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Cited by 94Nutrition and Health in AgingFrailty in Older AdultsMuscle metabolism and nutrition

Effects of Protein Supplementation Combined with Exercise Intervention on Frailty Indices, Body Composition, and Physical Function in Frail Older Adults

Open access
Liao, Chun-De, Lee, Pi-Hsia, Hsiao, Dun-Jen, Huang, Shih-Wei, Tsauo, Jau-Yih, Chen, Hung-Chou, Liou, Tsan-Hon·2018·Nutrients
DOI 10.3390/nu10121916PMC PMC6315527
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Abstract

Aging poses a high risk of lean mass loss, which can be effectively improved through resistance exercise training (RET), or multicomponent exercise training (MET) as well as nutrition supplementation, such as protein supplementation (PS). This study investigated the effects of PS plus exercise training on frail older individuals. A comprehensive search of online databases was performed to identify randomized controlled trials (RCTs) that reported the efficacy of PS combined with RET or MET in frail older individuals. The included RCTs were analyzed through a meta-analysis and risk-of-bias assessment. We finally included 22 RCTs in the meta-analysis, with a mean (range/total) Physiotherapy Evidence Database score of 6.7 (4–9/10). PS plus exercise training significantly improved the frailty status (odds ratio = 2.77; p = 0.006), lean mass (standard mean difference (SMD) = 0.52; p < 0.00001), leg strength (SMD = 0.37; p < 0.00001), and walking speed (SMD = 0.32; p = 0.002). Subgroup analyses revealed that PS plus MET exert significant effects on frailty indices, whereas PS plus RET further improves lean mass. Our findings suggest that PS plus RET as well as MET is effective in improving frailty status, lean mass, muscle strength, and physical mobility in frail older individuals.

AI snapshot

Written from the paper’s full text.

TL;DR

This systematic review and meta-analysis of 22 RCTs found that protein supplementation combined with exercise training improved frailty status, lean mass, leg strength, and walking speed in frail older adults. Subgroup analyses suggested protein plus multicomponent exercise training improved frailty indices, whereas protein plus resistance exercise training further improved lean mass.

Key findings

  • Protein supplementation plus exercise training significantly improved frailty status (OR = 2.77, 95% CI 1.34–5.74, p = 0.006), lean mass (SMD = 0.52, 95% CI 0.33–0.71, p < 0.00001), leg strength (SMD = 0.37, 95% CI 0.23–0.51, p < 0.00001), and walking speed (SMD = 0.32, 95% CI 0.05–0.59, p = 0.02).
  • Treatment success rates were higher for reducing fall events (OR = 3.36, 95% CI 1.21–9.34, p = 0.02) and improving chair-stand performance (OR = 1.86, 95% CI 1.03–3.37, p = 0.04).
  • Subgroup analyses showed that protein supplementation plus multicomponent exercise training exerted significant effects on frailty indices, whereas protein supplementation plus resistance exercise training significantly improved lean body mass (SMD = 0.61, 95% CI 0.35–0.88, p < 0.00001) and appendicular skeletal muscle mass (SMD = 0.75, 95% CI 0.32–1.18, p = 0.0006).
  • High-dose supplementation appeared to exert significant effects on lean body mass (SMD = 0.71, p < 0.00001), whereas protein plus multicomponent exercise training and low-dose supplementation did not.

Methods

  • Systematic review and meta-analysis of randomized controlled trials, registered at PROSPERO (CRD42018109176), following PRISMA guidelines.
  • Searched PubMed, EMBASE, Cochrane Library, PEDro, China Knowledge Resource Integrated Database, and Google Scholar; included 22 RCTs published 1994–2017 with 2113 frail older participants (1525 women), mean age 82.3 (SD 5.1) years.
  • Included trials tested protein supplementation plus resistance exercise training or multicomponent exercise training versus placebo, protein supplementation alone, exercise alone, or no intervention; outcomes included frailty indices, body composition, leg strength, and physical mobility, analyzed with fixed- or random-effects models using SMD or OR, with PEDro risk-of-bias assessment and subgroup analyses.

Limitations

  • The paper states that varying protein supplementation protocols (source, amount, timing) and exercise regimes made it difficult to endorse a definite conclusion about any specific type of protein or exercise training.
  • The paper states that some included RCTs had small sample sizes, some participants had impaired cognition, some trials had attendance/compliance below 80% or did not report compliance, and subgroup analyses had inadequate statistical power; sex-specific analyses could not be performed.
  • Evident from the text: heterogeneity was substantial for walking speed (I² = 75%) and moderate for lean body mass (I² = 51%), and several subgroup analyses included fewer than six RCTs, which the authors note should be cautiously interpreted.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.3390/nu10121916

Cites

93 of 93 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 73 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    Subgroup analyses revealed that PS plus MET exerts significant effects on frailty indices.

    “Subgroup analyses revealed that PS plus MET exert significant effects on frailty indices, whereas PS plus RET further improves lean mass.”
    Quote in the paperSubstantial claim
  • Findingown data

    PS plus exercise training significantly improved frailty status (OR = 2.77; p = 0.006) in frail older individuals.

    “PS plus exercise training significantly improved the frailty status (odds ratio = 2.77; p = 0.006)”
    Quote in the paperSubstantial claim
  • Findingown data

    PS plus exercise training significantly improved walking speed (SMD = 0.32; p = 0.002) in frail older individuals.

    “walking speed (SMD = 0.32; p = 0.002)”
    Quote in the paperSubstantial claim
  • Findingown data

    Subgroup analyses revealed that PS plus RET further improves lean mass.

    “Subgroup analyses revealed that PS plus MET exert significant effects on frailty indices, whereas PS plus RET further improves lean mass.”
    Quote in the paperSubstantial claim
  • Findingown data

    PS plus exercise training significantly improved leg strength (SMD = 0.37; p < 0.00001) in frail older individuals.

    “leg strength (SMD = 0.37; p < 0.00001)”
    Quote in the paperSubstantial claim
  • May combine two claims. 26
  • Classified as probably not a substantial claim. 12

  • May combine two claims.

    Findingown data

    The meta-analysis included 22 RCTs, with a mean PEDro score of 6.7 (range 4-9/10).

    “We finally included 22 RCTs in the meta-analysis, with a mean (range/total) Physiotherapy Evidence Database score of 6.7 (4–9/10).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    PS plus exercise training had significant medium-term (SMD = 0.64, p = 0.003; LoE moderate) and long-term (SMD = 0.51, p = 0.002; LoE strong) effects on lean body mass as well as appendicular lean mass.

    “The results of meta-analyses showed significant medium-term (SMD 0.64, p = 0.003; LoE, moderate) and long-term (SMD 0.51, p = 0.002; LoE, strong) effects of PS plus exercise training on lean body mass as well as appendicular lean mass”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Subgroup analyses showed that all factors generally exerted no effects on subgroup heterogeneity for leg strength and mobility (all p > 0.05), except significant subgroup differences between participant types (p = 0.01, I2 = 83.2%) and population areas (p = 0.002, I2 = 84.5%) for leg strength.

    “The results of subgroup analyses (Table 5) showed that all factors generally exerted no effects on subgroup heterogeneity for leg strength and mobility (all p > 0.05), except that significant subgroup differences in heterogeneity between different participant types (p = 0.01, I2 = 83.2%) and population areas (p = 0.002, I2 = 84.5%) were observed for leg strength.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Significant effects in favor of PS plus exercise training on frailty indices were noted at all follow-up durations, except that conflicting effects were identified for physical activity during all follow-up durations.

    “Generally, significant effects in favor of PS plus exercise training on frailty indices were noted at all follow-up durations, except that conflict effects could be identified in physical activity during all follow-up durations.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Egger's linear regression test indicated no evidence of obvious reporting bias among the RCTs for handgrip strength (t = 0.06, p = 0.95), walking speed (t = −0.07, p = 0.91), and lean body mass (t = −0.76, p = 0.48).

    “Egger’s linear regression test for handgrip strength also indicated no evidence of obvious reporting bias among the RCTs (t = 0.06, p = 0.95); similar results were obtained for walking speed (t = −0.07, p = 0.91) and lean body mass (t = −0.76, p = 0.48).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Subgroup analyses showed that study methodological quality, participant type, population area, control type, supplementation dose, exercise training type, and intervention duration had no effect on subgroup heterogeneity for all frailty indices (all p > 0.05), except significant subgroup differences for whole body mass (p = 0.03, I2 = 78.2%) and walking speed (p = 0.006, I2 = 80.8%).

    “The results of subgroup analyses (Table 3) showed that study methodological quality, participant type, population area, control type, supplementation dose, exercise training type, and intervention duration had no effect on subgroup heterogeneity for all frailty indices (all p > 0.05), except that significant subgroup differences in heterogeneity were observed between different supplementation dose”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    Both PS plus RET and PS plus MET exhibited significant effects on leg strength (SMD = 0.37, 95% CI 0.04-0.07, p = 0.03; I2 = 57% and SMD = 0.37, 95% CI 0.17-0.58, p = 0.0004; I2 = 24%, respectively); similar results were observed in chair stand and timed up-and-go performances.

    “A subgroup analysis of exercise training type revealed that both PS plus RET and PS plus MET exhibited significant effects on leg strength with an SMD of 0.37 (95% CI: 0.04–0.07, p = 0.03; I2 = 57%) and 0.37 (95% CI: 0.17–0.58, p = 0.0004; I2 = 24%), respectively; similar results were observed in chair stand and timed up-and-go performances.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    High-dose supplementations appeared to exert significant effects on lean body mass (SMD = 0.71, p < 0.00001; LoE strong), whereas PS plus MET and low-dose supplementation did not.

    “High-dose supplementations appeared to exert significant effects on lean body mass with an SMD of 0.71 (p < 0.00001; LoE, strong), whereas PS plus MET and low-dose supplementation did not.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Forest plots for physical function measures demonstrated a statistically significant effect in favor of PS plus exercise training (all p < 0.05; LoE strong) with the exception of ADLs.

    “Forest plots for all physical function measures demonstrated a statistically significant effect in favor of PS plus exercise training (all p < 0.05; LoE, strong) with exception of the ADLs”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Subgroup analyses showed that all factors generally had no effect on subgroup heterogeneity for lean body mass, appendicular lean mass, and fat mass (all p > 0.05), except significant subgroup differences between exercise types (p = 0.04, I2 = 75.3%) and supplementation doses (p = 0.04, I2 = 76.7%) for lean body mass.

    “The results of subgroup analyses (Table 4) showed that all factors generally had no effect on subgroup heterogeneity for lean body mass, appendicular lean mass, and fat mass (all p > 0.05), except that significant subgroup differences in heterogeneity were observed between different exercise types (p = 0.04, I2 = 75.3%) and supplementation doses (p = 0.04, I2 = 76.7%) for lean body mass.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    PS plus RET exhibited significant effects on lean body mass and appendicular skeletal muscle mass gains (SMD = 0.61, 95% CI 0.35-0.88, p < 0.00001; I2 = 34% and SMD = 0.75, 95% CI 0.32-1.18, p = 0.0006; I2 = 0%, respectively), whereas PS plus MET did not.

    “A subgroup analysis of exercise training type revealed that PS plus RET exhibited significant effects on lean body mass and appendicular skeletal muscle mass gains with an SMD of 0.61 (95% CI: 0.35–0.88, p < 0.00001; I2 = 34%) and 0.75 (95% CI: 0.32–1.18, p = 0.0006; I2 = 0%), respectively, whereas PS plus MET did not”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    Frailty is characterized by muscle weakness and slow walking speed and is closely associated with sarcopenia.

    “Frailty, characterized by muscle weakness and slow walking speed, has been considered to be closely associated with sarcopenia [1,2].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [1] Bernabei, 2014, Frailty, Physical Frailty, Sarcopenia: A New Conceptual Model, Stud. Health Technol. Inform.

      Not checked in the free run.

    • cites [2] Dodds, 2016, Sarcopenia and frailty: New challenges for clinical practice, Clin. Med. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    PS plus RET as well as MET is effective in improving frailty status, lean mass, muscle strength, and physical mobility in frail older individuals.

    “Our findings suggest that PS plus RET as well as MET is effective in improving frailty status, lean mass, muscle strength, and physical mobility in frail older individuals.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Frail persons, especially institutionalized residents, are at high risk of undernutrition and physical inactivity.

    “Because frail persons, especially institutionalized residents, are at a high risk of undernutrition [6] and physical inactivity [7,8]”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [6] Yannakoulia, 2017, Frailty and nutrition: From epidemiological and clinical evidence to potential mechanisms, Metabol. Clin. Exp. source

      Not checked in the free run.

    • cites [7] Rodrigues, 2016, Association of frailty in hospitalized and institutionalized elderly in the community-dwelling, Revista Brasileira de Enfermagem source

      Not checked in the free run.

    • cites [8] Abizanda, 2014, Frailty in INstitutionalized older adults from ALbacete. The FINAL Study: Rationale, design, methodology, prevalence and attributes, Maturitas source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    The study was conducted following PRISMA guidelines.

    “The present study was conducted by following the guidelines recommended by the Preferred Reporting Items for Systematic Reviews and Meta-Analysis [22].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [22] Shamseer, 2015, Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: Elaboration and explanation, BMJ source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    Major findings showed moderate to strong evidence that regardless of follow-up duration, PS plus RET or MET exerted overall significant effects on frailty indices as well as body composition, leg strength, and physical mobility in community-dwelling or institutionalized frail older individuals.

    “The major findings of the present study are summarized in Table 6 which showed moderate to strong evidence that regardless of the follow-up duration, PS plus RET or MET exerted overall significant effects on frailty indices as well as body composition (lean body mass and appendicular lean mass), leg strength, and physical mobility in community-dwelling or institutionalized frail older individuals.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The protocol for this study was registered at PROSPERO (registration number CRD42018109176).

    “The protocol for this study was registered at PROSPERO (registration number: CRD42018109176).”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    PS plus RET yielded greater SMDs for lean body mass and appendicular lean mass compared with PS plus MET, indicating that PS plus RET may have greater efficiency in muscle mass gain than PS plus MET.

    “we also observed that PS plus RET yielded greater SMDs for lean body mass and appendicular lean mass compared with PS plus MET, which was also supported by previous results regarding the intensity of RET for muscle hypertrophy [74] and further indicated that PS plus RET may have greater efficiency in muscle mass gain than PS plus MET did.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [74] Helms, 2016, Application of the Repetitions in Reserve-Based Rating of Perceived Exertion Scale for Resistance Training, Strength Cond. J. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    Levels of evidence for each outcome were graded according to a guideline of evidence synthesis derived from the criteria of van Tulder.

    “We graded the levels of evidence (LoE) for each outcome of interest according to the guideline of evidence synthesis [31] derived from the criteria of van Tulder [32] (Table S2).”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [31] Dorrestijn, 2009, Conservative or surgical treatment for subacromial impingement syndrome? A systematic review, J. Should. Elb. Surg. source

      Not checked in the free run.

    • cites [32] Furlan, 2003, Updated method guidelines for systematic reviews in the cochrane collaboration back review group, Spine source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Incorporating RET into MET is advised as a viable exercise type that can be easily adapted by frail individuals.

    “Therefore, incorporating RET into MET is advised as a viable exercise type that can be easily adapted by frail individuals [15,16].”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [15] Bibas, 2014, Therapeutic interventions for frail elderly patients: Part I. Published randomized trials, Progr. Cardiovasc. Dis. source

      Not checked in the free run.

    • cites [16] Jadczak, 2018, Effectiveness of exercise interventions on physical function in community-dwelling frail older people: An umbrella review of systematic reviews, JBI Database Syst. Rev. Implement Rep. source

      Not checked in the free run.

  • May combine two claims.

    Interpretationown data

    PS plus MET as well as PS plus RET had significant effects on whole body mass, walking speed, and leg strength, indicating that frail older adults responded favorably to PS plus MET in reversing or preventing frail status.

    “the results showed that PS plus MET as well as PS plus RET had significant effects on whole body mass, walking speed, and leg strength, which indicated that frail older adults responded favorably to PS plus MET in reversing or preventing frail status.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Interpretationown data

    The treatment success effects of PS plus exercise on fall events, frailty status, and chair-stand performance were regardless of follow-up duration, participant type, exercise type, and control type.

    “regardless of the follow-up duration, participant type, exercise type, and control type (Figure 2).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The quality of the included trials was assessed using the PEDro quality score to assess risk of bias.

    “The quality of the included trials was assessed using the PEDro quality score to assess the risk of bias.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    Recent systematic reviews summarized synergistic effects of PS and ET on body composition and strength in older individuals, most of which included healthy participants and trials using RET only.

    “Recent systematic reviews have summarized the synergistic effects of PS and ET on body composition and strength in older individuals [15,17,18,19,20], most of which included healthy participants [18,19,20,21] and included trials using RET only [18,19,20,21].”
    Quote in the paperSubstantial claim0 of 6 sources checked
    • cites [15] Bibas, 2014, Therapeutic interventions for frail elderly patients: Part I. Published randomized trials, Progr. Cardiovasc. Dis. source

      Not checked in the free run.

    • cites [17] Cheng, 2018, Systematic review and meta-analysis of the effect of protein and amino acid supplements in older adults with acute or chronic conditions, Br. J. Nutr. source

      Not checked in the free run.

    • cites [18] Colonetti, 2017, Effects of whey protein supplement in the elderly submitted to resistance training: Systematic review and meta-analysis, Int. J. Food Sci. Nutr. source

      Not checked in the free run.

    • cites [19] Finger, 2015, Effects of protein supplementation in older adults undergoing resistance training: A systematic review and meta-analysis, Sports Med. source

      Not checked in the free run.

    • cites [20] Liao, 2017, Effects of protein supplementation combined with resistance exercise on body composition and physical function in older adults: A systematic review and meta-analysis, Am. J. Clin. Nutr. source

      Not checked in the free run.

    • cites [21] Morton, 2018, A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults, Br. J. Sports Med. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    An adequate protein-enriched diet or sufficient PS enhances myofibrillar protein synthesis.

    “an adequate protein-enriched diet or sufficient PS enhances myofibrillar protein synthesis [18]”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [18] Colonetti, 2017, Effects of whey protein supplement in the elderly submitted to resistance training: Systematic review and meta-analysis, Int. J. Food Sci. Nutr. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductown data

    Two reviewers independently searched for articles, screened studies, and extracted data, with disagreements resolved by consensus and arbiters.

    “Two reviewers (C.D.L. and H.C.C.) independently searched for articles, screened studies, and extracted data. Any disagreements between the reviewers were resolved through consensus, with other team members (T.H.L. and D.J.H.) acting as arbiters.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Interpretationown data

    PS plus MET may exert significant effects on frailty indices, whereas PS plus RET further improves muscle mass loss in frail older individuals.

    “Taken together, we conclude that PS plus MET may exert significant effects on frailty indices, whereas PS plus RET further improves muscle mass loss in frail older individuals.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductreasoning

    No limitation was imposed on publication year and language to minimize publication and language bias.

    “No limitation was imposed on the publication year and language to minimize publication and language bias.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A sufficient PS up to 40 g or 1.6 g/kg/d after RET has been believed to augment the effects of resistance training on muscle mass gain in older adults.

    “a sufficient PS up to 40 g or 1.6 g/kg/d after RET has been believed to augment the effects of resistance training on muscle mass gain in older adults [19,21]”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [19] Finger, 2015, Effects of protein supplementation in older adults undergoing resistance training: A systematic review and meta-analysis, Sports Med. source

      Not checked in the free run.

    • cites [21] Morton, 2018, A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults, Br. J. Sports Med. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductcitation

    On the basis of the PEDro score, the methodological quality of the included RCTs was rated as high (≥7/10), medium (4-6/10), and low (≤3/10).

    “On the basis of the PEDro score, the methodological quality of the included RCTs was rated as high (≥7/10), medium (4–6/10), and low (≤3/10) [30].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [30] Briani, 2018, What interventions can improve quality of life or psychosocial factors of individuals with knee osteoarthritis? A systematic review with meta-analysis of primary outcomes from randomised controlled trials, Br. J. Sports Med. source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductcitation

    Several subgroups (such as participant types for lean body mass) included a small number of RCTs less than six, which may not have adequate power for detecting a difference among subgroups; the results of such subgroup analyses should be cautiously interpreted.

    “Several subgroups (such as participant types for lean body mass) included a small number of RCTs less than six, which may not have adequate power for detecting a difference among subgroups [89,90]; the results of such subgroup analyses should be cautiously interpreted.”
    Quote in the paperSubstantial claim0 of 2 sources checked
    • cites [89] Fu, 2011, Conducting quantitative synthesis when comparing medical interventions: AHRQ and the Effective Health Care Program, J. Clin. Epidemiol. source

      Not checked in the free run.

    • cites [90] Borenstein, M., Hedges, L.V., Higgins, J.P.T., and Rothstein, H.R. (2009). Notes on Subgroup Analyses and Meta-Regression. Introduction to Meta-Analysis, John Wiley & Sons. source

      Not checked in the free run.

  • May combine two claims.

    Study design and conductcitation

    We included RCTs with an attendance rate (or compliance) lower than 80% responding to exercise training and protein supplementations; in addition, 6 and 8 of 22 RCTs did not reported compliance to exercise and PS interventions.

    “we included RCTs with an attendance rate (or compliance) lower than 80% responding to exercise training [41,43,51,56,57] and protein supplementations [43]; in addition, 6 and 8 of 22 RCTs did not reported compliance to exercise and PS interventions.”
    Quote in the paperSubstantial claim0 of 5 sources checked
    • cites [41] Beck, 2016, Multidisciplinary nutritional support for undernutrition in nursing home and home-care: A cluster randomized controlled trial, Nutrition source

      Not checked in the free run.

    • cites [43] Bonnefoy, 2003, The effects of exercise and protein-energy supplements on body composition and muscle function in frail elderly individuals: A long-term controlled randomised study, Br. J. Nutr. source

      Not checked in the free run.

    • cites [51] Hofmann, 2016, Effects of elastic band resistance training and nutritional supplementation on muscle quality and circulating muscle growth and degradation factors of institutionalized elderly women: The Vienna Active Ageing Study (VAAS), Eur. J. Appl. Physiol. source

      Not checked in the free run.

    • cites [56] Oesen, 2015, Effects of elastic band resistance training and nutritional supplementation on physical performance of institutionalised elderly—A randomized controlled trial, Exp. Gerontol. source

      Not checked in the free run.

    • cites [57] Rosendahl, 2006, High-intensity functional exercise program and protein-enriched energy supplement for older persons dependent in activities of daily living: A randomised controlled trial, Aust. J. Physiother. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Previous studies regarding PS for older individuals demonstrated conflicted results: some identified effects of PS on muscle mass accretion and strength gain during exercise training in sarcopenic or frail individuals, whereas others concluded that PS provides no additional benefit in trained community-dwelling or institutionalized residents.

    “the previous studies regarding PS for the older individuals demonstrated conflicted results; some authors identified the effects of PS on muscle mass accretion and strength gain during exercise training in sarcopenic or frail individuals [54,58,84,85], whereas others concluded that PS provides no additional benefit in trained community-dwelling or institutionalized residents [44,48,49,56,86]”
    Quote in the paperSubstantial claim0 of 9 sources checked
    • cites [54] Kim, H., Suzuki, T., Kim, M., Kojima, N., Ota, N., Shimotoyodome, A., Hase, T., Hosoi, E., and Yoshida, H. (2015). Effects of exercise and milk fat globule membrane (MFGM) supplementation on body composition, physical function, and hematological parameters in community-dwelling frail Japanese women: A randomized double blind, placebo-controlled, follow-up trial. PLoS ONE, 10. source

      Not checked in the free run.

    • cites [58] Tieland, 2012, Protein supplementation increases muscle mass gain during prolonged resistance-type exercise training in frail elderly people: A randomized, double-blind, placebo-controlled trial, J. Am. Med. Dir. Assoc. source

      Not checked in the free run.

    • cites [84] Cabo, 2016, A Multicomponent Exercise Intervention that Reverses Frailty and Improves Cognition, Emotion, and Social Networking in the Community-Dwelling Frail Elderly: A Randomized Clinical Trial, J. Am. Med. Dir. Assoc. source

      Not checked in the free run.

    • cites [85] Tieland, 2012, Protein supplementation improves physical performance in frail elderly people: A randomized, double-blind, placebo-controlled trial, J. Am. Med. Dir. Assoc. source

      Not checked in the free run.

    • cites [44] Carlsson, 2011, Effects of high-intensity exercise and protein supplement on muscle mass in ADL dependent older people with and without malnutrition: A randomized controlled trial, J. Nutr. Health Aging source

      Not checked in the free run.

    • cites [48] Dirks, 2017, Protein Supplementation Augments Muscle Fiber Hypertrophy but Does Not Modulate Satellite Cell Content During Prolonged Resistance-Type Exercise Training in Frail Elderly, J. Am. Med. Dir. Assoc. source

      Not checked in the free run.

    • cites [49] Fiatarone, 1994, Exercise Training and Nutritional Supplementation for Physical Frailty in Very Elderly People, N. Engl. J. Med. source

      Not checked in the free run.

    • cites [56] Oesen, 2015, Effects of elastic band resistance training and nutritional supplementation on physical performance of institutionalised elderly—A randomized controlled trial, Exp. Gerontol. source

      Not checked in the free run.

    • cites [86] Bonnefoy, 2012, Efficacy of a home-based intervention programme on the physical activity level and functional ability of older people using domestic services: A randomised study, J. Nutr. Health Aging source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Previous systematic reviews have demonstrated nonsignificant effects on changes in body weight, muscle mass, muscle strength, and physical mobility in response to PS plus RET among older adults who mostly were healthy or nonfrail.

    “Previous systematic reviews have demonstrated nonsignificant effects on changes in body weight [21,71,87], muscle mass [19,87], muscle strength [19], and physical mobility [20] in response to PS plus RET among older adults who mostly were healthy or nonfrail.”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [21] Morton, 2018, A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults, Br. J. Sports Med. source

      Not checked in the free run.

    • cites [71] Hidayat, 2018, Effects of milk proteins supplementation in older adults undergoing resistance training: A meta-analysis of randomized control trials, J. Nutr. Health Aging source

      Not checked in the free run.

    • cites [87] Miller, 2014, Effects of Whey Protein and Resistance Exercise on Body Composition: A Meta-Analysis of Randomized Controlled Trials, J. Am. Coll. Nutr. source

      Not checked in the free run.

    • cites [19] Finger, 2015, Effects of protein supplementation in older adults undergoing resistance training: A systematic review and meta-analysis, Sports Med. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Interpretationnone given

    The results of the studies that reflected no significant intervention effect on primary or secondary outcomes may contribute negatively to the overall effect size.

    “the results of the studies that reflected no significant intervention effect on primary or secondary outcomes may contribute negatively to the overall effect size.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    There may have been sex differences for changes in body composition in response to PS plus exercise training.

    “there may have been sex differences for changes in body composition in response to PS plus exercise training [20,91,92,93]”
    Quote in the paperNot a substantial claim0 of 4 sources checked
    • cites [20] Liao, 2017, Effects of protein supplementation combined with resistance exercise on body composition and physical function in older adults: A systematic review and meta-analysis, Am. J. Clin. Nutr. source

      Not checked in the free run.

    • cites [91] Burd, 2009, Exercise training and protein metabolism: Influences of contraction, protein intake, and sex-based differences, J. Appl. Physiol. source

      Not checked in the free run.

    • cites [92] Arnarson, 2013, Effects of whey proteins and carbohydrates on the efficacy of resistance training in elderly people: Double blind, randomised controlled trial, Eur. J. Clin. Nutr. source

      Not checked in the free run.

    • cites [93] Leenders, 2013, Protein supplementation during resistance-type exercise training in the elderly, Med. Sci. Sports Exerc. source

      Not checked in the free run.

36 of 36

  • The paper relies on this without support.

    Muscle hypertrophy induced by RET highly depends on training intensity that is generally not tolerated and afforded by frail individuals.

    “However, muscle hypertrophy induced by RET highly depends on the training intensity that is generally not tolerated and afforded by frail individuals.”

  • The paper relies on this without support.

    An RET intensity as high as 80–95% 1-RM is not allowed for most frail older adults, especially institutionalized residents who are more dependent and usually have lower exercise adherence due to cardiopulmonary dysfunction or physical limitations.

    “However, an RET intensity as high as 80–95% 1-RM has been recommended to induce maximal muscle hypertrophy or muscle fiber adaptation [73,74], which is not allowed for most frail older adults, especially for the institutionalized residents who are more dependent and usually have lower exercise adherence rate due to cardiopulmonary dysfunction or physical limitations [75].”

  • The paper relies on this without support.

    Demented older individuals are more dependent and usually have lower adherence rates of exercise or nutrient interventions which may influence the intervention effects.

    “Demented older individuals are more dependent and usually have lower adherence rates of exercise or nutrient interventions which may influence the intervention effects.”
3 of 3

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Trial 61 is assigned to both RET and MET

    Minor

    The exercise-protocol section assigns trial 61 to MET, but the compliance discussion lists it among RET trials involving community dwellers.

  • Walking-speed p-values disagree

    Minor

    The abstract reports p = 0.002 for the walking-speed effect, while the results report p = 0.02 for the same overall SMD of 0.32.

2 of 2

Cites

Flagged first, then by citations

2 of the 95 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

  1. Higgins, J.P.T., and Green, S. (2011). Chapter 16: Special topics in statistics. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1.0 [Updated March 2011], The Cochrane Collaboration.

Cited by

Sorted by citations

Related

Authors
Liao, C.-D., Lee, P.-H., Hsiao, D.-J., Huang, S.-W., Tsauo, J.-Y., Chen, H.-C., & Liou, T.-H.
Affiliations
  • National Taiwan University (TW)
  • Taipei Medical University (TW)
  • Taipei Medical University-Shuang Ho Hospital (TW)
  • Wan Fang Hospital (TW)
Corresponding author
Liou, Tsan-Hon
ORCID
Venue
Nutrients
Publisher
MDPI AG
Published
2018-12-04
Volume
10
Issue
12
Pages
1916
ISSN
2072-6643 (ISSN-L)
DOI
10.3390/nu10121916
PMC
PMC6315527
OpenAlex
W2903362072
Cited by
94
References
95
Citations by year
2026: 5 · 2025: 7 · 2024: 13 · 2023: 19 · 2022: 14 · 2021: 15 · 2020: 15 · 2019: 5
FWCI
1.15
Type
journal article
Language
en
Open access
Licence
Locations
  • Nutrients (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Taipei Medical University-Shuang Ho Hospital, Ministry of Health and Welfare, Taiwan (W106HCP-14)
  • Taipei Medical University-Wan Fang Hospital, Taiwan (98TMU-WFH-05-3)
Topics
  • Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
  • Health Sciences › Medicine › Geriatrics and Gerontology › Frailty in Older Adults
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
Keywords
protein supplementation, frailty, older adults, resistance training, multicomponent exercise training, lean body mass, muscle strength, walking speed, physical function, body composition
MeSH terms
Aged, Aged, 80 and over, Body Composition, Dietary Proteins, Exercise Therapy, Female, Humans, Male, Randomized Controlled Trials as Topic, Frail Elderly, Dietary Supplements

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-10.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-10.

Statistics and arithmetic are recomputed, not judged.

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