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Review

Nutrition and Physical Activity in CKD

patients
Adamasco Cupisti Claudia D’Alessandro Giordano Fumagalli Valentina Vigo

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Mario Meola Caterina Cianchi Maria F. Egidi

Department of Clinical and Experimental Medicine, University of Pisa; Nephrology, Transplantation and
Dialysis Unit, AOUP, Pisa, Italy

Key Words
Chronic Kidney Disease • ESRD • Nutrition • Diet • Dialysis • Exercise • Physical activity

Abstract
Chronic kidney disease (CKD) patients are at risk for protein–energy wasting, abnormal body
composition and impaired physical capacity. These complications lead to increased risk of
hospitalization, morbidity and mortality.
In CKD patient as well as in healthy people, there is a close association between nutrition and
physical activity. Namely, inadequate nutrient (energy) intake impairs physical performance
thus favoring a sedentary lifestyle: this further contributes to loss of muscle strength and
mass, which limit the quality of life and rehabilitation of CKD patients. In CKD as well as in
end-stage-renal-disease patients, regular physical activity coupled with adequate energy and
protein intake counteracts protein–energy wasting and related comorbidity and mortality. In
summary, exercise training can positively influence nutritional status and the perception of
well-being of CKD patients and may facilitate the anabolic effects of nutritional interventions.

Copyright © 2014 S. Karger AG, Basel

Introduction

Although the modern treatment of chronic kidney disease (CKD) is addressed to

reduce progression of renal and cardiovascular damage, to prevent uremic complications
and to improve survival, new challenges must be considered. In order to prevent disability,
to improve quality of life and to maintain physical performance, it is important a proper
nutritional approach and a regular physical activity.
Throughout the course of CKD, diet and exercise are widely recommended not only
for improving the efficacy of drug and dialysis treatment, but also for offering specific
benefits on physical performance, quality of life and health status perception. Nutrition and

Adamasco Cupisti, MD, PhD Department of Clinical and Experimental Medicine, University of Pisa
Via Roma 67, 5651226 Pisa (Italy), Tel. 0039.50.997291
E-Mail adamasco.cupisti@med.unipi.it
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Cupisti et al.: Nutrition and Exercise in CKD

physical activity can also influence each other and closely interact both in healthy and in
CKD population.

Nutrition

In the clinical care of renal patients, nutritional therapy is very important. Since the early
stages of CKD, “ normalization” of dietary intake of energy, protein, sodium and phosphorus
play a crucial role for the renal protection. In more advances stages of CKD, protein-restricted
diets are able to prevent or ameliorate uremic symptoms or complications, such as metabolic
acidosis, mineral and bone disorders, insulin resistance, proteinuria, hypertension and fluid
retention, and to maintain nutritional status [1-3]. Evidence exists that protein-restricted
diets can delay the need of dialysis [4] , whereas the effect of slowing the rate of GFR decline

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is not so evident [5].
The severity of protein restriction depends on the level of the residual renal function
[6]. Consequently, in the pre-dialysis stages a very low-protein very low-phosphorus diet
supplemented with essential amino acids and keto-acids is the preferable option to improve
metabolic and nutritional parameters [7].
However, nutritional therapy is not only a matter of dietary protein intake, but it includes
also phosphorus and sodium restriction, and adequate energy intake. This is a crucial point
since maintenance of a good nutritional status is a pre-requisite and a target of nutritional
therapy that allows patients a good quality of life and physical performance. To this aim,
energy supply must equal, or even overcome, the energy requirement.
Shifting from conservative to dialysis therapy, increase of protein intake is needed [8].
However, an high protein intake conflicts with the limitation of phosphorus, potassium and
salt needed to avoiding the severe complications of hyperkalemia, hyperphosphatemia and
excessive interdialytic weight gain [9]. The other side of the nutritional concerns in end-stage-
renal-disease (ESRD) patients, is protein energy wasting (PEW) [10]. This quite prevalent
condition, especially in elderly dialysis patients, is strictly related to hospitalization,
morbidity and mortality [10, 11]
Even in renal transplanted patients, a correct nutritional approach represents a very
important aspects of the clinical care management [12].
Similarly to nutritional education and prescription, physical activity implementation
represents a continuum in the natural history of CKD patients (Fig. 1).

Exercise

It is well known that regular physical exercise is mandatory for the prevention and
treatment of obesity, diabetes and insulin resistance which are increasing factors of new
onset and of progression of CKD. Body weight lowering strategies should include, as first
step, a combination of mild energy reduction and an increase of energy expenditure by
aerobic exercise. Unfortunately, this strategy is not always successful [13].
During the course of CKD, physical activity and capacity are largely reduced. Physical
inactivity is a long-standing clinical problem among CKD patients especially those undergoing
dialysis treatment [14].
The 2011 Cochrane review [15] assessed the effect of regular exercise training in
adults with CKD and in kidney transplant recipients on several outcomes, including dietary
nutrient intake and parameters of nutritional status. It emerged that physical fitness and
physical functioning (defined as the ability and capacity to perform activities of daily living)
is severely reduced in adults with CKD and progressively declines from the early stages of
CKD to ESRD [15]. Regular exercise training can improve arterial blood pressure control and
heart rate, physical fitness walking capacity and several nutritional parameters and quality
of life. Positive effects had been found also in elderly CKD patients [16, 17, 18].
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Fig. 1. The “continuum” of exercise implementation and nutritional approach in the CKD patients.

Impaired muscle strength and a decline in physical function is often associated to PEW
which depends on the several abnormalities associated to renal failure. The pathogenesis
of the so-called “uraemic sarcopenia “ is multifactorial including physical inactivity that
represents a modifiable and a quite prevalent risk factor. Actually, most of the changes in
muscle structure and function seem to be related to deconditioning [19,20].
Data from the literature suggest that CKD patients should be stimulated to increase
their physical activity, including coordination and flexibility exercises associated with
aerobic and resistance training [21]. Exercise programs may be implemented in the dialysis
and/or in the non-dialysis day, depending on the patient’s need and willingness as well as on
the structural and functional resources [22].
Kouidie et al. evaluated the effects of long-term physical training (4 years) on HD
patients' fitness, perception of health and overall life situation [23]. They found that HD
patients are able to adhere to long-term physical training programs both on dialysis- and
non-dialysis days, with significant increase in exercise capacity especially after the first
year. The perception of health was higher in the majority of the patients [23]. The ability
of exercise training to alleviate depression and to increase the perception of feeling better
improved appetite and contributed to counteract the reduction of energy and protein intake
frequently found in HD patients [24].
Sakkas et al. [25] investigated the effect of 6 months of aerobic exercise training on
muscle morphology in HD patients and found beneficial effects on muscles with an increment
of cross sectional area, reduction of myofiber atrophy and changes in capillarization. They
observed that skeletal muscles of uraemic patients responded to exercise stimulus in the
same way as the normal population [25].
A correct nutritional approach and regular physical activity also represent very important
aspects of the clinical care management in renal transplanted patients [26]. Poor functional
capacity predicts a poor outcome for older patients undergoing renal transplantation [27].
Weight gain after kidney transplantation is a significant risk factor for diminished
long-term outcomes which affects up to 90% of kidney transplant recipients; changes in
dietary intake and lack of physical activity are strong factors causing weight gain following
kidney transplantation [26]. Gain in adiposity after renal transplantation is related to high
consumption of mono- and disaccharides, energy-rich drinks, and low daily physical activity
[28].
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Cupisti et al.: Nutrition and Exercise in CKD

Despite a number of benefits, the effect of increased physical activity on long-term

survival of HD patients are still lacking [23].

Exercise training and low protein diet in CKD

Proper nutrition and regular physical activity are relevant aspect at any stage of a renal
patient’s history (Fig.1). Although evidence exits about the positive clinical effects of low-
protein regimens in CKD, the fear that a protein restriction could cause protein malnutrition
and muscle wasting still remains. This could happen only if the energy intake is not adequate,
or the essential aminoacids intake is not sufficient or when metabolic acidosis is not
corrected. Basically, reduction of protein intake reduces protein synthesis but also reduces
protein catabolism, so nitrogen balance is maintained in equilibrium. However, when protein
and energy intakes are inadequately low, net protein catabolism occurs.
The effect of resistance training during low-protein regimens counteract the tendency

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to impaired muscle cell metabolism. Castaneda et al. [29] studied 26 CKD patients following
a low-protein (0.6 g/Kg b.w) diet. They found an increase in type I and II fiber cross-sectional
areas, an improvement of leucine oxidation, serum albumin levels and muscle strength and
a reduction of inflammation in patients who performed resistance training, when compared
to patients not undergoing resistance training. They concluded that resistance training
seems to be effective and protective even in CKD patients on a low-protein diet, by improving
protein utilization, muscle mass and function, and body composition [29, 30].
Although different from normal controls, no difference in muscle metabolism and
function was observed in patients on a very low protein diet (0.3 g/Kg/d) supplemented
with essential aminoacids and ketoacids when compared to patients on standard low-
protein (0.6 g/kg/d) diet [31].
It is crucial to underline that exercise activity is a matter of energy supply rather than
protein intake. In order to satisfy the increased energy requirement, it is mandatory that the
recommendation of increasing exercise and physical activities are also accompanied by the
recommendation to increase energy intake. In the CKD patients on low protein regimens, the
energy needs can be obtained by increasing the intake of protein-free foods which provide
carbohydrates and are almost free of protein, phosphorus, potassium or sodium [32]. These
protein-free products represent a real “green power fuel” for CKD patients.

Exercise training and Nutrition in ESRD

Concerning the influence of progressive resistance training on markers of nutritional
status, positive effects have been reported in the PEAK (Progressive Exercise for Anabolism
in Kidney Disease) study. HD patients undergoing 12 weeks of high intensity progressive
resistance training administered during dialysis treatment have reported an increase in
insulin sensitivity, a reduction of intramuscular lipids, a statistically significant increase
in total strength, body weight and BMI, mid-thigh and mid-arm circumference [33]. Frey
et al. did not find any differences in pre-albumin levels while pre-dialysis and post dialysis
albumin levels tend to slightly increase over time in ESRD patients who took part to an
aerobic exercise program performed during dialysis treatment [24].
Regular exercise training (regardless of type, intensity, length of intervention, or
supervision) was associated with a significant increase in energy intake. Instead, no
significantly increase of protein intake was reported in patients performing cardiovascular
and/or resistance exercise training [14]. Our experience confirm these findings: in a in a
cohort of hemodialysis patients, the level and intensity of spontaneous physical activity was
positively related to the daily energy intake energy [34].
Evidences exist that exercise is an effective anabolic strategy in particular when it is
performed close to the administration of nutritional supports both in healthy and CKD
subjects. Exercise increases insulin sensitivity and responsiveness [35]: insulin-stimulated
glucose and amino acids transport increased following muscle contraction even at a
constant receptors and nutrient concentrations [36]. It is known that supplementation of
carbohydrate in the early post-exercise stimulate a more rapid glycogen storage. A similar
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Cupisti et al.: Nutrition and Exercise in CKD

mechanism has been proposed for protein supplementation (probably insulin-mediated)

resulting in muscle hypertrophy and increase in muscle strength. Hence, a close relationship
exists among exercise, nutritional status and nutrients intakes, with particular attention to
the timing of the nutrients administration [37-39].
Both in healthy and CKD subjects, short-term studies showed that the combination of
exercise training and oral supplementation increases muscle protein content more than
exercise or nutritional supplementation alone. There is also evidence that intra-dialysis
exercise, combined with oral or parenteral nutrition, enhances amino acid uptake and
protein content in the muscle tissue of HD patients. Pupim et al [40] studied two groups of
HD patients: one only with intra dialytic parenteral nutrition (IDPN) and the other with IDPN
plus exercise. Patients were studied before, during, and 2 h after an HD session by use of a
infusion of L-[1-13C]leucine and L-[ring-2H5] phenylalanine. During HD, exercise combined
with IDPN promoted two-fold increment in forearm muscle essential amino acid uptake

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and muscle protein when compared with IDPN alone. Whole body protein homeostasis and
energy expenditure were not altered by exercise treatment [40].
These results are in accordance with those of Majchrzak et al [41] who found enhanced
anabolic effects of oral intradialytic nutritional supplementation on skeletal muscle protein
turnover after a single bout of resistance training. Similar findings have been reported by
Dong J et al. [42] who tested the effect of a long-term resistance training combined with
intradialytic oral supplementation in HD patients. The Authors found a statistically significant
increase in body weight that can be considered as a positive result. In fact evidence exists
that increasing body weight in HD patients improves their survival [42]. In a small cohort of
HD patients, 16 weeks of strength training was performed together with the administration
of protein or a no protein drink after every training session. After the training, improvements
in muscle strength and power, physical performance, and quality of life occurred. However,
no additional benefit was observed by combining the training and protein supplementation.
[43].
A randomized clinical trial is in progress for analyzing the impact of intra-dialysis
progressive exercise training and adequate nutritional supplementation on markers of PEW,
functional capacities and quality of life of adult patients in hemodialysis [44].

Conclusion

In summary, regular physical activity can positively affect the nutritional status and the
perception of well-being of CKD patients and may facilitate the anabolic effects of nutritional
interventions. Exercise training, coupled with adequate nutritional support is a therapeutic
intervention able to prevent the loss of lean body mass in CKD patients. In addition,
improving of quality of life is generally recorded. These strategies need to be implemented
and represent a promising field of investigations in all the stages of CKD.

Disclosure Statement

The authors of this work declare that they do not have any conflict of interests.

References

1 Mitch WE, Remuzzi G: Diets for patients with chronic kidney disease, still worth prescribing. J Am Soc
Nephrol 2004;15:234-237.
2 Fouque D, Aparicio M: Eleven reasons to control the protein intake of patients with chronic kidney disease.
Nature Clin Pract 2007;3:383-392.
 Kidney Blood Press Res 2014;39:107-113
DOI: 10.1159/000355784 © 2014 S. Karger AG, Basel
Published online: July 29, 2014 www.karger.com/kbr 112
Cupisti et al.: Nutrition and Exercise in CKD

3 Cupisti A, D’Alessandro C, Morelli E, Rizza GM, Galetta F, Franzoni F, Barsotti G: Nutritional status and
dietary manipulation in predialysis chronic renal failure patients. J Ren Nutr 2004;14:127-133.
4 Fouque D, Wamg P, Laville M, Boissel JP: Low protein diets delay end-stage renal disease in non diabetic
adults with chronic renal failure. Nephrol Dial Transplant 2000;15:1986-1992.
5 Kasiske BL, Lakatua JD, Ma JZ, Louis TA: A meta-analysis of the effects of dietary protein restriction on the
rate of decline in renal function Am J Kidney Dis 1998;31:954-961.
6 Aparicio M, Cano NJ, Cupisti A, Ecder T, Fouque D, Garneata L, Liou HH, Lin S, Schober-Halstenberg HJ,
Teplan V, Zakar G: Keto-acid therapy in predialysis chronic kidney disease patients: consensus statements. J
Ren Nutr 2009;19:S33-S35.
7 Aparicio M, Bellizzi V, Chauveau P, Cupisti A, Ecder T, Fouque D, Garneata L, Lin S, Mitch W, Teplan V, Yu
X, Zakar G: Do Ketoanalogues Still Have a Role in Delaying Dialysis Initiation in CKD Predialysis Patients?
Semin Dial 2013;26:714-719.
8 Fouque D, Vennegoor M, Ter Wee P, Wanner C, Basci A, Canaud B, Haage P, Konner K, Kooman J, Martin-
Malo A, Pedrini L, Pizzarelli F, Tattersall J, Tordoir J, Vanholder R: EBPG Guideline on Nutrition. Nephrol

Downloaded from http://karger.com/kbr/article-pdf/39/2-3/107/3048591/000355784.pdf by guest on 15 January 2024

Dial Transplant 2007;22:ii45–ii87.
9 Laville M, Fouque D: Nutritional aspects in hemodialysis. Kidney Int Suppl 2000;76:S133-139.
10 Fouque D, Kalantar-Zadeh K, Kopple J, Cano N, Chauveau P, Cuppari L, Franch H, Guarnieri G, Ikizler TA,
Kaysen G, Lindholm B, Massy Z, Mitch W, Pineda E, Stenvinkel P, Treviño-Becerra A, Wanner C: A proposed
nomenclature and diagnostic criteria for protein- energy wasting in acute and chronic kidney disease.
Kidney Int 2008;73:391-398.
11 Ikizler TA, Cano NJ, Franch H, Fouque D, Himmelfarb J, Kalantar-Zadeh K, Kuhlmann MK, Stenvinkel P,
TerWee P, Teta D, Wang AY, Wanner C: Prevention and treatment of protein energy wasting in chronic
kidney disease patients: a consensus statement by the International Society of Renal Nutrition and
Metabolism. Kidney Int 2013;84:1096-1107.
12 Chan M, Patwardhan A, Ryan C, Trevillian P, Chadban S, Westgarth F, Fry K; Caring for Australasians with
Renal Impairment; Dietitians Association of Australia: Evidence-based guidelines for the nutritional
management of adult kidney transplant recipients. J Ren Nutr 2011;21:47-51.
13 Baria F, Kamimura MA, Aoike DT, Ammirati A, Rocha ML, de Mello MT, Cuppari L: Randomized controlled
trial to evaluate the impact of aerobic exercise on visceral fat in overweight chronic kidney disease
patients. Nephrol Dial Transplant 2014;29:857-864.
14 Clyne N, Jogestrand T, Lins L, Pehrsson S, Ekelund L: Factors limiting physical working capacity in
predialytic uraemic patients. Acta Med Scand 1987;222:183-190.
15 Heiwe S, Jacobson SH: Exercise training for adults with chronic kidney disease. Cochrane Database Syst Rev
2011;10:CD003236.
16 Fitts SS, Guthrie MR, Blagg CR: Exercise coaching and rehabilitation counseling improve quality of life for
predialysis and dialysis patients. Nephron 1999;82:115-121.
17 Painter P, Carlson L, Carey S, Paul SM, Myll J: Physical functioning and health-related quality-of-life changes
with exercise training in hemodialysis patients. Am J Kidney Dis 2000;35:482-492.
18 Heiwe S, Tollbäck A, Clyne N: Twelve weeks of exercise training increases muscle function and walking
capacity in elderly pre-dialysis patients and healthy subjects. Nephron 2001;88:48-56.
19 Fahal IH: Uraemic sarcopenia: aetiology and implications. Nephrol Dial Transplant 2013, DOI 10.1093/
ndt/gft070.
20 Workeneh BT, Mitch WE: Review of muscle wasting associated with chronic kidney disease. Am J Clin Nutr
2010;91:1128S-1132S.
21 Johansen KL, Chertow GM, Ng AV, Mulligan K, Carey S, Schoenfeld PY, Kent-Braun JA: Physical activity levels
in patients on hemodialysis and healthy sedentary controls. Kidney Int 2000;57:2564-2570.
22 Kouidi E, Grekas D, Deligiannis A, Tourkantonis A: Outcomes of long-term exercise training in dialysis
patients: comparison of two training programs. Clin Nephr 2004;61:s31-s38.
23 Cupisti A, D'Alessandro C, Bottai A, Fumagalli G, Capitanini A: Physical activity and exercise training: a
relevant aspect of the dialysis patient's care. Intern Emerg Med 2013;8:31-34.
24 Frey S, Mir AR, Lucas M: Visceral protein status and caloric intake in exercising versus non-exercising
individuals with end-stage renal disease. J Ren Nutr 1999;9:71-77.
25 Sakkas GK, Sargeant AJ, Mercer TH, Ball D, Koufaki P, Karatzaferi C, Naish PF: Changes in muscle
morphology in dialysis patients after 6 months of aerobic exercise training. Nephrol Dial Transplant
2003;18:1854-1861.
 Kidney Blood Press Res 2014;39:107-113
DOI: 10.1159/000355784 © 2014 S. Karger AG, Basel
Published online: July 29, 2014 www.karger.com/kbr 113
Cupisti et al.: Nutrition and Exercise in CKD

26 Cupples CK, Cashion AK, Cowan PA, Tutor RS, Wicks MN, Williams R, Eason JD: Characterizing dietary
intake and physical activity affecting weight gain in kidney transplant recipients. Prog Transplant
2012;22:62-70.
27 Yango AF, Gohh RY, Monaco AP, Reinert SE, Gautam A, Dworkin LD, Morrissey PE: Excess risk of renal
allograft loss and early mortality among elderly recipients is associated with poor exercise capacity. Clin
Nephrol 2006;65:401-407.
28 Zelle DM, Kok T, Dontje ML, Danchell EI, Navis G, van Son WJ, Bakker SJ, Corpeleijn E: The role of
diet and physical activity in post-transplant weight gain after renal Transplantation. Clin Transplant
2013:27:E484-E490.
29 Castaneda C, Gordon PL, Uhlin KL, Levey AS, Kehayias JJ, Dwyer JT, Fielding RA, Roubenoff R, Singh MF:
Resistance training to counteract the catabolism of a low protein diet in chronic renal insufficiency: A
randomized, controlled trial. Ann Intern Med 2001;135:965-976.
30 Castaneda C, Gordon PL, Parker RC, Uhlin KL, Roubenoff R, Levey AS: Resistance training to reduce the

Downloaded from http://karger.com/kbr/article-pdf/39/2-3/107/3048591/000355784.pdf by guest on 15 January 2024

malnutrition-inflammation complex syndrome of chronic kidney disease. Am J Kidney Dis 2004;43:607-
616.
31 Cupisti A, Licitra R, Chisari C, Stampacchia G, D’Alessandro C, Galetta F, Rossi B, Barsotti G: Skeletal muscle
and nutritional status in chronic renal failure on a protein restricted diet. J Int Med 2004;255:115-124.
32 D’Alessandro C, Rossi A, Innocenti M, Ricchiuti G, Bozzoli L, Sbragia G, Meola M, Cupisti A: Dietary Protein
Restriction for Renal Patients: Don't Forget Protein-Free Foods. J Ren Nutr 2013;23:367-371.
33 Cheema B, Abas H, Smith B, O‘Sullivan A, Chan M, Patwardhan A, Kelly J, Gillin A, Pang G, Lloyd B, Singh MF:
Progressive exercise for anabolism in kidney disease (PEAK): a randomized, controlled trial of resistance
training during hemodialysis. J Am Soc Nephrol 2007;18:1594-1601.
34 Cupisti A, Capitanini A, Betti G, D'Alessandro C, Barsotti G: Assessment of habitual physical activity
and energy expenditure in dialysis patients and relationships to nutritional parameters. Clin Nephrol
2011;75:218-225.
35 Wasserman DH, Geer RJ, Rice DE, Bracy D, Flakoll PJ, Brown LL, Hill JO, Abumrad NN: Interaction of
exercise and insulin action in humans. Am J Physiol Endocrinol Metab 1991;260:E37-E45.
36 Zorzano A, Balon TW, Garetto LP, Goodman MN, Ruderman NB: Muscle α-aminoisobutyric acid transport
after exercise: enhance stimulation by insulin. Am J Physiol Endocrinol Metab 1985;248:E546-E552.
37 Andersen LL, Tufekovic G, Zebis MK, Crameri RM, Verlaan G, Kjaer M, Suetta C, Magnusson P, Aagaard P:
The effect of resistance training combined with timed ingestion of protein on muscle fiber size and muscle
strength. Metabolism 2005;54:151-156.
38 Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M: Timing of post-exercise protein intake is
important for muscle hypertrophy with resistance training in elderly humans. J Physiol 2001;535:301-311.
39 Levenhagen DK, Gresham JD, Carlson MG, Maron DJ, Borel MJ, Flakoll PJ: Post-exercise nutrient intake
timing in humans is critical to recovery of leg glucose and protein homeostasis. Am J Physiol Endocrinol
Metab 2001;280:E982-E993.
40 Pupim LB, Flakoll PJ, Levenhagen DK, Ikizler TA: Exercise augments the acute anabolic effects of
intradialytic parenteral nutrition in chronic hemodialysis patients. Am J Physiol Endocrinol Metab
2004;286:E589-E597.
41 Majchrzak KM, Pupim LB, Flakoll PJ, Ikizler TA: Resistance exercise augments the acute anabolic effects of
intradialytic oral nutritional supplementation. Nephrol Dial Transplant 2008;23:1362-1369.
42 Dong J, Sundell MB, Pupim LB, Wu P, Shintani A, Ikizler TA: The effect of resistance exercise to augment
long-term benefits of intradialytic oral nutritional supplementation in chronic hemodialysis patients. J Ren
Nutr 2011;21:149-159.
43 Molsted S, Harrison AP, Eidemak I, Andersen JL: The Effects of High-Load Strength Training With Protein-
or Nonprotein-Containing Nutritional Supplementation in Patients Undergoing Dialysis. J Ren Nutr
2013;23:132-140.
44 Magnard J, Deschamps T, Cornu C, Paris A, Hristea D: Effects of a six-month intradialytic physical ACTIvity
program and adequate NUTritional support on protein-energy wasting, physical functioning and quality
of life in chronic hemodialysis patients: ACTINUT study protocol for a randomized controlled trial. BMC
Nephrology 2013;14:259.