Coronavirus disease 2019 (COVID-19), a novel infectious disease due to a coronavirus identified as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), alarmed the health systems worldwide with its pandemic diffusion. Clinical manifestations depend mainly on the degree of respiratory system failure ranging from mild cases to acute respiratory distress syndrome (ARDS). However, it has been widely reported that COVID-19 is characterized also by extra-pulmonary, potentially life-threatening complications,[3,4] including cardiovascular accidents, such as ischemic and non-ischemic myocardial damage, pericardial diseases, and arrhythmias.[5-7] Diagnostic imaging[8-11] and biomarkers[12-14] might contribute to the early identification of a cluster of patients at risk of cardiac injuries and possibly predict COVID-19 development toward ARDS and/or multi-organ failure and mortality. Of course, computed tomography and cardiac magnetic resonance (CMR) have several limitations due, for example, to the possibility of contamination of personnel and patients; risk of transportation of high-risk patients; long time execution and interpretation of the exam (in particular for CMR); not easy repeatability of the exam in case of doubts or clinical worsening. Between diagnostic imaging, transthoracic echocardiography (TTE) is widely considered the first-choice for the evaluation of cardiac structures and function because of its reproducibility, feasibility, easy to do bedside, and for good cost-effectiveness.[15-17] The present review concerns recent evidence regarding clinical in-hospital utility of TTE, from Emergency Department to COVID wards and intensive care unit (ICU), to highlight its usefulness for assisting clinicians in the daily diagnostic and therapeutic management of the different cardiovascular manifestations of COVID-19.
MATERIALS AND METHODS
A literature search was conducted in PubMed MEDLINE from March 2020 to December 2022. MEDLINE was searched using keywords “COVID-19” and “echocardiography,” excluding studies on children, vaccination or mRNA vaccines against SARS-coV-2. To determine the study eligibility, two authors worked separately, in two different stages: in the first stage, the titles and abstracts of all search results were screened by an author using predefined keywords. In the second stage, another author assessed the articles’ eligibility. Case reports, narrative reviews, and non-English publications were excluded.
Transthoracic echocardiography and mortality in coronavirus disease 2019 patients: A prognostic tool?
The role of TTE in risk stratification of patients admitted with COVID-19 has been widely investigated. The purpose of this section of the review is to explore whether impaired cardiac structures and function predict COVID-19 prognosis. We have selected studies with adult patients hospitalized with documented COVID-19 infection subjected to TTE within 48–72 h of admission. In some studies, TTE was performed if requested in the context of clinical care. Clinical indications were mainly hypoxia, respiratory failure, hemodynamic instability, and suspected myocardial infarction. The mean age of patients was in the seventh decade of life with a male predominance in the majority of studies. The most common comorbidities, as expected, were hypertension, diabetes, and obesity. The percentage of patients receiving mechanical ventilation at the time of echocardiography varied from 20% to 100% in different studies. Mortality ranged from 11.6%, in studies with a lower percentage of ventilated patients, to 42%, in those with the highest percentage. Investigators assessed the characteristics of left and right ventricles in these patients sampling different parameters. In one of the first studies, Faridi et al. observed in patients hospitalized with COVID-19 in ICU, that left ventricular ejection fraction (LVEF) <50% was strongly associated with inpatient mortality, even though deaths were primarily from noncardiovascular causes and mortality rates were progressively increasing with more severe left ventricular dysfunction (P = 0.013).
Conversely, other authors found in patients admitted in ICU, that decreased LVEF is not uncommon and does not have a significant adverse effect on the prognosis of these patients, although elevation of cardiac biomarkers might predict mortality. In a cohort of patients who did not require intensive care overall ejection fraction (EF) is preserved. In detail, EF1, a measure of early systolic function and of predisposition to heart failure, is by contrast impaired in patients who have preclinical evidence of heart failure. The association of EF1 with mortality may, in part, explain the association of severity of COVID-19 with conditions such as hypertension, diabetes, and chronic kidney disease that are also risk factors for LV dysfunction.
Not only left ventricle (LV) characteristic but also right ventricular (RV) parameters may be used for the mortality prediction in COVID-19 subjects. During the hospital course, RV diastolic dysfunction, lower tricuspid annular plane systolic excursion (TAPSE), and higher pulmonary artery systolic pressure (PASP) predict disease progression to a critical stage, such as intubation for respiratory failure, shock, or ICU admission. Several investigators observed that impaired LVEF, impaired RV-function, and a tricuspid regurgitation >1 are associated with 30-day all-cause mortality. However, if for some authors RV failure and a relevant tricuspid regurgitation might be a consequence of COVID-19-induced pulmonary distress with development of elevation of the pulmonary artery pressure, others suggest that RV dysfunction is not dependent to respiratory parameters or mechanical ventilation. This is in line with the hypothesis that SARS-CoV-2 could cause direct damage to cardiomyocyte with subsequent RV overload and RV failure. As we will discuss in the dedicated paragraph, the RV longitudinal strain and RV enlargement are predictors of mortality, independent of pulmonary involvement and of LV function. The risk is proportional to the degree of dysfunction with moderate-to-severe RV systolic dysfunction resulting in higher odds than mild RV dysfunction. RV dysfunction compromises cardiac output, and this may explain the increased odds for vasopressors. This adverse remodelling conferred a >2-fold increase in risk for death. Conversely, patients without adverse RV remodelling (no RV dysfunction or dilation) were more likely to survive at hospital discharge. Moreover, recent studies evaluated the usefulness of new right ventricular function indices in predicting dysfunction and mortality. The RV longitudinal shortening fraction (RV-LSF) is an angle-independent and automatically calculated speckle-tracking parameter. RV systolic dysfunction is defined by an RV-LSF of <20%. In a cohort of moderate-to-severe ARDS patients due to COVID-19 under mechanical ventilation, RV systolic dysfunction defined by the RV-LSF was associated with higher 30-day mortalities.
Usefulness of echocardiography in intensive care unit
Cardiac damage, identified by biomarkers, electrocardiographic or echocardiographic features, has been recognized as an index of poor prognosis in patients hospitalized for COVID-19 infection. In this section, we focused on studies that analyzed cardiac impairment with early echocardiographic parameters in COVID-19 pneumonia and their association with severity disease and prognosis. Ceriani et al. collected 58 consecutive patients hospitalized for COVID-19 in a medium-intensity care unit. Eight of 58 patients who were included in the severe pneumonia group (38% of all patients) had an adverse evolution (six died, two were admitted to ICU and received mechanical ventilation). They had higher values of troponin, interlukin-6 and d-Dimer, but no significant new onset of major cardiac dysfunction was observed except for a mild increase in systolic pulmonary artery pressure compared to those with milder disease. These findings are in contrast with other studies that support the use of TTE to identify patients at low or high risk to develop ARDS. This could be explained by the fact that Ceriani group focused on early cardiac dysfunction before the eventual onset of mechanical ventilation, while other studies evaluated a high percentage of mechanically ventilated patients. In particular, Babu et al. included 87 patients, without previous heart failure, hospitalised with severe acute respiratory syndrome in which the most common echo findings were a raised PASP (36.8%) and RV dysfunction (26.4%), while 90.8% of patients had a preserved LVEF despite elevated troponin levels. The presence of RV dysfunction was significantly linked to adverse outcomes (odds ratio: 2.97, confidence interval 1.11–7.94, P < 0.03) but rather than a direct myocardial injury from SARS-Cov2, it could be linked to the severity of the respiratory involvement and to a consequent worse pulmonary prognosis. In the prospective multi-center ECHOVID-19 study involving 174 patients with COVID-19, only 14% had a known prevalent heart disease. About the echocardiography findings, patients developing ARDS had more impaired systolic function (lower LVEF: 51% vs. 59%, and global longitudinal strain (GLS): 13.7% vs. 16.9%). Among the 129 patients who had myocardial impairment (79% of all patients) defined by decreased systolic function and/or elevated cardiac biomarkers, 20 developed ARDS, while only 2 in the non-myocardial impairment group developed ARDS. Even if they found a connection between new myocardial echocardiographic impairment and development of ARDS, none of these studies confirmed a direct connection with mortality. In a multi-national observational study among 677 severely ill patients included from different countries, 69% of them received mechanical ventilation and underwent TTE during hospitalization in ICU. LV systolic dysfunction was found in 149 patients (23%) but was not associated with mortality. This is in line with Rodríguez-Santamarta et al. echocardiographic findings regarding 37 consecutive patients admitted to the ICU with ARDS without a previous history of heart failure or known LV systolic dysfunction. In this study patients were divided in two groups based on LVEF. Independently from biomarkers, none of the variables analyzed (LVEF <50%, right ventricular dysfunction, pericardial effusion, or regional wall motion abnormalities) were associated with death or readmission during follow-up.
Right ventricular involvement in coronavirus disease 2019
In COVID-19, cardiovascular manifestations can be the result of primary or secondary cardiac involvement, or even a worsening of previous cardiovascular disease (CVD). Multiple studies have provided information about different kinds of cardiac affections, some of them with different results regarding the frequency of right ventricular or left ventricular involvement.[33-35] Moreover, in the analysis restricted to patients without pre-existing CVD, one-third of the patients had an abnormal RV. Some studies have performed TTE on every subject with moderate COVID-19 disease not requiring invasive O2 and endotracheal intubation, highlighting that the only relevant changes were the RV parameters that significantly worsen in patients presenting disease progression (reduced fractional area change in 28%, reduced tricuspid lateral systolic velocity in 25%, reduced myocardial performance index in 20%, and reduced tricuspid annular plane systolic hike in 14%); others have only included subjects with a clear indication for echocardiography (thoracic pain, troponin elevation, D-dimer elevation, hemodynamic instability). On the other hand, Schott et al. showed that there was no specific correlation with D-dimer levels and RV dilation. Not surprisingly, many patients had a RV dilation, which could result from pulmonary embolism or elevated pulmonary vascular resistance from hypoxia and high mean airway pressures from extraordinary condition of mechanical ventilation. Similarly, there was no correlation with reduced LVEF and elevated troponin.
Lung parenchymal damage and altered pulmonary hemodynamic may determine pulmonary hypertension and secondary RV involvement, even in non-advanced disease stages, as a consequence of hypoxic vasoconstriction of the pulmonary circulation, use of positive end-expiratory pressure (PEEP) in mechanical ventilation, and pulmonary endothelial injury. Analogous studies showed that RV dysfunction is more prevalent than LV dysfunction, due to pulmonary hypertension, thrombotic or thromboembolic pulmonary disease. RV pressure overload secondary to acute pulmonary hypertension in COVID-19 may cause systolic and diastolic interventricular septal flattening with RV dilation and dysfunction compromising LV function via ventricular interdependence. Tricuspid regurgitation and increased central venous pressure exacerbate RV failure. Mechanical ventilation compromised accurate assessment of right atrial pressure. In the cohort of Jain et al., RV dysfunction is a known complication of hypoxemic injury, including ARDS and influenced by mechanical ventilation. Hemodynamic instability and RV dysfunction in the setting of ARDS are related to mortality. Along with respiratory symptoms, cardiovascular manifestations are also common and may adversely impact prognosis.[41-43] In ARDS, RV is subject to impaired function due to increased afterload, not only in COVID-19 patients. RV dysfunction is known to be an independent predictor of mortality in the non-COVID-19 setting and increasing ARDS severity is associated with increased frequency of RV dysfunction. While no single causative factor has been elucidated, there are several potential etiological factors which have been shown to increase RV afterload and impair RV contractility, both leading to RV dysfunction. ARDS, pulmonary micro-and macrothrombosis, and positive pressure ventilation with PEEP have all been shown to increase RV afterload with RV contractility being depressed by direct myocardial injury. The acute stress caused by hypoxemia and mechanical ventilation added to the prothrombotic status, hyperinflammatory condition, direct viral damage, and ischaemic injury places the RV in a critical position. Interestingly, D’Alto et al. found that COVID 19-induced ARDS is strictly characterized by the early and pronounced uncoupling of RV function from the pulmonary circulation; authors proposed that the noninvasive echocardiographic assessment by the TAPSE/PASP ratio adds, significantly and independently, a prognostic relevance to the PaO2/FIO2 ratio in these patients. Analogously, a recent study involving patients with COVID-19 ARDS reported that non-survivors presented PASP values at the upper limit of normal and decreased indices of RV systolic function, identifying longitudinal strain as an independent predictor of outcome. Pulmonary hypertension in COVID-19 may belong either to pulmonary hypertension due to lung parenchymal disease or more probably to chronic thromboembolic pulmonary hypertension. The TAPSE/PASP is easier to assess, can be part of standard bedside echocardiographic assessments as it does not require off-line analysis of images or a specific software, and might represent a more sensitive assessment of RV-PA coupling.[34,50] Furthermore, TAPSE assessment is important in the management of deteriorating patients, enabling early identification and treatment of cardiac damage. In the study by Manzur-Sandoval et al., the limited ability of the RV to maintain ventricular-arterial coupling was clearly one of the parameters with the highest prediction of mortality. Indeed, all the patients who presented with this altered parameter died, which suggests that the combination of RV dysfunction associated with pulmonary hypertension might be, eventually, two independent and simultaneous pathophysiological phenomena. This finding challenges the notion that only pulmonary hypertension generates RV dysfunction in response to increased afterload.
Speckle tracking echocardiography in coronavirus disease 2019: Reliable?
As we have already underline, TTE is considered the first-level diagnostic method used to evaluate the degree of cardiac involvement, guide clinical management and predict the prognosis of patients affected by COVID-19. However, TTE may be subjected to several factors that limit the feasibility of a highly operator-dependent and time-consuming method. The critical conditions of patients hospitalized in COVID-19 units, the non-invasive mechanical ventilatory support used, the infectious risk resulting from close and prolonged exposure and the lack of training of medical personnel have, in fact, often limited diagnostic instrumental approach. In this regard, speckle tracking or strain echocardiography (STE) can be considered a useful and reliable tool compared to traditional TTE to evaluate cardiac function even for a faster images acquisition and the possibility of offline reporting in a safer environment. STE allows measurement of global longitudinal deformation (GLS) of the right and left ventricles. GLS is a quantification of longitudinal myocardial shortening during systole. GLS values are expressed as negative percentage (shortening) and usually between − 20% and − 30% for both ventricles. Less negative values (e.g.-15%) indicate a decrease in longitudinal shortening. GLS is calculated automatically by modern echocardiographic software from a single cardiac view and the GLS estimate has been shown to be faster and less dependent on the operator than the estimate of the classic echo-Doppler indices of ventricular function. The measurement of myocardial strain using STE plays a clinical diagnostic and prognostic role in different cardiac diseases and provides an objective quantification of the strain and dynamics of the biventricular myocardium. In COVID-19 patients in whom both pulmonary and systemic inflammation may contribute to RV failure through overload and direct cardiomyocyte damage, STE has been recommended as the superior method for evaluation of RV involvement. In particular, STE may detect RV dysfunction more accurately and sensitively than conventional guideline-recommended echocardiographic parameters such as TAPSE, which assesses only basal longitudinal motion of the RV free wall and may not accurately reflect the whole performance. Moreover, RV strain seems to correlate with a worse prognosis (ARDS, needing to receive high flow oxygen and mechanical ventilation) as shown in the study by Rothschild et al. where clinical worsening was proportional to worsening of segmental STE of the right ventricle. In addition to the prognosis, it can be considered a good predictor of mortality as shown in the study by Li et al. in which the non-survived patients had, compared with the survivors, RV dilation with reduced systolic function and elevated pulmonary systolic artery pressure. Analogous results derived from the ECHOVID-19 study. Beyls et al., however, demonstrated that RV free wall longitudinal strain (RV-FWLS) and conventional RV parameters (including RV fractional area change, tricuspid TAPSE, and tricuspid tissue Doppler annular velocity) failed to predict mortality in 30 critical patients with COVID-related pneumonia admitted to the ICU; however, it is necessary to consider that the small number of the sample under examination, the acoustic window compromised by mechanical ventilation, the presence of COVID-related lung lesions and the patient’s forced decubitus, have limited the feasibility of the examination itself and made the interpretation of the results difficult. Other studies compared the biventricular mechanics of COVID-19 patients, evaluating LV global longitudinal strain (LVGLS), RV-FWLS and RV global strain (RVGS).[59,60] While LVGLS was decreased in all patients because it was influenced by arterial hypertension present in most of the study participants, RVGS and RV-FWLS were significantly reduced only in patients with adverse outcomes. However, as highlighted by Shmueli et al., LV dysfunction may be useful for detecting subclinical cardiac damage in hospitalized patients with elevated troponin, brain natriuretic peptide, and inflammatory markers. In this study, in fact, LVGLS was reduced in 80% of the patients enrolled, whereas EF and wall anomalies were less frequent. It is therefore possible to state that the evaluation of right ventricular strain assumes considerable importance in the classification of patients with COVID-19 for the purpose of risk stratification and mortality, even more than LV dysfunction. However, these studies did not analyze LVGLS values under which a correlation with mortality could have been observed. Indeed, Park et al. showed that LVGLS values >-13.8% in COVID-19 patients could be an early marker of mortality even in patients with an EF greater than 50%. Another LV function parameter, myocardial work efficiency (MWE), derived using LV pressure-strain loops at rest, is more sensitive than GLS to detect significant coronary artery disease in patients with no regional wall motion abnormalities and normal EF. It provides a more load independent measure of LV function by accounting for afterload. Impaired MWE is independently associated with in-hospital mortality in COVID-19 patients. In an international, multicentre cohort study, authors divided patients in two groups, with or without myocardial injury, defined as any elevation in cardiac troponin at the time of clinical presentation or during the hospitalization; they found that patients with myocardial injury had an increased prevalence of echocardiographic abnormalities: global LV dysfunction, regional LV wall motion abnormalities, grade II or III diastolic dysfunction, greater LV volumes, RV dysfunction and pericardial effusions. Among the entire study cohort of 305 patients, mechanical ventilation was required in 34.5% of patients and in-hospital mortality occurred in 18.7%. Compared with patients without myocardial injury, those with myocardial injury detected on TTE had higher rates of in-hospital death (26.8% vs. 5.2%; P < 0.0001). Conversely, myocardial injury without echocardiographic abnormalities was not a significant predictor of increased mortality.
In critical COVID-19 patients, cardiovascular function could be influenced by several factors, including systemic inflammatory response, hypoxemia, mechanical ventilation, direct myocardial injury, myocarditis, arterial dysfunction, and pulmonary embolism.[33,34,66] In the management of deteriorating patients, an exam easy to apply at bedside should play a central role in the clinical decisions, allowing better identification of pathogenesis and prompt treatment. From this point of view, echocardiography should be the first choice. The cardiac involvement in COVID-19 is often early and characterized by multiple clinical manifestations, such as ischemic and nonischemic myocardial damage, pulmonary hypertension, pericardial diseases, and arrhythmias. Making use of an early diagnosis and of means that can rapidly evaluate the prognostic evolution can greatly change the clinician’s choices. Early in-hospital echocardiographic evaluation is recommended also for non-COVID-19 patients since an early cardiovascular diagnosis could affect the in-hospital course and the rehospitalization rate. However, as already underline,[15,68] to ensure operator safety, it is inappropriate to undergo all patients to echocardiography. This literature review shows, among other things, as can be excluded from the examination asymptomatic patients, or with mild symptoms. Conversely, echocardiography appears important to evaluate the prognosis of hospitalized patients affected by severe pneumonia, in ARDS and complicated patients.
If on the one hand, TTE and STE could help clinicians to foresee patients with the worst evolution, on the other hand, TTE and STE may be useful for the follow-up in symptomatic patients also after their discharge.
In conclusion, this literature review shows that TTE evaluation should be considered in patients with COVID-19 to better characterize the cardiac substrate, to make a risk stratification in critically ill patients and to potentially guide management strategies.
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Conflicts of interest
There are no conflicts of interest.
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