Download Comprehensive assessment of biventricular function and aortic

European Heart Journal – Cardiovascular Imaging (2013) 14, 1010–1020
doi:10.1093/ehjci/jes298
Comprehensive assessment of biventricular
function and aortic stiffness in athletes with
different forms of training by three-dimensional
echocardiography and strain imaging†
Antonio Vitarelli*, Lidia Capotosto, Giuseppe Placanica, Fiorella Caranci,
Mario Pergolini, Francesco Zardo, Francesco Martino, Stefania De Chiara,
and Massimo Vitarelli
Sapienza University, Cardiac Dept., Via Lima 35, 00198 Rome, Italy
Received 21 September 2012; accepted after revision 26 November 2012; online publish-ahead-of-print 8 January 2013
Previous studies have shown distinct models of cardiac adaptations to the training in master athletes and different
effects of endurance and strength-training on cardiovascular function. We attempted to assess left-ventricular (LV)
function, aortic (Ao) function, and right-ventricular (RV) function in athletes with different forms of training by
using three-dimensional (3D) echocardiography, tissue Doppler imaging (TDI) and speckle-tracking imaging (STI).
.....................................................................................................................................................................................
Methods
We examined 35 male marathon runners (endurance-trained athletes, ETA), 35 powerlifting athletes (strengthand results
trained athletes, STA), 35 martial arts athletes (mixed-trained athletes, MTA), and 35 sedentary untrained healthy
men (controls, CTR). Two-dimensional and three-dimensional echocardiography were performed for the assessment
of LV and RV systolic/diastolic function. LV and RV longitudinal strain (LS) and LV torsion (LVtor) were determined
using STI (EchoPAC BT11, GE-Ultrasound). Maximum velocity of systolic wall expansion peaks (AoSvel) was determined using TDI. ETA experienced LV eccentric hypertrophy with increased 3D LV end-diastolic volume and mass
and significant increase in peak systolic apical rotation and LVtor. In all groups of athletes, RV-LS was reduced at rest
and improved after exercise. AoSvel was significantly increased in ETA and MTA and significantly decreased in STA
compared with CTR. There were good correlations between LV remodelling and aortic stiffness values. Multivariate
analysis showed aortic wall velocities to be independently related to LV mass index.
.....................................................................................................................................................................................
Conclusion
In strength-trained, endurance-trained, and mixed-trained athletes, ventricular and vascular response assessed
by 3DE, TDI, and STI underlies different adaptations of LV, RV, and aortic indexes.
----------------------------------------------------------------------------------------------------------------------------------------------------------Keywords
Echocardiography † Athlete’s heart † Tissue Doppler imaging † Speckle tracking imaging † Three-dimensional
echocardiography † Ventricular function † Aortic function
Introduction
The haemodynamic load caused by long-term training involves
both cardiac ventricular chambers, inducing an increase in ventricular diameters, wall thickness, and mass. These changes are usually
described as ‘athlete’s heart’.1 – 3 Adaptations to exercise are
dependent on the specific type of training performed. Previous
†
studies4 – 6 have shown distinct models of cardiac adaptations to
the training in master athletes and different effects of endurance
and strength-training on cardiovascular function. Further
reports7 – 9 pointed out that the classification of left-ventricular
hypertrophy in athletes as eccentric or concentric is not an absolute or dichotomous concept but has to be considered a relative
Presented in part at Euroecho Meeting, Budapest, Hungary, 7–10 December 2011.
*Corresponding author. Tel: +39 6 85301427; Fax: +39 6 8841926, Email: [email protected]
Published on behalf of the European Society of Cardiology. All rights reserved. & The Author 2013. For permissions please email: [email protected]
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Aims
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Assessment of biventricular function and aortic stiffness in athletes
Methods
Population
We examined 35 male marathon runners (endurance-trained athletes,
ETA), 35 powerlifting athletes (strength-trained athletes, STA), and 35
martial arts athletes performing combined strength and endurance
training (mixed-trained athletes, MTA). All of them were athletes participating in an organized team or individual sport in which regular
competition was a component. Each athlete trained for .15 h/week
and had participated in competition for .6 years. Thirty-five sedentary
untrained healthy age-matched male adults were selected as a control
group. Both groups were free of heart and systemic diseases and took
no medications. Subjects with echocardiographic recordings of inadequate quality were excluded. Ethical approval was obtained.
Echocardiography
All patients underwent transthoracic echocardiography with a commercially available cardiovascular ultrasound system (Vivid E9, GE,
Horten, Norway). Measurements of cardiac chambers and aortic diameters were made according to established criteria.23 Left-ventricular
ejection fraction by modified biplane Simpson method and mass index
were estimated.23 – 25 Peak early (E) and late (A) diastolic velocities, deceleration time, left-ventricular isovolumic relaxation time, and myocardial performance index were obtained using standard Doppler
practices.26,27 Right-ventricular systolic pressure (RVSP) was determined by continuous wave Doppler echocardiography. Twodimensional measurements of aortic diameters were made at enddiastole in parasternal long-axis views at four levels: aortic annulus,
sinuses of Valsalva, sinotubular junction, and proximal ascending
aorta. Mitral and tricuspid annulus velocities (Sa, Ea, Aa) were measured
by tissue Doppler imaging on the transthoracic four-chamber views.
Three-dimensional echocardiography
Transthoracic examination was carried out with the patient lying in the
left lateral recumbent position. The echocardiographic system was
equipped with dedicated software for dynamic three-dimensional acquisition. Standard parasternal, apical, and subcostal views were
used. Three-dimensional images were saved in digital form on the
hard disk of the ultrasound scanner and subsequently analysed using
the EchoPAC view (BT11, GE Ultrasound). The left- and right- ventricular end-diastolic volumes (LVEDV, RVEDV) and ventricular endsystolic volumes (LVESV, RVESV) were measured from each threedimensional echocardiographic data set. Left- and right-ventricular
ejection fractions (LVEF and RVEF) were determined. The process of
volume determination was done two times for each patient. Papillary
muscles were not included in the volume estimation.
Speckle-tracking imaging
The general principles that underlie the STI modalities have been
previously described.17 After tracing endocardial border at an endsystolic frame, the operator could validate the tracking quality and
adjust the endocardial border or modify the width of the region of
interest. Aortic valve opening and closure were selected on pulsedwave Doppler tracings recorded from the LV outflow tract. Frame
rate ranged from 60 to 100 frame/s, and three cardiac cycles were
stored in cineloop format for offline analysis. Longitudinal LV strain
was defined as the average of negative longitudinal strains of six segments of the septal and lateral walls in the apical four-chamber view
(Figure 1A). Average radial and circumferential strain of six mid-LV
segments was determined in the mid-short-axis view. The assessment of LV rotation by 2D speckle-tracking strain imaging required
the acquisition of the LV short-axis at the basal and apical level.
The basal level was defined as that which showed the mitral valve
tip and the apical level as that which was just proximal to the level
with LV cavity obliteration at end-systole. The time rotation curves
were displayed along the cardiac cycle. Counterclockwise rotation
was conventionally marked as positive value and clockwise rotation
as negative value when viewed from the LV apex. Peak apical and
basal rotation and peak LV torsion were obtained. Left-ventricular
torsion or twist (LVtor) was defined as the net difference (in
degrees) of apical and basal rotation at isochronal time points. Normalized torsion was torsion divided by LV ventricular diastolic longitudinal length between apex and mitral plane. Peak diastolic
untwisting velocity and time-to-peak untwisting velocity were measured. Twisting rate (TR) was defined28 as (peak LVtor – LVtorEarlySystole)/(time difference between these two events). Untwisting
rate (UTR) was defined as (peak LVtor – LVtorMVO)/(time difference between these two events), where MVO is mitral valve
opening. The analysis of strain and rotation parameters was performed offline using customized computer software (EchoPAC
BT11, GE Ultrasound).
To assess regional and global RV systolic function in the longitudinal
direction, we adopted a six-segment RV model (basal RV lateral wall,
mid-RV lateral wall, apical RV wall, apical septum, mid septum, and
basal septum). Peak systolic strain was recorded for the six RV myocardial segments and the entire RV myocardium. Global strain and
strain rate were calculated by averaging local strains along the entire
right ventricle using machine software.
Aortic function
To assess aortic distensibility, echocardiographic tracings were
obtained using a two-dimensional guided M-mode evaluation of
systolic and diastolic aortic diameter, 3 cm above the aortic valve.
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concept, and a combined training of endurance and power can
produce an extreme volume and pressure load.
Moreover, in competitive athletes, left-ventricular hypertrophy
can mimic pathological conditions (systemic arterial hypertension
or hypertrophic cardiomyopathy) and this distinction may have
important implications, particularly in adults who practice
regular physical activity.10 Although standard Doppler echocardiography has been widely used to distinguish athlete’s heart by
pathological LV hypertrophy,11,12 there are scanty data in the literature on the relationship between ventricular function and arterial function in athletes. Even the new echocardiographic
techniques13 – 22 applied to the study of wall motion and ventricular volumes such as tissue Doppler imaging (TDI), speckletracking imaging (STI), and three-dimensional echocardiography
(3DE), which were used to analyse LV function in different
types of physiological and pathological hypertrophy, have produced limited data on left- and right-ventricular volumes and
aortic stiffness.
Accordingly, we attempted to assess systemic ventricular –vascular function and right-ventricular function in athletes with different forms of training by using TDI, STI, and 3DE in order to assess
(1) biventricular volumetry and function at rest and after stress; (2)
aortic stiffness and its relationship with left-ventricular remodelling,
and (3) advantages of these new technologies compared with
standard ones.
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A. Vitarelli et al.
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Figure 1 Application of echocardiographic techniques in an athlete. (A). Speckle-tracking imaging (STI) and LV longitudinal strain. (B). Ascending aortic wall TDI velocity profile: aortic wall peak systolic radial strain is derived from velocity data. AAo ¼ wall late diastolic velocity;
EAo ¼ wall early diastolic velocity; SAo ¼ wall systolic velocity.
The elastic properties of the aorta were indexed by calculation29 – 31 of
aortic distensibility (D), stiffness index (SI), and pressure– strain elastic
modulus (Ep) as D ¼ 2(As – Ad)/[Ad (Ps 2 Pd)], SI ¼ ln(Ps / Pd) / (As –
Ad)/Ad, and Ep ¼ (Ps – Pd)/[(As 2 Ad)/ Ad], respectively, where As,
aortic diameter at end-systole; Ad, aortic diameter at end-diastole;
Ps, systolic blood pressure; Pd, diastolic blood pressure; and ln,
natural logarithm.
Aortic wall TDI velocities have been obtained as previously
described.32 By marking a region of interest on the 2D image in the
anterior aspect of the ascending aorta at the same point as in
M-mode measurements, velocities throughout the cardiac cycle for
this area can be determined (Figure 1B). Offline analysis of the velocity
data sets was performed using dedicated software (EchoPAC BT11,
GE Ultrasound). Tissue Doppler imaging tracing displayed accelerated
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Assessment of biventricular function and aortic stiffness in athletes
Statistics
3D volumetry in athletes and controls
Data are presented as mean value + SD. Linear correlations, univariate
and multivariate analysis were used for comparisons. Variables were
compared between groups by Student’s t-test. Differences were considered statistically significant when the P-value was , 0.05. To analyse
intraobserver variability, measurements of 2D strain parameters were
made at multiple sites in different patients on two different occasions.
For interobserver variability, a second investigator randomly made
measurements at the above different sites without knowledge of
other echocardiographic parameters. The intraobserver and interobserver variabilities were determined as the difference between the
two sets of observations divided by the mean of the observations
and expressed as a percentage.
ETA and MTA experienced LV eccentric hypertrophy, characterized by increased LV end-diastolic volume and mass (Figure 2).
Three-dimensional LVEDV, LVESV, RVEDV, and RVESV were
enlarged in athletes compared with controls (Table 3).
A close association between 3D LV and RV end-diastolic volume
in the three groups of athletes was found (r ¼ 0.72, P , 0.001).
On multiple linear regression analysis, the body surface area,
type and duration of training, and LV end-diastolic volume were
the only independent determinants of RV end-diastolic volume
(F ¼ 73.2, P , 0.005).
Exercise stress-echo
TDI –STI parameters in athletes
and controls
Results
Intraobserver variability was 4.6 + 2.8% for 3D-LVEDV, 5.3 + 4.9%
for 3D-LVESV, 4.8 + 3.6% for 3D-RVEDV, 5.7 + 5.8% for
Table 1
LV diastolic function measurements such as mitral Ea and tricuspid
Ea were increased in athletes compared with the control group
(Table 3).
Age, anthropometric, and clinical characteristics of the study population
Controls (n 5 35)
ETA (n 5 35)
STA (n 5 35)
MTA (n 5 35)
P-value
...............................................................................................................................................................................
Age
Body surface area (cm2)
28.3 + 11.4
1.89 + 0.23
28.7 + 10.7
1.91 + 0.15
30.3 + 9.4
1.98 + 0.18
29.4 + 9.8
1.93 + 0.13
NS
NS
Body mass index (kg/m2)
22.4 + 2.4
22.7 + 2.6
23.4 + 3.1
22.9 + 2.5
0.05*
Training experience (years)
HR (bpm)
/
69.5 + 9.1
9.6 + 2.9
54.1 + 5.6
9.1 + 3.2
65.8 + 8.6
9.7 + 3.1
60.1 + 7.4
NS
,0.005†
SBP (mmHg)
120.6 + 7.2
121.9 + 6.8
129.1 + 7.4
123.2 + 7.1
0.03‡
DBP (mmHg)
Double product (SBP x HR)
75.2 + 5.7
7335 + 1253
71.3 + 5.4
6731 + 1249
76.3 + 4.8
8247 + 1459
70.9 + 4.6
7121 + 1231
NS
0.01‡
RVSP
21.6 + 6.2
28.4 + 7.3
23.4 + 6.5
27.6 + 7.6
0.05§
DBP, diastolic blood pressure; ETA, endurance-trained athletes; HR, heart rate; MTA, mixed-trained athletes; NS, not significant; RVSP, right-ventricular systolic pressure;
SBP, systolic blood pressure; STA, strength-trained athletes.
*STA vs. controls.
†
ETA vs. controls.
‡
STA vs. ETA, MTA, and controls.
§
ETA and MTA vs. controls.
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Exercise stress-echo test was undertaken by bicycle ergometry in
the supine position, with initial workload set at 25 W and 25 W
increments every 2 min. Heart rate and rhythm were continuously
recorded by 12-lead ECG, and blood pressure was measured manually
during the last 30 s of each stage by sphygmomanometry. The following functional and echocardiographic indexes were assessed at peak
effort: maximal HR, maximal systolic blood pressure (SBP), maximal
workload (number of Watts achieved by bicycle test), rate– pressure
product (maximal HR x maximal SBP), LVEF, annular early diastolic
velocity (Ea), left-ventricular longitudinal strain (LV LS), left-ventricular
torsion (LVtor), aortic wall systolic velocity (AoSvel), RVEF, rightventricular longitudinal strain (RV LS).
3D-RVESV, 7.9 + 3.3% for STI longitudinal strain, 9.7 + 5.4% for STI
strain rate, and 4.7 + 3.2% for AoSvel. Interobserver variability was
5.1 + 3.3% for 3D-LVEDV, 6.2 + 5.6% for 3D-LVESV, 5.4 + 3.1%
for 3D-RVEDV, 8.2 + 5.6% for 3D-RVESV, 9.6 + 4.1% for STI longitudinal strain, 15.8 + 6.4% for STI strain rate, and 5.9 + 4.2% for AoSvel.
With regard to the data obtained with exercise, intraobserver variability was 8.1 + 3.8% for 3D-LVEDV, 10.9 + 5.8% for 3D-LVESV,
8.6 + 4.4% for 3D-RVEDV, 11.3 + 6.1% for 3D-RVESV, 11.7 +
3.6% for STI longitudinal strain, 16.3 + 4.6% for STI strain rate, and
6.2 + 4.2% for AoSvel. Interobserver variability was 9.3 + 5.2% for
3D-LVEDV, 13.8 + 6.5% for 3D-LVESV, 9.9 + 4.5% for 3D-RVEDV,
14.9 + 7.8% for 3D-RVESV, 13.3 + 4.9% for STI longitudinal strain,
18.8 + 6.7% for STI strain rate, and 7.7 + 5.8% for AoSvel.
The overall feasibility of speckle-tracking echocardiography at
rest and peak stress was 94% and overall feasibility of 3D echocardiography was 87%.
The baseline age, anthropometric, and clinical characteristics are
given in Table 1. Mmode/2D findings are given in Table 2.
expansion of the aortic wall followed by a slow deceleration, a plateau, and
then a rapid deceleration into diastole. This trace represents the mean of
the instantaneous velocity spectrum. Systolic maximum wall expansion
velocity (AoSvel, cm/s), wall contraction early diastolic velocity (AoEvel,
cm/s), and wall peak systolic radial strain (AoS, %) were derived.
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Table 2
M-mode/2D findings in athletes and controls
Controls (n 5 35)
mean + SD
ETA (n 5 35)
mean + SD
STA (n 5 35)
mean + SD
MTA (n 5 35)
mean + SD
P-value
LVED (mm)
LVES (mm)
48.2 + 4.3
29.3 + 2.6
55.7 + 4.9*
31.2 + 3.4
49.1 + 4.3
28.5 + 2.8
51.3 + 3.8†
29.7 + 3.1
0.01*, 0.05†
NS
IVST (mm)
9.5 + 1.6
10.5 + 1.7
12.4 + 1.4
10.6 + 1.5
0.01‡
PWT (mm)
RWT
8.7 + 1.8
0.42 + 0.07
10.3 + 1.5
0.40 + 0.09
12.3 + 1.2
0.46 + 0.06
10.4 + 1.7
0.41 + 0.08
0.05‡
0.01‡
LVM (g)
129 + 23
189 + 25
159 + 26
182 + 29
,0.05§
115 + 18
179 + 22
143 + 20
164 + 24
,0.05*,†
65 + 5
64 + 7
65 + 5
67 + 4
Parameters
...............................................................................................................................................................................
LV
M-mode
2D
LVEDV (mL)
LVEF
NS
Aorta
M-mode
29.1 + 3.5
29.7 + 3.3
30.8 + 3.4
29.5 + 3.1
NS
25.6 + 3.2
3.44 + 1.12
26.3 + 3.7
3.83 + 0.82
27.5 + 3.6
6.14 + 1.85
26.4 + 3.2
4.09 + 0.82
NS
0.02‡
AoEM (kPa)
31.1 + 2.1
30.3 + 2.3
45.5 + 5.1
30.7 + 2.4
0.03‡
72.6 + 15.2
81.4 + 14.2
48.1 + 14.2
79.7 + 14.4
0.05‡
Ao-An (mm)
23.4 + 3.1
23.6 + 3.2
24.9 + 3.3
23.8 + 3.1
0.05||
Ao-SV (mm)
Ao-ST (mm)
33.1 + 3.5
28.2 + 3.6
32.7 + 3.4
29.2 + 3.4
37.6 + 3.8
32.3 + 3.3
34.1 + 3.3
28.6 + 3.5
0.05||
0.05||
AAo (mm)
32.4 + 3.1
32.9 + 3.2
34.5 + 3.1
32.6 + 3.3
0.05||
22.6 + 2.3
26.9 + 2.6
23.3 + 2.4
25.3 + 2.1
0.05*, 0.03†
15 + 5
24+4
16 + 5
21 + 5
0.05*, 0.03†
2
AoD (m /Newton)
2D
RV
M-mode
RVED (mm)
2D
RVEDA (mm2)
2
RVESA (mm )
RVFAC (%)
8+3
10 + 2
9+4
9+3
NS
42 + 8
41 + 6
38 + 5
40 + 7
NS
AAo, ascending aorta; Ao-An, aortic annulus; AoD, aortic distensibility; AoED, aortic end-diastolic diameter; AoEM, aortic elastic modulus; AoES, aortic end-systolic diameter;
AoSI, aortic stiffness index; Ao-ST, aortic sinotubular junction; Ao-SV, aortic sinuses of Valsalva; LVED, left-ventricular end-diastolic diameter; LVES, left-ventricular end-systolic
diameter; LVM, left-ventricular mass; IVST, interventricular septal thickness; NS, not significant; PWT, posterior wall thickness; RVED, right-ventricular end-diastolic diameter;
RVEDA, right-ventricular end-diastolic area; RVESA, right-ventricular end-systolic area; RVFAC, right-ventricular fractional area change; RWT, right wall thickness; LVEDV,
left-ventricular end-diastolic volume; LVEF, left-ventricular ejection fraction.
*ETA vs. controls.
†
MTA vs. controls.
‡
STA vs. controls.
§
ETA, STA, MTA vs. controls.
||
STA vs. ETA, MTA, and controls.
LV longitudinal strain increased from base to apex in all groups
of athletes. There was a significant increase in peak systolic apical
rotation and peak LVtor in ETA and MTA (Figure 2, Table 3).
Global RV STI longitudinal strain was significantly lower than
control group in all athletes and was especially reduced in basal
segments (Table 3). Right-ventricular systolic pressure (RVSP)
was obtained by tricuspid regurgitation in 79/105 athletes
(Table 1). In these athletes, there was a close relation between
RVSP and RV LS (r ¼ 20.76, P , 0.001).
TDI-derived indexes of Ao function and
correlation with LV function
Aortic diameters at all levels were significantly larger in STA than in
ETA, MTA, and controls (Table 2). Aortic wall velocities and strain
were significantly decreased in STA (P , 0.001) and significantly
increased in MTA (P , 0.05) and ETA (P ¼ 0.003) compared
with controls (Figure 2, Table 3). By univariate analysis there was
a good correlation between LV remodelling and aortic function
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AoES (mm)
AoED (mm)
AoSI
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Assessment of biventricular function and aortic stiffness in athletes
parameters (Figure 3). Multivariate analysis showed aortic wall velocities and strain to be independently related to the body surface
area, type and duration of training, and LV mass index (F ¼ 74.1,
P , 0.001).
Bicycle ergometric test
During maximal physical effort (Table 4), ETA and MTA showed a
better functional capacity compared with STA, with greater
maximal workload achieved with lower maximal heart rate and
systolic blood pressure. The baseline increase in peak systolic
apical rotation translated into a highly significant increase in peak
systolic LV torsion after exercise. Right-ventricular strain was
reduced at rest (Table 3) and improved after exercise (Table 4).
Decreased AoSvel values persisted in STA during maximal physical
effort (Table 4).
Discussion
To our knowledge, a study assessing comprehensively biventricular
function and aortic distensibility in athletes with different forms of
training with the use of 3DE and strain imaging has not been
reported. Novel findings of this study in athletes were the assessment of 3D RV –LV volumes, the assessment of behaviour of
RV –LV deformation and torsion parameters and assessment of
TDI aortic wall properties. In athletes subjected to purer
endurance-type training, we found eccentric hypertrophy characterized by increased LV end-diastolic volume and mass as well as
LV torsion. Aortic wall velocities and strain were significantly
increased in endurance athletes and significantly reduced in power-
trained athletes compared with controls. The martial arts athletes
performing combined strength and endurance training presented a
significant increase in left-ventricular end-diastolic volume and
torsion and aortic wall velocities and strain but with lower significance values when compared with endurance athletes. All athletes
had increased LV longitudinal strain and decreased RV longitudinal
strain. A good correlation was shown between left- and rightventricular volumes and between LV function and aortic
parameters.
LV and RV volumes
Marathon athletes, involved in a high dynamic component of
aerobic training, developed an increase in the size of left- and
right-ventricular chambers, with a proportional increase in LV
thickness and volume caused by volume overload, thus showing
eccentric LV hypertrophy. On the other hand, power athletes,
involved in exercises with predominantly anaerobic component,
showed an increase in LV wall thickness and relative wall thickness,
with a geometric pattern of concentric hypertrophy due to the
high systolic systemic blood pressure caused by this type of exercise. Recent studies7 – 9 considered that the classification of leftventricular hypertrophy in athletes as eccentric or concentric is
not an absolute or dichotomous concept but rather a relative
concept. It should also be noted that genetic factors as well as
the somatotype could play a significant role for the cardiac dimensions in addition to the body dimensions.33 In our study, athletes
of martial arts with mixed training developed an intermediate
pattern of adaptation with increased cardiac volumes albeit to a
lesser extent than marathon runners. The use of 3DE helped to
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Figure 2 Three-dimensional left-ventricular end-diastolic volume index (3D-LVEDVI) (A), LV mass index (LVMI) (B), LV torsion (LVtor) (C),
and aortic wall velocity (AoSvel, D) in controls (CTR), endurance-trained athletes (ETA), strength-trained athletes (STA), and martial arts
athletes (MTA). *P , 0.005, †P ¼ 0.01, ‡P ¼ 0.02, §P ¼ 0.05, ||P ¼ 0.01, #P ¼ 0.02, **P , 0.005 (all P-values vs. CTR).
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Table 3
3D, TDI, and STI values in athletes and controls
Controls (n 5 35)
mean + SD
Parameters
ETA (n 5 35)
mean + SD
STA (n 5 35)
mean + SD
MTA (n 5 35)
mean + SD
193 + 26
103 + 11
154 + 23
82 + 13
179 + 27
95 + 10
P-value
...............................................................................................................................................................................
LV
3D
3D-LVEDV (mL)
3D-LVEDVI (mL/m2)
126 + 21
64 + 14
,0.005*, 0.03†
,0.005*, 0.01†
63 + 7
64 + 6
64 + 5
65 + 7
124 + 25
69 + 17
178 + 30
107 + 15
149 + 22
93 + 11
167 + 28
104 + 12
0.03*, 0.05†
0.02*, 0.05†
12.2 + 2.3
5.5 + 1.4
20.3 + 4.2
2.7 + 0.9
14.7 + 2.6
2.4 + 0.7
18.8 + 4.4
2.3 + 0.8
0.01*, 0.04†
0.04*, 0.03†
Global LS (%)
Global RS (%)
220.3 + 2.6
48.9 + 9.7
221.7 + 2.6
46.9 + 9.4
222.5 + 2.4
49.6 + 8.5
221.6 + 2.2
47.5 + 8.7
,0.05‡
NS
Global CS (%)
224.7 + 3.4
222.9 + 3.3
224.1 + 2.7
222.6 + 3.6
NS
14.6 + 4.3
10.1 + 3.6
21.5 + 5.2
14.2 + 4.3
15.8 + 4.5
10.8 + 3.7
20.8 + 5.4
13.8 + 3.9
26.7 + 2.3
27.7 + 2.2
26.8 + 1.9
27.6 + 2.4
1.8 + 0.4
2.5 + 0.5
1.9 + 0.8
2.4 + 0.6
3D-LVEF
LVM (g)
LVMI (g/m2)
NS
TDI
MV Ea (cm/s)
MV E/Ea
STI
0.01*
0.05*
NS
0.03*
78.9 + 15
93.9 + 21
83.1 + 16
92.2 + 22
NS
16.5 + 7.1
20.3 + 8.3
17.5 + 5.3
19.4 + 6.7
NS
61.7 + 24
94.2 + 29
64.2 + 23
80.6 + 31
0.03*
AoSvel (cm/s)
AoEvel (cm/s)
6.2 + 0.4
7.2 + 0.8
7.2 + 0.6
7.5 + 0.8
4.7 + 0.3
4.3 + 0.6
6.8 + 0.5
7.7 + 0.4
0.04*, ,0.005†
0.04†
AoS (%)
8.5 + 1.4
9.9 + 1.6
5.5 + 1.3
9.6 + 1.3
0.02*, ,0.005†
77 + 19
115 + 12
96 + 12
112 + 17
0.01*, 0.03†
40 + 8
56 + 7
63 + 10
55 + 4
54 + 10
52 + 7
59 + 12
54 + 6
0.01*, 0.02†
NS
11.6 + 2.4
4.6 + 1.1
19.6 + 4.7
3.4 + 0.7
15.5 + 3.2
2.4 + 0.6
18.9 + 4.3
2.9 + 1.1
0.02*, ,0.05†
0.04*, 0.01†
RV Global LS (%)
RV FW Basal LS (%)
228.2 + 3.8
225.7 + 2.9
226.7 + 2.9
221.2 + 2.3
227.4 + 3.4
222.3 + 2.2
226.3 + 3.2
221.5 + 2.4
0.03*, ,0.05†
0.01*, 0.04†
RV FW Apical LS (%)
229.8 + 4.2
229.3 + 4.8
229.8 + 4.3
228.9 + 4.6
NS
Normalized time to peak
UTV (%)
UTR (degrees/s)
Aorta
RV
3D
3D-RVEDV (mL)
2
3D-RVEDVI (mL/m )
3D-RVEF
TDI
TV Ea (cm/s)
TV E/Ea
STI
AoEvel, aortic wall early diastolic velocity; AoS, aortic wall peak radial strain; AoSvel, aortic wall systolic velocity; CS, circumferential strain; E, mitral inflow early diastolic velocity;
Ea, annular early diastolic velocity; EF, ejection fraction; FW, free wall; LS, longitudinal strain; LV, left ventricle; LVM, left-ventricular mass; LVMI, left-ventricular mass index; LVtor,
left-ventricular torsion; MV, mitral valve; NS, not significant; RS, radial strain; RV, right ventricle; time to peak UTV, time to peak untwisting velocity (expressed as percentage of
duration of diastole); UTR, untwisting rate; UTV, untwisting diastolic velocity; TV, tricuspid valve; 3D-LVEDV, three-dimensional left-ventricular end-diastolic volume; 3D-LVEDVI,
three-dimensional left-ventricular end-diastolic volume index; 3D-LVEF, three-dimensional left-ventricular ejection fraction; 3D-RVEDV, three-dimensional right-ventricular
end-diastolic volume; RVEDVI, three-dimensional right-ventricular end-diastolic volume index; 3D-RVEF, three-dimensional right-ventricular ejection fraction.
*ETA and MTA vs. controls.
†
STA vs. controls.
‡
ETA, MTA, and STA vs. controls.
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Peak LVtor (degrees)
Peak apical rotation
(degrees)
Peak basal rotation
(degrees)
Normalized peak LVtor
(degrees/cm)
Peak UTV (degrees/s)
1017
Assessment of biventricular function and aortic stiffness in athletes
the ventricular septum, also causes deformation of RV walls as well
as RV pressure and relaxation rate changes.
LV and RV wall velocities and strain
assess left- and right-ventricular volumes and better characterize
different cardiovascular adaptations. This is in keeping with previous reports21 that showed that 3DE offers more detailed information on LV remodelling compared with 2DE since it takes into
account differences in the length and shape of the LV chamber
and provides data on LV geometry, function, and synchronicity
of contraction, differently from patients with hypertrophic or
dilated cardiomyopathy that do not show LV harmonic
remodelling.
Our results have also highlighted a close association between LV
and RV end-diastolic volumes in the three groups of athletes.
Multivariate analysis has provided additional information about
this association with adjustment for several confounding factors.
These independent associations point to a mutual dependency
between the two ventricles in the trained heart. Overload alterations may be highly obvious in athletes that represent a model of
extreme physiological haemodynamic load with a large increase
in training-induced LV stroke volume. Ventricular interaction is
the expression of the close anatomical association between the
two ventricles, which are surrounded by common muscle fibres,
share a septal wall, and are enclosed within the pericardium. Leftventricular volumetric expansion, changing the location and size of
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Figure 3 (A) Relation in all the athletes between threedimensional left-ventricular end-diastolic volume index
(3D-LVEDVI) and aortic wall velocity (AoSvel) determined by
TDI. (B) Relation in all the athletes between LV mass index
(LVMI) and AoSvel.
Tissue Doppler findings showed higher early diastolic myocardial
velocity and Ea/Aa ratio in LV and RV lateral walls in ETA and
MTA compared with controls confirming previous reports.14 – 16
These observed differences in biventricular diastolic behaviour
suggest a supernormal diastolic function of athlete’s heart. Since
peak velocity and Ea/Aa ratio are the expression of abnormal atrioventricular pressure gradient and passive diastolic properties of
ventricular walls, their increase in ETA and MTA suggests a
training-induced improvement of left- and right-ventricular
compliance.
LV longitudinal strain increased significantly from base to apex in
all groups of athletes. Previous studies have used STI to characterize both athlete’s heart and pathological hypertrophy.17,18 Both
global LS (cutoff point , 219%) and E/Ea ratio (cutoff point ≤
6.16) appeared to be accurate to discriminate between controls
and hypertensive patients, with E/Ea ratio being more sensitive
and GLS more specific.34 It is known that the ‘physiological’ hypertrophy in athletes shows increased ventricular mass and normal organization of cardiac structure with no increase in collagen
content, whereas hypertrophic cardiomyopathy is associated
with structural myofibrillar changes, collagen accumulation, and
potential systolic and diastolic dysfunction. In our athletes, longitudinal strain was higher compared with controls, whereas radial and
circumferential strains were not significantly different. This is consistent with previous studies that compared various types of LV
systolic deformation and found that the behaviour of longitudinal
systolic function of subendocardial fibres allowed to distinguish
trained athletes and patients with systemic hypertension.35
Left-ventricular torsion, a key determinant in LV function in
cardiac diseases, has recently been analysed in the setting of exercise.18,36 In addition to the systolic twist, the subsequent early diastolic untwisting is an important marker of LV filling. Differently
from patients with pathological LV hypertrophy who do not experience torsion/untwisting augmentation during exercise, LV
torsion and untwisting rate have been shown to increase during
laboratory-based submaximal exercise in healthy persons.18 In athletes, some discordant data have been reported and both
increased or decreased torsion after training have been described
depending on study population, study design, and measurement
technique.36 We found a different behaviour of LV torsion after exercise in endurance and strength athletes since in marathon and
martial arts athletes we found a baseline increase in peak systolic
apical rotation that translated into a highly significant increase in
peak systolic LV torsion after exercise. The same increase was
not shown in power athletes. The underlying mechanisms responsible for this heterogeneous response of LV torsion are not well
understood. Left-ventricular torsion results from a complex arrangement of wall myocardial fibres and its progressive increase
during effort could reflect a higher contribution of subepicardial
vs. subendocardial layers blunted by local ischaemia. Another explanation could be based on the regular decrease in LV enddiastolic diameters observed with exercise intensity that could
enhance subepicardial layers. The current uncertainty regarding
1018
Table 4
A. Vitarelli et al.
Changes of functional and echocardiographic parameters during maximal physical effort
ETA (n 5 35)
STA (n 5 35)
MTA (n 5 35)
CTR (n 5 35)
165.9 + 15. 4
180.2 + 13.7
168.8 + 12. 9
177.4 + 14. 2
0.04*, ,0.05†
Maximal SBP (mmHg)
Rate– pressure product (bpm × mmHg × 1023)
173.49 + 24.7
30.8 + 3.1
195.11 + 24.1
34.6 + 2.2
175.82 + 23.1
31.8 + 3.3
165.16 + 22.2
28.4 + 3.5
0.03*, 0.04†
0.03*, ,0.05†
Maximal workload achieved (W)
207.42 + 33.9
173.31 + 30.8
197.18 + 36.5
157.13 + 35.3
0.02*, 0.03†
68 + 8
22.2 + 3.7
67 + 5
16.1 + 3.3
67 + 9
21.6 + 3.8
66 + 4
15.2 + 2.9
224.2 + 3.3
225.1 + 2.7
226.5 + 2.4
224.9 + 2.5
23.8 + 4.7
7.4 + 0.5
16.9 + 4.6
5.3 + 06
23.6 + 4.9
6.9 + 0.7
17.2 + 4.5
6.7 + 0.5
Bicycle ergometer
P-value
...............................................................................................................................................................................
Maximal HR (bpm)
3D-LVEF
MV Ea (cm/s)
LV Global LS (%)
Peak LVtor (degrees)
AoSvel (cm/s)
3D-RVEF
TV Ea (cm/s)
RV Global LS (%)
60 + 9
22.1 + 3.5
228.9 + 2.9
58 + 6
18.1 + 4.3
229.7 + 2.6
59 + 8
21.7 + 3.8
229.3 + 2.7
59 + 7
14.8 + 4.4
230.2 + 2.5
NS
,0.05‡
NS
,0.05‡
,0.05§
NS
,0.05‡
NS
AoSvel, aortic wall systolic velocity; CTR, controls; Ea, annular early diastolic velocity; EF, ejection fraction; HR, heart rate; LS, longitudinal strain; LV, left ventricle; LVtor,
left-ventricular torsion; MV, mitral valve; NS, not significant; RV, right ventricle; SBP, systolic blood pressure; TV, tricuspid valve.
*ETA vs. STA.
†
MTA vs. STA.
‡
ETA and MTA vs. CTR.
§
STA vs. CTR.
For two-dimensional parameters, the greatest limitation was the
effective frame rate which compromised frame-to-frame tracking
of the fast contracting myocardium while for Doppler indices
cardiac translation due to respiration increased the noise-to-signal
ratio due to several artefacts. Although the superior temporal
resolution of Doppler modalities is an advantage for exercise measures allowing these techniques to be more sensitive to dynamic
changes, it has been shown39 they have a greater variability in
quantification of myocardial values at all levels of exercise compared with two-dimensional methods. As regards 3D echocardiography, the resolution of the images was not as high as that obtained
with conventional scanners, due to the lower frame rates that
limited its feasibility. Another strong limitation to feasibility and reproducibility was high heart rates reached at the peak of the stress
test. However, in this study as in previous reports,40 quantifications
of left-ventricular volumes were reproducible also when heart rate
was high or resting images of sub-optimal quality.
Ao wall velocities and strain
Elastic properties of the aorta29 are important factors supporting
LV function. The functions of the aorta are not only those of a
blood conduit for tissues, but also an important modulator of
the entire cardiovascular system, which hinder cardiac intermittent
pulsatile flow to provide a constant flow in the capillary bed. By
virtue of its elastic properties, the aorta influences left-ventricular
function and coronary flow. Previous studies5 have shown an increase in the elastic properties of these endurance athletes and
several cardiovascular adaptations in power athletes related to
intermittent elevations of blood pressure during exercise in
muscle strength. It was also suggested that in these athletes, the
transient increase in cardiac output associated with high elevation
of systemic blood pressure may cause a chronic increase in wall
tension responsible for aortic dilation and regurgitation. In a
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the significance of high resting LV torsion suggests that using these
parameters to differentiate physiological and pathological LV remodelling is not feasible at the present time. The examination of
LV torsion ‘reserve’ during exercise in athletes may provide
further insight in the future.
RV function assessment in athletes is important due to the possible overlap between athlete’s heart and ARVD especially in the
presence of ventricular arrhythmias. Long-lasting RV volume overload could be the mechanism contributing to the development of
RV structural changes leading to functional abnormalities. A
number of studies using 2D echocardiography have demonstrated
transient RV systolic dysfunction in response to high-intensity
sports activity such as marathon running.22,37,38 It has been suggested37 that the adaptation to volume and pressure stress might
spatially differ within the RV as a result of differences in wall
stress between the apical and the inflow tract and that the basal
portion of the RV might be more vulnerable and prone to preferential dilatation and reduced strain, or both. Our results are partially in concordance with these findings. The greater regional
heterogeneity in RV strain compared with controls was more pronounced in endurance vs. power athletes and this seems to be
related to increased pulmonary artery pressure as well as to ventricular dilatation. However, there was an improvement of RV
strain after exercise with a behaviour similar to control subjects.
One can speculate that these ‘normal’ responses would differ
from those seen in patients with RV disease (such as ARVD or pulmonary hypertension) but it remains to be demonstrated that RV
dysfunction is accentuated with exercise using these new echocardiographic techniques.
The quantification of strain and strain rate as well as 3D ejection
fraction during exercise has proved to be difficult in the present
study as in previous reports.39 – 41 However, offline STI analysis
was feasible in most subjects after strenuous levels of exercise.
1019
Assessment of biventricular function and aortic stiffness in athletes
Limitations
Some limitations should be pointed out. First, technical limitations
of strain Doppler echocardiography should be considered. A technical limitation is that speckle-tracking echocardiography is dependent both on frame rate and image resolution. In addition,
the endocardial border tracing must be manually optimized. We
found frame rates in the range of 60 –100 Hz suitable for speckletracking analysis, that is a lower value than frame rate available with
Doppler strain. However, STI may overcome some TDI limitations
by assessing myocardial thickening in a manner less affected by
passive translational motion or tethering.
Also we have not directly estimated the exact distance between
the two short-axis levels, which could have affected LV torsion
measurements, nor have we selected reproducible anatomic landmarks for measuring apical rotation although we defined the apical
level just proximal to the level with LV luminal obliteration at the
end-systolic period.46 Furthermore, only one vessel bed (ascending
aorta) was examined to assess aortic stiffness, whereas in different
points the arterial wall distensibility may be different. Last, the accuracy of 3D volume and EF is related to the effects of endocardial
trabeculae that play an important role in the intermodality discordances in LV volume measurements,2 and could certainly be
expected to affect RV measurements even more, since the RV is
more heavily trabeculated. Moreover, the accuracy of 3D volume
and EF is less certain in significantly dilated right ventricles since
limited data are available in the literature.
Conclusions
The combined application of 3DE, TDI, and STI has shown that
ventricular and vascular response underlie different adaptations
of ventricular volumes and arterial stiffness in strength-,
endurance-, and mixed-trained athletes. Future studies in this direction with a larger sample size and longitudinal study design will
certainly increase our knowledge of cardiovascular adaptation of
the athletes.
Conflict of interest: none declared.
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