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ECG and morphologic adaptations in Arabic athletes: are the European Society of Cardiology's recommendations for the interpretation of the 12-lead ECG appropriate for this ethnicity?
  1. Nathan R Riding1,2,
  2. Othman Salah1,
  3. Sanjay Sharma3,
  4. François Carré4,
  5. Keith P George2,
  6. Abdulaziz Farooq1,
  7. Bruce Hamilton5,
  8. Hakim Chalabi6,
  9. Gregory P Whyte2,
  10. Mathew G Wilson1
  1. 1Department of Sports Medicine, ASPETAR, Qatar Orthopaedic and Sports Medicine Hospital, Doha, Qatar
  2. 2Research Institute for Sport and Exercise Science, Liverpool John Moores University, Liverpool, Merseyside, UK
  3. 3Department of Cardiovascular Sciences, St Georges University of London, London, UK
  4. 4Rennes 1 University, Pontchaillou Hospital, INSERM U 642, Rennes, France
  5. 5Departments of Sports Medicine, High Performance Sport New Zealand, Millenium Centre Auckland, New Zealand
  6. 6CMOs office, ASPETAR, Qatar Orthopaedic and Sports Medicine Hospital, Doha, Qatar
  1. Correspondence to Dr Mathew Wilson, Department of Sports Medicine, ASPETAR Qatar Orthopaedic and Sports Medicine Hospital, Doha PO Box 29222, Qatar; mathew.wilson{at}aspetar.com

Abstract

Aims To examine the cardiac structure and function of Arabic athletes and to establish if the European Society of Cardiology (ESC) guidelines for the interpretation of an athlete's ECG are applicable to this ethnicity.

Methods 600 high-level Arabic, 415 Black African, 160 Caucasian male athletes (exercising ≥6 h/week) and 201 Arabic controls presented for ECG and echocardiographic screening.

Results 9 athletes (0.7%) were identified with a cardiac pathology associated with sudden cardiac death. Two Arabics (0.3%) and five Black Africans (1.2%) were diagnosed with hypertrophic cardiomyopathy; a prevalence four times greater in Black African compared to Arabic athletes. Arabic athletes had significantly greater (p<0.05) left ventricular (LV) end-diastolic diameters, maximal LV wall thicknesses and LV mass compared with controls; yet were significantly smaller than Black African and Caucasian athletes. The percentage of athletes demonstrating LV hypertrophy (≥12 mm) was comparable between Arabic, Black African and Caucasian populations (0.5%, 0.5% and 0.6%, respectively). There was no difference in the frequency of an uncommon and training-unrelated ECG between Arabic and Caucasian. However, Black Africans demonstrated a significantly greater prevalence than Arabic and Caucasian athletes (20% vs 8.4% and 6.9%, p<0.001); specifically more right/left atrial enlargement and T wave inversion.

Conclusions Arabic athletes present significantly smaller cardiac dimensions than Black African and Caucasian athletes. There was no significant difference between the frequency of an uncommon and training-unrelated ECG between Arabic and Caucasian athletes. Therefore, the use of ESC guidelines for the interpretation of an athlete's ECG is clinically relevant and acceptable for use within Arabic athletes.

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Introduction

Regular and sustained intensive physical activity is associated with a number of electrophysiological and structural cardiac adaptations, all of which enhance diastolic filling. These spectral modifications are collectively referred to as the ‘athlete's heart’. The majority of studies investigating the ‘athletes heart’ are based on cohorts of Caucasian athletes. However, there is mounting evidence that an athlete's ethnicity has an important effect on the electrical and structural cardiovascular adaptations to prolonged and intensive exercise.1–4

The 2012 London Olympics saw 13 Arabic nations participate in the games. While both the International Olympic Committee (IOC), Fédération Internationale de Football Association (FIFA) and the European Society of Cardiology (ESC) recommend cardiovascular screening before undertaking competitive sport, there is little data on the impact of the Arabic ethnicity upon the cardiac manifestations of the athlete's heart.4 This lack of ethnic-specific data5 increases the risk of generating false-positive diagnoses and unnecessary disqualifications from competitive sport, when attempting to differentiate physiological adaptation from inherited cardiac pathology associated with sudden cardiac death (SCD). Thus, the aim of the study was to examine the cardiac structure and function of high-level Arabic athletes when presenting for preparticipation cardiovascular screening, using ECG and echocardiography.

Methods

Ethical approval was obtained from the Shafallah Medical Genetics Centre ethics committee, with all athletes completing informed consent in either Arabic or English.

Participants

Between November 2010 and June 2012, 1175 high-level male athletes (exercising ≥6 h/week) presented at our institution for preparticipation cardiac screening, of which 600 were Arabic, 415 Black African and 160 Caucasian. As previously described,4 the term ‘West-Asian’ denotes individuals of Gulf or Middle-Eastern descent, and “Black African” denotes individuals of African descent. For ease of reference, West-Asian athletes will be termed Arabic from this point onwards. Arabic athletes were recruited from seven Gulf States (Qatar, Bahrain, Oman, UAE, Kuwait, Yemen and Saudi Arabia) and five Middle-Eastern countries (Egypt, Jordan, Palestine, Iraq and Lebanon). Black African athletes from nine African countries (Sudan, Somalia, Ghana, Nigeria, Chad, Ivory Coast, Senegal, Cameroon and Ethiopia) were also recruited alongside Caucasian athletes from the USA, Canada, Australia, Russia, Bosnia, Serbia and Croatia. All Arabic athletes were compared to a cohort of 201 male Arabic control participants, who were not sedentary, but exercised ≤2 h/week. Strict exclusion criteria included individuals that had undergone previous cardiovascular screening with ECG and echocardiography. This was important as the population truly reflected those individuals who had not been excluded from competitive sport on the suspicion of harbouring an inherited cardiac pathology.

Preparticipation cardiovascular screening

All players were screened using a cardiovascular precompetition medical assessment form. Players completed the questionnaire regarding family history and personal symptoms in collaboration with an Arabic-speaking, French-speaking or English-speaking cardiac nurse. Measurement of height, body mass, left brachial artery blood pressure (BP), precordial auscultation in supine and standing positions, and assessment for any physical characteristics of Marfan's syndrome were undertaken by a Sports Medicine Physician.

Resting 12-lead ECG

A standard 12-lead ECG was obtained using a GE Mac 5500 (New York, USA) after a period of 5 min rest in the supine position. All ECGs were reported independently by two experienced investigators (OS and MGW) using criteria previously published4; with the third opinion sought from two international cardiologists (SS and FC). ECG characteristics were classified into ‘common and training-related’ and ‘uncommon and training-unrelated’ traits according to the recent 2010 ESC report.6

Echocardiography

Echocardiographic examination was performed using a commercially available ultrasound system (Philips, USA). Images of the heart were obtained in the standard planes, as previously described.7 The left ventricular (LV) wall thickness was measured from two-dimensional short-axis views in end-diastole, with the greatest measurement within the LV wall defined as the maximal LV wall thickness (mLVWT). M-mode echocardiograms derived from two-dimensional images in the parasternal long axis were used for the measurement of LV end-diastolic diameter (LVED), left atrial (LA) and aortic root (Ao) diameter according to American Society of Echocardiography standards,8 with LV diastolic volume (LV vol D) derived using Simpson's biplane methodology. LV mass (LVM) was calculated using the formula of Devereux,9 but was also scaled for body surface area (BSA). LV diastolic function was assessed using pulsed-wave Doppler recordings from apical four-chamber orientations. All data were analysed offline and a minimum of three cardiac cycles were averaged for all indices. For the tissue Doppler assessment of E’, the apical four-chamber orientation was utilised and a 2 mm sample volume was positioned at both the septal and lateral wall aspect of the mitral valve annulus ensuring the best alignment between wall motion and the ultrasound beam. The Nyquist limit was set between 10 and 35 cm/s. Peak early diastolic (E′) tissue myocardial velocity was recorded and E/E′ was calculated.

Further evaluation and follow-up

Athletes demonstrating symptoms, a family history of SCD, and echocardiographic and/or ECG abnormalities considered to represent pathological LV hypertrophy (LVH) were investigated further with 24 h ECG, maximal exercise testing and cardiac MRI to evaluate the broader phenotype of common cardiomyopathic processes such as hypertrophic cardiomyopathy (HCM) and arrhythmogenic right ventricular cardiomyopathy (ARVC). A diagnosis of disease was established using published criteria.10 All athletes were tracked for a minimum of 3 years.

Statistical analysis

Data were analysed using SPSS V.19 (Illinois, USA); presented as mean±SD (range) and percentage where appropriate. One way analysis of variance, using Bonferroni adjustments if applicable, was used to identify differences in anthropometric, ECG and echocardiographic characteristics between athlete ethnicities. Strength associations between cardiac structure against the athletes’ BSA, blood pressure and ECG characteristics were calculated via a Pearson's correlation coefficient (r). Where appropriate, an independent sample t test or χ2 test was used to assess the presence of confounders between participants with uncommon ECG findings and T wave inversion against cardiac structure, BSA and blood pressure. Since no confounders were detected, OR and 95% CI were determined between ethnicities. A p value <0.05 was considered significant.

Results

Identified cardiac pathology

Nine athletes (0.7%) were identified with a cardiac pathology associated with SCD, and were excluded from further analysis (table 1). Two Arabics (0.3%) and five Black Africans (1.2%) were diagnosed with HCM; with Black Africans having a prevalence of HCM four times greater than Arabic athletes. Four athletes were referred to a specialist cardiologist in their respective home countries, and three remain under the management of our international cardiologists (SS and FC). Two Arabic athletes demonstrated ECG diagnostic of Wolff-Parkinson-White syndrome and underwent electrophysiological study. Both were ablated as a result of electrophysiological findings, and returned to full competition following a 2-month postoperative recovery period.

Table 1

Outcomes of nine athletes identified with a cardiac disease associated with SCD

Demographics

Detailed demographics of the remaining athletes and controls are presented in table 2. Athletes competed in a range of competitive sports (n=23), with high-intensity intermittent sports dominating (soccer (60%), volleyball (8.8%), handball (8.8%) and basketball (8.5%)). Arabic athletes were significantly younger, smaller and lighter; resulting in a reduced BSA than that of their Black African and Caucasian counterparts. Arabic athletes presented with a greater incidence of a family history of SCD (<35 years) than Black African and Caucasian athletes (7.4% vs 3.9 and 2.5%, p<0.05). Despite Arabic athletes demonstrating significantly lower systolic BP's than Black African and Caucasian athletes, 17 football players were given a 24 h BP Holter monitor owing to systolic BP value >140 mm Hg at initial screening. There was no ethnic distinction in prevalence, with all subsequently reported as normal and returning to full competition.

Table 2

Comparison of demographic, personal symptoms and family history parameters between Arabic, Black African and Caucasian athletes, and Arabic controls

Ethnic differences in cardiac structure and function

Arabic athletes had a significantly greater (p<0.05) Ao, LA, LVED, mLVWT, LVM (LVM scaled) and E/A compared to controls (table 3). However, Arabic athletes were significantly (p<0.05) smaller in all absolute cardiac structural parameters than both Black African and Caucasian athletes. The percentage of athletes demonstrating LVH (≥12 mm) was not significantly different between Arabic, Black African and Caucasian populations (0.5%, 0.5% and 0.6%, respectively), with no athlete exceeding an mLVWT of 14 mm (Arabic 14 mm, Black African 14 mm and Caucasian 13 mm).

Table 3

Comparison of echocardiographic parameters between Arabic, Black African and Caucasian athletes, and Arabic controls

Caucasian athletes demonstrated a significantly (p<0.05) greater LVED, LV vol D and LVM than both Arabic and Black African athletes; with no difference in mLVWT between Black African and Caucasian athletes. While E/E′ was significantly reduced in Caucasian athletes versus Arabic and Black African, all athletes across ethnicities demonstrated normal diastolic function. For all three ethnicities, there was a significant association between resting systolic BP and BSA, LVED, mLVWT and LVM (p<0.001).

Ethnic differences in ECG features

In terms of common and training-related ECG changes, Arabic athletes demonstrated a greater frequency (p<0.05) of sinus bradycardia, first-degree AV block, incomplete right bundle branch block, voltage criteria for LVH and early repolarisation than controls (table 4). Apart from an increased incidence of pathological Q waves (>3 mm in depth in two or more leads (except III and aVR); 4% vs 1%, p<0.05), Arabic athletes did not differ in the prevalence of uncommon and training-unrelated ECG changes compared with controls. There was also no difference between Arabic and Caucasian in the frequency of an uncommon and training-unrelated ECG. However, a significantly higher prevalence of uncommon and training-unrelated ECG was observed in Black African than Arabic and Caucasian athletes (20% vs 8.4% and 6.9%, p<0.001), specifically more right atrial enlargement (RAE), left atrial enlargement (LAE) and T wave inversion. Accordingly, Black African athletes were significantly more likely to have uncommon and training-unrelated ECG changes than Arabic and Caucasian athletes (OR 2.65, 95% CI1.81 to 3.9, p<0.001 and OR 3.3, 95% CI1.7 to 6.35, p<0.001, respectively).

Table 4

Comparison of ECG parameters between Arabic, Black African and Caucasian athletes, and Arabic controls

Ethnic differences in repolarisation changes

Arabic athletes demonstrated a higher prevalence of early repolarisation than controls (82% vs 73%, p<0.05; table 5). Black African and Caucasian athletes demonstrated a greater prevalence of early repolarisation than Arabic athletes (88% and 88% vs 82%, respectively), with no difference between Black African and Caucasian athletes.

Table 5

Comparison of ECG repolarisation parameters between Arabic, Black African and Caucasian athletes, and Arabic controls

There was no difference in the prevalence of T wave inversion between Arabic and controls (2% vs 2%), or between Arabic and Caucasian athletes (2% vs 1%, table 5). However, Black African athletes demonstrated a significantly (p<0.001) greater prevalence of T wave inversion than Arabic and Caucasian (13% vs 2% and 1%, respectively). The most common pattern was T wave inversion isolated to V1–V4 (11% vs 1% and 1%, respectively). However, Black Africans also demonstrated significantly (p<0.001) more isolated inferior (n=14, 3%), isolated lateral (n=10, 2%) and inferolateral T wave inversions (n=8, 2%) than Arabic and Caucasian athletes; with five Black Africans also demonstrating deep (≥−0.2 mV) inferolateral T wave inversion. Accordingly, athletes of Black African descent were significantly more likely to have T wave inversion than Arabic and Caucasian athletes, respectively (OR 8.33, 95% CI 4.17 to 16.61, p<0.001 and (OR 11.22, 95% CI 2.7 to 46.67, p<0.001).

Further cardiovascular examination

All 65 athletes (10 Arabic, 53 Black African and 2 Caucasian) and 3 Arabic controls with T wave inversion, and 3 athletes (1 Arabic and 2 Black African) with an mLVWT≥13 mm, underwent maximal exercise testing and 24 h Holter monitoring, which were normal. Special consideration was paid to 10 asymptomatic athletes (1 Arabic, 8 Black African and 1 Caucasian) with inferolateral T wave inversion. Despite normal echocardiograms, 24 h Holter monitoring and exercise tests, all 10 underwent cardiovascular MRI (CMRI) with gadolinium. None demonstrated any structural abnormalities or late enhancement to indicate an underlying cardiomyopathy, and were given medical clearance to compete. Given the uncertainty regarding the long-term significance of inferolateral T wave inversion we have recommended yearly evaluation and advised the athletes to seek immediate medical attention in the event of cardiac symptoms.

Discussion

The correct differentiation of physiological cardiac adaptation owing to exercise from an inherited or congenital cardiac pathology is paramount, to identify athletes at risk of SCD. This study examines the electrophysiological and structural cardiac adaptations associated with exercise in 600 high-level Arabic male athletes, competing in a wide variety of sporting disciplines, compared with cohorts of high-level Black African and Caucasian athletes.

Prevalence of HCM

Our study identified nine athletes (0.7%) with a disease associated with SCD; with the prevalence of HCM in Black African (1.2%) four times greater than Arabic (0.3%) athletes. HCM is cited as the leading cause of sudden death in young athletes.11 However, the prevalence of HCM in Black African and Arabic athletes is approximately 13 times and 3 times greater, respectively, than that observed in previous studies among Caucasian athletes; estimated at approximately 0.1%.12 This higher prevalence is supported by a previous ECG-only screening study in Arabic and Black African athletes, that reported an SCD disease prevalence of 0.5% and 1%, respectively.4 Data collected in our facility suggest that up to 60% of our Black African athletes have never seen a physician before presenting for preparticipation screening. This in part may explain the unusually high prevalence of HCM in this previously unexamined and unselected population.

Ethnic differences in cardiac structure and function

The present study revealed that Arabic athletes have significant, yet modest increases in cardiac dimensions compared with those in controls; yet all cardiac dimensions in all parameters are significantly smaller than Black African and Caucasian athletes. In all Arabic athletes, absolute values did not exceed predicted normal upper limits, and are in line with data established from Caucasian athletes.12 The prevalence of LVH (mLVWT ≥ 12 mm) in athletes was comparable between all three ethnicities. Our study did not observe the greater frequency of LVH that has previously been reported in athletes of Black African ethnicity,13 with Black African athletes demonstrating an LVH prevalence comparable within their Arabic and Caucasian counterparts (0.5%, 0.5% and 0.6%, respectively). However, when examining the prevalence of a wall thickness ≥10 mm, Black African athletes demonstrated a trend for significantly (p<0.001) greater wall thicknesses that Arabic and Caucasian athletes (25% vs 12% and 14%, respectively), supporting the concept that certain Black African athletes may gravitate towards a physiologically thicker LV wall.

Ethnic differences in ECG features

Uncommon and training-unrelated ECG changes raising the suspicion of structural heart disease were reported in 12% of the athletes. Supported by previous data from an ECG-only investigation in Arabic athletes, there was no significant difference between the frequency of uncommon and training-unrelated ECG changes between Arabic and Caucasian athletes (8.4% vs 6.9%).4 However, Black African ethnicity continues to be positively associated with frequencies of uncommon ECG findings (20%), with Black African descent an independent predictor of uncommon ECG findings when compared with Arabic (2.7 : 1) and Caucasian (3.3 : 1) athletes. Specifically, Black African athletes demonstrate more RAE, LAE and T wave inversion than both Arabic and Caucasian athletes.

T wave inversion conundrum

The presence of T wave inversion is of major concern, as these ECG alterations are a recognised manifestation of HCM and ARVC. In total, 65 athletes and 3 controls displayed T wave inversion (a prevalence of 5.6%). Similar to previous studies,13 the most common pattern was T wave inversion isolated to V1–V4 (11% Black African vs 1% Arabic and 1% Caucasian), that was morphologically asymmetric or biphasic and proceeded by convex ST-segment elevation, but never ST-segment depression. Further work is required to understand the clinical significance behind the increased prevalence of isolated inferior and lateral T wave inversions in Black African, and its relationship with inherited cardiac pathology.

Deep T wave inversions in the inferolateral leads are common in HCM. The present study observed 10 asymptomatic athletes without a family history of SCD (0.9%; 1 Arabic, 8 Black African and 1 Caucasian) demonstrating inferolateral T wave inversions with normal echocardiograms. Subsequent investigations including CMRI, failed to identify phenotypic features of HCM or AVRC in any athlete. Comparison of T wave morphology in black patients with HCM demonstrates that T wave inversions are usually confined to the lateral leads (80% of cases); whereas T wave inversion in leads V1–V4 are only observed in 3–4% of HCM patients.3 Accordingly, we advise caution and request annual follow-up in the asymptomatic athlete who presents with inferolateral T wave inversion but normal or inconclusive imaging.14

Clinical implications for Arabic athletes

The present study demonstrates that the upper limits of physiological LVH established within Caucasian athletes,12 are clinically relevant to Arabic athletes. Accordingly, any Arabic athlete who presents values in excess of 12 mm should be viewed with caution, and should prompt further investigation to identify the underlying mechanism. Finally, the prevalence of an uncommon and training-unrelated ECG is comparable between Arabic and Caucasian athletes. Thus, the ESC guidelines for the interpretation of an athlete's ECG, based upon data derived from Caucasian athletes, are applicable to the Arabic athletic population.6 Consequently, the equivalent rate of false-positive ECG between Arabic and Caucasian athletes should be considered acceptable for the establishment of a preparticipation cardiovascular screening programme in athletes of Arabic ethnicity.

Limitations

All athletes with T wave inversion were followed for only 3 years. Yet the precise significance of such repolarisation changes, especially the high prevalence of inferolateral T wave inversion in Black African athletes, remains unresolved. There is no ‘gold-standard’ test for the diagnosis of the presence (or absence) of heart diseases in these athletes. Although genetic testing is the most specific method of diagnosing HCM, the diverse genetic heterogeneity of HCM and incomplete knowledge of all-causal mutations lend poor sensitivity to this diagnostic tool.

Conclusion

Arabic athletes have significant, yet modest increases in cardiac dimensions compared with Arab controls; yet all cardiac dimensions in all parameters were significantly smaller than Black African and Caucasian athletes. There was no significant difference between the frequency of uncommon and training-unrelated ECG changes between Arabic and Caucasian athletes. Therefore, the use of the ESC guidelines for the interpretation of an athlete's ECG, both established from data derived from Caucasian athletes, are clinically relevant and acceptable for use within Arabic athletes.

What this study adds

  • Arabic athletes have significant, yet modest increases in cardiac dimensions compared with Arab controls; yet cardiac dimensions in all parameters were significantly smaller than Black African and Caucasian athletes.

  • There was no significant difference between the frequency of uncommon and training-unrelated ECG changes between Arabic and Caucasian athletes.

  • Use of the ESC guidelines for the interpretation of an athlete's ECG, derived from data within Caucasian athletes, are clinically acceptable for use within Arabic athletes.

How might it impact on clinical practice in the near future

  • The rate of false-positive ECG between Arabic and Caucasian athletes should be considered acceptable for the establishment of a preparticipation cardiovascular screening programme in athletes of Arabic ethnicity.

  • Observing T wave inversion in both Arabic and Caucasian athletes (≥2 mm) in ≥2 contiguous leads (but not V1, aVR and III) requires further examination.

  • Future research should examine the mechanisms behind the higher prevalence of hypertrophic cardiomyopathy in Black African athletes than Arabic and Caucasian athletes.

Acknowledgments

Lead by Mrs Caroline Buckler, we acknowledge the sterling efforts of Aspetar's athlete screening team in the data collection; Nelly Khalil, Pascal Tahtouh, Farah Demachkieh, Manal Al Tarany, Zahia Al Khoury, Ezzoubair Moustaati and Diana El Chamaa.

References

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Footnotes

  • Contributors NRR and OS contributed to the study design, data collection, and preparation of the manuscript. SS, KG, BH, GPW and FC contributed to the interpretation of data and revision of the manuscript for intellectual content. AF contributed to data analysis. HC contributed to revision of the manuscript for intellectual content. MGW was the lead for this study and contributed to the study design, data collection, quality control of data, and preparation of the manuscript.

  • Competing interests None.

  • Ethics approval Shafallah Medical Genetics Center, Doha, Qatar.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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