Sudden cardiac death (SCD) in athletes is a major topic of concern in sports medicine and cardiology. Each case of SCD in a young athlete draws media attention and sparks debate on how best to prevent this outcome. However, designing a way to effectively predict such occurrence remains difficult. Even the incidence of SCD in athletes has been debated, ranging from 0.61-2.28/100,000.^1-4 While the most effective screening model remains unknown, it is becoming clear that the criteria employed for reading electrocardiograms (ECGs) in athletes has progressed substantially over the past decade.

First published in 1996, and formalized in 2007, the American Heart Association (AHA) recommended a 12-point history and physical exam to be used for athletes prior to participation. This included questions regarding personal and family medical history, as well as physical exam findings such as murmurs and blood pressure measurements.^5,6 By 2014, the AHA revised this to a 14-point screening process to also include history of having been restricted from competition and history of cardiac testing.⁷ The AHA recommends further cardiac work-up for any positive answer or exam abnormality. The AHA continues to recommend against universal use of ECG, although does support selective use of ECG when prudently conducted, and with adequate cardiology resources.

Intense athletic conditioning leads to cardiac chamber remodeling as part of a normal response to a high level of repetitive exercise. As a result, the "athlete's ECG," will have changes related to structural cardiac remodeling and increased vagal tone. Some of these findings are similar to pathologic changes found in non-athletes, and can look sinister even though they are normal adaptive findings. Thus, discriminating between training-related and pathologic ECG changes is challenging. False positive ECGs lead to further testing, which has financial implications and potential psychological effects on young athletes. However, false positives are not unique to the ECG and can be found in other assessment tools as well. A study of the AHA 14-point criteria found that approximately one quarter of athletes screened positive when using these criteria, which does not correlate with the rates of disease in this population.⁸ False positives have been identified with echocardiogram and cardiac magnetic resonance imaging (CMRI) as well.

Many groups have worked to refine ECG criteria for athletes to maintain sufficient rates of detecting cardiovascular abnormalities, while minimizing false positives. In 2010, the European Society of Cardiology (ESC) created recommendations for the interpretation of ECGs in athletes. They defined sinus bradycardia/arrhythmia, first-degree AV block, Mobitz I (Wenkebach) second-degree heart block, incomplete right bundle branch block (RBBB), early repolarization (including domed ST-segment elevation followed by T-wave inversion (TWI) confined to V2-V4 in black/African athletes), and isolated QRS voltage criteria for left ventricular hypertrophy (LVH) as physiologic (Group 1) adaptations of the athlete's heart to training.9 They recommended no further work-up for these changes unless the athlete reported a family history of SCD or personal symptoms suggestive of heart disease.⁹ At the same time, their guidelines defined other ECG abnormalities (Group 2) as definitive red flags requiring a more advanced cardiac work-up. These included non-Group 1 TWIs, ST-segment depression, pathological Q waves, left atrial enlargement, left axis deviation/left anterior hemiblock, right axis deviation/left posterior hemiblock, right ventricular hypertrophy (RVH), ventricular pre-excitation, complete left or right bundle branch block (LBBB, RBBB), long- or short-QT interval, and Brugada-like early repolarization.⁹

Over time, further research showed certain Group 2 changes could be physiologic, with up to 40% of certain athlete populations demonstrating such changes on their ECGs.¹⁰ The ESC criteria were developed based primarily on ECGs from white athletes. However, follow-up studies using ESC criteria demonstrated that black athletes were 2.5 times more likely to have an abnormal ECG, a figure that did not correlate with the likelihood of these athletes having underlying cardiac disease. While the criteria had a high sensitivity for detecting hypertrophic cardiomyopathy (HCM), they were still associated with a high overall false-positive rate, especially in black athletes. Additionally, analysis of ESC criteria using athletes of different nationalities showed that while there was a high sensitivity for Wolff-Parkinson-White (WPW) and HCM, there was an overall false-positive rate of 22.3%.¹¹ The Group 2 ECG findings of isolated right atrial enlargement (RAE), axis deviation, and RVH were found to be low yield for diagnosing cardiac pathology, leading to many of the false-positive ECGs.¹² One study of athletes showed that omitting isolated axis deviation or atrial enlargement reduced the false positive rate from 13% to 7.5%, with minimal drop in sensitivity of detecting cardiac pathology from 91% to 89.5%.¹² Such findings prompted further refinement of ECG interpretation criteria by other groups.

The Stanford criteria, published in 2011, further modified the ESC criteria. They maintained that training-induced changes (Group 1) did not warrant further work-up. The addition of new cutoffs for pathologic Q waves, left and right atrial abnormalities, axis deviation, QT prolongation, and arrhythmia, limited the number of abnormals.¹³ Examination of the Stanford criteria found a lower false-positive rate (8.1%) than the ESC criteria (26%).¹⁴ Thus, ECG interpretation improved; however, nearly one in ten athletes was still undergoing unnecessary cardiac testing.

In February 2012, an international group of experts met in Seattle, WA to further revise ECG guidelines for athlete's ages 14 to 35 years old. The Seattle criteria delineated training-related changes that were similar to the ESC Group 1 abnormalities, but added junctional escape rhythms and ectopic atrial rhythms to this group.^15,16 The new criteria redefined abnormal ECG findings warranting further workup. New thresholds/definitions were recommended for significant TWI, ST-segment depressions, left axis deviation, right axis deviation, ventricular pre-excitation, short QT, Brugada syndrome, non-specific intraventricular conduction delay, and arrhythmias.^14,15,17,18 The Seattle criteria have been shown to have a lower false-positive rate (2.5-6%) compared to ESC and Stanford criteria.^14,19 Overall, the use of the Seattle criteria resulted in 78% fewer abnormal variants than ESC criteria, with no change in sensitivity.¹⁴ The difference in false-positives was largely attributed to new thresholds for intraventricular conduction delay, QTc prolongation, and short QT interval. These findings were replicated in another study showing that the Seattle criteria offered a higher specificity without a reduction in sensitivity, as compared to ESC criteria.²⁰

A major limitation of these three criteria sets is that they are largely based on norms established from Caucasian athletes. A 2014 study applied the ESC and Seattle criteria to elite black and whites athletes ages 14 to 35 to develop the "Refined criteria."¹⁰ Most thresholds for defining variants were similar to previous, but the Refined criteria created a 'borderline' category of ECG variants that would not require further work-up if found in isolation. This category included left or right atrial enlargement, left or right axis deviation, and voltage criteria for right ventricular enlargement.¹⁰ The presence of two or more of these criteria would prompt further investigation. This borderline category was formulated after research showed that when found in isolation, these variants did not correlate well with pathologic cardiac disorders in asymptomatic athletes.^12,21 The authors of the Refined criteria found that while all (ESC, Seattle, and Refined) criteria had a high sensitivity for ECG-detectable major cardiac abnormalities (100%), the Refined criteria were associated with a lower false-positive rate in both white and black athletes (6.1% and 15.8%) as compared to the ESC criteria (26.5% and 59.9%) and Seattle criteria (7.9% and 20.7%).¹⁰ This was replicated in an ethnically diverse athletic population where the Refined criteria outperformed both the Seattle and ESC criteria in specificity while maintaining sensitivity for Arabic, black, and Caucasian athletes.¹¹

Recently, a 2nd International ECG Summit convened in Seattle, WA to revise athletic ECG interpretation guidelines, with a goal to further improve accuracy based on new and emerging research. The updated criteria will further define the ECG manifestations of physiologic changes in the athletic heart including setting age limits for anterior TWI, defining the pathologic PVC, and adjusting the Refined criteria regarding borderline abnormalities. A new feature to the guidelines will be to more clearly define the cardiac evaluation of ECG abnormalities once detected. This summit will be a culmination paper of over 10 years of updating cardiac screening criteria in athletes 12 to 35 years of age. The criteria are sure to maintain sensitivity rates for ECG readings in athletes, while further improving specificity. A tremendous amount of work has been done in the past 20 years to improve detection of cardiac abnormalities in athletes, with the goal to foster safe participation in athletics.

References

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2. Harmon KG, Asif IM, Ellenbogen R, Drezner JA. The incidence of sudden cardiac arrest and death in United States high school athletes. Br J Sports Med 2014;48:605.
3. Maron, BJ, Doerer JJ, Haas TS, Tierney DM, Mueller FO. Sudden deaths in young competitive athletes analysis of 1866 deaths in the united states, 1980–2006. Circulation 2009;119:1085-92.
4. Drezner JA, Harmon KG, Marek JC. Incidence of sudden cardiac arrest in Minnesota high school student athletes: the limitations of catastrophic insurance claims. J Am Coll Cardiol 2014;63:1455-6.
5. Maron BJ, Thompson PD, Puffer JC, et al. Cardiovascular preparticipation screening of competitive athletes. A statement for health professionals from the Sudden Death Committee (clinical cardiology) and Congenital Cardiac Defects Committee (cardiovascular disease in the young), American Heart Association. Circulation 1996; 94:850-6.
6. Maron BJ, Thompson PD, Ackerman MJ, et al. Recommendations and considerations related to preparticipation screening for cardiovascular abnormalities in competitive athletes: 2007 update: a scientific statement from the American Heart Association Council on Nutrition, Physical Activity, and Metabolism: endorsed by the American College of Cardiology Foundation. Circulation 2007;115:1643-55.
7. Maron BJ, Friedman RA, Kligfield P, et al. Assessment of the 12-Lead ECG as a screening test for detection of cardiovascular disease in healthy general populations of young people (12-25 Years of Age): a scientific statement from the American Heart Association and the American College of Cardiology. Circulation 2014;130:1303-34.
8. Dunn TP, Pickham D, Aggarwal S, et al. Limitations of Current AHA Guidelines and Proposal of New Guidelines for the Preparticipation Examination of Athletes. Clin J Sport Med 2015 April 24. [Epub ahead of print]
9. Corrado D, Pelliccia A, Heidbuchel H, et al. Recommendations for interpretation of 12-lead electrocardiogram in the athlete. Eur Heart J 2010;31:243-59.
10. Sheikh N, Papadakis M, Ghani S, et al. Comparison of electrographic criteria for the detection of cardiac abnormalities in elite black and white athletes. Circulation 2014;129:1637-49.
11. Riding NR, Sheikh N, Adamuz C, et al. Comparison of three current sets of electrocardiographic interpretation criteria for use in screening athletes. Heart 2015;101:384-90.
12. Gati S, Sheikh N, Ghani S, et al. Should axis deviation or atrial enlargement be categorised as abnormal in young athletes? The athlete's electrocardiogram: time for re-appraisal of markers of pathology. Eur Heart J 2013;34:3641-8.
13. Uberoi A, Stein R, Perez MV, et al. Interpretation of the electrocardiogram of young athletes. Circulation 2011;124:746-57.
14. Pickham D, Zarafshar S, Sani D, Kumar N, Froelicher V. Comparison of three ECG criteria for athlete pre-participation screening. J Electrocardiol 2014;47:769-74.
15. Drezner JA, Ackerman MJ, Anderson J, et al. Electrocardiographic interpretation in athletes: the 'Seattle Criteria'. Br J Sports Med 2013;47:122-4.
16. Drezner JA, Fischbach P, Froelicher V, et al. Normal electrocardiographic findings: recognising physiological adaptations in athletes. Br J Sports Med 2013;47:125-36.
17. Drezner JA, Ashley E, Baggish AL, et al. Abnormal electrocardiographic findings in athletes: recognising changes suggestive of cardiomyopathy. Br J Sports Med 2013;47:137-52.
18. Drezner JA, Ackerman MJ, Cannon BC, et al. Abnormal electrocardiographic findings in athletes: recognising changes suggestive of primary electrical disease. Br J Sports Med 2013;47:153-67.
19. Price DE, McWilliams A, Asif IM, et al. Electrocardiography-inclusive screening strategies for detection of cardiovascular abnormalities in high school athletes. Heart Rhythm 2014;11:442-9.
20. Brosnan M, La Gerche A, Kalman J, et al. The Seattle Criteria increase the specificity of preparticipation ECG screening among elite athletes. Br J Sports Med 2014;48:1144-50.
21. Zaidi A, Ghani S, Sheikh N, et al. Clinical significance of electrocardiographic right ventricular hypertrophy in athletes: comparison with arrhythmogenic right ventricular cardiomyopathy and pulmonary hypertension. Eur Heart J 2013;34:3649-56.

Keywords: Arrhythmias, Cardiac, Athletes, Atrioventricular Block, Blood Pressure, Bradycardia, Brugada Syndrome, Bundle-Branch Block, Cardiomyopathy, Hypertrophic, Cardiovascular Abnormalities, Death, Sudden, Cardiac, Depression, Follow-Up Studies, Electrocardiography, Goals, Heart, Heart Conduction System, Heart Defects, Congenital, Hypertrophy, Left Ventricular, Hypertrophy, Right Ventricular, Incidence, Magnetic Resonance Imaging, Polyvinyl Chloride, Sports, Sports Medicine

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