Editor's Note: Commentary based on Schnell F, Riding N, O'Hanlon R, et al. The recognition and significance of pathological T-wave inversions in athletes. Circulation 2014;131:165-73.

The electrocardiogram (ECG) plays a central role in the cardiovascular evaluation of athletes. The "Seattle Criteria",¹ and more recently the "Refined Criteria,"² have attempted to distinguish ECG patterns that are associated with systematic athletic training from those associated with underlying pathology. T-wave inversion (TWI) has become a particular focus of attention in this field as an ECG pattern that is considered highly suggestive of underlying cardiomyopathy. Pathologic TWI (PTWI) is here defined as a negative T-wave deflection of ≥2 mm in ≥2 leads, with the exception of aortic valve replacement (AVR), III, and V1, and excluding changes in V1-V4 in patients of Afro-Caribbean descent when preceded by a domed ST-segment.³ In 1960, Hiss⁴ reported the prevalence of abnormal T-waves as 0.86% in 67,375 Air Force members. More recently, Papadakis⁵ showed that in a large, primarily Caucasian population, by age 16 years, negatively deflected T-waves beyond V2 occur in only 0.1% of participants. Thus, PTWI is rare in healthy athletes, has been associated with serious cardiac pathology, and does not appear to reflect physiologic adaptation to exercise.^6-7

A recent article by Schnell and colleagues⁸ highlights several important concepts: 1) the significant association of cardiomyopathy with TWI in ≥2 leads; 2) the limitations of echocardiography; and 3) the importance of serial evaluation of asymptomatic athletes with TWI. The authors' stated goals were to "prospectively determine the prevalence of cardiac pathology in athletes presenting with PTWI," and to "examine the efficacy of including cardiac magnetic resonance imaging (CMRI)" in the evaluation of PTWI in athletes. Due to the distribution of TWI in their study population (64.5% had PTWI in II-III-aVF + V5-V6, 10.3% had PTWI in V5-V6, and 4.5% had PTWI in I-aVL + V5-V6), the article bears a particular focus on the diagnosis of hypertrophic cardiomyopathy (HCM) in athletes.

The study cohort is large, with 155 asymptomatic athletes found to have PTWI on surface ECGs out of a total population of 6,372 competitive athletes who had undergone a pre-participation screening ECG. In the PTWI group, 149 out of 155 patients were male, and ages ranged from 20-39 years. All patients underwent evaluation with physical examination, ECG interpreted using the Seattle Criteria¹, echocardiogram, exercise test, 24-hour Holter monitor, and CMRI. Cardiac pathology was detected in 44.5% of these patients, with HCM comprising 81% of diagnoses. Family history and ST-segment depression were found to be factors predictive of pathology. The authors highlight that echocardiogram yielded a diagnosis in 37 out of 61 cases (31 out of 51 cases of HCM, three out of four cases of arrhythmogenic right ventricular cardiomyopathy [ARVC], two out of two cases of left ventricular non-compaction, one out of four cases of myocarditis), and were suspicious for disease in a further 10 cases. CMRI was positive in all 37 cases diagnosed by echocardiogram, all 10 cases deemed suspicious by echocardiogram, and yielded a diagnosis in an additional 14 athletes. Eight more diagnoses were picked up by non-imaging-based testing, yielding a sensitivity of 88% for CMRI. The authors found cardiac conditions having known association with sudden cardiac death in 1.1% of the overall study population – a higher prevalence than previously published.⁹

The Schnell article is an important addition to the literature guiding evaluation of the athlete with abnormal ECG. Strengths of the article include its prospective, multicenter study design, large cohort, and thorough evaluation of each patient (at a surprisingly low cost). The authors also report follow-up (range 8 to 30 months) in athletes initially given sports clearance due to normal cardiac assessment, and in picking up five additional diagnoses, reinforce the importance of following these patients longitudinally. This point is particularly salient in adolescents in whom initial evaluation may take place prior to the development of overt findings on echocardiogram or CMRI.

The overall rate of pathology in this study was high, and some degree of over-diagnosis and referral bias may have been present. Diagnoses were made based on currently available guidelines, with European Society of Cardiology guidelines used for the diagnosis of HCM.¹⁰ In the absence of biopsy or genetic testing results, authors appear to assume 100% specificity for CMRI; thus, the high rate of pathology could be related to unidentified false positives. Speaking against over-diagnosis, however, the 54 patients with HCM (which made up 81% of pathology) were detrained for a period after diagnosis – 14 patients for three months and 40 patients for six months – with no significant change in left ventricular wall thickness. The high rate could also be related to a true poor sensitivity of echocardiography in HCM and lack of CMRI in prior studies, or to familiarity of the study centers with disease-related findings as highlighted by the 2009 North American Multidisciplinary Study of ARVC by Marcus and colleagues,¹¹ wherein core echocardiography laboratories identified pathology in a number of echocardiograms initially felt to be normal prior to referral.

In summary, the study by Schnell highlights the importance of repolarization abnormalities that can represent underlying cardiomyopathy. They also present an algorithm for evaluating these athletes, with CMRI used as second-line testing in those patients with normal echocardiogram. Given the diagnostic yield of echocardiography combined with its broad availability compared to CMRI, this algorithm is a reasonable approach to consider for the practicing sports cardiologist. Importantly, they did not recommend disqualification for those athletes with TWI who had normal imaging studies, but instead chose to educate them regarding the development of symptoms and placed them under yearly cardiac evaluation.

References

1. Drezner JA, Ackerman MJ, Anderson J, et al. Electrocardiographic interpretation in athletes: the 'Seattle criteria.' Br J Sports Med 2013;47:122-4.
2. Sheikh N, Papadakis M, Ghani S, et al. Comparison of ECG criteria for the detection of cardiac abnormalities in elite black and white athletes. Circulation 2014;129:1637-49.
3. Papadakis M, Carre F, Kervio G, et al. The prevalence, distribution, and clinical outcomes of electrocardiographic repolarization patterns in male athletes of African/Afro-Caribbean origin. Eur Heart J 2011;32:3641-8.
4. Hiss RG, Averill KH, Lamb LE. Electrocardiographic findings in 67,375 asymptomatic subjects. VIII. Non-specific T-wave changes. Am J Cardiol 1960;6:178-89.
5. Papadakis M, Basavarajaiah S, Rawlins J, et al. Prevalence and significance of T-wave inversions in predominantly Caucasian adolescent athletes. Eur Heart J 2009;30:1728-35.
6. Wasfy MM, Baggish AL. T-wave inversions in athletes: a sheep in wolf's clothing? Heart 2015;101:167-8.
7. Calo L, Sperandii F, Martino A, et al. Echocardiographic findings in 2261 young soccer players with or without inverted T waves at ECG. Heart 2015;101:193-200.
8. Schnell F, Riding N, O'Hanlon R, et al. Recognition and significance of pathological T-wave inversions in athletes. Circulation 2015;131:165-73.
9. Sharma S, Papadakis M. Interpreting the athlete's EKG: are all repolarization anomalies created equal? Circulation 2015;131:128-30.
10. Elliott PM, Anastasakis A, Borger MA, et al. 2014 ESC guidelines on diagnosis and management of hypertrophic cardiomyopathy : the Task Force for the Diagnosis and Management of Hypertrophic Cardiomyopathy of the European Society of Cardiology (ESC). Eur Heart J 2014;35:2733-79.
11. Marcus FI, Zareba W, Calkins H. ARVC/D, clinical presentation and diagnostic evaluation: results from the North American Multidisciplinary Study. Heart Rhythm 2009;6:984-92.

Keywords: Adaptation, Physiological, Adolescent, Algorithms, Aortic Valve, Arrhythmias, Cardiac, Arrhythmogenic Right Ventricular Dysplasia, Athletes, Biopsy, Cardiomyopathy, Hypertrophic, Cohort Studies, Death, Sudden, Cardiac, Depression, Echocardiography, Electrocardiography, Exercise Test, Follow-Up Studies, Genetic Testing, Goals, Heart Conduction System, Magnetic Resonance Imaging, Myocarditis, Physical Examination, Prevalence, Prospective Studies, Referral and Consultation, Sports, Ursidae

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