Original Paper

Nephron Clin Pract 2013;124:7278

DOI: 10.1159/000355856

Received: April 18, 2013

Accepted: September 17, 2013
Published online: October 18, 2013

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Benefits of Exercise Training
during
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Hemodialysis Sessions: A Prospective
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Abstract
Background: End-stage renal disease patients can be considered as cardiovascular time bombs due to their tremendous cardiovascular risk. Our study has determined the impact of 3 months of exercise training during dialysis on
some of the cardiovascular risk factors (arterial stiffness,
body composition and physical performance) in a chronic
hemodialyzed population. Methods: The study group (n =
19) and control group (n = 16) of chronic hemodialysis patients from Timisoara, Romania, were enrolled in a prospective cohort study. The intervention 40 min of exercise
training (with non-fistula hand and both lower limbs) during each hemodialysis session for 3 months was applied
only to the study group. The measurements made before
and after intervention were aortic pulse wave velocity
(PWV), aortic augmentation index, return time and both
central and peripheral blood pressure for arterial stiffness
evaluation, using the Arteriograph Tensiomed system, body

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composition by multifrequency bioimpedance and physical

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performance
(Myotest
PRO
system
dynamometer). Results:
We found
a significant
1-m/s
reduction
in PWV,
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a 12-second
increase
in return
time
a 10-mm
Hg reduction in both central and systolic blood pressure driven only
by the exercise training. Exercise training significantly increased the skeletal muscle mass and the soft lean mass of
the study group patients. Physical performance significantly improved in the study group jumping height by 1 cm,
lower limbs explosive power by 3 W/kg and non-fistula
hand strength prehension by 0.06 bar. Conclusions: Exercise training during dialysis has a positive effect on arterial
stiffness, body composition and physical performance of
chronic hemodialyzed patients.
2013 S. Karger AG, Basel

Introduction

Chronic kidney disease (CKD) patients have a high

risk of cardiovascular disease (CVD), which is not explained by the traditional cardiovascular risk factors. The
tremendous increase of CVD risk by 343% in patients
with eGFR <15 ml/min/1.73 m2 (a category which also
Claudiu Avram, MD
Department of Kinetic Therapy and Special Motricity
Faculty of Physical Education and Sport, West University of Timisoara
Str. Baba Dochia, bl.D1, sc.A, ap.14, RO300118 Timisoara (Romania)
E-Mail claudiu.avram@gmail.com

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Key Words
Arterial stiffness Body composition Cardiovascular risk
reduction Exercise training Hemodialysis Physical
performance

Benefits of Exercise Training during

Dialysis

Subjects and Methods

In our prospective cohort study, we enrolled 35 patients who
underwent chronic HD 4 h/session, 3 times/week in B/Braun Avitum, a private dialysis unit in Timisoara, Romania. All the patients
were dialyzed with high-flux, high-surface (1.82.2 m2) filters for
more than 3 months before the beginning of the study. The protocol was approved by the local ethics committee.
The study patients were separated into two groups group S
(study group, 19 patients) and group C (control group, 16 patients), according to their dialysis days (group S dialyzing on Monday, Wednesday, Friday and group C dialyzing on Tuesday, Thursday, Saturday).
The intervention was applied to group S, and consisted of 40
min of exercise training (with non-fistula hand and both lower
limbs) during the first 2 h of each HD session for 3 months (November 2011 to February 2012), under the supervision of a licensed
physical therapist. Group C received no exercise training during
dialysis.
Three female patients were lost to follow-up: 1 in group S
(transplantation) and 2 in group C (moved to another unit).
In order to supervise the exercise intensity and energy expenditure of group S patients, we used Polar FT80 heart rate monitors and
Borg scale 620 for rating of perceived exertion. The exercise training program consisted in 23 sets, 10 repetitions per set of resistance
exercises performed using elastic bands, dumbbells and ankle
weights in order to achieve an increase of exercise heart rate of 15
30 beats/min (depending on the patients exercise tolerance and the
presence of -blocking/ivabradine treatment) and/or a Borg scale
level of somewhat hard (1214). Each major muscle group involved in exercise was evaluated weekly using the 10RM test and the
resistance training adjusted to be between 70 and 85% of 10RM.
Each study patient was evaluated at the beginning of the study
(T0) and at the end of the study protocol (T1) with regard to arterial stiffness, body composition and physical performance.
Arterial stiffness was assessed by the measurement of aortic
PWV, Aix, return time (RT), both central and peripheral systolic
and diastolic blood pressure (SBPao, SBP, DBP), mean arterial
pressure (MAP), pulse pressure (PP) and heart rate (HR) using an
oscillometric method (Tensiomed Arteriograph; Medexpert Ltd.,
Hungary). Arterial stiffness evaluation was performed in a morning session, after a fasting period of at least 12 h, before dialysis,
with the patient in the supine position, resting for at least 15 min
before measurement.
Body composition was evaluated by multifrequency bioimpedance (frequency from 1 kHz to 1 MHz, using reactance analysis
method) with the body composition analyzer InBody720 (Biospace
Co. Ltd, Korea) and the following parameters were measured: total
body water (TBW), body mass index (BMI), skeletal muscle mass
(SMM), soft lean mass (SLM) and percentage of body fat (PBF).
Physical performance was measured using the Myotest PRO
system for lower limb parameters (jumping height, lower limbs
explosive power, lower limbs explosive force) and hand dynamometer for the left- and right-hand prehension strength measurement.
The level of daily physical activity of each patient was assessed
by using a digital pedometer (Omron Walking Style Pro, Italy),
which recorded the number of daily steps and the walking energy
expenditure of the subject. The pedometer was carried by the subject during the entire day, every day of the 3-month study period. A

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DOI: 10.1159/000355856

73

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includes dialyzed patients) leads to the conclusion that

dialyzed patients are cardiovascular time bombs very
fragile people with some highly dangerous heart condition and vascular pathological changes [1, 2].
Atherosclerosis (affecting the intima of the arteries)
and arteriosclerosis (affecting the media of the large and
middle-sized arteries), the most frequent causes of arterial stiffness, are highly prevalent in hemodialyzed (HD)
patients [3]. The link between stiff arteries and the increased number of cardiovascular events is well described.
The mechanism involves the increase of systolic pressure
load of the heart, due to a faster travel time of the pressure
wave through the conductance arteries, which will further exacerbate the already present left ventricular hypertrophy [4, 5].
Arterial stiffness (measured by pulse wave velocity
(PWV) and aortic augmentation index (Aix)) is one of the
vascular changes proven to be a major predictor of allcause and cardiovascular mortality in HD patients. The
HD patients whose PWV fails to improve under antihypertensive treatment have a worse cardiovascular prognosis, even though their blood pressure decreases [6].
These findings emphasize the importance of a treatment
that would address arterial stiffness reduction in order to
decrease the high cardiovascular risk of CKD patients.
There are some known pharmacological (antihypertensive drugs, statins, thiazolidinediones, nitrates, alagebrium) and non-pharmacological (physical exercise,
weight loss, low-salt diet, moderate alcohol consumption,
fish oil, -linoleic acid, garlic powder, hormonal replacement therapy) treatments that could decrease arterial
stiffness [7].
Few studies have followed the arterial stiffness parameters reduction by intradialytic physical training. Even so,
they have reached contradictory results: two of them (uncontrolled, on less than 20 patients) show an improvement of PWV or Aix after 3 months of exercise, while the
most comprehensive one, a randomized study on 70 patients, reported no significant differences in the vascular
parameters of the intradialytic trained, home-based exercise and usual care group, respectively, after 6 months [4,
8, 9].
The primary aim of our study has been to determine
the impact of a 3-month individualized exercise training
program during dialysis on the arterial stiffness parameters in a chronic HD population. As secondary aims of the
study, we followed the body composition and physical
performance changes produced by regular exercise during dialysis sessions.

20
p = 0.029

p = 0.154

10

p = 0.042

150

100

SG-T0

SG-T1

CG-T0

CG-T1

50

SG-T0

SG-T1

CG-T0

CG-T1

Fig. 1. Changes of PWV after 3 months of exercise training in pa-

Fig. 2. Changes of central SBP after 3 months of exercise training

tients from group S and group C. SG-T0 = Study group at baseline;

SG-T1 = study group after 3 months of training; CG-T0 = control
group at baseline; CG-T1 = control group after 3 months of training.

in patients from group S and group C. SG-T0 = Study group

at baseline; SG-T1 = study group after 3 months of training; CGT0 = control group at baseline; CG-T1 = control group after 3
months of training.

weekly check of the pedometers memory, performed by the physical therapists, was used in order to record the number of daily steps
and energy expenditure of each patient. All the measurements were
taken by the same operator, before a midweek dialysis session.
There were no changes in the chronic antihypertensive medication or in the HD parameters prescription made during the study
protocol. All the patients included in the study were dialyzed using
high-flux filters starting at least 3 months before the beginning of
the study.
Statistical analysis was performed using GraphPad Prism version 5 software. Data is presented as mean SD or percentages.
The relationship between the measured variables was evaluated by
linear regression, using Students t test (paired for the same group
and unpaired for between-group analysis) as the continuous variables within the groups were found to have normal distribution. A
p value <0.05 was considered necessary for establishing statistical
significance between differences.

tage 4.5 4.7 (1.219.6) years, while in group C (75%

women) the average age was 55.1 10.5 (range 3172)
years, and dialysis vintage 4.6 4.4 (0.320.8) years.

Results

The 35 study patients (68.6% women) were on average

56.7 9.2 (range 3172) years of age and had been on dialysis for 4.7 4.6 (0.320.8) years.
The two groups (S and C) were homogeneous in terms
of body composition, physical performances, daily activity, arterial stiffness, antihypertensive medication and
HD prescription and efficiency, as we found no statistical
significant differences at the beginning of the study (data
not shown).
In group S, of which 63.2% were women, the average
age was 55.6 9.3 (range 4071) years, and dialysis vin74

Nephron Clin Pract 2013;124:7278

DOI: 10.1159/000355856

Arterial Stiffness
Of the hemodynamic parameters analyzed, at the end
of the study there was a decrease of PWV by 1 m/s, a 10-mm
Hg reduction of both central and peripheral SBP and a
12-second increase in RT in group S patients, all statistically significant (fig.1, 2).
The comparison between groups S and C at the end of
the study protocol found only RT to be significantly different. The hemodynamic parameters analyzed and their
changes for both groups are presented in table1.
Body Composition
Regarding body composition, we found a statistically
significant increase in SMM and SLM of the study group
patients, but no changes in TBW, weight or body fat (table2).
Physical Performance
In terms of physical performance, we found that the
following parameters improved in group S: jumping
height, lower limbs explosive power and non-fistula hand
strength prehension. Patients in group C presented no
significant changes in their physical performance parameters (table3; fig.3).

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p = 0.302
p = 0.801

200
mm Hg

m/s

15

250

p = 0.356

Table 1. Changes in hemodynamic parameters after 3 months of exercise training in patients from group S and group C

Group S

PWV, m/s
RT
Aix aortic, %
SBP, mm Hg
DBP, mm Hg
SBPao, mm Hg
MAP, mm Hg
PP, mm Hg
HR, beats/min

Group C

p*

T0 (n = 19)

T1 (n = 18)

T0 (n = 16)

T1 (n = 14)

10.26 2.17
106.8 20.40
33.28 16.30
134.5 21.52
88.53 15.99
134.8 23.88
103.9 17.31
46.00 10.11
69.89 13.16

9.25 1.96
118.9 25.19
29.79 16.45
125.6 16.56
82.53 11.45
123.6 19.61
95.74 12.21
44.32 9.82
70.50 9.77

0.029
0.009
0.139
0.050
0.136
0.042
0.067
0.539
0.393

9.23 1.94
112.9 32.34
37.11 19.21
150.5 23.78
90.06 18.07
151.1 29.62
110.1 18.91
60.44 14.64
68.88 13.23

10.51 2.21
98.43 19.71
33.27 17.53
136.1 43.13
87.25 29.03
146.1 30.64
103.5 33.47
48.81 16.41
69.31 20.19

0.154
0.210
0.503
0.279
0.879
0.801
0.575
0.044
0.814

0.356
0.047
0.674
0.697
0.578
0.302
0.618
0.926
0.621

p* = Between groups at T1. Values are presented as mean SD.

Table 2. Changes in body composition after 3 months of exercise training in patients from group S and group C

Group S

TBW, l
Weight, kg
BMI
SMM, kg
SLM, kg
PBF, %

Group C

p*

T0 (n = 19)

T1 (n = 18)

T0 (n = 16)

T1 (n = 14)

40.99 8.93
81.53 16.49
27.96 4.05
30.89 7.12
52.56 11.42
31.11 10.6

40.97 8.42
82.45 18.21
28.28 4.44
32.33 8.4
53.62 11.34
31.07 10.15

0.841
0.126
0.139
0.027
0.037
0.966

37.53 8.39
77.41 19.72
28.52 6.57
28.12 6.89
48.13 10.79
32.71 12.89

39.79 8.57
80.18 20.92
29.42 6.77
29.85 6.52
50.46 10.53
31.41 14.00

0.246
0.039
0.857
0.234
0.266
0.441

0.720
0.646
0.668
0.654
0.603
0.776

p* = Between groups at T1. Values are presented as mean SD.

Table 3. Changes in physical performance after 3 months of exercise training in patients from group S and group C

Group S

Jumping height, cm
Lower limbs explosive power, W/kg
Lower limbs explosive force, N/kg
Non-fistula hand prehension, bar
Fistula hand prehension, bar

Group C

p*

T0 (n = 19)

T1 (n = 18)

T0 (n = 16)

T1 (n = 14)

13.19 3.64
19.29 5.48
17.87 2.96
0.52 0.17
0.53 0.20

14.28 3.66
22.06 7.14
19.26 5.26
0.58 0.1945
0.55 0.2054

0.007
0.003
0.054
0.001
0.427

12.22 3.56
19.32 5.75
18.49 2.26
0.54 0.21
0.52 0.21

13.32 4.04
19.55 4.76
19.46 2.11
0.52 0.27
0.54 0.24

0.179
0.969
0.066
0.441
0.727

0.505
0.296
0.903
0.432
0.924

Benefits of Exercise Training during

Dialysis

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p* = Between groups at T1. Values are presented as mean SD.

p = 0.969

40

W/kg

p = 0.003

p = 0.296

30
20
10
0

SG-T0

SG-T1

CG-T0

CG-T1

Fig. 3. Changes in lower limbs explosive power after 3 months of

exercise training in patients from group S and group C. SG-T0 =

Study group at baseline; SG-T1 = study group after 3 months of
training; CG-T0 = control group at baseline; CG-T1 = control
group after 3 months of training.

Pedometer-measured daily activity of the patients in

group S significantly increased from baseline to 3 months
later, both the average number of daily steps (3,079
2,483 vs. 3,767 2,878, p = 0.024) and the walking energy expenditure (67 64 vs. 101 77 calories, p = 0.001),
while in group C the daily activity remained the same: the
average number of daily steps (2,993 2,142 vs. 3,019
2,037, p = 0.142) and the walking energy expenditure (61
58 vs. 62 60). There was a significant difference between groups S and C at the end of the study, respectively: daily steps (3,767 2,878 vs. 3,019 2,037, p = 0.044)
and calories (101 77 vs. 62 60, p = 0.032).

Discussion

Regarding the hemodynamic changes, the 9-mm Hg

reduction of SBP and the 11-mm Hg decrease of aortic
blood pressure driven only by exercise training are consistent with other published study results [10].
Although the mean PWV values both in the study and
the control group patients were less than the cut-off value
of 12 m/s considered to be high in HD patients, the significant 1-m/s reduction of the PWV obtained with exercise training while the control group had a 1.3-m/s increase of the PWV represents a possible improvement of
the cardiovascular prognosis and mortality of the trained
patients [11, 12].
76

Nephron Clin Pract 2013;124:7278

DOI: 10.1159/000355856

Since the RT of the pulse wave is directly linked to the

PWV and inversely proportional to it, hence an indirect
measure of arterial stiffness, our results showing a statistically significant increase of the RT in the study group and
a decrease in the control group constitute further evidence of the aortic stiffness reduction following exercise
training.
Interestingly, the physical exercise had no impact on
the tone of small arteries and arterioles. Aortic Aix and
PP, two parameters that provide information on the small
vessels tone and endothelial dysfunction, suffered no significant changes throughout the study protocol. However, their mean detected values are definitely in the pathological range (Aix >10%, PP >40 mm Hg) [13]. One possible explanation for the lack of impact of the exercise
training on the small vessels tone is the typical calcification of the small arteries affecting the vast majority of
CKD patients from the early stages, especially those on
maintenance dialysis, a very advanced form of arteriosclerosis and arteriolosclerosis.
Although published studies have highlighted both SBP
and DBP reduction in the trained HD patients, our results
showed no statistical significant effect on the DBP, but a
reassuring 10-mm Hg decrease in both central and peripheral blood pressure was noticeable in the study group
[10].
The combined PWV and SBP reduction led to the conclusion that the main possible mechanism of arterial stiffness reduction by the exercise training was blood pressure-dependent and not a result of arterial wall structure
changes. According to a study published by Guerin et al.
[14], lowering blood pressure in end-stage renal disease
patients has a positive impact on survival only when accompanied by PWV improvement, an indicator of the
lack of advanced vascular lesions. We could not objectively analyze the extent of vascular wall damage in our
study population, but the positive results on SBP and the
non-significant changes of DBP are consistent with a
more probable involvement of neurohumoral mechanisms rather than structural adaptation changes (i.e. vascular remodeling or angiogenesis) driven by the exercise
training protocol.
Even though there were no significant differences between trained and non-trained patients at the end of the
study, the increase of muscular content of the body in the
study group is a highly desired result, as the gain of muscle mass is associated with an increase in HD patients
survival [15]. A previous study by Kouidi et al. [16] demonstrated the significant increases in type I, type IIa and
type IIx muscle fiber and reduction of atrophic fiber in
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50

HD patients following resistance exercise training. This

could be the case in our study as a potential mechanism
for increasing muscle mass in our HD patients.
HD patients are weak compared with the healthy sedentary population strength, and that weakness impairs
their physical function [1719]. Muscular performance
of the trained muscle groups improved significantly in
our trained patients (table3). These findings are consistent with the results of previous studies in which resistance training had a positive impact on strength and functional measures in patients with end-stage renal disease
[19, 20]. The probable mechanism of muscular performance improvement is muscle hypertrophy, as well as a
potential positive impact on mitochondrial energy metabolism found to be deficient in HD patients, as demonstrated in other published research results [21, 22].
In addition to the supervised training, there was an increase in the self-driven physical activity, the patients in
the study group becoming more physically active in their
everyday life by increasing the average number of daily
steps and the walking energy expenditure and becoming
significantly more physically active than the control
group by the end of the study. These findings could also
explain the increase in the muscle mass of the trained patients. An increase in the physical activity could lead to a
better survival rate, since previous studies proved a 62%
higher 1-year mortality risk of sedentary HD patients as
compared to the more active ones [17, 23].
Our study has some limitations. The small number of
patients and the relatively short duration of the intervention are two of them. We used licensed physical therapists
who applied a special set of physical exercises adjusted to

the dialysis session condition and no standardized cycle

ergometer. Another limitation of the study is the lack of
evaluation of the patients 2 months after the end of the
study, as the results published in the literature showed a
loss of hemodynamic positive effects 2 months after the
exercise training ceased [17, 24].
In our opinion, the most important result of our study
is the proof that, even in a very high cardiovascular risk
population, e.g. chronic HD patients, exercise training
can improve the aortic arterial stiffness and can be an effective non-pharmacological method of lowering SBP.
Another important finding is that even 3 months of 3
times/week intradialytic physical exercise may have a
positive effect on the body muscle mass and the strength
of a sedentary population and on its daily physical activity.

Conclusions

Exercise training during dialysis is a proven non-pharmacological method of decreasing arterial stiffness in a
low-trained high cardiovascular risk population, such as
chronic HD patients. Further well-designed studies are
needed to evaluate the direct correlation between physical exercise and cardiovascular morbidity and mortality
reduction in such patients.

Disclosure Statement
The authors have no conflicts of interest to disclose.

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Benefits of Exercise Training during

Dialysis

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Nephron Clin Pract 2013;124:7278

DOI: 10.1159/000355856

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