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      Essential notes: The use of Lung Ultrasound for COVID-19 in the intensive care unit

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          Abstract

          A Introduction Thoracic imaging is a key component of managing respiratory failure in patients with COVID-19. Timely access to routine chest X-rays (CXR) and computed tomography (CT) scans can however be challenging in a pandemic. Furthermore, resource utilisation is critical, and the safety of the patient and staff must be balanced carefully with the necessity of obtaining images. Point-of-care lung ultrasound (LUS) is a dynamic technique routinely used in intensive care to answer targeted questions and aid in practical procedures. 1 Whilst LUS has its limitations, and in isolation cannot provide a definitive diagnosis, it can be useful where resources are scarce. In this article we explore the use of LUS specifically in critically ill patients with COVID -19, outlining both essential aspects for new practitioners of LUS and points of high diagnostic yield. A Safety When using any imaging technology in the face of an infectious disease the equipment itself must not be allowed to become a vector for further spread. Ideally a dedicated ultrasound machine is required for the “red zone”, as was the case during the Ebola virus outbreak in 2014. 2 , 3 Basic principles of hygiene to minimise contamination include: the removal of organic debris from the probe and machine; disinfection with probe-compatible material; the use of sachets rather than bottled ultrasound gel; and clear documentation of the cleaning process. 4 Portable handheld machines are preferable, being easier both to cover during scanning and to clean. A Suggested approach There is currently no validated systematic approach for performing LUS in patients with COVID-19 pneumonitis, although the Intensive Care Society has made some recommendations. 5 There are several different techniques and choices of probe, including the Blue protocol. 6 The optimal approach where resources are limited must balance the following: • The need to answering the clinical question; • The workload in ICU; • The risks of disturbing the patient’s position, particularly when there is cardiovascular instability. LUS protocols for ICU assume users have a degree of expertise, time and appropriate resources. During a pandemic, providers may find themselves in temporary hospital structures with large numbers of critically ill patients. Protocols designed for normal working conditions may not address the context of a strained and overwhelmed system. We believe the following key points determine the highest yield approach to LUS in patients with COVID-19: • The changes seen are not homogenous, with normal areas interspaced between areas of abnormality (in contrast to bilateral, homogenous changes seen with cardiogenic pulmonary oedema). • Abnormal lung findings predominate in the posterolateral aspect of the chest. • Evaluating the heart accurately distinguishes symptoms as primarily pulmonary or cardiac in nature. 1 • The images obtained should ideally be reproducible, to allow comparison throughout progression of the disease within and between individual patients. We therefore recommend the following approach for those new to thoracic ultrasound. • Begin with a “survey” of the lungs in general using a probe that offers a wide field of view and maximises tissue penetration. The curvilinear (abdominal) probe allows a rapid survey of the lung fields but shadowing from the ribs can obscure much of the image. The cardiac probe provides superior views between ribs, and evaluation of cardiac function, but the narrower field of view prolongs the duration of the scan. Either is suitable, with the aim being to gain a rapid sense of the extent of disease. • Start at the lung bases as posteriorly as possible, accounting for the patient’s position and severity of illness. This allows identification of a dependent pleural effusion, and any involvement of the lower lung zones. • Then move systematically to the apex anteriorly, looking for any abnormalities at the pleural interface suggestive of a large pneumothorax, and reviewing as much of each lung as possible as you scan to gauge the extent of lung involvement. If any abnormalities are detected the higher resolution linear probe (8-12 MHz) should be used to examine these areas in more detail for characteristic findings. • Ultrasound cannot penetrate aerated lung, thus any pathology such as a hilar mass or an isolated central lung mass not in contact with the pleural surface can be missed. CT imaging of patients with COVID-19 pneumonitis suggests however that there is frequent pleural involvement. 7 This reduces the risk of missing lung involvement with LUS. Using this systematic approach should maximise the chances of detecting pleural abnormalities, whilst recognising limitations caused by the position of the patient or inexperience of the practitioner. B Appearance on Imaging LUS does not rely primarily on visualising actual pathology but instead uses artefacts generated by density changes at air/water or air/tissue interfaces. 8 Terminology and definitions are important. B-line patterns are frequently referred to in patients with COVID-19. By definition B-lines must arise from the pleura and erase A-lines. 9 In COVID-19 the vertical lines often originate however from subpleural consolidations and not from the pleura itself. Whilst similar, these are not strictly B-lines but instead C-lines, which are defined as originating below the pleura from consolidations or defects on the pleural surface 9 (Figure 1 ; Supplementary Videos 1 and 2). The ‘light-beam artefact’ that has also been described may be a confluence of C lines leading to a different appearance than that seen in pulmonary oedema or bacterial pneumonia. 10 The key difference between C-lines and B-lines is that C-lines are artefacts caused by viral-induced irregularities of the pleural surface and not caused by alveolar oedema, which gives rise to B-lines. This is similar to the ring-down pattern in tuberculosis, which affects the pleural interface causing defects and artefacts that arise from the pleura itself (Figure 2 ; Supplementary Videos 3 and 4). 11 However, the clinical implications of the differences between B-lines and alveolar oedema, and between C-lines and pleural-based defects, are still unclear with regard to diagnosis and treatment. True B-lines potentially suggest iatrogenic fluid overload or other pathology secondary to the viral pneumonitis. Where serial LUS shows improvement in the C-line pattern with increasing B-lines at the lung bases, this might suggest a need for treatment with diuretics in a patient whose cardiac function is decompensating. Figure 1 Both images are taken with the same ultrasound machine using phased array probe with similar settings. Probe in both cases is positioned in the mid axillary line at the base of the lung in the lower lung zone just above the diaphragm. Figure 1A is from a patient with known COVID-19 pulmonary disease. Ring-down artefacts are seen as C-lines (solid arrow) originating from a thickened pleura (thin arrow) and do not erase the underlying A-lines (hollow arrow). Figure 1B demonstrates true B-lines (hollow arrow) in a patient with pulmonary oedema originating from a thin pleural line (thin arrow) and erasing the A-lines below which are absent in the image. (Videos 1 and 2 in the supplemental material demonstrate differences dynamically) Figure 1 Figure 2 This figure demonstrates the similarity between the subpleural findings in COVID-19 and pulmonary tuberculosis. Figure 2A shows a linear probe positioned at the lung base in the midaxillary line and demonstrates pleural based abnormalities (hollow arrow) in a COVID-19 patient just below the pleura (thin arrow). Figure 2B is taken from a linear probe positioned at the lung apex in the midclavicular line and demonstrates similar findings of subpleural consolidations (hollow arrow) in a patient with tuberculosis. Note subpleural consolidations in both and dense ring-down artefacts originating below the pleura (Videos 3 and 4 in the supplemental material). Figure 2 Supplementary video related to this article can be found at https://doi.org/10.1016/j.bjae.2020.09.001 The following is/are the supplementary data related to this article: 1 2 3 4 B LUS and management strategies Work continues to identify the similarities and differences of pathological changes in COVID-19 pneumonitis compared to acute respiratory distress syndrome (ARDS). Gattinoni and colleagues recently proposed that patients with COVID-19 are classified into L and H phenotypes and speculated that different LUS patterns in each may help identify the severity of disease and facilitate management. 12 It is likely however that there is vast spectrum of presentations between the two phenotypes. 13 Therefore the strategy for artificial ventilation should not be based on LUS findings. Regular scanning combined with monitoring other clinical variables may allow clinicians to track disease progression; for instance, LUS may reveal changes in type and number of B-lines and pleural irregularities. Pleural effusion, lung consolidation, air bronchograms and hepatisation of the lung may be visible in advanced disease or can be associated with superimposed bacterial infections. Other lung pathologies such as pneumothorax and endobronchial intubation during prone positioning may also be identified by LUS. Both pathologies will abolish lung sliding, although in endobronchial intubation a lung pulse will remain. Pulmonary embolism (PE) is a frequent complication in COVID-19; LUS in conjunction with laboratory and clinical information can help in detection of PE. 14 , 15 However, the diagnostic accuracy of LUS in PE is poor, and echocardiography is not recommended in patients at low risk who are haemodynamically stable. Features suggestive of an acute PE include acute right ventricular dysfunction (McConnell’s sign, impaired tricuspid annulus plane systolic excursion [TAPSE], dilated right ventricle, distended inferior vena cava with no respiratory variation and flow reversal in the hepatic vasculature). Infrequently, thrombus may be seen in the right ventricle and main pulmonary artery. 15 As the majority of PEs originate from a deep venous thrombosis, diagnostic accuracy can be increased by incorporating compressive venous ultrasonography of the femoral and popliteal viens. 15 B Quality assurance LUS is operator-dependent and technical expertise is required to acquire and interpret images; reproducibility of images is crucial to allow monitoring of disease progression. Supervised practice during the early stages of learning may not be possible during a pandemic setting. During the Ebola pandemic physicians were trained to obtain images which were reviewed remotely by an expert for detailed analysis and quality assurance. This ‘telemedicine’ approach is used extensively in providing ultrasound training to front-line providers throughout the world and could also be used for patients with COVID-19. A Conclusions LUS is simple, easy to learn and reproducible if a systematic approach is used. Ultrasound could potentially have a major role in the management of patients with COVID-19 in ICU where resources are scarce and access to definitive imaging limited. It can help clinicians in quickly investigating alternative causes of hypoxia. As knowledge about COVID-19 continues to evolve, LUS may allow providers to individualise patients’ care in a highly variable disease. Declaration of interests RA is a trainee and podcast editor and editorial board member of BJA Education. DK declares no conflicts of interest.

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          Incidence of thrombotic complications in critically ill ICU patients with COVID-19

          Introduction COVID-19 may predispose to both venous and arterial thromboembolism due to excessive inflammation, hypoxia, immobilisation and diffuse intravascular coagulation. Reports on the incidence of thrombotic complications are however not available. Methods We evaluated the incidence of the composite outcome of symptomatic acute pulmonary embolism (PE), deep-vein thrombosis, ischemic stroke, myocardial infarction or systemic arterial embolism in all COVID-19 patients admitted to the ICU of 2 Dutch university hospitals and 1 Dutch teaching hospital. Results We studied 184 ICU patients with proven COVID-19 pneumonia of whom 23 died (13%), 22 were discharged alive (12%) and 139 (76%) were still on the ICU on April 5th 2020. All patients received at least standard doses thromboprophylaxis. The cumulative incidence of the composite outcome was 31% (95%CI 20-41), of which CTPA and/or ultrasonography confirmed VTE in 27% (95%CI 17-37%) and arterial thrombotic events in 3.7% (95%CI 0-8.2%). PE was the most frequent thrombotic complication (n = 25, 81%). Age (adjusted hazard ratio (aHR) 1.05/per year, 95%CI 1.004-1.01) and coagulopathy, defined as spontaneous prolongation of the prothrombin time > 3 s or activated partial thromboplastin time > 5 s (aHR 4.1, 95%CI 1.9-9.1), were independent predictors of thrombotic complications. Conclusion The 31% incidence of thrombotic complications in ICU patients with COVID-19 infections is remarkably high. Our findings reinforce the recommendation to strictly apply pharmacological thrombosis prophylaxis in all COVID-19 patients admitted to the ICU, and are strongly suggestive of increasing the prophylaxis towards high-prophylactic doses, even in the absence of randomized evidence.
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            COVID-19 pneumonia: different respiratory treatments for different phenotypes?

            The Surviving Sepsis Campaign panel recently recommended that “mechanically ventilated patients with COVID-19 should be managed similarly to other patients with acute respiratory failure in the ICU [1].” Yet, COVID-19 pneumonia [2], despite falling in most of the circumstances under the Berlin definition of ARDS [3], is a specific disease, whose distinctive features are severe hypoxemia often associated with near normal respiratory system compliance (more than 50% of the 150 patients measured by the authors and further confirmed by several colleagues in Northern Italy). This remarkable combination is almost never seen in severe ARDS. These severely hypoxemic patients despite sharing a single etiology (SARS-CoV-2) may present quite differently from one another: normally breathing (“silent” hypoxemia) or remarkably dyspneic; quite responsive to nitric oxide or not; deeply hypocapnic or normo/hypercapnic; and either responsive to prone position or not. Therefore, the same disease actually presents itself with impressive non-uniformity. Based on detailed observation of several cases and discussions with colleagues treating these patients, we hypothesize that the different COVID-19 patterns found at presentation in the emergency department depend on the interaction between three factors: (1) the severity of the infection, the host response, physiological reserve and comorbidities; (2) the ventilatory responsiveness of the patient to hypoxemia; (3) the time elapsed between the onset of the disease and the observation in the hospital. The interaction between these factors leads to the development of a time-related disease spectrum within two primary “phenotypes”: Type L, characterized by Low elastance (i.e., high compliance), Low ventilation-to-perfusion ratio, Low lung weight and Low recruitability and Type H, characterized by High elastance, High right-to-left shunt, High lung weight and High recruitability. COVID-19 pneumonia, Type L At the beginning, COVID-19 pneumonia presents with the following characteristics: Low elastance. The nearly normal compliance indicates that the amount of gas in the lung is nearly normal [4]. Low ventilation-to-perfusion (VA/Q) ratio. Since the gas volume is nearly normal, hypoxemia may be best explained by the loss of regulation of perfusion and by loss of hypoxic vasoconstriction. Accordingly, at this stage, the pulmonary artery pressure should be near normal. Low lung weight. Only ground-glass densities are present on CT scan, primarily located subpleurally and along the lung fissures. Consequently, lung weight is only moderately increased. Low lung recruitability. The amount of non-aerated tissue is very low; consequently, the recruitability is low [5]. To conceptualize these phenomena, we hypothesize the following sequence of events: the viral infection leads to a modest local subpleural interstitial edema (ground-glass lesions) particularly located at the interfaces between lung structures with different elastic properties, where stress and strain are concentrated [6]. Vasoplegia accounts for severe hypoxemia. The normal response to hypoxemia is to increase minute ventilation, primarily by increasing the tidal volume [7] (up to 15–20 ml/kg), which is associated with a more negative intrathoracic inspiratory pressure. Undetermined factors other than hypoxemia markedly stimulate, in these patients, the respiratory drive. The near normal compliance, however, explains why some of the patients present without dyspnea as the patient inhales the volume he expects. This increase in minute ventilation leads to a decrease in PaCO2. The evolution of the disease: transitioning between phenotypes The Type L patients may remain unchanging for a period and then improve or worsen. The possible key feature which determines the evolution of the disease, other than the severity of the disease itself, is the depth of the negative intrathoracic pressure associated with the increased tidal volume in spontaneous breathing. Indeed, the combination of a negative inspiratory intrathoracic pressure and increased lung permeability due to inflammation results in interstitial lung edema. This phenomenon, initially described by Barach in [8] and Mascheroni in [9] both in an experimental setting, has been recently recognized as the leading cause of patient self-inflicted lung injury (P-SILI) [10]. Over time, the increased edema increases lung weight, superimposed pressure and dependent atelectasis. When lung edema reaches a certain magnitude, the gas volume in the lung decreases, and the tidal volumes generated for a given inspiratory pressure decrease [11]. At this stage, dyspnea develops, which in turn leads to worsening P-SILI. The transition from Type L to Type H may be due to the evolution of the COVID-19 pneumonia on one hand and the injury attributable to high-stress ventilation on the other. COVID-19 pneumonia, Type H The Type H patient: High elastance. The decrease in gas volume due to increased edema accounts for the increased lung elastance. High right-to-left shunt. This is due to the fraction of cardiac output perfusing the non-aerated tissue which develops in the dependent lung regions due to the increased edema and superimposed pressure. High lung weight. Quantitative analysis of the CT scan shows a remarkable increase in lung weight (> 1.5 kg), on the order of magnitude of severe ARDS [12]. High lung recruitability. The increased amount of non-aerated tissue is associated, as in severe ARDS, with increased recruitability [5]. The Type H pattern, 20–30% of patients in our series, fully fits the severe ARDS criteria: hypoxemia, bilateral infiltrates, decreased the respiratory system compliance, increased lung weight and potential for recruitment. Figure 1 summarizes the time course we described. In panel a, we show the CT in spontaneous breathing of a Type L patient at admission, and in panel b, its transition in Type H after 7 days of noninvasive support. As shown, a similar degree of hypoxemia was associated with different patterns in lung imaging. Fig. 1 a CT scan acquired during spontaneous breathing. The cumulative distribution of the CT number is shifted to the left (well-aerated compartments), being the 0 to − 100 HU compartment, the non-aerated tissue virtually 0. Indeed, the total lung tissue weight was 1108 g, 7.8% of which was not aerated and the gas volume was 4228 ml. Patient receiving oxygen with venturi mask inspired oxygen fraction of 0.8. b CT acquired during mechanical ventilation at end-expiratory pressure at 5 cmH2O of PEEP. The cumulative distribution of the CT scan is shifted to the right (non-aerated compartments), while the left compartments are greatly reduced. Indeed, the total lung tissue weight was 2744 g, 54% of which was not aerated and the gas volume was 1360 ml. The patient was ventilated in volume controlled mode, 7.8 ml/kg of tidal volume, respiratory rate of 20 breaths per minute, inspired oxygen fraction of 0.7 Respiratory treatment Given this conceptual model, it follows that the respiratory treatment offered to Type L and Type H patients must be different. The proposed treatment is consistent with what observed in COVID-19, even though the overwhelming number of patients seen in this pandemic may limit its wide applicability. The first step to reverse hypoxemia is through an increase in FiO2 to which the Type L patient responds well, particularly if not yet breathless. In Type L patients with dyspnea, several noninvasive options are available: high-flow nasal cannula (HFNC), continuous positive airway pressure (CPAP) or noninvasive ventilation (NIV). At this stage, the measurement (or the estimation) of the inspiratory esophageal pressure swings is crucial [13]. In the absence of the esophageal manometry, surrogate measures of work of breathing, such as the swings of central venous pressure [14] or clinical detection of excessive inspiratory effort, should be assessed. In intubated patients, the P0.1 and P occlusion should also be determined. High PEEP, in some patients, may decrease the pleural pressure swings and stop the vicious cycle that exacerbates lung injury. However, high PEEP in patients with normal compliance may have detrimental effects on hemodynamics. In any case, noninvasive options are questionable, as they may be associated with high failure rates and delayed intubation, in a disease which typically lasts several weeks. The magnitude of inspiratory pleural pressures swings may determine the transition from the Type L to the Type H phenotype. As esophageal pressure swings increase from 5 to 10 cmH2O—which are generally well tolerated—to above 15 cmH2O, the risk of lung injury increases and therefore intubation should be performed as soon as possible. Once intubated and deeply sedated, the Type L patients, if hypercapnic, can be ventilated with volumes greater than 6 ml/kg (up to 8–9 ml/kg), as the high compliance results in tolerable strain without the risk of VILI. Prone positioning should be used only as a rescue maneuver, as the lung conditions are “too good” for the prone position effectiveness, which is based on improved stress and strain redistribution. The PEEP should be reduced to 8–10 cmH2O, given that the recruitability is low and the risk of hemodynamic failure increases at higher levels. An early intubation may avert the transition to Type H phenotype. Type H patients should be treated as severe ARDS, including higher PEEP, if compatible with hemodynamics, prone positioning and extracorporeal support. In conclusion, Type L and Type H patients are best identified by CT scan and are affected by different pathophysiological mechanisms. If not available, signs which are implicit in Type L and Type H definition could be used as surrogates: respiratory system elastance and recruitability. Understanding the correct pathophysiology is crucial to establishing the basis for appropriate treatment.
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              2014 ESC guidelines on the diagnosis and management of acute pulmonary embolism.

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                Author and article information

                Journal
                BJA Educ
                BJA Educ
                Bja Education
                Published by Elsevier Ltd on behalf of British Journal of Anaesthesia.
                2058-5349
                2058-5357
                26 September 2020
                26 September 2020
                Affiliations
                [1 ]Bloomsbury Institute for Intensive Care Medicine, University College London, UK
                [2 ]Medical College of Georgia, Augusta, ATL, USA
                Author notes
                []Corresponding author:
                Article
                S2058-5349(20)30120-7
                10.1016/j.bjae.2020.09.001
                7519715
                1d3d2392-77cd-4ebc-b801-21f6a695224d
                © 2020 Published by Elsevier Ltd on behalf of British Journal of Anaesthesia.

                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.

                History
                : 18 May 2020
                : 7 September 2020
                : 18 September 2020
                Categories
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                lung ultrasound,covid-19,intensive care medicine
                lung ultrasound, covid-19, intensive care medicine

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