• „ EXPERT OPINION AND POSITION PAPER

Echocardiography during the coronavirus disease 2019 pandemic — the impact of the vaccination program. A 2021 update of the expert opinion of the Working Group on Echocardiography of the Polish Cardiac Society

Piotr Szymański1, Andrzej Gackowski2, Katarzyna Mizia-Stec3, Jarosław D Kasprzak4, Magdalena Lipczyńska5, Piotr Lipiec6

Review Committee/Collaborators: Olga Trojnarska7, Paulina Wejner-Mik4, Danuta Sorysz8, Bożena Sobkowicz9, Zofia Oko-Sarnowska7, Andrzej Wysokiński10, Andrzej Szyszka11, Edyta Płońska-Gościniak12, Zbigniew Gąsior13, Michał Ciurzyński14*, Tomasz Pasierski15*, Piotr Hoffman5

1Clinical Cardiology Center, Central Clinical Hospital of the Ministry of the Interior in Warsaw and Center of Postgraduate Medical Education, Warszawa, Poland

2Jagiellonian University, Medical College, Institute of Cardiology, Department of Coronary Disease and Heart Failure, Noninvasive Cardiovascular Laboratory, John Paul II Hospital, Kraków, Poland

31st Department of Cardiology, Medical University of Silesia in Katowice, Katowice, Poland

41st Department of Cardiology, Medical University of Lodz, Bieganski Hospital, Łódź, Poland

5Department of Congenital Heart Disease, National Institute of Cardiology, Warszawa, Poland

6Department of Rapid Cardiac Diagnostics, Medical University of Lodz, Łódź, Poland

71st Department of Cardiology, Poznan University of Medical Sciences, Poznań, Poland

8Department of Cardiology and Cardiovascular Interventions, University Hospital, Kraków, Poland

9Department of Cardiology, Medical University in Bialystok, Białystok, Poland

10Department of Cardiology, Pomeranian Medical University, Szczecin, Poland

112nd Department of Cardiology, Poznan University of Medical Sciences, Poznań, Poland

12Department of Cardiology, Medical University of Lublin, Lublin, Poland

13Department of Cardiology, Medical University of Silesia in Katowice, Katowice, Poland

14Department of Internal Medicine and Cardiology Medical University of Warsaw, Warszawa, Poland

15Department of Medical Ethics and Palliative Medicine, Warsaw Medical University, Warszawa, Poland

*Reviewer on behalf of the Polish Cardiac Society

INTRODUCTION

The coronavirus disease 2019 (COVID-19) pandemic resulted in an urgent need to reorganize the work of echocardiography laboratories in order to ensure the safety of patients and protection of physicians, technicians, and other staff members. In the previous Expert Opinion of the Working Group on Echocardiography of Polish Cardiac Society we provided recommendations for the echocardiographic services, in order to ensure maximum possible safety and efficiency of imagers facing epidemic threat [1].

Restrictions imposed on transthoracic (TTE) and transesophageal (TEE) examinations due to the pandemic resulted in significant limitation of access of patients with cardiovascular diseases to services. Currently, a year after the initial document, there is a need to provide updated information on the current knowledge on the COVID-19 pandemic as well as, perhaps even more importantly, on the potential impact of the vaccination program and growing numbers of convalescents on everyday practice of echocardiographic laboratories. Moreover, with much better knowledge and larger experience in treating COVID-19 patients, and with the introduction of vaccination programs, recommendations for TTE or TEE adopted for epidemic conditions, and health requirements need to be updated. This update is especially appropriate now when a substantial proportion of medical personnel in Poland are vaccinated with two doses of a mRNA vaccine and when, despite the current peak of the pandemic, we must think about the goal of restoring full capacity of echocardiographic laboratories, once the pandemic is under control [2].

For the purpose of this document we define the latter as the low and decreasing number of cases; the number of positive tests/number of all tests below 5%; contact tracing system is active and fully operational; at least 70% of personnel and general adult population are vaccinated; no new viral strains escaping from acquired immunity are detected.

Importantly, while certain regulators accept fully vaccinated people gathering indoors without wearing masks, we propose that until the end of the pandemic also vaccinated personnel and patients should wear masks during echocardiographic examinations, both in the in-patient and out-patient settings [3]. This recommendation may change as knowledge about the efficacy of vaccination programs expands.

COVID-19 AND CARDIOVASCULAR DISEASE

The COVID-19 pandemic has numerous cardiovascular implications. Firstly, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) may adversely affect the cardiovascular system of infected patients. The proposed underlying pathophysiological mechanisms include hypoxemia, systemic inflammatory response, hypercoagulability, sympathetic stimulation, direct myocardial and vascular infection and myocyte necrosis. Myocardial injury detected by elevated cardiac biomarkers has been observed in 5% to 38% of hospitalized patients, depending on the criteria used. The most frequently described clinical manifestations of cardiovascular involvement include thromboembolism, arrhythmia, myocarditis, acute coronary syndrome, stress cardiomyopathy and heart failure, but the autopsy data suggest that their incidence may be underestimated [4, 5].

Secondly, one should consider adverse cardiovascular effects of drugs prescribed to treat SARS-CoV-2 and post-viral complications, such as pediatric inflammatory multisystem syndrome. Thirdly, pre-existing cardiovascular diseases are the most common comorbidities in infected patients, with hypertension being the most common one. Of note, both cardiac involvement during SARS-CoV-2 infection and preexisting cardiovascular disorders have been shown to be associated with more severe clinical course of COVID-19 and worse prognosis [6].

ACUTE AND LONG-TERM ECHOCARDIOGRAPHIC FINDINGS IN COVID-19 PATIENTS

COVID-19 is a primarily respiratory infection, with common cardiovascular involvement in severe and critical stages of the disease. Echocardiography represents a versatile diagnostic procedure requiring high level of physician-patient interaction, thus posing a risk for infection. This is especially true for transesophageal studies (also most of stress-echo protocols) which are highly aerosol-generating. The policies of use of TTE in COVID-19 healthcare facilities may vary, but the general indication depends on potential impact of findings upon the management of the patient. Both the evidence of cardiovascular involvement during COVID-19 and precise identification of preexisting cardiovascular conditions may contribute to proper management.

Cardiac dysfunction present prior to the SARS-CoV-2 infection can influence the findings, the clinical course of the infection and the prognosis. Therefore, prior to interpretation of the echocardiographic study, an attempt should be made to determine the preexisting cardiac pathology based on the history and available medical records. Symptoms reported during COVID-19 are nonspecific and can result from other organ damage (i.e., lungs, skeletal muscles, kidneys, nervous system, etc.) or from psychological reasons and stress. Therefore, TTE is crucial to detect and differentiate the cardiac and non-cardiac reasons.

The most important cardiac complications of COVID-19 are myocardial injury and cardiovascular thrombosis [7–9]. Myocardial damage is more frequently found in patients with abnormal electrocardiogram or elevated biomarkers (troponin or natriuretic peptides) and these patients should undergo TTE. It is probably more common in hospitalized patients. Nearly half of patients with elevated troponins had at least moderate left ventricular (LV) dysfunction, which was associated with doubled risk of death, comparing to patients with no LV wall motion abnormalities. Myocardial function impairment can be reversible or irreversible. Both left and right ventricular dilatation are associated with poor prognosis. Global or regional myocardial injury visible on echocardiography can be detected in up to 25% of hospitalized patients with COVID-19 and is associated with an increased risk of mortality. Intracardiac clots forming on the damaged cardiac endothelium or migrating from the veins to the pulmonary circulation may be observed (Figure 1).

Pericardial or pleural fluid initially reported as rare in COVID-19 patients, has been recently more frequently described in the context of perimyocarditis [10]. In a study at least mild pericardial effusion was found in 7.2% of severely ill patients with myocardial dysfunction [10]. Cardiac tamponade was also reported in a case study [11].

Most common clinical indications for TTE in the acute COVID-19 are hemodynamic assessment (including fluid status), rising cardiac biomarkers, suspicion of pulmonary embolism, acute coronary syndrome, heart failure, or myocarditis [13]. Other indications include history of cardiac disease, suspicion of endocarditis, and evaluation for cardioembolic source of stroke [14]. In practice, many TTE tests are performed in mechanically ventilated subjects hospitalized due to COVID-19. Thus, in patients with clinical deterioration, TTE exams (optionally combined with lung ultrasound [LUS] tests and 4-point venous compression ultrasound [CUS]) may be needed to document myocardial dysfunction or other complications indicating the need for early intensive treatment. It is particularly important in patients with preexisting heart disease or comorbidities. In most patients simplified protocols are preferred to limit personnel exposure to infected patients. Advanced analysis (e.g., strain imaging), if considered essential, can be performed offline to document subtle ventricular dysfunction.

Recovery of the myocardial damage is variable and long-term sequelae may persist, depending on the baseline status, the severity of viral or inflammatory damage, and the speed and completeness of recovery phase.

Some patients may never recover completely following acute COVID-19. Symptom-free convalescents do not require cardiac imaging, however lack of complete recovery is an indication for the control TTE. In most cases, echocardiography should be performed when there is no further risk of infecting the personnel. Subclinical myocarditis may be of some concern, especially in patients with innate or acquired immune deficits. As data is conflicting further studies are needed to assess the long-term cardiac consequences of SARS-CoV-2 infection.

Last but not least, abnormalities detected in COVID-19 or post-COVID-19 patients include also the results of delayed cardiac care, like myocardial infarction (untreated or treated late or without reperfusion) that can be complicated with classical mechanical complications [12]. Delayed diagnosis due to the pandemic can result in late detection of decompensated chronic conditions, such as valvular disease (predominantly aortic stenosis, mitral and tricuspid regurgitations) or heart failure of any origin.

LUNG ULTRASOUND

Radiography and computed tomography remain the mainstay for evaluation of COVID-19 pneumonia. Although LUS has proven its diagnostic value and capability in COVID-19 patients, it lacks standardization and suffers from the absence of quantitative approaches. Importantly, LUS findings are nonspecific for COVID-19. A diffuse pattern of B-lines, irregular pleural lines, and subpleural consolidations affecting mainly the lower lobe and posterior lung segments, which show a bilateral, patchy, and peripheral pattern, represent typical LUS findings in COVID‐19 pneumonia [15].

There is still great variability regarding the optimal technique, including different proposed scanning protocols and scoring algorithms. For this reason, Italian texperts proposed standardization for international use of LUS for the management of patients with COVID‐19 [16]. Fourteen standard areas (7 areas per lung) are suggested for scanning in each patient, using landmarks on chest anatomic lines (3 posterior — paravertebral line; 2 lateral — mid-axillary line; 2 anterior — mid-clavicular line). In the absence of a standardized score for COVID-19 patients, Italian experts proposed to use a previously validated scoring system. The final score is obtained by summing up the scores of each area. Some studies suggested that a higher LUS score indicating a poorly aerated lung and a more severe pulmonary involvement may thus be useful for predicting adverse outcomes in patients with COVID-19, and important for risk stratification in COVID-19 patients [17]. Canadian experts described the 6-zone (3 zones per lung) protocol aimed at speeding up and simplifying the examination dedicated for cardiologists (posterior basal, lateral and anterior — for each lung), and we propose to use this protocol (Figure 2) [18].

According to the experience and reports of many groups throughout the world, even with a rather empirical approach, LUS seems to be an useful, radiation-free, bedside method which can be applied after the TTE examination. Current enthusiasm for LUS should lead to high-quality controlled studies which can determine its real utility among COVID-19 patients.

Despite the fact that currently there is no clear data showing that LUS improves outcomes, the COVID-19 era poses unprecedented challenges, but also learning opportunities. Web based ultrasound simulators are available for training (Figure 3) [19].

COLLATERAL DAMAGE TO CARDIOVASCULAR HEALTHCARE

The COVID-19 pandemic has significantly impacted healthcare systems around the world, including echocardiography laboratories. A large portion of available resources has been repurposed towards fighting the pandemic. The remaining available cardiology departments and personnel have been often advised to defer scheduled elective procedures, especially those associated with increased risk of SARS-CoV-2 transmission, such as transesophageal echocardiography [1]. Moreover, patients’ fear of infection and the desire to not overburden the healthcare system have also been keeping them from seeking medical care in case of symptoms unrelated to COVID-19, both in urgent and chronic clinical scenarios [20]. Thus, the COVID-19 pandemic has adversely influenced the care and treatment of cardiovascular patients. The full scope and the long-term consequences of this “collateral damage” are yet to be determined, but the data published so far is already alarming, even though the exact extent of observed detrimental effects varies greatly between reports and affected regions. To date, most studies have concentrated on patients with acute myocardial infarction, indicating lower number of their hospital admissions, higher rate of delayed presentations and a significant reduction in coronary angiographies and percutaneous coronary interventions [21, 22]. However, the hospitalizations for heart failure and cardiac arrhythmias, as well as the cumulative number of hospitalizations for acute and chronic cardiovascular conditions have also markedly decreased during the pandemic [23]. Similarly, a substantial drop in the number of outpatient cardiovascular visits has been reported, although it was partly compensated using telehealth [24]. There also has been a considerable reduction in the number of inpatient and outpatient cardiac procedures and investigations [25, 26].

With regard to echocardiography, preliminary analysis of the survey study performed by the Working Group on Echocardiography of the Polish Cardiac Society suggests that the vast majority of centers have been performing significantly fewer examinations than before the pandemic. The drop has been most evident in TEE, in case of which indications for examination have been often reevaluated and narrowed, and a negative COVID-19 test prior to the procedure was required in the laboratories on non-COVID-19 wards. Most of the laboratories have also reported temporary shortages of staff due to COVID-19, quarantine or dispatching them to work in infectious disease departments. As a result, there even have been instances of temporary cessation of any activities. Moreover, a significant number of centers have been at least partially transformed to diagnose and treat COVID-19 patients. Thus, waiting times for both scheduled echocardiographic examinations and elective surgical and percutaneous procedures recommended for patients after echocardiographic examinations have been extended. Therefore, it comes as no surprise that a significant increase in out-of-hospital cardiac arrests and deaths was noted in the affected regions [27–29], and was accompanied by substantial overall excess mortality, which could not be explained by the number of COVID-19 fatalities [30, 31]. All these data call for urgent reintroduction of widely available echocardiography services.

REACTIVATION OF ECHOCARDIOGRAPHIC LABORATORIES

Despite the current peak of the pandemic, there is an urgent need for restoring full capacity of echocardiographic laboratories. It may be feasible in near future, as an increasing number of staff and patients are already either vaccinated or have recovered from COVID-19. Distinct separation of laboratories providing services for COVID-19 infected or COVID-free patients should be instituted, if logistically possible. Echocardiographic laboratories that are not directly involved in the care of COVID-19 patients should attempt to return to their full pre-pandemic activity and perform all study types, according to standard protocols, as well as try to alleviate collateral damage to the services caused by COVID-19. Waiting lists for echocardiographic examinations should be verified as prolonged waiting period for echocardiography examination has become a serious issue. Urgent patients for whom further delays may be life-threatening should be placed on a priority list (e.g., decompensated heart failure, severe aortic stenosis).

Although access to echocardiographic services should be urgently facilitated, all essential restrictive precautions and safety measures should be preserved, to minimize the risk of infecting other patients and medical personnel at the peak of the pandemic. Decrease of the number of cases following an effective vaccination program may however enable to modify some protective measures or get away from them in the future. It is therefore strongly recommended that every member of an echo team be vaccinated against SARS-CoV-2.

Echocardiographic protocols should be differentiated according to the location of the echocardiographic laboratory (in-patient vs outpatient, COVID-19 vs non-COVID-19 services) and the epidemiologic status of the patients examined. When separation of COVID-19 and non-COVID-19 patients is impossible for logistic reasons, patient management should include isolation of infectious patients and case grouping, possibly at the end of the day, to ensure appropriate personnel protection and disinfection of the facilities. For recommendations see also Table 1

, Figure 4.

Recommendations for non-COVID-19 in-patient echocardiographic services

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