key: cord-0713367-1p34ikma
authors: Guarracino, Fabio; Vetrugno, Luigi; Forfori, Francesco; Corradi, Francesco; Orso, Daniele; Bertini, Pietro; Ortalda, Alessandro; Federici, Nicola; Copetti, Roberto; Bove, Tiziana
title: Lung, Heart, Vascular, and Diaphragm Ultrasound Examination of COVID-19 Patients: A Comprehensive Approach
date: 2020-06-11
journal: J Cardiothorac Vasc Anesth
DOI: 10.1053/j.jvca.2020.06.013
sha: 1fda99fce60f5eaa176b6964c2878b92dbbe969b
doc_id: 713367
cord_uid: 1p34ikma

Lung ultrasound (LU) has a multitude of features and capacities that make it a useful medical tool to assist physicians contending with the pandemic spread of novel coronavirus disease-2019 (COVID-19) caused by coronavirus SARS-CoV-2. Thus, a LU approach to patients with suspected COVID-19 is being implemented worldwide. In non-critical COVID-19 patients, two new LU signs have been described and proposed: the “waterfall” and the “light beam” signs. Both signs have been hypothesized to increase the diagnostic accuracy of LU for COVID-19 interstitial pneumonia. In critically-ill patients, a distinct pattern of LU changes seems to follow the disease's progression, and this information can be used to guide decisions about when a patient needs to be ventilated, as occurs in other disease states similar to COVID-19. Furthermore, a new algorithm has been published, which enables the automatic detection of B-lines as well as quantification of the percentage of the pleural line associated with lung disease. In COVID-19 patients, a direct involvement of cardiac function has been demonstrated, and ventilator-induced diaphragm dysfunction might be present due to the prolonged mechanical ventilation often involved, as reported for similar diseases. For this reason, cardiac and diaphragm ultrasound evaluation is highly important. Last but not least, due to the thrombotic tendency of COVID-19 patients, particular attention should also be paid to vascular ultrasound. This review is primarily devoted to the study of LU in COVID-19 patients. We explain the significance of its “light and shadows”, bearing in mind the context in which LU is being used: the emergency department and the intensive care setting. The use of cardiac, vascular, and diaphragm ultrasound is also discussed, as a comprehensive approach to patient care.

From the Wuhan district in Chinawhere the first cases of novel coronavirus disease-2019 (COVID- 19) were isolated in early January 2020the coronavirus called SARS-CoV-2 quickly spread to many other countries around the world. 1 The organ most affected by COVID-19 is the lung, where the virus enters the host's cells via the plasma membrane receptor protein angiotensin-converting enzyme 2 (ACE2), expressed most abundantly in the alveolar type II cells of the lungs. 2 Although SARS-CoV-2 also affects other body systems, 3 the pulmonary involvement of COVID-19 is of particular concern, since the leading cause of COVID-19 related death is severe acute respiratory failure. 4 The proper examination of a COVID-19 patient's entire respiratory system is therefore of utmost importance. Direct cardiac involvement has also been demonstrated, and diaphragm dysfunction is possible, as in other diseases similar to COVID-19. [5] [6] The characteristics of COVID-19 patients, who as a result of their pathology must be isolated and whose transfers must be limited, make ultrasound a useful tool for the bedside management of these patients. 7 In fact, in the early phase of the disease, lung ultrasound seems to show similar findings compared with computed tomography (CT), and its data is superior compared with that obtained by chest x-ray. 8 The ultrasound machine is also easy to cleanan essential characteristic during a pandemic. In marked contrast, the use of chest x-rays and CT scans may increase the risk of contamination and infection spread. 9 Notwithstanding, LU sonographers are divided in two fractions: those who believe in a specific LU pattern of COVID-19 interstitial pneumonia, and those who reject this hypothesis. [10] [11] This review is primarily devoted to the study of LU in COVID-19 patients. We explain the significance of its "light and shadows", bearing in mind the context in which LU is being used: the emergency department (ED) and the intensive care setting. The use of cardiac, vascular and diaphragm ultrasound is also discussed, in the context of a comprehensive approach to patient care.

In the present context of the COVID-19 pandemic, Huang Y et al. 12 and Volpicelli et al., 13 described two new B-line signs using LU. In patients with respiratory symptoms, these signs have been supposed to have a high probability of detecting COVID-19 interstitial pneumonia. The authors have coined the terms "waterfall" and "light beam" to describe these artifacts, respectively, however, these signs may be equivalent.

The waterfall sign constitutes fused B-lines (note, the authors did not describe any other particular characteristic), which are localized more frequently in the posterior and inferior areas of the lungs. On the other hand, the light beam sign, which has been described in more depth, is "a shining band-form artifact spreading down from a large portion of a regular pleural line, often appearing and disappearing with an onoff effect in the context of a normal A-line lung pattern visible in the background". 14 ( Figure 1 and supplemental material video 1).

From the pathophysiological standpoint, Volpicelli et al. state that the light beam matches the ground glass opacification (GGO) seen on the CT scan. This sign seems to correspond to the commencement of interstitial syndrome (B-lines) in the context of a normal lung profile. An international observational multicenter study on this subject is ongoing. [13] [14] The entire spectrum of lung ultrasound signs in COVID-19 interstitial pneumonia is reported in table 1.

As stated above, the ultrasound characteristics of COVID-19 pneumonia have been extensively described and mainly include: morphological alterations of the pleural line, the presence of multiple B lines, "white lung" areas, and consolidations. [12] [13] [14] [15] However, the diagnostic approaches used in Italy during the COVID-19 outbreak have been highly heterogeneous, 16 reflecting the organization of each individual hospital and the radiological imaging tools (LU, chest radiography and CT scanners) and expertise at their disposalall of which will have influenced the decisions regarding the first diagnostic approach to apply. 17 Furthermore, the combination of specific and differentiated routes for patients suspected or not of COVID-19 could have played a decisive role in determining the diagnostic path to take.

Although obtaining sufficient access to radiological diagnostics has been complicated for many hospitals, the ongoing pandemic has certainly fostered a rise in the awareness about LU. The LU 12 zones approach (6 for each hemithorax) in patients with suspected COVID-19 infection has been implemented in many situations. 18 Its primary objective has been to "rule in" or "rule out" COVID-19 pneumonia. 16, 17, 19, 20 Determination of the absence or presence of hypoxemia, and its degree, together with the LU findings presents a quick and straightforward approach that is also sufficiently accurate and feasible, even in logistically difficult contexts.

The flowchart in figure 2 summarizes a triage hypothesis, based mainly on a clinical and ultrasonography approach to the adult patient arriving in the ED with clinically suspected COVID-19. The nasopharyngeal swab is performed in all patients, and despite the non-optimal sensitivity of the test, its specificity is in fact absolute. 21 An accurate diagnostic gold standard is currently lacking, and the diagnosis can only be confirmed with certainty if the swab is positive. Indeed, a negative LU exam only rules-out COVID-19

pneumopathy, but it does not exclude infection or, therefore, the contagiousness of a patient. Thus, in the case of a patient requiring hospitalization, if their swab is negative and LU cannot confirm clinically suspected COVID-19, the patient can be safely admitted to a non-COVID-19 ward.

Three categories of patients with known or suspected COVID-19 can be schematized: patients without hypoxemia (SpO 2 ≥ 95%), patients with mild hypoxemia (SpO 2 between 90 and 95%), and patients with severe hypoxemia (SpO 2 ≤ 90%).

Thanks to the high sensitivity of LU, a normal LU picture (A-profile with lung sliding) in a non-hypoxic patient can safely rule out COVID-19 pneumopathy. The presence of ultrasound signs compatible with COVID-19 pneumopathy allows these patients to be discharged, although under a strict surveillance program. It is recommended to perform the walking-test in these patients if executable. The patient can be discharged safely if saturation does not fall by more than 3 points following physical exertion. 22 In the case of hypoxemia (mild or severe), a negative LU means that COVID-19 can be excluded as the cause of pneumonia, requiring that an alternative diagnosis be identified. If LU detects signs compatible with a COVID-19 lung infection, the patient needs to be hospitalized (in the ward with the most appropriate intensity of care) following more detailed clinical evaluations. That said, given the high pre-test probability of infection in a pandemic context, like that for SARS-CoV-2, the specificity of the LU signs becomes much higher, but is still low and often not sufficient to confirm the diagnosis alone. 11 

The LU pattern in COVID-19 patients requiring intensive care may include any or all of the signs demonstrated in other forms of interstitial pneumonia and ARDS: B-line patterns with multiform vertical artifacts ranging from well-spaced B-lines, coalescent B-lines, and the so-called "white lung". 23 In the latter, multiple coalescent B-lines tend to merge providing a homogenous white shining pattern, implicating severe aeration loss ( Figure 3 and supplemental video 1). LU is also useful for monitoring the appearance of consolidations suggestive of atelectasis or superimposed pneumonia. [24] [25] Following a definite COVID-19 diagnosis, the proportion of the affected subpleural lung can be inferred from the proportion of the pleural line involved, and this quantification permits assessment of the severity and extension of the disease. In this scenario, emerging ultrasound methods based on computer-aided diagnosis are now available [26] [27] [28] and provide a further and potentially promising option in terms of faster data analysis and applicability to large sets of data, especially for novice sonographers with little or no previous LU experience. [29] [30] From the pathophysiological standpoint, severe COVID-19 is a disease with biphasic evolution, and two main phenotypes have been recognized, "type 1" and "type 2", reflecting different parenchymal alterations. 31 LU can help differentiate between the two types by demonstrating the degree of heterogeneity of aeration loss. 24 In "type 1", the aeration loss is homogeneously distributed among lung regions, with a more diffuse LU B-pattern, whereas in "type 2" loss of aeration and consolidations prevail in the dependent lung regions.

In ARDS patients (but yet to be proven in COVID-19), a simple LU has been shown to be able to predict the response to positive end-expiratory pressure (PEEP)-induced lung recruitment [32] [33] and pronation in terms of effective re-aeration of the dorsal lung.The evolution of the disease and the response to treatments can be inferred from LU aeration and re-aeration scores that are associated with extravascular lung water content and the average lung tissue density, as evaluated by CT scan. 28, 34 Moreover, LU can diagnose secondary complications of mechanical ventilation, such as pneumothorax, and detect central venous line malpositioning, 35 thus reducing the need for chest radiography. 36 

As outlined above, LU has the capacity to answer precise questions, depending on the setting in which it is used. In the emergency department, its high sensitivity allows for the rapid ruling in orout of COVID-19, as in other diseases similar to COVID-19. In particular, it has very high sensitivity in relation to the diagnosis of interstitial syndrome and ARDS. 37 Furthermore, the "light beam sign", seems to be associated with a high percentage of patients with COVID-19 pneumonia with a high pre-test probability, and may lean towards the diagnosis of lung involvement by COVID-19 in patients suspected of being infected. 14 LU allows for the clinical progress of patients admitted to the ICU to be monitored (e.g., by ultrasound profiling and the lung ultrasound score) and can predict the probability of successful extubation (the possibility of heart and diaphragm involvement and their ultrasound evaluation are discussed below). 18, [38] [39] The LU strategy may also allow for the transfer of a patient from the ICU to departments with a lower level of patient care intensity.

However, some aspects of LU still require more detailed assessment. As mentioned above, the specificity of the signs detected by LU in relation to SARS-CoV-2 infection is not very high. 11 This constitutes a real risk of misdiagnosis or the non-recognition of other pathologies persisting during this pandemic. Pulmonary edema, bacterial pneumonia, other forms of viral pneumonia (e.g., cytomegalovirus or H1N1 virus), and pulmonary fibrosis continue to be causes of acute respiratory failure and must be kept in mind when making a differential diagnosis. Finally, it needs to be mentioned that LU cannot detect lesions deep within the lung parenchyma. 40 It should also be noted that although numerous papers have been published dealing with the use of LU during this COVID-19 pandemic, very few (if any) offer evaluations of diagnostic accuracy in terms of sensitivity and specificity. It is our opinion that lung abnormalities may develop before clinical manifestations. A patient with respiratory symptoms compatible with COVID-19 pneumonia and a suspect ultrasound pattern should be treated as COVID-19 positive until proven otherwise. However, the specificity of the nasopharyngeal swab is currently probably higher than any imaging test. Therefore, the only current test (pending the serological tests under development) is positivity to the RT-PCR assay. 21 

Echocardiography and vascular ultrasound should also be applied in the management of critical COVID-19

patients. As reported in table 2, cardiac involvement may occur in these patients, either as a direct effect of the SARS-CoV-2 virus or as a consequence of lung disease and ventilatory management. 5,41-42 Vascular involvement has also been reported in COVID-19, and vascular ultrasound may be required for the clinical management of these patients. 43 Direct cardiac involvement may manifest as dilated cardiomyopathy, as a severe decrease in ventricular systolic function and pericardial effusion in the case of viral myocarditis, or as localized wall motion abnormalities or global ventricular depression in the case of ST-elevation myocardial infarction (STEMI). [41] [42] When looking at the effects of the virus on the lung, two pulmonary phenotypes of COVID-19 can be observed: the L phenotype, which shows preserved compliance; and the H phenotype, with high pulmonary elastance. [44] [45] The cardiac abnormalities related to these two types are likely to be distinct: in the L phenotype, one would expect less severe right heart impairment, since the pressure to deliver tidal volume should be lower, even in the setting of non-absolute protective ventilation; whereas in the H phenotype, repercussions on the right heart are more probable.

In L type dyspneic patients, either spontaneously breathing or on non-invasive respiratory support, the cardiac ultrasound exam may reveal ventricular interdependence elicited by the increased respiratory effort, causing considerable pleural negative pressure and showing diastolic ventricular septal shift, leading to left ventricular hypo-diastole and reduced stroke volume. At the other end of the spectrum, in a COVID-19 H type patient under positive pressure mechanical ventilation, the cardiac ultrasound exam can detect cardiac insults directly connected to ventilation. In this case, the previously reported alterations secondary to mechanical ventilation 46 are found, with particular involvement of the right ventricle, leading to ventricular dilation, tricuspid insufficiency, reduced systolic right heart function, and possible secondary left heart compression ( Figure 4 ). Ventilator-induced heart dysfunction might even be present in a patient with no previous cardiac dysfunction. 47 A cardiac ultrasound exam should assess right ventricular dimensions and function (usually by recording tricuspidal annular plane excursion, TAPSE), tricuspid regurgitation, systolic pulmonary arterial pressure (sPAP), and the ratio of TAPSE over sPAP, a surrogate of right ventricular-arterial coupling. 47 Left ventricular function, although less influenced by inspiratory pressures, can be directly altered by right heart dysfunction and needs to be evaluated. Considering that 50% of COVID-19 pneumonia patients are reported to suffer from systemic arterial hypertension, 4 diastolic evaluation should always be carefully assessed. Particular attention should also be paid to the diastolic profile of COVID-19 patients in whom LU reveals a pattern of increased extravascular lung water, especially when associated with reduced left ventricular function.

In COVID-19, increased thromboembolic risk has been reported, 48 in the form of venous thrombosis and pulmonary embolism. This can lead to acute pulmonary hypertension, right heart enlargement, and severe tricuspid regurgitation besides thethe presence of thrombi in the venous system, right atrium or ventricleall of which can be seen using transesophageal echocardiography (TEE) (supplemental video 2).

In critically ill COVID-19 patients, a prothrombotic status seems to be frequently observed, leading to venous thrombosis and pulmonary embolism. 49 A vascular ultrasound assessment with the routine use of compression ultrasonography (CUS) to rule in the presence of deep vein thrombosis (DVT) seems reasonable in mechanically ventilated critically ill subjects. CUS should be performed in the presence of neuromuscular blocking agent infusion, especially before pronation or changing postures, or prior to vascular cannulation. 50 Central venous cannulation in such patients may be tricky due to the physical interference caused by personal protective equipment (PPE), which could impair smooth manoeuvres and finger perceptual sensitivity. This may result in the rapid deterioration of a patient's condition, DVT, or the use of higher low molecular weight heparin (LMWH). Furthermore, although specific guidelines on central venous cannulation have yet to be published, to the best of our knowledge , the need to avoid complications in patients ventilated with elevated positive pressure, as required in pneumothorax, is clear; hence, it seems rational to prefer the routine use of ultrasonography to guide the cannulation procedure rather than relying on landmark approaches.

Identifying the right time to wean COVID-19 patients from mechanical ventilation is of critical importance.

Although this invasive support used in severe forms of COVID-19 is to be considered as lifesaving, prolonged use in this particular type of patient is directly associated with further complications (ventilatorassociated pneumonia, pneumothorax and pneumomediastinum, ventilator-induced diaphragmatic dysfunction, to name but a few). [51] [52] The decision to complete the weaning process must be taken with caution since extubation failure carries serious complications [53] [54] Recently published case series show that length of stay in the ICU and the duration of mechanical ventilation in severe cases of COVID-19 are almost always more than seven days, despite the fact that most of the patients are not elderly (mean age 63 years) and had few comorbidities other than COVID-19 respiratory distress. 4, 52 A long length of ICU stay and duration of mechanical ventilation (especially with prolonged use of neuromuscular blocking agents) can make weaning particularly challenging and increase the risk of ventilation-induced diaphragm dysfunction. 55 In patients deemed difficult to wean due to ultrasounddiagnosed ventilation-induced diaphragm dysfunction, the possibility of performing a tracheostomy must also be taken into consideration. Therefore, although the role of tracheostomy in COVID-19-related ARDS is still unknown, there are several reasons why it may be helpful in this setting. Firstly, a lower level of sedation is required, due to improved patient comfort, putting the patient in the best possible condition to generate effort. Furthermore, the reduction in airway resistance leads to reduced respiratory work. Both of which may facilitate the reduction in, and ultimately the liberation from, ventilatory support. [56] [57] However, these advantages must be weighed against the risks related to this aerosol-generating procedure. That said, a recently published case series reported no cases of medical team infection with the virus following the performance of twenty-eight tracheostomies in COVID-19 patients. 58 In recent years, much emphasis has been placed on the study of diaphragmatic dysfunction as a predictor of weaning failure (in non COVID-19 patients), and two sonographic indexes have been studied and validated for this purpose: diaphragmatic excursion (DE), and the diaphragm thickening fraction (DTF). DE is the maximum displacement of the diaphragm during breathing, quantified in M-Mode with a low-frequency probe (2) (3) (4) (5) , preferentially in the right subcostal area ( Figure 5 ). 59 An excellent diaphragm excursion measured with ultrasound and a long inspiratory time during the spontaneous breathing trial (SBT) may help predict successful weaning. At the same time, DE < 10 mm has been proved to be linked to a prolonged weaning period and increased weaning failure. [60] [61] [62] Since DE is only associated with lung volume during the inspiratory phase, and it cannot discern whether the excursion rate is due to the contractile activity of the diaphragm or due to the ventilator's positive pressure, its application is only reliable during a T-piece or low level CPAP spontaneous breathing trial. 6 Diaphragm thickness (DT) can be assessed using a 10-15-MHz linear array transducer in the zone of apposition between the mid-axillary or anterior-axillary line, in the 8 th to 11 th intercostal space. 6, 63 The DTF is calculated as the difference between the end-inspiration thickness and end-expiration thickness divided by the end-expiration thickness ( Figure 6, supplemental video 3) . The DTF is also known as the "ejection fraction" of the diaphragm and can provide a reliable indicator of diaphragm function and its actual contribution to respiratory effort. For this reason, the DTF can be helpful in choosing the appropriate time for weaning (a DTF ≥ 30% is a robust predictor of weaning success in both SBTs and pressure support tests) and in the daily assessment of the ventilation support tailored to the patient. During mechanical ventilation, both decreases and increases from baseline DTF (due to excessive or insufficient muscle unloading) are strongly connected to the risk of prolonged ventilator dependence. 64 After the first few days, when total support in COVID-19 severe patients is often needed, targeting an inspiratory effort level may accelerate liberation from ventilation. 65 CONCLUSION Lung ultrasoundwhen in the hands of expertsis a useful abedside tool for the care of COVID-19 patients and its capacity to rule out involvement of the respiratory system is of particular value. LU experts can presently be divided into two categories: those who believe in a "specific" LU pattern in COVID-19 vs. those who are sceptic. Thus, LU constitutes an evolving area of interestone in urgent need of further, accurate data. Assessing diaphragmatic function with ultrasound undoubtedly supports the clinical management of COVID-19 patients during the weaning process. In ventilated patients, cardiac, vascular and lung ultrasound should always be evaluated together in order to gain a more comprehensive understanding of the relationship between lung and potential cardiac and vascular abnormalities. 

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