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Management of Sarcopenia: A Network Meta-Analysis of Randomized Controlled Trials

Published:February 17, 2022DOI:https://doi.org/10.1016/j.jamda.2022.01.057

      Abstract

      Objective

      This study aimed to determine the comparative effectiveness of interventions in treatment of sarcopenia. The primary outcome was the measure of treatment effect on muscle mass, and secondary outcomes were the treatment effect on muscle strength and physical performance.

      Design

      Systematic review and network meta-analysis (NMA).

      Setting and Participants

      Participants with sarcopenia receiving interventions targeting sarcopenia in any setting.

      Methods

      Data sources: Relevant RCTs were identified by a systematic search of several electronic databases, including CINAHL, Embase, MEDLINE, and the Cochrane Central Registry of Controlled Trials (CENTRAL) from January 1995 to July 2019. Duplicate title and abstract and full-text screening, data extraction, and risk of bias assessment were performed.
      Data extraction: All RCTs examining sarcopenia interventions [mixed exercise (combined aerobic and resistance exercise), aerobic exercise, resistance exercise, balance exercise, physical activity and protein or nutrition supplementation, acupuncture, whole-body vibration, protein supplement or interventions to increase protein intake, any nutritional intervention other than protein, and pharmacotherapy] were included. Comparators were standard care, placebo, or another intervention.
      Data synthesis: We performed Bayesian NMA; continuous outcome data were pooled using the standardized mean difference effect size. Interventions were ranked using the surface under the cumulative ranking curve (SUCRA) for each outcome.

      Results

      A total of 59 RCTs were included after screening of 4315 citations and 313 full-text articles. Network meta-analysis of muscle mass outcome (including 46 RCTs, 3649 participants, 11 interventions) suggested that mixed exercise were the most effective intervention (SUCRA = 93.94%) to increase muscle mass. Physical activity and protein or nutrition supplementation, and aerobic exercise were the most effective interventions to improve muscle strength and physical performance, respectively. Overall, mixed exercise is the most effective intervention in increasing muscle mass and was one of the 3 most effective interventions in increasing muscle strength and physical performance.

      Conclusions and Implications

      Mixed exercise and physical activity with nutritional supplementation are the most effective sarcopenia interventions. Most of the included studies have a high risk of bias. More robust RCTs are needed to increase the confidence of our NMA results and the quality of evidence.

      Keywords

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      References

        • Marzetti E.
        • Calvani R.
        • Tosato M.
        • et al.
        Sarcopenia: an overview.
        Aging Clin Exp Res. 2017; 29: 11-17
        • Hou L.
        • Lei Y.
        • Li X.
        • et al.
        Effect of protein supplementation combined with resistance training on muscle mass, strength and function in the elderly: a systematic review and meta-analysis.
        J Nutr Health Aging. 2019; 23: 451-458
        • Du Y.
        • Karvellas C.J.
        • Baracos V.
        • Williams D.C.
        • Khadaroo R.G.
        • Acute Care and Emergency Surgery (ACES) Group
        Sarcopenia is a predictor of outcomes in very elderly patients undergoing emergency surgery.
        Surgery. 2014; 156: 521-527
        • von Haehling S.
        • Morley J.E.
        • Anker S.D.
        From muscle wasting to sarcopenia and myopenia: update 2012.
        J Cachexia Sarcopenia Muscle. 2012; 3: 213-217
        • Cruz-Jentoft A.J.
        • Baeyens J.P.
        • Bauer J.M.
        • et al.
        Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People.
        Age Ageing. 2010; 39: 412-423
        • Morley J.E.
        Sarcopenia in the elderly.
        Fam Pract. 2012; 29: i44-i48
        • Cruz-Jentoft A.J.
        • Landi F.
        • Schneider S.M.
        • et al.
        Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS).
        Age Ageing. 2014; 43: 748-759
        • Cooper C.
        • Dere W.
        • Evans W.
        • et al.
        Frailty and sarcopenia: definitions and outcome parameters.
        Osteoporos Int. 2012; 23: 1839-1848
        • Fielding R.A.
        • Vellas B.
        • Evans W.J.
        • et al.
        Sarcopenia: an undiagnosed condition in older adults. Current consensus definition: prevalence, etiology, and consequences. International Working Group on Sarcopenia.
        J Am Med Dir Assoc. 2011; 12: 249-256
        • Frontera W.R.
        • Hughes V.A.
        • Krivickas L.S.
        • Kim S.K.
        • Foldvari M.
        • Roubenoff R.
        Strength training in older women: early and late changes in whole muscle and single cells.
        Muscle Nerve. 2003; 28: 601-608
        • Kemmler W.
        • Wittke A.
        • Bebenek M.
        • Fröhlich M.
        • von Stengel S.
        High intensity resistance training methods with and without protein supplementation to fight cardiometabolic risk in middle-aged males: a randomized controlled trial.
        BioMed Res Int. 2016; 2016: 9705287
        • Cramer J.T.
        • Cruz-Jentoft A.J.
        • Landi F.
        • et al.
        Impacts of high-protein oral nutritional supplements among malnourished men and women with sarcopenia: a multicenter, randomized, double-blinded, controlled trial.
        J Am Med Dir Assoc. 2016; 17: 1044-1055
        • Yoshimura Y.
        • Wakabayashi H.
        • Yamada M.
        • Kim H.
        • Harada A.
        • Arai H.
        Interventions for treating sarcopenia: a systematic review and meta-analysis of randomized controlled studies.
        J Am Med Dir Assoc. 2017; 18: 553.e1-553.e16
        • Negm A.M.
        • Kennedy C.C.
        • Thabane L.
        • et al.
        Management of frailty: a systematic review and network meta-analysis of randomized controlled trials.
        J Am Med Dir Assoc. 2019; 20: 1190-1198
        • Hutton B.
        • Salanti G.
        • Caldwell D.M.
        • et al.
        The PRISMA extension statement for reporting of systematic reviews incorporating network meta-analyses of health care interventions: checklist and explanations.
        Ann Intern Med. 2015; 162: 777-784
        • Higgins J.P.T.
        • Altman D.G.
        • Gøtzsche P.C.
        • et al.
        The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials.
        BMJ. 2011; 343: d5928
        • DerSimonian R.
        • Laird N.
        Meta-analysis in clinical trials.
        Control Clin Trials. 1986; 7: 177-188
        • Higgins J.P.
        • Thompson S.G.
        • Deeks J.J.
        • Altman D.G.
        Measuring inconsistency in meta-analyses.
        BMJ. 2003; 327: 557-560
        • Higgins J.P.
        • Thompson S.G.
        Quantifying heterogeneity in a meta-analysis.
        Stat Med. 2002; 21: 1539-1558
        • Viechtbauer W.
        Confidence intervals for the amount of heterogeneity in meta-analysis.
        Stat Med. 2007; 26: 37-52
        • Furukawa T.A.
        • Barbui C.
        • Cipriani A.
        • Brambilla P.
        • Watanabe N.
        Imputing missing standard deviations in meta-analyses can provide accurate results.
        J Clin Epidemiol. 2006; 59: 7-10
        • White I.R.
        • Barrett J.K.
        • Jackson D.
        • Higgins J.P.
        Consistency and inconsistency in network meta-analysis: model estimation using multivariate meta-regression.
        Res Synth Methods. 2012; 3: 111-125
        • Veroniki A.A.
        • Vasiliadis H.S.
        • Higgins J.P.
        • Salanti G.
        Evaluation of inconsistency in networks of interventions.
        Int J Epidemiol. 2013; 42: 332-345
        • Jansen J.P.
        • Naci H.
        Is network meta-analysis as valid as standard pairwise meta-analysis? It all depends on the distribution of effect modifiers.
        BMC Med. 2013; 11: 159
        • Song F.
        • Altman D.G.
        • Glenny A.M.
        • Deeks J.J.
        Validity of indirect comparison for estimating efficacy of competing interventions: empirical evidence from published meta-analyses.
        BMJ. 2003; 326: 472
        • Brooks S.P.
        • Gelman A.
        General methods for monitoring convergence of iterative simulations.
        J Comput Graph Stat. 1997; 7: 434-455
        • Severini T.A.
        Bayesian interval estimates which are also confidence intervals.
        J R Stat Soc B (Method). 1993; 55: 533-540
        • Rucker G.
        • Schwarzer G.
        Ranking treatments in frequentist network meta-analysis works without resampling methods.
        BMC Med Res Methodol. 2015; 15: 58
        • Salanti G.
        • Ades A.E.
        • Ioannidis J.P.
        Graphical methods and numerical summaries for presenting results from multiple-treatment meta-analysis: an overview and tutorial.
        J Clin Epidemiol. 2011; 64: 163-171
        • Veroniki A.A.
        • Straus S.E.
        • Fyraridis A.
        • Tricco A.C.
        The rank-heat plot is a novel way to present the results from a network meta-analysis including multiple outcomes.
        J Clin Epidemiol. 2016; 76: 193-199
        • Mbuagbaw L.
        • Rochwerg B.
        • Jaeschke R.
        • et al.
        Approaches to interpreting and choosing the best treatments in network meta-analyses.
        Syst Rev. 2017; 6: 79
        • Sterne J.A.C.
        • Egger M.
        • Moher D.
        Cochrane Handbook for Systematic Reviews of Interventions.
        2008 (John Wiley and Sons, Inc)
        • Plummer M.
        JAGS: A program for analysis of Bayesian graphical models using Gibbs sampling.
        in: Hornik K. Leisch F. Zeileis A. Proceedings of the 3rd International Workshop on Distributed Statistical Computing (DSC 2003), March 20-22. 2003 (Vienna, Austria)
        • Plummer M.
        • Stukalov A.
        • Denwood M.
        Bayesian Graphical Models using MCMC. R package version 4-6.
        http://CRAN.R-project.org/package=rjags
        Date accessed: July 30, 2018
        • Lunn D.
        • Spiegelhalter D.
        • Thomas A.
        • Best N.
        The BUGS project: Evolution, critique and future directions.
        Stat Med. 2009; 28: 3049-3067
        • Béliveau A.
        • Boyne D.J.
        • Slater J.
        • Brenner D.
        • Arora P.
        BUGSnet: an R package to facilitate the conduct and reporting of Bayesian network Meta-analyses.
        BMC Med Res Methodol. 2019; 19: 196
        • Viechtbauer W.
        Conducting meta-analyses in R with the metafor package.
        J Stat Softw. 2010; 36: 1-48
        • Adams S.C.
        • Segal R.J.
        • McKenzie D.C.
        • et al.
        Impact of resistance and aerobic exercise on sarcopenia and dynapenia in breast cancer patients receiving adjuvant chemotherapy: a multicenter randomized controlled trial.
        Breast Cancer Res Treat. 2016; 158: 497-507
        • Aleman-Mateo H.
        • Carreon V.R.
        • Macias L.
        • Astiazaran-Garcia H.
        • Gallegos-Aguilar A.C.
        • Enriquez J.R.
        Nutrient-rich dairy proteins improve appendicular skeletal muscle mass and physical performance, and attenuate the loss of muscle strength in older men and women subjects: a single-blind randomized clinical trial.
        Clin Interv Aging. 2014; 9: 1517-1525
        • Aubertin-Leheudre M.
        • Lord C.
        • Khalil A.
        • Dionne I.J.
        Six months of isoflavone supplement increases fat-free mass in obese–sarcopenic postmenopausal women: a randomized double-blind controlled trial.
        Eur J Clin Nutr. 2007; 61: 1442-1444
        • Balachandran A.
        • Krawczyk S.N.
        • Potiaumpai M.
        • Signorile J.F.
        High-speed circuit training vs hypertrophy training to improve physical function in sarcopenic obese adults: a randomized controlled trial.
        Exp Gerontol. 2014; 60: 64-71
        • Basha M.A.
        • Mowafy Z.E.
        • Morsy E.A.
        Sarcopenic obesity and dyslipidemia response to selective exercise program after liver transplantation.
        Egypt J Med Hum Genet. 2015; 16: 263-268
        • Bauer J.M.
        • Verlaan S.
        • Bautmans I.
        • et al.
        Effects of a vitamin D and leucine-enriched whey protein nutritional supplement on measures of sarcopenia in older adults, the PROVIDE study: a randomized, double-blind, placebo-controlled trial.
        J Am Med Dir Assoc. 2015; 16: 740-747
        • Kemmler W.
        • Grimm A.
        • Bebenek M.
        • Kohl M.
        • von Stengel S.
        Effects of combined whole-body electromyostimulation and protein supplementation on local and overall muscle/fat distribution in older men with sarcopenic obesity: the randomized controlled Franconia Sarcopenic Obesity (FranSO) Study.
        Calcif Tissue Int. 2018; 103: 266-277
        • Kemmler W.
        • Kohl M.
        • Freiberger E.
        • Sieber C.
        • von Stengel S.
        Effect of whole-body electromyostimulation and/or protein supplementation on obesity and cardiometabolic risk in older men with sarcopenic obesity: the randomized controlled FranSO trial.
        BMC Geriatr. 2018; 18: 70
        • Kemmler W.
        • Weissenfels A.
        • Teschler M.
        • et al.
        Whole-body electromyostimulation and protein supplementation favorably affect sarcopenic obesity in community-dwelling older men at risk: the randomized controlled FranSO study.
        Clin Interv Aging. 2017; 12: 1503-1513
        • Kemmler W.
        • Teschler M.
        • Weissenfels A.
        • et al.
        Whole-body electromyostimulation to fight sarcopenic obesity in community-dwelling older women at risk. Results of the randomized controlled FORMOsA—sarcopenic obesity study.
        Osteoporos Int. 2016; 27: 3261-3270
        • Kenny A.M.
        • Kleppinger A.
        • Wang Y.
        • Prestwood K.M.
        Effects of ultra-low-dose estrogen therapy on muscle and physical function in older women.
        J Am Geriatr Soc. 2005; 53: 1973-1977
        • Kim H.K.
        • Suzuki T.
        • Saito K.
        • et al.
        Effects of exercise and amino acid supplementation on body composition and physical function in community-dwelling elderly Japanese sarcopenic women: a randomized controlled trial.
        J Am Geriatr Soc. 2012; 60: 16-23
        • Kim H.
        • Kim M.
        • Kojima N.
        • et al.
        Exercise and nutritional supplementation on community-dwelling elderly Japanese women with sarcopenic obesity: a randomized controlled trial.
        J Am Med Dir Assoc. 2016; 17: 1011-1019
        • Kim H.
        • Suzuki T.
        • Saito K.
        • et al.
        Effects of exercise and tea catechins on muscle mass, strength and walking ability in community-dwelling elderly Japanese sarcopenic women: a randomized controlled trial.
        Geriatr Gerontol Int. 2013; 13: 458-465
        • Liao C.D.
        • Tsauo J.Y.
        • Huang S.W.
        • Ku J.W.
        • Hsiao D.J.
        • Liou T.H.
        Effects of elastic band exercise on lean mass and physical capacity in older women with sarcopenic obesity: a randomized controlled trial.
        Sci Rep. 2018; 8: 2317
        • Liao C.D.
        • Tsauo J.Y.
        • Lin L.F.
        • et al.
        Effects of elastic resistance exercise on body composition and physical capacity in older women with sarcopenic obesity: a CONSORT-compliant prospective randomized controlled trial.
        Medicine. 2017; 96: e7115
        • Liberman K.
        • Njemini R.
        • Luiking Y.
        • et al.
        Thirteen weeks of supplementation of vitamin D and leucine-enriched whey protein nutritional supplement attenuates chronic low-grade inflammation in sarcopenic older adults: the PROVIDE study.
        Aging Clin Exp Res. 2019; 31: 845-854
        • Malafarina V.
        • Uriz-Otano F.
        • Malafarina C.
        • Martinez J.A.
        • Zulet M.A.
        Effectiveness of nutritional supplementation on sarcopenia and recovery in hip fracture patients. A multi-centre randomized trial.
        Maturitas. 2017; 101: 42-50
        • Bellomo R.G.
        • Iodice P.
        • Maffulli N.
        • Maghradze T.
        • Coco V.
        • Saggini R.
        Muscle strength and balance training in sarcopenic elderly: a pilot study with randomized controlled trial.
        Eur J Inflamm. 2013; 11: 193-201
        • Bo Y.
        • Liu C.
        • Ji Z.
        • et al.
        A high whey protein, vitamin D and E supplement preserves muscle mass, strength, and quality of life in sarcopenic older adults: a double-blind randomized controlled trial.
        Clin Nutr. 2019; 38: 159-164
        • Cebria I.I.M.A.
        • Balasch-Bernat M.
        • Tortosa-Chulia M.A.
        • Balasch-Parisi S.
        Effects of resistance training of peripheral muscles versus respiratory muscles in older adults with sarcopenia who are institutionalized: a randomized controlled trial.
        J Aging Phys Act. 2018; 26: 637-646
        • Chen H.T.
        • Chung Y.C.
        • Chen Y.J.
        • Ho S.Y.
        • Wu H.J.
        Effects of different types of exercise on body composition, muscle strength, and IGF-1 in the elderly with sarcopenic obesity.
        J Am Geriatr Soc. 2017; 65: 827-832
        • Maltais M.L.
        • Perreault K.
        • Courchesne-Loyer A.
        • Lagace J.C.
        • Barsalani R.
        • Dionne I.J.
        Effect of resistance training and various sources of protein supplementation on body fat mass and metabolic profile in sarcopenic overweight older adult men: a pilot study.
        Int J Sport Nutr Exerc Metab. 2016; 26: 71-77
        • Maltais M.L.
        • Ladouceur J.P.
        • Dionne I.J.
        The effect of resistance training and different sources of postexercise protein supplementation on muscle mass and physical capacity in sarcopenic elderly men.
        J Strength Cond Res. 2016; 30: 1680-1687
        • Yamada M.
        • Kimura Y.
        • Ishiyama D.
        • et al.
        Synergistic effect of bodyweight resistance exercise and protein supplementation on skeletal muscle in sarcopenic or dynapenic older adults.
        Geriatr Gerontol Int. 2019; 19: 429-437
        • Wei N.
        • Pang M.Y.
        • Ng S.S.
        • Ng G.Y.
        Optimal frequency/time combination of whole-body vibration training for improving muscle size and strength of people with age-related muscle loss (sarcopenia): a randomized controlled trial.
        Geriatr Gerontol Int. 2017; 17: 1412-1420
        • Wei N.
        • Pang M.Y.
        • Ng S.S.
        • Ng G.Y.
        Optimal frequency/time combination of whole body vibration training for developing physical performance of people with sarcopenia: a randomized controlled trial.
        Clin Rehabil. 2017; 31: 1313-1321
        • Takeuchi I.
        • Yoshimura Y.
        • Shimazu S.
        • Jeong S.
        • Yamaga M.
        • Koga H.
        Effects of branched-chain amino acids and vitamin D supplementation on physical function, muscle mass and strength, and nutritional status in sarcopenic older adults undergoing hospital-based rehabilitation: a multicenter randomized controlled trial.
        Geriatr Gerontol Int. 2019; 19: 12-17
        • Ritch C.R.
        • Cookson M.S.
        • Clark P.E.
        • et al.
        Perioperative oral nutrition supplementation reduces prevalence of sarcopenia following radical cystectomy: results of a prospective randomized controlled trial.
        J Urol. 2019; 201: 470-477
        • Park J.
        • Kwon Y.
        • Park H.
        Effects of 24-week aerobic and resistance training on carotid artery intima-media thickness and flow velocity in elderly women with sarcopenic obesity.
        J Atheroscler Thromb. 2017; 24: 1117-1124
        • Papanicolaou D.A.
        • Ather S.N.
        • Zhu H.
        • et al.
        A phase IIA randomized, placebo-controlled clinical trial to study the efficacy and safety of the selective androgen receptor modulator (SARM), MK-0773 in female participants with sarcopenia.
        J Nutr Health Aging. 2013; 17: 533-543
        • Molnar A.
        • Jonasne Sztruhar I.
        • Csontos A.A.
        • Ferencz C.
        • Varbiro S.
        • Szekacs B.
        Special nutrition intervention is required for muscle protective efficacy of physical exercise in elderly people at highest risk of sarcopenia.
        Physiol Int. 2016; 103: 368-376
        • Mason C.
        • Xiao L.
        • Imayama I.
        • et al.
        Influence of diet, exercise, and serum vitamin d on sarcopenia in postmenopausal women.
        Med Sci Sports Exerc. 2013; 45: 607-614
        • Invernizzi M.
        • de Sire A.
        • D'Andrea F.
        • et al.
        Effects of essential amino acid supplementation and rehabilitation on functioning in hip fracture patients: a pilot randomized controlled trial.
        Aging Clin Exp Res. 2019; 31: 1517-1524
        • Huang S.W.
        • Ku J.W.
        • Lin L.F.
        • Liao C.D.
        • Chou L.C.
        • Liou T.H.
        Body composition influenced by progressive elastic band resistance exercise of sarcopenic obesity elderly women: a pilot randomized controlled trial.
        Eur J Phys Rehabil Med. 2017; 53: 556-563
        • Dong Z.J.
        • Zhang H.L.
        • Yin L.X.
        Effects of intradialytic resistance exercise on systemic inflammation in maintenance hemodialysis patients with sarcopenia: a randomized controlled trial.
        Int Urol Nephrol. 2019; 51: 1415-1424
        • Dal Negro R.W.
        • Aquilani R.
        • Bertacco S.
        • Boschi F.
        • Micheletto C.
        • Tognella S.
        Comprehensive effects of supplemented essential amino acids in patients with severe COPD and sarcopenia.
        Monaldi Arch Chest Dis. 2010; 73: 25-33
        • El Hajj C.
        • Fares S.
        • Chardigny J.M.
        • Boirie Y.
        • Walrand S.
        Vitamin D supplementation and muscle strength in pre-sarcopenic elderly Lebanese people: a randomized controlled trial.
        Arch Osteoporos. 2019; 14: 4
        • Zhu L.Y.
        • Chan R.
        • Kwok T.
        • Cheng K.C.
        • Ha A.
        • Woo J.
        Effects of exercise and nutrition supplementation in community-dwelling older Chinese people with sarcopenia: a randomized controlled trial.
        Age Ageing. 2019; 48: 220-228
        • Zhou X.
        • Xing B.
        • He G.
        • Lyu X.
        • Zeng Y.
        The effects of electrical acupuncture and essential amino acid supplementation on sarcopenic obesity in male older adults: a randomized control study.
        Obes Facts. 2018; 11: 327-334
        • Zdzieblik D.
        • Oesser S.
        • Baumstark M.W.
        • Gollhofer A.
        • Konig D.
        Collagen peptide supplementation in combination with resistance training improves body composition and increases muscle strength in elderly sarcopenic men: a randomised controlled trial.
        Br J Nutr. 2015; 114: 1237-1245
        • Yoshimura Y.
        • Bise T.
        • Shimazu S.
        • et al.
        Effects of a leucine-enriched amino acid supplement on muscle mass, muscle strength, and physical function in post-stroke patients with sarcopenia: a randomized controlled trial.
        Nutrition. 2019; 58: 1-6
        • Wittmann K.
        • Sieber C.
        • von Stengel S.
        • et al.
        Impact of whole body electromyostimulation on cardiometabolic risk factors in older women with sarcopenic obesity: the randomized controlled FORMOsA—sarcopenic obesity study.
        Clin Interv Aging. 2016; 11: 1697-1706
        • Wei N.
        • Ng G.Y.F.
        The effect of whole body vibration training on quadriceps voluntary activation level of people with age-related muscle loss (sarcopenia): a randomized pilot study.
        BMC Geriatr. 2018; 18: 240
        • Vikberg S.
        • Sorlen N.
        • Branden L.
        • et al.
        Effects of resistance training on functional strength and muscle mass in 70-year-old individuals with pre-sarcopenia: a randomized controlled trial.
        J Am Med Dir Assoc. 2019; 20: 28-34
        • Tsekoura M.
        • Billis E.
        • Tsepis E.
        • et al.
        The effects of group and home-based exercise programs in elderly with sarcopenia: a randomized controlled trial.
        J Clin Med. 2018; 7: 480
        • Shahar S.
        • Kamaruddin N.S.
        • Badrasawi M.
        • et al.
        Effectiveness of exercise and protein supplementation intervention on body composition, functional fitness, and oxidative stress among elderly Malays with sarcopenia.
        Clin Interv Aging. 2013; 8: 1365-1375
        • Sammarco R.
        • Marra M.
        • Di Guglielmo M.L.
        • et al.
        Evaluation of hypocaloric diet with protein supplementation in middle-aged sarcopenic obese women: a pilot study.
        Obes Facts. 2017; 10: 160-167
        • Rooks D.
        • Praestgaard J.
        • Hariry S.
        • et al.
        Treatment of sarcopenia with bimagrumab: results from a phase II, randomized, controlled, proof-of-concept study.
        J Am Geriatr Soc. 2017; 65: 1988-1995
        • Rondanelli M.
        • Klersy C.
        • Terracol G.
        • et al.
        Whey protein, amino acids, and vitamin D supplementation with physical activity increases fat-free mass and strength, functionality, and quality of life and decreases inflammation in sarcopenic elderly.
        Am J Clin Nutr. 2016; 103: 830-840
        • Piastra G.
        • Perasso L.
        • Lucarini S.
        • et al.
        Effects of two types of 9-month adapted physical activity program on muscle mass, muscle strength, and balance in moderate sarcopenic older women.
        BioMed Res Int. 2018; 2018: 5095673
        • Nabuco H.C.G.
        • Tomeleri C.M.
        • Fernandes R.R.
        • et al.
        Effect of whey protein supplementation combined with resistance training on body composition, muscular strength, functional capacity, and plasma-metabolism biomarkers in older women with sarcopenic obesity: a randomized, double-blind, placebo-controlled trial.
        Clin Nutr ESPEN. 2019; 32: 88-95
        • Ishikawa T.
        • Yasuda T.
        • Doi T.
        • et al.
        The amino acid-rich elemental diet Elental preserves lean body mass during chemo- or chemoradiotherapy for esophageal cancer.
        Oncol Rep. 2016; 36: 1093-1100
        • Hassan B.H.
        • Hewitt J.
        • Keogh J.W.
        • Bermeo S.
        • Duque G.
        • Henwood T.R.
        Impact of resistance training on sarcopenia in nursing care facilities: a pilot study.
        Geriatr Nurs. 2016; 37: 116-121
        • Dieli-Conwright C.M.
        • Courneya K.S.
        • Demark-Wahnefried W.
        • et al.
        Effects of aerobic and resistance exercise on metabolic syndrome, sarcopenic obesity, and circulating biomarkers in overweight or obese survivors of breast cancer: a randomized controlled trial.
        J Clin Oncol. 2018; 36: 875-883
        • Dawson J.K.
        • Dorff T.B.
        • Todd Schroeder E.
        • Lane C.J.
        • Gross M.E.
        • Dieli-Conwright C.M.
        Impact of resistance training on body composition and metabolic syndrome variables during androgen deprivation therapy for prostate cancer: a pilot randomized controlled trial.
        BMC Cancer. 2018; 18: 368
        • Chen H.T.
        • Wu H.J.
        • Chen Y.J.
        • Ho S.Y.
        • Chung Y.C.
        Effects of 8-week kettlebell training on body composition, muscle strength, pulmonary function, and chronic low-grade inflammation in elderly women with sarcopenia.
        Exp Gerontol. 2018; 112: 112-118
        • Soares Mendes Damasceno G.
        • Teixeira T.
        • de Souza V.C.
        • et al.
        Acupuncture treatment in elderly people with sarcopenia: effects on the strength and inflammatory mediators.
        J Aging Res. 2019; 2019: 8483576
        • Wu P.Y.
        • Huang K.S.
        • Chen K.M.
        • Chou C.P.
        • Tu Y.K.
        Exercise, nutrition, and combined exercise and nutrition in older adults with sarcopenia: a systematic review and network meta-analysis.
        Maturitas. 2021; 145: 38-48