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Right Atrial and Ventricular Adaptations to Training in Male Caucasian Athletes: An Echocardiographic Study
CARDIAC EFFECTS OF ATHLETIC TRAINING
Right Atrial and Ventricular Adaptations to Training in Male Caucasian Athletes: An Echocardiographic Study Efstathios D. Pagourelias, PhD, Evangelia Kouidi, PhD, Georgios K. Efthimiadis, PhD, Asterios Deligiannis, PhD, Paraschos Geleris, PhD, and Vassilios Vassilikos, PhD, Thessaloniki, Greece
Background: The aim of this study was to investigate the systolic and diastolic properties of the right cardiac chambers (the right ventricle and right atrium) among different subsets of athletes to unveil potential variations in right ventricular and right atrial remodeling secondary to different training modes. Methods: A cohort of Caucasian male top-level athletes (n = 108; 80 endurance athletes [EAs], mean age, 31.2 6 10.4 years; 28 strength-trained athletes [SAs], mean age, 27.4 6 5.7 years) and untrained controls (n = 26; mean age, 26.6 6 5.6 years) (P = .327) were prospectively enrolled. Conventional echocardiographic parameters, including transtricuspid inflow, Doppler tissue imaging, and two-dimensionally derived peak systolic longitudinal strain and strain rate indices of the right ventricle and right atrium, were calculated. Results: EAs had greater internal right ventricular and right atrial dimensions compared with SAs and controls. There were no significant differences concerning strain between groups (23.1 6 3.7% in EAs vs 25.1 6 3.2% in SAs vs 23.1 6 3.5% in controls, P = .052), with SAs presenting higher global systolic strain rates (1.42 6 0.22 sec1 in SAs vs 1.21 6 0.21 sec1 in EAs vs 1.2 6 0.28 sec1 in controls, P = .016), as well as greater right atrial strain rate systolic and diastolic components. Training volume (highly vs moderately trained athletes) did not significantly influence deformation parameters. No significant differences concerning diastolic transtricuspid inflow and Doppler tissue imaging indices were also noted among different athlete groups and controls. Conclusions: Despite the existence of right geometric alterations in athletes participating in different sport disciplines, few meaningful differences in deformation and diastolic function exist. (J Am Soc Echocardiogr 2013;26:1344-52.) Keywords: Athlete’s heart, Doppler tissue imaging, Speckle-tracking echocardiography, Right cardiac cavities
Systematic training imposes a wide range of cardiovascular adaptations, both structural and functional, affecting both ventricles and atria.1,2 These physiologic changes occur to provide amplified cardiac output to satisfy increased metabolic demands during high-intensity workload.3,4 Although athletic training results in remodeling of all cardiac cavities, morphologic and functional adaptations of the right ventricle and right atrium have been given considerably less attention compared with those of the left ventricle From the Third Cardiology Department, Hippokration Hospital, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece (E.D.P., P.G., V.V.); the Sports Medicine Laboratory, Department of Physical Education and Sport Science, Aristotle University of Thessaloniki, Thessaloniki, Greece (E.K., A.D.); and the First Cardiology Department, Cardiomyopathies Center, AHEPA University Hospital, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece (G.K.E.). Dr. Pagourelias has received a postdoctoral research scholarship from the Research Committee of the Aristotle University of Thessaloniki, Greece. Reprint requests: Efstathios D. Pagourelias, PhD, Third Cardiology Department, Hippokration Hospital, Medical School, Aristotle University of Thessaloniki, 49 Konstantinoupoleos Str, 54642 Thessaloniki, Greece (E-mail: [email protected]). 0894-7317/$36.00 Copyright 2013 by the American Society of Echocardiography. http://dx.doi.org/10.1016/j.echo.2013.07.019
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and atrium, with a few recent studies focusing on geometric remodeling and systolic function of the right ventricle, based mainly on endurance athletes (EAs).5-12 Post-training right ventricular (RV) conditioning is a complicated phenomenon potentially influenced by many different parameters. Sport discipline has been proved to play a major role in the configuration of athlete’s heart.2 Volume overload imposed on the heart chambers by endurance training leads to cavity dilatation and to an ‘‘eccentric’’ left ventricular (LV) hypertrophy pattern, whereas strength sports subsequently cause less eccentric hypertrophy.13-15 Taking into consideration the interdependence and close anatomic relationship between the two ventricles,1 along with the fact that a disproportionate load is placed on the right ventricle compared with the left ventricle during exercise,16 we would expect that apart from a different LV morphology, strength-trained athletes (SAs) potentially develop different RVand right atrial (RA) structural and functional adaptations compared with those observed in EAs, excessively studied till now. Additionally, the impact of training volume on RV morphology, deformation, and diastolic function and the existence of RA structure and functional variations among different subsets of athletes are other key features not clarified by existing studies. Apart from its significance in understanding the physiology of exercise, the approach to RV and RA morphologic and functional
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adaptations to systematic training is important in preparticipation ARVC = Arrhythmogenic right screening of athletes. Previous ventricular cardiomyopathy studies assessing RV function in EAs have found echocardioBSA = Body surface area graphic measures of myocardial DTI = Doppler tissue imaging function lower than those seen in nonathletes, concluding that EA = Endurance athlete reduced RV function might FAC = Fractional area change reflect myocardial pathology.5,12 Given the overlap between LV = Left ventricular the athlete’s heart phenotype PALS = Peak atrial and that of arrhythmogenic longitudinal strain RV cardiomyopathy (ARVC), RA = Right atrial especially among athletes presenting cardiac enlargement RV = Right ventricular and frequent ventricular SA = Strength-trained athlete ectopy,17 it is essential to clarify deformation and diastolic funcSR = Strain rate tion indices among healthy SRS’ = Systolic strain rate athletes of different subsets, attempting to find RV functional 2D = Two-dimensional echocardiographic measures that may provide greater distinction between pathology and physiologic adaptation to exercise. Furthermore, assessment of RA deformation dynamics might be a useful tool in the study of right heart adaptations to exercise, as it may offer new indices for the discrimination of athlete’s heart from cardiomyopathic processes. Taking into consideration these assumptions, we hypothesized that morphologic adaptations of right heart cavities in athletes are not accompanied by RV systolic and diastolic functional impairment. For this reason, we sought to test RV systolic and diastolic function indices among different subsets of athletes on the basis of sport discipline (EAs vs SAs), training volume (highly vs moderately trained athletes), and RV morphology (dilatation or not) and to compare the derived values with those of healthy untrained controls. Additionally, we aimed to provide a range of data for global RA strain (ε) and strain rate (SR) indices in the aforementioned groups of athletes. Abbreviations
METHODS Study Population This was a prospective study designed and performed in Thessaloniki, in northern Greece, during the peak competitive seasons of 2011 and 2012. After contacting the National Federations of Sports as well as sports physicians and coaches of the top-level sports teams in northern Greece, asking to recruit athletes competing in national-level and international-level training in our region, 108 Caucasian male top-level athletes in different sport disciplines volunteered to participate in our study. All athletes had >3 years of training experience and exercised at least four times per week with $8 hours of weekly training workload. Our cohort consisted of 80 athletes involved in sports combining high dynamic and high static components, including endurance cycling, running, and triathlon, and 28 athletes performing tae kwon do, judo, and weightlifting, sports with high static and low dynamic demands.18 Athletes with $20 hours of training per week (the 75th percentile) were considered to be highly trained athletes (25% of EAs and 28.6% of SAs, P = .75), with moderately trained athletes having >8 and <20 hours of weekly training time. We adopted this cutoff because athletes in the upper quartile of training
volume shared characteristics of highly trained athletes, as these have been described in previous reports.5,12 All enrolled subjects were free from known cardiovascular disease, had negative family histories of cardiomyopathies or premature sudden death, and were not systematically taking any form of prescribed medications or illicit drugs. None of the involved athletes presented with abnormal electrocardiographic features according to a previous European Society of Cardiology report.19 Even though some enrollees fulfilled dimensional criteria for ARVC,20 none had subjective evidence of the disease, such as saccular outpouching, wall motion abnormalities, or prominent moderator bands. Additionally, 26 healthy nonathletic control subjects (training for <3 hours/week, with no previous training experience), served as a reference group, with the same exclusion criteria as used for athletes. All participants provided written informed consent at the time of enrollment, and the study was granted ethical approval by the research committee of the Aristotle University of Thessaloniki, Greece. Echocardiographic Assessment After complete personal and family medical histories, a careful physical examination, and 12-lead electrocardiography, the echocardiographic examination was performed, using a Vivid S5 scanner (GE Vingmed Ultrasound AS, Horten, Norway) with a broadband M3 S transducer. All echocardiographic examinations of participants were performed by the same experienced sonographer using the same standard protocol. EchoPAC dedicated software (GE Vingmed Ultrasound AS) permitted offline analysis of the studies. Standard LV two-dimensional (2D) parameters were obtained from parasternal and modified apical acoustic windows, after all settings were optimized to achieve optimal endocardial delineation in accordance with American Society of Echocardiography guidelines,21,22 while for the right ventricle, the dimensions shown in Figure 1 were calculated.23 RA end-systolic area was obtained from an apical four-chamber orientation focusing on the right cavities.23 Body surface area (BSA) was estimated according to the formula of DuBois and DuBois.24 Following a previously described methodology5 and taking into account that the proposed cutoffs suggested by the American Society of Echocardiography are not corrected for gender, ethnicity, athletic involvement, and/or BSA,23 RV dilatation was defined as a BSA-corrected RV inflow diameter >1 standard deviation of the mean of the control population of the present study (>2.22 cm/m2). RV diastolic function was assessed both by evaluation of transtricuspid inflow parameters and by means of pulsed-wave Doppler tissue imaging (DTI), using a 5-mm sample volume placed in the RV lateral wall of the tricuspid annulus at end-expiration (Figure 1). Three cardiac cycles were averaged for each parameter.23 Pulmonary artery systolic pressure was estimated according to RV assessment guidelines.23 2D Myocardial Speckle-Tracking For the acquisition of RV functional data, necessary for consequent 2D myocardial speckle-tracking analysis, the apical four-chamber orientation was used, and frame rates were as high as possible (not >90 frames/sec), with the focal point positioned at the midlevel of the RV cavity to minimize the impact of beam divergence.25 All images were optimized with gain, compression, and dynamic range to enhance myocardial definition with standardized depth, frequency, and insonation angle for all participants.11 For offline analysis, a region
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Figure 1 Assessment of basic right ventricular dimensions from parasternal short-axis and apical four-chamber views, along with evaluation of transtricuspid inflow parameters and tricuspid annular DTI velocities according to the American Society of Echocardiography guidelines.20 Using a parasternal short-axis orientation at the level of the aortic valve (top left), right ventricular outflow tract end-diastolic diameter (RVOT-Prox) was measured, while by visualizing a modified apical four-chamber orientation focusing on the right ventricle, basal right ventricular inflow diameter at the tips of the tricuspid valve (TV) leaflets (RVD1) and right ventricular midventricular short axis (RVD2) and long axis from right ventricular apex to the level of the tricuspid annulus (RVD3) were calculated (bottom left). Right ventricular end-diastolic area (RVEDA) and right ventricular end-systolic area (RVESA) were measured, allowing calculation of right ventricular FAC as (RVEDA RVESA)/RVEDA. Illustrated are also the E and A waves and the deceleration time (DT) of transtricuspid inflow (top right) and S0 , E0 , and A0 lateral tricuspid annular Doppler velocities (bottom right). Ao V, Aortic valve; LA, left atrium; LV, left ventricle; PV, pulmonary valve; RA, right atrium; RV, right ventricle. of interest was manually traced along the endocardial border from base to apex at the end of systole, and width was set to match the wall thickness. If the automated 2D analysis appraisal of acceptable tracking quality indicated inappropriate tracking, retracing was performed until all six RV myocardial segments (three septal and three RV free wall) were considered to be acceptable.25 The following parameters were measured: global longitudinal peak systolic ε as the average of all six RV myocardial segments, RV free wall longitudinal ε as the average of the three RV free wall segments, and basal RV free wall ε. Also, systolic SR (SRS’) along with early and late diastolic SRs were calculated as the average of the base, mid, and apical segments of the right ventricle (Figure 2). Additionally, using a similar methodology tracing the endocardial border of the right atrium, the following parameters were estimated: peak atrial longitudinal ε (PALS) and peak atrial contraction ε were measured using a six-segment model for the right atrium. SR and its components (RA peak SRS’, RA early diastolic SR, and RA late diastolic SR) were also measured starting from QRS onset.26 To minimize measurement bias, we randomly selected 70 of the total of 134 echocardiographic studies to reassess 2 days after initial analysis of each study. Intraobserver variation was estimated, because a single operator performed both data acquisition and measurement. During repeated measurements, the researcher was blinded to previous results. Intraobserver variability was expressed using the coefficient of variation.
Statistical Analysis Analyses were performed using SPSS Statistics version 19.0 (SPSS, Inc., Chicago, IL). Sample size was calculated using an a level of 0.05, power of 0.80, and (taking into consideration our regional athletic population sport disciplines’ distribution) a ratio of SAs to EAs of 1:3 to detect an absolute difference of 2 6 3% in mean global RV ε between groups on the basis of literature data.5 Two groups enrolling $75 EAs and $25 SAs each were deemed adequate to meet the aforementioned criteria. Data are expressed as mean 6 SD for continuous variables and as counts and/or percentages for categorical variables. Comparison of variables was performed with one-way analysis of variance with post hoc Bonferroni analysis for groups of more than two. Chi-square or Fisher’s exact tests (for expected cell values < 5) were used to compare nominally scaled variables. Correlations between variables were assessed using Pearson’s r coefficient. In an attempt to minimize statistical bias due to unequal sample sizes or to violations of assumptions of the parametric tests used, bootstrapping analysis was performed, randomly resampling the study population 1,000 times. Comparisons’ P values reported are those adjusted from bootstrapping analysis.27 Concerning intraobserver variability, the mean value of the two observations (x) performed for all the parameters for more than half
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Figure 2 Strain and SR curves of the right ventricle in a participating athlete. AVC, Aortic valve closure; 4CH, four-chamber; FR, frame rate; GS, global peak systolic ε; HR, heart rate; SRA0 , Late diastolic SR; SRE0 , early diastolic rate.
of the echocardiographic studies and the absolute value of difference between observations (e) 6 SD were determined. Reproducibility was assessed by the coefficient of variation: (e/x)100%.
Table 1 Age, anthropometric data, clinical characteristics, and performance measures of the study population Variable
RESULTS Basic Demographic and Standard LV Morphologic Parameters Age, anthropometric data, clinical characteristics, and performance measures of the study population are shown in Table 1. No significant differences concerning age and body habitus parameters between athletes and controls were recorded. As expected, athletes presented, because of exercise-induced remodeling, greater internal dimensions (LVend-diastolic diameter and volume) and LV mass index compared with controls (LV end-diastolic diameter, 5.3 6 0.35 cm in EAs vs 5 6 0.38 cm in SAs vs 4.6 6 0.5 cm in controls [P = .005]; LV end-diastolic volume, 133.2 6 21.2 mL in EAs vs 110 6 17 mL in SAs vs 106.8 6 16 mL in controls [P = .001]; LV mass index, 108.9 6 27.5 g/m2 in EAs vs 91.8 6 18.3 g/m2 in SAs vs 82.7 6 21 g/m2 in controls [P < .0005]). LV diastolic function remained well within ‘‘normal’’ limits, showing no significant differences with values obtained from nonathletes.
Age (y) BSA (m2) BMI (kg/m2) HR (beats/min) SBP (mm Hg) DBP (mm Hg) Training experience (y) Training volume (hours/week)
EAs (n = 80)
SAs (n = 28)
Controls (n = 26)
P (ANOVA)
31.2 6 10.4 1.98 6 0.15 21.9 6 2.5 50 6 7 120 6 7 70.3 6 8.5 11.3 6 8.3
27.4 6 5.7 1.95 6 0.21 21.2 6 2.8 56 6 6 125.4 6 8 78 6 3 10.3 6 5.6
26.6 6 5.6 2.01 6 0.16 22.4 6 2.4 65 6 9 120.6 6 8 75 6 9 NA
.327 .333 .353 <.001 .29 .25 .488
14.6 6 5.4
17.1 6 7.2 NA
.115
ANOVA, Analysis of variance; BMI, body mass index; DBP, diastolic blood pressure; HR, heart rate; NA, not applicable; SBP, systolic blood pressure. Data are expressed as mean 6 SD.
RV and RA Morphology and Function in EAs and SAs Echocardiographic parameters concerning right cavity dimensions and functional data including transtricuspid inflow and DTI indices
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Table 2 Morphologic and functional RV and RA parameters of EAs, SAs, and controls
Variable
Morphologic parameters RVOTd (cm) RVITd (cm) RVDm (cm) RVL (cm) RV EDA (cm2) RV ESA (cm2) RV FAC (%) RA area (cm2) Functional parameters Tricuspid E (cm/sec) Tricuspid A (cm/sec) E/A ratio DT (msec) RV FW S0 (cm/sec) RV FW E0 (cm/sec) RV FW A0 (cm/sec) E/E0 ratio PASP (mm Hg)
EAs (n = 80)
SAs (n = 28)
Bootstrapping analysis
Controls (n = 26)
Controls vs EAs
Controls vs SAs
EAs vs SAs
P (ANOVA)
3.7 6 0.5 4.1 6 0.4 3.1 6 0.5 8.9 6 0.6 26.6 6 4 13.2 6 2.7 50.4 6 7 17.5 6 2.7
3.4 6 0.77 3.7 6 0.4 3.0 6 0.5 8.5 6 0.6 22 6 3.5 10.5 6 1.5 51.2 6 9.8 15 6 3.6
3.2 6 0.66 3.8 6 0.6 2.6 6 0.5 8.8 6 0.7 19.2 6 3.9 10.9 6 2.4 42.7 6 7.2 14 6 4.1
0.001 0.024 <0.0005 1.00 <0.0005 0.074 0.029 <0.0005
0.927 0.523 0.017 0.517 0.037 1.00 0.006 0.844
0.087 <0.0005 0.887 0.113 0.001 0.006 0.257 0.005
.001 <.0005 <.0005 .114 <.0005 .016 .007 <.0005
66.9 6 13.3 42 6 11.2 1.64 6 0.30 141 6 15,8 15.3 6 2.2 17.3 6 2.7 10.7 6 2.8 3.9 6 1 21 6 8.3
66.3 6 13.6 38.9 6 10.7 1.76 6 0.42 155 6 14.4 16.6 6 2.1 18.1 6 1.3 11 6 2.2 3.6 6 0.66 22.4 6 8.6
68.7 6 9.5 35 6 5.7 1.98 6 0.28 145.3 6 13.4 14.8 6 1.7 17.5 6 2.9 10.2 6 2.1 4 6 0.85 18.3 6 8.6
1.00 0.007 <0.0005 0.592 0.731 1.00 1.00 1.00 0.494
1.00 0.488 0.031 0.048 0.006 1.00 0.70 0.497 0.211
1.00 0.448 0.195 <0.0005 0.02 0.364 1.00 0.419 1.00
.753 .008 <.0005 <.0005 .004 .299 .480 .192 .192
ANOVA, Analysis of variance; DT, deceleration time; EDA, end-diastolic area; ESA, end-systolic area; FW, free wall; PASP, pulmonary artery systolic pressure; RVDm, right midventricular diameter; RVITd, RV inflow tract diameter; RVL, RV length; RVOTd, RV outflow tract diameter. Data are expressed as mean 6 SD.
Table 3 Two-dimensional speckle-tracking ε and SR data for the right ventricle and right atrium of EAs, SAs, and controls
Variable
RV 2D ε and SR analysis GLS (%) FW average ε (%) SRS’ (sec1) SRE’ (sec1) SRA’ (sec1) RA 2D ε and SR analysis PALS (%) PACS (%) RASSR (sec1) RAEDSR (sec1) RALDSR (sec1)
Bootstrapping analysis
EAs (n = 80)
SAs (n = 28)
Controls (n = 26)
Controls vs EAs
Controls vs SAs
EAs vs SAs
P (ANOVA)
23.1 6 3.7 26.4 6 5.4 1.21 6 0.21 1.54 6 0.29 0.67 6 0.22
25.1 6 3.2 27.8 6 4.3 1.42 6 0.22 1.44 6 0.28 0.75 6 0.27
23.1 6 3.5 27 6 4.3 1.2 6 0.28 1.49 6 0.44 0.74 6 0.26
1.00 1.00 0.891 0.86 1.00
0.076 0.668 0.005 1.00 1.00
0.087 0.565 <0.0005 1.00 1.00
.052 .467 .016 .455 .872
43.9 6 15 13.4 6 6.4 1.7 6 0.8 1.66 6 0.63 1.4 6 0.6
51.7 6 20 15.6 6 13.4 2.23 6 0.55 1.57 6 0.24 1.81 6 0.6
44.3 6 10 12.8 6 5 2.02 6 0.33 2.16 6 0.53 1.73 6 0.39
1.00 1.00 0.213 0.001 0.073
0.368 0.717 1.00 0.002 1.00
0.115 0.725 0.01 1.00 0.031
.106 .416 .007 .001 .01
ANOVA, Analysis of variance; FW, free wall; GLS, global longitudinal ε; PACS, peak atrial contraction ε; RAEDSR, RA early diastolic SR; RALDSR, RA late diastolic SR; RASSR, RA peak SSR’; SRA0 , late diastolic SR; SRE0 , early diastolic rate. Data are expressed as mean 6 SD.
of EAs, SAs, and controls participating in our study are shown in Table 2. Different training modes induced different morphologic RV patterns, leading to greater RV and RA dilatation among EAs, with 8.1% and 18.6% of them fulfilling major and minor dimensional criteria, respectively, for ARVC, but without other disease signs. There were no significant differences concerning ε between groups (P = .085), with SAs presenting higher global SRS’, as well as greater RA SSR’ and RA late diastolic SR waves of RA SR and marginally nonsignificant higher PALS (Table 3). Also, the comparison of global, RV
free wall, and basal longitudinal ε between EAs and SAs is shown in Figure 3. Differences in Structural and Functional RV and RA Characteristics According to Training Volume Basic demographic parameters, including age (P = .186), BSA (P = .17), and LV mass (P = 1.00), did not significantly differ between highly and moderately trained athletes. Both athlete groups showed
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22.2 6 3.1% for controls, P = .005 and P = 1.00 after post hoc analysis for athlete groups; Figure 3). Additionally, the only significant difference between highly and moderately trained athletes concerned PALS, with highly trained athletes presenting 53.6 6 18.2% compared with 42.6 6 15.5% of moderately trained athletes and 44.6 6 9.3% of controls (P = .01 and post hoc P = .008 between athletes). No differences concerning diastolic function indices were noted between athlete groups and controls. Effect of RV Dilatation on ε and SR Values Twenty-six of 108 athletes in our study fulfilled the RV dilation criterion (24%), showing no significant differences concerning age (P = .072), BSA (P = .155), and total training years (P = .763) with athletes without RV dilatation. Training hours per week were less (13.1 6 2.8 hours/week) for the RV dilatation group compared with the nondilated RV group (15.9 6 7 hours/week), although this was marginally not significant (P = .051). The right atrium was significantly larger for the dilated group (18.7 6 3.4 vs 16.2 6 2.7 cm2, post hoc P = .002). Concerning ε and SR values, no significant differences were recorded, with athletes presenting RV dilatation showing values close to those of normal controls (Figure 3). Correlation Statistics between Deformation Indices and ‘‘Classic’’ RV Contractility Parameters Increased ε and SR values among athletes in our study were significantly correlated with enhanced tricuspid annular S0 wave (DTI S0 ) and greater fractional RV fractional area change (FAC), parameters showing global and regional enhancement of RV contractility. More specifically, in EAs, correlation between ε and DTI S0 and between ε and RV FAC yielded Pearson’s r values of 0.579 (P = .001) and 0.353 (P = .029), respectively, while an r value of 0.652 (P < .0005) was recorded for the correlation of RV SRS’ and DTI S0 . Accordingly, in SAs, significant correlations between the aforementioned parameters were also revealed (e.g., r = 0.596, P < .001, for the correlation between ε and RV FAC). Intraobserver Variability Analysis Concerning RV functional ε indices, coefficients of variation for RV ε, RV SRS’, RV early diastolic SR, RV late diastolic SR, and RA PALS were 10%, 7%, 9%, 9%, and 14%, respectively. Feasibility for 2D ε analysis of the right ventricle reached 100%, because all enrolled athletes and controls had adequate image quality to allow a complete set of RV ε measurements offline. Concerning RA ε analysis, the basal lateral segment was the more complicated to trace for speckletracking analysis, although this was accomplished for >95% of examined segments, excluding the rest from the reported results.
Figure 3 Box-plot graphs demonstrating RV longitudinal ε indices (global peak systolic ε, RV free wall ε, and basal RV ε) in different subsets of athletic populations (according to sport discipline [EAs vs SAs], training volume [highly trained vs moderately trained athletes], and RV dilatation). For classification criteria, see inside text. *Statistically significant difference. FW, Free wall; H., highly; M., moderately. greater ε values compared with controls (24.5 6 3.6% for highly trained and 24.8 6 2.9% for moderately trained athletes vs
DISCUSSION Systematic training imposes a wide range of adaptations, structural and functional, affecting both ventricles and atria.1,2 Concerning the right ventricle, geometric remodeling secondary to systematic training has been described in previous studies, while ambiguous results exist regarding deformation and diastolic function of the right ventricle among athletes, suggesting that observed changes could be attributed either to an acquired right cardiomyopathy secondary to long-term intensive exercise or to physiologic
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conditioning per se.5,10-12 Our study, taking advantage of different groups of athletes (EAs and SAs, highly and moderately trained athletes, with or without RV dilatation), has shown that despite the existence of differences in RV and RA geometric measures, few meaningful differences in deformation exist, as RV and RA systolic and diastolic functions remain within normal ranges. There has been an ongoing controversy concerning longitudinal deformation of the RV free wall and especially its basic lateral segment,5,10-12 raising concern about potential myocardial damage due to endurance exercise, implying that exhausting training might lead to a type of RV cardiomyopathy.28-32 Our study, in concordance with findings by Oxborough et al.11 as well as D’Andrea et al.,10,33 has shown that even among highly trained athletes or athletes with dilated right ventricles performing endurance or strength exercise, global RV ε and SR, including basal deformation, are at least preserved if not increased. Increased ε and SR values among athletes of our study were in positive correlation with enhanced DTI S0 wave and greater RV FAC, parameters showing global and regional enhancement of RV contractility,34,35 which along with RV dilatation contributes to increased preload and stroke volume. On the contrary, in a study by Teske et al.,5 there was a discrepancy between ‘‘classic’’ basal RV deformation indices (such as tricuspid annular plane systolic excursion and DTI RV lateral wall S0 ), which appear to be increased among elite athletes, and novel deformation parameters (such as ε and SR), which were decreased. In addition, even though a transient impairment of RV systolic function has been described after bouts of ultraendurance exercise,28-30,36 our study provides evidence that during rest, RV function among athletes remains normal. A significant percentage, especially of EAs in our study, fulfilled major dimension criteria for ARVC, stressing the need for differential diagnosis between ARVC and athlete’s heart in the context of preparticipation screening. Enhanced contraction of RV free wall segments in athletes demonstrated by our study, compared with regional and/ or global deformation impairment in ARVC,37 may facilitate differential diagnosis between the two entities. Additionally, assessment of RV diastolic function both with older echocardiographic indices (tricuspid inflow E/A ratio, tricuspid annular E0 and A0 waves, and RV E/E0 ratio) and novel parameters (global SR E and A waves) is another key feature permitting differential diagnosis between physiologic adaptations and pathologies of the right ventricle, because RV relaxation in athletes is well within normal limits.38 It is evident that current ARVC criteria show major limitations when applied for preparticipation screening, necessitating the use of novel deformation and diastolic function parameters in discriminating normal adaptations from pathologic variations. Apart from confirming RV and RA dilatation, especially among EAs, to act synergistically with LV dilatation for stroke volume augmentation,1 our study has shown a trend toward better deformation (global longitudinal ε and SRS’) among SAs. Increased RV ε and SR values observed in SAs may reflect a different morphology of the right ventricle, leading to different RV deformation patterns. Additionally, despite RA dilatation in athletes, the contractility of the atrium remains normal, contributing through atrioventricular coupling to preload increase and stroke volume augmentation. Values of RA ε obtained from our cohort of athletes do not differ compared with values introduced by two previous studies from the same center.39,40 On the other hand, pathologic conditions such as cardiomyopathies or other myocardial diseases are also accompanied by left atrial and/or RA enlargement, showing however decreased deformation indices.37 In this context, assessing functional alterations of the right atrium apart from its significance in the study of physiologic adapta-
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tions, it may serve as a useful discriminator of athlete’s heart from morphologically similar but life-threatening conditions such as ARVC. Limitations A potential limitation of our study could be considered the lack of hemodynamic data on the right ventricle, providing more accurate assessment of pulmonary artery systolic pressure and RA pressures. However, it has been demonstrated that there is a significant correlation between values obtained after catheterization and indices based on echocardiographic evaluation of the right ventricle. The disparity of enrolled groups (80 EAs vs 28 SAs vs 26 controls) reflects the arithmetic dominance of EAs in our regional population, along with the refusal of many highly trained SAs to participate in the study. In an attempt to minimize the effect of sample size inequality and statistical bias, bootstrapping analysis was adopted as being more robust than single parametric tests. The quantity and quality of training are crucial to describe the morphologic and functional athlete’s heart adaptations, and in this context maximal oxygen uptake is the gold standard and an objective measure of aerobic fitness. However, high-intensity static exercise is performed with anaerobic metabolism and static exercise training results in a small or no increase in maximal oxygen uptake. Because the exercise stimuli and sports demands of enrolled athletes in our study were different, athletes were classified according to their athletic experience and sport-specific performance. Evaluation of RV and RA ε and SR indices was based on EchoPAC software, a PC program developed by GE for 2D speckle-tracking of the left ventricle. As has been done in previous studies in this field,5,1012 LV-dedicated software was applied for RV and RA ε evaluation, and even though the reproducibility of measurements was good, changes in the software in the future or correlation studies with other imaging modalities (such as magnetic resonance imaging) may be useful to optimize the tracking quality of the right ventricle, improving the measurements performed. Even though up to 80% of RV global deformation is due to longitudinal ε, radial ε of the right ventricle was not estimated in this study. The lack of dedicated software in combination with the morphology of the RV free wall (too thin to develop significant traceable thickness during contraction) was an obstacle to assessing radial ε indices of the right ventricle. Similarly, RA ε and SR values were obtained only from the apical four-chamber view, because this is the only axis permitting the recording of RA longitudinal ε. CONCLUSIONS Systematic training imposes physiologic, morphologic, and functional adaptations on the right ventricle and right atrium. Despite differences in geometric remodeling among different subsets of athletes (EAs vs SAs, highly vs moderately trained athletes, with or without RV dilatation) and untrained controls, few meaningful differences in right cardiac cavity deformation and relaxation exist, suggesting that RV and RA systolic and diastolic function in athletes, irrespective of sport discipline, training volume, and physiologic remodeling, remain within the normal range. ACKNOWLEDGMENTS We thank all the athletes and healthy volunteers participating in the study. Additionally, we thank Vourdounis Nikos and
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Dimitrakopoulos Ioannis, local GE staff members, for their continuous technical support with EchoPAC software, along with the nurses and aid personnel of the Third Cardiology Department’s Acute Coronary Unit for their commitment to completion of the current research protocol. REFERENCES 1. Santamore WP, Dell’Italia LJ. Ventricular interdependence: significant left ventricular contributions to right ventricular systolic function. Prog Cardiovasc Dis 1998;40:289-308. 2. Pelliccia A, Maron MS, Maron BJ. Assessment of left ventricular hypertrophy in a trained athlete: differential diagnosis of physiologic athlete’s heart from pathologic hypertrophy. Prog Cardiovasc Dis 2012;54:387-96. 3. Pluim B, Zwinderman A, van der Laarse A, van der Waal E. The athlete’s heart. A meta-analysis of cardiac structure and function. Circulation 2000; 101:336-44. 4. Maron BJ, Pelliccia A. The heart of trained athletes: cardiac remodeling and the risks of sports, including sudden death. Circulation 2006;114: 1633-44. 5. Teske AJ, Prakken NH, De Boeck BW, Velthuis BK, Martens EP, Doevendans PA, et al. Echocardiographic tissue deformation imaging of right ventricular systolic function in endurance athletes. Eur Heart J 2009;30:969-77. 6. Ho SY, Nihoyannopoulos P. Anatomy, echocardiography, and normal right ventricular dimensions. Heart 2006;92(suppl):i2-13. 7. Prakken NH, Velthuis BK, Teske AJ, Mosterd A, Mali WP, Cramer MJ. Cardiac MRI reference values for athletes and nonathletes corrected for body surface area, training hours/week and sex. Eur J Cardiovasc Prev Rehabil 2010;17:198-203. 8. Scharhag J, Schneider G, Urhausen A, Rochette V, Kramann B, Kindermann W. Athlete’s heart: right and left ventricular mass and function in male endurance athletes and untrained individuals determined by magnetic resonance imaging. J Am Coll Cardiol 2002;40: 1856-63. 9. Scharhag J, Th€ unenk€ otter T, Urhausen A, Schneider G, Kindermann W. Echocardiography of the right ventricle in athlete’s heart and hearts of normal size compared to magnetic resonance imaging: which measurements should be applied in athletes? Int J Sports Med 2010;31:58-64. 10. D’Andrea A, Caso P, Bossone E, Scarafile R, Riegler L, Di Salvo G, et al. Right ventricular myocardial involvement in either physiological or pathological left ventricular hypertrophy: an ultrasound speckle-tracking two-dimensional strain analysis. Eur J Echocardiogr 2010;11:492-500. 11. Oxborough D, Sharma S, Shave R, Whyte G, Birch K, Artis N, et al. The right ventricle of the endurance athlete: the relationship between morphology and deformation. J Am Soc Echocardiogr 2012;25: 263-71. 12. La Gerche A, Burns AT, D’Hooge J, Macisaac AI, Heidb€ uchel H, Prior DL. Exercise strain rate imaging demonstrates normal right ventricular contractile reserve and clarifies ambiguous resting measures in endurance athletes. J Am Soc Echocardiogr 2012;25:253-62. 13. D’Andrea A, Limongelli G, Caso P, Sarubbi B, Della Pietra A, Brancaccio P, et al. Association between left ventricular structure and cardiac performance during effort in two morphological forms of athlete’s heart. Int J Cardiol 2002;86:177-84. 14. Utomi V, Oxborough D, Whyte GP, Somauroo J, Sharma S, Shave R, et al. Systematic review and meta-analysis of training mode, imaging modality and body size influences on the morphology and function of the male athlete’s heart. Heart. In press. 15. Spence AL, Naylor LH, Carter HH, Buck CL, Dembo L, Murray C, et al. A prospective randomised longitudinal MRI study of left ventricular adaptation to endurance and resistance exercise training in humans. J Physiol 2011;589:5443-52. 16. La Gerche A, Heidb€ uchel H, Burns AT, Mooney DJ, Taylor AJ, Pfluger HB, et al. Disproportionate exercise load and remodeling of the athlete’s right ventricle. Med Sci Sports Exerc 2011;43:974-81.
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17. Heidbuchel H, Hoogsteen J, Fagard R, Vanhees L, Ector H, Willems R, et al. High prevalence of right ventricular involvement in endurance athletes with ventricular arrhythmias. Role of an electrophysiologic study in risk stratification. Eur Heart J 2003;24:1473-80. 18. Mitchell JH, Haskell W, Snell P, Van Camp SP. Task Force 8: classification of sports. J Am Coll Cardiol 2005;45:1364-7. 19. Corrado D, Pelliccia A, Heidbuchel H, Sharma S, Link M, Basso C, et al. Section of Sports Cardiology, European Association of Cardiovascular Prevention and Rehabilitation. Recommendations for interpretation of 12lead electrocardiogram in the athlete. Eur Heart J 2010;31:243-59. 20. Marcus FI, McKenna WJ, Sherrill D, Basso C, Bauce B, Bluemke DA, et al. Diagnosis of arrhythmogenic right ventricular cardiomyopathy/dysplasia: proposed modification of the task force criteria. Circulation 2010;121: 1533-41. 21. Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, et al., American Society of Echocardiography’s Nomenclature and Standards Committee. Task Force on Chamber Quantification; American College of Cardiology Echocardiography Committee; American Heart Association; European Association of Echocardiography, European Society of Cardiology. Recommendations for chamber quantification. Eur J Echocardiogr 2006;7:79-108. 22. Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, et al. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol 1986;57:450-8. 23. Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, et al. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 2010;23: 685-713. 24. DuBois D, DuBois EF. A formula to estimate the approximate surface area if height and weight be known. Arch Intern Med 1916;17:863-71. 25. Horton KD, Meece RW, Hill JC. Assessment of the right ventricle by echocardiography: a primer for cardiac sonographers. J Am Soc Echocardiogr 2009;22:776-92. 26. Kutty S, Padiyath A, Li L, Peng Q, Rangamani S, Schuster A, Danford DA. Functional maturation of left and right atrial systolic and diastolic performance in infants, children, and adolescents. J Am Soc Echocardiogr 2013;26:398-409. 27. Davison AC, Hinkley DV. Bootstrap methods and their application. Cambridge, UK: Cambridge University Press; 2006. 28. La Gerche A, Connelly KA, Mooney DJ, MacIsaac AI, Prior DL. Biochemical and functional abnormalities of left and right ventricular function after ultra-endurance exercise. Heart 2008;94:860-6. 29. Neilan TG, Januzzi JL, Lee-Lewandrowski E, Ton-Nu TT, Yoerger DM, Jassal DS, et al. Myocardial injury and ventricular dysfunction related to training levels among nonelite participants in the Boston Marathon. Circulation 2006;114:2325-33. 30. Neilan TG, Ton-Nu TT, Jassal DS, Popovic ZB, Douglas PS, Halpern EF, et al. Myocardial adaptation to short-term high-intensity exercise in highly trained athletes. J Am Soc Echocardiogr 2006;19:1280-5. 31. George K, Shave R, Warburton D, Scharhag J, Whyte G. Exercise and the heart: can you have too much of a good thing? Med Sci Sports Exerc 2008; 40:1390-2. 32. Shave R, Baggish A, George K, Wood M, Scharhag J, Whyte G, et al. Exercise-induced cardiac troponin elevation: evidence, mechanisms, and implications. J Am Coll Cardiol 2010;56:169-76. 33. D’Andrea A, Riegler L, Golia E, Cocchia R, Scarafile R, Salerno G, et al. Range of right heart measurements in top-level athletes: the training impact. Int J Cardiol 2013;164:48-57. 34. D’Andrea A, Caso P, Sarubbi B, Limongelli G, Liccardo B, Cice G, et al. Right ventricular myocardial adaptation to different training protocols in top-level athletes. Echocardiography 2003;20:329-36. 35. Kasikcioglu E, Oflaz H, Akhan H, Kayserilioglu A. Right ventricular myocardial performance index and exercise capacity in athletes. Heart Vessels 2005;20:147-52.
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36. La Gerche A, Burns AT, Mooney DJ, Inder WJ, Taylor AJ, Bogaert J, et al. Exercise-induced right ventricular dysfunction and structural remodelling in endurance athletes. Eur Heart J 2012;33:998-1006. 37. Bauce B, Frigo G, Benini G, Michieli P, Basso C, Folino AF, et al. Differences and similarities between arrhythmogenic right ventricular cardiomyopathy and athlete’s heart adaptations. Br J Sports Med 2010;44:148-54. 38. Pagourelias ED, Efthimiadis GK, Parcharidou DG, Gossios TD, Kamperidis V, Karoulas T, et al. Prognostic value of right ventricular dia-
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stolic function indices in hypertrophic cardiomyopathy. Eur J Echocardiogr 2011;12:809-17. 39. Padeletti M, Cameli M, Lisi M, Malandrino A, Zaca V, Mondillo S. Reference values of right atrial longitudinal strain imaging by two-dimensional speckle tracking. Echocardiography 2012;29:147-52. 40. D’Ascenzi F, Cameli M, Padeletti M, Lisi M, Zaca V, Natali B, et al. Characterization of right atrial function and dimension in top-level athletes: a speckle tracking study. Int J Cardiovasc Imaging 2013;29:87-94.
Right Atrial and Ventricular Adaptations to Training in Male Caucasian Athletes: An Echocardiographic Study Efstathios D. Pagourelias, PhD, Evangelia Kouidi, PhD, Georgios K. Efthimiadis, PhD, Asterios Deligiannis, PhD, Paraschos Geleris, PhD, and Vassilios Vassilikos, PhD, Thessaloniki, Greece
Background: The aim of this study was to investigate the systolic and diastolic properties of the right cardiac chambers (the right ventricle and right atrium) among different subsets of athletes to unveil potential variations in right ventricular and right atrial remodeling secondary to different training modes. Methods: A cohort of Caucasian male top-level athletes (n = 108; 80 endurance athletes [EAs], mean age, 31.2 6 10.4 years; 28 strength-trained athletes [SAs], mean age, 27.4 6 5.7 years) and untrained controls (n = 26; mean age, 26.6 6 5.6 years) (P = .327) were prospectively enrolled. Conventional echocardiographic parameters, including transtricuspid inflow, Doppler tissue imaging, and two-dimensionally derived peak systolic longitudinal strain and strain rate indices of the right ventricle and right atrium, were calculated. Results: EAs had greater internal right ventricular and right atrial dimensions compared with SAs and controls. There were no significant differences concerning strain between groups (23.1 6 3.7% in EAs vs 25.1 6 3.2% in SAs vs 23.1 6 3.5% in controls, P = .052), with SAs presenting higher global systolic strain rates (1.42 6 0.22 sec1 in SAs vs 1.21 6 0.21 sec1 in EAs vs 1.2 6 0.28 sec1 in controls, P = .016), as well as greater right atrial strain rate systolic and diastolic components. Training volume (highly vs moderately trained athletes) did not significantly influence deformation parameters. No significant differences concerning diastolic transtricuspid inflow and Doppler tissue imaging indices were also noted among different athlete groups and controls. Conclusions: Despite the existence of right geometric alterations in athletes participating in different sport disciplines, few meaningful differences in deformation and diastolic function exist. (J Am Soc Echocardiogr 2013;26:1344-52.) Keywords: Athlete’s heart, Doppler tissue imaging, Speckle-tracking echocardiography, Right cardiac cavities
Systematic training imposes a wide range of cardiovascular adaptations, both structural and functional, affecting both ventricles and atria.1,2 These physiologic changes occur to provide amplified cardiac output to satisfy increased metabolic demands during high-intensity workload.3,4 Although athletic training results in remodeling of all cardiac cavities, morphologic and functional adaptations of the right ventricle and right atrium have been given considerably less attention compared with those of the left ventricle From the Third Cardiology Department, Hippokration Hospital, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece (E.D.P., P.G., V.V.); the Sports Medicine Laboratory, Department of Physical Education and Sport Science, Aristotle University of Thessaloniki, Thessaloniki, Greece (E.K., A.D.); and the First Cardiology Department, Cardiomyopathies Center, AHEPA University Hospital, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece (G.K.E.). Dr. Pagourelias has received a postdoctoral research scholarship from the Research Committee of the Aristotle University of Thessaloniki, Greece. Reprint requests: Efstathios D. Pagourelias, PhD, Third Cardiology Department, Hippokration Hospital, Medical School, Aristotle University of Thessaloniki, 49 Konstantinoupoleos Str, 54642 Thessaloniki, Greece (E-mail: [email protected]). 0894-7317/$36.00 Copyright 2013 by the American Society of Echocardiography. http://dx.doi.org/10.1016/j.echo.2013.07.019
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and atrium, with a few recent studies focusing on geometric remodeling and systolic function of the right ventricle, based mainly on endurance athletes (EAs).5-12 Post-training right ventricular (RV) conditioning is a complicated phenomenon potentially influenced by many different parameters. Sport discipline has been proved to play a major role in the configuration of athlete’s heart.2 Volume overload imposed on the heart chambers by endurance training leads to cavity dilatation and to an ‘‘eccentric’’ left ventricular (LV) hypertrophy pattern, whereas strength sports subsequently cause less eccentric hypertrophy.13-15 Taking into consideration the interdependence and close anatomic relationship between the two ventricles,1 along with the fact that a disproportionate load is placed on the right ventricle compared with the left ventricle during exercise,16 we would expect that apart from a different LV morphology, strength-trained athletes (SAs) potentially develop different RVand right atrial (RA) structural and functional adaptations compared with those observed in EAs, excessively studied till now. Additionally, the impact of training volume on RV morphology, deformation, and diastolic function and the existence of RA structure and functional variations among different subsets of athletes are other key features not clarified by existing studies. Apart from its significance in understanding the physiology of exercise, the approach to RV and RA morphologic and functional
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adaptations to systematic training is important in preparticipation ARVC = Arrhythmogenic right screening of athletes. Previous ventricular cardiomyopathy studies assessing RV function in EAs have found echocardioBSA = Body surface area graphic measures of myocardial DTI = Doppler tissue imaging function lower than those seen in nonathletes, concluding that EA = Endurance athlete reduced RV function might FAC = Fractional area change reflect myocardial pathology.5,12 Given the overlap between LV = Left ventricular the athlete’s heart phenotype PALS = Peak atrial and that of arrhythmogenic longitudinal strain RV cardiomyopathy (ARVC), RA = Right atrial especially among athletes presenting cardiac enlargement RV = Right ventricular and frequent ventricular SA = Strength-trained athlete ectopy,17 it is essential to clarify deformation and diastolic funcSR = Strain rate tion indices among healthy SRS’ = Systolic strain rate athletes of different subsets, attempting to find RV functional 2D = Two-dimensional echocardiographic measures that may provide greater distinction between pathology and physiologic adaptation to exercise. Furthermore, assessment of RA deformation dynamics might be a useful tool in the study of right heart adaptations to exercise, as it may offer new indices for the discrimination of athlete’s heart from cardiomyopathic processes. Taking into consideration these assumptions, we hypothesized that morphologic adaptations of right heart cavities in athletes are not accompanied by RV systolic and diastolic functional impairment. For this reason, we sought to test RV systolic and diastolic function indices among different subsets of athletes on the basis of sport discipline (EAs vs SAs), training volume (highly vs moderately trained athletes), and RV morphology (dilatation or not) and to compare the derived values with those of healthy untrained controls. Additionally, we aimed to provide a range of data for global RA strain (ε) and strain rate (SR) indices in the aforementioned groups of athletes. Abbreviations
METHODS Study Population This was a prospective study designed and performed in Thessaloniki, in northern Greece, during the peak competitive seasons of 2011 and 2012. After contacting the National Federations of Sports as well as sports physicians and coaches of the top-level sports teams in northern Greece, asking to recruit athletes competing in national-level and international-level training in our region, 108 Caucasian male top-level athletes in different sport disciplines volunteered to participate in our study. All athletes had >3 years of training experience and exercised at least four times per week with $8 hours of weekly training workload. Our cohort consisted of 80 athletes involved in sports combining high dynamic and high static components, including endurance cycling, running, and triathlon, and 28 athletes performing tae kwon do, judo, and weightlifting, sports with high static and low dynamic demands.18 Athletes with $20 hours of training per week (the 75th percentile) were considered to be highly trained athletes (25% of EAs and 28.6% of SAs, P = .75), with moderately trained athletes having >8 and <20 hours of weekly training time. We adopted this cutoff because athletes in the upper quartile of training
volume shared characteristics of highly trained athletes, as these have been described in previous reports.5,12 All enrolled subjects were free from known cardiovascular disease, had negative family histories of cardiomyopathies or premature sudden death, and were not systematically taking any form of prescribed medications or illicit drugs. None of the involved athletes presented with abnormal electrocardiographic features according to a previous European Society of Cardiology report.19 Even though some enrollees fulfilled dimensional criteria for ARVC,20 none had subjective evidence of the disease, such as saccular outpouching, wall motion abnormalities, or prominent moderator bands. Additionally, 26 healthy nonathletic control subjects (training for <3 hours/week, with no previous training experience), served as a reference group, with the same exclusion criteria as used for athletes. All participants provided written informed consent at the time of enrollment, and the study was granted ethical approval by the research committee of the Aristotle University of Thessaloniki, Greece. Echocardiographic Assessment After complete personal and family medical histories, a careful physical examination, and 12-lead electrocardiography, the echocardiographic examination was performed, using a Vivid S5 scanner (GE Vingmed Ultrasound AS, Horten, Norway) with a broadband M3 S transducer. All echocardiographic examinations of participants were performed by the same experienced sonographer using the same standard protocol. EchoPAC dedicated software (GE Vingmed Ultrasound AS) permitted offline analysis of the studies. Standard LV two-dimensional (2D) parameters were obtained from parasternal and modified apical acoustic windows, after all settings were optimized to achieve optimal endocardial delineation in accordance with American Society of Echocardiography guidelines,21,22 while for the right ventricle, the dimensions shown in Figure 1 were calculated.23 RA end-systolic area was obtained from an apical four-chamber orientation focusing on the right cavities.23 Body surface area (BSA) was estimated according to the formula of DuBois and DuBois.24 Following a previously described methodology5 and taking into account that the proposed cutoffs suggested by the American Society of Echocardiography are not corrected for gender, ethnicity, athletic involvement, and/or BSA,23 RV dilatation was defined as a BSA-corrected RV inflow diameter >1 standard deviation of the mean of the control population of the present study (>2.22 cm/m2). RV diastolic function was assessed both by evaluation of transtricuspid inflow parameters and by means of pulsed-wave Doppler tissue imaging (DTI), using a 5-mm sample volume placed in the RV lateral wall of the tricuspid annulus at end-expiration (Figure 1). Three cardiac cycles were averaged for each parameter.23 Pulmonary artery systolic pressure was estimated according to RV assessment guidelines.23 2D Myocardial Speckle-Tracking For the acquisition of RV functional data, necessary for consequent 2D myocardial speckle-tracking analysis, the apical four-chamber orientation was used, and frame rates were as high as possible (not >90 frames/sec), with the focal point positioned at the midlevel of the RV cavity to minimize the impact of beam divergence.25 All images were optimized with gain, compression, and dynamic range to enhance myocardial definition with standardized depth, frequency, and insonation angle for all participants.11 For offline analysis, a region
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Figure 1 Assessment of basic right ventricular dimensions from parasternal short-axis and apical four-chamber views, along with evaluation of transtricuspid inflow parameters and tricuspid annular DTI velocities according to the American Society of Echocardiography guidelines.20 Using a parasternal short-axis orientation at the level of the aortic valve (top left), right ventricular outflow tract end-diastolic diameter (RVOT-Prox) was measured, while by visualizing a modified apical four-chamber orientation focusing on the right ventricle, basal right ventricular inflow diameter at the tips of the tricuspid valve (TV) leaflets (RVD1) and right ventricular midventricular short axis (RVD2) and long axis from right ventricular apex to the level of the tricuspid annulus (RVD3) were calculated (bottom left). Right ventricular end-diastolic area (RVEDA) and right ventricular end-systolic area (RVESA) were measured, allowing calculation of right ventricular FAC as (RVEDA RVESA)/RVEDA. Illustrated are also the E and A waves and the deceleration time (DT) of transtricuspid inflow (top right) and S0 , E0 , and A0 lateral tricuspid annular Doppler velocities (bottom right). Ao V, Aortic valve; LA, left atrium; LV, left ventricle; PV, pulmonary valve; RA, right atrium; RV, right ventricle. of interest was manually traced along the endocardial border from base to apex at the end of systole, and width was set to match the wall thickness. If the automated 2D analysis appraisal of acceptable tracking quality indicated inappropriate tracking, retracing was performed until all six RV myocardial segments (three septal and three RV free wall) were considered to be acceptable.25 The following parameters were measured: global longitudinal peak systolic ε as the average of all six RV myocardial segments, RV free wall longitudinal ε as the average of the three RV free wall segments, and basal RV free wall ε. Also, systolic SR (SRS’) along with early and late diastolic SRs were calculated as the average of the base, mid, and apical segments of the right ventricle (Figure 2). Additionally, using a similar methodology tracing the endocardial border of the right atrium, the following parameters were estimated: peak atrial longitudinal ε (PALS) and peak atrial contraction ε were measured using a six-segment model for the right atrium. SR and its components (RA peak SRS’, RA early diastolic SR, and RA late diastolic SR) were also measured starting from QRS onset.26 To minimize measurement bias, we randomly selected 70 of the total of 134 echocardiographic studies to reassess 2 days after initial analysis of each study. Intraobserver variation was estimated, because a single operator performed both data acquisition and measurement. During repeated measurements, the researcher was blinded to previous results. Intraobserver variability was expressed using the coefficient of variation.
Statistical Analysis Analyses were performed using SPSS Statistics version 19.0 (SPSS, Inc., Chicago, IL). Sample size was calculated using an a level of 0.05, power of 0.80, and (taking into consideration our regional athletic population sport disciplines’ distribution) a ratio of SAs to EAs of 1:3 to detect an absolute difference of 2 6 3% in mean global RV ε between groups on the basis of literature data.5 Two groups enrolling $75 EAs and $25 SAs each were deemed adequate to meet the aforementioned criteria. Data are expressed as mean 6 SD for continuous variables and as counts and/or percentages for categorical variables. Comparison of variables was performed with one-way analysis of variance with post hoc Bonferroni analysis for groups of more than two. Chi-square or Fisher’s exact tests (for expected cell values < 5) were used to compare nominally scaled variables. Correlations between variables were assessed using Pearson’s r coefficient. In an attempt to minimize statistical bias due to unequal sample sizes or to violations of assumptions of the parametric tests used, bootstrapping analysis was performed, randomly resampling the study population 1,000 times. Comparisons’ P values reported are those adjusted from bootstrapping analysis.27 Concerning intraobserver variability, the mean value of the two observations (x) performed for all the parameters for more than half
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Figure 2 Strain and SR curves of the right ventricle in a participating athlete. AVC, Aortic valve closure; 4CH, four-chamber; FR, frame rate; GS, global peak systolic ε; HR, heart rate; SRA0 , Late diastolic SR; SRE0 , early diastolic rate.
of the echocardiographic studies and the absolute value of difference between observations (e) 6 SD were determined. Reproducibility was assessed by the coefficient of variation: (e/x)100%.
Table 1 Age, anthropometric data, clinical characteristics, and performance measures of the study population Variable
RESULTS Basic Demographic and Standard LV Morphologic Parameters Age, anthropometric data, clinical characteristics, and performance measures of the study population are shown in Table 1. No significant differences concerning age and body habitus parameters between athletes and controls were recorded. As expected, athletes presented, because of exercise-induced remodeling, greater internal dimensions (LVend-diastolic diameter and volume) and LV mass index compared with controls (LV end-diastolic diameter, 5.3 6 0.35 cm in EAs vs 5 6 0.38 cm in SAs vs 4.6 6 0.5 cm in controls [P = .005]; LV end-diastolic volume, 133.2 6 21.2 mL in EAs vs 110 6 17 mL in SAs vs 106.8 6 16 mL in controls [P = .001]; LV mass index, 108.9 6 27.5 g/m2 in EAs vs 91.8 6 18.3 g/m2 in SAs vs 82.7 6 21 g/m2 in controls [P < .0005]). LV diastolic function remained well within ‘‘normal’’ limits, showing no significant differences with values obtained from nonathletes.
Age (y) BSA (m2) BMI (kg/m2) HR (beats/min) SBP (mm Hg) DBP (mm Hg) Training experience (y) Training volume (hours/week)
EAs (n = 80)
SAs (n = 28)
Controls (n = 26)
P (ANOVA)
31.2 6 10.4 1.98 6 0.15 21.9 6 2.5 50 6 7 120 6 7 70.3 6 8.5 11.3 6 8.3
27.4 6 5.7 1.95 6 0.21 21.2 6 2.8 56 6 6 125.4 6 8 78 6 3 10.3 6 5.6
26.6 6 5.6 2.01 6 0.16 22.4 6 2.4 65 6 9 120.6 6 8 75 6 9 NA
.327 .333 .353 <.001 .29 .25 .488
14.6 6 5.4
17.1 6 7.2 NA
.115
ANOVA, Analysis of variance; BMI, body mass index; DBP, diastolic blood pressure; HR, heart rate; NA, not applicable; SBP, systolic blood pressure. Data are expressed as mean 6 SD.
RV and RA Morphology and Function in EAs and SAs Echocardiographic parameters concerning right cavity dimensions and functional data including transtricuspid inflow and DTI indices
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Table 2 Morphologic and functional RV and RA parameters of EAs, SAs, and controls
Variable
Morphologic parameters RVOTd (cm) RVITd (cm) RVDm (cm) RVL (cm) RV EDA (cm2) RV ESA (cm2) RV FAC (%) RA area (cm2) Functional parameters Tricuspid E (cm/sec) Tricuspid A (cm/sec) E/A ratio DT (msec) RV FW S0 (cm/sec) RV FW E0 (cm/sec) RV FW A0 (cm/sec) E/E0 ratio PASP (mm Hg)
EAs (n = 80)
SAs (n = 28)
Bootstrapping analysis
Controls (n = 26)
Controls vs EAs
Controls vs SAs
EAs vs SAs
P (ANOVA)
3.7 6 0.5 4.1 6 0.4 3.1 6 0.5 8.9 6 0.6 26.6 6 4 13.2 6 2.7 50.4 6 7 17.5 6 2.7
3.4 6 0.77 3.7 6 0.4 3.0 6 0.5 8.5 6 0.6 22 6 3.5 10.5 6 1.5 51.2 6 9.8 15 6 3.6
3.2 6 0.66 3.8 6 0.6 2.6 6 0.5 8.8 6 0.7 19.2 6 3.9 10.9 6 2.4 42.7 6 7.2 14 6 4.1
0.001 0.024 <0.0005 1.00 <0.0005 0.074 0.029 <0.0005
0.927 0.523 0.017 0.517 0.037 1.00 0.006 0.844
0.087 <0.0005 0.887 0.113 0.001 0.006 0.257 0.005
.001 <.0005 <.0005 .114 <.0005 .016 .007 <.0005
66.9 6 13.3 42 6 11.2 1.64 6 0.30 141 6 15,8 15.3 6 2.2 17.3 6 2.7 10.7 6 2.8 3.9 6 1 21 6 8.3
66.3 6 13.6 38.9 6 10.7 1.76 6 0.42 155 6 14.4 16.6 6 2.1 18.1 6 1.3 11 6 2.2 3.6 6 0.66 22.4 6 8.6
68.7 6 9.5 35 6 5.7 1.98 6 0.28 145.3 6 13.4 14.8 6 1.7 17.5 6 2.9 10.2 6 2.1 4 6 0.85 18.3 6 8.6
1.00 0.007 <0.0005 0.592 0.731 1.00 1.00 1.00 0.494
1.00 0.488 0.031 0.048 0.006 1.00 0.70 0.497 0.211
1.00 0.448 0.195 <0.0005 0.02 0.364 1.00 0.419 1.00
.753 .008 <.0005 <.0005 .004 .299 .480 .192 .192
ANOVA, Analysis of variance; DT, deceleration time; EDA, end-diastolic area; ESA, end-systolic area; FW, free wall; PASP, pulmonary artery systolic pressure; RVDm, right midventricular diameter; RVITd, RV inflow tract diameter; RVL, RV length; RVOTd, RV outflow tract diameter. Data are expressed as mean 6 SD.
Table 3 Two-dimensional speckle-tracking ε and SR data for the right ventricle and right atrium of EAs, SAs, and controls
Variable
RV 2D ε and SR analysis GLS (%) FW average ε (%) SRS’ (sec1) SRE’ (sec1) SRA’ (sec1) RA 2D ε and SR analysis PALS (%) PACS (%) RASSR (sec1) RAEDSR (sec1) RALDSR (sec1)
Bootstrapping analysis
EAs (n = 80)
SAs (n = 28)
Controls (n = 26)
Controls vs EAs
Controls vs SAs
EAs vs SAs
P (ANOVA)
23.1 6 3.7 26.4 6 5.4 1.21 6 0.21 1.54 6 0.29 0.67 6 0.22
25.1 6 3.2 27.8 6 4.3 1.42 6 0.22 1.44 6 0.28 0.75 6 0.27
23.1 6 3.5 27 6 4.3 1.2 6 0.28 1.49 6 0.44 0.74 6 0.26
1.00 1.00 0.891 0.86 1.00
0.076 0.668 0.005 1.00 1.00
0.087 0.565 <0.0005 1.00 1.00
.052 .467 .016 .455 .872
43.9 6 15 13.4 6 6.4 1.7 6 0.8 1.66 6 0.63 1.4 6 0.6
51.7 6 20 15.6 6 13.4 2.23 6 0.55 1.57 6 0.24 1.81 6 0.6
44.3 6 10 12.8 6 5 2.02 6 0.33 2.16 6 0.53 1.73 6 0.39
1.00 1.00 0.213 0.001 0.073
0.368 0.717 1.00 0.002 1.00
0.115 0.725 0.01 1.00 0.031
.106 .416 .007 .001 .01
ANOVA, Analysis of variance; FW, free wall; GLS, global longitudinal ε; PACS, peak atrial contraction ε; RAEDSR, RA early diastolic SR; RALDSR, RA late diastolic SR; RASSR, RA peak SSR’; SRA0 , late diastolic SR; SRE0 , early diastolic rate. Data are expressed as mean 6 SD.
of EAs, SAs, and controls participating in our study are shown in Table 2. Different training modes induced different morphologic RV patterns, leading to greater RV and RA dilatation among EAs, with 8.1% and 18.6% of them fulfilling major and minor dimensional criteria, respectively, for ARVC, but without other disease signs. There were no significant differences concerning ε between groups (P = .085), with SAs presenting higher global SRS’, as well as greater RA SSR’ and RA late diastolic SR waves of RA SR and marginally nonsignificant higher PALS (Table 3). Also, the comparison of global, RV
free wall, and basal longitudinal ε between EAs and SAs is shown in Figure 3. Differences in Structural and Functional RV and RA Characteristics According to Training Volume Basic demographic parameters, including age (P = .186), BSA (P = .17), and LV mass (P = 1.00), did not significantly differ between highly and moderately trained athletes. Both athlete groups showed
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22.2 6 3.1% for controls, P = .005 and P = 1.00 after post hoc analysis for athlete groups; Figure 3). Additionally, the only significant difference between highly and moderately trained athletes concerned PALS, with highly trained athletes presenting 53.6 6 18.2% compared with 42.6 6 15.5% of moderately trained athletes and 44.6 6 9.3% of controls (P = .01 and post hoc P = .008 between athletes). No differences concerning diastolic function indices were noted between athlete groups and controls. Effect of RV Dilatation on ε and SR Values Twenty-six of 108 athletes in our study fulfilled the RV dilation criterion (24%), showing no significant differences concerning age (P = .072), BSA (P = .155), and total training years (P = .763) with athletes without RV dilatation. Training hours per week were less (13.1 6 2.8 hours/week) for the RV dilatation group compared with the nondilated RV group (15.9 6 7 hours/week), although this was marginally not significant (P = .051). The right atrium was significantly larger for the dilated group (18.7 6 3.4 vs 16.2 6 2.7 cm2, post hoc P = .002). Concerning ε and SR values, no significant differences were recorded, with athletes presenting RV dilatation showing values close to those of normal controls (Figure 3). Correlation Statistics between Deformation Indices and ‘‘Classic’’ RV Contractility Parameters Increased ε and SR values among athletes in our study were significantly correlated with enhanced tricuspid annular S0 wave (DTI S0 ) and greater fractional RV fractional area change (FAC), parameters showing global and regional enhancement of RV contractility. More specifically, in EAs, correlation between ε and DTI S0 and between ε and RV FAC yielded Pearson’s r values of 0.579 (P = .001) and 0.353 (P = .029), respectively, while an r value of 0.652 (P < .0005) was recorded for the correlation of RV SRS’ and DTI S0 . Accordingly, in SAs, significant correlations between the aforementioned parameters were also revealed (e.g., r = 0.596, P < .001, for the correlation between ε and RV FAC). Intraobserver Variability Analysis Concerning RV functional ε indices, coefficients of variation for RV ε, RV SRS’, RV early diastolic SR, RV late diastolic SR, and RA PALS were 10%, 7%, 9%, 9%, and 14%, respectively. Feasibility for 2D ε analysis of the right ventricle reached 100%, because all enrolled athletes and controls had adequate image quality to allow a complete set of RV ε measurements offline. Concerning RA ε analysis, the basal lateral segment was the more complicated to trace for speckletracking analysis, although this was accomplished for >95% of examined segments, excluding the rest from the reported results.
Figure 3 Box-plot graphs demonstrating RV longitudinal ε indices (global peak systolic ε, RV free wall ε, and basal RV ε) in different subsets of athletic populations (according to sport discipline [EAs vs SAs], training volume [highly trained vs moderately trained athletes], and RV dilatation). For classification criteria, see inside text. *Statistically significant difference. FW, Free wall; H., highly; M., moderately. greater ε values compared with controls (24.5 6 3.6% for highly trained and 24.8 6 2.9% for moderately trained athletes vs
DISCUSSION Systematic training imposes a wide range of adaptations, structural and functional, affecting both ventricles and atria.1,2 Concerning the right ventricle, geometric remodeling secondary to systematic training has been described in previous studies, while ambiguous results exist regarding deformation and diastolic function of the right ventricle among athletes, suggesting that observed changes could be attributed either to an acquired right cardiomyopathy secondary to long-term intensive exercise or to physiologic
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conditioning per se.5,10-12 Our study, taking advantage of different groups of athletes (EAs and SAs, highly and moderately trained athletes, with or without RV dilatation), has shown that despite the existence of differences in RV and RA geometric measures, few meaningful differences in deformation exist, as RV and RA systolic and diastolic functions remain within normal ranges. There has been an ongoing controversy concerning longitudinal deformation of the RV free wall and especially its basic lateral segment,5,10-12 raising concern about potential myocardial damage due to endurance exercise, implying that exhausting training might lead to a type of RV cardiomyopathy.28-32 Our study, in concordance with findings by Oxborough et al.11 as well as D’Andrea et al.,10,33 has shown that even among highly trained athletes or athletes with dilated right ventricles performing endurance or strength exercise, global RV ε and SR, including basal deformation, are at least preserved if not increased. Increased ε and SR values among athletes of our study were in positive correlation with enhanced DTI S0 wave and greater RV FAC, parameters showing global and regional enhancement of RV contractility,34,35 which along with RV dilatation contributes to increased preload and stroke volume. On the contrary, in a study by Teske et al.,5 there was a discrepancy between ‘‘classic’’ basal RV deformation indices (such as tricuspid annular plane systolic excursion and DTI RV lateral wall S0 ), which appear to be increased among elite athletes, and novel deformation parameters (such as ε and SR), which were decreased. In addition, even though a transient impairment of RV systolic function has been described after bouts of ultraendurance exercise,28-30,36 our study provides evidence that during rest, RV function among athletes remains normal. A significant percentage, especially of EAs in our study, fulfilled major dimension criteria for ARVC, stressing the need for differential diagnosis between ARVC and athlete’s heart in the context of preparticipation screening. Enhanced contraction of RV free wall segments in athletes demonstrated by our study, compared with regional and/ or global deformation impairment in ARVC,37 may facilitate differential diagnosis between the two entities. Additionally, assessment of RV diastolic function both with older echocardiographic indices (tricuspid inflow E/A ratio, tricuspid annular E0 and A0 waves, and RV E/E0 ratio) and novel parameters (global SR E and A waves) is another key feature permitting differential diagnosis between physiologic adaptations and pathologies of the right ventricle, because RV relaxation in athletes is well within normal limits.38 It is evident that current ARVC criteria show major limitations when applied for preparticipation screening, necessitating the use of novel deformation and diastolic function parameters in discriminating normal adaptations from pathologic variations. Apart from confirming RV and RA dilatation, especially among EAs, to act synergistically with LV dilatation for stroke volume augmentation,1 our study has shown a trend toward better deformation (global longitudinal ε and SRS’) among SAs. Increased RV ε and SR values observed in SAs may reflect a different morphology of the right ventricle, leading to different RV deformation patterns. Additionally, despite RA dilatation in athletes, the contractility of the atrium remains normal, contributing through atrioventricular coupling to preload increase and stroke volume augmentation. Values of RA ε obtained from our cohort of athletes do not differ compared with values introduced by two previous studies from the same center.39,40 On the other hand, pathologic conditions such as cardiomyopathies or other myocardial diseases are also accompanied by left atrial and/or RA enlargement, showing however decreased deformation indices.37 In this context, assessing functional alterations of the right atrium apart from its significance in the study of physiologic adapta-
Journal of the American Society of Echocardiography November 2013
tions, it may serve as a useful discriminator of athlete’s heart from morphologically similar but life-threatening conditions such as ARVC. Limitations A potential limitation of our study could be considered the lack of hemodynamic data on the right ventricle, providing more accurate assessment of pulmonary artery systolic pressure and RA pressures. However, it has been demonstrated that there is a significant correlation between values obtained after catheterization and indices based on echocardiographic evaluation of the right ventricle. The disparity of enrolled groups (80 EAs vs 28 SAs vs 26 controls) reflects the arithmetic dominance of EAs in our regional population, along with the refusal of many highly trained SAs to participate in the study. In an attempt to minimize the effect of sample size inequality and statistical bias, bootstrapping analysis was adopted as being more robust than single parametric tests. The quantity and quality of training are crucial to describe the morphologic and functional athlete’s heart adaptations, and in this context maximal oxygen uptake is the gold standard and an objective measure of aerobic fitness. However, high-intensity static exercise is performed with anaerobic metabolism and static exercise training results in a small or no increase in maximal oxygen uptake. Because the exercise stimuli and sports demands of enrolled athletes in our study were different, athletes were classified according to their athletic experience and sport-specific performance. Evaluation of RV and RA ε and SR indices was based on EchoPAC software, a PC program developed by GE for 2D speckle-tracking of the left ventricle. As has been done in previous studies in this field,5,1012 LV-dedicated software was applied for RV and RA ε evaluation, and even though the reproducibility of measurements was good, changes in the software in the future or correlation studies with other imaging modalities (such as magnetic resonance imaging) may be useful to optimize the tracking quality of the right ventricle, improving the measurements performed. Even though up to 80% of RV global deformation is due to longitudinal ε, radial ε of the right ventricle was not estimated in this study. The lack of dedicated software in combination with the morphology of the RV free wall (too thin to develop significant traceable thickness during contraction) was an obstacle to assessing radial ε indices of the right ventricle. Similarly, RA ε and SR values were obtained only from the apical four-chamber view, because this is the only axis permitting the recording of RA longitudinal ε. CONCLUSIONS Systematic training imposes physiologic, morphologic, and functional adaptations on the right ventricle and right atrium. Despite differences in geometric remodeling among different subsets of athletes (EAs vs SAs, highly vs moderately trained athletes, with or without RV dilatation) and untrained controls, few meaningful differences in right cardiac cavity deformation and relaxation exist, suggesting that RV and RA systolic and diastolic function in athletes, irrespective of sport discipline, training volume, and physiologic remodeling, remain within the normal range. ACKNOWLEDGMENTS We thank all the athletes and healthy volunteers participating in the study. Additionally, we thank Vourdounis Nikos and
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