The frailty syndrome affects up to 38% of the older population, leading to health impairments and consequences in social life (Fried et al., 2001). Frailty is a complex interaction between physical variables, and there are different definitions in the literature (Abellan Van Kan et al., 2008; Markle-Reid & Browne, 2003; Rodriguez-Mañas et al., 2013). Rockwood et al. (1999) defined frailty as the difficulty to perform daily functional activities, whereas Fried et al. (2001) adopted five components to describe frailty: unintentional weight loss, weakness, poor endurance and energy, slowness, and low physical activity levels. Despite the different definitions, there is a consensus that frailty leads to vulnerability caused by the diminished interaction between systems and by negative health outcomes (Ferrucci et al., 2004; Hogan, MacKnight, Bergman, & Steering Committee, Canadian Initiative on Frailty and Aging, 2003), which places frail individuals at greater risk of disability, hospitalization, morbidity, and death.
Recently, a World Health Organization framework on healthy aging (Beard et al., 2016) suggested that intrinsic capacity is a more affordable concept to assess integrated care for older people, including clinical manifestations of the declines in physical and mental capacities as strong predictors of mortality and dependence in older age. Therefore, multidimensional interventions must be conducted to manage intrinsic capacity, focusing on impaired activities, predictors of daily living, and instrumental activities, such as low cognition, weak grip strength, and slow gait speed.
Regardless of the frailty definition, implementing physical activity interventions in frail populations should be a public health priority, as the benefits of exercise programs on functional performance, risk of falls, gait, balance, endurance, muscle strength, and power have already been shown in the literature for this population (Cadore, Rodriguez-Manas, Sinclair, & Izquierdo, 2013; Freiberger et al., 2012; Liu & Fielding, 2011). Considering the training organization, multimodal exercise programs (e.g., combining different physical components), mainly those including progressive resistance training (RT), have been demonstrated as an effective method for enhancing muscle mass, muscle strength, and functional performance (Izquierdo et al., 2017), whereas studies that investigated the performance of balance (i.e., yoga or tandem exercises; Kenny et al., 2010; Taylor et al., 2012; Wolf et al., 1996) or endurance training (Ehsani et al., 2003) alone showed significant effects only in rate of falls (47–58%), balance (4% in Timed Up and Go [TUG]), and cardiorespiratory capacity (17%). As previously stated by Fiatarone et al. (1990), it is important to include RT exercises in physical training interventions for preventing frailty and delay-related impairments in this syndrome (Cadore et al., 2013; Fiatarone et al., 1990; Izquierdo et al., 2017).
Previous review studies, including three systematic reviews (Cadore et al., 2013; Daniels, van Rossum, de Witte, Kempen, & van den Heuvel, 2008; Theou et al., 2011) and two meta-analyses (Chou, Hwang, & Wu, 2012; Giné-Garriga, Roque-Figuls, Coll-Planas, Sitja-Rabert, & Salva, 2014), have addressed the effects of physical exercise on the frailty syndrome (Cadore, Moneo, et al., 2014; Chou et al., 2012; Daniels et al., 2008; Giné-Garriga et al., 2014; Theou et al., 2011). More specifically, a meta-analysis by Giné-Garriga et al. (2014) investigated the effect of general exercise on physical performance in frail older adults and reported significant positive effects on usual and fast gait speed, Short Physical Performance Battery (SPPB) score, and balance tests (i.e., Semitandem and Berg score). Previous studies have also reported powerful effects of RT (i.e., included in a multimodal training) on physical function and incidence of falls in frail patients with dementia (Cadore, Moneo, et al., 2014). Even with a poor physical condition, the exercise intervention has been shown to improve functional outcomes that are affected by physical frailty and sarcopenia. However, the effect of RT as the main intervention or as part of a multimodal training for frail individuals has not been assessed in meta-analysis focused on the effectiveness of multimodal interventions on functional capacity enhancements in physical frail population.
Therefore, taking into account the arguments described previously, this study aimed to (a) assess the effects of RT programs alone or plus other training components (i.e., balance, endurance, gait retraining) on strength and functional outcomes in frail older adults compared with control groups using a meta-analytic approach and (b) determine both the influence of the training period and the RT intensity prescription method (percentage of one-repetition maximum [%1-RM] vs. rate of perceived effort [RPE]) in the main outcomes.
Methods
Study Selection Procedure
The study was undertaken in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses statement (Liberati et al., 2009), and the method used was based on the minimum criteria established by the Cochrane Back Review Group (Furlan, Pennick, Bombardier, & van Tulder, 2009).
The search was conducted up to January 2017 and considered the literature published in the past 12 years, using the following electronic databases: MEDLINE, accessed through PubMed; SPORTDiscus; and the Cochrane Central Register of Controlled Trials. We proposed to explore this period due to a greater quantity of articles published in the past 12 years about frailty and physical exercise, specifically involving RT. In addition, improvement of the methodological approach in physical evaluations (e.g., familiarization, test–retest) has allowed more precise posttraining values. Moreover, a manual search of references in published studies about the population of interest was performed, and queries of the literature were done using the electronic databases Cochrane Central Register of Controlled Trials, SPORTDiscus, and MEDLINE. The terms used were “frail older adult” and “resistance training,” in association with a list of sensitive terms to search for experimental studies. The reference lists were examined to detect studies potentially eligible for inclusion, and the complete search strategy used in PubMed is summarized in Table 1.
Search Strategy
| #1 Frail Older [MeSh]: Elderly, Frail OR Frail Elders OR Elder, Frail OR Elders, Frail OR Frail Elder OR Functionally-Impaired Elderly OR Elderly, Functionally-Impaired OR Functionally Impaired Elderly OR Frail Older Adults OR Adult, Frail Older OR Adults, Frail Older OR Frail Older Adult OR Older Adult, Frail OR Older Adults, Frail |
| #2 Resistance Training [MeSh]: Training, Resistance OR Strength Training OR Training, Strength OR Weight-Lifting Strengthening Program OR Strengthening OR Program, Weight-Lifting OR Strengthening Programs, Weight-Lifting OR Weight Lifting Strengthening Program OR Weight-Lifting OR Strengthening Programs OR Weight-Lifting Exercise Program OR Exercise Program, Weight-Lifting OR Exercise Programs, Weight-Lifting OR Weight Lifting Exercise Program OR Weight-Lifting Exercise Programs OR Weight-Bearing Strengthening Program OR Strengthening Program, Weight-Bearing OR Strengthening Programs, Weight-Bearing OR Weight Bearing Strengthening Program OR Weight-Bearing Strengthening Programs OR Weight-Bearing Exercise Program OR Exercise Program, Weight-Bearing OR Exercise Programs, Weight-Bearing OR Weight Bearing Exercise Program OR Weight-Bearing Exercise Programs |
| #3 #1 AND #2 |
Intervention, Controls, and Outcome Measures
This review included experimental studies that evaluated the effects of RT programs alone or combined with other training components (i.e., balance, endurance, gait retraining) on muscle strength and functional outcomes in frail older adults.
The parameters evaluated were lower limbs’ maximal strength and functional capacity. The inclusion criteria were the following: participants should be (a) 65 years and older and (b) defined as frail according to standardized criteria (e.g., Fried et al., 2001) or considered frail according to reduced physical function (e.g., Rockwood et al., 1999), according to measurements of physical performance scales (e.g., SPPB) or performance-based measures, such as gait, mobility, muscle strength, nutritional intake, weight change, balance, endurance, fatigue, and physical activity.
The exclusion criteria were the following: (a) the inclusion of participants with disabilities (e.g., advanced disability in performing activities daily living, dementia, or end-stage disease), (b) home-based interventions, (c) protein supplementation, and (d) crossover design and pilot studies.
Risk of Bias Assessment
The risk of bias assessment was performed independently by two investigators (P. Lopez and R. Grazioli) and took into consideration the following characteristics of the included studies: random sequence generation, blinding of outcome assessors, concealed allocation concealment, description of losses and exclusions, and intention-to-treat analysis. Studies without a clear description of these features were considered unclear or not reported.
Data Extraction
Titles and abstracts of all articles identified by the search strategy were independently evaluated by two researchers, in duplicate (P. Lopez and R. Grazioli). Abstracts that did not provide sufficient information regarding the inclusion and exclusion criteria were selected for full-text evaluation. In the second phase, the same reviewers independently evaluated these full-text articles and selected them in accordance with the eligibility criteria. Disagreements among reviewers were resolved by consensus, and if disagreement persisted, a third reviewer (R. Radaelli) was consulted. In case of lack of data for the meta-analysis, the corresponding author was contacted to request the missing data.
The data extraction was performed independently by the same two reviewers via a standardized form. Information on interventions, outcomes, and patients was collected. The primary outcomes analyzed were strength, gait speed, TUG, and SPPB. In addition, frailty criteria, intervention period, RT variables (i.e., frequency, intensity and volume), adverse events, and feasibility were informed and extracted.
Data Analysis
If the data available were sufficient and appropriate, the meta-analyses were performed using the Review Manager Software’s fixed-effects model. For continuous outcomes (e.g., strength, usual gait speed, TUG, and SPPB), the relative gains were extracted after the intervention and the number of participants was assessed at follow-up in the intervention group to estimate the standardized mean difference (SMD) of the intervention and its 95% confidence interval (CI).
Results
Search Results
All studies included in this meta-analysis aimed to investigate the effects of RT in the frail older population. A total of 373 studies were retrieved (PubMed [n = 303], Cochrane Central Register of Controlled Trials [n = 64], PEDro [n = 4], and SPORTDiscus [n = 2]). Of these, 106 studies were excluded, and after the titles and abstracts were evaluated, 217 studies were eligible for full-text reading. After applying inclusion and exclusion criteria, 11 studies were included by database search and four by manual search (Figure 1).
—Flowchart of literature review presents the different steps of search and study selection. CENTRAL = Central Register of Controlled Trials.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Flowchart of literature review presents the different steps of search and study selection. CENTRAL = Central Register of Controlled Trials.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Flowchart of literature review presents the different steps of search and study selection. CENTRAL = Central Register of Controlled Trials.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
Studies Included
A total of 15 studies were included in this meta-analysis (Figure 1), wherein 1,350 frail older participants (sample size = 24–616) were involved; the intervention periods ranged from 8 to 48 weeks. Four studies investigated the effect of RT only (Hess, Woollacott, & Shivitz, 2006; Ikezoe, Tsutou, Asakawa, Tsuboyama, 2005; Kryger & Andersen, 2007; Lustosa et al., 2011), and the other 11 studies investigated the effect of RT combined with other components (e.g., endurance and/or balance and/or gait retraining) in frailty (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010; Gudlaugsson et al., 2012; Jeon, Jeong, Petrofsky, Lee, & Yim, 2014; Kim et al., 2012, 2015; Lee et al., 2013; Ng et al., 2015; Rosendahl et al., 2006; Serra-Rexach et al., 2011; Zech et al., 2012). Among multimodal components, eight studies used RT plus balance training (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010; Jeon et al., 2014; Kim et al., 2015; Lee et al., 2013; Ng et al., 2015; Rosendahl et al., 2006; Zech et al., 2012), four used RT plus gait retraining (Cadore, Casas-Herrero, et al., 2014; Kim et al., 2015; Rosendahl et al., 2006; Zech et al., 2012), two used RT plus endurance training (Lee et al., 2013; Serra-Rexach et al., 2011), and one used RT plus flexibility training (Lee et al., 2013; Table 2).
Study Characteristics: Sample Size, Frailty Criteria, Intervention Time, Training Protocol, and Main Outcomes
| Study | N | Frailty criteria | Intervention time (weeks) | Training protocol | Main outcomes | ES |
|---|---|---|---|---|---|---|
| Cadore et al. (2014) | 24 | ≥3 Fried’s criteria | 12 | MULTIM: RT + EQ + GR | ↑Muscle strength Gait speed TUG | 0.66 × −0.49 0.57 × −1.33 −0.13 × 0.66 |
| Giné-Garriga et al. (2010) | 51 | Functional daily difficulties | 12 | MULTIM: RT + EQ | Muscle strength Gait speed | 2.5 × −0.66 3.0 × −0.5 |
| Gudlaugsson et al. (2012) | 117 | SPPB (>7 points) | 24 | MULTIM: RT + END | ↑Muscle strength ↑TUG ↑SPPB | 0.4 × −0.15 0.26 × 0.5 0.34 × 1.5 |
| Hess et al. (2006) | 27 | Functional daily difficulties | 10 | RT | ↑Muscle strength | 4.18 × −0.15 |
| Ikezoe et al. (2005) | 28 | Institutionalized older adults | 48 | RT | ↑Muscle strength | 0.44 × −0.51 |
| Jeon et al. (2014) | 62 | ≥3 falls recorded | 12 | MULTIM: RT + EQ + END | ↑TUG | −0.86 × 0.07 |
| Kim et al. (2012) | 155 | Appendicular muscle mass (<6.42 kg/m2), knee extension strength (1.01 N·m·kg−1), gait speed (<1.22 m/s), and BMI (<22) | 12 | MULTIM: RT + EQ + GR | Muscle strength ↑Gait speed | 0.06 × -0.53 0.79 × 0.14 |
| Kim et al. (2015) | 131 | ≥3 Fried’s criteria | 12 | MULTIM: RT + EQ + GR | Muscle strength ↑Gait speed ↑TUG | 0.21 × 0.04 0.42 × −0.21 −0.88 × −0.11 |
| Kryger and Andersen (2007) | 23 | Functional daily difficulties | 12 | RT | ↑Muscle strength | 3.41 × −0.41 |
| Lee et al. (2013) | 616 | ≥1 fall recorded | 12 | MULTIM: RT + EQ + END + FLEX | Muscle strength ↑TUG | 0.18 × 0.26 −0.11 × 0.01 |
| Lustosa et al. (2011) | 32 | ≥3 Fried’s criteria | 10 | RT | Muscle strength Gait speed ↑TUG | 0.26 × 0.46 0.7 × 0.02 −0.29 × 0.04 |
| Ng et al. (2015) | 246 | ≥3 Fried’s criteria | 24 | MULTIM: RT + EQ | Muscle strength | 0.41 × 0.23 |
| Rosendahl et al. (2006) | 191 | Functional daily difficulties | 12 | MULTIM: RT + EQ + GR | ↑Muscle strength Gait speed | 0.26 × 0.20 0.09 × −0.09 |
| Serra-Rexach et al. (2011) | 40 | Institutionalized older adults; ≥90 years | 8 | MULTIM: RT + END | ↑Muscle strength Gait speed TUG | 0.44 × −0.14 0.14 × −0.28 0.48 × 0.11 |
| Zech et al. (2012) | 69 | ≥3 Fried’s criteria | 12 | MULTIM: RT + EQ + GR | ↑SPPB | 0.41 × −0.23 |
Note. ES = effect size; ↑ = significantly improves in respective study (p ≤ .05); MULTIM = multimodal training; RT = resistance training; END = endurance training; EQ = equilibrium training; GR = gait retraining; FLEX = flexibility training; SPPB = Short Physical Performance Battery; TUG = Timed Up and Go; BMI = body mass index.
Different techniques were used to assess maximum muscle strength, such as isokinetic contractions (e.g., isometric and isokinetic contraction at 30 and 60 deg/s; Cadore, Casas-Herrero, et al., 2014b; Giné-Garriga et al., 2010; Ikezoe et al., 2005; Kim et al., 2012, 2015; Kryger & Andersen, 2007; Lee et al., 2013; Lustosa et al., 2011; Ng et al., 2015) and 1-RM tests (Hess et al., 2006; Kryger & Andersen, 2007; Rosendahl et al., 2006; Serra-Rexach et al., 2011). Eight studies evaluated the usual gait speed (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010; Gudlaugsson et al., 2012; Kim et al., 2012, 2015; Lustosa et al., 2011; Rosendahl et al., 2006; Serra-Rexach et al., 2011). Eight studies evaluated the TUG test (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010; Gudlaugsson et al., 2012; Jeon et al., 2014; Kim et al., 2015; Lee et al., 2013; Lustosa et al., 2011; Serra-Rexach et al., 2011), and two studies evaluated SPPB performance (Gudlaugsson et al., 2012; Zech et al., 2012). The measured outcomes are presented in Table 3.
List of Outcome Measures and Other Data Extracted From Included Studies
| Data | Type | Units |
|---|---|---|
| Maximum strength | Outcome | kg, N·m, and N·m·kg−1 |
| Gait speed | Outcome | m/s and s |
| TUG test | Outcome | s |
| SPPB | Outcome | Score |
| Intervention time | Covariate | Weeks |
| RT prescription | Covariate | 1-RM and RPE |
| Year | Year of publication | Year |
Note. TUG = Timed Up and Go test; SPPB = Short Physical Performance Battery; RT = resistance training; 1-RM = one-repetition maximum; RPE = rate of perceived effort.
The studies’ characteristics, such as sample size, frailty criteria, intervention period, training protocol, outcomes, and effect size, are presented in Table 3. In addition, the training frequency, volume, RT intensity, adverse events, and feasibility are presented in Table 4.
Resistance Training Characteristics
| Study | Frequency | Volume (Sets × Repetitions) | Intensity (RM or %1-RM) | Feasibility | Adverse events |
|---|---|---|---|---|---|
| Cadore et al. (2014) | 2 | 2–3 × 8–10 | 40–60% of 1-RM | 39 admitted and 32 randomized IG: adherence 50% | Three subjects report medicines complication |
| Giné-Garriga et al. (2010) | 2 | 1–2 × 6–15 | 8-RM | 1,177 admitted and 51 randomized IG: adherence 49% | No adverse event |
| Gudlaugsson et al. (2012) | 2 | 2 × 12 | 50% of 1-RM | 325 admitted and 117 randomized IG: adherence 86% | No adverse event |
| Hess et al. (2006) | 3 | 3 × 8 | 50–80% of 1-RM | – | – |
| Ikezoe et al. (2005) | 4–6 | 1 × 10 | – | – | – |
| Jeon et al. (2014) | 3 | – | – | 70 admitted and 70 randomized IG: adherence 88% | No adverse event |
| Kim et al. (2012) | 2 | – | – | 304 admitted and 155 randomized IG: adherence 92% | No adverse event |
| Kim et al. (2015) | 2 | – | – | 331 admitted and 131 randomized IG: adherence 94% | No adverse event |
| Kryger and Andersen (2007) | 3 | 3 × 8 | 50–80% of 1-RM | – | – |
| Lee et al. (2013) | 1 | – | – | 618 admitted and 616 randomized IG: adherence 89% | No adverse event |
| Lustosa et al. (2011) | 3 | – | – | – | No adverse event |
| Ng et al. (2015) | 2 | 1 × 8–15 | 60–80% of 1-RM | 584 admitted and 246 randomized IG: adherence 91% | Two subjects report pain |
| Rosendahl et al. (2006) | 2 | 1 × 8–12 | 8- to 12-RM | 487 admitted and 191 randomized IG: adherence 84% | – |
| Serra-Rexach et al. (2011) | 2 | 2–3 × 8–10 | 30–70% of 1-RM | 48 admitted and 40 randomized IG: adherence 80% | – |
| Zech et al. (2012) | 2 | – | – | 663 admitted and 69 randomized IG: adherence 78% | – |
Note. RM = repetition maximum; IG = intervention group.
Risk of Bias and Quality
The internal validity of the 15 studies was assessed by the Cochrane Handbook Criteria (Higgins & Green, 2008). Twelve studies met the random allocation criteria (80%); 14 did not present information about concealed allocation criteria (93.3%); nine studies met the criteria for blinded assessment (60%); 11 studies met the criteria for describing losses and exclusions (73.3%); and six studies (40%) met the intention-to-treat analysis criteria. The results of the risk of bias assessment are presented in Table 5.
Risk of Bias Assessment
| Study | Random sequence generation | Concealed allocation | Blinding of outcome assessor | Description of losses and exclusions | Intention-to-treat analysis |
|---|---|---|---|---|---|
| Cadore, Moneo, et al. (2014) | Y | – | Y | Y | – |
| Giné-garriga et al. (2010) | N | – | Y | Y | – |
| Gudlaugson et al. (2012) | Y | – | – | – | – |
| Hess et al. (2006) | N | – | – | – | – |
| Ikezoe et al. (2005) | N | – | – | Y | – |
| Jeon et al. (2014) | Y | – | Y | Y | – |
| Kim et al. (2012) | Y | – | Y | Y | Y |
| Kim et al. (2015) | Y | Y | Y | Y | Y |
| Kryger et al. (2007) | Y | – | – | Y | – |
| Lee et al. (2013) | Y | – | – | – | Y |
| Lustosa et al. (2011) | Y | – | Y | – | – |
| Ng et al. (2015) | Y | N | Y | Y | Y |
| Rosendahl et al. (2006) | Y | – | Y | Y | Y |
| Serra-rexach et al. (2011) | Y | – | Y | Y | Y |
| Zech et al. (2015) | Y | – | – | Y | – |
Effect of Interventions
Maximum strength of knee extensors
Thirteen studies involving 1,250 frail older people assessed maximum strength of the knee extensors (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010; Gudlaugsson et al., 2012; Hess et al., 2006; Ikezoe et al., 2005; Kim et al., 2012, 2015; Kryger & Andersen, 2007; Lee et al., 2013; Lustosa et al., 2011; Ng et al., 2015; Rosendahl et al., 2006; Serra-Rexach et al., 2011). The effect of the interventions on this outcome was found to be significant (SMD = 1.07, 95% CI [0.56, 1.58], I2 = 92%, p < .001). Sensitivity analyses of the intervention period indicated a significant positive effect estimated for studies with interventions shorter and longer than 12 weeks. However, periods ≤12 weeks showed greater positive effect (SMD = 1.25, 95% CI [0.57, 1.94], I2 = 94%, p < .001) when compared with periods >12 weeks (SMD = 0.89, 95% CI [0.14, 1.64], I2 = 85%, p < .05). Figure 2 shows a forest plot of the results of the knee extensors’ maximum strength.
—Effects of multimodal training on strength gains of intervention group compared with control group, based on intervention time, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on strength gains of intervention group compared with control group, based on intervention time, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on strength gains of intervention group compared with control group, based on intervention time, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
Regarding methods to prescribe RT intensity, sensitive analyses indicated a significant positive effect estimated on knee extensors’ muscle strength for the %1-RM method (SMD = 1.81, 95% CI [0.96, 2.66], I2 = 92%, p < .001), whereas RPE presented no significant effect (SMD = 0.30, 95% CI [−0.32, 0.91], I2 = 90%, p > .05; Figure 3). Table 3 provides information about the RT intensity used in each study.
—Effects of multimodal training on strength gains of intervention group compared with control group, based on intensity prescription, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on strength gains of intervention group compared with control group, based on intensity prescription, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on strength gains of intervention group compared with control group, based on intensity prescription, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
Gait Speed
Eight studies involving 498 frail older people measured usual gait speed matched criteria to be included in the meta-analysis (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010; Gudlaugsson et al., 2012; Kim et al., 2012, 2015; Lustosa et al., 2011; Rosendahl et al., 2006; Serra-Rexach et al., 2011), and a significant effect of exercise intervention on this outcome was found (SMD = 1.57, 95% CI [0.50, 2.64], I2 = 95%, p < .001).
Regarding the method of RT intensity prescription, sensitive analyses indicated a significant positive effect estimate for %1-RM method (SMD = 2.37, 95% CI [0.70, 4.04], I2 = 96%, p < .001), whereas RPE presented no significant effect (SMD = 0.35, 95% CI [−0.93, 1.64], I2 = 92%, p > .05; Figure 4).
—Effects of multimodal training on usual gait speed results of intervention group compared with control group, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on usual gait speed results of intervention group compared with control group, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on usual gait speed results of intervention group compared with control group, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
Timed Up and Go Test
Eight studies involving 983 frail older people that evaluated the TUG were included in the meta-analysis (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010; Gudlaugsson et al., 2012; Jeon et al., 2014; Kim et al., 2015; Lee et al., 2013; Lustosa et al., 2011; Serra-Rexach et al., 2011), and a significant positive effect on this outcome was found (SMD = −0.91, 95% CI [−1.45, −0.36], I2 = 90%, p ≤ .001).
Regarding the method of RT intensity prescription, the sensitive analyses indicated a significant positive effect estimated for both RPE and %1-RM method. However, %1-RM method showed a greater positive effect (SMD = −1.66, 95% CI [−3.30, −0.01], I2 = 94%, p ≤ .05) when compared with RPE (SMD = −0.47, 95% CI [−0.78, −0.17], I2 = 54%, p ≤ .01; Figure 5).
—Effects of multimodal training on TUG test results of intervention group compared with control group, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. TUG = Timed Up and Go; CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on TUG test results of intervention group compared with control group, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. TUG = Timed Up and Go; CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
—Effects of multimodal training on TUG test results of intervention group compared with control group, CI, IV, random effect model, and SD. Weight attributed to each study due to its statistical power. TUG = Timed Up and Go; CI = confidence interval; IV = inverse variance; RM = repetition maximum; RPE = rate of perceived effort; Std. = standardized.
Citation: Journal of Aging and Physical Activity 26, 3; 10.1123/japa.2017-0188
Short Physical Performance Battery
Two studies involving 144 frail older people that measured SPPB performance were included in this meta-analysis (Gudlaugsson et al., 2012; Zech et al., 2012). No significant effect on this outcome was found (SMD = 0.42, 95% CI [−0.11, 0.96], I2 = 52%, p > .05).
Discussion
The aim of the present meta-analysis was (a) to examine the effect of RT or multimodal training on strength and functional capacity and (b) to determine the influence of different training program variables (i.e., training intensity, frequency) in the main outcomes. As recently stated by World Health Organization (Beard et al., 2016), there is a need to build a qualified workforce to focus on reversing or slowing the declines in functional capacity in the frail older population. Proper levels of functional ability in older people with high risk of functional impairments are included in their basic rights, fundamental freedoms, and human dignity (Beard et al., 2016). Thus, based on the present results, performing progressive RT alone or combined with other training components is recommended as an effective intervention strategy for increasing physical aspects of frailty. Fifteen studies involving 1,350 frail older people were included in this meta-analysis, and, to the best of our knowledge, this is the first study to verify the effects of RT on the maximum strength, gait speed, TUG, and SPPB performance in frail older adults. All these significant increments are closely related to health in older people and are in accordance with essential issues reported by the World Health Organization (Beard et al., 2016). The current analysis emphasizes the importance of RT prescribed by the 1-RM method, and that even short training periods (i.e., ≤12 weeks) are able to improve muscle strength and functional capacity in frail individuals.
There are strong associations between neural impairments induced by aging, muscle power output, and functional capacity in older populations (Bassey et al., 1992; Bean et al., 2002; Clark, Fernhall, & Ploutz-Snyder, 2006; Clark, Manini, Bolanowski, & Ploutz-Snyder, 2006; Lang et al., 2010; Lexell, Downham, Larsson, Bruhn, & Morsing, 1995; Trappe et al., 2003). It has been extensively shown that RT is an efficient treatment method to enhance muscle strength, muscle power output, and functionality in robust older adults (Clark, Fernhall, & Ploutz-Snyder, 2006; Clark, Manini, et al., 2006; Trappe et al., 2003). However, there is less information regarding RT effects on these outcomes in frail older individuals. In a previous study, Churchward-Venne et al. (2015) examined the effect of 12 and 24 weeks of RT on muscle strength and functional capacity in robust, prefrail, and frail older adults, and their results showed increases in muscle strength of 23% and 35% after 12 and 24 weeks, respectively. In addition, it was reported that even participants who did not show a positive effect after 12 weeks demonstrated increases in muscle strength after 24 weeks of training. However, superior effect was found in shorter periods. Although it is not clear why these shorter periods have greater effect than longer periods, it is possible that these results could be related to the control of RT intensity. Indeed, in one of the studies that investigated RT effects in interventions longer than 12 weeks (Ikezoe et al., 2005), the intensity control method was RPE, which corroborates the hypothesis that a precise control of the RT intensity in some studies and the lower number of included studies could explain this discrepancy. In agreement, muscle strength increases after shorter periods (i.e., 12 weeks) have already been observed (Cadore, Casas-Herrero, et al., 2014b; Giné-Garriga et al., 2010; Hess et al., 2006; Kryger & Andersen, 2007).
To control RT intensity, the %1-RM and RPE methods are often used to enhance neuromuscular function (Izquierdo et al., 2017). In the current study, the results showed significantly greater increases in maximum strength when RT intensity was controlled by %1-RM (i.e., 30–80% of 1-RM) when compared with RPE. Cadore et al. (2014) investigated frail older individuals performing two to three sets of eight to 10 repetitions at 40–60% of 1-RM and found one of the greatest SMDs in the strength analysis, showing significant increases in maximum knee extensors’ strength of 20.2%. By contrast, some studies suggest and demonstrate the RT benefits using the RPE method to prescribe the training intensity in nonfrail older individuals to avoid maximum effort (Tiggemann et al., 2010) and allow assessment of discomfort, fatigue, and recovery after every training session (Scott, Duthie, Thornton, & Dascombe, 2016). However, to the best of our knowledge, this is the first meta-analysis comparing the effects of different methods to prescribe RT intensity on maximum strength in frail individuals. The present results suggest that the %1-RM method is more beneficial for increasing maximum strength of these individuals, and it accurately allows the execution of maximal or submaximal effort. In this sense, we can speculate that physically frail older people may present reduced perceptions of intensity, and, therefore, RPE may underestimate the workload during RT, which could potentially attenuate increases in maximum strength.
Usual gait speed is highly relevant to health due to its strong association with risk of falls, hospitalization, and need for care (Cesari et al., 2005; Studenski et al., 2003). Studies have shown a significant effect of RT combined with balance and/or gait retraining on usual gait speed (Cadore, Casas-Herrero, et al., 2014; Lustosa et al., 2011). Lustosa et al. (2011) have found significant improvements in usual gait speed (−10.1% on time of test) after 10 weeks of RT. Notwithstanding, there were a lack of details about the RT program used in their study. Likewise, Giné-Garriga et al. (2014), in a previous meta-analysis, evaluated the effect of physical exercise and demonstrated a positive effect of 0.6 m/s (95% CI [0.04, 0.08]) of increase on usual gait speed in frail older populations. In agreement with their study, the present meta-analysis showed a significant effect of RT on usual gait speed, although the significant effect was observed when RT prescription was based on 1-RM values, whereas RPE did not show significant effect. It should be mentioned that Giné-Garriga et al. (2014) and our meta-analyses have shown significant positive effects in gait speed, although using different inclusion criteria. Giné-Garriga et al. (2014) included general physical exercise as a main intervention, whereas in this work, we included studies only in which RT was used as central intervention or combined with other training components. Based on the present results regarding greater effect when using %1-RM as RT intensity control, we suggest that this method may promote superior increases in gait speed in frail older people.
Regarding factors associated with gait ability, balance, and sit-to-stand ability, the TUG test is strongly associated with the risk of falls in frail older adults (Casas-Herrero et al., 2013). Several experimental studies and meta-analyses have previously reported significant effects of multimodal training on TUG performance (Cadore, Casas-Herrero, et al., 2014; Gudlaugsson et al., 2012; Jeon et al., 2014; Lee et al., 2013; Lustosa et al., 2011). In a study conducted by Gudlaugsson et al. (2012) with frail older individuals, the intervention group used two sets of 12 repetitions at 50% of %1-RM, and it reported significant increases in TUG performance (−9.5% on time of performance). By contrast, two previous meta-analyses found no effect of RT combined with multimodal training on this outcome (Chou et al., 2012; Giné-Garriga et al., 2014). These differences may be attributed to the fact that the Giné-Garriga et al. (2014) meta-analyses included training programs in which RT was performed with elastic bands (Boshuizen, Stemmerik, Westhoff, & Hopman-Rock, 2005; Westhoff, Stemmerik, & Boshuizen, 2000). Furthermore, the Chou et al. (2012) meta-analysis contained studies with positive (Hauer, Pfisterer, Schuler, Bartsch, & Oster, 2003), negative (Latham et al., 2003), and neutral effects (Peri et al., 2008) on TUG performance. Thus, we suggest that the differences between the present study and previous meta-analyses (Chou et al., 2012; Giné-Garriga et al., 2014) may be attributed to the different training intensities used in the studies included in the present analysis, in which the inclusion criteria included the use of RT as the central intervention, as well as the use of a sensitive analysis to identify the method of the RT intensity prescription. Indeed, a previous meta-analysis (Borde, Hortobagyi, & Granacher, 2015) has reported that training intensity is a key factor influencing the neuromuscular gains in nonfrail individuals.
Previous studies have reported that low SPPB scores can predict hospitalization, care need, imbalance, and mortality (Guralnik et al., 2000; Guralnik & Winograd, 1994). Additionally, it has already been shown that multimodal training is effective to improve the SPPB score (Zech et al., 2012). In a previous study, Zech et al. (2012) investigated the effect of multimodal training on frail older individuals and showed significant increases in SPPB (10.2%) after 12 weeks of intervention. However, the present results did not show a significant effect of RT on SPPB performance, which is in disagreement with the meta-analysis by Giné-Garriga et al. (2014) that showed positive effects of exercise interventions on SPPB performance. Although we cannot suggest that RT adaptations promote a significant effect on SPPB based on our results, SPPB comprises different functional outcomes such as gait speed and chair rise tests that were substantially enhanced by RT combined with other types of training in previous studies (Cadore, Casas-Herrero, et al., 2014; Giné-Garriga et al., 2010). A possible explanation for the lack of effects in the present study could be the lower quantity of the included studies in our meta-analysis.
The present study has some limitations. The defined criteria allowed the inclusion of studies with different sets to define the frailty diagnostic, such as Fried’s criteria, and low functional performance (Rockwood et al., 1999); this may represent a limitation due to higher heterogeneity among the studies included. We observed a high value of heterogeneity in the maximum strength gains, usual gait speed, and TUG analyses (I2 > 50%), and these high I2 values may be attributed to the lack of information regarding training volume and intensity. However, although the frailty concept is still well consensual, it is important to point out that regardless the diagnosis used, positive effects of the RT interventions on physical outcomes of frailty were found. Another possible limitation of the present meta-analysis is that we also included studies that used RT as part of a multicomponent exercise intervention, and, in this case, it is not possible to attribute the functional adaptations only to the RT effects. Nevertheless, it is well described by systematic reviews and individual studies that RT is able to improve neuromuscular function and functional capacity in frail adults, and we focused specifically on main outcomes that are targeted by RT intervention.
In summary, RT alone or combined with other training components may be an effective intervention for increasing physical aspects of frailty, as shown in the present results. However, the method used to control RT intensity must be treated with caution. Thus, according to our results and based on previous studies (Cadore, Moneo, et al. 2014; Giné-Garriga et al., 2010; Gudlaugsson et al., 2012; Hess et al., 2006; Kryger & Andersen, 2007), initial periods of training (i.e., ≤12 weeks) and intensity prescribed by the %1-RM method (i.e., 40–80% of 1-RM) appear to lead to a greater magnitude of improvements on strength and functional capacity in the frail older adult population.
Acknowledgments
We would like to thank the
References
Abellan van Kan, G., Rolland, Y., Bergman, H., Morley, J.E., Kritchevsky, S.B., & Vellas, B. (2008). The I.A.N.A Task Force on frailty assessment of older people in clinical practice. The Journal of Nutrition, Health & Aging, 12, 29–37. PubMed ID: 18165842 doi:10.1007/BF02982161
Bassey, E.J., Fiatarone, M.A., O’Neill, E.F., Kelly, M., Evans, W.J., & Lipsitz, L.A. (1992). Leg extensor power and functional performance in very old men and women. Clinical Science, 82, 321–327. PubMed ID: 1312417 doi:10.1042/cs0820321
Bean, J.F., Kiely, D.K., Herman, S., Leveille, S.G., Mizer, K., Frontera, W.R., & Fielding, R.A. (2002). The relationship between leg power and physical performance in mobility-limited older people. Journal of the American Geriatrics Society, 50, 461–467. PubMed ID: 11943041 doi:10.1046/j.1532-5415.2002.50111.x
Beard, J.R., Officer, A., de Carvalho, I.A., Sadana, R., Pot, A.M., Michel, J.P., … Chatterji, S. (2016). The World report on ageing and health: A policy framework for healthy ageing. The Lancet, 387, 2145–2154. PubMed ID: 26520231 doi:10.1016/S0140-6736(15)00516-4
Borde, R., Hortobagyi, T., & Granacher, U. (2015). Dose-response relationships of resistance training in healthy old adults: A systematic review and meta-analysis. Sports Medicine, 45, 1693–1720. PubMed ID: 26420238 doi:10.1007/s40279-015-0385-9
Boshuizen, H.C., Stemmerik, L., Westhoff, M.H., & Hopman-Rock, M. (2005). The effects of physical therapists’ guidance on improvement in a strength-training program for the frail elderly. Journal of Aging and Physical Activity, 13, 5–22. PubMed ID: 15677832 doi:10.1123/japa.13.1.5
Cadore, E.L., Casas-Herrero, A., Zambom-Ferraresi, F., Idoate, F., Millor, N., Gomez, M., … Izquierdo, M. (2014). Multicomponent exercises including muscle power training enhance muscle mass, power output, and functional outcomes in institutionalized frail nonagenarians. Age, 36, 773–785. PubMed ID: 24030238 doi:10.1007/s11357-013-9586-z
Cadore, E.L., Moneo, A.B., Mensat, M.M., Munoz, A.R., Casas-Herrero, A., Rodriguez-Manas, L., & Izquierdo, M. (2014). Positive effects of resistance training in frail elderly patients with dementia after long-term physical restraint. Age, 36, 801–811. PubMed ID: 24243397 doi:10.1007/s11357-013-9599-7
Cadore, E.L., Rodriguez-Manas, L., Sinclair, A., & Izquierdo, M. (2013). Effects of different exercise interventions on risk of falls, gait ability, and balance in physically frail older adults: A systematic review. Rejuvenation Research, 16, 105–114. PubMed ID: 23327448 doi:10.1089/rej.2012.1397
Casas-Herrero, A., Cadore, E.L., Zambom-Ferraresi, F., Idoate, F., Millor, N., Martinez-Ramirez, A., … Izquierdo, M. (2013). Functional capacity, muscle fat infiltration, power output, and cognitive impairment in institutionalized frail oldest old. Rejuvenation Research, 16, 396–403. PubMed ID: 23822577 doi:10.1089/rej.2013.1438
Cesari, M., Kritchevsky, S.B., Penninx, B.W., Nicklas, B.J., Simonsick, E.M., Newman, A.B., … Pahor, M. (2005). Prognostic value of usual gait speed in well-functioning older people--results from the Health, Aging and Body Composition Study. Journal of the American Geriatrics Society, 53, 1675–1680. PubMed ID: 16181165 doi:10.1111/j.1532-5415.2005.53501.x
Chou, C.H., Hwang, C.L., & Wu, Y.T. (2012). Effect of exercise on physical function, daily living activities, and quality of life in the frail older adults: A meta-analysis. Archives of Physical Medicine and Rehabilitation, 93, 237–244. PubMed ID: 22289232 doi:10.1016/j.apmr.2011.08.042
Churchward-Venne, T.A., Tieland, M., Verdijk, L.B., Leenders, M., Dirks, M.L., de Groot, L.C., & van Loon, L.J. (2015). There are no nonresponders to resistance-type exercise training in older men and women. Journal of the American Medical Directors Association, 16, 400–411. PubMed ID: 25717010 doi:10.1016/j.jamda.2015.01.071
Clark, B.C., Fernhall, B., & Ploutz-Snyder, L.L. (2006). Adaptations in human neuromuscular function following prolonged unweighting: I. Skeletal muscle contractile properties and applied ischemia efficacy. Journal of Applied Physiology, 101, 256–263. PubMed ID: 16514004 doi:10.1152/japplphysiol.01402.2005
Clark, B.C., Manini, T.M., Bolanowski, S.J., & Ploutz-Snyder, L.L. (2006). Adaptations in human neuromuscular function following prolonged unweighting: II. Neurological properties and motor imagery efficacy. Journal of Applied Physiology, 101, 264–272. PubMed ID: 16514003 doi:10.1152/japplphysiol.01404.2005
Daniels, R., van Rossum, E., de Witte, L., Kempen, G.I., & van den Heuvel, W. (2008). Interventions to prevent disability in frail community-dwelling elderly: A systematic review. BMC Health Services Research, 8, 278. PubMed ID: 19115992 doi:10.1186/1472-6963-8-278
Ehsani, A.A., Spina, R.J., Peterson, L.R., Rinder, M.R., Glover, K.L., Villareal, D.T., … Holloszy, J.O. (2003). Attenuation of cardiovascular adaptations to exercise in frail octogenarians. Journal of Applied Physiology, 95(5), 1781–1788. PubMed ID: 12857764 doi:10.1152/japplphysiol.00194.2003
Ferrucci, L., Guralnik, J.M., Studenski, S., Fried, L.P., Cutler, G.B., Jr., Walston, J.D., … Interventions on Frailty Working Group. (2004). Designing randomized, controlled trials aimed at preventing or delaying functional decline and disability in frail, older persons: A consensus report. Journal of the American Geriatrics Society, 52, 625–634. PubMed ID: 15066083 doi:10.1111/j.1532-5415.2004.52174.x
Fiatarone, M.A., Marks, E.C., Ryan, N.D., Meredith, C.N., Lipsitz, L.A., & Evans, W.J. (1990). High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA, 263, 3029–3034. PubMed ID: 2342214 doi:10.1001/jama.1990.03440220053029
Freiberger, E., de Vreede, P., Schoene, D., Rydwik, E., Mueller, V., Frandin, K., & Hopman-Rock, M. (2012). Performance-based physical function in older community-dwelling persons: A systematic review of instruments. Age and Ageing, 41, 712–721. PubMed ID: 22885845 doi:10.1093/ageing/afs099
Fried, L.P., Tangen, C.M., Walston, J., Newman, A.B., Hirsch, C., Gottdiener, J., … Cardiovascular Health Study Collaborative Research Group. (2001). Frailty in older adults: Evidence for a phenotype. The Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, 56, 146–157. PubMed ID: 11253156 doi:10.1093/gerona/56.3.M146
Furlan, A.D., Pennick, V., Bombardier, C., van Tulder, M., and Editorial Board, Cochrane Back Review Group. (2009). 2009 updated method guidelines for systematic reviews in the Cochrane Back Review Group. Spine, 34, 1929–1941. PubMed ID: 19680101 doi:10.1097/BRS.0b013e3181b1c99f
M., Giné-Garriga, M., Guerra, E., Pages, T.M., Manini, R., Jimenez, & Unnithan, V.B. (2010). The effect of functional circuit training on physical frailty in frail older adults: A randomized controlled trial. Journal of Aging and Physical Activity, 18, 401–424. PubMed ID: 20956842 doi:10.1123/japa.18.4.401
Giné-Garriga, M., Roque-Figuls, M., Coll-Planas, L., Sitja-Rabert, M., & Salva, A. (2014). Physical exercise interventions for improving performance-based measures of physical function in community-dwelling, frail older adults: A systematic review and meta-analysis. Archives of Physical Medicine and Rehabilitation, 95, 753–769.e3. PubMed ID: 24291597 doi:10.1016/j.apmr.2013.11.007
Gudlaugsson, J., Gudnason, V., Aspelund, T., Siggeirsdottir, K., Olafsdottir, A.S., Jonsson, P.V., … Johannsson, E. (2012). Effects of a 6-month multimodal training intervention on retention of functional fitness in older adults: A randomized-controlled cross-over design. The International Journal of Behavioral Nutrition and Physical Activity, 9, 107. PubMed ID: 22963328 doi:10.1186/1479-5868-9-107
Guralnik, J.M., Ferrucci, L., Pieper, C.F., Leveille, S.G., Markides, K.S., Ostir, G.V., … Wallace, R.B. (2000). Lower extremity function and subsequent disability: Consistency across studies, predictive models, and value of gait speed alone compared with the short physical performance battery. The Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, 55, M221–M231. PubMed ID: 10811152 doi:10.1093/gerona/55.4.M221
Guralnik, J.M., & Winograd, C.H. (1994). Physical performance measures in the assessment of older persons. Aging, 6, 303–305. PubMed ID: 7893776
Hauer, K., Pfisterer, M., Schuler, M., Bartsch, P., & Oster, P. (2003). Two years later: A prospective long-term follow-up of a training intervention in geriatric patients with a history of severe falls. Archives of Physical Medicine and Rehabilitation, 84, 1426–1432. PubMed ID: 14586908 doi:10.1016/S0003-9993(03)00267-3
Hess, J.A., Woollacott, M., & Shivitz, N. (2006). Ankle force and rate of force production increase following high intensity strength training in frail older adults. Aging Clinical and Experimental Research, 18, 107–115. PubMed ID: 16702779 doi:10.1007/BF03327425
Higgins, J.P.T., & Green, S. (2008). Cochrane handbook for systematic review of interventions. Chichester, UK: John Wiley & Sons Ltd.
Hogan, D.B., MacKnight, C., Bergman, H., and Steering Committee, Canadian Initiative on Frailty and Aging. (2003). Models, definitions, and criteria of frailty. Aging Clinical and Experimental Research, 15, 1–5. PubMed ID: 14580013 doi:10.1007/BF03324472
Ikezoe, T., Tsutou, A., Asakawa, Y., & Tsuboyama, T. (2005). Low intensity training for frail elderly women: Long-term effects on motor function and mobility. Journal of Physical Therapy Science, 17(1), 43–49. doi:10.1589/jpts.17.43
Izquierdo, M., Casas-Herrero, A., Martinez-Velilla, N., Alonso-Bouzon, C., Rodriguez-Manas, L., & en representación del Grupo de Investigadores. (2017). [An example of cooperation for implementing programs associated with the promotion of exercise in the frail elderly. European Erasmus + <<Vivifrail>> program]. Revista espanola de geriatria y gerontologia, 52, 110–111. PubMed ID: 27132063 doi:10.1016/j.regg.2016.03.004
Jeon, M.Y., Jeong, H., Petrofsky, J., Lee, H., & Yim, J. (2014). Effects of a randomized controlled recurrent fall prevention program on risk factors for falls in frail elderly living at home in rural communities. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research, 20, 2283–2291. PubMed ID: 25394805 doi:10.12659/MSM.890611
Kenny, A.M., Boxer, R.S., Kleppinger, A., Brindisi, J., Feinn, R., & Burleson, J.A. (2010). Dehydroepiandrosterone combined with exercise improves muscle strength and physical function in frail older women. Journal of American Geriatric Society, 58(9), 1707–1714. PubMed ID: 20863330 doi:10.1111/j.1532-5415.2010.03019.x
Kim, H., Suzuki, T., Kim, M., Kojima, N., Ota, N., Shimotoyodome, A., … Yoshida, H. (2015). Effects of exercise and milk fat globule membrane (MFGM) supplementation on body composition, physical function, and hematological parameters in community-dwelling frail Japanese women: A randomized double blind, placebo-controlled, follow-up trial. PLoS ONE, 10, e0116256. PubMed ID: 25659147 doi:10.1371/journal.pone.0116256
Kim, H.K., Suzuki, T., Saito, K., Yoshida, H., Kobayashi, H., Kato, H., & Katayama, M. (2012). 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 American Geriatric Society, 60(1), 16–23. PubMed ID: 22142410 doi:10.1111/j.1532-5415.2011.03776.x
Kryger, A.I., & Andersen, J.L. (2007). Resistance training in the oldest old: Consequences for muscle strength, fiber types, fiber size, and MHC isoforms. Scandinavian Journal of Medicine & Science in Sports, 17, 422–430. PubMed ID: 17490465 doi:10.1111/j.1600-0838.2006.00575.x
Lang, T., Streeper, T., Cawthon, P., Baldwin, K., Taaffe, D.R., & Harris, T.B. (2010). Sarcopenia: Etiology, clinical consequences, intervention, and assessment. Osteoporosis International, 21, 543–559. PubMed ID: 19779761 doi:10.1007/s00198-009-1059-y
Latham, N.K., Anderson, C.S., Lee, A., Bennett, D.A., Moseley, A., Cameron, I.D., & Fitness Collaborative, G. (2003). A randomized, controlled trial of quadriceps resistance exercise and vitamin D in frail older people: The Frailty Interventions Trial in Elderly Subjects (FITNESS). Journal of the American Geriatrics Society, 51, 291–299. PubMed ID: 12588571 doi:10.1046/j.1532-5415.2003.51101.x
Lee, H.C., Chang, K.C., Tsauo, J.Y., Hung, J.W., Huang, Y.C., Lin, S.I., & Fall Prevention Initiatives in Taiwan (FPIT) Investigators. (2013). Effects of a multifactorial fall prevention program on fall incidence and physical function in community-dwelling older adults with risk of falls. Archives of Physical Medicine and Rehabilitation, 94, 606–615.e1. PubMed ID: 23220343 doi:10.1016/j.apmr.2012.11.037
Lexell, J., Downham, D.Y., Larsson, Y., Bruhn, E., & Morsing, B. (1995). Heavy-resistance training in older Scandinavian men and women: Short- and long-term effects on arm and leg muscles. Scandinavian Journal of Medicine & Science in Sports, 5, 329–341. PubMed ID: 8775717 doi:10.1111/j.1600-0838.1995.tb00055.x
Liberati, A., Altman, D.G., Tetzlaff, J., Mulrow, C., Gotzsche, P.C., Ioannidis, J.P., … Moher, D. (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: Explanation and elaboration. BMJ, 339, b2700. PubMed ID: 19622552 doi:10.1136/bmj.b2700
Liu, C.K., & Fielding, R.A. (2011). Exercise as an intervention for frailty. Clinics in Geriatric Medicine, 27, 101–110. PubMed ID: 21093726 doi:10.1016/j.cger.2010.08.001
Lustosa, L.P., Silva, J.P., Coelho, F.M., Pereira, D.S., Parentoni, A.N., & Pereira, L.S. (2011). Impact of resistance exercise program on functional capacity and muscular strength of knee extensor in pre-frail community-dwelling older women: A randomized crossover trial. Revista Brasileira de Fisioterapia, 15, 318–324. PubMed ID: 21971726 doi:10.1590/S1413-35552011000400010
Markle-Reid, M., & Browne, G. (2003). Conceptualizations of frailty in relation to older adults. Journal of Advanced Nursing, 44, 58–68. PubMed ID: 12956670 doi:10.1046/j.1365-2648.2003.02767.x
Ng, T.P., Feng, L., Nyunt, M.S., Feng, L., Niti, M., Tan, B.Y., … Yap, K.B. (2015). Nutritional, physical, cognitive, and combination interventions and frailty reversal among older adults: A randomized controlled trial. The American Journal of Medicine, 128, 1225–1236.e1. PubMed ID: 26159634 doi:10.1016/j.amjmed.2015.06.017
Peri, K., Kerse, N., Robinson, E., Parsons, M., Parsons, J., & Latham, N. (2008). Does functionally based activity make a difference to health status and mobility? A randomised controlled trial in residential care facilities (The Promoting Independent Living Study; PILS). Age and Ageing, 37, 57–63. PubMed ID: 17965045 doi:10.1093/ageing/afm135
Rockwood, K., Stadnyk, K., MacKnight, C., McDowell, I., Hebert, R., & Hogan, D.B. (1999). A brief clinical instrument to classify frailty in elderly people. The Lancet, 353, 205–206. PubMed ID: 9923878 doi:10.1016/S0140-6736(98)04402-X
Rodriguez-Mañas, L., Feart, C., Mann, G., Vina, J., Chatterji, S., Chodzko-Zajko, W., … FOD-CC Group. (2013). Searching for an operational definition of frailty: A Delphi method based consensus statement: The frailty operative definition-consensus conference project. The Journals of Gerontology, Series A: Biological Sciences and Medical Sciences, 68, 62–67. PubMed ID: 22511289 doi:10.1093/gerona/gls119
Rosendahl, E., Lindelof, N., Littbrand, H., Yifter-Lindgren, E., Lundin-Olsson, L., Haglin, L., … Nyberg, L. (2006). High-intensity functional exercise program and protein-enriched energy supplement for older persons dependent in activities of daily living: A randomised controlled trial. The Australian Journal of Physiotherapy, 52, 105–113. PubMed ID: 16764547 doi:10.1016/S0004-9514(06)70045-9
Scott, B.R., Duthie, G.M., Thornton, H.R., & Dascombe, B.J. (2016). Training monitoring for resistance exercise: Theory and applications. Sports Medicine, 46, 687–698. PubMed ID: 26780346 doi:10.1007/s40279-015-0454-0
Serra-Rexach, J.A., Bustamante-Ara, N., Hierro Villaran, M., Gonzalez Gil, P., Sanz Ibanez, M.J., Blanco Sanz, N., … Lucia, A. (2011). Short-term, light- to moderate-intensity exercise training improves leg muscle strength in the oldest old: A randomized controlled trial. Journal of the American Geriatrics Society, 59, 594–602. PubMed ID: 21453381 doi:10.1111/j.1532-5415.2011.03356.x
Studenski, S., Perera, S., Wallace, D., Chandler, J.M., Duncan, P.W., Rooney, E., … Guralnik, J.M. (2003). Physical performance measures in the clinical setting. Journal of the American Geriatrics Society, 51, 314–322. PubMed ID: 12588574 doi:10.1046/j.1532-5415.2003.51104.x
Taylor, D., Hale, L., Schluter, P., Waters, D.L., Binns, E.E., McCracken, H., … Wolf, S.L. (2012). Effectiveness of tai chi as a community-based falls prevention intervention: A randomized controlled trial. Journal of the American Geriatrics Society, 60(5), 841–848. PubMed ID: 22587850 doi:10.1111/j.1532-5415.2012.03928.x
Theou, O., Stathokostas, L., Roland, K.P., Jakobi, J.M., Patterson, C., Vandervoort, A.A., & Jones, G.R. (2011). The effectiveness of exercise interventions for the management of frailty: A systematic review. Journal of Aging Research, 2011, 1–19. PubMed ID: 21584244 doi:10.4061/2011/569194
Tiggemann, C.L., Korzenowski, A.L., Brentano, M.A., Tartaruga, M.P., Alberton, C.L., & Kruel, L.F. (2010). Perceived exertion in different strength exercise loads in sedentary, active, and trained adults. Journal of Strength and Conditioning Research, 24, 2032–2041. PubMed ID: 20634752 doi:10.1519/JSC.0b013e3181d32e29
Trappe, S., Gallagher, P., Harber, M., Carrithers, J., Fluckey, J., & Trappe, T. (2003). Single muscle fibre contractile properties in young and old men and women. The Journal of Physiology, 552, 47–58. PubMed ID: 12837929 doi:10.1113/jphysiol.2003.044966
Westhoff, M.H., Stemmerik, L., & Boshuizen, H.C. (2000). Effects of a low-intensity strength-training program on knee-extensor strength and functional ability of frail older people. Journal of Aging and Physical Activity, 8, 214–227.
Wolf, S.L., Barnhart, H.X., Kutner, N.G., McNeely, E., Coogler, C., & Xu, T. (1996). Reducing frailty and falls in older persons: An investigation of Tai Chi and computerized balance training. Atlanta FICSIT Group. Frailty and Injuries: Cooperative Studies of Intervention Techniques. Journal of the American Geriatrics Society, 44(5), 489–497. PubMed ID: 8617895 doi:10.1111/j.1532-5415.1996.tb01432.x
Zech, A., Drey, M., Freiberger, E., Hentschke, C., Bauer, J.M., Sieber, C.C., & Pfeifer, K. (2012). Residual effects of muscle strength and muscle power training and detraining on physical function in community-dwelling prefrail older adults: A randomized controlled trial. BMC Geriatrics, 12, 68. PubMed ID: 23134737 doi:10.1186/1471-2318-12-68
