ArticlePDF Available

Characterisation of LV myocardial exercise function by 2-D strain deformation imaging in elite adolescent footballers

Authors:

Abstract and Figures

Purpose Few data exist on the descriptions of LV myocardial mechanics and reserve during dynamic exercise of adolescent athletes. The aim of this study was to describe the LV myocardial and cardiopulmonary changes during exercise using 2-D strain deformation imaging. Methods Elite adolescent male football players (n = 42) completed simultaneous cardiopulmonary exercise testing (CPET) and exercise echocardiography measurement of LV myocardial deformation by 2-D strain imaging. LV longitudinal and circumferential 2-D strain and strain rates were analyzed at each stage during incremental exercise to a work rate of 150 W. Additionally, exercise LV myocardial deformation and its relation to metabolic exercise parameters were evaluated at each exercise stage and in recovery using repeated measures ANOVA, linear regression and paired t tests. Results LV peak systolic baseline 2-D strain (longitudinal: − 15.4 ± 2.5%, circumferential: − 22.5 ± 3.1%) increased with each exercise stage, but longitudinal strain plateaued at 50 W (mean strain reserve − 7.8 ± 3.0) and did not significantly increase compared to subsequent exercise stages (P > 0.05), whilst circumferential strain (mean strain reserve − 11.6 ± 3.3) significantly increased (P < 0.05) throughout exercise up to 150 W as the dominant mechanism of exercise LV contractility increase. Regression analyses showed LV myocardial strain increased linearly relative to HR, VO2 and O2 pulse (P < 0.05) for circumferential deformation, but showed attenuation for longitudinal deformation. Conclusion This study describes LV myocardial deformation dynamics by 2-D strain and provides reference values for LV myocardial strain and strain rate during exercise in adolescent footballers. It found important differences between LV longitudinal and circumferential myocardial mechanics during exercise and introduces a methodology that can be used to quantify LV function and cardiac reserve during exercise in adolescent athletes.
Content may be subject to copyright.
Vol.:(0123456789)
1 3
European Journal of Applied Physiology (2021) 121:239–250
https://doi.org/10.1007/s00421-020-04510-6
ORIGINAL ARTICLE
Characterisation ofLV myocardial exercise function by2‑D strain
deformation imaging inelite adolescent footballers
GuidoE.Pieles1,2,3 · LucyGowing1· DianeRyding4· DavePerry4· StevenR.McNally4· A.GrahamStuart2·
CraigA.Williams1
Received: 6 June 2019 / Accepted: 19 September 2020 / Published online: 8 October 2020
© The Author(s) 2020
Abstract
Purpose Few data exist on the descriptions of LV myocardial mechanics and reserve during dynamic exercise of adolescent
athletes. The aim of this study was to describe the LV myocardial and cardiopulmonary changes during exercise using 2-D
strain deformation imaging.
Methods Elite adolescent male football players (n = 42) completed simultaneous cardiopulmonary exercise testing (CPET)
and exercise echocardiography measurement of LV myocardial deformation by 2-D strain imaging. LV longitudinal and
circumferential 2-D strain and strain rates were analyzed at each stage during incremental exercise to a work rate of 150W.
Additionally, exercise LV myocardial deformation and its relation to metabolic exercise parameters were evaluated at each
exercise stage and in recovery using repeated measures ANOVA, linear regression and paired t tests.
Results LV peak systolic baseline 2-D strain (longitudinal: −15.4 ± 2.5%, circumferential: −22.5 ± 3.1%) increased with
each exercise stage, but longitudinal strain plateaued at 50W (mean strain reserve −7.8 ± 3.0) and did not significantly
increase compared to subsequent exercise stages (P > 0.05), whilst circumferential strain (mean strain reserve −11.6 ± 3.3)
significantly increased (P < 0.05) throughout exercise up to 150W as the dominant mechanism of exercise LV contractility
increase. Regression analyses showed LV myocardial strain increased linearly relative to HR, VO2 and O2 pulse (P < 0.05)
for circumferential deformation, but showed attenuation for longitudinal deformation.
Conclusion This study describes LV myocardial deformation dynamics by 2-D strain and provides reference values for
LV myocardial strain and strain rate during exercise in adolescent footballers. It found important differences between LV
longitudinal and circumferential myocardial mechanics during exercise and introduces a methodology that can be used to
quantify LV function and cardiac reserve during exercise in adolescent athletes.
Keywords Exercise stress echocardiography· Ventricular function· Myocardial reserve· Training· Adolescent athletes
Abbreviations
CPET Cardio-pulmonary exercise testing
EF Ejection faction
FFR Force–frequency relationship
Fps Frames per second
FS Fractional shortening
GET Gas exchange threshold
IVSd Interventricular septal diastolic diameter
LV Left ventricle
LVIDd Left ventricular internal diastolic diameter
LVIDs Left ventricular internal systolic diameter
Communicated by Massimo Pagani.
This article is published as part of the Special Issue on Assessment
of cardiovascular function during human activities.
* Guido E. Pieles
guido.pieles@bristol.ac.uk
1 Institute ofSport Exercise andHealth (ISEH), University
College London, LondonW1T7HA, UK
2 Bristol Congenital Heart Centre, The Bristol Heart Institute,
University Hospitals Bristol NHS Foundation Trust, Upper
Maudlin Street, BristolBS28BJ, UK
3 National Institute forHealth Research (NIHR)
Cardiovascular Biomedical Research Centre, Bristol Heart
Institute, Upper Maudlin Street, BristolBS28BJ, UK
4 Manchester United Football Club, Football Medicine
andScience Department, AON Training Complex, Birch
Road, Carrington, ManchesterM314BH, UK
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
240 European Journal of Applied Physiology (2021) 121:239–250
1 3
LVPWd Left ventricular posterior wall diastolic
diameter
Sc Circumferential peak systolic strain
SCD Sudden cardiac death
Sl Longitudinal peak systolic strain
SRc Circumferential peak systolic strain rate
SRl Longitudinal peak systolic strain rate
VO2peak Peak oxygen consumption
W Watts
2-D strain 2-Dimensional strain
Introduction
The adaptation of left ventricular (LV) morphology to ath-
letic training in adults has been well described in several
seminal publications and meta-analyses (Morganroth etal.
1975; Nishimura etal. 1980; Maron 1986; Utomi et al.
2013). But few data exist on the adaptation of the LV in the
rapidly increasing population of adolescent athletes. Where
available, studies in adolescent athletes have concentrated
on LV morphology and cardiac functional adaptations at
rest (Sharma etal. 2002; Makan etal. 2005; Di Paolo etal.
2012; Pela etal. 2016, McClean etal. 2017). Like adult ath-
letes, adolescent athletes are also at risk of sudden cardiac
death (SCD) (Malhotra etal. 2018). Importantly, 33–56% of
SCD events in young athletes occur with exertion (Roberts
etal. 1980; Epstein etal. 1986; Harmon etal. 2011; Chandra
etal. 2013), but the underlying pathophysiological mecha-
nisms are poorly understood, in part, because imaging data
describing LV physiology during exercise in particular in
adolescents are still rare. Exercise stress echocardiography
has recently, however, been shown to differentiate physi-
ological LV functional adaptive processes from myocardial
disease, where function decreases, in adult athletes (La Ger-
che etal. 2013; Sanz-de la Garza etal. 2017) and it has also
been shown to unmask cardiac dysfunction that is not detect-
able at rest in the paediatric and adolescent congenital heart
disease population (Roche etal. 2011, Roche etal. 2014). No
studies have so far described LV myocardial response during
exercise in adolescent athletes. The gold standard methodol-
ogy for LV myocardial performance assessment, also during
exercise, is contractility assessment by end-systolic elastance
using conductance catheters, which is an invasive technique
(Izawa etal. 1996; Inagaki etal. 1999). To overcome this
problem and particularly important in the paediatric popula-
tion, myocardial deformation imaging by 2-D strain during
exercise has recently been shown to present a more practical
alternative. Furthermore, proof of principle studies including
reference values for 2-D strain during exercise in non-athlete
adolescents have recently become available (Boissiere etal.
2013; Pieles etal. 2015; Cifra etal. 2016).
2D strain imaging, including measurement of peak sys-
tolic strain and strain rate, is less load-dependent than other
classic echocardiographic techniques of LV function, such
as ejection fraction (Weidemann etal. 2002a, b). These con-
siderations are paramount when assessing LV function dur-
ing exercise with its significant pre- and after-load changes,
additionally 2-D strain imaging shows angle independency,
which is important to counteract significant translational
heart movement during exercise. Importantly, 2-D strain at
rest has been shown to differentiate adaptive from maladap-
tive processes in adult athletes (Kansal etal. 2011). The
application of 2-D strain imaging during exercise stress
echocardiography is, therefore, an appropriate methodol-
ogy to enhance current practice in quantitatively assessing
myocardial function and reserve in adolescent athletes.
One further challenge that remains is to integrate cardiac
exercise function to the measurement of other organ sys-
tems. Cardio-pulmonary exercise testing (CPET) is the gold
standard (Astrand 1971; Paridon etal. 2006) and has been
used in diagnosis, risk stratification and outcome prediction
in children and adults with cardiac disease (Rhodes etal.
2010; Guazzi etal. 2012). However, a major limitation of
CPET is that it does not provide direct data on exercise-
related changes in myocardial function or cardiac reserve
(Bassett and Howley 2000). Simultaneous measurement of
cardiac performance by 2-D strain echocardiography and
metabolic exercise response by CPET can, thus, overcome
this limitation and a pilot study from our group has shown
its suitability in healthy adolescent volunteers (Pieles etal.
2015). Therefore, the aim of this study was to utilise the
integrated methodology of exercise echocardiography with
CPET to describe LV myocardial exercise response in rela-
tion to exercise metabolism during strenuous exercise in
adolescent elite footballers.
Methods
Participants
Forty-two healthy elite male players from an English Pre-
mier League football academy (mean age 15.4 ± 1.7 y,
stature 172.2 ± 9.7cm, body mass 58.7 ± 11.0kg, BMI
19.6 ± 2.1kgm2, lean body mass 47.2 ± 7.5kg, body surface
area 1.69 ± 0.20m2), volunteered to participate in this pro-
spective cohort study and prior to participation, parent/carer
and adolescents duly signed a consent form and/or an assent
form, respectively. UK National Research Ethics Service
(NRES) approval was obtained. Participants were screened
for cardiac disease by pre-participation questionnaire physi-
cal examination, 12-lead ECG and resting echocardiography.
National elite training status was defined as consisting of
a minimum of 12h per week training and game time and
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
241European Journal of Applied Physiology (2021) 121:239–250
1 3
selection, actively participating in competition including
international tournaments and possessing a contract into the
clubs elite training programme (Araujo and Scharhag 2016).
Cardio‑pulmonary exercise testing
An incremental CPET on a recumbent cycle ergometer
(Ergosana GMBH, Bitz, Germany) positioned at a 45°
inclination (25W∙3min−1 increments) was performed to
volitional exhaustion at a pedaling frequency of 70 ± 5rpm.
Exercise stages of 3min were used to obtain a steady state
and enough time to obtain echocardiographic data. Ventila-
tion volume and expired gas composition were measured
breath-by-breath using a metabolic cart (Metalyzer II, Cor-
tex, Leipzig, Germany) with calibration, measurement and
analysis of metabolic gas parameters during exercise and
recovery performed as described previously (Pieles etal.
2015). Participants were requested to avoid strenuous exer-
cise for at least 12h preceding each visit and to arrive at the
laboratory in a rested and hydrated state 2h after a meal.
Echocardiography
Prior to exercise stress testing, participants underwent a full
structural and functional resting (baseline) echocardiogram
following international paediatric guidelines (Lai etal.
2006, Lopez etal. 2010). Echocardiographic measurements
and analysis were performed using an Artida machine and
a 2.0–4.8MHz transducer and UltraExtendV3.2 software
(Canon Medical Systems, Japan). LV diameters were meas-
ured from two-dimensional (2-D) echocardiography in the
parasternal short axis view at the base of the LV. Ejection
fraction (EF) was calculated using the Simpson 2-D biplane
method.
2‑D myocardial strain analysis
A parasternal short axis and LV focused apical 4-chamber
view were captured for 2-D strain analysis. Three cardiac
cycles were acquired at rates of 60–100 frames per second
(Fps), analysis was performed on one manually selected
cardiac cycle. The endocardial borders were manually con-
toured at end-systole with the range of interest adjusted to
include the whole myocardium. Mean peak systolic longitu-
dinal (Sl) and circumferential (Sc) strain were defined as the
maximal deformation value of a segment during systole in
the endocardial segment and is represented as a percentage
(%); mean peak systolic strain rate (SR) was defined as the
maximal rate of deformation of a segment in systole over
time and is expressed in 1/s (Voigt etal. 2015). Circumferen-
tial peak systolic strain was measured at the base of the LV.
Mean values for circumferential and longitudinal strain were
calculated for each stage only if good tracking was obtained
in a minimum of four segments. Image acquisition and off-
line analysis were performed by an investigator experienced
in paediatric echocardiography (GEP).
Exercise stress echocardiography
Exercise stress echocardiography and 2-D strain analy-
sis were performed using the same protocol and by the
same internationally accredited operator, as described by
our research group previously (Pieles etal. 2015). Briefly,
focused echocardiography was performed for 2-D strain
analysis during free breathing exercise 60s into each exer-
cise stage at baseline (rest), 0 (unloaded pedaling), 50, 100,
150W and during recovery at 2min (Rec2) and 6min (Rec6)
after end of exercise. The gas exchange threshold (GET),
representing the break point in breath-by-breath values of
carbon dioxide uptake and oxygen uptake was expressed as
a percentage of VO2peak. Myocardial reserve was defined
as the difference in 2-D mean peak systolic strain between
baseline and each exercise stage to up to 150W. Strain val-
ues were not calculated at work rates higher than 150W to
ensure sufficient image quality and frame rate for reliable
strain analysis. Only images with high frame rates of 60–100
Fps were used to ensure capture of sufficient Fps for 2-D
strain analysis at higher heart rates. A minimum of 3 cardiac
cycles were recorded to capture at least one cardiac cycle in
expiration to obtain best image quality, which was confirmed
visually and then used to perform strain analysis (Fig.1).
Statistics
Descriptive statistics (mean and SD) of measured and
derived variables were used to characterize the sample
(Table1). Prior to analyses, diagnostic plots were created to
provide checks for heteroscedasticity, normality and influ-
ential observations (Figs.2, 3). Outliers were identified as
being > 1.5 times the IQR (interquartile range) using box and
whisker plots. Differences between strain and strain rate and
were assessed with repeated measures ANOVA and Least
Significance Difference post hoc test. Strain reserve vari-
ables were assessed using paired t tests to compare between
rest and individual exercise stage only. Development of
myocardial deformation was tested and is described as the
difference between each subsequent exercise stage (Fig.4),
as well as the differences compared to rest (Tables2 and 3).
Relationships between strain parameters and CPET variables
were determined using scatterplots, Pearson’s correlations
and linear regression analysis (Figs.5 and 6). All statistical
analyses were performed using R Core Team (Vienna, Aus-
tria) and using SPSS Statistics Software (Version20.0. IBM
Corp, USA) and GraphPad Prism (Version5.04, La Jolla,
USA). A probability level of P < 0.05 was accepted to indi-
cate statistical significance.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
242 European Journal of Applied Physiology (2021) 121:239–250
1 3
Results
All participants had a structurally and functionally nor-
mal heart. Participants had normal LV dimensions (IVSd
9.7 ± 1.3mm, LVPWd 8.9 ± 1.3mm, LVIDd 44.5 ± 3.8mm,
LVIDs 32 ± 5.8mm) with all individual z scores within ± 2
and normal LV systolic function with a mean FS of 33 ± 3%
and a mean EF of 64 ± 5%. Table1 represents the mean
(SD) CPET data. The exercise duration was 25:44 ± 5:46
(min:s) with a mean peak power output of 211 ± 45W.
Relative VO2peak was 49.1 ± 6.5mL·kg−1·min−1, GET was
129 ± 38W and 69 ± 13% of VO2peak or 33.3mL·kg−1·min−1.
Oxygen consumption and HR as shown in Fig.2 signifi-
cantly increased linearly up to end exercise (P < 0.05).
LV myocardial performance duringexercise—2‑D
strain
Analysis of 2-D LV strain was feasible up to a work
rate of 100W and a mean HR of 134 ± 13 b∙min−1 in
90% of subjects for longitudinal and 98% of subjects for
circumferential strain and to 150W and a mean HR of
161 ± 16 b∙min−1 in 60% of subjects for longitudinal and
88% for circumferential 2-D strain (Table2). Initiation
of exercise (0W) resulted in a significant increase of LV
mean peak systolic longitudinal strain (LV Sl) compared
to baseline (P = 0.001) and this linear increase was main-
tained up to 50W (P = 0.001). A plateauing effect at the
higher power outputs between 50 and 150W was shown
(Fig.4), where inter-stage comparisons were not signif-
icantly different between 50 and 100W (P = 0.06) and
100 and 150W (P = 0.91) (Fig.4.). This plateau effect for
LV Sl corresponded to a VO2peak of between 52 and 75%
(Table1 and Figs.3 and 4) falling into the range, where
GET occurred, specifically 12% and 59% of participants
were at GET at 100W and 150W, respectively. In contrast,
inter-stage comparisons from baseline and exercise stages
up to 150W for LV mean peak systolic circumferential
strain (Sc) showed a linear and significant increase (all
comparisons P = 0.001) (Fig.4). LV Sl and LV Sc showed
a similar profile during the recovery, during immediate
recovery (2min) period decreasing towards baseline level
Fig. 1 Representative 2-D strain images and strain curves for LV Sl (top) and LV Sc (bottom) at baseline (left, HR = 72bpm) and during moder-
ate exercise (right, 100W, HR = 134bpm)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
243European Journal of Applied Physiology (2021) 121:239–250
1 3
to 120% (Sl) and 114% (Sc) of baseline strain, respec-
tively, and continuing this trend to 6min recovery. Impor-
tantly however, values did not reach baseline values at
6min recovery (P < 0.05) (Table2 and 3). Myocardial
reserve measured by 2-D strain was more pronounced in
the circumferential plane, LV Sl reserve was −7.8 ± 3.0
vs −11.6 ± 3.3 for LV Sc reserve (Fig.3). Strain rate (SR)
during exercise increased significantly (P = 0.001) between
most exercise stages for the longitudinal and circumferen-
tial myofibre direction and did not reach a plateau at higher
exercise stages (Table3 and Fig.4). Three comparisons
for longitudinal SR between 0W and 6minrec (P = 0.84)
and 50W and 2minrec (P = 0.65) and circumferential
SR for 0W and 6minrec (P = 0.75) were found not to be
significantly different. Strain rate reserve was significantly
different at all stages compared to baseline (P < 0.001)
(Table3).
Table 1 Baseline, exercise, and recovery cardiopulmonary exercise testing parameters of the athlete cohort (n = 42)
CI is defined as the mean ± 2 standard deviations
Test stage Absolute VO2,
L∙min−1
Relative VO2,
mL∙kg−1∙min−1
Heart rate, b∙min−1 Oxygen pulse,
mL∙beat−1
VO2/VO2peak % Par-
ticipants
(n)
Baseline – 69 ± 11 – 42
0W 0.51 ± 0.10 8.86 ± 1.84 88 ± 11 5.90 ± 1.51 18.0 ± 3.2 42
25W 0.67 ± 0.12 11.71 ± 2.15 97 ±12 7.05 ± 1.70 24.0 ± 4.7 42
50W 0.91 ± 0.10 15.86 ± 2.78 107 ±11 8.55 ± 1.51 32.5 ± 6 42
75W 1.18 ± 0.12 20.64 ± 3.74 120 ± 12 9.91 ± 1.59 42.4 ± 8.6 42
100W 1.44 ± 0.13 25.33 ± 4.71 134 ± 13 10.84 ± 1.50 51.9 ± 10 42
125W 1.75 ± 0.18 30.46 ± 6.59 148 ± 15 11.89 ± 1.65 61.4 ± 11.5 40
150W 2.10 ± 0.26 36.00 ± 7.32 161 ± 16 13.30 ± 2.26 72.5 ± 12 39
175W 2.34 ± 0.23 39.46 ± 7.24 168 ± 13 14.02 ± 1.89 78.5 ± 11.0 34
200W 2.55 ± 0.17 40.40 ± 6.61 173 ± 8 15.02 ± 1.39 81.8 ± 9.2 23
225W 2.91 ± 0.26 42.00 ± 6.13 177 ± 10 17.58 ± 1.20 85.5 ± 10.2 13
250W 3.47 ± 0.51 47.37 ± 6.73 180 ± 13 20.54 ± 0.18 88.5 ± 8.5 4
275W 3.90 ± N/A 50.47 ± N/A 200 ± N/A 19.48 ± N/A 83.4 ± N/A 1
Max exercise 2.46 ± 0.62 49.11 ± 6.54 173 ± 13 13.29 ± 3.04 87.2 ± 7.1 42
2min rec 0.66 ± 0.23 11.25 ± 2.81 109 ± 13 6.09 ± 1.86 23.2 ± 5.3 42
6min rec 0.47 ± 0.21 7.85 ± 2.64 98 ± 12 4.86 ± 1.89 16.1 ± 5.8 42
Fig. 2 Mean (SD) responses of VO2 (left) and HR (right) up to peak
exercise and during recovery for participants. Proportion of partici-
pants that reached the respective work rates are indicated. Filled dots
show statistical difference compared to the subsequent stage at the
P < 0.05 level. Please see also Table1
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
244 European Journal of Applied Physiology (2021) 121:239–250
1 3
Force–Frequency relationship
Figures5 and 6 represent the scatterplot of the relation-
ship between strain, strain rate and chronotropic exercise
response. Both, strain and strain rate increased with HR dur-
ing exercise in a moderate linear relationship, confirming a
positive physiological force–frequency relationship (FFR)
between HR and all investigated strain and strain rate param-
eters (P < 0.001). Sc showed a stronger correlation to heart
rate than Sl (R2 = 0.56 vs 0.31, P < 0.001) (Fig.5). Compared
to strain, strain rate showed a stronger relationship for all
strain rate values (Figs.5 and 6).
Relationship betweenexercise myocardial
performance andmetabolic exercise parameters
LV Sl, LV Sc, LV SRl and LV SRc increased linearly to
absolute and relative VO2 and O2 pulse, the positive rela-
tionships are shown in the scatterplots in Figs.5 and 6. The
strength of the linear relationships was stronger for strain
rate compared to strain and was also stronger for LV Sc
compared to LV Sl for all variables assessed (Figs.5 and 6).
Discussion
In this study, we describe for the first time, the LV myo-
cardial contractile response to exercise in elite adolescent
footballers by 2-D strain imaging. Using a novel approach
piloted previously by our group (Pieles etal. 2015), which
combines 2-D strain imaging with simultaneous metabolic
evaluation using CPET, we investigated the mechanics of LV
contraction under exercise stress, as well as the relationship
of exercise LV function to metabolic exercise parameters.
LV myocardial performance duringexercise
Strain and strain rates at baseline were comparable to pub-
lished reference data in healthy adolescents (Marcus etal.
2011). We found an incremental increase in LV Sl and LV
Sc in response to exercise and in accordance to previous
exercise strain assessment studies in adult elite athletes
(La Gerche etal. 2012). The increase in LV Sc, a param-
eter of myocardial contractility of circumferential myo-
cardiac fibres, was more pronounced and increased more
linearly to 150W whereas LV Sl, which describes contrac-
tility of longitudinal myocardial fibres, reached a plateau
at moderate work rates (50–100W), coinciding with GET
as a possible associated mechanism. The contribution of
circumferential myocardial contractility was more pro-
nounced as shown by a higher absolute strain increase for
circumferential strain over longitudinal strain (−34.0 ± 4%
vs −22.4 ± 4%), as well as a higher circumferential strain
reserve (−11.6 ± 3.3 vs −7.8 ± 3.0) (Figs.3 and 4). This
observation points towards a differential exercise contri-
bution of LV longitudinal and circumferential myocar-
dial fibres with dominance of circumferential myofibre
motion at higher work rates. This is in accordance with
one previous adult study (Stohr etal. 2014) and also con-
firmed by animal studies (Kovacs etal. 2015), that showed
Fig. 3 a Mean LV peak systolic longitudinal strain and circumferen-
tial strain at each exercise stage (baseline to 6min recovery); b Mean
LV peak systolic longitudinal strain and circumferential strain reserve
at each exercise stage (baseline to 6min recovery) showing a plateau-
ing effect for mean peak systolic LV longitudinal strain
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
245European Journal of Applied Physiology (2021) 121:239–250
1 3
recruitment of circumferential myofibres during exercise
confers a higher contractility. This observation is also in
accordance with data from non-athlete adolescents in our
previous study (Pieles etal. 2015). While specific loading
conditions during exercise might to some degree influ-
ence our 2-D strain values (Greenberg etal. 2002), we
validated this result by measuring strain rate (Table3
and Fig.6), which is the least load-dependent parameter
(Ferferieva etal. 2012), and in accordance, absolute cir-
cumferential systolic strain rate increase was also more
pronounced than longitudinal systolic strain (−3.71 ± 0.71
vs −2.05 ± 0.34) as was circumferential strain rate reserve
(−2.51 ± 0.77 vs −1.29 ± 0.37). In contrast to strain, how-
ever, strain rate increased continuously to 150W without a
plateau in both fibre directions. Strain rate has previously
been shown to be the most accurate noninvasive measure-
ment of contractility during dobutamine (Greenberg etal.
2002) and exercise stress (La Gerche etal. 2012) also com-
pared to strain. As a derivative of myocardial velocities,
it is very sensitive and less influenced by pre- and after-
load changes and translational tissue motion changes that
even strain is susceptible to (Greenberg etal. 2002). While
Fig. 4 Myocardial performance response during exercise as meas-
ured by mean LV peak systolic longitudinal (Sl) and circumferential
(Sc) strain and strain rate (SRl, SRc), respectively. Letters above each
stage show statistical significant difference (ANOVA and post-hoc
test) in comparison with the selected exercise stage, such that letters
correspond to: b = 0 W, c = 50W, d = 100W, e = 150W, f = 2min rec
and g = 6min rec; (e.g. in left upper panel at baseline significant dif-
ferences found compared to 0, 50, 100, 150, 2min rec and 6min rec)
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
246 European Journal of Applied Physiology (2021) 121:239–250
1 3
intrinsic myofiber contractile force still increases at higher
exercise stages leading to continuous strain rate increase,
this phenomenon would not have been captured as well by
strain. The plateauing effect of strain values in our study,
can be hypothesized to be a result of the susceptibility of
strain to stroke volume changes (Weidemann etal. 2002a,
b) which has been shown to not alter significantly at near
maximal exercise (Higginbotham etal. 1986). Our previ-
ous data in healthy non-athlete adolescents of similar age
using the same methodology (Pieles etal. 2015) showed
similar development for strain and strain rate.
Table 2 Mean LV peak systolic
longitudinal and LV peak
systolic circumferential strain
response during exercise
P values compare strain parameters at each exercise stage compared to baseline. CI is defined as the
mean ± 2 standard deviations
Test stage Strain value SD Lower CI Upper CI Strain reserve P value Partici-
pants
(n)
LV peak systolic longitudinal strain
Baseline −15.3 2.5 −20.2 −10.3 0 ± 0 – 42
0W −19.9 3.2 −26.3 −13.6 −4.4 ± 2.3 < 0.001 39
50W −21.9 3.3 −28.6 −15.3 −6.6 ± 2.7 < 0.001 40
100W −22.7 3.5 −29.6 −15.7 −7.2 ± 3.2 < 0.001 37
150W −22.5 4.1 −30.7 −14.2 −8 ± 3 < 0.001 19
2min rec −17.9 2.9 −23.7 −12.1 −2.7 ± 2.7 < 0.001 37
6min rec −16.9 2.3 −21.4 −12.3 −1.4 ± 2.5 0.003 38
LV peak systolic circumferential strain
Baseline −22.5 3.1 −28.7 −16.3 0 ± 0 < 0.001 42
0W −26.9 2.8 −32.6 −21.2 −4.1 ± 2.5 < 0.001 40
50W −30.7 3.2 −37.2 −24.3 −8.2 ± 3 < 0.001 42
100W −33.0 3.7 −40.5 −25.6 −10.5 ± 3.4 < 0.001 41
150W −34.3 4.0 −42.3 −26.2 −11.8 ± 3.2 < 0.001 34
2min rec −24.9 3.2 −31.3 −18.5 −2.6 ± 3.3 < 0.001 41
6min rec −22.8 2.6 −28.0 −17.5 −0.4 ± 3.2 < 0.001 41
Table 3 Mean LV peak systolic
longitudinal and LV peak
systolic circumferential strain
rate response during exercise
P values compare strain parameters at each exercise stage compared to baseline. CI is defined as the
mean ± 2 standard deviations
Test stage Strain rate value SD Lower CI Upper CI SR reserve P value Partici-
pants
(n)
LV peak systolic longitudinal strain rate
Baseline −0.84 0.18 −1.21 −0.47 0 ± 0 – 42
0W −1.15 0.26 −1.67 −0.62 −0.3 ± 0.3 < 0.001 41
50W −1.50 0.31 −2.13 −0.87 −0.7 ± 0.3 < 0.001 42
100W −1.76 0.43 −2.62 −0.91 −0.9 ± 0.5 < 0.001 40
150W −2.05 0.34 −2.73 −1.37 −1.3 ± 0.4 < 0.001 14
2min rec −1.44 0.30 −2.04 −0.84 −0.6 ± 0.3 < 0.001 38
6min rec −1.12 0.27 −1.65 −0.58 −0.3 ± 0.3 < 0.001 38
LV peak systolic circumferential strain rate
Baseline −1.26 0.19 −1.64 −0.88 0 ± 0 – 42
0W −1.50 0.29 −2.09 −0.91 −0.2 ± 0.3 < 0.001 40
50W −1.97 0.51 −2.98 −0.95 −0.7 ± 0.6 < 0.001 42
100W −2.47 0.48 −3.42 −1.52 −1.2 ± 0.5 < 0.001 41
150W −3.05 0.94 −4.93 −1.17 −1.8 ± 1 < 0.001 26
2min −1.76 0.41 −2.58 −0.93 −0.5 ± 0.4 < 0.001 40
6min −1.47 0.29 −2.05 −0.90 −0.2 ± 0.3 < 0.001 40
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
247European Journal of Applied Physiology (2021) 121:239–250
1 3
Force–Frequency relationship
Both, strain and strain rate followed the physiological
force–frequency relationship (FFR), a fundamental relation-
ship of healthy myocardium demonstrated in the paediatric
population (Roche etal. 2011), by an incremental increase in
contractility as measured by strain and strain rate in relation
to HR. An abnormal FFR during exercise has recently been
shown in children with heart disease (Roche etal. 2014),
and hence the data on FFR development during exercise
presented here could become a tool to detect early LV dys-
function in adolescent athletes. For athletes in particular, the
detailed description of LV myocardial performance during
exercise is of importance, as reduced 2-D strain and exer-
cise-induced LV dysfunction are early signs in adolescent
and adult subclinical hypertrophic cardiomyopathy (Sakata
etal. 2008; Forsey etal. 2014), which is a major cause of
sudden cardiac death in the athlete population (Malhotra
Fig. 5 Scatterplots representing the increase of LV myocardial performance as measured by mean LV peak systolic longitudinal (Sl) and circum-
ferential (Sc) strain in relation to HR and metabolic exercise parameters
Fig. 6 Scatterplots representing the increase of LV myocardial performance as measured by mean LV peak systolic longitudinal (SRl) and cir-
cumferential (SRc) strain rate in relation to HR and metabolic exercise parameters
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
248 European Journal of Applied Physiology (2021) 121:239–250
1 3
etal. 2018). Hence, the use of 2-D strain during exercise
stress echocardiography has the potential to further increase
the utility of 2-D strain in the early detection of myocardial
disease, in particular in athletes where myocardial disease is
often concealed and remains a diagnostic challenge (Sheikh
etal. 2015).
LV myocardial performance inrecovery
2-D strain values at recovery showed a tendency to return to
baseline values, but showed significant differences between
baseline and recovery (Fig.4 and Table2). Equally, strain
rate, as the best measure of contractility, did not return to
baseline at 2 and 6min recovery (Table3), both strain and
strain rate recovery mechanics indicating a higher myocar-
dial performance demand in the recovery phase. This will
also have been influenced by the higher HR via the described
FFR compared to pre-exercise baseline values (Table1).
We previously described albeit statistically non-significant,
a reduction of 2-D strain during recovery in a non-athlete
adolescent cohort as a reflection of altered myocardial recov-
ery function after maximal exercise (Pieles etal. 2015), but
this was not observed in the athlete cohort, which might
present a specific athletic myocardial adaptation, but would
require a direct comparison study, that was beyond the scope
of this paper.
Myocardial performance andmetabolic exercise
parameters
Study participants showed higher fitness levels with a supe-
rior VO2peak compared to previous published data in age
matched non-athlete adolescents using the same exercise
test methodology (Pieles etal. 2015). Ventricular mechan-
ics are highly dependent not only on HR as discussed above,
but also on exercise intensity, work rate and metabolic state
(Armstrong etal. 2016). We have, therefore, also investi-
gated the relationships between longitudinal and circum-
ferential myocardial performance by strain and strain rate
and absolute and relative VO2 and O2 pulse. Scatterplots
confirmed a linear relationship (Figs.5 and 6) for absolute
and relative VO2 and O2 pulse. Importantly, as R2 values
(Figs.5 and 6) show, there exists a stronger relationship of
absolute and relative VO2 and O2 pulse with Sc compared
to Sl also indicating a dominance of circumferential fibre
shortening during exercise as discussed above. The relation-
ship between strain and O2 pulse found supports the clinical
use of peak O2 pulse as a surrogate parameter for cardiac
function during clinical CPET testing, and vice versa, vali-
dating 2-D strain during exercise as an alternative tool to
more accurately and directly measure LV myocardial func-
tion during clinical exercise testing. Here, Sc might be the
superior parameter over Sl to be used during exercise stress
echocardiography judging by its closer relationship to abso-
lute and relative VO2 and O2 pulse. Further work is needed
to determine if this relationship is different in the setting of
myocardial disease.
Limitations
There are a number of technical challenges when assess-
ing simultaneous echocardiography and CPET that need
to be acknowledged. First is the requirement for a semi-
supine position to acquire satisfactory images resulting in
a position-specific CPET response (Warburton etal. 2002),
which was shown to be feasible and valid in children (May
etal. 2013). Second, as a result of insufficient HR vs frame
rate ratio, 2-D strain measurements were not performed at
the maximal end-exercise stage of the test. Tissue Doppler
imaging with higher acquisition frame rates could theo-
retically overcome this, however, this technique is angle-
dependent and paediatric exercise studies (Cifra etal. 2016)
have not yielded data at maximal exercise intensities. Good
intra- and inter-observer reliability of 2-D strain measure-
ments, paramount during exercise echocardiography (Picano
etal. 1991), using the same hard- and software, protocol and
the same echocardiographer were established in our previous
pilot study (Pieles etal. 2015). The intra- and interobserver
average variance for baseline, exercise, and recovery strain
values there ranged from 0.6 to 8% with and intraclass cor-
relation coefficient (ICC) between r = 0.78 and 0.98 for LV
Sl; from 0.9 to 9.1% with ICC between r = 0.87 and 0.98 for
LV Sc. Our study cohort was extremely homogenous and a
more heterogeneous sample might have provided more sub-
tle inter-subject associations. While this is, to our knowledge
to date, the largest cohort study using 2-D strain exercise
echocardiography in adolescent athletes, further larger stud-
ies will need to be conducted to create large-scale normative
data.
Conclusion
This study characterized the LV myocardial mechanics dur-
ing exercise in elite adolescent athletes using 2-D strain
imaging. It describes the normal response of myocardial
function during exercise and recovery and showed, that there
is a specific response of longitudinal and circumferential
myocardial performance to exercise stress, knowledge that
in the future might help differentiate between adaptive and
maladaptive myocardial function in paediatric athletes and
those with myocardial disease. Additionally, it provides the
first initial reference data for 2-D strain and strain rate val-
ues of the LV during exercise in the healthy adolescent elite
athlete population.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
249European Journal of Applied Physiology (2021) 121:239–250
1 3
Acknowledgements This study was supported by the National Insti-
tute for Health Research (NIHR) Biomedical Research Centre at the
University Hospitals Bristol NHS Foundation Trust and the University
of Bristol. The views expressed in this publication are those of the
author(s) and not necessarily those of the NHS, the National Institute
for Health Research or theDepartment of Health. At the time of the
study, GEP held a NIHR Academic Clinical Lectureship. We would
like to thank the athletes and staff at Manchester United Football Club
Youth Academy for their commitment to this research project. This
study is part of a research partnership between Canon Medical Systems
UK, Manchester United Football Club and the Universities of Bristol.
The research partnership between Canon Medical Systems and the Uni-
versity of Bristol is a contractual research partnership that determines
the independence of the research from either parties’ interests.
Author contributions GEP, CAW and AGS conceived and designed the
research, GEP and CAW conducted experiments, analysed data, wrote
and reviewed the manuscript. All authors edited, read and approved
the manuscript.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict of
interest.
Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
tion, 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://creat iveco mmons .org/licen ses/by/4.0/.
References
Araujo CG, Scharhag J (2016) Athlete: a working definition for medical
and health sciences research. Scand J Med Sci Sports 26(1):4–7
Armstrong C, Samuel J, Yarlett A, Cooper SM, Stembridge M, Stohr
EJ (2016) The effects of exercise intensity vs. metabolic state on
the variability and magnitude of left ventricular twist mechanics
during exercise. PLoS ONE 11(4):e0154065
Astrand PO (1971) Methods of ergometry in children. Definitions,
testing procedures, accuracy and reproduceability. Acta Paediatr
Scand Suppl 217:9–12
Bassett DR Jr, Howley ET (2000) Limiting factors for maximum oxy-
gen uptake and determinants of endurance performance. Med Sci
Sports Exerc 32(1):70–84
Boissiere J, Maufrais C, Baquet G, Schuster I, Dauzat M, Doucende
G, Obert P, Berthoin S, Nottin S (2013) Specific left ventricular
twist-untwist mechanics during exercise in children. J Am Soc
Echocardiogr 26(11):1298–1305
Chandra N, Bastiaenen R, Papadakis M, Sharma S (2013) Sudden car-
diac death in young athletes: practical challenges and diagnostic
dilemmas. J Am Coll Cardiol 61(10):1027–1040
Cifra B, Mertens L, Mirkhani M, Slorach C, Hui W, Manlhiot C, Fried-
berg MK, Dragulescu A (2016) Systolic and diastolic myocardial
response to exercise in a healthy pediatric cohort. J Am Soc
Echocardiogr 29(7):648–654
Di Paolo FM, Schmied C, Zerguini YA, Junge A, Quattrini F, Culasso
F, Dvorak J, Pelliccia A (2012) The athlete’s heart in adolescent
Africans: an electrocardiographic and echocardiographic study. J
Am Coll Cardiol 59(11):1029–1036
Ferferieva V, Van den Bergh A, Claus P, Jasaityte R, Veulemans P,
Pellens M, La Gerche A, Rademakers F, Herijgers P, D’Hooge
J (2012) The relative value of strain and strain rate for defining
intrinsic myocardial function. Am J Physiol Heart Circ Physiol
302(1):H188–195
Forsey J, Benson L, Rozenblyum E, Friedberg MK, Mertens L (2014)
Early changes in apical rotation in genotype positive children with
hypertrophic cardiomyopathy mutations without hypertrophic
changes on two-dimensional imaging. J Am Soc Echocardiogr
27(2):215–221
Greenberg NL, Firstenberg MS, Castro PL, Main M, Travaglini A,
Odabashian JA, Drinko JK, Rodriguez LL, Thomas JD, Garcia MJ
(2002) Doppler-derived myocardial systolic strain rate is a strong
index of left ventricular contractility. Circulation 105(1):99–105
Guazzi M, Adams V, Conraads V, Halle M, Mezzani A, Vanhees L,
Arena R, Fletcher GF, Forman DE, Kitzman DW, Lavie CJ, Myers
J, Eacpr, and Aha (2012) EACPR/AHA Joint Scientific State-
ment. Clinical recommendations for cardiopulmonary exercise
testing data assessment in specific patient populations. Eur Heart
J 33(23):2917–2927
Harmon KG, Asif IM, Klossner D, Drezner JA (2011) Incidence of
sudden cardiac death in National Collegiate Athletic Association
athletes. Circulation 123(15):1594–1600
Higginbotham MB, Morris KG, Williams RS, McHale PA, Coleman
RE, Cobb FR (1986) Regulation of stroke volume during sub-
maximal and maximal upright exercise in normal man. Circ Res
58(2):281–291
Inagaki M, Yokota M, Izawa H, Ishiki R, Nagata K, Iwase M, Yamada
Y, Koide M, Sobue T (1999) Impaired force-frequency relations
in patients with hypertensive left ventricular hypertrophy. A pos-
sible physiological marker of the transition from physiological to
pathological hypertrophy. Circulation 99(14):1822–1830
Izawa H, Yokota M, Nagata K, Iwase M, Sobue T (1996) Impaired
response of left ventricular relaxation to exercise-induced adren-
ergic stimulation in patients with hypertrophic cardiomyopathy. J
Am Coll Cardiol 28(7):1738–1745
Kansal MM, Lester SJ, Surapaneni P, Sengupta PP, Appleton CP,
Ommen SR, Ressler SW, Hurst RT (2011) Usefulness of two-
dimensional and speckle tracking echocardiography in “Gray
Zone” left ventricular hypertrophy to differentiate professional
football player’s heart from hypertrophic cardiomyopathy. Am J
Cardiol 108(9):1322–1326
Kovacs A, Olah A, Lux A, Matyas C, Nemeth BT, Kellermayer D,
Ruppert M, Torok M, Szabo L, Meltzer A, Assabiny A, Birtalan
E, Merkely B, Radovits T (2015) Strain and strain rate by speckle
tracking echocardiography correlate with pressure-volume loop
derived contractility indices in a rat model of athlete’s heart. Am
J Physiol Heart Circ Physiol 00828:02014
La Gerche A, Burns AT, D’Hooge J, Macisaac AI, Heidbuchel H,
Prior DL (2012) Exercise strain rate imaging demonstrates nor-
mal right ventricular contractile reserve and clarifies ambiguous
resting measures in endurance athletes. J Am Soc Echocardiogr
25(3):253–262
La Gerche A, Baggish AL, Knuuti J, Prior DL, Sharma S, Heidbu-
chel H, Thompson PD (2013) Cardiac imaging and stress testing
asymptomatic athletes to identify those at risk of sudden cardiac
death. JACC Cardiovasc Imaging 6(9):993–1007
Lai WW, Geva T, Shirali GS, Frommelt PC, Humes RA, Brook MM,
Pignatelli RH, Rychik J, E. Task Force of the Pediatric Council of
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
250 European Journal of Applied Physiology (2021) 121:239–250
1 3
the American Society of, and E. Pediatric Council of the Ameri-
can Society (2006) Guidelines and standards for performance of
a pediatric echocardiogram: a report from the Task Force of the
Pediatric Council of the American Society of Echocardiography.
J Am Soc Echocardiogr 19(12):1413–1430
Lopez L, Colan SD, Frommelt PC, Ensing GJ, Kendall K, Younoszai
AK, Lai WW, Geva T (2010) Recommendations for quantification
methods during the performance of a pediatric echocardiogram:
a report from the Pediatric Measurements Writing Group of the
American Society of Echocardiography Pediatric and Congenital
Heart Disease Council. J Am Soc Echocardiogr 23(5):465–495
Makan J, Sharma S, Firoozi S, Whyte G, Jackson PG, McKenna WJ
(2005) Physiological upper limits of ventricular cavity size in
highly trained adolescent athletes. Heart 91(4):495–499
Malhotra A, Dhutia H, Finocchiaro G, Gati S, Beasley I, Clift P, Cowie
C, Kenny A, Mayet J, Oxborough D, Patel K, Pieles G, Rakhit D,
Ramsdale D, Shapiro L, Somauroo J, Stuart G, Varnava A, Walsh
J, Yousef Z, Tome M, Papadakis M, Sharma S (2018) Outcomes
of cardiac screening in adolescent soccer players. N Engl J Med
379(6):524–534
Marcus KA, Mavinkurve-Groothuis AM, Barends M, van Dijk A, Feuth
T, de Korte C, Kapusta L (2011) Reference values for myocardial
two-dimensional strain echocardiography in a healthy pediatric
and young adult cohort. J Am Soc Echocardiogr 24(6):625–636
Maron BJ (1986) Structural features of the athlete heart as defined by
echocardiography. J Am Coll Cardiol 7(1):190–203
Maron BJ, Roberts WC, McAllister HA, Rosing DR, Epstein SE (1980)
Sudden death in young athletes. Circulation 62(2):218–229
Maron BJ, Epstein SE, Roberts WC (1986) Causes of sudden death in
competitive athletes. J Am Coll Cardiol 7(1):204–214
May LJ, Punn R, Olson I, Kazmucha JA, Liu MY, Chin C (2013)
Supine cycling in pediatric exercise testing: disparity in perfor-
mance measures. Pediatr Cardiol.
McClean G, Riding NR, Ardern CL, Farooq A, Pieles GE, Watt V,
Adamuz C, George KP, Oxborough D, Wilson MG (2017) Electri-
cal and structural adaptations of the paediatric athlete’s heart: a
systematic review with meta-analysis. Br J Sports Med.
Morganroth J, Maron BJ, Henry WL, Epstein SE (1975) Comparative
left ventricular dimensions in trained athletes. Ann Intern Med
82(4):521–524
Nishimura T, Yamada Y, Kawai C (1980) Echocardiographic evaluation
of long-term effects of exercise on left ventricular hypertrophy and
function in professional bicyclists. Circulation 61(4):832–840
Paridon SM, Alpert BS, Boas SR, Cabrera ME, Caldarera LL, Daniels
SR, Kimball TR, Knilans TK, Nixon PA, Rhodes J, Yetman AT,
C. o. A. H. American Heart Association Council on Cardiovas-
cular Disease in the Young, and Y. Obesity (2006) Clinical stress
testing in the pediatric age group: a statement from the Ameri-
can Heart Association Council on Cardiovascular Disease in the
Young, Committee on Atherosclerosis, Hypertension, and Obesity
in Youth. Circulation 113(15):1905–1920
Pela G, Crocamo A, Li Calzi M, Gianfreda M, Gioia MI, Visioli F, Pat-
toneri P, Corradi D, Goldoni M, Montanari A (2016) Sex-related
differences in left ventricular structure in early adolescent non-
professional athletes. Eur J Prev Cardiol 23(7):777–784
Picano E, Lattanzi F, Orlandini A, Marini C, LAbbate A (1991) Stress
echocardiography and the human factor: the importance of being
expert. J Am Coll Cardiol 17(3):666–669
Pieles GE, Gowing L, Forsey J, Ramanujam P, Miller F, Stuart AG,
Williams CA (2015) The relationship between biventricular myo-
cardial performance and metabolic parameters during incremental
exercise and recovery in healthy adolescents. Am J Physiol Heart
Circ Physiol 309(12):H2067–2076
Rhodes J, Ubeda Tikkanen A, Jenkins KJ (2010) Exercise testing and
training in children with congenital heart disease. Circulation
122(19):1957–1967
Roche SL, Vogel M, Pitkanen O, Grant B, Slorach C, Fackoury C,
Stephens D, Smallhorn J, Benson LN, Kantor PF, Redington AN
(2011) Isovolumic acceleration at rest and during exercise in
children normal values for the left ventricle and first noninvasive
demonstration of exercise-induced force-frequency relationships.
J Am Coll Cardiol 57(9):1100–1107
Roche SL, Grosse-Wortmann L, Friedberg MK, Redington AN, Ste-
phens D, Kantor PF (2014) Exercise echocardiography demon-
strates biventricular systolic dysfunction and reveals decreased
left ventricular contractile reserve in children after tetralogy of
fallot repair. J Am Soc Echocardiogr.
Sakata K, Ino H, Fujino N, Nagata M, Uchiyama K, Hayashi K, Konno
T, Inoue M, Kato H, Sakamoto Y, Tsubokawa T, Yamagishi M
(2008) Exercise-induced systolic dysfunction in patients with non-
obstructive hypertrophic cardiomyopathy and mutations in the
cardiac troponin genes. Heart 94(10):1282–1287
Sanz-de la Garza M, Giraldeau G, Marin J, Grazioli G, Esteve M,
Gabrielli L, Brambila C, Sanchis L, Bijnens B, Sitges M (2017)
Influence of gender on right ventricle adaptation to endurance
exercise: an ultrasound two-dimensional speckle-tracking stress
study. Eur J Appl Physiol 117(3):389–396
Sharma S, Maron BJ, Whyte G, Firoozi S, Elliott PM, McKenna WJ
(2002) Physiologic limits of left ventricular hypertrophy in elite jun-
ior athletes: relevance to differential diagnosis of athlete’s heart and
hypertrophic cardiomyopathy. J Am Coll Cardiol 40(8):1431–1436
Sheikh N, Papadakis M, Schnell F, Panoulas V, Malhotra A, Wilson M,
Carre F, Sharma S (2015) Clinical profile of athletes with hyper-
trophic cardiomyopathy. Circ Cardiovasc Imaging 8(7):e003454
Stohr EJ, Gonzalez-Alonso J, Bezodis IN, Shave R (2014) Left ven-
tricular energetics: new insight into the plasticity of regional con-
tributions at rest and during exercise. Am J Physiol Heart Circ
Physiol 306(2):H225–232
Utomi V, Oxborough D, Whyte GP, Somauroo J, Sharma S, Shave
R, Atkinson G, George K (2013) Systematic review and meta-
analysis of training mode, imaging modality and body size influ-
ences on the morphology and function of the male athlete’s heart.
Heart 99(23):1727–1733
Voigt JU, Pedrizzetti G, Lysyansky P, Marwick TH, Houle H, Baumann
R, Pedri S, Ito Y, Abe Y, Metz S, Song JH, Hamilton J, Sengupta
PP, Kolias TJ, d’Hooge J, Aurigemma GP, Thomas JD, Badano LP
(2015) Definitions for a common standard for 2D speckle track-
ing echocardiography: consensus document of the EACVI/ASE/
Industry Task Force to standardize deformation imaging. J Am
Soc Echocardiogr 28(2):183–193
Warburton DE, Haykowsky MJ, Quinney HA, Blackmore D, Teo KK,
Humen DP (2002) Myocardial response to incremental exercise
in endurance-trained athletes: influence of heart rate, contractility
and the Frank-Starling effect. Exp Physiol 87(5):613–622
Weidemann F, Jamal F, Kowalski M, Kukulski T, D’Hooge J, Bijnens
B, Hatle L, De Scheerder I, Sutherland GR (2002a) Can strain rate
and strain quantify changes in regional systolic function during
dobutamine infusion, B-blockade, and atrial pacing–implications
for quantitative stress echocardiography. J Am Soc Echocardiogr
15(5):416–424
Weidemann F, Jamal F, Sutherland GR, Claus P, Kowalski M, Hatle L,
De Scheerder I, Bijnens B, Rademakers FE (2002b) Myocardial
function defined by strain rate and strain during alterations in
inotropic states and heart rate. Am J Physiol Heart Circ Physiol
283(2):H792–799
Publisher’s Note Springer Nature remains neutral with regard to
jurisdictional claims in published maps and institutional affiliations.
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
1.
2.
3.
4.
5.
6.
Terms and Conditions
Springer Nature journal content, brought to you courtesy of Springer Nature Customer Service Center GmbH (“Springer Nature”).
Springer Nature supports a reasonable amount of sharing of research papers by authors, subscribers and authorised users (“Users”), for small-
scale personal, non-commercial use provided that all copyright, trade and service marks and other proprietary notices are maintained. By
accessing, sharing, receiving or otherwise using the Springer Nature journal content you agree to these terms of use (“Terms”). For these
purposes, Springer Nature considers academic use (by researchers and students) to be non-commercial.
These Terms are supplementary and will apply in addition to any applicable website terms and conditions, a relevant site licence or a personal
subscription. These Terms will prevail over any conflict or ambiguity with regards to the relevant terms, a site licence or a personal subscription
(to the extent of the conflict or ambiguity only). For Creative Commons-licensed articles, the terms of the Creative Commons license used will
apply.
We collect and use personal data to provide access to the Springer Nature journal content. We may also use these personal data internally within
ResearchGate and Springer Nature and as agreed share it, in an anonymised way, for purposes of tracking, analysis and reporting. We will not
otherwise disclose your personal data outside the ResearchGate or the Springer Nature group of companies unless we have your permission as
detailed in the Privacy Policy.
While Users may use the Springer Nature journal content for small scale, personal non-commercial use, it is important to note that Users may
not:
use such content for the purpose of providing other users with access on a regular or large scale basis or as a means to circumvent access
control;
use such content where to do so would be considered a criminal or statutory offence in any jurisdiction, or gives rise to civil liability, or is
otherwise unlawful;
falsely or misleadingly imply or suggest endorsement, approval , sponsorship, or association unless explicitly agreed to by Springer Nature in
writing;
use bots or other automated methods to access the content or redirect messages
override any security feature or exclusionary protocol; or
share the content in order to create substitute for Springer Nature products or services or a systematic database of Springer Nature journal
content.
In line with the restriction against commercial use, Springer Nature does not permit the creation of a product or service that creates revenue,
royalties, rent or income from our content or its inclusion as part of a paid for service or for other commercial gain. Springer Nature journal
content cannot be used for inter-library loans and librarians may not upload Springer Nature journal content on a large scale into their, or any
other, institutional repository.
These terms of use are reviewed regularly and may be amended at any time. Springer Nature is not obligated to publish any information or
content on this website and may remove it or features or functionality at our sole discretion, at any time with or without notice. Springer Nature
may revoke this licence to you at any time and remove access to any copies of the Springer Nature journal content which have been saved.
To the fullest extent permitted by law, Springer Nature makes no warranties, representations or guarantees to Users, either express or implied
with respect to the Springer nature journal content and all parties disclaim and waive any implied warranties or warranties imposed by law,
including merchantability or fitness for any particular purpose.
Please note that these rights do not automatically extend to content, data or other material published by Springer Nature that may be licensed
from third parties.
If you would like to use or distribute our Springer Nature journal content to a wider audience or on a regular basis or in any other manner not
expressly permitted by these Terms, please contact Springer Nature at
onlineservice@springernature.com
... 4 CPET-ESE has thus been implemented in clinical practice and research, as it can provide a comprehensive evaluation of cardiorespiratory function. 2,[5][6][7][8] It combines the advantages of both CPET and ESE but has no current standard methodology, which negatively impacts adoption and uniform practice. 2 In addition, important limitations of current protocols have emerged when used in conjunction with state-of-the-art imaging. ...
... 2 In addition, important limitations of current protocols have emerged when used in conjunction with state-of-the-art imaging. 5 Adapting CPET protocols for ESE is a complex task, as both modalities will have different needs and technical limitations. Current guidelines recommend that CPET is performed using an incremental ramp protocol, with comprehensive maximal testing criteria. ...
... 11,12 We have previously shown that in adolescent athletes and healthy children, cardiac function increases only modestly beyond moderate-intensity exercise. 5,16 There have been previous studies using variations of steadystate submaximal exercise, but all were within the moderate-intensity domain. 7,[13][14][15]31 Previous studies, especially when using STE, either limit the peak exercise to when imaging is still feasible 30 or impose an HR upper limit, 15 to allow for a good balance between purpose and usability. ...
Article
Background Exercise stress echocardiography (ESE) provides a non-invasive estimation of diastolic function during exercise and can provide insight into systolic-diastolic coupling response. Current protocols are confounded by individual variation in fitness and exercise tolerance, which in turn leads to ESE normative data being difficult to define. Aims This study aims to use ESE to describe the relationship between diastolic and systolic left ventricular function in healthy volunteers using physiologically defined personalised exercise intensity domains, accounting for individual HR response, exercise intensity and cardiorespiratory fitness. Methods Participants underwent resting echocardiography, then a maximal CPET followed by ESE consisting of two 6-minute stages: 1; Moderate intensity (M-Int) at 90% of the work rate at the gas exchange threshold (GET) and 2; High intensity (H-Int) at 40% of the difference between GET and peak exercise. Average (septal and lateral) peak systolic (LV-S’) and diastolic (LV-E’) longitudinal annular velocities as well as early diastolic mitral inflow velocity (E) were measured. E/E’ ratio was calculated to estimate LV diastolic filling pressure. Physical activity (PA) levels were assessed using age-appropriate questionnaires. Random effects linear mixed models were used to analyse exercise test data. Results A total of 101 healthy children and adults (mean age 37.8 ± 15.7 years, range 9-65, male 48.5%) were included. Participants’ PA was low in 13%, moderate in 54% and high in 33% and mean peak VO2 was 36.1 ± 7.7 ml/min/kg (range 21.3 to 60.2). LV-S’ increased significantly between rest, M-Int and H-Int, while E/E’ ratio remained constant, after adjusting for heart rate (Figure 1A and B). There was a significant inverse relationship between E/E’ ratio and LV-S’ at rest (b: -0.39, p<0.001), M-Int (b: -0.7, p=0.007) and H-Int (b: -0.65, p=0.03), shown in Figure 2. When adjusted by exercise intensity, HR, age, gender, PA levels and peak VO2, this relationship remained statistically significant for M-Int (b: -0.42, p=0.02) and H-Int, (b: -0.71, p<0.001) but not for rest (b: -0.01, p=0.9). In addition to E/E’ ratio, other factors associated with LV-S’ change during exercise were HR, age, gender and peak VO2 (p<0.1 for all). Older age was associated with overall higher E/E' values (main effect 0.04/year) but not higher relative changes during exercise (interaction with Rest: p<0.001, M-Int: p=0.7, H-Int: p=0.5). Conclusion This study shows dynamic changes in systolic-diastolic coupling during exercise, in healthy volunteers, not present at rest. Systolic-diastolic coupling could provide insight into pathological exercise limiting mechanisms, such as in heart failure with preserved ejection fraction. A sub-maximal individualised ESE protocol can be a useful tool to assess this physiological mechanism, without the bias of individual variation in cardiorespiratory fitness affecting current protocols. Figure 1 Figure 2
... 4 CPET-ESE has thus been implemented in clinical practice and research, as it can provide a comprehensive evaluation of cardiorespiratory function. 2,[5][6][7][8] It combines the advantages of both CPET and ESE but has no current standard methodology, which negatively impacts adoption and uniform practice. 2 In addition, important limitations of current protocols have emerged when used in conjunction with state-of-the-art imaging. ...
... 2 In addition, important limitations of current protocols have emerged when used in conjunction with state-of-the-art imaging. 5 Adapting CPET protocols for ESE is a complex task, as both modalities will have different needs and technical limitations. Current guidelines recommend that CPET is performed using an incremental ramp protocol, with comprehensive maximal testing criteria. ...
... 11,12 We have previously shown that in adolescent athletes and healthy children, cardiac function increases only modestly beyond moderate-intensity exercise. 5,16 There have been previous studies using variations of steadystate submaximal exercise, but all were within the moderate-intensity domain. 7,[13][14][15]31 Previous studies, especially when using STE, either limit the peak exercise to when imaging is still feasible 30 or impose an HR upper limit, 15 to allow for a good balance between purpose and usability. ...
Article
Full-text available
Aims The value of cardiopulmonary exercise testing (CPET) and exercise stress echocardiography (ESE) in managing cardiac disease is well known, but no standard CPET-ESE protocol is currently recommended. This pilot study aims to compare feasibility and cardiac function responses between a new high intensity single stage combined test (CPET-hiESE) and a standard maximal ESE (smESE). Methods After screening and maximal CPET, all volunteers (n = 21) underwent three ESE modalities: 1) based on the gas exchange threshold (hiESE-GET, 40% of peak-GET, 6 minutes), 2) based on heart rate (HR) (hiESE-HR, 80% of peak HR, 6 minutes) and 3) smESE (85% of predicted peak HR for age, 3 minutes). Speckle tracking echocardiography (STE) and tissue Doppler imaging (TDI) were measured at each step. Results There was superior image quality and data completeness for right ventricle (RV) strain for both hiESE modalities compared to smESE (71.4% and 76.2% vs 42.9%, p = 0.07). Left ventricular STE data completeness was similar for all three conditions. Despite systematically higher HR, work-rate and levels of exertion in the smESE compared to hiESE, STE and TDI parameters were not systematically different. Concordance correlation coefficients ranged from 0.56 to 0.88, lowest for strain rate parameters and mean difference from -0.34 to 1.53, highest for TDI measurements. Conclusions The novel CPET-hiESE protocol allowed for better data completeness, at lower levels of exertion compared to smESE, without systematically different cardiac reserve measurements in healthy participants. This single stage protocol can be individualised to clinical populations, which would provide practical advantages to standard testing.
... With increased body movement during exercise, reverberations and shadowing may influence the quality of speckle tracking, which may lead to underestimation of peak values [24]. Indeed, larger variability at higher intensities is matched with a greater loss of sufficient speckle tracking, with increased cardiovascular demand, thus required heart rate in children [26]. Although Liu et al. [27] identified similar longitudinal and circumferential ε acquired above or below 60 Hz at 160 bpm in children, the quantity of available data at high heart rates (~160 bpm) has been reported to be 59% [27] and 60% [26] for 4-chamber images. ...
... Indeed, larger variability at higher intensities is matched with a greater loss of sufficient speckle tracking, with increased cardiovascular demand, thus required heart rate in children [26]. Although Liu et al. [27] identified similar longitudinal and circumferential ε acquired above or below 60 Hz at 160 bpm in children, the quantity of available data at high heart rates (~160 bpm) has been reported to be 59% [27] and 60% [26] for 4-chamber images. Successful speckle tracking relies on sufficient temporal resolution [24], which can be maximised to improve tracking success through elevated frame rates; however, this is at the detrimental limitation of spatial resolution. ...
... Indeed, variations in success with image acquisition and analysis may be due to the adopted cycling positions. In the adolescent literature, various cycling body positions for stress echocardiography have been used, including upright [23,25,32,33], semi-supine [26], and supine [27]. Irrespective of the mode used, it is important that consideration is given to the knowledge that altering posture will induce different physiological responses; thus, a trade-off exists among standardization, image quality [31], and ecological validity. ...
Article
Full-text available
There is an increase in the prevalence of elite youth sports academies, whose sole aim is to develop future elite athletes. This involves the exposure of the child and adolescent athlete to high-volume training during a period of volatile growth. The large amount of data in this area has been garnered from the resting echocardiographic left ventricular (LV) evaluation of the youth athlete; while this can provide some insight on the functional adaptations to training, it is unable to elucidate a comprehensive overview of the function of the youth athletes’ LV during exercise. Consequently, there is a need to interrogate the LV responses in-exercise. This review outlines the feasibility and functional insight of capturing global indices of LV function (Stroke Index-SVIndex and Cardiac Index-QIndex), systolic and diastolic markers, and cardiac strain during submaximal and maximal exercise. Larger SVI and QI were noted in these highly trained young athletes compared to recreationally active peers during submaximal and maximal exercise. The mechanistic insights suggest that there are minimal functional systolic adaptions during exercise compared to their recreationally active peers. Diastolic function was superior during exercise in these young athletes, and this appears to be underpinned by enhanced determinants of pre-load.
... CPET is a valuable tool to evaluate the responses of the cardiac, pulmonary, vascular, and musculoskeletal systems to exercise [101][102][103][104]. Although still underutilized, its high reproducibility offers important prognostic and diagnostic information [105] and can be integrated with other imaging techniques [106]. Different from an EST, CPET involves measurements of respiratory oxygen uptake, carbon dioxide production, and ventilatory measures during a symptom-limited exercise test. ...
... Through the identification of ventilatory thresholds, the physician may draw out a personally tailored program with the appropriate level of intensity associated with possible enhancements for healthy athletes and proven benefits for patients with chronic diseases [116,117]. Moreover, CPET should be part of the routine assessment of patients with cardiomyopathies who wish to exercise to obtain information about functional capacity and risk stratification [97,106,118,119]. ...
Article
Full-text available
“Athlete’s heart” is a spectrum of morphological, functional, and regulatory changes that occur in people who practice regular and long-term intense physical activity. The morphological characteristics of the athlete’s heart may overlap with some structural and electrical cardiac diseases that may predispose to sudden cardiac death, including inherited and acquired cardiomyopathies, aortopathies and channelopathies. Overdiagnosis should be avoided, while an early identification of underlying cardiac life-threatening disorders is essential to reduce the potential for sudden cardiac death. A step-by-step multimodality approach, including a first-line evaluation with personal and family history, clinical evaluation, 12-lead resting electrocardiography (ECG), followed by second and third-line investigations, as appropriate, including exercise testing, resting and exercise echocardiography, 24-hour ECG Holter monitoring, cardiac magnetic resonance, computed tomography, nuclear scintigraphy, or genetic testing, can be determinant to differentiate between extreme physiology adaptations and cardiac pathology. In this context, cardiovascular imaging plays a key role in detecting structural abnormalities in athletes who fall into the grey zone between physiological adaptations and a covert or early phenotype of cardiovascular disease.
... Using the advanced modalities of 2-D strain imaging (myocardial deformation imaging) it shows a promising role in the early differentiation of physiological versus pathological remodeling with our group already using the capabilities of the Canon systems in this area to publish reference values for adolescent athletes (Figs. 2-4) 35 . Echocardiography is therefore a primary profiling tool in our approach from the age of 14 years onwards, an age where we commonly observe the first presentation of the common inherited cardiomyopathies. ...
... This modality is again helping us decipher the grey zone of cardiac remodeling in athletes, and work from our group has gone some way to doing this within the pediatric footballer. Pieles and colleagues 35 identified that the more reliable and valid measures of strain and strain rate during exercise were similar between the footballers and non-footballers. In highlighting the specific response to exercise this will allow us to help further differentiate between the adaptive, physiological response versus the maladaptive pathological myocardial function in pediatric athletes. ...
Research
Full-text available
The project is related to the use of exercise echo cardiography and young athletes, as part fo an on-going heart health of yougn athletes.
... Using the advanced modalities of 2-D strain imaging (myocardial deformation imaging) it shows a promising role in the early differentiation of physiological versus pathological remodeling with our group already using the capabilities of the Canon systems in this area to publish reference values for adolescent athletes (Figs. 2-4) 35 . Echocardiography is therefore a primary profiling tool in our approach from the age of 14 years onwards, an age where we commonly observe the first presentation of the common inherited cardiomyopathies. ...
... This modality is again helping us decipher the grey zone of cardiac remodeling in athletes, and work from our group has gone some way to doing this within the pediatric footballer. Pieles and colleagues 35 identified that the more reliable and valid measures of strain and strain rate during exercise were similar between the footballers and non-footballers. In highlighting the specific response to exercise this will allow us to help further differentiate between the adaptive, physiological response versus the maladaptive pathological myocardial function in pediatric athletes. ...
Article
Background Barth syndrome is a rare, life-threatening X-linked recessive mitochondrial disorder of lipid metabolism primarily affecting males. Previous research suggests that bezafibrate may ameliorate cellular lipid abnormalities and reduce cardiac dysfunction in an animal model. Objectives Estimate the effect of bezafibrate on clinical, biochemical, and quality-of-life outcomes. Investigate whether within-participant clinical changes parallel in vitro changes in cardiolipin ratio/profile and mitochondrial morphology when each participant’s cells are cultured with bezafibrate. Investigate as for objective 2, culturing each participant’s cells with resveratrol. Describe the most feasible methods and standardised outcome measures to optimise the conduct of future trials and evaluations in Barth syndrome. Describe features of the research infrastructure which optimised recruitment, retention and communication with families and people with Barth syndrome. Describe the perceptions of participants and their families about the research and any important potential barriers to participation. Design Randomised, placebo-controlled, crossover trial of bezafibrate versus placebo. Setting NHS hospital providing UK-wide Barth Syndrome Service. Participants Males aged ≥ 6 years with a confirmed diagnosis of Barth syndrome with stable cardiac status, able to swallow tablets of bezafibrate/placebo. Exclusions were: hypersensitivity or allergy to bezafibrate or any component of bezafibrate; hepatic, liver or renal dysfunction; gallbladder disease; or recent deterioration in general health. Interventions Fifteen weeks of bezafibrate in one period and placebo in a second period, or vice versa (randomly allocated), with at least a 1-month washout between periods. Main outcome measures The primary outcome was peak V O 2 ; secondary outcomes were cardiac function rest and exercise echocardiography and magnetic resonance imaging, cardiolipin ratio, quality of life, dynamic skeletal muscle P-magnetic resonance spectroscopy, mitochondrial studies and neutrophil counts, and adverse events. Outcomes were measured at baseline and the end of each period. Results Eleven males were studied; all attended all three assessments. There was no difference in peak V O 2 between periods (0.66 ml/kg/min lower with bezafibrate than placebo, 95% confidence interval 2.34 to 1.03; p = 0.43). There was a trend towards a higher left ventricular ejection fraction with bezafibrate when measured by echocardiography but not magnetic resonance imaging, and better echocardiography-derived rest longitudinal and circumferential strain with bezafibrate. There was no difference in quality of life or cardiolipin ratio between periods. Skeletal muscle ³¹ P magnetic resonance spectroscopy was performed cross-sectionally and showed a trend to higher Tau and lower Q max indices in the bazafibrate group. Two participants had serious, expected adverse reactions when taking bezafibrate; otherwise, bezafibrate was well tolerated. Limitations The sample size was very small; the bezafibrate dose may have been too low or 15 weeks too short to observe an effect; measurements of mitochondrial content and membrane potential were highly variable; P-magnetic resonance spectroscopy was available only at the final assessment. Conclusions This study did not show significant improvement in the primary and secondary outcomes with bezafibrate treatment. Future work Elamipretide, studied in a small crossover trial in the USA, is another potential intervention which may be worth evaluating in an international study. Trial registration This trial is registered as ISRCTN58006579. Funding This award was funded by the National Institute for Health and Care Research (NIHR) Efficacy and Mechanism Evaluation (EME) programme (NIHR award ref: 12/205/56) and is published in full in Efficacy and Mechanism Evaluatio n; Vol. 11, No. 13. See the NIHR Funding and Awards website for further award information.
Article
Despite exercise intolerance being predictive of outcomes in pulmonary arterial hypertension (PAH), its underlying cardiac mechanisms are not well described. The aim of the study was to explore the biventricular response to exercise and its associations with cardiorespiratory fitness in children with PAH. Participants underwent incremental cardio-pulmonary exercise testing and simultaneous exercise echocardiography on a recumbent cycle ergometer. Linear mixed models were used to assess cardiac function variance and associations between cardiac and metabolic parameters during exercise. Eleven participants were included with a mean age 13.4 ±2.9 years. Right ventricle (RV) systolic pressure (RVsp) increased from a mean of 59 ±25 mmHg at rest to 130 ±40 mmHg at peak exercise (p<0.001), while RV fractional area change (RV-FAC) and RV free wall longitudinal strain (RVFW-S l ) worsened (35.2% vs 27%, p=0.09 and -16.6% vs -14.6%, p=0.1, respectively). At low and moderate intensity exercise, RVsp was positively associated with stroke volume and O 2 pulse (p<0.1). At high intensity exercise RV-FAC, RVFW-S l and left ventricular longitudinal strain were positively associated with oxygen uptake and O 2 pulse (p<0.1), while stroke volume decreased towards peak (p=0.04). In children with PAH, the increase of pulmonary pressure alone does not limit peak exercise, but rather the concomitant reduced RV functional reserve, resulting in RV-PA uncoupling, worsening of inter-ventricular interaction and LV dysfunction. A better mechanistic understanding of PAH exercise physiopathology can inform stress testing and cardiac rehabilitation in this population.
Article
Full-text available
Aims Cardiac adaptations in elite, male adolescent youth soccer players have been demonstrated in relation to training status. The time course of these adaptations and the delineation of the influence of volatile growth phases from the training effect on these adaptations remain unclear. Consequently, the aims of the study were to evaluate the impact of 3 years of elite‐level soccer training on changes in left ventricular (LV) structure and function in a group of highly trained elite youth male soccer players (SP) as they transitioned through the pre‐to‐adolescent phase of their growth. Methods Twenty‐two male youth SP from the highest Level of English Premier League Academy U‐12 teams were evaluated once a year for three soccer seasons as the players progressed from the U‐12 to U‐14 teams. Fifteen recreationally active control participants (CON) were also evaluated over the same 3‐year period. Two‐dimensional transthoracic echocardiography was used to quantify LV structure and function. Results After adjusting for the influence of growth and maturation, training‐induced increases in Years 2 and 3 were noted for: LV end diastolic volume (LVEDV; p = 0.02) and LV end systolic volume (LVESV; p = 0.02) in the SP compared to CON. Training‐induced decrements were noted for LV ejection fraction (LVEF; p = 0.006) and TDI‐S′ (p < 0.001). Conclusions An increase in training volume (Years 2 and 3) were aligned with LV volumetric adaptations and decrements in systolic function in the SP that were independent from the influence of rapid somatic growth. Decrements in systolic function were suggestive of a functional reserve for exercise.
Article
Full-text available
Background Reports on the incidence and causes of sudden cardiac death among young athletes have relied largely on estimated rates of participation and varied methods of reporting. We sought to investigate the incidence and causes of sudden cardiac death among adolescent soccer players in the United Kingdom. Methods From 1996 through 2016, we screened 11,168 adolescent athletes with a mean (±SD) age of 16.4±1.2 years (95% of whom were male) in the English Football Association (FA) cardiac screening program, which consisted of a health questionnaire, physical examination, electrocardiography, and echocardiography. The FA registry was interrogated to identify sudden cardiac deaths, which were confirmed with autopsy reports. Results During screening, 42 athletes (0.38%) were found to have cardiac disorders that are associated with sudden cardiac death. A further 225 athletes (2%) with congenital or valvular abnormalities were identified. After screening, there were 23 deaths from any cause, of which 8 (35%) were sudden deaths attributed to cardiac disease. Cardiomyopathy accounted for 7 of 8 sudden cardiac deaths (88%). Six athletes (75%) with sudden cardiac death had had normal cardiac screening results. The mean time between screening and sudden cardiac death was 6.8 years. On the basis of a total of 118,351 person-years, the incidence of sudden cardiac death among previously screened adolescent soccer players was 1 per 14,794 person-years (6.8 per 100,000 athletes). Conclusions Diseases that are associated with sudden cardiac death were identified in 0.38% of adolescent soccer players in a cohort that underwent cardiovascular screening. The incidence of sudden cardiac death was 1 per 14,794 person-years, or 6.8 per 100,000 athletes; most of these deaths were due to cardiomyopathies that had not been detected on screening. (Funded by the English Football Association and others.)
Article
Full-text available
Aim: To describe the electrocardiographic (ECG) and echocardiographic manifestations of the paediatric athlete's heart, and examine the impact of age, race and sex on cardiac remodelling responses to competitive sport. Design: Systematic review with meta-analysis. Data sources: Six electronic databases were searched to May 2016: MEDLINE, PubMed, EMBASE, Web of Science, CINAHL and SPORTDiscus. Inclusion criteria: (1) Male and/or female competitive athletes, (2) participants aged 6-18 years, (3) original research article published in English language. Results: Data from 14 278 athletes and 1668 non-athletes were included for qualitative (43 articles) and quantitative synthesis (40 articles). Paediatric athletes demonstrated a greater prevalence of training-related and training-unrelated ECG changes than non-athletes. Athletes ?14 years were 15.8 times more likely to have inferolateral T-wave inversion than athletes <14 years. Paediatric black athletes had significantly more training-related and training-unrelated ECG changes than Caucasian athletes. Age was a positive predictor of left ventricular (LV) internal diameter during diastole, interventricular septum thickness during diastole, relative wall thickness and LV mass. When age was accounted for, these parameters remained significantly larger in athletes than non-athletes. Paediatric black athletes presented larger posterior wall thickness during diastole (PWTd) than Caucasian athletes. Paediatric male athletes also presented larger PWTd than females. Conclusions: The paediatric athlete's heart undergoes significant remodelling both before and during 'maturational years'. Paediatric athletes have a greater prevalence of training related and training-unrelated ECG changes than non-athletes, with age, race and sex mediating factors on cardiac electrical and LV structural remodelling.
Article
Full-text available
Background Characteristic right ventricle (RV) remodelling is related to endurance exercise in male athletes (MAs), but data in female athletes (FAs) are scarce. Our aim was to evaluate sex-related influence on exercise-induced RV remodelling and on RV performance during exercise. Methods Forty endurance athletes (>10 training hours/week, 50% female) and 40 age-matched controls (<3 h moderate exercise/week, 50% female) were included. Echocardiography was performed at rest and at maximum cycle-ergometer effort. Both ventricles were analysed by standard and speckle-tracking echocardiography. ResultsEndurance training induced similar structural and functional cardiac remodelling in MAs and FAs, characterized by bi-ventricular dilatation [~34%, left ventricle (LV); 29%, RV] and normal bi-ventricular function. However, males had larger RV size (p < 0.01), compared to females: RV end-diastolic area (cm2/m2): 15.6 ± 2.2 vs 11.6 ± 1.7 in athletes; 12.2 ± 2.7 vs 8.6 ± 1.6 in controls, respectively, and lower bi-ventricular deformation (RV global longitudinal strain (GLS) (%): −24.0 ± 3.6 vs −29.2 ± 3.1 in athletes; −24.9 ± 2.5 vs −30.0 ± 1.9 in controls, and LVGLS: −17.5 ± 1.4 vs −21.9 ± 1.9 in athletes; −18.7 ± 1.2 vs −22.5 ± 1.5 in controls, respectively, p < 0.01). During exercise, the increase in LV function was positively correlated (p < 0.01) with increased cardiac output (∆%LV ejection fraction, r = +0.46 and ∆%LVGLS, r = +0.36). Improvement in RV performance was blunted at high workloads, especially in MAs. Conclusion Long-term endurance training induced similar bi-ventricular remodelling in MAs and FAs. Independently of training load, males had larger RV size and lower bi-ventricular deformation. Improvement in RV performance during exercise was blunted at high workloads, especially in MAs. The potential mechanisms underlying these findings warrant further investigation.
Article
Full-text available
Increased left ventricular (LV) twist and untwisting rate (LV twist mechanics) are essential responses of the heart to exercise. However, previously a large variability in LV twist mechanics during exercise has been observed, which complicates the interpretation of results. This study aimed to determine some of the physiological sources of variability in LV twist mechanics during exercise. Sixteen healthy males (age: 22 ± 4 years, [Formula: see text]O2peak: 45.5 ± 6.9 ml∙kg-1∙min-1, range of individual anaerobic threshold (IAT): 32-69% of [Formula: see text]O2peak) were assessed at rest and during exercise at: i) the same relative exercise intensity, 40%peak, ii) at 2% above IAT, and, iii) at 40%peak with hypoxia (40%peak+HYP). LV volumes were not significantly different between exercise conditions (P > 0.05). However, the mean margin of error of LV twist was significantly lower (F2,47 = 2.08, P < 0.05) during 40%peak compared with IAT (3.0 vs. 4.1 degrees). Despite the same workload and similar LV volumes, hypoxia increased LV twist and untwisting rate (P < 0.05), but the mean margin of error remained similar to that during 40%peak (3.2 degrees, P > 0.05). Overall, LV twist mechanics were linearly related to rate pressure product. During exercise, the intra-individual variability of LV twist mechanics is smaller at the same relative exercise intensity compared with IAT. However, the absolute magnitude (degrees) of LV twist mechanics appears to be associated with the prevailing rate pressure product. Exercise tests that evaluate LV twist mechanics should be standardised by relative exercise intensity and rate pressure product be taken into account when interpreting results.
Article
Full-text available
Background: The aims of the present study were to evaluate the feasibility and reproducibility of color Doppler tissue imaging (DTI) and two-dimensional speckle-tracking echocardiography during semisupine cycle ergometric stress echocardiography and to establish normal myocardial systolic and diastolic left ventricular (LV) and right ventricular (RV) response to exercise in children. Methods: This was a single-center prospective study of 62 healthy children (35 girls). The median age was 14 years (range, 8-19 years). A stepwise semisupine cycle ergometric protocol was used. Color DTI peak systolic (s') and peak diastolic (e') velocities and myocardial acceleration during isovolumic contraction were measured in the LV lateral wall, RV free wall, and septum. Early mitral inflow Doppler (E) was measured from the apical four-chamber view, and the ratio of diastolic filling to tissue early diastolic velocity (E/e') was calculated. LV and RV longitudinal strain were measured from four-chamber apical views. LV circumferential strain was derived from the parasternal short-axis view at the midventricular level. The relationship of each parameter with increasing heart rate was evaluated at each stage of exercise. Results: During exercise color DTI, velocities were obtained in 96% of subjects, with isovolumic contraction having the lowest feasibility among DTI measurements (89%). Strain analysis was measurable in 87% of subjects, with LV longitudinal strain measured in 98% of the subjects compared with 93% for circumferential strain. RV longitudinal strain had the lowest feasibility (70%). A linear relationship was observed between heart rate and color DTI velocities, E, E/e', and myocardial longitudinal and circumferential strain. The relationship between isovolumic contraction and heart rate was exponential. Conclusions: This study provides reference values for systolic and diastolic reserve during exercise in healthy children as measured by color DTI and two-dimensional speckle-tracking echocardiography. These data allow the evaluation of myocardial response in pediatric cardiac disease.
Article
Full-text available
Background: LV and RV myocardial reserve during exercise in adolescents has not been directly characterized. The aim of this study was to quantify myocardial performance response to exercise using two dimensional speckle tracking echocardiography and describe the relationship between myocardial reserve, respiratory and metabolic exercise parameters. Materials and methods: A total of 23 healthy boys and girls (mean age 13.2±2.7 y; stature 159.1±16.4 cm; body mass 49.5±16.6 kg; BSA 1.47±0.33 m(2) completed an incremental cardiopulmonary exercise test (25 W∙3 min increments) with simultaneous acquisition of 2-D trans-thoracic echocardiography at rest, each exercise stage up to 100W and in recovery at 2 min and 10 min. 2-D LV (LV Sl) and RV (RV Sl) longitudinal strain and LV circumferential strain (LV Sc) were analyzed to define the relationship between myocardial performance reserve and metabolic exercise parameters. Results: Participants achieved a peak oxygen uptake (VO2peak) of 40.6±8.9 mL∙kg(-1)∙min(-1) and a work rate of 154±42 W. LV Sl and LV Sc and RV Sl increased significantly across work rates (p<0.05). LV Sl during exercise was significantly correlated to resting strain, VO2peak, oxygen pulse and work rate (0.530 ≤ r ≤ 0.784, p<0.05). Discussion: This study identifies a positive and moderate relationship between LV and RV myocardial performance and metabolic parameters during exercise using a novel methodology. Relationships detected present novel data directly describing myocardial adaptation at different stages of exercise and recovery that in the future can help directly assess cardiac reserve in patients with cardiac pathology.
Article
Full-text available
Contractile function is considered to be precisely measurable only by invasive hemodynamics. We aimed to correlate strain values measured by speckle tracking echocardiography (STE) with sensitive contractility parameters of pressure-volume (P-V) analysis in a rat model of exercise-induced left ventricular (LV) hypertrophy. LV hypertrophy was induced in rats by swim training and was compared to untrained controls. Echocardiography was performed using a 13MHz linear transducer to obtain LV long- and short-axis recordings for STE analysis (GE EchoPAC). Global longitudinal and circumferential strain (GLS, GCS) and systolic strain rate (LSr, CSr) were measured. LV P-V analysis was performed using a pressure-conductance microcatheter and load-independent contractility indices (slope of the end-systolic P-V relationship [ESPVR], preload recruitable stroke work [PRSW] and maximal dP/dt - end-diastolic volume relationship [dP/dtmax-EDV]) were calculated. Trained rats had increased LV mass index (trained vs control; 2.76±0.07 vs 2.14±0.05g/kg, p<0.001). P-V loop derived contractility parameters were significantly improved in the trained group (ESPVR: 3.58±0.22 vs 2.51±0.11mmHg/μl; PRSW: 131±4 vs 104±2mmHg, p<0.01). Strain and strain rate parameters were also supernormal in trained rats (GLS: -18.8±0.3 vs -15.8±0.4%, LSr: -5.0±0.2 vs -4.1±0.1Hz, GCS -18.9±0.8 vs -14.9±0.6%, CSr: -4.9±0.2 vs -3.8±0.2Hz, p<0.01). ESPVR correlated with GLS (r=-0.71), LSr (r=-0.53), but robustly with GCS (r=-0.83) and CSr (r=-0.75, all p<0.05). PRSW was strongly related to GLS (r=-0.64) and LSr (r=-0.71, both p<0.01). STE can be a feasible and useful method for animal experiments. In our rat model, strain and strain rate parameters closely reflected the improvement in intrinsic contractile function induced by exercise training. Copyright © 2014, American Journal of Physiology - Heart and Circulatory Physiology.
Article
Background: Professional athletes exhibit lower left ventricular wall thicknesses, diameters and mass (in females), with less frequent training-related electrocardiogram (ECG) changes, as compared with controls. Methods: We studied the association of sex with left ventricular structure in trained early adolescents. Two hundred and six adolescent Caucasian athletes (mean age 13.8 ± 1.6, range 11.8-16.9 years, 158 males and 48 females), with similar degree of training underwent ECG and echocardiographic measurements of left ventricular diameters, thicknesses and mass, with relative wall thickness as the remodelling index. Results: As compared with females, males exhibited greater maximal wall thickness (males = 8.7 ± 1.2 vs. females = 7.9 ± 0.8) and indexed left ventricular mass (100 ± 18 g/m(2) vs. 79 ± 12, p < 0.001), without differences in relative wall thickness (males = 0.35 ± 0.04 vs. females = 0.34 ± 0.04) and with higher prevalence of ECG-based left ventricular hypertrophy, sinus bradycardia and ST-elevation. An analysis of covariance, using age, body surface area, systolic blood pressure, heart rate and sex as the covariates, reported that sex is a strong predictor of left ventricular mass, maximal wall thickness, left ventricular diastolic diameter and ECG-based left ventricular hypertrophy. In a binary logistic regression model analysis sex, like left ventricular mass, predicted ST-trait elevation. Conclusions: Our results suggest that, in early adolescence, female athletes have lower left ventricular mass and thicknesses compared with males, without geometrical differences. Therefore, sex, independent of age, is a strong determinant of structural parameters also in early adolescent athletes. These data indicate that sex-specific parameters are needed in the pre-participation cardiovascular screening of adolescent athletes.
Article
Background—The phenotype of individuals with hypertrophic cardiomyopathy (HCM) who exercise regularly is unknown. This study characterized the clinical profile of young athletes with HCM. Methods and Results—The electrical, structural, and functional cardiac parameters from 106 young (14–35 years) athletes with HCM were compared with 101 sedentary HCM patients. A subset of athletes with HCM exhibiting morphologically mild (13–16 mm), concentric disease was compared with 55 healthy athletes with mild physiological left ventricular hypertrophy (LVH). Most athletes with HCM (96%) exhibited T-wave inversion and had milder LVH (15.8±3.4 mm versus 19.7±6.5 mm, P<0.001), larger left ventricular cavity dimensions (47.8±6.0 mm versus 44.3±7.7 mm, P<0.001), and superior indices of diastolic function (average E/E′ 7.9±2.4 versus 10.7±3.9, P<0.001) compared with sedentary HCM patients. In athletes with HCM, LVH was frequently (36%) confined to the apex and only 15 individuals (14%) exhibited mild concentric LVH mimicking physiological LVH. In these 15 athletes, conventional structural and functional cardiac parameters showed modest sensitivity and specificity for differentiating HCM from physiological LVH: 13% had a left ventricular cavity >54 mm, 87% had a left atrium ≤40, and 100% had an E/E′ <12. Conclusions—Athletes with HCM exhibit less LVH, larger left ventricular cavities, and normal indices of diastolic function compared with sedentary patients. Only a minority of athletes with HCM constitute the conventional gray zone of mild, concentric LVH. In this minority, conventional echocardiographic parameters alone are insufficient to differentiate HCM from physiological LVH and should be complemented by additional structural and functional assessments to minimize the risk of false reassurance.