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Exercise Snacking to Improve Muscle Function in Healthy Older Adults: A Pilot Study

Exercise Snacking to Improve Muscle Function in Healthy Older Adults: A Pilot Study Hindawi Journal of Aging Research Volume 2019, Article ID 7516939, 9 pages https://doi.org/10.1155/2019/7516939 Clinical Study Exercise Snacking to Improve Muscle Function in Healthy Older Adults: A Pilot Study 1,2 1 1,2 Oliver J. Perkin , Polly M. McGuigan, and Keith A. Stokes Department for Health, University of Bath, Bath BA2 7AY, UK Centre for Sport, Exercise and Osteoarthritis Research Versus Arthritis, Chesterfield, UK Correspondence should be addressed to Oliver J. Perkin; o.j.perkin@bath.ac.uk Received 20 June 2019; Revised 30 August 2019; Accepted 10 September 2019; Published 3 October 2019 Guest Editor: Marco C. Uchida Copyright©2019OliverJ.Perkinetal.+isisanopenaccessarticledistributedundertheCreativeCommonsAttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Loss of muscle mass and strength are seemingly accepted as part of the ageing process, despite ultimately leading to the loss of independence. Resistance exercise is considered to be primary defence against loss of muscle function in older age, but it typically requires access to exercise equipment often in a gym environment. +is pilot study aimed at examining the effect of a 28-day, unsupervised home-based exercise intervention on indices of leg strength and muscle size in healthy older adults. Twenty participants were randomly assigned to either maintain their habitual physical activity levels (Control; n � 10; age, 74 (5) years; 2 2 body mass, 26.3 (3.5)kg/m ) or undertake “exercise snacks” twice daily (ES; n � 10; age, 70 (4) years; body mass, 25.0 (3.4)kg/m ). Both groups consumed 150g of yogurt at their breakfast meal for the duration of the intervention. Sixty-second sit-to-stand score improved by 31% in ES, with no change in Control (p<0.01). Large effect sizes were observed for the difference in change scores between the groups for interpolated maximum leg pressing power (6% increase in ES) and thigh muscle cross-sectional area (2% increase in ES). +e present pilot data suggest that exercise snacking might be a promising strategy to improve leg muscle function and size in older adults and that further investigation into zero-cost exercise strategies that allow high frequency of training is warranted. Progressive resistance exercise training improves muscle 1. Introduction strength in older adults, and it is accompanied by multi- Frailty is underpinned by a progressive loss of muscle faceted improvements in health and function [6, 7]. Tra- mass and strength, particularly from the lower limbs, and ditionally, heavy load resistance training has been regarded is associated with increased risk of falls and reduced as the most effective strategy to increase muscle strength, due quality of life [1, 2]. +ere is a minimum threshold of to associated neural and hypertrophic adaptations [8, 9]. strength required to complete tasks of daily living in- Recent evidence suggests that low-load resistance training dependently, and finding means to delay individuals can also be efficacious in increasing muscle strength, par- reaching this “frailty threshold” has been identified as an ticularly in an untrained population, albeit to a lesser degree urgent health care priority [3]. With muscle mass lost at in comparison to high-load resistance training [10, 11]. 0.5–1% per year after 50 years of age [4] and strength lost Training with low loads and low overall session volume may even more rapidly [5], modest improvements of a few allow for increased training frequency, as recovery times percent in muscle size and strength from a training may be shorter between sessions [12]. Dankel et al. [13] programme may, in essence, represent postponement of suggests that manipulation of training frequency to maintain frailty measurable in years. Crucially, intervention is overall training volume with more sessions of lower load needed before older adults’ functional capacity declines across a week may even increase hypertrophic training re- past the point that exercise is no longer a safe means to sponses. Although this has not yet been borne out empir- maintain muscle strength. ically [8], it is intuitively appealing to reason that a reduced 2 Journal of Aging Research training session load with short recovery times may suit an sessions and during the last week of the intervention, older population previously doing no formal exercise be- physical activity and diet were assessed. See Figure 1 for a schematic overview of the pilot study timeline. cause it may overcome some of the barriers to starting an exercise programme [14]. Short bouts of exercise spread across the day, termed 2.1. Participants. Twenty healthy, community-dwelling, “exercise snacks,” have received attention as a time-efficient older men and women (65–80 years), not undertaking regular exercise strategy. Francois et al. [15] identified that exercise structured exercise, were recruited for the pilot study through snacking before each meal, consisting of six discrete local newspaper advertisement and social media. Individuals minutes of exercise separated by one minute of rest, im- who were nonsmokers, had BMI of ≥20<30kg/m , had no proved glycaemic control the following day in middle-aged contraindications to exercise or recent history of musculo- adults with impaired glucose handling. Jenkins et al. [16] skeletal injury, and had scored 8 or above with no score of reported improvements in cardiorespiratory fitness in zero on any test of the SPPB [18] at the initial screening were healthy inactive adults performing three sets of maximum invited to take part in the pilot study. Participants were effort 60-step stair climbs a day, three times a week, for six assigned to groups by way of minimisation to limit differences weeks. +e improvement in exercise tolerance included an in mean age, BMI, and 60-second sit-to-stand (STS) score at increase in maximum power output during a VO peak test the screening visit, on account of the small sample size on a cycle ergometer [16]. +is suggests that an exercise [19, 20]. An individual outside of the study team performed snacking model may have the potential to improve function participant group allocation. Participant characteristics beyond just cardiovascular fitness. As such, exercise recorded during screening are presented in Table 1. All snacking was examined in the present pilot study with the participants provided written informed consent. +e protocol aim of providing a stimulus to improve leg strength in older was approved by the National Health Service (NHS) South adults that could be undertaken in the home on a daily basis West—Frenchay Research Ethics Committee (Ref: 16/SW/ without the need for supervision. 0300) and registered on ClinicalTrials.gov (Identifier: +e primary aim of the present pilot study was to in- NCT02991989). vestigate the effects of four weeks of twice daily “exercise snacking” on maximum number of sit-to-stands from a chair performed in one minute, compared with a control 3. Measures group maintaining their habitual physical activity patterns. +e secondary aims were to assess adherence to the exercise 3.1. Imaging. Participants arrived at the laboratory for trial snacking intervention, along with the effects on force, ve- days following a 10-hour overnight fast, having drunk 1 pint locity, and power, during leg press dynamometry and on of water, and having not undertaken exhaustive exercise in whole-body and lower limb anthropometry. +e proposed the previous 24 hours. Participants were asked to void before intervention was specifically designed to be suitable to weight was measured with electronic scales (BC543, Tanita, perform in the home environment, without the need for Amsterdam, Netherlands). Whole-body composition, supervision or specific exercise equipment. +e overall whole-body lean mass, and leg lean mass were estimated objective of this pilot study was to inform future work on using a DXA system (QDR software version 12.4.2, Hologic exercise strategies extending to populations with lifestyle- Discovery W, Bedford, MA) by differentiating the fat, bone, compromising age-related loss of muscle strength or mass. and lean (nonbone nonfat) masses. A spine phantom was used for the quality control scan performed at the start of every trial day before participant testing, as per the man- 2. Materials and Methods ufacturer’s guidelines. Participants wore the same light A two-group experimental research design was used in this clothes for pre- and postintervention trials and removed all pilot study to examine the effects of twice daily “exercise metal items. +e investigator positioned the participant to be snacking” on muscle function and size in healthy, com- laying supine on the scanning bed such that body regions munity-dwelling older adults. For 28 days, one group un- could be partitioned upon analysis. Manual placement of dertook a home-based exercise snacking intervention (ES) boundaries between discrete anatomical regions was con- and the other group acted as a nonexercising control by ducted for all scans by the same investigator (OJP), before maintaining habitual physical activity levels. As a control analysis using manufacturer’s software. Lower limb (calf and thigh) muscle cross-sectional area variable, both groups were provided with 150g of yogurt to consume as part of their breakfast meal for the 28 days, to (mCSA) was assessed by peripheral quantitative computed tomography (pQCT; XCT3000, StraTec Medizintechnik both act as a “positive control” to reduce participant dropout from the Control group and to achieve optimal dietary GmbH, Pforzheim, Germany). During the preintervention protein intake [17]. All participants completed two famil- trial, tibia (medial knee joint line to medial malleolus) and iarisation sessions to functional measures used in the pre- femur length (greater trochanter to lateral knee joint line) of and postintervention assessment, separated by at least seven the dominant leg were measured using a fabric tape measure days, with the second session completed at least five days whilst participants were standing. Scans were performed before the preintervention assessments. Function testing and with the participant laying supine on a bed with leg placed imaging measures were completed on the day before and the through the scanning gantry and foot strapped into a day after the 28-day intervention. Between familiarisation footplate. Scout scans were performed at the distal ends of Journal of Aging Research 3 Eligibility assessment and familiarisation session 1 with muscle function measures 7 days of physical activity monitoring and 3-day food diary Familiarisation session 2 with muscle function measures >5 days Preintervention assessments of muscle function and imaging measures Exercise snacking group Control group (I) 28 days of twice daily exercise (I) 28 days maintaining habitual snacking; one in the morning physical activity levels and one in the evening around meal time (II) 28 days of 150 g yoghurt (II) 28 days of 150 g yoghurt consumed with the breakfast consumed with the breakfast meal daily meal daily (III) 7 days of physical activity (III) 7 days of physical activity monitoring and 3-day food monitoring and 3-day food diary during last week diary during last week Postintervention assessments of muscle function and scanning measures Figure 1: A schematic overview of the pilot study timeline. Table 1: Participant characteristics at screening. repetitions were not counted aloud, with participants instructed to complete repetitions at the fastest rate they could Control (n �10; \ �7) ES (n �10; \ �7) manage until told to stop. Immediately on completion of the Age (years) 74 (5) 70 (4) STS, a rating of perceived exertion (RPE) was assessed using Body mass (kg) 70.9 (11.9) 69.7 (9.9) Borg’s RPE 15-grade scale [23]. BMI (kg/m ) 26.3 (3.5) 25.0 (3.4) Maximum leg pressing velocity, force, and power char- SPPB score 11 (1) 12 (1) STS score at screening 29 (12) 29 (10) acteristics were measured on a seated pneumatic leg press PAL at screening 1.63 (0.19) 1.70 (0.14) dynamometer (A420, Keiser , Fresno, CA). Data collection, processing, and analysis were performed as described pre- Data are presented as mean (standard deviation). ES: exercise-snacking group; BMI: body mass index; SPPB: short physical performance battery; viously [24]. Briefly, during familiarisation sessions, partici- STS: 60-second sit-to-stand test; PAL: physical activity level (ratio of total pants completed tests of one-repetition maximum (1-RM) leg energy expenditure to basal metabolic rate). pressing force against self-selected increments in resistance. No emphasis was placed on contraction velocity for the 1-RM the tibia and femur to locate the end of bones, respectively. test, and participants were instructed to reach 1-RM within 15 Single 2D slice scans were performed at 66% of the tibia repetitions with self-selected interrepetition rest. Participants length proximally from the medial malleolus, and 25% of the then performed a series of approximately 10 discrete repe- femur length proximally to the lateral femoral epicondyle, titions, each performed at maximum concentric contraction based on the bone lengths previously recorded. Scan images velocity against an incrementally increasing pedal resistance, were analysed using the BoneJ plugin (Version 1.4.2) for up to a resistance equalling the previously achieved 1-RM. On ImageJ (1.44p, Wayne Rasband, National Institutes of trial days, a set warm-up was performed based on the 1-RM Health, USA) [21, 22]. Following scanning measures, par- achieved in the second familiarisation, consisting of 5 ×30%- ticipants were provided with a breakfast of their choice, 1RM, 5 ×50%-1RM, 2 ×70%-1RM, and 1 ×80%-1RM, fol- which was matched on the postintervention trial day. lowed by five minutes of seated rest. +e aforementioned incremental test was then performed, with the tenth repetition 3.2. Functional Measures. A maximum number of repeated at a resistance equal to the 1-RM achieved in the second STS in 60 seconds were performed from a chair with a seat familiarisation. To extrapolate theoretical maximum con- height of 44cm, with arms folded across the chest and traction velocity (V ) and force (F ), linear regression of max max reaching full hip and knee extension on standing. During force and velocity at which peak power of each repetition familiarisation, a researcher counted the number of repe- occurred was calculated. Interpolated peak power (P ) was max titions aloud, with a timing clock in view of the participant. determined by numerical differentiation of the second-order On trial days, participants were not in view of a clock and polynomial calculated from the force-power profile, i.e., from 4 Journal of Aging Research peak power and the force at the instant of peak power for each logbook, regardless of whether they were related to the repetition [25]. intervention. 3.6. Statistical Analysis. Shapiro–Wilks tests of normality 3.3. Physical Activity. Free-living physical activity was assessed on seven consecutive days by continuous wear of were performed on participant characteristic data recor- ded at screening (age, body mass, BMI, and STS score) due an armband mounted physical activity monitor (Sense- Wear, BodyMedia, Inc., Pittsburg, PA, USA). +is was to the small sample size. Participant characteristic vari- ables were normally distributed, thus compared with in- undertaken between the familiarisation sessions before the dependent-samples t-test. Outcome variables were intervention period as a baseline measure and during the analysed with a two-way repeated measures ANOVA, and last week of the intervention period. Physical activity level where there was a significant interaction or time effect was (PAL) was calculated as estimated mean daily energy ex- penditure/resting metabolic rate (estimated using the observed, a Holm–Bonferroni post hoc test performed. Statistical significance was accepted at p<0.05. To infer the World Health Organisation equation). Only days with >95% wear time achieved were included in the analysis. magnitude of differences between the groups, Hedges g effect size for difference in change scores between the Participants were instructed to remove the armband for water-based activity, such as bathing or showering, and any groups was calculated, to account for low sample size [26]. Effect sizes were classed as small (0.2), moderate (0.5), and water-based activities were recorded in the logbook. large (0.8) according to Cohen [27]. Data are presented as mean (standard deviation); ANOVA and post hoc analysis 3.4. Diet Records. +ree-day weighed diet records (two were performed using SPSS v22.0 (SPSS Inc., Chicago, IL), weekdays and one weekend) were completed by partici- and effect size analysis was performed using Microsoft pants. Again, this was undertaken between familiarisation Excel 2016. sessions and during the last week of the intervention pe- riod. Commercially available online software (v4.312 4. Results Nutritics Education, Dublin, Ireland) was used for diet record analysis, all of which was performed by the same 4.1. FunctionalMeasures. Adherence to the ES intervention researcher (OJP). Mean daily intake of total kcal, carbo- was 98% (2 (1) sessions out of 56 sessions missed), and no hydrate (CHO), protein (PRO), and fat were obtained and adverse events occurred during the intervention period in calculated relative to body mass using screening body mass either group. Pre- to postintervention STS scores were and postintervention body mass for baseline and in- significantly increased (p<0.01) in the ES group (29 (8) to tervention dietary records, respectively. Between pre- and 38 (13)), compared with the Control group (29 (14) to 29 postintervention trials, participants consumed 150 g of (13)). +ere was a large between-group effect size of yogurt (Natural flavour, Skyr, Arla ; 98 kcal, 0.3g fat, 6 g g �1.40 for the difference in STS change scores (Figure 2). carbohydrate, 16.5g protein) as part of their breakfast meal. +ere was no significant change in RPE for the STS pre- Participants were provided with food weighing scales and a and postintervention in either group (Control: 13 (3) to 14 logbook to record whether the full 150g of yogurt had been (2); ES: 13 (2) to 14 (2)). +ere were no significant time or consumed each day and deliberately not given any further interaction effects for V , F , or P (Table 2). Effect max max max instruction concerning dietary intake. sizes for change scores between the groups were moderate for V and F (g �0.62 and g �0.49, respectively) and max max large for P (g �0.81). max 3.5. Intervention. +e Control group was asked to continue with their habitual physical activities for 28 days. +e exercise snacking group was asked to perform two bouts of 4.2. Anthropometry. One participant from the Control “exercise snacking” per day, once in the morning and once group was removed from DXA analysis due to movement in the evening. Exercise snacking bouts consisted of five artefact on one scan. As shown in Table 3, there were no exercises, each undertaken for one minute with the aim to significant changes in body mass, or DXA measured % complete as many repetitions as possible in that minute. body fat, total lean mass, or lean leg mass in either group, Between each exercise, participants rested for one minute. but a moderate effect size for the difference in leg lean mass +e exercises were STS from a chair, seated knee exten- change scores (g �0.68). sions of alternating legs, standing knee bends of alter- One participant from the ES group was removed from nating legs, marching on the spot, and standing calf raises the calf pQCT scan analysis, and one participant from the (see Supplemental Figures S1–S5, respectively). Partici- Control group was removed from the thigh pQCT scan pants were advised to hold onto a chair for stability during analysis, both due to movement artefact. Calf mCSA did standing exercise if they felt the need to. +e STS exercise not change significantly for either group, with an effect size was performed first, with the number of repetitions for difference in the change scores between the groups completed recorded in a provided logbook as a means to being g �0.10. +ere were no statistically significant assess adherence. Any adverse events during the in- changes in thigh mCSA in either group, although there was tervention period for either group were to be recorded in a a large effect size for the difference in change scores Journal of Aging Research 5 Pre Post Pre Post Time point Control ES Figure 2: Individual changes in sit-to-stand score from pre- to postintervention of either 28 days of yogurt at breakfast only (Control) or yogurt at breakfast and exercise snacking twice daily (ES). Horizontal bars connected with solid lines display group mean. denotes significant difference in change score between the groups (p<0.01). Table 2: Summary data of leg pressing outcome measures. Group Pre Post %Δ p g Control 1.61 (0.29) 1.56 (0.24) − 3 V (m/s) 0.19 0.62 max ES 1.75 (0.34) 1.81 (0.23) 3 Control 950 (290) 929 (170) − 2 F (N) 0.29 0.49 max ES 984 (249) 1032 (289) 5 Control 370 (98) 363 (86) − 2 P (W) 0.09 0.81 max ES 446 (170) 472 (166) 6 ES: exercise snacking group; V : extrapolated maximum leg pressing velocity; F : extrapolated maximum leg pressing force; P : interpolated maximum max max max leg pressing power. Data are presented as mean (SD); %Δ, pre- to postchange within groups, p values for interaction effect from two-way repeated measures ANOVA, and Hedges g effect size of difference in changed scores between the groups. Table 3: Summary of body mass and dual energy X-ray absorptiometry measures. Group Pre Post %Δ p g Control 70.5 (11.2) 70.3 (11.4) 0 Body mass (kg) 0.64 0.27 ES 69.0 (10.0) 69.0 (10.0) 0 Control (n � 9) 35.1 (7.4) 35.2 (6.8) 0 % body fat 0.34 0.48 ES 34.0 (7.0) 33.7 (7.0) − 1 Control (n � 9) 44.8 (8.6) 44.6 (8.4) 0 Lean mass (kg) 0.37 0.44 ES 44.9 (6.5) 45.0 (6.4) 0 Control (n � 9) 15.3 (2.4) 15.3 (2.3) 0 Leg lean mass (kg) 0.17 0.68 ES 15.3 (2.0) 15.5 (2.2) 1 ES: exercise snacking group. Data are presented as mean (SD); %Δ, pre- to postchange within groups; p values for interaction effect from two-way repeated measures ANOVA, and Hedges g effect size of difference in changed scores between the groups. Group size was n � 10 unless stated otherwise. dietary protein and fat intake (g �0.71 and g �0.60, re- between the groups (g �0.96) with an increase of 2% in the ES group (see Figure 3). spectively) (see Table 4). 5. Discussion and Implications 4.3. Physical Activity and Diet. +ere were no changes in PAL in either group from baseline assessment to the last +e impact of undertaking 28 days of twice daily home- week of the intervention, nor were there changes in total based exercise snacking, supplemented with 150g of yogurt energy (kcal/kg/day) or carbohydrate intake (g/kg/day). at breakfast, on lower limb muscle function and an- +ere were significant time effects for an increase in daily thropometry was explored in healthy older adults. Ad- protein intake (p<0.01) and decrease in daily fat intake herence to the exercise regime was very high (98%), and (p<0.05). Because there were no differences between the participants in the ES group showed marked improve- groups, the effect size for the pooled change score (pre- to ments in the number of sit-to-stands performed in 60 postintervention for all participants) were moderate for seconds, with no improvement in the Control group. Sit-to-stands/minute 6 Journal of Aging Research 90 80 80 70 70 60 60 50 50 40 40 30 Pre Post Pre Post Pre Post Pre Post Group Group Control Control ES ES (a) (b) Figure 3: Individual changes in pQCT measured (a) calf muscle at 66% tibia and (b) thigh muscle group at 25% femur, pre- and postintervention of either 28 days of yogurt at breakfast only (Control) or yogurt at breakfast and exercise snacking twice daily (ES). Horizontal bars connected with solid lines display group mean. Table 4: Summary data of dietary intake preintervention and during the intervention. Group Pre During %Δ p g Control 28 (7) 26 (6) − 9 Energy intake (kcal/kg/day) 0.73 0.18 ES 28 (6) 27 (9) − 4 Control 3.02 (0.88) 2.82 (0.84) − 7 CHO intake (g/kg/day) 0.84 0.09 ES 2.95 (1.21) 2.66 (0.85) − 10 Control 1.01 (0.19) 1.17 (0.30) 17 PRO intake (g/kg/day) 0.73 0.16 ES 1.10 (0.21) 1.30 (0.34) 19 Control 1.11 (0.47) 0.83 (0.28) − 25 Fat intake (g/kg/day) 0.67 0.19 ES 1.32 (0.40) 1.11 (0.40) − 15 ES: exercise snacking group; CHO: carbohydrates; PRO: protein. Data are presented as mean (SD); %Δ, pre- to postchange within groups; p values for interaction effect from two-way repeated measures ANOVA, and Hedges g effect size of difference in changed scores between the groups. Large effect sizes were also observed in the change scores the test). Although the improvement in STS is likely largely due to task-specific training, the movement pattern is for interpolated maximum leg pressing power and thigh muscle cross-sectional area, albeit the absolute increases nonetheless relevant for tasks of daily living [30]. Given that the mode of training applied no external load beyond in these variable appear modest. +e exercise snacking regime consisted of five leg ex- body weight and did not require participants to exercise to ercises; each completed twice a day across two bouts, with momentary failure, improvements in leg press V and max the aim to complete as many repetitions of each exercise as F of 3% and 5%, respectively, along with a trend toward max possible in a minute with no external load above body significant increases in P (6% increase; p � 0.09) were max weight. +is mode of exercise deviates from successful perhaps not expected and provide an indication of the home-based exercise programmes explored previously; potential efficacy of this type of “little and often” primarily, in that, all exercise was nonloaded, participants intervention. undertook exercise twice a day, there were no supervised As a point of comparison, in the study by Bean et al. [31], exercise sessions in the home, and the programme lasted older adults trained three times a week for 12 weeks, com- only four weeks [28]. +e ES group showed significantly pleting three sets of 10 repetitions of maximum concentric improved STS score, with the 31% improvement in the STS contraction speed exercises similar to those of the present in 60 seconds in the present pilot study being remarkably pilot study, whilst wearing a weighted vest. +e weighted vest similar to the 30% improvement in 30-second STS score group increased maximum leg press power by 12%, also observed after six weeks of resistance training in older assessed with pneumatic leg press dynamometry. Although adults by Cavani et al. [29]. With 60-second STS being one the present pilot study employed an intervention only one- of the exercises completed twice daily for the ES group, this third of the programme duration as the aforementioned was not unexpected, even though the conditions between study, and without external loading, a 6% increase in P was max exercise bouts and testing sessions were deliberately dif- observed. Whether functional improvements of the exercise ferent (self-timed vs. no information of time remaining in snacking regime over longer training durations would Calf mCSA (cm ) Thigh mCSA (cm ) Journal of Aging Research 7 range of 1.2 to 1.6g/kg/day as a more appropriate daily continue to increase with the only element of progression being completion of more repetitions in a minute cannot be protein intake was achieved in the present pilot study with the addition of 16.5g of dairy protein at breakfast. However, known. It should be noted that although the participants in the present pilot study were previously undertaking no further inspection of the absolute change in dietary protein regular structured exercise, they were healthy and not consumption highlighted that total protein intake increased functionally impaired, so were perhaps more physiologically by ≈10g/day. +ere was not an increase in daily protein receptive to the training stimulus provided than a frail or intake equal to the amount contained in the yogurt possibly clinical population might be [32]. Nonetheless, increases in because protein that would have been included in the F and P of 5% and 6%, respectively, represent changes breakfast meal may have been replaced with the yogurt. +is max max with real-world relevance given the estimated annual loss of is potentially important on a per meal basis, as larger protein muscle strength of 1–5% described by Seene and Kaasik [33], doses are required to maximally stimulate muscle protein synthesis in older adults. Moreover, this potentially serves to particularly as the strength and power gains were achieved in four weeks with a zero-cost exercise intervention. However, highlight the challenges with supplementing older adult diets with additional protein. In any case, whether an extra whether these task-specific increases in strength and power lead to clinically relevant improvements in outcomes, such as 10g/d protein intake would lead to clinically relevant out- delaying dynapenia/sarcopenia or frailty, would require comes in an older population is questionable. +e lack of further investigation and long-term follow-up. increase in strength or hypertrophy in the Control group +ere were some small but noteworthy changes in an- support the work of Kim et al. [37], finding that even thropometric measures of the legs following the ES in- adjusting protein distribution for 8 weeks without the ad- tervention. In particular, leg lean mass measured by DXA dition of exercise does not increase muscle mass or strength in older adults. Importantly, this was despite achieving over increased by 1% (g �0.68) and thigh mCSA increased by 2% with a large effect size (g �0.98). In comparison to an effect 1.2g/kg/day of protein, highlighting the importance of a combination of exercise and nutrition to address muscle loss size of 0.39 (0.17) (95% CI: 0.05, 0.73) for hypertrophy induced by low-load resistance exercise training calculated with ageing However, the duration of the intervention in the present pilot study was very short, and the use of only three- in a recent meta-analysis by Schoenfeld et al. [11], the po- tential increase in muscle size observed in present pilot is day diet records are often criticised for a bias toward under notable. No mechanisms for an increase in muscle size were reporting [38]. Consequently, these data should not be seen examined in this work, but it could be in part due to the to undermine the potential health and body composition comparatively high frequency of training, although this of benefits of a longer-term increase in dietary protein intake course can only be speculated due to the scarcity of studies for older adults not meeting recommended quantities of using twice daily exercise programmes [8, 13]. It is also dietary protein intake [39]. +ere are a number of crucial considerations when possible that any hypertrophy observed in the present pilot study was in part due to the additional protein ingested at contextualising the present findings. Most obviously, the pilot study design employed cannot support the efficacy of breakfast via the yogurt supplement. +is notion would be supported by the evidence of Mamerow et al. [34], albeit in a exercise snacking without dietary protein supplementation. +e addition of two further groups (a true nonexercising younger population, that 24-hour muscle protein synthesis rate was greater with an even distribution of protein control group and an exercise snacking without yogurt throughout the day compared with a more traditional, group) would shed light on the importance of the additional evening heavy, protein distribution. Although it is en- protein at breakfast, but it would require a large increase in couraging that two independent measurement techniques sample size. Moreover, based on the effect size of the present concomitantly suggest that a short-term exercise snacking pilot study data, power calculations (G∗power, Version intervention may have potential to increase leg muscle size, 3.1.9.4) indicated that for statistically significant differences in P the absolute changes were small, and exercise-induced oe- (α � 0.05 and power �0.8), 27 participants per group max dema from the previous day’s exercise cannot be ruled out as would have been required using the current research design. a potential confounder in this instance [35]. However, this Equally, group sizes of 19 would have been required for seems unlikely given the nature of the exercise snacking statistically significant differences in thigh mCSA. By in- bouts, the fact that participants would have been accustomed creasing sample size, a traditional randomisation strategy to to the exercise after 28 days, and that the increase in mCSA allocate participants to study groups could have been ap- was not observed in the calf muscle group that was also propriate, whereas due to a small sample size, minimisation measured by pQCT [36]. was implemented as means to reduce chance difference in Both groups modestly increased daily protein intake per baseline characteristics of groups in this present pilot study kilogram of body mass by 17% and 19% during the in- [20]. Although the adherence to the exercise programme was tervention (Control and ES, respectively), going from 1.05 very high, it cannot be assumed that this would persist (0.20)g/kg/day to 1.24 (0.32)g/kg/day (pooled mean). Al- longer than four weeks or in other older populations [40]. though the older adults in the present pilot study were Investigation of physiological mechanisms to support the previously consuming over-the-recommended daily allow- strength and hypertrophic gains observed in the present ance (RDA) of protein, Phillips et al. [17] present convincing findings may also allow for further optimisation of the rationale that the RDA may not represent an optimal daily exercise regime itself, creating a potentially more efficacious protein intake for older adults in particular. +e suggested training stimulus. In the same vein, a longer-term follow-up 8 Journal of Aging Research would also be required to establish whether the physiological unilaterally alternating the moving leg, aiming to fully ex- adaptions might continue to occur if the exercise stimulus tend the knee at the end of the movement. Supplementary were to be maintained. It should of course not be overlooked Figure S3: standing knee bends, with repetitions performed that high-load resistance training has superior effects on unilaterally alternating the moving leg, aiming the shank to increasing muscle mass and strength [11, 41], potentially reach parallel with the floor whilst the thigh stays vertical. through more pronounced neural adaptations [42], and Supplementary Figure S4: marching on the spot, with hands more easily accommodates progressive overload to facilitate held at waist height (or one holding a chair for balance if continuous improvements in muscle mass and strength. required) and aiming to bring thighs up to parallel with the However, accepting that access and cost of exercise par- floor. Supplementary Figure S5: standing calf raises, per- ticipation and lack of knowledge of exercise modalities are formed bilaterally holding onto a chair for balance, aiming to often key barriers to exercise in older adults [43], very simple rise as high onto tiptoes as possible and returning heels to the home-based exercise snacking-style regimes are a promising floor between repetitions. (Supplementary Materials) strategy to engage older adults in exercise. References 6. Conclusions [1] J. A. Faulkner, L. M. Larkin, D. R. Claflin, and S. V. Brooks, In conclusion, although underpowered to show statistically “Age-related changes in the structure and function of skeletal significant changes, the present study highlights the po- muscles,” Clinical and Experimental Pharmacology and tential efficacy of a 28-day, home-based “little and often” Physiology, vol. 34, no. 11, pp. 1091–1096, 2007. [2] T. J. 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Exercise Snacking to Improve Muscle Function in Healthy Older Adults: A Pilot Study

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Copyright © 2019 Oliver J. Perkin et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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10.1155/2019/7516939
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Hindawi Journal of Aging Research Volume 2019, Article ID 7516939, 9 pages https://doi.org/10.1155/2019/7516939 Clinical Study Exercise Snacking to Improve Muscle Function in Healthy Older Adults: A Pilot Study 1,2 1 1,2 Oliver J. Perkin , Polly M. McGuigan, and Keith A. Stokes Department for Health, University of Bath, Bath BA2 7AY, UK Centre for Sport, Exercise and Osteoarthritis Research Versus Arthritis, Chesterfield, UK Correspondence should be addressed to Oliver J. Perkin; o.j.perkin@bath.ac.uk Received 20 June 2019; Revised 30 August 2019; Accepted 10 September 2019; Published 3 October 2019 Guest Editor: Marco C. Uchida Copyright©2019OliverJ.Perkinetal.+isisanopenaccessarticledistributedundertheCreativeCommonsAttributionLicense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Loss of muscle mass and strength are seemingly accepted as part of the ageing process, despite ultimately leading to the loss of independence. Resistance exercise is considered to be primary defence against loss of muscle function in older age, but it typically requires access to exercise equipment often in a gym environment. +is pilot study aimed at examining the effect of a 28-day, unsupervised home-based exercise intervention on indices of leg strength and muscle size in healthy older adults. Twenty participants were randomly assigned to either maintain their habitual physical activity levels (Control; n � 10; age, 74 (5) years; 2 2 body mass, 26.3 (3.5)kg/m ) or undertake “exercise snacks” twice daily (ES; n � 10; age, 70 (4) years; body mass, 25.0 (3.4)kg/m ). Both groups consumed 150g of yogurt at their breakfast meal for the duration of the intervention. Sixty-second sit-to-stand score improved by 31% in ES, with no change in Control (p<0.01). Large effect sizes were observed for the difference in change scores between the groups for interpolated maximum leg pressing power (6% increase in ES) and thigh muscle cross-sectional area (2% increase in ES). +e present pilot data suggest that exercise snacking might be a promising strategy to improve leg muscle function and size in older adults and that further investigation into zero-cost exercise strategies that allow high frequency of training is warranted. Progressive resistance exercise training improves muscle 1. Introduction strength in older adults, and it is accompanied by multi- Frailty is underpinned by a progressive loss of muscle faceted improvements in health and function [6, 7]. Tra- mass and strength, particularly from the lower limbs, and ditionally, heavy load resistance training has been regarded is associated with increased risk of falls and reduced as the most effective strategy to increase muscle strength, due quality of life [1, 2]. +ere is a minimum threshold of to associated neural and hypertrophic adaptations [8, 9]. strength required to complete tasks of daily living in- Recent evidence suggests that low-load resistance training dependently, and finding means to delay individuals can also be efficacious in increasing muscle strength, par- reaching this “frailty threshold” has been identified as an ticularly in an untrained population, albeit to a lesser degree urgent health care priority [3]. With muscle mass lost at in comparison to high-load resistance training [10, 11]. 0.5–1% per year after 50 years of age [4] and strength lost Training with low loads and low overall session volume may even more rapidly [5], modest improvements of a few allow for increased training frequency, as recovery times percent in muscle size and strength from a training may be shorter between sessions [12]. Dankel et al. [13] programme may, in essence, represent postponement of suggests that manipulation of training frequency to maintain frailty measurable in years. Crucially, intervention is overall training volume with more sessions of lower load needed before older adults’ functional capacity declines across a week may even increase hypertrophic training re- past the point that exercise is no longer a safe means to sponses. Although this has not yet been borne out empir- maintain muscle strength. ically [8], it is intuitively appealing to reason that a reduced 2 Journal of Aging Research training session load with short recovery times may suit an sessions and during the last week of the intervention, older population previously doing no formal exercise be- physical activity and diet were assessed. See Figure 1 for a schematic overview of the pilot study timeline. cause it may overcome some of the barriers to starting an exercise programme [14]. Short bouts of exercise spread across the day, termed 2.1. Participants. Twenty healthy, community-dwelling, “exercise snacks,” have received attention as a time-efficient older men and women (65–80 years), not undertaking regular exercise strategy. Francois et al. [15] identified that exercise structured exercise, were recruited for the pilot study through snacking before each meal, consisting of six discrete local newspaper advertisement and social media. Individuals minutes of exercise separated by one minute of rest, im- who were nonsmokers, had BMI of ≥20<30kg/m , had no proved glycaemic control the following day in middle-aged contraindications to exercise or recent history of musculo- adults with impaired glucose handling. Jenkins et al. [16] skeletal injury, and had scored 8 or above with no score of reported improvements in cardiorespiratory fitness in zero on any test of the SPPB [18] at the initial screening were healthy inactive adults performing three sets of maximum invited to take part in the pilot study. Participants were effort 60-step stair climbs a day, three times a week, for six assigned to groups by way of minimisation to limit differences weeks. +e improvement in exercise tolerance included an in mean age, BMI, and 60-second sit-to-stand (STS) score at increase in maximum power output during a VO peak test the screening visit, on account of the small sample size on a cycle ergometer [16]. +is suggests that an exercise [19, 20]. An individual outside of the study team performed snacking model may have the potential to improve function participant group allocation. Participant characteristics beyond just cardiovascular fitness. As such, exercise recorded during screening are presented in Table 1. All snacking was examined in the present pilot study with the participants provided written informed consent. +e protocol aim of providing a stimulus to improve leg strength in older was approved by the National Health Service (NHS) South adults that could be undertaken in the home on a daily basis West—Frenchay Research Ethics Committee (Ref: 16/SW/ without the need for supervision. 0300) and registered on ClinicalTrials.gov (Identifier: +e primary aim of the present pilot study was to in- NCT02991989). vestigate the effects of four weeks of twice daily “exercise snacking” on maximum number of sit-to-stands from a chair performed in one minute, compared with a control 3. Measures group maintaining their habitual physical activity patterns. +e secondary aims were to assess adherence to the exercise 3.1. Imaging. Participants arrived at the laboratory for trial snacking intervention, along with the effects on force, ve- days following a 10-hour overnight fast, having drunk 1 pint locity, and power, during leg press dynamometry and on of water, and having not undertaken exhaustive exercise in whole-body and lower limb anthropometry. +e proposed the previous 24 hours. Participants were asked to void before intervention was specifically designed to be suitable to weight was measured with electronic scales (BC543, Tanita, perform in the home environment, without the need for Amsterdam, Netherlands). Whole-body composition, supervision or specific exercise equipment. +e overall whole-body lean mass, and leg lean mass were estimated objective of this pilot study was to inform future work on using a DXA system (QDR software version 12.4.2, Hologic exercise strategies extending to populations with lifestyle- Discovery W, Bedford, MA) by differentiating the fat, bone, compromising age-related loss of muscle strength or mass. and lean (nonbone nonfat) masses. A spine phantom was used for the quality control scan performed at the start of every trial day before participant testing, as per the man- 2. Materials and Methods ufacturer’s guidelines. Participants wore the same light A two-group experimental research design was used in this clothes for pre- and postintervention trials and removed all pilot study to examine the effects of twice daily “exercise metal items. +e investigator positioned the participant to be snacking” on muscle function and size in healthy, com- laying supine on the scanning bed such that body regions munity-dwelling older adults. For 28 days, one group un- could be partitioned upon analysis. Manual placement of dertook a home-based exercise snacking intervention (ES) boundaries between discrete anatomical regions was con- and the other group acted as a nonexercising control by ducted for all scans by the same investigator (OJP), before maintaining habitual physical activity levels. As a control analysis using manufacturer’s software. Lower limb (calf and thigh) muscle cross-sectional area variable, both groups were provided with 150g of yogurt to consume as part of their breakfast meal for the 28 days, to (mCSA) was assessed by peripheral quantitative computed tomography (pQCT; XCT3000, StraTec Medizintechnik both act as a “positive control” to reduce participant dropout from the Control group and to achieve optimal dietary GmbH, Pforzheim, Germany). During the preintervention protein intake [17]. All participants completed two famil- trial, tibia (medial knee joint line to medial malleolus) and iarisation sessions to functional measures used in the pre- femur length (greater trochanter to lateral knee joint line) of and postintervention assessment, separated by at least seven the dominant leg were measured using a fabric tape measure days, with the second session completed at least five days whilst participants were standing. Scans were performed before the preintervention assessments. Function testing and with the participant laying supine on a bed with leg placed imaging measures were completed on the day before and the through the scanning gantry and foot strapped into a day after the 28-day intervention. Between familiarisation footplate. Scout scans were performed at the distal ends of Journal of Aging Research 3 Eligibility assessment and familiarisation session 1 with muscle function measures 7 days of physical activity monitoring and 3-day food diary Familiarisation session 2 with muscle function measures >5 days Preintervention assessments of muscle function and imaging measures Exercise snacking group Control group (I) 28 days of twice daily exercise (I) 28 days maintaining habitual snacking; one in the morning physical activity levels and one in the evening around meal time (II) 28 days of 150 g yoghurt (II) 28 days of 150 g yoghurt consumed with the breakfast consumed with the breakfast meal daily meal daily (III) 7 days of physical activity (III) 7 days of physical activity monitoring and 3-day food monitoring and 3-day food diary during last week diary during last week Postintervention assessments of muscle function and scanning measures Figure 1: A schematic overview of the pilot study timeline. Table 1: Participant characteristics at screening. repetitions were not counted aloud, with participants instructed to complete repetitions at the fastest rate they could Control (n �10; \ �7) ES (n �10; \ �7) manage until told to stop. Immediately on completion of the Age (years) 74 (5) 70 (4) STS, a rating of perceived exertion (RPE) was assessed using Body mass (kg) 70.9 (11.9) 69.7 (9.9) Borg’s RPE 15-grade scale [23]. BMI (kg/m ) 26.3 (3.5) 25.0 (3.4) Maximum leg pressing velocity, force, and power char- SPPB score 11 (1) 12 (1) STS score at screening 29 (12) 29 (10) acteristics were measured on a seated pneumatic leg press PAL at screening 1.63 (0.19) 1.70 (0.14) dynamometer (A420, Keiser , Fresno, CA). Data collection, processing, and analysis were performed as described pre- Data are presented as mean (standard deviation). ES: exercise-snacking group; BMI: body mass index; SPPB: short physical performance battery; viously [24]. Briefly, during familiarisation sessions, partici- STS: 60-second sit-to-stand test; PAL: physical activity level (ratio of total pants completed tests of one-repetition maximum (1-RM) leg energy expenditure to basal metabolic rate). pressing force against self-selected increments in resistance. No emphasis was placed on contraction velocity for the 1-RM the tibia and femur to locate the end of bones, respectively. test, and participants were instructed to reach 1-RM within 15 Single 2D slice scans were performed at 66% of the tibia repetitions with self-selected interrepetition rest. Participants length proximally from the medial malleolus, and 25% of the then performed a series of approximately 10 discrete repe- femur length proximally to the lateral femoral epicondyle, titions, each performed at maximum concentric contraction based on the bone lengths previously recorded. Scan images velocity against an incrementally increasing pedal resistance, were analysed using the BoneJ plugin (Version 1.4.2) for up to a resistance equalling the previously achieved 1-RM. On ImageJ (1.44p, Wayne Rasband, National Institutes of trial days, a set warm-up was performed based on the 1-RM Health, USA) [21, 22]. Following scanning measures, par- achieved in the second familiarisation, consisting of 5 ×30%- ticipants were provided with a breakfast of their choice, 1RM, 5 ×50%-1RM, 2 ×70%-1RM, and 1 ×80%-1RM, fol- which was matched on the postintervention trial day. lowed by five minutes of seated rest. +e aforementioned incremental test was then performed, with the tenth repetition 3.2. Functional Measures. A maximum number of repeated at a resistance equal to the 1-RM achieved in the second STS in 60 seconds were performed from a chair with a seat familiarisation. To extrapolate theoretical maximum con- height of 44cm, with arms folded across the chest and traction velocity (V ) and force (F ), linear regression of max max reaching full hip and knee extension on standing. During force and velocity at which peak power of each repetition familiarisation, a researcher counted the number of repe- occurred was calculated. Interpolated peak power (P ) was max titions aloud, with a timing clock in view of the participant. determined by numerical differentiation of the second-order On trial days, participants were not in view of a clock and polynomial calculated from the force-power profile, i.e., from 4 Journal of Aging Research peak power and the force at the instant of peak power for each logbook, regardless of whether they were related to the repetition [25]. intervention. 3.6. Statistical Analysis. Shapiro–Wilks tests of normality 3.3. Physical Activity. Free-living physical activity was assessed on seven consecutive days by continuous wear of were performed on participant characteristic data recor- ded at screening (age, body mass, BMI, and STS score) due an armband mounted physical activity monitor (Sense- Wear, BodyMedia, Inc., Pittsburg, PA, USA). +is was to the small sample size. Participant characteristic vari- ables were normally distributed, thus compared with in- undertaken between the familiarisation sessions before the dependent-samples t-test. Outcome variables were intervention period as a baseline measure and during the analysed with a two-way repeated measures ANOVA, and last week of the intervention period. Physical activity level where there was a significant interaction or time effect was (PAL) was calculated as estimated mean daily energy ex- penditure/resting metabolic rate (estimated using the observed, a Holm–Bonferroni post hoc test performed. Statistical significance was accepted at p<0.05. To infer the World Health Organisation equation). Only days with >95% wear time achieved were included in the analysis. magnitude of differences between the groups, Hedges g effect size for difference in change scores between the Participants were instructed to remove the armband for water-based activity, such as bathing or showering, and any groups was calculated, to account for low sample size [26]. Effect sizes were classed as small (0.2), moderate (0.5), and water-based activities were recorded in the logbook. large (0.8) according to Cohen [27]. Data are presented as mean (standard deviation); ANOVA and post hoc analysis 3.4. Diet Records. +ree-day weighed diet records (two were performed using SPSS v22.0 (SPSS Inc., Chicago, IL), weekdays and one weekend) were completed by partici- and effect size analysis was performed using Microsoft pants. Again, this was undertaken between familiarisation Excel 2016. sessions and during the last week of the intervention pe- riod. Commercially available online software (v4.312 4. Results Nutritics Education, Dublin, Ireland) was used for diet record analysis, all of which was performed by the same 4.1. FunctionalMeasures. Adherence to the ES intervention researcher (OJP). Mean daily intake of total kcal, carbo- was 98% (2 (1) sessions out of 56 sessions missed), and no hydrate (CHO), protein (PRO), and fat were obtained and adverse events occurred during the intervention period in calculated relative to body mass using screening body mass either group. Pre- to postintervention STS scores were and postintervention body mass for baseline and in- significantly increased (p<0.01) in the ES group (29 (8) to tervention dietary records, respectively. Between pre- and 38 (13)), compared with the Control group (29 (14) to 29 postintervention trials, participants consumed 150 g of (13)). +ere was a large between-group effect size of yogurt (Natural flavour, Skyr, Arla ; 98 kcal, 0.3g fat, 6 g g �1.40 for the difference in STS change scores (Figure 2). carbohydrate, 16.5g protein) as part of their breakfast meal. +ere was no significant change in RPE for the STS pre- Participants were provided with food weighing scales and a and postintervention in either group (Control: 13 (3) to 14 logbook to record whether the full 150g of yogurt had been (2); ES: 13 (2) to 14 (2)). +ere were no significant time or consumed each day and deliberately not given any further interaction effects for V , F , or P (Table 2). Effect max max max instruction concerning dietary intake. sizes for change scores between the groups were moderate for V and F (g �0.62 and g �0.49, respectively) and max max large for P (g �0.81). max 3.5. Intervention. +e Control group was asked to continue with their habitual physical activities for 28 days. +e exercise snacking group was asked to perform two bouts of 4.2. Anthropometry. One participant from the Control “exercise snacking” per day, once in the morning and once group was removed from DXA analysis due to movement in the evening. Exercise snacking bouts consisted of five artefact on one scan. As shown in Table 3, there were no exercises, each undertaken for one minute with the aim to significant changes in body mass, or DXA measured % complete as many repetitions as possible in that minute. body fat, total lean mass, or lean leg mass in either group, Between each exercise, participants rested for one minute. but a moderate effect size for the difference in leg lean mass +e exercises were STS from a chair, seated knee exten- change scores (g �0.68). sions of alternating legs, standing knee bends of alter- One participant from the ES group was removed from nating legs, marching on the spot, and standing calf raises the calf pQCT scan analysis, and one participant from the (see Supplemental Figures S1–S5, respectively). Partici- Control group was removed from the thigh pQCT scan pants were advised to hold onto a chair for stability during analysis, both due to movement artefact. Calf mCSA did standing exercise if they felt the need to. +e STS exercise not change significantly for either group, with an effect size was performed first, with the number of repetitions for difference in the change scores between the groups completed recorded in a provided logbook as a means to being g �0.10. +ere were no statistically significant assess adherence. Any adverse events during the in- changes in thigh mCSA in either group, although there was tervention period for either group were to be recorded in a a large effect size for the difference in change scores Journal of Aging Research 5 Pre Post Pre Post Time point Control ES Figure 2: Individual changes in sit-to-stand score from pre- to postintervention of either 28 days of yogurt at breakfast only (Control) or yogurt at breakfast and exercise snacking twice daily (ES). Horizontal bars connected with solid lines display group mean. denotes significant difference in change score between the groups (p<0.01). Table 2: Summary data of leg pressing outcome measures. Group Pre Post %Δ p g Control 1.61 (0.29) 1.56 (0.24) − 3 V (m/s) 0.19 0.62 max ES 1.75 (0.34) 1.81 (0.23) 3 Control 950 (290) 929 (170) − 2 F (N) 0.29 0.49 max ES 984 (249) 1032 (289) 5 Control 370 (98) 363 (86) − 2 P (W) 0.09 0.81 max ES 446 (170) 472 (166) 6 ES: exercise snacking group; V : extrapolated maximum leg pressing velocity; F : extrapolated maximum leg pressing force; P : interpolated maximum max max max leg pressing power. Data are presented as mean (SD); %Δ, pre- to postchange within groups, p values for interaction effect from two-way repeated measures ANOVA, and Hedges g effect size of difference in changed scores between the groups. Table 3: Summary of body mass and dual energy X-ray absorptiometry measures. Group Pre Post %Δ p g Control 70.5 (11.2) 70.3 (11.4) 0 Body mass (kg) 0.64 0.27 ES 69.0 (10.0) 69.0 (10.0) 0 Control (n � 9) 35.1 (7.4) 35.2 (6.8) 0 % body fat 0.34 0.48 ES 34.0 (7.0) 33.7 (7.0) − 1 Control (n � 9) 44.8 (8.6) 44.6 (8.4) 0 Lean mass (kg) 0.37 0.44 ES 44.9 (6.5) 45.0 (6.4) 0 Control (n � 9) 15.3 (2.4) 15.3 (2.3) 0 Leg lean mass (kg) 0.17 0.68 ES 15.3 (2.0) 15.5 (2.2) 1 ES: exercise snacking group. Data are presented as mean (SD); %Δ, pre- to postchange within groups; p values for interaction effect from two-way repeated measures ANOVA, and Hedges g effect size of difference in changed scores between the groups. Group size was n � 10 unless stated otherwise. dietary protein and fat intake (g �0.71 and g �0.60, re- between the groups (g �0.96) with an increase of 2% in the ES group (see Figure 3). spectively) (see Table 4). 5. Discussion and Implications 4.3. Physical Activity and Diet. +ere were no changes in PAL in either group from baseline assessment to the last +e impact of undertaking 28 days of twice daily home- week of the intervention, nor were there changes in total based exercise snacking, supplemented with 150g of yogurt energy (kcal/kg/day) or carbohydrate intake (g/kg/day). at breakfast, on lower limb muscle function and an- +ere were significant time effects for an increase in daily thropometry was explored in healthy older adults. Ad- protein intake (p<0.01) and decrease in daily fat intake herence to the exercise regime was very high (98%), and (p<0.05). Because there were no differences between the participants in the ES group showed marked improve- groups, the effect size for the pooled change score (pre- to ments in the number of sit-to-stands performed in 60 postintervention for all participants) were moderate for seconds, with no improvement in the Control group. Sit-to-stands/minute 6 Journal of Aging Research 90 80 80 70 70 60 60 50 50 40 40 30 Pre Post Pre Post Pre Post Pre Post Group Group Control Control ES ES (a) (b) Figure 3: Individual changes in pQCT measured (a) calf muscle at 66% tibia and (b) thigh muscle group at 25% femur, pre- and postintervention of either 28 days of yogurt at breakfast only (Control) or yogurt at breakfast and exercise snacking twice daily (ES). Horizontal bars connected with solid lines display group mean. Table 4: Summary data of dietary intake preintervention and during the intervention. Group Pre During %Δ p g Control 28 (7) 26 (6) − 9 Energy intake (kcal/kg/day) 0.73 0.18 ES 28 (6) 27 (9) − 4 Control 3.02 (0.88) 2.82 (0.84) − 7 CHO intake (g/kg/day) 0.84 0.09 ES 2.95 (1.21) 2.66 (0.85) − 10 Control 1.01 (0.19) 1.17 (0.30) 17 PRO intake (g/kg/day) 0.73 0.16 ES 1.10 (0.21) 1.30 (0.34) 19 Control 1.11 (0.47) 0.83 (0.28) − 25 Fat intake (g/kg/day) 0.67 0.19 ES 1.32 (0.40) 1.11 (0.40) − 15 ES: exercise snacking group; CHO: carbohydrates; PRO: protein. Data are presented as mean (SD); %Δ, pre- to postchange within groups; p values for interaction effect from two-way repeated measures ANOVA, and Hedges g effect size of difference in changed scores between the groups. Large effect sizes were also observed in the change scores the test). Although the improvement in STS is likely largely due to task-specific training, the movement pattern is for interpolated maximum leg pressing power and thigh muscle cross-sectional area, albeit the absolute increases nonetheless relevant for tasks of daily living [30]. Given that the mode of training applied no external load beyond in these variable appear modest. +e exercise snacking regime consisted of five leg ex- body weight and did not require participants to exercise to ercises; each completed twice a day across two bouts, with momentary failure, improvements in leg press V and max the aim to complete as many repetitions of each exercise as F of 3% and 5%, respectively, along with a trend toward max possible in a minute with no external load above body significant increases in P (6% increase; p � 0.09) were max weight. +is mode of exercise deviates from successful perhaps not expected and provide an indication of the home-based exercise programmes explored previously; potential efficacy of this type of “little and often” primarily, in that, all exercise was nonloaded, participants intervention. undertook exercise twice a day, there were no supervised As a point of comparison, in the study by Bean et al. [31], exercise sessions in the home, and the programme lasted older adults trained three times a week for 12 weeks, com- only four weeks [28]. +e ES group showed significantly pleting three sets of 10 repetitions of maximum concentric improved STS score, with the 31% improvement in the STS contraction speed exercises similar to those of the present in 60 seconds in the present pilot study being remarkably pilot study, whilst wearing a weighted vest. +e weighted vest similar to the 30% improvement in 30-second STS score group increased maximum leg press power by 12%, also observed after six weeks of resistance training in older assessed with pneumatic leg press dynamometry. Although adults by Cavani et al. [29]. With 60-second STS being one the present pilot study employed an intervention only one- of the exercises completed twice daily for the ES group, this third of the programme duration as the aforementioned was not unexpected, even though the conditions between study, and without external loading, a 6% increase in P was max exercise bouts and testing sessions were deliberately dif- observed. Whether functional improvements of the exercise ferent (self-timed vs. no information of time remaining in snacking regime over longer training durations would Calf mCSA (cm ) Thigh mCSA (cm ) Journal of Aging Research 7 range of 1.2 to 1.6g/kg/day as a more appropriate daily continue to increase with the only element of progression being completion of more repetitions in a minute cannot be protein intake was achieved in the present pilot study with the addition of 16.5g of dairy protein at breakfast. However, known. It should be noted that although the participants in the present pilot study were previously undertaking no further inspection of the absolute change in dietary protein regular structured exercise, they were healthy and not consumption highlighted that total protein intake increased functionally impaired, so were perhaps more physiologically by ≈10g/day. +ere was not an increase in daily protein receptive to the training stimulus provided than a frail or intake equal to the amount contained in the yogurt possibly clinical population might be [32]. Nonetheless, increases in because protein that would have been included in the F and P of 5% and 6%, respectively, represent changes breakfast meal may have been replaced with the yogurt. +is max max with real-world relevance given the estimated annual loss of is potentially important on a per meal basis, as larger protein muscle strength of 1–5% described by Seene and Kaasik [33], doses are required to maximally stimulate muscle protein synthesis in older adults. Moreover, this potentially serves to particularly as the strength and power gains were achieved in four weeks with a zero-cost exercise intervention. However, highlight the challenges with supplementing older adult diets with additional protein. In any case, whether an extra whether these task-specific increases in strength and power lead to clinically relevant improvements in outcomes, such as 10g/d protein intake would lead to clinically relevant out- delaying dynapenia/sarcopenia or frailty, would require comes in an older population is questionable. +e lack of further investigation and long-term follow-up. increase in strength or hypertrophy in the Control group +ere were some small but noteworthy changes in an- support the work of Kim et al. [37], finding that even thropometric measures of the legs following the ES in- adjusting protein distribution for 8 weeks without the ad- tervention. In particular, leg lean mass measured by DXA dition of exercise does not increase muscle mass or strength in older adults. Importantly, this was despite achieving over increased by 1% (g �0.68) and thigh mCSA increased by 2% with a large effect size (g �0.98). In comparison to an effect 1.2g/kg/day of protein, highlighting the importance of a combination of exercise and nutrition to address muscle loss size of 0.39 (0.17) (95% CI: 0.05, 0.73) for hypertrophy induced by low-load resistance exercise training calculated with ageing However, the duration of the intervention in the present pilot study was very short, and the use of only three- in a recent meta-analysis by Schoenfeld et al. [11], the po- tential increase in muscle size observed in present pilot is day diet records are often criticised for a bias toward under notable. No mechanisms for an increase in muscle size were reporting [38]. Consequently, these data should not be seen examined in this work, but it could be in part due to the to undermine the potential health and body composition comparatively high frequency of training, although this of benefits of a longer-term increase in dietary protein intake course can only be speculated due to the scarcity of studies for older adults not meeting recommended quantities of using twice daily exercise programmes [8, 13]. It is also dietary protein intake [39]. +ere are a number of crucial considerations when possible that any hypertrophy observed in the present pilot study was in part due to the additional protein ingested at contextualising the present findings. Most obviously, the pilot study design employed cannot support the efficacy of breakfast via the yogurt supplement. +is notion would be supported by the evidence of Mamerow et al. [34], albeit in a exercise snacking without dietary protein supplementation. +e addition of two further groups (a true nonexercising younger population, that 24-hour muscle protein synthesis rate was greater with an even distribution of protein control group and an exercise snacking without yogurt throughout the day compared with a more traditional, group) would shed light on the importance of the additional evening heavy, protein distribution. Although it is en- protein at breakfast, but it would require a large increase in couraging that two independent measurement techniques sample size. Moreover, based on the effect size of the present concomitantly suggest that a short-term exercise snacking pilot study data, power calculations (G∗power, Version intervention may have potential to increase leg muscle size, 3.1.9.4) indicated that for statistically significant differences in P the absolute changes were small, and exercise-induced oe- (α � 0.05 and power �0.8), 27 participants per group max dema from the previous day’s exercise cannot be ruled out as would have been required using the current research design. a potential confounder in this instance [35]. However, this Equally, group sizes of 19 would have been required for seems unlikely given the nature of the exercise snacking statistically significant differences in thigh mCSA. By in- bouts, the fact that participants would have been accustomed creasing sample size, a traditional randomisation strategy to to the exercise after 28 days, and that the increase in mCSA allocate participants to study groups could have been ap- was not observed in the calf muscle group that was also propriate, whereas due to a small sample size, minimisation measured by pQCT [36]. was implemented as means to reduce chance difference in Both groups modestly increased daily protein intake per baseline characteristics of groups in this present pilot study kilogram of body mass by 17% and 19% during the in- [20]. Although the adherence to the exercise programme was tervention (Control and ES, respectively), going from 1.05 very high, it cannot be assumed that this would persist (0.20)g/kg/day to 1.24 (0.32)g/kg/day (pooled mean). Al- longer than four weeks or in other older populations [40]. though the older adults in the present pilot study were Investigation of physiological mechanisms to support the previously consuming over-the-recommended daily allow- strength and hypertrophic gains observed in the present ance (RDA) of protein, Phillips et al. [17] present convincing findings may also allow for further optimisation of the rationale that the RDA may not represent an optimal daily exercise regime itself, creating a potentially more efficacious protein intake for older adults in particular. +e suggested training stimulus. In the same vein, a longer-term follow-up 8 Journal of Aging Research would also be required to establish whether the physiological unilaterally alternating the moving leg, aiming to fully ex- adaptions might continue to occur if the exercise stimulus tend the knee at the end of the movement. Supplementary were to be maintained. It should of course not be overlooked Figure S3: standing knee bends, with repetitions performed that high-load resistance training has superior effects on unilaterally alternating the moving leg, aiming the shank to increasing muscle mass and strength [11, 41], potentially reach parallel with the floor whilst the thigh stays vertical. through more pronounced neural adaptations [42], and Supplementary Figure S4: marching on the spot, with hands more easily accommodates progressive overload to facilitate held at waist height (or one holding a chair for balance if continuous improvements in muscle mass and strength. required) and aiming to bring thighs up to parallel with the However, accepting that access and cost of exercise par- floor. Supplementary Figure S5: standing calf raises, per- ticipation and lack of knowledge of exercise modalities are formed bilaterally holding onto a chair for balance, aiming to often key barriers to exercise in older adults [43], very simple rise as high onto tiptoes as possible and returning heels to the home-based exercise snacking-style regimes are a promising floor between repetitions. (Supplementary Materials) strategy to engage older adults in exercise. References 6. Conclusions [1] J. A. Faulkner, L. M. Larkin, D. R. Claflin, and S. V. Brooks, In conclusion, although underpowered to show statistically “Age-related changes in the structure and function of skeletal significant changes, the present study highlights the po- muscles,” Clinical and Experimental Pharmacology and tential efficacy of a 28-day, home-based “little and often” Physiology, vol. 34, no. 11, pp. 1091–1096, 2007. [2] T. J. 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Journal of Aging ResearchHindawi Publishing Corporation

Published: Oct 3, 2019

References