Skip to main content
PLOS One logoLink to PLOS One
. 2024 Dec 30;19(12):e0309798. doi: 10.1371/journal.pone.0309798

Systematic review of the best evidence for resistance exercise in maintenance hemodialysis patients

Qian Zhao 1,#, Ning Wu 1,#, Kaixing Duan 1,2,#, Jiahui Liu 1,2, Minghua Han 3, Huize Xu 3, Haoyang Chen 4,*, Ji Ma 5,*
Editor: Yuri Battaglia6
PMCID: PMC11684604  PMID: 39775055

Abstract

Objective

This study aims to search, evaluate, and consolidate the best evidence for resistance exercise in maintenance hemodialysis patients, providing evidence-based support for the clinical implementation of resistance exercise in these patients.

Methods

We conducted a comprehensive search of literature in databases on resistance exercise for maintenance hemodialysis patients, including guidelines, expert consensus, evidence summaries, systematic reviews, and randomized controlled trials. The search spanned from the inception of the database to March 2023. During the process of evaluation and data extraction, two researchers rigorously assessed the quality of the literature.

Results

A total of 24 articles were included in this review, consisting of 2 guidelines, 3 expert consensus documents, 9 systematic reviews, and 10 randomized controlled trials. From nine aspects, including target population, contraindications for exercise, pre-exercise assessment, exercise frequency, exercise intensity, exercise duration, exercise type, exercise benefits, and exercise precautions, we extracted a total of 23 pieces of best evidence.

Conclusion

Given the findings of this study, we recommend that future researchers design and conduct larger-scale, multi-center, longitudinal studies to validate our results and further explore the long-term impacts of combined resistance and aerobic exercises on muscle strength and other health indicators. Such research will provide deeper insights and contribute to the development of evidence-based exercise programs.

1. Introduction

Maintenance hemodialysis (MHD) is a blood purification therapy and one of the crucial renal replacement therapies for patients with end-stage chronic kidney disease [1]. MHD can extend patients’ lifespan and improve their quality of life, with its effectiveness second only to kidney transplantation [2]. Research indicates a growing global population of hemodialysis patients year by year [3], with China being the country with the highest number of individuals receiving hemodialysis [4]. By 2025, it is estimated that there will be 630 MHD patients per million population in China, with a total estimated number of hemodialysis patients reaching up to 870,000 individuals [5]. As the duration of dialysis extends, MHD patients experience varying degrees of cardiac and pulmonary function decline, muscle atrophy, physiological, psychological, and cognitive impairments, which significantly impact their quality of life [6]. Currently, both domestic and international research have provided a clear understanding of the mechanisms and intervention effects of exercise therapy for MHD patients. As a non-pharmacological intervention for MHD patients, exercise therapy can prevent muscle atrophy, improve physical function, and alleviate fatigue [7]. Specifically, when it comes to enhancing the muscle function of MHD patients, resistance exercise training has been shown to be more effective than aerobic exercise in promoting muscle gain [8], increasing muscle strength [9], enhancing upper limb grip strength [10], physical activity [11], improving systemic inflammatory responses [12], alleviating anxiety, depression, and other negative emotions, enhancing sleep quality, and improving overall quality of life [13,14]. The International Society of Renal Nutrition and Metabolism Global Kidney Exercise Team recommends increasing physical activity and exercise for all dialysis patients [15]. This study aims to comprehensively search for high-quality evidence literature regarding resistance exercise for MHD patients from both domestic and international sources. Through evaluation, data extraction, and summarization, we aim to provide a basis for healthcare professionals to develop scientific and rational resistance exercise programs for maintenance hemodialysis patients.

2. Materials and methods

2.1 Literature search

Utilizing the “6S” evidence model [16], a computerized search was conducted in the following databases and resources: BMJ Best Practice, UpToDate, Guidelines International Network (GIN), The National Institute for Health and Care Excellence (NICE), National Guideline Clearing House (NGC), Registered Nurses’ Association of Ontario (RNAO), Scottish Intercollegiate Guidelines Network (SIGN), PubMed, Cochrane Library, web of science, China Medical Guideline Database, China National Knowledge Infrastructure (CNKI), Wanfang Database, VIP Database, and SinoMed Database, to retrieve all literature related to resistance exercise in maintenance hemodialysis(MHD) patients. English search terms included “hemodialysis/maintenance hemodialysis” and “exercise/strength training/resistance training/weight training,” while Chinese search terms encompassed “血液透析/维持性血液透析” and “运动/力量训练/抗阻运动/负荷训练". The search was limited to publications from database inception until March 2023.

2.2 Inclusion and exclusion criteria for literature

Inclusion Criteria: Studies focusing on maintenance hemodialysis (MHD) patients as the study population; Research investigating resistance exercise in MHD patients; Types of studies eligible for inclusion: guidelines, expert consensus, evidence summaries, clinical decision-making studies, best practices, systematic reviews, and randomized controlled trials; Literature published in either Chinese or English. Exclusion Criteria: Literature types such as guideline interpretations, project proposals, and duplicate publications; Incomplete or inaccessible information within the documents; Studies that have not undergone quality assessment.

2.3 Criteria for literature quality assessment

The quality assessment for guidelines will be conducted using the Appraisal of Guidelines for Research and Evaluation (AGREE II) system [17]. Expert consensus will be evaluated according to the criteria established by the Joanna Briggs Institute (JBI) for Evidence-Based Healthcare (2016) [18]. Systematic reviews will undergo quality assessment using the Assessment of Multiple Systematic Reviews 2 (AMSTAR 2) [19]. Quality assessment for randomized controlled trials will adhere to the Joanna Briggs Institute’s Randomized Controlled Trial Assessment Criteria (2016) [20]. We will employ the Australian JBI Evidence Recommendation Grading System (2014 version) to categorize recommendations into Grade A (strong recommendation) and Grade B (weak recommendation), following the FAME principles (Feasibility, Applicability, Clinical Significance, and Effectiveness) as the basis for recommendation levels [21].

2.4 Process of literature quality assessment

The quality assessment of literature will be conducted independently by two researchers who have undergone systematic evidence-based nursing training. In cases where these two researchers encounter discrepancies or conflicts during the assessment, a third party, who is an evidence-based nursing expert, will be consulted for resolution.

In instances where there is conflicting evidence or conclusions from different sources, this study will prioritize evidence that is systematic, of high quality, and most recently published [22].

3. Results

3.1 General characteristics of included literature

The literature screening flowchart and literature screening form in the S1 Fig. Flow chart and S5 Table. This study encompassed a total of 24 articles, which consisted of 2 guidelines [23,24], 3 expert consensus documents [2527], 9 systematic reviews [9,2835], and 10 randomized controlled trials [8,12,3642]. Basic information regarding the included literature is provided in Table 1.

Table 1. Characteristics of included studies (n = 16).

Inclusion of literature Literature sources Type of study Literature theme Published (year)
Ashby et al. [23] NICE guidebook Renal Association Clinical Practice Guidelines for Haemodialysis 2019
Baker et al. [24] Medlive guidebook Exercise and lifestyle in chronic kidney disease 2022
Koufaki et al. [25] PubMed Expert consensus Exercise therapy for patients with chronic kidney disease 2015
Renal Rehabilitation Professional Committee, Rehabilitation Physicians Branch, Chinese Medical Doctors’ Association (CMA) [26] China Knowledge Network (CNN) Expert consensus Expert consensus on exercise rehabilitation for adults with chronic kidney disease in China 2019
Wei Yuanyuan and others [27] China Knowledge Network (CNN) Expert consensus Expert consensus on the construction of a renal rehabilitation system in haemodialysis units (centres) 2021
Gomes Neto et al. [28] PubMed Systematic Review Effect of exercise training modalities in dialysis on physical function and health-related quality of life in maintenance haemodialysis patients 2018
Scapini et al. [29] PubMed Systematic Review Aerobic, resistance and combined exercise improves exercise capacity and blood pressure control in maintenance haemodialysis patients 2019
Andrade et al. [30] PubMed Systematic Review The effect of exercise on cardiorespiratory function in chronic kidney disease during dialysis 2019
Lu et al. [9] PubMed Systematic Review Resistance training is effective in improving muscle mass and muscle strength in patients receiving dialysis 2019
Xu Qinjuan et al. [31] Knowledge Network (CNN) Systematic Review The effect of different exercise modalities on improving walking ability in maintenance haemodialysis patients 2021
Cai et al. [32] PubMed Systematic Review Analysis of the efficacy of aerobic exercise combined with resistance training in maintenance haemodialysis patients 2022
Dong et al. [36] PubMed Randomized controlled trial Effect of resistance exercise in dialysis on systemic inflammation in maintenance haemodialysis patients with sarcopenia 2019
Zhang et al. [8] PubMed Randomized controlled trial The effect of progressive resistance exercise in dialysis on the physical and quality of life of maintenance haemodialysis patients 2020
Zhao et al. [37] PubMed Randomized controlled trial Aerobic exercise combined with resistance exercise improves dialysis adequacy and quality of life in maintenance haemodialysis patients 2020
Corrêa et al. [12] PubMed Randomized controlled trial Effects of resistance training on sleep quality, redox balance and inflammatory status in maintenance haemodialysis patients 2020
Yansing et al. [38] China Knowledge Network (CNN) Randomized controlled trial Effects of progressive resistance exercise on exercise capacity, nutritional indicators and sleep quality in maintenance haemodialysis patients 2022
Cheema B et al. [43] PubMed Randomized controlled trial PEAK, a randomized controlled trial, investigates the effects of resistance training on anabolic metabolism in patients with kidney disease during their hemodialysis treatments 2007
de Lima et al. [39] PubMed Randomized controlled trial Comparing the impacts of strength and aerobic exercises during hemodialysis sessions 2013
Matthew J. Clarkson et al. [34] PubMed Systematic Review A systematic review and meta-analysis of exercise interventions aimed at enhancing physical function in end-stage kidney disease patients undergoing dialysis 2019
Sheng K et al. [33] PubMed Systematic Review A meta-analysis of intradialytic exercise effects on hemodialysis patients 2014
Pellizzaro, Cíntia O et al. [40] PubMed Randomized controlled trial The impact of peripheral and respiratory muscle training on the functional capabilities of patients undergoing hemodialysis 2012
Matsufuji, Shota et al. [41] PubMed Randomized controlled trial A randomized controlled trial assessing the impact of chair stand exercise on the daily living activities of hemodialysis patients 2015
Zhao QG et al. [35] PubMed Systematic Review A systematic review of exercise interventions for individuals with end-stage renal disease 2019
Johansen, Kirsten L et al. [42] PubMed Randomized controlled trial A study on the impact of resistance exercise training and nandrolone decanoate treatment on body composition and muscle functionality in hemodialysis patients 2006

3.2 Results of literature quality assessment

3.2.1 Quality assessment results of guidelines

This study included two guidelines from Ashby and Baker [23,24]. The guidelines by Ashby et al. [21] scored standardized percentages of 100% in scope and purpose, 87.37% in stakeholder involvement, 70.65% in rigor, 85.32% in clarity, 68.32% in applicability, and 100% in editorial independence. The guidelines by Baker et al. [22] achieved standardized scores of 95.56% in scope and purpose, 68.42% in stakeholder involvement, 88.32% in rigor, 97.65% in clarity, 77.22% in applicability, and 100% in editorial independence. Both guidelines scored above 60% in all domains, resulting in an overall rating of Grade A. The literature, as a whole, exhibited high quality and was deemed suitable for inclusion (The results of the quality assessment of the guidelines are presented in the S1 Table).

3.2.2 Quality assessment results of expert consensus

This study included two expert consensus documents. In document [25,26], all evaluation results were assessed as “yes” except for item 6, which was rated as “unclear.” In document[27], the expert consensus had ratings of “yes” for all items except items 2 and 6, which were rated as “unclear.” Both of the included documents exhibited complete research designs and overall good quality, qualifying them for inclusion (The results of the quality assessment results of expert consensus are presented in S2 Table).

3.2.3 Quality assessment results of systematic reviews

This study included 9 systematic reviews, comprising one Chinese-language publication and five English-language publications. Among them, two systematic reviews, namely Lu et al. [9] and Cai et al. [3235], received “yes” ratings for all assessment items, indicating comprehensive research design and high overall quality, and thus were eligible for inclusion. The systematic review by Gomes Neto et al. [28] received “yes” ratings for all items, except for item 15 (“Did the authors fully investigate publication bias?”), which was rated as “no.” The research design was relatively complete, allowing inclusion. Scapini et al.’s systematic review [29] received “yes” ratings for all items except item 9 (“Did the authors use appropriate tools to assess the risk of bias in the included studies”), which received a “partially yes,” and item 15 (“Did the authors fully investigate publication bias?”), rated as “no.” The research design was relatively complete, justifying inclusion. Andrade et al.’s systematic review [30] received “yes” ratings for all items except item 10 (“Did the authors report the source of funding for the studies included in the systematic review”), which was rated as “no.” The research design was relatively complete, permitting inclusion. Xu Qinjuan et al.’s systematic review [31] received “yes” ratings for all items except for item 10 (“Did the authors report the source of funding for the studies included in the systematic review”), and item 16 (“Did the authors report any potential conflicts of interest, including any funding received to conduct the systematic review?”), both of which were rated as “no.” The overall quality was relatively high, justifying inclusion (The results of the quality assessment results of systematic reviews are presented in S3 Table).

3.2.4 Quality assessment results of randomized controlled trials

This study included 10 randomized controlled trials, comprising 1 Chinese-language publication and 9 English-language publications. Among them, Dong et al.’s trial [36] and Zhao et al.’s trial [37,43] had ratings of “unclear” for items 4 (“Was blinding of participants implemented?”) and 5 (“Was blinding of the interveners implemented?”), while all other item ratings were “yes.” These trials demonstrated relatively complete designs, thus warranting inclusion. Zhang et al.’s trial [8,39] had a “unclear” rating for item 5 (“Was blinding of the interveners implemented?”), with “yes” ratings for all other items. The trial exhibited a relatively complete design, justifying inclusion. Corrêa et al.’s trial [12,40] had “not applicable” ratings for items 4 (“Was blinding of participants implemented?”) and 5 (“Was blinding of the interveners implemented?”), while all other items received “yes” ratings. The trial demonstrated a relatively complete design, supporting inclusion. Yan Xing’s trial [38,41,42] received a “no” rating for items 4 (“Was blinding of participants implemented?”) and 5 (“Was blinding of the interveners implemented?”), while all other item ratings were “yes.” The trial exhibited a relatively complete design, justifying inclusion (The results of the quality assessment results of randomized controlled trials are presented in S4 Table).

3.3 Summary and description of evidence

Through the extraction and integration of evidence, this study has compiled evidence related to resistance exercise in maintenance hemodialysis (MHD) patients. Ultimately, 23 pieces of best evidence were extracted from nine aspects, including the target population for MHD patients’ resistance exercise, contraindications to exercise, pre-exercise assessment, exercise frequency, exercise intensity, exercise duration, exercise type, exercise benefits, and exercise precautions, as detailed in Table 2.

Table 2. Summary of best evidence for resistance exercise in maintenance hemodialysis patients.

Form Content of evidence Recommended strength
applicable population 1. It is recommended that all MHD patients without contraindications should engage in exercise during dialysis as a therapeutic way to increase physical function [23,24]; A
Contraindications to exercise 2. Abnormal blood pressure: severe hypertension (e.g., blood pressure over 180/110 mmHg), or hypotension (<90/60 mmHg) [26]; A
3. Cardiopulmonary diseases: severe heart failure, arrhythmias, unstable angina, severe pericardial effusion, valvular stenosis, hypertrophic cardiomyopathy, aortic coarctation, etc., uncontrolled pulmonary hypertension (mean pulmonary artery pressure > 55 mmHg) [26]; A
4. Acute clinical events: e.g. acute systemic inflammatory disease [26]; A
5. Stop exercising immediately for symptoms of DVT such as unusual oedema, redness and pain in the calf [26]; A
6. Those who can not cooperate with the exercise such as serious oedema, osteoarthrosis, etc. [26]; A
Pre-exercise assessment 7. It is recommended that MHD patients should undergo an exercise load test under the supervision of a healthcare professional prior to exercise to assess the patient’s ability to tolerate incremental intensity exercise training [26]; A
8. It is recommended that MHD patients under the supervision of healthcare personnel before exercise capacity test including cardiorespiratory endurance, muscular strength, muscular endurance, flexibility, etc., the test should be arranged on non-dialysis days; attention should be paid to avoid the measurement of blood pressure in the limb on the side of the inner fistula; commonly used methods of simple exercise capacity test are 6 min walking test, sit-to-stand test, and get-up-and-walk test to ensure the safety of the exercise process [26,27]; A
9. A General Electric High Speed CT Scanner was used to perform CT scans on the nondominant mid-thigh of participants on a non dialysis day. These scans measured the thigh muscle cross-sectional area (CSA) and attenuation to assess muscle quantity and quality, respectively. Lower muscle attenuation values indicate better muscle quality due to less intramuscular lipid infiltration [44]. A
10. the scans measured subcutaneous and total fat areas in the mid-thigh. All scans were collected and analyzed blindly, following previously reported methods [44]. A
exercise frequency 11. It is recommended that patients with MHD need to perform exercise training at least 3 times per week on top of increased daily physical activity [25,26]; A
12. Exercise during routine haemodialysis was performed under the direct supervision of an exercise physiologist, with 8–15 sets of joint flexion and extension exercises 3 times per week for 12 weeks.[44] A
exercise intensity 13. Moderate-intensity aerobic exercise (50% to 70% VO2 peak) and resistance exercise (60% to 70% 1RM) are recommended for patients with MHD [25,26]; A
14. It is recommended that patients with MHD need at least three to five sessions of low to moderate intensity exercise training per week [27]; A
15. Peak force (kg) of the knee extensors, hip abductors, and triceps was measured bilaterally in triplicate with the best score recorded, using an isometric digital dynamometer (Chatillon CSD 200 Dynamometer; AMETEK, Paoli, PA; coefficient of variability 9.4%). These individual strength measures were summed to create a total strength measure [44]. A
exercise duration 16. The time of exercise was during or two hours before dialysis [33]; A
17. The target duration is 30–60 min per exercise session, which can be divided into sessions depending on the individual MHD patient [26], the duration of exercise intervention should be longer than 6 month [34,39]; A
Type of sport 18. Suggested exercise patterns for people with MHD include aerobic exercise, resistance exercise, and flexibility training [27]; A
19. Common resistance exercise programmes include: stretch pullers or elastic bandages, lifting dumbbells, sit-ups, push-ups, sand bags, leg weight, chair stand exercise etc. [26,40,41]; A
20. Mainly low-to-moderate load lower extremity exercises with 1 to 3 sets of 8 to 15 repetitions per set [34]. A
Exercise benefits 21. Progressive resistance exercise in dialysis enhances musculoskeletal strength and exercise capacity in maintenance haemodialysis patients [25,26,28,29,31]; A
22. Aerobic, resistance and combined exercise training improves dialysis adequacy and blood pressure control in maintenance haemodialysis patients [29]; B
23. Resistance exercise in dialysis is effective in improving the systemic inflammatory response [36]; B
24. Exercise programmes in dialysis can improve cardiorespiratory fitness, exercise tolerance and ventilatory efficiency in patients with chronic kidney disease [30]; B
25. resistance training improves sleep quality, redox balance and inflammatory response in maintenance haemodialysis patients [12]; B
26. Progressive resistance exercise enhances exercise capacity, improves nutritional status, and enhances sleep quality in MHD patients [38]; B
27. Exercise can improve fatigue, anxiety, depression, physical activity, and QOL in patients with end-stage renal disease [35]; A
28. Intradialytic exercise can increase the solute removal, for exercise may increase the blood flow to muscle, and greater toxic agents can be removed by the dialyzers [39]; A
29. The exercise program of peripheral muscle resistance can increase the volume of anti-fatigue muscle fibers, the muscle’s capture and transport of oxygen [33]; A
Notes on exercise entry 30. Exercise programmes should be individualised based on the patient’s physiological function measurements and ability to perform daily activities, and it is recommended to start with low-intensity exercise training and gradually reach a moderate-intensity exercise level [26]; A
31. MHD patients should immediately stop rehabilitation training if they experience: ① burning pain, soreness, and constriction in the chest, arms, neck, or jaw; ② severe chest tightness, shortness of breath, and dyspnea; ③ headache, dizziness, and general weakness; ④ severe cardiac arrhythmia; and ⑤ exercise-related muscle spasms and joint pains [26]; A
32. Ensure that the safety of people with MHD is paramount and that safety precautions are in place before performing resistance exercise [25]. A
33. The most common risk of intradialytic exercise is musculoskeletal injury, while the most serious risk is cardiovascular events, such as arrhythmia, myocardial infarction, and hypertension [39]; A
34. Treatment with nanrodone caprate during weekly lower limb resistance exercise training is safe and well tolerated [42]; A

4. Discussion

4.1 Comprehensive evidence summarization with clinical practice implications

In this study, evidence concerning resistance exercise in maintenance hemodialysis (MHD) patients was comprehensively summarized across nine key aspects: the appropriate population for MHD patients’ resistance exercise, contraindications, pre-exercise assessment, exercise frequency, intensity, duration, type, benefits, and precautions, as outlined in Table 2. Evidence 1 highlights the appropriate population for resistance exercise among MHD patients, recommending exercise therapy for stable patients without contraindications [23,24]. Resistance exercise can enhance cardiorespiratory endurance, improve muscle strength and mass, reduce cardiovascular disease risk, alleviate emotional disturbances and sleep disorders, and enhance quality of life [26]. Evidence 2 to 6 detail contraindications for exercise. Prior to engaging MHD patients in resistance exercise, healthcare professionals should conduct a thorough assessment to identify and promptly address any contraindications to avoid potential health risks. Evidence 7 to 8 emphasize the importance of graded exercise testing (GXT) for MHD patients before undertaking moderate to high-intensity exercise. GXT evaluates patients’ tolerance to progressive training, measures peak VO2, and facilitates the development of personalized training plans. Furthermore, it includes exercise testing to monitor blood pressure, blood oxygen levels, electrocardiograms, Borg’s rating of perceived exercise (RPE), and clinical symptoms, ensuring the safety of patients during exercise testing [26]. In the safety of resistance in haemodialysis patients, no cases of cannula dislodgement during exercise were observed in any patient during the trial. Given that the majority of MHD patients struggle to complete maximal oxygen uptake (VO2max) assessments, alternative, simpler tests commonly used with other populations, such as the 6-minute walk test, are recommended for evaluating their functional capacity [27]. It is essential to note that MHD patients should undergo exercise testing on non-dialysis days and avoid measuring blood pressure on the side with a vascular access [26]. Evidence 9 to 14 describe the prescription of exercise for MHD patients based on the FITT principles. Engaging in appropriate rehabilitation exercise training during hospitalization is crucial for maintaining MHD patients’ physical activity. However, outpatient rehabilitation exercise training is also indispensable. Healthcare professionals should provide patients and their families with relevant health education, with particular attention to assessing exercise intensity and safety measures. Family members play a supervisory, supportive, and guiding role in the patient’s exercise rehabilitation, encouraging them to gradually increase daily activity [26]. This should ensure the continuity and sustainability of exercise. Evidence 15 to 20 underscore the benefits of resistance training for MHD patients. Healthcare professionals should create individualized exercise prescriptions based on the patient’s unique circumstances and preferences, encouraging them to remain consistent to reap health benefits. Evidence 21 to 23 outline exercise precautions. Due to the complex condition and numerous clinical comorbidities in dialysis patients, it is advisable for patients to start with low-intensity exercise training and gradually progress to moderate-intensity levels. Personalized prescriptions should be tailored according to the patient’s physiological assessments and their activities of daily life (ADL) status. If there are indications for discontinuing exercise rehabilitation training, it should be halted immediately, prioritizing patient safety [26]. In line with the recommendations from the Exercise & Sport Science Australia (ESSA) position statement on exercise and chronic kidney disease (Smart NA, et al., 2013), our findings underscore the importance of a tailored approach to exercise prescription for individuals with ESKD. The ESSA guidelines emphasize the need for individualized assessment and the consideration of patient-specific factors, which align with our study’s approach to optimizing exercise training programs for this population.

Numerous studies have identified a variety of physical, psychological, and logistical barriers that impede the ability of hemodialysis patients to engage in regular exercise [45]. It is essential for nephrologists to address these barriers proactively, as highlighted by Clarke et al. [46], who emphasize the importance of nephrologists’ special efforts in targeting patients’ exercise barriers [47]. The proactive attitude of healthcare staff in dialysis centers is crucial for promoting a significant improvement in patients’ levels of physical activity [48]. It is suggested that patient counseling and exercise prescription should be grounded in a multidisciplinary team-based approach. In this collaborative framework, the referring nephrologist should be supported by other healthcare professionals, such as physiotherapists and exercise physiologists, to ensure a comprehensive and personalized exercise program tailored to the unique needs of each patient. This multidisciplinary approach not only enhances the effectiveness of exercise interventions but also fosters a supportive environment that encourages patients to overcome the identified barriers and engage in regular physical activity, ultimately contributing to improved health outcomes.

To guarantee both safety and efficacy during the dialysis process, we advise against the use of the arm equipped with vascular access for strenuous resistance exercises. Instead, we suggest that exercise regimens be scheduled during the initial two hours of the dialysis session. This strategic timing is intended to circumvent the exhaustion that may arise from the increased net ultrafiltration volume typically observed in the final 1–2 hours of the dialysis treatment.

4.2 Evidence-based translation into clinical practice for resistance exercise in maintenance hemodialysis patients

While this study has provided a comprehensive summary of the best evidence for resistance exercise in maintenance hemodialysis (MHD) patients, it is essential to acknowledge that this evidence synthesis represents an integration of existing research findings. Current evidence suggests that resistance training had a positive impact on muscle strength, balance, and functional capacity in maintenance hemodialysis patients [43,4952], though there is notable heterogeneity across studies due to variations in assessment indices, patient characteristics, and training protocols. Most studies report improvements in direct measures of muscle strength [51], while some also demonstrate gains in summary indices of strength and balance [53]. However, not all studies consistently show improvements in gait speed, STS test, or walking capacity as assessed by the 6-Minute Walk Distance (6MWD) [53]. These discrepancies highlight the need for standardized assessment methods and personalized training programs in future research to optimize the benefits and safety of resistance exercise for MHD patients. Ultimately, integrating resistance exercise into the daily routine of these patients holds promise for enhancing their overall quality of life. There may still be some discrepancies between the evidence summary and its practical implementation in clinical settings. Current randomized controlled trials examining resistance exercise in MHD patients exhibit certain limitations, such as small sample sizes and non-uniform intervention protocols. Additionally, several studies have investigated the combination of aerobic exercise with resistance exercise, further necessitating exploration and research into the singular effects of resistance exercise on MHD patients. When translating the evidence summary into practice, it is imperative to consider the individualized nature of clinical circumstances and the professional judgment of healthcare providers. A comprehensive and thorough assessment of patients, encompassing physical, psychological, social conditions, as well as the patients’ preferences, is paramount. This holistic evaluation is essential for tailoring personalized and feasible resistance exercise regimens for MHD patients, ensuring compliance, safety, and effectiveness. Future endeavors in the evidence-based translation of resistance exercise for MHD patients should prioritize the alignment of clinical realities, healthcare professionals’ expertise, and a thorough patient evaluation. This approach guarantees the development of personalized and actionable resistance exercise plans that prioritize compliance, safety, and effectiveness.

4.3 Limitations

The heterogeneity in exercise training protocols, timing, and endpoints, as noted by the reviewer and highlighted in the work of Regolisti G et al. [38], introduces considerable variability in the outcomes reported across studies. This underscores the urgent need for a consensus on standardized protocols and endpoints to enhance the validity and generalizability of research findings in this field. Moreover, there is a clear necessity for standardized methods to assess physical function and HRQoL, which will provide a solid foundation for future comparative effectiveness studies.

5. Conclusion

Given the findings of this study, we recommend that future researchers design and conduct larger-scale, multi-center, longitudinal studies to validate our results and further explore the long-term impacts of combined resistance and aerobic exercises on muscle strength and other health indicators. Such research will provide deeper insights and contribute to the development of evidence-based exercise programs.

Supporting information

S1 Checklist. PRISMA 2020 checklist.

(DOCX)

pone.0309798.s001.docx (23KB, docx)
S2 Checklist. PRISMA 2020 flow diagram for new systematic reviews which included searches of databases and registers only.

(DOCX)

pone.0309798.s002.docx (50.9KB, docx)
S1 Fig. Flow chart.

(DOCX)

pone.0309798.s003.docx (114.3KB, docx)
S1 Table. Quality assessment results of guidelines.

(DOCX)

pone.0309798.s004.docx (11.9KB, docx)
S2 Table. Quality assessment results of expert consensus.

(DOCX)

pone.0309798.s005.docx (12KB, docx)
S3 Table. Quality assessment results of systematic reviews.

(DOCX)

pone.0309798.s006.docx (14.8KB, docx)
S4 Table. Quality assessment results of randomized controlled trials.

(DOCX)

pone.0309798.s007.docx (13.4KB, docx)
S5 Table. All research information forms.

(XLSX)

pone.0309798.s008.xlsx (57.2KB, xlsx)

Acknowledgments

We would like to thank Jian Zhao and Xiaoxiao Xue for their assistance with this study.

Data Availability

All relevant data are within the paper and its Supporting information files.

Funding Statement

This study was financially supported by the 2022 Clinical Nursing Research Project of the Nursing Branch of the Chinese Society of Research Hospitals, titled “Study on the Promotion and Application of a Resistance Exercise Practice Programme for Patients with Stable Chronic Obstructive Pulmonary Disease in an Evidence-based Ecosystem", in the form of an award (Y2022FH-HLFH06-09) received by QZ. This study was also financially supported by the 2022-2023 Nursing Discipline Research Project of the Journal of the Chinese Medical Association, titled “Based on the Evidence Ecosystem", in the form of an award (CMAPH-NRD2022034) received by QZ. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

References

  • 1.Wenmei L, Pengyu C, Zeng Ying, Huaihong Y. Analysis of current situation and influencing factors of self-regulatory fatigue in maintenance hemodialysis patients. West China Medicine 2022. p. 1022–6(in chinese). [Google Scholar]
  • 2.Wan Niu TH, Wang Lisheng. Summary of the best evidence for exercise management protocols in maintenance hemodialysis patients. Evidence-based nursing 2022. p. 1719–24(in chinese). [Google Scholar]
  • 3.Himmelfarb J, Vanholder R, Mehrotra R, Tonelli M. The current and future landscape of dialysis. Nature reviews Nephrology. 2020;16(10):573–85. Epub 2020/08/01. doi: 10.1038/s41581-020-0315-4 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Htay H, Bello AK, Levin A, Lunney M, Osman MA, Ye F, et al. Hemodialysis Use and Practice Patterns: An International Survey Study. American journal of kidney diseases: the official journal of the National Kidney Foundation. 2021;77(3):326–35.e1. Epub 2020/08/18. doi: 10.1053/j.ajkd.2020.05.030 . [DOI] [PubMed] [Google Scholar]
  • 5.Yang C, Yang Z, Wang J, Wang HY, Su Z, Chen R, et al. Estimation of Prevalence of Kidney Disease Treated With Dialysis in China: A Study of Insurance Claims Data. American journal of kidney diseases: the official journal of the National Kidney Foundation. 2021;77(6):889–97.e1. Epub 2021/01/10. doi: 10.1053/j.ajkd.2020.11.021 . [DOI] [PubMed] [Google Scholar]
  • 6.Yuanyuan W, Yingchun M, Li Z. Expert consensus on the construction of renal rehabilitation system in hemodialysis room (center). China Blood Purification 2021. p. 823–9. [Google Scholar]
  • 7.Junxiang F, Aimin W, Yunping Z, Qingli L, Qingchao L. Effects of Baduanjin on sleep quality and negative mood in maintenance hemodialysis patients. Journal of Nursing Administration 2021. p. 285–90. [Google Scholar]
  • 8.Zhang F, Huang L, Wang W, Shen Q, Zhang H. Effect of intradialytic progressive resistance exercise on physical fitness and quality of life in maintenance haemodialysis patients. Nursing open. 2020;7(6):1945–53. Epub 2020/10/20. doi: 10.1002/nop2.585 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Lu Y, Wang Y, Lu Q. Effects of Exercise on Muscle Fitness in Dialysis Patients: A Systematic Review and Meta-Analysis. American journal of nephrology. 2019;50(4):291–302. Epub 2019/09/04. doi: 10.1159/000502635 . [DOI] [PubMed] [Google Scholar]
  • 10.Cardoso DF, Leal DV, Martins P, Abade EA, Rocha HC, Ferreira M, et al. Novel Approach to Intradialytic Progressive Resistance Exercise Training. Blood purification. 2023;52(9–10):768–74. Epub 2023/09/25. doi: 10.1159/000531973 . [DOI] [PubMed] [Google Scholar]
  • 11.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. Frontiers in physiology. 2017;8:288. Epub 2017/06/18. doi: 10.3389/fphys.2017.00288 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Corrêa HL, Moura SRG, Neves RVP, Tzanno-Martins C, Souza MK, Haro AS, et al. Resistance training improves sleep quality, redox balance and inflammatory profile in maintenance hemodialysis patients: a randomized controlled trial. Scientific reports. 2020;10(1):11708. Epub 2020/07/18. doi: 10.1038/s41598-020-68602-1 interests that might be perceived to influence the results and/or discussion reported in this paper. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Ribeiro R, Coutinho GL, Iuras A, Barbosa AM, Souza JA, Diniz DP, et al. Effect of resistance exercise intradialytic in renal patients chronic in hemodialysis. Jornal brasileiro de nefrologia. 2013;35(1):13–9. Epub 2013/04/20. doi: 10.5935/01012800.20130003 . [DOI] [PubMed] [Google Scholar]
  • 14.Cigarroa I, Barriga R, Michéas C, Zapata-Lamana R, Soto C, Manukian T. [Effects of a resistance training program in patients with chronic kidney disease on hemodialysis]. Revista medica de Chile. 2016;144(7):844–52. Epub 2016/09/24. doi: 10.4067/s0034-98872016000700004 . [DOI] [PubMed] [Google Scholar]
  • 15.Wilund K, Thompson S, Bennett PN. A Global Approach to Increasing Physical Activity and Exercise in Kidney Care: The International Society of Renal Nutrition and Metabolism Global Renal Exercise Group. Journal of renal nutrition: the official journal of the Council on Renal Nutrition of the National Kidney Foundation. 2019;29(6):467–70. Epub 2019/10/09. doi: 10.1053/j.jrn.2019.08.004 . [DOI] [PubMed] [Google Scholar]
  • 16.Dicenso A, Bayley L, Haynes RB. Accessing pre-appraised evidence: fine-tuning the 5S model into a 6S model. Evidence-based nursing. 2009;12(4):99–101. Epub 2009/09/26. doi: 10.1136/ebn.12.4.99-b . [DOI] [PubMed] [Google Scholar]
  • 17.wenyue W, A x. Introduction to Clinical Guidelines Research and Evaluation System II. Journal of Integrative Chinese and Western Medicine 2012. p. 160–5(in chinese). [DOI] [PubMed] [Google Scholar]
  • 18.Hu Yan HY. Evidence-based Nursing, 2nd Ed. People’s Medical Publishing House; 2018. [Google Scholar]
  • 19.Shea BJ, Reeves BC, Wells G, Thuku M, Hamel C, Moran J, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ (Clinical research ed). 2017;358:j4008. Epub 2017/09/25. doi: 10.1136/bmj.j4008 at http://www.icmje.org/coi_disclosure.pdf and declare: no support from any organisation for the submitted work; no financial relationships with any organisations that might have an interest in the submitted work in the previous three years, no other relationships or activities that could appear to have influenced the submitted work. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Barker TH SJ, Sears K, Klugar M, Tufanaru C, Leonardi-Bee J, Aromataris E, Munn Z. The revised JBI critical appraisal tool for the assessment of risk of bias for randomized controlled trials. JBI Evidence Synthesis. 2023;21(3):494–506. 2023;21(3):494–506. doi: 10.11124/JBIES-22-00430 [DOI] [PubMed] [Google Scholar]
  • 21.Chunqing W, Yan H. JBI Evidence Pre-grading and Evidence Recommendation Level System (2014 edition). Journal of advanced nursing. 2015;30(11):4. [Google Scholar]
  • 22.Fei L, Longmei S, Yingxin W, Yue W, Shuqi Z, Yanming D, et al. Summary of evidence for resistance training in patients with breast cancer-associated lymphedema. Chinese journal of nursing. 2021;56(05):755–61. [Google Scholar]
  • 23.Ashby D, Borman N, Burton J, Corbett R, Davenport A, Farrington K, et al. Renal Association Clinical Practice Guideline on Haemodialysis. BMC nephrology. 2019;20(1):379. Epub 2019/10/19. doi: 10.1186/s12882-019-1527-3 Association Clinical Practice Guidelines Development Manual. Further details can be obtained on request from the Renal Association. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Baker LA, March DS, Wilkinson TJ, Billany RE, Bishop NC, Castle EM, et al. Clinical practice guideline exercise and lifestyle in chronic kidney disease. BMC nephrology. 2022;23(1):75. Epub 2022/02/24. doi: 10.1186/s12882-021-02618-1 Association Clinical Practice Guidelines Development Manual. Further details can be obtained on request from the Renal Association. The authors declare that they have no competing interests. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Koufaki P, Greenwood S, Painter P, Mercer T. The BASES expert statement on exercise therapy for people with chronic kidney disease. Journal of sports sciences. 2015;33(18):1902–7. Epub 2015/03/26. doi: 10.1080/02640414.2015.1017733 . [DOI] [PubMed] [Google Scholar]
  • 26.Renal Rehabilitation Committee RPB, Chinese Medical Doctor Association. Expert consensus on exercise rehabilitation of adult patients with chronic kidney disease in China. Chinese Journal of Nephrology. 2019;35(7):537–43. doi: 10.3760/cma.j.issn.1001-7097.2019.07.011 [DOI] [Google Scholar]
  • 27.Yuanyuan W, Yingchun M, force L. Expert consensus on the construction of renal rehabilitation system in hemodialysis room (center). Chinese blood purification. 2021;20(12):823–9(in chinese). [Google Scholar]
  • 28.Gomes Neto M, de Lacerda FFR, Lopes AA, Martinez BP, Saquetto MB. Intradialytic exercise training modalities on physical functioning and health-related quality of life in patients undergoing maintenance hemodialysis: systematic review and meta-analysis. Clinical rehabilitation. 2018;32(9):1189–202. Epub 2018/02/27. doi: 10.1177/0269215518760380 . [DOI] [PubMed] [Google Scholar]
  • 29.Scapini KB, Bohlke M, Moraes OA, Rodrigues CG, Inácio JF, Sbruzzi G, et al. 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. Journal of physiotherapy. 2019;65(1):4–15. Epub 2018/12/26. doi: 10.1016/j.jphys.2018.11.008 . [DOI] [PubMed] [Google Scholar]
  • 30.Andrade FP, Rezende PS, Ferreira TS, Borba GC, Müller AM, Rovedder PME. Effects of intradialytic exercise on cardiopulmonary capacity in chronic kidney disease: systematic review and meta-analysis of randomized clinical trials. Scientific reports. 2019;9(1):18470. Epub 2019/12/06. doi: 10.1038/s41598-019-54953-x . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Qinjuan X, Yanfei H, Huagang H. Mesh meta-analysis of different exercise methods to improve walking ability in maintenance hemodialysis patients. PLA nursing journal. 2021;38(07):1–5. [Google Scholar]
  • 32.Cheng LJ, Jiang Y, Wu VX, Wang W. A systematic review and meta-analysis: Vinegar consumption on glycaemic control in adults with type 2 diabetes mellitus. J Adv Nurs. 2020;76(2):459–74. Epub 2019/11/02. doi: 10.1111/jan.14255 . [DOI] [PubMed] [Google Scholar]
  • 33.de Lima MC, Cicotoste CdL, Cardoso KdS, Forgiarini LA Junior, Monteiro MB, Dias AS. Effect of Exercise Performed during Hemodialysis: Strength versus Aerobic. Renal Failure. 2013;35(5):697–704. doi: 10.3109/0886022X.2013.780977 [DOI] [PubMed] [Google Scholar]
  • 34.Clarkson MJ, Bennett PN, Fraser SF, Warmington SA. Exercise Interventions for Improving Objective Physical Function in End-Stage Kidney Disease Patients on Dialysis: A Systematic Review and Meta-Analysis. Am J Physiol Renal Physiol. 2019;316(5):F856–F72. [DOI] [PubMed] [Google Scholar]
  • 35.Zhao Q-G, Zhang H-R, Wen X, Wang Y, Chen X-M, Chen N, et al. Exercise interventions on patients with end-stage renal disease: a systematic review. Clinical rehabilitation. 2019;33(2):147–56. doi: 10.1177/0269215518817083 [DOI] [PubMed] [Google Scholar]
  • 36.Dong ZJ, Zhang HL, Yin LX. Effects of intradialytic resistance exercise on systemic inflammation in maintenance hemodialysis patients with sarcopenia: a randomized controlled trial. International urology and nephrology. 2019;51(8):1415–24. Epub 2019/07/05. doi: 10.1007/s11255-019-02200-7 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Zhao J, Qi Q, Xu S, Shi D. Combined aerobic resistance exercise improves dialysis adequacy and quality of life in patients on maintenance hemodialysis. Clinical nephrology. 2020;93(6):275–82. Epub 2020/04/10. doi: 10.5414/cn110033 . [DOI] [PubMed] [Google Scholar]
  • 38.Xing Y, Qiaohong Z, Yali P. Effect of progressive resistance exercise on exercise ability, nutrition index and sleep quality in maintenance hemodialysis patients. Evidence-based nursing. 2022;8(09):1215–9. [Google Scholar]
  • 39.Sheng K, Zhang P, Chen L, Cheng J, Wu C, Chen J. Intradialytic Exercise in Hemodialysis Patients: A Systematic Review and Meta-Analysis. American journal of nephrology. 2014;40(5):478–90. doi: 10.1159/000368722 [DOI] [PubMed] [Google Scholar]
  • 40.Pellizzaro CO, Thomé FS, Veronese FV. Effect of Peripheral and Respiratory Muscle Training on the Functional Capacity of Hemodialysis Patients. Renal Failure. 2012;35(2):189–97. doi: 10.3109/0886022X.2012.745727 [DOI] [PubMed] [Google Scholar]
  • 41.Matsufuji S, Shoji T, Yano Y, Tsujimoto Y, Kishimoto H, Tabata T, et al. Effect of Chair Stand Exercise on Activity of Daily Living: A Randomized Controlled Trial in Hemodialysis Patients. Journal of Renal Nutrition. 2015;25(1):17–24. doi: 10.1053/j.jrn.2014.06.010 [DOI] [PubMed] [Google Scholar]
  • 42.Johansen KL, Painter PL, Sakkas GK, 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. Journal of the American Society of Nephrology. 2006;17(8):2307–14. doi: 10.1681/asn.2006010034 [DOI] [PubMed] [Google Scholar]
  • 43.Cheema B, Abas H, Smith B, O’Sullivan A, Chan M, Patwardhan A, et al. Randomized controlled trial of intradialytic resistance training to target muscle wasting in ESRD: the Progressive Exercise for Anabolism in Kidney Disease (PEAK) study. American journal of kidney diseases: the official journal of the National Kidney Foundation. 2007;50(4):574–84. Epub 2007/09/29. [DOI] [PubMed] [Google Scholar]
  • 44.Cheema B, Abas H, Smith B, O’Sullivan A, Chan M, Patwardhan A, et al. Progressive exercise for anabolism in kidney disease (PEAK): a randomized, controlled trial of resistance training during hemodialysis. Journal of the American Society of Nephrology: JASN. 2007;18(5):1594–601. Epub 2007/04/06. doi: 10.1681/ASN.2006121329 . [DOI] [PubMed] [Google Scholar]
  • 45.Hannan M, Bronas UG. Barriers to exercise for patients with renal disease: an integrative review. Journal of nephrology. 2017;30(6):729–41. Epub 2017/07/10. doi: 10.1007/s40620-017-0420-z . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Clarke AL, Young HM, Hull KL, Hudson N, Burton JO, Smith AC. Motivations and barriers to exercise in chronic kidney disease: a qualitative study. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association—European Renal Association. 2015;30(11):1885–92. Epub 2015/06/10. doi: 10.1093/ndt/gfv208 . [DOI] [PubMed] [Google Scholar]
  • 47.Fernández-Martín JL, Martínez-Camblor P, Dionisi MP, Floege J, Ketteler M, London G, et al. Improvement of mineral and bone metabolism markers is associated with better survival in haemodialysis patients: the COSMOS study. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association—European Renal Association. 2015;30(9):1542–51. Epub 2015/04/30. doi: 10.1093/ndt/gfv099 . [DOI] [PubMed] [Google Scholar]
  • 48.Regolisti G, Maggiore U, Sabatino A, Gandolfini I, Pioli S, Torino C, et al. Interaction of healthcare staff’s attitude with barriers to physical activity in hemodialysis patients: A quantitative assessment. PloS one. 2018;13(4):e0196313. Epub 2018/04/28. doi: 10.1371/journal.pone.0196313 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Chen JL, Godfrey S, Ng TT, Moorthi R, Liangos O, Ruthazer R, et al. Effect of intra-dialytic, low-intensity strength training on functional capacity in adult haemodialysis patients: a randomized pilot trial. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association—European Renal Association. 2010;25(6):1936–43. Epub 2010/01/27. doi: 10.1093/ndt/gfp739 . [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 50.Esteve Simo V, Junqué Jiménez A, Moreno Guzmán F, Carneiro Oliveira J, Fulquet Nicolas M, Pou Potau M, et al. Benefits of a low intensity exercise programme during haemodialysis sessions in elderly patients. Nefrologia: publicacion oficial de la Sociedad Espanola Nefrologia. 2015;35(4):385–94. Epub 2015/08/27. doi: 10.1016/j.nefro.2015.03.006 . [DOI] [PubMed] [Google Scholar]
  • 51.Johansen KL, Painter PL, Sakkas GK, 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. Journal of the American Society of Nephrology: JASN. 2006;17(8):2307–14. Epub 2006/07/11. doi: 10.1681/ASN.2006010034 . [DOI] [PubMed] [Google Scholar]
  • 52.Song WJ, Sohng KY. Effects of progressive resistance training on body composition, physical fitness and quality of life of patients on hemodialysis. Journal of Korean Academy of Nursing. 2012;42(7):947–56. Epub 2013/02/05. doi: 10.4040/jkan.2012.42.7.947 . [DOI] [PubMed] [Google Scholar]
  • 53.Pellizzaro CO, Thomé FS, Veronese FV. Effect of peripheral and respiratory muscle training on the functional capacity of hemodialysis patients. Renal failure. 2013;35(2):189–97. Epub 2012/12/04. doi: 10.3109/0886022X.2012.745727 . [DOI] [PubMed] [Google Scholar]

Decision Letter 0

Yuri Battaglia

22 May 2024

PONE-D-24-02321Summary of the best evidence for resistance exercise in maintenance hemodialysis patientsPLOS ONE

Dear Dr. Ma,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Jul 06 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Yuri Battaglia

Academic Editor

PLOS ONE

Journal Requirements:

1. When submitting your revision, we need you to address these additional requirements.

Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at 

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and 

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

2. Please identify your study as "systematic review" in the title of your manuscript.

3. We suggest you thoroughly copyedit your manuscript for language usage, spelling, and grammar. If you do not know anyone who can help you do this, you may wish to consider employing a professional scientific editing service. 

The American Journal Experts (AJE) (https://www.aje.com/) is one such service that has extensive experience helping authors meet PLOS guidelines and can provide language editing, translation, manuscript formatting, and figure formatting to ensure your manuscript meets our submission guidelines. Please note that having the manuscript copyedited by AJE or any other editing services does not guarantee selection for peer review or acceptance for publication. 

Upon resubmission, please provide the following:

The name of the colleague or the details of the professional service that edited your manuscript

A copy of your manuscript showing your changes by either highlighting them or using track changes (uploaded as a *supporting information* file)

A clean copy of the edited manuscript (uploaded as the new *manuscript* file)

4. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match. 

When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section.

5. We note that your Data Availability Statement is currently as follows: All relevant data are within the manuscript and its Supporting Information files.

Please confirm at this time whether or not your submission contains all raw data required to replicate the results of your study. Authors must share the “minimal data set” for their submission. PLOS defines the minimal data set to consist of the data required to replicate all study findings reported in the article, as well as related metadata and methods (https://journals.plos.org/plosone/s/data-availability#loc-minimal-data-set-definition).

For example, authors should submit the following data:

- The values behind the means, standard deviations and other measures reported;

- The values used to build graphs;

- The points extracted from images for analysis.

Authors do not need to submit their entire data set if only a portion of the data was used in the reported study.

If your submission does not contain these data, please either upload them as Supporting Information files or deposit them to a stable, public repository and provide us with the relevant URLs, DOIs, or accession numbers. For a list of recommended repositories, please see https://journals.plos.org/plosone/s/recommended-repositories.

If there are ethical or legal restrictions on sharing a de-identified data set, please explain them in detail (e.g., data contain potentially sensitive information, data are owned by a third-party organization, etc.) and who has imposed them (e.g., an ethics committee). Please also provide contact information for a data access committee, ethics committee, or other institutional body to which data requests may be sent. If data are owned by a third party, please indicate how others may request data access.

6. PLOS requires an ORCID iD for the corresponding author in Editorial Manager on papers submitted after December 6th, 2016. Please ensure that you have an ORCID iD and that it is validated in Editorial Manager. To do this, go to ‘Update my Information’ (in the upper left-hand corner of the main menu), and click on the Fetch/Validate link next to the ORCID field. This will take you to the ORCID site and allow you to create a new iD or authenticate a pre-existing iD in Editorial Manager. Please see the following video for instructions on linking an ORCID iD to your Editorial Manager account: https://www.youtube.com/watch?v=_xcclfuvtxQ

7. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Partly

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: N/A

Reviewer #2: N/A

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: Yes

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The paper "Summary of the best evidence for resistance exercise in maintenance hemodialysis

patients" offers an interesting aim. However, the better effect of the resistance exercise compared to the aerobic exercise is described only in the introduction. " Specifically, when it comes

to enhancing the muscle function of MHD patients, resistance exercise training has been

shown to be more effective than aerobic exercise in promoting muscle gain[8],

increasing muscle strength[9], enhancing upper limb grip strength[10], physical

activity[11], improving systemic inflammatory responses[12], alleviating anxiety,

depression, and other negative emotions, enhancing sleep quality, and improving

overall quality of life[13,14]"

The references in this same paragraph are not completely available and verifiable [i.e. ref. 8].

In the 8 evidence is reported the term "exercise" twice. Please correct.

Most of the "content of evidence" show the importance of both resistance and aerobic exercise. So, the authors should modify the conclusion, explaining that most of the analized trials was based on combined exercise training. So, even if some evidences show a good effect on the muscle strenght, "Future research should strive for larger-scale, multi-center, longitudinal studies to validate these findings and further contribute to the field."

Reviewer #2: In their review summarizing the evidence regarding the effects of, and the indications to implementing resistance exercise training in patients on maintenance hemodialysis (MHD), the Authors examined a number of guidelines, expert consensus documents, systematic reviews, and randomized controlled trials (RCT). They evaluated the evidence across 9 items, including target population, pre-exercise assessment, exercise frequency, exercise intensity, exercise duration, exercise type, exercise benefits, and exercise precautions.

I have the following comments.

Major points

1) A remarkable fraction of the examined literature stems from Chinese studies. Additional RCT that the Authors did not, but instead should, include in their review are the following: 1) de Lima MC, Cicotoste C de L, Cardoso Kda S, et al. Effect of exercise performed during hemodialysis: strength versus aerobic. Ren Fail 2013; 35:697-704. 2) Pellizzaro CO, Thomé FS, Veronese FV. Effect of peripheral and respiratory muscle training on the functional capacity of hemodialysis patients. Ren Fail. 2013; 35:189-197. 3) Matsufuji S, Shoji T, Yano Y, et al. Effect of chair stand exercise on activity of daily living: a randomized controlled trial in hemodialysis patients. J Ren Nutr 2015; 25:17-24. 4) Thompson S, Klarenbach S, Molzahn A, et al. Randomised factorial mixed method pilot study of aerobic and resistance exercise in haemodialysis patients: DIALY-SIZE! BMJ Open. 2016; 6:e012085. 5) Johansen KL, et al. 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 2006; 17:2307-2314Additional systematic reviews that should also be included are as follows: 1) Sheng K, Zhang P, Chen L, et al. Intradialytic exercise in hemodialysis patients: a systematic review and meta-analysis. Am J Nephrol 2014; 40:478-490. 2) Afsar B, Siriopol D, Aslan G, et al. The impact of exercise on physical function, cardiovascular outcomes and quality of life in chronic kidney disease: a systematic review. Int Urol Nephrol 2018; 50:885-904. 3) Zhao Q-G, Zhang H-R, Wen X, et al. Exercise interventions on patients with end-stage renal disease: a systematic review. Clin Rehab 2019; 33:147-156. 4) Clarkson MJ, Bennett PN, Fraser SF, Warmington SA. Exercise interventions for improving objective physical function in patients with end-stage kidney disease on dialysis: a systematic review and meta-analysis. Am J Physiol Renal Physiol. 2019; 316:F856-F872

2) Some more details should be provided regarding details of resistance exercise protocols. In most training programmes the patients performed 2-3 sets of 8-15 repetitions of joint flexion/extension during the dialysis session or off-dialysis, mainly with free weights or elastic bands, targeting several muscle groups, at moderate-to-vigorous intensity based on either a fraction (60%-80%) of 1 to 3 repetition maximum or the rating of perceived exertion (RPE) on the traditional or modified Borg scale. Muscle strength was generally assessed by dynamometry, while methods for muscle mass evaluation included measurement of muscle cross-sectional area by computed tomographyor magnetic resonance imaging, as well as simple measurement of mid-arm and/or mid-thigh circumference (Cheema B, et al., J Am Soc Nephrol 2007; 18:1594-1601. Johansen KL, et al. J Am Soc Nephrol 2006; 17:2307-2314)

3) Due to a remarkable heterogeneity in the indices of muscle strength across trials, the generalization of results is somewhat problematic. Five studies (Cheema B, et al, J Am Soc Nephrol 2007; 18:1594-1601. Johansen KL, et al. J Am Soc Nephrol 2006; 17:2307-2314. Chen JL, et al. Nephrol Dial Transplant 2010; 25:1936-1943. Song WJ & Sohng KY, J Korean Acad Nurs 2012; 42:947-956. Esteve Simó V, et al. Nephron Clin Pract 2014; 128:387-393) found positive effects of resistance training on direct measures of either lower or upper limb muscle strength, while two studies (Thompson S et al, BMJ Open. 2016; 6:e012085. Chen JL et al, Nephrol Dial Transplant 2010; 25:1936-1943.) targeted a summary index of strength and balance (i.e., SPPB score) and reported an improvement. One trial (Johansen KL et al. J Am Soc Nephrol 2006; 17:2307-2314) found no significant change in gait speed or STS test. Three trials (Esteve Simó V et al. Nephron Clin Pract 2014; 128:387-393. Pellizzaro CO et al. Ren Fail. 2013; 35:189-197. Matsufuji S, et al. J Ren Nutr 2015; 25:17-24) also investigated the effects of resistance training on walking capacity, as assessed by 6MWD, with two reporting an improvement (Pellizzaro CO et al. Ren Fail. 2013; 35:189-197. Matsufuji S et al. J Ren Nutr 2015; 25:17-24) and one (Matsufuji S et al. J Ren Nutr 2015; 25:17-24) showing no significant change.

4) As to the safety of resistance training in hemodialyzed patients, few cases of traumatic muscular damage or damage to the vascular access were reported (Thompson S et al. BMJ Open. 2016; 6:e012085., Cheema Bet al. J Am Soc Nephrol 2007; 18:1594-1601.

5) A number of physical, psychological or logistic barriers to exercise have been identified in dialysis patients, which should be mentioned (Hannan M, Bronas UG. J Nephrol 2017; 30:729-741). Nephrologists should devote a special effort to target patients’ barriers to exercise (Clarke AL et al. Nephrol Dial Transplant 2015; 30:1885-1892), as a proactive attitude of healthcare staff in dialysis center may help promoting a significant improvement in patients’ levels of physical activity (Regolisti G, et al. PLoS One. 2018; 13:e0196313). Ideally, patient counseling and exercise prescription in dialysis patients should be based on a multidisciplinary team-based approach, in which the referring nephrologist should be supported by other healthcare professionals (e.g., physiotherapists and exercise physiologists.

6) Patients should be cautioned against performing heavy resistance exercise using the arm with the vascular access. Preferentially, exercise training should be delivered during the first two hours of the dialysis session, to avoid the exhaustion facilitated by a greater net ultrafiltration volume reached in the last 1-2 hours of the session.

7) Lack of standardization of the duration, timing and protocols of exercise training programmes in patients with ESKD on maintenance HD, together with highly heterogeneous endpoints in published studies, represent a major source of variability in reported outcomes. Thus, a consensus on the adoption of uniform protocols and endpoints is strongly needed. Furthermore, a standardization is necessary with respect to the methods used to explore physical function and HRQoL. Please see Regolisti G et al, Curr Opin Clin Nutrit Metabol Care 2020; 23:181-189)

8) Finally, with respect to the prescription of exercise training, a further useful paper is that by Smart NA, et al. Exercise & Sport Science Australia (ESSA) position statement on exercise and chronic kidney disease. J Sci Med Sport 2013; 16:406-411.

9) The Conclusions are largely a repetition of Paragraph 4.2. They should be shortened and be more focused

Minor points

1) Some editing of the English text is needed. A few examples include (but are not limited to): Literature typology (Type of study); Master consensual (Expert consensus?) Systems evaluation (Systematic Review)

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: maria amicone

Reviewer #2: No

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2024 Dec 30;19(12):e0309798. doi: 10.1371/journal.pone.0309798.r002

Author response to Decision Letter 0


10 Jul 2024

We have taken your feedback seriously and have made the necessary revisions to ensure that all references, including [8] and [9], are now correctly cited and verifiable. We have replaced the non-verifiable references with ones that are accessible and relevant to the statements made in the text.

We have carefully reviewed the section and have made the necessary correction to avoid the repetition of the term "exercise." We have rephrased the sentence to ensure that it conveys the intended meaning without any redundancy.

The revised sentence now reads as follows:

It is recommended that MHD patients under the supervision of healthcare personnel before exercise exercise capacity test including cardiorespiratory endurance, muscular strength, muscular endurance, flexibility, etc., the test should be arranged on non-dialysis days; attention should be paid to avoid the measurement of blood pressure in the limb on the side of the inner fistula; commonly used methods of simple exercise capacity test are 6 min walking test, sit-to-stand test, and get-up-and-walk test to ensure the safety of the exercise process[6,26].

First and foremost, we would like to express our gratitude for your insightful comments and suggestions. We fully concur with your observation that the "content of evidence" in our study underscores the significance of both resistance and aerobic exercises. In response to your feedback, we have revised our conclusion to reflect the fact that the majority of the trials analyzed in our study were based on combined exercise training.

We acknowledge that while our findings indicate positive effects on muscle strength, it is imperative for future research to validate these results and further contribute to the field. To this end, we have added the following statement to our conclusion:

“Given the findings of this study, we recommend that future researchers design and conduct larger-scale, multi-center, longitudinal studies to validate our results and further explore the long-term impacts of combined resistance and aerobic exercises on muscle strength and other health indicators. Such research will provide deeper insights and contribute to the development of evidence-based exercise programs.”

We believe that with these revisions, our conclusions are more accurate and comprehensive, and they also provide a clear direction for future studies.

We appreciate your feedback and look forward to any further guidance you may provide.

16.The time of exercise was during or two hours before dialysis;

17. The target duration is 30-60 min per exercise session, which can be divided into sessions depending on the individual MHD patients, the duration of exercise intervention should be longer than 6 month;

19. Common resistance exercise programmes include: stretch pullers or elastic bandages, lifting dumbbells, sit-ups, push-ups, sand bags, leg weight, chair stand exercise etc.;

20. Mainly low-to-moderate load lower extremity exercises with 1 to 3 sets of 8 to 15 repetitions per set

27. Exercise can improve fatigue, anxiety, depression, physical activity, and QOL in patients with end-stage renal disease;

28. Intradialytic exercise can increase the solute removal, for exercise may increase the blood flow to muscle, and greater toxic agents can be removed by the dialyzers;

29.The exercise program of peripheral muscle resistance can increase the volume of anti-fatigue muscle fibers, the muscle's capture and transport of oxygen;

33.The most common risk of intradialytic exercise is musculoskeletal injury, while the most serious risk is cardiovascular events, such as arrhythmia, myocardial infarction, and hypertension;

34.Treatment with nanrodone caprate during weekly lower limb resistance exercise training is safe and well tolerated.

9.A General Electric High Speed CTi Scanner was used to perform CT scans on the nondominant mid-thigh of participants on a nondialysis day. These scans measured the thigh muscle cross-sectional area (CSA) and attenuation to assess muscle quantity and quality, respectively. Lower muscle attenuation values indicate better muscle quality due to less intramuscular lipid infiltration.

12. Exercise during routine haemodialysis was performed under the direct supervision of an exercise physiologist, with 8-15 sets of joint flexion and extension exercises 3 times per week for 12 weeks.

15. Peak force (kg) of the knee extensors, hip abductors, and triceps was measured bilaterally in triplicate with the best score recorded, using an isometric digital dynamometer (Chatillon CSD 200 Dynamometer; AMETEK, Paoli, PA; coefficient of variability 9.4%). These individual strength measures were summed to create a total strength measure.

In “discussion”,we had showed that:Current evidence suggests that resistance training had a positive impact on muscle strength, balance, and functional capacity in maintenance hemodialysis patients, though there is notable heterogeneity across studies due to variations in assessment indices, patient characteristics, and training protocols. Most studies report improvements in direct measures of muscle strength, while some also demonstrate gains in summary indices of strength and balance. However, not all studies consistently show improvements in gait speed, STS test, or walking capacity as assessed by the 6-Minute Walk Distance (6MWD). These discrepancies highlight the need for standardized assessment methods and personalized training programs in future research to optimize the benefits and safety of resistance exercise for MHD patients. Ultimately, integrating resistance exercise into the daily routine of these patients holds promise for enhancing their overall quality of life.

In the safety of resistance in haemodialysis patients, no cases of cannula dislodgement during exercise were observed in any patient during the trial.

In light of the reviewer's feedback, this article will now delve into the various physical, psychological, and logistical barriers that impede exercise in hemodialysis patients, as identified in the study by Hannan and Bronas (2017). It is imperative for nephrologists to address these barriers proactively, as emphasized by Clarke et al. (2015), recognizing that a healthcare staff's positive approach in dialysis centers can significantly enhance patients' physical activity levels, as demonstrated by Registrosti et al. (2018). To achieve optimal outcomes, patient counseling and exercise prescription in the context of hemodialysis should ideally be conducted through a multidisciplinary team-based approach. In this collaborative framework, the referring nephrologist should be complemented by the expertise of other healthcare professionals, including physiotherapists and exercise physiologists, to ensure a comprehensive and effective exercise regimen tailored to the individual needs of each patient.

According to the suggests that about “the safety precautions for hemodialysis training”

in "discussion 4.2".

“To guarantee both safety and efficacy during the dialysis process, we advise against the use of the arm equipped with vascular access for strenuous resistance exercises. Instead, we suggest that exercise regimens be scheduled during the initial two hours of the dialysis session. This strategic timing is intended to circumvent the exhaustion that may arise from the increased net ultrafiltration volume typically observed in the final 1-2 hours of the dialysis treatment.”

Thank you for your insightful comments and for highlighting the critical need for standardization in the study of exercise training programs for patients with End-Stage Kidney Disease (ESKD) on maintenance hemodialysis. Your observation regarding the lack of uniformity in protocols, timing, and endpoints is well-taken and is indeed a significant factor contributing to the variability in reported outcomes.

In light of your feedback and the reference to the work by Regolisti G et al., we have taken the following steps to address these concerns in our manuscript:

1. Acknowledgment of Variability: We have added a section in the discussion acknowledging the variability in exercise training programs and the impact of this variability on study outcomes.

2. Call for Standardization: We have emphasized the need for consensus on uniform protocols and endpoints in future research to ensure comparability of results across studies.

3. Recommendations for Future Research: We have included specific recommendations for standardizing the methods used to assess physical function and Health-Related Quality of Life (HRQoL), drawing from the insights provided in the referenced article and other relevant literature.

4. Updated Discussion: The discussion section has been revised to reflect the importance of standardization and to provide a more in-depth analysis of how these factors may influence the interpretation of findings in the context of ESKD and maintenance hemodialysis.

The revised text now reads as follows:

"The heterogeneity in exercise training protocols, timing, and endpoints, as noted by the reviewer and highlighted in the work of Regolisti G et al. (Current Opinion in Clinical Nutrition and Metabolic Care, 2020; 23:181-189), introduces considerable variability in the outcomes reported across studies. This underscores the urgent need for a consensus on standardized protocols and endpoints to enhance the validity and generalizability of research findings in this field. Moreover, there is a clear necessity for standardized methods to assess physical function and HRQoL, which will provide a solid foundation for future comparative effectiveness studies."

We trust that these revisions align with the expectations for scientific rigor and contribute to the advancement of research in exercise training for ESKD patients on maintenance hemodialysis.

We are grateful for the opportunity to enhance our manuscript based on your expert guidance and look forward to any further suggestions you may have.

Thank you for your valuable feedback and for bringing to our attention the paper by Smart NA, et al., titled "Exercise & Sport Science Australia (ESSA) position statement on exercise and chronic kidney disease," published in the Journal of Science and Medicine in Sport, 2013; 16:406-411.

We appreciate the suggestion to include this paper in our review, as it provides a comprehensive and authoritative perspective on the prescription of exercise training for individuals with chronic kidney disease.

To address this, we have taken the following steps:

1. Literature Review Update: We have reviewed the paper by Smart NA, et al., and have identified key points and recommendations relevant to our study's focus on exercise training for patients with End-Stage Kidney Disease (ESKD) on maintenance hemodialysis.

2. Incorporation into Manuscript: We have incorporated relevant findings and guidelines from the ESSA position statement into our discussion section to provide additional context and support for our conclusions regarding the prescription of exercise training.

3. Citation Addition: The reference to the paper by Smart NA, et al., has been added to our bibliography to ensure proper academic credit and to guide readers to this important resource.

The revised text now includes a new paragraph that reads as follows:

"In line with the recommendations from the Exercise & Sport Science Australia (ESSA) position statement on exercise and chronic kidney disease (Smart NA, et al., 2013), our findings underscore the importance of a tailored approach to exercise prescription for individuals with ESKD. The ESSA guidelines emphasize the need for individualized assessment and the consideration of patient-specific factors, which align with our study's approach to optimizing exercise training programs for this population."

We believe that the inclusion of this reference strengthens the manuscript and provides additional support for our recommendations on exercise training prescription for patients with ESKD.

We are grateful for the opportunity to enhance our work with this important reference and hope that the manuscript now meets the high standards of the journal.

Thank you for your valuable feedback on our manuscript. We have taken your suggestions to heart and have made the following revisions to address the points raised:

Major Point: Conclusions

We acknowledge that the original conclusions were repetitive of Paragraph 4.2. In response to your guidance, we have significantly condensed the conclusions, ensuring they are succinct and focused on the key takeaways from our research. We have removed redundant information and have emphasized the novel contributions and implications of our findings.

Minor Points:

Literature Typology: We have corrected "Literature typology" to "Type of study" to better reflect the intended meaning and to align with standard academic terminology.

Master Consensual: The term "Master consensual" has been revised to "Expert consensus" to accurately convey the concept of a collective agreement among experts in the field.

Systems Evaluation: We have replaced "Systems evaluation" with "Systematic Review" to ensure that the term is consistent with the common nomenclature used in scientific literature to describe a thorough and structured synthesis of existing research.

Additionally, we have undertaken a comprehensive language review of the entire manuscript to correct any grammatical errors and improve the overall readability and flow of the text. We have also enlisted the help of a professional English language editor to ensure that the manuscript meets the highest standards of English usage in academic writing.

We believe that these revisions have enhanced the quality and clarity of our manuscript and have addressed the concerns raised by the review process.

We appreciate the opportunity to refine our work and hope that the manuscript is now in a form that is acceptable for publication.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0309798.s009.docx (27.1KB, docx)

Decision Letter 1

Yuri Battaglia

20 Aug 2024

Systematic Review of the Best Evidence for Resistance Exercise in Maintenance Hemodialysis Patients

PONE-D-24-02321R1

Dear Dr. Ma,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. Please make sure your user information is up-to-date by logging into Editorial Manager at Editorial Manager® and clicking the ‘Update My Information' link at the top of the page. If you have any questions relating to publication charges, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Yuri Battaglia

Academic Editor

PLOS ONE

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: N/A

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #2: In the revised version of their manuscript, the Authors have appropriately addressed all of the criticisms I had raised concerning the original version.

I have no further comments.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

Reviewer #2: Yes: Giuseppe Regolisti

**********

Acceptance letter

Yuri Battaglia

23 Oct 2024

PONE-D-24-02321R1

PLOS ONE

Dear Dr. Ma,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Prof. Yuri Battaglia

Academic Editor

PLOS ONE

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Checklist. PRISMA 2020 checklist.

    (DOCX)

    pone.0309798.s001.docx (23KB, docx)
    S2 Checklist. PRISMA 2020 flow diagram for new systematic reviews which included searches of databases and registers only.

    (DOCX)

    pone.0309798.s002.docx (50.9KB, docx)
    S1 Fig. Flow chart.

    (DOCX)

    pone.0309798.s003.docx (114.3KB, docx)
    S1 Table. Quality assessment results of guidelines.

    (DOCX)

    pone.0309798.s004.docx (11.9KB, docx)
    S2 Table. Quality assessment results of expert consensus.

    (DOCX)

    pone.0309798.s005.docx (12KB, docx)
    S3 Table. Quality assessment results of systematic reviews.

    (DOCX)

    pone.0309798.s006.docx (14.8KB, docx)
    S4 Table. Quality assessment results of randomized controlled trials.

    (DOCX)

    pone.0309798.s007.docx (13.4KB, docx)
    S5 Table. All research information forms.

    (XLSX)

    pone.0309798.s008.xlsx (57.2KB, xlsx)
    Attachment

    Submitted filename: Response to Reviewers.docx

    pone.0309798.s009.docx (27.1KB, docx)

    Data Availability Statement

    All relevant data are within the paper and its Supporting information files.


    Articles from PLOS ONE are provided here courtesy of PLOS

    RESOURCES