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Effects of Physical Exercise Programs on Sarcopenia Management, Dynapenia, and Physical Performance in the Elderly: A Systematic Review of Randomized Clinical Trials

Effects of Physical Exercise Programs on Sarcopenia Management, Dynapenia, and Physical... Hindawi Journal of Aging Research Volume 2019, Article ID 1959486, 7 pages https://doi.org/10.1155/2019/1959486 Review Article Effects of Physical Exercise Programs on Sarcopenia Management, Dynapenia, and Physical Performance in the Elderly: A Systematic Review of Randomized Clinical Trials 1,2,3 1,2 4 Renato Gorga Bandeira de Mello , Roberta Rigo Dalla Corte, Joana Gioscia, 1,2,5 and Emilio Hideyuki Moriguchi School of Medicine at the Federal University of Rio Grande do Sul (UFRGS), Department of Internal Medicine, Porto Alegre, Brazil Hospital de Clınicas de Porto Alegre, Section of Internal Medicine, Porto Alegre, Brazil Post-Graduation Studies Program in Endocrinology, UFRGS, Porto Alegre, Brazil School of Medicine at the Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Brazil Post-Graduation Studies Program in Cardiology and Cardiovascular Sciences, UFRGS, Porto Alegre, Brazil Correspondence should be addressed to Renato Gorga Bandeira de Mello; rgmello@hcpa.edu.br Received 26 July 2019; Accepted 10 October 2019; Published 20 November 2019 Guest Editor: Priscila Sampaio Copyright © 2019 Renato Gorga Bandeira de Mello et al. )is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction. Sarcopenia is a prevalent condition in the elderly population, imposing a significant impact over their functional ability as well as their quality of life. Furthermore, it is associated with greater incidence of major geriatric outcomes, as reduced mobility, falls, loss of independence, cognitive impairment, and all-cause mortality. Physical Exercise Programs directed to improve muscle mass and its function may be key to reduce sarcopenia consequences. However, a significant heterogeneity is found in clinical trials, especially as a consequence of different exercise protocols applied to research subjects. Objectives. To access the effects of physical exercise programs compared to no exercise interventions to improve sarcopenia components and its determinants in sarcopenic elder individuals. Methods. A systematic review was conducted in the Pubmed database to identify randomized clinical trials (RCTs) which tested the effects of physical exercise programs to manage sarcopenia components in sarcopenic elder individuals. Two independent reviewers assessed the studies’ eligibility according to specified inclusion criteria in a four-step strategy. Data regarding population characteristics, muscle mass, muscle quality, muscle strength, and muscle function were extracted from each one of the included studies. Assessment of quality and individual studies risk of bias were assessed through Cochrane Risk of Bias Tool . Assuming theoretical expected heterogeneity among studies, especially regarding different physical exercise programs and different outcome measurements, authors decided to be conservative and present study results in descriptive tables. Results. Search strategy retrieved 298 papers on PubMed database. )ree more were identified through manual search, being 301 studies revised for inclusion. 278 were excluded during title/abstract review. After further evaluation of 23 full- texts, 5 RCTs were included. All 5 trials tested the efficacy of isolated exercise programs to improve sarcopenia components in the elderly compared to no physical intervention. Resistance training was the main intervention component in all included trials compared to inactive control groups (health education mainly). Physical training improved muscle strength, muscle quality, and muscle function compared to inactive control groups. Considering muscle mass, no differences were demonstrated. Data meta- analysis was not possible to be performed due to high heterogeneity among trials and small number of studies for each outcome comparison. Conclusion. Heterogeneity among trials and small number of RCTs limited robust conclusions and data meta- analysis. However, resistance training protocols can improve muscle strength and physical performance in elders previously diagnosed with sarcopenia, although its effect size and clinical impact are barely relevant. 2 Journal of Aging Research )e eligible criteria are predefined by the characteristics of 1. Introduction the primary studies. At this point, it is only necessary to According to the European Working Group on Sarcopenia define the following criteria: the target population, the in- in older people revised consensus, sarcopenia is a skeletal tervention, and the outcomes. Characteristics of the in- muscle disorder in which muscle strength is the key feature cluded study populations, such as intervention types and of a clinical condition with increased risk for major geriatric outcome measure, are presented in Table 1. outcomes [1]. It is a prevalent condition in the elderly, Population: elderly (>65 years) with diagnosed sarco- varying according to age-related variables especially when penia; intervention and control: physical exercise programs different clinical settings where compared. In community- compared to a control group (no exercise); outcomes: sar- dwelling samples, a wide prevalence range was found from copenia, muscle mass, muscle strength, physical perfor- 1% to 29%; and in long-term care facilities, the range is mance, and muscle quality; length of follow-up: not 14–33% [2]. However, it is presumed that this heterogeneity specified; study design: randomized clinical trial. )ere was would be also explained by different applied diagnostic no limitation of gender. )e types of exercises were pre- criteria. dominantly resistance training (Table 1). It is postulated that physical exercise programs can shift sarcopenia clinical course. A systematic review was con- ducted in 2014, and the authors concluded that physical 1.2.2. Search Strategy. A systematic search was conducted in exercise has an impact on improving muscle strength and the PubMed electronic articles database using the following physical performance; however, interventions did not sig- strategy: (((Sarcopenia) AND (Elderly)) AND ((Physical nificantly improved muscle mass. Several limitations were activity) OR (Exercise)) AND (Clinical trial)). No specific pointed out to explain the low impact of exercise in- date limit was defined; no language limitation was imposed; terventions: lack of standardization of exercise protocols, all available studies were included. Last search was con- low duration of interventions, heterogeneity in outcome ducted on June 30th, 2019. For those articles with limited measurements, and selection bias due to heterogeneous access or incomplete data, the authors were contacted di- eligibility criteria. rectly by email. Additional manual search was performed to Most recently, in 2017, the last published systematic increase search sensitivity. review regarding exercise and sarcopenia showed better physical performance after resistance training exercise in- (1) Study Selection and Data Collection Process. Step 1: two tervention, but no improvement in muscle strength [3]. independent reviewers assessed all titles and abstracts to Beyond physical exercise impact on physical performance verify eligibility criteria on Revision. Step 2 included a full- and muscle strength and mass, it is important to access its text revision for further eligibility assessment. Step 3: effects on reducing major geriatric outcomes. Guerreiro et al. duplicates were excluded. Final inclusion results are demonstrated that both muscle mass estimated by bedside presented in the systematic review inclusion flowchart ultrasound and muscle performance and strength in hos- (Figure 1). A standardized Microsoft Office ExcelTM pitalized elderly patients are important predictors for spreadsheet was used to organize independent data col- functional decline, rehospitalization, and death [4]. How- lection. Investigators followed a step by step extraction ever, most clinical trials testing physical exercise in sarco- process according to the PICOTS prespecified strategy, penic elder patients yet do not access its effects over major extracting study ́s population data, followed by in- clinical geriatric outcomes. tervention description, outcomes variables collection, and Considering the aforementioned reasons, the main its main results. objective of this systematic review is to analyze the effec- Quality and individual studies risk of bias were assessed tiveness of physical exercise on improving sarcopenia in through Cochrane Risk of Bias Tool [11] and are presented older populations. Muscle mass, muscle function, muscle in Table 1. strength, and physical resistance improvement in the elderly will be investigated. Furthermore, we will show these effects on the incidence of major geriatric outcomes. 2. Data Analysis Assuming theoretical expected heterogeneity among studies, 1.1. Methods. )is systematic review protocol followed the especially regarding different physical exercise programs and Preferred Reporting Items for Systematic Reviews and Meta- different outcome measurements, authors decided to be Analyses (PRISMA) recommendations [5]. conservative and present study results in descriptive tables. We assumed that lack of studies’ exercise protocols stan- dardization as well as lack of outcomes measurement 1.2. Design: Systematic Review of Randomized Clinical standardization limits data meta-analysis as theoretical Trials (RCTs) homogeneity assumption is not reached. Publication bias was also assessed by trim and fill 1.2.1. Eligibility Criteria. RCT testing effects of physical strategy. Analyses were performed using the software exercise programs were compared to those of a physically Comprehensive Meta-AnalysisTM version 3—free trial inactive control group on sarcopenia clinical variables in [12]. elderly populations previously diagnosed with sarcopenia. Journal of Aging Research 3 Table 1: Basic characteristics of included randomized controlled clinical trials. Outcome Reference Population Design Intervention Control measurement and Main results definition Muscle mass: apendicular lean mass: no significant differences between Measured by DEXA groups Skeletal muscle mass: Muscle quality (Nm/ apendicuar lean mass kg) Strasser 33 women and men Resistance training (ALM in kg) Baseline 6 months et al. [6] (82.4± 6.0 years) with (RT): 12 weeks elastic Control group (CG) RCT Muscle quality: Extension force Moderate impaired health status band resistance (n � 17) isokinetic force RT: 10.1± 2.9 RoB (mostly sarcopenic) training (n � 16) measurement of knee 12.1± 2.6 flexion and extension CG: 11.5± 2.5 9.9± 3.0 (Nm/kg) P � 0.006 Flexion force (MQ) RT: 5.2± 1.4 6.8± 1.0 CG: 5.7± 1.5 5.5± 1.5 P � 0.009 Results presented as mean differences Measured by DEXA between groups (RT- Muscle CG) mass—apendicular Muscle mass (kg) lean Mass (ALM in ALM: 0.99 (0.33, 1.66) kg) P< 0.01 Resistance training Muscle quality (MQ) Liao et al. Muscle quality (N/kg) 56 sarcopenic or obese (RT): 12 weeks of Control group (CG) after lower limb [7] MQ-LE: 1.82 (1.25, women (mean± SD RCT elastic band resistance matched by age muscle flexion (kg/kg) High 2.39) P< 0.01 age 67.3± 5.1 years) training (ERT) (n � 23) Physical capacity and RoB Function (n � 33) function outcomes TUG: − 1.64 (− 2.34, Timed Up and Go − 0.95) P< 0.01 (TUG in s); gait speed GS: 0.14 (0.33, 0.25) (GS in m/s) P< 0.05 Quality of life (qol QoL measured by SF-36) SF-36: 13.62 (6.47, 20.76) P< 0.001 Measured by bioeletrical Resistance training 139 sarcopenic elderly impedance analysis No differences in Kim (RT): 12 weeks elastic women; 69 Control group (CG) (BIA) muscle mass, strength, et al.[8] band for upper limbs randomized to RCT Health education Apendicular skeletal and function were Moderate and ankle weight for resistance training or (n � 34) muscle mass (kg) observed after RoB lower limb training control group Performance intervention (n � 35) TUG; GS; grip strength Measured by Apendicular muscle bioeletrical Resistance training mass: no difference 138 sarcopenic elderly impedance analysis Kim (RT): 12 weeks elastic Performance women; 64 Control group (BIA) et al.[9] band for upper limbs Grip strength: no randomized to RCT (CG): health Apendicular skeletal Moderate and ankle weight for difference resistance training or education (n � 32) muscle mass (kg) RoB lower limb training. GS and TUG: no control group Performance relevant differences (n � 32) TUG; GS; grip found strength 4 Journal of Aging Research Table 1: Continued. Outcome Reference Population Design Intervention Control measurement and Main results definition Measured by Apendicular muscle bioeletrical mass: no difference Exercise group (EG): impedance analysis Walking speed (m/s) 155 sarcopenic elderly 12 weeks combined Kim (BIA) Baseline 6 months women; 78 training—warm up; Control group et al.[10] Apendicular skeletal EG: 1.31± 0.24 randomized to RCT strengthening (CG): health Moderate muscle mass (kg) 1.50± 0.23 P � 0.007 exercise group or exercise, balance and education (n � 39) RoB Performance CG: 1.19± 0.21 control group gait training, and cool Walking speed, knee 1.22± 0.23 down. (n � 39) extension strength Strength: no (Nm/kg) difference RCT �randomized clinical trial; RoB: risk of bias; in accordance with Cochrane’s risk of bias tool. 2.1. Results. A total number of 298 studies were retrieved by RT exercise protocols significantly improved the muscle search strategy application on PubMed database. )ree more function measured by gait speed (GS) as well as by the Timed studies were found in a previous meta-analysis and included Up and Go test (TUG) in 3 of 5 studies as described in in the next step [3]. 278 studies were excluded in the Step 1 Table 3. Kim et al. [8, 9] did not evidence the muscle function improvement after RT. reviewing process. In Step 2, 23 full-text articles were reviewed for further eligibility evaluation and 18 were ex- In [7], quality of life was accessed before and after ex- cluded. )e reasons for the exclusion of these studies are ercise interventions and it was possible to show significant described in the flowchart of Figure 1. Finally, 5 randomized improvement in QoL in the RT group when compared to clinical trials were included in this present systematic review control (mean difference 13.62 (6.47, 20.76); P< 0.001), as described in the inclusion flowchart (Figure 1). especially a relevant difference in the physical component of Table 1 presents study details regarding population, the SF-36 questionnaire. study design, interventions, control groups, outcome mea- surements, and main results [6–10]. 3. Discussion All five studies have high to moderate risk of bias according to Cochrane’s risk of bias tool. In three studies In this systematic review to assess the effectiveness of ex- conducted by Kim et al., direct comparison of physical ercise training to improve sarcopenia-related outcomes in training against inactive control is only possible in a study sarcopenic elder populations, a sensitive search strategy subsample composed by two different intervention groups retrieved 301 studies on PubMed database. During the first (exercise versus health education groups). step review process, 278 papers were excluded and 23 more Different measurement protocols were applied to as- were excluded after full-paper review, leading to 5 RCTs to sess outcomes among studies. In two studies—Strasser be included in this study. et al. [6] and Liao et al. [7]—dual-energy X-ray absorp- RCTs results according to sarcopenia component varied tiometry was used to measure muscle mass as well as significantly. Only one study evidenced muscle mass gain; muscle quality. All studies conducted by Kim et al. [8–10] muscle quality, on the other hand, was improved in both measured these variables using bioelectrical impedance studies that this factor was measured. Although effects over analysis. muscle strength and muscle mass were not clear, muscle function—walking speed and Timed Up and Go test—was homogeneously improved among studies, but the size effect seems to be limited. 2.2. Main Results However, it is presumed that resistance training prevents 2.2.1. Muscle Mass, Muscle Quality, Strength, and Function. muscle mass wasting because it stimulates muscle hyper- Results regarding muscle mass, muscle strength, and muscle trophy and increases muscle strength, as postulated by quality are summarized in Table 2. Muscle mass was only Johnston et al. [13], and also it is postulated that resistance significantly improved in the RCT conducted by Liao et al. training is a key strategy to treat sarcopenia; only one clinical [7] Sarcopenic elder patients submitted to 12 weeks in- trial [7] evidenced improvement of muscle mass after a tervention of resistance training (RT) gained almost 1 kg of physical exercise protocol was applied in elder individuals appendicular muscle mass (AMM) compared to the control previously diagnosed with sarcopenia. One possible expla- group. All other 4 studies did not show muscle mass dif- nation resides in lack of power to detect significant differ- ferences compared to control. However, when muscle ences in the other 4 trials, as sample sizes are quite small. quality was analyzed, significant results were found by both Another reason is the duration of resistance training pro- Strasser et al. [6] and Liao et al. [7]. Kim et al. did not access tocols, especially exercise volume of training—defined as the the muscle quality in neither 3 studies. Muscle strength was total work sets per exercise session. Peterson et al. dem- not improved after RT intervention. onstrated that the greater the volume training the greater the Journal of Aging Research 5 Records identified through Manual identification PubMed Titles and abstracts excluded Records screened 19 not sarcopenic elderly 140 not RCT 93 not exercise vs control 26 outcome not sarcopenia Full-text records assessed for eligibility Full-text records excluded 14 not sarcopenic elderly 2 not RCT 1 not exercise vs control Studies included in qualitative synthesis 1 duplicate databese Studies included in quantitative synthesis Figure 1: Flowchart of records retrieved, screened, and included. [6] and Liao et al. [7] Both studies have more robust muscle mass gain [14]. Furthermore, they showed a sig- nificant effect attenuation of physical interventions methodology than those already included in the Yoshimura according to aging, one possible strong explanation for lack review. Its results were also more consistent, showing sig- of exercise training effect. nificant improvement in both muscle mass and muscle In comparison with previous systematic reviews that quality. Furthermore, these both recent RCTs evidenced evaluated the effect of physical exercises over sarcopenia improvements in muscle function in sarcopenic elderly components, published in 2014 [2] and 2017 [3], this present submitted to a resistance training protocol, allowing to review included only RCTs in which physical training hypothesize that exercises may have relevant impact over protocols alone were compared to control groups to improve major geriatric outcomes as falls, immobility, and de- muscle associated outcomes in previously diagnosed sar- pendence. Moreover, Liao et al. showed better results in copenic elderly. Cruz-Jentoft et al. included trials testing the quality of life scores in those randomized to physical exercise. aforementioned interventions in different clinical scenarios, as in frail participants, community-dwelling elderly, and in )e authors decided not to run data meta-analysis to postoperative hip-replacement therapy patients. Regardless identify a single summary effect for each dependent var- of methodological differences between Cruz-Jentoft and this iable as a significant heterogeneity among studies was review, results are similar, i.e., no robust effects were assumed, especially regarding intervention protocols and demonstrated in most included RCTs. )e present search measurement of sarcopenia components. Also noteworthy strategy has resemblance to those used in Yoshimura et al.’s is the small sample sizes included in the clinical trials, systematic review [3]. Although they tried to meta-analyze imputing worrisome power limitations to detect signifi- data to show summary effects for several dependent vari- cant outcome differences. All 5 studies have moderate to ables, most forest plots are provided in less than 3 studies, in high risk of bias in accordance with the Cochrane risk of discordance with meta-analysis guides recommendations. bias tool. Assuming these aforementioned limitations in conjunction with small number of available RCTs, it is not )eoretically, only 2 studies are needed to perform a meta- analysis, but it may carry several important biases as well as recommended to run data meta-analysis due to high risk of statistical inferences especially when random effect models bias as meta-analysis will directly reflect the study biases. are chosen; the number of studies matters, according to Additionally, as described by Borenstein et al. [16], it is Guolo and Varin [15]. Besides that, it is possible to point a very important to avoid “mixing apples and oranges,” significant difference in the Yoshimura et al. study: two more referring to misplaced comparisons by data meta-analysis studies were added to the state of the art regarding physical from theoretically heterogeneous studies, the specific case activity to manage sarcopenia in the elderly—Strasser et al. found in this systematic review. Included Eligibility Screening Identification 6 Journal of Aging Research Table 2: Muscle mass, strength, and muscle quality mean differences between groups. Muscle mass (kg) Muscle strength Muscle quality Mean Mean After Mean Baseline After exercise Baseline After exercise Baseline difference difference exercise difference Study I C I C I C I C I C I C Strasser I: 0.5 & & & & ∗ ∗ ∗ ∗ 17.8 17.7 18.3 18.2 NA NA NA NA NA 10.1 11.5 12.1 9.9 I: 2.0 et al. [6] C: 0.5 Liao et al. I: 0.28 I: 7.57 # # # # £ £ £ £ ∗∗ ∗∗ ∗∗ ∗∗ 36.5 37.0 36.8 36.5 13.6 15.26 21.17 13.59 2.47 2.95 4.07 2.49 I: 1.6 [7] C: − 0.44 C: − 1.67 Kim I: − 2.79 I: 21.4 ∗ ∗ ∗ ∗ 15.79 16.86 13.0 12.9 181.3 197.5 202.7 204.1 NA NA NA NA NA et al.[8] C: − 3.9 6 C: 6.6 Kim et al. I: 1.23 I: − 1.66 $ $ $ $ ∗ ∗ ∗ ∗ 14.79 13.96 14.45 14.11 51.39 47.54 49.73 43.13 NA NA NA NA NA [9] C: − 0.34 C: − 4.41 Kim et al. I: 0.29 I: 0.02 ∗ ∗ ∗ ∗ & & & & 13.9 13.57 14.19 13.67 1.12 1.14 1.14 1.0 NA NA NA NA NA [10] C: 0.1 C: − 0.14 # $ & £ I: intervention; C: control; NA not available; N: Newton; Nm: Newton meter; Nm/kg: Newton meter/kilogram; N/kg” Newton/kilogram; ASM: ∗∗ appendicular skeletal muscle mass; FFM: fat free mass. Table 3: Muscle function mean differences between groups. Walking speed TUG Baseline After exercise Mean difference Baseline After exercise Mean difference Study I C I C I C I C I: 0.02 I: 7.57 Liao et al. [7] 1.51 1.16 1.53 1.14 8.4 9.51 7.08 9.45 C: − 0.02 C: − 1.67 I: 0.2 Kim et al. [8] 1.1 1.1 1.3 1.2 NA NA NA NA NA C: 0.1 I: 0.1 I: − 1.66 Kim et al. [9] 1.26 1.27 1.36 1.26 8.81 8.43 7.03 8.88 C: − 0.01 C: − 4.41 I: 0.19 Kim et al. [10] 1.31 1.19 1.5 1.22 NA NA NA NA NA C: 0.03 I: intervention; C: control; NA: not available; TUG: Timed Up and Go test; walking speed in m/s (meters/second); TUG in s (seconds). Initiative (EWGSOP and IWGS),” Age and Ageing, vol. 43, 4. Conclusions no. 6, pp. 748–759, 2014. [3] Y. Yoshimura, H. Wakabayashi, M. Yamada, H. Kim, Heterogeneity among trials and small number of RCTs A. Harada, and H. Arai, “Interventions for treating sarco- limited robust conclusions and data meta-analysis. How- penia: a systematic review and meta-analysis of randomized ever, resistance training protocols can improve muscle controlled studies,” Journal of the American Medical Directors strength and physical performance in elders previously di- Association, vol. 18, no. 6, pp. 553.e1–553.e16, 2017. agnosed with sarcopenia, although its effect size and clinical [4] A. C. Guerreiro, A. C. Tonelli, R. Orzechowski, R. R. Dalla impact are barely relevant. Two trials were published since Corte, E. H. Moriguchi, and R. B. de Mello, “Bedside ultra- last available systematic review, both of it showing positive sound of quadriceps to predict rehospitalization and func- results of resistance training protocols over muscle quality tional decline in hospitalized elders,” Frontiers in Medicine, and muscle function as well as better results in quality of life vol. 4, p. 122, 2017. scores. [5] D. Moher, A. Liberati, J. Tetzlaff, and D. G. Altman, “Preferred reporting Items for systematic reviews and meta-analyses: the PRISMA statement,” Annals of Internal Medicine, vol. 151, Conflicts of Interest no. 4, pp. 264–269, 2009. [6] E. M. Strasser, M. Hofmann, B. Franzke et al., “Strength )e authors declare that they have no conflicts of interest. training increases skeletal muscle quality but not muscle mass in old institutionalized adults: a randomized, multi-arm parallel and controlled intervention study,” European Journal References Physical and Rehabilitation Medicine, vol. 54, no. 6, pp. 921– 933, 2018. [1] A. J. Cruz-Jentoft, G. Bahat, J. Bauer et al., “Sarcopenia: re- [7] C. D. Liao, J. Y. Tsauo, S. W. Huang, J. W. Ku, D. J. Hsiao, and vised European consensus on definition and diagnosis,” Age T. H. Liou, “Effects of elastic band exercise on lean mass and and Ageing, vol. 48, no. 1, pp. 16–31, 2019. physical capacity in older women with sarcopenic obesity: a [2] A. J. Cruz-Jentoft, F. Landi, S. M. Schneider et al., “Prevalence randomized controlled trial,” Scientific Reports, vol. 8, no. 1, of and interventions for sarcopenia in ageing adults: a sys- p. 2317, 2018. tematic review. Report of the International Sarcopenia Journal of Aging Research 7 [8] H. Kim, M. Kim, N. Kojima et al., “Exercise and nutritional supplementation on community-dwelling elderly Japanese women with sarcopenic obesity: a randomized controlled trial,” Journal of the American Medical Directors Association, vol. 17, no. 11, pp. 1011–1019, 2016. [9] H. Kim, T. Suzuki, K. Saito 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,” Geriatrics & Gerontology In- ternational, vol. 13, no. 2, pp. 458–465, 2013. [10] H. K. Kim, T. Suzuki, K. Saito 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,” Journal of the American Geriatrics Society, vol. 60, no. 1, pp. 16–23, 2012. [11] J. A. C. Sterne, J. Savovic, ´ M. J. Page et al., “RoB 2: a revised tool for assessing risk of bias in randomised trials,” BMJ, vol. 366, Article ID l4898, 2019. [12] M. Borenstein, L. Hedges, J. Higgins, and H. Rothstein, Comprehensive Meta-Analysis Version 3, Biostat Inc., Engle- wood, NJ, USA, 2013. [13] A. P. W. Johnston, M. De Lisio, and G. Parise, “Resistance training, sarcopenia, and the mitochondrial theory of aging,” Applied Physiology, Nutrition, and Metabolism, vol. 33, no. 1, pp. 191–199, 2008. [14] M. D. Peterson, A. Sen, and P. M. Gordon, “Influence of resistance exercise on lean body mass in aging adults,” Medicine & Science in Sports & Exercise, vol. 43, no. 2, pp. 249–258, 2011. [15] A. 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Effects of Physical Exercise Programs on Sarcopenia Management, Dynapenia, and Physical Performance in the Elderly: A Systematic Review of Randomized Clinical Trials

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Copyright © 2019 Renato Gorga Bandeira de Mello et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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10.1155/2019/1959486
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Hindawi Journal of Aging Research Volume 2019, Article ID 1959486, 7 pages https://doi.org/10.1155/2019/1959486 Review Article Effects of Physical Exercise Programs on Sarcopenia Management, Dynapenia, and Physical Performance in the Elderly: A Systematic Review of Randomized Clinical Trials 1,2,3 1,2 4 Renato Gorga Bandeira de Mello , Roberta Rigo Dalla Corte, Joana Gioscia, 1,2,5 and Emilio Hideyuki Moriguchi School of Medicine at the Federal University of Rio Grande do Sul (UFRGS), Department of Internal Medicine, Porto Alegre, Brazil Hospital de Clınicas de Porto Alegre, Section of Internal Medicine, Porto Alegre, Brazil Post-Graduation Studies Program in Endocrinology, UFRGS, Porto Alegre, Brazil School of Medicine at the Federal University of Rio Grande do Sul (UFRGS), Porto Alegre, Brazil Post-Graduation Studies Program in Cardiology and Cardiovascular Sciences, UFRGS, Porto Alegre, Brazil Correspondence should be addressed to Renato Gorga Bandeira de Mello; rgmello@hcpa.edu.br Received 26 July 2019; Accepted 10 October 2019; Published 20 November 2019 Guest Editor: Priscila Sampaio Copyright © 2019 Renato Gorga Bandeira de Mello et al. )is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Introduction. Sarcopenia is a prevalent condition in the elderly population, imposing a significant impact over their functional ability as well as their quality of life. Furthermore, it is associated with greater incidence of major geriatric outcomes, as reduced mobility, falls, loss of independence, cognitive impairment, and all-cause mortality. Physical Exercise Programs directed to improve muscle mass and its function may be key to reduce sarcopenia consequences. However, a significant heterogeneity is found in clinical trials, especially as a consequence of different exercise protocols applied to research subjects. Objectives. To access the effects of physical exercise programs compared to no exercise interventions to improve sarcopenia components and its determinants in sarcopenic elder individuals. Methods. A systematic review was conducted in the Pubmed database to identify randomized clinical trials (RCTs) which tested the effects of physical exercise programs to manage sarcopenia components in sarcopenic elder individuals. Two independent reviewers assessed the studies’ eligibility according to specified inclusion criteria in a four-step strategy. Data regarding population characteristics, muscle mass, muscle quality, muscle strength, and muscle function were extracted from each one of the included studies. Assessment of quality and individual studies risk of bias were assessed through Cochrane Risk of Bias Tool . Assuming theoretical expected heterogeneity among studies, especially regarding different physical exercise programs and different outcome measurements, authors decided to be conservative and present study results in descriptive tables. Results. Search strategy retrieved 298 papers on PubMed database. )ree more were identified through manual search, being 301 studies revised for inclusion. 278 were excluded during title/abstract review. After further evaluation of 23 full- texts, 5 RCTs were included. All 5 trials tested the efficacy of isolated exercise programs to improve sarcopenia components in the elderly compared to no physical intervention. Resistance training was the main intervention component in all included trials compared to inactive control groups (health education mainly). Physical training improved muscle strength, muscle quality, and muscle function compared to inactive control groups. Considering muscle mass, no differences were demonstrated. Data meta- analysis was not possible to be performed due to high heterogeneity among trials and small number of studies for each outcome comparison. Conclusion. Heterogeneity among trials and small number of RCTs limited robust conclusions and data meta- analysis. However, resistance training protocols can improve muscle strength and physical performance in elders previously diagnosed with sarcopenia, although its effect size and clinical impact are barely relevant. 2 Journal of Aging Research )e eligible criteria are predefined by the characteristics of 1. Introduction the primary studies. At this point, it is only necessary to According to the European Working Group on Sarcopenia define the following criteria: the target population, the in- in older people revised consensus, sarcopenia is a skeletal tervention, and the outcomes. Characteristics of the in- muscle disorder in which muscle strength is the key feature cluded study populations, such as intervention types and of a clinical condition with increased risk for major geriatric outcome measure, are presented in Table 1. outcomes [1]. It is a prevalent condition in the elderly, Population: elderly (>65 years) with diagnosed sarco- varying according to age-related variables especially when penia; intervention and control: physical exercise programs different clinical settings where compared. In community- compared to a control group (no exercise); outcomes: sar- dwelling samples, a wide prevalence range was found from copenia, muscle mass, muscle strength, physical perfor- 1% to 29%; and in long-term care facilities, the range is mance, and muscle quality; length of follow-up: not 14–33% [2]. However, it is presumed that this heterogeneity specified; study design: randomized clinical trial. )ere was would be also explained by different applied diagnostic no limitation of gender. )e types of exercises were pre- criteria. dominantly resistance training (Table 1). It is postulated that physical exercise programs can shift sarcopenia clinical course. A systematic review was con- ducted in 2014, and the authors concluded that physical 1.2.2. Search Strategy. A systematic search was conducted in exercise has an impact on improving muscle strength and the PubMed electronic articles database using the following physical performance; however, interventions did not sig- strategy: (((Sarcopenia) AND (Elderly)) AND ((Physical nificantly improved muscle mass. Several limitations were activity) OR (Exercise)) AND (Clinical trial)). No specific pointed out to explain the low impact of exercise in- date limit was defined; no language limitation was imposed; terventions: lack of standardization of exercise protocols, all available studies were included. Last search was con- low duration of interventions, heterogeneity in outcome ducted on June 30th, 2019. For those articles with limited measurements, and selection bias due to heterogeneous access or incomplete data, the authors were contacted di- eligibility criteria. rectly by email. Additional manual search was performed to Most recently, in 2017, the last published systematic increase search sensitivity. review regarding exercise and sarcopenia showed better physical performance after resistance training exercise in- (1) Study Selection and Data Collection Process. Step 1: two tervention, but no improvement in muscle strength [3]. independent reviewers assessed all titles and abstracts to Beyond physical exercise impact on physical performance verify eligibility criteria on Revision. Step 2 included a full- and muscle strength and mass, it is important to access its text revision for further eligibility assessment. Step 3: effects on reducing major geriatric outcomes. Guerreiro et al. duplicates were excluded. Final inclusion results are demonstrated that both muscle mass estimated by bedside presented in the systematic review inclusion flowchart ultrasound and muscle performance and strength in hos- (Figure 1). A standardized Microsoft Office ExcelTM pitalized elderly patients are important predictors for spreadsheet was used to organize independent data col- functional decline, rehospitalization, and death [4]. How- lection. Investigators followed a step by step extraction ever, most clinical trials testing physical exercise in sarco- process according to the PICOTS prespecified strategy, penic elder patients yet do not access its effects over major extracting study ́s population data, followed by in- clinical geriatric outcomes. tervention description, outcomes variables collection, and Considering the aforementioned reasons, the main its main results. objective of this systematic review is to analyze the effec- Quality and individual studies risk of bias were assessed tiveness of physical exercise on improving sarcopenia in through Cochrane Risk of Bias Tool [11] and are presented older populations. Muscle mass, muscle function, muscle in Table 1. strength, and physical resistance improvement in the elderly will be investigated. Furthermore, we will show these effects on the incidence of major geriatric outcomes. 2. Data Analysis Assuming theoretical expected heterogeneity among studies, 1.1. Methods. )is systematic review protocol followed the especially regarding different physical exercise programs and Preferred Reporting Items for Systematic Reviews and Meta- different outcome measurements, authors decided to be Analyses (PRISMA) recommendations [5]. conservative and present study results in descriptive tables. We assumed that lack of studies’ exercise protocols stan- dardization as well as lack of outcomes measurement 1.2. Design: Systematic Review of Randomized Clinical standardization limits data meta-analysis as theoretical Trials (RCTs) homogeneity assumption is not reached. Publication bias was also assessed by trim and fill 1.2.1. Eligibility Criteria. RCT testing effects of physical strategy. Analyses were performed using the software exercise programs were compared to those of a physically Comprehensive Meta-AnalysisTM version 3—free trial inactive control group on sarcopenia clinical variables in [12]. elderly populations previously diagnosed with sarcopenia. Journal of Aging Research 3 Table 1: Basic characteristics of included randomized controlled clinical trials. Outcome Reference Population Design Intervention Control measurement and Main results definition Muscle mass: apendicular lean mass: no significant differences between Measured by DEXA groups Skeletal muscle mass: Muscle quality (Nm/ apendicuar lean mass kg) Strasser 33 women and men Resistance training (ALM in kg) Baseline 6 months et al. [6] (82.4± 6.0 years) with (RT): 12 weeks elastic Control group (CG) RCT Muscle quality: Extension force Moderate impaired health status band resistance (n � 17) isokinetic force RT: 10.1± 2.9 RoB (mostly sarcopenic) training (n � 16) measurement of knee 12.1± 2.6 flexion and extension CG: 11.5± 2.5 9.9± 3.0 (Nm/kg) P � 0.006 Flexion force (MQ) RT: 5.2± 1.4 6.8± 1.0 CG: 5.7± 1.5 5.5± 1.5 P � 0.009 Results presented as mean differences Measured by DEXA between groups (RT- Muscle CG) mass—apendicular Muscle mass (kg) lean Mass (ALM in ALM: 0.99 (0.33, 1.66) kg) P< 0.01 Resistance training Muscle quality (MQ) Liao et al. Muscle quality (N/kg) 56 sarcopenic or obese (RT): 12 weeks of Control group (CG) after lower limb [7] MQ-LE: 1.82 (1.25, women (mean± SD RCT elastic band resistance matched by age muscle flexion (kg/kg) High 2.39) P< 0.01 age 67.3± 5.1 years) training (ERT) (n � 23) Physical capacity and RoB Function (n � 33) function outcomes TUG: − 1.64 (− 2.34, Timed Up and Go − 0.95) P< 0.01 (TUG in s); gait speed GS: 0.14 (0.33, 0.25) (GS in m/s) P< 0.05 Quality of life (qol QoL measured by SF-36) SF-36: 13.62 (6.47, 20.76) P< 0.001 Measured by bioeletrical Resistance training 139 sarcopenic elderly impedance analysis No differences in Kim (RT): 12 weeks elastic women; 69 Control group (CG) (BIA) muscle mass, strength, et al.[8] band for upper limbs randomized to RCT Health education Apendicular skeletal and function were Moderate and ankle weight for resistance training or (n � 34) muscle mass (kg) observed after RoB lower limb training control group Performance intervention (n � 35) TUG; GS; grip strength Measured by Apendicular muscle bioeletrical Resistance training mass: no difference 138 sarcopenic elderly impedance analysis Kim (RT): 12 weeks elastic Performance women; 64 Control group (BIA) et al.[9] band for upper limbs Grip strength: no randomized to RCT (CG): health Apendicular skeletal Moderate and ankle weight for difference resistance training or education (n � 32) muscle mass (kg) RoB lower limb training. GS and TUG: no control group Performance relevant differences (n � 32) TUG; GS; grip found strength 4 Journal of Aging Research Table 1: Continued. Outcome Reference Population Design Intervention Control measurement and Main results definition Measured by Apendicular muscle bioeletrical mass: no difference Exercise group (EG): impedance analysis Walking speed (m/s) 155 sarcopenic elderly 12 weeks combined Kim (BIA) Baseline 6 months women; 78 training—warm up; Control group et al.[10] Apendicular skeletal EG: 1.31± 0.24 randomized to RCT strengthening (CG): health Moderate muscle mass (kg) 1.50± 0.23 P � 0.007 exercise group or exercise, balance and education (n � 39) RoB Performance CG: 1.19± 0.21 control group gait training, and cool Walking speed, knee 1.22± 0.23 down. (n � 39) extension strength Strength: no (Nm/kg) difference RCT �randomized clinical trial; RoB: risk of bias; in accordance with Cochrane’s risk of bias tool. 2.1. Results. A total number of 298 studies were retrieved by RT exercise protocols significantly improved the muscle search strategy application on PubMed database. )ree more function measured by gait speed (GS) as well as by the Timed studies were found in a previous meta-analysis and included Up and Go test (TUG) in 3 of 5 studies as described in in the next step [3]. 278 studies were excluded in the Step 1 Table 3. Kim et al. [8, 9] did not evidence the muscle function improvement after RT. reviewing process. In Step 2, 23 full-text articles were reviewed for further eligibility evaluation and 18 were ex- In [7], quality of life was accessed before and after ex- cluded. )e reasons for the exclusion of these studies are ercise interventions and it was possible to show significant described in the flowchart of Figure 1. Finally, 5 randomized improvement in QoL in the RT group when compared to clinical trials were included in this present systematic review control (mean difference 13.62 (6.47, 20.76); P< 0.001), as described in the inclusion flowchart (Figure 1). especially a relevant difference in the physical component of Table 1 presents study details regarding population, the SF-36 questionnaire. study design, interventions, control groups, outcome mea- surements, and main results [6–10]. 3. Discussion All five studies have high to moderate risk of bias according to Cochrane’s risk of bias tool. In three studies In this systematic review to assess the effectiveness of ex- conducted by Kim et al., direct comparison of physical ercise training to improve sarcopenia-related outcomes in training against inactive control is only possible in a study sarcopenic elder populations, a sensitive search strategy subsample composed by two different intervention groups retrieved 301 studies on PubMed database. During the first (exercise versus health education groups). step review process, 278 papers were excluded and 23 more Different measurement protocols were applied to as- were excluded after full-paper review, leading to 5 RCTs to sess outcomes among studies. In two studies—Strasser be included in this study. et al. [6] and Liao et al. [7]—dual-energy X-ray absorp- RCTs results according to sarcopenia component varied tiometry was used to measure muscle mass as well as significantly. Only one study evidenced muscle mass gain; muscle quality. All studies conducted by Kim et al. [8–10] muscle quality, on the other hand, was improved in both measured these variables using bioelectrical impedance studies that this factor was measured. Although effects over analysis. muscle strength and muscle mass were not clear, muscle function—walking speed and Timed Up and Go test—was homogeneously improved among studies, but the size effect seems to be limited. 2.2. Main Results However, it is presumed that resistance training prevents 2.2.1. Muscle Mass, Muscle Quality, Strength, and Function. muscle mass wasting because it stimulates muscle hyper- Results regarding muscle mass, muscle strength, and muscle trophy and increases muscle strength, as postulated by quality are summarized in Table 2. Muscle mass was only Johnston et al. [13], and also it is postulated that resistance significantly improved in the RCT conducted by Liao et al. training is a key strategy to treat sarcopenia; only one clinical [7] Sarcopenic elder patients submitted to 12 weeks in- trial [7] evidenced improvement of muscle mass after a tervention of resistance training (RT) gained almost 1 kg of physical exercise protocol was applied in elder individuals appendicular muscle mass (AMM) compared to the control previously diagnosed with sarcopenia. One possible expla- group. All other 4 studies did not show muscle mass dif- nation resides in lack of power to detect significant differ- ferences compared to control. However, when muscle ences in the other 4 trials, as sample sizes are quite small. quality was analyzed, significant results were found by both Another reason is the duration of resistance training pro- Strasser et al. [6] and Liao et al. [7]. Kim et al. did not access tocols, especially exercise volume of training—defined as the the muscle quality in neither 3 studies. Muscle strength was total work sets per exercise session. Peterson et al. dem- not improved after RT intervention. onstrated that the greater the volume training the greater the Journal of Aging Research 5 Records identified through Manual identification PubMed Titles and abstracts excluded Records screened 19 not sarcopenic elderly 140 not RCT 93 not exercise vs control 26 outcome not sarcopenia Full-text records assessed for eligibility Full-text records excluded 14 not sarcopenic elderly 2 not RCT 1 not exercise vs control Studies included in qualitative synthesis 1 duplicate databese Studies included in quantitative synthesis Figure 1: Flowchart of records retrieved, screened, and included. [6] and Liao et al. [7] Both studies have more robust muscle mass gain [14]. Furthermore, they showed a sig- nificant effect attenuation of physical interventions methodology than those already included in the Yoshimura according to aging, one possible strong explanation for lack review. Its results were also more consistent, showing sig- of exercise training effect. nificant improvement in both muscle mass and muscle In comparison with previous systematic reviews that quality. Furthermore, these both recent RCTs evidenced evaluated the effect of physical exercises over sarcopenia improvements in muscle function in sarcopenic elderly components, published in 2014 [2] and 2017 [3], this present submitted to a resistance training protocol, allowing to review included only RCTs in which physical training hypothesize that exercises may have relevant impact over protocols alone were compared to control groups to improve major geriatric outcomes as falls, immobility, and de- muscle associated outcomes in previously diagnosed sar- pendence. Moreover, Liao et al. showed better results in copenic elderly. Cruz-Jentoft et al. included trials testing the quality of life scores in those randomized to physical exercise. aforementioned interventions in different clinical scenarios, as in frail participants, community-dwelling elderly, and in )e authors decided not to run data meta-analysis to postoperative hip-replacement therapy patients. Regardless identify a single summary effect for each dependent var- of methodological differences between Cruz-Jentoft and this iable as a significant heterogeneity among studies was review, results are similar, i.e., no robust effects were assumed, especially regarding intervention protocols and demonstrated in most included RCTs. )e present search measurement of sarcopenia components. Also noteworthy strategy has resemblance to those used in Yoshimura et al.’s is the small sample sizes included in the clinical trials, systematic review [3]. Although they tried to meta-analyze imputing worrisome power limitations to detect signifi- data to show summary effects for several dependent vari- cant outcome differences. All 5 studies have moderate to ables, most forest plots are provided in less than 3 studies, in high risk of bias in accordance with the Cochrane risk of discordance with meta-analysis guides recommendations. bias tool. Assuming these aforementioned limitations in conjunction with small number of available RCTs, it is not )eoretically, only 2 studies are needed to perform a meta- analysis, but it may carry several important biases as well as recommended to run data meta-analysis due to high risk of statistical inferences especially when random effect models bias as meta-analysis will directly reflect the study biases. are chosen; the number of studies matters, according to Additionally, as described by Borenstein et al. [16], it is Guolo and Varin [15]. Besides that, it is possible to point a very important to avoid “mixing apples and oranges,” significant difference in the Yoshimura et al. study: two more referring to misplaced comparisons by data meta-analysis studies were added to the state of the art regarding physical from theoretically heterogeneous studies, the specific case activity to manage sarcopenia in the elderly—Strasser et al. found in this systematic review. Included Eligibility Screening Identification 6 Journal of Aging Research Table 2: Muscle mass, strength, and muscle quality mean differences between groups. Muscle mass (kg) Muscle strength Muscle quality Mean Mean After Mean Baseline After exercise Baseline After exercise Baseline difference difference exercise difference Study I C I C I C I C I C I C Strasser I: 0.5 & & & & ∗ ∗ ∗ ∗ 17.8 17.7 18.3 18.2 NA NA NA NA NA 10.1 11.5 12.1 9.9 I: 2.0 et al. [6] C: 0.5 Liao et al. I: 0.28 I: 7.57 # # # # £ £ £ £ ∗∗ ∗∗ ∗∗ ∗∗ 36.5 37.0 36.8 36.5 13.6 15.26 21.17 13.59 2.47 2.95 4.07 2.49 I: 1.6 [7] C: − 0.44 C: − 1.67 Kim I: − 2.79 I: 21.4 ∗ ∗ ∗ ∗ 15.79 16.86 13.0 12.9 181.3 197.5 202.7 204.1 NA NA NA NA NA et al.[8] C: − 3.9 6 C: 6.6 Kim et al. I: 1.23 I: − 1.66 $ $ $ $ ∗ ∗ ∗ ∗ 14.79 13.96 14.45 14.11 51.39 47.54 49.73 43.13 NA NA NA NA NA [9] C: − 0.34 C: − 4.41 Kim et al. I: 0.29 I: 0.02 ∗ ∗ ∗ ∗ & & & & 13.9 13.57 14.19 13.67 1.12 1.14 1.14 1.0 NA NA NA NA NA [10] C: 0.1 C: − 0.14 # $ & £ I: intervention; C: control; NA not available; N: Newton; Nm: Newton meter; Nm/kg: Newton meter/kilogram; N/kg” Newton/kilogram; ASM: ∗∗ appendicular skeletal muscle mass; FFM: fat free mass. Table 3: Muscle function mean differences between groups. Walking speed TUG Baseline After exercise Mean difference Baseline After exercise Mean difference Study I C I C I C I C I: 0.02 I: 7.57 Liao et al. [7] 1.51 1.16 1.53 1.14 8.4 9.51 7.08 9.45 C: − 0.02 C: − 1.67 I: 0.2 Kim et al. [8] 1.1 1.1 1.3 1.2 NA NA NA NA NA C: 0.1 I: 0.1 I: − 1.66 Kim et al. [9] 1.26 1.27 1.36 1.26 8.81 8.43 7.03 8.88 C: − 0.01 C: − 4.41 I: 0.19 Kim et al. [10] 1.31 1.19 1.5 1.22 NA NA NA NA NA C: 0.03 I: intervention; C: control; NA: not available; TUG: Timed Up and Go test; walking speed in m/s (meters/second); TUG in s (seconds). Initiative (EWGSOP and IWGS),” Age and Ageing, vol. 43, 4. Conclusions no. 6, pp. 748–759, 2014. [3] Y. Yoshimura, H. Wakabayashi, M. Yamada, H. Kim, Heterogeneity among trials and small number of RCTs A. Harada, and H. Arai, “Interventions for treating sarco- limited robust conclusions and data meta-analysis. How- penia: a systematic review and meta-analysis of randomized ever, resistance training protocols can improve muscle controlled studies,” Journal of the American Medical Directors strength and physical performance in elders previously di- Association, vol. 18, no. 6, pp. 553.e1–553.e16, 2017. agnosed with sarcopenia, although its effect size and clinical [4] A. C. Guerreiro, A. C. Tonelli, R. Orzechowski, R. R. Dalla impact are barely relevant. Two trials were published since Corte, E. H. Moriguchi, and R. B. de Mello, “Bedside ultra- last available systematic review, both of it showing positive sound of quadriceps to predict rehospitalization and func- results of resistance training protocols over muscle quality tional decline in hospitalized elders,” Frontiers in Medicine, and muscle function as well as better results in quality of life vol. 4, p. 122, 2017. scores. [5] D. Moher, A. Liberati, J. Tetzlaff, and D. G. Altman, “Preferred reporting Items for systematic reviews and meta-analyses: the PRISMA statement,” Annals of Internal Medicine, vol. 151, Conflicts of Interest no. 4, pp. 264–269, 2009. [6] E. M. Strasser, M. Hofmann, B. Franzke et al., “Strength )e authors declare that they have no conflicts of interest. training increases skeletal muscle quality but not muscle mass in old institutionalized adults: a randomized, multi-arm parallel and controlled intervention study,” European Journal References Physical and Rehabilitation Medicine, vol. 54, no. 6, pp. 921– 933, 2018. [1] A. J. Cruz-Jentoft, G. Bahat, J. Bauer et al., “Sarcopenia: re- [7] C. D. Liao, J. Y. Tsauo, S. W. Huang, J. W. Ku, D. J. Hsiao, and vised European consensus on definition and diagnosis,” Age T. H. Liou, “Effects of elastic band exercise on lean mass and and Ageing, vol. 48, no. 1, pp. 16–31, 2019. physical capacity in older women with sarcopenic obesity: a [2] A. J. Cruz-Jentoft, F. Landi, S. M. 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