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European Journal of Applied Physiology (2021) 121:239–250
https://doi.org/10.1007/s00421-020-04510-6
ORIGINAL ARTICLE
Characterisation ofLV myocardial exercise function by2‑D strain
deformation imaging inelite adolescent footballers
GuidoE.Pieles1,2,3 · LucyGowing1· DianeRyding4· DavePerry4· StevenR.McNally4· A.GrahamStuart2·
CraigA.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 150W.
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 50W (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 150W 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 ofSport Exercise andHealth (ISEH), University
College London, LondonW1T7HA, UK
2 Bristol Congenital Heart Centre, The Bristol Heart Institute,
University Hospitals Bristol NHS Foundation Trust, Upper
Maudlin Street, BristolBS28BJ, UK
3 National Institute forHealth Research (NIHR)
Cardiovascular Biomedical Research Centre, Bristol Heart
Institute, Upper Maudlin Street, BristolBS28BJ, UK
4 Manchester United Football Club, Football Medicine
andScience Department, AON Training Complex, Birch
Road, Carrington, ManchesterM314BH, UK
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240 European Journal of Applied Physiology (2021) 121:239–250
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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 etal.
1975; Nishimura etal. 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 etal. 2002; Makan etal. 2005; Di Paolo etal.
2012; Pela etal. 2016, McClean etal. 2017). Like adult ath-
letes, adolescent athletes are also at risk of sudden cardiac
death (SCD) (Malhotra etal. 2018). Importantly, 33–56% of
SCD events in young athletes occur with exertion (Roberts
etal. 1980; Epstein etal. 1986; Harmon etal. 2011; Chandra
etal. 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 etal. 2013; Sanz-de la Garza etal. 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 etal. 2011, Roche etal. 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 etal. 1996; Inagaki etal. 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 etal.
2013; Pieles etal. 2015; Cifra etal. 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 etal. 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 etal. 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 etal. 2006) and has been
used in diagnosis, risk stratification and outcome prediction
in children and adults with cardiac disease (Rhodes etal.
2010; Guazzi etal. 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 etal.
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 ± 9.7cm, body mass 58.7 ± 11.0kg, BMI
19.6 ± 2.1kgm2, lean body mass 47.2 ± 7.5kg, body surface
area 1.69 ± 0.20m2), 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 12h per week training and game time and
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241European Journal of Applied Physiology (2021) 121:239–250
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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 (25W∙3min−1 increments) was performed to
volitional exhaustion at a pedaling frequency of 70 ± 5rpm.
Exercise stages of 3min 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 etal.
2015). Participants were requested to avoid strenuous exer-
cise for at least 12h preceding each visit and to arrive at the
laboratory in a rested and hydrated state 2h after a meal.
Echocardiography
Prior to exercise stress testing, participants underwent a full
structural and functional resting (baseline) echocardiogram
following international paediatric guidelines (Lai etal.
2006, Lopez etal. 2010). Echocardiographic measurements
and analysis were performed using an Artida machine and
a 2.0–4.8MHz 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 etal. 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 etal. 2015). Briefly,
focused echocardiography was performed for 2-D strain
analysis during free breathing exercise 60s into each exer-
cise stage at baseline (rest), 0 (unloaded pedaling), 50, 100,
150W and during recovery at 2min (Rec2) and 6min (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 150W. Strain val-
ues were not calculated at work rates higher than 150W 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
(Table1). 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 (Tables2 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.
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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 ± 1.3mm, LVPWd 8.9 ± 1.3mm, LVIDd 44.5 ± 3.8mm,
LVIDs 32 ± 5.8mm) 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%. Table1 represents the mean
(SD) CPET data. The exercise duration was 25:44 ± 5:46
(min:s) with a mean peak power output of 211 ± 45W.
Relative VO2peak was 49.1 ± 6.5mL·kg−1·min−1, GET was
129 ± 38W and 69 ± 13% of VO2peak or 33.3mL·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 duringexercise—2‑D
strain
Analysis of 2-D LV strain was feasible up to a work
rate of 100W 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 150W and a mean HR of
161 ± 16 b∙min−1 in 60% of subjects for longitudinal and
88% for circumferential 2-D strain (Table2). Initiation
of exercise (0W) 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 50W (P = 0.001). A plateauing effect at the
higher power outputs between 50 and 150W was shown
(Fig.4), where inter-stage comparisons were not signif-
icantly different between 50 and 100W (P = 0.06) and
100 and 150W (P = 0.91) (Fig.4.). This plateau effect for
LV Sl corresponded to a VO2peak of between 52 and 75%
(Table1 and Figs.3 and 4) falling into the range, where
GET occurred, specifically 12% and 59% of participants
were at GET at 100W and 150W, respectively. In contrast,
inter-stage comparisons from baseline and exercise stages
up to 150W 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 (2min) 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 = 72bpm) and during moder-
ate exercise (right, 100W, HR = 134bpm)
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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 6min recovery. Impor-
tantly however, values did not reach baseline values at
6min recovery (P < 0.05) (Table2 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 (Table3 and Fig.4). Three comparisons
for longitudinal SR between 0W and 6minrec (P = 0.84)
and 50W and 2minrec (P = 0.65) and circumferential
SR for 0W and 6minrec (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)
(Table3).
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
0W 0.51 ± 0.10 8.86 ± 1.84 88 ± 11 5.90 ± 1.51 18.0 ± 3.2 42
25W 0.67 ± 0.12 11.71 ± 2.15 97 ±12 7.05 ± 1.70 24.0 ± 4.7 42
50W 0.91 ± 0.10 15.86 ± 2.78 107 ±11 8.55 ± 1.51 32.5 ± 6 42
75W 1.18 ± 0.12 20.64 ± 3.74 120 ± 12 9.91 ± 1.59 42.4 ± 8.6 42
100W 1.44 ± 0.13 25.33 ± 4.71 134 ± 13 10.84 ± 1.50 51.9 ± 10 42
125W 1.75 ± 0.18 30.46 ± 6.59 148 ± 15 11.89 ± 1.65 61.4 ± 11.5 40
150W 2.10 ± 0.26 36.00 ± 7.32 161 ± 16 13.30 ± 2.26 72.5 ± 12 39
175W 2.34 ± 0.23 39.46 ± 7.24 168 ± 13 14.02 ± 1.89 78.5 ± 11.0 34
200W 2.55 ± 0.17 40.40 ± 6.61 173 ± 8 15.02 ± 1.39 81.8 ± 9.2 23
225W 2.91 ± 0.26 42.00 ± 6.13 177 ± 10 17.58 ± 1.20 85.5 ± 10.2 13
250W 3.47 ± 0.51 47.37 ± 6.73 180 ± 13 20.54 ± 0.18 88.5 ± 8.5 4
275W 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
2min rec 0.66 ± 0.23 11.25 ± 2.81 109 ± 13 6.09 ± 1.86 23.2 ± 5.3 42
6min 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 Table1
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244 European Journal of Applied Physiology (2021) 121:239–250
1 3
Force–Frequency relationship
Figures5 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 betweenexercise myocardial
performance andmetabolic 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 etal. 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 duringexercise
Strain and strain rates at baseline were comparable to pub-
lished reference data in healthy adolescents (Marcus etal.
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 etal. 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 150W whereas LV Sl, which describes contrac-
tility of longitudinal myocardial fibres, reached a plateau
at moderate work rates (50–100W), 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 etal. 2014) and also con-
firmed by animal studies (Kovacs etal. 2015), that showed
Fig. 3 a Mean LV peak systolic longitudinal strain and circumferen-
tial strain at each exercise stage (baseline to 6min recovery); b Mean
LV peak systolic longitudinal strain and circumferential strain reserve
at each exercise stage (baseline to 6min recovery) showing a plateau-
ing effect for mean peak systolic LV longitudinal strain
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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 etal. 2015). While specific loading
conditions during exercise might to some degree influ-
ence our 2-D strain values (Greenberg etal. 2002), we
validated this result by measuring strain rate (Table3
and Fig.6), which is the least load-dependent parameter
(Ferferieva etal. 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 150W 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 etal.
2002) and exercise stress (La Gerche etal. 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 etal. 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 = 50W, d = 100W, e = 150W, f = 2min rec
and g = 6min rec; (e.g. in left upper panel at baseline significant dif-
ferences found compared to 0, 50, 100, 150, 2min rec and 6min rec)
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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 etal. 2002a,
b) which has been shown to not alter significantly at near
maximal exercise (Higginbotham etal. 1986). Our previ-
ous data in healthy non-athlete adolescents of similar age
using the same methodology (Pieles etal. 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
0W −19.9 3.2 −26.3 −13.6 −4.4 ± 2.3 < 0.001 39
50W −21.9 3.3 −28.6 −15.3 −6.6 ± 2.7 < 0.001 40
100W −22.7 3.5 −29.6 −15.7 −7.2 ± 3.2 < 0.001 37
150W −22.5 4.1 −30.7 −14.2 −8 ± 3 < 0.001 19
2min rec −17.9 2.9 −23.7 −12.1 −2.7 ± 2.7 < 0.001 37
6min 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
0W −26.9 2.8 −32.6 −21.2 −4.1 ± 2.5 < 0.001 40
50W −30.7 3.2 −37.2 −24.3 −8.2 ± 3 < 0.001 42
100W −33.0 3.7 −40.5 −25.6 −10.5 ± 3.4 < 0.001 41
150W −34.3 4.0 −42.3 −26.2 −11.8 ± 3.2 < 0.001 34
2min rec −24.9 3.2 −31.3 −18.5 −2.6 ± 3.3 < 0.001 41
6min 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
0W −1.15 0.26 −1.67 −0.62 −0.3 ± 0.3 < 0.001 41
50W −1.50 0.31 −2.13 −0.87 −0.7 ± 0.3 < 0.001 42
100W −1.76 0.43 −2.62 −0.91 −0.9 ± 0.5 < 0.001 40
150W −2.05 0.34 −2.73 −1.37 −1.3 ± 0.4 < 0.001 14
2min rec −1.44 0.30 −2.04 −0.84 −0.6 ± 0.3 < 0.001 38
6min 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
0W −1.50 0.29 −2.09 −0.91 −0.2 ± 0.3 < 0.001 40
50W −1.97 0.51 −2.98 −0.95 −0.7 ± 0.6 < 0.001 42
100W −2.47 0.48 −3.42 −1.52 −1.2 ± 0.5 < 0.001 41
150W −3.05 0.94 −4.93 −1.17 −1.8 ± 1 < 0.001 26
2min −1.76 0.41 −2.58 −0.93 −0.5 ± 0.4 < 0.001 40
6min −1.47 0.29 −2.05 −0.90 −0.2 ± 0.3 < 0.001 40
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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 etal. 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 etal. 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
etal. 2008; Forsey etal. 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
etal. 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
etal. 2015).
LV myocardial performance inrecovery
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 Table2). Equally, strain
rate, as the best measure of contractility, did not return to
baseline at 2 and 6min recovery (Table3), 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 (Table1).
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 etal. 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 andmetabolic 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 etal. 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 etal. 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 etal. 2002),
which was shown to be feasible and valid in children (May
etal. 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 etal. 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
etal. 1991), using the same hard- and software, protocol and
the same echocardiographer were established in our previous
pilot study (Pieles etal. 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 theDepartment 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/.
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