Academic Editors: Vincenzo Russo, Saverio Muscoli and Giuseppe Mascia
Background: In young athletes, the level of competitiveness in sports is increasing, as well as frequency and intensity of exercise training. Adaptations of the cardiac system to this increased workload imposed by exercise has not yet been studied sufficiently. In adults, studies point towards a shift from the functional athlete’s heart towards pathological cardiac remodelling, with ventricular arrythmia and impaired cardiac function, that is exercise-related. This systematic review investigates cardiac adaptations to exercise in junior athletes compared to inactive controls. Methods: Three electronic databases (PubMed/Medline, ScienceDirect and Web of Science) were searched for studies assessing 2-dimensional transthoracic echocardiography (2D TTE) and 2-dimensional speckle tracking echocardiography (2D STE) parameters in junior athletes, aged 7–19 years, compared to inactive controls. Data was screened and extracted by two reviewers; study quality and risk of bias was assessed by three reviewers. Results: Eight out of 1460 studies met all inclusion criteria, with all studies reporting results on 2D TTE and six studies reporting results on 2D STE parameters in 540 (51 girls) junior athletes and 270 (18 girls) controls. There is evidence for structural cardiac adaptations of the left ventricle and both atria in junior athletes. Results regarding left ventricular function are controversial with a tendency to improved function in dynamic exercising athletes. Left ventricular mass and relative wall thickness point towards higher values in static exercising athletes. Conclusions: Cardiac adaptations to exercise occur in children and adolescents. These adaptations are more pronounced in structural left ventricular parameters. Functional parameters are preserved or slightly improved in junior athletes but not impaired by exercise.
Young athletes performing sports on a competitive level practice between 10–20 hours a week at moderate to high intensities [1]. To keep up with the increased demands imposed on the body by intensive physical exercise, the cardiovascular system has to increase its capacity by a factor of 5–6 compared to moderate exercise [2]. Additionally, the level of competitiveness is increasing as well as training frequency, intensity, and demands that are placed into children’s training sessions [3, 4]. Several studies have reported cardiac remodelling in children and adolescents [5, 6, 7, 8]. Apparently, cardiac adaptation does not require the time span of a long professional training career.
To provide an overview of the current state of research regarding structural and functional cardiac adaptation in junior athletes, and to present results of these studies regarding the influence of exercise on the cardiovascular system, we performed this systematic review, searching electronic databases for studies investigating the cardiac structure and function in male and female junior athletes (7–19 years) compared to a non-active control group by two-dimensional transthoracic echocardiography (2D TTE) or 2D speckle tracking echocardiography (STE).
This review is in line with the PRISMA Statement [9].
Search strategy and selection criteria: We searched databases PubMed/Medline, ScienceDirect, and Web of Science. Inclusion criteria were (1) exercising or active children and/or adolescents, aged 7–19 years; (2) comparison of athletes with an inactive control group (CG); (3) performing 2-dimensional transthoracic echocardiography and/or 2-dimensional speckle tracking echocardiography. The exact search term was: ((children OR adolescents) AND (activ* OR trained OR exercise) AND (echocardiography or speckle tracking) AND (control group)). Only articles published in English were included. Review articles and meta-analyses were not considered, as well as articles including animal studies and the use of patients. Further exclusion criteria were: (1) not meeting our age criteria; (2) not exercising regularly/at a competitive level; (3) no inactive control-group; (4) other cardiac imaging methods. Results were screened by two researchers separately (HW and TE).
Risk of bias assessment: The risk of bias assessment for methods was performed according to an 11-item checklist for case-control studies [10]. To assess the risk of bias in study results a 12-item checklist was applied based on a recent review [4]. Three researchers (HW, LB, TE) screened the methods section and checked each study’s results. If no agreement could be found a consensual decision was made.
Data extraction: A standardized data extraction form was set up (TE) and cross-checked (HW). Where study data was unclear, authors of the corresponding publication were contacted.
Quality assessment: Study’s quality was assessed with the study quality assessment tool by the NIH National Blood, Heart, and Lung Institute [11]. Criteria were rated by three researchers (HW, LB, TE). If no agreement could be found a consensual decision was made.
In total, eight of 1460 studies met all inclusion criteria. Most of the studies (1424/97.7%) were excluded after the first screening. The majority of these studies did not deal with the matter of this review (43%), included patients (29%), did not meet our age criteria (16.5%), included animals (7%), or were recommendations or reviews (4%). Results of our search and reasons for excluding studies are shown in Fig. 1.
Flow chart of the study selection process.
Regarding the risk of bias assessment for methods full agreement was met in 44% of cases. Regarding the risk of bias assessment in reporting results, the researchers fully agreed in 93% of cases (see Supplementary Table 1 and Supplementary Table 2).
Five studies were rated to be of good quality [3, 12, 13, 14, 15], one as fair [16] and two studies as being of poor quality [17, 18]. Full agreement between the researchers was met in 60.6% and a majority agreement in 38.3% of the categories. Authors did not agree on 1 point (1.1%) (see Supplementary Table 3).
Sample sizes varied from n = 44 to n = 300 participants [3, 12, 13, 14, 17]. Only
two studies included female athletes [14, 16]. All studies included athletes
performing predominantly dynamic (soccer and tennis) or mixed types of sports
(basketball, running, cross-country skiing). Three studies included static types
of sports [16, 17, 18]. A minimum training history of two years was required in four
studies [14, 16, 17, 18]. Athletes in other studies trained for an average 4–6 years
[12, 15, 18]. Training time per week varied from 2.5–3 hours [14, 16] up to 15
hours [17]. The control group’s activity level was
Anthropometric characteristics of study participants (age, body height, body mass, body surface area [BSA], body mass index [BMI]) as well as heart rate, systolic blood pressure [SBP], and diastolic blood pressure [DBP] are displayed in Supplementary Table 5.
Four authors reported a significantly lower heart rate in athletes compared to
controls (p
There was a huge variety of echocardiographic parameters and their methodological approach which made it difficult to compare these studies. Most authors focused on parameters regarding the left heart [12, 14, 15, 16, 17, 18] and two studies on the right heart’s structure and function [3, 13]. Results were categorized according to the heart’s structure and function.
Six studies focused on LV structure [12, 14, 15, 16, 17, 18]. As structural parameters are largely influenced by BSA [19, 20] only indexed parameters were compared: LV end-diastolic diameter (LVEDD), LV end-systolic diameter (LVESD), interventricular septal thickness (IVS), LV wall thickness (LVWT), LV posterior wall thickness (LVPWT), mean wall thickness (MWT), relative wall thickness (RWT), LVM, LV length, LV end-diastolic volume (LVEDV), and LV end-systolic volume (LVESV). LVEDD was significantly higher in athletes in two studies [14, 15]. The latter also reported a significantly higher LVEDS. Binnetoglu et al. [16] reported similar mean values for LVEDD and LVESD in athletes and controls, except for basketball players. Athletes’ IVS was significantly higher in three studies [14, 15, 16], LVPWT was significantly increased in five studies [14, 15, 16, 17, 18]. Sulovic et al. [18] reported a higher RWT in athletes. In addition, static exercising athletes had a significantly higher RWT compared to dynamic exercising athletes. The same for LVM held true in this study and in three other studies [14, 15, 17, 18]. Binnetoglu et al. [16] reported the same findings in soccer players vs. tennis players and controls and a significantly increased LVM in wrestlers vs. tennis players. In summary, there is evidence of structural cardiac adaptations in junior athletes. These adaptations cannot be exclusively attributed to either dynamic or static types of sport (see Supplementary Table 6).
LV systolic function is represented by stroke volume (SV), LV ejection fraction (EF), fractional shortening (FS), cardiac output (Q), cardiac index, peak systolic myocardial velocity (S’), LV myocardial performance index (Tei index), concentricity, and sphericity index.
Endurance athlete’s EF was significantly increased in the study by Rundqvist et al. [14]. Divided into dynamic and static types of sport, Sulovic et al. [18] reported a significantly higher EF in dynamic exercising athletes and a significantly reduced EF in static exercising athletes. Contrary to these findings, three studies did not report significant differences [15, 16, 17]. The same is reported for FS [15, 16].
Diastolic function is represented by eleven parameters: mitral annulus plane systolic excursion (MAPSE), peak early LV diastolic filling velocity (E), peak late LV diastolic filling velocity (A), E/A ratio (E/A), deceleration time of E (DT), early diastolic myocardial velocity (E’), late diastolic myocardial velocity (A’), E/E’ ratio (E/E’), and E’/A’ ratio (E’/A’).
Significant differences for E and A are reported by Binnetoglu et al. [16] and Sulovic et al. [18]. Swimmers’ E was significantly higher than the other athletes and the CG [16]. Sulovic et al. [18] reported a significantly higher E in dynamic compared to static exercising athletes, and a significantly reduced E in the latter, compared to controls. Wrestlers [16] had a reduced A compared to controls as well as static exercising athletes compared to dynamic exercising athletes and controls [18]. E/A was significantly higher in athletes in the study by Rundvqist et al. [14]. Summarized, the studies reported contradictory findings regarding LV function (Supplementary Table 7).
Two studies assessed RV structure [3, 14] with the following parameters: right
ventricular outflow tract (RVOT) assessed in the parasternal long-axis view
(PLAX) and the parasternal short-axis view (PSAX), RVOT distal diameter, RV basal
diameter, RV mid-cavity diameter, RV end-diastolic area, and RV end-systolic
area. All RV parameters in D’Ascenzi et al.’s [3] study failed
significance (indexed to BSA) except for RV end-systolic area. RV parameters by
Rundqvist et al. [14] were significantly higher in athletes compared to
controls (p
Diastolic parameters as tricuspid annular plane systolic excursion (TAPSE), E/A, E’, A’, E/E’, and E’/A’ were assessed by two authors [3, 14]. RV systolic function was assessed with two parameters: S’ and RV fractional area change (FAC). Only TAPSE, indexed to BSA, was significantly higher in athletes whereas RV FAC was significantly reduced [14]. Summarized, there are conflicting results on the effect of exercise on RV function (Supplementary Table 9).
D’Ascenzi et al. [13] reported results of biatrial remodelling. Four other authors [14, 15, 17, 18] assessed LA diameter and LA volume. There were no significant differences in the study by D’Ascenzi et al. [13] and Sulovic et al. [18]. Rundqvist et al.’s [14] study showed an increased LA diameter and volume. Soccer players in the study by Zdravkovic et al. [15] had an increased diameter compared to controls. Summarized, three out of five studies reported increased left atria dimensions in athletes (Supplementary Table 10).
Two authors reported results of RA structure [13, 14]. Parameters assessed were: RA area, RA diameter, and RA volume. Soccer players in the study by D’Ascenzi et al. [13] had a significantly larger RA volume compared to controls. Rundqvist et al. [14] observed a significantly increased RA area and diameter in endurance athletes. Summarized, there is evidence of the influence of exercise on right atrial structure (Supplementary Table 11).
Six of the eight studies assessed myocardial strain by 2D speckle tracking echocardiography [3, 12, 13, 14, 16, 17]. Four studies assessed LV function [12, 14, 16, 17], two authors focused on the RV [3, 14], and/or function of the atria, respectively [13, 14]. This categorization was further followed to compare studies’ results. All studies applied the same software for off-line analysis (EchoPAC, GE Healthcare), but used different versions. All performed the analysis from 40 frames/s to 80–100 frames/s and measured myocardial movement selecting the heart cycle with the most defined endocardial border at end-diastole. Authors, however, applied different recommendations on how to perform 2D STE (Supplementary Table 4).
Three studies [12, 16, 17] reported results on four-chamber longitudinal strain.
Whereas Beaumont et al. [12] did not observe significant differences
between soccer players and controls, basketball players in the study by
Binnetoglu et al. [16] had a significantly lower strain (p
Again, basketball players in the study by Binnetoglu et al. [16]
presented the lowest GLS compared to other study groups (p
Two studies [12, 16] reported results on circumferential and radial strain but
for different LV segments. Beaumont et al. [12] measured circumferential
and radial strain at the mitral valve or basal level, respectively, and
mid-ventricular at the mid-papillary muscle level [12]. Circumferential strain
differed significantly at both levels between soccer players and controls with
higher values in soccer players. They did not observe significant differences
regarding radial strain. In contrast, Binnetoglu et al. [16] reported
global circumferential and radial strain, measured at the anteroseptal, anterior,
lateral, posterior, inferior, and septal wall but did not state at which
segmental level [16]. The combined group of athletes showed a significantly lower
circumferential strain (p
D’Ascenzi et al. [3] and Rundqvist et al. [14] reported RV
longitudinal strain values assessed at the four-chamber view. Both authors took
measurements of the RV free wall only, subdivided into basal, mid, and apical
segments, and did not observe significant differences between athletes and
controls (p
Two of six studies reported results on 2D STE of the LA, however, D’Ascenzi et al. [13] and Rundqvist et al. [14] did not investigate the same LA parameters. D’Ascenzi et al. [13] reported results on peak atrial longitudinal strain (PALS), which is a measure of LA deformation during the reservoir phase, and peak atrial contraction strain (PACS), which is the myocardial strain during atrial systole [21, 22]. They did not report significant differences between athletes and controls. Rundqvist et al. [14] assessed LA total strain measured at the four- and two-chamber view with subdividing the LA into six segments each [23] and also did not observe significant differences between athletes and controls either. Summarized, there is no evidence of an influence of exercise on LA strain, (Supplementary Table 13).
Only D’Ascenzi et al. [13] reported results on 2D STE of the right atrium, assessed at the four-chamber view with subdividing RA into six segments. Analogous to LA function, PALS and PACS of the right atrium were assessed. The authors did not find significant differences between athletes and controls. Summarized, there is no evidence for an influence of exercise on RA strain (Supplementary Table 13).
This systematic review compared results of eight studies assessing 2D TTE and 2D STE parameters in junior athletes vs. an inactive CG. The main findings of the study were: (1) Training-induced chamber-remodelling does occur in junior athletes. (2) Results regarding 2D TTE assessed LV and RV function are conflicting and do not provide a clear statement pointing towards an improved function in athletes. (3) LV function assessed by 2D STE was improved in junior athletes in two of three studies. RV and atrial function were not affected by exercise.
Overall, five of six studies observed increased LV dimensions. These results are
in line with other authors [4, 5, 7, 8, 24, 25, 26]. Mc Clean et al. [4],
reported increased LV morphometry in a meta-analysis involving
LV hypertrophy, defined by an LVM
Regarding LV wall dimensions, a LVWT or IVSD
In conclusion, exercise does have an impact on LV structure in young athletes. This impact is influenced by athletes’ age, hence pubertal and hormonal status and also by training volume and intensity. Most studies observed significantly increased LV diameter, LVWT, and LVM in athletes.
Results regarding LV function did not clearly state significantly different
results between athletes and controls or within the athletic groups. None of the
studies reported any adverse results regarding a significantly impaired LV
function. Three authors [12, 14, 18] noticed an improved systolic function by a
significantly increased EF in soccer players and dynamic sports, respectively.
Rundqvist et al. [14] observed a significantly improved diastolic
function (E/A) as well as Sulovic et al. [18] in endurance-trained
athletes (E). This result is in line with other studies [5, 24, 32, 33]. Unnithan
et al. [33] compared 22 highly trained soccer players (12
In conclusion, results are controversial and do not allow a clear statement. Regarding LV systolic function, there are studies reporting improved results in young athletes but also no significantly different results compared with controls. The same is for LV diastolic function. If significantly increased results were reported, they were reported in endurance athletes but not in strength-trained athletes.
Two studies assessed RV structure [3, 14] with conflicting results. D’Ascenzi
et al. [3] only noted a significant increase in RV end-systolic area
index in swimmers compared to controls. All other parameters failed statistical
significance when indexed to BSA. Rundqvist et al. [14] observed a
significantly increased RVOT, RV basal diameter index, and RV end-systolic area
index. RV adaptation is expected in athletes as the RV works hand-in-hand with
the LV [36, 37]. Strength training, on the contrary, does not affect the RV to
the same extent that endurance exercise does, and pulmonary vasculature is
protected by high pressures [30, 38]. Current literature does not provide better
insight into RV structure in children and adolescents. Only one study could be
found that assessed RV structure in this age group [39]. Allen et al.
[39] reported RVWT and RV cavity in 77 swimmers (32 females), aged 10.8 (5–17)
years. All participants exceeded the 95th percentile of reference values for
RVWT, and most of the participants for RV cavity. La Gerche et al. [38]
noticed a significant increase in RV volume right after a competition in 40 adult
athletes (37
Two studies investigated RV function in junior athletes [13, 14]. Rundqvist et al. [14] found a functional remodelling in endurance-trained athletes whereas D’Ascenzi et al. [3] observed no differences between swimmers and controls for most parameters and a significantly reduced RV FAC in swimmers. La Gerche et al. [38, 42] confirmed these results in adults at rest and immediately after a competition. Thus, the slightly reduced resting function that was preserved during exercise rather bears a contractile reserve but does not represent impaired RV function [42]. Reduced RV function in highly trained athletes immediately after a competition mostly recovered after one week but long-term structural remodelling is likely [38]. The adverse consequence of this is ventricular arrhythmia, which is observed in trained adults, associated with a longer duration of exercise [29, 38, 43]. To prevent this adverse adaptation in children and adolescents, a closer observation of junior athletes is needed—especially in a longitudinal setting.
Five studies examined LA structure [13, 14, 15, 17, 18], and two studies assessed RA
structure [13, 14]. All studies except for two [13, 18] reported significantly
increased LA and RA dimension and volumes which is in line with studies in adult
athletes [44, 45, 46, 47, 48, 49]. During exercise, the LA adapts to pressure and volume
overload, which leads to LA dilatation [45]. Pelliccia et al. [48]
observed marked atrial dilatation (
In conclusion, LA diameter and volume, RA volume, area, and diameter were increased in athletes, indicating a significant influence of exercise. As a consequence of LA dilatation, atrial flutter or fibrillation could arise as complication. Therefore, more focus should be placed on atrial examination to detect adverse adaptations as early as possible.
Six of eight studies included in this review performed STE analysis [3, 12, 13, 14, 16, 17]. 2D STE is accepted as an early marker for systolic dysfunction as it detects a decrease in contractility when EF is still within normal limits [50, 51].
Two of four studies reported improved LV function in junior athletes. In the
study by Simsek et al. [17], this difference did not depend on the types
of sports, as there were no significant differences between endurance and
strength athletes. On the contrary, Binnetoglu et al. [16] observed a
significantly reduced strain in basketball players compared to other groups and
controls whereas Rundqvist et al. [14] did not observe significant
differences in strain between endurance athletes and controls. The latter is in
line with no significant results reported by other authors [33, 52, 53] who
compared 22 soccer players (12.0
Two studies assessed RV function in junior athletes [3, 14] and did not observe
significantly different values in athletes and controls. Furthermore, there was a
tendency toward lower strain values in athletes vs. controls. Bjerring et
al. [52] observed a significantly reduced RV GLS (28
Two studies investigated atrial function by 2D STE [13, 14]. D’Ascenzi
et al. [13] examined biatrial function in swimmers vs. controls and did
not report significant differences. Rundqvist et al. [14] observed
non-significant differences in LA strain between endurance athletes and controls.
One study was identified that examined LA function in n = 595 highly trained
soccer players (25.1
The number of studies investigating cardiac adaptations in young athletes is
limited. Comparability of existing studies is difficult due to differences in age
groups, different types of sports, whether male or female athletes are being
compared, and, importantly the difference in the parameters assessed by
echocardiography itself. The latter calls for a consensual recommendation on how
to assess the pediatric athlete’s heart by 2D TTE and 2D STE and on how to report
these data [56]. If available, sex- and age-dependent z-scores should be reported
instead of absolute values [4, 56]. In total, 51 parameters have been assessed by
2D TTE in eight studies, regarding the left and right heart structure and
function, and 15 different parameters with 2D STE. All parameters have been
assessed in different cohorts, with sub-groups of n = 16 to n = 100 participants,
predominantly males. The age varied from 10.8
Most echocardiographic parameters are indexed to BSA, to account for
anthropometric differences in subjects and to enable comparability [19]. However,
how parameters were indexed contributed to variation in echo parameters.
Diameters were either not indexed to BSA or indexed to BSA or BSA
Overall, as requested by D’Ascenzi [44], recommendations on how to assess cardiac function in this pediatric sub-group, are required. In addition, studies that assess cardiac function in a longitudinal setting [33] could provide better insight into the process of cardiac adaptation in junior athletes, help us to differentiate between physiological and pathological adaptations and to recognize these differences at a very early stage.
Cardiac adaptation to exercise does occur in children and adolescents—even in very young athletes. These adaptations are more pronounced in structural parameters, whereas functional parameters are preserved or slightly improved. The underlying stimuli for cardiac adaptation have been identified as being factors like the training history, training volume and intensity, the types of sports [70], genetics [58] and pubertal and hormonal status [31, 71, 72].
The variability, given by the nature of the cohort of junior athletes and the individual sports emphasizes the need to standardize variables, e.g., the test and measures we apply and how results are reported. Recommendations on the assessment of cardiac function in junior athletes are needed as well as studies with a longitudinal design.
2D STE, 2-dimensional speckle tracking echocardiography; 2D TTE, 2-dimensional transthoracic echocardiography; A, peak late LV diastolic filling velocity; A’, late diastolic myocardial velocity; BMI, body mass index; BSA, body surface area; CG, control group; DBP, diastolic blood pressure; DT, deceleration time of E; E, peak early LV diastolic filling velocity; E’, early diastolic myocardial velocity; E’/A’, E’/A’ ratio; E/A, E/A ratio; E/E’, E/E’ ratio; EF, ejection fraction; FAC, fractional area change; FS, fractional shortening; GLS, global longitudinal strain; IVS, interventricular septal thickness; LV, left ventricle; LVEDD, LV end-diastolic diameter; LVEDV, LV end-diastolic volume; LVESD, LV end-systolic diameter; LVESV, LV end-systolic volume; LVM, left ventricular mass; LVPWT, LV posterior wall thickness; LVWT, LV wall thickness; MAPSE, mitral annulus plane systolic excursion; MWT, mean wall thickness; PACS, peak atrial contraction strain; PALS, peak atrial longitudinal strain; PLAX, parasternal long-axis view; PSAX, parasternal short-axis view; Q, cardiac output; RVOT, right ventricular outflow tract; RWT, relative wall thickness; S’, peak systolic myocardial velocity; SBP, systolic blood pressure; SV, stroke volume; TAPSE, tricuspid annular plane systolic excursion.
HW designed the research study and drafted the manuscript. HW and TE performed the literature research and screened publications, performed the data extraction, risk of bias, and quality assessment. LB performed the risk of bias, and quality assessment, and reviewed the manuscript. FM, NS and ROF screened and reviewed echocardiographic results, and reviewed the manuscript. All authors contributed to editorial changes in the manuscript. All authors read and approved the final manuscript.
Not applicable.
Thanks to Susan Perkins, for language edits.
This research received no external funding.
The authors declare no conflict of interest.