Received: 13 June 2019 Revised: 21 November 2019 Accepted: 27 December 2019

DOI: 10.1111/1744-9987.13469

ORIGINAL ARTICLE

Exercise training during hemodialysis sessions: Physical

and biochemical benefits

Esther Torres1 | Ines Aragoncillo1,2 | Jorge Moreno3 | Almudena Vega1,2 |

Soraya Abad1,2 | Ana García-Prieto1 | Nicolas Macias1,2 |
Andres Hernandez1 | Maria Teresa Godino3 | Jose Luño1,2

1
Department of Nephrology, Hospital
General Universitario Gregorio Marañon,
Abstract
Madrid, Spain Chronic inflammation, protein-energy wasting, and poor physical functioning are
2
Spanish Research Network highly prevalent among patients with chronic kidney disease (CKD). These factors
(REDINREN), Madrid, Spain
are associated with disability and increase of cardiovascular risk. The aim of this
3
Servicio de Rehabilitación, Hospital
General Universitario Gregorio Maranón,
study is to evaluate the effects of exercise training during hemodialysis
Madrid, Spain (HD) sessions on physical functioning, body composition, and nutritional and
inflammatory status. We performed a prospective intervention study including
Correspondence
Esther Torres, Department of Nephrology, patients on prevalent HD therapy. Patients were evaluated at baseline visit by
Hospital General Universitario Gregorio Rehabilitation and Physiotherapy specialists and the exercise program was adapted
Marañon, Madrid, Spain.
to each patient's physical capacity. In addition to demographic, clinical, body com-
Email: estertor.ag@gmail.com
position and functional ability data, serum markers regarding nutritional and
inflammatory status were collected at baseline and after 3 months of exercise train-
ing. We observed a significant improvement after 3-month follow-up in functional
ability (6 minute walk test [6MWT] [403.15 ± 105.4 vs 431.81 ± 115.5 m,
P < .001], sit-to-stand repetitions in 30 seconds [12.2 ± 4.2 vs 14.1 ± 5.0 repetitions,
P = .003] and dynamometry [24.5 ± 11.9 vs 29.5 ± 12.5 kg, P < 0.001]), body com-
position with increase of body mass index (BMI) (23.7 ± 4.4 vs 24.1 ± 4.7 kg/m2,
P = 0.01) at the expense of lean tissue index (LTI) (14.9 ± 3.7 vs 16.2 ± 2.9 kg/m2,
P = 0.038) and lipid parameters with LDL-cholesterol decrease (70.2 ± 17.9 vs
64.9 ± 21.3 mg/dL, P = .03) and lower serum triglyceride levels (125.8 ± 54.0 vs
108.2 ± 44.6 mg/dL, P = .006). In addition, we found a decrease in iron (155.6
± 148.2 vs 116.7 ± 110.8 mg, P = .029) and erythropoietin (117.5 ± 84.2 vs 99.2
± 74.5 μg, P = .023) requirements. The implementation of exercise training pro-
grams during HD can improve physical functioning, body composition and lipid
and anemia profile. Supervised exercise programs could be included as part of HD
patient care to improve physical capacity in these patients.

KEYWORDS
bioimpedance, body composition, cardiovascular events, chronic kidney disease, exercise
training, hemodialysis, nutritional status, physical functioning

© 2019 International Society for Apheresis, Japanese Society for Apheresis, and Japanese Society for Dialysis Therapy

Ther Apher Dial. 2020;1–7. wileyonlinelibrary.com/journal/tap 1

2 TORRES ET AL.
1 | INTRODUCTION
Incidence and prevalence of chronic kidney disease
(CKD) has significantly increased worldwide over the
past decades due to an aging population with a rising
prevalence of comorbid factors such as diabetes and
hypertension.1
Muscle wasting, abnormalities in muscle function,
low exercise capacity, and poor physical functioning are
highly prevalent among patient with CKD.2–4 Protein-
energy wasting (PEW), a term to describe loss of body
protein mass and fuel reserves condition,5 is frequently
observed in patients with CKD and has been associated
with chronic inflammation, metabolic acidosis, oxidative
stress, accumulation of uremic toxins, malnutrition, and
insulin resistance.6
In addition to these problems, CKD is related to
comorbid conditions such as hypertension, diabetes
mellitus, heart failure, arteriosclerosis, and the dialysis
procedure per se which contributes to exacerbation of
PEW.7 These factors are associated with loss of inde-
pendence, development of disability, and increase of
cardiovascular risk and mortality.8 The advantages of
exercise in the general population are related to better
control of diabetes and insulin resistance, improve-
ment in BP control, reduced risk for cardiovascular
mortality and improved psychological and physical
functioning with an enhancement in health-related
quality of life.2 All these comorbidities are especially
common in patients with CKD; therefore, exercise
training could provide important advantages in CKD
patients.
Many studies carried out in HD patients have shown
an improvement in muscular functioning, aerobic capac-
ity, cardiovascular function, walking capacity, and
health-related quality of life with programs combining
aerobic and resistance exercise during HD.7,9–18 With an
increasing proportion of elderly patients in HD units with
higher sedentary behavior, it is necessary to find strate-
gies to improve their physical functioning.
On this basis, we performed a study to evaluate the
benefits of exercise training during HD sessions on physi-
cal functioning, body composition, and nutritional and
inflammatory status in patients with CKD in HD.
2 | P A T I E N T S A N D ME T H O D S
2.1 | Design of the study
This is a prospective, intervention, and noncontrolled
study to assess the effects of exercise training routine
during HD sessions on physical functioning, body
composition, and nutritional and inflammatory status. The
design was performed in collaboration with nephrology
and rehabilitation doctors from Gregorio Marañon Hospi-
tal, in Madrid, Spain. Variables were collected at the begin-
ning of the study and after 3 months.
Informed consent was obtained. The study was con-
ducted according to the Declaration of Helsinki. Ethical
approval was granted by local ethical committee from
Gregorio Marañon Hospital on 29 June 2017.
2.2 | Study population
We included patients on HD therapy from a single center
in Madrid. Inclusion criteria were age > 18 years, clinical
stability with no hospitalizations in the previous 3 months
and 3-month prevalence in HD program before the inclu-
sion. Exclusion criteria were physical or psychological
inability to exercise, recent cardiovascular event or any
other comorbidity to contraindicate mild or moderate
exercise.
2.3 | Baseline variables
At baseline, demographic and clinical data were col-
lected, including age, sex, CKD etiology, time under HD
therapy, functional ability, body composition, and labo-
ratory variables. All parameters were collected
predialysis. We also collected data about lipid lowering
therapy, monthly dose of erythropoietin (EPO), monthly
dose of iron supply, and number of daily phosphate
blinders.
Body composition was assessed by bioimpedance
using BIS (body composition monitor, Fresenius Medi-
cal Care, Bad Homburg, Germany). Measurements
were taken after a 10-minute resting period in the
supine position. Weight, body mass index (BMI), lean
tissue index (LTI [kg/m 2]), and fat tissue index (FTI
[kg/m2 ]) data were collected. Hydration parameters
such as total body water (TBW [L]), intracellular water
(ICW [L]), extracellular water (ECW [L]), and fluid
overload (OH [L]) considered as excess water were
also evaluated.
Functional ability was assessed by the 6 minute-walk
test (6MWT [m]), sit-to-stand repetitions in 30 seconds
and upper extremity strength measured by dynamometry.
Evaluated laboratory variables were total cholesterol,
low-density lipoprotein cholesterol (LDL), high-density
lipoprotein cholesterol (HDL), triglycerides, proteins, albu-
min, hemoglobin, ferritin, and C-reactive protein (CRP).
Laboratory variables were measured using standard-
ized methods with autoanalyzer.
TORRES ET AL. 3

2.4 | Exercise training Exercises were performed with one's own body weight or
with ballasts, depending on ability and evolution of
Patients were evaluated at baseline visit by rehabilitation patients.
and physiotherapy specialists and exercises were adapted Lower limbs exercises consisted of 20 repetitions with
to each patient physical capacity. each leg, alternating legs for each exercise (knee extension,
The exercise routine was based on sets of bending hip flexion, and hip abduction). A set consisted of three exer-
and stretching of arms and legs repetitions, hip abduc- cises with both members and the objective was four sets.
tion, and hand grip exercises. Upper limbs exercises consisted of 20 repetitions of
The exercise routine was performed during the first shoulder flexion, elbow flexion, elbow extend, shoulder
hour of each HD session, with an approximate duration adduction, and exercises with hand grip. These exercises
of 45 to 50 minutes during three weekly sessions. were conducted with the arm without the arteriovenous
fistula. A set consisted of five exercises and the objective
was to achieve four sets.
T A B L E 1 Baseline characteristics of the study If patients were able to perform 20 repetitions with
population (n = 36) one's own body weight easily ballasts were added. They
Baseline characteristics Value took breaks as needed.
Age (years), mean ± SD 56 ± 17
The exercise program was monitored by the staff of
HD units in each HD session and the weights lifted and
Sex (male %) 61%
hand grip resistances were progressively increased
Hypertension (%) 89%
according to the progression of patients.
Diabetes mellitus (%) 31% Patients were followed-up for 3 months and we deter-
CKD etiology (%) mined laboratory variables, body composition, physical
Glomerular 31% test, and drug therapy again after this period. We evalu-
Diabetes 19% ated results and incidents during the follow-up.
Vascular 8%
Interstitial 6%
2.5 | Statistical analysis
Polycystic 11%
Unknown 8% All variables were analyzed using a Kolmogorov-Smirnov
Other 17% test to classify them as normally or non-normally distrib-
Vascular access (%) uted. Qualitative variables were given with their frequency
Arteriovenous fistula 75%
distribution. Quantitative variables were given as mean and
SD (SD) or median and interquartile range (IQR) depending
Central venous catheter 25%
on their distribution. Quantitative variables were analyzed
Duration of HD (years), mean ± SD 3.36 ± 4.6
using Student's t-test and ANOVA. All statistical analyses were
Abbreviations: CKD, chronic kidney disease; HD, hemodialysis. performed with SPSS 20.0 software (SPSS; Chicago, IL).
P values < .05 were considered statistically significant.

F I G U R E 1 Physical test. Variables are

expressed as a mean ± SD (SD). 6MWT:
6 minute walk test
4 TORRES ET AL.

3 | R E SUL T S compared to baseline evaluation in the 6MWT (403.15

± 105.4 m vs 431.81 ± 115.5 m, P < .001), sit-to-stand
We included 51 patients out of 84 total prevalent patients repetitions in 30 seconds (12.2 ± 4.2 vs 14.1 ± 5.0 repeti-
in our HD unit. Of these, 15 patients left study early in tions, P = .003), and dynamometry (24.5 ± 11.9 vs 29.5
first months due to: transfer to other center (two ± 12.5 kg, P < .001) (Figure 1).
patients), exitus (one patient), surgery, and hospitaliza- As shown in Table 2, body composition also improved
tion (one patient) or voluntary leaving for lack of adhe- during follow-up with increased BMI (23.7 ± 4.4 vs 24.1
sion unrelated to adverse events (11 patients). ± 4.7 kg/m2, P = .01) at the expense of LTI (14.9 ± 3.7 vs
A total of 36 patients were analyzed with a mean age 16.2 ± 2.9 kg/m2, P = .038) with minimum reduction of
of 56 ± 17 years. Baseline characteristics of the study FTI (8.0 ± 4.9 vs 7.4 ± 4.8 kg/m2, P = .27). We observed
population are shown in Table 1. About 78% of the an increase in total body water (38.2 ± 8.6 vs 39.4
patients lived accompanied, 12% alone and none in resi- ± 9.0 L, P = .05) with slight decrease in OH (1.6 ± 1.8 vs
dence; 83% were autonomous to walk. 1.4 ± 1.3 L, P = .599), an increase in ICW (20.7 ± 5.2 vs
All patients underwent high flux hemodialysis ther- 21.6 ± 5.2 L, P = .034) and nonsignificant increase in
apy three times a week in 240 minute sessions achieving ECW (17.5 ± 3.9 vs 17.8 ± 4.1 L, P = .366).
Kt/V > 1.4. Laboratory variables analyzed before and after follow-
Regarding physical functioning, we observed a signifi- up are shown in Table 3. We observed a significant
cant improvement at the end of the 3-month follow-up improvement in lipid parameters with total cholesterol
decline (146.1 ± 25.5 vs 135.1 ± 27.2 mg/dL, P = .002) at
the expense of LDL-cholesterol (70.2 ± 17.9 vs 64.9
TABLE 2 Corporal composition and hydration statementa
± 21.3 mg/dL, P = .03) and lower triglyceride levels
Basal 3-month P (125.8 ± 54.0 vs 108.2 ± 44.6 mg/dL, P = 0.006) with
2
BMI (kg/m ), mean ± SD 23.7 ± 4.4 24.1 ± 4.7 .01 nonsignificant increase of HDL-cholesterol. There were
2
LTI (kg/m ), mean ± SD 14.9 ± 3.7 16.2 ± 2,9 .038 no significant changes in total proteins levels, albumin
2 levels, phosphate levels or inflammatory parameters ana-
FTI (kg/m ), mean ± SD 8.0 ± 4.9 7.4 ± 4.8 .274
lyzed as CRP or ferritin.
TBW (L), mean ± SD 38.2 ± 8.6 39.4 ± 9.0 .05
Twenty-one patients were treated with statins with no
ICW (L), mean ± SD 20.7 ± 5.2 21.6 ± 5.2 .034 modifications during the study period. Statin therapy was
ECW (L), mean ± SD 17.5 ± 3.9 17.8 ± 4.1 .366 not started in the other 15 patients during the follow-up
OH (L), mean ± SD 1.6 ± 1.8 1.4 ± 1.3 .599 period.
a We observed a significant decrease on monthly
Variables are expressed as a mean ± SD (SD).
Abbreviations: BMI, body mass index; ECW, extracellular water; FTI, fast darbepoetin alfa dose and monthly iron (III) hydroxide-
tissue index; ICW, intracellular water; LTI, lean tissue index; OH, sucrose complex dose from 117.5 ± 84.2 to 99.2 ± 74.5 μg
overhydration; TBW, total body water. (P = .023) and from 155.6 ± 148.2 to 116.7 ± 110.8 mg

TABLE 3 Laboratory parametersa

Basal 3 months P
Total cholesterol (mg/dL), mean ± SD 146.1 ± 25.5 135.1 ± 27.2 .002
LDL (mg/dL), mean ± SD 70.2 ± 17.9 64.9 ± 21.3 .03
HDL (mg/dL), mean ± SD 46.9 ± 13.3 47.7 ± 13.9 .548
Triglycerides (mg/dL), mean ± SD 125.8 ± 54.0 108.2 ± 44.6 .006
Proteins (g/dL), mean ± SD 6.5 ± 0.6 6.7 ± 0.5 .137
Albumin (g/dL), mean ± SD 3.9 ± 0.5 4.0 ± 0.4 .535
Hemoglobin (g/dL), mean ± SD 11.7 ± 1.4 11.8 ± 1.1 .809
Ferritin (ng/mL), mean ± SD 262.1 ± 232.7 288,8 ± 278.2 .228
Transferrin saturation (%), mean ± SD 26.2 ± 8.5 35.0 ± 26.8 .072
CRP (mg/dL), mean ± SD 0.6 ± 0.9 0.5 ± 0.7 .766
Phosphorus (mg/dL), mean ± SD 4.5 ± 1.6 4.5 ± 1.5 .885
a
Variables are expressed as a mean ± SD (SD).
Abbreviations: CRP, C-reactive protein; HDL, high-density lipoprotein cholesterol, LDL, low-density lipoprotein cholesterol.
TORRES ET AL.
(P = .029), respectively. Even though anemia treatment
was decreased, serum hemoglobin and ferritin levels
were stable through the study (Table 3). We not found
differences between number of daily phosphate blinders
before and after the study.
Results did not change after adjustment for sex, age,
and levels of albumin and hemoglobin. Adverse events
related to exercise routine were not reported.
4 | DISCUSSION
Based on our results, the implementation of an individu-
alized exercise program in prevalent stable HD patients
can contribute to improve physical functioning, body
composition, and lipid profile with a decrease of EPO
and iron doses to maintain adequate anemia control.
Nowadays, with an increasing proportion of elderly
patients in HD units with higher sedentary behavior and
comorbidity, it is necessary to find strategies to improve
their mobility and quality of life.1–4,19 O´Hare et al
reported a strong association between sedentary behavior
and increased mortality in a large cohort of incident dialy-
sis patients.20 Johansen et al found that HD patients have
significant muscle atrophy and increased non-contractile
tissue compared with healthy controls, even when
corrected for habitual activity level. This atrophy can be
associated with poor physical functioning so any strategy
to improve this condition should be implemented.21
Cardiovascular mortality is the main cause of death
among CKD patients and exercise programs could reduce
that risk.3,21–23 However, when we evaluate the cardio-
vascular risk of HD patients with analytical and clinical
parameters, we should take into account the phenome-
non called “reverse epidemiology,” in which some classi-
cal risk factor patterns like high blood pressure
(BP) levels, increased body size, high plasma homocyste-
ine, or high cholesterol levels have a paradoxical associa-
tion with mortality. These data are based on big
epidemiological studies that show a close relation of mal-
nutrition and inflammation syndrome with lower BP,
body size, homocysteine, and total cholesterol found in
the patients with worse prognosis.23,24 In any case, these
same studies show a clear correlation between sedentary
behavior and mortality.2 Moreover, sedentary behavior
would be expected to be associated with malnutrition,
cardiovascular diseases, and therefore higher mortality.
Our results show a decrease of serum cholesterol
levels by decrease of serum LDL cholesterol levels and
significant decrease of serum triglyceride levels after
3 months of an individualized exercise program during
the dialysis sessions. These results should be correlated
with the presence or absence of malnutrition or
5
inflammation for its correct interpretation in this popula-
tion. There was no increase when we looked at inflam-
matory parameters such as CRP or ferritin and there
were no changes on proteins or albumin levels, which
remained normal. Therefore, we can interpret these
results as favorable, as we believe that all measures able
to meliorate cholesterol levels are positive.
In general population, active people and aerobic
training are associated with increased HDL-C and lower
triglycerides and LDL-C,25,26 but data about lipid profile
in HD patients undertaking exercise training are
heterogeneous.
It has been reported that exercise training in HD
patients improves lipid profile27–31 as we have observed
in our study. Some studies performed by Goldberg et al
have shown a decrease of triglyceride serum levels with
increase of HDL-C serum levels.29–31 However, these
results are inconsistent across studies and some of them
have not shown changes in lipid profile. Thus, more stud-
ies are necessary to verify these data.32–34
Another interesting finding in our study is an
increase of muscle mass, with increase of intracellular
water without increase of overhydration measured by
bioimpendance. Previous studies showed that patients
with lower lean tissue have a higher mortality risk in
stage 4 CKD.35 Given the fact that muscle wasting and
overhydration are also associated with loss of indepen-
dence, development of disability, and increase of cardio-
vascular risk and death, exercise programs could be very
beneficial in these regards.2–4
Koudi et al evaluated the effects of exercise training
performing muscle biopsies before and after exercise
training and they observed an impressive improvement
in muscular atrophy as well as increase in peak aerobic
power (VO2peak), exercise time, peak muscle strength of
the lower limbs, and in nerve conduction velocity.36 Our
results showing an increase of muscle mass by bio-
impedance are in accordance to this study as it is an indi-
rect measure of the increase in muscle strength.
Many studies carried out in HD patients have also
shown an improvement in physical functioning with pro-
grams combining aerobic and resistance exercise during
HD and in the interdialysis period.7,9–18 One of them con-
ducted by Storer et al showed an improvement of cardio-
pulmonary fitness, endurance, muscle strength,
fatigability, and physical function in 12 HD patients who
performed 9 weeks of leg-cycling during HD.13 Mercer
et al also observed that low-volume exercise rehabilita-
tion during 12 weeks can improve activity of daily living-
related functional capacity and self-reported functional
status of 22 HD patients.15
In our study the individualized exercise program was
monitored by staff of HD units in each HD session and
6 TORRES ET AL.
the weights lifted and hand grip resistances were progres-
sively increased according to the progression of patients.
After 3 months, we observed a marked improvement in
6MWT before and after exercise training and an increase
in numbers of sit-to-stand repetitions in 30 seconds. We
also observed an increase of the upper extremity strength
measured with dynamometry. It is especially important
to adapt any exercise program to the individual patient
capacity, in order to avoid adverse events. We did not
have any significant adverse event and at the same time
we realized that many patients were motivated to con-
tinue exercising daily out of the dialysis unit.
Another important finding in this study was the
decrease of monthly EPO and iron therapy. Since anemia
monitoring is a major part of HD patient care, these find-
ings could be relevant to improve anemia control and
reduce sanitary costs.
As several studies demonstrate that physical exercise
benefits in CKD patients, it would be advisable to include
supervised programs of exercise as a part of HD patient
care. Nevertheless, these programs have been underdevel-
oped in the HD units from many barriers such as high age
and comorbidity, lack of human and structural resources,
and low motivation of patients or medical staff.4,18,37
One limitation of this study is that the cohort of
patients was younger and less comorbid than the usual
population on HD. In addition, the design without a con-
trol group may limit extrapolation of the results; however,
the main findings such as the improvement in physical
functioning, body composition, and lipid and anemia pro-
file are large during the follow-up mostly. Our study
showed that marked improvement of physical functioning
could be achieved after only 3 months of follow-up with
simple exercises, adapted to the physical characteristics of
each patient and easy to monitor by HD unit staff.
5 | C ON C L U S I ON
The implementation of exercise training programs dur-
ing hemodialysis can improve physical functioning,
body composition, and nutritional parameters. Further-
more, it is possible to decrease iron and EPO therapy in
these patients maintaining good control of serum hemo-
globin levels. New strategies are necessary to bring exer-
cise programs to elderly patients with higher comorbid
conditions. This kind of programs could improve physi-
cal capacity in our patients and motivate them to con-
tinue performing active behaviors in their daily life,
outside of HD units. Given the encouraging results
obtained in this study and according to the evidence
found in literature, supervised exercise programs should
be included as a part of HD patient care.
CONFLICT OF INTEREST
The authors declare no potential conflict of interest.
ORCID
Esther Torres https://orcid.org/0000-0002-1524-3270
Ana García-Prieto https://orcid.org/0000-0003-3578-
8590
RE FER EN CES
1. Xie Y, Bowe B, Mokdad AH, et al. Analysis of the global bur-
den of disease study highlights the global, regional, and
national trends of chronic kidney disease epidemiology from
1990 to 2016. Kidney Int. 2018;94(3):567–581.
2. Kirsten LJ. Exercise in the end-stage renal disease population.
J Am Soc Nephrol. 2007;18:1845–1854.
3. Jung TD, Park SH. Intradialytic exercise programs for hemodi-
alysis patients. Chonnam Med J. 2011;47:61–65.
4. Tentori F, Elder SJ, Thumma J, et al. Physical exercise among
participants in the dialysis outcomes and practice patterns
study (DOPPS): Correlates and associated outcomes. Nephrol
Dial Transplant. 2010;25:3050–3062.
5. Fouque D, Kalantar-Zadeh K, Kopple J, et al. A proposed
nomenclature and diagnostic criteria for protein-energy
wasting in acute and chronic kidney disease. Kidney Int. 2008;
73(4):391–398.
6. Morishita Y, Nagata D. Strategies to improve physical activity
by exercise training in patients with chronic kidney disease. Int
J Nephrol Renov Dis. 2015;8:19–24.
7. Carrero JJ, Stenvinkel P, Cuppari L, et al. Etiology of the
protein-energy wasting syndrome in chronic kidney disease: A
consensus statement from the International Society of Renal
Nutrition and Metabolism (ISRNM). J Ren Nutr. 2013;23(2):
77–90.
8. Menon V et al. Cardiovascular risk factors in chronic kidney
disease. Kidney Int. 2005;68(4):1413–1418.
9. Heiwe S, Jacobson SH. Exercise training in adults with CKD: A
systematic review and metaanalysis. Am J Kidney Dis. 2014;64:
383–393.
10. Suh MR, Jung HH, Kim SB, Park JS, Yang WS. Effects of
regular exercise on anxiety, depression, and quality of life
in maintenance hemodialysis patients. Ren Fail. 2002;24:
337–345.
11. Kouidi E, Lacovides A, Lordanidis P, et al. Exercise renal reha-
bilitation program (ERRP): Psychosocial effects. Nephron.
1997;77:152–158.
12. Oh-Park M, Fast A, Gopal S, et al. Exercise for the dialyzed:
Aerobic and strength training during hemodialysis. Am J Phys
Med Rehabil. 2002;81:814–821.
13. Storer TW, Casaburi R, Sawelson S, Kopple JD. Endurance
exercise training during hemodialysis improves strength,
power, fatigability and physical performance in maintenance
haemodialysis patients. Nephrol Dial Transplant. 2005;20:
1429–1437.
14. Painter P, Carlson L, Carey S, Paul SM, Myll J. Low-
functioning hemodialysis patients improve with exercise train-
ing. Am J Kidney Dis. 2000;36:600–608.
15. Mercer TH, Crawford C, Gleeson NP, Naish PF. Low-volume
exercise rehabilitation improves functional capacity and self-
TORRES ET AL.
reported functional status of dialysis patients. Am J Phys Med
Rehabil. 2002;81:162–167.
16. Van Vilsteren MC, de Greef MH, Huisman RM. The effects of a
low-to-moderate intensity pre-conditioning exercise program
linked with exercise counselling for sedentary hemodialysis
patients in The Netherlands: Results of a randomized clinical
trial. Nephrol Dial Transplant. 2005;20:141–146.
17. Chen JL, Godfrey S, Ng TT, et al. Effect of intradialytic, low-
intensity strength training on functional capacity in adult
hemodialysis patients: A randomized pilot trial. Nephrol Dial
Transplant. 2010;25:1936–1943.
18. Esteve Simó V, Junqué A, Fulquet M, et al. Complete low-
intensity endurance training programme in haemodialysis
patients: Improving the care of renal patients. Nephron Clin
Pract. 2014;128(3–4):387–393.
19. Kutsuna T, Matsunaga A, Matsumoto T, et al. Physical activity
is necessary to prevent deterioration of the walking ability of
patients undergoing maintenance hemodialysis. Ther Apher
Dial. 2010;14:193–200.
20. O'Hare AM, Tawney K, Bacchetti P, et al. Decreased survival
among sedentary patients undergoing dialysis: Results from the
dialysis morbidity and mortality StudyWave 2. Am J Kidney
Dis. 2003;41:447–454.
21. Johansen KL, Shubert T, Doyle J, Soher B, Sakkas GK, Kent-
Braun JA. Muscle atrophy in patients receiving hemodialysis:
Effects on muscle strength, muscle quality, and physical func-
tion. Kidney Int. 2003;63(1):291–297.
22. Foley RN, Parfrey PS, Sarnak MJ. Epidemiology of cardiovascu-
lar disease in chronic renal disease. J Am Soc Nephrol. 1998;9
(12 Suppl):S16–S23.
23. Liu Y, Coresh J, Eustace JA, et al. Association between choles-
terol level and mortality in dialysis patients role of inflamma-
tion and malnutrition. JAMA. 2004;291(4):451–459.
24. Baigent C, Wheeler DC. Should we reduce blood cholesterol
to prevent cardiovascular disease among patients with
chronic renal failure? Nephrol Dial Transplant. 2000;15:
1118–1119.
25. Yoshida H, Ishikawa T, Suto M, et al. Effects of supervised aer-
obic exercise training on serum adiponectin and parameters of
lipid and glucose metabolism in subjects with moderate dys-
lipidemia. J Atheroscler Thromb. 2010;17(11):1160–1166.
26. Yao M, Lichtenstein AH, Roberts SB, et al. Relative influence
of diet and physical activity on cardiovascular risk factors in
urban Chinese adults. Int J Obes. 2003;27(8):920–932.
27. Song WJ, Sohng KY. Effects of progressive resistance training
on body composition, physical fitness and quality of life of
7
patients on hemodialysis. J Korean Acad Nurs. 2012;42:
947–956.
28. Groussard C, Rouchon-Isnard M, Coutard C, et al. Beneficial
effects of an intradialytic cycling training program in patients
with end-stage kidney disease. Appl Physiol Nutr Metab. 2015;
40:550–556.
29. Goldberg AP, Hagberg JM, Delmez JA, Haynes ME,
Harter HR. Metabolic effects of exercise training in hemodialy-
sis patients. Kidney Int. 1980;18(6):754–761.
30. Goldberg AP, Hagberg JM, Delmez JA, et al. The metabolic
and psychological effects of exercise training in hemodialysis
patients. Am J Clin Nutr. 1980;33(7):1620–1628.
31. Goldberg AP, Geltman EM, Hagberg JM, et al. Therapeutic
benefits of exercise training for hemodialysis patients. Kidney
Int. 1983;24(16):S-303–S-309.
32. Liao MT, Liu WC, Lin FH, et al. Intradialytic aerobic cycling
exercise alleviates inflammation and improves endothelial pro-
genitor cell count and bone density in hemodialysis patients.
Medicine. 2016;95:e4134.
33. Wilund KR, Tomayko EJ, Wu PT, et al. Intradialytic exercise
training reduces oxidative stress and epicardial fat: A pilot
study. Nephrol Dial Transplant. 2010;25:2695–2701.
34. Afshar R, Shegarfy L, Shavandi N, Sanavi S. Effects of aerobic
exercise and resistance training on lipid profiles and inflamma-
tion status in patients on maintenance hemodialysis. Indian J
Nephrol. 2010;20:185–189.
35. Vega A, Abad S, Macías N, et al. Low lean tissue mass is an
independent risk factor for mortality in patients with stages
4 and 5 non-dialysis chronic kidney disease. Clin Kidney J.
2017;10:170–175.
36. Kouidi E, Albani M, Natsis K, et al. The effects of exercise
training on muscle atrophy in hemodialysis patients. Nephrol
Dial Transplant. 1998;13:685–699.
37. Delgado C, Johansen KL. Deficient counseling on physical
activity among nephrologists. Nephron Clin Pract. 2010;116:
c330–c336.
How to cite this article: Torres E, Aragoncillo I,
Moreno J, et al. Exercise training during
hemodialysis sessions: Physical and biochemical
benefits. Ther Apher Dial. 2020;1–7. https://doi.
org/10.1111/1744-9987.13469