Why, when, and how to use lung ultrasound during the COVID-19 pandemic: enthusiasm and caution

The coronavirus disease-2019 (COVID-19) pandemic is one of the major current global health issues, due to its high rate of infection and increasing mortality. SARS-CoV-2 is a novel coronavirus that spreads easily from symptomatic and asymptomatic patients through close contact and respiratory droplets, causing a severe acute respiratory infection in a certain percentage of cases.1 It is a challenge for clinicians to provide early diagnosis to isolate patients and prevent the most severe forms of acute distress respiratory syndrome (ARDS) or COVID-19 ARDS (CARDS), which represent a serious burden even for the most advanced medical systems.2,3 Diagnosis of COVID-19 is based on the real-time reverse transcription–PCR (rRT–PCR) analysis of respiratory tract specimens. However, rRT–PCR has a low sensitivity, translating in a subgroup of patients admitted to the hospital with the typical clinical aspects of the diseases but with false negative specimens. Chest computed tomography (CT) has a high sensitivity for the diagnosis of COVID-19 pneumonia, so it is considered the reference imaging method.4,5 Chest CT analysis of patients with COVID-19 pneumonia typically shows bilateral and peripheral ground-glass opacities, crazy paving, and consolidations in a patchy distribution, that worsen with the progression of the disease.6 Nevertheless, the feasibility of CT can be limited by its availability, the need to mobilize the patient, and the long-term risks related to ionizing radiation.7 Bedside real-time lung ultrasound (LUS) for the assessment of COVID-19 pneumonia could support and integrate lung imaging with several advantages.8–10 In fact, beyond its consolidated importance as a diagnostic and prognostic tool in heart failure and critically ill patients,11–13 LUS can detect some typical characteristics of COVID-19 pneumonia.8–10,14 The present review describes the role of LUS for the evaluation of COVID-19 pulmonary involvement and its applications for triaging, monitoring, and prognostic management of these patients. LUS is showing a growing value in everyday clinical practice, especially in the emergency and intensive care settings. This imaging modality is portable, quick, repeatable, easy to learn, as compared with other ultrasonographic techniques, and with high inter-rater and intra-rater reproducibility.15,16 It can reduce a patient’s exposure to ionizing radiation and contribute to the safety of the healthcare providers by minimizing the need for moving the patient, therefore reducing the incidence of cross-contamination and the number of healthcare professionals exposed to the patient. Moreover, the growing use of small and portable handheld devices is running in parallel with the wider integration of point-of-care ultrasound in daily practice as an extension to bedside clinical examination.17,18 The high sensitivity of LUS for the detection of pulmonary involvement allows it to be a reliable monitoring tool for the regular assessment of patients with COVID-19. LUS can be performed at all steps in the evaluation of COVID-19 patients. Table 1 summarizes the main aspects of the use of LUS in different COVID-19 clinical scenarios. Clinical scenarios where LUS can support the management of COVID-19 patients Portable Quick and bedside ‘Grey’ cases Potential increase of false positives Quick and bedside More sensitive than chest X-ray Differential diagnosis with other conditions causing acute dyspnoea Overlapping patterns in patients with comorbidities Risk stratification Monitoring subclinical pulmonary worsening Monitoring treatment response Quick and bedside Dynamic May anticipate clinical deterioration Risk stratification Monitoring/titration of mechanical ventilation Quick and bedside Dynamic Portable Quick and bedside ‘Grey’ cases Potential increase of false positives Quick and bedside More sensitive than chest X-ray Differential diagnosis with other conditions causing acute dyspnoea Overlapping patterns in patients with comorbidities Risk stratification Monitoring subclinical pulmonary worsening Monitoring treatment response Quick and bedside Dynamic May anticipate clinical deterioration Risk stratification Monitoring/titration of mechanical ventilation Quick and bedside Dynamic Clinical scenarios where LUS can support the management of COVID-19 patients Portable Quick and bedside ‘Grey’ cases Potential increase of false positives Quick and bedside More sensitive than chest X-ray Differential diagnosis with other conditions causing acute dyspnoea Overlapping patterns in patients with comorbidities Risk stratification Monitoring subclinical pulmonary worsening Monitoring treatment response Quick and bedside Dynamic May anticipate clinical deterioration Risk stratification Monitoring/titration of mechanical ventilation Quick and bedside Dynamic Portable Quick and bedside ‘Grey’ cases Potential increase of false positives Quick and bedside More sensitive than chest X-ray Differential diagnosis with other conditions causing acute dyspnoea Overlapping patterns in patients with comorbidities Risk stratification Monitoring subclinical pulmonary worsening Monitoring treatment response Quick and bedside Dynamic May anticipate clinical deterioration Risk stratification Monitoring/titration of mechanical ventilation Quick and bedside Dynamic In the Emergency Department (ED), LUS can be employed for an early detection of pulmonary involvement in symptomatic patients suspected for COVID-19, with still pending rRT–PCR, as soon as they arrive. A typical LUS pattern, even in the absence of rRT–PCR results, should prompt isolation and treatment of the pulmonary involvement. Even with negative rRT–PCR, a typical LUS examination should lead to managing the patient as having a high probability for COVID-19, and to repeating the swab. In this scenario, LUS is more sensitive than chest X-ray, whereas CT scan should be reserved for confirmation in doubtful cases and for a better definition of the pulmonary involvement, when needed. In patients who have a diagnosis of COVID-19, LUS is useful to detect pulmonary involvement and to grade it. There are no validated scoring systems to clearly differentiate a mild from a moderate or severe degree but, as a general rule, a few separated B-lines in a limited number of chest areas would indicate a mild degree, whereas coalescent and compacted B-lines, with peripheral consolidations diffuse all over the chest, indicate a more severe involvement. In these patients, LUS can also help in monitoring treatment effects; in patients with an initial mild LUS pattern and clinical picture, a daily LUS monitoring can anticipate the clinical deterioration, which is not so uncommon in these patients, often at 7–14 days from symptom onset. In patients in the intensive care unit (ICU), LUS is a useful tool in monitoring disease progression as well as the effects of mechanical ventilation and recruitment manoeuvres of deaerated lung areas, mainly based on positive end-expiratory pressure (PEEP) titration and prone positioning. Again, this approach is not validated in the specific cohort of COVID-19 patients; however, it has demonstrated good results in patients with ARDS, especially when coupled with an integrated cardiac and diaphragmatic evaluation.19 Several studies suggested the value of a lung aeration score to monitor the progression of lung aeration before and after extubation, and to predict extubation failure.20,21 Therefore, we would suggest utilizing LUS as part of a wider extubation protocol that integrates the standard clinical assessment, ventilatory parameters, and lung mechanics along with the lung and diaphragmatic ultrasonographic findings. Another potential and novel application of LUS is home monitoring. LUS is a suitable tool to be applied in out-of-hospital settings, especially with handheld devices.18 Bringing the diagnostic armamentarium to the patient, instead of bringing the patient to the hospital, can be extremely convenient in a pandemic situation with a high risk of viral spreading. LUS is the most suitable chest imaging tool for this approach. Symptomatic fragile patients who cannot easily access the hospital can be evaluated directly at home with a very sensitive examination for lung involvement, which can help in the decision-making before the availability of rRT–PCR results. LUS can be especially decisive with a clearly negative or clearly positive examination; in the case of more ambiguous cases, LUS could, at least in theory, lead to a higher number of hospitalizations, which is a risk that should be taken into account. However, LUS can help in the differential diagnosis of other acute conditions that may have caused undifferentiated symptoms in these patients, especially when coupled with a focus cardiac ultrasound (FoCUS).22 With the need for strict physical distancing, a home-based evaluation can also significantly reduce the contact with other patients and the number of interactions with the healthcare personnel. The convex or microconvex transducers are the most universally used for LUS, as they allow a good visualization of the parenchymal alterations while also providing a reasonable view of the pleural line. The examination should start by adjusting the machine on the lung pre-set (or abdominal pre-set if lung pre-set is not available), with a depth of ∼8–10 cm (6–8 cm for slim subjects, 10–12 cm or more for obese subjects); gain should be optimized on the whole image, and the focus should be adjusted to the area of interest (e.g. the pleural line). The probe could be placed vertically perpendicular to the ribs (longitudinal approach) or horizontally along the intercostal spaces (transverse/oblique approach). Phased array transducers could also be used to visualize the parenchyma, albeit with more limited visualization of the pleura. Each point should be examined for at least one complete respiratory cycle (∼5–6 s). At the moment, there is no validated scanning scheme for COVID-19 patients. Therefore, it is advisable to rely on previously validated schemes that have already proven to be useful, although in different conditions, such as ARDS (Figure 1), which represents a good balance between being simple and comprehensive.23 Whenever possible, we recommend to include the scanning of the posterior zones, where lung lesions are more commonly seen in these patients.6 If the patient cannot move from the supine position, the posterolateral part of the chest can usually be scanned by turning the patient to his/her side. For these reasons, LUS scanning in COVID-19 patients should be as thorough as possible, and even if different schemes and areas are considered, in a given area, all available thoracic space should be checked, and the worst LUS picture should be considered. Proposal for lung ultrasound scanning scheme in COVID-19 patients (adapted from Bouhemad et al.23). COVID-19 presented a challenging clinical dilemma for clinicians at the frontline, with its atypical features which are different from the classical presentation of ARDS. Two different phenotypes have been described, at least in a theoretical model:24 the more frequent phenotype ‘L’ typically presents with normal to mildly reduced lung compliance, albeit with a level of hypoxaemia disproportionate to the relatively preserved lung compliance, in which chest CT typically shows predominantly peripheral ground-glass opacifications that worsens with the progression of the disease. On the other hand, the less frequent phenotype ‘H’ is more similar to the classic ARDS presentation with reduced lung compliance and evidence of dense lobar consolidations on chest CT. LUS is potentially able to distinguish these two phenotypes, based on the different signs and patterns. In COVID-19, we typically see various grades of multiple B-lines with patchy distribution. B-lines can be separated or coalescent, including pictures of sonographic ‘white lung’ (Figure 2). B-lines are often visible in the context of ‘spared’ areas of good aeration in which we see multiple horizontal A-lines that are reverberations of the pleural line. A recently described finding is observed in most patients in the early phases of COVID-19 pneumonia: it is a shiny ‘light beam’ (Supplementary material online, Video S1), that is a band-like artefact, often appearing and disappearing with respiration.9,10 Other common findings in COVID-19 are an irregular ‘fragmented’ pleural line with small peripheral consolidations (Supplementary material online, Video S2). Larger consolidations characterize the phenotype ‘H’ or a superimposed bacterial pneumonia (Supplementary material online, Video S3), and it is debeated whether they may represent pulmonary infarctions. Large pleural effusions are not commonly seen, whereas trivial localized pleural effusion can be visualized in the context of more deaerated areas. Table 2 and Figure 2 summarize the common LUS findings in COVID-19. LUS findings correlated to chest CT progressing from normal aeration (A), to progressively more deaerated conditions: coalescent B-lines (B and C), small peripheral consolidation (D), large consolidation (E). The red box in (C) shows an area of ground-glass opacification on CT corresponding to confluent B-lines on LUS. Main LUS differences between COVID-19 involvement and other conditions that may yield respiratory symptoms B-lines Pleural line Patchy, non-gravity related distribution Separated and more often coalescent Very defined spared areas Light beam Homogeneous, gravity-related distribution Usually separated or coalescent in more severe cases No spared areas Patchy, non-gravity-related distribution Separated and more often coalescent Spared areas Usually more prevalent at lung bases Usually separated B-lines or coalescent in more severe cases Usually no spared areas Consolidations Pleural effusion Usually small peripheral consolidations Larger consolidations in more advanced phases or with superimposed bacterial pneumonia. Large pleural effusion rare Trivial localized pleural effusion in the context of more deaerated areas Frequent, variable size Trasudate, not complex appearance Usually bilateral (often larger on the right side) Rare, unless in very advanced cases or acute phases Usually not large B-lines Pleural line Patchy, non-gravity related distribution Separated and more often coalescent Very defined spared areas Light beam Homogeneous, gravity-related distribution Usually separated or coalescent in more severe cases No spared areas Patchy, non-gravity-related distribution Separated and more often coalescent Spared areas Usually more prevalent at lung bases Usually separated B-lines or coalescent in more severe cases Usually no spared areas Consolidations Pleural effusion Usually small peripheral consolidations Larger consolidations in more advanced phases or with superimposed bacterial pneumonia. Large pleural effusion rare Trivial localized pleural effusion in the context of more deaerated areas Frequent, variable size Trasudate, not complex appearance Usually bilateral (often larger on the right side) Rare, unless in very advanced cases or acute phases Usually not large Main LUS differences between COVID-19 involvement and other conditions that may yield respiratory symptoms B-lines Pleural line Patchy, non-gravity related distribution Separated and more often coalescent Very defined spared areas Light beam Homogeneous, gravity-related distribution Usually separated or coalescent in more severe cases No spared areas Patchy, non-gravity-related distribution Separated and more often coalescent Spared areas Usually more prevalent at lung bases Usually separated B-lines or coalescent in more severe cases Usually no spared areas Consolidations Pleural effusion Usually small peripheral consolidations Larger consolidations in more advanced phases or with superimposed bacterial pneumonia. Large pleural effusion rare Trivial localized pleural effusion in the context of more deaerated areas Frequent, variable size Trasudate, not complex appearance Usually bilateral (often larger on the right side) Rare, unless in very advanced cases or acute phases Usually not large B-lines Pleural line Patchy, non-gravity related distribution Separated and more often coalescent Very defined spared areas Light beam Homogeneous, gravity-related distribution Usually separated or coalescent in more severe cases No spared areas Patchy, non-gravity-related distribution Separated and more often coalescent Spared areas Usually more prevalent at lung bases Usually separated B-lines or coalescent in more severe cases Usually no spared areas Consolidations Pleural effusion Usually small peripheral consolidations Larger consolidations in more advanced phases or with superimposed bacterial pneumonia. Large pleural effusion rare Trivial localized pleural effusion in the context of more deaerated areas Frequent, variable size Trasudate, not complex appearance Usually bilateral (often larger on the right side) Rare, unless in very advanced cases or acute phases Usually not large Using a standardized scanning scheme enables us to assign a score to each lung zone and, therefore, assess the overall lung aeration. As for the scanning scheme, in the absence of a standardized score for COVID-19 patients, it is reasonable to rely on a previously validated score.23 Score 0: predominant A-lines or <3 separated B-lines. Score 1: at least three B-lines or coalescent B-lines of the a clearly irregular pleural line. Score at least three B-lines or coalescent B-lines of the with a clearly irregular pleural line. Score coalescent B-lines of the a clearly irregular pleural line. Score coalescent B-lines of the with a clearly irregular pleural line. Score large consolidations least It is useful to characterize the consolidation or of pleural effusion should be as The score is by the of each The are not in the this is a more which is useful they are very frequent in COVID-19 which is with the of the It however, not demonstrated that this of used in other conditions such as pneumonia and be to characterize these patients. On the one hand, it is that a higher sonographic score a less a pulmonary on the other hand, in COVID-19 patients, the different LUS patterns and distribution may be more to the on different especially when patients into the theoretical LUS is often used in the differential diagnosis of acute dyspnoea and respiratory Other acute conditions, such as and pulmonary pulmonary or bacterial pneumonia, can still be a of symptoms and in the differential diagnosis of patients suspected of having COVID-19 pneumonia. In these cases, the integration with the patient’s medical physical and other findings is even more than LUS findings in COVID-19 however, some that can at least the with a degree of to the or absence of the typical COVID-19 LUS patterns 2). It be that the between the examination and the of symptom is to the sensitivity and of the LUS a negative LUS scanning very close to symptom cannot the of progression of the disease to pneumonia. LUS diagnosis of a mild degree of pneumonia in a patient with typical symptoms for days may a better LUS patients with pulmonary usually bilateral B-lines which are separated in the phases and to be more confluent and in more advanced In of when B-lines are confluent and it is to one by it is the percentage of by the pleural line that should be considered, and by of of B-lines the pleural line at least when a cardiac probe in the this percentage can be easily applied to the convex probe as for a better In pulmonary B-lines to a gravity-related distribution over the chest, so it would be to B-lines on the chest and no B-lines or B-lines at the lung the spared areas are usually not The pleural line has a and regular even in patients, and a irregular ‘fragmented’ pleural line or peripheral small consolidations are unless there is a with ARDS have the most similar LUS pattern to COVID-19 patients, with non-gravity-related distribution of B-lines, irregular pleural and consolidations of different from small peripheral consolidations to larger with the most between COVID-19 pneumonia and a more ARDS LUS pattern is the of initial between the of the LUS picture and the clinical with relatively asymptomatic COVID-19 patients with normal or close to normal and very advanced LUS seen in patients in other ARDS Pleural effusion is also usually larger and more frequent in classical ARDS. In bacterial pneumonia, LUS usually shows consolidations of variable but often large and with a which can be present in the more advanced phases of COVID-19, but not typically in the early B-lines can be present as a multiple B-lines in one area of the chest usually indicate the of a consolidation that is not peripheral to be seen by LUS, or of a consolidation not in the lung parenchyma, so through B-lines we are the the Other can be seen from the of a which should not be considered as B-lines. the from the pleural line a consolidation should be considered as B-lines, with lung such as pulmonary have a LUS pattern of multiple B-lines, usually and diffuse at the lung In the very early the pleural line can be relatively showing a normal whereas in more advanced the pleural line is progressively more irregular and It is to that of the sonographic pleural line should not be considered as of alterations of the which is not directly in these the is a sonographic that is not directly related to the and of the pleura. 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