Cardiology

Electrocardiographic manifestations of COVID-19

a b s t r a c t

Introduction: Coronavirus disease of 2019 (COVID-19) is a lower respiratory tract infection caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). This disease can impact the cardiovascular system and lead to abnormal electrocardiographic findings. Emergency clinicians must be aware of the ECG manifestations of COVID-19.

Objective: This narrative review outlines the pathophysiology and electrocardiographic findings associated with COVID-19.

Discussion: COVID-19 is a potentially critical illness associated with a variety of ECG abnormalities, with up to 90% of critically ill patients demonstrating at least one abnormality. The ECG abnormalities in COVID-19 may be due to cytokine storm, hypoxic injury, electrolyte abnormalities, Plaque rupture, Coronary spasm, microthrombi, or di- rect endothelial or myocardial injury. While sinus tachycardia is the most common abnormality, others include supraventricular tachycardias such as atrial fibrillation or flutter, ventricular arrhythmias such as ventricular tachycardia or fibrillation, various bradycardias, interval and axis changes, and ST segment and T wave changes. Several ECG presentations are associated with poor outcome, including atrial fibrillation, QT interval prolonga- tion, ST segment and T wave changes, and ventricular tachycardia/fibrillation.

Conclusions: This review summarizes the relevant ECG findings associated with COVID-19. Knowledge of these findings in COVID-19-related Electrocardiographic presentations may assist emergency clinicians in the evalua- tion and management of potentially infected and infected patients.

Published by Elsevier Inc.

  1. Introduction

In December 2019, an outbreak of a lower respiratory tract dis- ease caused by the severe acute respiratory syndrome coronavirus 2 was first reported in Wuhan, China [1]. This was sub- sequently termed coronavirus disease of 2019 (COVID-19) by the World Health Organization and has been declared a global pandemic, infecting millions worldwide [2]. While much of the focus has been on the respiratory system, COVID-19 can also cause a variety of car- diac complications [3-8] and a range of electrocardiographic abnor- malities. Studies have described COVID-19 related myocarditis [9-12], cardiac tamponade [13], Brugada-like pattern [14], transient ST segment elevations [15], as well as medication-induced cardiac

* Corresponding author at: 3841 Roger Brooke Dr, Fort Sam, Houston, TX 78234, United States of America.

E-mail addresses: [email protected] (B. Long), [email protected] (W.J. Brady).

dysrhythmias [16-18]. Myocardial involvement in COVID-19 has been associated with poor outcomes, especially in myocardial injury which occurs in 22-44% of critical or severe cases [4-8]. Therefore, it is crucial that the emergency clinician recognize the electrocardio- graphic (ECG) manifestations of COVID-19 [19,20]. This narrative review provides a discussion of the various electrocardiographic presentations encountered in the COVID-19-infected patient.

  1. Methods

This narrative review outlines the underlying pathophysiology and ECG manifestations of COVID-19. A literature review of PubMed and Google Scholar databases was performed for articles up to October 23, 2020, using the keywords ‘COVID’ OR ‘SARS-CoV-2’ OR ‘coronavirus’ OR ‘SARS’ AND ‘ECG’ OR ‘EKG’ OR ‘electrocardiogram’ for this narrative review. The authors included case reports and series, retrospective and prospective studies, systematic reviews and meta-analyses, clinical guidelines, and other narrative reviews. Commentaries and letters were

https://doi.org/10.1016/j.ajem.2020.12.060 0735-6757/Published by Elsevier Inc.

also included. The literature search was restricted to studies published or translated into English. The initial literature search revealed over 200 articles, with the majority of these articles consisting of case reports. Authors reviewed all relevant articles and decided which studies to in- clude for the review by consensus, with focus on emergency medicine-relevant articles, including guidelines. A total of 80 resources were selected for inclusion in this review.

  1. Discussion
    1. Pathophysiology

SARS-CoV-2 is an RNA virus that utilizes the angiotensin converting enzyme 2 (ACE2) receptor to enter cells by receptor-mediated endocy- tosis [21,22]. Compared to SARS-CoV-1, SARS-CoV-2 displays tighter li- gand binding to the ACE2 receptor, located in several tissues, including the lungs, heart, kidneys, gastrointestinal tract, vasculature, and skin [3,23]. Respiratory symptoms associated with COVID-19 primarily come from ACE2 expression in the type 2 lung alveolar cells; however, over 7.5% of myocardial cells also express the ACE2 receptor [24-28]. While the presence of the ACE2 receptor can account for cardiac injury, the etiology of the Cardiovascular effects that may occur in COVID-19 is likely multifactorial. The virus can cause a hyperinflammatory state, leading to Vascular inflammation, cardiac injury, plaque instability, hy- percoagulability, and myocardial depression [25-28]. Pathologic data re- veal cardiac interstitial inflammatory infiltration and necrosis, with blood vessels demonstrating microthrombi and inflammation [26,29- 31]. COVID-19 may also result in cytokine storm, sepsis, disseminated intravascular coagulation, and ultimately Multiorgan dysfunction and death. Myocardial abnormalities with ECG changes in COVID-19 may be due to this cytokine storm, hypoxic injury, electrolyte abnormalities, plaque rupture, coronary spasm, and microthrombi, as well as direct en- dothelial or myocardial injury [3-8,11,32].

There are a variety of arrhythmias and ECG abnormalities that may

ventricular dysrhythmias:”>occur in COVID-19 [3,4,19,20]. Interestingly, the interpretation of the ECG, with either dysrhythmia recognition or identification of a concerning morphologic issue, is unchanged from the non-COVID-19 patient; in contrast, the context of the patient presentation and thus the clinical impact of the ECG findings has significantly changed. ECG abnormalities are common, present in 93% of hospitalized critically ill patients in one study [32]. Palpitations, likely reflective of dysrhythmia, may be the initial presenting symptom in approximately 7% of patients, and one study suggests 17% of patients in the general cohort and 44% of patients in the intensive care unit (ICU) setting experience dysrhyth- mias [3,4,19,20,33]. Another study reported a 9.6% rate of dysrhythmias [34]. Arrhythmias and ECG abnormalities are more common in critically ill patients [33,35], which may occur in 33-93% of these cases [36,37], and they are also associated with increased risk of in-hospital mortality (odds ratio [OR]1.95) and need for mechanical ventilation [38]. A study of 1258 patients found atrial fibrillation/flutter (OR 2.5), right ventricu- lar (RV) strain (OR 2.7), and ST segment abnormalities (OR 2.4) to be as- sociated with increased risk of mechanical ventilation and death [19]. Emergency clinicians should note that RV strain electrocardiographi- cally presents with ST segment depression and T wave inversion in the right to mid-precordial (leads V1-V4) and the inferior leads (leads II, III, and aVF). Of the inferior leads, lead III frequently demonstrates the most obvious findings due to it direct imaging of the right ventricu- lar muscle mass. Over 8% of deaths may be due to dysrhythmias in the setting of COVID-19 [39].

    1. Supraventricular tachycardias (SVT)

Sinus tachycardia is the most common supraventricular tachycardia encountered in the ill COVID-19 patient, resulting from the usual causes, including hypovolemia, hypoperfusion, hypoxia, elevated body temper- ature, pain, and anxiety. After sinus tachycardia, atrial fibrillation (Fig. 1)

is the next most commonly seen SVT [40-42]; atrial fibrillation can pres- ent in a number of fashions, including new-onset, recurrence of a pre- existing dysrhythmia, and persistence of permanent atrial fibrillation with new rapid ventricular response. In the majority of patients with significant COVID-19 infection and atrial fibrillation, the rate will be quite rapid, thus the ECG will demonstrate atrial fibrillation with rapid ventricular response. Both sinus tachycardia and atrial fibrillation are independent predictors of illness severity, myocardial injury, and poor outcomes in COVID-19 [40]. One study conducted in New York hospitals found atrial fibrillation/flutter was present in 14.3% of patients at admis- sion and occurred in 10.1% of patients during hospitalization [39]. An- other study found atrial fibrillation/flutter to be present in 22% of critically ill patients requiring mechanical ventilation [32]. Atrial fibrilla- tion is more common in patients following an inflammatory insult such as cardiomyopathy from COVID-19 and occurs in up to half of patients admitted to the ICU [41-46]. Two case reports demonstrated the highly variable impact that COVID-19 has on the heart [47,48]; in one case [47], the patient experienced both atrial flutter and atrial fibrillation, eventu- ally reverting to sinus rhythm 48 h later.

There is a paucity of literature evaluating the presence of other types of SVT, such as atrioventricular nodal reentry tachycardia (AVNRT), in COVID-19 patients. In most instances of AVNRT from the pre-COVID-19 era, patients with AVNRT are frequently younger and lack significant acute and chronic cardiorespiratory ailments; this typical AVNRT presentation likely explains the relative paucity of literature on this dysrhythmia in the COVID-19 patient. Refer to Fig. 2 for the ECG of a 19-year-old patient with palpitations and dys- pnea who presented with AVNRT. The patient was appropriately treated with adenosine but experienced persistent dyspnea after un- complicated conversion to sinus tachycardia. Further evaluation re- vealed that she was positive for COVID-19, and she was admitted to the hospital with persistently low oxygen saturations. She ultimately did well and was discharged from the hospital 5 days later, without AVNRT recurrence.

malignant ventricular arrhythmias are a known complication of viral myocarditis and cardiomyopathy, with Ventricular tachycardia and/or ventricular fibrillation (VF) occurring in 1-6% of patients [19,35,36,49-52]. In patients with COVID-19, these arrhythmias may be due to a combination of QT interval prolonging medications, meta- bolic abnormalities, and myocardial inflammation [19,20,46,49-53]. COVID-19 patients with elevated troponin have been shown to have a higher incidence of VT than those with normal troponins [5,44].

VT with a pulse is seen with both monomorphic and polymorphic presentations. Monomorphic ventricular tachycardia (MVT) is the most frequent form of VT seen in the COVID-19 patient, frequently resulting from structural heart disease such as acute coronary syndrome with STEMI, myocardial injury, or myocarditis; patients with pre- existing structural heart disease of many types can provide the substrate for MVT during periods of extreme physiologic stress due to the range of issues encountered in the COVID-19-infected patient. Polymorphic VT (PVT), including the PVT subtype Torsade de pointes, results from func- tional (i.e., non-structural) heart disease and is likely less common; it most often occurs in situations involving medication toxicities, electro- lyte abnormality, and various pro-arrhythmic states (e.g. Brugada syn- drome, long QT syndrome).

Cardiac arrest dysrhythmias include the traditional 4 rhythm sce- narios: the “shockable” (pulseless VT and VF) and “non-shockable” (pulseless electrical activity [PEA] and asystole) dysrhythmias. Spe- cific dysrhythmia diagnosis in the cardiac arrest patient, whether out-of-hospital or hospital-based, is unchanged in the COVID-19 pandemic. During the pandemic, the occurrence of both out-of- hospital cardiac arrest (OHCA) and hospital-based cardiac arrest

Image of Fig. 1

Fig. 1. Atrial fibrillation with rapid ventricular response in a COVID-19-infected 76 year-old female with new-onset atrial fibrillation.

have increased based on recent data [54-58]. A study conducted in Italy found close to a 60% increase in OHCA in 2020 compared to 2019 [54]. A second study in France found a 52% increase in OHCA between Febru- ary and April 2020, compared to 2019 [55]. This unfortunate increased rate of OHCA has also been seen in the United States. For example, in New York City there was a three-fold higher rate of patients undergo- ing resuscitation in the out-of-hospital setting when compared to a similar 2019 pre-pandemic period; the odds ratio (OR) of encountering “non-shockable” dysrhythmias increased significantly with an OR for PEA of 3.50 and an OR for asystole of 1.99 [56]. The mortality rate of pa- tients in cardiac arrest increased in all three studies [54-56]. There are several factors that may contribute to this increased occurrence with more frequent poor outcome, including the COVID-19 infection itself as well as the delays in seeking care related to the pandemic, and lower rates of important bystander care in the pre-arrival period of car- diac arrest management [59].

Patients hospitalized with COVID-19 are at increased risk of cardiac arrest, but the rhythms associated with cardiac arrest vary in the

inpatient population. A study focusing on hospitalized patients in New York City noted that asystole occurred most often, followed by PEA and then pulseless VT/VF [39]. Another study found 9 patients out of 700 experienced cardiac arrest, with only one having a shockable rhythm [57]. A study of 136 Chinese inpatients with COVID-19 compli- cated by cardiac arrest during hospitalization found most arrests were respiratory in origin with non-Shockable rhythms (90% asystole and 4% PEA); only 3% survived to 30 days, with just 1% having intact neuro- logic function [58].

Bradycardias and AVB are less commonly encountered as com- pared to tachydysrhythmias, though they may account for up to 11.8% of cardiac dysrhythmias [60,61]. A case report details a patient with COVID-19 presenting with first-degree atrioventricular block (AVB); during hospitalization, the rhythm transitioned to Mobitz type 1 second-degree AVB with further evolution ultimately to

Image of Fig. 2

Fig. 2. Atrioventricular nodal re-entrant tachycardia in a 19 year-old patient with palpitations and dyspnea who presented with AVNRT. The patient was appropriately treated with adenosine but experienced persistent dyspnea after uncomplicated conversion to sinus tachycardia; further evaluation revealed that she was positive for COVID-19.

third-degree AVB [60]. Other cases describe older patients with mul- tiple cardiac risk factors experiencing progression to high-grade AVB (second-degree type II and third-degree AVB) and/or intra- ventricular conduction block; many of these patients developing these more concerning Conduction abnormalities progressed rapidly to cardiac arrest [10,56,60-64]. Three of these dysrhythmias (Sinus bradycardia, junctional rhythm, idioventricular rhythm) occurred immediately prior to cardiac arrest onset – thus, in these cases, the development of significant bradycardia in the critically ill COVID-19 patient is a marker of risk of impending Cardiovascular collapse [65].

    1. Interval and axis abnormalities

QT interval prolongation may occur in over 13% of patients with COVID-19 infection, and several medications previously used for COVID-19 may prolong the QT interval, including chloroquine, hydroxychloroquine, and azithromycin [66-68]. QT interval prolonga- tion is associated with more critical illness requiring ICU admission, as well as cardiac injury and mortality [61,69]. Left and Right bundle branch blocks may occur in up to 12% of patients at the time of admission or during hospitalization [32,39]. Significant QT interval prolongation may lead to torsade des pointes. Fig. 3 is the ECG of a patient with COVID-19-related myocarditis; the ECG reveals atrial fibrillation with a mean rate of approximately 100 bpm, significant QRS complex widen- ing, Right axis deviation, poor R wave progression, and ST segment ele- vation in the anterolateral leads.

QRS complex axis deviation has been reported, usually involving sit- uations presenting with RV strain; such patients are frequently experiencing acute respiratory failure from multi-lobar pneumonia and/or pulmonary embolus with large Clot burden. Electrocardiograph- ically, these patients present with right axis deviation along with prom- inent R waves in leads V1 and V2 and ST segment depression/T wave inversion in leads II, III, aVF, and V1 to V4 [19]. Fig. 4 shows the inferior and right to mid precordial leads with T wave inversion, indicative of RV strain, in a patient with significant pulmonary embolus.

    1. Morphologic presentations ST segment, T wave, and QRS complex abnormalities

The interpretation of the ECG in the patient with chest pain or a sim- ilar presentation is more challenging in the COVID-19 pandemic. Emer- gency clinicians must consider STEMI, myocardial injury, and myocarditis, as all three clinical entities present with ST segment and T wave abnormalities. COVID-19 infection associated with myocardial injury may demonstrate ST segment deviations (elevation or depres- sion), T wave inversion, and pathologic Q waves [3-5,19,20,69]. One study found ST segment and T wave changes to be the most common abnormality in patients requiring ICU admission, occurring in 40% of pa- tients [70]. Another investigation noted that nonspecific repolarization changes including ST segment and T wave abnormalities were encoun- tered in 41% of patients; reportedly, these findings resulted from myo- cardial injury and are associated with poor outcomes, including increased need for ICU admission, more frequent mechanical ventila- tory support, and increased mortality [32,40]. A case series included 18 patients with COVID-19 infection and ST segment elevation, 10 of which had ST segment elevation at the time of presentation and 8 devel- oped ST segment elevation during hospitalization [71]. Ultimately, acute myocardial infarction (AMI) was diagnosed in 8 patients, while 10 dem- onstrated nonocclusive (i.e., not involving ACS) myocardial injury [71]. Myocarditis and/or myopericarditis associated with COVID-19 infection can demonstrate ECG findings resembling occlusive AMI, such as focal ST segment elevation with reciprocal change [11,72,73].

In the patient with ST segment elevation, the distinction be- tween STEMI, myocardial injury, and myocarditis may not be possi- ble strictly based upon ECG interpretation, which can make this particularly challenging. In the aforementioned case series of ST segment elevation in COVID-19-infected patients [71], STEMI was suggested with focal ST segment elevations, while myocardial in- jury demonstrated diffuse or widespread ST segment elevation. The clinical presentation can provide diagnostic clues and aid in the distinction of STEMI versus myocardial injury/myocarditis. Chest pain is a frequent presentation in the STEMI patient, while it

Image of Fig. 3

Fig. 3. COVID-19-related myocarditis with atrial fibrillation, QRS complex widening, right axis deviation, poor R wave progression, and ST segment elevation.

Image of Fig. 4

Fig. 4. right ventricular strain with T wave inversions in the inferior and right to mid precordial leads.

is less common with myocardial injury/myocarditis which more often involves dyspnea and other symptoms consistent with acute viral infection [1]. echocardiographic findings such as focal wall motion abnormalities with depressed left ventricular function sug- gest STEMI while myocardial injury more often demonstrates nor- mal left ventricular function or diffuse dysfunction [2]. Figs. 3 and 5-8 depict ST segment elevation corresponding to STEMI (Figs. 5 and 6) and myocardial injury (Figs. 7 and 8) in COVID-19-infected patients.

COVID-19 may also result in an unmasked Brugada pattern on ECG in patients with existing pathology. A pseudo-Brugada type 1 pattern is associated with fever and changes in myocardial sodium channels [74-76]. Type 1 is demonstrated by convex ST segment el- evation>2 mm in more than1 lead of V1-V3, followed by a negative T wave.

    1. Electrocardiographic presentations of COVID-19-related pulmonary embolism

PE has been recognized as a presenting issue and/or complication of COVID-19, particularly in patients with severe illness [77-79]. This COVID-19-related predisposition to venous thromboembolism likely occurs via several different mechanisms, including increased Angiotensin II activity and related thrombogenic effects via enhanced coagulation system and Platelet function, cytokine-mediated activation of the coagulation cascade, and a potential direct effect of the viral infec- tion, causing localized Inflammatory process and enhanced focal throm- bosis [77-79].

Sinus tachycardia and/or atrial fibrillation with rapid ventricular re- sponse are commonly encountered in the setting of critical illness, in- cluding PE and COVID-19 [77-80]. Electrocardiographic findings of

Image of Fig. 5

Fig. 5. Inferior STEMI with focal ST segment elevation in leads II, III, and aVF and reciprocal ST segment depression in lead aVL in a COVID-19-infected patient.

Image of Fig. 6

Fig. 6. anterior STEMI with focal ST segment elevation in leads V1 to V4 and reciprocal ST segment depression in the inferior leads in a COVID-19-infected patient.

Image of Fig. 7

Fig. 7. Myocardial injury in a COVID-19-infected patient with diffuse ST segment elevation in the inferior, lateral, and anterior regions. Bedside echocardiography revealed no focal wall motion abnormalities with only mild diffuse hypokinesis.

Image of Fig. 8

Fig. 8. Myocardial injury in a COVID-19-infected patient with diffuse ST segment elevation in the anterior and lateral regions. This patient was initially taken to the cardiac catheterization laboratory with no coronary occlusive lesions noted. The serum troponin values were extremely elevated but in a plateau pattern, rather than the typical rise and fall patient of acute myocardial infarction.

right ventricular strain, as discussed previously, are also frequently en- countered. In a recent review of PE in patients with COVID-19 infection, ECG findings most often involved non-specific abnormalities, including sinus tachycardia and minimal ST segment or T wave changes. More specific findings, suggestive of right ventricular strain, were encoun- tered in only one-third of patients. The classic S1Q3T3 pattern was seen in less than 10% of COVID-19-related PE [77]. Other electrocardio- graphic presentations typical of PE include anterior T wave inversion and right bundle branch block [77,78]. In non-COVID-19 patients with

PE, a normal ECG is encountered in approximately one-fifth of such in- dividuals [80]. In patients with COVID-19 and critical illness, the ECG is rarely entirely normal when PE is diagnosed. While ECG findings may suggest PE, an ECG should not be used to rule in or rule out the disease.

  1. Conclusions

COVID-19 can negatively impact the cardiovascular system and lead to Abnormal ECG findings, which may be due to cytokine storm, hypoxic

injury, electrolyte abnormalities, plaque rupture, coronary spasm, microthrombi, as well as direct endothelial or myocardial injury. The most common finding is sinus tachycardia, but others include SVTs such as atrial fibrillation or flutter, ventricular arrhythmias such as VT or VF, bradycardia, interval and axis changes (QT prolongation), and ST segment and T wave changes. Knowledge of these ECG abnormalities may assist emergency clinicians in evaluation and management of pa- tients with COVID-19.

Declaration of Competing Interest

There are no conflicts of interest for any author.

Acknowledgements

BL, TM, MR, WB, MG, and MS conceived the idea for this manuscript and contributed substantially to the writing and editing of the review. This manuscript did not utilize any grants, and it has not been presented in abstract form. This clinical review has not been published, it is not un- der consideration for publication elsewhere, its publication is approved by all authors and tacitly or explicitly by the responsible authorities where the work was carried out, and that, if accepted, it will not be pub- lished elsewhere in the same form, in English or in any other language, including electronically without the written consent of the copyright- holder. This review does not reflect the views or opinions of the U.S. government, Department of Defense, U.S. Army, U.S. Air Force, or SAUSHEC EM Residency Program.

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