagnosis of PTX is increasing, and an illustrative selection is presented in table 2. Due to competing concerns, such as spinal injury, haemodynamic compromise and the need for clinical interventions, patients most often lie on their backs. In this supine position, the intrapleural air collects anteromedially to the lung parenchyma where it is particularly difficult to detect and quantify in anteroposterior CXR [32, 33, 59]. This is the first lung area to be examined in the extended Focused Assessment with Sonography for Trauma (eFAST) protocol, which may explain the increased sensitivity of US to diagnose PTXs that are otherwise undetected on CXRs (i.e. occult PTX) [70]. Three reviews and https://doi.org/10.1183/2312508X.10006317

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ing

dow sha

Ba tw ing

tw Ba

Rib

Ri bs ha do w

a)

b)

Depth Time Skin

Depth

Rib shadow

c)

Time

Figure 6. Step-by-step diagnostic approach for the US detection of pneumothorax (PTX). Thick arrows indicate the pleural line, thin arrows indicate B-lines and crosses indicate the lung points. a) When examining a supine patient, the US scan should always start in the anterior–inferior chest area (i.e. at the third to forth intercostal space) between the parasternal and the midclavicle line (i.e. an area close to the mammilla) (left image). If PTX is present, the intrapleural air will move and reside in front of the lung and can easily be detected by an US probe placed adjacent. The initial plane of the probe is longitudinal to visualise two ribs and identify the echogenic pleural line passing between and under the ribs (middle image). The image of two rib shadows connected by this pleural line resembles the wingspread of a bat, hence the term “bat sign” (right image). Beginning each LUS procedure by identifying the “bat sign” is important because doing so immediately targets the parietal and visceral pleura, where all the dynamic movements and artefacts originate. b) The next step is to slightly rotate the probe so that it is aligned with the intercostal space (left image). This is an oblique plane that gives an extended view of the pleural line without interfering rib shadows, because the axis is alongside the intercostals (middle image). In doing so, remember not to place the probe on top of a rib, as this will reflect a hyperechoic motionless white line (i.e. the cortex of the bone) on the US screen that resembles the pleural line. The scanning then follows the curve of the lateral and inferior chest (i.e. the direction indicated by the arrow drawn on the chest), and at any level, the US operator carefully evaluates the images for signs of horizontal lung sliding and vertical echogenic B-lines that extend from the parietal pleura to the end of the screen (middle and right image). Lung sliding and/or B-lines rule out PTX, whereas both signs are absent if the pleural layers are separated by air. Sometimes it is necessary to use M-mode scanning to make the correct diagnosis (right images in b and c). The seashore pattern rules out PTX, while the stratosphere pattern suggests PTX. c) When lung sliding is absent in the anterior chest, the progressive movement of the probe towards the lateral-inferior chest is useful to look for the area where the collapsed lung is still in contact with the inside of the chest wall. This location is called the lung point (middle and right images) and corresponds to the place where lung sliding and/or B-lines intermittently appear during respiration (best illustrated in video clips). The detection of the lung point is 100% pathognomonic for PTX, and is useful to evaluate the size of a PTX as it marks the lateral extension of intrapleural air inside the chest. The cutaneous projections of the observed lung points (middle image, white double-ended arrow) can be marked by a pen cross on the chest to make a topographical map of the lateral extension of the PTX (left image). The more lateral the lung points are, the more extensive the intrapleural air volume (i.e. PTX size). Reproduced and modified from [1] with kind permission from N.P. Oveland.

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1) Lung sliding? Seashore

Yes PTX still possible

No

2D

B-lines

M-mode 2) B-line(s)

2D

3) Lung point?

Yes

No

PTX

Seashore

No

Lung point

Yes

Stratosphere

No PTX

M-mode Lung pulse

4) Lung pulse?

Yes

No 2D

Figure 7. Diagnostic decision making using a flow chart to distinguish pneumothorax (PTX) and normal lungs. 1) The first sign to be checked is lung sliding, which excludes PTX, but a lack of sliding may be due to other medical conditions involving pleural adhesions that result in motionless pleura (e.g. pleurisy, massive pneumonia, complete atelectasis, fibrosis, severe asthma, emphysema, one-lung intubation, oesophageal intubation, apnoea). In chest trauma cases, the absence of lung sliding is more likely to indicate PTX. 2) The visualisation of even one isolated B-line demonstrates the adjoining of the visceral pleura to the parietal pleura and rules out PTX. In the presence of PTX, the US image lacks B-lines but can have horizontal echogenic A-lines that run parallel to the pleural line (i.e. artefacts that appear under the pleural line at a depth exactly corresponding to the distance from the skin to the parietal pleural layer). A-lines have less diagnostic value because they are found both in normal lungs and with PTX, and only indicate air inside the chest (i.e. they do not distinguish air inside the lungs from intrapleural air). The absence of B-lines has 100% sensitivity but only 60% specificity (in itself not enough for PTX to safely be ruled in). 3) In contrast to the other US signs, the lung point confirms the diagnosis of PTX and is pathognomonic for the presence of air within the pleural cavity. Unfortunately, not all patients present this sign. One explanation for this absence with a large PTX is the complete retraction of the lung with elimination of lung sliding in the anterior, lateral and posterior locations on the chest, and thus no lung point can be visualised. Pleural adhesions may also cause motionless pleura and thereby limit the likelihood of obtaining this sign. However, detection of the lung point is important to confirm PTX and evaluate its size. 4) A lung pulse is useful in the absence of lung sliding and is often observed in patients with consolidated motionless lungs, apnoea syndromes and main bronchus endotracheal intubation. The transmission of heartbeats through the lung parenchyma generates a lung pulse sign, which, similar to lung sliding, rules out PTX. Reproduced and modified from [1] with kind permission from N.P. Oveland.

meta-analyses concluded that bedside US performed by clinicians is a more sensitive screening test than supine anteroposterior CXR for the detection of PTXs in adult patients with blunt chest trauma [67–69]. However, critics state that if the PTX is so small as to be https://doi.org/10.1183/2312508X.10006317

55

First author [ref.]

LICHTENSTEIN [55] LICHTENSTEIN [56] LICHTENSTEIN [57] DULCHAVSKY [65] ROWAN [50] BLAIVAS [48] SOLDATI [66] ZHANG [37] https://doi.org/10.1183/2312508X.10006317

SOLDATI [36] WILKERSON [67] DING [68] ALRAJHI [69] VOLPICELLI [60]

Study design/ publication type

Details of patients or included studies

Not reported ICU patients: 43 lungs with PTX, 68 normal lungs Prospective ICU patients: 41 lungs with PTX, 146 normal lungs observational study Prospective ICU patients: 66 lungs with PTX, 233 normal lungs observational study Prospective 382 trauma patients: 39 lungs with PTX observational study Prospective 27 trauma patients: 11 lungs with PTX observational study Prospective 176 trauma patients: 53 lungs with PTX observational study Prospective 186 trauma patients: 56 lungs with PTX observational study Prospective 135 trauma patients: 29 lungs with PTX observational study Prospective 109 trauma patients: 25 lungs with PTX observational study Evidence-based Four prospective observational studies review Meta-analysis 20 English-language studies: 15 prospective, four not reported and one retrospective Systematic review Eight English-language prospective studies and meta-analysis Conference reports Consensus meetings of 28 experts; and expert panel evidence-based guidelines for LUS extracted from 320 references

US sign(s)

Reference Sensitivity Specificity test % %

LS LS, B-lines

CXR, CT CXR, CT

95.3 100.0

91.1 96.5

LP

CXR, CT

66.0

100.0

LS, B-lines

CXR

94.9

100.0

LS, B-lines

CT

100.0

94.0

LS

CT, ROA

98.1

99.2

LS, B-lines, LP

CXR, CT

98.2

100.0

LS, B-lines, LP

CT, ROA

86.2

97.2

LS, B-lines, LP

CT

92.0

99.4

LS, B-lines, LP

CT, ROA

NA

NA

LS, B-lines, LP

CT, ROA

88.0

99.0

LS, B-lines

CT, ROA

90.9

98.2

NA

NA

NA

NA

ICU: intensive care unit; LS: lung sliding; LP: lung point; ROA: release of air; NA: not applicable. Reproduced and modified from [1] with kind permission from N.P. Oveland.

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Table 2. A historical selection of articles that support the use of TUS scanning for the diagnosis of pneumothorax (PTX) (index test)

PNEUMOTHORAX | N.P. OVELAND

undetectable on CXR, then it is unlikely to require intervention and use of US will not have changed the management [71]. This may be valid for spontaneously breathing patients but not in patients receiving positive-pressure ventilation. Detecting even small amounts of air in the latter is highly relevant, as mechanical ventilation triples the risk of observation failure and the need for a chest tube [12]. Moreover, even if a small PTX is left undrained, prognosis, follow-up and observational strategy in the emergency department, operation room or intensive care unit change when PTX is recognised (e.g. as seen in the first clinical scenario). Evaluation of PTX size

Another remaining question is how best to manage and monitor occult PTX. The hypothesis is that an identifiable cohort of positive-pressure ventilated patients can safely be observed without the insertion of a chest tube [72]. Although it may seem reasonable to consider the size of the PTX before making treatment decisions, a large prospective observational study found PTX size not to be an independent predictor of observation failure with the subsequent need for chest-drain insertion. However, other factors that do predict failure have been identified. Positive-pressure ventilated patients have a tripled risk, and those with respiratory distress are six times more likely to fail observation. In addition, the patients with a progression of their PTX (i.e. occult PTX found on follow-up CXR) are 70 times more likely to undergo a tube thoracostomy [14]. Thus, the assessment of PTX extension and any subsequent change in size is particularly important in these patients. In standard clinical practice, the methods to do this have been CT imaging or CXR. While CT has proved to be highly accurate in quantifying the volume of a PTX [34, 73, 74], CXR readings are equivalently low [38]. The conceptual basis for using bedside TUS in occult PTX patients is that any PTX size progression should be detected early and treated promptly, without the need for patient transport or radiation exposure. The US lung point sign marks the lateral edge of the intrapleural air layer, as demonstrated through comparison with CT and CXR images (figure 6) [10, 36, 48, 75]. Thus, the more lateral the lung point is on the chest wall, the greater the extension of the air layer [9]. However, the lung point will not be found if the lung is completely retracted. A possible contribution of bedside TUS is that it can be used to follow the progression of a PTX during positive-pressure ventilation [10, 75]. This strategy of repeated chest US examinations should be adopted if a decision is made to observe mechanically ventilated trauma patients with occult PTX without placing a chest tube (e.g. the PTX followed in the second clinical scenario). Although the ongoing OPTICC (Occult Pneumothoraces in Critical Care) trial is set to determine the treatment strategy of an occult PTX in general [72], future research should try to find any relationship between the cutaneous projections of the lung points on the chest, marked with US, and the best treatment options. More knowledge is definitely important, as the level of evidence for US evaluation of PTX size is still too subtle and the accuracy of the method has been questioned and debated [48, 76, 77]. Haemodynamic instability

Trauma is a leading cause of morbidity and mortality [2], where patients with additional chest injuries have an increased haemodynamic instability [6]. In some extremities, patients may die from causes that are preventable if promptly diagnosed and aggressive lifesaving therapeutic procedures initiated. In a setting when other image tests are not https://doi.org/10.1183/2312508X.10006317

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Figure 8. Pre-hospital PoCUS. Photograph provided by N.P. Oveland.

applicable, the introduction of eFAST has revolutionised trauma care through improved diagnostic accuracy, increased clinical confidence and tailored resuscitation manoeuvres [70, 78]. Of the eight treatable causes of cardiac arrest (i.e. the 4Ts and 4Hs), PoCUS can help in the diagnosis of cardiac tamponade, hypovolaemia, pulmonary embolism and PTX [79]. In the extreme emergency of cardiac arrest, more of the US diagnosis should rely on simple signs and protocols (e.g. the SESAME (Sequential Emergency Scanning Assessing Mechanism or Origin of Shock of Indistinct Cause) protocol [80]). Thus, to rule in or rule out PTX in an arrested patient, one should rely strictly on lung sliding, B-lines and a lung pulse, without the need to look for the lung point at the lateral chest (the lung is most probably totally collapsed). Furthermore, only scan the anterior chest in one location per side. Any absence of lung sliding, B-lines and a lung pulse of unstable patients should induce the clinician to insert a needle or chest tube immediately [9]. Out-of-hospital and remote areas

In recent years, PoCUS has developed rapidly due to miniaturisation of US machines. The attributes of increasing portability, image quality and power durability of these machines have made them ideal working tools that can be cart mounted or hand carried to the patient’s bedside in or out of the hospital environment. In fact, US scans can be performed in almost any clinical setting and are low risk, rapid and repeatable [45, 78]. These features make TUS suitable in remote and extreme environments, where radiographic evaluation is delayed or impossible, such as wilderness sports events, military conflicts, rural medicine and space aviation [46, 81, 82]. In pre-hospital critical care, the encounter with emergency medical service (EMS) staff and helicopter EMS (HEMS) staff is the first step of triage for ill patients (figure 8). This setting naturally requires the capacity to make a quick diagnosis to tailor the level of care and treatment strategies. These rapid diagnoses are often made with limited information and time, and it is paramount to remain “goal directed” based on predefined, often binary, clinical questions to identify life-threatening conditions and hasten correct treatment (e.g. is there a PTX: yes/no) [70]. Furthermore, technology allowing real-time 58

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videoconference assistance for interpreting PoCUS images may prove important for some (H)EMS systems (i.e. remote telementored US) [83]. Real-time transmission of a video showing the placement of the probe on the patient’s body as well as the corresponding PoCUS image has been tested in a North Sea offshore oil installation, and the study produced clinically useful information in 96.4% of cardiac cases and 87.8% of abdominal cases in all (100%) of the LUS images (N.P. Oveland, unpublished data). This remote telementored US modality is limited only by network availability, as other necessary videoconference and PoCUS equipment is readily available “off the shelf”. Finally, the increasing costs of hi-tech diagnostic hardware, such as angiographic radiography, CT and MRI machines, limit their availability in developing countries. In fact, the World Health Organization (WHO) has stated that two-thirds of the world’s population has no access to these imaging technologies. The paradox is that 80–90% of all diagnostic problems could potentially be solved by basic radiography and US examinations [84]. The low cost and increasing availability of machines makes this a tool of choice in developing countries [85]. Pitfalls

Several conditions could mislead the operator or hinder the TUS examination when applied to detect signs of PTX. Some of these are medical conditions with motionless pleura, as explained in figure 7. An important condition common in trauma patients and iatrogenic PTX is s.c. emphysema (i.e. air that has leaked into the s.c. tissue). This may give artefacts on the US screen often described as “false lung sliding” based on movement of echogenic muscular layers resembling the pleural line, and US images with “false B-lines” as air within the s.c. tissue gives echogenic lines that spread like vertical rays, reaching the lower

Table 3. Key points related to the US diagnosis of pneumothorax (PTX) How to scan?

The sonographic signs of PTX include the following (strong/level A): Presence of lung point(s) Absence of lung sliding Absence of B-lines Absence of lung pulse In the supine patients, first scan the anterior chest and progress more laterally (strong/level A) Adjuncts such as M-mode or colour mode may be used (strong/level A) Microconvex transducers are preferred in adults, but others such as linear probes can also be used based on preference and clinical setting (strong/level B)

When to scan?

TUS should be used in all clinical settings when PTX is a possible diagnosis

What does TUS add?

TUS more accurately rules in PTX than supine anteroposterior CXR (strong/level B) TUS more accurately rules out PTX than supine anteroposterior CXR (strong/level A) TUS may be a better initial diagnostic test for PTX than CXR, and hence lead to a better outcome (no consensus/level C) TUS is a useful tool to differentiate small and large PTXs, using detection of the lung point (no consensus/level C)

Information from [60].

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edge of the screen without fading [9]. These linear artefacts are called emphysema or E-lines and differ from true B-lines as they do not arise from the pleural line [53]. Furthermore, foreign bodies such as bullets and shrapnel within the s.c. tissue will generate similar vertical artefacts that are not true B-lines. Another phenomenon is the “double lung point” where an air bubble is trapped between two areas of adherent pleural layers. In this case, the laterality of the lung point fails to indicate the real extension of the PTX, while two lung points surrounding the air bubble may be visualised [86, 87]. Similar although rare, septated and complex PTXs with posterior locations are difficult to diagnose [53]. Finally, external factors such as voluminous clothing and chest dressings, limited workspace inside ambulances and helicopters, and ambient lighting outside of hospitals make the diagnosis of PTX more challenging. Further reading

This Monograph highlights the endless possibilities of TUS for diagnosis of multiple clinical conditions of the chest. In the last 5 years, numerous publications have been published for TUS detection of PTX alone. Many are written by pioneers of TUS, such as Giovanni Volpicelli and Daniel A. Lichtenstein, but it is beyond the scope of this chapter to give a complete review of this literature. For some suggested books, reviews and guideline articles, see [53, 88–93].

Conclusion In 2012, Giovanni Volpicelli led an expert group, using a grading of recommendation, assessment, development and evaluation (GRADE) method, to publish the first international evidence-based recommendation for point-of-care TUS. The key points related to the US diagnosis of PTX from this consensus with level of recommendation (i.e. strong or weak) and level of evidence (i.e. high to low level, labelled A–C) are summarized in table 3 [60].

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Disclosures: None declared.

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| Chapter 5 Pleural effusion Christopher Merrick1, Rachelle Asciak2,3,4, Anthony Edey5, Fabien Maldonado1 and Ioannis Psallidas2,3,4 Pleural effusions represent a significant disease burden globally. TUS, performed by both radiologists and physicians, has increasingly become an essential tool in the evaluation and management of pleural effusions. It detects pleural effusions with higher sensitivity and specificity than CXR, and provides valuable information about the size and depth of the pleural effusion, the echogenicity of the fluid, the presence of septated or loculated fluid, pleural thickening and nodularity, and the presence of any contralateral pleural effusion. TUS can provide information on diaphragm position and movement with respiration, and can assess the presence of lung sliding and the accessibility of pockets of fluid in loculated pleural effusions, thereby improving the success rate and safety of pleural procedures. Given the added detail that US provides and its increasing availability, it is no surprise that its use is increasingly expanding in clinical practice. Cite as: Merrick C, Asciak R, Edey A, et al. Pleural effusion. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 64–74 [https:// doi.org/10.1183/2312508X.10014817].

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leural effusions represent a significant burden of disease globally, related to both primary pleural and systemic pathologies. It is estimated that 3000 people per million of the population are affected by pleural effusion [1]. A broad range of diagnostic and treatment modalities is available to the physician treating individuals suffering from pleural effusion. The role of TUS in pleural effusion is multifaceted, and this technique is useful for diagnosis, treatment and even, in some cases, prognosis. It is useful in both inpatient and outpatient settings for treating individuals with pleural disease.

Physician competency With the growing use of bedside US by treating clinicians, there is an increasing awareness that US practice need no longer be isolated to the radiology department. Bedside TUS has been shown to decrease expense, as well as time in hospital [2]. Optimal management of pleural effusion from a healthcare cost and patient wellness perspective is best initiated by 1 Vanderbilt University Medical Center, Tennessee, Nashville, TN, USA. 2Oxford Centre for Respiratory Medicine, Churchill Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK. 3Oxford Respiratory Trials Unit, Nuffield Dept of Medicine, University of Oxford, UK. 4Laboratory of Pleural and Lung Cancer Translational Research, Nuffield Dept of Medicine, University of Oxford, UK. 5Dept of Radiology, Southmead Hospital, North Bristol NHS Trust, Bristol, UK.

Correspondence: Ioannis Psallidas, Oxford University NHS Foundation Trust, Old Road, Churchill site, Oxford, OX3 7LE, UK. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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the chest physician through skilled TUS analysis and TUS-guided procedures at the bedside. However, patient safety requires that bedside physicians have received appropriate training and hands-on experience with TUS prior to independent use for management of patients. Multiple studies have demonstrated a decreased incidence of iatrogenic thoracentesis complications following initiation of formalised TUS training and regular use of US for percutaneous procedures [3, 4]. An increasing number of respiratory medicine training programmes internationally are creating formal US training programmes to promote physician competency. Competence in pleural US is now a compulsory part of respiratory medicine training programmes in the UK [5]. The Royal College of Radiologists stipulates that obtaining a certificate of basic TUS competence (level 1) includes keeping a logbook of US examinations by the trainee and an assessment of competence by an experienced trainer. Required competencies include the performance of safe and accurate examinations, recognition of anatomy and pathology, recognition of when to appropriately refer for a second opinion, and an understanding of the relationship between US imaging and other imaging techniques. With more practice and experience, including the performance of noncomplex US-guided procedures, and with conductance of research in US, the trainee can then be certified as level 2 competent. Level 3 is an advanced level of practice, which in the UK would usually equate to a consultant radiologist with a subspecialty practice [6]. At all stages, respiratory physicians should collaborate with radiologists, and TUS findings should be correlated and combined with other imaging techniques, such as CT scanning, in order to deliver the best care for patients with pleural effusions. With the growing use of US in various specialties, there is also a move to integrate US training into medical school curricula [7].

Pleural effusion Aetiology and pathogenesis

The pleural space is a tightly regulated virtual space that contains a small amount of pleural fluid in physiological conditions, governed by a balance of plasma ultrafiltration and venous and lymphatic drainage. This delicate balance can be disturbed in a variety of situations, such as in the setting of pleural tumour, infection, and lymphatic obstruction or disruption, resulting in a net accumulation of pleural fluid. Pleural effusions are categorised as exudative or transudative, based on time-honoured criteria involving fluid lactate dehydrogenase and protein, which remains an initial crucial step in determining the aetiology of the pleural effusion [8]. Exudative pleural effusions typically result from a combination of pleural space inflammation from increased cellular recruitment and decreased lymphatic drainage. Transudative effusions, characterised by low fluid lactate dehydrogenase and protein levels, are the consequence of alterations of the Starling law, which regulates capillary microcirculation and can be observed in such processes as congestive heart failure, renal insufficiency, and hypoalbuminaemia from liver disease or proteinuria. Rarely, pleural effusions may result from the accumulation of extravascular fluid that finds its way into the pleural space, such as in the case of intrapleural misplacement of central venous access (infusothorax), transdiaphragmatic passage of ascites or, rarely, urine in the setting of hydronephrosis (hydrothorax and https://doi.org/10.1183/2312508X.10014817

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urinothorax, respectively) or chyle (chylothorax) [9, 10]. Invariably, any given case of pleural effusion may be multifactorial and can incorporate a combination of the above mechanisms. Epidemiology

Pleural effusions represent the end result of a variety of clinical conditions, which vary based on patient characteristics and local disease patterns. There are an estimated 1.4 million cases of pleural effusions annually in the United States, with an estimated incidence of pleural effusion in the developed world of 320 cases per 100 000 persons per year [11]. There are no obvious gender predilections, and men and women seem to be affected equally. Pleural effusions are much less common in children, where they are primarily due to infectious aetiologies [12]. Diagnosis

Pleural effusions are sometimes clinically asymptomatic and discovered incidentally on routine imaging. When symptomatic, they result in varying degrees of breathlessness, felt to be the consequence of diaphragmatic dysfunction due to the weight of the column of fluid, according to the length–tension inappropriateness theory [13]. CXR typically serves as the initial evaluation for pleural effusion. At the time of diagnosis, a minority of cases are found to be bilateral on CXR, which typically results from congestive heart failure [14]. Effusion characteristics can vary widely based on effusion aetiology and chronicity. The fluid character may range from viscous and loculated to thin and free flowing. The variability in fluid volume and character can significantly affect findings on physical examination, often yielding physical examination inferior to CXR for detection of pleural effusions [15]. TUS has, however, been shown to be superior to both CXR and physical examination for detection of pleural effusion. It can provide immediate valuable information at the bedside on the character, volume and complexity of the pleural effusion not typically evident on conventional radiographic imaging [15–17]. TUS serves a key role in pleural effusion evaluation, as fluid echogenicity, diaphragmatic motion and the appearance of the pleura are all important considerations in investigating the aetiology of an effusion and planning the subsequent diagnostic and therapeutic steps.

Sonographic characteristics of pleural effusions Basic principles

A basic understanding of US image appearance is required for adequate pleural effusion evaluation on TUS. On US, fluid or structural characteristics such as density affect the sonographic appearance of the structure in question; this appearance is referred to as echogenicity. Unimpeded passage of US through tissue is associated with a lack of echoes, rendering the images hypoechoic (grey) or anechoic (black), for example as seen in a simple effusion. Increasing complexity and density of material increase the echogenicity and may be uniform or heterogeneous; thus, proteinaceous fluid contains uniform internal echoes rendering the fluid grey or white (hyperechoic) on the image. US is reflected by air and cannot penetrate it; gas interfaces produce a bright linear interface with disorganised, irregular bright shadowing distal to the line, which is simply an absence of echoes and not amenable to interrogation. 66

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Simple effusion

Simple effusions are characterised by a free-flowing consistency and lack of loculations. On US, these effusions are found as homogeneous hypoechoic fluid collections just deep to the chest wall [18]. Compressed lung can be visualised as a moderately hyperechoic structure on the far side of the fluid collection. The diaphragm is visualised as a hyperechoic rounded stripe on the inferior border of the pleural effusion (figure 1). Transudative effusions, such as those due to cardiac or renal disease, are most commonly simple. The ability of US to discriminate between transudative and exudative effusions was evaluated in a small prospective cohort of patients with pleural effusions [19]. This study demonstrated that anechoic effusions could be either transudates or exudates, but transudates were always anechoic. Echogenic effusions were always exudates. As would be expected, complex-appearing or septated effusions were indicative of exudates. Finally, homogeneous echogenic effusions were due to empyema or haemorrhage [19]. Categorisation of effusion based on US appearance is generally described as follows: anechoic, complex septated, complex nonseptated or homogeneous nonseptated. Complex effusion

Complex effusions are characterised by loculations (collections of fluid that do not follow gravity) and septations (fibrin strands) and are typically not free flowing. On US, the appearance of complex effusions is characterised by heterogeneous fluid collections with interspersed hyperechoic tissue strands. These effusions are typically composed of cellular material, which can organise into fibrinous or proteinaceous strands of cellular debris called septations (figure 2). These septations can ultimately result in the compartmentalisation of the pleural effusion into several smaller locules, which may or may not communicate with one another. Effusion complexity is variable, and can range from relatively mild with only a few loculations to severe complexity with a substantial loculation burden and intense heterogeneity of the fluid collection on US. Exudative effusions, such as those due to malignancy and infection, are often complex. Effusion chronicity also appears to be important in terms of development of a complex effusion. A simple effusion, if left untreated for a substantial period of time, may develop loculations [20].

*

Figure 1 . A simple pleural effusion with echogenic contents, in this case a transudate. Note that atelectasis (arrow) has a texture similar to liver (*). https://doi.org/10.1183/2312508X.10014817

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Figure 2. A complex, septated effusion with dense, organising fibrinous material. Note the pleural margin deep to the collection (arrow) with noisy, disorganised echoes distally in place of the aerated lung.

Lung consolidation/hepatisation

Pleural effusion is frequently found in the presence of pulmonary infection or consolidation. This is especially true in the hospitalised or critically ill patient. The lung filled with products of infection (consolidated) on US has a uniform speckled pattern with an appearance similar to the liver. Within areas of consolidation, air bronchgrams are visible as paired hyperechoic lines. It is useful to confirm internal pulmonary vascularity to exclude infarction or occasionally organising fibrinous debris, which can also have a similar appearance. Finally, atelectatic lung looks similar in texture but shows volume loss compared with consolidation (figure 1) [21]. Nonexpandable lung evaluation

Nonexpandable lung (NEL) is an important consideration in pleural effusion management as it affects patient symptomatic relief and the likelihood of effusion re-accumulation. It is defined by a lack of visceral and parietal pleural apposition following effusion drainage. NEL occurs in a variety of clinical scenarios, such as proximal airway occlusion, primary visceral pleural fibrosis in the absence of an obvious inflammatory source, or secondary visceral pleural fibrosis in the setting of chronic inflammatory pleural effusions. Patients with NEL are less likely to experience an improvement in dyspnoea, and are more likely to experience pain with pleural drainage from excessively negative pleural pressures, which may occasionally result in pneumothorax ex vacuo and, rarely, re-expansion pulmonary oedema [22, 23]. The diagnosis is usually established by the presence of remaining pleural fluid after thoracentesis was stopped due to pain (typically felt anteriorly) or, when available, via pleural manometry. There have been recent attempts to identify these patients based on pre-drainage TUS characteristics. A single study evaluated M-mode and speckle tracking imaging to evaluate transmitted cardiac impulse through the atelectatic lung [24]. This approach was based on the theory that NEL, with its thickened visceral pleura, would transmit the cardiac impulse less efficiently. These results suggest that advanced US imaging techniques may outperform manometry in the early diagnosis of NEL, which could have significant implications in terms of patient management. While intriguing, these results need confirmation, and the technique remains anecdotal [25]. 68

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Predictors of breathlessness: septation analysis and paradoxical motion

In a recent analysis of patient-reported outcome measures following pleural effusion drainage, patients were asked to complete a visual analogue scale (VAS) for symptoms before and after fluid drainage [26]. It was demonstrated that both the volume of pleural fluid drained and the number of septations on TUS appeared to affect the degree of dyspnoea improvement that patients experienced. Specifically, it was demonstrated that patients with five or more septations per TUS image improved less after intercostal chest-drain insertion than other patients, and this appeared to be independent of the volume of pleural fluid removed during the procedure (figure 3). Multivariate analysis suggested that the number of septations was, in fact, the only independent predictor of VAS change [26]. In pleural effusion, there is a well-established phenomenon of paradoxical diaphragmatic motion in the setting of large pleural effusions [27]. This paradoxical motion is most notable in the setting of left-sided effusions, as the right hemithorax is bounded inferiorly by the liver, which more effectively prevents diaphragmatic inversion. The mechanism of paradoxical motion is attributed to diaphragmatic contraction in inhalation, which results in diaphragmatic elevation in the presence of a large effusion. The presence of paradoxical diaphragmatic movement serves as an indirect indicator of projected clinical response to effusion drainage. When compared with individuals without paradoxical movement, those with such movement are more likely to experience meaningful improvements in dyspnoea and pulmonary mechanics following effusion drainage [28].

Role of US in malignant pleural effusion Malignant pleural effusion (MPE) is the most common cause of massive unilateral pleural effusion (defined as occupying more than two-thirds of the hemithorax) in the Western world and affects over 150 000 people annually in the United States alone [14, 29]. Diagnosis of MPE is based on fluid cytology and often requires additional diagnostic procedures such as pleural biopsy and pleuroscopy. In patients presenting with pleural

Figure 3. Pleural effusion with a single prominent septation centrally and another at both the top and bottom of the screen. This patient would be expected to experience less dyspnoeic improvement following drainage than an individual with more than five septations.

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disease suggestive of MPE, TUS has been found to have a diagnostic sensitivity of 73% and a specificity of 100%. Pleural thickening of >1 cm is highly suggestive of MPE (figure 4). As such, TUS can be highly beneficial in the diagnostic evaluation of suspected MPE but is not sufficient to confirm the diagnosis [30].

Role of US in pleural space infections Pleural infection is a significant cause of pleural disease and appears to be on the rise globally due to improved clinical recognition and diagnostics, in addition to a hypothesised replacement phenomenon attributable to increasing use of multivalent pneumococcal vaccines [31, 32]. Complicated pleural space infections are defined by ongoing signs of sepsis in spite of adequate antibiotic treatment, and these effusions require drainage. Thoracic catheter size is an area of frequent debate informed by regional practices and individual experience. Prospective post hoc analysis of randomised controlled trial data has demonstrated no significant difference in clinical outcomes or referral for surgery among patients receiving either small-bore, wire-guided thoracic catheters or traditional large-bore chest tubes [33]. Prior to publication of these data, one study evaluated the accuracy of TUS in determining sonographic effusion characteristics that predict successful drainage by small-bore catheters (12–16 French gauge). Complex septated effusions were more likely to fail treatment if drained by small-bore catheters than complex unseptated effusions [34]. However, it deserves mentioning that standard medical treatment at the time of this study primarily comprised the use of antibiotics. These data need to be interpreted in light of the advent of intrapleural fibrinolytic–nuclease therapy for the management of complicated pleural space infections [35].

Fluid volume estimation It is important to estimate effusion volume prior to drainage, especially in those high-risk patients who may be harmed by thoracentesis, such as those on mechanical ventilation or those with coagulopathy. Based on small cohort studies, there are basic assessments that can be done to estimate pleural effusion volume. For the spontaneously breathing patient, measurement of the distance between the chest wall and lung margin was evaluated [36].

Rib Parietal Visceral

Figure 4. Longitudinal US image showing gross pleural thickening (1.4 cm; indicated by crosses). Note the pleura is hyperechoic; the echogenicity of malignant pleural thickening is variable and ranges from low through intermediate to hyperechoic.

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The technique required patients to lie in a supine position and perform a maximum breath-hold while US images were obtained over the laterodorsal chest wall just superior to the margin of the diaphragm. An effusion depth of 20 mm was found to correlate with a mean volume of 380 mL, and 40 mm with 1000 mL. TUS was found to far outperform lateral decubitus chest radiography in terms of effusion volume estimation [36]. For the mechanically ventilated patient, a basic formula has been proposed to determine effusion volume [37]. TUS was performed with the patient supine at 15° and the probe was placed in the posterior axillary line. Based on a single series of observational data, the pleural fluid volume could be estimated by multiplying the maximal distance (in millimetres) between the visceral and parietal pleura by a factor of 20 [37]. It should be noted that multiple different formulae have been proposed, but none has been independently validated or demonstrated to be superior to any other at predicting effusion volume.

Special considerations Mechanically ventilated patients

Pleural effusion is common in the intensive care unit setting, given the multitude of comorbid illnesses such as sepsis, malnourishment, cardiac dysfunction and iatrogenic volume overload. Evaluation of such effusions is paramount, especially in situations of concern for complicated parapneumonic effusions or malignancy. There are multiple imaging modalities available to the clinician in this setting including, primarily, CXR. Frequent, or sometimes daily, CXRs are obtained in the intensive care unit setting and often provide the first insight to incidentally diagnosed pleural effusions. In multiple prospective cohorts, the performance of TUS versus CXR in detecting pleural effusion in mechanically ventilated patients was examined [15]. TUS was found to far outperform CXR in both its sensitivity and specificity for pleural effusion detection. The sensitivity and specificity of TUS to detect pleural effusion in a mechanically ventilated patient have been demonstrated to be 93% and 97%, respectively [38]. As one would imagine, the diagnostic accuracy of TUS also far surpassed that of auscultation in the mechanically ventilated patient [17].

Future directions TUS is an actively growing field of research, given its immense clinical utility. In recent years, its usefulness has flourished from an occasional novelty in bedside assessment to a cornerstone of evaluation and management of pleural effusion. A major area of investigation in TUS is in evaluating its ability to predict procedural success in terms of patient-oriented outcomes. Predictors of procedural success

The SIMPLE (Efficacy of sonographic and biological pleurodesis indicators of malignant pleural effusion) prospective trial is currently underway and aims to assess whether lack of lung sliding as detected by TUS can reliably predict successful talc pleurodesis in patients with MPE, and to determine the effect of this on improving the quality and efficacy of care provided to patients with MPE (ISRCTN trial number 16441661). https://doi.org/10.1183/2312508X.10014817

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Following the results from the previously mentioned septation analysis study [26], detection of septations on TUS has the potential to predict the symptomatic outcome of subsequent pleural procedures, and a larger multicentre study is needed to confirm these results and to study the septation score in more detail. TUS assessment of the diaphragm in patients with pleural effusions, including hemidiaphragm flattening, inversion and paradoxical motion, has been suggested as a potential predictor of symptomatic response to pleural procedures. The PLEASE (Pleural effusion and symptom evaluation) trial is currently underway in Australia assessing the effect of pleural effusion drainage on diaphragm mechanics [39]. Imaging enhancement

Finally, the use of contrast-enhanced TUS is an area of interest that may hold benefit for evaluation of patients with MPE. It can be difficult to differentiate pleural thickening in the setting of effusion due to similar sonographic characteristics (figure 5). There is a small body of data and experience using hexafluoride-based contrast for enhancement of pleural-based nodules. Contrast can be beneficial in enhancing nodule visibility and may be helpful in forming a differential diagnosis based on the US qualities of the nodules [40]. Currently, CEUS remains a niche technique due to the technical limitations of appropriate training and equipment, and further investigation and clinical experience is needed with this modality.

Conclusion TUS is rapidly becoming a cornerstone as a management modality for the chest physician caring for patients with pleural effusion. TUS is sensitive for detection of pleural effusion and is useful in further evaluation and categorisation of effusion type based on fluid sonographic characteristics. As such, it is pivotal in guiding therapy directed towards effusion, and is even beneficial in elucidating which patients will benefit most from effusion drainage. TUS has increased the safety of bedside procedures and simplified patient care, thus providing the potential to decrease costs and hospital length of stay for those

Figure 5. Pleural nodularity, seen prominently on the diaphragmatic pleura. The pleural effusion is echogenic and confirmed as an exudate in this case of pleural malignancy. Contrast-enhanced TUS may have a role in improving visualisation of pleural nodularity in the setting of pleural effusion.

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hospitalised with pleural effusion-related disease. Bedside TUS carried out by a physician should serve a foundational role in the management of both ambulatory and hospitalised patients suffering from pleural effusion.

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Disclosures: F. Maldonado has received a grant from Centurion, outside the submitted work. I. Psallidas has worked part-time as Medical Science Director at AstraZeneca, but his work was on a different disease area and was not linked with pleural effusion.

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| Chapter 6 Interstitial syndrome Luna Gargani B-lines are probably the most “revolutionary” sign of LUS and can be used for the evaluation of interstitial syndrome. They indirectly visualise different degrees of partial deaeration of the pulmonary parenchyma, and therefore can be seen in the presence of both hydrostatic and inflammatory pulmonary oedema, as well as in pulmonary fibrosis. Assessment of B-lines can thus be applied to many different diseases, such as heart failure, end-stage renal disease, acute lung injury, interstitial lung disease and pre-eclampsia. To differentiate these conditions, a thorough integration with the clinical picture is absolutely necessary, but some LUS characteristics can also significantly improve B-line specificity and overall LUS diagnostic accuracy ( pattern of distribution over the thorax, response to therapy and association with other LUS signs, such as pleural line alterations, small and large consolidations, and pleural effusion). The clinical usefulness of B-lines has been demonstrated not only for diagnosis but also for monitoring and prognosis. Cite as: Gargani L. Interstitial syndrome. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 75–86 [https://doi.org/10. 1183/2312508X.10006517].

P

ulmonary interstitial syndrome comprises a group of lung disease affecting the lung interstitium. Although sonography cannot be used to evaluate the lung because the pulmonary air represents an insurmountable obstacle to the US beam, it is possible to recognise sonographic patterns, including “artefactual” B-lines, which can be used effectively in many settings. These can aid in the differential diagnosis of dyspnoea, and can be used to monitor the response to therapy.

Sonographic signs of interstitial syndrome B-lines Definition In recent years, B-lines have been described as the sonographic sign of pulmonary interstitial syndrome. It is difficult to define sonographic interstitial syndrome, as this is a term derived from radiology, where it refers to a pattern that can be applied both to CXR and to chest CT, including linear, reticular, nodular and pseudonodular alterations. Institute of Clinical Physiology, National Research Council, Pisa, Italy. Correspondence: Luna Gargani, Institute of Clinical Physiology, National Research Council, via Moruzzi 1 – 56124, Pisa, Italy. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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B-lines have officially been defined as “discrete laser-like vertical hyperechoic reverberation artefacts that arise from the pleural line, extend to the bottom of the screen without fading, and move synchronously with lung sliding” [1]. B-lines are indeed sonographic artefacts, which do not depict real anatomical structures but rather are the result of the peculiar acoustic properties of the lung. The physical genesis of B-lines is not yet fully understood, although some sound hypotheses have been proposed [2]. To understand what B-lines represent in the context of LUS basic semiotics, we have to refer strictly to the physical interaction between the US beam and the pulmonary parenchyma. When the pulmonary parenchyma is normally or over-aerated, the US beam is usually unable to penetrate below the pleural line; the resulting image thus shows all of the structures above the pleura (e.g. adipose tissue, muscles, fascia) and the pleura itself as a hyperechoic horizontal line moving synchronously with respiration. The structures above the pleural line are sonographically portrayed as corresponding to real anatomical entities. This is not true for what is depicted below the pleural line, unless the lung is consolidated. Whether the sonographic pleural line fully corresponds to the anatomical pleura is still debated. A reduction in pulmonary aeration changes the physical acoustic interaction between the US beam and the lung, allowing the US beam to partially penetrate the lung parenchyma, and resulting in the appearance of B-lines. A complete or almost complete pulmonary deaeration would generate the sonographic display of a consolidation, with direct imaging of the anatomical consolidated parenchyma. Milder degrees of deaeration do not allow direct imaging of the lung parenchyma but generate B-lines, which are more numerous as long as the air diminishes. It follows that B-lines are visible in the presence of a partial deaeration of the lung, which is, however, not consolidated. This condition is not necessarily linked only to alterations of the pulmonary interstitial space, making the term “interstitial syndrome” somewhat of an oversimplification, although very figurative. Referring to a condition of “partial deaeration”, which characterises the pre-consolidated lung, seems more appropriate [2, 3]. However, the term interstitial syndrome is suitable for most pathology, and it is true that those conditions that do not purely affect the interstitial space usually show additional signs to B-lines. Characteristics There are some typical features of B-lines that help in the differentiation from other artefacts. Table 1 presents the main B-line characteristics. These elements are especially useful to differentiate B-lines from Z-lines. Z-lines are vertical hyperechoic artefacts that, similar to B-lines, arise from the pleural line, although the pleural origin is better defined for B-lines. Moreover, Z-lines do not reach the edge of the screen and do not clearly move with lung sliding [4]. Z-lines are usually less hyperechoic than the relative pleural line. Z-lines do not seem to have pathological meaning. Figure 1 shows a Z-line and B-lines.

Pleural line

The pleural line is a cornerstone of LUS. It is the first structure that should be searched for, and its movement, referred to as lung sliding, should always be identified before moving on to further evaluations. When lung sliding is not apparent, the different potential causes of 76

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Table 1. Characteristics of sonographic B-lines Characteristic

Comments

Arise from the pleural line

Always true Common feature to Z-lines (whose origin is, however, less defined) Always true Z-lines do not clearly move with lung sliding A-lines may still be visible, but are covered/erased by B-lines at the intersection point Z-lines do not erase A-lines Similar echogenicity as the pleural line Z-lines are usually less hyperechoic than the pleural line Quite subjective Usually better defined compared with Z-lines May partially depend on the machine setting Z-lines usually fade away before reaching the bottom of the screen

Move synchronously with lung sliding (with respiration) Erase A-lines Hyperechoic Well defined Extend to the bottom of the screen without fading

absent lung sliding should be taken into account, and the LUS examination should continue to exclude or confirm the main clinical suspicion. The normal pleura is visualised by LUS as a hyperechoic horizontal thin line, representing the apposition of the parietal with the visceral pleura layers (figure 1). The pleural line may appear abnormal in some pathological conditions, such as acute lung injury/acute respiratory distress syndrome (ALI/ARDS) or interstitial lung disease (ILD). The appearance of the pleural line can be helpful in contributing to the differential diagnosis of the aetiology of B-lines [5–7], as detailed in the following section.

a)

b)

Figure 1. a) Z-line (arrow). b) B-lines (arrow).

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Diffuse versus focal interstitial syndrome

The mere presence of B-lines is not enough to characterise a lung from the sonographic point of view. A few B-lines, especially at the lung bases, can be present in healthy subjects and do not have a specific pathological meaning. A positive examination for B-lines needs the presence of multiple, diffuse, bilateral B-lines. Multiple B-lines means at least three B-lines between two ribs when applying the probe longitudinally, or at least three close B-lines along the intercostal space when applying the probe obliquely or transversally. Diffuse B-lines means that multiple B-lines should be seen in at least two regions of the lung and bilaterally (i.e. in both hemithoraxes) [1]. As thoracic regions, the eight-region scanning scheme proposed by Volpicelli et al. [1] is usually accepted. Another scanning scheme that is accepted and has been used in many studies is the 28-scanning-site scheme [8], which is more time consuming but allows a type of quantification of B-lines that, although imprecise, has been shown to correlate with clinical [9, 10], biochemical [11], radiological [12, 13], echocardiographic [9], gravimetric [14] and invasive [15] parameters related to the interstitial involvement of the lung. Moreover, it has shown clear prognostic value in both acute and chronic patients [16–20]. The definition of multiple B-lines as at least three B-lines between two ribs can be in part subjective and does not take into account different thoracic dimensions. In acute conditions, this is usually not so relevant, because the US patterns tend to be clear and straightforward. However, clinical reasoning is mandatory, and a blind adherence to the US picture, unrelated to the patient’s characteristics, should be avoided. It is also crucial to distinguish between the abovementioned situation of positive scanning for multiple, diffuse, bilateral B-lines and so-called focal interstitial syndrome, which refers to multiple B-lines, usually limited to one region, and monolateral. This condition can be present in healthy asymptomatic subjects ( probably linked to previous pulmonary parenchymal involvement), whereas, in a patient with signs/symptoms such as dyspnoea, tachypnoea, fever or chest pain, multiple focal B-lines should raise the suspicion of pulmonary abnormalities not clearly visible by LUS at that time. It is typical to find multiple focal B-lines in a patient with fever and/or chest pain, especially if scanned early after the appearance of symptoms, and then to visualise a consolidation in the same area after a few hours. Multiple focal B-lines may represent the perilesional oedema of the consolidation that is being formed, or a consolidation that is not peripheral enough to be detected clearly by LUS. Thus, the clinical context must always be the guide to orient these findings.

Clinical applications Cardiogenic pulmonary oedema

In recent years, many studies have confirmed that B-lines can be useful in the detection, monitoring and prognosis of patients with cardiogenic pulmonary oedema [6, 21, 22]. The first published data were about the differential diagnosis of patients with acute dyspnoea. In this setting, a positive LUS scanning for B-lines can help differentiate from other causes of acute dyspnoea, in particular from exacerbation of COPD [11, 23–25]. Again, it is important not to refer to the mere presence of B-lines but to assess multiple, diffuse, bilateral B-lines, as patients with COPD, as well as healthy subjects, may show a few 78

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B-lines. In a large multicentric prospective study on >1000 patients with acute dyspnoea, adding LUS to the standard clinical evaluation in the emergency department improved the accuracy of acute heart failure (AHF) diagnosis (sensitivity and specificity 97%), with a net reclassification index of the LUS-implemented approach compared with the standard work-up of 19.1% [25]. This study addressed the diagnostic performance of LUS, whereas an improvement in outcomes was not evaluated in the LUS-implemented group. LUS evaluation of B-lines for the differential diagnosis of AHF compared with other causes of acute dyspnoea also seemed a more effective method of implementation of PoCUS in a large cohort of consecutive adult patients presenting with dyspnoea and admitted after emergency department evaluation [26]. The presence of multiple bilateral B-lines increased the sensitivity of the diagnosis of AHF from 77% (standard evaluation) to 88% ( p90%. These patients should therefore be treated immediately according to clinical presentation and laboratory findings, without further imaging procedures. In cases of tuberculosis and diseases of the frame of the lung, sonography is the optimum method of visualising small pleural effusions and subpleural consolidations. Cite as: Mathis G. Pneumonia. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 87–101 [https://doi.org/10.1183/2312508X. 10006617].

P

neumonia has been documented as a forgotten killer [1]. According to the data released by the World Health Organization (WHO), lower respiratory tract infection is the leading cause of infectious disease-related mortality worldwide and refers to the top-ranking cause of death in low-income countries. Pneumonia accounts for 16% of all deaths in children 90% (table 2) [42–49]. LUS may therefore be able to rule in pneumonia but not rule it out [43]. 92

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b) a)

c)

e) d)

f)

Figure 6. Follow-up in a patient with pneumonia. LUS shows the regression better than CXR. Day 1: a) CXR, b) LUS with brochoaerograph, and c) LUS with regular vascularisation. Day 6: d) CXR with rest shadowing, and e and f ) LUS with reventilation according to the clinical course.

The scope of the results is based on different inclusion criteria and various populations. Overall, pooled positive and negative likelihood ratios (LR) were 20 and 0.06, respectively [40, 42, 45]. A combination of auscultation and LUS increased the positive LR to 42.9 and decreased the negative LR to 0.04 [29]. https://doi.org/10.1183/2312508X.10006617

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Table 2. Eight meta-analyses of LUS in CAP First author [ref.]

Year

Studies n

Patients n

Sensitivity Specificity

DOR AUC

Reference method

CHAVEZ [42] HU [43] YE [44]

2014 2014 2014

12 9 5

1353 1080 742

0.95 0.97 0.95

0.96 0.94 0.90

? 510 151

0.98 0.99 0.97

0.91 0.91 0.85

0.89 0.90 0.80

? 97 50

? 0.97 0.93

0.88 0.85

0.86 0.93

65 174

0.95 0.98

CXR/CT CXR/CT Discharge diag. ? CT Final/ discharge CR/CT Clin/ imaging

BERLET [45] XIA [46] LLAMAS-ALVAREZ [47] LONG [48] ALZAHRANI [49]

2015 2016 2017

7 14 16

1010 1911 2359

2017 2017

12 20

1515 2513

DOR: diagnostic odds ratio; AUC: area under the curve; ?: unknown.

One of the studies evaluated critically ill patients in intensive care (n=3) and found a pooled sensitivity of 72% and a pooled specificity of 86% [46]. LUS can therefore help accurately diagnose pneumonia and may be promising as an alternative resource to traditional approaches. Indications for the use of sonography where pneumonia is suspected or present are as follows: 1) dyspnoea and fever, pleuritic pain; 2) to confirm a diagnosis of pneumonia; 3) a pleural/basal shadow on CXR; 4) visualisation of abscesses; 5) isolation of pathogens; 6) abscess drainage; and 7) follow-up of consolidation and pleural effusion.

A comparison of imaging tools Currently, international guidelines recommend CXR as the routine evaluation method for suspected pneumonia. However, CT is now the gold standard for detecting lung consolidation. In six studies that used chest CT as the sole criteria, LUS exhibited a pooled sensitivity of 91% and a pooled specificity of 90% [29, 34, 40, 42, 45, 47]. Recent studies show that ⩽25% more cases of pneumonia can be visualised with LUS than with CXR when CT is used as the reference method. In 112 patients with CAP correctly diagnosed with LUS and radiograph at baseline, both examinations were repeated between days 13 and 16. Concordant results were observed in 85 (75.6%) patients (35 negative, 48 positive, two equivocal). 11 cases of CAP were diagnosed with LUS but not radiograph. Conversely, nine cases of CAP were detected with radiography but were missed with LUS, controlled by CT, as is the gold standard [29]. LUS is a reliable tool for bedside diagnosis of ventilator-associated pneumonia. LUS was effective in reducing the number of CXRs, the relative medical costs and the radiation exposure in the intensive care unit (ICU), without affecting patient outcome [15, 50–54]. LUS has a sufficiently high interrater reliability for the detection of lung consolidation [40]. In a feasibility and safety trial for the substitution of LUS for CXR when diagnosing pneumonia in children, there was a 38.8% reduction in CXR among subjects with 94

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Figure 7. Persistent pleural effusion in a 32-year-old woman. Note the nodular and large thickening below the visceral pleura, seen through the 15 mm-wide pleural effusion. The diagnosis of tuberculosis was confirmed with sonography-guided biopsy.

pneumonia compared with no reduction in the control group. Novice and experienced physician-sonologists achieved 30.0% and 60.6% reductions, respectively, in CXR use. There were no cases of missed pneumonia among the study participants [55]. In conclusion, some authors propose that LUS should be used as the first-line examination instead of CXR, and that chest CT should be reserved for complicated cases. Therefore, the investigator should use LUS after performing a stethoscope-based investigation in patients with fever and dyspnoea, particularly in the ED and the ICU [56–58].

Tuberculosis and other infections Lung tuberculosis (TB) offers very different findings in every imaging modality. LUS is very limited because it does not provide a complete overview of the chest. However, in some fields, LUS can provide information additional to that of other radiographic techniques, with better resolution, as follows: narrow pleural effusions; small subpleural nodules; small fluid collections in a consolidated lung; and finally, better visualisation of the lymph nodes (figure 7). Tuberculotic abscesses and cavern formations may be detected as hypoechogen fluid collections, but air in the cavern may prevent visualisation of their dimension. Further radiographic imaging is indispensable in this setting. Follow-up is possible in patients with pleural effusion, pleural and subpleural nodules, lung consolidations coming up to pleura line, and enlargement of the lymph nodes. Post-tuberculous nodular scars look like neoplasms and can be differentiated with US-guided core biopsy, in doubt through labour testing by PCR [4, 59, 60]. As previously discussed, the usefulness of LUS in the diagnosis and follow-up of TB is limited. LUS can raise the suspicion of TB, according to clinical presentation, and represents a complementary, sometimes better imaging modality. Diagnosis is possible with US-guided puncture (figure 7). In some cases, monitoring is also possible. There is less literature on this topic, and this latter point was derived from expert meetings. https://doi.org/10.1183/2312508X.10006617

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Figure 8. Aspergillosis in a 38-year old woman. The consolidation is inhomogeneus with large air inlets, not a typical tree-like bronchoaerogram.

Several reports discuss rarer infectious lung consolidations, such as aspergillosis, echinococcosis or chronic organising pneumonia (figures 8 and 9) [6]. Their size and shape can be demonstrated as well as their vascularisation. Rheuma nodules are detected in a few cases, and are at fist sight similar to metastases (figure 10). Diagnosis is possible with US-guided puncture (figure 8). In some cases, monitoring is also possible.

Figure 9. Chronic organising pneumonia after fungal sepsis and 11 days in intensive care with ventilation. 5 weeks later, the patient had cachexia and dyspnoea. Subpleural consolidations with air inlets and irregular borders were noted. Diagnosis was confirmed using US-guided biopsy.

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Figure 10. Rheuma nodule in a 63-year-old patient with rheumatoid arthritis in remission. Metastasis was initially suspected and this was constantly seen in follow-up.

Interstitial lung disease The pleura is involved in many interstitial lung diseases. Pleural changes are better demonstrated with sonography than with other imaging modalities. In patients with dyspnoea or pleuritic pain, a diffuse interstitial syndrome, point-of-care LUS can lead to the next efficient diagnostic steps. Sonographic signs of interstitial lung disease are as follows: 1) multiple B-lines in irregular distribution; 2) fragmented pleura with pleura thickening 3) subpleural consolidations (figure 9b); and 4) minimal pleural effusions (figure 9a). The primary sonographic sign to be identified is the presence of multiple B-lines in a diffuse and nonhomogeneous distribution. B-lines are defined as discrete laser-like vertical hyperechoic reverberation artefacts that arise from the pleural line ( previously described as “comet tails”), extend to the bottom of the screen without fading, and move synchronously with lung sliding [45]. Patients with diffuse parenchymal lung disease (e.g. exogen allergic alveolitis, pulmonary fibrosis) often have pleural line abnormalities; the distribution of B-lines correlates with signs of fibrosis on CT [13, 42, 47, 48, 61–63]. The value of the method lies in the detection of a serious condition and in steering the diagnostician’s attention towards a specific target (figures 10 and 11). Therapy controls are highly efficient in cases of minimal pleural effusions and subpleural infiltrations; no method is superior to sonography in this regard.

The limitations of LUS The US image does not provide a complete overview of the chest. However, it does show a certain portion of the lung surface and thus provides diagnostic information about a variety of problems. LUS cannot see the depth of the healthy lung. Only alterations reaching up to the pleura, pathological artefacts and consolidations can be visualised. https://doi.org/10.1183/2312508X.10006617

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a)

b)

c)

Figure 11. Sarcoidosis. A 26-year-old male with “a cold”: dyspnoea, moderate pleuritic pain. a) Minimal basal pleural effusion. Fragmented pleura line with B-lines. b) Subpleural consolidations. c) Corresponding CT showing intrapulmonal alterations.

A lot of studies and eight meta-analyses have considered CAP. There is less research is on hospital-acquired pneumonia and lung consolidations in ICU. High-frequency and positive end expiratory pressure ventilated patients show less or no dynamic bronchoaerograms in consolidations. It is therefore difficult to differentiate obstructive atelectasis from pneumonia. Expectations based on clinical history and the patient’s physical presentation could be a further bias to the imaging examination. The examiner’s education and experience, and bad documentation could be further limitations.

Conclusion Based on the literature, LUS has a high accuracy of >90% in the diagnosis of community-acquired pneumonia. LUS cannot rule out pneumonia. The sonographer should strictly exercise the signs and sonomorphologic criteria. LUS has advantages beyond those of CXR when used in certain situations, such as for bedridden patients, in the emergency room, in pregnant patients, in children and so on. LUS lacks ionising exposure and can be performed at the bedside as well as in follow-up, especially in cases with 98

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parapneumonic effusion. Beyond CAP, other inflammatory lung diseases are less frequently studied. In these conditions, the value auf LUS is limited but it can help to plan further diagnostic strategies and imaging procedures.

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Disclosures: None declared.

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| Chapter 8 Pulmonary embolism Giovanni Volpicelli The diagnosis of pulmonary embolism is often a complex process that starts from clinical suspicion and is guided by risk stratification in selected populations. LUS may have a role in this process, as it is a valid technique that is highly specific for diagnosing typical peripheral lung infarctions and highly sensitive in ruling out alternative pulmonary diagnoses to pulmonary embolism. Either alone, or in particular in combination with cardiac and venous US, sonographic examination of the lung represents a valid alternative to a multidetector CT scan when the latter is unavailable or contraindicated. Moreover, when integrated in the pre-test clinical risk score assessment of pulmonary embolism, a multiorgan US based on evaluation of pulmonary peripheral infarctions and deep vein thrombosis is useful to improve the performance of the Wells score. Integration of US in the process to assess the risk score for pulmonary embolism may significantly reduce the number of unnecessary CT scans. Finally, LUS is also useful in all undifferentiated emergency situations, such as cardiac arrest, shock and respiratory failure, to orientate the diagnosis and include the possibility of unexpected pulmonary embolism. Cite as: Volpicelli G. Pulmonary embolism. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 102–114 [https://doi.org/ 10.1183/2312508X.10006717].

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he diagnostic process for pulmonary embolism is a typical example of a complex problem-solving procedure, particularly in an emergency situation. The clinical symptoms and signs of pulmonary embolism are not specific, and the diagnosis cannot rely on history and physical examination alone. In practice, patients are stratified into groups of expected prevalence before deciding how to proceed in order to rule the disease in or out. This stratification defines the pre-test probability, which can be assessed either empirically (“gestalt”) or by applying clinical prediction rules calculated using independent clinical predictors. These predictors have been strongly validated by multivariate regression models in cohorts of patients with suspected pulmonary embolism [1]. In the context of patients with suspected pulmonary embolism, LUS should be evaluated as a diagnostic method. More than simply finalising the diagnosis of pulmonary diseases and injuries, very often it may contribute to expedite the process, to guide further diagnostic steps and to help restrict the differential possibilities. The main principle of the efficacy of US in examination of the lung is based on the fact that changes in the condition of Dept of Emergency Medicine, San Luigi Gonzaga University Hospital, Torino, Italy. Correspondence: Giovanni Volpicelli, Dept of Emergency Medicine, San Luigi Gonzaga University Hospital, Torino, Italy. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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pulmonary aeration and density, even at a regional extension, generate different US patterns that may help rule in or out various diseases and injuries [2].

General considerations: the Bayesian era To optimise the diagnostic process and favour the safest and quickest decision making, the modern clinician is required to orient their mind between accredited rules on a daily basis. We currently live in the era of Bayesian medicine, which is the best-known approach for complex problem solving. According to Bayes’ theorem, the diagnostic process depends on consideration of the specific population being examined and the level of risk of having the disease in these patients [3]. Moreover, a complex evaluation of costs, benefits and invasiveness of the investigating tools must be considered to orientate the diagnostic work-up. Thus, the clinician cannot rely only on the calculated absolute accuracy of a positive or negative test to evaluate sufficiently the probability of disease; consideration about the prevalence of the disease in the tested population, as well as evaluation of the availability and opportunity to submit the patient to a specific test, are issues that may have a significant influence on the process. Thus, the three main steps that characterise the diagnostic work-up for pulmonary embolism are: 1) a suspicion of pulmonary embolism, 2) assessing the pre-test probability and 3) deciding the most appropriate test to finalise the diagnosis. This is a diagnostic cascade that cannot be interrupted. For instance, the diagnostic process for pulmonary embolism cannot perform correctly in a population without clinical symptoms or signs that support the suspicion. In addition, without stratifying the probability risk, the accuracy of the applied diagnostic tests will remain undefined. The European Society of Cardiology (ESC) has produced specific guidelines for the diagnostic process of pulmonary embolism [4], which start from the consideration of suspected pulmonary embolism. However, in the real practice of the emergency setting, suspicion of pulmonary embolism is not always the first step to initiate the diagnostic process. Sometimes, pulmonary embolism is a hidden or unlikely possibility, inside a more complex diagnostic process for undifferentiated respiratory failure, shock and hypotension, pleuritic pain or syncope, often in complex multipathological elderly patients. In these situations, pulmonary embolism may represent an even harder diagnostic challenge. The diagnostic process is also challenged by the difficult conditions that may be encountered, for example, in the case of unstable patients who cannot be moved in the radiology unit, or when the high risks linked to irradiation, allergies and renal failure contraindicate a contrast-enhanced CT scan.

LUS in pulmonary embolism In general, the main diagnostic possibilities for demonstrating pulmonary embolism are: 1) detecting the presence of a thrombus in the main pulmonary artery tree, 2) detecting the presence of a source thrombus in the deep venous system or in the right heart, 3) observing the upstream effect of the artery occlusion (i.e. the haemodynamic consequence visible in the right cardiac function) and 4) visualising the downstream effect of the artery occlusion in the form of peripheral pulmonary infarcts. The last condition is potentially detected by LUS. Indeed, peripheral infarctions are due to a cascade of events following the https://doi.org/10.1183/2312508X.10006717

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thrombotic occlusion of a secondary pulmonary artery, which causes, in rapid sequence, collapse of surfactant, inflow of interstitial fluid and erythrocytes, and congestion of the alveolar spaces. Histological investigation of the infarcted lung reveals the alveolar spaces to be congested with erythrocytes, but the structure of the organ is fully preserved. From the US point of view, this phenomenon is simply a condition of loss of aeration and an increase in density of a small region of the peripheral lung. As such, it is potentially readily detected by a change in the US pattern of the affected area when the latter is explored by the sonographic probe. The usefulness of LUS for pulmonary embolism has been investigated in the literature over the last 15–20 years, and it is clear that US represents a new and efficient tool in the armamentarium of physicians facing clinical conditions where pulmonary embolism is included in the differential diagnosis. The specific properties of the modern PoCUS make this tool particularly suitable at the bedside for guiding complex diagnostic processes [5]. US is a powerful, noninvasive diagnostic tool that may be repeated at the bedside to monitor changes in time, and may reduce costs and time, and is even more efficient when used by clinicians. In the existing literature, the validation of LUS for pulmonary embolism followed three sequential steps. The use of LUS alone was the first step, demonstrating that US had the potential to visualise lung infarcts and that it was a valid alternative to CT scans in the diagnostic work-up of pulmonary embolism. Next, multiorgan US was used to show that a combination of LUS with cardiac and venous US could improve the performance of each organ examination considered alone, particularly considering the potential of LUS to detect alternative pulmonary diagnoses. This multiorgan and multitask examination is even more valid as an alternative to CT scans, not only to confirm but especially to rule out the disease. Finally, the US-enhanced prediction rule was used to demonstrate that LUS, in combination with venous US, may be useful to improve the performance of the pre-test prediction rule in the diagnostic process for pulmonary embolism. Thus, LUS contributes to the definition of the pre-test clinical probability of disease and guides further diagnostic steps in patients with suspected pulmonary embolism. These three steps are discussed further. LUS alone: visualisation of lung infarcts

Several studies explored the accuracy of LUS for pulmonary embolism by investigating its potential in visualising the peripheral infarctions. The most significant was a multicentre study performed on 352 patients with suspected pulmonary embolism and admitted to internal medicine and pulmonology wards [6]. LUS was performed at the bedside and targeted to the visualisation of typical triangular or rounded pleural-based lesions. The main hypothesis was that at least two of these lesions were pathognomonic of the disease. The US technique consisted of scanning the whole chest in the anterior, lateral and posterior areas by longitudinal and oblique intercostal scans. The typical US lesions indicating peripheral lung infarctions appeared as small, well-defined consolidations with sharp margins, usually of triangular or rounded shape, with interruption of the pleural line and the absence of air bronchogram and vascularisation. These infarcts are considered significant when the diameter at the pleural surface is >5 mm (figure 1). In the study, the authors investigated four US patterns, assigning to each of them different diagnostic criteria in terms of probability of the disease: 1) confirmation of pulmonary embolism when at least two of these typical lung infarctions were detected, 2) probable pulmonary embolism when one typical lesion was detected combined with a corresponding low-grade pleural 104

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Figure 1. Two examples of typical infarcts detected by LUS in two cases of confirmed pulmonary embolism. The typical consolidations are hypoechoic images of size >5 mm, wedge or round shaped, pleural based and without air bronchogram or vascularisation.

effusion, 3) possible pulmonary embolism when small (5 mm) is currently widely accepted among experts. Lungs are wide organs. Thus, exploring the lung surface by US to look for consolidations should be extended to the whole chest, including the anterior, lateral and posterior walls. A whole-chest examination may be complex to perform in some patients and in some specific settings, particularly in an emergency setting and in the critically ill. There are some situations where LUS may reveal infarctions more reliably if guided in a restricted area by the patient’s symptoms. This is typically the case for pleuritic pain. The usefulness of US to reveal pulmonary radio-occult conditions causing pleuritic pain has been clearly demonstrated [8, 9]. In these cases, US is very efficient simply because pain reveals the involvement of the parietal pleura. Thus, when the pain is due to a pulmonary disease, it is peripheral and potentially visible by LUS. Pleuritic pain is also a common and frequent symptom in pulmonary embolism. Unpublished data obtained by analysing three databases from multicentre studies on LUS for pulmonary embolism have shown that LUS performed better in terms of sensitivity and specificity in the subgroup of patients complaining of pleuritic pain (table 1) [10–12]. The first international consensus conference on point-of-care LUS discussed the evidence on the usefulness of LUS for pulmonary embolism [13]. The results confirmed the usefulness of LUS as a valid alternative to CT when the latter cannot be used. This validated technique is based on whole-chest examination for the detection of typical images corresponding to pulmonary infarctions. The sonographic signs are small (1–3 cm, range 0.5–7 cm), pleural-based, echo-poor consolidations with sharp margins and without central vascularisation. These signs have a good specificity, but the studies analysed by the consensus process did not show an optimal sensitivity (80%). In practice, in suspected pulmonary embolism with a level of probability of disease that indicates further testing, and Table 1. Diagnostic performance of LUS for the diagnosis of pulmonary embolism in unselected patients, and in patients without and with pleuritic chest pain

Patients n Sensitivity % (95% CI) Specificity % (95% CI) PPV % (95% CI) NPV % (95% CI) PLR (95% CI) NLR (95% CI)

All patients

No pleuritic chest pain

Pleuritic chest pain

872 57.0 (51.0–62.9) 94.9 (92.9–96.6) 84.1 (78.1–89.0) 82.4 (79.4–85.2) 11.3 (7.83–16.20) 0.45 (0.40–0.52)

655 49.5 (42.7–56.4) 94.8 (92.3–97.7) 82.2 (74.5–88.4) 79.5 (75.8–82.8) 9.50 (6.24–14.46) 0.53 (0.47–0.61)

217 81.5 (70.0–90.1) 95.4 (90.7–98.1) 88.3 (77.4–95.2) 92.4 (87.0–96.0) 17.71 (8.51–36.84) 0.19 (0.11–0.31)

The meta-analysis was performed on the databases of three multicentre studies [10–12]. Data represent work in progress and are unpublished. PPV: positive predictive value; NPV: negative predictive value; PLR: positive likelihood ratio; NLR: negative likelihood ratio.

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when a CT scan cannot be undertaken, the caring physician should consider LUS. Detection of typical US signs allows diagnosis with good specificity, but the absence of typical infarctions does not rule this out with certainty, and further testing would be necessary when the probability of disease remains high. The consensus conference also recommended the use of LUS in pleuritic pain, as this technique is highly reliable in the detection of pulmonary conditions not visible by chest radiography, including lung peripheral infarctions due to pulmonary embolism [13]. Multiorgan US for diagnosis

In the diagnostic process for pulmonary embolism, organs other than the lung may also be the object of an US examination and may provide indirect signs of the disease. Cardiac US Cardiac US is targeted to the demonstration of the haemodynamic effect of pulmonary embolism (i.e. dysfunction of the right ventricle) [10, 14, 15]. The most used sign is dilation of the ventricle, which is assessed semi-quantitatively by comparing the end-diastole measures of the diameters of the two ventricles [10]. The normal dimension of the right ventricle, when compared with the left ventricle, is fixed in terms of percentage at a cut-off that is slightly variable depending on the window used, between the apical, subcostal and parasternal windows [10, 14, 16]. In the apical four chambers (i.e. the optimal view for assessing the right dilation), the diameters of the two ventricles are assessed close to the valve level, and a ratio of 0.9 represents the cut-off value to define dilation. Evidence of right-ventricle dilation is a sign of acute strain in haemodynamically unstable patients with suspected pulmonary embolism, and should confirm the diagnosis when CT cannot be performed [4]. However, dilation of the right ventricle has two main limitations in the diagnostic process for pulmonary embolism. First, it is not sensitive enough to also be used in stable patients [4]. In cases of pulmonary embolism with stable haemodynamics, it is quite common to observe a normal right ventricle. Second, in patients with chronic diseases, right-ventricle dilation may exist prior to the acute event, thus inducing a misdiagnosis. The ESC guidelines recommend considering additional US signs indicating chronic dilation, and do not recommend the use of echocardiography as part of the diagnostic work-up in haemodynamically stable, normotensive patients and in patients who are not high risk [4]. Additional dynamic echocardiography signs, such as depressed contractility or a disturbed ejection pattern of the right ventricle, may be considered, but these signs are more complex to assess in an emergency situation. Assessment of the thickness of the free walls of the right ventricle is more practical and may help in differentiating chronic situations. Venous US Compressive venous US has an important role in the diagnostic work-up of pulmonary embolism. Lack of compressibility of the deep veins of the legs at two points, corresponding to the common femoral and the popliteal veins, with some extension to the proximal main tributary veins, is the validated US sign allowing direct confirmation of a source of thrombosis [17–19]. The technique consists of pressing the probe on the veins visualised on the screen in the short axis. Lack of total occlusion of the pressured vein is a highly specific sign, which authorises the caring physician to finalise the diagnosis in patients with suspected pulmonary embolism, independent from CT scan confirmation [4]. However, as for right-ventricle dilation in echocardiography, evidence of a thrombus during venous US is also of low sensitivity, as ∼50% of patients with confirmed pulmonary embolism have no more thrombotic material deposited in the peripheral deep veins. In https://doi.org/10.1183/2312508X.10006717

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some cases, corresponding to 4% of unselected patients with pulmonary embolism, mobile right-heart thrombi are visible by transthoracic echocardiography [20]. This sign also allows confirmation of pulmonary embolism and concludes the diagnostic work-up. Multiorgan US Echocardiography for right-ventricle dilation and venous compressive US for signs of thrombosis are currently considered part of the bedside point-of-care examination. This is due to the widespread use of new portable machines and growing evidence on the reliability of bedside US in the hands of the clinician. In the diagnostic work-up of pulmonary embolism, echocardiography, venous US and LUS all have the potential to be of use. However, in the existing literature, these three techniques considered alone have demonstrated good specificity but low sensitivity [6, 14, 19]. When negative, none of the three examinations considered alone is enough to rule out the disease in an unselected population with an open diagnostic dilemma for pulmonary embolism. Thus, the question was raised as to whether a combination of the three techniques might improve this insufficient sensitivity.

The answer to this question was provided by a multicentre trial that demonstrated, in 357 patients, the high feasibility and reliability of a multiorgan US evaluation in suspected pulmonary embolism, targeted to visualisation of lung infarcts, dilation of the right ventricle and lack of compressibility of the deep leg veins [10]. In this study, the negative predictive value of the multiorgan approach was increased to 95%, compared with 84.6% for LUS, 74.8% for echocardiography and 82.2% for venous US alone. The study also showed that LUS and echocardiography may be useful to diagnose alternative conditions to pulmonary embolism, such as pneumonia, pneumothorax, pleural effusion, pericardial effusion and cardiogenic pulmonary oedema [10]. Using this potential, the combination of negative multiorgan US coupled with a positive alternative diagnosis raised the negative predictive value to 100%. This combination was observed in 37% of cases in the population showing positive D-dimer result or a high-probability Wells score. Considering also the positive diagnosis of deep vein thrombosis obtained in the same population (17.9% of patients), there was a high percentage of patients (55%) who might avoid an MDCT scan, which would still be considered necessary if based on the conventional rules [10]. Another study tested the multiorgan approach for pulmonary embolism. This study was focused mainly on the hypothesis that integrating US of the lung, heart and leg veins may be useful to reduce the number of CT scans in cases of suspected pulmonary embolism [21]. Again, the results of the study were encouraging, as the authors found 56% of cases where the sonographic alternative diagnosis to pulmonary embolism or the direct visualisation of the venous peripheral thrombi might allow the avoidance of CT scans, with 100% sensitivity in a population of 96 patients. Indeed, the conclusion of the study was that a multiorgan US approach safely reduces the number of unnecessary CT scans ordered to rule out pulmonary embolism. In this study, the authors applied LUS only for diagnosing alternative pulmonary conditions and did not consider the potential of a direct visualisation of pulmonary infarctions [21]. The same authors concluded that incorporating this adjunctive LUS technique would allow an even greater reduction in the use of unnecessary CT scans. My personal comment is that, rather than just confirming pulmonary embolism, LUS for infarctions may allow a safe exclusion of the disease when the multiorgan test is negative, as was demonstrated by the study of NAZERIAN et al. [10]. Indeed, KOENIG et al. [21] observed 30% of cases where pulmonary embolism was confirmed although cardiac and venous US examinations were negative, but in the absence of alternative diagnoses. Thus, the question remains unanswered as to whether integrating the US investigation for infarctions might 108

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have improved the results for this 30%, using not only the confirmation of an alternative disease but also the negativity of the three tests to rule out the disease. The international consensus conference also discussed the integration of LUS in a multiorgan approach for pulmonary embolism and concluded that, when used in conjunction with echocardiography for right-ventricle dilation and leg-vein US for proximal thrombi, the sensitivity rises [13]. The consensus conference also noted the results of a study on the BLUE protocol [22]. This is a protocol for LUS validated in the selected population of critically ill patients with acute respiratory failure. In this population, regular sliding with predominant A-lines (normal aeration) in the anterior chest coupled with signs of thrombosis in the deep veins allow the confirmation of pulmonary embolism. Using these criteria, the diagnosis of pulmonary embolism was obtained with good specificity (99%) by the authors [22]. However, the validity of this approach is limited to populations with the specific characteristics reported in the study. These experiences from multiorgan US further confirm the usefulness of LUS for pulmonary embolism. When LUS is integrated in a multiorgan approach, it represents a better alternative to CT when the latter is unavailable or contraindicated. Prediction rule enhanced by US

Following the Bayesian methodology, the diagnostic work-up for pulmonary embolism is guided by standardised prediction rules to define the probability of disease and orientate the process. Once the validity of LUS as an alternative to CT scans in the diagnostic work-up of pulmonary embolism had been explored, there was one further question that remained unanswered: is it useful to integrate US into the clinical prediction rule that is applied in the suspicion of pulmonary embolism? For assessing the probability of disease, the ESC guidelines recommend the combination of D-dimer tests with clinical scores, such as the Wells score, which optimises the diagnostic process, and the use of a CT scan for final confirmation [4]. The clinical score is based on evaluation of a list of items, of which the most weighted are the probability of pulmonary embolism and clinical signs of deep vein thrombosis [23]. These two items are based on considerations that are strictly subjective and remain highly variable when decided by physicians with different skills and experience. Both the alternative pulmonary diagnosis and the venous thrombosis are two conditions that PoCUS can objectively confirm at the bedside during the first examination of patients with suspected pulmonary embolism. Thus, the hypothesis that integration of the clinical evaluation with US of the lung and leg veins might improve the efficiency of the pre-test clinical scoring needs to be investigated. A recent multicentre study responded to this question by investigating 446 patients with suspected pulmonary embolism in the emergency department of four academic institutions [10]. LUS for the evaluation of typical pulmonary infarctions or alternative pulmonary conditions, and compression US of the leg veins for peripheral thrombi were performed during the first evaluation in all patients. The objective results of the bedside US examination were used to adjudicate the first two items of the Wells score, replacing the clinical subjective judgements. After finalisation of the diagnosis, based on a combination of MDCT scan and clinical follow-up, the performances of the traditional clinical Wells score and the US-enhanced Wells score were compared. The results of the study demonstrated a better performance of the US-enhanced Wells score in terms of both https://doi.org/10.1183/2312508X.10006717

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sensitivity (12% increase) and specificity (22% increase) [11]. The conclusion of the study was that a diagnostic strategy that integrates clinical information, lung and venous US, and D-dimer results may increase the performance of risk stratification and may reduce the use of CT scans in the diagnostic approach to pulmonary embolism, while still maintaining an acceptable safety profile. Figure 2 shows a newly proposed diagnostic algorithm for suspected pulmonary embolism, based on venous US, US Wells scores and D-dimer results. The application of this revolutionary US/clinical scoring would hypothetically have allowed the avoidance of 50.5% of CT scans in the population of the study. These data pave the way for a new consideration of the usefulness of PoCUS for pulmonary embolism, which includes the significant potential of LUS. Rather than just serving to confirm the diagnosis when CT is contraindicated or unavailable, a systematic application to the whole unselected population with suspected pulmonary embolism may allow further optimisation of the diagnostic work-up and reduce the need for confirmatory CT.

LUS in cardiac arrest, undifferentiated hypotension and respiratory failure In the daily practice of crowded and busy emergency departments and in critically ill patients, physicians face challenging and complex diagnostic situations where pulmonary embolism may be unlikely but should still be included as a possibility. In these situations,

Suspected pulmonary embolism

Diagnosis of DVT

Venous US

DVT excluded

US Wells score ≤4

Negative D-dimer

Pulmonary embolism ruled out

LUS

Positive D-dimer

US Wells score >4

Multidetector CTPA

Pulmonary embolism ruled in

Figure 2. Proposed flow chart for the diagnostic work-up in suspected pulmonary embolism, based on the integration of venous US and LUS with clinical scoring and D-dimer results. This new strategy allows the avoidance of unnecessary multidetector CT scans in a higher percentage of patients than the traditional combination of clinical scoring/D-dimer results. DVT: deep vein thrombosis; CTPA: CT pulmonary angiogram.

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the conventional guidelines based on risk stratification may sometimes be inappropriate. Indeed, the guidelines work in common situations where the first step is a strong suspicion of pulmonary embolism. This is not always the case in some undifferentiated emergencies, where the spectrum of diagnostic hypothesis is too wide to assign a specifically oriented diagnostic work-up. In cardiac arrest, in undifferentiated hypotension and shock, and in acute respiratory failure, the possibility of pulmonary embolism is always considered but rarely represents the first hypothesis. In these situations, the added value of PoCUS is increased. Several studies have demonstrated that LUS performed in the first examination of the patient at the bedside contributes to orientate the diagnosis in acute shock and respiratory failure; in a multiorgan US combination, it was possible to rule pulmonary embolism in or out with high pooled sensitivity and specificity [22, 24, 25].

Conclusion and future perspectives The role of LUS in the diagnostic work-up for pulmonary embolism is highly variable when considering the characteristics of the population, the haemodynamic condition of the patient, the probability of the disease and the availability of alternative tools, as well as the related biological risks and costs. There is already good evidence that LUS may be extremely useful in the diagnostic work-up of pulmonary embolism at the bedside. PoCUS is a relatively low-cost technology, is free from irradiation, is noninvasive, and is easily performed and repeatable at the bedside in the hands of trained clinicians. In contrast, a CT scan is costly, invasive and difficult to perform in emergency situations. We should never forget that the advanced and wealthy health systems of western countries serve only a small minority of humankind. Most of the world’s population have no access to advanced and costly technology. In resource-scarce areas, US may be the only available imaging tool. Moreover, the invasiveness of CT with the possible side-effects of irradiation and contrast medium injection, together with the inability to move unstable patients to the radiology area, sometimes mean that this technology is contraindicated. In cases where it is not possible to perform CT scans, LUS targeted to visualisation of peripheral lung infarctions may be a valid alternative. Once the typical infarcts are detected, the diagnosis becomes highly probable. If no typical infarcts are detected, the sensitivity is not enough to conclude a diagnosis of exclusion. A multiorgan approach that includes lung, cardiac and venous US, which also considers the possibility of evaluating alternative cardiac and pulmonary diagnoses to pulmonary embolism, increases the sensitivity and may be considered safe to rule the condition in or out in the unselected population with suspected pulmonary embolism. Table 2 summarises the efficacy of each individual US pattern in ruling the condition in or out in patients with suspected pulmonary embolism. Further studies are needed to compare US with pulmonary scintigraphy (V/Q scan), which to date represents the accredited alternative to CT scans in the ESC guidelines [4]. The PIOPED (Prospective investigation of pulmonary embolism diagnosis) II trial showed that the sensitivity of a high-probability V/Q scan was 77.4%, while the specificity of a very low probability or normal V/Q scan was 97.7% [26]. However, the occurrence of a nondiagnostic intermediate V/Q scan represents the main criticism of this method. In the same study, only 73.5% of patients had a conclusive V/Q scan, but this percentage may be far lower in common daily practice. A V/Q scan is an invasive procedure, although the irradiation for an average-sized adult (1.1 mSv) is lower than that for CT angiography (2–6 mSv) but still significant [27]. Thus, for ethical reasons, LUS and lung scintigraphy cannot be compared by simple https://doi.org/10.1183/2312508X.10006717

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observational protocols using CT angiography as the gold standard. Rather, more expensive randomised controlled trials would be indicated, based on a comparison of two different populations and using complex follow-up strategies to confirm the diagnosis. Further efforts should also be made to better standardise the US criteria for the diagnosis of typical infarctions. Indeed, the sonographic appearance of the peripheral infarctions changes with time ( personal observations). This change may represent a limitation of the technique if there is no consideration of the difference in time between the onset of symptoms and the LUS examination.

Table 2. Significance of single US patterns in ruling pulmonary embolism in or out in the bedside diagnostic work-up of suspected pulmonary embolism US pattern

Rule in

Rule out

Pulmonary infarctions

+

−

Alternative pulmonary diagnosis

−

++

DVT

++

−

Dilated RV

++

−

Pulmonary infarcts plus dilated RV plus DVT

+++

−

−

++

−

+++

Absence of pulmonary infarcts, normal RV, compressible deep veins Absence of pulmonary infarcts, normal RV, compressible deep veins, plus alternative pulmonary diagnosis

Comments

Positivity is two or more typical wedge-shaped or rounded pleural-based lesions of >5 mm; it should be considered when a CT study is not available [6] Strong evidence of an alternative diagnosis to pulmonary embolism at LUS, including pulmonary oedema, pneumonia and pneumothorax, is highly sensitive to rule out pulmonary embolism [10, 21] Evidence of a thrombosed deep vein allows the diagnosis to be finalised without the need for CT [10, 21] This is only valid in the extreme emergency situations of cardiac arrest and shock; evidence of a dilated RV authorises the physician to proceed with lifesaving treatment [4] Positivity of all three organ US signs is highly specific and allows the diagnosis to be concluded; this is even more specific than evidence of DVT alone, as some cases of DVT do not show pulmonary embolism [10] Negativity of the three organ US signs allows the exclusion of pulmonary embolism with a high NPV (95%) [10] Negativity of the three organ US signs plus evidence of an alternative pulmonary diagnosis allow exclusion of pulmonary embolism with the highest sensitivity (NPV 100%) [10, 21]

–: a negative pattern cannot be considered conclusive; +: a positive pattern is useful to orientate the diagnosis rather than conclusive; ++: a positive pattern may be considered conclusive but only in some conditions; +++: a positive pattern is safely conclusive. DVT: deep vein thrombosis; RV: right ventricle; NPV: negative predictive value.

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Another suggestive potential of LUS is its integration in the clinical prediction rule for risk assessment. Integrating lung and venous US with the Wells score and D-dimer results in the first examination of a patient with suspected pulmonary embolism improves the performance of the process for clinical risk assessment, thus contributing to a reduction in the number of unnecessary CT scans. Further studies are needed to test, in sufficient numbers of patients, a new diagnostic strategy based on steps in succession, starting with venous US, and followed by LUS, integrated US Wells scores and D-dimer results (figure 2). In conclusion, evidence of the usefulness of US in pulmonary embolism has come to the fore in recent years, and more evidence will certainly be derived in the future. This should be enough to alert the main scientific societies and start the long and complex process to conform future societal guidelines on pulmonary embolism.

References 1.

2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14.

15. 16.

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Wells PS, Anderson DR, Rodger M, et al. Excluding pulmonary embolism at the bedside without diagnostic imaging: management of patients with suspected pulmonary embolism presenting to the emergency department by using a simple clinical model and D-dimer. Ann Intern Med 2001; 135: 98–107. Volpicelli G. Lung sonography. J Ultrasound Med 2013; 32: 165–171. Le Gal G, Righini M. Controversies in the diagnosis of venous thromboembolism. J Thromb Haemost 2015; 13: Suppl. 1, S259–S265. Konstantinides SV, Torbicki A, Agnelli G, et al. ESC guidelines on the diagnosis and management of acute pulmonary embolism. Eur Heart J 2014; 35: 3033–3069. Moore CL, Copel JA. Point-of-care ultrasonography. N Engl J Med 2011; 364: 749–757. Mathis G, Blank W, Reissig A, et al. Thoracic ultrasound for diagnosing pulmonary embolism: a prospective multicenter study of 352 patients. Chest 2005; 128: 1531–1538. Squizzato A, Rancan E, Dentali F, et al. Diagnostic accuracy of lung ultrasound for pulmonary embolism: a systematic review and meta-analysis. J Thromb Haemost 2013; 11: 1269–1278. Volpicelli G, Caramello V, Cardinale L, et al. Diagnosis of radio-occult pulmonary conditions by real-time chest ultrasonography in patients with pleuritic pain. Ultrasound Med Biol 2008; 34: 1717–1723. Volpicelli G, Cardinale L, Berchialla P, et al. A comparison of different diagnostic tests in the bedside evaluation of pleuritic pain in the ED. Am J Emerg Med 2012; 30: 317–324. Nazerian P, Vanni S, Volpicelli G, et al. Accuracy of point-of-care multiorgan ultrasonography for the diagnosis of pulmonary embolism. Chest 2014; 145: 950–957. Nazerian P, Volpicelli G, Gigli C, et al. Diagnostic performance of Wells score combined with point-of-care lung and venous ultrasound in suspected pulmonary embolism. Acad Emerg Med 2017; 24: 270–280. Reissig A, Heyne JP, Kroegel C. Sonography of lung and pleura in pulmonary embolism: sonomorphologic characterization and comparison with spiral CT scanning. Chest 2001; 120: 1977–1983. Volpicelli G, Elbarbary M, Blaivas M, et al. International evidence-based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012; 38: 577–591. Grifoni S, Olivotto I, Cecchini P, et al. Utility of an integrated clinical, echocardiographic, and venous ultrasonographic approach for triage of patients with suspected pulmonary embolism. Am J Cardiol 1998; 82: 1230–1235. Miniati M, Monti S, Pratali L, et al. Value of transthoracic echocardiography in the diagnosis of pulmonary embolism: results of a prospective study in unselected patients. Am J Med 2001; 110: 528–535. Steering C. Single-bolus tenecteplase plus heparin compared with heparin alone for normotensive patients with acute pulmonary embolism who have evidence of right ventricular dysfunction and myocardial injury: rationale and design of the Pulmonary Embolism Thrombolysis (PEITHO) trial. Am Heart J 2012; 163: 33–38. Bernardi E, Camporese G, Buller HR, et al. Serial 2-point ultrasonography plus D-dimer vs whole-leg color-coded Doppler ultrasonography for diagnosing suspected symptomatic deep vein thrombosis: a randomized controlled trial. JAMA 2008; 300: 1653–1659. Elias A, Colombier D, Victor G, et al. Diagnostic performance of complete lower limb venous ultrasound in patients with clinically suspected acute pulmonary embolism. Thromb Haemost 2004; 91: 187–195. Le Gal G, Righini M, Sanchez O, et al. A positive compression ultrasonography of the lower limb veins is highly predictive of pulmonary embolism on computed tomography in suspected patients. Thromb Haemost 2006; 95: 963–966.

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Disclosures: None declared.

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| Chapter 9 Lung tumours Christian Görg1, Corinna Trenker1 and Andreas Schuler2 The diagnostic value of TUS of lung tumours, especially bronchial carcinomas, is limited and dependent on the localisation of the tumour. Focused clinical use is to be distinguished in the context of primary diagnosis, staging, therapy response and tumour growth. Symptom-oriented practice is important at the bedside for palliative patients, in point-of-care sonography, in the emergency room and in intensive care units. Different US-based procedures, such as transcutaneous US, EUS and EBUS are used for distinct approaches to lung tumours. B-mode imaging, colour Doppler sonography, CEUS and US-controlled interventions are the sonographic modalities used in daily clinical practice and for special clinical questions. In special clinical indications, US is the primary guideline diagnostic procedure. Transthoracic LUS is limited by physical factors such as absorption and reflection and, in principle, by a high interobserver variability, as well as differences in device and examining competence. Cite as: Görg C, Trenker C, Schuler A. Lung tumours. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 115–128 [https:// doi.org/10.1183/2312508X.10006817].

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ung tumours are amongst the most frequently seen malignant tumours in the world and are one of the most common causes of cancer death [1]. Smoking is a major risk factor. Clinical symptoms are uncharacteristic and include cough, dyspnoea, haemoptysis, weight loss and occasional chest pain. Diagnostic procedures, therapy and follow-up are presented in the current guidelines [2]. A whole-body PET (PET-CT) in combination with an all-body CT, a radiographic thorax examination and EBUS, is part of the standard diagnostic procedure [3]. Transoesophageal US (EUS), angiography, MRI, mediastinoscopy and ultimately transcutaneous sonography are additional methods. The aims of the diagnostic procedures are correct tumour diagnosis and characterisation of the cancer, including TNM (tumour, node, metastases) classification [4–7]. In the context of diagnosis and therapy of lung tumours, transcutaneous LUS is used for primary tumour diagnosis and differential diagnosis, histological confirmation, staging, therapy response, aftercare and detection of tumour- or therapy-associated complications [8, 9]. The following modalities are used: B-mode imaging [10–12], colour Doppler sonography (CDS) [13, 14], CEUS [15– 18] and US-guided biopsy [19, 20]. The benefits of US examination are: high spatial resolution, real-time conditions, the absence of radiation exposure [21], arbitrary repeatability, and the possibility of bedside examination. Last but not least, ultrasound 1 Universitatsklinikum Giessen und Marburg, Marburg, Germany. 2Alb Fils Kliniken, Zentrum Innere Medizin, Helfenstein Klinik Geislingen, Geislingen, Germany.

Correspondence: Christian Görg, Universitatsklinikum Giessen und Marburg – Standort Marburg. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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examination as a dialogue is important for tumour patients [22]. LUS is limited by interobserver variability, a lack of overview, and physically induced limitations on the thorax caused by sound reflexion behind bony structures and the air-filled lung [23]. According to the diagnostic guidelines, the following indications for US can be distinguished. 1) Visualisation and characterisation of peripheral pleural-based lung tumours [24] with regard to thoracic wall infiltration [25, 26], the possibility of histological diagnosis with percutaneous tumour biopsy [27–29], detection of pleural effusion [30–32] and initiation of paracentesis (T-Stage) [33]. 2) Visualisation and characterisation of the peripheral collar [4, 34, 35] and mediastinal lymph nodes with percutaneous and endosonographic US, and possibly US-guided biopsy (N-Stage). 3) Specific presentation, characterisation and, where appropriate, histological preservation of otherwise unclear tumour formations within the context of staging procedures (M-Stage) [9, 36].

Lung sonography where a lung tumour is suspected In the diagnosis and differential diagnosis of bronchial carcinoma, CT of the thorax is the standard procedure for T-classification, and where possible, should be taken as the basis of US examination. An indication for transthoracic LUS does not exist in general, but can be deployed in a focused manner, according to the clinical questions. First, basic and sonographic criteria of lung tumour assessment will be presented. Subsequently, sonographic findings will be presented with regard to the clinical questions. Lung sonography where a lung tumour is suspected is limited and depends on the presentation of the primary tumour. In general, peripheral lung tumours can be differentiated from central tumours. While peripheral tumours can be visualised due to contact with the pleural/thoracic wall, central lung tumours can only be detected with associated obstructive atelectasis or pleural effusion with compression-induced atelectasis (figure 1) [37, 38]. In B-mode imaging, pulmonary consolidations are characterised by their size, margins and echogenicity, and the homogeneity of the lung tissue. In CDS, vascularisation is evaluated by the extent of the CDS (missing, reduced, marked flow signals) and the vascular patterns (regular, disordered vessels) [39]. With spectral curve analysis (SCA), high-impedance can be differentiated from low-impedance flow signals in the consolidated lung; high-impedance flow signals can be assigned to the pulmonary arteries and low-impedance flow signals to the bronchial arteries [40–42]. Tumour neoangiogenic capacity is attributed to the bronchial arteries [43–46]. CEUS of the thorax is possible and has to be performed according to the guidelines of the European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB) [15]. The first evaluation criterion is the “time to enhancement”. Pulmonary artery supply of a pulmonary lesion can be determined by early arterial enhancement before systemic vascular enhancement. Bronchial artery supply is characterised by delayed arterial enhancement at the same time as systemic vascular presentation. Further CEUS evaluation criteria are the 116

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Figure 1. Patient with lung consolidation primarily suspected of pneumonia. Histological examination due to bronchoscopy revealed bronchioloalveolar nonsmall cell lung cancer. a) CXR shows a right-sided lung consolidation. b) CT shows a right-sided homogeneous lung consolidation. c) B-mode US shows a homogeneous hypoechoic lung consolidation without airbronchogram. d) Colour Doppler sonography shows marked regular vessels. e) Spectral curve analysis shows a high impedant flow signal due to pulmonary arterial supply. f) CEUS shows marked pulmonary arterial enhancement in the arterial phase (10 s). g) CEUS shows marked enhancement in the parenchymal phase (1 min).

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“extent of enhancement” (none, reduced, marked) and the “homogeneity of enhancement” (homogeneous, inhomogeneous). These CEUS patterns may be analysed in the arterial and parenchymal phase [16, 18]. Another procedure is US-guided biopsy of thoracic tumours [19, 20, 47]. Differentiation is made between the size of the biopsies (core needle: >1 mm needle diameter; fine needle: 90% US) [69]. Specificity is lower with all imaging modalities to exclude malignancy. Lymph node metastasis in the neck are mostly hypoechoic, with a transversal diameter of ⩾5 mm. Transcutaneous lymph node core needle biopsy for histological purposes is highly recommended in such patients. Patients with mediastinal lymph node metastasis in N3 https://doi.org/10.1183/2312508X.10006817

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Figure 4. Patient with histologically proven nonsmall cell lung cancer and pleural effusion. a) CXR shows a left-sided basal opafication suggestive of pleural effusion. b) CT shows a left-sided pleural effusion with pleural nodules. c) B-mode US shows a left-sided echofree pleural effusion with echoic nodular pleural lesions. d) CEUS shows an enhancement of the pleural lesions suggestive of pleural carcinosis. Cytological examination of the pleural fluid shows tumour cells.

position have ⩽51% enlarged supraclavicular lymph nodes which are not palpable. Positive histology findings in lymph nodes of the neck lead to a complete change in therapeutic management due to inoperability at stage IIIB lung cancer [4, 34]). Particularly in patients with negative cyto-histology for primary tumours or mediastinal lymph nodes seen in other biopsy procedures (such as transbronchial biopsy), EUS or transcutaneous ultrasound provide histological proof of malignancy in the supraclavicular lymph nodes and avoid other more invasive procedures (such as mediastinoscopy and thoracoscopy).

Are there distinct sonographic patterns of lymph node metastasis in the neck?

It is well known that there are specific signs of malignancy in sonographic patterns of supraclavicular lymph node metastasis. Malignancy is strongly suspected if there is loss of the central hyperechoic hilum within the lymph node, as well as a round-shaped mostly hypoechoic lymph node with a transversal diameter of ⩾5 mm. Sometimes borders are not sharp, and in aggressively growing lymph node metastasis there might be signs of infiltration in the muscles, vessels or soft tissue. Vascularisation criteria for malignancy are peripheral vessels, an irregular vascular pattern and a chaotic spreading of vessels with different flow directions [70]. 122

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What are the potential differential diagnoses in enlarged or suspicious lymph nodes?

There is a wide range of potential differential diagnoses in enlarged or suspicious lymph nodes of the neck. The three main categories of enlargement are: inflammation, malignant lymphoma and metastasis. The US morphology of inflammatory lymph nodes is generally ⩽2 cm in diameter (oval or triangular), has clear and sharp margins, has a hyperechoic hilum compared with a hypoechoic cortex and has regular centrally located vascularisation in colour or power Doppler. A common finding of inflammatory lymphadenopathy is lymph nodes positioned one beside the other, in a row. Lymph nodes in tuberculosis sometimes show central hypoechoic (pseudocystic) areas due to central necrosis. Malignant lymphomas are mostly round shaped, very hypoechoic and do not have a central hilum sign and therefore cannot be differentiated from lymph node metastasis. With high-resolution transducers, a micronodular reticular structure can often be seen [71]. Vascularisation may be centrally located and may also be in in the peripheral zones of the lymph node [70]. Various head and neck malignoma of several primary origins can lead to lymph node metastasis: thyroid, parathyroid, pharyngeal and laryngeal tumours, salivary gland carcinoma, skin tumours and others. Chest tumours (lung cancer, breast cancer) and sometimes other cancers can lead to lymph node metastasis in the neck. Biopsy of suspicious lymph nodes is therefore highly recommended.

What is the preferred procedure to achieve a pathological diagnosis in enlarged or suspicious lymph nodes in the neck?

Enlarged or suspicious lymph nodes in the neck found using sonography can almost always be easily punctured with ( permanent) US-controlled histology (core needle biopsy) (figure 5). This is the most common and safest way to obtain histological specimens with only a minimal rate of complication [72]. Punctures should only be performed if there is any (diagnostic and/or therapeutic) consequence of the histological result. A colour Doppler should be performed to avoid accidental vessel injuries. The nerve bundle should be demonstrated if there is any doubt about its location in relation to the lymph nodes or other tumour presentation [69]. In a lymph node with a transversal diameter of ⩾5mm, a sufficient histological specimen can be achieved in nearly 100% of cases with an experienced examiner and an 18-G (1.2-mm) core needle. Cytology is less sensitive and specific for definite diagnosis; this is due to smaller specimen size and relatively less experience amongst pathologists. It is also increasingly necessary to perform immunohistological examinations with the acquired specimen to prove or exclude molecular mimicry and mutation. Clinically speaking, a proven supraclavicular lymph node metastasis refers to lung cancer stage N3 (figure 5).

Endosonographic staging in the evaluation of mediastinal lymph nodes The mediastinum, EBUS and EUS are covered elsewhere in this Monograph [73]. https://doi.org/10.1183/2312508X.10006817

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TU

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Figure 5. Supraclavicular lymph node metastasis in a patient with nonsmall cell lung cancer (Pancoast tumour). a) Location of the primary tumour (TU) in the right upper lung near to the pleura, beside the sternum (ST). Real-time US did not demonstrate an infiltration of the parietal pleura. Fine-needle aspiration of the primary lesions was not performed due to the location dorsal to the Arteria Mammaria interna (AMI). b) EBUS-FNA was performed for cytology of the mediastinal lymph node in position 3 (pretracheal). c) Suspicious supraclavicular lymph nodes on the left side (contralateral): hypoechoic, round shaped, >0.5 cm in short transversal axis. d) US-guided transcutaneous core-needle biopsy demonstrated histologically proven N3 stage (metastasis of nonsmall cell lung cancer). Two lymph nodes were punctured in one session.

Transcutaneous sonographic staging in the evaluation of PET-positive lesions If there are any suspicious positive lesions (in the lymph nodes, soft tissue/small part, bones, abdomen, chest) on PET-CT that could potentially be seen with transcutaneous US, then go for it! This means the supraclavicular lymph node positions as well as the supra-aortal and upper mediastinal positions could be seen transcutaneously. And by extension, this means all other previously mentioned lesions wherever they are. If there is any possibility of/necessity to achieve histology this should be done using real-time US 124

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Figure 6. Patient with swollen head and mediastinal tumour primarily suspected for lung cancer. a) CXR shows a mediastinal opafication suggestive of lung cancer. b and c) B-mode US of the left-sided jugular vein shows in the longitudinal and transversal scan, an echoic dilated venous vessel suggestive of vena cava superior syndrome. d) B-mode US shows a left-sided apical echoic lung consolidation. Histology revealed large cell lymphoma.

guidance before performing more invasive procedures (i.e. CT-guided puncture, mediastinoscopy, surgery) (figure 6).

Focused sonography in tumour- or therapy-associated symptoms or complications Focused US in tumour- or therapy-associated symptoms or complications is the main task of sonography in patients with lung tumours [9, 74, 75]. Systematic presentation of all the indications for US performance would exceed the dimensions of this chapter. In emergency sonography, vena cava superior syndrome, effusion-caused pericardial tamponade and massive pleural effusion present lung tumour complications that require immediate sonographic diagnosis and therapy. Vena cava superior syndrome presents neck and head swelling and impresses sonographically with dilated echogenic veins and a reduced, missing or reverse flow in the jugular veins (figure 5) [76]. Not infrequently, enlarged collar lymph nodes or mediastinal tumour formation can be detected at initial presentation and biopsied using US guidance for definitive diagnosis and therapy. Using the subcostal left-sided scan, the presentation of a pericardial effusion is possible due to the four chamber view. The https://doi.org/10.1183/2312508X.10006817

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indications and contraindications of massive pleural effusion can be relieved immediately. In addition to radiographic imaging, focused sonography is also helpful for the documentation of therapy response and for symptom-oriented follow-up in patients with lung tumours [9].

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ERS MONOGRAPH | THORACIC ULTRASOUND 58. Maskell NA, Gleeson FV, Davies RJ. Standard pleural biopsy versus CT-guided cutting-needle biopsy for diagnosis of malignant disease in pleural effusion: a randomised controlled trial. Lancet 2003; 361: 1326–1331. 59. Adams RF, Gleeson FV. Percutaneous image-guided cutting-needle biopsy of the pleura in the presence of a suspected malignant effusion. Radiology 2001; 219: 510–514. 60. Görg C, Schwerk WB, Görg K, et al. Pleural effusion: an acoustic window “for sonography of pleural metastases. JCU 1991; 19: 93–97. 61. Görg C. Transcutaneous contrast enhanced sonography of pleural-based pulmonary lesions. Eur J Radiol 2007; 64: 213–221. 62. Qureshi NR, Rahman NM, Gleeson FV. Thoracic ultrasound in the diagnosis of malignant pleural effusion. Thorax 2009; 64: 139–143. 63. Diacon AH, Schuurmans MM, Theron J, et al. Transbronchial needle aspirates: comparison of two preparation methods. Chest 2005; 127: 2015–2018. 64. Caremani M, Benci A, Lapini L, et al. Contrast enhanced ultrasonography (CEUS) in peripheral lung lesions: a study of 60 cases. J Ultrasound 2008; 11: 89–96. 65. Cao BS, Wu JH, Li XL, et al. Sonographically guided transthoracic biopsy of peripheral lung and mediastinal lesions: role of contrast-enhanced sonography. J Ultrasound Med 2011; 30: 1479–1490. 66. Reißig A, Kroegel C. Accuracy of transthoracic sonography in excluding post-interventional pneumothorax and hydro pneumothorax. Comparison to chest radiography. Eur J Radiol 2005; 53: 463–470. 67. Chung MJ, Goo JM, Im JG, et al. Value of high-resolution ultrasound in detecting a pneumothorax. Eur Radiol 2005; 15: 930–935. 68. Sartori S, Tombesi P, Trevisani L, et al. Accuracy of transthoracic sonography in detection of pneumothorax after sonographically guided lung biopsy: prospective comparison with chest radiography. AJR 2007; 188: 37–41. 69. Blank W. Sonographisch gezielte Punktionen und Drainagen. In: Seitz K, Schuler A, Rettenmaier G. (Hrsg) Klinische Sonographie und sonographische Differentialdiagnose. Stuttgart, Thieme, 2008; 1217–1251. 70. Tschammler A, Beer M, Hahn D. Differential diagnosis of lymphadenopathy: power Doppler vs color Doppler sonography. Eur Radiol 2002; 12: 1794–1799. 71. Ahuja ST, Yin M, Huen HJ, et al. “Pseudocystic” appearance of non-Hodgkins lymphomatous nodes: an infrequent finding with high resolution transducers. Clin Radiol 2001; 56: 111–115. 72. Schuler A, Blank W, Braun B. Sonographisch-interventionelle diagnostik bei thymomen. Ultraschall Med 1995; 16: 62. 73. Herth FJF. The mediastinum. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 161–171. 74. Volpicelli G, Elbarbary M, Blaivas M, et al. International evidence based recommendations for point-of-care lung ultrasound. Intensive Care Med 2012; 38: 577–591. 75. Solomon SD, Saldana F. Point-of-care ultrasound in medical education – stop listening and look. N Engl J Med 2014; 370: 1083–1085. 76. Arcasoy SM, Jett JR. Superior pulmonary sulcus tumors and Pancoast’s syndrome. N Engl J Med 1994; 337: 1370– 1376.

Disclosures: None declared.

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| Chapter 10 The diaphragm Giovanni Ferrari1, Søren Helbo Skaarup2, Francesco Panero3 and John M. Wrightson4 This chapter covers US evaluation of diaphragm function, and describes the methods and US techniques used to measure movement and thickening of the diaphragm. Current validated techniques that assess diaphragm function are often invasive or expose the patient to ionising radiation. US is a noninvasive, easily repeatable bedside tool allowing direct visualisation of the muscle. There are a number of applications of DUS, from assessment and emergency medicine to respiratory medicine. DUS has become a useful tool in evaluating diaphragm dysfunction, suggesting its use to predict discontinuation from mechanical ventilation and to evaluate muscle atrophy during mechanical ventilation. It also has an important role in assessing respiratory effort, and in evaluating diaphragm paralysis and the mechanical consequences of pleural effusion. Thus, DUS is a fast, easy procedure that can identify diaphragm dysfunction, monitor muscle activity over time and provide useful information during invasive procedures such as thoracentesis. Cite as: Ferrari G, Helbo Skaarup S, Panero F, et al. The diaphragm. In: Laursen CB, Rahman NM, Volpicelli G, eds. Thoracic Ultrasound (ERS Monograph). Sheffield, European Respiratory Society, 2018; pp. 129–147 [https://doi.org/10.1183/2312508X.10006917].

T

he diaphragm represents the main respiratory muscle but prior to the widespread use of US remained challenging to assess. This is of relevance given that diaphragm dysfunction is frequent in the critically ill, with patients developing a degree of muscular atrophy and weakness secondary to mechanical ventilation [1]. Ventilation-induced diaphragm dysfunction (VIDD) portends complications such as patient–ventilator asynchrony, weaning failure, pneumonia, prolonged intubation and a stay in the intensive care unit (ICU). Therefore, its recognition and grading is of significant importance. DUS has emerged as a valuable tool in such critically ill patients. By evaluating the movement and thickening of the diaphragm, clinically relevant information can be obtained for weaning trials, monitoring of respiratory efforts, investigating diaphragmatic paralysis and defining acute dyspnoea. Within a broader arena, DUS also allows assessment of suspected diaphragmatic paralysis, detection of structural abnormalities and prediction

1 Pulmonary Medicine, Ospedale Mauriziano Umberto I, Torino, Italy. 2Dept of Pulmonary Medicine and Allergy, Aarhus University Hospital, Aarhus, Denmark. 3High Dependency Unit, San Giovanni Bosco Hospital, Torino, Italy. 4Oxford Centre for Respiratory Medicine, Churchill Hospital, Oxford University Hospitals NHS Foundation Trust, Oxford, UK.

Correspondence: Giovanni Ferrari, Pneumologia, Ospedale Mauriziano Umberto I, Largo Turati 62, 10128 Torino, Italy. E-mail: [email protected] Copyright ©ERS 2018. Print ISBN: 978-1-84984-093-4. Online ISBN: 978-1-84984-094-1. Print ISSN: 2312-508X. Online ISSN: 2312-5098.

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of probable pleural malignancy. A number of studies have demonstrated its easy learning, high reproducibility and good correlation with other validated measures. This chapter provides a summary of the pathology affecting the diaphragm and proposes methods for assessing diaphragm function and structure using DUS. We highlight specific examples of DUS use, particularly where there is an evidence base.

DUS assessment in illness Many disorders affect the structure and function of the diaphragm, including those affecting its innervation (central and peripheral nervous system and neuromuscular junction) and the muscular and tendinous diaphragm itself, and other disorders causing mechanical disruption of the diaphragm (including pleural and pulmonary causes) (table 1). Identification and quantification of the effects of these disorders on the diaphragm is of relevance to physicians from a wide range of specialities, including pulmonologists, intensivists, neurologists, spinal physicians, radiologists and surgeons.

Table 1. Disorders that affect the diaphragm and their site of effect Site of effect

Disorder

Neurological: brain and spinal cord

Arnold–Chiari malformation Multiple sclerosis Motor neurone disease Poliomyelitis Quadriplegia Spinal muscular atrophy Stroke Syringomyelia Charcot–Marie–Tooth disease Chronic inflammatory demyelinating polyneuropathy Critical illness polyneuropathy Idiopathic Guillain–Barré syndrome Neuralgic neuropathy Tumour compression Botulism Drugs/organophosphates Lambert–Eaton syndrome Myasthenia gravis Abdominal pathology (including ascites) Acid maltase deficiency Disuse atrophy, ventilator-induced diaphragm dysfunction Eventration Hernia (e.g. Bochdalek, hiatus, Morgagni) Glucocorticoids Lung hyperinflation (COPD/asthma) Lung tumour/other restrictive parenchymal disorder Muscular dystrophies Myositis (infectious, inflammatory, metabolic) Pleural thickening/fluid Tumour invasion

Neurological: phrenic nerve

Neuromuscular junction

Muscle

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Diaphragm functional assessment relied previously on cumbersome fluoroscopic or phrenic nerve stimulation studies, while anatomical assessment relied on cross-sectional imaging. Using US, both functional and structural assessment is possible in a multitude of settings [2–9]. These include: 1) the clinic room for assessment of basal opacity, where DUS enables differentiation of diaphragmatic paralysis, consolidation, subpulmonic effusion, diaphragmatic nodularity/thickening, diaphragmatic hernia and abdominal pathology, 2) the procedural room for assessment of diaphragm position prior to pleural puncture, where diaphragmatic inversion may predict a symptomatic benefit of pleural fluid drainage, 3) the emergency room for assessment of the diaphragm as part of rapid US assessment after trauma and of medical patients with acute dyspnoea, and 4) the ICU for assessment of basal opacities, where assessment of diaphragmatic function ( particularly over time) is of relevance in weaning from mechanical ventilation.

DUS technique The diaphragm is the most important muscle in breathing. Contraction of the diaphragm causes it to move in a craniocaudal direction, thereby increasing intrathoracic volume and decreasing intrathoracic pressure. This results in inspiratory airflow into the lungs. The intercostal and pectoral musculature also contributes to inspiration but to a lesser extent during tidal breathing. Sufficient diaphragmatic function is considered vital [5]. During exhalation, the diaphragm relaxes and, due to elastic recoil of the lungs, the diaphragm is passively drawn cranially to its resting position. In a forced exhalation manoeuvre, the diaphragm is relaxed, and contraction of internal intercostal and abdominal muscles leads to rapid exhalatory airflow. Assessment of both diaphragm excursion and diaphragm thickening may be used as tools for functional assessment. Evaluation of diaphragm excursion M-mode The time motion mode (M-mode) may be used to measure the excursion of the diaphragm. While there is no consensus on how the M-mode should be performed, most authors suggest the use of a curvilinear low-frequency transducer placed in the midclavicular line and angled in a cranial direction (figure 1). The M-mode line is placed at the posterior part of the diaphragm where there is maximal movement and excursion.

On the right side, the liver acts as an acoustic window, and the diaphragm is easily identified as a hyperechoic curved line abutting the liver (figure 2). Left hemidiaphragm imaging is more difficult due to the poor acoustic window of the spleen and the gas content of the stomach. Many studies describing the M-mode technique only assess the right hemidiaphragm [10, 11], while others note a lower success evaluating the left [12]. The probe should be placed in the subcostal area, between the midclavicular and the anterior axillary line, directing the US beam medially, dorsally and cranially [12]. The angle of incidence of the US beam should be perpendicular to the direction of the muscle movement [13]. As the patient inhales, the abdominal wall is pushed forward, potentially displacing the transducer, and https://doi.org/10.1183/2312508X.10006917

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Figure 1. US evaluation of diaphragm movement with a curvilinear transducer in the sagittal plane in the midclavicular line (red line). The transducer is angled cranially and uses the liver as an acoustic window.

this may result in an excursion measurement error [14]. It is therefore important to stabilise the transducer during the examination. B-mode Another method of quantifying diaphragm excursion is to use brightness mode (B-mode) to measure craniocaudal movement during breathing. This method is simple and can be used at both hemidiaphragms [15–17]. A curvilinear low-frequency transducer is placed perpendicularly in a lower intercostal space (ICS) between the mid- and posterior axillary

Figure 2. The right hemidiaphragm is identified as a curved hyperechoic structure posterior to the liver. The M-mode line (white line) is placed to measure maximal excursion (bottom panel).

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line using the liver or spleen as an acoustic window. Other authors have proposed that the craniocaudal movement of the portal vein can also be measured as a surrogate for diaphragm excursion [18]. Other methods New methods to assess diaphragm movement, such as speckle tracking, are under investigation but require further validation [19–21]. The rate of diaphragm excursion has also been studied [22]. Evaluation of diaphragm thickness and thickening

Diaphragm muscular thickness increases during contraction, and US evaluation of this provides further information about diaphragm function. A high-frequency linear transducer (7–12 MHz) is used to visualise the zone of apposition (where the diaphragm abuts the chest wall laterally), located a few centimetres deep [23]. The transducer can be placed across two ribs and then rotated obliquely to fit in the ICS for accurate sonographic identification of the diaphragm. Lower intercostal areas are examined in the anterior axillary line (figure 3). On inspiration, movement of the lung may prevent imaging of the diaphragm; when this occurs, the probe should be moved to a more inferior ICS. During US, the diaphragm appears as a hypoechoic structure superior to the liver or spleen, flanked by two thin hyperechoic lines, which are the diaphragmatic pleura (superficially) and the peritoneum (deeper) (figure 4). The minimal thickness in the resting

Figure 3. US evaluation of diaphragm thickness and thickening during breathing. A high-frequency transducer is placed at the anterior axillary line (red line) identifying the diaphragm at the zone of apposition superficial to the liver or spleen.

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1+ +

Figure 4. The diaphragm identified as a three-layered structure superficial to the liver or spleen. Hyperechoic layers of the diaphragmatic pleura (thoracic side) and the peritoneum (abdominal side) surround the hypoechoic diaphragm. Thickness is measured with the calliper function in maximal inhalation and exhalation (indicated by crosses and a dotted line). “1” indicates the diaphragmatic pleura.

diaphragm is 12–15 mm [24, 25]. Accurate assessment of thickness requires that the US beam is perpendicular to the diaphragm, rather than oblique [26]. An increase in diaphragm thickness during breathing is measured in either B-mode or M-mode using the calliper function in end-expiration (functional residual capacity (FRC)) and end-inspiration during deep breathing (total lung capacity (TLC)). At least three measurements should be recorded to minimise errors. Several derived parameters may be calculated, which relate thickness TLC to thickness at FRC [25, 26]. These include: 1) thickening ratio=tdiTLC/tdiFRC, where tdiTLC is the diaphragm thickness at TLC and tdiFRC is the diaphragm thickness at FRC, and 2) diaphragm thickening fraction (Dtf )=(tdiTLC−tdiFRC)/tdiFRC.

Standardisation and validity of DUS Despite the previously discussed techniques of functional assessment using DUS, a clear consensus on the optimal technique has not been established. Normal values of diaphragm excursion and thickness and thickening fractions have, however, been established with good inter- and intra-observer variation. Both excursion and thickness have also been compared with non-US references, including spirometric measurements of exhaled air volumes. Thickness

Measurement of diaphragm thickness by US demonstrates close correlation with postmortem findings [27]. Normal values of diaphragm thickness were examined by CARRILLO-ESPER et al. [28] in end-expiration in 109 healthy men and women, finding a normal resting diaphragm of 18 mm (men) and 14 mm (women). No relationship was found between thickness and body mass index or thorax circumference [24, 28]. Diaphragm thickness should increase by at least 20% at maximal inspiration, with a minimal side-to-side variation [24]. Thickening during breathing is related to spirometric lung volumes [29]; however, during quiet breathing there is considerable variability, and up 134

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to one-third of healthy people show no increase in thickening during tidal breathing [25]. Intra- and inter-rater agreement is high [30], including during mechanical ventilation (although more so on the right than on the left) [31]. Excursion

Evaluation of excursion during breathing has mostly been undertaken using M-mode in a subcostal midclavicular view. There is a linear relationship between M-mode excursion and exhaled lung volume measured by spirometry [10, 11, 17]. A linear relationship has also been found using other US methods that measure craniocaudal movement of the diaphragm or the portal vein [18]. Movement is correlated to sex and weight [16]. Normal values for men and women have been proposed as 1.0 and 0.9 cm during quiet breathing, 1.8 and 1.6 cm during a sniff manoeuvre, and 4.7 and 3.6 cm during deep breathing [12]. Another study reported similar findings [32]. Examination is feasible and relatively fast, even by inexperienced operators [22]. Reproducibility is high but dependent on operator experience [22, 12]. Due to difficulty with sonographic access, reproducibility is lower for the left hemidiaphragm [17, 12]. When comparing DUS with chest radiography, US can detect poor diaphragm movement even with a normal radiographic diaphragm position, and, conversely, the finding of an elevated hemidiaphragm does not always correspond to decreased movement at US examination [33]. DUS can therefore be seen to provide rapid and reproducible information about diaphragm function that cannot be obtained as easily and safely by other diagnostic modalities. Despite the lack of consensus-based standardised methodology, it seems likely that DUS is set to become the primary tool for evaluation of diaphragm function.

Monitoring diaphragm thickness during mechanical ventilation Mechanical ventilation is a lifesaving procedure, but prolonged mechanical ventilation (PMV) is associated with severe complications, such as tracheal injury, infection and ventilator-associated pneumonia. Moreover, PMV promotes diaphragm atrophy and contractile dysfunction [34], termed VIDD [35]. Although many patients on mechanical ventilation can be weaned early, difficulties in weaning are encountered in ∼30% of patients, with >40% of the time spent in the ICU being spent weaning from mechanical ventilation [36]. During mechanical ventilation, the ventilator provides part or all of the work of breathing for the patient, according to the ventilator modality employed. Several studies have shown that, during controlled mechanical ventilation (CMV), diaphragm atrophy has a rapid onset, while other muscles show no atrophy [37, 38]. DUS is a promising method to evaluate the diaphragm during mechanical ventilation. Experimental data suggest that a reduction in diaphragm thickness over time can indicate atrophy of the muscle itself. An early assessment of diaphragm dysfunction prior to extubation may be important to avoid the risk of extubation failure [39]. Assuming that mechanical ventilation has an unloading effect on respiratory muscles that leads to diaphragm atrophy and dysfunction, GROSU et al. [40] measured muscle thickness https://doi.org/10.1183/2312508X.10006917

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in seven intubated patients from the first day of intubation until extubation, tracheostomy or death. They found a daily average of 6% decrease in diaphragm thickness and that thinning of the diaphragm occurred within 48 h of intubation. SCHEPENS et al. [41] studied right hemidiaphragm thickness in 53 patients ventilated for at least 72 h. The mean baseline value was 1.9 cm; compared with baseline, diaphragm thickness decreased >10% in 77% of the patients studied, remained stable in 19% and increased in 4%. The daily rate of thickness reduction was 10.9%. The main variable associated with diaphragm thinning was length of ventilation, while disease severity (assessed by the Simplified Acute Physiology Score II), steroid use, muscle relaxants or sepsis on admission were not associated with a decrease in thickness. In a small study of eight patients receiving either pressure support ventilation (PSV) or assist-control ventilation (ACV), a decline in diaphragm thickness was observed only in patients receiving ACV, while subjects receiving PSV showed an increase in thickness [42]. Similarly, EL-MORSY et al. [43] studied diaphragm thickness in 67 mechanically ventilated patients, stratified by ventilatory modalities (CMV, ACV and spontaneous ventilation). CMV and ACV were associated with significantly higher rates of diaphragmatic atrophy than spontaneous modes. A daily decrease in thickness was observed in patients treated with CMV and ACV, while in spontaneous modalities a daily increase in thickness was observed [43]. ZAMBON et al. [44] measured daily atrophy rates in critically ill mechanically ventilated patients, categorising the subjects into four classes: 1) spontaneous breathing or continuous positive airway pressure, 2) PSV of 5–12 cmH2O (low PSV), 3) PSV of >12 cmH2O (high PSV) and 4) CMV. The authors reported, for the first time, that the degree of diaphragm atrophy was associated with different ventilation settings and observed a linear relationship between ventilation support and Dtf. GOLIGHER et al. [45] described the evolution of diaphragm thickness over time in patients during mechanical ventilation. A total of 128 mechanically ventilated patients and 10 control patients were enrolled. Thickness and Dtf were measured daily. Diaphragm thickness remained unchanged in 47 subjects (44%), decreased by >10% in 47 subjects (44%) and increased by >10% in 13 subjects (12%). Changes in thickness occurred early. Thickness was stable over time in nonventilated control subjects and in patients following extubation [45]. To evaluate the impact of mechanical ventilation on the diaphragm, a recent study by GOLIGHER et al. [46] evaluated whether ventilator-induced changes in diaphragm thickness were associated with clinical outcomes, such as days of ventilation, re-intubation, tracheostomy or death. Both increases and decreases in diaphragm thickness and Dtf were assessed. The risk of PMV was increased with either a decrease or an increase in diaphragm thickness compared with baseline values [46]. Such findings suggest that atrophy is associated with PMV and also that insufficient muscle unloading (suggested by an increase in thickness) may be associated with diaphragmatic injury. The authors hypothesised that an intermediate Dtf could be associated with the shortest duration of ventilation. In a post-hoc analysis, the length of ventilation was lower in patients with an intermediate Dtf (mean value of 15–30%) over the first 3 days of ventilation. ICU length of stay and complications were lower in this group. Patients with Dtf values similar to normal subjects (i.e. 15–30%) during the first 3 days of ventilation had a shorter duration of 136

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mechanical ventilation, while subjects with lower or higher values of Dtf had a longer duration of mechanical ventilation and a higher risk of ventilation [46]. In conclusion, the findings of these studies suggest that changes in diaphragm thickness are common in mechanically ventilated patients, occur early and may be modulated by the intensity of respiratory muscle work performed by the patient [45]. The degree of atrophy may be associated with the duration of mechanical ventilation and not with other risk factors for muscle atrophy, such as sepsis.

Weaning from mechanical ventilation Diaphragm dysfunction is frequent in critically ill patients either as a result of VIDD or due to direct effects of cardiac or abdominal surgery [47]. An early assessment of diaphragm dysfunction prior to weaning should be considered to avoid the risk of extubation failure. Previously, bedside assessment of diaphragm dysfunction was challenging, and the gold standard of measurement of transdiaphragmatic pressure (PTD) was usually limited to research studies [48]. The role of DUS in predicting weaning success has been investigated by studies measuring either excursion [39, 49, 50] or thickness and Dtf [50–52]. Both diaphragm excursion and Dtf measurements performed during a spontaneous breathing trial (SBT) in intubated/ tracheotomised patients have shown utility in predicting weaning success. JIANG et al. [49] assessed diaphragm excursion in mechanically ventilated patients by evaluating displacement of the liver or spleen. A threshold of 1.1 cm had a better performance in predicting weaning success compared with traditional parameters (maximal inspiratory pressure (MIP), rapid shallow breathing index (RSBI) and expiratory tidal volume) with a sensitivity and specificity of 84% and 83%, respectively, a positive predictive value (PPV) of 82%, a negative predictive value (NPV) of 86% and an accuracy of 84%. KIM et al. [39] evaluated diaphragm dysfunction in 82 patients during a SBT by assessing vertical excursion or paradoxical movements of the diaphragm. A cut-off value of 1.0 cm was found, and patients with diaphragm dysfunction according to this criterion had longer weaning times and a higher frequency of re-intubation [39]. In a recent study, FARGHALY and HASAN [50] observed that a threshold value of diaphragmatic excursion of ⩾10.5 mm was associated with successful extubation with a sensitivity and specificity of 87% and 71%, respectively. Another recent study by SPADARO et al. [53] compared the role of a new index, the diaphragmatic-RSBI (D-RSBI), as opposed to RSBI, to predict weaning failure. Diaphragm displacement and D-RSBI performed better than traditional RSBI at predicting weaning outcome, and D-RSBI had the best diagnostic accuracy with a cut-off value of >1.3 breaths min−1 mm−1, giving a sensitivity of 94%, specificity of 65%, PPV of 57% and NPV of 96%. Excursion as a weaning index should be assessed only during a SBT and not in patients receiving mechanical ventilation (which would give a false assessment of contractile activity). Moreover, variables such as abdominal or thoracic compliance, tidal volume, rib https://doi.org/10.1183/2312508X.10006917

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cage or abdominal muscle activity, and the presence of ascites may affect diaphragm motion and excursion assessment. Several studies have evaluated the role of Dtf in predicting extubation success. DININO et al. [51] studied 63 patients weaned either by a SBT (27 patients) or a pressure support trial (36 patients). A Dtf cut-off value of 30% was associated with a PPV of 91% and NPV of 63% for successful extubation with a sensitivity and specificity of 88% and 71%, respectively. FERRARI et al. [52] evaluated Dtf in 46 tracheotomised patients during a SBT. A threshold Dtf of >36% was associated with a successful SBT with a sensitivity of 82%, specificity of 88%, PPV of 92% and NPV of 75%. Moreover, a significant difference between diaphragm thickness at TLC and residual volume was observed between patients who succeeded and those who failed the SBT. Finally, FARGHALY and HASAN [50] assessed Dtf percentage in 54 patients with a cut-of value of 34.2%, giving a sensitivity and specificity of 90% and 64%, respectively. In these three studies, the assessment of Dtf performed similarly to other weaning indexes, such as RBSI or MIP measurement. Thus, according to these preliminary studies, the optimal threshold values for predicting weaning success are 1 cm for diaphragm excursion and 30–36% for Dtf. DUS provides important information for the weaning process. In particular, Dtf performs comparably to other weaning indexes, such as RSBI or MIP. Further randomised controlled studies are warranted to validate the role of DUS in the weaning process.

Respiratory effort monitoring Validated methods of assessment of diaphragmatic function rely on direct measurement of patient-generated pressures: maximum inspiratory/expiratory pressure, airway pressure decrease at 100 ms after onset of inspiration (P0.1) and oesophageal pressure (Poes). PTD, calculated as the difference between Poes and gastric pressure (Pga), obtained from double-balloon catheters, together with twitch magnetic phrenic nerve stimulation, represent the gold standards [54]. Nevertheless, all of these suffer from limitations: they all need a discrete grade of collaboration from the patient, while the latter two are both invasive and potentially distressing [48]. DUS has been studied as a proxy of respiratory effort and work of breathing in healthy volunteers [17, 55] and in people suffering from neuromuscular diseases [56, 57]. DUS offers many advantages over other measures, being a noninvasive, repeatable bedside technique allowing direct visualisation of the diaphragm and discrimination of the dysfunctional side. Few studies have compared DUS with other methods in mechanically ventilated patients in terms of either movement of one hemidiaphragm or thickness change [31, 58–60]. LEROLLE et al. [59] compared the best diaphragmatic excursion on maximal inspiratory effort from FRC with both PTD and the derived Gilbert index (GI). GI evaluates the contribution of the diaphragm to respiratory pressure swing during quiet tidal breathing: a GI value of >0.30 is normal, while a GI value of ⩽0 indicates severe diaphragmatic dysfunction [61]. The authors evaluated a cohort of 28 post-cardiac surgery patients requiring prolonged invasive mechanical ventilation, who were then at risk of diaphragmatic dysfunction [59]. All but one patient exhibited an abnormal PTD. The best diaphragmatic excursion and GI value correlated significantly (Spearman’s ρ=0.64; 138

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p=0.001), with lower values of excursion among those with severe muscle dysfunction (GI >0 versus GI ⩽0, 30 versus 19 mm; p=0.007). Discrimination capability (assessed with a receiver operating characteristic curve) for the best diaphragmatic excursion with respect to a severe impairment (GI ⩽0) was 93%, with an optimal cut-off point of 25 mm, showing a sensitivity and specificity of 100% and 85%, respectively. When applied to a different cohort of patients with an uncomplicated post-operative course, none of them showed a best diaphragmatic excursion of 48 h of invasive ventilation. They compared the Dtf of the right hemidiaphragm with both PTD and the transdiaphragmatic pressure–time product (PTPdi, an estimate of the work of breathing) at four different levels of pressure support (0, 5, 10 and 15 cmH2O, positive end-expiratory pressure of 5 cmH2O for all) during tidal ventilation. Dtf was calculated as the fractional thickening of the muscle at the apposition zone between end-inspiration and end-expiration. With increasing levels of pressure support ( progressive muscular unloading), PTPdi and Dtf decreased similarly. Dtf was higher for spontaneously breathing patients (i.e. maximum workload) and lowest for the highest pressure support (i.e. minimum burden) (47.4% versus 16.3%; p