■
`
`Article
`Peripheral Electrical and Magnetic Stimulation to
`Augment Resistance Training
`
`Jawad F. Abulhasan *, Yvonne L. D. Rumble, Emma R. Morgan, William H. Slatter and
`Michael J. Grey
`
`School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Edgbaston Campus,
`Birmingham, West Midlands B15 2TT, UK; y.rumble@hotmail.co.uk (Y.L.D.R.); morgan3193@gmail.com (E.R.M.);
`slatter@hotmail.co.uk (W.H.S.); drmichaeljgrey@gmail.com (M.J.G.)
`* Correspondence: jawad.abulhasan@gmail.com; Tel.: +965-6666-7770
`
`Academic Editors: Giuseppe Musumeci and Paola Castrogiovanni
`Received: 5 June 2016; Accepted: 30 August 2016; Published: 13 September 2016
`
`Abstract: Electrical stimulation (ES) and magnetic stimulation (MS), applied peripherally, may
`be used to elicit muscle contractions to increase muscle hypertrophy, increase muscle strength
`and reduce knee laxity in rehabilitation following injury. We aimed to examine the effect of a
`three-week exercise programme designed to induce muscle hypertrophy augmented by peripheral
`ES and MS. We hypothesised that the use of peripheral stimulation to augment voluntary drive
`during a resistance-training protocol would induce more repetitions thus leading to increased thigh
`circumference, muscle layer thickness, and quadriceps strength whilst decreasing knee laxity. Thirty
`healthy participants were divided randomly into either ES, MS or Control groups. Five resistance
`training sessions were carried out, consisting of four sets of quadriceps extensions. During the first
`three sets the participants performed eight repetitions at 85% of their 1-repetition maximum (1-RM).
`On the last set, the participants were instructed to perform the exercise until failure. The augmentation
`of peripheral stimuli allowed the MS and ES groups to continue to exercise producing, on average,
`4 ± 2 and 7 ± 6 additional repetitions with ES and MS, respectively. Following the training, significant
`increases were observed for both 1-RM (p = 0.005) and muscle layer thickness (p = 0.031) whilst no
`change was observed in thigh circumference (p = 0.365). Knee laxity decreased (p = 0.005). However,
`there were no significant differences in the stimulation groups compared with control for any of
`these measurements. The additional repetitions elicited by stimulation after the point of failure
`suggests that peripheral electrical and/or magnetic stimulation may be useful as an adjunct for
`resistance training. However, this effect of resistance training augmented by peripheral stimulation
`on hypertrophy, strength and knee laxity may be small.
`
`Keywords: k electrical stimulation; magnetic stimulation; strength
`
`1. Introduction
`
`Resistance training is frequently used to promote muscle hypertrophy, strength and knee laxity.
`Electrical stimulation (ES) and magnetic stimulation (MS) have been used as an adjunct to athletic
`training [1–3], although it is more commonly used as a rehabilitation therapy to promote quadriceps
`strength after surgery [4–7], quadriceps hypertrophy [8], to investigate different types of muscle
`fatigue [9], daily functional activities after stroke [10], and osteoarthritis patients [11,12]. However, the
`evidence concerning the usefulness of peripheral stimuli as an adjunct to training programmes for
`enhancing muscle hypertrophy, strength, knee laxity and training healthy people is not conclusive.
`One reason for the inconsistence effects reported in the literature is the methods by which stimulation
`is applied.
`
`J. Funct. Morphol. Kinesiol. 2016, 1, 328–342; doi:10.3390/jfmk1030328
`
`www.mdpi.com/journal/jfmk
`
`Journal of
`Functional Morphology
`and Kinesiology
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`Kyung-Min et al. [4] systematically reviewed the literature assessing the effect of ES on
`quadriceps strength and functional performance following knee surgery. They reported significant
`effect sizes of quadriceps isometric and isotonic torque (ranging from −0.74 to 3.81) at 6 weeks
`post-operatively, in contrast, the effect sizes of the lateral step-up test and functional reach test were
`not significant (ranging from 0.07 to 0.64). The authors concluded that ES with exercise may be more
`effective in enhancing quadriceps strength than exercise alone. In a more recent systematic review,
`Hewlett et al. [10] examined the ability of ES to improve walking speed, wrist extension and ankle
`dorsiflexion, and investigated whether it is more effective than training alone. They showed that
`ES had a mean moderate effect (0.40, 0.09−0.72; 95% CI) on activity compared to no or a placebo
`intervention. In addition, the stimulation group showed a mean large effect on upper limb activity
`(0.69, 0.33−1.05; 95% CI) and a small effect on walking speed (0.08 m/s, 0.02−0.15; 95% CI) compared
`to the control group. Their findings suggest that ES could be used in patients after traumatic injuries
`where functions have been affected.
`The literature lacks a gold standard anteroposterior knee laxity measure to assess anterior cruciate
`ligament (ACL) injuries [13]. As a result, clinicians rehabilitate the injured knee through a variety of
`resistance training protocols with the aim of strengthening thigh muscles to overcome knee instability.
`Beretta-Piccoli et al. [14] reported that patients showed less fatigability after 24 months of ACL
`rehabilitation compared to a group of patients who underwent less than 12 months rehabilitation.
`This suggests that long term resistance training strategies after ACL reconstruction should be
`implemented to reduce knee injury rates. Taradaj et al. [7] assessed if ACL-reconstructed male
`football players (n = 40) benefited from ES as an adjunct to their regular protocol after knee ACL
`reconstruction. To the authors’ knowledge, this study design had the shortest protocol for their
`experiment (one month), and both the intervention and control groups received three sessions weekly
`consisting of the same exercise programme. The intervention group received ES on both right and left
`quadriceps three times daily, three days a week. The comparison of post-training measures showed a
`significant difference in favour of the stimulation group in the quadriceps extension (30.1% versus 4.6%,
`p = 0.002) and thigh circumference (1.4% versus 0.6%, p = 0.04). The authors concluded that there is
`evidence of the benefit of peripheral ES in restoring quadriceps muscle mass and strength in football
`players. Barcellona et al. [15] investigated the effect of two sets of 20-RM (LOW group) and 20 sets
`of 2-RM (HIGH group) quadriceps open kinetic chain resistance training on anterioposterior knee
`laxity. Unlike the HIGH and control groups, the LOW group demonstrated a mean reduction of
`5 cm in anterior knee laxity after a twelve-week training protocol. The authors concluded that knee
`extensor open kinetic chain resistance training at the corrected dose may lead to a reduction in anterior
`knee laxity of the ACL-injured knee. To the author’s knowledge, this study is the only one that has
`investigated the effect of quadriceps hypertrophy training on anterioposterior knee laxity.
`In addition to its clinical use, the effect of peripheral stimulation as an adjunct to weight training
`has been investigated in healthy people. Kubiak et al. [3] compared quadriceps strength torque in
`control (n = 9), isometric exercise (n = 10) and ES (n = 10) groups before and after a five-week training
`protocol consisting of three sessions per week. The quadriceps of the stimulation group received 15-s
`long stimulation contractions with a 50-s rest period between each contraction. All the participants
`tolerated a stimulation intensity which ranged between 75% and 134% of the MVIC, and significant
`strength increases (p < 0.05) were seen for all in both the electrical and isometric exercise groups.
`Szecsi et al. [1] evaluated the mechanical power generated by healthy participants during MS or ES
`induced ergometer training conditions; MS produced more mechanical power (23.8 ± 9.1 W) and
`longer cycling exercise compared to ES (11.3 ± 11.3 W). Bax et al. [16] systematically reviewed the
`literature that investigated the effect of ES as an adjunct to training on the quadriceps femoris muscle
`strength for both healthy and ACL-reconstructed participants. A number of important conclusions
`were highlighted in this review. They suggested that the application of ES for both injured and
`non-injured participants is likely to be more appropriate as an adjunct to rather than a replacement
`of resistance training. They also suggest voluntary activity together with ES likely results in greater
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`efficacy. Their meta-analysis indicated that publication bias may be present in the literature regarding
`whether the included studies represent the full spectrum of trials performed in actual research practice.
`Finally, they highlighted the observation that the literature in this field lacks high quality studies and
`that further research is necessary.
`Recently, peripheral MS has been trialled as an alternative to ES [9,17]. As this technique is
`novel, there is a dearth of literature examining its efficacy as an adjunct to training programmes for
`quadriceps circumference, muscle layer thickness, strength and knee laxity. Previously, peripheral MS
`has been restricted to the study of fatigue [18] and it has been reported that peripheral stimulation
`might minimise the effect of muscle fatigue and shorten the time spent in recovery [1,7,18]. In addition,
`peripheral stimulation alongside weight training may be preferred by patients and athletes as it
`is characterised by portability (ES) and less pain (MS) compared to alternative methods, such as
`stretching, massage and cold water immersion [11,19]. Moreover, the application of peripheral ES and
`MS will bypass central nervous system (CNS) fatigue, and, therefore, it may be more efficacious if
`applied at the point of voluntary muscle failure in order to induce additional repetitions. Nevertheless,
`studies that showed a positive effect of peripheral stimulation used subjective outcome measures
`(e.g., pain), which increase the chances of false positive results [20,21].
`We aimed to determine whether peripheral ES and MS applied at the point of muscle failure
`following voluntary exercise could induce greater hypertrophy, strength and less anterior knee laxity
`than voluntary muscle activity alone. We hypothesised that a three-week training protocol using
`peripheral ES or MS applied at the point of voluntary muscle failure would induce more repetitions,
`and increase thigh circumference, muscle layer thickness, quadriceps strength, whilst decreasing
`anterior knee laxity compared to the controls.
`
`2. Materials and Methods
`
`2.1. Participants
`Thirty healthy participants (16 females, mean age 20 ± 4 SD years, range = 18–37; and 14 males,
`mean age 19 years ± 1 SD, range = 18–20) were recruited. All the participants were undergraduate
`university students who performed active regular exercise of not less than 30 min of physical activity
`at least five times per week. Participants were screened for previous knee injuries and neuromuscular
`conditions, and agreed not to undergo any additional leg strength training during the three weeks
`of this study. All participants provided written informed consent prior to participating in the study.
`The experimental procedures were conducted in accordance to the Declaration of Helsinki and were
`approved by the ethical committee of the University of Birmingham Science, Technology, Engineering
`and Mathematics (STEM) committee (ethics approval code: ERN-14-0188).
`
`2.2. Study Design
`
`The study was carried out over 21 days and had a between-participant design with four
`dependent variables: girth measurement of the thigh muscle, quadriceps muscle layer thickness, knee
`anterioposterior laxity measure, and maximum weight lift of the quadriceps extension. Participants
`were randomly assigned to one of the three study groups: strength training only (control), strength
`training with electrical stimulation (ES), or strength training with magnetic nerve stimulation (MS).
`The study had two independent variables: time (pre vs. post) and group (electrical vs. magnetic vs.
`control). The study protocol started with baseline testing and a weight training session on day one,
`followed by two rest days, which were also provided between each subsequent training session. After
`the final training session all the participants rested for a week to ensure no peripheral fatigue existed as
`a result of the training protocol. Finally, on day 21, post-experimental testing was conducted (Figure 1).
`All measurements were carried out on the participant’s dominant leg in a non-fatigued state.
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`['s~;;ii~~················1 f Aii"·~;~~~·~·······i
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`
`3. Anterior
`knee stability
`
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`
`(30 s rest I •~----'
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`
`BO 1/o of 1-RM +
`individualized electrical
`stimulation threshold
`applied
`
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`
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`
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`
`4.1-RM
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`threshold applied
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`
`i 5 sessions from Day 4 and every 2 days i Day 21
`
`[ Day 1
`:
`
`Figure 1. Flow diagram of the weight training protocol for the three groups. All performed a baseline
`measure before any weight training followed by four sets of resistance quadriceps weight training.
`The first three were standardised to eight repetitions only at 80% of 1-RM. The fourth set was aimed
`to reach the maximum number of repetition a participant can could perform. For the intervention
`groups both received either stimulation to assess whether extra repetitions could be induced or not
`at point of muscle failure. ES = electrical stimulation; MS = magnetic stimulation; reps = repetitions;
`1-RM = 1-repetition maximum.
`
`2.3. Procedures
`
`Baseline and post-exercise measures for thigh circumference (Section 2.4.1), muscle layer thickness
`(Section 2.4.2) and knee laxity (Section 2.4.4) were recorded with the participant laying supine on a
`plinth. The baseline and post-exercise 1-RM assessment (Section 2.4.3) and fatiguing exercises were
`conducted with the participant seated in Cybex chair (Cybex VR3, International Inc., Owatonna,
`MA, USA).
`The study training protocol was designed to focus on hypertrophy rather than strength. Previous
`research has suggested that optimum hypertrophy gains in healthy individuals are best obtained when
`performing the 1-repetition maximum (1-RM) technique (see [22] for review), although it has also been
`shown that training with higher intensities can also lead to strength gains in addition to hypertrophy
`(e.g., [23,24]). Each participant performed three sets of 8 repetitions at 80% of their 1-RM (as defined
`in Section 2.4.3) with 30 s rest between each set (Figure 1). This was followed by a fourth set, also
`performed at 80% of the 1-RM, where the participant exercised to the point of muscle failure. Failure
`was defined as the point at which a participant could no longer voluntarily contract the quadriceps
`to fully extend the leg. At this point either electrical (ES group) or magnetic (MS group) stimuli
`were provided to augment the voluntary effort thus allowing the participants to perform additional
`repetitions beyond the point of failure. In both cases, stimuli were delivered to the motor point of
`the rectus femoris muscle. Electrical stimuli were delivered through self-adhesive surface stimulating
`electrodes (Compex Easy Snap, Compex Global, Surrey, UK) using the Mi Compex 3, Professional
`(Compex Global), with a pulse duration of 400 µs and a pulse frequency of 50 Hz. To determine the
`magnitude of the stimuli, the intensity of stimulation was increased to the point where the greatest
`contraction was produced within the individual tolerance level of the participant. This intensity
`was recorded as their maximum threshold. The magnitude for magnetic stimuli (MagPro ×100,
`MagVenture, Farum, Denmark) was determined in a similar manner increasing the stimulation from
`5% intensity until reaching their maximum threshold.
`
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`2.4. Assessment Methods
`
`All testing and weight training sessions were supervised by a certified strength and conditioning
`coach. Post-testing was carried out by an experimenter who had remained blinded throughout the data
`collection sessions to avoid bias when reading the follow up results. Post-training measurements were
`carried out at roughly the same time of day (±2 h) to reduce the effect of circadian fluctuations [25,26].
`All measures were taken from the participant dominant leg.
`
`2.4.1. Thigh Circumference
`
`Thigh circumference was measured with the participant lying supine position on a plinth.
`The measurement was taken at the midpoint between the anterior superior iliac spine (ASIS) and
`the lateral epicondyle of the femur, and the position was marked with a permanent marker. Three
`measures of thigh circumference were made with a medical tape recording to the nearest millimetre,
`from which a median value was calculated for use in the statistical analysis.
`
`2.4.2. Muscle Layer Thickness
`
`With the participant in the same position as for the circumference measure, rectus femoris (RF)
`muscle layer thickness (MLT) was obtained using a Phillip Sonos D2 5500 ultrasound (US) with an
`11-3L probe at an image depth of 7 cm. Measurements were made using the ultrasound’s calliper
`function. Rectus femoris MLT measures were repeated three times to the nearest millimetre, from
`which a median value was calculated for use in the statistical analysis (Figure 2).
`
`Figure 2. Illustration of how the muscle layer thickens was measured using the ultrasound image for
`every participant. The distance between the upper layer and lower layer of the rectus femoris muscle
`image was measured using the integrated US arrow. The US gives the exact distance between the
`two heads of the arrow which corresponds to the thickness of the measured muscle.
`
`2.4.3. Maximal Leg Extension
`
`Knee extension strength was measured with a Cybex VR3 (Figure 3). The participant was
`seated with the back support and tibia pad adjusted to fit the individual’s height, and these seating
`
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`adjustments were recorded in order to replicate the participant’s position in all tests. Each participant
`sat with the hips straight and in line with each other, knees at 90 degrees, the back in a comfortable
`position and toes dorsiflexed. Following a short warm-up, participants were instructed to perform
`two repetitions at increasing weight and were challenged with ensuring that their legs reached full
`extension in a controlled manner. Once the participant could not complete as repetition, this weight
`was recorded as their one-repetition maximum (1-RM).
`
`Figure 3. Voluntary leg extension setup and participant in the starting position of the weight training
`programme. The participant was instructed to fully extend their lower limbs with a slow and
`controlled movement and then return to the starting point. This cycle was counted as one successfully
`completed repetition.
`
`2.4.4. Knee Anterioposterior Laxity Test
`
`A KT-2000 knee arthrometer (MEDmetric Corp., San Diego, CA, USA) was used to measure the
`anteroposterior displacement of the femur on the tibia. For this measure the participant remained
`relaxed in a supine position on the plinth with their dominant knee supported at 30◦ of flexion as
`measured using a goniometer. Initially, the KT-2000 device was secured over the participant’s leg in the
`ideal position with reference to the knee joint line. Both knees were supported on a firm, comfortable
`platform placed proximal to the popliteal space. In addition, a foot support, supplied in the KT-2000
`arthrometer kit, was used to position the leg symmetrically and to avoid external rotation of the
`tibia. Next, the Lachman test, forced anterior displacement of the tibia with respect to the femur,
`was performed by holding the femur and pulling on the handle of the KT-2000 (Figure 4). Anterior
`displacement was measured to the nearest millimetre. Three trials were conducted, with the median
`calculated for use in the statistical analysis.
`
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`Figure 4. The experimental procedure of the KT-2000 arthrometer and the position of the knee joint,
`placement of the examiner hands and the direction of the tibial pull is illustrated.
`
`2.5. Statistical Analysis
`
`An independent t-test was used to compare the additional number of repetitions elicited with ES
`or MS augmentation after voluntary failure. One-way analyses of variance (ANOVA) tests were used
`to compare the number of repetitions induced in each group during the final set before stimulation.
`In addition, two-way (ANOVA) tests were used to examine the time effect (pre and post) and the group
`effects in the three different study groups (control, ES and MS) for each of the four dependent variables.
`The normality of the data was assessed using the Kolmogorov-Smirnov test and there were equal
`variances of the dependent variables, which were assessed using the Levene’s test, across all levels of
`the independent variables. The level of significance was set at p ≤ 0.05 for all measures. If significance
`was achieved, then a Tukey post-hoc test was planned to be performed. All the statistical analyses of
`the data were executed using SPSS Statistics 22 Software (IBM, New York, NY, USA).
`
`3. Results
`
`All participants completed the study successfully and tolerated the stimulation well. At the end
`of the three-week training protocol, the maximum number of repetitions in the final set was 8 ± 2,
`9 ± 1 and 10 ± 1 for the control, ES and MS groups, respectively. A one-way ANOVA indicated that
`there was no significant difference in the mean number of repetitions during the final set between the
`groups (p = 0.538) (Figure 5).
`All the participants exposed to stimulation were able to complete addition repetitions; ES = 4 ± 2
`and MS = 7 ± 6, range (1–20). No significant difference between the number of additional repetitions
`for the ES and MS groups were observed (p = 0.187) (Figure 5). Participants in the ES group showed
`more confidence and comfort than the MS group during stimulation. This may be because the ES
`group had the ability to self-control the intensity of the stimulation as opposed to the MS group, were
`the intensity of the stimulation was controlled by the experimenter.
`Following the training, significant time-effect increases were observed for both 1RM (p = 0.005)
`and muscle layer thickness (p = 0.031), whilst no change in thigh circumference (p = 0.365) was
`noted, and knee laxity was observed to decrease (p = 0.005). However, there were no group-effect
`changes for the stimulation groups compared to the control group for any of the measurements: 1-RM
`F(2,27) = 0.90, p = 0.415, partial η2 = 0.03, ICC = 0.60, statistical power = 0.20 (Figure 6c), muscle layer
`thickness F(2,27) = 0.34, p = 0.712, partial η2 = 0.01, ICC = 0.73, statistical power = 0.10 (Figure 6b), thigh
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`circumference F(2,27) = 2.10, p = 0.132, partial η2 = 0.07, ICC = 0.75, statistical power = 0.41 (Figure 6a),
`and anterior knee laxity, F(2,27) = 1.23, p = 0.300, partial η2 = 0.04, ICC = 0.35, statistical power = 0.25
`(Figure 6d).
`
`Mean number of reppelitions at lhe final set pre and posl
`stimulalion
`
`■ Post-stimulation
`LJ Pre-stimulation
`
`30
`
`25
`
`20
`
`15
`
`10
`
`5
`
`o,-'--'--~___,_ _ ___ .__._ __ ...,_
`Control
`8ectrical
`Magnetic
`
`Figure 5. Bar plot of the mean number of repetitions each group performed during the final set
`before the addition of stimulation at the point of failure and the extra number of repetitions induced
`after muscle failure had been reached during the last training set in the two intervention groups.
`No significant difference in the mean of extra repetition numbers was observed between the two
`intervention groups. Data are expressed as mean ± standard deviation. ES = Electrical stimulation
`group, MS = magnetic stimulation group.
`
`a. M&an difference or thigh circumre,ence cctn)
`3.0- p = 0.1Jl
`
`b. Mean difference of muscle layer thickness (cm}
`p-0.712
`
`2.5·
`
`2 .0-
`
`1 .-5 "
`
`1.0-
`
`0 .0- -"--~-'-(cid:173)
`Control
`
`El~trical
`
`Magnetic
`
`0.5
`
`0.
`
`control
`
`T
`
`c. Mean difference of 1-RM (kg) p- 0.JI~
`
`d. ~an d'tfertnce or anter10r knee la)(lly (mm> p = fl30fl
`
`1
`
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`COl'l!rol
`
`Electflcal
`
`Me;netic
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`
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`
`Cort10i
`
`Figure 6. Bar plots of the means of the difference between baseline and post-training measures for all
`three groups for (a) thigh circumference; (b) muscle layer thickness; (c) 1-repetition maximum and
`(d) anterioposterior knee laxity. No significant difference was observed between the three groups. Data
`are expressed as mean ± standard deviation.
`
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`4. Discussion
`
`The aim of this study was to determine if peripheral ES or MS applied at the point of muscle
`failure following voluntary exercise could induce greater hypertrophy, strength and lesser anterior
`knee laxity than voluntary muscle activity alone. Both peripheral ES and MS elicited additional
`repetitions following voluntary muscle failure. However, as applied in the present study, the effect of
`such training on muscle hypertrophy, strength and anterior knee laxity was not significantly different
`from voluntary training alone; hence the effect may be small.
`The literature describes a variety of approaches that have been used to evaluate muscle strength,
`such as hand-held dynamometer, isokinetic machines, 1-RM and maximal voluntary contraction
`technique. There is a consensus in the literature that the 1-RM is a reliable and relatively cost-effective
`technique, as it requires non-laboratory equipment and consequently is considered one of the most
`commonly used techniques to assess muscle strength in non-laboratory situations [27–31]; therefore,
`this measure was used to assess quadriceps muscle strength in this study. The number of extra
`repetitions for each participant in the final set was widespread (range, ES; 2–8; MS = 1–20). Despite
`the fact that a firm procedure was used, in this study, to establish a participant’s 1-RM, several factors
`may have affected the outcome and there remains the possibility that the participants who executed a
`higher number of repetitions had not in fact exercised at their 1-RM. This may be due to both neural
`and psychological supraspinal drive inhibition operating on the muscle motor units [32]. Belanger
`and McComas [33] reported that 50% of participants did not reach their 1-RM even when they were
`asked to exert force with their maximal volition. Therefore, this study shows that our developed 1-RM
`technique can better ensure that maximum weight is reached. This could be achieved by overtaking
`the neural inhibition through the use of peripheral stimulation. Thus, the results of this study show
`that the use of ES and MS alongside the traditional 1-RM technique can help better predict the actual
`1-RM for the quadriceps muscle. This novel technique could be a useful tool to accurately measure the
`maximum voluntary contraction of patients after injury and/or athletes during training. Thus, our
`novel technique could help guide the return-to-play decision as maximum strength and hypertrophy
`is warranted for safe return-to-play [23,34,35].
`Although the effect of weight training on muscle hypertrophy has been investigated in numerous
`studies, there is no information, to our knowledge, regarding the effect of ES and MS applied at
`the point of muscle failure following voluntary exercise on hypertrophy. Even though previous
`investigations have used ES or MS as standalone study arms to enhance hypertrophy [36–38], no
`study has investigated if stimulation applied at the point of muscle failure following voluntary
`exercise could induce greater hypertrophic changes than voluntary muscle activity alone. Our results
`indicate that there was no significant hypertrophic difference in the thigh circumference F(2,27) = 2.10,
`p = 0.132, partial η2 = 0.01 (Figure 6a) or muscle layer thickness F(2,27) = 0.34, p = 0.712, partial
`η2 = 0.01 (Figure 6b) following the application of ES or MS between the study groups. This may
`be due to fat loss [39] or non-hypertrophic adaptation of the neuromuscular system in response to
`static resistance training [40], rather than a change within the quadriceps circumference. In line with
`the above, Carolan and Cafarelli, [41] reported that after the first week of their training protocol the
`quadriceps extension antagonist muscle (hamstring) showed a decrease in muscle co-activation by
`20%. This non-hypertrophic adaptation of the neuromuscular system resulted in a reduction of thigh
`circumference post-training.
`The results of the presented study showed no significant difference in strength, although there
`was a trend for the stimulated groups to be greater than the controls (Figure 6). In addition, our results
`showed a small trend towards a decrease in muscle size as determined by thigh circumference
`(Figure 6a) and muscle layer thickness (Figure 6b). This is seemingly paradoxical, but Brook et al. [42] in
`his recent review concluded that the adaptations of muscle mass and strength to resistance-type training
`are as yet unclear. Previous literature has shown inconsistent results in the effect of resistance-type
`exercises on muscle mass and strength. For example, Farup et al. [43] reported a significant increase in
`both quadriceps muscle mass and strength [42–44] following a 10-week resistance training programme.
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`In contrast, McBride et al. [45] reported a significant gain in quadriceps strength with no gain in
`lean muscle mass following a 12-week programme of leg press resistance training. The controversy
`in the literature regarding the relationship between strength and hypertrophy gains after resistance
`training may be explained by the insensitivity of the muscle lean mass measures and differences in
`muscle-fibre types [46]. Magnetic resonance scanning, dual-energy X-ray absorptiometry (DXA), and
`computed tomography (CT) are considered the best measures of muscle mass [47,48] but they are not
`cost-effective. US is a commonly used, cost-effective, portable and quick device with which to quantify
`hypertrophy [49–51]. Unlike [43,52,53] who used DXA, MRI and CT, respectively, as a measure of lean
`muscle mass and reported significant hypertrophic changes, we used US to measure hypertrophic
`changes. It is crucial to shed light on the notion that the existing literature on “changes” in lean
`muscle mass in response to resistance training depends upon the method chosen to detect muscle
`hypertrophy [54]. Hence, experience of the principle investigator in performing the US procedure and
`the insensitivity of the US device may have played a role in the outcome of our study. Consequently,
`more studies are needed in order to confirm if peripheral ES and MS applied at the point of muscle
`failure following voluntary exercise can induce significant hypertrophic changes more than voluntary
`muscle activity alone in terms of the use of sensitive measures of hypertrophic muscle changes.
`Although the baseline measures differed between participants in the three groups, the tendency to
`a positive change of quadriceps strength as measured by the 1-RM (Figure 6c) in all groups is promising,
`despite the non-significant difference between the groups (CONT = 29.30 ± 10 kg, ES = 35.55 ± 21.38 kg,
`MS = 36.85 ± 23.61 kg). Previous studies have found a significant effect of ES on muscle strength
`versus a control group [7], and over periods as short as five weeks [2,3,12]. However, no studies
`have investigated if peripheral ES and MS applied at the point of muscle failure following voluntary
`exercise could induce greater strength changes than voluntary muscle activity alone. H