ASAIO Journal 2011
The Effect of Prolonged Intradialytic Exercise in Hemodialysis
Efficiency Indices
CHRISTOFOROS D. GIANNAKI,*† IOANNIS STEFANIDIS,*‡ CHRISTINA KARATZAFERI,‡§ NIKOS LIAKOS,储 VIOLETA ROKA,*
IOANNA NTENTE,§ AND GIORGOS K. SAKKAS*‡
Optimal hemodialysis (HD) dose is very important to pa-
tients’ health and survival, and various indices of adequacy
have been incorporated into the current clinical practice to
monitor HD efficiency. Exercise during HD could facilitate
solute removal; however, it is still unknown whether pro-
longed intradialytic exercise could further improve HD
efficiency. Ten stable “high-functioning” HD patients volun-
teered to participate. The patients were studied under two
scenarios during HD: 1) supine exercise (cycling) for 3 hours
at 40% of maximum exercise capacity and 2) no exercise as
usual. Blood sampling was acquired pre- and post-HD in both
scenarios to calculate the HD efficiency indices. All patients
completed the exercise regime with no adverse effects.
Rather, all efficiency indices significantly improved in the
prolonged exercise scenario, compared with the no-exercise
one. In particular Kt/V, urea reduction ratio, and creatinine
reduction ratio significantly improved by 20%, 11%, and
26%, respectively, while potassium plasma levels were re-
duced by 77.5% (p < 0.05). In conclusion, prolonged low-
intensity intradialytic exercise improved HD efficiency, with
no adverse effects. HD patients should be encouraged to
participate in exercise regimes not only for the known long-
term benefits regarding their cardiovascular health but also
for the acute effect of exercise in the HD adequacy. ASAIO
Journal 2011; 57:213–218.
T he uremic syndrome is a consequence of a failing kidney
function that leads to the accumulation of body fluids and
byproducts which in turn induce systemic damages in a
concentration-dependent manner.1 Hemodialysis (HD) is a
substitute to transplantation therapy that occurs three times a
week for approximately 4 hours per session and lasts until the
patient receives an allograph or for a patient’s whole life.
Optimal HD dose and dialysis frequency is very important to
patients’ health and survival and for these reasons various
From the *Departments of Nephrology, School of Medicine, Uni-
versity of Thessaly, Larissa, Greece; †Department of Life and Health
Sciences, University of Nicosia, Nicosia, Cyprus; ‡Center for Research
and Technology-Thessaly, Greece; §Department of Sport Science,
University of Thessaly, Trikala, Greece; and 储Department of Biochem-
istry, School of Medicine, University of Thessaly, Larissa, Greece.
Submitted for consideration September 2010; accepted for publica-
tion in revised form February 2011.
Reprint Requests: Christoforos D. Giannaki, PhD, University General
Hospital of Larissa, Nephrology Clinic, Hemodialysis Unit, Mezourlo
Hills, GR 41-110 Larissa, Greece. Email: giannaki@med.uth.gr.
DOI: 10.1097/MAT.0b013e318215dc9e
213
indices of adequacy have been incorporated into the current
clinical practice to monitor dialysis efficiency.1
An HD treatment is characterized as “adequate” when the
patients are fully rehabilitated from uremia symptoms, have
good nutritional status, sufficient production of red blood cells,
maintain normal blood pressure, and the development of neu-
ropathy is prevented.2 The most popular HD adequacy index
is the Kt/Vurea, which represents the urea clearance at t time of
HD treatment per unit of urea distribution volume. A good Kt/V
is translated into better solute removal and this has been
associated with less organ toxicity since in the medium long
term the vital organs are generally exposed into less toxicity
reducing thus the severity of systemic damage.3 HD efficiency
can be improved by manipulating HD procedure in ways such
as increasing the duration or frequency of HD session, increas-
ing the HD solution flow rate, and by using high-flux HD
techniques.
Survival in patients treated with HD is influenced by the
dialysis dose and unfortunately the statistics are disappointing
for such a “lifesaving therapy.”4 The results of the HEMO study
show that the minimum recommended dialysis dose is also the
best possible attainable and therefore interest is now turning to
alternative approaches modifying the HD session to improve
patients treatment and survival.5
Intradialytic exercise also influence HD efficiency when it is
implemented either chronically6,7 or acutely.8 A single bout of
60-minute intradialytic exercise at submaximal level improved
HD efficiency by 14%, corresponding approximately to a
20-minute extra HD time.8 For the past three decades, intra-
dialytic exercise programs have been applied in many HD
units worldwide to improve the patient’s general health and
quality of life. Benefits from an exercise training program
include improvements in muscle size and composition, func-
tional capacity and cardiorespiratory fitness, blood pressure,
cardiac dysfunction, and improving mental health.9 –13 Such
improvements have been also observed after daily HD (six
sessions/week) or nocturnal HD (for a review, see Ref. 1);
however, such treatment options require specific and com-
plex organization including training centers for patients,
in-house nursing assistance, and 24/7 technical assistance
and support.14
So far, there are no available treatment options that can be
applied within an HD protocol without modifying the duration or
the frequency of HD. Even though such approaches could be
very effective in terms of HD adequacy, they alter patients’ life
schedule; reduce quality of life leading inevitably to a very low
adherence. Although brief intermediate exercise during HD
can improve dialysis efficiency by 14%,8 it has not yet been
examined whether a single bout of continued low-intensity
214 GIANNAKI ET AL.
intradialytic exercise could possibly lead to further improve-
ments in HD efficiency markers. The current study aims to
examine whether a low-intensity intradialytic continued aero-
bic exercise bout lasting for approximately 3 hours could
further improve HD efficiency markers.
Methods
Subjects
Thirty-six stable HD patients were screened for the current
study; however, only 10 patients (45.7 ⫾ 10.9 years, 2 fe-
males) fulfilled the inclusion criteria and agreed to participate
to the study. All patients gave written informed consent for
study participation after full explanation of the procedure. The
study was approved by the Human Research and Ethics Com-
mittee at the University of Thessaly.
Inclusion Criteria
The entry criteria for the study were receipt of chronic HD
for 6 months or more with adequate HD delivery (Kt/V ⬎1.0),
stable clinical condition, and arm arteriovenous fistula. Pa-
tients should have scored on the subjective physical health
component scale in the Short Form-36 (SF-36) health survey
quality of life questionnaire a score ⱖ75 points, which was
considered as the cut-off point for “high-conditioning” HD
patients.
Exclusion Criteria
Patients were not allowed to participate to the study if
they had reasons for being in a catabolic state (including
malignancies, HIV, opportunistic infections, infections that
required intravenous antibiotics, etc.), within 3 months be-
fore enrollment. In addition, patients were excluded if they
had any serious cardiovascular disease or even experienced
a cardiac event or angina in the past, as well as if they had
symptoms of uncontrolled hypertension or hypotension dur-
ing the HD session.
Study Design
The patients were studied under two different scenarios that
took place during HD in the same mid-week day of two
consecutive weeks. In particular, in the first scenario, the
patient was required to act as usual during a typical HD
session. In contrast, the second scenario required the patient to
continuously cycle in the supine position for 3 hours during
the HD session. The order of the scenarios was always the
same (the no-exercise scenario applied first) to eliminate any
exercise effect induced by the prolonged exercise regime,
which could influence the following week’s testing. In both
scenarios, blood samples were collected before and after the
initiation and the termination of the HD session to calculate
the dialysis efficacy indices. The patients were asked to avoid
any food and fluid intake during HD in both scenarios. In
addition, the patients were recommended to maintain a stable
fluid intake during the 2-week period of the study.
Rate of Perceived Exertion
To assess the patient’s self-reported level of intensity during
the exercise session, we used the scale of rating of perceived
exertion (RPE) developed by Borg.15 Briefly, the Borg RPE scale
is 15-point scale (ranges from 6 to 20), with 6 to denote “no
exertion at all” and 20 to denote “maximal exertion.”
HD Procedure
The patients underwent the HD therapy (Fresenius 4008B,
Oberursel, Germany) with low-flux, hollow-fiber dialyzers and
bicarbonate buffer. The HD session lasted 4 hours. An enoxa-
parin dose of 40 – 60 mg was administered intravenously
before the beginning of each HD treatment session. Erythro-
poietin (EPO) therapy was given after the completion of HD
session to normalize hemoglobin levels within 11–12 g/dl. The
dialysate temperature was maintained at 36.5°C in both sce-
narios to keep a relatively constant body temperature. The
dialysate temperature was assessed through a sensor in the
blood line of the HD machine. The HD procedure was per-
formed exactly the same way for both scenarios, while all HD
sessions lasted precisely 4 hours.
HD Efficiency Indices
To calculate HD efficiency indices, blood samples were
collected from the arterial needle exactly before the initializa-
tion of the HD session as well as from the arterial line after 20
seconds of slow blood flow (100 ml/min) according to the
clinical practice guidelines for HD adequacy of the National
Kidney Foundation.16
A single-pool Kt/V was calculated from pre- and post-HD
blood urea nitrogen (BUN) measurements according to the
Daugirdas second-generation formula17 as follows:
Kt/V ⫽ ⫺In共R ⫺ 0.008 * t兲 ⫹ 共4 ⫺ 3.5 * R兲 * UF/W
where R denotes the ratio of the post-HD to pre-HD BUN
concentration, t indicates HD treatment time in hours, UF
denotes the volume of fluid removed during the HD treat-
ment in liters, and W indicates the post-HD body weight in
kilograms.
The reduction ratios of BUN and creatinine were calculated
from pre- and post-HD BUN and creatinine concentrations,
respectively:
URR: [(urea pre
⫺ urea post hemodialysis)/urea pre hemodialysis] ⫻ 100%
CRR: [(creatinine per
⫺ creatinine post-hemodialysis)/ creatinine pre hemodialysis]
⫻ 100%
Exercise Regime
The exercise regime required the patients to participate in an
intradialytic exercise program on a bedside cycle ergometer
(Model 881 Monark Rehab Trainer, Monark Exercise AB,
Varberg, Sweden). Exercise session included supine cycling for
a duration of 3 hours in an intensity of 40% of the patient’s
maximal exercise capacity. The appropriate level of exercise
has been estimated through a modified version of Åstrand
Bicycle Ergometer Test Protocol during a previous dialysis
session,18 2 weeks before the start of the study with a cali-
 EXERCISE EFFECT ON HEMODIALYSIS EFFICIENCY 215

brated ergometer. The exercise regime started 30 minutes after Table 1. General Patients’ Characteristics and Functional
the initiation of the HD session and ended 30 minutes before Capacity
the end of the HD session. The exercise regimes were per-
Variables Patients Data
formed under the continuous supervision of an exercise phys-
iologist and a nephrologist, while blood pressure and heart rate N 10
levels were monitored automatically by the dialysis machine. Female/male 2/8
Patients were allowed to watch TV or listen to music during the Age (yr) 45.7 ⫾ 10.9
BMI (kg/m2) 27.0 ⫾ 3.7
exercise session (and the same practices were adopted in both Kt/V 1.09 ⫾ 0.03
scenarios). Years in hemodialysis 3.5 ⫾ 1.9
Albumin (g/dl) 4.2 ⫾ 0.3
Serum ferritin (ng/ml) 216.7 ⫾ 131.3
Criteria of Potential Discontinuation of the Exercise Protocol Serum iron (␮g/dl) 65.3 ⫾ 19.1
Hct 38.9 ⫾ 4.0
The exercise protocol would be terminated in the case of a
Hb (g/dL) 12.7 ⫾ 1.2
patient complaining for muscle cramps, giving an hypotension SF-36 physical health dimension 83.1 ⫾ 7.6
episode, arrhythmias, chest pain, exhaustion or excessive fa- NSRI test (s) 52.1 ⫾ 9.6
tigue, reporting a score in Borg scale ⬎17, or if a repetitive STS-60 (rep) 30.7 ⫾ 3.6
disturbance (alarm) of the HD procedure occurred.
BMI, body mass index; Kt/V, hemodialysis adequacy, Hct, hemat-
ocrit; Hb, hemoglobin; SF36, simple questionnaire; NSRI, North
Subjective Physical Health Assessment Staffordshire Royal Infirmary test; STS-60, sit-to-stand test 60 s.

The patient’s subjective quality of life outcomes were eval-

uated by using a SF-36 health survey version modified for
patients receiving HD therapy.19 The patient’s grade in the
physical health component was considered as “physical func-
tioning” score.20,21
Functional Capacity Assessment
The patient’s functional capacity levels were evaluated us-
ing the North Staffordshire Royal Infirmary (NSRI) walk test and
by a sit-to-stand test (STS-60), both used successfully for the
assessment of functional capacity of HD patients.20 Briefly, the
NSRI walk test consists of the time in seconds taken to com-
plete a task of 50 m continuous walk, climbing up 22 stairs
(total elevation 3.3 m), climbing down 22 stairs, and walking
back 50 m to the starting point.22 The STS-60 test is considered
as a surrogate index of muscular endurance and it assesses the
number of sit-to-stand cycles achieved in 60 seconds.23
Statistical Analysis
The changes in the examined variables between the exercise
and the no-exercise scenario as well as the differences within
the predialysis data between the two scenarios were evaluated
using paired t tests. All analyses were carried out using the
Statistical Package for the Social Sciences software (SPSS for
Windows, version 13.0, Chicago, IL). Data are presented as
mean ⫾ SD, and the level for statistical significance was set at
p ⱕ 0.05. Based on post hoc power analysis, the 10 recruited
subjects provided an 81.3% power to detect a standardized
effect size of 1.01, with ␣ ⫽ 0.05 and critical t ⫽ 2.26.
potassium levels before and after HD in the exercise session
also appeared to be significantly increased (p ⫽ 0.046) (1.26 ⫾
0.16 exercise vs. 0.71 ⫾ 0.22 no exercise) (Figure 4).
None of the patients complained for any special discomfort
during the exercise regime. Assessed by the Borg RPE scale, no
patient reported a score above 17, which would have indi-
cated a “heavy effort.” In addition, none of the monitored
parameters showed evidence for discontinuation of the exer-
cise session according to the guidelines of the American Col-
lege of Cardiology and the American Heart Association.24 Our
participants were assessed as “high functioning patients” be-
cause they scored ⬎75% in the SF-36 physical health dimen-
sion. Reinforcing the previous statement, the patients of the
current study had also scored high values in both functional
tests (STS60 and NSRI) compared with other studies using the
same methodology.23
Discussion
This is the first study to investigate whether a single bout of
low-intensity prolonged intradialytic exercise could help im-
prove HD efficiency markers. We found that an HD session in
combination with low-intensity exercise was well tolerated by
our high-functioning HD patients and resulted in a significant
improvement in all examined indices of HD adequacy com-
pared with the traditional no-exercise scenario.
According to the literature, only one study has so far at-
tempted to investigate the potential effect of exercise on HD
efficiency.8 In particular, Kong et al.8 using an acute interme-

Results Table 2. Prehemodialysis Values in the Two Scenarios

The patients’ characteristics and functional capacity data are No-Exercise Exercise
presented in Table 1. The statistical analysis of the examined Variables Session Session p
variables did not show any significant differences between the
Weight (kg) 80.4 ⫾ 9.1 80.5 ⫾ 9.2 0.753
“pre-hemodialysis” values for the two consecutive mid-week Urea prehemodialysis (mg/dl) 136.6 ⫾ 38.1 143.4 ⫾ 38.8 0.536
HD sessions (p ⬎ 0.05) (Table 2). Creatinine prehemodialysis 7.8 ⫾ 1.8 8.6 ⫾ 2.4 0.062
Kt/V, CRR, and URR were found to be significantly improved (mg/dl)
in the exercise session compared with the no-exercise session, Potassium prehemodialysis 4.3 ⫾ 0.7 4.5 ⫾ 0.7 0.237
(mmol/L)
p ⬍ 0.05 (Figures 1–3). In addition, the difference within the
216 GIANNAKI ET AL.
Figure 1. Kt/V in the exercise and no-exercise hemodialysis ses-
sion. Large rectangles represent the average values, while smaller
shapes represent individual data in the no-exercise and exercise
hemodialysis sessions. Data are mean values. Kt/V, hemodialysis
adequacy.
diate exercise bout of approximately 60-minute duration ob-
served significant improvements in Kt/V and URR as well as
urea, creatinine, and potassium post-HD rebound. In the study
by Kong et al., the Kt/V increased by 14% as a result of a single
exercise bout and the authors estimated that this improvement
was equivalent to extending the HD session by 20 minutes.
In the current study, we used a prolonged intradialytic ex-
ercise regime using “high-functioning” HD patients to assess
whether an additional improvement would occur. Indeed, our
data revealed that this type of exercise could evoke significant
improvements in Kt/V, URR, and CRR by 20%, 11% and 26%,
respectively, compared with the no-exercise scenario. It seems
that a prolonged exercise regime could achieve better scores in
HD adequacy than the conventional 45-minute intradialytic
exercise regimes. However, it appears logical to question the
Figure 2. Creatinine reduction ratio in the exercise and no-
exercise hemodialysis session. Large rectangles represent the av-
erage values, while smaller shapes represent individual data in the
no-exercise and exercise hemodialysis sessions. Data are mean
values. CRR, creatinine reduction ratio.
Figure 3. Urea reduction ratio in the exercise and no-exercise
hemodialysis session. Large rectangles represent the average
values, while smaller shapes represent individual data in the
no-exercise and exercise hemodialysis sessions. Data are mean
values. URR, urea reduction ratio.
applicability of such a prolong regime in such fragile popula-
tion. It is very encouraging that in the current study, 10 of 36
patients were capable of participating in such a trial despite the
fact that HD patients are known for their very low fitness and
functional capacity levels.10 In addition, by using a simple
questionnaire (SF36), it appears that patients can be screened
for their functional status, and if they score above 75% in the
“Physical Health” component, they would be more likely to be
able to participate in such regime,21 whereas if they score
lower, a possible reduction in the duration of exercise could be
considered.
The possible mechanism by which exercise could enhance
the removal of urea and creatinine is not entirely clear. How-
Figure 4. Change between pre- and posthemodialysis in plasma
potassium concentrations in the exercise and no-exercise hemodi-
alysis session. Large rectangles represent the average values, while
smaller shapes represent individual data in the no-exercise and
exercise hemodialysis sessions. Data are mean values.
 EXERCISE EFFECT ON HEMODIALYSIS EFFICIENCY
ever, it is known that large amounts of urea and creatinine are
taken up and stored in low-perfusion tissues such as skeletal
muscles, skin, and bones.25 On the other hand, exercise in-
duces vasodilatation and augments muscle blood flow, there-
fore enhancing the perfusion between muscle fibers and
capillaries.26 –28 The increased perfusion induced by the exer-
cise lead to a rise in the exchange between the intercellular
and intravascular compartments within the skeletal muscles.
The increased blood flow that follows exercise activity mobi-
lizes the intramuscular urea and creatinine and transfer them
into the systemic circulation and from there and through the
HD filter outside the patients’ body. It might be also suggested
that the vasoconstriction of the nonworking muscles might
induce a stronger stimulus, superior or additive to the vasodi-
latative one, leading to a reduction of the perfused volume and
thus a better/faster solute removal as a consequence.
A very impressive effect of this exercise protocol was ob-
served in the removal of the potassium plasma levels. Even
though it is known that exercise increases release of potassium
from the working skeletal muscles into plasma,29 a reduction
of 77.5% in potassium plasma concentrations was observed
after the applied exercise regime. This is very important as one
of the most common and silent conditions that could lead to a
heart attack and/or arrhythmias in HD patients is hyperkale-
mia.30 Hyperkalemia is a condition of medical emergency,
which requires immediate dialysis to reduce total body potas-
sium levels not only in HD patients but also in other chronic
and acute conditions. It is often encountered after excessive
consumption of vegetables and fruits despite the specific nu-
tritional guidelines applied to HD patients against consump-
tion of “potassium-rich” products. The fact that prolonged
exercise during dialysis appeared to be efficacious in terms of
reducing potassium levels compared with the conventional
HD could be a useful tool in patients who have difficulties in
controlling blood potassium levels.
Even though the benefits derived from an exercise training
program in HD patients are very well established, in fact, the
majority of the nephrologists still hesitate to implement exer-
cise as part of a routine HD care, while the patients remained
inactive with poor exercise capacity and low quality of
life.31,32 We strongly recommend that the HD patients should
be encouraged and motivated to participate in supervised
exercise training programs and as we saw in the current study,
a 25% of the patients could tolerate such a long-lasting exer-
cise regimes. Taking into account the fact that the median age
of patients entering in HD appeared to be slightly decreased in
the recent years,33 it would be even easier to recruit younger
patients in such exercise programs.
Limitations
In the current trial, we did not assess any postdialysis re-
bound phenomena of the examined substances. The lack of
those measurements does not allow us to discuss in depth the
possible effects of the prolonged exercise regime in postdialy-
sis kinetics and the predicted Kt/V and leaves us presently
unable to calculate the effects of the current exercise scenario
on solute removal, expressed by dialysis time.
In conclusion, this is the first study to examine the effect of
prolonged intradialytic exercise on HD adequacy. We found
that preselected “high-functioning” HD patients could tolerate
217
such type of exercise regime with no side effects, resulting in
significant improvements in HD efficiency markers compared
with a typical no-exercise HD session. Taking into account the
fact that the study was realized using low-flux treatments, these
findings have the added value of improving overall treatment
efficiency and potassium removal. Further studies should ex-
amine whether there is an appropriate exercise approach for
low-functioning patients. Hemodialysis patients should be en-
couraged and motivated to participate in intradialytic exercise
programs not only for the well-known long-term benefits re-
garding the cardiovascular health but also for the acute bene-
fits in the HD adequacy.
Acknowledgment
The authors thank the nursing staff at the hemodialysis unit of the
University Hospital of Larissa and the General Hospital of Trikala for
their cooperation. The authors also thank all hemodialysis patients for
participating in this study.
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