Return to Activity After SARS-CoV-2 Infection: Cardiac Clearance for Children and Adolescents

Abstract

Context:

Sedentary behavior and inability to participate in organized physical activity has negatively affected the physical and mental health of children and adolescents; however, cardiac injury and associated risk for sudden cardiac death with return to activity remains a major concern. Guidelines have been proposed for return to activities; however, these fail to address the needs of younger children and those participating in more casual activities. Guidance is needed for primary care providers to facilitate safe return to everyday activity and sports and to help direct appropriate laboratory, electrocardiographic, and anatomical assessment.

Evidence Acquisition:

Review of computerized databases of available literature on SARS-CoV-2 infection in children and postinfection sequelae, risk factors for sudden cardiac death, and previous return to play recommendations.

Study Design:

Clinical guidelines based on available evidence and expert consensus.

Level of Evidence:

Level 4.

Results:

In this report, we review the literature on return to activity after SARS-CoV-2 infection and propose recommendations for cardiac clearance for children and adolescents. Though severe disease and cardiac injury is less common in children than in adults, it can occur. Several diagnostic modalities such as electrocardiography, echocardiography, cardiac magnetic resonance imaging, and serologic testing may be useful in the cardiac evaluation of children after SARS-CoV-2 infection.

Conclusion:

Gradual return to activity is possible in most children and adolescents after SARS-CoV-2 infection and many of these patients can be cleared by their primary care providers. Providing education on surveillance for cardiopulmonary symptoms with return to sports can avoid unnecessary testing and delays in clearance.

COVID-19 has infected nearly 3 million children and adolescents, or roughly 13% of total cases, in the United States, ¹⁵ prompting broad shutdowns of schools and athletics programs in an effort to curb its spread.^11,39 There is growing evidence that cardiac involvement, including arrhythmia, myocarditis, and ventricular dysfunction, occurs in pediatric patients who either are positive for SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), have an asymptomatic or mild case or who have multisystem inflammatory syndrome in children (MIS-C).^{1,6,8,12,14,27,43,45,49,50} In spite of these cardiac risks, restriction from physical activity poses many long-term risks to both the physical and the mental health of children and adolescents. Several studies have shown increased rates of sedentary behavior and physical deconditioning, worsening dietary habits, and high rates of depression among athletes during the COVID-19 pandemic.^17,36,38,42 Long-term sedentary behavior may also result in an increased risk of obesity and lead to cardiometabolic disorders in children ⁴⁴ and adults.

As cases numbers initially declined and the mechanisms of transmission were understood, restrictions were eased, allowing for some distance to allow for in-person school and athletics programs to resume.^21,39 But with the return of the virus in high numbers and the lingering consequences of cardiac injury, significant concerns have been raised with the goal of clearing these patients for return to sports and physical activity. However, because of limited availability of data, recommendations on return to activities after a positive SARS-CoV-2 test have been largely based on expert opinion.^2,4,18,30,40 The guidelines currently published to address this issue are directed toward older children partaking in competitive or elite sports. No guidelines have been published to address the needs of younger children (<12 years) or those interested in recreational activities such as vigorous chores, gym class, pickup games, and independent physical activity. To date, children between 1 and 12 years appear less likely to experience severe COVID-19 complications and may be less likely to transmit infection but can still develop MIS-C. Older children in early to late adolescence appear to be more vulnerable to the infection and its numerous complications. ¹⁹ In this report, we aim to bridge this gap by providing guidelines for primary care providers in return-to-play decision making for patients 4 to 21 years who have tested positive for SARS-CoV-2. This age range was selected to cover those old enough to participate in physically strenuous activities and those who participate in recreational or competitive sports. The selected age group is particularly important, as many are currently unlikely to qualify for SARS-CoV-2 vaccination because of younger age and/or absence of underlying comorbidities, and no recommendations currently exist in this age group to address regular activities. Children younger than 4 years generally do not participate in organized sports or physical activity and are not covered by the recommendations in this work.

Traditional Preparticipation Clearance for Sports

Clearance for children and adolescents prior to sports participation varies by location but generally includes completing a preparticipation physical evaluation, which includes a complete history and physical examination performed by a primary care provider. ³ The presence of “red flags” such as murmur, exertional chest pain, syncope, near syncope, exercise intolerance, or personal or family histories of cardiac conditions, including arrhythmia syndromes, cardiomyopathy, or sudden cardiac death, typically prompt a referral for cardiology clearance.^33,37 Presence of SARS-CoV-2 infection, with uncertain risk of myocardial involvement, has added another dimension to this clearance process for participation in sports and gym class. Guidelines have been published by the American Academy of Pediatrics and American College of Cardiology for return to sports^2,18; however, these do not specifically address noncompetitive activities, younger children, or the intensity of the desired activities or level of competition. Additionally, as the myocardial injury that occurs after SARs-CoV-2 can result from direct viral injury or, more commonly in children, from the resulting immune response, it is possible that this can occur in both asymptomatic and symptomatic cases, regardless of the severity of the initial infection. For this reason, gradual return to exercise after infection along with ongoing surveillance for cardiac symptoms extending beyond the period of quarantine must be emphasized regardless of initial disease severity. Different sports and activities likely provide different levels of risk in return to play, and the intensity of the desired activity should be considered when deciding on whether to clear a patient.

The severity of initial COVID infection in children can range from asymptomatic to severe, requiring hospitalization for respiratory or circulatory support. When compared with adults, the initial infection in children is generally mild. In addition, a small number of pediatric patients may present with MIS-C without previous evidence of SARS-CoV-2 infection. In children with MIS-C, the risk of cardiac involvement, including coronary aneurysm, myopericarditis, arrhythmias, or decreased ventricular function, has been reported as high as 80%. ²⁴

Assessment of Cardiac Injury and Risk after Sars-Cov-2 Infection

All patients who test positive for SARS-CoV-2 should notify their primary care provider. This communication should include medical documentation of infection and report of symptoms and severity. Regardless of illness severity, patients should be screened for the presence of new-onset cardiac signs and symptoms, including chest pain, exertional intolerance, exertional syncope, tachycardia, or palpitations since their SARS-CoV-2 infection. It is preferred that all children who have had SARS-CoV-2 infection be seen by their primary care provider. When symptoms are present, a thorough history and physical examination are critical in distinguishing true cardiac from more benign etiologies. For example, chest pain may result from coughing and tachycardia while shortness of breath, exertional or orthostatic intolerance, and autonomic dysfunction may be sequelae of sedentary behavior and physical deconditioning. ⁹ A cardiac evaluation should be performed if there is suspicion for true cardiopulmonary symptoms. In many cases, written clearance may be required by the school or the athletic trainer prior to return to sports or gym class, necessitating a formal encounter.

Though long-term data are limited, cardiac injury should remain a clinical concern even after recovery from acute illness, in particular when considering return to physical activity. Murine models have previously demonstrated that exercise can worsen myocardial damage, ²⁹ and up to 20% of cases of sudden death occurring during physical exertion are due to viral myocarditis. ²¹ Despite its relative rarity, the consequences of unrestricted exercise after myocarditis can be catastrophic and must be considered during clearance for physical activity after SARS-CoV-2 infection. While providing clearance for return to sports, it is important to recommend graded return to exercise, including gym class, with surveillance for symptoms such as chest pain, exertional intolerance, exertional syncope, tachycardia, or palpitations.

Electrophysiologic Considerations

Despite having low sensitivity for detection of myocarditis, the electrocardiogram (ECG) is a widely available and low-cost tool that offers valuable and reliable information on the health of the cardiac conduction system. Several conduction system abnormalities have been reported in children with COVID-19 and/or MIS-C, including first-, second-, and third-degree (complete) atrioventricular block, all followed by complete recovery.^7,13,22 Other abnormalities associated with acute SARS-CoV-2 infection include T wave abnormalities ⁴⁹ and prolongation of the corrected QT interval (QTc), even in the absence of known QTc-prolonging medications such as hydroxychloroquine. ²⁸ A standard surface ECG may show changes associated with myocarditis or pericarditis such as Q waves, T wave abnormalities or PR depression, and diffuse ST elevation. The addition of some form of ambulatory cardiac monitoring such as Holter or an event monitor may also increase detection of conduction abnormalities. Additional tools including exercise stress testing may also be used when there is a potential rhythm issue because it can closely recreate physiologic conditions during exercise and when paired with ECG data can help assess patient risk prior to clearance for physical activity. Exercise stress testing is particularly helpful in determining if the patient can be safely cleared for activities, especially when the patient has ventricular dysfunction or myocardial injury on ECG abnormalities.

Imaging Considerations

Several modalities exist with which to assess cardiac involvement and resulting exercise risk. Transthoracic echocardiogram can be useful in the evaluation of global left ventricular function, localized wall motion abnormalities, valvar dysfunction, and pericardial effusions. ⁵ Abnormal findings on echocardiogram are present in more than half of adult patients during COVID-19 hospitalizations. ²⁰ This does not seem to be the case in pediatric patients, with the exception of those with MIS-C, with cardiac involvement present in up to 80% of cases. Abnormalities in this population include left ventricular dysfunction and coronary artery abnormalities, among others. Ventricular strain may also be reduced, even in the absence of clinical symptoms, making it potentially useful in early detection of subclinical myocardial damage.^24,35 Cardiac magnetic resonance imaging (CMRI) is helpful in detection of subclinical injury, with 1 study of adults showing myocardial inflammation independent of illness severity. ²⁵ However, the clinical significance of these findings as well as their relevance to children has yet to be established and must be considered in the context of the broader clinical picture. In an expert consensus statement, Phelan et al ⁴¹ advocates for the use of CMRI in cases where there are persistent clinical concerns or abnormal findings on initial cardiac workup.

Importantly, CMRI findings of myocardial inflammation must be interpreted in the context of known relation to biopsy-proven myocarditis, the gold standard for diagnosis, ³¹ though most providers do not routinely perform biopsies in pediatric patients suspected of having myocarditis ¹⁰ because of concerns with procedural risk and insufficient sampling. Criteria have been published for diagnosing myocarditis using CMRI^25,26 and are often quoted in CMRI studies of COVID patients. Using these criteria, 1 study of 145 competitive student athletes showed that MRI evidence of myocarditis was only present in 1.4% of cases after asymptomatic, mild, or even moderate infection. The study concluded that the utility of MRI as a screening tool for myocarditis was low in the setting of nonsevere infection and normal serum assays. ⁴⁶ Echocardiogram is not easily available in all communities and may not be easily authorized by insurance companies. The access to CMRI is even more limited and adds to a higher resource utilization and cost of care.

Proposed Recommendations for Return to Physical Activity

It is important to recognize that viral transmission during physical activity is possible. Though reinfection with SARS-CoV-2 is rare, it has occurred.^47,48 All precautions must be continued even after recovery from SARS-CoV-2 infection to prevent further spread. These include wearing masks whenever possible, practicing social distancing and hand hygiene, and maximizing outdoor activities to minimize the risk of transmission. The lowest risk activities include those that take place outdoors with minimal close contact such as golf, outdoor track and field, skiing, and tennis. Higher risk activities include those that take place indoors or require close contact, such as basketball, hockey, and wrestling. When possible, school gym classes and recesses should be held outdoors with masks. Those with suspected or known exposures should quarantine as per Centers for Disease Control and Prevention guidelines (10-14 days as of the time of writing) even in the absence of symptoms. Detection of viral RNA by polymerase chain reaction may remain positive well after the infectious period is over ³² ; therefore, a negative test should not be required for return to play. A recent report suggests that natural immunity may persist for up to 8 months after infection but with more variants one cannot be sure, and social distancing recommendations should be followed. ¹⁶ Though antibody testing plays an important epidemiological role, its use in consideration for allowing pediatric patients and decisions for return to play activity should be based on presence of symptoms.

A minimum wait of 10 days after a positive SARS-CoV-2 test or symptom onset in addition to resolution of symptoms for 24 hours is currently recommended prior to return to any activity or sport. Once cleared, return to full activity should be gradual and escalate over a 7-day period as proposed by Elliott et al ²³ and endorsed by the American Academy of Pediatrics, as shown in Table 1. A more gradual approach may be necessary depending on patient tolerance. Those participating in low-intensity activities, such as bowling or golf, may require less time to return to full activity, while those participating in high-intensity sports such as soccer or basketball may require more. Surveillance for symptoms should be continued as these children return to activities, and this must be done by the individual, family, and, where applicable, coaches and trainers. Figure 1 details our recommended approach to clearance for physical activity in those positive for SARS-Cov-2, though it is important to note that this protocol is intended to serve as a framework and care must be individualized to the specific patient in question.

Table 1.

Gradual return to play protocol ^{a , b}

Stage	Period	Maximum Duration	Activity
1	Day 1-2	15 minutes	Light activity, walking, easy exercise bike (<70% HR max)
2	Day 3	30 minutes	Above, plus simple movement drills, may consider jogging (<80% HR max); no resistance training
3	Day 4	45 minutes	Add more complex training (<80% HR max), including light resistance training
4	Day 5-6	60 minutes	Resume normal training activities (<80% HR max)
5	Day 7	As tolerated	Full participation in usual activities at usual intensity, including competition

HR, heart rate.

^aAdapted from Elliott et al. ²³

^bProgressions listed are suggested minimums—stages may and likely should be extended depending on patient tolerance.

Figure 1.

Return to activity. Algorithm for referral and return-to-play decision making. CMRI, cardiac magnetic resonance imaging; ECG, electrocardiogram; MIS-C, multisystem inflammatory syndrome in children.

Asymptomatic/Mild/Moderate Symptoms

Gradual return to activities after a positive SARS-CoV-2 test may begin in asymptomatic individuals after a 10-day quarantine and at least 24 hours after resolution of noncardiac symptoms in the absence of pain- or fever-reducing medications. The patient and family, if applicable, should be educated on self-monitoring for symptoms of cardiac involvement (chest pain, dizziness, shortness of breath, palpitations, syncope, near-syncope) with return to activity after the quarantine period. In the absence of cardiac symptoms or other primary provider concerns the patient may progress through return to play as recommended. If the patient reports symptoms with return to activity at school or during organized sports, he or she should notify school officials or team medical personnel and be evaluated by one’s primary care provider. In cases where there is a concern on history, physical examination, or preparticipation physical evaluation form, a referral to pediatric cardiology should be made. Based on this assessment, the cardiologist should perform a thorough guided history and physical examination and consider further testing as needed, including an ECG, echocardiogram, and Holter or event monitor. If there remain concerns for possible cardiac involvement, stress test and blood work, including high-sensitivity cardiac troponin and N-terminal pro-B type natriuretic peptide, should be obtained. If these are abnormal, or there is still suspicion for cardiac involvement, then CMRI may be indicated. Some organizations may require cardiac testing such as ECG, echocardiogram, or blood work before return to sports after SARS-CoV-2 infection, but these tests should only be ordered if clinically indicated.

Severe Symptoms

These patients should be followed by a cardiologist, even after discharge. It is important to establish outpatient cardiology care and defer decisions regarding physical activity participation pending cardiac evaluation. This group is more likely to require advanced cardiac imaging such as CMRI in addition to closer monitoring for cardiac dysrhythmia. Return to sports/activity should be directed by the cardiologist.

Multisystem Inflammatory Syndrome in Children

All patients diagnosed with MIS-C should be restricted from sports even after discharge from initial hospitalization. Rather than a single disease entity, the presentation of MIS-C encompasses a spectrum ranging from mild to severe disease. Further follow-up after discharge should be based on severity of initial symptoms as well as findings on subsequent outpatient visits. In those with myocardial involvement, exercise restriction is suggested for 3 to 6 months after resolution of symptoms with normalization of the ECG, echocardiogram, ambulatory cardiac monitor, and cardiac enzymes required prior to return to sports as per general myocarditis guidelines. ³⁴ A CMRI is suggested prior to return to sports for those patients. MIS-C patients without cardiac involvement, as evidenced by normal N-terminal pro-B type natriuretic peptide, troponin levels, and normal ECG and echocardiographic features, could be allowed to return to sports after their 2- or 6-week visit with cardiology, depending on age and intensity of sports participation. As with other presentations, gradual escalation of activity, with ongoing surveillance for concerning symptoms, is suggested.

Conclusion

Children between the ages of 4 and 21 years who are positive for SARS-CoV-2 may return to gradual increase in their physical activity after the 10 days of quarantine, provided they do not have any symptoms referable to the cardiovascular system and have been cleared by their primary care provider and/or cardiologist if appropriate. The cardiac symptoms can even develop in those who were asymptomatic or had mild to moderate symptoms during SARS-CoV-2 infection. Patients should be educated on self-monitoring of cardiac symptoms with return to exercise and should be encouraged to seek immediate evaluation if they develop. The risk of cardiac involvement is high in children diagnosed with MIS-C and restriction of sports for 3 to 6 months is advised for those with cardiac involvement.