Skip to main content
Download PDF

Effect of maximum exercise on left ventricular deformation and its correlation with cardiopulmonary exercise capacity in competitive athletes

Echo Research & Practice volume 10, Article number: 17 (2023) Cite this article

Abstract

Background

Global longitudinal strain (GLS) and global myocardial work index (GWI) allow early detection of subclinical changes in left ventricular (LV) systolic function. The aim of the study was to investigate the immediate effects of maximum physical exercise by different exercise testing methods on early post exercise LV deformation parameters in competitive athletes and to analyze their correlation with cardiopulmonary exercise capacity.

Methods

To reach maximum physical exercise, cardiopulmonary exercise testing (CPET) was performed by semi-recumbent ergometer in competitive handball players (n = 13) and by treadmill testing in competitive football players (n = 19). Maximum oxygen uptake (VO2max) indexed to body weight (relative VO2max) was measured in all athletes. Transthoracic echocardiography and blood pressure measurements were performed at rest and 5 min after CPET in all athletes. GLS, GWI and their changes before and after CPET (ΔGLS, ΔGWI) were correlated with (relative) VO2max.

Results

In handball and football players, GLS and GWI did not differ significantly before and after CPET. There were no significant correlations between GLS and relative VO2max, but moderate correlations were found between ΔGWI and relative VO2max in handball (r = 0.631; P = 0.021) and football players (r = 0.592; P = 0.008). Furthermore, handball (46.7 ml/min*kg ± 4.7 ml/min*kg vs. 37.4 ml/min*kg ± 4.2; P = 0.004) and football players (58.3 ml/min*kg ± 3.7 ml/min*kg vs. 49.7 ml/min*kg ± 6.8; P = 0.002) with an increased ΔGWI after CPET showed a significant higher relative VO2max.

Conclusion

Maximum physical exercise has an immediate effect on LV deformation, irrespective of the used testing method. The correlation of relative VO2max with ΔGWI in the early post exercise period, identifies ΔGWI as an echocardiographic parameter for characterizing the current individual training status of athletes.

Introduction

In competitive athletes, transthoracic echocardiography (TTE) is a widely used noninvasive imaging modality that allows the assessment of left ventricular (LV) systolic function by LV ejection fraction (EF) and by LV deformation analysis by speckle tracking [1, 2].

Global longitudinal strain (GLS) is defined as the percentage longitudinal shortening (change in length compared to baseline length) during systole. GLS allows early detection of subclinical myocardial damage, e.g., due to myocardial fibrosis [3,4,5,6,7,8]. Normal GLS values range from − 16.0 to − 22.0%. Unfortunately GLS is significantly affected by afterload conditions [9].

A relatively new echocardiographic approach involves the assessment of non-invasive pressure strain loops (PSL). The global myocardial work index (GWI) is a modern echocardiographic parameter which is based on PSL and combines myocardial deformation imaging using 2D speckle tracking with non-invasive afterload determination using brachial cuff blood pressure measurement [10]. Values of GWI will automatically be calculated by the respective program after speckle tracking analyses have been performed and blood pressure values have been entered. Russell et al. repeatedly demonstrated that loop areas by invasively measured LV pressure and speckle-tracking echocardiography were identical compared with the non-invasive method by estimated LV pressure and speckle-tracking echocardiography [10]. GWI has proven to be afterload-independent and related to myocardial deformation and contractile function [11, 12]. For this reason, GWI might offer advantages over GLS in athletes exposed to different afterload conditions during exercise. Normal values of GWI range from 1900 to 2100 mmHg% [9]. In contrast to LVEF, GLS and GWI have been shown to be reliable in distinguishing between physiological adaption (e.g., LV hypertrophy due to exercise) and pathological changes (e.g., hypertrophic cardiomyopathy) in the athletes’ heart [13, 14].

Cardiopulmonary exercise testing (CPET) is an established method to characterize the pulmonary, vascular, musculoskeletal, and cardiac system in competitive athletes. Maximum oxygen uptake (VO2max) is considered the international standard for determining physical capacity [15, 16]. CPET can be helpful to assess and optimize the athlete’s current training condition [17,18,19]. Since VO2max is highly dependent on the athlete’s body type, it is often indexed to body weight (relative VO2max). In addition to the athlete’s body type, age, gender, and sport type also appear to have a significant impact on VO2max. In healthy males aged 18 and 30 years, a mean relative VO2max of 48 ml/min*kg has been reported [20].

In general CPET is performed using a cycle ergometer or treadmill [21, 22]. The cycle ergometer is well applicable in patients with unfavorable conditions (e.g., obesity, joint issues, deconditioning) and allows convenient intra-test procedures (ECG, blood pressure, blood sampling) due to less movement artefacts. Treadmill ergometry is more susceptible to movement artefacts, yet it allows running at predefined speed and incline, activates more muscle groups and can lead to higher levels of peak oxygen uptake [22, 23].

The objective of the present study was to investigate the effect of maximum physical exercise by different testing methods on LV deformation in competitive athletes and to analyze the relationship between cardiopulmonary exercise capacity and LV deformation parameters. We hypothesized that the effect of maximum physical exercise on LV deformation does not differ between the two testing methods and GWI can be used as a surrogate parameter for VO2max.

Methods

Study population and study design

The study population (n = 32) was composed of competitive handball (n = 13) and football (n = 19) players from the first handball and football division in Germany. Handball and football players were considered separately because of differences in body size and constitution. Furthermore, the test modalities at the corresponding centers were different, so that this division seemed reasonable. Due to their different physical constitution and the cardiovascular demands resulting from different types of exercise. All athletes provided informed consent after full explanation of the purpose and order of all procedures. The study was conducted in accordance with the Declaration of Helsinki and was approved by the ethical committee of the University of Leipzig (073/18-ek).

All athletes were enrolled in the outpatient clinic of cardiology from May until July 2020 (handball players) and in July 2021 (football players). They were tested for SARS-CoV-2 and had a negative PCR test taken at most 48 h before the examination. All athletes were asymptomatic and completely free of cardiovascular diseases or risk factors. A physical examination including vital parameters was performed in all subjects. Further, an electrocardiogram at rest, incremental CPET, and TTE (before and 5 min after CPET) were performed. Blood pressure was assessed by non-invasive brachial cuff measurement in supine position at rest and 5 min after CPET simultaneously with the acquisition of apical views by TTE. The examination protocol of the athletes (semi-recumbent vs. treadmill testing) was set by the respective sports federations. Logistic procedures of CPET and TTE examinations were limited by the surrounding conditions at the corresponding centers. The workflow after completion of CPET and before the beginning of post-exercise TTE was supervised by two non-medical assistants. TTEs were performed by two physicians with two ultrasound machines, so that the post-exercise TTE could be performed as soon as possible in all athletes, within a maximum of 5 min. Some restructuring was necessary with the aim of performing both TTE (at rest and after CPET) in a standardized manner under the same conditions in left lateral position to avoid methodological effects on LV deformation, e.g., effects of changes in position (upright posture vs. left lateral position). Image acquisition of post-exercise TTE was focused on strain measurements, so that cineloops of apical, midventricular, and basal parasternal short-axis views, a LVOT Doppler spectrum for timing of aortic valve opening (AVO) and closure (AVC) all three standardized apical views were acquired within a maximum of 3 min. Each sequence was documented 3 times. Thus, the acquisition time of these 19 cineloops averaged 2 min.

Incremental cardiopulmonary exercise test for handball players

CPET was performed on a semi-recumbent ergometer (GE eBike, GE Healthcare GmbH, Solingen, Germany) at a constant speed of 60–70 revolutions per minute (rpm). The semi-supine angle was about 45° without lateral rotation in all handball players. The test started at a workload of 50W with an increase of 50W every 3 min until volitional exhaustion occurred. Each subject continued for an additional 5-min recovery period at a workload of 25W. In the CPET, ergospirometry data were collected using a digital spirometer (Vyntus™ CPX, Vyaire Germany, Hoechberg, Germany). Absolut and relative oxygen consumption (VO2max) were assessed to characterize the respiratory function of athletes. VO2max, minute ventilation (VE), and heart rate (HR) (GE Cardiosoft, GE Healthcare GmbH, Solingen, Germany) were monitored continuously at rest, during CPET, and during recovery. In addition to VO2max the individual fitness index for weight-independent comparisons of athletes’ cardiopulmonary exercise capacity was calculated by the following: absolute VO2max/(weight0,73) [24].

Incremental cardiopulmonary exercise test for football players

Run performance diagnostics were performed on a treadmill (HP Cosmos, Traunstein, Germany) to determine VO2max (Comsed, Rome, Italy), peak performance (Ppeak), maximum heart rate (HRmax), and lactate threshold (LT), as well as running economy and fractional utilization of VO2max at LT. The testing protocol contained a 2-phase test consisting of an incremental, sub-maximal exercise test (phase 1) followed by a ramp test (phase 2) interspersed with an 8 min break (4 min active walking at 4 km/h followed by 4 min passive rest) [25].

Athletes started the incremental test at 8.0 km/h at a treadmill incline of 0%. The test was completed when (i) blood lactate has increased by ≥ 1 mmol/L compared to the previous stage, (ii) Borg value was > 17 (on the 6–20 scale), (iii) the respiratory exchange ratio was > 1.0 in two consecutive stages. Criteria (ii) and (iii) were introduced to prevent athletes who do not achieve a blood lactate increase of ≥ 1 mmol/L from becoming prematurely exhausted before the upcoming ramp protocol. The last stage was terminated when the result of the blood lactate level of the previous stage was displayed and was ≥ 1 mmol/L compared with the penultimate stage (generally 1 to 1.5 min). The start speed of the ramp test and the speed of LT determined in the incremental test (equal to the speed of the stage before the lactate increase of ≥ 1 mmol/L) were increased by 1 km/h every minute until voluntary exhaustion.

Transthoracic echocardiography

TTE was performed using a Vivid E9 or E95 ultrasound system with a 4Vc phased array probe (GE Healthcare Vingmed Ultrasound AS, Horten, Norway). Post-processing analyses were performed with the EchoPac software (Version 203, GE Healthcare Vingmed Ultrasound AS, Horten, Norway). LV morphology was characterized by LV dimensions (M-Mode) including LV length, relative wall thickness (RWT), LV mass (LVM) (by the Devereux formula), and LV mass index (LVMi) according to current recommendations [26]. LV systolic function was characterized by LVEF based on LV end-diastolic (LVEDV) and end-systolic volume (LVESV) assessed by LV biplane planimetry by the modified Simpson’s rule in the apical 2- and 4-chamber view as well as by Cardiac Index (CI) (by Doppler echocardiography) [27]. Myocardial deformation was characterized by GLS using 2D speckle tracking analysis of the apical long axis-, 2-, and 4-chamber-view according to current recommendations [3, 4, 28]. The endocardial contour was manually adjusted, whereas only segments with accurate tracking were accepted. Tracking areas were manually adjusted to enable full myocardial tracking.

Additionally, GWI was calculated by using the longitudinal strain analysis of the apical LV long axis-, 2-, and 4-chamber-view coupled with the noninvasive blood pressure measurements to attain a pressure-strain loop of the LV [10]. This analysis was performed by post-processing using EchoPac software. In all athletes, the change in GLS (ΔGLS) and GWI (ΔGWI) was calculated by the difference between pre and post CPET values.

Diastolic function was characterized by maximum blood flow velocities (Vmax) of E- and A-wave, E/A-ratio, myocardial Vmax of e′ and a′ of the basal septal and lateral mitral annulus, septal and lateral E/e′-ratio (including average E′/e′-ratio (septal and lateral)) and systolic pulmonary artery pressure (sPAP) according to current recommendations [29]. In all athletes three cardiac cycles were assessed according to current literature [30].

Statistical analysis

All statistical analyses were performed using SPSS Statistics (version 24.0, IBM, Armonk, NY) and Microsoft Office Excel (version 16.53, Microsoft). Continuous variables were expressed as mean value ± standard deviation (SD). Further, percentage changes after CPET compared to resting conditions were stated. In consideration of the small sample size, we decided to forgo distribution analyses. Statistical significance was accepted for P value < 0.05. Student’s t-test was used to compare the echocardiographic results before and after CPET.

Pearson correlation coefficient r was used to test the correlation between different echocardiographic parameters at rest, after CPET and for the percentage change of each parameter after CPET compared to resting conditions: r ≤ 0.5 (poor correlation), r = 0.5–0.7 (moderate correlation) and r ≥ 0.7 (good correlation).

Intra- and interobserver variabilities of main echocardiographic parameters (LV volumes, LVEF, GLS, CI, sPAP) were assessed in randomly selected athletes (n = 10). The second investigator used the same datasets, and both were blinded to each other’s results.

Results

Baseline characteristics of handball and football players are shown in Table 1.

Table 1 Baseline characteristics
Full size table

Semi-recumbent ergometer

Left ventricular volumes were significantly lower after physical exertion compared to resting conditions (Table 2). Left ventricular ejection fraction was similar before and after CPET (Table 2). E/A-ratio was significantly decreased after physical exertion, mainly due to a reduction of the A-wave (Table 3). Myocardial early (e′) diastolic tissue velocities were significantly lower, although this did not lead to a reduction of E/e′, mainly due to consistent passive diastolic filling velocities (E-wave) (Table 3). After CPET sPAP was still in normal ranges.

Table 2 Conventional echocardiographic parameters of left ventricular morphology and function
Full size table
Table 3 Parameters of left ventricular diastolic and right ventricular function
Full size table

Global longitudinal strain (− 18.8 ± 1.6% vs. − 18.1 ± 1.7%; P = 0.079) and GWI did not differ before and after CPET (1838 ± 316 mmHg% vs. 1975 ± 223 mmHg%; P = 0.197). Specifically, GWI increased in eight and decreased in five handball players after CPET (Fig. 1). Athletes with an increase in GWI after CPET showed higher relative VO2max values (46.7 ml/min*kg ± 4.7 ml/min*kg vs. 37.4 ml/min*kg ± 4.2; P = 0.004) (Fig. 1). Athletes with a decrease in GWI after CPET had the lowest relative VO2max values (Fig. 1). At maximum physical exercise VO2max was 4214 ± 489 ml/min and relative VO2max was 43.1 ± 6.4 ml/min*kg. Calculated fitness index was 149 ± 20 ml/min*kg.

Fig. 1
figure 1

Relative VO2max in competitive handball (A1) and football players (B1) with increased (↑) global myocardial work index (GWI) after cardiopulmonary exercise test (CPET) compared to the athletes with decreased GWI (↓). The correlation between the change of GWI (ΔGWI) after CPET with relative VO2max as a surrogate parameter for cardiopulmonary exercise capacity in competitive handball (A2) and football players (B2)

Full size image

No correlation with VO2max or relative VO2max was shown for GLS at rest, after CPET, and ΔGLS. In contrast, there was a correlation between GWI after CPET and VO2max (r = 0.631; P = 0.021), ΔGWI and VO2max (r = 0.762; P = 0.002), as well as ΔGWI and relative VO2max (r = 0.671; P = 0.012; Table 4).

Table 4 Correlations between left ventricular deformation and cardiopulmonary exercise capacity
Full size table

Treadmill testing

Left ventricular volumes were significantly lower after physical exertion compared to resting conditions (Table 2). Left ventricular ejection fraction was similar before and after CPET (Table 2). E/A-ratio and E/e′ were significantly lower after CPET (Table 2). sPAP was in normal ranges before and after CPET.

Global longitudinal strain (− 18.3 ± 1.7% vs. − 17.7 ± 1.6%; P = 0.119) and GWI did not differ before and after CPET (1899 ± 281 mmHg% vs. 1963 ± 370 mmHg%; P = 0.461). GWI increased in 11 and decreased in eight football players after CPET (Fig. 1). Athletes with an increase in GWI after CPET showed higher relative VO2max values (58.3 ml/min*kg ± 3.7 ml/min*kg vs. 49.7 ml/min*kg ± 6.8; P = 0.002) (Fig. 1). At maximum physical exercise VO2max was 4306 ± 594 ml/min and relative VO2max was 54.7 ± 6.5 ml/min*kg. Calculated fitness index was 178 ± 20 ml/min*kg.

No correlation with VO2max or relative VO2max was shown for GLS at rest, after CPET, and ΔGLS. However, GWI after CPET and relative VO2max (r = 0.459; P = 0.048) as well as ΔGWI and relative VO2max (r = 0.592; P = 0.008) showed moderate correlations (Table 4).

Intra- and interobserver variabilities

Intraobserver variabilities of GLS measurements were 2.16% at rest (P = 0.638) and 2.61% after CPET (P = 0.491). Interobserver variabilities of GLS measurements were 3.91% at rest (P = 0.337) and 4.23% after CPET (P = 0.312). Intra- and interobserver variabilities for LV volumes, LVEF, CI, and sPAP measurements were < 5% without reaching statistical significance.

Discussion

The main findings of the present study are: (1) GLS and GWI did not differ significantly before and after semi-recumbent ergometer and treadmill testing. (2) There was no significant correlation between GLS and (relative) VO2max, but (3) there were significant correlations between ΔGWI and relative VO2max in semi-recumbent ergometer and treadmill testing.

Baseline echocardiographic parameters

Changes of conventional echocardiographic parameters after CPET (e.g. LV volumes), were in line with the results of previous studies and have already been described [31]. Both, low intra- and interobserver variabilities highlight the quality of data acquisition as well as the robustness of conventional but also deformation parameters, e.g. GLS [7].

Impact of maximum exercise on early post exercise global longitudinal strain

The impact of pre- and afterload conditions on LV systolic function has already been described [32]. In general data analyzing the impact of physical stress on LV deformation are scarce and the results of previous studies are highly heterogeneous. Some previous clinical studies have proven a significant impact of pre- and afterload conditions on GLS [33,34,35,36]. Nevertheless, GLS was not able to predict load-independent contractility in a porcine model [37]. The impact of different CPET methods on global longitudinal strain in competitive athletes has not been described before.

Liang et al. assessed GLS in 15 swimming athletes before and after high-intensity exercise, where GLS was significantly lower after high-intensity exercise [38]. The decrease of GLS was explained by negative effects on myocardial cells based on anaerobic glycolysis due to ischemia, hypoxia, and the formation of lactic acid with a reduction of myocardial contraction force and consequently, a decrease of LV myocardial contractile function [39]. These results were in contrast to Gruca et al., where GLS was significantly increased in 69% of 111 male elite basketball players in the first minute after maximum physical exertion due to treadmill testing [40]. The increase of GLS at peak exercise was explained by a lower baseline and peak HR, which could not be observed in our study. Neither athletes on semi-recumbent ergometer and treadmill showed significant correlations with HR or differences of mean GLS before and after CPET. Mean GLS was slightly lower after both, semi-recumbent ergometer, and treadmill testing, but did not reach statistical significance. This finding can be explained by higher blood pressure after CPET and consequently higher afterload conditions which was already described in an experimental pig model of aortic banding [36]. It needs to be considered that athletes of different sports are exposed to different forms of physical exercise, and these in turn also have different effects on the cardiovascular system especially on LV remodeling. However, the results of our study are consistent with those of Santoro et al. where GLS was assessed in 27 male water polo players and did not differ significantly before and after 6 repetitions of 100-m freestyle swimming sets [41].

Whereas Gianturco et al. demonstrated a very strong correlation between VO2max and GLS in a cohort of 20 soccer referees and proposed GLS as a specific parameter to assess football referees performance [42], there was no significant correlation between VO2max and GLS in our study. The lack of correlation between GLS and VO2max does not allow conclusions to be drawn about cardiopulmonary exercise capacity based on GLS values in male handball and football players.

The discrepancy between the results of Gianturco et al. and our study is not fully comprehensible. A possible explanation could be the different training conditions between the football referees and the competitive athletes in this study. In addition the measurements of LV deformation were performed by a different vendor compared to this study. Ünlü et al. previously showed that different vendors have a significant impact on tracking feasibility [43].

Impact of maximum exercise on early post exercise global myocardial work index

Global myocardial work index has proven to be a reliable method for assessing LV function and enables to detect subtle myocardial changes. In noninvasive estimation of LV pressure, GWI based on the pressure strain loop incorporates the current afterload condition and is able to assess LV mechanical function and the myocardial oxygen consumption [44].

Sengupta et al. assessed GWI in 24 recreational athletes before as well as up to a maximum of 2 and 72 h after completing a marathon and found either a decrease in GWI or no change in GWI [45]. A decrease of GWI was attributed to differences in HR and lower LV filling volumes. According to the results of the present study, both aspects could also be observed in professional athletes immediately after CPET, because TTE was performed 5 min after CPET in the present study. GWI has proved to be afterload-independent permitting a more comprehensive assessment of LV systolic function [12], which is beneficial in athletes exposed to different physical exercise. Although systolic blood pressure as a surrogate parameter for afterload conditions was increased in all athletes after CPET. In this study, irrespective of the CPET method, mean GWI did not differ before and after CPET and an individual increase or decrease in GWI was observed in each athlete. This finding lead to the assumption that LV deformation is significantly affected by maximum exercise, whereas the method of exercise testing, semi-recumbent ergometer, or treadmill, does not make a difference.

Correlation between VO2max and GWI

Tokodi et al. described a moderate correlation between CPET-derived relative VO2max and GWI at rest in a cohort of 20 elite swimmers [46], which was not observed in our study. However, there was a significant correlation between relative VO2max and ΔGWI in both cohorts. This observation can be explained by the fact that well-trained athletes with higher fitness levels show a pronounced increase in GWI after CPET according to their relative VO2max, whereas a decrease in GWI after CPET seems to be associated with a lower cardiopulmonary exercise capacity. An explanation for this correlation could be, that athletes with a higher VO2max presumably express higher myocardial load to facilitate the larger oxygen uptake. It can be assumed that ΔGWI can be considered as a surrogate parameter to assess the current training condition of athletes.

Limitations

The number of subjects was limited by the size of the teams in the German handball and football Bundesliga studied at Leipzig University Hospital. However, these highly selected young and healthy competitive athletes highlight the exceptionality of the present cohort. Therefore, the results are not directly applicable to patients with cardiovascular disease. Both semi-recumbent ergometer and treadmill testing could not be performed in all athletes due to their limited time schedule for testing. For the most standardized image acquisition possible, TTE was performed in handball and football players 5 min after CPET and not at maximum exercise. In addition, the determination of LV deformation parameters by 2D speckle tracking analyses is often erroneous at very high heart rates, so that most likely some LV segments would not have been tracked reliably. The modality of incremental cardiopulmonary exercise test was predetermined by the respective medical team leader.

Conclusion

VO2max is considered an important indicator of athlete’s training condition and maximum performance capacity. In the present study we confirmed that maximum exercise has a significant effect on LV deformation, irrespective of the exercise method.

Further, we were able to demonstrate a significant correlation between ΔGWI and VO2max directly after CPET, so that the current training condition or maximum performance capacity of an athlete might also be estimated by a single modern imaging parameter instead of only VO2max. Further studies are needed to clarify whether athletes who demonstrate a decrease in GWI and a lower VO2max after CPET have a higher performance potential and thus their maximal performance capacity can be further improved. If so, GWI could be used as a modern imaging parameter to characterize the athletes’ maximum performance capacity, which would considerably enrich and simplify individual performance diagnostics.

Availability of data and materials

The authors confirm that the data supporting the findings of this study are available within the article.

References

  1. Mitchell C, Rahko PS, Blauwet LA, Canaday B, Finstuen JA, Foster MC, Horton K, Ogunyankin KO, Palma RA, Velazquez EJ. Guidelines for performing a comprehensive transthoracic echocardiographic examination in adults: recommendations from the American Society of Echocardiography. J Am Soc Echocardiogr. 2019;32:1–64.

    PubMed  Google Scholar 

  2. Grazioli G, Sanz M, Montserrat S, Vidal B, Sitges M. Echocardiography in the evaluation of athletes. F1000Res. 2015;4:151.

    PubMed  PubMed Central  Google Scholar 

  3. Voigt JU, Pedrizetti G, Lysyansky P, Marwick TH, Houle HC, Baumann R, et al. Definitions for a common standard for 2D speckle tracking echocardiography: consensus document of the EACVI/ASE/Industry Task Force to standardize deformation imaging. Eur Heart J Cardiovasc Imaging. 2015;16:1–11.

    CAS  PubMed  Google Scholar 

  4. Mor-Avi V, Lang RM, Badano LP, Belohlavek M, Cardim NM, Derumeaux G, Galderisi M, Marwick T, Nagueh SF, Sengupta PP, Sicari R, Smiseth OA, Smulevitz B, Takeuchi M, Thomas JD, Vannan M, Voigt J-U, Zamorano JL. Current and evolving echocardiographic techniques for the quantitative evaluation of cardiac mechanics: ASE/EAE consensus statement on methodology and indications endorsed by the Japanese Society of Echocardiography. J Am Soc Echocardiogr. 2011;24:277–313.

    PubMed  Google Scholar 

  5. Tops LF, Delgado V, Marsan NA, Bax JJ. Myocardial strain to detect subtle left ventricular systolic dysfunction: LV systolic dysfunction and GLS. Eur J Heart Fail. 2017;19:307–13.

    PubMed  Google Scholar 

  6. Biering-Sørensen T, Biering-Sørensen SR, Olsen FJ, Sengeløv M, Jørgensen PG, Mogelvang R, Shah AM, Jensen JS. Global longitudinal strain by echocardiography predicts long-term risk of cardiovascular morbidity and mortality in a low-risk general population: The Copenhagen City Heart Study. Circ Cardiovasc Imaging. 2017;10: e005521.

    PubMed  PubMed Central  Google Scholar 

  7. Cheng S, Larson MG, McCabe EL, Osypiuk E, Lehman BT, Stanchev P, Aragam J, Benjamin EJ, Solomon SD, Vasan RS. Reproducibility of speckle-tracking-based strain measures of left ventricular function in a community-based study. J Am Soc Echocardiogr. 2013;26:1258-1266.e2.

    PubMed  Google Scholar 

  8. Kouris NT, Kostopoulos VS, Psarrou GA, Kostakou PM, Tzavara C, Olympios CD. Left ventricular ejection fraction and Global Longitudinal Strain variability between methodology and experience. Echocardiography. 2021;38:582–9.

    PubMed  Google Scholar 

  9. Truong VT, Vo HQ, Ngo TNM, Mazur J, Nguyen TTH, Pham TTM, Le TK, Phan H, Palmer C, Nagueh SF, Chung ES. Normal ranges of global left ventricular myocardial work indices in adults: a meta-analysis. J Am Soc Echocardiogr. 2021;S0894–7317(21):00826–9.

    Google Scholar 

  10. Russell K, Eriksen M, Aaberge L, Wilhelmsen N, Skulstad H, Remme EW, Haugaa KH, Opdahl A, Fjeld JG, Gjesdal O, Edvardsen T, Smiseth OA. A novel clinical method for quantification of regional left ventricular pressure–strain loop area: a non-invasive index of myocardial work. Eur Heart J. 2012;33:724–33.

    PubMed  PubMed Central  Google Scholar 

  11. Hubert A, Le Rolle V, Leclercq C, Galli E, Samset E, Casset C, Mabo P, Hernandez A, Donal E. Estimation of myocardial work from pressure–strain loops analysis: an experimental evaluation. Eur Heart J Cardiovasc Imaging. 2018;19:1372–9.

    PubMed  Google Scholar 

  12. Chan J, Edwards NFA, Khandheria BK, Shiino K, Sabapathy S, Anderson B, Chamberlain R, Scalia GM. A new approach to assess myocardial work by non-invasive left ventricular pressure–strain relations in hypertension and dilated cardiomyopathy. Eur Heart J Cardiovasc Imaging. 2019;20:31–9.

    PubMed  Google Scholar 

  13. Bewarder Y, Lauder L, Kulenthiran S, Schäfer O, Ukena C, Percy Marshall R, Hepp P, Laufs U, Stöbe S, Hagendorff A, Böhm M, Mahfoud F, Ewen S. Global longitudinal strain differentiates physiological hypertrophy from maladaptive remodeling. IJC Heart Vasc. 2022;40: 101044.

    Google Scholar 

  14. BorziÌ D, Saladino S, Losi V, Faro D, Monte I. Strain and myocardial work index during echo exercise to evaluate myocardial function in athletes. J Cardiovasc Echogr. 2022;32:82.

    Google Scholar 

  15. Glaab T, Taube C. Practical guide to cardiopulmonary exercise testing in adults. Respir Res. 2022;23:9.

    PubMed  PubMed Central  Google Scholar 

  16. Rapp D, Scharhag J, Wagenpfeil S, Scholl J. Reference values for peak oxygen uptake: cross-sectional analysis of cycle ergometry-based cardiopulmonary exercise tests of 10 090 adult German volunteers from the Prevention First Registry. BMJ Open. 2018;8: e018697.

    PubMed  PubMed Central  Google Scholar 

  17. Petek BJ, Gustus SK, Wasfy MM. Cardiopulmonary exercise testing in athletes: expect the unexpected. Curr Treat Options Cardio Med. 2021;23:49.

    Google Scholar 

  18. Fleg JL, Piña IL, Balady GJ, Chaitman BR, Fletcher B, Lavie C, Limacher MC, Stein RA, Williams M, Bazzarre T. Assessment of functional capacity in clinical and research applications: an advisory from the Committee on Exercise, Rehabilitation, and Prevention, Council on Clinical Cardiology, American Heart Association. Circulation. 2000;102:1591–7.

    CAS  PubMed  Google Scholar 

  19. Fletcher GF, Balady G, Froelicher VF, Hartley LH, Haskell WL, Pollock ML. Exercise standards: a statement for healthcare professionals from the American Heart Association. Circulation. 1995;91:580–615.

    CAS  PubMed  Google Scholar 

  20. Shvartz E, Reibold RC. Aerobic fitness norms for males and females aged 6 to 75 years: a review. Aviat Space Environ Med. 1990;61:3–11.

    CAS  PubMed  Google Scholar 

  21. Albouaini K, Egred M, Alahmar A, Wright DJ. Cardiopulmonary exercise testing and its applicationThis is a reprint of a paper that appeared in Heart , October 2007, Volume 93, pages 1285–92. Reprinted with kind permission of the authors and publisher. Postgraduate Med J. 2007;83:675–682.

  22. Datta D, Normandin E, ZuWallack R. Cardiopulmonary exercise testing in the assessment of exertional dyspnea. Ann Thorac Med. 2015;10:77.

    PubMed  PubMed Central  Google Scholar 

  23. O’Donnell DE, Elbehairy AF, Faisal A, Webb KA, Neder JA, Mahler DA. Exertional dyspnoea in COPD: the clinical utility of cardiopulmonary exercise testing. Eur Respir Rev. 2016;25:333–47.

    PubMed  PubMed Central  Google Scholar 

  24. Jensen K, Johansen L, Secher NH. Influence of body mass on maximal oxygen uptake: effect of sample size. Eur J Appl Physiol. 2001;84:201–5.

    CAS  PubMed  Google Scholar 

  25. Stöggl TL, Blumkaitis JC, Strepp T, Sareban M, Simon P, Neuberger EWI, Finkenzeller T, Nunes N, Aglas L, Haller N. The Salzburg 10/7 HIIT shock cycle study: the effects of a 7-day high-intensity interval training shock microcycle with or without additional low-intensity training on endurance performance, well-being, stress and recovery in endurance trained athletes—study protocol of a randomized controlled trial. BMC Sports Sci Med Rehabil. 2022;14:84.

    PubMed  PubMed Central  Google Scholar 

  26. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Rietzschel ER, Rudski L, Spencer KT, Tsang W, Voigt J-U. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2015;28:1-39.e14.

    PubMed  Google Scholar 

  27. Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, et al. Recommendation for cardiac chamber quantification by echocardiography in adults: an up-date from the American Society of Echocardiography and the European Association of Cardi-ovascular Imaging. Eur Heart J Cardiovasc Imaging. 2015;16:233–70.

    PubMed  Google Scholar 

  28. Thomas JD, Badano LP. EACVI-ASE-industry initiative to standardize deformation imaging: a brief update from the co-chairs. Eur Heart J Cardiovasc Imaging. 2013;14:1039–40.

    PubMed  Google Scholar 

  29. Nagueh SF, Smiseth OA, Appleton CP, Byrd BF, Dokainish H, Edvardsen T, et al. Recommendations for the evaluation of left ventricular diastolic function by echocardiog-raphy: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr. 2016;29:277–314.

    PubMed  Google Scholar 

  30. Jozwiak M, Mercado P, Teboul J-L, Benmalek A, Gimenez J, Dépret F, Richard C, Monnet X. What is the lowest change in cardiac output that transthoracic echocardiography can detect? Crit Care. 2019;23:116.

    PubMed  PubMed Central  Google Scholar 

  31. Nixon PGF. Human circulation regulation during physical stress. L. B. Rowell. Oxford University Press, London, 1986. No. of pages: 416. Price: £35.00. Stress Med 1988;4:124–125.

  32. Zimmer H-G. Who discovered the frank-starling mechanism? Physiology. 2002;17:181–4.

    Google Scholar 

  33. Nafati C, Gardette M, Leone M, Reydellet L, Blasco V, Lannelongue A, Sayagh F, Wiramus S, Antonini F, Albanèse J, Zieleskiewicz L. Use of speckle-tracking strain in preload-dependent patients, need for cautious interpretation! Ann Intensive Care. 2018;8:29.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Roy C, Duclos G, Nafati C, Gardette M, Lopez A, Pastene B, Gaudray E, Boussuges A, Antonini F, Leone M, Zieleskiewicz L. Left ventricular longitudinal strain variations assessed by speckle-tracking echocardiography after a passive leg raising maneuver in patients with acute circulatory failure to predict fluid responsiveness: a prospective, observational study. PLoS ONE. 2021;16: e0257737.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Carasso S, Cohen O, Mutlak D, Adler Z, Lessick J, Reisner SA, Rakowski H, Bolotin G, Agmon Y. Differential effects of afterload on left ventricular long- and short-axis function: insights from a clinical model of patients with aortic valve stenosis undergoing aortic valve replacement. Am Heart J. 2009;158:540–5.

    PubMed  Google Scholar 

  36. Donal E, Bergerot C, Thibault H, Ernande L, Loufoua J, Augeul L, Ovize M, Derumeaux G. Influence of afterload on left ventricular radial and longitudinal systolic functions: a two-dimensional strain imaging study. Eur J Echocardiogr. 2009;10:914–21.

    PubMed  Google Scholar 

  37. Dahle GO, Stangeland L, Moen CA, Salminen P-R, Haaverstad R, Matre K, Grong K. The influence of acute unloading on left ventricular strain and strain rate by speckle tracking echocardiography in a porcine model. Am J Physiol Heart Circul Physiol. 2016;310:H1330–9.

    Google Scholar 

  38. Liang C, Ma Y, Gao C, Zhang J, Yang M, Chen G, Fu S, Zhu T. Two-dimensional strain echocardiography technology for evaluation of myocardial strain in swimming athletes after high-intensity exercise. Echocardiography. 2017;34:169–75.

    PubMed  Google Scholar 

  39. Scharhag J, Herrmann M, Urhausen A, Haschke M, Herrmann W, Kindermann W. Independent elevations of N-terminal pro–brain natriuretic peptide and cardiac troponins in endurance athletes after prolonged strenuous exercise. Am Heart J. 2005;150:1128–34.

    CAS  PubMed  Google Scholar 

  40. Gruca MM, Cheema B, Garg G, Ryan J, Thomas JD, Rigolin VH, Zielinski AR, Puthumana JJ. Strain echocardiography to describe left ventricular function pre- and postexercise in elite basketball athletes: a feasibility study. Echocardiography. 2021;38:1165–72.

    PubMed  Google Scholar 

  41. Santoro A, Alvino F, Antonelli G, Cameli M, Bertini M, Molle R, Mondillo S. Left ventricular strain modifications after maximal exercise in athletes: a speckle tracking study. Echocardiography. 2015;32:920–7.

    PubMed  Google Scholar 

  42. Gianturco L, Bodini B, Gianturco V, Lippo G, Solbiati A, Turiel M. Left ventricular longitudinal strain in soccer referees. Oncotarget. 2017;8:39766–73.

    PubMed  PubMed Central  Google Scholar 

  43. the EACVI-ASE-Industry Standardization Task Force, chaired by, the participating companies, Ünlü S, Mirea O, Bézy S, Duchenne J, Pagourelias ED, Bogaert J, Thomas JD, Badano LP, Voigt J-U. Inter-vendor variability in strain measurements depends on software rather than image characteristics. Int J Cardiovasc Imaging. 2021;37:1689–97.

    Google Scholar 

  44. Takaoka H, Takeuchi M, Odake M, Yokoyama M. Assessment of myocardial oxygen consumption (Vo2) and systolic pressure-volume area (PVA) in human hearts. Eur Heart J. 1992;13:85–90.

    PubMed  Google Scholar 

  45. Sengupta S, Jain R, Burkule N, Olet S, Khandheria BK. Myocardial work index: a novel method for assessment of myocardial function in south Asian Recreational Athletes. J Patient Centered Res Rev. 2020;7:147–56.

    Google Scholar 

  46. Tokodi M, Oláh A, Fábián A, Lakatos BK, Hizoh I, Ruppert M, Sayour AA, Barta BA, Kiss O, Sydó N, Csulak E, Ladányi Z, Merkely B, Kovács A, Radovits T. Novel insights into the athlete’s heart: is myocardial work the new champion of systolic function? Eur Heart J Cardiovasc Imaging. 2022;23:188–97.

    PubMed  Google Scholar 

Download references

Funding

Open Access funding enabled and organized by Projekt DEAL.

Author information

Author notes

  1. J. Kandels and S. Stöbe contributed equally to this work.

  2. S. Fikenzer and A. Hagendorff contributed equally to this work.

Authors and Affiliations

  1. Klinik und Poliklinik für Kardiologie, Universitätsklinikum Leipzig, Liebigstr. 20, 04103, Leipzig, Germany

    J. Kandels, S. Stöbe, A. Kogel, U. Rudolph, U. Laufs, S. Fikenzer & A. Hagendorff

  2. Klinik und Poliklinik für Orthopädie, Unfallchirurgie Und Plastische Chirurgie, Universitätsklinikum, 04103, Leipzig, Germany

    P. Hepp

  3. RasenBallsport Leipzig GmbH, Cottaweg 3, 04177, Leipzig, Germany

    H. Riepenhof & R. P. Marshall

  4. Center for Rehabilitation and Sports Medicine, BG Klinikum Hamburg, 21033, Hamburg, Germany

    H. Riepenhof & J. N. Droste

  5. Red Bull Athlete Performance Center, 5303, Salzburg, Austria

    J. N. Droste & T. Stoeggl

  6. Department of Sport and Exercise Science, Universität Salzburg, 5020, Salzburg, Austria

    T. Stoeggl

  7. Department of Orthopedic and Trauma Surgery, Martin-Luther-University Halle-Wittenberg, 06120, Halle, Germany

    R. P. Marshall

Authors
  1. J. Kandels
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. S. Stöbe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Kogel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Hepp
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. H. Riepenhof
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. J. N. Droste
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. T. Stoeggl
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. R. P. Marshall
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. U. Rudolph
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. U. Laufs
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. S. Fikenzer
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. A. Hagendorff
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AH, JK and SF designed the study. AH and SS performed all the echocardiographic examinations. JK and SS analysed the data. AK performed the statistics. JK and SS wrote the manuscript. The rest of the authors provided critical feedback and helped shape the research, analysis and manuscript.

Corresponding author

Correspondence to J. Kandels.

Ethics declarations

Ethics approval and consent to participate

All athletes provided informed consent to participate and publish after full explanation of the purpose and order of all procedures. The study was conducted in accordance with the Declaration of Helsinki and was approved by the ethical committee of the University of Leipzig (073/18-ek).

Competing interests

The authors have nothing to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kandels, J., Stöbe, S., Kogel, A. et al. Effect of maximum exercise on left ventricular deformation and its correlation with cardiopulmonary exercise capacity in competitive athletes. Echo Res Pract 10, 17 (2023). https://doi.org/10.1186/s44156-023-00029-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s44156-023-00029-6

Keywords

Echo Research & Practice

ISSN: 2055-0464

Contact us