Novel echocardiographic techniques for the evaluation of athletes’ heart: A focus on speckle-tracking echocardiography

Abstract

Background

The development and rapid dissemination of two-dimensional echocardiography led to important further advances in our understanding of athletes’ heart that has been the subject of several echocardiographic studies involving many thousands of athletes. The description of ventricular chamber enlargement, myocardial hypertrophy and atrial dilatation has led to a more comprehensive understanding of cardiac adaptation to exercise conditioning. Most recently, advanced echocardiographic techniques have begun to clarify significant functional adaptations of the myocardium that accompany previously reported morphological features of athletes’ heart. In particular, speckle-tracking echocardiography (STE) has recently provided further insights into the characterisation of myocardial properties.

Discussion

STE is a relatively new, largely angle-independent, non-invasive imaging technique that allows for an objective and quantitative evaluation of global and regional myocardial function. STE has enhanced our understanding of athletes’ heart through a comprehensive characterisation of biventricular and biatrial function, providing novel insights into the investigation of physiological adaptation of the heart to exercise conditioning. These peculiarities can provide further useful data to distinguish between athletes’ heart and cardiomyopathies. Furthermore, STE represents a promising tool to address new concerns on right ventricular function and to increase understanding of the complexity of the non-systemic circulation, especially in the athletic population.

Conclusion

This review article analyses new data on cardiac function in athletes by novel echocardiographic techniques with a particular attention to the application of STE to characterise biventricular and biatrial function in athletes.

Introduction

The heart of the athlete has intrigued clinicians and scientists for more than a century. Early investigations in the late 1800s and early 1900s documented cardiac enlargement and bradyarrhythmias in individuals with above-normal exercise capacity. Since that time, scientific understanding of the association between sports participation and specific cardiac adaptations has paralleled advances in cardiovascular diagnostic techniques. Now, it is well known that participation in high-volume, high-intensity training programmes results in significant morphological and functional remodelling of cardiac chambers. These central and peripheral cardiovascular adaptations facilitate the generation of a large and sustained cardiac output and enhance the extraction of oxygen from exercising muscle.¹

The development and rapid dissemination of two-dimensional (2D) echocardiography has led to important further advances in our understanding of athletes’ heart that has been the subject of several echocardiographic studies involving many thousands of athletes.^2–7 The description of ventricular chamber enlargement, myocardial hypertrophy and atrial dilatation has led to a more comprehensive understanding of cardiac adaptation to exercise conditioning. Most recently, advanced echocardiographic techniques have begun to clarify significant functional adaptations of the myocardium that accompany previously reported morphological features of athletes’ heart. In particular, speckle-tracking echocardiography (STE) has recently provided further insights into the characterisation of the myocardial properties of athletes. This review article analyses new data on cardiac function in athletes by novel echocardiographic techniques, with particular attention to the application of STE to characterise athletes’ heart. We searched MEDLINE, Embase and the Cochrane Library database using the key terms ‘strain’, ‘speckle-tracking echocardiography’, ‘myocardial deformation’, ‘left ventricle’, ‘right ventricle’, ‘left atrium’, ‘right atrium’, ‘athletes’ and ‘training’. To ensure the identification of all relevant studies, the reference lists of these articles were scrutinised to identify further studies pertinent to the topic. The search was limited to adult human studies published in English. Abstracts without full text and editorial comments were excluded.

Speckle-tracking echocardiography

STE is a relatively new, largely angle-independent, non-invasive imaging technique that allows for an objective and quantitative evaluation of global and regional myocardial function. While older techniques of strain and strain rate, derived by tissue Doppler, are characterised by a low signal to noise ratio, with a lot of experience needed to interpret the data properly, STE is a relatively simple, reliable and reproducible technique.^8,9 Moreover, in contraat to tissue Doppler, which requires a precise alignment with the ultrasound beam, STE-based analysis of myocardial contraction allows the quantification of fibre deformation through virtually any plane of the space, regardless to the imaging plane. Using STE, blocks or kernels of speckles are semi-automatically traced frame by frame, providing local displacement information, useful to calculate all the spatial components of myocardial strain and strain rate.^8,9 In particular, myocardial strain is a dimensionless parameter expressed as the percentage of myocardial deformation; negative values indicate shortening or compression, while positive values indicate lengthening or stretching. Depending on spatial resolution, selective analysis of epicardial, mid-wall and endocardial function may be possible, obtaining longitudinal, radial and circumferential strain.^10–12 In addition, STE offers an evaluation of the occurrence, velocity and direction of left ventricular (LV) rotation.¹³ STE can be applied to both ventricles and atria. However, while all LV segments can be analysed successfully in most patients, signal quality may be suboptimal for atria and the right ventricle, because of their thin walls.⁸ It is noteworthy that whereas feasibility is best for longitudinal and circumferential strain, it is more challenging for radial strain.⁸ The main limitations of this new echocardiographic technique are that STE relies on good imaging quality and that differences among vendors still exist, driven by the fact that STE analysis is performed on data stored in a proprietary scan line format, which cannot be analysed by other vendors’ software. Thus, the lack of a standardisation of different speckle-tracking algorithms among vendors makes it difficult to establish normal values and to compare data generated by different centres. However, efforts are being made to improve the communication between vendors, and use similar algorithms for the assessment of myocardial strain also promoted by the American Society of Echocardiography.¹⁴

Left ventricular mechanics

The human heart has a complex structure of muscular fibres, organised in layers. LV sub-endocardial and sub-epicardial fibres have a longitudinal disposition, from the apex to the base, drawing a spiral around the ventricle (sub-epicardial are clockwise oriented, sub-endocardial are counter clockwise, seen from the apex to the base), while the mid-wall fibres are circumferential.¹⁵ Contraction and relaxation of all these fibres generates a complex deformation and movement of the LV walls both in systole and diastole. The final global result is systolic blood ejection into the aorta and diastolic ventricular filling.

The left ventricle also had a wringing motion around its long axis induced by contracting myofibres in the LV wall, called twisting.¹⁶ Twisting is generated by the opposite rotation of the LV base and the apex. Basal and apical LV rotation are expressed in degrees as well as twisting, which is their algebraic sum; torsion is obtained dividing twisting by the length of the LV cavity, in degrees/cm. LV twisting is followed by rapid isovolumic untwisting of the ventricle.¹⁷ The left-handed helix of the epicardium dominates rotational motion due to its longer lever arm from the centre of the LV. The endocardial layer, with a right-handed helix, moves together with the epicardium, although providing some opposition to epicardial motion.¹⁸ As a result of twisting, epicardial and endocardial sarcomere shortening in all directions tends to be equilibrated during ejection, resulting in reduced stress between myocardial fibres.¹⁹ During contraction, potential elastic energy is stored and its release (recoil) causes rapid untwisting^20,21 and contributes to active suction of blood from the atria.²² The recent introduction of STE has drawn new attention to LV mechanics and to LV twisting.^23,24 The STE technique can allow a reliable assessment of myocardial deformation along the three-dimensional (3D) geometrical axes (longitudinal, circumferential and radial strain) throughout the cardiac cycle and it has shown the ability to quantify transmural (endocardium and epicardium) twisting.²⁵

Speckle-tracking echocardiography to assess LV function in athletes’ heart

Longitudinal, radial and circumferential strain

The main echocardiographic studies using 2D STE in athletes’ heart are summarised in Table 1. Richand et al. analysed 29 professional soccer players, 26 patients with hypertrophic cardiomyopathy (HCM) and 17 sedentary controls.²⁶ They found that radial and transverse strains were significantly higher in athletes as compared with controls, whereas longitudinal strain was lower. However, compared to patients with HCM, professional athletes had higher values for transverse, radial and circumferential strains. Thus, the authors concluded that, while 2D STE was able to identify specific patterns of myocardial deformation in athletes, controls and patients with HCM, the lower value of global LV longitudinal strain observed in athletes (as compared to controls) could be a marker of a specific myocardial adaptation to the exercise-induced increase in volume overload, according to La Place’s law.²⁶ Caselli et al. recently confirmed these findings in Olympic athletes, demonstrating that, despite being within the normal range, LV longitudinal strain is lower compared with controls.²⁷ Conversely, further cross-sectional studies showed minimal or no differences in global LV longitudinal, radial and circumferential strains, as compared to healthy controls,^28–31 and Simsek and colleagues found that athletes had even higher values of global longitudinal strain (GLS) as compared with controls.³²

In order to allow a differential diagnosis of physiological (adaptive) versus pathological (maladaptive) LV hypertrophy, many studies have been designed to assess differences in LV mechanical deformation in athletes and in patients with essential hypertension^30,31 and non-obstructive HCM.^26,29,33 All these studies agree with a reduction in longitudinal strain as an early sign of LV dysfunction. This finding can be explained by the fact that the subendocardium is the first layer to be involved in many cardiac diseases (such as ischaemic, hypertensive, diabetic and valvular heart diseases) and longitudinal strain, primarily related to the myocardial deformation of subendocardial fibres, is expected to be impaired in the early stages of the cardiac disease. Conversely, circumferential and radial strains could still be normal when longitudinal dysfunction appears, becoming impaired when the natural course of the disease progresses.

In view of the growing application of 2D STE on the integrated imaging-based diagnosis of cardiomyopathies, knowing whether exercise modifies LV strain is of extreme importance. However, although STE has been applied in athletes’ heart to characterise LV myocardial deformation properties in cross-sectional studies comparing athletes to controls, at the present time only a few longitudinal data are available regarding the time and extent of training-induced changes. In 2010, Weiner and colleagues³⁴ longitudinally examined male university rowers, providing data on exercise-induced LV twist mechanic changes; however, longitudinal, circumferential and radial strains were not reported in that study. Spence et al. reported that, in untrained subjects randomly assigned to endurance or resistance training, LV longitudinal strain did not change, despite an increase in LV mass and in LV volumes.³⁵

Another important parameter to take into account when applying a speckle-tracking technique to athletes’ heart is LV geometry. Indeed, changes in mechanical loading of the LV are often accompanied by a change in LV shape through a process in which the LV tends to become more spherical and/or the wall thickness increases,³⁶ and exercise is known to cause LV remodelling characterised by concentric or eccentric hypertrophy, according to the type of training, the gender and the ethnicity.^1–7,37 However, regional longitudinal wall curvature and thickness are important determinants for the amplitude and shape of the transmural distribution in passive end-diastolic fibre stress and strain.³⁸ Thus, although other authors demonstrated that the influence of geometry on fibre stress and strain is present, but moderate in character,³⁹ it seems reasonable when applying STE to athletes’ heart to take into account the geometry of the LV in order to interpret the values obtained accurately. According to these considerations, the sports discipline is specified in Table 1, reporting STE-derived values for the LV.

Taken together, these data seem to suggest that a reduction in LV GLS is an uncommon feature in athletes’ heart and cannot be considered a physiological adaptation to training, irrespective of the training period when cardiac examination is performed. Thus, in the presence of significantly reduced LV strain, the individual athlete should be carefully evaluated, particularly in the presence of doubtful LV hypertrophy. Despite the definition of a normal range being limited by inherent variability by age, by haemodynamic conditions and by differences among vendors, as expressed before, the current recommended normal value for the normal population is ≥18 with standard deviations of 2–3%, and a measure of ≤12% definitively constitutes an abnormal value.⁷

Left ventricular twisting and untwisting

Strain-derived LV twisting is probably the more intriguing novel parameter in the assessment of athletes’ heart physiology. STE-based case–control studies on athletes’ heart demonstrated lower values of LV twisting in professional soccer players⁴⁰ and in elite cyclists.²⁸ Notting et al. observed that the reduction in LV twist is mainly driven by a reduction in apical rotation, with the LV apex being more sensible and dependent to the sympathetic activity than the LV base,²⁸ as demonstrated in an animal model by a greater β-adrenergic receptor density and/or increased myocardial responsiveness to adenylate stimulation in apical myocardium.⁴¹

The reduction in apical rotation and in LV twisting observed in athletes seems to be related to training-induced changes in sympathovagal balance, and could be interpreted as a functional reserve to help the athlete sustain the delivery of oxygen and energetic substrates to the muscles while performing a training session or a competition. This hypothesis seems to be confirmed by studies on healthy subjects showing an increase in LV twisting during laboratory-based submaximal exercise.^24,42,43

Although LV twisting seems to give a relevant contribution in studies investigating cardiac physiology, its role in the differential diagnosis, and particularly in the identification of pathological hypertrophy, is not well established and deserves more insights, contrary to the clinical utility of LV longitudinal strain. Indeed, Cappelli et al. found that in patients with hypertension, LV longitudinal strain was reduced while LV torsion was increased, compared with controls, with no differences between athletes and controls.³⁰ Conversely, Galderisi and colleagues, analysing 19 sedentary controls, 22 top-level rowers and 18 young newly diagnosed patients with hypertension, found that, despite significant differences among the groups in LV longitudinal strains, LV torsion was similar among athletes, controls and hypertensive patients.³¹ Interestingly, while Soullier et al. demonstrated that patients with HCM had lower values of LV longitudinal, radial and twist compared with controls, while exercise induced a modest increase in LV longitudinal strain, it was not able to change LV twist in these patients.³³

According to these results, further data are necessary on LV twist mechanics before the widespread use of this parameter in clinical practice, particularly in the setting of the differential diagnosis between athletes’ heart and pathological hypertrophy.

Speckle-tracking echocardiography for the assessment of right ventricular function: novel insights for sports cardiologists

Although athletic training results in remodelling of all cardiac cavities, morphological and functional adaptations of the right ventricle have been given considerably less attention compared with those of the left ventricle and atrium. The formal assessment of the right ventricle has often been neglected primarily because of the lack of simple and reliable methods to estimate right ventricular (RV) function. Indeed, the right ventricle has a complex geometry, a wide range of loading conditions and a great heterogeneity of regional function.⁴⁴ However, recently the interest in the assessment of RV function has grown, at least in part because novel echocardiographic techniques, and particularly STE, have the ability to overcome some of the major limitations to RV quantification.

STE has recently been applied to the investigation of the right ventricle in athletes, as summarised in Table 2. While some authors have investigated differences among the left and the right ventricle in absolute values of STE-derived strain,⁴⁵ others have analysed the relationship between RV size and myocardial deformation, demonstrating a lack of allometric association with RV global strain.⁴⁶ Controversial data on RV strain in athletes are currently available: indeed, while Oxborough et al. found that athletes show normal values of RV longitudinal strain,⁴⁶ Teske et al. demonstrated lower values of GLS in elite athletes compared to non-elite athletes and controls, as a consequence of much lower basal deformation.⁴⁷ Although the mechanisms behind this discrepancy remain to be elucidated, a modest reduction in systolic deformation at the inlet portion of the right ventricle (i.e. the basal wall) can be explained by different curvature changes in RV apex and basis, acting as a mechanism to modulate wall stress and resulting in differences in strain between apical and basal RV segments. Moreover, exercise-induced RV dilatation primarily involves both the RV inlet portion and the main body, and to a lesser extent the right ventricle outflow tract.⁴⁸

In 2012, La Gerche et al., using STE and strain rate imaging, demonstrated that resting measures of RV function in athletes are a poor surrogate of RV function reserve and, in endurance athletes, measures obtained at rest should not be interpreted as a sign of subclinical myocardial damage, but rather as exercise-induced physiological changes.⁴⁹ Particularly for the basal segment, the authors hypothesised that, given that volume is greatest at the RV base, a lesser degree of deformation may be required to generate the same stroke volume, thereby explaining why RV deformation may be reduced in this region.⁴⁹

Pagourelias et al. recently confirmed that morphological adaptations of right heart cavities are not accompanied by RV functional impairment.⁵⁰ Indeed, even among highly trained athletes, global RV longitudinal strain is preserved, if not increased, providing evidence that RV function at rest remains within the normal range in athletes, irrespective of sports discipline, training volume and morphological remodelling. Recently, combining 2D STE with 3D echocardiography, Esposito et al. demonstrated that RV global and free-wall longitudinal strain were even greater in rowers as compared with sedentary controls (P < 0.005 and P < 0.001, respectively), with free-wall longitudinal strain being related to LV end-diastolic volume and stroke volume.⁵¹

However, concerns have recently been raised about the detrimental effects of strenuous and chronic exercise training on RV morphology and function in cohorts of endurance athletes, prompting the clinical question of exercise-induced RV damage.^49,52,53 Given its ability to characterise RV function, 2D STE has often been used by researchers investigating exercise-induced arrhythmogenic RV cardiomyopathy. Indeed, Oxborough and colleagues provided new data on RV dysfunction after ultra-endurance exercise⁵⁴ demonstrating that, after a 161-km marathon, while RV size significantly increased, RV strain significantly decreased post-race (−27% to −24%, P = 0.004) together with a decrease in LV longitudinal (−18.3% to −16.3%, P = 0.012), circumferential (−20.2% to −15.7%) and radial (53.4% to 40.3%, P = 0.009) strain. Furthermore, in conjunction with a reduction in peak RV strain, a slight delay in time to peak strain was observed. According to these data, the authors suggested that the marked impact a single endurance event can have on RV structure and function represents a ‘cardiac fatigue’ process from which well-trained athletes recover.

In 2011, La Gerche and colleagues applied 2D STE to the right ventricle of 40 athletes investigated at baseline, immediately following an endurance race, and one week post-race.⁵³ In that study the authors used conventional echocardiography and STE in conjunction with cardiac magnetic resonance, demonstrating that RV function (measured by RV ejection fraction, RV fractional area change, RV tricuspid annular plane systolic excursion and RV longitudinal strain) decreased post-race, with a mostly complete recovery after one week. In particular, RV strain decreased post-race (−27.2 ± 3.4 vs. −23.7 ± 3.7%, P = 0.001) and a recovery was observed after one week (−25.6 ± 3.0%).

While the acute effects of single bouts of exercise before and after a race have been investigated, particularly in endurance athletes, both the short and long-term effects of training in athletes have received less attention. Two-dimensional STE seems to be a promising tool to address concerns arising from the current literature and to increase understanding of the complexity of the non-systemic circulation, especially in the athletic population.

Notably, RV strain imaging has demonstrated the fundamental ability to identify regional wall motion abnormalities in patients with arrhythmogenic RV cardiomyopathy/dysplasia (ARVC/D).⁵⁵ RV regional abnormalities have also been detected by STE in asymptomatic patient carriers of genetic mutations for ARVC/D.⁵⁶ Thus, strain and strain rate imaging, being able to quantify regional RV dysfunction objectively, may improve our ability to diagnose ARVC/D and to distinguish between physiology and pathology. Given the usefulness of STE for the investigation of RV myocardial deformation, sports cardiologists will probably be more confident with this new technology in the next few years. However, to date, studies investigating RV function in athletes by STE remain limited, and it is crucial to qualify the normal reference values for strain imaging of each RV regional segment in the athletic population and to know whether significant changes do occur during the season, before deciding whether such findings should provoke further evaluation.

Atrial remodelling in athletes: when morphology is not enough

Several studies have focused on left atrial (LA) size in highly trained athletes, demonstrating that LA enlargement is a component of athletes’ heart, occurring in close association with LV cavity enlargement.^57–59 However, LA size is known to be insufficient to provide mechanistic information about the LA itself and, contrary to the previous belief, peculiarities of LA remodelling in the context of athletes’ heart go beyond the mere dimensional volumetric increase. Indeed, the application of 2D STE to the left atrium of athletes demonstrated that strain imaging is able to identify a peculiar adaptation of LA myocardial deformation to exercise conditioning.⁵⁶ Indeed, athletes show a shift in the pattern of ventricular filling period towards early diastole, which is accompanied by a lower LA active contribution to LV filling exhibited in comparison with sedentary controls, with peak atrial contraction strain being lower in athletes as compared with controls (P < 0.0001).⁶⁰

The extent of LA adaptation in athletes modifies during the competitive season according to changes in loading conditions,⁶¹ and LA functional remodelling has been demonstrated to be dynamic in nature, both in male and female athletes.^62,63

Two-dimensional STE has been applied in athletes also to the right atrium. Using 2D STE in 100 top-level athletes we found that both peak atrial longitudinal strain and peak atrial contraction strain were reduced in athletes as compared with controls (P ≤ 0.001 for both), with the former exhibiting a better diastolic function.⁶⁴ Thus, similar to the left atrium, the right atrium of athletes also had a peculiar adaptation to training that goes beyond mere cavity enlargement. Two years later, Pagourelias et al. applied STE to the right atrium in a cohort of 108 athletes (80 endurance and 28 strength-trained athletes), reporting similar values and confirming that in athletes, despite a dilatation of the right atrium, the functional properties remain preserved, contributing through atrioventricular coupling to preload increase and stroke volume augmentation.⁵⁰ Thus, while atrial dilatation can be found both in athletes’ heart and in cardiomyopathies, in the latter, contrary to athletes’ heart, atrial function is not preserved and deformation indices are decreased.^{48,57,65–67} Taken together, the application of STE to the atria may not only provide further insights into the investigation of physiological adaptations to exercise, but may also serve as a new, useful parameter to distinguish between athletes’ heart and cardiomyopathies.

Furthermore, the interest for an evaluation of LA mechanical function in the athletic population has been raised, given the possibility to clarify the controversial relationship between atrial fibrillation and exercise conditioning, by a detailed study of biatrial function. A new non-invasive estimation of LA stiffness, using intra-cavity filling pressures in conjunction with the percentage of maximal LA myocardial deformation, has recently been proposed as a reliable method,⁶⁸ demonstrating good agreement with the invasively assessed LA stiffness.⁶⁹ The E/e′ ratio is used in conjunction with LA global peak atrial longitudinal strain to derive a non-invasive dimensionless parameter of LA stiffness.^68–71 It has been demonstrated that LA stiffness is a predictor of the maintenance of sinus rhythm after cardioversion for atrial fibrillation,⁷⁰ and it may predict atrial fibrillation recurrences after pulmonary vein isolation.⁶⁸ In the context of physiological remodelling, the assessment of LA stiffness in athletes has clarified exercise-induced atrial adaptation, demonstrating that, despite a greater LA size, this physiological remodelling is accompanied by a low LA stiffness,^63,72 contrary to data found in patients with cardiomyopathies or atrial fibrillation.

Conclusions

Deformation imaging has enhanced our understanding of athletes’ heart through a comprehensive characterisation of biventricular and biatrial function, providing novel insights into the investigation of physiological adaptation of the heart to exercise conditioning. These peculiarities also seem to be promising to provide further useful data to distinguish between athletes’ heart and cardiomyopathies. Despite the growing body of evidence in the past few years, more data based on STE echocardiography are needed to identify clearly the potential of these new imaging techniques in the clinical context. Furthermore, in view of the growing application of STE in the integrated imaging-based diagnosis of cardiomyopathies, despite recent studies demonstrating that exercise is not able to affect LV strain significantly during the agonistic season, further data are warranted to characterise the possible training-induced dynamic changes in LV strain values.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of interest

None declared.

References