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Inicio Endocrinología, Diabetes y Nutrición (English ed.) Effects of physical exercise in sarcopenia. A systematic review
Journal Information
Vol. 68. Issue 3.
Pages 159-169 (March 2021)
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3031
Vol. 68. Issue 3.
Pages 159-169 (March 2021)
Original article
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Effects of physical exercise in sarcopenia. A systematic review
Efectos del ejercicio físico en el anciano con sarcopenia. Una revisión sistemática
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3031
David E. Barajas-Galindoa,
Corresponding author
dabarajas@saludcastillayleon.es

Corresponding author.
, Elena González Arnáiza, Pablo Ferrero Vicenteb, María D. Ballesteros-Pomara
a Unidad de Nutrición Clínica y Dietética, Departamento de Endocrinología y Nutrición, Complejo Asistencial Universitario de León, León, Spain
b Departamento de Medicina de Familia, Área Asistencial de León, León, Spain
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Tables (5)
Table 1. Inclusion and exclusion criteria of the articles reviewed.
Table 2. Methodological quality of articles included in the systematic review.
Table 3. Main variables recorded in the articles analyzed in the review.
Table 4. Exercise protocol in studies included in the systematic review.
Table 5. Results in the main variables in articles included in the review.
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Abstract

From the third decade of life and due to multiple causes, muscle mass and strength are gradually lost, which affects the function of the musculoskeletal system.

This combined loss of muscle mass and strength with aging is called sarcopenia, and is associated with greater morbidity and mortality in the elderly. Early treatment is therefore essential, and physical exercise is the therapeutic approach that has given the best results.

This literature review intended to analyze the effect of physical exercise, excluding the role that other treatments proposed, including the nutritional approach, could play in the treatment of sarcopenia, refers to 12 articles.

In studies including high intensity strength exercises in isolation, either alone or combined with aerobic exercise, improvements were seen in muscle mass, muscle strength, and functional test times. There is also a significant increase in fat-free mass in individuals who exercised more frequently (more than two sessions per week).

Current evidence shows that strength-resistance training and its combination in multimodal programs with aerobic exercise show significantly beneficial effects on anthropometric and muscle function parameters. Programs of prescribed exercises including strength exercises adequate to the characteristics should therefore be adapted to the characteristics of each individual and replace the usual practice of prescribing aerobic exercises (walking) only.

Keywords:
Sarcopenia
Physical exercise in elderly
Elderly
Older adults
Resumen

A partir de la tercera década de la vida, y por causas multifactoriales, se pierde masa y fuerza muscular de forma progresiva, afectando a la funcionalidad del aparato locomotor.

A esta pérdida combinada de masa y fuerza muscular que aparece con el envejecimiento se le denomina sarcopenia, la cual se asocia a una mayor morbimortalidad en el sujeto anciano, por lo que el tratamiento precoz es fundamental, siendo el ejercicio físico la estrategia terapéutica que mejores resultados ha demostrado.

En esta revisión bibliográfica realizada para analizar el efecto individual del ejercicio físico, excluyendo el papel que podría representar en el tratamiento de la sarcopenia otras propuestas desde el enfoque nutricional, se incluyen 12 artículos.

En aquellos estudios que incluían ejercicios de fuerza de alta intensidad de forma aislada, exclusivamente o combinado con ejercicio aeróbico, se observa mejoría de la masa muscular, fuerza muscular y tiempos en pruebas funcionales. Existe asimismo un incremento significativo de masa libre de grasa en individuos que realizaban ejercicio con mayor frecuencia (más de 2 sesiones a la semana).

La evidencia actual demuestra que los entrenamientos basados en fuerza-resistencia y la combinación en programas multimodales con ejercicio aeróbico muestran efectos significativamente beneficiosos sobre parámetros antropométricos y de funcionalidad muscular, debiendo por tanto adecuarse los programas de ejercicios pautados, incluyendo ejercicios de fuerza adaptados a las características de cada individuo, y sustituir a la práctica habitual de prescribir en exclusiva ejercicios de tipo aeróbico (caminar).

Palabras clave:
Sarcopenia
Ejercicio en anciano
Deporte en anciano
Envejecimiento activo
Full Text
Introduction

The key feature of human aging is the loss of functional reserve.1,2 Since the third decade of life, the musculoskeletal system begins to experience a slow but progressive loss of muscle mass and strength. From 50 years of age, muscle mass decreases by 1%–2% a year, and muscle strength decreases by 1.5%–3% annually from 65 years of age.2 These physical and functional changes vary between sexes, with progression being slower in men and sharper in women, which is probably related to the coexistence of menopause.2,3

The term sarcopenia has recently been used to refer to this combined loss of muscle mass and strength associated with aging,4 with the added characteristic that such loss should be involuntary.2 A close relationship has been shown between a decreased muscle mass and an increased risk of institutionalization and mortality, regardless of other associated risk factors,5 and also with dependence, which increases 2–5-fold in subjects with sarcopenia as compared to subjects of the same age without this diagnosis.6

One of the main problems for incorporation of the term sarcopenia into daily clinical practice is the lack of a unified criterion for defining sarcopenia,7 because although there is agreement that muscle mass loss should be sufficient to cause symptoms8 and that the definition of sarcopenia should include three criteria: loss of muscle mass, loss of strength, and qualitative changes in muscle tissue,1 there is no accepted standard method for measuring muscle mass, and the level of loss of muscle mass and/or function from which an elderly person may be considered “pathologically sarcopenic” is also not clearly established.

Diagnosis of sarcopenia is therefore complex, and has been quite often based on the consensus criteria established by the European Working Group on Sarcopenia in Older People9 in 2018, in which sarcopenia is diagnosed in three steps: an initial screening test (SARC-F), followed by a strength test to establish the probability of sarcopenia, and finally a confirmatory test with of muscle mass assessment. There is also a complementary fourth step to assess severity of sarcopenia with function tests. The consensus criteria proposed in 2009 by the International Working Group in Sarcopenia consisting of a walking speed below 1 m/s and an objective decrease in muscle mass have also been used.10

Despite these difficulties to define the condition, it is clear that aging of the population has increased the importance and interest of this clinical situation, leading to an increase in therapeutic efforts aimed at preventing and/or reversing sarcopenia. This treatment approach focuses on three mainstays:

  • 1.

    Nutritional intervention based on covering the calorie and protein requirements of each individual, with supplemental supplies if required.11

  • 2.

    Pharmacological intervention such as use of vitamin D, testosterone or growth hormone, that has been ineffective or even counterproductive in various studies due to adverse effects in the elderly population.

  • 3.

    Physical exercise, which has been shown to be a very useful tool for fighting and preventing sarcopenia and is not contraindicated in elderly people when duly adapted.12 When considering a training program for the treatment of sarcopenia, it should be taken into account that there are different types of exercise, and a unique or mixed program may be planned combining the different types of exercise.

Aerobic exercise is continuous activity of several muscle groups that increases heart rate above its resting level for a sustained period of time, and should be adjusted based on maximum heart rate (HRmax). In an exercise program for elderly patients, an intensity of activity at 60%–75% of HRmax for 30 min three days a week is recommended.13

Strength exercise is an activity in which muscle builds strength against resistance. Depending on its intensity, there are other three subtypes14: low intensity, <40% of a maximum repetition (maximum weight with which a single repetition can be performed [1MR]); moderate intensity, = 40%–60% of 1RM; and high intensity, >60% of 1MR.

Neuromuscular exercise is the activity that works with balance and proprioception with the aim of improving posture and preventing falls. Exercises may be static or dynamic.

Objectives

The primary objective of this systematic review is to assess the effect of different types of physical exercise on sarcopenia. For this, the concept of sarcopenia is defined, the implications of this condition for health are detailed, and the type, frequency, and dosage of exercise are assessed to determine changes in muscle mass and strength.

Methods

A systematic review. An initial search was made in the Pubmed database using the keywords exercise, sarcopenia and elderly. The advanced search was adjusted to studies published in the last 10 years (2008–2018), clinical trials, and studies conducted in humans.

The search strategy was as follows: (exercise [MeSH Terms] OR exercise [All Fields]) AND (sarcopenia [MeSH Terms] OR sarcopenia [All Fields]) AND (aged [MeSH Terms] OR aged [All Fields] OR elderly [All Fields]) AND (Clinical Trial [ptyp] AND 2008/01/01 [PDat]: 2018/12/31 [PDat] AND humans [MeSH Terms]).

The following databases were subsequently reviewed: Scopus, Scielo, and Web Science.

After an initial review of the abstracts, the full text of the articles that met the inclusion criteria were examined. The articles selected because they complied with the inclusion and exclusion criteria (Table 1) were evaluated using the PEDro scale15 to determine their methodological quality.

Table 1.

Inclusion and exclusion criteria of the articles reviewed.

Inclusion criteria  Exclusion criteria 
Studies assessing people with sarcopenia  Studies relating sarcopenia to other diseases 
Sample of subjects aged ≥65 years  Studies including oral nutritional supplements as treatment 
Studies published between 2008 and 2018  Studies in languages other than Spanish or English 
Studies with clinical trial design  Studies not conducted in humans 
Studies including strength, resistance, balance, aerobic, or mixed physical exercises  Studies not using exercise alone as treatment (nutritional support or vibrating platforms) 

Methodological quality was also determined using other methods such as the number of citations received, the impact factor, the quartile, or the SCImago Journal Rank (Table 2).

Table 2.

Methodological quality of articles included in the systematic review.

Articles  PEDro  References  Quartile  IF  SJR 
Mueller et al.27, 2009  92  2.401  1.263 
Kemmler et al.23, 2010  78  4.127  2.680 
Kemmler et al.19, 2013  43  3.077  1.308 
Cadore et al.16, 2013  218  –  2.9  – 
Fragala et al.17, 2014  52  3.224  1.261 
Reid et al.24, 2014  80  4.902  2.489 
Liu et al.14, 2014  64  2.517  0.919 
González et al.26, 2013  11  2.121  0.750 
Hong et al.25, 2016  3.224  1.261 
Piastra et al.20, 2018  2.583  0.795 
Chen et al.30, 2018  3.224  1.261 
Wu et al.21, 2018  2.656  0.905 

IF: impact factor; SJR: SCImago Journal Rank.

The flow chart shows the procedure for selecting the 12 articles making up the final sample of this systematic review (Fig. 1).

Figure 1.

Flowchart for selecting studies for systematic review based on exclusion and inclusion criteria.

(0.08MB).

The parameters most commonly studied by the publications included in our study are muscle mass (MM), muscle strength (MS), and physical tests.

Given the variability of parameters included in the articles, only the most important variables are included methodologically in this description:

Morphological variables were assessed based on:

  • Body fat: assessed by measurement of skin folds and/or bioimpedance.

  • Fat-free mass or lean body mass (LBM): includes intra- and extracellular water, the bone mineral system, and muscle and visceral proteins. This was assessed by densitometry (DXA) or electrical bioimpedance (BIA).

  • MM: assessed by computed tomography, DXA, or BIA.

  • Appendicular MM: the sum of the lean mass of the legs and arms. It was assessed by DXA or BIA

  • MS: assessed using a dynamometer.

Functional test variables were assessed using:

  • Timed up and go: this assesses if the subject is able to rise from a chair with armrests, walk three meters, turn, walk back those three meters, and down sit again.16–18

  • Short Physical Performance Battery: this consists of three physical tests, a balance test, a short walk (4 m) at the usual pace, and rising from a chair five consecutive times. Score ranges from 0 (lowest) and 12 (best).16,19

  • Chair rise test: this consists of measuring over 30 s how many times can a subject sit down on and rise from a chair.16,17

  • Walking speed: time taken to walk five meters at a normal pace.16,20

Results

Twelve articles were selected in this systematic review, and were analyzed and compared. All of them were prospective, randomized clinical trials except for the Wu et al. study,21 which was not randomized, and the retrospective analysis of data collected in the SEFIP study,22 published by Kemmler et al.23

Because of the great variability of outcome variables analyzed in the different studies, only the most common and relevant variables, grouped in the categories of muscle power, contraction speed, muscle strength, muscle mass, neuromuscular activation, physical tests, cross-sectional area of muscle (CSA), metric contraction tests (MVIC), muscle quality index, extrinsic coordination, body fat, MBL, adherence, and stability were selected. Table 3 shows assessment of these variables in each of the studies evaluated in this review.

Table 3.

Main variables recorded in the articles analyzed in the review.

Articles variables  Mueller et al.27 (2009)  Kemmler et al.23 (2010)  Kemmler and von Stengel19 (2013)  Cadore et al.16 (2013)  Fragala et al.17 (2014)  Reid et al.24 (2014)  Liu et al.14 (2014)  González et al.26 (2013)  Hong et al.25 (2016)  Piastra et al.20 (2018)  Chen et al.3 (2018)  Wu et al.21 (2018) 
Muscle power                     
Contraction rate                         
Muscle strength       
Muscle mass     
Neuromuscular activation                       
Physical tests       
CSA                     
MVIC                         
Muscle quality                     
Eccentric coordination                       
Body fat                 
LBM               
Adherence                     
Stability                   

CSA: cross-sectional area of muscle; LBM: lean body mass; MVIC: contraction tests.

The training programs of the different studies were mainly based on two types of exercise: strength-only exercises17,19,24 and multimodal exercises,25,26 the latter including combinations of neuromuscular,16 resistance, and aerobic exercises, among which walking was the usual exercise of choice.17

Table 4 gives a detailed description of the training protocols of each study, including their duration and number of weekly sessions. The training performed by the control group in studies intended to compare the efficacy of different training systems is also detailed where appropriate. In studies where training of the control group is not detailed, this group does not perform exercise.

Table 4.

Exercise protocol in studies included in the systematic review.

Article  Duration (weeks)  Frequency  Description of training 
Mueller et al.27 (2009)  12  Twice weekly (45 min)  EG: 4 LL exercises (leg press, knee extension, leg flexion, and hip extension); activation + gymnastics for 10 min; 20 min training (individual loads in first 6 sessions, then gradually increasing); cooling + stretching for 10 min 
      CG: activation for 10 min, training for 5 min, with a gradual increase in time by 5-min periods to 20 min and in load volume 
Kemmler et al.23 (2010)  72  2–4 times per week (20–60 min)  EG: 3 exercises with elastic bands (high and low rowing and shoulder raise). 65%–70% of 1MR. In addition to 20 min of aerobic exercise and isometric exercises 
Kemmler and von Stengel19 (2013)  72  60 min per session  EG: HF ≥ 2 sessions/week and LF < 2 sessions/week 
      CG: <20 sessions/18 months 
      Exercises: supervised: resistance, coordination, isometric strength, functional gymnastics, flexibility, and dynamic strength; unsupervised: resistance, balance, and flexibility 
Cadore et al.16 (2013)  12  Twice weekly (40 min)  EG: machines and multicomponents: 8/10 repeats (40%–60% 1RM) 
      Exercises: (1) knee extension; (2) hip extension; (3) chest press 
      In addition to walking, balance, and flexibility exercises 
Fragala et al.17 (2014)  12  Twice weekly (60–90 min)  EG: machines, dumbbells, and body weight (3 × 8–15) 
      Exercises: knee extension, knee flexion, rowing, pull, biceps and triceps curl, chest and shoulder press. Bodyweight exercises: squats, displacements, abdominals, heel raising, and deadlift 
Reid et al.24 (2014)  16  Twice weekly  EG: machines: 2 exercises at high and low intensity are compared in concentric phase 
      Exercises: (1) leg press; (2) knee extension. 
      Low intensity: 3 × 10 (40% 1RM). High intensity 3 × 10 (70% 1RM) 
Liu et al.14 (2014)  +24  Twice weekly  EG: multimodal exercise protocol: flexibility, balance, strength, and aerobic exercise 
      Basically focused on walking 
González et al.26 (2013)  Twice weekly (60 min)  EG: 2 sessions/week. Two previous test sessions 
      Exercises: 3 sets of each exercise; 8–15 repeats of each. Squats, knee lift, kicks, torso rotation, arm rotations 
Hong et al.25 (2016)  12  3 times per week (20–40 min)  EG: 3 sessions/week for 12 weeks 
      Exercises: using video console games; 5 min heating, 10–30 min of exercise, 5 min to return to normal. Biceps, triceps and leg curls, squat, leg lift 
Piastra et al.20 (2018)  36  Twice weekly (60 min)  RE: 15 min of warming and motor coordination exercise, 30 min of low/moderate intensity muscle toning with weights of 0.5–1–1.5 kg, 15 min of muscle stretching 
      PE: 15 min of cardiovascular activation, mobilization of hip and shoulder joints, 15 min of mobilization of neck and shoulders, 30 min of mobilization of spine, abdominal muscles, buttocks, hamstrings, and psoas. Spine stretching and final relaxation 
Chen et al.30 (2018)  12  60 min each session, twice weekly. Each separate session 48 h  EG: 2 sessions/week for 8 weeks, then 4 weeks off 
      Exercises: 5 movements per session. For each exercise, 3 sets of 8–12 repeats. Movements: kettlebell swing, kettlebell deadlift, kettlebell goblet squat, squat lunge, kettlebell row, single arm kettlebell row, biceps curl, triceps extension, two-arm kettlebell military press. Turkish get up and comprehensive dynamic workout 
Wu et al.21 (2018)  12  90 min each session, twice weekly  EG: 2 sessions/week for 12 weeks 
      Exercises: using video console games. Combination of strength exercise with elastic band and core on mat with balance training 

LL: lower limbs; PE: postural exercise; RE: resistance exercise; CG: control group; EG: experimental group.

Table 5 lists each of the articles examined for this review and provides details on the sample size, age, and sex distribution of participants, and description and duration of the intervention. The last column summarizes the most significant results as regards the impact of exercise prescribed in sarcopenia, assessed as changes in MM and/or MS and/or functional tests.

Table 5.

Results in the main variables in articles included in the review.

Article and year  Sample  Methods  Study parameters  Results 
Mueller et al.27 (2009)  T: 62  - EG1: (RET)  - MM (CT)  Subjects improved in TUG regardless of their group, but there were no improvements in BBS 
  ♂: 26  - EG2: (EET)  - FT (TUG and Berg Balance Scale)  MM: significantly increased for the RET and TSE groups, but not for the CG group 
  ♀: 36  - CG: (cognitive training)  - Body fat  Body fat: reduction in total body fat and skin folds 
  Age: 71–89 years  Intervention time: 12 weeks     
Kemmler et al.24 (2010)  T: 227  - EG1: (RE + WB-EMS)  - MM (DEXA)  Significant improvements in parameters tested in the RE group as compared to the control group 
  ♀: 227  - EG2: (RE)  - MS (K flex. + isometric dynamometer)  Body fat: total fat and thigh fat reduction 
  Age: 69 ± 4 years  - CG  - FT (TUG)   
    Intervention time: 72 weeks  - Body fat   
Cadore et al.16 (2013)  T: 24  - EG1: (RE + CnF [40%−60% 1RM] + multimodal)  - MM (CT)  MM: significant improvement with RE 
  ♂: 7  - CG (mobility exercises)  - MS (grip, K ext. and H flex. with isomet. dynamom. + CP and LLP with dynamic 1MR)  MS: improvement in RE in both isometric and with dynamometer 
  ♀: 17  Intervention time: 12 weeks  - FT (TUG, chair rise, walking speed)  FT: significant increase with RE CSA: significant changes seen 
  Age: 89−96 years    - CSA (CT)   
Kemmler et al.19 (2013)  T: 227  - EG (115): EG-HF (79) and EG-LF (36)  - LBM, ASMM (DXA)  LBM: significant increase in LBM in EG-HF and little increase in EG-LF 
  ♀: 227  - CG (112)    ASMM: non-significant increase in EG-HF and significant decrease in EG-LF 
  Age ≥65 years  Intervention time: 18 months     
Reid et al.24 (2014)  T: 52  - EG1: (high intensity RE + CnF; 70%)  - MM (CT)  MM: n/s 
  ♂: 19  - CG (low intensity RE + CnF; 40%)  - MS (1RM in K ext. R and LLP)  MS: significant improvement in both groups. No differences between groups 
  ♀: 33    - FT (SPPB)  FT: significant improvement in both groups. No differences between groups 
    Intervention time: 16 weeks  - CSA (CT)  CSA: gains of 5%–12% 
  Age: 73−83 years       
Fragala et al.17 (2014)  T: 23  - EG1: (RE + detraining)  - MM (DEXA)  RE and CON: increase in FT, walking speed, chair rise 
  ♂: 13  - CG: (RE)  - MS (grip dynamometer)  Detraining and CON: increase in FT, walking speed, chair rise 
  ♀: 10  Intervention time: 12 weeks  - FT (TUG, chair rise, walking speed)   
  Age: 70.5 ± 6 years    - LBM   
Liu et al.14 (2014)  T: 177  - EG1: (RE [strength, flexibility, aerobic exercise])  - MM (DEXA)  This study only analyzed the FT parameter, which improved after 24 weeks with RE as compared to the CON group. 
  ♂: 51  - CG: (ED)  - MS (dynamometer)   
  ♀: 126    - FT (SPPB + walking speed)   
  Age: 76.5 ± 4 years    - Body fat   
González et al.26 (2013)  T: 23  - EG: RET  Static balance assessment (in seconds)  EG: improved static balance 
  ♂: 12  - CG: BADL    CG: worsening of static balance 
  ♀: 11  Intervention time: 6 weeks     
  Age: 70 ± 5 years       
Hong et al.25 (2016)  T: 23  - EG (11): RE (with video console)  - MM (DEXA)  Significant improvement in MMI and AMMI 
  ♂: 10/♀: 13  - CG (12)  - Senior fitness test (SFT): speed, chair stand, arm curl test  Significant improvement in chair stand 
  Age: 69-93 years  Intervention time: 12 weeks     
Piastra et al.20 (2018)  T: 66  - EG (33): RE  - LBM, MM, MMI (BIA)  LBM, MM, MMI, and FS: significant improvement with RE 
  ♀: 66  - CC (33): PE  - MS (dynamometer)  Balance: decrease with RE and increase with PE with eyes closed; with eyes open, decrease in RE and no difference in PE 
  Age ≥65 years    - Balance (SFP)  Balance time: increase with RE with eyes both open and closed; decrease with PE with eyes closed 
    Intervention time: 36 weeks     
Chen et al.30 (2018)  T: 33  - EG: FIT (KT) + detraining  - Body composition: peso, MM, FM, AMMI }  In EG: statistically significant increase in MM, AMMI, ASM/m2, and MS in both weeks 8 and 12 as compared to CG 
  ♀: 33  - CG: BADL  - Sarcopenia (ASM/m2 
  Age: 65-75 years  Intervention time: 12 weeks  MS: manual and back dynamometer}   
Wu et al.21 (2018)  T: 17  - EG (6): ER + PE + BE (with video console)  - MS (dynamometer)  Improvement in hand grip dynamometer and timed up and go test 
  ♂: 12  - CG (7)  - FT: Up and go, 6 min walk test   
  ♀: 5  Intervention time: 12 weeks     
  Age ≥65years       

BADL: basic activities of daily living; ASMM: appendicular skeletal muscle mass; BIA: bioelectrical impedance analysis; CSA: cross-sectional area of muscle; Cniso: isometric contraction; CnS: slow contraction; CnF: Fast contraction; DEXA: dual X-ray absorptiometry; BE: balance exercise; EET: eccentric exercise; ED: education group; PE: postural exercise; RE: resistance exercise; H ext.: hip extension; K ext.: knee extension; Ex. S: explosive strength; IS: isometric strength; MS: muscle strength; FIT: fitness; K flex.; knee flexion; CG: control group; EG-HF: experimental group-high frequency; EG: experimental group; EG-LF: experimental group-low frequency; MMI: muscle mass index; LBM: lean body mass; MM: muscle mass; MVIC: isometric contraction test; FT: functional test; SFP: static force platform; LLP: lower limb press; CP: chest press; RET: conventional resistance exercise; RM: maximum repetition; MRI: magnetic resonance imaging; SL: high intensity strength/high volume; SPPB: short physical performance battery; SS: high intensity strength/low volume; CT: computed tomography; TUG: timed up and go; WB-EMS: whole body electromyostimulation.

Muscle mass results from studies with groups of subjects who followed training programs in which aerobic exercise (walk) predominates showed no positive results in MM. The number of people with criteria for sarcopenia even increased at the end of the study, as occurred in the Mueller et al. study27 with subjects in the control group.

This review found that all studies where a significant change was seen in MM gain included strength exercises with dumbbells, machines or elastic bands, with modest results in studies based on low-intensity strength exercises24 where MM increased by approximately 1%, and markedly better results in those based on high intensity functional training, with an MM gain of 2%–5%16,17 in similar time periods. These differences are clearly exemplified by the Piastra et al. study20, which compared two groups with high- versus low-intensity strength training. Benefits were not only seen in anthropometric parameters (LBM, MM, MMI, MS), but also in static balance26 and functional parameters, with improved times in the timed up and go test17,23 and in walking speed.

The study with the best overall results was the one performed by Cadore et al.16, reporting a positive increase in all parameters analyzed (MM +3.3%, MS +144%, and physical tests +58%) using a multimodal exercise program consisting of two weekly 40 min sessions combining three series of high-intensity strength exercises (8–10 repetitions) with balance and aerobic exercises. Another unique feature of this study was that it included older patients (89–96 years), showing that a multifunctional exercise-based intervention can be effective and well tolerated by nonagenarians.

As regards training frequency, the results of the Kemmler et al. study19 showed a significant increase in LBM in subjects who exercised more frequently (more than two sessions per week) than in those with more limited frequency of exercise (less than two sessions per week). No increase related to the greater frequency of training was seen in appendicular muscle mass, but this significantly decreased in subjects with low training frequency.

Discussion

MM and MS are significantly related, with reduction in one of them leading to reduction in the other,18 triggering the occurrence of sarcopenia.17 Physical exercise is known to have positive effects on MM and especially on MS, and is therefore currently considered the main tool for managing sarcopenia to avoid increased comorbidity, falls in elderly patients, and the resultant dependence.28

The purpose of this study was to conduct a systematic review to separately study the effectiveness of exercise in sarcopenia, comparing different training protocols and types of exercise, observing improvements in body composition in older people with a muscle mass lower than desired.

In the MM results reported by studies based on aerobic (walking) exercise protocols only, no positive results were seen in MM,16 and the number of people with criteria for sarcopenia was even higher at the end of the study. By contrast, studies where a significant change was seen as MM gain and improved functionality and static balance always included strength exercises, either alone or combined with mixed strength and aerobic exercise programs, with the latter providing the best results.16

A separate comment should be made of the frequency and duration of the proposed training sessions, which will undoubtedly have an impact on the changes generated by the exercise, particularly in the elderly. In this regard, the conclusions of the Kemmler et al. study,19 which showed benefits when training frequency was higher than 2 weekly sessions, are interesting. The recommendation to establish 48 h of rest in training of the same muscle group should however be taken into account, as it has been shown in the general population that this is not only helpful for muscle rest, but also to achieve better results.29 The Chen et al. study30 was the only one including this recommendation in its exercise protocol.

At least two systematic reviews have been previously published on this subject,31,32 and their conclusions are in line with the above considerations; the most marked benefit is achieved with high-intensity strength exercise programs. It should be noted however that both reviews include studies also including nutritional supplementation, and it cannot therefore be concluded that the benefit seen only comes from the prescribed exercise, which limits the conclusions drawn from them. To our knowledge, this is the first systematic review including only studies based on assessment of physical exercise.

Limitations for drawing conclusions include the difficulty to analyze and compare the results, as there is no consensus established for measurement and homogenization, particularly as regards functional tests, but also for anthropometric tests, and each study assessed different variables. Another important limitation is the great variability in the age ranges of the different studies, from 65 to over 90 years. No study assessed the potential differences in the efficacy results by age range. No sex differences in results have been evaluated either, though some studies such as the one reported Mueller et al.27 specified in the methodology that different initial weight loads were applied in strength exercises depending on sex.

These are usually short-term studies, except for the Kemmler et al. study,23 which lasted up to 72 weeks, and therefore report short-term results. When a structured, long-term training plan is made, it should be taken into account that the muscle, when subject to the same stimulus, adapts and generates a physiological plateau without achieving changes in physical qualities such as strength. Changes should be made either in strength weight, in the number of series or repetitions or in exercise duration in order to achieve better results, such as an increasing exercise load in elderly subjects with sarcopenia, something which must still be specifically analyzed with new studies.

Conclusions

Exercise has significant benefits in elderly patients with sarcopenia. Aerobic (walking) exercises routinely prescribed in clinical practice do not achieve significant benefits.

Current evidence shows that training based on strength-resistance and its combination in multimodal programs with aerobic and balance exercise have significantly beneficial effects on anthropometric and muscle function parameters, and that exercises should be adapted to the characteristics of each subject.

Authorship

D.E. Barajas Galindo, E. González Arnáiz, and P. Ferrero Vicente are responsible for the conception and design of the study. All authors participated in the writing and review of the final version of the manuscript.

Conflict of interest

None.

References
[1]
R. Mañas, et al.
Aproximación al desarrollo de un programa nacional de investigación sobre Envejecimiento desde el concepto de fragilidad.
SEGG, 36 (2001), pp. 24-35
[2]
B. Lloyd, D. Williamson, N. Singh, R. Hansen, T. Diamond, T. Finnegan, et al.
Recurrent and injurious falls in the year following hip fracture: a prospective study of incidence and risk factors from the sarcopenia and hip fracture study.
J Gerontol A Biol, 64A (2009), pp. 599-609
[3]
R. Burgos Peláez.
Sarcopenia en ancianos.
Endocrinol Nutr, 53 (2006), pp. 335-344
[4]
R. Carrillo, J.M. Bermejo, C. Peña, U. Gabriel, C. Cortés.
Fragilidad y sarcopenia.
Rev Fac Med Univ Nac Auton Mex, 54 (2011), pp. 12-21
[5]
L.V. Cares, C.C. Domínguez, M.J. Fernández, C.R. Farías, G. Win-tin Chang, G. Fasce, et al.
Evolución de la capacidad funcional en adultos mayores hospitalizados en la unidad geriátrica de agudos del Hospital Clínico de la Universidad de Chile.
Rev Med Chile, 141 (2013), pp. 419-427
[6]
J. Morley, L. Cao.
Rapid screening for sarcopenia.
J Cachexia Sarcopenia Muscle, 6 (2015), pp. 312-314
[7]
F. Masanés Torán, M. Navarro López, E. Sacanella Meseguer, A. López Soto.
¿Qué es la sarcopenia?.
J Sem Reu, 11 (2010), pp. 14-23
[8]
R. Baumgartner, K. Koehler, D. Gallagher, L. Romero, S. Heymsfield, R. Ross, et al.
Epidemiology of sarcopenia among the elderly in New Mexico.
Am J Epidemiol, 147 (1998), pp. 755-763
[9]
A. Cruz-Jentoft, G. Bahat, J. Bauer, Y. Boirie, O. Bruyère, T. Cederholm, et al.
Sarcopenia: revised European consensus on definition and diagnosis.
[10]
K. Choi.
Sarcopenia and sarcopenic obesity.
J Clin Endocrinol Metab, 28 (2013), pp. 86
[11]
L. Spence, E. Lipscomb, J. Cadogan, B. Martin, M. Wastney, M. Peacock, et al.
The effect of soy protein and soy isoflavones on calcium metabolism in postmenopausal women: a randomized crossover study.
Am J Clin Nutr, 81 (2005), pp. 916-922
[12]
L. Heredia.
Ejercicio físico y deporte en los adultos mayores. GEROINFO.
RNPS, 1 (2006), pp. 1-10
[13]
C. Fuenmayor, E. Ramón, G. Villabón, T. Saba.
Sarcopenia-visión clínica de una entidad poco conocida y mucho menos buscada.
Rev Venez Endocrinol Metab, 5 (2007), pp. 3-7
[14]
C. Liu, X. Leng, F. Hsu, S. Kritchevsky, J. Ding, C. Earnest, et al.
The impact of sarcopenia on a physical activity intervention: the lifestyle interventions and independence for elders pilot study (LIFE-P).
J Nutr Health Aging, 18 (2013), pp. 59-64
[15]
Reliability of the PEDro scale for rating quality of randomized controlled trials.
Phys Ther, 83 (2003), pp. 713-721
[16]
E. Cadore, A. Casas-Herrero, F. Zambom-Ferraresi, F. Idoate, N. Millor, M. Gómez, et al.
Multicomponent exercises including muscle power training enhance muscle mass, power output, and functional outcomes in institutionalized frail nonagenarians.
[17]
M. Fragala, D. Fukuda, J. Stout, J. Townsend, N. Emerson, C. Boone, et al.
Muscle quality index improves with resistance exercise training in older adults.
Exp Gerontol, 53 (2014), pp. 1-6
[18]
A. Machado, D. García-López, J. González-Gallego, N. Garatachea.
Whole-body vibration training increases muscle strength and mass in older women: a randomized-controlled trial.
Scandinavian J Sci Med Sport, 20 (2009), pp. 200-207
[19]
W. Kemmler, S. von Stengel.
Exercise frequency, health risk factors, and diseases of the elderly.
Arch Phys Med Rehab, 94 (2013), pp. 2046-2053
[20]
G. Piastra, L. Perasso, S. Lucarini, F. Monacelli, A. Bisio, V. Ferrando, 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), pp. 1-10
[21]
Y. Wu, J. Lin, P. Wu, Y. Kuo.
Effects of a hybrid intervention combining exergaming and physical therapy among older adults in a long-term care facility.
Geriatr Gerontol Int, 19 (2018), pp. 147-152
[22]
W. Kemmler, S. von Stengel, K. Engelke, et al.
Exercise effects on bone mineral density, falls, coronary risk factors, and health care costs in older women: the randomized controlled Senior Fitness and Prevention (SEFIP) study.
Arch Intern Med, 170 (2010), pp. 179-185
[23]
W. Kemmler, S. von Stengel, K. Engelke, L. Häberle, J. Mayhew, W. Kalender.
Exercise, body composition, and functional ability.
Am J Prev Med, 38 (2010), pp. 279-287
[24]
K. Reid, K. Martin, G. Doros, D. Clark, C. Hau, C. Patten, et al.
Comparative effects of light or heavy resistance power training for improving lower extremity power and physical performance in mobility-limited older adults.
J Gerontol A Biol Sci Med, 70 (2014), pp. 374-380
[25]
J. Hong, J. Kim, S. Kim, H. Kong.
Effects of home-based tele-exercise on sarcopenia among community-dwelling elderly adults: body composition and functional fitness.
Exp Gerontol, 87 (2017), pp. 33-39
[26]
A. González, G. Mangine, M. Fragala, J. Stout, K. Beyer, J. Bohner, et al.
Resistance training improves single leg stance performance in older adults.
Aging Clin Exp Res, 26 (2013), pp. 89-92
[27]
M. Mueller, F. Breil, M. Vogt, R. Steiner, K. Lippuner, A. Popp, et al.
Different response to eccentric and concentric training in older men and women.
Eur J Appl Physiol, 107 (2009), pp. 145-153
[28]
A. Bogaerts, C. Delecluse, A. Claessens, W. Coudyzer, S. Boonen, S. Verschueren.
Impact of whole-body vibration training versus fitness training on muscle strength and muscle mass in older men: a 1-year randomized controlled trial.
J Gerontol A Biol Sci Med Sci, 62 (2007), pp. 630-635
[29]
F. Pareja-Blanco, D. Rodríguez-Rosell, P. Aagaard, L. Sánchez-Medina, J. Ribas-Serna, R. Mora-Custodio, et al.
Time course of recovery from resistance exercise with different set configurations.
J Strength Cond Res, 1 (2018),
[30]
H. Chen, H. Wu, Y. Chen, S. Ho, Y. Chung.
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, 112 (2018), pp. 112-118
[31]
Y. Yoshimura, H. Wakabayashi, M. Yamada, H. Kim, A. Harada, H. Arai.
Interventions for treating sarcopenia: a systematic review and meta-analysis of randomized controlled studies.
J Gerontol A Biol Sci Med, 18 (2017), pp. 553.e1-553.e16
[32]
L. Vlietstra, W. Hendrickx, D. Waters.
Exercise interventions in healthy older adults with sarcopenia: A systematic review and meta-analysis.
Australs J Ageing, 37 (2018), pp. 169-183

Please cite this article as: Barajas-Galindo DE, González Arnáiz E, Ferrero Vicente P, Ballesteros-Pomar MD. Efectos del ejercicio físico en el anciano con sarcopenia. Una revisión sistemática. Endocrinol Diabetes Nutr. 2021;68:159–169.

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