Next Article in Journal
Low Serum Magnesium is Associated with Incident Dementia in the ARIC-NCS Cohort
Next Article in Special Issue
Estimation of Sodium and Potassium Intake: Current Limitations and Future Perspectives
Previous Article in Journal
What Was First, Obesity or Inflammatory Bowel Disease? What Does the Gut Microbiota Have to Do with It?
Previous Article in Special Issue
24-h Urine Collection: A Relevant Tool in CKD Nutrition Evaluation
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

The Effect of Exercise on Nutritional Status and Body Composition in Hemodialysis: A Systematic Review

by
Dimitra Rafailia Bakaloudi
1,
Antonios Siargkas
1,
Kalliopi Anna Poulia
2,
Evangelia Dounousi
3 and
Michail Chourdakis
1,*
1
Laboratory of Hygiene, Social & Preventive Medicine and Medical Statistics, School of Medicine, Faculty of Health Sciences, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece
2
Department of Nutrition and Dietetics, Laiko General Hospital, 11527 Athens, Greece
3
Department of Nephrology, Faculty of Medicine, School of Health Sciences, University of Ioannina, 45110 Ioannina, Greece
*
Author to whom correspondence should be addressed.
Nutrients 2020, 12(10), 3071; https://doi.org/10.3390/nu12103071
Submission received: 5 August 2020 / Revised: 27 September 2020 / Accepted: 2 October 2020 / Published: 8 October 2020
(This article belongs to the Special Issue Nutrition Management for CKD (Chronic Kidney Disease))

Abstract

:
Chronic kidney disease (CKD) is associated with aggravating factors which can affect both body composition and nutritional status. The purpose of the present systematic review was to investigate the potential effects of any physical activity on body composition or nutritional status among patients with stage 5 CKD undergoing hemodialysis (HD). A literature search on PubMed, Scopus, Web of Science, Google Scholar, and Cochrane was conducted and 14 randomized clinical trials were included. Skeletal muscle index and mid-arm muscular circumference increased after resistance exercise, and the results on body mass index, % body fat, and lean body mass varied. Serum albumin and C-reactive protein, in most cases, showed a slight increase and decrease, respectively. An improvement was also observed in body strength and overall performance status. The results suggest that physical activity can be beneficial for both the body composition and nutritional status of patients undergoing HD and can help in the prevention of sarcopenia. However, further research is needed mainly in the field of nutritional status.

1. Introduction

Chronic kidney disease (CKD) is a major health problem with an estimated global prevalence of 11–13% [1]. Chronic kidney disease progression is divided into five stages and patients in the last stage are characterized by a progressive kidney failure and the need of renal replacement therapy (RRT), i.e., hemodialysis (HD), peritoneal dialysis (PD) or transplantation [2]. In CKD, physiological alterations of metabolism and physiology of the body are present such as deterioration of renal function, uremia as well as electrolyte and mineral derangements [3]. Patients with end-stage renal disease (ESRD) have increased risk of cardiovascular diseases (CVDs) and subsequently higher mortality risk compared to healthy adults [4]. Moreover, in stage 5 CKD there is a higher prevalence of malnutrition, chronic inflammation and oxidative stress, anemia, vitamin D deficiency, insulin resistance, functional capacity deterioration, lean body mass (LBM) wasting, and cachexia [5,6,7,8]. Nutritional status seems to worsen in long dialysis periods, and this is associated with the high rate of muscle mass and fat wasting [9] as well as a decrease in health-related quality of life (HrQoL) [10,11]. Decreased nutrient intake, due to the fact of anorexia or even dietetic restrictions, is also a common problem of stage 5 CKD [12]. The aforementioned alterations seem to have a negative impact on nutritional status and negatively affect body composition in patients undergoing HD [8,13,14].
Muscle functionality in patients with stage 5 CKD has been found to be compromised in previous studies [15,16,17]. This can be associated with lower performance status, physical activity intolerance, and muscle weakness [17], factors that can contribute to a higher percentages of patients with CKD leading a sedentary lifestyle [17,18]. Sarcopenia, the loss of skeletal muscle mass and its functionality, is highly prevalent in patients with CKD and is strongly associated with higher morbidity and mortality [19]. Patients with sarcopenia progressively lose muscle mass and strength, whereas the degree of sarcopenia is associated with the stage of CKD, especially in men [20]. In older adults, where sarcopenia is even more frequent due to the impact of aging, lower physical activity, and more prevalent ESRD, sarcopenia is even more profound and most of the time is refractory [21]. According to recently published studies, sarcopenic obesity, i.e., the co-existence of sarcopenia and obesity, not only diminishes any potential benefit from obesity (described as “obesity paradox”) but leads to substantially worse outcomes [22,23,24,25].
Enhancing physical activity has shown a beneficial impact on improving body composition in healthy subjects [26]. However, in patients with CKD, the symptoms of anemia, vascular dysfunction (arterial stiffness), muscle abnormalities, chronic metabolic acidosis, and inflammation can induce protein degradation which is associated with exercise intolerance and sedentary behavior among this population [27,28,29]. Moreover, there is a growing interest of the effect of physical activity and the overall health in patients with CKD, as it is considered to be one of the best ways to preserve muscle mass in this population [30]. According to the current guidelines for patients with CKD, including patients undergoing HD, physical activity is not contraindicated; on the contrary, it is considered to act beneficially [31]. However, HD patients have to counteract the “obligatory” sedentary time during HD sessions, resulting in even lower physical activity levels, lower physical performance, and a lower HrQoL [32].
In previous systematic reviews, the beneficial effects of exercise on the physical health of patients undergoing HD [33,34,35,36,37,38] as well as on the QoL were illuminated [39,40,41,42,43,44,45]. In two studies by Lu et al. [46] and Molsted et al. [47], the positive effects of exercise on muscle mass and muscle strength in patients undergoing HD were also stressed out. Nevertheless, according to our knowledge, there are no published studies in which the total body composition and nutritional status of patients undergoing HD in relation to exercise have been examined.

2. Materials and Methods

The current study is a systematic review of randomized clinical trials (RCTs). The PubMed, Scopus, Web of Science, Google Scholar, and Cochrane database searches were performed (up to 21 July 2020) according to the following main search string: ((physical activity) OR (exercise)) AND (hemodialysis OR (renal failure) OR (kidney failure)). Our systematic review was conducted according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement [48] (detailed information can be found in Table S1) and the Protocol was electronically submitted in the Prospero Library (CRD42020181769).
Initially, the output of our results (15.982 studies) was input into a reference database (EndNote X7 for Windows, Thomson Reuters) and duplicates were removed. Then, all titles and abstracts were examined for relevance by two researchers (DB and AS), and a third reviewer KAP was consulted when any doubts emerged. Overall, this resulted in the exclusion of 15.964 studies for not complying with the inclusion/exclusion criteria. The population of interest were patients undergoing HD with a duration of treatment of more than 3 months, >18 years old, and engaged in any type of physical activity. The control for the eligible RCTs were patients undergoing HD for more than 3 months, >18 years old but without performing significant physical activity at the baseline of intervention. Incomplete studies, studies with different control groups, studies not in the English language, or published before 2000 were excluded. As a result, 18 RCT studies [49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66] were characterized as acceptable; details regarding the eligibility process can be found in the flow diagram presented in Figure 1.
The main outcomes were the differences in nutritional status between the intervention and control groups using the examined serum albumin (sALB) and C-Reactive protein (CRP) and the effect of exercise on body composition using as the main evaluation variables: body mass index (BMI), mid-arm muscular circumference (MAMC) measurements, % of body fat (%BF), lean body mass (LBM), and skeletal muscle index (SMI) assessment. Muscle and fat mass (FM) evaluation methods included anthropometry (i.e., skinfold thickness and circumference measurements), computed topographies, dual-energy x-ray absorptiometry (DEXA), multiple-frequency bioelectrical impendence analysis (BIA) by various methods (i.e., body composition monitor, BCM; Fresenius Medical Care, Bad Homburg, Germany Maltron Inc., BioScan 920-2S Multifrequency Analyzer). The evaluation of total muscle strength, functionality, and the effects on performance status were reported as secondary outcomes. Assessment tools for hand grip strength (HGS) were a variety of dynamometers (Chatillon CSD 200 Dynamometer; Ametek Inc, Paoli, PA; CV, 9.4%, Lafayette Instrument, Lafayette, IN, T.K.K. 5401 GRIP D, Takei Science Instruments, Niigata, Japan, Cybex Inc., Ronkonkoma, NY, Takei TKK 5001 Tokyo, Japan, Jamar Hydraulic Hand Dynamometer) and the Wells Bench test. Exercise performance evaluations were conducted mainly by walking tests. The most common test was the 6 min walk test (6MWT) [67] or other similar tests.
The quality evaluation of the eligible studies was conducted using the Cochrane Collaboration tool to assess risk of bias [68].

3. Results

The main characteristics of the included studies are presented in Table 1. In total, 945 patients undergoing HD were included in our study. The duration of physical activity intervention varied from 8 weeks to 2 years in eligible studies, and the frequency ranged from 2 to 4 times per week.
The assessment of risk of bias was conducted for all the 18 studies. In 11 studies, high or low unclear risk of bias was detected due to the absence of blinding of participants and/or outcome assessment [49,50,51,52,53,55,57,60,62,64,65]. Five studies were considered as low or unclear risk of bias because of selective reporting [49,55,57,62,65], and in only three studies high, or unclear risk of bias was detected due to the incomplete outcome of the data [55,63,66]. A summary of the assessment of risk of bias can be found in Figure 2 and Figure 3. A p-value <0.05 was considered of statistical significance. Statistical assessment of included studies included paired t-test, Wilcoxon or Mann–Whitney U test as appropriate and/or analysis of covariance (ANCOVA). These p-values show the level of significance of seen changes after the exercise parameters.

3.1. Body Mass Index (BMI)

Results regarding BMI changes among patients undergoing HD after the exercise intervention are presented in Table 2. These interventions (resistance training and/or pedaling) lasted for 12–18 weeks and BMI was calculated at baseline and at the end of the intervention. Body mass index was found to be increased in the intervention group in comparison to the non-active group (0.3 versus −0.1, 0.28 versus 0.2, 0.25 versus 0.03, 0.1 versus −0.3 accordingly) [50,53,55,62]. Similarly, Abreu et al. reported a significantly greater reduction of BMI in the control group versus the intervention group (−0.3 versus −0.1) [49]. In a study by Kopple et al. [57], a reduction in BMI was detected in all exercising groups irrespective of the type of training, (i.e., −0.3 m/kg2 in the endurance training group, −1.0 m/kg2 in the strength training group, and −0.2 m/kg2 in the combined group), whereas in the control group, BMI increased by 0.1 m/kg2 at the end of the intervention [57]. The same outcomes were reported by Marinho et al. [60], where resistance exercise led to a slight reduction (−0.1 m/kg2) of the BMI in the intervention group, while in the non-active group the reduction was found to be higher by 0.2 kg/m2 at the end of the intervention. Finally, in a study by Liao et al. [58], pedaling on a cycle ergometer during HD did not have any significant effects on BMI, while non-active patients reported a higher BMI (0.24 kg/m2) at the end of the study. On the contrary, pedaling in the Wilund et al. [66] study led to slight increase in BMI in the active patients in comparison to the non-active group in which a slight decrease was observed [66].

3.2. Mid-Arm, Waist, and Midthigh Circumferences

Increased MAMC was found in the physical active groups with patients following a program of resistance exercise for 30–50 min, 2–3 times/week in comparison to the non-active groups [49,50,61,64]. Moreover, in the studies by Abreu et al. [49] and Song et al. [64], waist circumference (WC) was found to be lower in the active subjects, whereas in non-active patients, WC increased [49,64]. In a study by Cheema et al. [50] an increase in midthigh circumference was reported among active patients, while the control group was found to have a slight decrease (+0.7 versus −0.3 cm, respectively) [50]. The results regarding circumferences are presented in Table 3.

3.3. Body Fat

The effect of exercise on the percentage of body fat (%BF) seemed to vary among the studies included in this systematic review, an effect that can be partially attributed to the type of exercise performed [51,55,56,57,59,60,61,62,64]. The results regarding %BF can be found in Table 4. In the studies by Johansen et al. [56] and Olvera-Soto et al. [61] there was a significantly higher increase in %BF in the exercise group versus the control group [56,61]. According to Rosa et al. [62] after 12 weeks of follow-up, %BF was reduced, but in non-active subjects the reduction was greater (mean difference −1.23% in the non-active versus −0.71% in the active group) [62]. Marinho et al. [60] reported a higher reduction in %BF in the intervention group compared to the controls (mean difference −0.9% versus −0.6%, respectively) [60]. The three types of exercise (endurance cycling, strength, and combined exercise) in the study by Kopple et al. [57] resulted in different outcomes for %BF [57]. Endurance cycling decreased %BF by ~0.5%, resistant exercise led to a slight increase in body fat by ~0.2%, and combined exercise decreased %BF by ~1.2% [57]. Similarly, in the Chen et al. [51] and Song et al. [64] studies, resistance exercise led to decrease in %BF in the active group in comparison to the control group in which an increase in %BF was observed [51,64]. Furthermore, in the study by Loppes et al. [59], the exercise intervention did not significantly affect %BF in the group following a high-intensity program, while in the group of moderate intensity, the reduction was slightly higher than the control group [59]. In the Groussard et al. [55] study, the low intensity of the resistance exercise did not have a statistical significant effect on %BF [55].
According to the study by Johansen et al. [56], lean body mass (LBM) decreased after 12 weeks of follow-up in both the intervention and control groups, but the decrease was greater in the intervention group [56]. In the study by Kopple et al. [57], the endurance cycling resulted in a slight reduction in LBM by ~−0.7 kg, while resistance training and combined exercise resulted in an increase in LBM by ~0.4 kg and ~0.5 kg, respectively [57]. Surprisingly, in the non-active group, LBM was higher by ~0.7 kg [57]. Similar outcomes recorded by Marinho et al. [60], where resistance exercise led to increased LBM compared to the initial measurement, but the increase was smaller in the intervention group compared to the controls (~1% versus 3%) [60]. On the contrary, in the studies by Chen et al. [51], Lopes et al. [59], and Rosa et al. [62], LBM increased after the intervention, while in the non-physically active subjects, LBM decreased or showed a slighter increase [51,59,62]. Similarly, in the Song et al. [64] study, an increase in the skeletal body mass was observed in the intervention group compared to the non-active group in which the skeletal body mass decreased [64]. Changes in LBM are presented in Table 5.

3.4. Skeletal Muscle Index

Two studies included in this systematic review examined changes in SMI, and both of them concluded that there was a significant improvement in SMI in the intervention group [59,65]. Resistance training with high-load led to a greater increase in SMI compared to the moderate-load group [59]. Moreover, in the aerobic exercise groups, the increase in SMI was greater than in the combined aerobic-resistance exercise group (0.15 versus 0.04, p < 0.05) [65]. The relevant results are presented in Table 6.
In the studies by Abreu et al. [49] and Wilund et al. [66], resistance and aerobic exercise did not significantly affect sALB, while CRP decreased compared to the non-active group [49,66]. Moreover, a slight increase in sALB and a reduction in CRP were observed by both Cheema et al. [50] and Kopple et al. [57], where resistance exercise [50] and cycling were the interventions, respectively [57]. Cycling in Liao et al. [58] increased sALB and decreased CRP after a 12 week intervention [58]. Resistance exercise resulted in a slight reduction in sALB, while combined exercise (i.e., cycling and resistance exercise) did not result in any significant effects on sALB [57]. In both groups (i.e., cycling and combined exercise), CRP increased [57]. Endurance-resistance training had an impact neither on sALB nor on CRP [54], while resistance-stretching exercise led to a greater decrease in CRP compared to the controls after a 2 year follow-up [52]. Increased CRP was also found in an intervention with resistance-exercise by Marinho et al. [60], and according to the data from Suhardjono et al. [65] there was a greater reduction in CRP only in subjects following combined aerobic-resistance exercise compared to the non-active patients undergoing HD [65]. The SALB and CRP changes are presented in Table 7.

3.5. Strength and Functionality Evaluation

In the majority of the studies included in our systematic review, strength increased after the intervention [50,51,54,56,59,61,62,64,65]. Resistance exercise significantly increased the total strength of active subjects, while in the control group there was a slight reduction of strength after the intervention period [50,51,56,64]. Endurance training also led to a notable increase in strength, measured by HGS measurement. More specifically, there was a mean increase of 12.4 N in the intervention group versus 0.7 N in the control group [54]. Non-significant differences in handgrip strength were recorded by Cooke et al. [53] and Suhardjono et al. [65] after pedaling [53,65] and in the moderate-intensity resistance exercise group by Lopes et al. [59]. These changes are presented in Table 8.

3.6. Performance Status

Regarding to the performance status, several studies illuminated a significant improvement in physically active subjects [50,52,53,54,55,62] as can be seen in Table 9. Assessment tools used for the evaluation of performance status were walking tests with modifications in distance and time. In the majority of the studies, the 6MWT method was used. Significant ameliorations were observed mainly after resistance exercise [50,52,54,62], while in the aerobic intervention group, an improvement was noted but at a lower grade [53,65]. However, in the study by Johansen et al. [56], resistance exercise led to a smaller improvement in gait speed compared to the non-active group, (2.7 cm/s versus 6 cm/s, respectively) [56].

4. Discussion

The aim of our systematic review was to investigate the effects of exercise on the nutritional status and body composition among patients undergoing HD. According to our systematic review, physical activity in patients undergoing HD resulted in beneficial outcomes, i.e., improved muscle strength and muscle mass, better performance status, increased Alb, and decreased CrP. Regarding the effects of physical activity on BMI, the findings were inconclusive. A decrease in BMI is not always desirable for patients undergoing HD, as in most cases it is difficult to identify if this reduction is associated with a decrease in LBM or in FM. According to studies including measurements of MAMC, there was a significant increase of this parameter in the physically active groups following resistance exercise. This improvement advocates an increase in muscle mass. Therefore, the reduction in BMI that was found was mostly accompanied by an increase in MAMC which means a preservation of muscle mass, with a relevant reduction in FM. These results are in concordance with studies including measurements of muscle mass by BIA and the calculation of SMI in which muscle mass as well as SMI increased after resistance exercise and were found to have a tendency to increase in the aerobic training group [46,69].
The results regarding body composition changes were inconclusive. Aerobic exercise and especially cycling seemed to reduce %BF [57]. On the other hand, results from our review could not significantly correlate physical activity with changes in LBM between intervention and control groups. The fact that the %BF results were unclear could explain similar uncertainty in LBM changes since the latter is defined as the difference between total body weight and body fat weight. Moreover, LBM estimation is influenced by fluids’ balance in the body, which in HD patients is heavily modified as a result of the fluid management between the HD sessions and the intradialytic fluid management.
One of the most commonly used laboratory markers for the evaluation of nutritional status is sALB [70,71]. However, sALB, as a nutritional parameter is characterized by a low specificity due to the fact of its long half-time, lasting approximately 20 days [72]. Therefore, nutritional status cannot be assessed solely by sALB [73]. Inflammation is also a significant factor influencing nutritional status and at the same time affecting the levels of sALB [73,74]. A variety of factors increase inflammation status in patients undergoing HD, i.e., alterations in gut microbiota, vascular disorders, and immunosuppression [74,75,76]. Therefore, the evaluation of both sALB and CRP can be used for the first approach of the overall nutritional and inflammatory status of patients undergoing HD [74]. Regarding the effect of physical activity on sALB and CRP, in the majority of studies, resistance exercise decreased CRP and slightly increased sALB, whereas aerobic exercise resulted in a reduction in sALB and an increase in CRP. A possible explanation of the irregularity of the results is the limited intervention time which could possibly mask the positive effects on sALB due to its long half time.. Nevertheless, in the study by Cheng et al. [52], with an intervention of resistance exercise lasting for 2 years, there was a slight increase in sALB and a decline in CRP. In the Cheema et al. [50] study, the protein catabolic rate showed a slight increase in the active group compared to passive group in which a slight decrease was observed (0.02 ± 0.31 g/kg/d versus −0.04 ± 0.17 g/kg/d). In the same study, a mini-nutritional assessment (MNA) was used in order to assess the risk of malnutrition and showed that the score was better in the passive group after the intervention [50]. On the contrary, in the Frih et al. [54] study in which the MNA was also performed, it was observed that the nutritional status was ameliorated after the intervention of resistance exercise [54]. Specifically, at baseline in the passive and intervention group, the risk of malnutrition was 85.7% and 70% accordingly, and in the final assessment the risk of malnutrition in the intervention group was 23.8% compared to an 85% risk for the passive group [54]. Further research is needed in this field in order to reach to safe conclusions due to the fact that nutritional and inflammation status can be affected both negatively and positively by lifestyle and nutritional parameters, i.e., smoking and overall food quality [10]. According to the existing studies, only in one study was pre-albumin, which can better reflect nutritional status, recorded [77]. A significant increase in pre-albumin was observed after resistance training compared to non-active patients [77]. Chan et al. [78] and Zhang et al. [79] found preliminary evidence that resistance training can reduce malnutrition and no significant improvement in nutrient intake, respectively.
According to our results, physical activity, especially resistance exercise, has a beneficial effect on body strength as measured by HGS dynamometry. Both upper and lower body mass strength were found to be increased at the end of the intervention in the active group versus the non-active one. On the other hand, cycling did not result in any statistically significant change in muscle strength. All types of exercise resulted in improvements in performance status, but resistance exercise seems to be the superior. However, we cannot ignore the fact that aerobic exercise is associated with improved cardiorespiratory function, lipid profile improvement, and an overall improvement in mental health and QoL [42]. Therefore, combined exercise could be the ideal choice for HD patients, providing a combination of positive results in many aspects of the patients’ lives. According to the recently revised criteria for the diagnosis of sarcopenia, muscle strength is the first alarming sign of sarcopenia, followed by the reduction of muscle mass [80]. Skeletal muscle mitochondrial dysfunction as well as reduction of muscle mitochondria are more prevalent in patients with CKD and could provide an explanation of the higher prevalence of sarcopenia in this population [81,82]. Mitochondria dysfunction plays an important role in inflammation and oxidative stress and, therefore, contributes to the pathogenesis of atherosclerosis and CVD [83,84]. According to Balakrishnan et al. [85], resistance exercise seems to act protectively by increasing the biogenesis and restoration muscle mitochondria in patients with CKD [85]. Therefore, the improvement in functional tests and the performance status after the analysis of the included RCTs in our study, especially of studies with interventions of resistance exercise protocols, could be a guide towards interventions that could prevent sarcopenia in this population [80].
Moreover, two recently published studies in which performance status [86] and strength [87] were examined concluded that the heterogeneity and the indistinct bias of the existing studies cannot lead to general conclusions [86,87].
The significant strengths of our systematic review are the careful selection of included studies, where all of them were randomized and had a similar control group. Moreover, most of the physical activity interventions were intradialytic, i.e., during the HD session and, therefore, physical activity was supervised during the entire time, had a specific duration and frequency (2–3 times per week), and was not omitted or skipped. Some limitations in the present study are that the assessment tools for body composition were different, and this could produce a bias of the results. The remarkable variability observed in the protocols and duration of training programs may partly explain the inconclusive evidence for some of the parameters. Moreover, serum prealbumin, which could be a more sensitive nutritional marker, was not assessed and, therefore, it could not be evaluated. Moreover, as nutritional intake was recorded in none of the RCTs, no conclusions can be derived about the possible effect of nutritional parameters in combination with exercise in patients undergoing HD.

5. Conclusions

Physical activity, in particular resistance exercise, seems to influence the body composition of patients undergoing HD. Increased MAMC and SMI were observed, whereas the results regarding %BF, LBM, and BMI were not clear. Resistance exercise may also control inflammation in patients undergoing HD, something that can have beneficial effects on lowering nutritional risks and/or malnutrition, but further research is needed in this field. Finally, performance status and strength (i.e., muscle functionality) can be improved in physically active patients undergoing HD, an effect with an undeniably positive impact on the QoL of all these patients. However, it needs to be noted that the existing evidence is insufficient to prove significant beneficial effects of exercise training on body composition and markers of nutritional/inflammation status mainly due to the high heterogeneity of protocols (in duration and type of exercise programs) of the existing clinical studies.

Supplementary Materials

The following are available online at https://www.mdpi.com/2072-6643/12/10/3071/s1, Table S1: Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) Checklist.

Author Contributions

D.R.B. and A.S. searched the databases; D.R.B. and A.S. wrote the paper; K.A.P., E.D., and M.C. made the necessary recommendations; and K.A.P. and M.C. revised the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

BCMBody composition monitor
BFBody fat
BMIBody mass index
CKDChronic kidney disease
CRPC-reactive protein
CVDCardiovascular diseases
DEXADual-energy x-ray absorptiometry
ESRDEnd-stage renal disease
FMFat mass
HDHemodialysis
HrQoLHealth related quality of life
HGSHand grip strength
LBMLean body mass
MAMCMid arm muscular circumference
MNAMini-Nutritional Assessment
PDPeritoneal dialysis
RCTRandomized clinical trial
RRTRenal replacement therapy
sALBSerum Albumin
SDStandard deviation
SMISkeletal muscle mass
QoLQuality of life
WCWaist circumference
6MWT6 min walk test

References

  1. Hill, N.R.; Fatoba, S.T.; Oke, J.L.; Hirst, J.A.; O’Callaghan, C.A.; Lasserson, D.S.; Hobbs, F.D. Global Prevalence of Chronic Kidney Disease—A Systematic Review and Meta-Analysis. PLoS ONE 2016, 11, e0158765. [Google Scholar] [CrossRef]
  2. Levey, A.S.; Coresh, J.; Balk, E.; Kausz, A.T.; Levin, A.; Steffes, M.W.; Hogg, R.J.; Perrone, R.D.; Lau, J.; Eknoyan, G. National Kidney Foundation practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Ann. Intern. Med. 2003, 139, 137–147. [Google Scholar] [CrossRef]
  3. Vaziri, N.D. Dyslipidemia of chronic renal failure: The nature, mechanisms, and potential consequences. Am. J. Physiol. Physiol. 2006, 290, F262–F272. [Google Scholar] [CrossRef]
  4. Tonelli, M.; Wiebe, N.; Culleton, B.; House, A.; Rabbat, C.; Fok, M.; McAlister, F.; Garg, A.X. Chronic kidney disease and mortality risk: A systematic review. J. Am. Soc. Nephrol. 2006, 17, 2034–2047. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Levin, A.; Li, Y.C. Vitamin D and its analogues: Do they protect against cardiovascular disease in patients with kidney disease? Kidney Int. 2005, 68, 1973–1981. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Siew, E.D.; Ikizler, T.A. Insulin resistance and protein energy metabolism in patients with advanced chronic kidney disease. Sem. Dial. 2010, 23, 378–382. [Google Scholar] [CrossRef] [PubMed]
  7. Slee, A.D. Exploring metabolic dysfunction in chronic kidney disease. Nutr. Metab. 2012, 9, 36. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  8. Iorember, F.M. Malnutrition in Chronic Kidney Disease. Front. Pediatr. 2018, 6, 161. [Google Scholar] [CrossRef] [PubMed]
  9. Lim, H.-S.; Kim, H.-S.; Kim, J.K.; Park, M.; Choi, S.J. Nutritional Status and Dietary Management According to Hemodialysis Duration. Clin. Nutr. Res. 2019, 8, 28–35. [Google Scholar] [CrossRef] [Green Version]
  10. Laws, R.A.; Tapsell, L.C.; Kelly, J. Nutritional status and its relationship to quality of life in a sample of chronic hemodialysis patients. J. Ren. Nutr. 2000, 10, 139–147. [Google Scholar] [CrossRef]
  11. Cohen, S.D.; Kimmel, P.L. Nutritional status, psychological issues and survival in hemodialysis patients. Contrib. Nephrol. 2007, 155, 1–17. [Google Scholar] [CrossRef] [PubMed]
  12. Ikizler, T.A. Optimal nutrition in hemodialysis patients. Adv. Chronic Kidney Dis. 2013, 20, 181–189. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Omari, A.M.; Omari, L.S.; Dagash, H.H.; Sweileh, W.M.; Natour, N.; Zyoud, S.H. Assessment of nutritional status in the maintenance of haemodialysis patients: A cross-sectional study from Palestine. BMC Nephrol. 2019, 20, 92. [Google Scholar] [CrossRef] [PubMed]
  14. Keane, D.; Gardiner, C.; Lindley, E.; Lines, S.; Woodrow, G.; Wright, M. Changes in Body Composition in the Two Years after Initiation of Haemodialysis: A Retrospective Cohort Study. Nutrients 2016, 8. [Google Scholar] [CrossRef] [Green Version]
  15. Painter, P. Physical functioning in end-stage renal disease patients: Update. Hemodial. Int. 2005, 9, 218–235. [Google Scholar] [CrossRef]
  16. Painter, P.; Roshanravan, B. The association of physical activity and physical function with clinical outcomes in adults with chronic kidney disease. Curr. Opin. Nephrol. Hypertens. 2013, 22, 615–623. [Google Scholar] [CrossRef]
  17. Roshanravan, B.; Robinson-Cohen, C.; Patel, K.V.; Ayers, E.; Littman, A.J.; de Boer, I.H.; Ikizler, T.A.; Himmelfarb, J.; Katzel, L.I.; Kestenbaum, B.; et al. Association between physical performance and all-cause mortality in CKD. J. Am. Soc. Nephrol. 2013, 24, 822–830. [Google Scholar] [CrossRef] [Green Version]
  18. Johansen, K.L.; Chertow, G.M.; Ng, A.V.; Mulligan, K.; Carey, S.; Schoenfeld, P.Y.; Kent-Braun, J.A. Physical activity levels in patients on hemodialysis and healthy sedentary controls. Kidney Int. 2000, 57, 2564–2570. [Google Scholar] [CrossRef] [Green Version]
  19. Hirai, K.; Ookawara, S.; Morishita, Y. Sarcopenia and Physical Inactivity in Patients with Chronic Kidney Disease. Nephrourol. Mon. 2016, 8, e37443. [Google Scholar] [CrossRef] [Green Version]
  20. Moon, S.J.; Kim, T.H.; Yoon, S.Y.; Chung, J.H.; Hwang, H.J. Relationship between Stage of Chronic Kidney Disease and Sarcopenia in Korean Aged 40 Years and Older Using the Korea National Health and Nutrition Examination Surveys (KNHANES IV-2, 3, and V-1, 2), 2008–2011. PLoS ONE 2015, 10, e0130740. [Google Scholar] [CrossRef] [Green Version]
  21. Domanski, M.; Ciechanowski, K. Sarcopenia: A major challenge in elderly patients with end-stage renal disease. J. Aging Res. 2012, 2012, 754739. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Tabibi, H.; As’habi, A.; Najafi, I.; Hedayati, M. Prevalence of dynapenic obesity and sarcopenic obesity and their associations with cardiovascular disease risk factors in peritoneal dialysis patients. Kidney Res. Clin. Pract. 2018, 37, 404–413. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Malhotra, R.; Deger, S.M.; Salat, H.; Bian, A.; Stewart, T.G.; Booker, C.; Vincz, A.; Pouliot, B.; Ikizler, T.A. Sarcopenic Obesity Definitions by Body Composition and Mortality in the Hemodialysis Patients. J. Ren. Nutr. 2017, 27, 84–90. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Androga, L.; Sharma, D.; Amodu, A.; Abramowitz, M.K. Sarcopenia, obesity, and mortality in USA adults with and without chronic kidney disease. Kidney Int. Rep. 2017, 2, 201–211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Kim, J.K.; Kim, S.G.; Oh, J.E.; Lee, Y.K.; Noh, J.W.; Kim, H.J.; Song, Y.R. Impact of sarcopenia on long-term mortality and cardiovascular events in patients undergoing hemodialysis. Korean J. Intern. Med. 2019, 34, 599–607. [Google Scholar] [CrossRef] [PubMed]
  26. Mohammadi, H.R.; Khoshnam, M.S.; Khoshnam, E. Effects of Different Modes of Exercise Training on Body Composition and Risk Factors for Cardiovascular Disease in Middle-aged Men. Int. J. Prev. Med. 2018, 9, 9. [Google Scholar] [CrossRef] [PubMed]
  27. Van Craenenbroeck, A.H.; Van Craenenbroeck, E.M.; Van Ackeren, K.; Hoymans, V.Y.; Verpooten, G.A.; Vrints, C.J.; Couttenye, M.M. Impaired vascular function contributes to exercise intolerance in chronic kidney disease. Nephrol. Dial. Transplant. 2016, 31, 2064–2072. [Google Scholar] [CrossRef]
  28. Kosmadakis, G.C.; Bevington, A.; Smith, A.C.; Clapp, E.L.; Viana, J.L.; Bishop, N.C.; Feehally, J. Physical exercise in patients with severe kidney disease. Nephron. Clin. Pract. 2010, 115, c7–c16. [Google Scholar] [CrossRef]
  29. Nishikawa, M.; Ishimori, N.; Takada, S.; Saito, A.; Kadoguchi, T.; Furihata, T.; Fukushima, A.; Matsushima, S.; Yokota, T.; Kinugawa, S.; et al. AST-120 ameliorates lowered exercise capacity and mitochondrial biogenesis in the skeletal muscle from mice with chronic kidney disease via reducing oxidative stress. Nephrol. Dial. Transplant. 2015, 30, 934–942. [Google Scholar] [CrossRef] [Green Version]
  30. K/DOQI clinical practice guidelines for cardiovascular disease in dialysis patients. Am. J. Kidney Dis. Off. J. Natl. Kidney Found. 2005, 45, S1–S153.
  31. Milam, R.H. Exercise Guidelines for Chronic Kidney Disease Patients. J. Ren. Nutr. 2016, 26, e23–e25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Matsuzawa, R.; Roshanravan, B. Management of Physical Frailty in Patients Requiring Hemodialysis Therapy. Contrib. Nephrol. 2018, 196, 101–109. [Google Scholar] [CrossRef] [PubMed]
  33. Cheema, B.S.; Singh, M.A. Exercise training in patients receiving maintenance hemodialysis: A systematic review of clinical trials. Am. J. Nephrol. 2005, 25, 352–364. [Google Scholar] [CrossRef] [PubMed]
  34. Fuzari, H.K.B.; Leite, J.; Souza, H.; Rocha, T.; de Andrade, A.D.; Marinho, P. Exercise effectiveness of arteriovenous fistula maturation in chronic renal patients: A systematic review with meta-analysis. Int. J. Ther. Rehabil. 2017, 24, 98–104. [Google Scholar] [CrossRef]
  35. Qiu, Z.; Zheng, K.; Zhang, H.; Feng, J.; Wang, L.; Zhou, H. Physical Exercise and Patients with Chronic Renal Failure: A Meta-Analysis. BioMed Res. Int. 2017, 2017, 7191826. [Google Scholar] [CrossRef]
  36. Scapini, K.B.; Bohlke, M.; Moraes, O.A.; Rodrigues, C.G.; Inacio, J.F.S.; Sbruzzi, G.; Leguisamo, C.P.; Sanches, I.C.; Tourinho, H.; Irigoyen, M.C. Combined training is the most effective training modality to improve aerobic capacity and blood pressure control in people requiring haemodialysis for end-stage renal disease: Systematic review and network meta-analysis. J. Physiother. 2019, 65, 4–15. [Google Scholar] [CrossRef]
  37. Wyngaert, K.V.; Van Craenenbroeck, A.H.; Van Biesen, W.; Dhondt, A.; Tanghe, A.; Van Ginckel, A.; Celie, B.; Calders, P. The effects of aerobic exercise on eGFR, blood pressure and VO (2) peak in patients with chronic kidney disease stages 3-4: A systematic review and meta-analysis. PLoS ONE 2018, 13, e0203662. [Google Scholar] [CrossRef]
  38. Yang, H.; Wu, X.; Wang, M. Exercise Affects Cardiopulmonary Function in Patients with Chronic Kidney Disease: A Meta-Analysis. BioMed Res. Int. 2017, 2017, 6405797. [Google Scholar] [CrossRef] [Green Version]
  39. De Medeiros, A.I.C.; Fuzari, H.K.B.; Rattesa, C.; Brandao, D.C.; de Melo Marinho, P.E. Inspiratory muscle training improves respiratory muscle strength, functional capacity and quality of life in patients with chronic kidney disease: A systematic review. J. Physiother. 2017, 63, 76–83. [Google Scholar] [CrossRef]
  40. Koufaki, P.; Greenwood, S.A.; Macdougall, I.C.; Mercer, T.H. Exercise therapy in individuals with chronic kidney disease: A systematic review and synthesis of the research evidence. Annu. Rev. Nurs. Res. 2013, 31, 235–275. [Google Scholar] [CrossRef]
  41. Neto, M.G.; de Lacerda, F.F.R.; Lopes, A.A.; Martinez, B.P.; Saquetto, M.B. Intradialytic exercise training modalities on physical functioning and health-related quality of life in patients undergoing maintenance hemodialysis: Systematic review and meta-analysis. Clin. Rehabil. 2018, 32, 1189–1202. [Google Scholar] [CrossRef]
  42. Pei, G.Q.; Tang, Y.; Tan, L.; Tan, J.X.; Ge, L.; Qin, W. Aerobic exercise in adults with chronic kidney disease (CKD): A meta-analysis. Int. Urol. Nephrol. 2019, 51, 1787–1795. [Google Scholar] [CrossRef] [PubMed]
  43. Pu, J.; Jiang, Z.; Wu, W.; Li, L.; Zhang, L.; Li, Y.; Liu, Q.; Ou, S. Efficacy and safety of intradialytic exercise in haemodialysis patients: A systematic review and meta-analysis. BMJ Open 2019, 9, e020633. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Sheng, K.; Zhang, P.; Chen, L.; Cheng, J.; Wu, C.; Chen, J. Intradialytic exercise in hemodialysis patients: A systematic review and meta-analysis. Am. J. Nephrol. 2014, 40, 478–490. [Google Scholar] [CrossRef] [PubMed]
  45. Young, H.M.L.; March, D.S.; Graham-Brown, M.P.M.; Jones, A.W.; Curtis, F.; Grantham, C.S.; Churchward, D.R.; Highton, P.; Smith, A.C.; Singh, S.J.; et al. Effects of intradialytic cycling exercise on exercise capacity, quality of life, physical function and cardiovascular measures in adult haemodialysis patients: A systematic review and meta-analysis. Nephrol. Dial. Transplant. 2018, 33, 1436–1445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Lu, Y.; Wang, Y.J.; Lu, Q. Effects of Exercise on Muscle Fitness in Dialysis Patients: A Sys tematic Review and Meta-Analysis. Am. J. Nephrol. 2019, 50, 291–302. [Google Scholar] [CrossRef] [PubMed]
  47. Molsted, S.; Bjorkman, A.S.D.; Lundstrom, L.H. Effects of strength training to patients undergoing dialysis: A systematic review. Dan. Med. J. 2019, 66, 9. [Google Scholar]
  48. Liberati, A.; Altman, D.G.; Tetzlaff, J.; Mulrow, C.; Gotzsche, P.C.; Ioannidis, J.P.; Clarke, M.; Devereaux, P.J.; Kleijnen, J.; Moher, D. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: Explanation and elaboration. PLoS Med. 2009, 6, e1000100. [Google Scholar] [CrossRef]
  49. Abreu, C.C.; Cardozo, L.; Stockler-Pinto, M.B.; Esgalhado, M.; Barboza, J.E.; Frauches, R.; Mafra, D. Does resistance exercise performed during dialysis modulate Nrf2 and NF-kappa B in patients with chronic kidney disease? Life Sci. 2017, 188, 192–197. [Google Scholar] [CrossRef]
  50. Cheema, B.; Abas, H.; Smith, B.; O’Sullivan, A.; Chan, M.; Patwardhan, A.; Kelly, J.; Gillin, A.; Pang, G.; Lloyd, B.; et al. 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. [Google Scholar] [CrossRef] [Green Version]
  51. Chen, J.L.; Godfrey, S.; Ng, T.T.; Moorthi, R.; Liangos, O.; Ruthazer, R.; Jaber, B.L.; Levey, A.S.; Castaneda-Sceppa, C. Effect of intra-dialytic, low-intensity strength training on functional capacity in adult haemodialysis patients: A randomized pilot trial. Nephrol. Dial. Transplant. 2010, 25, 1936–1943. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Cheng, Y.J.; Zhao, X.J.; Zeng, W.; Xu, M.C.; Ma, Y.C.; Wang, M. Effect of Intradialytic Exercise on Physical Performance and Cardiovascular Risk Factors in Patients Receiving Maintenance Hemodialysis: A Pilot and Feasibility Study. Blood Purif. 2019. [Google Scholar] [CrossRef]
  53. Cooke, A.B.; Ta, V.; Iqbal, S.; Gomez, Y.H.; Mavrakanas, T.; Barre, P.; Vasilevsky, M.; Rahme, E.; Daskalopoulou, S.S. The Impact of Intradialytic Pedaling Exercise on Arterial Stiffness: A Pilot Randomized Controlled Trial in a Hemodialysis Population. Am. J. Hypertens. 2018, 31, 458–466. [Google Scholar] [CrossRef] [PubMed]
  54. Frih, B.; Jaafar, H.; Mkacher, W.; Ben Salah, Z.; Hammami, M.; Frih, A. The Effect of Interdialytic Combined Resistance and Aerobic Exercise Training on Health Related Outcomes in Chronic Hemodialysis Patients: The Tunisian Randomized Controlled Study. Front. Physiol. 2017, 8, 288. [Google Scholar] [CrossRef] [PubMed]
  55. Groussard, C.; Rouchon-Isnard, M.; Coutard, C.; Romain, F.; Malarde, L.; Lemoine-Morel, S.; Martin, B.; Pereira, B.; Boisseau, N. Beneficial effects of an intradialytic cycling training program in patients with end-stage kidney disease. Appl. Physiol. Nutr. Metab. 2015, 40, 550–556. [Google Scholar] [CrossRef]
  56. Johansen, K.L.; Painter, P.L.; Sakkas, G.K.; Gordon, P.; Doyle, J.; Shubert, T. Effects of resistance exercise training and nandrolone decanoate on body composition and muscle function among patients who receive hemodialysis: A randomized, controlled trial. J. Am. Soc. Nephrol. JASN 2006, 17, 2307–2314. [Google Scholar] [CrossRef]
  57. Kopple, J.D.; Wang, H.; Casaburi, R.; Fournier, M.; Lewis, M.I.; Taylor, W.; Storer, T.W. Exercise in maintenance hemodialysis patients induces transcriptional changes in genes favoring anabolic muscle. J. Am. Soc. Nephrol. JASN 2007, 18, 2975–2986. [Google Scholar] [CrossRef] [Green Version]
  58. Liao, M.T.; Liu, W.C.; Lin, F.H.; Huang, C.F.; Chen, S.Y.; Liu, C.C.; Lin, S.H.; Lu, K.C.; Wu, C.C. Intradialytic aerobic cycling exercise alleviates inflammation and improves endothelial progenitor cell count and bone density in hemodialysis patients. Medicine 2016, 95, e4134. [Google Scholar] [CrossRef]
  59. Lopes, L.C.C.; Mota, J.F.; Prestes, J.; Schincaglia, R.M.; Silva, D.M.; Queiroz, N.P.; Freitas, A.; Lira, F.S.; Peixoto, M.D.G. Intradialytic Resistance Training Improves Functional Capacity and Lean Mass Gain in Individuals on Hemodialysis: A Randomized Pilot Trial. Arch. Phys. Med. Rehabil. 2019, 100, 2151–2158. [Google Scholar] [CrossRef]
  60. Marinho, S.M.; Mafra, D.; Pelletier, S.; Hage, V.; Teuma, C.; Laville, M.; Carraro Eduardo, J.C.; Fouque, D. In Hemodialysis Patients, Intradialytic Resistance Exercise Improves Osteoblast Function: A Pilot Study. J. Ren. Nutr. 2016, 26, 341–345. [Google Scholar] [CrossRef]
  61. Olvera-Soto, M.G.; Valdez-Ortiz, R.; Lopez Alvarenga, J.C.; Espinosa-Cuevas Mde, L. Effect of Resistance Exercises on the Indicators of Muscle Reserves and Handgrip Strength in Adult Patients on Hemodialysis. J. Ren. Nutr. 2016, 26, 53–60. [Google Scholar] [CrossRef]
  62. Rosa, C.S.D.; Nishimoto, D.Y.; Souza, G.D.E.; Ramirez, A.P.; Carletti, C.O.; Daibem, C.G.L.; Sakkas, G.K.; Monteiro, H.L. Effect of continuous progressive resistance training during hemodialysis on body composition, physical function and quality of life in end-stage renal disease patients: A randomized controlled trial. Clin. Rehabil. 2018, 32, 899–908. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Silva, V.; Belik, F.S.; Hueb, J.C.; Goncalves, R.D.; Caramori, J.C.T.; Vogt, B.P.; Barretti, P.; Bazan, S.G.Z.; De Stefano, G.; Martin, L.C.; et al. Aerobic Exercise Training and Nontraditional Cardiovascular Risk Factors in Hemodialysis Patients: Results from a Prospective Randomized Trial. Cardiorenal Med. 2019, 9, 391–399. [Google Scholar] [CrossRef]
  64. Song, W.J.; Sohng, K.Y. Effects of progressive resistance training on body composition, physical fitness and quality of life of patients on hemodialysis. J. Korean Acad. Nurs. 2012, 42, 947–956. [Google Scholar] [CrossRef] [Green Version]
  65. Suhardjono; Umami, V.; Tedjasukmana, D.; Setiati, S. The effect of intradialytic exercise twice a week on the physical capacity, inflammation, and nutritional status of dialysis patients: A randomized controlled trial. Hemodial. Int. 2019, 23, 486–493. [Google Scholar] [CrossRef] [PubMed]
  66. Wilund, K.R.; Tomayko, E.J.; Wu, P.T.; Ryong Chung, H.; Vallurupalli, S.; Lakshminarayanan, B.; Fernhall, B. Intradialytic exercise training reduces oxidative stress and epicardial fat: A pilot study. Nephrol. Dial. Transplant. 2010, 25, 2695–2701. [Google Scholar] [CrossRef] [Green Version]
  67. Enright, P.L. The six-minute walk test. Respir. Care 2003, 48, 783–785. [Google Scholar]
  68. Higgins, J.P.T.; Altman, D.G.; Gøtzsche, P.C.; Jüni, P.; Moher, D.; Oxman, A.D.; Savović, J.; Schulz, K.F.; Weeks, L.; Sterne, J.A.C. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 2011, 343, d5928. [Google Scholar] [CrossRef] [Green Version]
  69. Conlon, J.A.; Newton, R.U.; Tufano, J.J.; Penailillo, L.E.; Banyard, H.G.; Hopper, A.J.; Ridge, A.J.; Haff, G.G. The efficacy of periodised resistance training on neuromuscular adaptation in older adults. Eur. J. Appl. Physiol. 2017, 117, 1181–1194. [Google Scholar] [CrossRef]
  70. Keller, U. Nutritional Laboratory Markers in Malnutrition. J. Clin. Med. 2019, 8. [Google Scholar] [CrossRef] [Green Version]
  71. Cabrerizo, S.; Cuadras, D.; Gomez-Busto, F.; Artaza-Artabe, I.; Marin-Ciancas, F.; Malafarina, V. Serum albumin and health in older people: Review and meta analysis. Maturitas 2015, 81, 17–27. [Google Scholar] [CrossRef]
  72. Levitt, D.G.; Levitt, M.D. Human serum albumin homeostasis: A new look at the roles of synthesis, catabolism, renal and gastrointestinal excretion, and the clinical value of serum albumin measurements. Int. J. Gen. Med. 2016, 9, 229–255. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  73. Friedman, A.N.; Fadem, S.Z. Reassessment of albumin as a nutritional marker in kidney disease. J. Am. Soc. Nephrol. 2010, 21, 223–230. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  74. Hanafusa, N.; Nitta, K.; Okazaki, M.; Komatsu, M.; Shiohira, S.; Kawaguchi, H.; Tsuchiya, K. Serum albumin level adjusted with C-reactive protein predicts hemodialysis patient survival. Ren. Replace. Ther. 2017, 3, 9. [Google Scholar] [CrossRef] [Green Version]
  75. Anders, H.J.; Andersen, K.; Stecher, B. The intestinal microbiota, a leaky gut, and abnormal immunity in kidney disease. Kidney Int. 2013, 83, 1010–1016. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  76. Girndt, M.; Sester, M.; Sester, U.; Kaul, H.; Kohler, H. Molecular aspects of T—and B-cell function in uremia. Kidney Int. Suppl. 2001, 78, S206–S211. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Castaneda, C.; Gordon, P.L.; Uhlin, K.L.; Levey, A.S.; Kehayias, J.J.; Dwyer, J.T.; Fielding, R.A.; Roubenoff, R.; Singh, M.F. Resistance training to counteract the catabolism of a low-protein diet in patients with chronic renal insufficiency. A randomized, controlled trial. Ann. Intern. Med. 2001, 135, 965–976. [Google Scholar] [CrossRef]
  78. Chan, D.; Cheema, B.S. Progressive Resistance Training in End-Stage Renal Disease: Systematic Review. Am. J. Nephrol. 2016, 44, 32–45. [Google Scholar] [CrossRef]
  79. Zhang, F.; Zhou, W.; Sun, Q.; Zhai, Y.; Zhang, Y.; Su, H.; Wang, Z. Effects of intradialytic resistance exercises on physical performance, nutrient intake and quality of life among haemodialysis people: A systematic review and meta-analysis. Nurs. Open 2019. [Google Scholar] [CrossRef] [Green Version]
  80. Cruz-Jentoft, A.J.; Bahat, G.; Bauer, J.; Boirie, Y.; Bruyère, O.; Cederholm, T.; Cooper, C.; Landi, F.; Rolland, Y.; Sayer, A.A.; et al. Sarcopenia: Revised European consensus on definition and diagnosis. Age Ageing 2018, 48, 16–31. [Google Scholar] [CrossRef] [Green Version]
  81. Kemp, G.J.; Crowe, A.V.; Anijeet, H.K.; Gong, Q.Y.; Bimson, W.E.; Frostick, S.P.; Bone, J.M.; Bell, G.M.; Roberts, J.N. Abnormal mitochondrial function and muscle wasting, but normal contractile efficiency, in haemodialysed patients studied non-invasively in vivo. Nephrol. Dial. Transplant. 2004, 19, 1520–1527. [Google Scholar] [CrossRef]
  82. Tamaki, M.; Miyashita, K.; Wakino, S.; Mitsuishi, M.; Hayashi, K.; Itoh, H. Chronic kidney disease reduces muscle mitochondria and exercise endurance and its exacerbation by dietary protein through inactivation of pyruvate dehydrogenase. Kidney Int. 2014, 85, 1330–1339. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Ide, T.; Tsutsui, H.; Hayashidani, S.; Kang, D.; Suematsu, N.; Nakamura, K.; Utsumi, H.; Hamasaki, N.; Takeshita, A. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ. Res. 2001, 88, 529–535. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. López-Armada, M.J.; Riveiro-Naveira, R.R.; Vaamonde-García, C.; Valcárcel-Ares, M.N. Mitochondrial dysfunction and the inflammatory response. Mitochondrion 2013, 13, 106–118. [Google Scholar] [CrossRef] [PubMed]
  85. Balakrishnan, V.S.; Rao, M.; Menon, V.; Gordon, P.L.; Pilichowska, M.; Castaneda, F.; Castaneda-Sceppa, C. Resistance training increases muscle mitochondrial biogenesis in patients with chronic kidney disease. Clin. J. Am. Soc. Nephrol. 2010, 5, 996–1002. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Ferrari, F.; Helal, L.; Dipp, T.; Soares, D.; Soldatelli, Â.; Mills, A.L.; Paz, C.; Tenório, M.C.C.; Motta, M.T.; Barcellos, F.C.; et al. Intradialytic training in patients with end-stage renal disease: A systematic review and meta-analysis of randomized clinical trials assessing the effects of five different training interventions. J. Nephrol. 2020, 33, 251–266. [Google Scholar] [CrossRef]
  87. Regolisti, G.; Sabatino, A.; Fiaccadori, E. Exercise in patients on chronic hemodialysis: Current evidence, knowledge gaps and future perspectives. Curr. Opin. Clin. Nutr. Metab. Care 2020, 23, 181–189. [Google Scholar] [CrossRef]
Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of the study selection process.
Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram of the study selection process.
Nutrients 12 03071 g001
Figure 2. Risk of bias graph of included studies.
Figure 2. Risk of bias graph of included studies.
Nutrients 12 03071 g002
Figure 3. Risk of bias summary for included studies.
Figure 3. Risk of bias summary for included studies.
Nutrients 12 03071 g003
Table 1. Characteristics of included Studies.
Table 1. Characteristics of included Studies.
IdentityExercise TypeStrength Assessment ToolPerformance Status AssessmentBody Composition Assessment ToolParticipants Exercise GroupFemale/Male Exercise GroupMean Age Exercise Group (Years)Participants Control GroupFemale/Male Control GroupMean Age Control Group (Years)
Abreu et al. [49]Resistance exercise
3 times/week for 12 weeks
N/AN/ACircumferences and skinfold thickness2554.5%/45.5%45.7 ± 15.21961.5%/38.5%42.5 ± 13.5
Cheema et al. [50]Resistance exercise
3 times/week for 12 weeks
HGS 16MWTComputed tomography and standard protocols by dietician247/1760.0 ± 5.3258/1765.0 ± 12.9
Chen et al. [51]Resistance exercise
2 times/week for 24 weeks
ΝANADEXA2210/1271.1 ± 12.62211/1166.9 ± 13.4
Cheng et al. [52]Resistance exercise
3 times/week for 2 years
N/A6MWTN/A6728/3954.6 ± 12.66525/4055.8 ± 11.98
Cooke et al. [53]Aerobic exercise
3 times/week for 16 weeks
HGS 26 m course as quickly as possibleN/A103/758.2 ± 17.2103/752.5 ± 15.4
Frih et al. [54]Resistance training
4 times/week for 16 weeks
HGS 36MWTN/A210/2164.2 ± 3.4200/2065.2 ± 3.1
Groussard et al. [55]Aerobic exercise
3 days/weak for 3 months
NA6MWTDEXA83/566.5 ± 4.6103/768.4 ± 3.7
Johan-sen et al. [56]Resistance exercise
3 times/week for 12 weeks
HGS 4Walking 6 m at their usual pace and as fast as possibleDEXA208/1254.4 ± 13.6206/1456.8 ± 13.8
Kopple, et al. [57] *Aerobic exercise
3 times/week for 18 weeks
N/AN/ADEXA104/645.9 ± 4.1145/941.3 ± 3.3
Kopple et al. [57] *Resistance training
3 times/week for 18 weeks
N/AN/ADEXA156/946.0 ± 2.7145/941.3 ± 3.3
Kopple et al. [57] *Combined exercise
3 times/week for 18 weeks
N/AN/ADEXA125/742.7 ± 3.8145/941.3 ± 3.3
Liao et al. [58]Aerobic exercise
3 times/week for 12 weeks
N/A6MWTDEXA2012/862 ± 82011/962 ± 9
Lopes et al. [59] #Resistance exercise (moderate load)
3 times/week for 12 weeks
HGSN/ADEXA146/848.1 ± 10.8201/1356.9 ± 12.4
Lopes et al. [59] #Resistance exercise (heavy load)
3 times/week for 12 weeks
HGSN/ADEXA167/956.2 ± 12.5201/1356.9 ± 12.4
Marinho et al. [60]Resistance exercise
3 times/week for 8 weeks
N/AN/ABCM63/371.5 (58.5–87.2) *74/376.0 (59.0-83.0) *
Olvera-Soto et al. [61]Resistance exercise
2 times/week for 12 weeks
HGS 5N/ACircumferences and skinfolds3016/1428.5 (23–46.5) *3112/201929 (19–38) *
Rosa et al. [62]Resistance exercise
3 times/weeks for 12 weeks
Wells Bench test6MWTDEXA288/202054.5 ± 11.97249/1557.10 ± 16.20
Silva et al. [63]Aerobic exercise
3 times/week for 12 weeks
N/AN/AN/A147/750 ± 17.2146/858 ± 15.0
Song et al. [64]Resistance exercise
3 times/week for 12 weeks
HGS 6N/AInBody s1072012/852.1 ± 12.4208/1254.6 ± 10.1
Suhardjonoc et al. [65] @Aerobic exercise
2 times/week for 12 weeks
HGS 6walk 4 m back and forth for an 8 m distanceBIA4214/2849.8 ± 11.73921/1850.5 ± 10.8
Suhardjonoc et al. [65] @Combined exercise
2 times/week for 12 weeks
HGS 6walk 4 m back and forth for a total distance of 8 mBIA3921/1850.5 ± 10.83921/1850.5 ±10.8
Wilund et al. [66]Aerobic exercise
3 days/week for 4 months
N/AN/AN/A74/360.8 ± 3.285/359.0 ± 4.9
N/A: not applicable; 6MWT: 6 min walk test; BC: body composition; DEXA: dual-energy X-ray absorptiometry, BIA: bioimpedance analysis (Maltron Inc., BioScan 920 2S Multifrequency Analyzer); BCM: body composition monitor; HGS: handgrip strength; *,#,@ same control group; 1 isometric digital dynamometer (Chatillon CSD 200; Dynamometer; Ametek Inc, Paoli, PA; CV, 9.4%); 2 hand dynamometer (Lafayette Instrument, Lafayette, IN); 3 dynamometer (T.K.K. 5401 GRIP D, Takei Science; Instruments, Niigata, Japan); 4 computerized dynamometer (Cybex Inc., Ronkonkoma, NY); 5 Analogue Handgrip Dynamometer Takei TKK 5001 Tokyo, Japan; 6 Jamar Hydraulic Hand Dynamometer; 7 Biospace, Seoul, Korea. Values are presented as: mean ± SD. * Median (interquartile range).
Table 2. Results on BMI after intervention.
Table 2. Results on BMI after intervention.
IdentityExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Abreu et al. [49]23.9 ± 4.723.8 ± 4.5Not reported24.4 ± 4.824.1 ± 4.9Not reported>0.05
Cheema et al. [50]27.0 ± 6.0Not reported0.3 ± 0.528.0 ± 5.7Not reported0.1 ± 0.50.02
Cooke et al. [53]25.6 ± 4.3Not reported0.28 (−0.23–0.95)27.2 ± 6.1Not reported0.20 (−0.03–0.45)0.485
Groussard et al. [55]29.4 ± 2.129.5 ± 1.9Not reported26.5 ± 1.826.2 ± 1.9Not reported>0.05
Kopple et al. [57] a26.9 ± 1.926.6 ± 1.8Not reported24.9 ± 1.125.1 ± 1.2Not reported>0.05
Kopple et al. [57] b28.7 ± 2.527.7 ± 2.5Not reported24.9 ± 1.125.1 ± 1.2Not reported>0.05
Kopple et al. [57] c26.2 ± 1.526.0 ± 1.5Not reported24.9 ± 1.125.1 ± 1.2Not reported>0.05
Liao et al. [58]22.9 ± 3.322.96 ± 3.36Not reported23.67 ± 4.1623.91 ± 5.27Not reported0.054
Marinho et al. [60]28.5 (21.1–35.8)28.4 (21.8–36.2)Not reported28.4 (20.8–35.2)28.6 (23.6–35.2)Not reported>0.05
Rosa et al. [62]26.4 ± 4.4826.6 ± 4.44Not reported25.54 ± 3.9525.5 ± 4.03Not reported0.752
Wilund et al. [66]30.1 ± 2.430.3 ± 2.5Not reported29.0 ± 2.028.3 ± 1.8Not reported<0.05
a Same control group; variables displayed as mean ± SD, median (interquartile range). a: Resistance exercise; b: combined exercise; c: aerobic exercise. a,b,c: same control group.
Table 3. Results on MAMC.
Table 3. Results on MAMC.
IdentityExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Abreu et al. [49]32.3 ± 14.633.9 ± 14.7Not reported35.6 ± 12.434.9 ± 15.2Not reported>0.05
Cheema et al. [50]30.1 ± 4.0Not reported0.4 ± 1.430.1 ± 4.0Not reported−0.6 ± 0.90.004
Olvera-Soto et al. [61]23.4 (20.3–25.4)24.1 (20.3–26.5)2.15 (−0.25 to 4.84) *22.6 (19.7–25.2)22.5 (19.6–25.5)0.67 (−1.35 to 2.87) *<0.01
Song et al. [64]23.4 ± 1.423.5 ± 1.40.1 ± 0.723.7 ± 2.723.8 ± 2.60.0 ± 0.60.747
Variables displayed as the mean ± SD, median (interquartile range); * percentage (interquartile range).
Table 4. Effects on Body Fat.
Table 4. Effects on Body Fat.
IdentityExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Chen et al. [51] (%)31.3 ± 10.429.6 ± 9.8Not reported30.8 ± 11.233.1 ± 10.1Not reported0.9
Groussard et al. [55] (%)32.2 ± 3.132.4 ± 3.2Not reported27.2 ± 2.727.3 ± 2.8Not reported>0.05
Johansen et al. [56] (kg)22.4 ± 11.324.5 ± 11.12.2 ± 2.921.3 ± 11.921.4 ± 12.10.2 ± 1.60.05
Kopple et al. [57] a (%)27.3 ± 3.026.8 ± 3.4Not reported24.3 ± 2.525.1 ± 2.6Not reported<0.01
Kopple et al. [57] b (%)23.5 ± 2.623.7 ± 2.6Not reported24.3 ± 2.525.1 ± 2.6Not reported<0.01
Kopple et al. [57] c (%)28.3 ± 2.627.1 ± 2.8Not reported24.3 ± 2.525.1 ± 2.6Not reported<0.01
Lopes et al. [59] A (kg)20.0 ± 2.519.9 ± 2.5Not reported24.7 ± 2.124.6 ± 2.1Not reported0.69
Lopes et al. [59] B (kg)23.7 ± 2.323.3 ± 2.3Not reported24.7 ± 2.124.6 ± 2.1Not reported0.69
Marinho et al. [60] (kg)47.4 (33.6–48.8)46.8 (35.0-48.6)Not reported53.0 (42.1–54.8)52.1 (45.5–55.3)Not reported>0.05
Olvera-Soto et al. [61] (%)16 (12.2–21.1)16.8 (13.1–20.3)5.43 (0.0 to 5.21) *14 (9.4–18.3)14.3 (11.3–18.8)0.42 (−13.2 to 7.97) *0.03
Rosa et al. [62] (%)23.8 ± 9.2123.10% ± 8.40Not reported23.15 ± 8.9821.92 ±8.81Not reported0.619
Song et al. [64] (%)27.5 ± 9.426.0 ± 8.6−1.5 ± 3.726.0 ± 9.327.2 ± 8.91.2 ± 3.80.020
a,b Same control group; variables displayed as the mean ± SD, median (interquartile range); * percentage (interquartile range). a: Resistance exercise; b: Combined exercise; c: Aerobic exercise. A: Resistance exercise (moderate load); B: Resistance exercise (heavy load). a, b, c: same control group. A, B: same control group 3.4. Lean body mass.
Table 5. Effects on Lean Body Mass (kg).
Table 5. Effects on Lean Body Mass (kg).
IdentityExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Chen et al. [51]45.8 ± 8.947.9 ± 9.9Not reported47.8 ± 9.046.3 ± 8.7Not reported0.5
Johansen et al. [56]47.5 ± 12.347.1 ± 11.2−0.3 ± 3.048.4 ± 8.248.2 ± 8.8−0.1 ± 1.60.66
Kopple et al. [57] a52.1 ± 0.2851.4 ± 0.27Not reported47.7 ± 0.2748.4 ± 0.26Not reported>0.05
Kopple et al. [57] b47.3 ± 0.2647.7 ± 0.27Not reported47.7 ± 0.2748.4 ± 0.26Not reported>0.05
Kopple et al. [57] c48.0 ± 0.3348.5 ± 0.32Not reported47.7 ± 0.2748.4 ± 0.26Not reported>0.05
Lopes et al. [59] A39.1 ± 2.139.4 ± 2.2Not reported41.6 ± 1.841.5 ± 1.8Not reported0.60
Lopes et al. [59] B41.6 ± 0.841.9 ± 0.8Not reported41.6 ± 1.841.5 ± 1.8Not reported0.60
Marinho et al. [60] (%)34.7 (32.3–53.3)35.7 (32.8–50.3)Not reported24.4 (18.9–39.0)27.4 (23.8–34.0)Not reported>0.05
Rosa et al. [62]46.55 ± 9.0347.55 ± 9.49Not reported43.48 ± 8.0244.04 ± 8.23Not reported0.277
Song et al. [64] (kg) *21.4 ± 3.622.2 ± 3.70.8 ± 1.022.8 ± 5.322.5 ± 5.2−0.3 ± 1.10.002
a,b Same control group, * skeletal body mass, variables displayed as the mean ± SD, median (interquartile range). a: Resistance exercise; b: Combined exercise; c: Aerobic exercise. A: Resistance exercise (moderate load); B: Resistance exercise (heavy load). a, b, c: same control group. A, B: same control group.
Table 6. Effects on SMI (kg/m2).
Table 6. Effects on SMI (kg/m2).
IdentityExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Lopes et al. [59] a6.4 ± 1.26.6 ± 1.2Not reported6.8 ± 1.036.6 ± 1.1Not reported<0.01
Lopes et al. [59] b6.7 ± 1.26.8 ± 1.1Not reported6.8 ± 1.036.6 ± 1.1Not reported<0.01
Suhardjono et al. [65] AMales 10.4 ± 1.16
Females 9.77 ± 0.58
Not reported0.15
(−2.11–2.89)
Males 9.92 ± 1.46
Females 9.79 ± 1.17
Not reported0.01
(−6.14–7.33)
>0.05
Suhardjono et al. [65] BMales 9.92 ± 1.46
Females 9.79 ± 1.17
Not reported0.04
(−0.85–4.19)
Males 9.92 ± 1.46
Females 9.79 ± 1.17
Not reported0.01
(−6.14–7.33)
>0.05
a,b Same control group; variables displayed as the mean ± SD or median (min–max). a: Resistance exercise (moderate load); b: Resistance exercise (heavy load). a, b: same control group. A: Combined exercise; B; Aerobic exercise. A, B: same control group. 3.6. Serum Albumin and C-Reaction Protein
Table 7. Changes in sALB (g/dl) and CRP (mg/L).
Table 7. Changes in sALB (g/dl) and CRP (mg/L).
IdentityParameterExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Abreu et al. [49]sALB4.3 ± 0.34.3 ± 0.3Not reported4.2 ± 0.24.2 ± 0.2Not reported
CRP7.7 ± 6.05.8 ± 4.48.54 ± 4.28.4 ± 7.5>0.05
Cheema et al. [50]sALB3.45 ± 0.31Not reported0.03 ± 0.243.36 ± 0.79Not reported0.01 ± 0.240.45
CRP0.78 ± 0.60−0.08 ± 0.370.72 ± 0.550.24 ± 0.370.02
Cheng et al. [52]sALB4.05 ± 0.274.09 ± 0.18Not reported3.96 ± 0.324.02 ± 0.36Not reported0.747
hs-CRP0.25 (0.08–0.37)0.15 (0.06–0.55) 0.28 (0.16–0.43)0.26 (0.15–0.52)
Frih et al. [54]sALB3.96 ± 0.350.40 ± 0.26Not reported3.99 ± 0.374.04 ± 0.37Not reported
CRP4.1 ± 1.34.1 ± 1.34.1 ± 1.14.0 ± 1.4>0.05
Kopple et al. [57] asALB3.7 ± 0.13.8 ± 0.1Not reported3.9 ± 0.13.9 ± 0.1Not reported>0.05
CRP4.5 ± 1.52.5 ± 0.62.1 ± 0.42.8 ± 0.8
Kopple et al. [57] bsALB3.9 ± 0.13.8 ± 0.1Not reported3.9 ± 0.13.9 ± 0.1Not reported
CRP3.5 ± 0.84.2 ± 1.32.1 ± 0.42.8 ± 0.8>0.05
Kopple et al. [57] csALB3.8 ± 0.13.8 ± 0.1Not reported3.9 ± 0.13.9 ± 0.1Not reported
CRP4.6 ± 1.45.8 ± 2.12.1 ± 0.42.8 ± 0.8>0.05
Liao et al. [58]sALB3.89 ± 0.334.16 ± 0.30Not reported4.00 ± 0.354.01 ± 0.42Not reported
Hs-CRP1.25 ± 2.010.78 ± 0.831.24 ± 2.041.23 ± 0.21<0.05
CRP0.7 ± 0.330.6 ± 0.201.2 ± 0.971.5 ± 0.89<0.01
Wilund et al. [66]CRP5.2 ± 0.78 4.9 ± 0.69Not reported6.2 ± 0.22.6.0 ± 0.67Not reported<0.05
sALB3.9 ± 0.143.9 ± 0.153.8 ± 0.09 3.8 ± 0.06
sALB: serum Albumin, CRP: C-Reactive Protein, Hs-CRP: high sensitivity C-Reactive Protein; a same control group; variables displayed as the mean ± SD or the median (interquartile range). a: Resistance exercise; b: Combined exercise; c: Aerobic exercise. a, b, c: same control group
Table 8. Results of the strength evaluation.
Table 8. Results of the strength evaluation.
IdentityParameterExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Cheema et al. [50]Total strength98.1 ± 36.6Not reported15.2 ± 15.486.0 ± 33.8Not reported−2.4 ± 13.80.002
Chen et al. [51]Knee extensors strength (kg)11.4 ± 5.015.8 ± 5.0Not reported14.8 ± 6.012.1 ± 6.1Not reported0.08
Cooke et al. [53]HGS23.2 ± 10.5Not reported1.3 (−0.5, 6.5)25.9 ± 13.8Not reported2.5 (−0.5, 4.0)0.464
Frih et al. [54]Handgrip
force (N)
29.8 ± 6.037.4 ± 4.8Not reported29.3 ± 5.630 ± 5.2Not reported<0.05
Johansen et al. [56]Knee extension 3RM (lb)14.0 ± 8.422.6 ± 11.68.6 ± 6.919.2 ± 8.720.0 ± 9.10.8 ± 2.0<0.0001
Hip abduction 3RM (lb)8.5 ± 5.215.4 ± 6.96.9 ± 5.011.8 ± 4.311.8 ± 5.9−0.1 ± 2.5<0.0001
Hip flexion 3RM (lb)7.6 ± 5.313.7 ± 6.86.1 ± 4.310.9 ± 4.511.4 ± 6.30.5 ± 2.7<0.0001
Lopes a et al. [59] aHGS (kg)29.2 ± 10.232.1 ± 11.4Not reported25.3 ± 9.125.4 ± 9.9Not reported0.60
Lopes a et al. [59] bHGS (kg)30.0 ± 8.729.9 ± 10.1Not reported25.3 ± 9.125.4 ± 9.9Not reported0.60
Olveira-Soto et al. [61]HGS (kg)19.6 (11–28)21.2 (13–32)Not reported19.8 (14-26)17.8 (15-26)Not reported<0.01
Rosa et al. [62]HGS (kg/strength)65.7 ± 23.366.61 ± 22.22Not reported59.21 ± 20.6658.52 ± 18.19Not reported0.213
Song et al. [64]HGS (kg)26.3 ± 8.528.7 ± 9.02.4 ± 2.826.2 ± 10.227.8 ± 11.81.6 ± 4.00.465
Leg muscle strength (kg)33.0 ± 15.337.3 ± 19.04.3 ± 8.734.8 ± 20.333.4 ± 19.5−1.4 ± 7.00.027
Suhardjono b et al. [65] AHGS (kg)Males: 24.8 ± 9.19
Females: 14.6 ± 4.66
Not reported−0.08
(−2.83–18.50)
Males: 22.1 ± 9.26
Females: 17.3 ± 8.27
Not reported−0.1
(2.78)
>0.05
Suhardjono b et al. [65] BHGS (kg)Males: 21.6 ± 8.84
Females: 18.3 ± 5.45
Not reported0
(−5.33–9.50)
Males: 22.1 ± 9.26
Females: 17.3 ± 8.27
Not reported−0.1
(2.78)
>0.05
HGS: Handgrip strength; RM: repetition maximum; a,b same control group; variables displayed as the mean ± SD, median (interquartile range), median (min–max). a: Resistance exercise (moderate load); b: Resistance exercise (heavy load). a, b: same control group. A: Combined exercise; B; Aerobic exercise. A, B: same control group.
Table 9. Changes on performance status.
Table 9. Changes on performance status.
IdentityTest UsedExercise Group BeforeExercise Group AfterExercise Group ChangeControl Group BeforeControl Group AfterControl Group Changep-Value
Cheema et al. [50]6MWT (m)496.0 ± 138.9Not reported19.6 ± 4.0412.6 ± 138.9Not reported1.5 ± 23.70.16
Cheng et al. [52]6MWT (m)439.1 ± 85.5490.5 ± 70.3Not reported460.3 ± 79.1456.7 ± 94.1Not reported0.207
Cooke et al. [53]6 m course as quickly as possible (m/s)0.8 ± 0.2Not reported0.02
(−0.02, 0.11)
0.9 ± 0.3Not reported−0.11
(−0.17, 0.08)
0.158
Frih et al. [54]6MWT (m)420 ± 35.1480.5 ± 31.9Not reported422.2 ± 26.6415.6 ± 36.3Not reported<0.05
Groussard et al. [55]6MWT (m)406 ± 18500 ± 30Not reported376 ± 20406 ± 18Not reported<0.001
Johansen et al. [56]Walking 6m at their usual pace and as fast as possible (gait speed-cm/s)100.9 ± 35.5103.5 ± 34.22.7 ± 17.399.8 ± 31.5105.7 ± 31.16.0 ± 17.20.71
Rosa et al. [62]6MWT (m)506.1 ± 130.3526.5 ± 126.2Not reported452.65 ± 169.19469.4 ± 162.9Not reported0.277
Suhardjono et al. [65] aWalk 4 m back and forth for a total distance of 8 m (m/s)Males: 0.86 ± 0.25
Females: 0.81 ± 0.2
Not reported0.08 ± 0.16Males: 0.8 ± 0.25
Females: 0.81 ± 0.23
Not reported0.07 ± 0.19>0.05
Suhardjono et al. [65] bWalk 4 m back and forth for a total distance of 8 m (m/s)Males: 0.87 ± 0.19
Females: 0.85 ± 0.17
Not reported0.10 ± 0.12Males: 0.8 ± 0.25
Females: 0.81 ± 0.23
Not reported0.07 ± 0.19>0.05
6MWT: 6 min walk test; variables displayed as the mean ± SD or median (interquartile range). a: Combined exercise; b: Aerobic exercise. a, b: same control group.

Share and Cite

MDPI and ACS Style

Bakaloudi, D.R.; Siargkas, A.; Poulia, K.A.; Dounousi, E.; Chourdakis, M. The Effect of Exercise on Nutritional Status and Body Composition in Hemodialysis: A Systematic Review. Nutrients 2020, 12, 3071. https://doi.org/10.3390/nu12103071

AMA Style

Bakaloudi DR, Siargkas A, Poulia KA, Dounousi E, Chourdakis M. The Effect of Exercise on Nutritional Status and Body Composition in Hemodialysis: A Systematic Review. Nutrients. 2020; 12(10):3071. https://doi.org/10.3390/nu12103071

Chicago/Turabian Style

Bakaloudi, Dimitra Rafailia, Antonios Siargkas, Kalliopi Anna Poulia, Evangelia Dounousi, and Michail Chourdakis. 2020. "The Effect of Exercise on Nutritional Status and Body Composition in Hemodialysis: A Systematic Review" Nutrients 12, no. 10: 3071. https://doi.org/10.3390/nu12103071

APA Style

Bakaloudi, D. R., Siargkas, A., Poulia, K. A., Dounousi, E., & Chourdakis, M. (2020). The Effect of Exercise on Nutritional Status and Body Composition in Hemodialysis: A Systematic Review. Nutrients, 12(10), 3071. https://doi.org/10.3390/nu12103071

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop