International  Journal  of
Environmental Research
and Public Health
Article
Right Ventricular Diastolic Dysfunction
after Marathon Run
Zuzanna Lewicka-Potocka 1,2
, Alicja D ˛abrowska-Kugacka 1,*
, Ewa Lewicka 1
,
Rafał Gał ˛aska 2, Ludmiła Daniłowicz-Szymanowicz 1, Anna Faran 1,
Izabela Nabiałek-Trojanowska 1,2
, Marcin Kubik 1, Anna Maria Kaleta-Duss 1
and Grzegorz Raczak 1
1
Department of Cardiology and Electrotherapy, Medical University of Gda´nsk, 80-210 Gda´nsk, Poland;
zuzanna.lewicka@gumed.edu.pl (Z.L.-P.); ewa.lewicka@gumed.edu.pl (E.L.);
ludmila.danilowicz-szymanowicz@gumed.edu.pl (L.D.-S.); anfar@wp.pl (A.F.);
izabela.nabialek-trojanowska@gumed.edu.pl (I.N.-T.); mkubik@gumed.edu.pl (M.K.);
ania.m.kaleta@gmail.com (A.M.K.-D.); grzegorz.raczak@gumed.edu.pl (G.R.)
2
First Department of Cardiology, Medical University of Gda´nsk, 80-210 Gda´nsk, Poland; rgal@gumed.edu.pl
*
Correspondence: alicja.dabrowska-kugacka@gumed.edu.pl; Tel.: +48-601-910-480
Received: 19 June 2020; Accepted: 21 July 2020; Published: 24 July 2020


Abstract: It has been raised that marathon running may signiﬁcantly impair cardiac performance.
However, the post-race diastolic function has not been extensively analyzed. We aimed to assess
whether the marathon run causes impairment of the cardiac diastole, which ventricle is mostly
aﬀected and whether the septal (IVS) function is altered. The study included 34 male amateur runners,
in whom echocardiography was performed two weeks before, at the ﬁnish line and two weeks after
the marathon. Biventricular diastolic function was assessed not only with conventional Doppler
indices but also using the heart rate-adjusted isovolumetric relaxation time (IVRTc). After the run,
IVRTc elongated dramatically at the right ventricular (RV) free wall, to a lesser extent at the IVS and
remained unchanged at the left ventricular lateral wall. The post-run IVRTc_IVS correlated with
IVRTc_RV (r = 0.38, p < 0.05), and IVRTc_RV was longer in subjects with IVS hypertrophy (88 vs.
51 ms; p < 0.05). Participants with measurable IVRT_RV at baseline (38% of runners) had longer
post-race IVRTc_IVS (102 vs. 83 ms; p < 0.05). Marathon running inﬂuenced predominantly the RV
diastolic function, and subjects with measurable IVRT_RV at baseline or those with IVS hypertrophy
can experience greater post-race diastolic fatigue.
Keywords: marathon run; amateur runners; diastolic function; right ventricle; relaxation; isovolumic
relaxation time; myocardial performance index
1. Introduction
There is increasing evidence that prolonged intense exercise, such as marathon running, can aﬀect
cardiac performance [1]. Recently, this form of sports activity has gained popularity, but the question
remains about its safety for amateur non-elite runners, who are often middle-aged [2].
It has been raised that the right ventricle (RV) may be the “Achilles heel” of the competing
heart, because RV enlargement and reduction in RV contractility was observed following marathon
running [3]. An increase in oxygen demand during prolonged exercise, followed by the augmentation
of cardiac output and a proportionate rise in pulmonary artery pressure, ultimately aﬀects RV, which is
not adapted to high vascular resistance [4,5]. In the presence of common septum and pericardium
constraint, dysfunction of one ventricle aﬀects the other in the process of ventricular interdependence.
Apart from their dominant role in this interaction, the septal muscle ﬁbers that obliquely bind both
Int. J. Environ. Res. Public Health 2020, 17, 5336; doi:10.3390/ijerph17155336
www.mdpi.com/journal/ijerph
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ventricles also fulﬁl a major function in the overall movement of the RV [6,7]. Exercise-induced cardiac
fatigue has been studied mainly in terms of depressed systolic function [8]. In contrast, a small number
of studies have assessed the cardiac diastole among amateur marathon runners from pre-event to
in-run testing, especially regarding RV. According to the theory of myocardial damage progression,
the diastole tends to become impaired before the systole, and, in several diseases, the slowing of
relaxation was shown as an early sign of myocardial damage [9–11]. The prolongation of the isovolumic
relaxation time (IVRT) may reﬂect the delayed relaxation ﬁlling pattern and therefore be the ﬁrst
marker of developing diastolic dysfunction [12]. In this study, we analyzed the pathophysiology of
heart exhaustion associated with a marathon competition, with special attention to diastolic function
and interventricular septum involvement.
2. Materials and Methods
After having received acceptance of the study protocol from the Independent Bioethics Commission
for Research of the Medical University of Gdansk (NKBBN/104/2016), via advertisements sent to
local sport clubs, we recruited male amateur marathon runners planning to run in the 2nd PZU
Marathon in Gda´nsk, Poland. The study was conducted in accordance with the Declaration of Helsinki.
Detailed study information was provided to all volunteers and written consent was obtained from
each participant before entering the study. We enrolled subjects who were at deﬁned age (20–55 years
old) and showed no chronic diseases. The study protocol consisted of three stages and participants
were examined two weeks before the marathon run (stage I), at the marathon ﬁnish line (stage II) and
two-weeks after the competition (stage III). At each stage, physical and echocardiographic examination
(ECHO) was performed. Moreover, at baseline (stage I), the training history was collected and a
cardiopulmonary exercise test (CPET) was performed. Detailed characteristics of the examined amateur
marathon runners have been previously presented [13]. During the competition, participants were
allowed to rehydrate on a whim and no food intake restrictions were advised. The temperature was
around 12 ◦C and the wind speed was around 21.5 km/h.
The ECHO was carried out with a commercially available system (Vivid E9, GE Healthcare, Horten,
Norway), in accordance with the recommendations of the American Society of Echocardiography and
European Association of Cardiovascular Imaging [14]. All analyses and measurements (averaged
from three consecutive beats) were performed oﬀ-line by two researchers, using echocardiographic
quantiﬁcation software (EchoPac 201, GE Healthcare, Norway). By means of two-dimensional (2D)
and M-mode ECHO, cardiac dimensions were obtained, including diastolic interventricular septum
diameter (IVSd) in the parasternal long-axis view (PLAX). The end-systolic right atrial (RA) area was
calculated in the apical four-chamber (A4C) view and the left atrial (LA) volume indexed to body
surface area (LAVI) was obtained from the apical two-chamber and A4C views. At end-diastole,
the basal LV and RV transversal dimensions (LVd BAS and RVd BAS) were acquired in the A4C view
and, subsequently, the RVd/LVd BAS ratio was calculated to assess diastolic ventricular interaction.
The transverse RV diameter was also measured in the middle of the RV inﬂow (RVd MID) in the
RV-focused apical view, as described in detail previously [14].
The diastolic function of LV and RV was assessed with pulsed wave Doppler (PWD) and spectral
Doppler tissue imaging (DTI) indices according to the guidelines [15,16]. In the 4C view, the PWD
transmitral (MV) and transtricuspid (TV) ﬂow velocities were obtained: peak early (E), peak atrial (A)
and E/A ratio. Spectral DTI mitral annular velocities, namely peak systolic (S’), peak early diastolic (E’),
peak atrial diastolic (A’), E’/A’ ratio, were assessed at basal septum (S’IVS, E’IVS, A’IVS) and LV lateral
wall (S’LW, E’LW, A’LW). Then, the following ratios were calculated: E_MV/E’_LW, E_MV/E’_IVS and
E_MV/E’_AVG (E’ averaged from IVS and LW) [16]. Corresponding tricuspid annular velocities were
obtained (S’RV, E’RV, A’RV), along with E_TV/E’_RV ratio. Spectral DTI isovolumic relaxation time
(IVRT) was estimated at the lateral mitral (IVRT_LW), tricuspid RV (IVRT_RV) and septal (IVRT_IVS)
level, as the interval between the end of the S’-wave and the beginning of the E’-wave, as described
previously [17,18]. In order to compensate for the augmented heart rate after exercise, the heart
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rate-adjusted IVRT (IVRTc) was calculated as the ratio of the IVRT and square RR (interval between
two subsequent beats, given in seconds).
RV and LV global performance was assessed by the DTI-derived myocardial performance index
(MPI), which was analyzed in the 4C view at the lateral tricuspid (MPI_RV), lateral mitral (MPI_LW)
and septal annulus (MPI_IVS). MPI was calculated with the formula (ICT + IVRT)/ET, where ICT is the
isovolumic contraction time, measured from the cessation of A′ -wave to the onset of S’-wave, and ET
is the ejection time, measured as the width of S’-wave. The DTI-derived MPI was chosen over the
PWD as it is derived from one cardiac cycle and therefore is more reliable [19].
The RV four-chamber longitudinal strain (including ventricular septum), here also referred to
as “RV global strain” (RV 4CSL) was measured in the RV-focused 4C view, in accordance with the
consensus document on deformation imaging [20]. Along with the guidelines, tricuspid annular plane
systolic excursion (TAPSE) and RV fractional area change (RV FAC) were additionally calculated
to measure the RV systolic function, and regarding the LV ejection fraction (LV EF) and LV global
longitudinal strain (LV GLS), assessment was performed [14,15].
The study subjects were divided into 2 groups on the basis of the baseline IVRT_RV: (1) IVRT_RV
= 0 ms or (2) IVRT_RV > 0 ms. Another division was performed according to the presence of IVS
hypertrophy, deﬁned as IVSd > 11 mm.
Data analysis was performed using Statistica 13.3 software (Statsoft Inc., Tulsa, Oklahoma, United
States). The normality of variables was tested with the Shapiro–Wilk test. Data are presented as
mean ± SD (if normally distributed) or median with ﬁrst and third quartile (25th; 75th percentile)
(if non-normally distributed). The comparison between 3 stages was performed with ANOVA analysis
and the post-hoc Tukey test for normally distributed data. Non-normally distributed measurements
were compared with Friedman ANOVA and post-hoc for Friedman ANOVA. Comparisons between
predeﬁned groups were performed by Student’s t-test for independent samples or the Mann–Whitney
U test, where appropriate. The p-value of < 0.05 was considered signiﬁcant. Spearman’s correlation was
calculated to determine the dependency of ECHO measurements and parameters of cardiorespiratory
ﬁtness obtained in the CPET.
3. Results
Thirty-four amateur marathon runners, with a mean age of 40 ± 8 years, who ﬁnished the
competition, were enrolled in the study. All participants were men of Caucasian race with no relevant
medical history. Training history and CPET results have been recently published [13]. In brief, the
mean training distance was 56.5 ± 19.7 km/week, and the mean marathon ﬁnishing time was 3.7 ± 0.4 h.
The mean oxygen uptake at anaerobic threshold (VO2AT) was 39.7 ± 6.9 mL/kg/min. Tables 1–3
provide the comparison of 2D ECHO measurements between three stages, including measures of both
ventricles (Table 1), Doppler parameters of LV performance (Table 2) and the RV Doppler indices
(Table 3).
There were no signiﬁcant diﬀerences between parameters from stages I and III, apart from
E_MV and E’_RV (Tables 2 and 3). Running the marathon had no impact on the LV systolic function
(Table 1). There were no relevant valvular regurgitations among marathon runners at any stage of the
study. Reduced ratios of E/A_MV and E/A_TV were observed after the competition (Tables 2 and 3).
The results obtained by PWD were consistent with DTI-derived E’/A’ in both RV and LV (Tables 2
and 3). On the contrary, the E/E’ ratios remained at the same level after the race (Tables 2 and 3).
The most striking evidence of impaired RV relaxation was shown on the basis of the IVRT analysis
(Figure 1).
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Table 1. Echocardiographic parameters of the left and right ventricle obtained in amateur marathon runners.
Parameter
Stage I
Stage II
Stage III
ANOVA
p-Value
Post-Hoc
p-Value
Mean ± SD 1 or
Median (1st; 3rd Quartile) 2
Stage
I vs. II
Stage
I vs. III
LV EF (%)
61.8 ± 4.9
60.5 ± 4.4
60.7 ± 4.5
* 0.38
-
-
LV GLS (%)
−19.9 ± 2.3
−19.4 ± 2.1
−19.7 ± 2.2
* 0.41
-
-
RV 4CSL (%)
−22.0 ± 2.8
−20.80 ± 2.6
−21.49 ± 2.5
* <0.05
<0.05
0.46
TAPSE (mm)
25.0 ± 3.6
24.0 ± 3.7
25.0 ± 2.7
* 0.56
-
-
RV FAC (%)
43 (37; 45)
39 (35; 44)
41 (36; 45)
ˆ 0.19
-
-
RVd MID (cm)
3.4 ± 0.6
3.7 ± 0.5
3.5 ± 0.5
* <0.01
<0.01
0.08
RVd BAS (cm)
3.8 ± 0.4
3.8 ± 0.5
3.9 ± 0.5
* 0.44
-
-
LVd BAS (cm)
4.8 ± 0.4
4.6 ± 0.3
4.9 ± 0.3
* <0.001
<0.01
0.88
RVd/LVd BAS
0.77 ± 0.1
0.82 ± 0.1
0.79 ± 0.1
* <0.05
<0.05
0.59
1—when normally distributed; 2—when non-normally distributed; Stage I—two weeks before the marathon run; Stage II—at the marathon ﬁnish line; Stage III—two weeks after the
marathon run; LV —left ventricular; EF—ejection fraction; GLS—global longitudinal strain; RV—right ventricular; 4CSL—four-chamber longitudinal strain = global strain; TAPSE—tricuspid
annular plane systolic excursion; FAC—fractional area change; RVd MID—RV mid-cavity end-diastolic dimension; LVd BAS—LV basal end-diastolic diameter; RVd BAS—RV basal
end-diastolic diameter; RVd/LVd BAS—basal RV to LV end-diastolic diameter ratio; SD—standard deviation; * ANOVA with post-hoc Tukey test if applicable; ˆ Friedman ANOVA with
post-hoc average rank test if applicable.
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Table 2. Left ventricular parameters obtained by means of the pulsed wave Doppler and spectral Doppler tissue imaging in amateur marathon runners.
Parameter
Stage I
Stage II
Stage III
ANOVA
p-Value
Post-Hoc
p-Value
Mean ± SD 1 or
Median (1st; 3rd Quartile) 2
Stage
I vs. II
Stage
I vs. III
S’_LW (cm/sec)
11 ± 3
11 ± 3
11 ± 3
* 0.88
-
-
E’_LW (cm/sec)
15 (12; 17)
12 (10; 15)
14 (13; 16)
ˆ <0.001
<0.05
ns
A’_LW (cm/sec)
8 (7;9)
10 (9; 11)
8 (7; 9)
ˆ <0.001
<0.05
ns
E’/A’_LW
1.8 (1.4; 2.1)
1.2 (1.0; 1.5)
1.9 (1.6; 2.3)
ˆ <0.001
<0.05
ns
IVRT_LW (ms)
53 ± 17
54 ± 19
56 ± 15
* 0.99
-
-
IVRTc_LW
53 ± 17
59 ± 23
54 ± 15
* 0.28
-
-
MPI_LW
0.41 ± 0.08
0.45 ± 0.17
0.42 ± 0.07
* 0.20
-
-
S’_IVS (cm/sec)
8 (8; 9)
9 (8; 10)
9 (7; 10)
ˆ 0.24
-
-
E’_IVS (cm/sec)
11 ± 2
10 ± 2
11 ± 2
* <0.001
<0.01
0.73
A’_IVS (cm/sec)
8 (8; 10)
10 (9; 11)
8 (7; 10)
ˆ <0.001
<0.05
ns
E’/A’_IVS
1.3 ± 0.4
1.0 ± 0.3
1.4 ± 0.4
* <0.001
<0.001
0.26
IVRT_IVS (ms)
82 (65; 95)
80 (68; 94)
78 (64; 86)
ˆ 0.46
-
-
IVRTc_IVS
78 (66; 92)
92 (77; 108)
73 (65; 85)
ˆ <0.001
<0.05
ns
MPI_IVS
0.55 (0.44; 0.59)
0.53 (0.44; 0.6)
0.47 (0.44; 0.54)
ˆ 0.09
-
-
E_MV (cm/sec)
71 (67; 87)
67 (55; 77)
78 (68; 92)
ˆ <0.01~
ns
ns
A_MV (cm/sec)
51 ± 10
65 ± 14
56 ± 11
* <0.001
<0.001
0.29
E/A_MV
1.5 ± 0.4
1.1 ± 0.3
1.5 ± 0.4
* <0.001
<0.001
0.7
E_MV/E’_LW
5.4 ± 1.2
5.5 ± 1.6
5.6 ± 1.8
* 0.66
-
-
E_MV/E’_IVS
7.1 ± 1.5
7.0 ± 1.8
7.6 ± 2.0
* 0.34
-
-
E_MV/E’_AVG
6.3 (5.2; 7.0)
5.8 (5.0; 7.2)
6.2 (5.4; 7.3)
ˆ 0.74
-
-
1—when normally distributed; 2—when non-normally distributed; LW—parameter measured at the lateral mitral annulus; IVS—parameter measured at the septal mitral annulus;
S’—peak systolic tissue velocity; E’—peak early diastolic tissue velocity; A’—peak atrial diastolic tissue velocity; IVRT—isovolumic relaxation time; IVRTc—IVRT adjusted for heart rate;
MPI—myocardial performance index; MV—mitral inﬂow; E—peak early ﬂow velocity; A—peak atrial ﬂow velocity; AVG—averaged for parameters obtained at IVS and LW; ns-p-value of
>0.05 of post-hoc average rank test for Friedman ANOVA; ~ ANOVA test p <0.05, but post-hoc test revealed the diﬀerence between stages II and III, which was not the question of our
study. * ANOVA with post-hoc Tukey test if applicable; ˆ Friedman ANOVA with post-hoc average rank test if applicable. For other abbreviations, see Table 1.
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Table 3. Right ventricular parameters obtained by means of the pulsed wave Doppler and spectral Doppler tissue imaging in amateur marathon runners.
Parameter
Stage I
Stage II
Stage III
ANOVA
p-Value
Post-Voc
p-Value
Mean ± SD 1 or
Median (1st; 3rd Quartile) 2
Stage
I vs. II
Stage
I vs. III
S’_RV (cm/sec)
14 (13; 16)
14 (13.5; 16)
15 (13; 16)
ˆ 0.51
-
-
E’_RV (cm/sec)
12 (11; 15)
12 (9; 14)
14 (13; 16)
ˆ <0.05 ~
ns
ns
A’_RV (cm/sec)
13 (10; 14)
16 (13; 20)
13 (12; 16)
ˆ <0.01
<0.05
ns
E’/A’_RV
1.0 (0.9; 1.2)
0.7 (0.6; 0.9)
1.2 (0.9; 1.3)
ˆ <0.001
<0.05
ns
IVRT_RV (ms)
0 (0; 29)
52 (32; 70)
21 (9; 34)
ˆ <0.001
<0.05
ns
IVRTc_RV (ms)
0 (0; 27)
58 (39; 78)
20 (0; 35)
ˆ <0.001
<0.05
ns
MPI_RV
0.28 (0.22; 0.37)
0.48 (0.35; 0.64)
0.33 (0.25; 0.41)
ˆ <0.001
<0.05
ns
E_TV (cm/sec)
55 ± 13
49 ± 11
56 ± 11
* 0.18
-
-
A_TV (cm/sec)
33 ± 10
46 ± 15
31 ± 8
* <0.001
<0.001
0.99
E/A_TV
1.7 ± 0.4
1.2 ± 0.3
1.9 ± 0.6
* <0.001
<0.001
0.55
E_TV/E’_RV
4.5 ± 1.1
4.2 ± 1.7
3.9 ± 1.0
* 0.44
-
-
1—when normally distributed; 2—when non-normally distributed; RV—right ventricular parameters measured at the lateral tricuspid annulus; TV—transtricuspid inﬂow. * ANOVA with
post-hoc Tukey test if applicable; ˆ Friedman ANOVA with post-hoc average rank test if applicable. For other abbreviations, see Tables 1 and 2.
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Int. J. Environ. Res. Public Health 2020, 17, x 
6 of 13 
 
 
Figure 1. Changes in the right ventricular isovolumic relaxation time (IVRT_RV) between the three 
study stages. (a) IVRT_RV was undetectable at stage I (two weeks before the marathon run) and (c) 
at stage III (two weeks after the competition); (b) in contrast, the appearance of IVRT_RV and its 
prolongation up to 104 ms at stage II (at the marathon finishing line). 
The marathon run resulted in significant prolongation of IVRTc_RV, which was found in 24 out 
of 34 runners (71%). The IVRT_RV appeared in 58% of subjects, in whom it was undetectable at the 
baseline. The marathon impact on the relaxation was different for the RV and LV: immediately after 
Figure 1. Changes in the right ventricular isovolumic relaxation time (IVRT_RV) between the three
study stages. (a) IVRT_RV was undetectable at stage I (two weeks before the marathon run) and
(c) at stage III (two weeks after the competition); (b) in contrast, the appearance of IVRT_RV and its
prolongation up to 104 ms at stage II (at the marathon ﬁnishing line).
The marathon run resulted in signiﬁcant prolongation of IVRTc_RV, which was found in 24 out
of 34 runners (71%). The IVRT_RV appeared in 58% of subjects, in whom it was undetectable at the
Int. J. Environ. Res. Public Health 2020, 17, 5336
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baseline. The marathon impact on the relaxation was diﬀerent for the RV and LV: immediately after
the run, IVRTc elongated dramatically at the RV free wall, to a lesser extent at the IVS and remained at
the same level at the LV lateral wall (Figure 2).
Int. J. Environ. Res. Public Health 2020, 17, x 
7 of 13 
 
the run, IVRTc elongated dramatically at the RV free wall, to a lesser extent at the IVS and remained 
at the same level at the LV lateral wall (Figure 2). 
 
Figure 2. Changes in the heart rate-adjusted isovolumic relaxation time between the three stages of 
the study, assessed in the spectral Doppler tissue imaging (a) at the lateral tricuspid annulus 
(IVRTc_RV), (b) at septum (IVRTc_IVS) and (c) at the lateral mitral annulus (IVRTc_LW). 
In post-marathon analysis, there was a correlation between IVRTc_RV and IVRTc_IVS (r = 0.38, 
p < 0.05), and IVRTc_RV was significantly longer in runners with IVS hypertrophy (88 vs. 51 ms; p < 
Figure 2. Changes in the heart rate-adjusted isovolumic relaxation time between the three stages of the
study, assessed in the spectral Doppler tissue imaging (a) at the lateral tricuspid annulus (IVRTc_RV),
(b) at septum (IVRTc_IVS) and (c) at the lateral mitral annulus (IVRTc_LW).
In post-marathon analysis, there was a correlation between IVRTc_RV and IVRTc_IVS (r = 0.38,
p < 0.05), and IVRTc_RV was signiﬁcantly longer in runners with IVS hypertrophy (88 vs. 51 ms;
Int. J. Environ. Res. Public Health 2020, 17, 5336
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p < 0.05). At the baseline, 13 (38%) participants presented measurable IVRT_RV, and in this group,
a longer post-race IVRTc_IVS was revealed (102 vs. 83 ms; p < 0.05).
MPI measurements paralleled the IVRT results. After the race, a signiﬁcant prolongation at
the RV free wall was observed, accompanied by a trend towards its increase at IVS (p = 0.09) but
unchanged MPI at the LV lateral wall (Tables 2 and 3). There was a post-marathon reduction in RV
deformation, but other 2D parameters assessing RV systolic function did not change after the race
(Table 1). The cardiorespiratory ﬁtness assessed in CPET was a predictor of RV performance during
marathon running. Participants with higher VO2AT had lower MPI_RV post-race (r = −0.41, p < 0.05).
After the race, the RV enlargement and diminishment of the LV diameter was observed: RVd
MID and RVd/LVd BAS became signiﬁcantly larger and LVd BAS signiﬁcantly decreased (Table 1).
As presented previously, the median IVSd was 11 mm, with a range of 7–17 mm [13], and in nine
participants who were signiﬁcantly older (44 ± 4 vs. 37 ± 9 years, p < 0.05), IVSd was > 11 mm.
There were no diﬀerences in the pre- and post-marathon left and right atrial sizes, expressed as
LAVI and RA area. Nevertheless, there was a correlation between the post-marathon RA enlargement
and IVRT_RV (r = 0.48, p < 0.05) and MPI_RV (r = 0.58, p < 0.05). Moreover, in the post-race analysis,
larger RA areas were found in subjects with more evident diastolic ventricular interaction, as indicated
by an increased RVd/LVd BAS ratio (r = 0.49, p < 0.05). Notably, participants with IVRT_RV > 0 ms at
baseline and those with IVS hypertrophy (IVSd > 11 mm) presented signiﬁcantly larger LAVI and RA
areas after the run (p < 0.05).
4. Discussion
There is an ongoing debate regarding whether intense exercise, such as running a marathon,
is harmful to an overloaded heart [1]. Even if marathon-induced changes in cardiac function develop,
they are diﬃcult to register and show, as documented by the discrepancies between reports on this
topic. In this study, we demonstrated the post-run RV enlargement, the increase in the RV/LV ratio
and ambiguous ﬁndings on the RV systolic function (manifested in the decline in RV global strain but
not in TAPSE, FAC or S’RV). The analysis of MPI, which reﬂects both systolic and diastolic function,
showed changes only at the RV free wall. Our study revealed RV diastolic dysfunction manifesting
as the post-run prolonged relaxation, especially at the RV free wall and to a lesser degree at the IVS.
Although we found diﬀerences in the post-race E/A ratios for both ventricles, we do not interpret these
results as diastolic impairment but rather as the marathon-induced impact of increased heart rate.
All abnormalities were transient and not observed in the control examination performed two weeks
after the marathon run. DTI-derived IVRTc proved to be the most sensitive marker of the RV diastolic
failure among amateur marathon runners. We suggest that the threshold level of exercise that causes
myocardial damage is diﬀerent for RV and LV, as there was no change in IVRTc at the LV lateral wall.
With the variety of possible diastolic parameters, a question arises which should be considered
in amateur marathon runners. The diastole consists of isovolumic relaxation, rapid ﬁlling, diastasis
and atrial contraction, and each can be assessed depending on clinical indications [12]. With reference
to RV, the guidelines suggest the assessment of transtricuspid E/A ratio, E/E’ ratio and RA size [15].
The recognition of abnormal LV diastolic function in patients with preserved LV EF relies on E’ velocities,
average E/E’ ratio, LAVI and peak tricuspid regurgitation velocity [16]. Nevertheless, due to the
preload and afterload-dependence of the diastolic indices, their measurements should be interpreted
with caution [16].
With reference to diastolic function, the majority of previous studies among marathon runners
have focused mainly on the LV and documented generally the post-race decrease in E/A ratio [21–24].
In our study we revealed similar ﬁndings for both ventricles, with mitral and transtricuspid inﬂow
velocities having acted similarly. However, Doppler measurements have some limitations as they are
strongly load-dependent [15,25]. Thus, the hydration status of runners is relevant, as ﬂuid loss causes
the decrease in E-, A-velocities and E/A ratio [26]. Moreover, as the duration of diastole is inversely
correlated with heart rate, the atrial contraction gains signiﬁcance over the rapid ﬁlling in case of
Int. J. Environ. Res. Public Health 2020, 17, 5336
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tachycardia, resulting in decreased E/A ratio [15,27]. Undoubtedly, such results do not necessarily
reﬂect diastolic dysfunction, as the E/E’ ratio after the run remained at the same level. Therefore,
we argue for the utility of PWD indices in recognition of diminished ventricular relaxation among
marathon runners.
IVRT is a more reliable parameter and among Doppler indices is the earliest to alter in the
case of impaired relaxation [12]. Furthermore, it is reproducible and easy to obtain. It has been
shown that inadequate IVRT_LV shortening during dobutamine stress echocardiography was the only
Doppler diastolic parameter able to discriminate patients with residual ischemia after myocardial
infarction [18]. With reference to RV, IVRT_RV correlates well with the RV systolic pressure and this
non-invasive parameter is able to distinguish patients with elevated pulmonary pressure from those
without [17]. Additionally, invasively measured early RV relaxation is abnormal in patients with
pulmonary hypertension with preserved RV contractility [11].
In previous reports on marathon runners, no signiﬁcant post-race alterations were noticed in
IVRT_LV, which is consistent with our results [28,29]. However, in this study, IVRT was measured
additionally for the RV free wall and septum, and to preclude the impact of heart rate increase during
exercise, the heart rate-adjusted IVRT (IVRTc) was calculated. To our knowledge, our study is the
ﬁrst to report on the pre- and post-marathon IVRTc within the LV and RV. We showed the acute
post-marathon impairment of the RV relaxation, manifesting by IVRTc_RV prolongation.
In contrast to the LV, in a well-functioning RV, we rather expect IVRT to be undetectable. IVRT
becomes measurable when RV impairment occurs or when RV has to overcome a signiﬁcant increase in
pulmonary artery pressure [19]. The fact that more than half of runners who had IVRT_RV undetectable
at baseline developed it after the race is alarming and indicates that marathon running can seriously
overload the RV and alter its performance. The prolongation of RV relaxation probably reﬂects the
exercise-induced augmentation of pulmonary artery pressure. No increment in tricuspid or pulmonary
regurgitation was registered in ECHO performed several minutes after the race; therefore, the pressure
increase seems transient. Exercise ECHO studies in patients with pulmonary hypertension do conﬁrm
that the increase in peak tricuspid regurgitation velocity returns to baseline values brieﬂy after exercise
cessation [30]. The analysis of IVRT_RV allows us to monitor changes in pulmonary vasculature,
independently of tricuspid regurgitation velocity.
The recognition of detectable IVRT_RV at the baseline in 38% of the studied runners suggests the
existence of pre-marathon RV overload or even subclinical damage in these subjects. Most strikingly,
they showed more evident post-race diastolic impairment, with a signiﬁcant increase in atrial sizes
and longer IVS relaxation. The presence of measurable resting IVRT_RV raises questions about the
individual’s upper limit of endurance exercise and their predisposition to training-induced cardiac
fatigue. We hypothesize about the possibility of a “cumulative” alteration of the RV diastole due to
repetitive RV exhaustion. Previously, it was demonstrated that greater marathon-induced decrement
of RV contractility happened in less-trained runners [24]. Though we did not ﬁnd a direct correlation
between changes in IVRT_RV and the amount of training, cardiorespiratory ﬁtness assessed in CPET
was a predictor of global RV performance during the marathon run.
The inﬂuence of the marathon run on the LV relaxation was complex. There was no signiﬁcant
change in IVRTc_LW, but interestingly, the IVRTc_IVS was extended. Therefore, the impairment of
septal relaxation mirrored abnormalities in the RV free wall. Changes in septal function may be
explained as alterations in continuity with RV damage. Although IVS is mainly a constituent part
of the LV, it also shares muscle ﬁbers with RV [31]. Therefore, IVS is involved in the functioning
of both RV and LV and also transmits the altered load conditions from one ventricle to another [6].
Our study demonstrates the post-marathon increase in diastolic ventricular interaction with enlarged
RV and reduced LV. In accordance with former research that showed the post-run right to left IVS
displacement [32], we speculate that another factor that could account for impaired septal relaxation is
enhanced ventricular dependence.
Int. J. Environ. Res. Public Health 2020, 17, 5336
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Due to its complicated structure, an accurate 2D analysis of the RV’s performance remains
challenging and often requires multiparametric assessment [33]. We revealed the post-marathon
decline in global RV function, demonstrated by MPI, which combines systolic and diastolic function
and does not depend on heart rate or ventricular geometry [34]. In previous studies, MPI was shown
to correlate well with RV EF derived from cardiac magnetic resonance (CMR) imaging and was used to
assess ventricular function in many diseases [34–36]. In pulmonary arterial hypertension, MPI_RV is
successful in determining the severity of the disease and in patient monitoring [36]. To our knowledge,
our study is the ﬁrst reporting on the pre- and post-endurance MPI and for both LV and RV [37,38].
In contrast to RV, we found no signiﬁcant change in MPI_LV, which conﬁrms the notion that
marathon running does not alter the LV diastole. Notably, only an insigniﬁcant trend of MPI_IVS
prolongation was observed (p = 0.09). However, it is unclear whether this is due to the IVS involvement
in RV diastolic impairment or whether it reﬂects a decrease in septal contractility. This requires further
examination to determine whether septal diastolic dysfunction precedes its systolic impairment and
whether a drop in IVS contractility appears at some point during repetitive marathon attendance. With
reference to septum, the negative eﬀect of “cumulative exercise dose” was previously proved in a CMR
study that analyzed the late gadolinium enhancement and found that the occurrence of myocardial
ﬁbrosis in IVS near the RV attachment correlated with the longevity of sport competition [32]. In our
study, we demonstrated that the eﬀort-induced remodeling of IVS and the degree of its hypertrophy
is relevant to the RV’s performance during the marathon run. Though IVS hypertrophy is generally
considered a physiological adaptation to endurance exercise, we found that the presence of IVS with a
width of > 11 mm appeared to be a predictor of more evident post-race diastolic fatigue.
Our results showed the impaired relaxation of the RV, with inconclusive observations regarding
RV systolic function, as only RV deformation decreased. Additionally, we demonstrated that, after the
marathon run, RV enlargement and LV diminishment appear. We presume that the sequence of cardiac
changes started with elevated pulmonary pressure due to the exercise-induced increase in cardiac
output, which inﬂuenced RV relaxation, as the ﬁrst marker of developing dysfunction. Consequently,
the RV enlarged and, due to pericardium constraint, the LV diminished its volume.
The observation regarding post-race RA size is also very interesting. Although we did not observe
changes in atrial size in the whole group, post-race RA enlargement was greater in runners with
longer post-race IVRT_RV, MPI_RV and larger RV volume. Additionally, in runners with impaired RV
function at the baseline (IVRT_RV > 0 ms) and in those with hypertrophied septum, the atria after the
run were bigger than in runners without these abnormalities.
Our study has an important limitation. As we did not include women in the study group,
we cannot apply our ﬁndings to the population of female runners. Therefore, we are not able to discuss
possible gender diﬀerences in RV diastolic fatigue caused by marathon running.
5. Conclusions
In amateur participants, the marathon run inﬂuences predominantly the RV diastole, and post-race
IVRT assessment reveals the dramatic impairment of relaxation at the RV free wall, with concomitant
alteration of the IVS. The division of LV_IVRTc into IVRTc_LW and IVRTc_IVS and their separate
analyses is crucial, as marathon running does not inﬂuence the relaxation of the LV lateral wall.
The RV MPI and RV strain analysis, showing the decline in RV global function, follows the IVRTc
observations, demonstrating that marathon attendance overburdens mainly the RV. Nevertheless,
RV overload through enhanced diastolic ventricular interaction also aﬀects LV, causing a decrease
in LV cavity and alteration of IVS function. At this point, we also indicate that there is a group of
runners predisposed to occurrence of diastolic dysfunction after the marathon. Participants with
evidence of detectable IVRT_RV at the baseline or those with IVS hypertrophy are endangered by
greater post-race cardiac exhaustion. These subjects may require constant cardiac monitoring if they
continue to exercise intensively.
Int. J. Environ. Res. Public Health 2020, 17, 5336
12 of 14
Author Contributions: Conceptualization, Z.L.-P., A.D.-K. and E.L.; Data curation, Z.L.-P., A.D.-K., E.L., R.G.,
L.D.-S., A.F., I.N.-T., M.K. and A.M.K.-D.; Formal analysis, Z.L.-P. and A.D.-K.; Funding acquisition, A.D.-K., E.L.
and G.R.; Investigation, Z.L.-P., A.D.-K., E.L., R.G., L.D.-S., A.F., I.N.T., M.K., A.M.K.-D. and G.R.; Methodology,
Z.L.-P., A.D.-K. and E.L.; Project administration, A.D.-K. and G.R.; Resources, A.D.-K., E.L. and G.R.; Software,
Z.L.-P. and A.D.-K. Supervision, A.D.-K., E.L. and G.R.; Validation, Z.L.-P., A.D.-K., R.G., L.D.-S., A.F., I.N.T., M.K.
and A.M.K.-D.; Visualization, Z.L.-P.; Writing—original draft, Z.L.-P.; Writing—review and editing, A.D.-K. and
E.L. All authors have read and agreed to the published version of the manuscript.
Funding: This research received no external funding.
Conﬂicts of Interest: The authors declare no conﬂict of interest.
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Right Ventricular Diastolic Dysfunction after Marathon Run.
Lewicka-Potocka, Zuzanna,Dąbrowska-Kugacka, Alicja,Lewicka, Ewa,Gałąska, Rafał,Daniłowicz-Szymanowicz, Ludmiła,Faran, Anna,Nabiałek-Trojanowska, Izabela,Kubik, Marcin,Kaleta-Duss, Anna Maria,Raczak, Grzegorz