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Cardiac adaptations to intense physical exercise in African/Afro-Carribean athletes

An article from the e-journal of the ESC Council for Cardiology Practice

The cardiac manifestations of prolonged exercise are determined by several demographic factors including ethnicity. Substantial left ventricular hypertrophy and marked repolarisation changes have been observed in recent studies in athletes of African/Afro-Caribbean origin, which overlap with the phenotypic manifestations of those of hypertrophic cardiomyopathy - the commonest cause of sudden death in young athletes. This article focuses on the spectrum of electrocardiographic and echocardiographic manifestations of black athlete’s heart and provides practical information in differentiating cardiac pathology from physiological adaptation. 

Rehabilitation


Background

Participation in regular and prolonged physical exercise is associated with unique adaptations in cardiac structure and function in a phenomenon termed ‘athlete’s heart’. Cardiac remodelling comprising of increased ventricular wall thickness and increased cavity dimensions permit enhanced filling of the left ventricle in diastole and augmentation of stroke volume, even at rapid heart rates, to facilitate the generation of a large and sustained cardiac output (1). Such changes are reflected on the surface 12-lead electrocardiography (ECG) and 2-D echocardiogram. The magnitude to which this adaptation occurs is influenced by several demographic factors of the athlete including age, gender, ethnicity and body surface area as well as the sporting discipline (2). Previous studies in Caucasian athletes have demonstrated that the most advanced changes occur in adult male athletes participating in endurance sport and on rare occasions, may overlap with those observed in individuals with sinister cardiac disorders, notably cardiomyopathies. In contrast there are few data in athletes of African/Afro-Caribbean (black) ethnicity.

Consideration in black athletes

The past 3 decades have witnessed an explosion in the number of black athletes participating in competitive sport in Europe and the US with representation at national and international level. Levels of participation in certain sporting disciplines are often disproportionate to the respective populations in various countries, for example, in the UK only 2% of the population is black but 20% make up the English Premier Football League. In the US, only 13% of the population is of black origin yet 75% of the National Football League and National Basketball Association are of black ethnicity.

In parallel with the increased participation rates amongst black athletes, there has been increased awareness of sudden cardiac death in sport from the cardiomyopathies and ion channel diseases. Worryingly, the prevalence of sudden cardiac death, particularly from hypertrophic cardiomyopathy (HCM), has been consistently demonstrated to be significantly higher in black athletes when compared to their white counterparts (3-5). Data from Italy, where athletes undergo mandatory pre-participation cardiovascular screening incorporating the 12-lead ECG, has shown that individuals with cardiomyopathy can be readily identified and subsequently deaths amongst competitive athletes can be minimised (6). So compelling is the evidence, that the Italian pre-participation screening model has been adopted by various sporting organisations including the International Olympic Committee, FIFA and UEFA. However recommendations enabling the differentiation of physiological ECG changes from those suggestive of pathology are derived solely from Caucasian athletes.

Previous studies in young healthy black individuals demonstrate that they exhibit more marked repolarisation changes on ECG and studies in hypertensive patients reveal a greater magnitude of left ventricular hypertrophy (LVH) in black individuals compared with white individuals with similar blood pressures (7,8). Thus, it can be expected that the pre-load and after-load stresses associated with exercise may result in physiological cardiac manifestations in black athletes which overlap with disease phenotypes, particularly HCM, resulting in unnecessary over-investigation or unfair disqualification from competitive sport.

There are few data on ECG and echocardiographic manifestations in black male athletes from the US which have shown a higher prevalence of LVH and ECG abnormalities, including bizarre repolarisation changes, compared with white athletes (9,10).  However, the studies are associated with a number of limitations.  The majority have focussed on American football players of large body surface area (2.2-2.4m2) and would not be regarded as representative of the majority of black athletes competing in Europe.  The conclusions from these studies assume that all black athletes are a homogeneous population yet the demographic differences between an East African long distance runner and an Afro-Caribbean sprinter could be significant. There are no data on female black athletes and adolescent black athletes or any longitudinal follow-up data on the precise significance of the ECG and echocardiographic manifestations of cardiac adaptations in black athletes.

Structural Cardiac Changes

A recent study by Basavarajaiah et al. from the UK compared 300 asymptomatic and normotensive black athletes with 300 white athletes of similar age and body surface area who participated in identical sporting disciplines (11). Six major sporting disciplines were examined including soccer, field and track athletics, basketball, boxing. All athletes participated at regional or national level and trained for an average 14 hours per week. Comparison of echocardiographic data demonstrated that the left ventricular wall thickness (LVWT) in black athletes was on average 13% greater in black athletes than in white athletes (11.3mm vs 10.0mm respectively; p<0.001).  Irrespective of the sporting discipline, black athletes always demonstrated greater LVWT than white athletes in this study. Of the black athletes, 18% exhibited a LVWT exceeding 12mm and 3% showed a wall thickness ≥ 15mm In contrast to the white athletes, which could be consistent with morphologically mild HCM. In contrast, only 4% of white athletes had a LVWT of greater than 12mm and none revealed a LVWT of > 14mm (Figure 1). None of the black athletes with LVH exhibited other phenotypic features of HCM on echocardiography, CMR, exercise stress testing or 24 hour ECG monitoring. Also, none of the black athletes exhibited a LVWT > 16mm, therefore, it would be reasonable to infer that wall thickness measurements of a greater magnitude could be consistent with a diagnosis of HCM.

One limitation of this study, however, is that it focussed only on six sporting disciplines where black individuals excelled to the same level as white athletes. In particular, disciplines such as rowing, cycling or swimming where male white athletes have been shown to exhibit LVH were excluded as black individuals have low participation rates in these disciplines (2).  More recent data from collaboration between the UK and France addressed this by comparing 911 black male athletes with 858 white male athletes participating at national level in 22 different sporting disciplines (12). The study demonstrated that 13% of all black athletes had a LVWT of more than 12mm compared with just 2% of white athletes but again none of the black athletes had a wall thickness of greater than 16mm, indicating that in this particular ethnic group, a LVWT of 16mm should be considered the upper limit of physiological LVH in male athletes.
ECG Changes.

Sinus bradycardia, voltage criteria for chamber enlargement and repolarisation abnormalities, including ST segment elevation, on the resting ECG are common findings in athletes (Figure 2). Data from the US evaluating 1,959 American football players demonstrated ECG abnormalities were twice as common in black athletes compared to white athletes. Black athletes revealed diverse ECG abnormalities, including LV hypertrophy and repolarisation changes in 25% of cases. Deep T wave inversions (> -0.2 mV), commonly associated with cardiomyopathy, were reported in 2.6% of black athletes in comparison to just 0.2% of white athletes (10).

The study previously described by Basavarajaiah et al. (11) also compared ECG changes in 300 black athletes and 300 of their white counterparts and demonstrated that voltage criteria for LVH (using Sokolow-Lyon criteria) was significantly more prevalent in black athletes than in white athletes (68% vs 40% respectively, p <0.001). There was also a significantly higher prevalence of repolarisation abnormalities in black athletes in comparison to white athletes, specifically, ST segment elevation (85% vs 62% respectively, p <0.001) and deep T wave inversion (12% vs 0% respectively, p <0.001). Of particular relevance was the fact that deep T wave inversions in black athletes were confined predominantly to leads V1-V4 of the 12-lead ECG.

Papadakis et al. reported similar findings in a large cohort of black British and French athletes. Deep T wave inversions were identified in 16% of black athletes compared to just 2% of white athletes and were predominantly confined to leads V1-V4 (12). Further comprehensive clinical evaluation proved no evidence of pathology in these athletes. In small subsets the group demonstrated resolution of such changes within 6 weeks of detraining (usually during the off season) suggesting that T wave inversions in leads V1-V4 are likely to represent a benign finding in black athletes.  During a mean follow up of 69 months, there was one case of aborted sudden cardiac death in an athlete who exhibited deep T wave inversions in the inferior and lateral leads but a structurally normal heart. A second athlete with similar changes was diagnosed with HCM and disqualified from competitive sport, therefore the authors recommend caution when attributing deep T wave inversions in the inferior or lateral leads to physiological adaptation. Indeed it is our bias that deep T wave inversions in the inferior and/or lateral leads are harbingers of cardiac pathology and a risk factor for potentially fatal ventricular arrhythmias and should be investigated comprehensively. Other ECG patterns indicating cardiac pathology include pathological Q waves, ST segment depression > 1mm or left bundle branch block.

Female black athletes and adolescent black athletes

Female Black Athletes

Data from adult male athletes cannot simply be extrapolated to female or adolescent athletes since age and sex have been shown to have an important influence on cardiac adaptation in athletes (13).  A recent study by Rawlins et al. evaluating ethnic differences in cardiac adaptation to exercise in 440 nationally ranked female athletes (55% black vs 45% white) using 12-lead ECG and echocardiography addressed this issue (14). Female athletes of similar age, body surface area and participating in similar sporting discipline were studied and results demonstrated interesting similarities with those observed when comparing male black and white athletes. Even in females, black athletes revealed a greater LVWT than white athletes (9.2 mm vs 8.6mm representing a 7% difference between the two groups, p <0.001). Of the female black athletes, 3% demonstrated a wall thickness exceeding 11mm (but never > 13mm). In contrast, none of the white athletes had a LVWT in excess of 11mm (Figure 3).

Comparison of ECG changes in female athletes, demonstrated no difference in cardiac chamber enlargement, LVH or bundle branch block between black and white athletes, which is contrary to the results observed in male athletes (Figure 4). However, T wave inversions were more common in female black athletes compared to female white athletes (14% vs 2% respectively, p <0.001).  Deep T wave inversions (> -0.2mV) were present in 2% of black athletes but in 0% of the white female athletes. As with male black athletes, deep T wave inversions in female black athletes were confined to leads V1-V4.

Adolescent Black Athletes

There are no published studies in cardiac adaptation in adolescent athletes. Preliminary data (unpublished) from our group based on comparisons between 199 black athletes with 597 white athletes (25% female) reveals 8% of adolescent black athletes exhibit a LV wall thickness of greater than 12mm compared with just 1% of adolescent white athletes. Thus, in black adolescent athletes, black individuals have an 8-fold higher chance of having a LVH of greater than 12mm compared to white athletes.

LEARNING POINTS

  1. Black athletes exhibit more LVH than white athletes.
  2. Black athletes reveal more marked repolarisation abnormalities than white athletes. 
  3. LVH of greater than 16mm in a male black athlete, and 14mm in a female black athlete are suggestive of pathological LVH rather than physiological LVH. 
  4. Deep T wave inversions in leads V1-V4 are common in black athletes and appear to be benign.
  5. Deep T wave inversions in the inferior or lateral leads raise suspicion of cardiac pathology (HCM) and require further clinical evaluation.

FIGURE 1. Distribution of left ventricular wall thickness in 300 male black and 300 male white athletes of similar age and body surface area and participating in identical sporting disciplines (11).



FIGURE 2. Patterns of early repolarisation changes seen in the precordial leads, (A) in leads V1-V3/4 and (B) in leads V4-6.
(A) 1. concave ST segment elevation; 2. convex ST segment elevation; 3. convex ST segment elevation with biphasic T waves; 4. T wave inversion; 5. deep T wave inversions (> -0.2mV). (B) 1. Concave ST segment elevation with high amplitude T waves; 2. concave ST segment elevation with normal T waves; 3. T wave inversions; 4. convex ST segment elevation; 5. deep T wave inversion (> -0.2mV).

FIGURE 3. The distribution of maximal LV wall thickness in 240 female black athletes and 200 female white athletes (14).



FIGURE 4. Pie charts comparing ECG abnormalities between female black athletes and white athletes. Black athletes exhibited a higher prevalence of ST-segment elevation and T-wave inversions than white athletes. LAE = left atrial enlargement; RAE = right atrial enlargement; LVH = left ventricular hypertrophy; ST Elev = ST-segment elevation; and Inv T = T-wave inversion (14).

 

Conclusion:

In conclusion, black athletes represent a unique subset of individuals who demonstrate a greater prevalence of LVH and marked repolarisation changes as part of normal physiological adaptation to intensive exercise. Such manifestations may overlap with those observed in HCM and pre-participation screening using ECG has the potential for generating false positive results. The afore-mentioned article provides comprehensive data permitting the differentiation between physiological changes from those indicative of cardiac pathology, a clinical dilemma which can prove challenging for even the most experienced sports cardiologists. Future studies are required to assess the long-term significance of LV hypertrophy and repolarisation abnormalities in black athletes.

References


1. Huston TP, Puffer JC, Rodney WM. The athletic heart syndrome. The New England Journal of Medicine. 1985;313(1):24-32
2. Pelliccia A, Maron BJ, Spataro A, Proschan MA, Spirito P. The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes. The New England Journal of Medicine. 1991;324(5):295-301
3. Maron BJ, Shirani J, Poliac LC, Mathenge R, Roberts WC, Mueller FO. Sudden death in young competitive athletes. Clinical, demographic, and pathological profiles. Journal of the American Medical Association. 1996;276(3):199-204.
4. Maron BJ, Carney KP, Lever HM, Lewis JF, Barac I, Casey SA, Sherrid MV. Relationship of race to sudden cardiac death in competitive athletes with hypertrophic cardiomyopathy. Journal of the American College of Cardiology. 2003;41(6):974-80
5. 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(8):1085-92
6. Corrado D, Basso C, Pavei A, Michieli P, Schiavon M, Thiene G. Trends in sudden cardiovascular death in young competitive athletes after implementation of a preparticipation screening program. Journal of the American Medical Association. 2006;296:1593-1601
7. Wasserburger RH. Observations on the juvenile pattern of adult negro males. The American Journal of Medicine. 1955;18:428-37
8. Xie X, Liu K, Stamler J, Stamler R. Ethnic differences in electrocardiographic left ventricular hypertrophy in young and middle aged employed American men. The American Journal of Cardiology. 1994;73:564-7
9. Choo JK, Abernethy WB 3rd, Hutter AM Jr. Electrocardiographic observations in professional football players. American Journal of Cardiology. 2002;90(2):198-200
10. Magalski A, Maron BJ, Main ML, McCoy M, Florez A, Reid KJ, Epps HW, Bates J, Browne JE. Relation of race to electrocardiographic patterns in elite American football players. Journal of the American College of Cardiology. 2008;51(23):2250-5.
11. Basavarajaiah S, Boraita A, Whyte G, Wilson M, Carby L, Shah A, Sharma S. Ethnic differences in left ventricular remodeling in highly-trained athletes relevance to differentiating physiologic left ventricular hypertrophy from hypertrophic cardiomyopathy. Journal of the American College of Cardiology. 2008;51(23):2256-62
12. Papadakis M, Carre F, Kervio G, Rawlins J, Carby L, Panoulas V, Chandra N, Sharma S. Ethnic differences in repolarisation patterns in elite male athletes and clinical outcomes (Abstract). Europrevent 2010. Abstract No. 424, Sports Cardiology
13. Sharma S, Maron BJ, Firoozi S, Whyte Elliott PM, McKenna WJ. Physiologic limits of left ventricular hypertrophy in junior elite athletes: Relevance to differential diagnosis of athlete’s heart and hypertrophic cardiomyopathy.  Journal of the American College of Cardiology 2002;40(8):1431-6
14. Rawlins J, Carre F, Kervio G, Papadakis M, Chandra N, Edwards C, Whyte GP, Sharma S. Ethnic differences in physiological cardiac adaptation to intense physical exercise in highly trained female athletes. Circulation. 2010;121(9):1078-85

VolumeNumber:

Vol8 N°34

Notes to editor


Dr Navin Chandra (1) BSc (Hons), MBBS, MRCP
Dr Michael Papadakis (1) MBBS, MRCP
Professor Sanjay Sharma (1) BSc (Hons), MD, FRCP (UK), FESC
(1) St George’s University of London, Division of Cardiac &Vascular Sciences, Cranmer Terrace, London, UK

Correspondence Author:
Professor Sanjay Sharma BSc (Hons), MD, FRCP (UK), FESC
Professor of Cardiology & Consultant Cardiologist
St George’s University of London, Cranmer Terrace, London, SW17 0RE, UK
Tel: 0208 725 5939
Fax: 0208 725 3328
Email: ssharma21@hotmail.com

The content of this article reflects the personal opinion of the author/s and is not necessarily the official position of the European Society of Cardiology.