Myocardial performance index in female athletes
Alsafi et al. Cardiovascular Ultrasound
Myocardial performance index in female athletes
Zahraa Alsafi 0 3
Andreas Malmgren 0 3
Petri Gudmundsson 2
Martin Stagmo 1
Magnus Dencker 0 3
0 Department of Medical Imaging and Physiology, Skåne University Hospital, Lund University , Malmö , Sweden
1 Department of Cardiology, Skåne University Hospital, Lund University , Lund , Sweden
2 Department of Biomedical Science, Malmö University , Malmö , Sweden
3 Department of Medical Imaging and Physiology, Skåne University Hospital, Lund University , Malmö , Sweden
Background: Long-term intensive training leads to morphological and mechanical changes in the heart generally known as “athlete's heart”. Previous studies have suggested that the diastolic and systolic function of the ventricles is unaltered in athletes compared to sedentary. The purpose of this study was to investigate myocardial performance index (MPI) by pulsed wave Doppler (PWD) and by tissue Doppler imaging (TDI) in female elite athletes compared to sedentary controls. Methods: The study consisted of 32 athletes (mean age 20 ± 2 years) and 34 sedentary controls (mean age 23 ± 2 years). MPI by PWD and TDI were measured in the left (LV) and right ventricle (RV) in both groups. Moreover, comparisons of MPI by the two methods and between the LV and RV within the two groups were made. Results: There were no significant differences in MPI between athletes and controls (p > 0.05), whereas the LV had significantly higher MPI compared to RV (p < 0.001, in athletes and controls). The agreement and the correlation between the two methods measuring MPI showed low agreement and no correlation (athletes RV r = −0.027, LV r = 0.12; controls RV r = 0.20, LV r = 0.30). Conclusion: The global function of the LV and RV measured by MPI with PWD and TDI is similar in female athletes compared to sedentary controls. Conversely, both MPI by PWD and by TDI shows a significant difference between the LV and RV. However, the agreement and correlation between conventional methods of measuring MPI by PWD compared to MPI by TDI is very poor in both these populations.
Athlete's heart; Diastolic function; Echocardiography; Left ventricle; Myocardial performance index; Right ventricle; Systolic function
Persistent vigorous training increases the need for
oxygenated blood to metabolic tissues in the body leading
to morphological and mechanical changes in the heart
generally known as “athlete’s heart” [
]. The function
of the athlete’s heart has not been extensively studied,
with regard to different sports and female gender.
Moreover, the function of the left ventricle (LV) has been
examined more than the right ventricle (RV) [
Sports can be divided into different categories but can
be classified in three main groups; dynamic, static or
combined (dynamic and static) sports [
Morphologic changes of the athlete’s heart are related to the type
of sport practised by the athlete but it is also related to
Myocardial performance index (MPI) is an easily
measured index for the assessment of global heart function,
combining both systolic and diastolic components. It can
be derived from both pulsed wave Doppler (PWD) and
tissue Doppler imaging (TDI) and is defined as the sum of
the isovolumic contraction time (ICT) and the isovolumic
relaxation time (IRT) divided by the ejection time (ET)
]. MPI has been shown to be independent of
HR, blood pressure, loading conditions and the geometry
of the ventricles [
11, 17, 20, 21
] and can be used to
evaluate the function of both the RV and the LV .
No studies up till now have, to our knowledge,
investigated MPI in both RV and LV in female athletes. For this
reason, the aim of this study was to gain further
understanding of the function of female athlete’s heart by
evaluating differences in conventional MPI and MPI by
TDI in elite female team-handball players compared to a
sedentary group of females.
The study consisted of 35 female elite team-handball
players (mean age 20 ± 2 years) and 34 sedentary
controls (mean age 23 ± 2 years). Of the 35 handball
players, two were excluded because of cardiovascular
disease, one because of a bicuspid aortic valve and one
because of a recent hospitalization of suspected
myocarditis. Another handball player was excluded due to
insufficient quality of echocardiographic image recording.
Hence, the final study population included a total of 32
female elite team-handball players. The females included
in the control group did not perform any or only slight
physical activity, less than two hours a week and were a
similar age to the handball players. Weight and height
were measured with participants dressed in light
clothing. Body mass index (BMI) was calculated as the weight
in kilograms divided by the height in meters squared
(kg/m2). The formula by Du Bois and Du Bois [
used for the calculation of BSA. Systolic (SBP) and
diastolic (DBP) blood pressure was measured in a supine
position in the right arm after 10 min rest (Omron M8
Comfort, Omron Healthcare, Kyoto, Japan). All
participants were given a written questionnaire to define their
amount of training during a week. The female elite
handball players trained in average 10.8 ± 2.3 h per
week, whereas 1.7 h were strength training and another
1.8 h per week were fitness training. The remaining of
the training time was used for team-game handball
training. Two of the participants in the control group
were smokers, while none of the athletes were
smokers. All participants gave their written informed
consent to take part in the study. The study was approved by
the Regional Ethical Review Board of Lund University in
Participants were examined using an iE33 (Philips Medical
systems, Andover, MA, USA) ultrasound equipment,
with an S3 transducer, according to current guidelines
by American Society of Echocardiography [
previously described [
]. The study was performed with
the participants resting in a left lateral decubitus
position. All measurements were performed three times
on separate cardiac cycles and averaged. One
experienced echocardiographer performed all examinations
and measurements were performed off-line by another
single observer using Xcelera (Philips Medical systems,
Andover, MA, USA).
Conventional pulsed wave Doppler
To derive MPI of RV (MPIRV) by conventional PWD, an
apical four-chamber view was obtained and the sample
volume was placed between the tips of the leaflets of the
tricuspid valve. An interval “a” was measured from the
end to the onset of tricuspid inflow and it represents the
sum of ICT, IRT and ET. The right ventricular ejection
time (RVET) was obtained from the short-axis view and
the sample volume was placed below the pulmonary valve.
The interval “b” that represents the RVET was measured
from the onset to the end of the RV outflow.
MPI of LV (MPILV) was measured from the apical
four-chamber view by placing the sample volume at the
tips of the mitral valve leaflets. From the end to the
onset of mitral inflow “a” interval was measured. From
the apical five-chamber view with the sample volume
placed below the aortic valve, “b” interval was measured
between onset and end of LV outflow. MPI was later
calculated as (a-b)/b, representing (ICT + IRT)/ET [
The mean differences of MPI by PWD and TDI were
tested between the two groups. Moreover, MPILV and
MPIRV were tested within each group.
Tissue Doppler imaging
MPI by TDI (TDMPI) was obtained from the apical
four-chamber view by placing the sample volume at the
lateral mitral annulus, lateral tricuspid annulus and
septal annulus. Measurements of TDI isovolumic
contraction time (tICT) were obtained by measuring from
the end of a′-wave (atrial-contraction wave) to the onset
of s-wave (myocardial systolic wave); TDI isovolumic
relaxation time (tIRT) was obtained by measuring between
the end of the S-wave and the onset of the e′-wave
(early-diastolic wave); TDI ejection time (tET) was
measured from onset to the end of s-wave (Fig. 1). TDMPI
was then calculated as (tICT + tIRT)/tET [
]. A mean
value was additionally calculated between TDMPI at
lateral mitral annulus (TDMPIlm) and TDMPI at septal
annulus (TDMPIs) that was named (mTDMPIm/s), and
also between TDMPI at lateral tricuspid annulus
(TDMPIlt) and TDMPIs, (mTDMPIt/s).
A comparison was made between all TDMPI parameters,
where TDMPIlm was compared to TDMPIs and to
TDMPIlt. Furthermore, TDMPIs was compared to TDMPIlt
and finally mTDMPIm/s compared to mTDMPIt/s. The
comparisons were made within each group but also the same
comparisons were made in both groups combined.
Because the echocardiographic measurements were
performed by one observer, intra variability measurements were
made in 5 subjects in the athletes group and 5 subjects in the
sedentary control group. The intra variability measurements
in the athlete group in MPIRV was 7,6%, MPILV 9,2%,
TDMPIlm 6,4%, TDMPIs 7,3%, TDMPIlt 4,4%, TDMPIm/s
5% and TDMPIt/s 5,6%. In the sedentary group MPIRV was
8%, MPILV 3,4%, TDMPIlm 3,7%, TDMPIs 2,8%, TDMPIlt
3,2%, TDMPIm/s 1,6% and TDMPIt/s was 2,0%.
All statistical analyses were performed using standard
statistical software (SPSS version 22.0, Inc., Chicago, IL,
USA). Data are expressed as mean ± standard deviation
(SD). The data was tested for normal distribution, by a
visual analysis of histograms and by a Q-Q plot, which
showed a normal distributed material. The independent
Student’s t-test was used to test for mean differences
between the two groups. The paired Student’s t-test was
used to test for mean differences between different
parameters within a group. Bland-Altman plots were used
to test the agreement between the conventional MPI by
PWD and TDMPI. The correlation between the two
methods was tested with Pearson’s correlation
coefficient. Values were considered statistically significant at a
p-value below 0.05.
The acquired images were of good quality in all subjects,
which made all planned measurements possible. All
demographics and subject characteristics are presented
in Table 1. The study population consisted of totally 66
participants, 32 athletes and 34 sedentary controls. Age,
length, weight, BMI, BSA, DBP and HR were
significantly different between the two groups. There were no
significant differences in SBP and MPI data between
athletes and controls.
MPIRV compared to MPILV showed a significant
difference in the athletes group as well as in the sedentary
group. The results are displayed in Table 2.
Heart rate (beats/min) 56 ± 8
SBP (mm Hg)
DBP (mm Hg)
Data values are presented as mean ± SD
Body mass index (BMI), Body surface area (BSA), Diastolic blood pressure
(DBP), Systolic blood pressure (SBP), Mean value of tissue Doppler myocardial
performance index derived from lateral mitral annulus and septum
(mTDMPIm/s), Mean value of tissue Doppler myocardial performance index
derived from lateral tricuspid annulus and septum (mTDMPIt/s), Conventional
myocardial performance index of left ventricle (MPILV), Conventional
myocardial performance index of right ventricle (MPIRV), Myocardial
performance index by tissue Doppler of lateral mitral annulus (TDMPIlm),
Myocardial performance index by tissue Doppler of lateral tricuspid annulus
(TDMPIlt), Myocardial performance index by tissue Doppler of
All TDMPI parameters were compared to each other
in both groups and all parameters showed a significant
difference except for two in the athletes group, TDMPIlm
compared to TDMPIlt. Likewise, TDMPIm/s compared to
TDMPIt/s in the athletes group did not show any
difference. When both athletes group and sedentary group were
put together, all parameters showed a significant
difference. All results are displayed in Tables 3 and 4.
The Bland and Altman analysis illustrated in Fig. 2 shows
a clinically important disagreement between the
conventional MPI by PWD and MPI by TDI. Figure 2
demonstrates a comparison between MPIRV and TDMPIRV in
athletes (the mean difference was 0.21 and 95% limits of
agreement from −0.08 to 0.29) and in the sedentary
controls MPIRV compared to TDMPIRV showed a mean
difference of 0.25 (95% limits of agreement from −0.018 to
0.50). A comparison between MPILV and TDMPILV in
athletes (the mean difference was 0.12 and 95% limits of
agreement from −0.06 to 0.29) and in the sedentary
controls MPILV compared to TDMPILV showed a mean
difference of 0.17 (95% limits of agreement from −0.015 to 0.35).
We found no statistically significant correlation between
the two methods measured in both RV (r = −0.027) and
LV (r = 0.12) in the athletes group and RV (r = 0.20) and
LV (r = 0.30) in the sedentary controls.
Data values are presented as mean ± SD
Mean value of tissue Doppler myocardial performance index derived from
lateral mitral annulus and septum (mTDMPIm/s), Mean value of tissue Doppler
myocardial performance index derived from lateral tricuspid annulus and
septum (mTDMPIt/s), Myocardial performance index by tissue Doppler of
lateral mitral annulus (TDMPIlm), Myocardial performance index by tissue
Doppler of lateral tricuspid annulus (TDMPIlt), Myocardial performance index
by tissue Doppler of septum (TDMPIs)
Athletes: A vs B p = 0.001, A vs C p = 0.16, B vs C p = < 0.001, D vs E p = 0.15.
Sedentary: A vs B p = 0.001, A vs C p = 0.045, B vs C p = < 0.001, D vs
E p = 0.03
Mean ± SD
0.48 ± 0.07
0.53 ± 0.08
This is the first report, to our knowledge, on MPI in
female athletes and also the first to measure MPI in both
LV and RV. This study has demonstrated that there is no
significant difference in conventional MPI by PWD and
TDMPI between female elite team-handball players and
sedentary controls. We have also shown that
conventional MPI by PWD is significantly higher in LV
compared to RV in both groups.
Team-handball is classified as a highly dynamic and
moderate static sport, thus combining static and
dynamic training, which has more
morphological/structural effects on the heart compared to other sports [
The cardiac dimensions of our study population have
previously been examined by Malmgren and co-workers
], who showed a significant enlargement of cardiac
dimensions in female elite team-handball players
compared to sedentary controls. Thus, showing that cardiac
remodelling appears in elite female handball players as it
does in athletes practicing endurance or team game
]. Hence, our findings are supported in the
study of Dzudie et al. [
] that included 21 male
teamhandball players and 21 male controls showing
morphological changes between the group of athletes compared
to the control group but no difference in the LV diastolic
function or ejection fraction (EF) between the two
groups. In the meta-analysis by Pluim et al. [
relation between cardiac geometry and cardiac systolic
and diastolic function could be found in athletes.
Furthermore, no differences in cardiac systolic and
diastolic function between athletes and sedentary
controls were demonstrated [
]. Additionally, Butz and
] studied the morphologic cardiac changes
by echocardiography in 100 male professional handball
players and reported a degree of hypertrophy and
increased LV mass and end diastolic diameter in their
study population [
]. However, they could not show
any differences in diastolic function, nor in systolic or
early diastolic velocities. Hence the results of the
mentioned studies are similar to ours showing no significant
difference in MPI between athletes and controls.
This current study did not show any difference in
MPILV nor MPIRV between the two groups, which is in
disagreement with the study by Kasikcioglu et al. [
that involved 52 male athletes whereas 30 athletes were
runners and 32 wrestlers, and a group of 43 sedentary
controls. The study stated a significant difference in
MPIRV between the athletes and the controls, showing a
lower MPI at the RV of athletes compared to controls.
Moreover, the study of Tüzün and co-workers [
included 66 elite male athletes (36 sprinters and 30
endurance athletes) and 33 sedentary controls were able
to demonstrate a significant difference in MPILV
between athletes and controls. MPI was reported as
0.37 ± 0.07 in sprinters and 0.36 ± 0.05 in endurance
athletes and these results corresponds to our value of
MPILV in athletes, which was reported as 0.35 ± 0.07.
However, the value of MPI in the sedentary controls in
both studies mentioned [
] is much higher and does
not correspond to ours. Also, their results does not
correspond to earlier studies where the normal range for
MPI was reported as 0.34 ± 0.04 in healthy volunteers
by Moller et al. . Previous studies have reported
more effect on male athlete’s heart compared to females
]. Furthermore, this present study consisted of a
lower number of participants compared to the study by
Kasikcioglu et al. , which may be a limitation in the
possibility of reporting a significant difference between
the two groups. Besides, the male athletes in the
mentioned study [
] trained as a minimum 10 h per week
for at least 8 years. The athletes in our study had been
training at elite level from 0 to 8 years. The significant
difference in RV in the male athletes could have been
caused by training for a longer period of time compared
to the female athletes of this current study.
In both athletes and sedentary controls there is a
significant difference in MPI by PWD between LV and RV.
This difference may exist due to the different shape and
geometry between the LV and the RV. The size of the
RV is about two-thirds the size of the LV [
] and the
RV wall is thinner (2–5 mm) compared to the wall of
the LV (7–11 mm) [
]. Also, the LV has a twisting and
rotating motion when contracting, while the twisting
and rotating motion does not contribute to the
contraction of the RV [
]. Besides, the pressure in the RV
reaches an early peak compared to the LV and also a
rapid decline in pressure. This is due to the low
pulmonary artery diastolic pressure that the RV needs to exceed
while contracting and therefore the ICT is shorter in RV
compared to LV. The filling in RV starts before the LV
and finishes after and also the IRT is shorter in RV
compared to LV [
]. All of these different characters of LV
and RV may be a reason of the significant difference
between the ventricles seen in MPI by PWD. However,
even though there are differences between the ventricles,
they still generally pump the same effective stroke
When TDMPI parameters were compared to one
another in each group separately, all comparisons showed a
significant difference in the sedentary control group.
Although in the athletes group the TDMPIlm compared to
TDMPIlt did not show any significant difference, neither
did mTDMPIm/s compared to mTDMPIt/s. As seen in
Table 3 the p-values in both groups follow the same
pattern, whereas the p-value of TDMPIlm compared to
TDMPIlt and mTDMPIm/s compared to mTDMPIt/s
shows a weak significance in the sedentary controls.
Consequently, since all other result were similar between both
groups as well as the fact that all participants are young
healthy subjects, they were all merged as a group to make
the same comparisons. The results of this analysis are
presented in Table 4 showing a significant difference between
all TDMPI parameters. This indicates that TDMPI
measured at the mitral, tricuspid and septal annulus is
significantly different in all young and healthy subjects. These
findings are similar to our findings presented from the
conventional MPI by PWD that showed a difference in
MPI between the two ventricles. Both LV and RV affect the
septal annulus and therefore a significant difference is seen
when comparing mTDMPIm/s and mTDMPIt/s. The
different characters mentioned previously between the
ventricles, also support these results showing a difference
between LV and RV. The study by Rojo et al. [
included 77 patients with a previous myocardial infarction
and a control group of 20 healthy young subjects, TDMPI
was measured at septal annulus and lateral mitral annulus
and additionally a mean value between those two
measurements was calculated. In the healthy control group
TDMPIlm compared to TDMPIs did not show any
significant difference while in the present study there is a
significant difference. The current study has a larger number of
subjects included, which may be an explanation of that.
The results of this study have not been adjusted for age
even though there was a significant difference in age
between the athletes and the sedentary controls. Normally,
the vascular stiffening is increased from the age of 30 and
onward in both male and females [
]. The stiffening
mostly affects the diastolic function of the LV, whereas the
early diastolic filling rate decreases after the age of 20, so
that by the age of 80, the early diastolic filling rate is
declined to nearly 50% [
]. Since both groups are healthy
young people, mostly in their early twenties, the
adjustment for age was not considered to be of any significance.
The HR of athletes was significantly lower compared to
the sedentary controls, but no adjustment for HR was
made in this study. The reason is that MPI has been
established to be independent of HR in a study by Tei et al.
] consisting of 37 normal subjects and 26 patients with
primary pulmonary hypertension. In that study, HR was
correlated with each Doppler parameter in normal
subjects and patients with primary pulmonary hypertension.
The results showed a significant correlation between HR
and ICT, IRT and ET. Though, there was no significant
association between HR and MPI [
Keser et al. [
] showed a good correlation between
the two methods measuring MPI and suggested the use
of TDI when measuring MPI. This is due to the
superiority of the methods’ sensitivity in not being affected by
HR fluctuations. Also Harada et al. [
] showed very
good correlation between the two methods. However,
more recent studies have presented moderate to low
correlation between the conventional way of measuring
MPI and the modified method by TDI. Rojo et al. [
suggested that the modified MPI by TDI is not possible to
be used as an alternative to the conventional MPI by
PWD due to the weak correlation between the two
methods. The present study consisting of a higher number
of participants compared to previously mentioned studies
did not show any correlation between the two methods of
measuring MPI and the agreement between the methods
was shown to be low. Our findings are similar to those of
Rojo et al. [
] that showed poor agreement between the
methods due to longer systolic intervals and shorter
diastolic intervals when measuring with TDI.
Furthermore, the Bland-Altman plots in Fig. 2 shows
that the TDI measurements always show higher MPI
values compared to measuring with PWD. These
findings can be supported by the fact that the upper
reference limit of MPI by PWD is 0.40, while the upper
reference limit of TDMPI is 0.55 [
]. The difference
between the two methods is that TDMPI is measured in
one cardiac cycle, while the inflow and outflow velocities
in left ventricle outflow tract and right ventricle outflow
tract measured by the PWD are not possible to measure
from the same cardiac cycle [
]. This might explain
that no correlation was seen between the two methods.
Moreover, newer echocardiographic methods exist to
evaluate LV and RV function in athletes. Vitarelli and
] used TDI, speckle-tracking imaging
(STI) and three-dimensional echocardiography to assess
systemic ventricular-vascular function and RV function
in athletes. They showed that ventricular and vascular
response in athletes underlie different adaptations of
ventricular volumes and arterial stiffness. STI was also used
by Oxborough et al. [
] to estimate RV structure and
function in ultra-endurance athletes and determine whether
changes in the RV are correlated with alterations in LV
function. The study could demonstrate that there is a RV
dilatation and dysfunction in the recovery after an
ultramarathon. Likewise LV systolic and diastolic function also
is reduced after an ultramarathon which is believed to be a
result of a combination of essential reduction in function
and RV interaction. Additionally, Knackstedt et al. [
STI in former world class swimmers to evaluate the cardiac
function, employing longitudinal strain and
circumferential strain. The results of their study are in concordance
with ours, showing that there is no definite LV or RV
dysfunction in athletes using modern imaging modalities.
The limitation of measuring MPI in the conventional way
by PWD is that the inflow and outflow velocities are
measured separately. The reproducibility of the method is
therefore reduced and is also affected by fluctuations in
the HR during the examination. This makes the
calculation of the index more complex, because several cardiac
cycles have to be obtained to average the measurements.
The global function of the LV and RV measured by MPI
with PWD and TDI is similar in female elite team-handball
players compared to sedentary controls. Conversely, both
MPI by PWD and TDMPI shows a significant difference
between LV and RV, whereas LV has higher MPI compared
to RV. However, the agreement and correlation between
conventional methods of measuring MPI by PWD
compared to TDMPI is not good and therefore TDMPI should
not be used interchangeably with MPI by PWD.
BMI: Body Mass Index; BSA: Body surface area; EF: Ejection fraction;
ET: Ejection time; HR: Heart rate; ICT: Isovolumic contraction time;
IRT: Isovolumic relaxation time; LV: Left ventricle; MPI: Myocardial
performance index; MPI_LV: Myocardial performance index of left ventricle;
MPI_RV: Myocardial performance index of right ventricle; MRI: Magnetic
resonance imaging; mTDMPI_m/s: mean value of myocardial performance
index by tissue Doppler measured at lateral mitral annulus and septal
annulus; mTDMPI_t/s: mean value of myocardial performance index by tissue
Doppler measured at lateral tricuspid annulus and septal annulus;
PWD: Pulsed wave Doppler; RV: Right ventricle; RVET: Right ventricular
ejection time; SD: Standard deviation; STI: Speckle tracking imaging;
SV: Stroke volume; TDI: Tissue Doppler imaging; TDMPI: Myocardial
performance index by tissue Doppler; TDMPI_lm: Myocardial performance
index by tissue Doppler at lateral mitral annulus; TDMPI_lt: Myocardial
performance index by tissue Doppler at lateral tricuspid annulus;
TDMPI_s: Myocardial performance index by tissue Doppler at septal annulus;
tET: Ejection time by tissue Doppler; tICT: Isovolumic contraction time by
tissue Doppler; tIRT: Isovolumic relaxation time by tissue Doppler
Availability of data and materials
All data generated or analysed during this study are included in this
The authors’ contributions were as follows: All authors designed the study.
AM was responsible for recruiting the subjects and performed all
examinations on both groups. ZA made all measurements on the
echocardiographic images and interpreted the patient data to evaluate the
global heart function using PWD and TDI and made all statistical
calculations. ZA wrote the first draft of the manuscript. AM, PG, MD and MS
were major contributors in writing the manuscript. All authors made critical
revisions of the manuscript. All authors read and approved the final
Ethics approval and consent to participate
This study was approved by the Regional Ethical Review Board, Lund,
Sweden. All participants gave their written informed agreement to take part
in the study. Reference number 2012/77.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Submit your next manuscript to BioMed Central
and we will help you at every step:
1. Pluim BM , Zwinderman AH , van der Laarse A , van der Wall EE . The athlete's heart. A meta-analysis of cardiac structure and function . Circulation . 2000 ; 101 ( 3 ): 336 - 44 .
2. Wernstedt P , Sjostedt C , Ekman I , Du H , Thuomas KA , Areskog NH , et al. Adaptation of cardiac morphology and function to endurance and strength training. A comparative study using MR imaging and echocardiography in males and females . Scand J Med Sci Sports . 2002 ; 12 ( 1 ): 17 - 25 .
3. Dzudie A , Menanga A , Hamadou B , Kengne AP , Atchou G , Kingue S . Ultrasonographic study of left ventricular function at rest in a group of highly trained black African handball players . Eur J Echocardiogr . 2007 ; 8 ( 2 ): 122 - 7 .
4. Mitchell JH , Haskell W , Snell P , Van Camp SP. Task Force 8: classification of sports . J Am Coll Cardiol . 2005 ; 45 ( 8 ): 1364 - 7 .
5. Pelliccia A , Maron BJ , Di Paolo FM , Biffi A , Quattrini FM , Pisicchio C , et al. Prevalence and clinical significance of left atrial remodeling in competitive athletes . J Am Coll Cardiol . 2005 ; 46 ( 4 ): 690 - 6 .
6. Sharma S. Athlete's heart-effect of age, sex, ethnicity and sporting discipline . Exp Physiol . 2003 ; 88 ( 5 ): 665 - 9 .
7. Pelliccia A , Culasso F , Di Paolo FM , Maron BJ . Physiologic left ventricular cavity dilatation in elite athletes . Ann Intern Med . 1999 ; 130 ( 1 ): 23 - 31 .
8. Pelliccia A , Maron BJ , Spataro A , Proschan MA , Spirito P. The upper limit of physiologic cardiac hypertrophy in highly trained elite athletes . N Engl J Med . 1991 ; 324 ( 5 ): 295 - 301 .
9. Barbier J , Ville N , Kervio G , Walther G , Carre F . Sports-specific features of athlete's heart and their relation to echocardiographic parameters . Herz . 2006 ; 31 ( 6 ): 531 - 43 .
10. Miller D , Farah MG , Liner A , Fox K , Schluchter M , Hoit BD . The relation between quantitative right ventricular ejection fraction and indices of tricuspid annular motion and myocardial performance . J Am Soc Echocardiogr . 2004 ; 17 ( 5 ): 443 - 7 .
11. Tei C , Dujardin KS , Hodge DO , Bailey KR , McGoon MD , Tajik AJ , et al. Doppler echocardiographic index for assessment of global right ventricular function . J Am Soc Echocardiogr . 1996 ; 9 ( 6 ): 838 - 47 .
12. Pagourelias ED , Kouidi E , Efthimiadis GK , Deligiannis A , Geleris P , Vassilikos V . Right atrial and ventricular adaptations to training in male Caucasian athletes: an echocardiographic study . J Am Soc Echocardiogr . 2013 ; 26 ( 11 ): 1344 - 52 .
13. Su HM , Lin TH , Voon WC , Lee KT , Chu CS , Lai WT , et al. Differentiation of left ventricular diastolic dysfunction, identification of pseudonormal/restrictive mitral inflow pattern and determination of left ventricular filling pressure by Tei index obtained from tissue Doppler echocardiography . Echocardiography . 2006 ; 23 ( 4 ): 287 - 94 .
14. Tei C , Nishimura RA , Seward JB , Tajik AJ . Noninvasive Doppler-derived myocardial performance index: correlation with simultaneous measurements of cardiac catheterization measurements . J Am Soc Echocardiogr . 1997 ; 10 ( 2 ): 169 - 78 .
15. Keser N , Yildiz S , Kurtog N , Dindar I. Modified TEI index: a promising parameter in essential hypertension? Echocardiography . 2005 ; 22 ( 4 ): 296 - 304 .
16. Tei C , Ling LH , Hodge DO , Bailey KR , Oh JK , Rodeheffer RJ , et al. New index of combined systolic and diastolic myocardial performance: a simple and reproducible measure of cardiac function-a study in normals and dilated cardiomyopathy . J Cardiol . 1995 ; 26 ( 6 ): 357 - 66 .
17. Harada K , Tamura M , Toyono M , Yasuoka K. Comparison of the right ventricular Tei index by tissue Doppler imaging to that obtained by pulsed Doppler in children without heart disease . Am J Cardiol . 2002 ; 90 ( 5 ): 566 - 9 .
18. Rojo EC , Rodrigo JL , Perez de Isla L , Almeria C , Gonzalo N , Aubele A , et al. Disagreement between tissue Doppler imaging and conventional pulsed wave Doppler in the measurement of myocardial performance index . Eur J Echocardiogr . 2006 ; 7 ( 5 ): 356 - 64 .
19. Gaibazzi N , Petrucci N , Ziacchi V . Left ventricle myocardial performance index derived either by conventional method or mitral annulus tissueDoppler: a comparison study in healthy subjects and subjects with heart failure . J Am Soc Echocardiogr . 2005 ; 18 ( 12 ): 1270 - 6 .
20. Carluccio E , Biagioli P , Alunni G , Murrone A , Zuchi C , Biscottini E , et al. Improvement of myocardial performance (Tei) index closely reflects intrinsic improvement of cardiac function: assessment in revascularized hibernating myocardium . Echocardiography . 2012 ; 29 ( 3 ): 298 - 306 .
21. Tei C , Dujardin KS , Hodge DO , Kyle RA , Tajik AJ , Seward JB . Doppler index combining systolic and diastolic myocardial performance: clinical value in cardiac amyloidosis . J Am Coll Cardiol . 1996 ; 28 ( 3 ): 658 - 64 .
22. Vonk MC , Sander MH , van den Hoogen FH, van Riel PL , Verheugt FW , van Dijk AP. Right ventricle Tei-index: a tool to increase the accuracy of noninvasive detection of pulmonary arterial hypertension in connective tissue diseases . Eur J Echocardiogr . 2007 ; 8 ( 5 ): 317 - 21 .
23. Arnlov J , Lind L , Andren B , Riserus U , Berglund L , Lithell H . A Dopplerderived index of combined left ventricular systolic and diastolic function is an independent predictor of cardiovascular mortality in elderly men . Am Heart J . 2005 ; 149 ( 5 ): 902 - 7 .
24. Lind L , Andren B , Arnlov J . The Doppler-derived myocardial performance index is determined by both left ventricular systolic and diastolic function as well as by afterload and left ventricular mass . Echocardiography . 2005 ; 22 ( 3 ): 211 - 6 .
25. Du Bois D , Du Bois EF. A formula to estimate the approximate surface area if height and weight be known . 1916 . Nutrition. 1989 ; 5 ( 5 ): 303 - 11 .
26. Rudski LG , Lai WW , Afilalo J , Hua L , Handschumacher MD , Chandrasekaran K , et al. Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography . J Am Soc Echocardiogr . 2010 ; 23 ( 7 ): 685 - 713 .
27. Malmgren A , Dencker M , Stagmo M , Gudmundsson P . Cardiac dimensions and function in female handball players . J Sports Med Phys Fitness . 2015 ; 55 ( 4 ): 320 - 8 .
28. Butz T , van Buuren F , Mellwig KP , Langer C , Oldenburg O , Treusch KA , et al. Systolic and early diastolic left ventricular velocities assessed by tissue Doppler imaging in 100 top-level handball players . Eur J Cardiovasc Prev Rehabil . 2010 ; 17 ( 3 ): 342 - 8 .
29. Kasikcioglu E , Oflaz H , Akhan H , Kayserilioglu A . Right ventricular myocardial performance index and exercise capacity in athletes . Heart Vessel . 2005 ; 20 ( 4 ): 147 - 52 .
30. Tuzun N , Ergun M , Alioglu E , Edem E , Tengiz I , Aytemiz F , et al. TEI Index in elite sprinters and endurance athletes . J Sports Med Phys Fitness . 2015 ; 55 ( 9 ): 988 - 94 .
31. Moller JE , Poulsen SH , Egstrup K. Effect of preload alternations on a new Doppler echocardiographic index of combined systolic and diastolic performance . J Am Soc Echocardiogr . 1999 ; 12 ( 12 ): 1065 - 72 .
32. Bleeker GB , Steendijk P , Holman ER , Yu CM , Breithardt OA , Kaandorp TA , et al. Assessing right ventricular function: the role of echocardiography and complementary technologies . Heart . 2006 ; 92 ( Suppl 1 ): i19 - 26 .
33. Auger DA , Zhong X , Epstein FH , Spottiswoode BS . Mapping right ventricular myocardial mechanics using 3D cine DENSE cardiovascular magnetic resonance . J Cardiovasc Magn Reson . 2012 ; 14 : 4 .
34. Haddad F , Hunt SA , Rosenthal DN , Murphy DJ . Right ventricular function in cardiovascular disease, part I: anatomy, physiology, aging, and functional assessment of the right ventricle . Circulation . 2008 ; 117 ( 11 ): 1436 - 48 .
35. Hollingsworth KG , Blamire AM , Keavney BD , Macgowan GA . Left ventricular torsion, energetics, and diastolic function in normal human aging . Am J Physiol Heart Circ Physiol . 2012 ; 302 ( 4 ): H885 - 92 .
36. Vitarelli A , Capotosto L , Placanica G , Caranci F , Pergolini M , Zardo F , et al. Comprehensive assessment of biventricular function and aortic stiffness in athletes with different forms of training by three-dimensional echocardiography and strain imaging . Eur Heart J Cardiovasc Imaging . 2013 ; 14 ( 10 ): 1010 - 20 .
37. Oxborough D , Shave R , Warburton D , Williams K , Oxborough A , Charlesworth S , et al. Dilatation and dysfunction of the right ventricle immediately after ultraendurance exercise: exploratory insights from conventional two-dimensional and speckle tracking echocardiography . Circ Cardiovasc Imaging . 2011 ; 4 ( 3 ): 253 - 63 .
38. Knackstedt C , Hildebrandt U , Schmidt K , Syrocki L , Lang A , BjarnasonWehrens B , et al. Analysis of right and left ventricular deformation in former world class swimmers: evaluation using speckle tracking . J Sports Med Phys Fitness . 2015 ; 55 ( 9 ): 978 - 87 .