The athlete’s heart and cardiomyopathies

The differentiation of the athlete’s heart and cardiomyopathies like hypertrophic cardiomyopathy (HCM), dilated cardiomyopathy (DCM), arrhythmogenic cardiomyopathy (AC) or left ventricular non-compaction (LVNC) are the most critical clinical dilemma (figure 1).

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Figure 1

Differentiating athlete’s heart from HCM, DCM, AC and LVNC. AC, arrhythmogenic cardiomyopathy ; DCM, dilated cardiomyopathy; GLS, global longitudinal strain; HCM, hypertrophic cardiomyopathy; LA, left atrium; LV, left ventricle; LVEDD, left ventricular end-diastolic diameter; LVEF, left ventricular ejection fraction; LVH, left ventricular hypertrophy; LVNC, left ventricular non-compaction; LVOT, left ventricular outflow tract; RA, right atrium; RV, right ventricle; RVIT, right ventricular inflow tract; RVOT, right ventricular outflow tract; RVWMA, right ventricular wall motion abnormalities.

Athlete’s heart

Athlete’s heart describes cardiac structural, functional and electrical adaptations to repetitive intense or extensive exercise. Physiological cardiac adaptations in athletes mainly depend on the duration, intensity and type of training with differentiation of isotonic (dynamic) exercise resulting in volume overload and isometric (static) exercise characterised by a pressure overload.8 9 As most sporting disciplines are defined by a varying degree of isometric and isotonic components, a new classification of sports in four groups based on the physiological characteristics of exercise (endurance, power, skill and mixed) has been proposed.1 A more detailed description of the athlete’s heart is provided in the online supplemental material.

Hypertrophic cardiomyopathy

HCM is a common genetic cardiomyopathy with a prevalence of approximately 1 in 500 individuals, characterised by unexplained LV hypertrophy.10 A small proportion of competitive athletes (ie, 2%) may present with LV wall thickness of 13–15 mm, which overlaps mild HCM.11 12 ,1 Compared with pathological hypertrophy, exercise-induced chamber thickening is always proportional to the type of sport participated (mainly in combined power and endurance disciplines), is harmonic (homogeneous distribution of wall thickness), symmetric (involves all four chambers) and is reversible after detraining.2 Moreover physiological hypertrophy is never accompanied by a loss of function, and the systolic and diastolic indices are not altered in athletes.13 Further important morphological characteristic to support a physiological hypertrophy is the absence of fibrosis or scars on cardiovascular MRI.14

The distribution of HCM is inhomogeneous and likely follows genetic clusters with a higher prevalence in the USA (2%–18%) than in Italy (3%).15 In this setting, an ECG has been proposed as primary tool and echocardiography only as secondary investigation. The overlap between athlete’s heart and HCM is challenging in black athletes.16 Phenocopies of HCM, especially hypertensive heart disease, are clinically challenging. In athletes with previously unknown or uncontrolled arterial hypertension, hypertrophy of the LV could also stem from hypertensive heart disease. Here, the clinical history and serial blood pressure measurements are the cornerstone for the diagnosis. Also echocardiography helps to distinguish athlete’s heart from hypertensive heart disease: degree and type (athletes: eccentric, HCM: concentric) of LV hypertrophy, regression of LV hypertrophy to detraining, reduced LV function, diastolic dysfunction, increased LV filling pressures, reduced LV e′-velocity, reduced atrial function, reduced LV and left atrial deformation indexes, and harmonic biventricular and biatrial remodelling.17

Arrhythmogenic cardiomyopathy

AC is an inherited heart muscle disease with a prevalence of 1 in 5000 in the general population.18 It is pathologically characterised as fibro-fatty replacement of the ventricular myocardium and clinically by ventricular electrical instability, which may lead to ventricular tachyarrhythmia and arrhythmic cardiac arrest, mostly in young people.19 The right ventricle (RV) is more often and earlier affected than the LV so that this condition was previously termed arrhythmogenic right ventricular cardiomyopathy (ARVC). This cardiomyopathy is particularly important to recognise since ARVC athletes have an up to 5.4 times higher relative risk of SCD than ARVC patients not involved in competitions.5

Differentiation between athlete’s heart and AC may be challenging, as a significant proportion of endurance athletes have a dilated RV, meeting the dimensional criteria of AC.20 To meet the diagnostic criteria for AC, however, RV enlargement should be associated with regional akinesia, dyskinesia or aneurysms of the RV. In athletes, RV dilatation is never associated with global or regional functional abnormalities, suggesting a physiological adaptation to increased cardiac output.21 Also, harmonic dilatation of the RV rather than asymmetric dilatation of outflow tract with normal sized inflow tract indicates athlete’s heart, whereas in AC a disproportionate dilatation of the RV outflow tract may be observed.21

Additionally, in case of disproportionate dilatation of the RV and/or right atrium, an atrial septal defect should be excluded as it could be responsible for volume overload of the right chambers and mimic AC.

Dilated cardiomyopathy

DCM is defined as dilatation of the LV accompanied by systolic dysfunction in the absence of coronary artery disease (CAD), hypertension or valvular disease. At least 25% of DCM are familial. Echocardiography is key to diagnose LV cavity dimension and systolic function as well as diastolic parameters. Athlete’s heart and DCM show considerable overlap as both can show a significantly enlarged LV cavity. While a combination of left ventricular end-diastolic diameter (LVEDD) ≥60 mm and a reduced resting LVEF should raise suspicion of DCM in athletes, LV cavity dimensions in healthy endurance athletes often are outside these limits.22 Indexation of LVEDD might overcome this diagnostic dilemma, however, not entirely.23 Additionally, a significant dilatation of the LV is usually observed in high endurance athletes. In 286 elite cyclists, 11% met diagnostic criteria for DCM.24 Diastolic function proves valuable in differentiating DCM from athlete’s heart. Endurance athletes have higher peak E-waves and e′ than sedentary controls, and patients with DCM have abnormal myocardial relaxation or echocardiographic signs of enhanced filling pressure.25 Besides, most athletes show normal indices of longitudinal function with systolic velocity >10 cm/s and also normal global longitudinal strain.26 Additionally, stress echocardiography demonstrates that LVEF augments in athletes with a low/borderline resting LVEF as opposed to patients with DCM.2

LVNC cardiomyopathy

LVNC is a rare and yet unclassified cardiomyopathy and characterised by prominent myocardial trabeculations and intertrabecular recesses communicating with the LV cavity.2 A detailed discussion of LVNC vs athlete’s heart is provided in the online supplemental material.

The role of echocardiography in screening of athletes <35 years

In athletes aged <35 years, the majority of SCD incidences are due to inherited cardiac diseases such as HCM, arrhythmogenic (right ventricular) cardiomyopathy (AC/ARVC), congenital anomalies of coronary arteries, pre-excitation syndromes, conduction and ion channel diseases.5 27 Aside of specific symptoms that can lead to diagnosis, SCD often occurs as the first clinical manifestation.

As 5%–31% of autopsies of SCD victims show no evidence of structural heart anomalies, research has focused on early unmasking cardiac pathologies.27 Electrocardiography has been widely recognised as a sensitive and specific screening tool.6 Nevertheless, 9.5%–16.3% of SCD cases have been related to structural with no associated electrical anomalies.27 Moreover, the utility of electrocardiography in athletes is still debated, since exercise induces alterations with no or uncertain clinical significance and ethnical differences have to be considered.28

Echocardiography was shown to be efficient and cost-effective in detecting subclinical congenital diseases requiring follow-up. In adolescent football players, echocardiographic screening was able to diagnose congenital or acquired structural cardiac defects in 1.2%–4.5%.29 During 20-year follow-up, no SCD was registered,29 and 28% had pathological signs during clinical evaluation, and none of them had electrocardiographic alterations.30 Early detection of asymptomatic structural heart conditions has important prognostic implications.

Valvular anomalies

Mitral valve prolapse has a prevalence of 2.5%–6% in the general population and about 1.5% in athletes.31 In epidemiological studies, mitral valve prolapse accounted for 7%/13% of fatal events in young adults male/female <40 years.32 Mitral valve prolapse-related SCD seems to be related to myocardial fibrosis due to mechanical myocardial stretch in the myocardium close to papillary muscles or to the mitral annulus or a mitral annulus disjunction. Clinically, premature ventricular contractions originating from these regions may be detected or myocardial fibrosis may be detected on CMR with late gadolinium enhancement.32 Echocardiography can reliably detect the disease and its severity, and therefore is necessary to get prognostic information and to schedule follow-up examinations and training recommendations.

Bicuspid aortic valve is often asymptomatic until severe aortic regurgitation, aortic stenosis or vascular complications develop. ECG at rest and during exercise may be normal or show unspecific alterations, and a diastolic murmur might be difficult to evaluate.4 It is therefore possible that this condition is missed at conventional PPS.4 Epidemiological studies showed a prevalence of 2.5% of bicuspid aortic valve in athletes aged 10–45 years, most presented with echocardiographic evidence of aortic dilation independent of the athletes’ age, while minor ECG alterations were present in <50%.31 Since bicuspid aortic valve is a congenital condition, a once-in-a-lifetime echocardiography allows to identify affected subjects in order to plan an individualised follow-up and exercise recommendation before complications arise. Additionally, due to its hereditary pattern, screening of the athlete’s family has further impact.

Aortic dilatation

Aortic dilatation is often related to bicuspid aortic valve, connective tissue disease or arterial hypertension that often progresses asymptomatically until serious complications arise, such as aortic dissection. Aortic enlargement of ≥40 mm (males) and of ≥34 mm (females) is considered a pathological not a physiological training adaption, although male endurance athletes had larger diameters than male strength athletes.33 A cross-sectional study showed that clinically relevant aortic dilatation is common among endurance athletes (61±6 years; 60% men). Elite competitor status and sport type (rowing) were independently associated with aortic size after correction for confounders. Prospective follow-up is warranted to establish clinical outcomes in this population.34 Again, a more individualised approach may help to prioritise certain athletes for echocardiography.

Athletes with an aortic root enlargement ≥40 mm and Marfan syndrome should quit competitive sports.2 11 PPS would help to detect those at risk and develop an adequate individual follow-up and timely surgery, if indicated, during their career and once the athletes retire.2

Coronary artery anomalies

Athletes had a 79 times higher relative risk of SCD due to coronary artery anomaly compared with non-athletes in epidemiological studies.5 The prevalence of coronary anomalies on coronary CT angiography is relatively high (2.6%).35 Coronary artery anomalies are frequently missed at standard screening, due to lack of suspicious symptoms. Echocardiography can easily identify the origin of the left coronary artery (99%) and the right coronary artery (96%) in the majority of cases and is therefore the ideal technique since it is low cost and radiation free.36 A prompt recognition could address further investigations for the prognostic stratification.1

Role of echocardiography in screening of athletes aged >35 years

PPS has primarily been developed for young and professional athletes. However, several registries have shown that the majority of SCD in athletes occurs in recreational athletes, especially in master athletes aged >35 years.37 Independently from their competitive level, athletes aged >35 years should be assessed regarding their cardiovascular risk during exercise. Up to 90% of exercise-related SCD in master athletes is related to known/silent CAD.38 The European Society of Cardiology (ESC) suggests cardiovascular risk assessment by using the Systematic COronary Risk Evaluation (SCORE). If SCORE is high or if the subject intends to newly (re-)start a moderate to high-intensity activity, a screening (history, physical examination and ECG) is suggested, with maximal exercise testing as second-line screening method.2 39

Coronary artery disease

The relative risk of SCD due to premature CAD was found to be 2.6 times higher in athletes aged 29±5 years, compared with non-athletes.5 The risk of premature CAD is often missed by classic screening methods. Echocardiographic detection of atherosclerotic plaques at the sinutubular junction, in the aortic arch or the abdominal aorta might point to a systemic atherosclerotic burden in otherwise asymptomatic subjects and in absence of wall motion anomalies.40 Echocardiography may help with risk stratification of older, yet asymptomatic, athletes. Other options include exercise testing and stress echocardiography. We speculate that implementation of aortic assessment for atherosclerotic manifestations during echocardiography might increase the diagnostic yield of the detection of subclinical CAD cost-effectively. Otherwise, coronary artery CT would be an option to screen for subclinical CAD. This screening approach showed a higher detection rate in coronary calcium scoring than exercise testing.41

Echocardiography might further help to diagnose previous silent myocarditis (regional wall motion abnormalities due to myocardial scarring), late onset of various cardiomyopathies and pathological remodelling to exercise as possible manifestation of late-onset cardiomyopathy. The potential additional diagnostic yield of echocardiography in athletes aged <35 years and >35 years is summarised in figure 2.

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Figure 2

Potential additional diagnostic yield of echocardiography in athletes aged <30–35 years and >30–35 years. SCD, sudden cardiac death.

Proposed recommendations on echocardiography in athletes

The efficacy of electrocardiographic PPS identifying athletes at risk of SCD has already been demonstrated. As such, it should be regularly performed in leisure and competitive athletes.1 Prevention of SCD in athletes is crucial in competitive as well as recreational athletes. From a medical perspective, there is no reason to use different screening protocols for recreational and professional athletes. The individual risk estimation is crucial, and it should guide the decision whether a screening should be considered or not. Although not recommended by the ESC,42 some major sporting bodies have implemented echocardiography in their mandated cardiovascular evaluation protocols. Fédération Internationale de Football Association (FIFA) and the Union of European Football Association (UEFA), as well as the Union Cycliste Internationale (UCI) mandate an echocardiography in PPS.

Two pitfalls have to be considered: diagnostic necessity and cost-effectiveness.

Diagnostic necessity: echocardiography when added to standard screening (personal and family history, physical examination and ECG) had only little added value in detecting HCM.43 We agree, that ECG has a high sensitivity to detect HCM; however, it should be considered that ECG may be silent in a minority of cases, especially in subclinical disease. However, we have to look beyond cardiomyopathies in the prevention of SCD in athletes. Echocardiography may detect conditions that remain undetected using standard screening measures.

Cost-effectiveness largely relies on the costs of echocardiography and the follow-up investigations. Significant differences in health-related cost exist among countries. One approach to optimise cost-effectiveness is to provide an echocardiographic examination that is less expensive. As such, a focused cardiac ultrasound examination as an adjunct to clinical evaluation to recognise specific signs of a limited spectrum of cardiovascular diseases has recently been proposed as routine screening. The investigation is performed by an operator who is specifically trained to recognise particular echocardiographic signs in a specific population, such as athletes.44 The estimated cost for such an echocardiographic screening would not substantially increase costs, also considering that the echocardiographic screening as we suggest it is only necessary once or twice in the lifetime of an athlete.45 The focused cardiac ultrasound approach has been primarily tested in the emergency room setting and only limited studies are available in athletes. However, it is evident that a focused approach will be less sensitive for various cardiac pathologies than a complete and carefully performed echocardiography. The cost of a routinely performed full echocardiography was reported to be superior but approximately 30% higher as compared with an ECG-based screening (with other investigations performed on-demand) in adolescent athletes.46

Echocardiography could be integrated in the screening concept of athletes. The first echocardiography could take place at the beginning of the athletic career (ie, during adolescence) to rule out congenital coronary or valvular abnormalities and/or aortic dilatation. Also, borderline ECG changes may then be easier to interpret. Moving forward in their career to ‘master athlete status’ (ie, >35 years), a second echocardiography, mainly to detect wall motion abnormalities, dilation of the aorta, disproportionate dilation of the atria, atherosclerotic plaques in the ascending aorta, aortic arch and abdominal aorta, late-onset cardiomyopathies and to assess cardiovascular changes that develop through life-long athletic activity (eg, atrial fibrillation due to atrial dilation and RV-fatigue) could be performed. Preferably, echocardiography could be performed on-site of the cardiovascular evaluation to reduce associated costs and time delays until the athlete can be cleared.47 Despite current recommendations, echocardiography is already a first-line PPS tool in both professional and amateur competitive athletes, as recently reported by a real-world international survey.48 Our suggested screening algorithm for athletes including echocardiography is outlined in figure 3.

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Figure 3

Proposed screening algorithm for recreational and competitive athletes including echocardiography. CCTA, coronary computed tomography angiography; CAD, coronary artery disease; LDL-C, low-density lipoprotein cholesterol.

As minimal dataset for screening echocardiography, we suggest the present version of the echocardiographic evaluation of the precompetition medical assessment (PCMA) as demanded by FIFA. PCMA integrates a ‘straight forward’ and focused approach, although keeping an elaborate ‘full’ echocardiographic exam to prevent the missing of important findings49 (see online supplemental material).

If a cardiac abnormality is detected, a follow-up echocardiography could be regularly repeated as suggested by the disease depending on the sport performed.

We understand that some sporting bodies claim to mandate screening especially in professional athletes due to legal issues. We do, however, not advocate for mandatory mass screenings. As recreational and professional athletes can both suffer SCD, we think that both should be screened. Education and information of the potential benefits, risks and costs of screening should be provided to every athlete and also to official sporting bodies. The ‘informed athlete’ as well as informed officials of sporting bodies can then decide if screening should be performed. Accessibility to screening, including echocardiography at least twice in an athlete’s life, should be open to all athletes who want it.

Current screening strategies in athletes as proposed by the ESC and the American Heart Association/American College of Cardiology, as well as our suggestion are summarised in table 1.