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J Am Coll Cardiol Img, 2009; 2:350-363, doi:10.1016/j.jcmg.2008.12.011
© 2009 by the American College of Cardiology Foundation
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State-of-the-Art Paper

Athlete's Heart: The Potential for Multimodality Imaging to Address the Critical Remaining Questions

Andre La Gerche, MBBS, FRACP*, Andrew J. Taylor, MBBS, FRACP, PhD{dagger}, David L. Prior, MBBS, FRACP, PhD*,*

* St Vincent's Hospital and University of Melbourne, Melbourne, Australia
{dagger} Alfred Hospital and Baker IDI Heart and Diabetes Institute, Melbourne, Australia


   Abstract
Top
 Abstract
Imaging Modalities
 Defining the Athletic Heart...
 Separating Athlete's Heart From...
 Conclusions
 REFERENCES
 
Moderate exercise is a powerful therapy in the treatment and prevention of cardiac disease, but intense habitual exercise leads to cardiac adaptations for which the prognostic benefits are less clear. The athlete's heart syndrome refers to the morphological and electrical remodeling which occurs to varying extents dependent upon the sporting discipline. Its accurate differentiation from pathological entities is critical. This review describes the role multi-modality imaging serves in determining the limitations and consequences of intense exercise. Tissue characterization and imaging studies during exercise are emphasized as important future directions of inquiry with the potential to address remaining controversies.

Key Words: athlete's heart • cardiac structure • cardiac function • myocardial injury

Abbreviations and Acronyms
  CMR = cardiac magnetic resonance
  HCM = hypertrophic cardiomyopathy
  LA = left atrial
  LV = left ventricle
  LVEF = left ventricular ejection fraction
  LVH = left ventricular hypertrophy
  PET = position emission tomography
  RV = right ventricle
  SPECT = single-photon emission computed tomography
  TDI = tissue Doppler imaging

The heart of an elite athlete has long been recognized to differ from the heart of a nonathlete, and these changes have been termed the athlete's heart syndrome. Investigations have predominantly focused on differentiating the athlete's heart from potentially lethal pathological conditions that may produce a similar cardiac morphology, so that "at-risk" athletes can be advised against continued sporting participation. In this regard, both established and novel cardiac imaging modalities have been used and the issue is of practical importance because athletes are frequently referred to the cardiologist with symptoms of fatigue, palpitations, or presyncope.

Numerous large observational and cohort studies have confirmed the graded benefit of exercise on cardiovascular health and mortality (1), resulting in a clear need to promote moderate exercise in the general community. However, the assumption that the positive relationship between the benefit of exercise intensity and exercise duration continues into the realms of intense competitive sport is more controversial and is also clinically relevant. Recent research questions whether the athlete's heart syndrome is completely benign or whether it may impact on long-term health and sporting performance. Newer imaging modalities may have an important role in addressing this important line of enquiry. This review will explore frequently encountered diagnostic challenges and summarize the role cardiac imaging plays in defining the boundaries of what constitutes the athlete's heart syndrome, the limitations of our understanding of physiology, and the significance of morphological remodeling.


   Imaging Modalities
Top
 Abstract
 Imaging Modalities
Defining the Athletic Heart...
 Separating Athlete's Heart From...
 Conclusions
 REFERENCES
 
As in other areas of cardiology, the important areas of interest in sports cardiology relate to morphology, function, metabolic activity, and tissue characterization. Figure 1 schematically details the relative contribution of differing imaging modalities toward a more complete understanding of the physiology in athlete's heart syndrome. Echocardiography has contributed most to our current understanding of cardiac morphology in athletes and is likely to remain critical given its low cost, widespread availability, and lack of ionizing radiation. High temporal resolution enables the assessment of myocardial function during exercise and interpretation of myocardial characteristics during the short isovolumic and rapid acceleration phases of cardiac motion. Cardiac magnetic resonance (CMR) has excellent spatial resolution down to 1.5 to 2.0 mm2 (in plane) and image quality that is not influenced significantly by body habitus, which permits the very precise assessment of cardiac chamber size, myocardial mass, and systolic function in almost all people. This is particularly relevant for assessment of the irregularly-shaped right ventricle (RV), where it is considered the gold standard.


Figure 1
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  		Figure 1 Important Domains of Study in Athlete's Heart

Demonstrating the progressive importance of function, exercise studies and tissue characterization and detailing the potential for each imaging modality to progress current understanding. Angio = angiography; CMR = cardiac magnetic resonance; CT = computed tomography; Echo = echocardiography.

 
Radionuclide ventriculography provides accurate measures of ventricular function that do not rely upon geometrical assumptions and also has been used to assess function with exercise. Its potential in athletes has not been realized, probably as the result of cost and significant radiation exposure. Positron emission tomography (PET) and single-photon emission computed tomography (SPECT) imaging have been used to evaluate perfusion reserve in athletes. Cardiac computed tomography scanning has shown great promise in the evaluation of coronary artery disease and offers superb spatial resolution for anatomical definition. It has, however, been seldom used in the athlete population despite the advent of multislice scanners with shorter acquisition times. The limited temporal resolution, radiation dose, and limited ability to evaluate function have largely restricted its use to older athletes in whom noninvasive evaluation of coronary anatomy is relevant.

Although most imaging studies have described a unique cardiac structure in athletes, few attempt to elucidate the significance of such changes. As illustrated in Figure 1, tissue characterization may be important in this future endeavor. An imaging technique capable of identifying subtle changes in myocardial and interstitial tissue composition may ascertain whether the morphological changes observed in athletes are physiological or pathological, permitting better differentiation between the normal heart, the normal athlete's heart, and the truly abnormal heart.


   Defining the Athletic Heart Syndrome
Top
 Abstract
 Imaging Modalities
 Defining the Athletic Heart...
Separating Athlete's Heart From...
 Conclusions
 REFERENCES
 
The athlete's left ventricle.   Numerous studies have evaluated the structure of athletes' hearts, enabling a comprehensive description of the normal ranges for this group. Pluim et al. (2) performed a meta-analysis of 66 echocardiography studies that compared 1,451 athletes with 813 control subjects. Athletes were grouped into 3 similarly sized groups based upon the differing physiological loads of each type of exercise, i.e., endurance, power, or a combination of power and endurance. In endurance sports (long-distance running), volume loading of the heart predominates, with cardiac output increasing as much as 8-fold and only moderate increases in systemic blood pressure. In power sports (involving lifting or throwing of heavy objects), blood pressure can increase spectacularly (up to 480/350 mm Hg, for example) (3), whereas only a moderate increase in cardiac output occurs. In combined sports (cycling and rowing), there is a substantial increase in both volume and pressure loading. In all groups, athletes had significantly larger left ventricular (LV) diameters and greater LV hypertrophy (LVH) than control patients. Although the modeling was progressively more eccentric in athletes performing more endurance training, most athletes maintain relatively balanced hypertrophy (4). Cardiac magnetic resonance imaging has validated these findings, with smaller cohorts being required given the improved accuracy of this modality in measuring wall thickness, mass and volumes (5,6). Figure 2 presents a range of published measures of cardiac structure and function in athletes and nonathletes.


Figure 2
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  		Figure 2 Changes in Morphology and Function in Athlete's Heart

Ranges of values for athletes' hearts are obtained from published studies. Proposed cutoff values for athletes (bold) beyond which pathology may be considered. *IVSd and LVM ranges include black athletes; {dagger}normal ranges not validated. EF = ejection fraction; IVSd = interventricular septal defect; LA = left atrial; LVEDV = left ventricular end-diastolic volume; LVIDm = left ventricular internal diameter at midventricle; LVM = left ventricular mass; RVEDV = right ventricular end-diastolic volume; RVEF = right ventricular ejection fraction; RVFAC = right ventricular function area change.

 
The athlete's right ventricle.   A number of echocardiographic studies have assessed right ventricular geometry and function in both male and female athletes (7–10). The definition of the RV's complex structure is far superior using CMR. This enables quantification of RV mass and wall thickness. Scharhag et al. (5) described changes mirroring those of the LV with increases in mass, end-diastolic, and stroke volumes relative to nonathletes. The ratio of LV to RV size was maintained, leading to the conclusion that athlete's heart syndrome involves balanced remodeling of both ventricles.

Real-time 3-dimensional echocardiography can provide measures of LV volumes and mass comparable with CMR in normal and diseased hearts, and this technique has been validated in athletes (11,12). Although recent studies have offered renewed optimism for 3-dimensional echocardiography derived measures of RV function, there are no current studies in athletes. It may be anticipated that the outstanding correlations with CMR reported by Niemann et al. (13) would be more difficult to obtain in the enlarged hearts of athletes.

The athlete's atria.   Athlete's heart syndrome is not confined to ventricular remodeling. Left atrial (LA) enlargement is a consistent finding in echocardiographic descriptions of cardiac structure in athletes (14–18). Pelliccia et al. (17) noted that marked LA enlargement (>45 mm in transverse dimension) was rare (<2% of 1,777 competitive athletes studied). LA dilation was proportional to LV dilation and the extent of endurance sport performed. Whether the LA enlargement increases the risk of subsequent atrial fibrillation remains a contentious issue (14–16,18).

Cardiac function during exercise.   Maximal oxygen update is increased in athletes as the result of up-regulation of both cardiopulmonary delivery and skeletal muscle utilization. Compared with nonathletes, the greatest difference is the ability to increase cardiac output. This is attributable to enhanced stroke volume because maximal heart rate is not enhanced by athletic training (19). The exact nature of stroke volume augmentation is the source of some debate (20,21), but recent studies suggest contributions from increased diastolic volume, more rapid diastolic filling, and enhanced systolic contractility compared with nonathletes (22). These assessments are based on the indirect method of acetylene rebreathing developed by Grollman 80 years ago (23). We now have the imaging tools for direct cardiac assessment during exercise; yet, their use in athletes has thus far been limited.

Echocardiographic measures such as tissue Doppler imaging (TDI) and strain rate imaging are gaining increasing acceptance as reproducible measures of myocardial function during exercise. Commercial ergometers enabling exercise in a semirecumbent position with lateral tilt are readily available (Fig. 3); however, respiratory and body movement can further compound limitations in spatial resolution. Ergometers that are compatible with CMR and nuclear imaging have now been developed and may enable very accurate volume assessments to be obtained during exercise. Using these modalities, compromises in temporal resolution are required at greater heart rates. Despite these technical challenges, imaging modalities offer potential advances over indirect gas elimination techniques for understanding of cardiac mechanics with exercise.


Figure 3
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  		Figure 3 Stress Echocardiography to Exclude a Cardiomyopathy

Exercise can be used to differentiate low systolic function from a myopathic process. Imaging during exercise is critical in athletes and can be achieved using a recumbent ergometer (top panel). End systolic frames at rest (A and B) and peak exercise (C and D) demonstrate excellent augmentation of low-normal resting function.

 
The hemodynamics of exercise remain incompletely understood, especially in the extremes of well-trained athletes. Elevation in LA pressure with exercise has been considered a pathological phenomenon. However, during intense exercise athletes may develop significant increases in LV filling pressures (24,25). Although these findings have been derived by direct catheterization, the validation of noninvasive echocardiographic measures of LA pressure with exercise (26) enable these observations to be tested on larger groups of athletes. Pulmonary artery systolic pressure also can increase dramatically in well-trained athletes during intense exercise, resulting in a disproportionate increase in RV after load when compared with that of the LV (25). Pulmonary artery systolic pressure can be accurately quantified by echocardiographic interrogation of tricuspid regurgitant signals at rest and with exercise (27) and, using this technique, Bossone et al. (28) demonstrated that pulmonary artery systolic pressure increases were more profound in athletes during exercise than in nonathletes.

Despite the theoretical incentives to measure myocardial mechanics during exercise, only a few investigators have attempted this in athletic cohorts. D'Andrea et al. (29) used echocardiographic TDI measures to demonstrate augmentation of both systolic and diastolic function during exercise in 25 elite swimmers. Adler et al. (30) observed similar augmentation of systolic and diastolic function in power athletes (weight lifters) when compared with control patients. After isometric exercise (3 "power-presses") the athletes showed only a small increase in heart rate but a significantly greater increase in stroke volume and ejection fraction, which probably was related to enhanced early myocardial relaxation, as demonstrated by enhanced early diastolic mitral annular velocities. In contrast, Vinereanu et al. (31) found no significant difference in the extent of augmentation between different athletic groups (power and endurance) and nonathletes. The reason for these inconsistencies is not easily explained given the similar methodology.

To avoid the compromise of image quality in real-time exercise studies, early post-recovery studies may be a reasonable substitute. In athletes, this has significant limitations. Chronotropic and inotropic recovery may be so brisk that measures are affected significantly by the time from exercise cessation. Neilan et al. (32) and Poh et al. (33) conducted 2 studies using echocardiographic measures within 10 min of exercise cessation. Seventeen elite rowers showed augmentation of LV systolic function (measured by tissue velocity, strain, and torsion), but attenuation of diastolic tissue velocities and RV apical strain. In contrast, after a 3,000-m speed skating event, there was augmentation of both systolic and diastolic function in both ventricles. It is unclear whether we can attribute these differences to the seemingly subtle differences in physiological demands of skating versus rowing or the difficulties of using measures with significant variability in a setting of rapidly changing physiology. Despite these limitations, attempts at reconstructing cardiac physiology during or after exercise remain important.

Cardiac function at rest.   It is a far easier prospect to measure cardiac function in athletes at rest than during exercise and important to know whether the enhanced diastolic and systolic function seen during exercise is also apparent at rest. There are some inconsistencies in current evidence regarding whether athletes demonstrate supranormal, normal, or even reduced measures of cardiac function at rest. All of the available literature in these comparisons involves echocardiographic measures of chamber volume, myocardial velocities, or deformation.

Table 1 (41–49,63,65) summarizes the range of findings from echocardiographic studies of myocardial motion and deformation. Zoncu et al. (41) and Caso et al. (42) reported supranormal systolic and diastolic myocardial velocities. Poulsen et al. (43) described enhanced velocities in power athletes, but not endurance athletes. Other studies observed no differences (44–46) or even lower myocardial velocities and strain rate in endurance athletes (47,48). King et al. (49) found no difference between early diastolic myocardial velocities in 30 control patients and 36 elite athletes, nor was there a difference in a noninvasive measure of LV filling pressure. Because of a substantial difference between groups in LV size, they argued that this represents a reduction in LV stiffness in athletes.


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  		Table 1 Comparison in Functional Measures Between Athletes and Nonathletes
 
Cardiac metabolism and perfusion in athletes.   The assessment of myocardial perfusion has been largely undertaken using nuclear imaging, although magnetic resonance imaging and contrast echocardiography may be useful in future studies. Athletes have been assumed to have a favorable coronary risk profile because of the protective effect of exercise and effects on risk factors. Although the assumption of lower atherosclerotic burden has recently been challenged (50), no studies that used SPECT for this purpose have been performed to date. However, SPECT has been used to address the etiology of sinus bradycardia in athletes. Estorch et al. (51) used iodine-123-metaiodobenzylguanidine to measure sympathetic innervation. A preponderance of iodine-123-metaiodobenzylguanidine defects were found in the inferior wall of athletes with bradycardia compared with those without, and the authors concluded that sympathetic denervation contributed to the autonomic imbalance resulting in bradycardia. The extent to which this represents physiological or pathological change and whether there are prognostic implications has not been subsequently studied.

PET has been used to assess myocardial perfusion in athletes. PET scanning has the advantage over SPECT of being able to quantify perfusion rather than simply qualifying regional variability. Because the radiopharmaceuticals used for PET have very short half-lives requiring image acquisition at the time of contrast administration, most studies have used pharmacologically mediated hyperemic states. Kalliokoski et al. (52) demonstrated that despite significantly increased muscle mass, athletes had similar myocardial perfusion to untrained subjects at rest and after adenosine infusion. A subsequent study that used supine bicycle exercise within the PET scanner demonstrated that increased myocardial mass did not impede adequate blood supply in athletes.


   Separating Athlete's Heart From Cardiac Pathology
Top
 Abstract
 Imaging Modalities
 Defining the Athletic Heart...
 Separating Athlete's Heart From...
Conclusions
 REFERENCES
 
Clinical scenario 1: The power athlete with LV hypertrophy: is it hypertrophic cardiomyopathy?.   Evaluations of differences between athlete's heart and cardiac pathology have focused on conditions in which the cardiac morphology is similar. Hypertrophic cardiomyopathy (HCM) and hypertensive heart disease have served as frequent comparators. As the leading cause of sudden cardiac death in younger populations, the discrimination of HCM from athlete's heart has immediate clinical relevance. Maron et al. (53) has tabled criteria to help in differentiation while recognizing that there remains a "grey zone" in which a definitive diagnosis remains elusive. Cardiac imaging is critical in refining diagnostic certainty, particularly in power and team sports, in which a number of high-profile cases of sudden cardiac death have emphasized its importance. In endurance sport, HCM is an extremely rare occurrence (54), probably reflecting that the inherent impairment in diastolic filling in HCM seems at odds with the supranormal cardiac outputs required of endurance sport. An example of hypertrophic cardiomyopathy in an endurance athlete is shown in Figure 4.


Figure 4
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  		Figure 4 A Young Athlete With Hypertrophic Cardiomyopathy

Example of the importance of CMR in diagnosing HCM in a young athlete who presented with aborted sudden cardiac death and in whom echocardiography was not diagnostic. Left ventricular wall thickness of 12 mm was within ranges accepted for his athletic training (A and B). Mitral inflow and early diastolic annular motion were normal (C and D). The concentric nature of the hypertrophy was atypical for an athlete (E = diastole, F = systole) resulting in intracavity obstruction (blue arrow). T1-weighted images after the administration of gadolinium contrast (G and H) demonstrate apical scarring (red arrows).

 
All available imaging modalities have been used to find a clear measure to differentiate physiological from pathological hypertrophy. Initial studies focused on geometric differences; however, more recent studies have focused on established and novel functional, metabolic and tissue characteristics.

Morphological Differences
In Caucasian athletes, LV wall thickness rarely exceeds 12 mm in males (4) and 11 mm in females (9,55,56), whereas in black athletes a significant minority may have marked LVH (≥15 mm) without other evidence of cardiac pathology (57). These measurements provide cutoff values beyond which athletes should certainly be evaluated for the possibility of a cause of LVH beyond athletic conditioning alone. Peterson et al. (58) used CMR-derived LV volumes to demonstrate improved diagnostic accuracy when wall thickness is related to measures of LV size. This index demonstrated excellent predictive accuracy for HCM, although the use of endurance athletes (with expected LV dilation) as comparator seems less clinically relevant. Caselli et al. (12) derived a novel index termed the mass dispersion index, which measures the differing myocardial masses of the LV myocardial segments. This concept relies upon the hypothesis that HCM is more likely to have significant regional variation in wall thickness and mass. They reported an excellent positive predictive value for the discrimination of HCM whereas athletes, hypertensive patients, and control patients were not separated.

Reversibility of physiologic hypertrophy with detraining has been used as a method to discriminate this from pathological hypertrophy (59). Maron et al. (60) first addressed this approach in 6 Olympic athletes with significant cardiac hypertrophy. After a mean of 3 months of detraining, there was a 24% reduction in ventricular mass resulting in all athletes being close to normal reference values. The same authors subsequently described complete regression of increased LV wall thickness but substantial residual chamber dilation in 8 of 40 elite athletes after a period of detraining (61). The significance of persisting LV dilation remains uncertain.

Functional Differences
When attempting to differentiate athletes from subjects with pathological LVH, functional measures appear promising. A summary of findings from 6 studies is provided in Table 2 (47,62–66). Four of these studies demonstrated attenuation of both systolic (Sm) and early diastolic (Em) myocardial velocities in those subjects with pathological LVH. Different measures were offered as the most accurate means of excluding pathology. Vinereanu et al. (63) determined Sm to be the most specific measure, D'Andrea et al. (64) suggested RV Em, and Saghir et al. (65) proposed longitudinal strain. The relatively small numbers of subjects and differences in study populations preclude assuming superiority of one measure but do suggest that functional measures may increase diagnostic accuracy. The findings also support the physiological hypothesis that myocardial function (particularly diastolic) is superior in athletes.


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  		Table 2 Comparison in Functional Measures Between Athletes and Pathological Hypertrophy
 
Why Richand et al. (47) did not also observe these differences in myocardial velocities in a study comparing soccer players with HCM patients is not clear. The only significant difference between groups was in radial strain, whereas longitudinal strain and TDI annular velocity measures did not differentiate the groups. As a recent and novel mode of investigation, D'Andrea et al. (66) used echocardiographic TDI-derived strain of the LA wall to determine that LA strain was reduced in hypertensive subjects relative to athletes and control patients.

Clinical scenario 2: The endurance athlete with cardiac enlargement and low ejection fraction: is it a dilated cardiomyopathy?.   In the most extreme athletic training, cardiac remodeling can be profound. Abergel et al. (67) performed echocardiography on 286 Tour de France cyclists. More than half of the athletes had LV diastolic dimensions exceeding 60 mm and 11.7% had a left ventricular ejection fraction (LVEF) <52%. In 37 athletes, the echocardiogram was repeated after 3 years. Cardiac dimensions increased and LVEF decreased slightly, but significantly. The reduced LVEF was interpreted as reduced systolic function. An alternative explanation may, in part, be the mathematical "underestimation" that comes when expressing stroke volume as a ratio of an extremely large end-diastolic volume. In fact the cyclists had greater stroke volumes than control patients and a normal resting cardiac output.

Nonetheless, this highlights a clinical conundrum; how do you diagnose pathology in the setting of cardiac function that is below the normal range by conventional measures? In our experience, this is not an uncommon problem. The typical referral follows an echocardiographic assessment performed for screening in a well athlete in whom concern is raised after the finding of a grossly enlarged heart and a low LVEF. The situation is even more complex when the study is performed in the context of malaise, a decrement in athletic performance or palpitations. A simple functional assessment may not suffice. One case report of an Olympic cyclist competing at the highest level despite myocarditis and sustained ventricular tachycardia (68) highlight the risks of assuming that if they can "do more than their doctor they cannot be too sick." As opposed to the study of HCM, there is little evidence on which to base practice.

If resting measures do not differentiate the athlete from the patients, one might assume that a cardiomyopathy would result in systolic dysfunction, which is more demonstrable during exercise. The athlete's heart should demonstrate excellent augmentation of systolic function. Abernethy et al. (69) demonstrated good augmentation of systolic function in professional footballers with low-normal LVEF. In contrast, some studies in heart failure populations have observed no exercise-induced increment in LVEF using echocardiography (70) and first-pass radionuclide ventriculography (71), whereas others reported some degree of augmentation (72). There are, however, no studies comparing response to exercise in athletes and in those with dilated cardiomyopathies. As it might be optimistic to assume a dichotomous response, a measure of normal augmentation needs to be established.

Clinical scenario 3: The endurance athlete with palpitations and cardiac enlargement: is it arrhythmogenic right ventricular cardiomyopathy?.   The diagnosis of arrhythmogenic right ventricular cardiomyopathy (ARVC) can be extremely challenging. Criteria for its diagnosis were established in 1994 (73) based upon clinical, structural, electrical, and functional characteristics. Demonstration of global or regional RV dysfunction satisfies minor or major criteria for ARVC depending upon severity. Difficulties in quantification are even more apparent in athletes. RV end-diastolic volumes are 20% to 30% greater than control patients (5,34), which may be interpreted as abnormal, particularly if the concomitant LV enlargement is not considered.

Chronic RV abnormalities and acute dysfunction after endurance sporting events have both been described. Heidbüchel et al. (35) proposed the term "exercise-induced right ventricular cardiomyopathy" in reference to the disproportionate rates of RV dysfunction in elite athletes presenting with serious arrhythmias. They characterized RV function by using echocardiography, CMR, and/or ventriculography, with many subjects being investigated using all modalities. They subsequently reported a slight, but significant reduction in RV function in those athletes with arrhythmias compared with both control patients and athletes without ventricular arrhythmias (34). It may be that the division between ARVC and the effects of exercise is not absolute and exercise may accelerate the development of ARVC in those who are genetically predisposed (36). The athlete presented in Figure 5 demonstrates the need for multiple diagnostic modalities to identify the presence of ARVC in triathletes.


Figure 5
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  		Figure 5 An Athlete With Ventricular Tachycardia and an Abnormal Right Ventricle

Cardiovascular magnetic resonance study of an elite triathlete after sustained ventricular tachycardia. Cine images in diastole (A) and systole (B) demonstrate an enlarged right ventricle (RV) with reduced systolic function. Note also the septal shift in diastole suggesting significant volume loading. T1-weighted (late gadolinium enhancement) images (C and D) demonstrate increased signal (arrows) of uncertain significance given the spatial resolution constraints within the thin walled RV. A RV focus was identified on electrophysiology studies, which correlated with fibrosis on biopsy.

 
In contrast, some authors have suggested that athletes' RV function is in fact superior to nonathletes. D'Andrea et al. (64) reported supra-normal RV free wall myocardial systolic velocities and Kasikcioglu et al. (10) reported enhanced RV myocardial performance index values in athletes when compared with control patients. It may be concluded, therefore, that although athletes may have impaired RV function immediately after intense endurance exercise and in the context of ventricular arrhythmias, healthy athletes, at rest, should have RV functional measures that are at least as good as the nonathletic population. This is, however, a topical and controversial area that has potentially been underappreciated until recent advances in RV imaging.

Can extreme exercise result in myocardial injury?.   Athlete's heart is a physiological response to intermittent exercise loading, but it is not clear whether this process is entirely benign. The assertion that the athlete's heart syndrome may be pathological arises from the fact that every other model of cardiac enlargement portends an adverse prognosis. Inherited and acquired heart diseases resulting in hypertrophy or dilation are associated with adverse outcomes and, in most cases, are proportional to the extent of cardiac remodeling (37). Is an athlete's heart any different? This question was first addressed in 1873 when John Morgan profiled the excellent health profile of 251 men who had rowed for Oxford Boating Club in the decades preceding (38). Subsequent studies have been limited by small sample sizes and have largely failed to address the impact of sustained high-level athletic activity over decades. Some have provided reassurance (39,40), whereas others have raised speculation of permanent structural remodeling and an increased prevalence of arrhythmias (14,18,35).

Endurance sporting events are increasing in popularity, with U.S. marathons having a 2% to 5% per annum growth in participation during the last decade (74). Although the benefits of moderate exercise are substantial, the extrapolation of these benefits to larger "doses" of exercise is unproven. Questions have been raised by studies reporting increases in biomarkers of myocardial injury after intense, prolonged exercise (75–77). The significance of transient increases in cardiac troponins and B-type natriuretic peptide remains uncertain. Rifai et al. (76) reported troponin elevations associated with reduced LVEF and segmental wall motion abnormalities (in a nonvascular distribution) on echocardiography in subjects immediately after an ultraendurance triathlon. Further studies have subsequently shown similar biochemical and functional abnormalities after endurance events lasting between 3 and 17 h (75,77), whereas other studies have detected only minimal or no evidence of myocardial dysfunction (78,79) despite similar methodology. The duration of myocardial dysfunction is also uncertain.

The cause of these abnormalities remains unclear. The possibility of metabolic abnormalities as a cause of "cardiac fatigue" was addressed using PET imaging. Kalliokoski et al. (80) studied 7 athletes before and after a marathon. Relative to the basal state, athletes had increased myocardial perfusion and an improved response to adenosine with lower coronary flow resistance. This would suggest that ischemia, even microvascular, is not the explanation for the observed abnormalities.

Of particular interest is the differential effect of prolonged exercise on the right and left ventricles. In those studies in which post-race abnormalities were detected, there seems to be an exaggerated effect on RV function (75,77,81). If this observation is indeed real, it raises speculation as to whether the thinner-walled RV has less reserve to deal with the rigors of exercise and/or whether it reflects the disproportionate increases in RV after-load. The significance of these post-exercise RV abnormalities and their relationship to the syndrome of permanent RV injury and arrhythmias described by Heidbüchel et al. (35) needs to be defined.

Tissue characterization may hold the key to evaluation of the athlete's heart as the ability to reliably identify ultrastructural changes in the myocardium such as inflammation and fibrosis will have significant implications. Discussion regarding the significance of transient elevations in biomarkers, myocardial dysfunction, and remodeling will remain speculative until it can clearly be demonstrated that myocardial fibrosis is not an end product. The possibility of "exercise-induced" inflammation has been raised in animal models (82). Unexplained myocardial fibrosis has been noted after sudden death of thoroughbred horses (83,84) and, although it must be again emphasized that it is an extremely rare event, reports of myocardial fibrosis remain unexplained in some cases of sudden death in young athletes (85–87).

Chafizadeh et al. (88) studied tissue characteristics in 16 athletes before and after an ultraendurance triathlon and noted that integrated backscatter was significantly increased after the race. However, enthusiasm for this technique has been largely superseded by other imaging modalities. In particular, CMR has demonstrated improved sensitivity at detecting myocardial edema (by the use of T2-weighted images), inflammation, and scar (by the use of late gadolinium enhancement). Delayed clearance of gadolinium can be quantified on T1-weighted studies and has been used to diagnose myocarditis (89) and subclinical infarcts (90).

Moreover, the extent of late gadolinium enhancement correlated with arrhythmias and clinical outcomes in hypertrophic, dilated, and RV cardiomyopathies (91–93). In athletes, Möhlenkamp et al. (50) investigated 108 older athletes with noninvasive coronary risk stratification and CMR. Late gadolinium enhancement was observed in 12% of the athletes. Although the authors concluded that this was likely explained by their greater-than-expected atherosclerotic disease burden, the late gadolinium enhancement was in a subendocardial distribution (more classically ascribed to coronary events) in only a minority. Interestingly, the presence of late gadolinium enhancement correlated with the number of marathons previously completed, thereby raising the possibility that intense sport participation may lead to myocardial scarring, whether or not myocardial ischemia is a contributing factor.


   Conclusions
Top
 Abstract
 Imaging Modalities
 Defining the Athletic Heart...
 Separating Athlete's Heart From...
 Conclusions
REFERENCES
 
Multimodality cardiac imaging has been used in all of its forms to study the intrigues of the athlete's heart syndrome. A description of the changes in cardiac morphology and function has permitted this syndrome to be differentiated from serious cardiac pathology, which may mimic it in many cases. There are, however, significant challenges left. The biggest of these is also the oldest question: does intense exercise pose an excess risk to athletes? The fact that sudden death in athletes is a rare occurrence does not obviate the need to understand its etiology. Cardiac imaging has failed to conclusively answer this question, although recent advances may hold the key. The ability to accurately assess cardiac function during exercise and the ability to characterize cardiac tissue structure remain the greatest challenges. They also offer the greatest potential in finally resolving these century old questions.


   Footnotes
 
Dr. La Gerche is supported by a National Heart Foundation/National Health and Medical Research Council Post Graduate Research Scholarship.

* Reprint requests and correspondence: Dr. David L. Prior, Cardiac Investigation Unit, St. Vincent's Hospital, P.O. Box 2900, Fitzroy, VIC 3065, Australia (Email: david.prior{at}svhm.org.au).

Manuscript received November 10, 2008; accepted December 16, 2008.


   REFERENCES
Top
 Abstract
 Imaging Modalities
 Defining the Athletic Heart...
 Separating Athlete's Heart From...
 Conclusions
 REFERENCES
 

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