– Written by Carmen Adamuz, Qatar, Mark Hamilton, UK, Guido E Pieles, Qatar

 One of the greatest privileges of being Sports Cardiologist is having the opportunity to look at the heart of wonderful athletes which sports records and achievements are as marvelous as their own heart.

Cardiac imaging lies at the core of the work of a sports cardiologist and besides providing crucial clinical information it is also a fascinating journey of discovery when evaluating an ‘Athlete’s heart” with its unique adaptations to extensive training. Physiological remodeling generally manifests as harmonic enlargement of the cavities and often eccentric remodeling, it may be accompanied by a certain degree of wall thickening and borderline or even mildly reduced systolic function at rest that shows excellent contractile reserve on exercise. These changes can be extreme in some athletes, especially in those participating in endurance sports, in which remarkable structural changes raise the questions for differential diagnosis with some forms of cardiomyopathy.

It is in this setting that the cardiovascular multimodality imaging plays a crucial role in Sports Cardiology, from the resting echocardiography complemented with advanced techniques such as speckle tracking (Figure 1,2,3), 3D (Figure 4) and exercise echocardiography (Figure 5) to the most advanced cardiac magnetic resonance (CMR) (Figure 5), computed tomography angiography (CTA) (Figure 6), or scintigraphy studies. The innovations and development of new techniques and resources in cardiac imaging means also advancing and pushing knowledge boundaries in Sports Cardiology which drives the appreciation we sports cardiologists have for these resources.

RESTING TRANSTHORACIC ECHOCARDIOGRAPHY

1. Role of Echocardiography in the Cardiovascular Evaluation/Cardiac Screening of Athletes

Transthoracic echocardiography (TTE) is a cost-effective first-line imaging modality to evaluate the Athlete’s heart and differentiate physiological cardiac adaptations from pathological findings due to an underlying cardiovascular condition, especially those that may increase the risk of sudden cardiac death (SCD) during sports participation such as inherited cardiomyopathies, myocarditis, congenital abnormality of the coronary arteries, or aortic pathologies. TTE is always indicated in case of symptoms, family history of inherited cardiac condition or SCD in young relatives under the age of 40 years old, abnormal physical examination or in case of abnormal findings in the ECG. Athletes with cardiac pathology will also frequently require TTE in the follow-up.

TTE is not universally included in primary cardiac athlete screening protocols, but it has become a common practice for some clinicians. For us, at Aspetar, a TTE is always included in the first routine assessment of athletes and repeated periodically based on the age of the athlete and the type of sport.  The TTE protocol should be comprehensive, following the guidelines for TTE of the ASE for adults or children and must include the visualization and documentation of the origin of the coronary arteries, since this abnormality is one of the most common causes of SCD in young athletes. A proposed dataset for the echocardiography of athletes has already been published^, When available, the use of 3D techniques for the assessment of volume and ejection fraction (EF) of left and right ventricles should be used and strain imaging should complement the evaluation to detect subclinical abnormalities, especially in grey cases where discrimination between physiological adaptations and cardiac pathology may be complex.

2. Echocardiographic Features of the Athlete’s Heart and the Grey Zone to Cardiomyopathies

The interpretation of echocardiography in athletes requires expertise and understanding of the profound changes associated with the cardiac remodeling in athletes in the specific context of each individual and how to discriminate those changes from true pathology. The most important determinants of the cardiac adaptation to exercise are age, sex, ethnicity, type of sport, length of competitive activity and genetic factors.

The load associated with exercise training promotes harmonic enlargement of the four cardiac chambers. Left ventricle (LV) dilatation is therefore common in athletes which mean LV end diastolic diameter (LVEDD) of 48 mm in caucasian women (ranging 38 to 66 mm) and 55 mm in caucasian men (ranging 43 to 70 mm) are beyond the standard cut-off dimensions of LV cavity for normal population - up to 14% of elite athletes of both genders show diameters larger than 60 mm. The upper limit of normality (95th percentile) of the LVEDD was 63 mm for men and 57 for women in a cohort of 4267 elite, mostly caucasian, athletes. Considering only endurance athletes such as those engaged in cycling, triathlon, or rowing, the dimension of the LV may be even larger with LVEDD up to 66 mm in females, and 70 mm in males⁶. The differentiation of normality and abnormality on these athletes may be complex, especially since frequently there is a mild reduction on the systolic function which difficult the differential diagnosis with pathology such as dilated cardiomyopathy (DCM). In a cohort of elite cyclists it was found  that 51% had LVEDD over 60mm, 15% had mild reduction on the EF and up to 11% meet diagnostic criteria for DCM.

LV wall thickness should be measured in all LV segments from base to apex examined in end-diastole, preferably in the 2D short-axis view, ensuring that the wall thickness is recorded at mitral, mid-LV, and apical levels. Athletes may also develop mild wall thickening, with or without association with concomitant LV chamber dilation. The normal geometry of the athletic remodeling is the eccentric remodeling with relative wall thickness (RWT) <0.42, with balanced LV enlargement and wall thickening.  Isolated concentric remodeling (RWT ≥ 0.42 with normal LV mass index -LVMI-) may be seen in athletes involved in sports with a high static component such as weightlifting, being also found in athletes descendants of hypertensive parents. The presence of concentric hypertrophy (increased LVMI and RWT ≥ 0.42) requires careful differentiation from pathology (i.e. pressure overload due to arterial hypertension, or features of hypertrophic cardiomyopathy). Ethnicity has a great influence on the manifestations of the athlete’s heart with athletes of black ethnicity more prone to left ventricle wall thickening than caucasians. LV wall thickening attributable to athletic remodeling rarely exceed 12-13 mm in caucasian athletes^,  and 15 mm in black athletes. Adolescent athletes may have wall thickness Z-score of 2.0 to 3.3¹⁰, like those found in adolescents with genotype-positive for hypertrophic cardiomyopathy (HCM). During the follow up progression to a more LV hypertrophy seems to occur only in HCM genotype–positive patients, while athletes will develop larger LV volumes.

Systolic function, as measured by LV EF is normal or may be mildly reduced at rest, especially in endurance in athletes⁹, demonstrating excellent contractile reserve during exercise. This reflects the fact that stroke volume, not EF, is physiologically regulated; large ventricles eject a lower fraction of end-diastolic volume than smaller ventricles under resting conditions. However, studies using pulsed wave tissue Doppler (TDI), and speckle-tracking echocardiography (strain imaging) have shown that endurance athletes typically demonstrate preserved or enhanced systolic function^{, ,}.

Diastolic function in athletes is typically normal, although athletes with higher strength training load who have abnormal LV geometry (concentric pattern) may demonstrate mildly impaired indices of diastolic function. Abnormal transmitral filling profiles and reductions in early diastolic tissue velocities should raise suspicion for pathology¹⁸.

Athletes, especially those of black ethnicity, frequently show a hypertrabecular pattern that may require differential diagnosis with left ventricular non-compaction pattern, a sign of LV cardiomyopathy. Physiological hypertrabeculation is typically accompanied by normal thickening of the compacted layer, preserved or mildly reduced systolic function, with excellent contractile reserve on exercise and normal or enhanced diastolic function¹⁸. A recent study has shown that up to 6.5% of adolescent athletes with significant hypertrabeculation may meet criteria for LV cardiomyopathy, but athletes have normal 2-D strain results.

Dilation of the Right ventricle (RV) in athletes is proportionated to the degree of LV remodeling (RV/LV ratio <0.6). The finding of isolated RV enlargement should raise suspicion of pathology. Similarly, the RV enlargement in athletes is never associated with aneurysmal dilation or segmental dysfunction.  Nevertheless, athletes frequently show RV outflow tract (RVOT) dilatation that meet the criteria for arrhythmogenic cardiomyopathy (ACM). In a study of 102 endurance athletes, RV was larger than normal values in over one-half of the athletes and 28% had a RVOT dilatation meeting major criteria for ACM. In a cohort of 391 adolescent athletes, 14.8% did meet the major modified Task Force Criteria for RVOT dilation. Speckle tracking techniques have demonstrated to be very useful in the differentiation of normality from pathology in athletes with RVOT dilatation meeting diagnostic criteria for ACM^23,24 . Similarly to the LV, mild reductions in RV systolic function under resting conditions are often observed in trained endurance athletes with normal contractile reserve in exercise echocardiography.  RV function, as assessed by systolic strain and indices of diastolic function are normal in athletes. RV hypertrophy is very uncommon in athletes and should raise suspicion.

Atrium are also enlarged in many athletes compared to the non-athlete population. Studies have shown that both left atrium (LA) and right atrium (RA) undergo similar increases in size in endurance athletes. There are no differences in atrial strain when comparing athletes and sedentary controls.

Aortic root dimensions in healthy elite athletes are within the established limits for the general population. Mild aortic sinus or ascending aortic dilation may occur in young athletes but absolute aortic measurements of ≥40 mm (men) and ≥34 mm (women) are uncommon and should prompt additional investigations.

A systematic review and metanalysis from our group showed that echocardiographic changes related with athletic remodeling are already present in the heart of paediatric athletes older than 12 years, who have significantly greater LVDd (+8.2%), wall, RWT, LVM (+27.6%) and LA diameter (+12.3%) than non-athletes. One per cent of adolescent athletes had LV wall thick­ness >12 mm, in particular those of afro-caribbean origin. There were no significant differences in cardiac functional parameters between athletes and non-athletes.

Some athletes with extreme cardiac remodeling can meet criteria for cardiomyopathies and should be carefully evaluated. Athletes should always be assessed within a specific clinical context, with careful attention to family history, sports history and personal medical history, presence of symptoms or abnormal signs on the physical examination that can support suspicious diagnosis. The appropriate interpretation of the ECG of athletes is key in this context and after the echocardiography, if questions remain regarding possible pathology, additional tests such as exercise echocardiography, CMR, ambulatory ECG monitorization, cardiopulmonary exercise test etc. may be required.

Echocardiographic findings suggestive of pathology vs healthy athletic adaptation are summarized in Table 1.

3. Myocardial Mechanics in the Echocardiographic Evaluation of Athletes

Strain imaging is a method for measuring regional or global deformation of the myocardium. It can be done by using tissular doppler (TDI), which evaluates the velocity at which the myocardium contracts and relaxes, or speckle-tracking echocardiography (STE), which evaluates the motion and deformation of myocardial tissue by using the naturally occurring speckle patterns in the myocardium. The use of strain and strain rate has been demonstrated to be a very useful tool to differentiate physiological from abnormal cardiac remodeling^,24. Currently, left ventricular global longitudinal strain (GLS) is considered a reliable and objective method for evaluating LV systolic function (Figure 1), with the advantage of detecting subtle abnormalities even when the ejection fraction (EF) appears to be preserved.

The study of myocardial mechanics includes not only GLS, but also radial and circumferential strain, LV twist, atrial and RV strain as potential methods of distinguishing normality from pathology.  While radial strain has fallen out of favor because of poor reliability and reproducibility, left ventricular circumferential strain (CS) analysis (Figure 2) has shown to be robust and predictive of exercise performance during exercise. RV longitudinal 2-D strain analysis is important to exclude right-sided inherited pathologies such as arrhythmogenic cardiomyopathy (Figure 3). Recent studies using application of myocardial work (MW) analysis to evaluate myocardial performance in athletes has highlighted the role of this new methodology in sports cardiology in the differentiation of athlete’s heart from pathology, nevertheless the use of this technique is still vendor dependent and therefore very limited. Emerging other novel echocardiography technologies continue to help create a real time image of cardiac morphology and physiology, for example functional 3-D strain imaging enables us now to accurately visualize cardiac morphology and function of all chambers simultaneously in one heart beat (Figure 4.)

CARDIAC IMAGING DURING EXERCISE

It is important to note, that echocardiography is almost exclusively performed at rest, providing only limited knowledge on cardiac adaptation to exercise. The intriguing question is how the heart copes with intense exercise and what physiological mechanisms exist to facilitate a more than five times increase in cardiac output during exercise. These questions can only be directly addressed when imaging the heart during exercise. Importantly, this might also decipher what pathophysiological mechanisms might lead to SCD in athletes, as 33–56% of SCD events in young athletes occur with exertion^,. To investigate the heart under stress using quantitative methods has been trialled and researched more recently using echocardiography³¹ or cardiac MRI^, and many leading centres such as Aspetar include exercise echocardiography into the assessment of athletes. Exercise echocardiography is however not recommended to be integrated into first-line screening practice and is an investigation used to exclude or help diagnose underlying cardiac disease in athletes when family history, symptoms or positive screening investigation results exist.

Exercise echocardiography has benefited significantly from recent exciting developments in imaging equipment and processing technology, allowing for robust quantitative analysis providing unique insides into cardiac adaptive mechanisms and myocardial response to exercise^,31.  This knowledge is important in particular for athletes, where resting parameters of cardiac function may sometimes be lower than expected. It here allows us to classify whether reduced cardiac resting function has a physiological or pathological origin.

One such powerful tool is 2-D and 3-D myocardial strain imaging. This technique has enabled the detection of early even subclinical cardiac dysfunction or early cardiomyopathies previously not detectable. Studies into inherited cardiomyopathies for example have used strain imaging recently to pick up early disease in particular in diseases such as arrhythmogenic right ventricular cardiomyopathy, where early diagnosis is notoriously difficult and sudden cardiac arrest is the first presentation³². Using 2-D strain during exercise echocardiography has for example described the mechanisms, how the and increase in myocardial performance (cardiac reserve), measured by 2-D strain contributes significantly to the required increase in cardiac output and that this myocardial performance remains elevated to exercise levels into the recovery period in young athletes, indicating that myocardial performance plays a role in the removal of the post exercise oxygen debt⁴⁴. Exercise 2-D strain also highlighted, that myocardial performance during exercise is similar between youth athletes and their non athlete peers - exercise training does not lead to an increase in myocardial systolic performance and that the greater efficiency of an athlete’s heart lies elsewhere^{, 31}. In detailing the specific physiological response to exercise can be hypothesised to aid in the differentiation between the adaptive, physiological response vs the maladaptive pathological myocardial function in athletes.

A further step in obtaining a comprehensive picture of the cardio-pulmonary exercise physiology is the simultaneous performance of cardiopulmonary oxygen consumption (VO2) assessment, the gold standard exercise assessment of lungs and heart also in youth^, with quantitative exercise echocardiography (Figure 4), as besides a detail description of cardiac performance, it adds information on the metabolic and respiratory response to exercise, this providing additional invaluable data on aerobic and anaerobic fitness for the sports scientist and coaching team. This novel approach provides direct data on the much-investigated relationship between myocardial performance and metabolic parameters. A stress ECG run at the same time allows to exclude or diagnose exercise-induced arrhythmias, completing a time efficient and comprehensive cardiac profiling pathway in one setting (Figure 5.)

Cardiac MRI during exercise can provide data on cardiac volumetrics, more reliable calculation of cardiac output and blood flow, it requires however a complex set up that has hampered studies for many years. Recently however some research groups have succeeded in using exercise MRI to gain invaluable insights into cardiac physiology^41,40,.  Exercise MRI has helped for example to accurately describe physiological but also pathophysiological mechanisms of right ventricular adaptation to exercise and gave evidence to the concept, that early RV pathology, often not detectable at rest can be unmasked by exercise and delineated using exercise MRI. While exercise MRI is mainly used in the research setting,  the strength of MRI as a secondary investigation tool in sports cardiology lies however in performing cardiac MRI scans in athletes at rest.

CARDIAC MRI IN SPORTS CARDIOLOGY

Cardiac MRI is an important tool in the cardiac assessment of athletes. It has been used in primary screening, and while very accurate in delineating anatomy, in particular coronary arteries and volumetrics of the heart its cost- effectiveness and complex set up makes it unsuitable for primary cardiac screening.

It is however gold standard when it comes to assessing cardiac volumes and inherited cardiomyopathies also in athletes (Pelliccia, Caselli et al. 2018) comparable to TTE in its capacity to assess cardiac function and overall ventricular morphology, cardiac MRI has advantages when quantifying cardiac chamber volumes, coronary artery and vessel anatomy and blood flow patterns of the heart.

Cardiac function assessment using MRI have also been used describing focal myocardial wall motion abnormalities (WMA) with good accuracy, which is important as these WMA are early diagnostic findings in many cardiomyopathies in particular ACM also in athletes.

Compared to TTE, cardiac MRI has lower spatial and temporal resolution, but excellent contrast with blood pool makes it superior for the assessment of features important in diagnoses – cardiac chamber volumes, morphology, wall thickness and mass and it is usually superior to TTE in assessing regional wall motion in both ventricles. For these reasons cardiac MRI is the optimal tool when there is, after echocardiography, doubt in these parameters.

However, what sets cardiac MRI apart from other imaging modalities is tissue characterization – in short the ability to determine if the myocardium and interstitium are normally constituted. This has both diagnostic and prognostic use as early cardiomyopathies can mimic the athletic heart and vice versa, prominent physiological athletic adaptation such as eccentric (dilatation) and hypertrophic changes of the myocardium can be mistaken for cardiac disease. Cardiac MR imaging modalities such as T1 and T2 mapping have also improved detection of subtle acute myocardial disease such as infection associated to oedema and fibrosis, fatty infiltration or mild scarring. Pre and post contrast T1 tissue mapping is used to assess if the myocardium has a normal balance between interstitium and myocytes – important in the hypertrophic cardiomyopathies where the interstitium can be diffusely abnormal and when wall thickening could be due to athletic adaption (Figure 6). STIR/ T2 tissue mapping can detect focal and diffuse oedema allowing the detection of pathologies with an inflammatory component such as acute myocarditis. Turbo-spin imaging which has a role in detecting fat, which is important in Arrhythmogenic Ventricular Cardiomyopathy (Figure 7), which also frequently is associated with unbalanced RV dilatation and wall motion abnormality. Contrast cardiac MRI using Gadolinium is an invaluable tool to visualize current or previous cardiac injury such oedema, necrosis or fibrosis as a consequence of inherited or acquired cardiomyopathies, focal ischaemic cardiac disease or infection in athletes⁵⁰. In particular in the diagnostic but also follow up assessment of acute and subacute myocarditis, a significant cause of sudden cardiac events in athletes, gadolinium imaging (so called late enhancement) has a crucial role as it can delineate fibrotic changes, where as little as 1 gram of focal fibrosis can be detected. Fibrosis is a substrate for arrhythmias, in turn risk factors for sudden cardiac events in athletes, but can also be found in asymptomatic athletes, which poses a significant challenge when risk stratifying athletes. Beyond diagnosis of acute cardiac disease, cardiac MRI has an important role in decision making on return to play, for example after viral myocarditis. Contrast cardiac MRI can also aid in detecting thrombi in the cardiac chambers secondary to cardiac dysfunction, infection or systemic coagulation disorders – important to prevent stroke, PE or other thrombo-embolic events. Finally, sometimes it is important to take advantage of the whole body and flow imaging capabilities of MRI to discount mimics or other causes of myocardial disease such as congenital abnormalities leading to RV volume loading such as anomalous pulmonary venous drainage and optimally quantify arterial valve regurgitation. All above MRI techniques can help differentiate between physiology and pathology in athletes in the so called “grey zone”, where disease and physiological adaptation overlap and provide reassurance or diagnostic certainty and a cardiac MRI service should therefore be included in the modern set up of any sports cardiology department.

Computed tomography in sports cardiology

Coronary CT is the optimal non-invasive investigation for coronary artery course, position, myocardial bridging and atheroma, but is not often performed in young elite athletes as a clinical concern does not often arise. However, in the context of unexplained exertional chest pain or collapse, CT has the ability to delineate the anatomical information needed in more complex cases (Figure 8). In the older athlete (>age 40 years) coronary atheroma starts to become prevalent and the threshold for investigation may lower. CT is so effective as it is able to accurately assess coronary branches to 1-1.5 mm diameter due to combined spatial, temporal and contrast resolution that greatly exceeds MRI which is only the first choice if assessment of the proximal origin and course of proximal coronary arteries only are required as in Figure 9. While radiation dose should always be respected it has greatly reduced in recent decades and overall quality and accuracy means it is now considered the first line investigation for coronary artery disease. Other indications for cardiac CT are rare in athletes but may arise if other imaging modalities are not diagnostic – for example chamber size, ventricular morphology, pericardial assessment (thickening, calcification) and extra cardiac vascular anomalies. Typically, the acquisition time for a cardiac CT is <1 second so this can be of value if claustrophobia is a concern.

Cardiac imaging is key to the evaluation, diagnosis, treatment of follow up of the athlete’s heart. A comprehensive assessment of morphology and function of the athlete heart requires multiple imaging modalities and specific expertise. A knowledge of physiological adaptation and an awareness that phenotypes of disease can be very different from what is encountered in the non-athletic population are paramount. Most importantly, a close collaboration between sports cardiologist and radiologist is key to provide a bespoke athlete imaging service of the heart.

Carmen Adamuz Ph.D., M.D.

Cardiologist

Aspetar Orthopaedic and Sports Medicine Hospital,

Doha, Qatar

Mark Hamilton M.D.

Consultant Cardiac Radiologist

Department of Radiology

Bristol Heart Institute,

Bristol, UK

Guido E Pieles M.D., Ph.D.

Head of Sports Cardiology & Screening

Aspetar Orthopaedic and Sports Medicine Hospital,

Doha, Qatar

Contact: guido.pieles@aspetar.com

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