CLINICAL RESEARCH: CARDIOMYOPATHY
Prevalence of Hypertrophic Cardiomyopathy in Highly Trained AthletesRelevance to Pre-Participation Screening
Sandeep Basavarajaiah, MBBS, MRCP*, ,
Matthew Wilson, MSc, MPhil ,
Gregory Whyte, PhD,
Ajay Shah, PhD, FRCP*,
William McKenna, DSc, FRCP, FESC, FACC and
Sanjay Sharma, BSc (Hons), MD, FRCP*,,*
* King’s College Hospital, London, England
University Hospital, London, England
Olympic Medical Institute, London, England
The Heart Hospital, London, England.
Manuscript received August 20, 2007;
revised manuscript received October 24, 2007,
accepted October 29, 2007.
* Reprint requests and correspondence: Dr. Sanjay Sharma, King’s College Hospital, Denmark Hill, London, United Kingdom SE5 9RS. (Email: ssharma21{at}hotmail.com).
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Abstract
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Objectives: This study sought to determine the prevalence of hypertrophic cardiomyopathy (HCM) in elite athletes.
Background: Hypertrophic cardiomyopathy is considered to be the most common cause of exercise-related sudden death in young athletes. The prevalence of HCM in elite athletes has never been reported but has important implications with regard to pre-participation screening for the disorder.
Methods: Between 1996 and 2006, 3,500 asymptomatic elite athletes (75% male) with a mean age of 20.5 ± 5.8 years (range 14 to 35 years) underwent 12-lead electrocardiography and 2-dimensional echocardiography. None had a known family history of HCM.
Results: Of the 3,500 athletes, 53 (1.5%) had left ventricular hypertrophy (mean 13.6 ± 0.9, range 13 to 16), and of these 50 had a dilated left ventricular cavity with normal diastolic function to indicate physiological left ventricular hypertrophy. Three (0.08%) athletes with left ventricular hypertrophy had a nondilated left ventricular cavity and associated deep T-wave inversion that could have been consistent with HCM. However, none of the 3 athletes had any other phenotypic features of HCM on further noninvasive testing and none had first-degree relatives with features of HCM. One of the 3 athletes agreed to detrain for 12 weeks, which showed resolution of electrocardiography and echocardiographic changes confirming physiologic left ventricular hypertrophy.
Conclusions: The prevalence of HCM in highly trained athletes is extremely rare. Structural and functional changes associated with HCM naturally select out most individuals from competitive sports. Screening athletes with echocardiography is not cost effective. However, electrocardiography is useful in selecting out those individuals who may have pathological left ventricular hypertrophy for subsequent echocardiography.
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Abbreviations and Acronyms
| | ECG = electrocardiography | | HCM = hypertrophic cardiomyopathy | | LV = left ventricle/ventricular | | LVH = left ventricular hypertrophy | | SCD = sudden cardiac death |
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Hypertrophic cardiomyopathy (HCM) is considered to be the most common cause of exercise-related sudden cardiac death (SCD) in young (<35 years) athletes in the U.S. (1–4). The sudden death of some high-profile athletes of HCM has led some sporting organizations in the United Kingdom to implement relatively elaborate, independent cardiovascular screening programs composed of 12-lead electrocardiography (ECG) and 2-dimensional echocardiography in all athletes to identify HCM. Indeed, given the therapeutic strategies now available to prevent sudden death, such as the implantable cardioverter-defibrillator, the necessity for early identification of HCM in athletes has become magnified. In the United Kingdom and in many other developed countries, cardiovascular evaluation of athletes is usually confined to athletes competing at the regional or national level.
Although the prevalence of HCM in the general population is 0.2% (5), the precise prevalence of HCM in the most highly trained athletes is unknown. Calculations based on the Italian pre-participation screening program involving over 34,000 athletes indicate that the estimated prevalence of HCM in individuals participating in regular organized sporting activity is approximately 0.07% (6). However, data from this series were not confined specifically to elite athletes.
The aim of this study was to determine the prevalence of HCM in some of the most highly ranked athletes in the United Kingdom to aid in justification for or against screening for HCM in this cohort.
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Methods
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Setting.
Although there is no formal government-sponsored pre-participation screening program in the United Kingdom, certain sporting bodies such as the British Lawn Tennis Association, the Premiership football and rugby league, and the national swimming and boxing squads have adopted mandatory self-funded pre-participation screening programs for athletes comprising personal, family, and drug history; physical examination; 12-lead ECG; and echocardiography with a view to further investigations if necessary. Dr. Sharma has been responsible for performing cardiovascular evaluation in elite athletes in these sporting disciplines since 1996 at St George’s Hospital Medical School, Olympic Medical Institute (Northwick Park Hospital), University Hospital Lewisham, and King’s College Hospital.
Athletes.
Between 1996 and 2006, 3,500 asymptomatic elite athletes between 14 years and 35 years (mean age 20.5 years) underwent 12-lead ECG and 2-dimensional transthoracic echocardiography as a part of pre-participation screening for HCM. Of these, 2,625 (75%) were male and 875 (25%) were female. Just over 98% of athletes were Caucasian; the remainder were of West African decent. The athletes had a mean body surface area of 1.86 ± 0.16 m2 (range 1.36 to 2.29 m2).
Written consent was obtained from individuals older than 16 years and from a parent or guardian for those younger than 16 years. The athletes participated in 15 different sporting disciplines, but the vast majority of the study group (71%) represented football, rugby, tennis, and swimming (Table 1). The term elite was used in relation to achievements in the athletic arena; all athletes competed at the regional level and approximately 60% at the national level during the study period.
Ethical approval for the study was granted by Harrow Research Ethics Committee to the Cardiac Risk in the Young (CRY), Centre of Sports Cardiology.
ECG.
A standard 12-lead ECG examination was performed during quiet respiration in a supine position and analyzed using a Marquette Hellige (Milwaukee, Wisconsin) ECG recorder. The electrodes were placed carefully to ensure consistency of the precordial lead locations, and ECGs were recorded at a paper speed of 25 mm/s. The PR interval; QRS duration; QT interval; QRS axis; Q-, R-, S-, and T-wave voltage; and ST-segments were measured in each lead using calipers and a millimeter ruler as described elsewhere (7).
The QT intervals were corrected for the heart rate (QTc) using the Bazett formula (8). A QTc interval of >440 ms in men and 460 ms in women was considered abnormal.
Left ventricular (LV) hypertrophy (LVH) was defined by the Sokolow-Lyon voltage criterion. The LVH was defined by the sum of the S waves in V1 and the R waves in V5 exceeding 3.5 mV (9).
Echocardiography.
Two-dimensional echocardiography was performed with the subjects resting in a left lateral decubitus position, using an Acuson Computed Sonograph 128XP/10c (San Jose, California) with 3-MHz transducer. Images of the heart were obtained in the standard parasternal long-axis and short-axis and apical 4-chamber planes, as previously described (10). The LV wall thickness was measured from 2-dimensional short-axis views in end diastole, with the greatest measurement within the LV wall defined as the maximal wall thickness.
M-mode echocardiograms derived from 2-dimensional images in the parasternal long axis were used for the measurement of LV end-diastolic and -systolic dimensions, left atrial diameter, and aortic root according to American Society of Echocardiography standards (11). Three to 5 consecutive measurements were taken, and the average was calculated.
Percent LV shortening fraction was calculated as an index of systolic function. Pulsed Doppler recordings were performed at the distal margins of mitral valve leaflets to provide an index of diastolic function (12).
Criteria for consideration of the diagnosis of HCM in athletes.
Based on previous publications and our own experience of an athlete’s heart, athletes with a LV wall thickness >12 mm were considered to have LVH (13–15). Athletes with LVH and a relatively nondilated LV in terms of athletic training (<56 mm) (16) in association with any one of the following were considered to have findings that could be consistent with pathological LVH rather than physiological hypertrophy: 1) impaired diastolic function (17); 2) enlarged left atrial diameter >45 mm in athletes <18 years old (18) and up to 50 mm in older athletes (19); 3) LV outflow obstruction caused by systolic anterior motion of the anterior mitral valve leaflet (20); 4) left bundle branch block (21); 5) ST-segment depression or deep T-wave inversions (<–0.2 mV) in 2 contiguous leads (except V1 and V2 in athletes age <16 years old) (22,23) on the ECG; and 6) a family history of HCM in first-degree relatives.
Athletes with a family history of HCM or those showing the echocardiographic and/or ECG abnormalities considered to represent pathological LVH were investigated further with 48-h ECG (24), cardiopulmonary exercise test (25), and cardiac magnetic resonance imaging (26) to evaluate the broader phenotype of HCM and to assess risk of SCD (27). The 48-h ECG was performed to check specifically for nonsustained ventricular tachycardia. The cardiopulmonary test was performed to identify abnormalities in exercise blood pressure response, exercise arrhythmias, and estimation of peak oxygen consumption. The cardiac MRI scan was performed to exclude apical HCM.
In athletes with persisting diagnostic uncertainty after the investigations above, first-degree relatives were invited for screening for HCM and/or attempts were made to persuade the individual to detrain for 3 months followed by repeat evaluation (28,29).
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Results
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None of the athletes in the study had a family history of HCM in first-degree relatives, and none had experienced angina, breathlessness disproportionate to the amount of exercise performed, or exertional syncope.
The diagnosis of HCM was excluded by echocardiography in 3,447 (98.5%) on the basis of a LV wall thickness <12 mm, absence of systolic anterior motion of the anterior mitral valve leaflet causing LV outflow obstruction, and normal diastolic function.
Athletes with an LV wall thickness >12 mm (LVH).
Of the 3,500 athletes, 53 (1.5%) showed a maximal LV wall thickness exceeding 12 mm and were considered to have LVH (Fig. 1) (16). All 53 athletes were male and represented a variety of ball, racket, and endurance sporting disciplines, and all 53 participated in sport at the national level. The echocardiographic characteristics of these athletes are shown (Table 2). None of the athletes with LVH had indexes of diastolic dysfunction, an enlarged left atrial diameter, or systolic anterior motion of the anterior mitral valve leaflet and associated LV outflow obstruction. Fifty of the 53 athletes with LVH had an associated dilated LV and normal systolic function, consistent with physiological LVH (14,15).
Twenty athletes in this cohort had deep T-wave inversions in at least 2 contiguous inferior and/or lateral leads. None of the athletes with LVH had left bundle branch block or ST-segment depression in 2 or more contiguous ECG leads.
Athletes with LVH and a nondilated LV.
Only 3 of the 53 athletes with LVH had a nondilated LV, which could be considered to represent morphologically mild HCM. None of the athletes had any other echocardiographic features of HCM (Table 2). All 3 athletes also showed deep T-wave inversions in inferior and/or lateral leads (Fig. 2). The 48-h Holter monitoring did not reveal any episodes of nonsustained ventricular tachycardia or paroxysmal atrial fibrillation in any of the 3 athletes. All 3 athletes exercised to the point of volitional exhaustion and achieved >95% of the predicted heart rate for age. All 3 athletes showed an adequate blood pressure response to exercise and achieved high peak oxygen consumption and anaerobic threshold values (Table 3). Cardiac magnetic resonance scans using gadolinium-diethylenetriamene pentacetate (0.1 mmol/kg) in all 3 athletes revealed normal left and right ventricular structure and function. In relation to the diagnosis of HCM, there was no evidence of apical HCM, marked hypertrophy of anterolateral free wall, or myocardial fibrosis.
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Figure 2 Electrocardiograms and Parasternal Short-Axis Views of the LV at the Level of Papillary Muscle of the 3 Athletes With LVH and a Nondilated LV Cavity
All 3 athletes showed left ventricular hypertrophy (LVH) associated with a nondilated left ventricular (LV) cavity and inferior and lateral leads.
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Table 3 Echocardiographic and Cardiopulmonary Exercise Parameters in Athletes With Left Ventricular Hypertrophy and a Nondilated Left Ventricular Cavity Size
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Both parents and siblings of all 3 athletes accepted invitations for screening for HCM with 12-lead ECG and 2-dimensional echocardiography, which did not reveal any conventional diagnostic features of the disorder to indicate familial disease.
Only 1 of the 3 athletes was persuaded to detrain for 3 months, after which there was regression of LV hypertrophy on echocardiography and resolution of the deep T-wave inversion on the ECG (Fig. 3) (30). The 2 remaining athletes declined detraining through fear of team deselection and continued to exercise. Both athletes agreed to be genotyped for known HCM-causing sarcomeric contractile protein gene mutations, which did not yield a diagnosis.
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Figure 3 Electrocardiograms of a Swimmer With LVH and Inferolateral T-Wave Inversions Before and After Detraining for 12 Weeks
Detraining was associated with regression of left ventricular hypertrophy (LVH) on echocardiography and normalization of deep T-wave inversions after detraining.
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Athletes with other cardiac abnormalities on ECG and echocardiography.
Twenty-six athletes (0.7%) had cardiac diagnoses other than LV hypertrophy, including Wolff-Parkinson-White ECG pattern (n = 6), isolated long QT interval (>460 ms) (n = 9), mitral valve prolapse (n = 5), atrial septal defect (n = 2), bicuspid aortic valve (n = 3), and cortriatriatum (n = 1) (31).
Thirty-five (1%) athletes showed deep T-wave inversions in contiguous leads. Of these, 20 had LV hypertrophy (17 with a dilated LV and 3 with a nondilated LV). The remaining 15 (0.4%) athletes had deep T-wave inversions in the absence of LV hypertrophy.
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Discussion
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Prevalence of HCM in elite athletes.
Hypertrophic cardiomyopathy is repeatedly cited as the leading cause of sudden death in young athletes (1–4). This cross-sectional study shows that the prevalence of HCM in elite British athletes is extremely low. Of the 3,500 athletes studied, only 3 (0.09%) athletes had LV morphology that could have been regarded to be consistent with mild HCM after initial evaluation with ECG and echocardiography. However, in 1 of the 3 athletes, the diagnosis was excluded after demonstration of regression of LVH on echocardiography and associated resolution of repolarization changes on ECG (30). The remaining 2 athletes had mild LVH and an associated nondilated LV, but neither had any other morphologic features of HCM or the broad phenotype of the disorder on 48-h ECG monitoring and exercise stress testing. Outside the context of familial disease, neither athlete could be regarded as having unequivocal diagnostic features of HCM.
Interestingly, both athletes were of West African decent, which may have had a bearing on the magnitude of hypertrophy in response to exercise and repolarization changes on the ECG (32). The 2 athletes in question also showed high peak oxygen consumption and anaerobic threshold, indicating the ability to generate and sustain a large cardiac output for prolonged periods. In contrast, most individuals with HCM (33), including those participating in regular physical activity (34), have been shown to have low peak oxygen consumption irrespective of symptomatic status or magnitude of LVH. Genetic testing failed to identify a disease-causing mutation in both athletes, but based on the genetic heterogeneity of HCM, the investigators concede that the diagnosis of HCM cannot be excluded with certainty by a negative genetic test.
Even if a diagnosis of HCM were entertained in the 2 athletes of West African ancestry above, the prevalence of HCM in elite athletes is no more than 0.06%, compared with 0.2% in the general population. The pathophysiological manifestations of HCM, notably LVH, nondilated LV, impaired myocardial relaxation, myocardial ischemia, dynamic LV outflow obstruction, and mitral regurgitation, are probably not conducive to achieving substantial increases in cardiac stroke volume in most affected individuals. We suspect that most individuals with HCM are selected out from competing in high-level sport where physical endurance is a major component.
There were a significant number of athletes with LVH, but all had a dilated LV cavity, indicating physiological LVH. Although LV dilatation is also recognized in HCM, it is usually a manifestation of end-stage disease and is associated with New York Heart Association functional class III or IV (35).
Sudden death in sport attributed to HCM.
Hypertrophic cardiomyopathy is diagnosed at post-mortem examination in some young high-profile athletes dying suddenly during sport. Whether all such deaths are based on the identification of myocyte disarray, the histologic hallmark of HCM, is uncertain, but reliance on macroscopic appearance and cardiac weight alone has the potential for a false diagnosis of HCM in an athlete with physiological hypertrophy. The Italian pathologists from the center of excellence in the Veneto region have consistently reported fewer cases of HCM in athletes dying suddenly during sport compared with other nations, even before their screening program (36). A protagonist for HCM being the most common cause of death in athletes would argue that there is a lower cluster of the HCM gene pool in the Mediterranean region; however, an antagonist may argue that a thorough histologic examination of the heart by a cardiac pathology expert excludes HCM and identifies an alternative cause such as arrhythmogenic right ventricular cardiomyopathy or an accessory pathway.
Screening for HCM in elite athletes.
Screening for HCM specifically with echocardiography in elite athletes is not cost effective because several thousand athletes would have to be screened to identify one with HCM. The investigators concede that HCM shows marked morphologic and functional heterogeneity allowing a very small fraction of affected individuals to compete at national and international levels (37); however, this cannot justify large-scale screening for HCM with echocardiography in all elite athletes. Further, certain genetic mutations show age-related penetrance, therefore the absence of LVH in adolescence or young adulthood does not rule out the possibility of developing HCM in the future (38).
Ironically the study identified 15 individuals with either the Wolff-Parkinson-White ECG pattern (n = 6) or a long QT interval (n = 9), which are considered rare causes of SCD in young athletes (3) but may claim more lives in athletes than originally thought. Neither disorder precludes cardiac function and would not necessarily be selected out by intense physical exertion. All athletes with the Wolff-Parkinson-White pattern had an identifiable accessory pathway that was ablated, permitting resumption of competitive sport. Of the 9 athletes with a long QTc interval, 3 were diagnosed with unequivocal long QT syndrome based on a Schwartz points score of 4 (n = 2) (39), evidence of disease in a first-degree relative (n = 2), or a positive genetic diagnosis (n = 1) and were disqualified from competitive sports. Diagnostic uncertainty persists with the remaining 6, who have continued to compete for a mean period of 3 years without adverse cardiac events.
Eleven athletes (0.3%) with a normal ECG showed minor congenital structural abnormalities that were not hemodynamically significant and did not result in disqualification from sport.
Our experience suggests that screening elite athletes using an ECG is more likely to identify individuals with other conditions implicated in SCD and also to identify those who may have pathological LVH. The absence of ST-segment depression, deep T-wave inversions, and left bundle branch block will exclude almost all cases of HCM as shown by longitudinal follow-up of previously screened Italian athletes (40).
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Conclusions
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The prevalence of HCM in elite athletes is significantly less than in the general population; the demands of strenuous exercise on the cardiovascular system select out most individuals with HCM. Screening all elite athletes with echocardiography, the accepted gold-standard investigation for HCM, has a poor yield, with many thousand athletes needing to be screened to identify a single individual with HCM. The ECG is useful in identifying individuals who may have pathological LVH and other congenital electrical disorders that may prove fatal. Based on the British experience of systematic cardiovascular screening of elite athletes, we propose that echocardiography in athletes to screen for HCM should be reserved only for athletes with symptoms suggestive of underlying cardiovascular disease, a murmur indicative of LV outflow obstruction, family history of HCM in first-degree relatives or specific ECG changes, notably deep T-wave inversions, ST-segment depression, pathological Q waves, left bundle branch block, or extreme leftward cardiac axis (23,41). Our study reveals that only 1% of athletes in this study would be expected to undergo echocardiography to exclude HCM based on the proposed recommendations, which has a massive cost-saving implication, particularly for financially less endowed sporting clubs.
Study limitations.
Almost all of the athletes in this study were Caucasian. Of the small proportion of athletes of West African origin, 2 had features that could have been consistent with HCM; however, subsequent evaluation was more suggestive of physiological LVH. We have concerns that a more detailed study of cardiac structure is required in this particular ethnic group to permit accurate cardiovascular evaluation and minimize the risk of a false-positive diagnosis of HCM.
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Acknowledgments
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The authors acknowledge the invaluable assistance of Cardiac Risk in the Young (CRY) for providing the electrocardiography and echocardiography machines for the study.
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Footnotes
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Dr. Basavarajaiah is supported by a junior cardiac research fellow grant from the charity organization Cardiac Risk in the Young.
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References
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M. Papadakis, G. Whyte, and S. Sharma
Preparticipation screening for cardiovascular abnormalities in young competitive athletes
BMJ,
September 29, 2008;
337(sep29_1):
a1596 - a1596.
[Full Text]
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S. Basavarajaiah, A. Boraita, G. Whyte, M. Wilson, L. Carby, A. Shah, and S. Sharma
Ethnic differences in left ventricular remodeling in highly-trained athletes relevance to differentiating physiologic left ventricular hypertrophy from hypertrophic cardiomyopathy.
J. Am. Coll. Cardiol.,
June 10, 2008;
51(23):
2256 - 2262.
[Abstract]
[Full Text]
[PDF]
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Hypertrophic Cardiomyopathy in Elite Athletes
Journal Watch (General),
April 17, 2008;
2008(417):
3 - 3.
[Full Text]
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Screening Elite Athletes for Hypertrophic Cardiomyopathy: Needle in a Haystack?
Journal Watch Cardiology,
April 2, 2008;
2008(402):
2 - 2.
[Full Text]
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L. Faber and F. van Buuren
Athlete screening for occult cardiac disease: no risk, no fun?
J. Am. Coll. Cardiol.,
March 11, 2008;
51(10):
1040 - 1041.
[Full Text]
[PDF]
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