Introduction

The preparticipation examination (PPE) is the practice of screening athletes prior to athletic activity to identify medical conditions that may place the athlete at increased risk for adverse events during athletic participation. Electrocardiography (ECG) is increasingly utilized to improve PPE in identifying occult cardiac pathology; however, its role in routine screening is controversial. Broad based cardiovascular screening in athletes with inclusion of ECGs is practiced systematically in Italy^1-4 and Israel.⁵ In the United States, the American Heart Association (AHA) consensus expert panel does not endorse mandatory athlete screening with inclusion of ECGs.⁶ Limitations of ECGs in screening athletes include, but are not limited to, false positives, false negatives, and inter-observer interpretation variability.⁷ Various ECG patterns that are considered abnormal in the general adult population are commonly seen in athletes.⁸ Multiple ECG criteria have been published to differentiate normal training related variants from pathological findings.^8-12 In this Expert Analysis, the authors will discuss the rapid evolution of ECG criteria for athletes, examine ethnic related ECG patterns, and review the limited data on gender specific ECG findings.

The Evolution of ECG criteria in Athletes

With increasing clinical experience and systematic screening protocols, several of which have included concomitant echocardiography, ECG criteria have been refined resulting in fewer false positives. In 2001, one of the earliest athlete specific criteria was proposed by Pelliccia et al. ECG patterns were differentiated into a spectrum from normal findings to "distinctly abnormal" patterns which suggested an increased likelihood of underlying cardiomyopathy (Table 1).¹¹ In 2010, the European Society of Cardiology (ESC) proposed criteria to differentiate ECG findings consistent with "athletes heart" from pathological findings, known as group 1 and 2 ECG patterns (Table 2).⁹ Although ESC criteria improved specificity, false positives were still high, particularly in black athletes.^13-16 Further refinement led to the Seattle criteria in 2013, which emphasized ethnic specific ECG findings (Table 3). More recently, the "Refined criteria" demonstrated increased specificity (94%) with maintained sensitivity (Table 4).¹²

Table 1: ECG Criteria Proposed by Pelliccia et al

Normal	Mildly Abnormal	Distinctly Abnormal
Patterns commonly associated with athlete's heart syndrome and characterized by ≥1 of the following: 1. Increased PR interval duration >0.2s 2. Mild increase in R- or S-wave voltage (25-29mm) 3. Early Repolarization (ST-segment elevation ≥2 mm in >2 leads exclusive of V2 and V3) 4. Incomplete RBBB (rsR' in V1 <0.12 s) 5. Sinus bradycardia <60 beats/min	Patterns suggestive cardiovascular disease and characterized by ≥1 of the following: 1. Increased R- or S-wave voltage (30-34 mm) in any lead 2. Q waves (2-3 mm) in depth and present in ≥2 leads 3. Repolarization patterns with flat, minimally inverted, or particularly tall (i.e., ≥15 mm) T waves in ≥2 leads exclusive of AVR 4. Abnormal precordial R-wave progression with R>S-wave only in V5-V6 5. RBBB (rsR' ≥0.12 s in lead V1) 6. Right atrial enlargement (peaked p waves ≥2.5 mm in leads II, III, or V1) 7. Left atrial enlargement (prolonged positive p wave in lead II and/or deep prolonged negative p wave in V1) 8. Short PR interval ≤0.12 s	Patterns strongly suggestive of cardiovascular disease and characterized by ≥1 of the following: 1. Increased R- or S-wave voltage ≥35 mm in any lead 2. Q waves ≥4 mm in depth and present in ≥2 leads 3. Repolarization pattern with inverted T-wave >2 mm in ≥2 leads exclusive of AVR 4. LBBB 5. Marked left (≤ -30°) or right (≥110°) QRS axis deviation 6. Wolff-Parkinson-White pattern 7. Atrial fibrillation

Table 2: ESC 2010 Criteria

Group 1: common and training-related ECG changes	Group 2: uncommon and training-unrelated ECG changes
1. Sinus bradycardia 2. First-degree AV block 3. Incomplete RBBB 4. Early repolarization 5. Isolated QRS voltage criteria for LVH	1. T-wave inversion 2. ST-segment depression 3. Pathological Q-waves 4. Left atrial enlargement 5. Left-axis deviation/left anterior hemiblock 6. Right-axis deviation/left posterior hemiblock 7. Right ventricular hypertrophy 8. Ventricular pre-excitation 9. Completed LBBB or RBBB 10. Long- or short-QT interval 11. Brugada-like early repolarization

Table 3: Seattle criteria

Normal ECG findings

Abnormal ECG finding

1. Sinus bradycardia (≥ 30 bpm) 2. Sinus arrhythmia 3. Ectopic atrial rhythm 4. Junctional escape rhythm 5. 1° AV block (PR interval > 200 ms) 6. Mobitz Type I (Wenckebach) 2° AV block 7. Incomplete RBBB 8. Isolated QRS voltage criteria for LVH 9. Early repolarization (ST elevation, J-point elevation, J-waves or terminal QRS slurring) 10. Convex (‘domed’) ST segment elevation combined with T-wave inversion in leads V1–V4 in black/African athletes

1. T-wave inversion beyond V2 in white athletes and V4 in black athletes 2. ST segment depression 3. Pathologic Q waves 4. Complete left bundle branch block 5. Intraventricular conduction delay 6. Left axis deviation 7. Left atrial enlargement 8. Right atrial enlargement 9. Right ventricular hypertrophy pattern 10. Ventricular pre-excitation 11. Long QT interval ≥470 ms in males and ≥480 in females 12. Short QT interval ≤320 ms 13. Brugada-like ECG pattern 14. Profound sinus bradycardia (<30 bpm) 15. Atrial tachyarrhythmias 16. Premature ventricular contraction 17. Ventricular arrhythmias

Table 4: Refined criteria proposed by Sheikh et al

Training Related Normal Variants (Not warranting further investigation)	Borderline Variants (Only if ≥2 are present then warrants further investigation)	Training Unrelated Changes (Warranting further investigation)
1. Sinus bradycardia 2. First-degree AV block 3. Incomplete RBBB 4. Early repolarization 5. Isolated QRS voltage criteria for LVH	1. Left atrial enlargement 2. Right atrial enlargement 3. Left axis deviation 4. Right axis deviation 5. Right ventricular hypertrophy 6. T-wave inversions up to V4 in black athletes	1. ST-segment depression 2. Pathological Q-waves 3. Ventricular pre-excitation 4. T-wave inversions beyond V1 in white athletes and beyond V4 in black athletes 5. Complete LBBB or RBBB 6. QTc ≥470 ms in males and ≥ ms in females 7. Brugada-like early repolarization 8. Atrial or ventricular arrhythmias 9. ≥2 PVCs per 10 sec tracing

The Influence of Ethnicity on the Prevalence of ECG Patterns in Athletes

There are historical assertions that ECG patterns differ among the healthy black and white population. In the early 1950s, certain ECG findings such as, J-point, left ventricular hypertrophy (LVH) and ST-segment elevation were observed more commonly in young black men without heart disease compared to white men.^17-19 Ethnic specific ECG differences, particularly in black athletes, later emerged among American football players.^20,21 Using the earliest ECG criteria proposed by Pelliccia et al., abnormal ECGs were significantly more common among black athletes than white athletes (30% vs. 13%; p<0.0001) by a factor of >2:1.²² In a National Football League study, black race was the only predictor of an abnormal ECG. This difference was still observed when evaluating ECG patterns considered to be "distinctly abnormal" (6% in blacks vs. 2% in white; p = 0.0005).²² Similar racial differences were also observed in soccer athletes.23 ECG criteria for LVH were observed more commonly in black athletes than white athletes (89% vs. 42%; p <0.001).²³ While early repolarization, specifically ST-segment elevation with concave shape, was present with similar prevalence between white and black athletes, domed or convex shaped ST-segment elevation was observed almost exclusively in black athletes (34% vs. 1%; p<0.001).²³ Deeply inverted T-waves (TWI), greater than 2 mm, were more commonly observed in blacks than white athletes (14% vs. 3%; p<0.05), of which almost half of the TWI among black athletes were confined to the anterior leads.²³ With the criteria proposed by Pelliccia et al., isolated R/S-wave voltage, LVH, TWI and convex ST elevations were also found more commonly in black athletes.

Racial differences between athletes are also evident with the criteria proposed by the ESC.⁹ The prevalence of group 2 ECG patterns (Table 2) were higher in black athletes (18%-58%) compared to white athletes (6%-21%).^13,15 Interestingly, Chandra et al., evaluated the ESC criteria in athletes and non-athletes and observed that in contrast with white individuals in whom the prevalence of group 2 ECG patterns were similar in non-athletes and athletes (21.5% vs. 21.3%; p =0.826), the prevalence of group 2 ECG patterns almost doubled in black athletes compared with black non-athletes (57.7% vs. 28.5%; p<0.001).¹³ T-wave inversion, mainly confined to the anterior leads, was the most common group 2 ECG pattern observed in black athletes.^13,15 T-wave inversions were also more common in black female athletes.²⁴ Black ethnicity again demonstrated the strongest association with group 2 ECG patterns as was previously observed by Magalski et al.¹³ ESC criteria decreased the percentage of both black and white athletes with abnormal ECGs when compared to Pelliccia's criteria, but continued to demonstrate a higher prevalence of abnormal ECGs among blacks. While isolated R/S-wave voltage changes, TWI, convex ST segment elevations changes, and LVH were the most prevalent abnormal ECG patterns with Pelliccia's criteria, the ESC criteria showed TWI and atrial enlargement as the most prevalent abnormal ECG pattern among black athletes compared to white athletes.

An emerging contemporary criteria proposed by Sheikh et al., referred to as the "Refined criteria", similarly found consistent ethnic variation.¹² Notably the refined criteria demonstrated improved specificity when compared to Seattle and ESC criteria.¹² Using the ESC criteria, 40.4% of black athletes had abnormal ECG patterns compared to 16.4% of white athletes, while Seattle criteria observed a reduction in abnormal ECGs in both races (18.4% in blacks vs. 7.1% in whites) but the ethnic difference persisted.^12,13,15 The reduction in abnormal ECGs was driven by an increase in the QTc cut-offs, but more importantly, the recognition that isolated anterior TWI in asymptomatic black athletes is a benign finding (Figure 1).¹⁴ However, the Refined criteria classified less black (11.5%) and white athletes (5.3%) with abnormal ECGs compared to Seattle criteria. This was largely due to categorizing isolated atrial enlargement or axis deviation as training related ECG patterns since prior studies showed poor correlation of those ECG patterns to underlying cardiac disorders (Figure 2).^25,26 Nonetheless, black athletes consistently had more abnormal ECGs than whites using the refined criteria, of which TWI (located mainly in the inferior and lateral leads) was the main ECG pattern abnormality between two ethnicities (6% in blacks vs. 3.5% in whites)(Figure 3).¹²

Figure 1

Figure 2: Asymptomatic 19-year-old female rower

Figure 3

Other Ethnic Specific ECG Findings

Recent data are widening the spectrum of ethnic specific differences in ECG findings. Using the ESC criteria, West-Indians had comparable prevalence of group 2 ECG changes as white athletes (7.9% vs. 5.8%).¹⁵ Arabic athletes have a similar prevalence of abnormal ECG findings as white athletes, regardless of which ECG criteria are used.¹⁴ Interestingly, ECG differences were observed even among Africans depending on region.^27,28

Gender Specific ECG Findings

Despite the increasing studies in athletes, there is limited data on gender specific ECG differences. Using the Pelliccia's criteria, women had more normal ECGs when compared to men (78% vs. 55%; p=<0.01) in European Olympic athletes.¹¹ Similar findings were replicated in American collegiate athletes (69.6% vs. 60.6%; p=0.03).²⁹ Overall, both the European and American cohorts did observe that "distinctly abnormal" ECGs were significantly higher in men than women (17% vs. 8%; P<0.001 and 14.7% vs. 5.5%; P<0.001 respectively).^11,29

Using the 2010 ESC criteria, a similar gender specific difference was observed.^11,30 However, a higher proportion of athletes were considered normal (89% in women vs. 80% in men; p=0.004).³⁰ Left atrial enlargement, left axis deviation, and TWI were more prevalent in men than women.

While earlier criteria noted differences between men and women, Seattle criteria suggests otherwise. The Seattle criteria failed to show a statistically significant difference between genders (96% of men vs. 97% of women with normal ECGs; p=0.55).^10,31 The lack of gender difference seen in the Seattle compared to the ESC criteria is largely explained by the "stricter re-definition" of abnormal T wave inversions (TWI), QTc interval, and left atrial enlargement in the former.³¹ In summary, there is a relative dearth of data on gender specific ECG differences. Further studies are needed to delineate if specific abnormal ECG patterns are more prevalent based on gender.

Future Directions

As ECG criteria have evolved, the specificity in detecting cardiac abnormalities has improved without effecting sensitivity. Important among contemporary criteria is the recognition that certain ethnic related ECG patterns are benign. However, defining ethnicity is quite complex as seen by varying prevalence of abnormal ECGs even amongst African athletes.²⁸ Future studies should continue to focus on ethnic and gender specific differences as well as consider age and sport specific ECG differences. Although addition of ECGs in PPE increased the sensitivity to identify cardiomyopathies, ion channel disorders, and ventricular pre-excitation, there are other anomalies, such as anomalous origin of the coronary artery and aortic dilation responsible for sudden cardiac death that are not detected by ECG.⁷

Conclusion

Over the past decade, ECG criteria for athletes have rapidly evolved. Ethnic specific criteria increase the specificity of ECG as a screening method. However, black athletes continue to have more abnormal ECG patterns such as T-wave inversions compared to other ethnicities. There is limited data on gender specific differences. More studies are needed to better incorporate the role of gender, ethnicity, age, level of training, and sporting discipline into the interpretation of ECGs in athletes.

References

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Keywords: Arrhythmia, Sinus, Athletes, Atrial Fibrillation, Atrioventricular Block, Bradycardia, Bundle-Branch Block, Cardiomegaly, Exercise-Induced, Cardiomyopathies, Coronary Vessels, Death, Sudden, Cardiac, Echocardiography, Electrocardiography, Heart Conduction System, Hypertrophy, Right Ventricular, Hypertrophy, Left Ventricular, Prevalence, Tachycardia, Ventricular Premature Complexes, Sports

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