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Effects of Resistance Training on Functional Strength and Muscle Mass in 70-Year-Old Individuals With Pre-sarcopenia: A Randomized Controlled Trial

Open AccessPublished:November 07, 2018DOI:https://doi.org/10.1016/j.jamda.2018.09.011

      Abstract

      Objective

      Sarcopenia has been defined as age-related loss of muscle mass and function. The aim of this randomized controlled trial was to examine the effects of a 10-week instructor-led resistance training program on functional strength and body composition in men and women aged 70 years with pre-sarcopenia.

      Design, Setting, and Participants

      Participants were randomized to either 10 weeks of a physical training regimen including optional nutritional supplementation (n = 36) or to a control group (n = 34) (ClinicalTrials.gov, no. NCT03297632). The main outcome was changes in the Short Physical Performance Battery (SPPB) score. Secondary outcomes included the Timed Up and Go test, chair sit-stand time, lean body mass, and fat mass.

      Results

      The intervention had no significant effect on SPPB in the total cohort (P = .18), when comparing changes in the intervention group with the control group. However, those given the intervention in the male subcohort increased 0.5 ± 0.4 (mean ± standard error for the difference) points in SPPB during follow-up (P = .02) compared to male controls. With respect to secondary outcomes, the intervention group decreased 0.9 ± 0.6 seconds in chair sit-stand time compared to controls (P = .01). Furthermore, the intervention resulted in significantly greater improvements for the training group than control group in all measures of body composition (P ≤ .01 for all). For example, lean body mass increased by a mean of 1147 ± 282 g (P < .001), and total fat mass decreased by a mean of 553 ± 225 g (P = .003), favoring the intervention group.

      Conclusion/Implications

      The main finding of this intervention study is that an easy-to-use, functional resistance training program was effective in maintaining functional strength and increasing muscle mass in older adults with pre-sarcopenia.

      Keywords

      The term “sarcopenia” is often used to describe muscle atrophy, and currently sarcopenia affects up to 50% of individuals aged ≥80 years.
      • Burton L.A.
      • Sumukadas D.
      Optimal management of sarcopenia.
      The European Working Group on Sarcopenia in Older People (EWGSOP) has proposed the staging of sarcopenia as “pre-sarcopenia,” defined as low muscle mass, and “sarcopenia,” defined as low muscle mass and strength or poor physical performance.
      • Cruz-Jentoft A.J.
      • Baeyens J.P.
      • Bauer J.M.
      • et al.
      Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People.
      Low muscle mass and sarcopenia have been shown to independently predict falls, fractures, mortality, and overall poor health,
      • Janssen I.
      • Heymsfield S.B.
      • Ross R.
      Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability.
      • Beaudart C.
      • Zaaria M.
      • Pasleau F.
      • et al.
      Health outcomes of sarcopenia: A systematic review and meta-analysis.
      which often influence quality of life in older people. Given the consequences of sarcopenia associated with aging,
      • Goodpaster B.H.
      • Park S.W.
      • Harris T.B.
      • et al.
      The loss of skeletal muscle strength, mass, and quality in older adults: The health, aging and body composition study.
      • Siparsky P.N.
      • Kirkendall D.T.
      • Garrett Jr., W.E.
      Muscle changes in aging: Understanding sarcopenia.
      preventive measures with focus on older people would be of importance. Because physical inactivity predisposes for muscle wasting and loss of function, one important strategy to prevent sarcopenia could include increased physical activity.
      Resistance training (RT) programs have been demonstrated to increase muscle function and muscle mass to some degree in the general older individual.
      • Hazell T.
      • Kenno K.
      • Jakobi J.
      Functional benefit of power training for older adults.
      • Tschopp M.
      • Sattelmayer M.K.
      • Hilfiker R.
      Is power training or conventional resistance training better for function in elderly persons? A meta-analysis.
      Less is known about the effects of RT programs in older individuals with sarcopenia or pre-sarcopenia, which is of interest given the consequences outlined above. Furthermore, additional knowledge is also needed considering feasibility, sustainability, and safety of RT in individuals with sarcopenia or pre-sarcopenia.
      • Aagaard P.
      • Suetta C.
      • Caserotti P.
      • et al.
      Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure.
      As older individuals seem to prefer easy, accessible training regimens that are easy to perform in any setting, body weight–based exercise programs may be preferable to programs involving gym equipment.
      • Borde R.
      • Hortobagyi T.
      • Granacher U.
      Dose-response relationships of resistance training in healthy old adults: A systematic review and meta-analysis.
      The purpose of this study was to examine the effects of a 10-week instructor-led body weight–based resistance exercise program in men and women aged 70 years with pre-sarcopenia. The primary objective was to investigate whether the program improved functional strength. A secondary objective was to examine whether the training improved body composition including muscle mass.

      Methods

      Study Design

      The present investigation is a randomized, controlled, parallel-group, 2-arm trial with 1:1 allocation ratio (ClinicalTrials.gov, no. NCT03297632). This study was approved by the regional research ethical review board of Umeå (Dnr 2017-132-31M), with extension and reported according to the CONSORT guidelines.
      • Schulz K.F.
      • Altman D.G.
      • Moher D.
      CONSORT Group
      CONSORT 2010 statement: Updated guidelines for reporting parallel group randomised trials.

      Participants

      The participants included in the present study were selected from an ongoing, population-based, primary prevention study: the Healthy Ageing Initiative (HAI). In short, all 70-year-old individuals living in Umeå municipality, northern Sweden, were invited to complete a health survey with the aim of reducing the future risk of noncommunicable disease. The HAI study has no exclusion criteria and an attendance rate of 68% of the eligible population. The research protocol has been described in detail elsewhere.
      • Johansson J.
      • Nordstrom A.
      • Nordstrom P.
      Objectively measured physical activity is associated with parameters of bone in 70-year-old men and women.
      The eligibility criteria for the present study were based on the normative values of the first diagnosis criterion for pre-sarcopenia and sarcopenia laid out by the EWGSOP, which in this population translated to appendicular lean mass index (defined as arm lean mass + leg lean mass divided by height squared) ≤ 7.29 (range, 5.69-7.29) among men, and ≤5.93 (range, 4.50-5.93) among women.
      • Cruz-Jentoft A.J.
      • Baeyens J.P.
      • Bauer J.M.
      • et al.
      Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People.

      Intervention

      All participants were assessed at baseline, then randomized to a control or intervention group using a total of 72 opaque sealed envelopes containing notes with “Training” or “Control” written on them (36 of each). Envelopes were prepared and controlled by A.H. and N.S. prior to randomization. The envelopes were then scrambled before each participant was allowed to draw an envelope and thus find out which group they were allocated to under the supervision of S.V. and L.B. Participants in the control group were asked to go about their normal lives and were scheduled for a second assessment 10 weeks later. Persons in the intervention group were assigned to participate in a 10-week instructor-led progressive RT program consisting of 3 sessions (∼45 minutes each) per week with groups of ≤12 participants. All participants were assessed at the end of the intervention. The investigator performing the assessments at baseline and follow-up was blinded to group allocation.
      The RT intervention was designed to increase participants' functional strength and muscle mass. Moderate to high RT intensity was applied using the Borg CR-10 scale,
      • Capodaglio E.M.
      Comparison between the CR10 Borg's scale and the VAS (visual analogue scale) during an arm-cranking exercise.
      • Borg G.
      • Hassmén P.
      • Lagerström M.
      Perceived exertion related to heart rate and blood lactate during arm and leg exercise.
      with participants' perceived exertion scoring 6 to 7 of a maximum of 10. During the sessions, 8 exercises were performed with the aim of engaging muscle groups in the whole body, with a focus on strengthening of the lower-extremity muscles using functional exercises that are relevant for activities of daily living.
      • Borg G.
      • Hassmén P.
      • Lagerström M.
      Perceived exertion related to heart rate and blood lactate during arm and leg exercise.
      Also, suspension bands were used as support for a majority of the exercises. Please see Supplementary Figure 1 for pictures and supplementary video for a short film describing the exercises performed in the RT intervention.
      All training sessions started with 5 to 10 minutes of whole-body warm-up exercises. During the first week of training, no weight was used; the focus was on learning the exercises in a safe way using only participants' body weight and suspension bands. In the first week, exercises were performed in 2 sets of 12 repetitions each, followed by 3 sets of 10 repetitions each in weeks 2 to 4. The intensity of the program increased in terms of sets and resistance, with maintenance of CR-10 scores of 6 to 7. In weeks 5 to 7, participants performed 4 sets of 10 repetitions each. Up until this point, participants had been instructed that concentric and eccentric muscle contractions should last for approximately 2 seconds each. In weeks 8 to 10, the focus was on muscle power training using the same exercises, although participants were instructed to perform these exercises with considerably faster muscle contractions. During the training sessions, 2 instructors were present and supervised the training. The instructors' role was both to make sure the exercises were performed correctly, in a safe way, and also to monitor the maintenance of intensity. Once a week, the instructors noted the weight each participant used in every exercise by using a luggage scale. During the training sessions, instructors asked the participants what they scored on CR-10 scale; if they scored less than 6, more weight was added progressively. By using a protocol where the weight each participant used every week was noted, participants knew where to start the next week. For the exercises without weights, such as resistance band exercises, markers on the floor were used to easily know where to start and how to increase resistance. Resistance bands and weight vests, weight belts, and backpacks filled with weights or water bottles were offered. A nutritional supplement (taken once a day for 10 weeks) was also offered to participants in the intervention group, but it was not a mandatory component of the program. The 250-mL liquid supplement was milk based with added milk protein, supplying 175 kcal in the form of 19 g carbohydrates, 21 g protein, and 1.5 g fat (week 1-7 of the intervention) or 10 g carbohydrates, 30 g protein, and 1.5 g fat (week 8-10 of the intervention) (Gainomax Protein Drink, Norrmejerier, Umeå, Sweden).

      Assessment

      Primary outcome

      Functional strength and physical function in the lower extremities were assessed using the Short Physical Performance Battery (SPPB).
      • Guralnik J.M.
      • Simonsick E.M.
      • Ferrucci L.
      • et al.
      A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission.
      The SPPB includes assessment of a standing balance test, a walk test, and a chair sit-stand test. For the balance test, participants were asked to stand in a side-by-side position, a semitandem position, and a full-tandem position. To receive 1 point and advance to the semitandem stance, participants had to be able to hold the side-by-side position for at least 10 seconds. The same procedure was used for the tandem positions. The walk test included a 4-m walk from standing position in preferred gait speed (the fastest time of 2 trials was used). For the chair sit-stand test, participants were asked to complete 5 chair sit-stand cycles as rapidly as possible with the arms folded across the chest.
      Total SPPB scores (range, 0-12) were calculated by summing up the 3 individual scores [each ranging from 0 (unable to complete test) to 4]. Cut points for individual test scores of 1 to 4 were based on previously established quartiles of timed performance (for the gait speed and chair sit-stand tests) or criteria (for the balance test), according to the methods developed by Guralnik et al.
      • Guralnik J.M.
      • Simonsick E.M.
      • Ferrucci L.
      • et al.
      A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission.
      Higher total scores indicated greater lower-extremity functional strength.

      Secondary outcomes

      The separate tests included in the SPPB were used as separate outcomes. Participants performed the Timed Up and Go (TUG) test, which quantifies functional mobility, lower-leg muscle strength, and gait performance.
      • Capodaglio E.M.
      Comparison between the CR10 Borg's scale and the VAS (visual analogue scale) during an arm-cranking exercise.
      Participants started in a seated position on a chair with armrests, then stood and walked 3 m at normal gait speed, turned 180°, walked back to the chair, and sat down. The test was performed once and timed.
      Using a hydraulic hand dynamometer (Jamar; Patterson Medical, Warrenville, IL), isometric muscle strength was tested as a marker of general body strength. Participants were instructed to stand while maintaining the nondominant arm at 90° with the elbow close to the waist, and the maximum grip strength (in kilograms) was measured. The maximum value obtained in 2 consecutive attempts was recorded. Participants' height while barefoot (in meters) was determined using a stadiometer (Holtain Limited; Crymych, Dyfed, United Kingdom) and their body weight (in kilograms) was measured using a clinical scale (HL 120; Avery Berkel, Fairmont, MN). Body mass index was calculated by dividing the body weight with height squared.
      Lean body mass (LBM) was analyzed using a Lunar iDXA device (GE Healthcare Lunar, Madison, WI).
      • Borg G.
      • Hassmén P.
      • Lagerström M.
      Perceived exertion related to heart rate and blood lactate during arm and leg exercise.
      The appendicular lean mass index was calculated by dividing the total muscle mass in the arms and legs by height squared, according to the EWGSOP standard. Also total fat mass (FM) was derived from the iDXA scan.
      • Guralnik J.M.
      • Simonsick E.M.
      • Ferrucci L.
      • et al.
      A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission.

      Statistical Analysis

      Descriptive statistics were calculated, and values are presented as means and standard deviations. The paired-samples t-test was used to assess changes within groups in functional strength and body composition over time (baseline to post-intervention). Between-group comparison of outcome measures was conducted using analysis of covariance, where the value for the outcome at the 10th week of follow-up was used as independent variable with adjustment for baseline values for the outcome.
      • Zhang S.
      • Paul J.
      • Nantha-Aree M.
      • et al.
      Empirical comparison of four baseline covariate adjustment methods in analysis of continuous outcomes in randomized controlled trials.
      Statistical interaction for the outcomes of interest was tested by creating product interaction terms for sex and intervention (both 0 or 1), which were added to the other independent variables (sex, intervention, and baseline value for the outcome variable tested) in the statistical models. For these analyses, P values < 0.1 were considered to be significant. For all other analyses, P values < .05 were considered to be significant. All statistical tests were performed using SPSS software (version 24 for Macintosh; IBM Corporation, Armonk, NY) by researchers blinded to participant allocation.

      Results

      Participant Recruitment, Allocation, and Adherence to Intervention

      Of the 787 individuals who had been participating in the HAI study during the past year (August 2016 to July 2017), a total of 161 persons (76 men and 85 women) met the inclusion criterion based on a low muscle mass, as defined in the Methods section. Recruitment ceased when the predetermined sample size of 72 subjects (34 men and 38 women) was met. The main reason for declining participation was due to not having the time to participate. Of the 72 persons included, 2 persons failed to attend baseline testing, week 1 August 2017, resulting in a total study sample of 70 persons prior to randomization (Figure 1). After baseline testing, 36 persons were randomized to the intervention group and 34 persons to the control group. Four of the 36 participants randomized to the intervention group dropped out before the intervention started because of lack of time, and one person dropped out after 8 weeks of the intervention because of severe disease; thus, 31 participants in the intervention group finished the assessment conducted after 10 weeks. The mean intervention attendance rate to the training sessions was 91% (range, 63%-100%) and 26 of 31 (84%) participants in the intervention group chose to take the nutritional supplement. All participants assigned to the control group finished the second assessment.
      Figure thumbnail gr1
      Fig. 1Flow chart of study participants and allocation.

      Participant Characteristics

      The characteristics of the sample, including baseline data, are shown in Table 1. The mean age of the participants was 70.9 ± 0.03 years, with equal representation of men and women (54% women). Body mass indices ranged from 16.4 to 32.4 (mean, 23.3). The groups had similar characteristics at baseline, although the intervention group performed slightly better at tests on physical function, for example, walking speed and sit-to-stand time. The LBM measurements for the 2 groups were similar. Four subjects in each group reported a previous fracture.
      Table 1Participant Characteristics at Baseline
      VariablesControl (n = 34)Intervention (n = 36)Total (N = 70)
      Age, y70.0 ± 0.2970.9 ± 0.2870.9 ± 0.03
      Female, n (%)18 (53)20 (56)38 (54)
      Height, m1.69 ± 0.111.68 ± 0.091.69 ± 9.63
      Weight, kg67.4 ± 14.064.8 ± 11.566.1 ± 12.7
      BMI23.33 ± 3.0122.72 ± 2.3523.01 ± 2.69
      SPPB
       Walk, s3.8 ± 0.983.3 ± 0.693.5 ± 0.87
       Sit to stand, s10.6 ± 4.089.5 ± 2.7310.1 ± 3.46
       Balance, 0-43.7 ± 0.73.8 ± 0.53.8 ± 0.6
       Total score11.0 ± 1.7111.4 ± 1.3811.2 ± 1.55
      TUG, s9.9 ± 2.349.0 ± 1.839.4 ± 2.13
      Hand grip, kg29.9 ± 11.132.0 ± 10.031.0 ± 10.5
      DXA measurements
       Total fat mass23.06 ± 8.0720.53 ± 4.9821.82 ± 6.72
       Total lean mass41.84 ± 8.6041.66 ± 7.7041.74 ± 8.10
       Arm lean mass4.55 ± 1.444.46 ± 1.304.50 ± 1.36
       Leg lean mass13.63 ± 3.1013.46 ± 2.8013.54 ± 2.91
       ALMI6.24 ± 0.856.25 ± 0.866.24 ± 0.85
      ALMI, appendicular lean mass index; BMI, body mass index; DXA, dual-energy x-ray absorptiometry.
      Values are presented as means ± standard deviations, except where otherwise indicated.

      Effects of the Intervention on Estimates of Functional Strength

      When comparing the intervention group and control group, the change in the SPPB total during follow-up was not significant (P = .18), although the sit-to-stand test was significantly improved by 0.9 ± 0.6 (mean ± standard error for the difference) seconds in the intervention group compared with the control group (P = .01; Table 2). Moreover, there was a significant interaction for sex with respect to the effects of the intervention during follow-up for several outcomes (P < .10). In men (Figure 2), the intervention group increased 0.5 ± 0.4 points during follow-up in the SPPB total score (P = .02) and decreased 1.2 ± 0.6 seconds in TUG (P = .04) compared to that in male controls. During follow-up, the intervention group showed improvement in all functional outcomes, including the total SPPB score (all P < .05), TUG time (P < .001), and handgrip strength (P = .007). In contrast, the control group showed no improvement in functional outcomes, except for TUG time (P = .02).
      Table 2Changes in the Outcomes During the 10-Week Intervention Period
      Within-Group DifferencesBetween-Group Differences
      Control (n = 34)Intervention (n = 31)Control (n = 34)Intervention (n = 31)
      Baseline10 wkPBaseline10 wkPDifferenceDifferenceP
      SPPB
       Walk, s3.81 ± 0.983.85 ± 1.64.833.29 ± 0.723.09 ± 0.67.0070.05 ± 1.27−0.20 ± 0.39.24
       Sit to stand, s10.6 ± 4.0810.5 ± 4.00.469.43 ± 2.818.25 ± 2.12.005−0.30 ± 2.24−1.18 ± 2.19.01
       Balance, 0-43.7 ± 0.73.8 ± 0.5.373.8 ± 0.53.8 ± 0.5>.9990.1 ± 0.50.0 ± 0.5.54
       Total score, 0-1211.0 ± 1.7111.1 ± 1.94.8211.4 ± 1.4511.7 ± 0.97.0480.06 ± 1.510.32 ± 0.87.18
      TUG, s9.89 ± 2.349.10 ± 3.14.028.90 ± 1.947.57 ± 1.53<.001−0.78 ± 1.87−1.33 ± 1.44.12
      Handgrip, kg30.0 ± 11.130.5 ± 10.6.4130.7 ± 9.5532.0 ± 10.7.0070.56 ± 3.901.30 ± 2.50.36
      DXA measurement
       Total fat mass, kg23.1 ± 8.0723.1 ± 7.91.8920.5 ± 4.9920.0 ± 4.64.0020.022 ± 0.90−0.56 ± 0.90.003
       Total lean mass, kg41.8 ± 8.6441.9 ± 8.63.6940.8 ± 7.6041.9 ± 7.94<.0010.007 ± 1.351.17 ± 0.80<.001
       Arm lean mass, kg4.56 ± 1.444.57 ± 1.46.714.30 ± 1.224.53 ± 1.31<.0010.015 ± 0.220.23 ± 0.28<.001
       Leg lean mass, kg13.6 ± 3.0713.6 ± 3.02.6613.2 ± 2.8113.6 ± 2.82<.001−0.044 ± 0.650.44 ± 0.37<.001
       ALMI6.24 ± 0.856.23 ± 0.86.586.17 ± 0.876.40 ± 0.89<.001−0.005 ± 0.250.24 ± 0.17<.001
      ALMI, appendicular lean mass index.
      Values are presented as means ± SDs.
      Figure thumbnail gr2
      Fig. 2Changes from baseline in functional strength in the intervention group and control group for men and women separately. Means and standard error of the mean are presented.

      Effects of the Intervention on Body Composition

      The intervention group showed significant improvement in LBM and FM compared with the control group (P < .01 for both; Table 2) during follow-up. Thus, LBM increased by 1147 ± 282 g (P < .001) and total FM decreased by a mean of 553 ± 225 g (P = .003), compared with the control group. In addition, lean arm mass, lean leg mass, and the appendicular lean mass index improved in the intervention group compared to the control group (P < .001 for all). LBM increased 2.8% in the intervention group whereas FM decreased 2.4%, with no apparent sex difference in intervention effect (Figure 3). In the control group, no significant change in any body composition parameter was observed during the intervention period.
      Figure thumbnail gr3
      Fig. 3Changes from baseline in body composition in the intervention group and control group for men and women separately. Means and standard error of the mean are presented. (ALMI, appendicular lean mass index.)

      Effects of the Intervention on Perceived Health and Side Effects

      During the course of the training intervention, several aspects of perceived health and possible side effects were documented from the intervention group. A participant who previously had undergone shoulder surgery experienced shoulder pain, particularly during push-ups, with pain sensations also between training sessions. Another participant experienced vertigo on a few occasions during training sessions. A third participant experienced knee pain that endured for about 1 week. Most of the participants in the training group reported delayed-onset muscle soreness, mainly located to hamstrings and quadriceps femoris. Furthermore, 2 participants reported cessation of back pain, a condition they had well before the start of the study. Additionally, another participant reported less headache and total relief of neck pain as compared to before the start of the intervention.

      Discussion

      In the present randomized study, a 10-week body weight–based RT program resulted in significant effects on the primary outcome of the SPPB test, but only in the male subgroup. With respect to the other functional outcomes, there was a significant effect of the intervention on the sit-to-stand test in the total cohort of men and women. Overall, all outcomes improved significantly in the intervention group, whereas all results but the TUG time remained stable in the control group. With respect to body composition, the intervention group improved in all measures of body composition, including high gains in LBM, compared with the control group. Importantly, all exercises were designed so that they would be easy to perform in participants' homes, in contrast to programs involving the use of weight machines.
      • Borde R.
      • Hortobagyi T.
      • Granacher U.
      Dose-response relationships of resistance training in healthy old adults: A systematic review and meta-analysis.
      Low muscle mass is known to independently predict falls,
      • Landi F.
      • Liperoti R.
      • Russo A.
      • et al.
      Sarcopenia as a risk factor for falls in elderly individuals: Results from the ilSIRENTE study.
      fractures, and overall poor health, including death.
      • Beaudart C.
      • Zaaria M.
      • Pasleau F.
      • et al.
      Health outcomes of sarcopenia: A systematic review and meta-analysis.
      The development of a customized physical training program that could improve muscle strength and mass in frail older individuals is thus of interest. Weight training is known to predominantly increase muscle strength initially by neuromuscular adaptation, in younger and older individuals.
      • Hakkinen K.
      • Alen M.
      • Kallinen M.
      • et al.
      Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people.
      The observed increase in muscle mass during a training period of only 10 weeks was thus an unexpected, though encouraging finding of this study. Thus, RT programs most often have limited effects on muscle hypertrophy in older adults,
      • Hakkinen K.
      • Alen M.
      • Kallinen M.
      • et al.
      Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people.
      and the effects seem to be influenced by aging. In a meta-analysis including a total of 1328 individuals with a mean age of 65 years, the effects of RT on lean body were rather similar to that in our study, albeit during 20 weeks of training.
      • Peterson M.D.
      • Sen A.
      • Gordon P.M.
      Influence of resistance exercise on lean body mass in aging adults: A meta-analysis.
      In addition, the effects were lower in subjects with a higher age. The effects of training in our study are especially encouraging because we only included individuals with low muscle mass, which may be regarded as irreversible in older people. The increases in muscle mass could have been influenced both by the nutritional supplement offered to individuals in the intervention group and the specific RT program used. Several previous studies have identified protein intake as a key factor for sarcopenia prevention in older people,
      • Baum J.I.
      • Kim I.Y.
      • Wolfe R.R.
      Protein consumption and the elderly: What is the optimal level of intake?.
      • Nowson C.
      • O'Connell S.
      Protein requirements and recommendations for older people: A review.
      • Wolfe R.R.
      • Miller S.L.
      • Miller K.B.
      Optimal protein intake in the elderly.
      especially during RT in adults.
      • Morton R.W.
      • Murphy K.T.
      • McKellar S.R.
      • et al.
      A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults.
      This was the reason for offering the supplement, and the effects seen on muscle mass was likely influenced by this component. In addition, the type and high intensity of training most likely influenced the gains seen. The participants were highly motivated and trained at high intensity 3 times a week, with a participation rate of 91%. Previously, high-intensity RT programs, rather than training at low intensity, has been shown to result in high increases in muscle strength in untrained older individuals.
      • Csapo R.
      • Alegre L.M.
      Effects of resistance training with moderate vs heavy loads on muscle mass and strength in the elderly: A meta-analysis.
      • Hagerman F.C.
      • Walsh S.J.
      • Staron R.S.
      • et al.
      Effects of high-intensity resistance training on untrained older men. I. Strength, cardiovascular, and metabolic responses.
      Given the high effects of the RT program on muscle mass, similar improvements would be expected on the functional measures. However, the improvements were smaller and reached significance predominantly in the male subcohort. These gender-specific effects may be attributable to external factors, such as motivation and competition, which were observed during training and could have influenced the results. In support of this hypothesis, the effects of the intervention on LBM were similar in men and women. The relatively low effects on the main outcome of SPPB also can be explained likely by a ceiling effect. Thus, the mean baseline score was 11.2 of a maximum of 12, with no room for improvement for many participants. This ceiling effect was obvious for the standing balance test, whereas the intervention had significant effect on the sit-to-stand test that also is part of the SPPB. As an increase in lean arm mass was observed in the intervention group, the assessment of upper body strength in addition to lower extremity strength, for example, the Continuous Scale–Physical Functional Performance,
      • Cress M.E.
      • Petrella J.K.
      • Moore T.L.
      • Schenkman M.L.
      Continuous-scale physical functional performance test: Validity, reliability, and sensitivity of data for the short version.
      might therefore have been of interest to test in addition to hand grip strength.
      A potential limitation of the present study is the sample size. A larger sample would have increased the statistical power of the analysis, which might have influenced the results, especially in the sex-stratified analysis. Yet, the effect of the intervention on body composition was significant, and the lack of effect on SPPB scores in the total cohort was likely also influenced by a ceiling effect. In addition, we could not determine whether the observed effects of the intervention were due to the training program and/or the recovery drink. Thus, the inclusion of an additional training group that did not receive the recovery drink would have been of value. Given the effects especially on muscle mass in the intervention group, the possibility of a measurement error must be considered. However, the changes seen in fat mass and LBM were in accordance with the changes seen in total body weight, measured by a digital scale. In addition, any measurement error would influence the intervention and control groups similarly. Finally, dual-energy x-ray absorptiometry has been demonstrated to be very accurate in determining LBM and changes in LBM.
      • Guralnik J.M.
      • Simonsick E.M.
      • Ferrucci L.
      • et al.
      A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission.
      • Branski L.K.
      • Norbury W.B.
      • Herndon D.N.
      • et al.
      Measurement of body composition in burned children: Is there a gold standard?.
      The major strength of the present study was the randomized design with assessors blinded to the intervention, decreasing the risk of bias and confounding. Another strength is the design of the training program, which does not require gym equipment and focuses on functional exercises that are easy to perform in any setting.

      Conclusions/Relevance

      The key finding of this study is that an easy-to-use strength training program with a focus on body weight–based exercises was effective in preventing loss in functional strength and increasing muscle mass and in older adults with pre-sarcopenia. Based on our experience with the intervention program, we suggest that it is important to progressively increase training load and to motivate participants to train at a high intensity. These improvements may influence future falls, fractures, and overall poor health. Finally, the effects with respect to muscle mass should be examined further in additional studies to determine whether they were caused jointly by nutritional supplementation and training. The sample for the present study was population based, with no exclusion criteria applied to men and women with pre-sarcopenia. We thus believe that the results can be generalized to older individuals with low muscle mass.

      Acknowledgments

      The authors would like to thank all of the amazing participants for their enthusiasm in participating in this project and making this study possible. We would also like to thank Monica Ahlenius for her management of participant recruitment and Sabine Björk for her help with data collection, and Umeå School of Sport Sciences at Umeå University for financial support.

      Supplementary Data

      References

        • Burton L.A.
        • Sumukadas D.
        Optimal management of sarcopenia.
        Clin Interv Aging. 2010; 5: 217-228
        • Cruz-Jentoft A.J.
        • Baeyens J.P.
        • Bauer J.M.
        • et al.
        Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People.
        Age Ageing. 2010; 39: 412-423
        • Janssen I.
        • Heymsfield S.B.
        • Ross R.
        Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability.
        J Am Geriatr Soc. 2002; 50: 889-896
        • Beaudart C.
        • Zaaria M.
        • Pasleau F.
        • et al.
        Health outcomes of sarcopenia: A systematic review and meta-analysis.
        PLoS One. 2017; 12: e0169548
        • Goodpaster B.H.
        • Park S.W.
        • Harris T.B.
        • et al.
        The loss of skeletal muscle strength, mass, and quality in older adults: The health, aging and body composition study.
        J Gerontol A Biol Sci Med Sci. 2006; 61: 1059-1064
        • Siparsky P.N.
        • Kirkendall D.T.
        • Garrett Jr., W.E.
        Muscle changes in aging: Understanding sarcopenia.
        Sports Health. 2014; 6: 36-40
        • Hazell T.
        • Kenno K.
        • Jakobi J.
        Functional benefit of power training for older adults.
        J Aging Phys Act. 2007; 15: 349-359
        • Tschopp M.
        • Sattelmayer M.K.
        • Hilfiker R.
        Is power training or conventional resistance training better for function in elderly persons? A meta-analysis.
        Age Ageing. 2011; 40: 549-556
        • Aagaard P.
        • Suetta C.
        • Caserotti P.
        • et al.
        Role of the nervous system in sarcopenia and muscle atrophy with aging: Strength training as a countermeasure.
        Scand J Med Sci Sports. 2010; 20: 49-64
        • Borde R.
        • Hortobagyi T.
        • Granacher U.
        Dose-response relationships of resistance training in healthy old adults: A systematic review and meta-analysis.
        Sports Med. 2015; 45: 1693-1720
        • Schulz K.F.
        • Altman D.G.
        • Moher D.
        • CONSORT Group
        CONSORT 2010 statement: Updated guidelines for reporting parallel group randomised trials.
        BMJ. 2010; 340: c332
        • Johansson J.
        • Nordstrom A.
        • Nordstrom P.
        Objectively measured physical activity is associated with parameters of bone in 70-year-old men and women.
        Bone. 2015; 81: 72-79
        • Capodaglio E.M.
        Comparison between the CR10 Borg's scale and the VAS (visual analogue scale) during an arm-cranking exercise.
        J Occup Rehabil. 2001; 11: 69-74
        • Borg G.
        • Hassmén P.
        • Lagerström M.
        Perceived exertion related to heart rate and blood lactate during arm and leg exercise.
        Eur J Appl Physiol Occup Physiol. 1987; 56: 679-685
        • Guralnik J.M.
        • Simonsick E.M.
        • Ferrucci L.
        • et al.
        A short physical performance battery assessing lower extremity function: association with self-reported disability and prediction of mortality and nursing home admission.
        J Gerontol. 1994; 49: M85-M94
        • Zhang S.
        • Paul J.
        • Nantha-Aree M.
        • et al.
        Empirical comparison of four baseline covariate adjustment methods in analysis of continuous outcomes in randomized controlled trials.
        Clin Epidemiol. 2014; 6: 227-235
        • Landi F.
        • Liperoti R.
        • Russo A.
        • et al.
        Sarcopenia as a risk factor for falls in elderly individuals: Results from the ilSIRENTE study.
        Clin Nutr. 2012; 31: 652-658
        • Hakkinen K.
        • Alen M.
        • Kallinen M.
        • et al.
        Neuromuscular adaptation during prolonged strength training, detraining and re-strength-training in middle-aged and elderly people.
        Eur J Appl Physiol. 2000; 83: 51-62
        • Peterson M.D.
        • Sen A.
        • Gordon P.M.
        Influence of resistance exercise on lean body mass in aging adults: A meta-analysis.
        Med Sci Sports Exerc. 2011; 43: 249-258
        • Baum J.I.
        • Kim I.Y.
        • Wolfe R.R.
        Protein consumption and the elderly: What is the optimal level of intake?.
        Nutrients. 2016; 8: E359
        • Nowson C.
        • O'Connell S.
        Protein requirements and recommendations for older people: A review.
        Nutrients. 2015; 7: 6874-6899
        • Wolfe R.R.
        • Miller S.L.
        • Miller K.B.
        Optimal protein intake in the elderly.
        Clin Nutr. 2008; 27: 675-684
        • Morton R.W.
        • Murphy K.T.
        • McKellar S.R.
        • et al.
        A systematic review, meta-analysis and meta-regression of the effect of protein supplementation on resistance training-induced gains in muscle mass and strength in healthy adults.
        Br J Sports Med. 2018; 52: 376-384
        • Csapo R.
        • Alegre L.M.
        Effects of resistance training with moderate vs heavy loads on muscle mass and strength in the elderly: A meta-analysis.
        Scand J Med Sci Sports. 2016; 26: 995-1006
        • Hagerman F.C.
        • Walsh S.J.
        • Staron R.S.
        • et al.
        Effects of high-intensity resistance training on untrained older men. I. Strength, cardiovascular, and metabolic responses.
        J Gerontol A Biol Sci Med Sci. 2000; 55: B336-B346
        • Cress M.E.
        • Petrella J.K.
        • Moore T.L.
        • Schenkman M.L.
        Continuous-scale physical functional performance test: Validity, reliability, and sensitivity of data for the short version.
        Phys Ther. 2005; 85: 323-335
        • Branski L.K.
        • Norbury W.B.
        • Herndon D.N.
        • et al.
        Measurement of body composition in burned children: Is there a gold standard?.
        JPEN J Parenter Enteral Nutr. 2010; 34: 55-63