key: cord-1035250-brc7vtbw
authors: Erickson, Jacob L.; Poterucha, Joseph T.; Gende, Alecia; McEleney, Mark; Wencl, Corey M.; Castaneda, Marisa; Gran, Lindsay; Luedke, Joel; Collum, Jill; Fischer, Karen M.; Jagim, Andrew R.
title: The use of electrocardiogram screening to clear athletes for return to sport following COVID-19 infection
date: 2021-02-08
journal: Mayo Clin Proc Innov Qual Outcomes
DOI: 10.1016/j.mayocpiqo.2021.01.007
sha: 8179806ade2dbe0f6df3460a87bf9be2385f3438
doc_id: 1035250
cord_uid: brc7vtbw

Objective To quantify the occurrence rate of abnormal ECG findings and symptoms following COVID-19 infection. Patients Adult patients (>18 years old) who were participating in collegiate athletics and previously tested positive for COVID-19 between August 2020 to November 2020. Methods In this retrospective study, we report findings of electrocardiogram (ECG) testing to screen athletes for cardiac abnormalities following COVID-19. Athletes underwent general examinations and ECG screening prior to being medically cleared for a return to sport following COVID-19. Predetermined predictors were grouped into categorical variables including: 1) Sex; 2) Symptom severity; and 3) BMI (normal vs. overweight = > 24 kg∙m-2). These were used to examine differences of abnormal rates occurred between different predictor categories. Results Of the 170 athletes screened, 6 (3.5%) presented with abnormal ECG criteria and were referred to cardiology. We found no evidence that symptom severity, sex and BMI category were associated with a higher rate of abnormal ECG (p > 0.05). Greater severity of COVID-19 symptoms were associated with higher percentage of ST depression, T-wave inversion, ST-T changes and presence of fQRS. Loss of smell, loss of taste, headache and sore throat were the most prevalent symptoms with 32.9%, 38.8%, 36.5% and 25.3% of athletes reporting each symptom, respectively. Conclusions Preliminary findings indicate a low risk of myocardial injury secondary to COVID-19 infection with less than4% of patients presenting with abnormal ECG and 10% requiring referral to a cardiologist. While viral myocarditis was not demonstrated in any athlete referred for cardiology assessment, two patients developed effusative viral pericarditis.

There continues to be debate regarding the level of risk for athletes following infection and the appropriate diagnostic testing that may be warranted as part of a medical clearance for return to sport. 1 Epidemiological trends indicate that younger demographics tend to present with fewer symptoms and are less likely to be hospitalized. 2 However, given the novelty of the virus and the uncertainty regarding its systemic long-term effects, sports medicine clinicians are faced with difficult decisions regarding how to clear athletes for return to sport. A primary concern for athletes is the potential risk for myocardial injury secondary to infection, which may elevate risk of cardiac events during high levels of physical exertion. 3, 4 In a recent study, 5 4 of 26 collegiate athletes who had previously tested positive for presented with findings suggestive of myocarditis after cardiovascular magnetic resonance despite two of the patients being completely asymptomatic. However, the clinical relevance of these findings and appropriate timelines for a resumption of physical activity has still yet to be fully elucidated. In the absence of strong clinical evidence regarding the prevalence of cardiac pathology following COVID-19, evidence-based decisions and the development of return to play guidelines prove challenging. A recent consensus statement recommended a two-week surveillance period for asymptomatic patients and electrocardiogram plus transthoracic echocardiograms in patients with mild symptoms following COVID-19 infection. 6 However, each level of competition may opt to consult with local sports medicine clinicians and cardiologists to utilize customized protocols and diagnostics to clear athletes for a return to sport depending on available resources. For example, professional and National Collegiate Athletics Association (NCAA) Division I programs may utilize a diverse array of diagnostic tests with cardiovascular magnetic resonance imaging likely serving as the gold standard for the detection J o u r n a l P r e -p r o o f of myocarditis as a universal screening program for all athletes who test positive for COVID-19.

At smaller institutions, this battery of testing may not be feasible and, therefore, athletes may be left to consult with their parents or primary care providers to determine the best course of action. At the NCAA Division III level within the United States, local institutions were advising athletes to obtain medical clearance from a physician prior to returning to sport. In addition to a general physical examination, all athletes underwent an electrocardiogram (ECG) to screen for any cardiac abnormalities that may have warranted further diagnostics and a consult with a cardiologist. However, the utility of these tests to detect clinical abnormalities following COVID-19 infection in asymptomatic patients or those with mild to moderate symptoms has yet to be determined. Additionally, there is currently a lack of cardiovascular profiles in athletes following COVID-19 infection. This information would play an important role in appropriate risk stratification for return to play protocols in sport. Therefore, the aim of the current study was to quantify the occurrence rate of abnormal ECG findings when being used as part of a medical clearance for return to sport following COVID-19 infection. A secondary aim was to document the frequency and severity of COVID-19 symptoms in adult athletes.

During the fall semester of 2020, a convenience sample of collegiate athletes from two NCAA Division III universities who tested positive for COVID-19 were included in this retrospective analysis. All athletes were required to obtain medical clearance from their respective university's medical director prior to returning to sport. It was determined that this clearance should consist of, at a minimum, a general physical examination, documentation of symptoms and an ECG to J o u r n a l P r e -p r o o f screen for any cardiac abnormalities that may warrant further diagnostics and follow-up with a cardiologist. In this retrospective study, a chart review was completed to quantify the occurrence of abnormal ECG findings and document the severity and frequency of COVID-19 related symptoms. Predetermined predictors were grouped into categorical variables and included: 1) Sex; 2) Symptom severity; and 3) BMI classification (normal weight vs. overweight => 24 kg•m -2 ). These were used to examine whether statistically significant differences of abnormal rates occurred between different predictor categories. Symptoms were recorded through electronic questionnaire distributed by athletic training staff and self-reported during the clinical examination. Overall symptom severity was graded using a 1-4 scale with 1 = asymptomatic; 2 = mild (nonspecific and self-limited fatigue; anosmia or ageusia; nausea, vomiting, and/or diarrhea; headache; cough; sore throat; and nasopharyngeal congestion); 3 = Moderate (persistent fever > 38°C or chills; myalgias, severe lethargy, hypoxia or pneumonia; and/or cardiovascular symptoms [dyspnea and chest pain; tightness or pressure at rest or during exertion]); and 4 = severe (hospitalized) using previously described categories. 3, 7 The study period was August 2020 -December 2020.

A standard resting 12-lead ECG was completed for all athletes and recorded using onscreen digital software (Marquette 12SL ECG Analysis Program for Adults, GE Healthcare MAC 3500) with a digital sampling rate of 4,000 Hz. In our study two physicians evaluated all study participants for consistency in management and test interpretation using International criteria for ECG interpretation in athletes. 8 . All ECGs were independently reviewed by the two physicians for interpretation agreement and in cases where disagreement arose, a third physician was to review for majority agreement. We used threshold criteria for further cardiovascular consultation and testing in any athlete with moderate symptoms and/or had an abnormal or J o u r n a l P r e -p r o o f borderline ECG at the time of their initial evaluation (22.54 ± 14.20 days after positive test). For consistency in chart review, athletes were categorized based on symptoms they listed on their questionnaire. Patients with an abnormal ECG or prolonged moderate symptoms were referred to a cardiologist for further testing. If any athlete listed shortness of breath, but the symptom was completely resolved at the time of their evaluation, they were not sent on for further cardiovascular evaluation in the setting of a normal ECG (n = 15).

Study subjects included collegiate male and female athletes between the ages of 18-25 yrs. of age. The study protocols were approved by the Institutional Review Board at Mayo Clinic (IRB# 20-011123) and a waiver of consent was provided due to the retrospective nature of the current study.

The presence of and frequency of common COVID-19 symptoms were reported using percentages. Athlete descriptive characteristics by sex were reported using mean and standard deviation for continuous variables and percentages for categorical variables. Predetermined predictors were grouped into categorical variables and included: 1) Sex; 2) Symptom severity; and 3) BMI > 24 kg•m -2 . Chi-square tests were performed to examine whether statistically significant differences of abnormal rates occurred between different predictor categories and prevalence of symptoms across each category. In cases where categorical variables or symptom categories had less than 5 subjects, a Fisher's exact test was used to examine differences between the variables. Alpha was set at p ≤ 0.05 for determination of statistical significance. All data J o u r n a l P r e -p r o o f were analyzed using the Statistical Package for the Social Sciences (IBM SPSS Statistics for Windows, Version 25.0; Armonk, NY: IBM Corp.).

A total of 170 athletes were screened during the study period. Table 2 presents a summary of physical characteristics of all patients. The average time between positive test and medical screening was (mean ± SD; 95% Confidence Interval) 22.54 ± 14.20 (20.38, 24.70) days. Of the 170 athletes screened, 6 (3.5%) presented with abnormal or borderline ECG and were referred to a cardiologist for further testing. Ten additional patients were referred based on symptom severity or duration of symptoms experience. Table 3 provides a summary of further diagnostics and final outcomes for patients with abnormal ECG findings and those referred to cardiology based on symptoms. As no athletes had severe symptoms, this group was not analyzed. Symptom severity was not associated with a higher rate of abnormal ECG (χ 2 = 0.054; p = 0.817). Greater severity of COVID-19 symptoms were associated with higher percentage of ST depression, Twave inversion, ST-T changes and presence of fQRS in those with abnormal findings. Abnormal ECG results were found in 2.2% of men and 5.1% of women. We did not find evidence that BMI category (;p = 1.0) or sex (p = 0.418) were associated with abnormal ECG findings. Further cardiovascular diagnostic testing was indicative of post-COVID effusative viral pericarditis (n = 2) and xiphoiditis (n = 1); all three subjects had moderate symptoms. There was a significant difference between sexes for symptom severity (χ 2 = 14.136; p < 0.01). Table 4 presents a summary of symptom categorization and frequency by sex. Loss of smell, loss of taste, headache and sore throat were the most prevalent symptoms with 32.9%, 38.8%, 36.5% and 25.3% of athletes reporting each symptom, respectively.

J o u r n a l P r e -p r o o f Erickson 9 The primary aim of the current study was to examine the occurrence rate of abnormal ECG screenings in a convenience sample of collegiate athletes who had previously tested positive for COVID-19. The results of the current study indicate that, of the 170 athletes who were screened, 6 (3.5%) presented with abnormal cardiac rhythms while 16 patients (9.4%) total required referral to a cardiologist. Of those with abnormal cardiac rhythms or who were referred to cardiologist based on symptom severity or duration, 8 patients reported mild symptoms and 8

reported moderate symptoms at the time of examination. In comparison, in a cohort of 431 older patients (mean age of 74 years) hospitalized with severe COVID-19 illness, ECG was abnormal in 93% of the patients. 9 In a similar study, it was reported that abnormal ECG findings appeared to be associated with severity of COVID-19 infection as a higher percentage of ST depression, T-wave inversion, ST-T changes and presence of fQRS were noted in patients classified as severely ill vs non-severe. 10 Although athletes are markedly different from older adult populations, who are likely less active with a higher risk of comorbidities, the normal ECG findings from the majority of athletes in the current study are encouraging.

A novel finding from the current study is that a higher percentage of women were categorized as having moderate symptoms compared to men. These findings are contradictory to previous reports indicating men typically experience more severe outcomes and have a higher case fatality rate compared to women, albeit in older populations. [11] [12] [13] Loss of smell, loss of taste, headache and sore throat were the most prevalent symptoms with 32.9%, 38.8%, 36.5% and 25.3% of athletes reporting each symptom, respectively. These symptoms are in alignment with those commonly reported in adults with mild to moderate disease. 14, 15 The current study findings are unique in that in otherwise-healthy adults who are asymptomatic or present with mild symptoms of COVID-19, an ECG would typically not be warranted, rather patients would be instructed to J o u r n a l P r e -p r o o f manage their symptoms at home unless further testing or care would be needed. However, the use of ECGs in sport to screen athletes for cardiac abnormalities is not unprecedented as some sports medicine professionals often recommend it for all athletes prior to competing, despite a lack of any cardiovascular symptoms. The primary focus of such a surveillance strategy tends to be on detecting cardiac myopathy in an effort to prevent sudden cardiac death in athletes during high levels of exertion. For reference, over a 5-year surveillance period using widespread ECG screening, an abnormal occurrence rate of 6.6% was reported when using the Stanford criteria. 16 More recently, among a cohort of 1,686 NCAA Division I athletes, a surveillance screening period identified an abnormal ECG rate of 1.8% when using the International Criteria. 17 In the current study, which had a smaller sample size, we report a slightly higher abnormal ECG rate of 3.5%, compared to the 1. The results of the current study add to the growing body of literature regarding the pathophysiological effects of COVID-19 in young, otherwise healthy adult athletes. In this small cohort of athletes, there was an ECG abnormality rate of 3.5%, with follow up diagnostics also indicating low rates of myocardial injury secondary to COVID-19 infection for those requiring a consult with cardiology. It is important to note, even some patients with mild symptoms (n = 5), exhibited abnormal cardiac rhythms. No patients in our study classified as asymptomatic or mild symptoms were found to have evidence of myocardial injury if they completed further diagnostic cardiovascular testing based on an initial abnormal ECG. This would align with new evidence 3 suggesting against cardiovascular risk stratification in less than moderately symptomatic, young, healthy athletes.

Overall, adults between the ages of 15-24 years represent approximately 0.18% of all COVID-19 related deaths. 2 The low death rate, in conjunction with preliminary findings indicating a low degree of symptom severity and low rate of abnormal ECG findings reported in the current study, suggest the overall risk for young adult athletes is likely low; however, the long-term physiological effects secondary to COVID-19 infection are still currently unknown. The findings from the current study are in alignment with those described in the review by Kim et al., 3 adding further support that cardiovascular risk stratification should only be considered in athletes with persistent moderate symptoms. Therefore, athletes should take every precaution to avoid COVID-19 and if infected, use a gradual progression when returning back to physical activity while closely monitoring symptoms. Additionally, athletes with comorbid medical conditions such as asthma, dyslipidemia, sickle cell trait and diabetes may want to exercise caution when making decisions regarding a return to play as there is currently limited evidence on how these sub-populations may be affected by COVID-19, despite being regularly active. 18 The Center for J o u r n a l P r e -p r o o f Erickson 12 Disease Control also provides a summary of medical conditions which may predispose an individuals to more severe symptoms following COVID-19 infection. 19 Further, if athletes continue to experience symptoms > 2 weeks post-infection, it is recommended to follow-up to determine if additional testing is warranted.

A limitation of the current study was the questionnaire used to document self-reported symptoms of the athletes. The questionnaire included symptoms at any point and for any duration no matter how brief after testing positive for COVID-19 or any underlying context. Given institutional policies for evaluation of recently COVID-19 positive patients, we were not able to see these athletes until minimum of 10 days from symptom onset in the clinic. Several of the athletes who had a moderate category symptom had symptoms completely resolve by the time of their evaluation. In these cases, if their ECG was normal, they were managed based on their symptoms at the time of evaluation, which were almost always less severe than during initial onset. Current recommendations on categorizing symptom severity do not explicitly define duration of symptoms for every category because we do not have concrete evidence. In this cohort of athletes, we determined management based on symptoms present at their evaluation. All athletes in the current cohort were followed during their return to play progression using an interdisciplinary continuum of care and supervision. To date, there have been no adverse events with their return. Another limitation of the current study was an omission of any pre-existing medical conditions of the athletes included in this cohort. As previously discussed, certain underlying medical conditions may influence symptom severity following COVID-19 infection.

There were also a small number of athletes who had abnormal ECG results, which did not allow J o u r n a l P r e -p r o o f Erickson 13 us to adjust for covariates in the statistical model. Further studies should be carried out to ascertain the effect of possible confounders and the association of sex in abnormal ECG.

Findings from the current study indicate a low degree of symptom severity and low rate of abnormal ECG findings in a cohort of athletes, suggesting the overall risk for young adult athletes is likely low; however, the long-term physiological effects secondary to COVID-19 infection are still currently unknown. Loss of smell, loss of taste, headache and sore throat were the most prevalent symptoms with 32.9%, 38.8%, 36.5% and 25.3% of athletes reporting each symptom, respectively. Further study on categorizing symptom severity should take into account duration of symptoms. Limited data from the current study would suggest the symptom of 'shortness of breath,' for example, in and of itself may not be enough to classify someone as having moderate symptoms. More research is need to determine if an athlete that has shortness of breath, but resolves by day 10, is at a lower risk for myocardial injury when compared to an athlete that continues experiencing shortness of breath at the time of medical evaluation after self-isolation. Further, elucidating duration of symptoms to more accurately classify symptom severity, could prove useful and become an important indicator of which athletes require further testing. All athletes from the current study that were asymptomatic or mildly asymptomatic and presented with an abnormal ECG that went on to further cardiovascular testing, were able to return to activity without complication. This further supports the limited value of widespread cardiovascular testing in athletes with less than moderate category symptoms and symptoms that resolve in less than 10 days. These findings can help guide prognostic information and policy development for clearing athletes for a return to sport. Further study is needed using prospective study designs to understand the relationship between COVID-19 symptom severity, confounding J o u r n a l P r e -p r o o f related myocardial disease among a larger sample of athletes. Additionally, long-term surveillance data are needed to examine long-term physiological effects following COVID-19 infection in athletes.

J o u r n a l P r e -p r o o f 

Balancing act: when is an elite athlete who has had COVID-19 safe to return to play? When does prudent investigation go offside into overmedicalising?

CDC Coronavirus Disease

Coronavirus Disease 2019 and the Athletic Heart: Emerging Perspectives on Pathology, Risks, and Return to Play

Myocarditis in athletes: A clinical perspective

Cardiovascular Magnetic Resonance Findings in Competitive Athletes Recovering From COVID-19 Infection

A Game Plan for the Resumption of Sport and Exercise After Coronavirus Disease 2019 (COVID-19) Infection

Mild or Moderate Covid-19

International criteria for electrocardiographic interpretation in athletes: Consensus statement

Electrocardiographic features of 431 consecutive, critically ill COVID-19 patients: an insight into the mechanisms of cardiac involvement

The effect of the severity COVID-19 infection on electrocardiography

Impact of sex and gender on COVID-19 outcomes in Europe

Sex-specific clinical characteristics and prognosis of coronavirus disease-19 infection in Wuhan, China: A retrospective study of 168 severe patients

Sex differences in immune responses that underlie COVID-19 disease outcomes

Clinical Presentation of COVID-19: A Systematic Review Focusing on Upper Airway Symptoms

Covid-19: Symptoms are common after acute phase of disease, Italian study shows

Five-Year Experience with Screening Electrocardiograms in National Collegiate Athletic Association Division I Athletes

Evaluation of a Preparticipation Cardiovascular Screening Program Among 1,686 National Collegiate Athletic Association Division I Athletes: Comparison of the Seattle, Refined, and International Electrocardiogram Screening Criteria

Comorbid Medical Conditions in Young Athletes: Considerations for Preparticipation Guidance During the COVID-19 Pandemic

People with Certain Medical Conditions

F2019-ncov%2Fneed-extra-precautions%2Fgroups-at-higher-risk.html

J o u r n a l P r e -p r o o f