Abstract
Aims:
Athlete’s heart has been extensively studied, particularly regarding global myocardial remodeling in normal systodiastolic function and supernormal deformation reserve. Based on specific morphological characteristics, it is commonly classified as eccentric and concentric remodeling; however, the recent interest in echocardiography lies in the dynamicity of the vorticity flow inside the LV chamber, primarily correlated with diastolic function. This study aims to verify the potential additional contribution of vortex analysis in characterizing the athlete’s heart.
Methods and Results:
A group of 23 highly trained athletes was studied using two-dimensional standard and deformation echo parameters and vortex examination. A dedicated software (HyperDoppler-ESAOTE) defined geometrical and dynamic vortex parameters (area, length, depth, energy dissipation [ED], vorticity fluctuation, and kinetic energy fluctuation). The data obtained were compared with a group of 26 active nonathletes and a group of 23 normal subjects. Body mass index differed among the three groups, with higher values in normal subjects (normal = 27.2 ± 5.7; active = 22.9 ± 2.6; triathletes = 22.1 ± 1.8; P = 0.01). Indexed left ventricle mass was significantly higher in triathletes (triathletes = 96.9 ± 14.9; active = 87.6 ± 15; normal = 79.5 ± 15.7; P = 0.003) as twist (triathletes = 12.3 ± 3.9; active = 9.8 ± 3.7; normal = 8.1 ± 3.1; P = 0.001), expressing a supernormal apical reserve. Diastolic function was normal in both groups. In the presence of normal geometrical vortex data, vortex energetic parameters were significantly higher in triathletes (ED = 1.10 ± 0.41, P < 0.001; vorticity fluctuation = 0.89 ± 0.04, P < 0.001; kinetic energy fluctuation = 1.01 ± 0.08, P < 0.001).
Conclusions:
Vortex analysis complements the morphological remodeling of the athlete’s heart. It can contribute to defining the effects of training intensity and energy consumption. Future research will focus on potential modifications in different sports.
Keywords: HyperDoppler, sport, strain
INTRODUCTION
Athlete’s heart is a physiological condition characterized by progressive myocardial remodeling due to regular training.[1,2]
Some noninvasive methods have been further used to better define the morphological modifications. A new method for the noninvasive evaluation of intracardiac flow, by HyperDoppler analysis, has been proposed.[3] This innovative approach investigates the flow dynamic pattern inside LV, providing data about the geometrical and energetic aspects of the flow.[4,5] A specific contribution of this method in the definition of the athlete’s heart, has not yet been studied. This study aims to verify the potential additional contribution of vortex analysis in characterizing the athlete’s heart.
METHODS
Populations studied
A group of 23 triathletes (T), aged 35 ± 11 years of age, from a trained Italian triathlon team (6 females and 17 males), and two additional groups were included. One group consisted of 25 active subjects named “normal healthy subjects” (HS) (aged 40 ± 14.9 years of age, including 7 females and 18 males) and the other group comprised 26 sedentary subjects(S) (aged 42 ± 15.7 years of age; 15 males and 11 females). All participants were Caucasian and from Italy and they were without evidence of chronic disease in the anamnestic report or family history of sudden cardiac death.
The triathlete group underwent daily training for at least 10 h/week for over 5 years. The healthy subjects group trained on average 3–4 h/week at moderate intensity, while the sedentary group did not perform a structured physical activity.
Consent and ethical considerations
All participants provided informal written consent to participate in the study and to publish the collected data. The study adheres to the Declaration of Helsinki. No local ethics committee approval was deemed necessary as this is an observational study, and the data are available in the Sports Medicine Center’s dataset as part of sport and lifestyle reconditioning programs.
Exclusion criteria
Exclusion criteria, clarified during the checkup, included a history of sudden death in the family, any cardiac or metabolic disease, drug assumption for any noncommunicable chronic disease, or the abuse of illicit substances; the presence of electrocardiogram (ECG) abnormalities was also included in these criteria.
Protocol study
All subjects underwent evaluation under resting conditions. A comprehensive anamnesis was conducted, including a familial history and potential previous diseases. A concise narrative of lifestyle habits was obtained. The quantity of weekly physical activity was assessed regarding METs/hour/week, considering the number of daily steps and the exercise intensity range. In addition, information about any additional programmed physical activity at moderate intensity was gathered through a simple and validated questionnaire called the International Physical Activity Questionnaire (IPAQ).[6] This investigation aimed to differentiate athletes from active and sedentary subjects. The three groups were classified as inactive (IPAQ < 700), sufficiently active (IPAQ 700–2519), and active (IPAQ > 2520), as delineated in the results tables. This classification was used to divide the subjects into three groups. A standard clinical evaluation, including measurements of systolic and diastolic blood pressure and a 12-lead ECG, was performed to exclude any pathological patterns. Furthermore, a two-dimensional (2D) echocardiographic examination was conducted, encompassing the acquisition of standard, deformation, and HyperDoppler parameters. All data obtained were compared among the three groups.
Standard two-dimensional echo parameters
Following the American Heart Association Guidelines, a complete traditional echocardiogram using MLX8exp Release F100001 (Esaote, Florence, Italy) equipped with a 2.5 MHz probe was performed in each subject at rest.[7] The basal 2D systodiastolic and Doppler parameters were obtained, including 2D measures as interventricular septum, posterior wall thickness, left ventricular end-diastolic diameter and left ventricular end-diastolic volume, left ventricular end-systolic diameter, and left ventricular end-systolic volume, left atrial dimension (LA) and left atrial volume, aortic root dimension, peak velocities of pulsed wave Doppler transmitral flow during early diastole (E) and atrial systole (A), deceleration time of early diastolic flow (DTc), and isovolumetric relaxation time, along with Tissue Doppler (E1, A1, and S1) parameters. The left ventricular mass index (LV mass g/m2) was evaluated using the Devereux formula.[8] Ejection fraction (EF) was calculated using the Simpson rule method. The severity of any valve insufficiency was assessed by the extent of the regurgitant jet on a 0–4 scale, using the color-flow mapping method from the four-chamber view, according to the ACC/AHA guidelines.[7] For the right ventricle (RV) definition, the RV outflow tract diameter was measured, and normal function was confirmed by the tricuspid annular plane systolic excursion expressed in mm and Power Doppler analysis at the pulmonary valve. Pulmonary pressure was also indirectly measured by the acceleration time.
Strain analysis
All subjects underwent a comprehensive echocardiographic examination to assess myocardial deformation parameters, including global longitudinal strain (GLS) from two chambers, three chambers, and four chambers. A dedicated software (XStrain tm-ESAOTE-Florence, Italy) was employed to calculate myocardial deformation. Following the criteria outlined in the European Association of Cardiovascular Imaging/ASE consensus document, average myocardial deformation was derived from images captured over the entire cardiac cycle at a high frame rate.[9] The 2D images from the 4-chamber views were subjected to postprocessing using X-Strain software, providing an angle-independent tool for evaluating velocities and strain. This software facilitates the automatic assessment of dynamic properties of the endocardial border and subendocardial tissue from 2D B-mode echocardiographic clips. A key deformation parameter, such as the GLS of the left ventricle, was considered.
HyperDoppler analysis
The Vortex analysis involved the assessment of geometrical parameters (Area, depth, length, intensity) and energetic parameters (fluctuation, dissipation, and Kinetic fluctuation). These data were derived from a 3C apex view and underwent further postprocessing analysis of strain detection using dedicated software from ESAOTE – Mylab X8 exp, employing the HyperDoppler method. Image acquisition was carried out utilizing the ESAOTE MyLabX8 exp echo scanner and PX 1-5 cardiac probe (ESAOTE, Florence, Italy), which were consistent with the conventional examination equipment. Subjects were positioned in the left lateral decubitus position, as previously described in the literature.[10,11] A specific apical 3C view, including the aortic tract, was used [Figure 1a and b]. Particular attention was paid to including the LV cavity and the LV outflow tract within the corner of the color Doppler sector as much as possible. The depth and width of the sector were set to achieve a Color Doppler frame rate of 21 fps. The repetition frequency of the Color Doppler pulse was 4.4 MH [Figure 1a and b].
Figure 1.
HyperDoppler postprocessing analysis. (a) report the reconstruction of left ventricle vortex by HyperDoppler method and the measurement of geometric and kinetic (b) It is added the reconstruction of vortex by a colour map and the principal axis of left ventricle forces
Electrocardiogram analysis
To exclude any eventual ECG abnormalities as potential elements of disturbance of the flow dynamic pattern, a baseline 12-lead electrocardiogram was obtained at rest conditions. Cardiologists and sports medicine specialists reviewed all the ECGs. ECGs were analyzed according to the sports cardiology guidelines for resting electrocardiograms consisting of nine domains: the presence of a Q wave, QRS axis deviation, high-amplitude R waves, ST segment depression, T-wave abnormalities, AV conduction defects, ventricular conduction defects, arrhythmias, and a miscellaneous items domain (including low QRS amplitude, ST segment elevation, pathologic QRS transition zone, and high P or T wave).[12] The QT interval was also manually assessed and corrected according to the Bazett formula (QTc = QT time/√RR interval). An ECG was positive for CAD if a Q wave, ST segment depression, and/or a pathologic T wave was present. All ECG features were analyzed only if the ECG was considered of sufficient quality to be interpreted.
Statistical analysis
The Shapiro–Wilk test was used to assess the normal distribution of data. Due to their asymmetric distribution, differences between groups were tested by the Mann–Whitney’s U-test and Kruskal–Wallis test, followed by the Conover test for multiple comparisons. All calculations used IBM-SPSS® version 26.0 (IBM Corp., Armonk, NY, USA, 2019). A two-sided P < 0.05 was considered statistically significant.
RESULTS
All the data are presented as mean ± SD and are detailed in the tables. The three groups were similar in age; however, the BMI was significantly higher in the sedentary group compared to the other groups. Standard echocardiographic parameters were within the normal range for all groups [Table 1]. Higher values, particularly concerning left ventricle dimensions and LV-indexed mass [Figure 2], were observed in triathletes, reflecting an advanced level of training. Diastolic parameters were within the normal range for all subjects investigated. Distinctions were however noted in trained athletes compared to the other groups, although all values were within the normal range.
Table 1.
Principal echocardiographic two-dimensional parameters
| Sedentary - 14 male; 10 female (n=25), mean±SD (95% CI) | Normal (HS) - 18 male; 4 female, (n=24), mean±SD (95% CI) | Triathletes - 17 male; 5 female, (n=22), mean±SD (95% CI) | P | |||||
|---|---|---|---|---|---|---|---|---|
| Age (years) | 42.0±15.7 (43.8–57.7) | 40.0±14.9 (33.7–45.7) | 35.0±11.0 (14.7–24.7) | NS | ||||
| BMI (kg/m2) | 27.2±5.7 (24.6–31.3) | 22.9±2.6 (22.2–24.2) | 22.1±1.8 (21.8–23.8) | <0.001§ | ||||
| LVDd (mm) | 48.5±3.7 (45.3–49.3) | 49.4±3.4 (47.1–50.32) | 49.3±3.4 (49.5–52.7) | NS | ||||
| LVSd (mm) | 30.9±3.9 (28.1–32.8) | 29.9±4.3 (28.2–31.7) | 30.9±5.7 (29.6–34.1) | NS | ||||
| LV IVS (mm) | 9.1±0.1 (8.6–9.7) | 9.0±0.7 (8.7–9.3) | 9.7±0.7 (9.3–10.1) | NS | ||||
| LVPW (mm) | 9.5±1.3 (8.8–10.2) | 8.9±0.8 (8.5–9.2) | 9.5±0.5 (9.2–9.8) | NS | ||||
| EF (%) | 68.1±6.8 (64.5–71.8) | 67.2±5.9 (64.9–69.6) | 62.7±5.1 (59.9–65.5) | NS | ||||
| LVI mass (g/m2) | 79.5±15.7 (69.8–87.9) | 87.6±15 (81.6–93.6) | 96.9±14.9 (102.4–117.4) | 0.003* | ||||
| TAPSE (mm) | 23.1±3.4 (16.2–28.8) | 24±4.3 (22.3–25.7) | 26.8±5 (15.3–21.1) | 0.02* | ||||
| E/A | 1.3±0.5 (0.9–1.5) | 1.6±0.6 (1.4–1.9) | 1.9±0.4 (2.0–3.2) | 0.001§ | ||||
| DT (ms) | 195.6±37.5 (189.3–223.3) | 200.6±40.8 (184.3–216.9) | 197.2±34.7 (166.9–216.1) | NS | ||||
| IVRT | 64.2±27 (53.8–74.5) | 78.2±30.7 (65.9–90.5) | 63.1±26.9 (52.1–74.1) | NS | ||||
| E1 (cm/s) | 0.10±0.02 (0.8–0.10) | 0.12±0.03 (0.07–0.16) | 0.11±0.03 (0.9–0.15) | NS | ||||
| A1 (cm/s) | 0.09±0.02 (0.8–0.11) | 0.08±0.02 (0.07–0.10) | 0.08±0.01 (0.7–0.9) | NS | ||||
| E/eʹ septum | 6.6±1.5 (6.1–7.2) | 6.15±2.09 (5.3–7) | 7.33±1.24 (6.8–7.8) | 0.03* |
*Significance with P<0.05 between sedentary < triathletes, §Significance with P<0.001 between sedentary < triathletes. BMI=Body mass index, LVDd=Left ventricle diastolic diameter, LVSd=Left ventricle systolic diameter, LV IVS=Left ventricle interventricular septum thickness, LVPW=Left ventricle posterior wall, EF=Ejection fraction, LVI mass=Left ventricle indexed mass, TAPSE=Tricuspid annular plane systolic excursion, E/A=E wave/A wave ratio, DT=Deceleration time, IVRT=Isovolumetric relaxation time, E1=E1 wave, A1=A1 wave, E/E1=E/E1 ratio, NS=Nonsignificant, SD=Standard deviation, HS=Healthy subjects, CI=Confidence interval
Figure 2.
Cardiac mass index (CMI) in the three groups: CMI resulted higher in triathletes compared to others
On the other hand, specific deformation parameters such as GLS and Twist exhibited higher values in the triathletes’ group, demonstrating significant differences and better performance compared to the other two groups [Figure 3]. This finding is well-documented in the literature as an expression of high myocardial performance [Table 2]. Significant differences in energetic parameters (kinetic energy fluctuation and vorticity fluctuation) measured from the HyperDoppler analysis were also observed in highly trained athletes (T) compared to healthy subjects (HS) and sedentary (S) groups. A distinctive trend was identified for the Energy Dissipation parameter (ED in triathletes 1.10 ± 0.41 > HS 0.78 ± 0.24 > S 0.54 ± 0.24) in the absence of geometrical modifications of the flow pattern. This aspect can suggest an independent marker of an athlete’s heart. On the contrary, no substantial differences were found among the LV HyperDoppler geometrical flow data [Figures 2 and 3].
Figure 3.
Global longitudinal strain (GLS) (a) and twist (b) of left ventricular (LV): The left graph (a) reports the GLS of the LV in the three groups that resulted in more negative in triathletes (3rd group); the right graph (b) showing the twist values of the LV in the three groups; triathletes have higher values
Table 2.
Deformation and vortex analysis by speckle tracking and HyperDoppler model
| Sedentary, mean±SD (95% CI) | HS, mean±SD (95% CI) | Triathletes, mean±SD (95% CI) | P | |||||
|---|---|---|---|---|---|---|---|---|
| GLS (%) | −17.08±7.87 (−20.1–14.1) | −18.76±2.34 (−19.7–17.8) | −20.09±3.01 (−21.3–18.7) | <0.05* | ||||
| Twist | 8.1±3.2 (6.8−9.3) | 9.8±3.6 (8.4−11.3) | 12.18±3.6 (10.7−13.7) | <0.001§ | ||||
| Vortex | ||||||||
| Area (cm2) | 0.22±0.60 (0.19–0.24) | 0.23±0.07 (0.2–0.25) | 0.29±0.36 (0.15–0.45) | NS | ||||
| Depth (mm) | 0.28±0.07 (0.25–0.31) | 0.34±0.13 (0.29–0.39) | 0.27±0.06 (0.25–0.3) | NS | ||||
| Length (mm) | 0.53±0.15 (0.47–0.59) | 0.40±0.33 (0.27–0.54) | 0.50±0.07 (0.47–0.53) | NS | ||||
| Intensity | −0.32±0.09 (−0.35–0.28) | −0.34±0.19 (−0.42–0.27) | −0.30±0.06 (−0.32–0.28) | NS | ||||
| ED | 0.54±0.24 (0.45–0.63) | 0.78±0.24 (0.68–0.88) | 1.10±0.41 (0.93–1.26) | <0.000 | ||||
| Fluctuation | 0.76±0.09 (0.72–0.79) | 0.83±0.07 (0.8–0.86) | 0.89±0.04 (0.87–0.91) | <0.000 | ||||
| Kinetic energy fluctuation | 0.91±0.12 (0.87–0.96) | 0.94±0.13 (0.89–0.99) | 1.01±0.08 (0.98–1.05) | <0.009 | ||||
| Shear stress fluctuation | −0.38±0.28 (−0.49–0.27) | −0.43±0.12 (−7.1–1.8) | −0.48±0.10 (−0.57–0.35) | NS |
*Significance with P<0.05 between sedentary < triathletes, §Significance with P<0.001 between sedentary < triathletes. GLS=Global longitudinal strain, NS=Nonsignificant, SD=Standard deviation, HS=Healthy subjects, CI=Confidence interval, ED=Energy dissipation
DISCUSSION
Progressive myocardial remodeling, particularly in highly trained athletes, has been a focal point of interest in sports medicine. Accurately defining and identifying an athlete’s heart often proves to be crucial, especially in cases of increased wall thickness. While standard and deformation echocardiographic parameters support the identification of normal cardiac function, they may not always be exhaustive in pinpointing the gray zone of hypertrophy, particularly in elite athletes. The combined measurement of myocardial remodeling with the flow vortex pattern helps detect potential structural cardiac disease. Magnetic resonance imaging has previously described the visualization of vortex paths related to the asymmetric function of the myocardial walls. The sinuous flow inside the heart and the eventual asymmetric arrangement have been elegantly described in specific studies by the MRI method.[5,13] More recently, a new noninvasive model, by echocardiographic method, can offer information on systolic–diastolic time to detect potential alterations in myocardial structure.[14,15]
In the physiological or pathological adaptation of the heart, with the geometrical modification, the hemodynamic forces event and can evoke or anticipate the cardiac changes. This could contribute to predict the physiological adaptation versus the maladaptive adequation. Studies suggest that intracardiac forces participate in the development of the grown heart.[14] In addition, the eventual directional deviation on intraventricular flow can participate or clarify a diverse energetic dispendium in the myocardial function. From the present investigation, in fact, the energetic parameters result to be significantly higher in trained athletes at elevated intensity. Noninvasive cardiac evaluation of the heart is a widely used technique in sports medicine, especially in decision-making processes to identify an athlete’s heart. Geometrical remodeling of all myocardial chambers, due to regular and high-intensity training, can lead to specific increases in wall thickness and progressive enlargement of the cavities and major torsion representing the athlete’s heart. Despite physiological differences due to various sports, such as dynamic or resistance training, the athlete’s heart is characterized by normal systolic–diastolic function and morphological values at the upper limits of the normal range. A normal diastolic function characterizes the physiological behavior of a trained heart. Studies in sports medicine report as different kinds of training can induce different myocardial remodeling with predominant modification in chamber size or in wall thickness, normally associated with a prevalent aerobic or a counter-resistance exercise. The recent and modern interpretation of these modifications do not recognize an effective different morphology of athlete’s heart.[16] Hence, it seems important to better define the intracardiac characteristics in addition to the well-known modification dedicated to the shape evaluation. Furthermore, other subtle structural conditions, indicating pathological enlargement of ventricular chambers not as a consequence of sports activity, can be misleading. In this context, among the geometrical and kinetic parameters calculated by vortex analysis, the potential increase in ED due to the physiological myocardial remodeling associated with a higher heart contraction has not yet been investigated.
Therefore, using additional parameters in echocardiography to identify this trend early to an extreme condition seems necessary. In addition to deformation parameters, a new approach to studying flow dynamic modifications due to geometrical and energy activity in athletes is important.
The combination of geometrical and energetic parameters in the left ventricular (LV) chamber could be helpful in better identifying the athlete’s heart. From the obtained results, comparing these data in three different groups at different levels of training highlights the energetic HyperDoppler as a specific marker of workload when associated with normal systolic function. Since HyperDoppler analysis has been primarily studied in the diastolic phase, in this investigation, especially the energetic parameters seem to be related to a major systolic function.[17] This hypothesis is supported by the strain data, which demonstrate a behavior substantially similar to the ED. This aspect could reasonably be used in cases of the gray zone of myocardial hypertrophy, where preserved systolic function needs to be demonstrated to clarify any suspicions of fibrosis or disarranged fibers’ presence.
Physiological changes of left and right myocardial chambers, especially in elite athletes due to high training, are associated with increased performance.[18] Noninvasive methods are preferred and largely used to define myocardial remodeling; the deformation parameters are often involved. Vortex ring formation is a prominent feature of intracardiac flow and is known to differ between healthy and failing hearts. This aspect has been investigated by authors in the context of heart failure and HyperDoppler analysis has been also proposed in the selection of responsive to cardiac resynchronization therapy[5,10,19,20,21,22] The validity and reliability of the HyperDoppler technique have been investigated, and a normal behavior of flow dynamics within the left ventricular (LV) has been demonstrated. Literature increasingly suggests a broader application of this method in specific categories of athletes.[17]
CONCLUSION
Considering that the LV EF can be different among athletes and that the Strain pattern is not associated with a specific cardiac remodeling, Vortex analysis can be considered an adequate method to estimate the cardiac working regimen.
HyperDoppler could be proposed to investigate specific heart efficiency parameters. From the results obtained, the energetic data (ED and fluctuation) are particularly indicative of the athlete’s heart remodeling. However, the exact range has not been universally defined in the athlete’s heart, excluding a few experiences. This investigation aims to contribute to this aspect. The potential clinical application of this method in cardiology sports medicine could have an impact, especially in the suspected cases in which the negative evidence of structured diseases by the MRI exam needs additional information. It is reasonable to hypothesize that vortex formation could be a prominent feature of intracardiac flow parameters to distinguish subjects with a higher heart performance, to reduce the doubts in the initial phase of a structural heart failing, or to confirm the physiological remodeling of a trained heart. Inside a hypothetical large involvement of the HyperDoppler, many other studies will be necessary to combine the systolic and diastolic phase analysis in diverse physiological or pathological cardiac adaptations. The results obtained suggest this hypothesis. However, they have not been studied in this investigation. In conclusion, despite the potentially interesting application of the method in cardiac sports medicine, necessity of specific expertise, and sophisticated elaboration in the postprocessing analysis, can represent the main disadvantage for an imminent significant diffusion.
Ethical statement
Ethical review and approval were waived for this study due to availability of the data in the website of the Center, as consequence they are regularly followed for the sports medicine evaluation. Informed consent was obtained from all subjects involved in the study.
Conflicts of interest
There are no conflicts of interest.
Funding Statement
Nil.
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