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      Lung Ultrasound for Treatment of Patients With COVID‐19 : Please Report Your Settings and Mechanical Index

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          Abstract

          Abbreviations COVID‐19 coronavirus disease 2019 LUS lung ultrasound US ultrasound One of the most concerning characteristics of the severe acute respiratory syndrome coronavirus 2 pandemic is its fast contagion rate: the number of total confirmed cases grows approximately exponentially in many countries. 1 In this rapidly evolving scenario, clear and unambiguous information on patient treatment strategies must be exchanged efficiently. This is particularly important regarding the use of valuable resources for diagnosis and evaluation of disease progression. A bulk of recent literature is showing the usefulness of ultrasound (US) imaging for the assessment of lung interstitial diseases in general. 2 This is even more true of point‐of‐care US in the context of the coronavirus disease 2019 (COVID‐19) pandemic. 3 In this context, lung ultrasound (LUS) is gaining momentum as a highly valuable and practical resource in the evaluation of COVID‐19 pneumonia and acute respiratory distress syndrome. In addition to the well‐known advantages of US imaging compared to other imaging modalities (use of nonionizing radiation, lower equipment cost, portability, real‐time imaging, and relatively easy disinfection of the equipment), LUS allows imaging of patients at the bedside, reducing complications from patient movement and the risk of staff exposure. 4 Various studies have suggested that LUS has superior performance to chest radiography to detect pneumonia. 5 , 6 The advantage of LUS may become more relevant in health systems with limited resources, such as those in low‐ and middle‐income countries. Lung US differs from US imaging of other tissues in that there is not a one‐to‐one relationship between the appearance of lung parenchyma in the image and its structure. As a consequence of the high air content and low density of the lung, sound does not propagate in the parenchyma as it does in soft tissues. In particular, in the healthy lung, the presence of air‐filled alveoli leads to multiple US scattering, which prevents conventional B‐mode imaging but could be exploited for the assessment of interstitial diseases, as shown by Mohanty et al 7 As a result, LUS is mostly based on the detection and evaluation of artifacts that arise when the assumptions of the image formation process in the scanner (small variations in sound speed and single scattering) are not met. 8 Among the artifacts suggested to have relevance for the evaluation of COVID‐19 pneumonia and acute respiratory distress syndrome are vertical brightness strikes that extend axially from the pleural line. 9 The physical nature of B‐lines is not yet well understood. One of the current working hypotheses is that these artifacts represent propagation within zones of tissue with reduced aeration that trap sound. Demi et al 10 recently showed evidence of this hypothesis by recreating these artifacts in tissue‐mimicking phantoms with bubbles to mimic air‐filled alveoli. Moreover, similar results have been also shown in clinical data. 11 Crucially, these phenomena are highly dependent on the US frequency. This suggests that LUS findings should be interpreted by considering the scanning frequency and related settings (focal depth and use of filters). In addition, other LUS features, such as the appearance of the pleural line, bronchograms, and consolidations, vary with the frequency (a higher frequency provides finer detail). Another critical issue to consider while performing LUS examinations is the increased risk of inducing tissue damage associated with cavitation. Air pockets in lung tissue can oscillate with the pressure changes of the oscillating acoustic pulse and enter cavitation. Although no complications have been reported in humans under clinical settings, studies in animal models show evidence of pulmonary capillary hemorrhage at diagnostic frequencies. 12 The likelihood of these effects increases with the acoustic output and scanning time. Thus, clinicians should closely monitor the mechanical index, which is associated with acoustic energy exposure and the likelihood of inducing cavitation. On the basis of this evidence, we strongly advocate for authors of clinical studies and case reports to provide detailed information on the scanning settings, especially the scanning frequency and the mechanical index. As medical organizations and groups advance toward standardizing the use of LUS in the severe acute respiratory syndrome coronavirus 2 setting, 13 the inclusion of detailed information on the system settings, acoustic exposure, as well of anatomic views will help clinicians understand the reported findings and how they relate to the progression of the disease. This standardization in the reporting effort will contribute to making LUS more reproducible, thus facilitating its adoption worldwide. In this context, clinicians must abide by the as‐low‐as‐reasonably‐achievable principle, 14 exposing the patient to the minimum acoustic energy without compromising valuable information.

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          Proposal for International Standardization of the Use of Lung Ultrasound for Patients With COVID ‐19

          Growing evidence is showing the usefulness of lung ultrasound in patients with the 2019 new coronavirus disease (COVID‐19). Severe acute respiratory syndrome coronavirus 2 has now spread in almost every country in the world. In this study, we share our experience and propose a standardized approach to optimize the use of lung ultrasound in patients with COVID‐19. We focus on equipment, procedure, classification, and data sharing.
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            Is There a Role for Lung Ultrasound During the COVID ‐19 Pandemic?

            Lung ultrasound (LUS) has evolved considerably over the last years with respect to its theoretical and operative aspects. Consequently, its clinical application has come to be sufficiently known and widespread. One of the characteristic aspects of LUS is the ability to define the alterations affecting the ratio between tissue and air in the superficial lung.1 Normally, the lung surface mainly consists of air. Incident ultrasound (US) waves are thus generally completely back‐reflected by the visceral pleural plane, especially when healthy. In this context, the scattering of US waves produces artifactual images characterized by horizontal reverberations of the pleural line (A‐lines) and mirror effects. When the ratio between air, tissue, fluid, or other biological components is reduced, the lung no longer presents itself as an almost complete specular reflector. Hence, various types of localized vertical artifacts appear on the US images in relation to the alterations of the subpleural tissue.2, 3 These artifacts have generally been called B‐lines,4 but recently it has become clear that B‐lines are very heterogeneous in their appearance. Moreover, their heterogeneity may be exploited as a means to characterize the alterations of the lung surface.5 Another well‐known phenomenon linked to the increase in subpleural lung density (in the absence of consolidated tissue) is the coalescence of many vertical artifacts in more extended echogenic patterns, in which the individual artifacts are still recognizable or fused in a single homogeneous subpleural echogenic area (white lung). When the subpleural density goes toward the value of 1 g/mL (about that of the solid tissue), then consolidations appear. Therefore, the clinician, through the visual inspection of LUS images, can detect, at the subpleural level, nonconsolidative increases in the ratio between full (tissue) and empty (air) and assess them in a range between normal and consolidative. Topographic images of the lesions can also be acquired. Finally, the extent of these lesions on the lung surface, as well as their evolution or regression over time, can also be evaluated. The study of these patterns shows very high sensitivity in cases of interstitial and alveolar‐interstitial lung diseases, which have a peripheral distribution. Numerous studies on acute respiratory distress syndrome (ARDS)6 confirm this. Other studies related to the 2009 pandemic influenza A (H1N1) epidemic7 confirm these hypotheses even in a virally infectious setting. The recent pneumonia outbreak spreading from Wuhan, China, in December 2019 is caused by the 2019 novel coronavirus infection, defined as new coronavirus disease (COVID‐19).8 This epidemic currently involves many areas of the world, with particular incidence in Italy, representing a serious challenge to public health and the efficiency of the health care structures. The histopathologic appearance of initial COVID‐19 pneumonia is characterized by alveolar damage, which includes alveolar edema, while the inflammatory component is patchy and mild. Reparative processes with pneumocyte hyperplasia and interstitial thickening can occur. The advanced phases show gravitational consolidations similar to those of ARDS. There are hemorrhagic necrosis, alveolar congestion, edema, flaking, and fibrosis.9 An analysis of the available computed tomographic (CT) data from patients with COVID‐19 pneumonia10 shows largely bilateral lesions that are patchy and also confluent, appearing as ground glass or with a mixed consolidative and ground glass pattern. Ten percent of lesions with a crazy‐paving appearance are reported. The lesions often have a wedge‐like appearance with a pleural base. Major consolidations may show air bronchograms. Pleural effusion is absent. Patchy or confluent lesions tend to be distributed along the pleura. The lobe most frequently affected is the lower right lobe, followed by the upper and lower left lobes. The posterior lung is involved in 67% of cases.11 Given that LUS can identify changes in the physical state of superficial lung tissue, which correlate with histopathologic findings and can be identified on CT but remain hidden in a large percentage of chest radiographs, the role of LUS can be relevant in the context of the COVID‐19 epidemic. It should also not be underestimated that, in experimental models of ARDS, LUS has proved capable of detecting lung lesions before the development of hypoxemia. The current clinical evidence (although not yet represented in the literature), the theoretical bases of LUS in the aerated lung, and LUS findings of similar aspects in other diseases (ARDS and flu virus pneumonia) strongly suggest the potential diagnostic accuracy of LUS, which may be useful in the following situations: Triage (pneumonia/non‐pneumonia) of symptomatic patients at home as well as in the prehospital phase. Diagnostic suspicion and awareness in the emergency department setting. Prognostic stratification and monitoring of patients with pneumonia on the basis of the extension of specific patterns and their evolution toward the consolidation phase in the emergency department setting. Treatment of intensive care unit patients with regard to ventilation and weaning. Monitoring the effect of therapeutic measures (antiviral or others). Reducing the number of health care professionals exposed during patient stratification (a single clinician would be necessary to perform an objective medical examination and imaging investigation directly at the patient’s bed). From the current clinical evidence, we consider the LUS patterns of patients with COVID‐19 pneumonia quite characteristic. The first pulmonary manifestations are represented by a patchy distribution of interstitial artifactual signs (single and/or confluent vertical artifacts and small white lung regions). Subsequently, these patterns extend to multiple areas of the lung surface. The further evolution is represented by the appearance, still patchy, of small subpleural consolidations with associated areas of white lung. The evolution in consolidations, especially in a gravitational position, with or without air bronchograms, and their increasing extension along the lung surface indicate the evolution toward the phase of respiratory insufficiency that requires invasive ventilatory support. Figures 1 and 2 show the US characteristics of the interstitial syndrome present in intermediate COVID‐19 pneumonia. Early viral pneumonia shows few, usually bilateral, pulmonary lung areas characterized by single or bundled, pneumogenic‐type vertical artifacts, or small areas of white lung. Advanced COVID‐19 pneumonia shows evident consolidations, especially in the posterobasal regions, and widespread patchy artifactual changes. This pattern is similar to that of ARDS. In this context, the development of algorithms able to aid the clinician with a real‐time detection and localization system is of great interest.12 Figure 1 Top, Two images from a patient confirmed with COVID‐19 pneumonia. Typical vertical pneumogenic large artifacts originate from the pleural line or from small, blurred subpleural consolidations. Their origin is not point‐like. Bottom, The pleural line is interrupted by more visible yet small consolidations. Large vertical artifacts are seen arising from the consolidations, and they are superimposed on areas of white lung (convex transducer, intercostal scans). Figure 2 Similar findings from a second patient confirmed with COVID‐19 pneumonia. Studies aimed at clarifying the diagnostic and prognostic role of LUS in COVID‐19 are urgently needed. The well‐known advantages of LUS in terms of portability, bedside evaluations, safety, and the possibility of repeating the examination during follow‐up cannot be overlooked and should be exploited and implemented. Moreover, the possibility of performing a LUS examination at the bedside minimizes the need for transferring the patient, with a potential risk of further infection spreading among health care personnel. Comparison with chest radiography and/or a lung CT scan might help in designing a proper diagnostic workup according to the general and local technological and human resources. A suggested acquisition protocol is described below: Use convex or linear transducers. The latter are preferable to study the detail of the pleural and subpleural alterations. Use a single–focal point modality (no multifocusing), and set the focal point on the pleural line. Preferably, scans need to be intercostal (not orthogonal to the ribs) to cover the widest surface possible with a single scan. Evaluate the presence of the artifactual patterns in multiple areas and bilaterally to study the extent of the lung surface affected. Ideally, 16 areas in total should be evaluated: anterior midclavicular (apical, medial, and basal), right and left; posterior paraspinal (apical, medial, and basal), right and left; and lateral axillary (apical and basal), medial right and left.
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              COVID-19 outbreak: less stethoscope, more ultrasound

              In their Correspondence in The Lancet Respiratory Medicine, Jonathan Cheung and colleagues stressed the need to ensure staff safety in the airway management of patients with 2019 novel coronavirus disease (COVID-19). 1 This safety should be guaranteed from the patient's first assessment. In fact, maintaining the safety of the doctor, who meets many people during his daily activity, avoids the spread of the disease to other patients and the possible creation of new epidemic outbreaks. However, patients with fever and respiratory symptoms do still need to be seen. The standard method involves doing an objective examination and carrying out any radiological tests, such as chest radiography or chest CT. This means the use of tools such as a stethoscope and radiological devices, with the possibility of contamination of the medical devices and nosocomial spreading of the virus; eventually, this can cause the contagion of health-care workers (from doctor to nurse to radiology technicians) and already hospitalised patients who have a higher risk of developing severe COVID-19. During such a diffusive outbreak there is still the need to guarantee both the patients' rights to be evaluated according to the highest standards of care and, at the same time, the health-care workers' safety. Therefore, it is important that the minimum number of health-care workers and medical devices be exposed to suspected or confirmed cases of COVID-19. In this regard, in 2016, Copetti highlighted how lung ultrasound could have several advantages compared with the use of the stethoscope, to the extent that it could be replaced. 2 His famous article entitled “Is lung ultrasound the stethoscope of the new millennium? Definitely yes” was visionary in 2016 and now, in this historical period, very pertinent. In our opinion, the use of ultrasound is now essential in the safe management of the COVID-19 outbreaks, since it can allow the concomitant execution of clinical examination and lung imaging at the bedside by the same doctor. In order to minimise the use of medical devices and health-care professionals, we introduced a specific procedure for the evaluation of children with suspected COVID-19, based on the use of lung ultrasound by one paediatrician and another assistant, wearing the standard personal protections as per WHO indications. 3 The paediatrician prepares the ultrasound pocket device, which comprises a wireless probe and a tablet. The probe and tablet are placed in two separate single-use plastic covers (figure ). No other medical devices are used. When the two operators enter the isolation room, the paediatrician uses the probe and does the lung ultrasound, the assistant holds the tablet and freezes and stores the images, touching neither the patient nor the surrounding materials. The stethoscope is not used because it is more difficult to have specific covers and there is a higher probability to mistakenly touch either the ocular or oral mucosa with it. Lung auscultation is therefore substituted by lung visualisation with the ultrasound. After the procedure, in a dedicated area, the operators easily remove the probe and tablet from the covers, simply letting them slip onto clean towels, where the devices are further sterilised. Figure The ultrasound pocket device © 2020 Davide Pata 2020 Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active. During a COVID-19 outbreak, it is important to minimise the health care–patient interactions to only the necessary procedures. There are several studies showing the accuracy of lung ultrasound in detecting lung pathologies, from bacterial and viral pneumonia to acute respiratory distress syndrome 4 and its non-inferiority to chest x-ray and clinical examination.2, 4 Therefore, we believe that such a procedure could reduce health-care workers' risk of exposure and also patient movement from the consultation room to the radiology room. Considering the contagiousness of the virus and the need to reduce nosocomial outbreaks, we strongly suggest promotion of lung ultrasound in this setting.
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                Author and article information

                Contributors
                libertario.demi@unitn.it
                Journal
                J Ultrasound Med
                J Ultrasound Med
                10.1002/(ISSN)1550-9613
                JUM
                Journal of Ultrasound in Medicine
                John Wiley & Sons, Inc. (Hoboken, USA )
                0278-4297
                1550-9613
                21 July 2020
                : 10.1002/jum.15389
                Affiliations
                [ 1 ] Instituto de Física Universidad Nacional Autónoma de México Mexico City Mexico
                [ 2 ] Pulmonary Medicine Unit, Department of Medical and Surgical Sciences Fondazione Policlinico Universitario Agostino Gemelli, Istituto di Ricovero e Cura a Carattere Scientifico Rome Italy
                [ 3 ] Diagnostic and Interventional Ultrasound Unit Valle del Serchio General Hospital Lucca Italy
                [ 4 ] Department of Mechanical and Aerospace Engineering North Carolina State University Raleigh North Carolina USA
                [ 5 ] Department of Information Engineering and Computer Science University of Trento Trento Italy
                Author notes
                [*] [* ] Address correspondence to Libertario Demi, PhD, Department of Information Engineering and Computer Science, University of Trento, via Sommarive 9, 38123 Povo, Trento, Italy.

                E‐mail: libertario.demi@ 123456unitn.it

                Author information
                https://orcid.org/0000-0003-0637-7282
                https://orcid.org/0000-0003-2843-9966
                https://orcid.org/0000-0002-0635-2133
                Article
                JUM15389
                10.1002/jum.15389
                7405175
                32691856
                4a79f592-a643-464e-85bf-668e640327dc
                © 2020 American Institute of Ultrasound in Medicine

                This article is being made freely available through PubMed Central as part of the COVID-19 public health emergency response. It can be used for unrestricted research re-use and analysis in any form or by any means with acknowledgement of the original source, for the duration of the public health emergency.

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                : 03 May 2020
                : 06 May 2020
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