The 2019 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has dramatically changed the sports landscape, compelling sports medical providers to adapt to evolving scientific discoveries and adopt ever-changing guidelines that protect our athletes, ourselves, and our staff. Much of the discussion on return to play during the COVID pandemic revolves around preventing infection transmission and identifying return to play guidelines. However, burgeoning knowledge of the cardiac effects of SARS-CoV-2 compels the sports medicine community to be poised to manage cardiac complications in athletes (^1–5). Of significant concern for athlete safety is the potential development of myocarditis and subsequent malignant arrhythmias associated with SARS-CoV-2 infection. While the exact prevalence of myocarditis is unknown, cardiac arrhythmia is the second most common complication from SARS-CoV-2 infection and studies have suggested up to 36% of patients with SARS-CoV-2 infection have myocardial injury (^1,2,4,6–8). The clinical significance of this in athletes as they return to play has yet to be determined. However, as athletes return to play, there is a high potential for increased prevalence of malignant arrhythmias on the sidelines during the SARS-CoV-2 era and its recovery. It is critical for sideline providers to understand the pathophysiology of the virus so as to appreciate the potential malignant arrhythmias due to SARS-CoV-2.

The SARS-CoV-2 virus binds with a high affinity to the angiotensin-converting enzyme (ACE-2) receptor, which provides viral entry into the human cells (⁹). ACE-2 receptors are highly expressed in the intestine, endothelial cells, lungs, and the heart, which account for the symptom profile that is seen in the setting of active infection. The high prevalence of ACE-2 receptors in the myocardium precipitates SARS-CoV-2 infection to cause various types of myocardial injury, including myocardial infarction, heart failure, ventricular arrhythmias, and myocarditis. For our young healthy athletes with minimal comorbidities, of greatest concern is the development of myocarditis. While the relationship between SARS-CoV-2 and myocarditis is well documented, the exact mechanism is not yet fully elucidated (^1,2,4–10). Myocarditis is the pathologic inflammation of the myocyte with associated infiltration of inflammatory cells into the myocardium (¹¹). It is proposed that SARS-CoV-2 binds to the ACE-2 receptor on myocytes, causing direct myocardial death, which stimulates an innate immune response. The inflammatory cells of our immune response recognize our own myocyte proteins, which are released when the cell lyses, similar to that of a viral antigen, resulting in molecular mimicry and chronic inflammation to the myocardium from infiltration of mononuclear cells (^4,12). Myocyte necrosis and chronic inflammation of the myocardium lead to fibrosis and adverse structural and electrical cardiac remodeling predisposing athletes to the development of malignant arrhythmias and heart failure (^12,13).

The concept of myocarditis resulting in sudden cardiac arrest in athletes is not novel. Myocarditis occurs in 1% to 5% of all patients with acute viral infection and is listed within the top 3 of common causes of sudden cardiac death in athletes (^5,12,14). Myocardial inflammation, pathologic myocardial remodeling, and cytokine release create a proarrhythmic environment that perpetuates the development of ventricular tachycardia, ventricular fibrillation, conduction blocks resulting in bradycardia, atrial fibrillation, and tachyarrhythmia (^4,7,9,11,13). Studies have shown that even in patients with minimal symptoms from infection by SARS-CoV-2, there are MRI findings of cardiac inflammation (¹⁰). Unfortunately, the exact duration of the proarrythmic influence on the myocardium from myocarditis and SARS-CoV-2 is unknown (⁷).

Recognizing that there is a strong correlation between SARS-CoV-2 infection and myocarditis, and that myocarditis has the potential to produce malignant arrhythmias, highlights how important it is for sideline provider to revisit their emergency action plans (EAPs). Providers must prepare to respond to stable tachyarrhythmia, bradycardia, and sudden cardiac arrest on the sidelines with the added complication of using appropriate precautions to limit viral exposure. In the setting of sudden cardiac arrest, defined as malfunction or cessation of the electrical mechanical activity of the heart, time is of the essence (¹⁵). Meaningful neurologic outcomes and return to spontaneous circulation are enhanced if high-quality compressions and the administration of an automated external defibrillator (AED) are performed within 4 min of the athlete's collapse (¹⁵). The most common arrhythmia resulting in sudden cardiac death in athletes is ventricular fibrillation (¹⁵). Sustained ventricular tachycardia is the most common ventricular arrhythmia due to scar-related reentry as seen in myocarditis, but this can quickly degenerate into ventricular fibrillation (¹⁶). Ventricular fibrillation results in a nonperfusing mechanical activity of the ventricle, and appropriate perfusion to the coronary arteries and brain is only accomplished through immediate compressions. Defibrillation by an AED is the ultimate treatment by shocking the fatal cardiac rhythm back into a perfusing rhythm. Providers must be automated in their response and efficient in their approach to the collapsed athlete to optimize outcomes. Unfortunately, SARS-CoV-2 creates a hurdle to the timely deployment of Advanced Cardiac Life Support because of the need to wear personal protective equipment (PPE), which minimizes exposure to modified droplets and maintain safety precautions for medical providers and bystanders.

A review of the most recent American Heart Association recommendations and National EMS protocols suggest that the algorithmic approach to a collapsed athlete should be the following: 1) protect yourself, 2) modify jaw thrust, 3) take control, 4) carotid pulse, 5) compressions, and 6) AED.

Step 1: Protect Yourself: Modified Droplet Personal Protective Gear

An athlete collapsing in the field of play creates an emotionally charged environment, and our natural reaction is to immediately run to the athlete to provide care. However, we must go against our instincts and first protect ourselves by donning modified droplet PPE. Modified droplet PPE includes an N95 mask, eye protection, and gloves (³). While the differential for a collapsed athlete includes head trauma, resulting in loss of consciousness; cervical spine injury; or cardiac collapse; in an unwitnessed event, collapse should be assumed to be due to a cardiovascular cause. The World Health Organization has listed cardiopulmonary resuscitation (CPR) as an aerosolizing procedure, which may transmit infection because of the changes in thoracic pressure as occurs with chest compressions (³). Therefore, to protect the caregiver from becoming infected, providers should don modified droplet PPE prior to responding to a collapsed athlete.

Step 2: Modified Jaw Thrust

Trying to determine if an athlete collapsed because of malignant arrhythmia and cardiac arrest can actually be very difficult. Basic life support teaches us to arouse the patient and look for breathing; however, this may be difficult in a helmeted athlete who collapses face down. Also, in more than 50% of sudden cardiac arrest (SCA) cases, athletes demonstrated myoclonic jerks, seizure-like activity, or abdominal movements or gasps after collapsing (¹⁷). Agonal respirations or the myoclonic jerks associated with global tissue hypoxia cause confusion as to the etiology of the collapse and can significantly delay appropriate care in the setting of cardiovascular collapse (¹⁷). The modified jaw thrust is a proven method used by anesthesiologists to assess sedation and the airway motor reflex (Fig. 1) (¹⁸). This simple maneuver can be performed in supine helmeted athletes and allows for a quick assessment of a patient's consciousness. It is performed by placing two fingers just superior and posterior to the angle of the mandible while pushing in and forward. Typically, an unconscious athlete will have airway obstruction because of their tongue, mouth guard, and/or the loss of pharyngeal tone (¹⁸). The modified jaw thrust allows for opening of the airway and passive oxygenation. In young healthy athletes, this can prolong the hemoglobin desaturation curve and provide greater than 8 min until the oxygen desaturation curve falls below 90% (¹⁹). As a first step, the modified jaw thrust should be performed as a pain generator to assess for airway compromise. If an athlete does not clinch their eyes or provide some purposeful movement in response to a jaw thrust, there should be concern about their level of consciousness and providers need to immediately progress to the next step in the algorithm. If there are two providers who have appropriate modified droplet PPE, one provider can continue to hold the modified jaw thrust as the other provider continues down the algorithm, but should place a surgical mask over their mouths to minimize aerosolization of the virus during chest compressions (Fig. 2).

Step 3: Carotid Pulse

If an athlete does not respond with purposeful movements or respirations to a modified jaw thrust, providers should immediately feel for a carotid pulse. The carotid pulse can be quickly palpated from the modified jaw thrust position by sliding your fingers down the anterior aspect of the sternocleidomastoid muscle. The pulse should be felt at the level of the cricoid membrane just posterior to the larynx. In the setting of hypotension, the carotid pulse is the last pulse to be lost and correlates to a systolic blood pressure of 60 to 70 mm Hg (²⁰). The accuracy of carotid pulse palpation even in medical providers is 80% sensitive so after 10 s, if no pulse is appreciated, the patient should be assumed to be pulseless, and the care team should progress immediately to the next step in the algorithm (²¹).

Step 4: Take Control of the Situation and Lead by Following your EAP

At this point in the algorithm, it is critical to take control of the situation and provide leadership to minimize exposure to bystanders and provide timely lifesaving treatment. Prior to any competitive event, medical providers should identify three to four people who will safely and effectively provide care for a collapsed athlete. These roles are as follows: one to two code responders, AED runner, and scene control. A hand signal should be identified, which can signal all providers on site that a cardiac arrest has occurred, at which point the identified personnel will perform their predetermined roles for the medical code. The number of code responders who will deliver medical care should be limited, and each must wear full modified droplet PPE. To help reduce cognitive burden during an event, providers should have premade modified droplet PPE bags consisting of an N95, goggles, and gloves. These should be attached to the sideline AED and within a provider's sideline kit to minimize delay (²²). Ideally, a code responder is someone who will run onto the field for the initial assessment of the athlete while wearing modified droplet PPE. Recognizing that provider fatigue occurs within 3 min of compressions, ideally two medical providers should be identified as code responders (²³). One person provides compressions, and the other holds a modified jaw thrust after a surgical mask has been applied over the athlete's mouth (²³). These roles can be switched after the first shock is delivered or after 2 min of compressions to optimize the quality of compressions delivered. A previously identified AED runner will immediately grab the AED ideally from the sideline, at the first indication of a collapsed athlete, and deliver it to the code providers. The AED runner does not need to be medically trained and can utilize a surgical mask only as long as they deliver the AED and immediately move back from the code. Scene control will be tasked with calling 911 and will direct all bystanders away from the medical code to minimize bystander exposure. All bystanders need to be moved away from the patient receiving CPR, as this is an aerosol-generating procedure, and if positive pressure ventilation or intubation occurs, viral particles can remain suspended in the air with a half-life of ≈1 hour (²²). The scene control provider also will monitor and enforce appropriate PPE utilization of the medical providers to protect the personnel.

Step 5: Compressions

Numerous studies have shown that compression-only CPR is superior to conventional CPR (^22,24,25). A code responder who is dressed in modified droplet PPE must, without delay, start compressions on a collapsed athlete and aim for consistent compressions and minimize interruptions. High-quality compressions performed at a depth of 5 cm with a goal of 100 to 120 compressions per minute provides 30% to 40% of normal cardiac output (¹⁵). Consistent and quality compressions can achieve cerebral perfusion pressure as high as 60% of coronary artery perfusion pressure. Therefore myocardial oxygen supply increases after just five to seven compressions but quickly drops off with interruptions in chest compressions. This highlights the need for immediate, high quality, consistent CPR (¹⁵). Studies have shown that having providers perform compression to the tune of “Stayin' Alive” can improve the quality of compression (²⁶). As stated above, compression-only CPR shows improved outcomes, but quickly leads to provider fatigue, thus having two providers designated to provide care can optimize compression delivery (²⁴).

Step 6: AED

The most common arrhythmia in SCA in athletes is ventricular fibrillation. Myocarditis and cardiac complications from SARS-CoV-2 infection are associated with nonperfusing ventricular arrhythmias. Thus, the single most important thing we can do as medical providers on the sidelines is to assure that an AED is readily accessible to defibrillate the heart back into a perfusing rhythm. To optimize outcomes, we must assure that we can implement an AED within 4 min of an athlete's collapse to convert them to a perfusing rhythm (^15,17,27). If prompt CPR and defibrillation are provided, SCA is survived 89% of the time in athletes (¹⁷). However, it is important to remember during this pandemic that AED utilization alone also is considered an aerosolizing procedure because of the belief that tonic muscle spasms caused by defibrillation are thought to produce airflow. Thus, it is important that providers are adequately protected with modified droplet PPE prior to defibrillation (³). With the potential for malignant arrhythmias due to SARS-CoV-2 infection, an AED needs to be on the sidelines so it can be implemented within 4 min of athlete collapse (see Fig. 1).

Sideline providers also should be prepared to recognize and manage tachyarrhythmia and bradycardia because of the structural and electrical remodeling of the heart that occurs during SARS-CoV-2 myocarditis (^2,7,28,29). Other rhythms, such as atrial fibrillation and SVT, are seen with viral induced cardiac injury (³⁰). If an athlete develops palpitations on the sideline, providers should remove the athlete from play and assess for stability. Unstable symptoms include syncope, persistent chest pain, and signs of poor perfusion. In this situation, EMS needs be immediately called, the athlete placed supine, and the provider should don modified droplet PPE. An AED should be called for but not used unless the athlete decompensates into a pulseless rhythm. In most situations, athletes will be stable with symptoms of shortness of breath, palpitations, mild chest pain, and lightheadedness. In this case, vagal maneuvers can be attempted because these can terminate some arrhythmias. All Valsalva maneuvers should be performed with the medical provider in modified droplet PPE. Vagal maneuvers work to transiently increase the intrathoracic pressure and aortic pressure, thus causing a vagal response, which stimulates bradycardia at the level of the atrioventricular node (³¹). There are many ways to perform vagal maneuvers. The easiest includes breathing against a closed glottis, such as blowing against a syringe for 15 s in the supine position (³¹). The modified Valsalva maneuver is a very effective vagal maneuver, with a success rate of 40%, double that of standard Valsalva (²⁷). The modified Valsalva is performed with the athlete initially in a seated upright position. The athlete then blows against a syringe for 15 s while their head is laid flat in a supine position and their legs are lifted in an extended position, 45 to 90 degrees off the ground (²⁷). If this successfully terminates the arrhythmia, the athlete still needs be seen by a medical provider prior to being cleared to play. Any persistent tachyarrhythmia should be transported to the emergency department for further evaluation and work-up.

In the setting of myocarditis, inflammatory injury to the sinus and/or atrioventricular nodes can precipitate bradycardia and heart block (^7,13). These athletes are most likely to present with shortness of breath, exercise intolerance, and syncope (¹³). If, in the setting of these symptoms, the athlete is found to have a heart rate less than 60 bpm, further medical work-up is required prior to return to play. If an athlete develops symptomatic bradycardia on the sidelines, they should be placed in the supine position to improve cerebral blood flow, and EMS should be called. The medical provider should don PPE and prepare themselves to respond to SCA should the bradycardia decompensate into a nonperfusing rhythm.

The clinical significance of the effects of SARS-CoV-2 on the athlete heart is yet to be fully understood. However, by being prepared to quickly recognize and respond to cardiovascular collapse and implement an AED, survival can be enhanced. To protect our athletes and all medical providers, EAPs should be revised and practiced to include the modified approach to SCA in the era of SARS-CoV-2 and should include the six steps outlined.