INFLUENCE OF RELATIVE BLOOD FLOW RESTRICTION PRESSURE ON MUSCLE ACTIVATION AND MUSCLE ADAPTATION BRITTANY R. COUNTS, BS,1 SCOTT J. DANKEL, BS,1 BRIAN E. BARNETT, BS,1 DAEYEOL KIM, MS,2 J. GRANT MOUSER, BS,2 KIRSTEN M. ALLEN, BS,2 ROBERT S. THIEBAUD, PhD,3 TAKASHI ABE, PhD,1 MICHAEL G. BEMBEN, PhD,2 and JEREMY P. LOENNEKE, PhD1 1

Kevser Ermin Applied Physiology Laboratory, Department of Health, Exercise Science, and Recreation Management, University of Mississippi, P.O. Box 1848, University, Mississippi 38677, USA 2 Department of Health and Exercise Science, Neuromuscular Research Laboratory, University of Oklahoma, Norman, Oklahoma, USA 3 Department of Kinesiology, Texas Wesleyan University, Fort Worth, Texas, USA Accepted 30 June 2015 ABSTRACT: Introduction: The aim of this study was to investigate the acute and chronic skeletal muscle response to differing levels of blood flow restriction (BFR) pressure. Methods: Fourteen participants completed elbow flexion exercise with pressures from 40% to 90% of arterial occlusion. Pre/post torque measurements and electromyographic (EMG) amplitude of each set were quantified for each condition. This was followed by a separate 8-week training study of the effect of high (90% arterial occlusion) and low (40% arterial occlusion) pressure on muscle size and function. Results: For the acute study, decreases in torque were similar between pressures [–15.5 (5.9) Nm, P 5 0.344]. For amplitude of the first 3 and last 3 reps there was a time effect. After training, increases in muscle size (10%), peak isotonic strength (18%), peak isokinetic torque (1808/s 5 23%, 608/s 5 11%), and muscular endurance (62%) changed similarly between pressures. Conclusion: We suggest that higher relative pressures may not be necessary when exercising under BFR. Muscle Nerve 53: 438–445, 2016

Low-load resistance exercise [20%–30% concentric 1-repetition maximum (1RM)] in combination with blood flow restriction (BFR) increases muscle size and strength in a variety of populations.1–3 When applied appropriately, this stimulus has been found to provide a safe and effective stimulus in the absence of measurable muscle damage.4,5 The mechanisms behind these beneficial effects are not completely known, but metabolic accumulation–induced fatigue may be playing an influential role in the muscle adaptations observed after this type of exercise. To illustrate, metabolic accumulation in combination with a reduced oxygen environment may increase recruitment of higher threshold (type II) muscle fibers.6,7 This suggests that higher pressures, resulting in a greater reduction in oxygen and subsequent increase in metabolic accumulation,8 may augment muscle fiber Abbreviations: 1RM, 1-repetition maximum; ANOVA, analysis of variance; bSBP, brachial systolic blood pressure; EMG, electromyography; FR, blood flow restriction; MVC, maximal voluntary contraction Additional Supporting Information may be found in the online version of this article. Key words: arterial occlusion; hypertrophy; KAATSU; perceptual response; resistance training; vascular occlusion training Correspondence to: J.P. Loenneke; e-mail: [email protected] C 2015 Wiley Periodicals, Inc. V

Published online 2 July 2015 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/mus.24756

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recruitment with low-load resistance exercise in combination with BFR. Muscle fiber recruitment may be important, as it has been previously suggested that increased recruitment is related to some degree with changes in muscle protein synthesis.9 To illustrate, lower body low-load exercise to volitional fatigue results in high levels of muscle activation,10–12 and has also been found to produce muscle protein synthetic13 and muscle hypertrophic responses similar to higher load resistance training.14,15 We recently observed that higher relative pressures (pressures based on individual limb circumference) may not augment muscle activation in the lower body.12 However, due to the lack of statistical power to compare across groups, only qualitative analyses could be completed across pressures (40%–60% estimated arterial occlusion). Furthermore, no published study to date has compared the hypertrophic responses of BFR training under different occlusion pressures. Thus, the purpose of this study was 2-fold. First, we sought to determine, using a within-subject design, whether or not higher relative pressures provide an increase in muscle activation over lower pressures. We hypothesized that muscle activation would not be augmented to a large degree with higher pressures. Second, based on the acute muscle activation data, we sought to determine whether differences in muscle adaptation would be observed after 8 weeks of resistance training with either high or low pressures applied. Although similar muscle activation was reported across pressures, we hypothesized that exercising with higher relative pressures may attenuate some of the gains in muscle mass due to the reduction in total exercise volume observed with higher pressures from the acute study. METHODS Participants.

For experiment 1, 14 physically active participants (10 men, 4 women) were recruited. “Physically active” was defined as being active 3 or more days per week with an upper body resistance training component 2 or more days per week for at least the previous 3 months. Physically active MUSCLE & NERVE

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participants were used to better reflect the actual acute responses to different exercise and limit the possibility of a training effect due to repeated testing. For experiment 2, a total of 8 non–resistance-trained men (n 5 5) and women (n 5 3) volunteered to participate in this study. One man enrolled but dropped out before the first visit, therefore analysis was conducted on the remaining 7 participants. Participants were excluded if they had at least 1 risk factor for thromboembolism. The experiments were approved by the university’s institutional review board, and each participant gave written informed consent before participation. Experiment 1 Study Design. During the initial visit participants had standing arterial occlusion pressure determined and were then tested on each arm for the unilateral dumbbell elbow flexion 1repetition maximum (1RM). Participants were then familiarized with the BFR stimulus and maximal voluntary contraction (MVC) testing. Next, participants were scheduled for the first of 3 testing visits with a minimum of 5 and a maximum of 10 days between visits. Participants completed all of the exercise conditions in random order (1 condition per arm) across 3 separate visits (2 conditions per visit). The exercise bouts within each day were separated by 10 min of rest. For each condition, the participants were instructed to complete 1 set of 30 repetitions followed by 3 sets of 15 repetitions at 30% of their concentric 1RM at 40%, 50%, 60%, 70%, 80%, or 90% of their standing arterial occlusion pressure. All conditions were separated by 30-s rest periods between sets. A metronome was used to ensure that the participants held the cadence of 1 s for the concentric muscle action and 1 s for the eccentric muscle action during the unilateral elbow flexion exercise. If the participant could not maintain the cadence during a particular set, the set was stopped, and the participant rested for 30 s until the next set. Muscle activation was measured at pre-exercise (no BFR) and during each set of exercise (with BFR). The elbow flexor MVC was performed on an isokinetic dynamometer pre- and post-exercise to determine fatigue. All testing sessions were completed before the participant exercised for that day, and each visit was completed at least 24 h after the last upper body workout. Electromyography and Isometric Fatigue. Electromyographic (EMG) signals were recorded from the biceps brachii of the arm during exercise. Electrodes were placed on a line between the medial acromion and the antecubital fossa at a distance of one-third from the antecubital fossa. The skin was shaved, abraded, and cleaned with alcohol wipes. Bipolar electrodes were placed over the muscle Relative BFR Pressure

belly with an inter-electrode distance of 20 mm. The ground electrode was placed on the seventh cervical vertebrae at the neck. The surface electrodes were connected to an amplifier and digitized (Biopac Systems, Inc., Goleta, California). The signal was filtered (low-pass filter 500 HZ, high-pass filter 10 HZ), amplified (1,0003), and sampled at a rate of 1 kHZ. Before the exercise bout, the participant performed 2 isometric MVCs with the biceps brachii at a joint angle of 908 with a 30-s rest between MVCs on an isokinetic dynamometer. The EMG was recorded continuously from the biceps brachii during each exercise bout. LabView 7.1 (National Instrument Corp., Austin, Texas) computer software was used to analyze the data. EMG amplitude (root mean square, RMS) was analyzed from the average of the first 3 repetitions and the average of the last 3 repetitions for each set and expressed relative to the highest preexercise MVC (%MVC). Experiment 2 Study Design. Based on findings from the acute study, we sought to determine whether the acute changes would translate to chronic muscle adaptation. Thus, participants completed 8 weeks of low-load unilateral elbow flexion training with 1 arm exercising at low pressure (40% arterial occlusion) and the other arm exercising at higher pressure (90% arterial occlusion). The participants visited the laboratory for a total of 26 visits. The first 2 pre-training visits consisted of paperwork and baseline measurements, followed by 22 separate training sessions and 2 post-training visits (48–72 h after last training session) that measured changes caused by the exercise intervention (Fig. 1). Participants trained 2 times per week for the first 2 weeks followed by 3 training sessions per week for weeks 3–8. A similar number of training sessions has previously been shown to produce measurable changes in muscle size and strength.16,17 The goal reps for each exercise protocol included 1 set of 30 repetitions followed by 3 sets of 15, with 30-s rest periods between sets. Exercise was completed to a metronome with 1 s for the concentric and 1 s for the eccentric portion of the exercise. Participants were stopped before completing the goal number of repetitions, when they were unable to lift the load with proper form or keep to the beat of the metronome. Training load was adjusted every 2 weeks to maintain 30% of 1RM. A non-BFR control condition was not included, as previous studies have consistently shown that repetition-matched protocols without BFR do not lead to meaningful changes in muscle size and strength.1 Determination of 1RM. For experiments 1 and 2, the maximum load that could be lifted for the MUSCLE & NERVE

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FIGURE 1. Outline of experiment 2. Mth, muscle thickness; 1RM, 1-repetition maximum; 30% to failure is test of muscle endurance.

unilateral dumbbell curl through a full range of motion with proper form was assessed and recorded as the concentric 1RM. Briefly, participants completed 5 reps of light weight (3.41 kg) as a warm-up, and then weight was progressively increased until the load could not be lifted successfully through a full range of motion.18 Each arm was tested in a random order, and all participants reached their 1RM within 5 attempts. To ensure strict form, participants completed their concentric 1RM with their back and heels against a wall and with feet shoulder width apart. Determination of Arterial Occlusion Pressure. For experiments 1 and 2, a narrow (5-cm-wide bladder) nylon cuff was applied to the most proximal part of the arm. Pressure was regulated using a cuff inflator system (E 20 Rapid Cuff Inflator; Hokanson, Bellevue, Washington). The pulse at the wrist (arterial blood blow) was detected using a hand-held bidirectional Doppler probe placed on the radial artery. The cuffs were inflated to 50 mm Hg and quickly raised to the participant’s previously measured systolic blood pressure. Pressure was then slowly increased until the arterial flow was no longer detected during inflation. Arterial occlusion pressure was recorded to the nearest 1 mm Hg as the lowest cuff pressure at which a pulse was not present.

For experiment 2, muscle size was estimated by B-mode ultrasound (SSD-500 with a 5-MHZ probe; Aloka). Ultrasound measurements of the biceps brachii were taken halfway between the acromion process and lateral epicondyle and 10 cm proximal to the lateral epicondyle. Muscle size of the anterior forearm was measured at 30% proximal between the styloid process and the head of the ulna. Three images were taken at each site, printed, and analyzed by an investigator who was blinded to the arm’s condition. The average of the 3 measurements was used for final analysis. Muscle Muscle Thickness.

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thicknesses of the deltoid and triceps were also measured to demonstrate stability of the measurement across time, as those muscle groups were not expected to change with strict elbow flexion exercise. The minimal difference (i.e., reliability) needed to be considered real for the anterior portion of the upper and lower arm was calculated to be 0.2 cm. Muscle Endurance. Participants completed as many repetitions of unilateral elbow flexion exercise as they could to a metronome with 1 s for the concentric and 1 s for the eccentric portion of the lift. The load used was 30% of the predetermined 1RM for that test day. All participants kept their back and heels against a wall with their feet shoulder width apart to ensure strict form throughout testing. Isokinetic Elbow Flexion Strength. Isokinetic torque was measured using an isokinetic dynamometer (Quickset System 4; Biodex) Measurements were taken on both arms in random order. First, participants completed 2 sets of 3 at 1808/s separated by 90 s of rest. This was then repeated at 608/s. All values were gravity corrected. The minimal differences needed for changes to be considered real were calculated as 5 Nm for 1808/s and 3 Nm for 608/s. Ratings of Discomfort. Ratings of discomfort were quantified using the Borg discomfort scale (CR101) before each exercise bout and after each set for all training sessions, Methods have been described in detail previously.19 Statistical Analyses. All data were analyzed using SPSS 22.0 software (SPSS, Inc., Chicago, Illinois) with variability represented as standard deviation (SD). For experiment 1, there were no baseline differences in MVC, thus a 1-way analysis of variance (ANOVA) was completed for the MVC change scores (mean decrease from baseline) and MUSCLE & NERVE

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overall exercise volume to determine whether differences existed between conditions. For EMG, a 6 (condition) 3 4 (time) repeated-measures ANOVA was used. A significant result from the repeatedmeasures ANOVA was followed by a 1-way ANOVA to determine where the difference occurred across time within each visit and within each time-point across visits. Statistical significance was set at an alpha level of 0.05. For experiment 2, a 2 (condition) 3 3 (time) repeated-measures ANOVA was completed for muscle thickness, maximal isotonic strength, and exercise volume. A significant result from the repeatedmeasures ANOVA was followed by a 1-way ANOVA to determine where the difference occurred across time within each pressure, and a paired-sample ttest was used to determine where the differences occurred between pressures within each timepoint. A 2 (condition) 3 2 (time) repeatedmeasures ANOVA was completed for isokinetic strength. Follow-up tests included paired sample ttests across time within each pressure and across pressures within each time-point. For ratings of discomfort, Wilcoxon-related samples non-parametric tests determined differences between pressures within each set of exercise. Statistical significance was set at an alpha level of 0.05. RESULTS Experiment 1.

Participants. Participants (n 5 14), on average, were 24 6 3 years old, 174 6 7 cm in height, 79.7 6 11.3 kg in weight, and had a 1RM for the right arm of 18 6 6 kg and a 1RM for the left arm of 19 6 6 kg, and had a standing arterial occlusion pressure of 140 6 14 mm Hg for the right arm and 143 6 17 mm Hg for the left arm. Maximal Voluntary Contraction. There were no significant differences across arterial occlusion pressures in the MVC change scores from baseline (P 5 0.344). The grand mean decline in torque from baseline was 215.5 6 5.9 Nm. Exercise Volume. There were significant differences in exercise volume across pressures, with less volume being completed at the highest pressures (P < 0.001; Fig. 2B). EMG. There was no significant interaction with amplitude of the first 3 repetitions (P 5 0.456; Table 1). In addition, there was no significant main effect for condition (P 5 0.850), but there was for time (P < 0.001), with amplitude increasing from the first set. For the last repetitions, there was no significant interaction with EMG amplitude (P 5 0.450; Table 1). In addition, there was no significant main effect for condition (P 5 0.881), but there was for time (P 5 0.021).

Participants. Participants (n 5 7), on average, were 23 6 3 years old, 169.6 6 9.5 cm

Experiment 2.

Relative BFR Pressure

FIGURE 2. Mean total exercise volume completed across pressures in the acute study (experiment 1). Conditions with different letters represent significant differences between conditions (P  0.05). Variability is represented as standard deviations.

in height, 56.7 6 11.3 kg in weight, and had a standing arterial occlusion pressure of 129 6 19 mm Hg for the high-pressure arm and 133 6 19 mm Hg for the low-pressure arm. Thus, the mean pressure used during exercise was 116 6 17 mm Hg and 53 6 7 mm Hg for the high- and lowpressure arms, respectively. Of the 22 training sessions, 2 participants missed 1 training session each, translating into an overall completion rate of 99%. Muscle Thickness. There was no significant interaction with muscle thickness at the mid–upper arm (P 5 0.258; Fig. 3A) or 10 cm above the elbow joint (P 5 0.674; Fig. 3B). In addition, there was no significant main effect for condition (P  0.151), but there was for time (P < 0.001). With the forearm, there was no interaction (P 5 0.338) or main effect of condition, but there was a main effect of time (P 5 0.04). Follow-up tests for forearm muscle size identified a significant increase from pre to post [1.8 6 0.1 cm vs. 1.9 6 0.2 cm], but this difference did not exceed the error of our measurement. In addition, no significant differences were observed across time for the triceps or deltoid (data not shown). Muscle Strength. There was no significant interaction with muscle strength (P 5 0.909). In addition, there was no significant main effect for condition (P 5 0.409), but there was for time (P < 0.001). Maximal isotonic strength (1RM) increased from pre to mid [11.2 6 5 kg vs. 12.2 6 5.5 kg] to post [13.2 6 5.8 kg], with significant differences between each time-point (P  0.006). Isokinetic Torque. There was no significant interaction with isokinetic strength at 1808/s (P 5 0.480; Fig. 3C) or 608/s (P 5 0.386; Fig. 3D). In addition, MUSCLE & NERVE

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Table 1. Muscle activation from experiment 1. EMG amplitude first 3 reps (%MVC) Arterial occlusion 40% 50% 60% 70% 80% 90%

Set 1 33 (9) 38 (13) 43 (31) 36 (20) 37 (13) 36 (20)

Arterial occlusion 40% 50% 60% 70% 80% 90%

Set 1 53 (16) 62 (27) 71 (45) 62 (43) 61 (26) 57 (35)

Set 2 Set 3 46 (19) 48 (18) 51 (17) 56 (21) 58 (32) 56 (30) 49 (26) 52 (26) 53 (23) 45 (15) 53 (37) 53 (39) EMG amplitude last 3 reps (%MVC) Set 2 Set 3 61 (22) 56 (23) 74 (34) 64 (38) 71 (37) 65 (39) 65 (37) 59 (30) 68 (41) 66 (48) 64 (53) 58 (49)

Time Set 4 44 (14) 53 (23) 56 (28) 49 (23) 55 (31) 51 (33)

1 vs. 2, 3, 4

Set 4 49 (16) 63 (38) 60 (35) 55 (30) 61 (40) 56 (43)

2 vs. 3, 4; 3 vs. 4

Variability represented as standard deviations. Main effects of time are noted in the “Time” column at far right. The different numbers represent significant differences between sets (P  0.05).

there was no significant main effect for condition (P  0.633), but there was for time (P  0.014). Muscle Endurance. There was no significant interaction with muscle endurance (P 5 0.901). In addition, there was no significant main effect for condition (P 5 0.265), but there was for time (P < 0.001). The number of repetitions completed to failure increased from pre [37 (7) repetitions] to post [60 (13) repetitions]. Rating of Discomfort. Ratings of discomfort between pressures were statistically compared in the first, eleventh, and last training sessions. Ratings of discomfort were significantly different

between pressures for most sets of exercise (Table 2). When plotted across time, the peak discomfort was almost always higher in the high-pressure arm (see Fig. S1 in the Supplementary Material, available online). Exercise Volume. There was no significant interaction with the average repetitions completed in the first set in weeks 1, 4, or 8 (P 5 0.08; Table 3). In addition, there was no significant main effect for condition (P 5 0.08) or time (P 5 0.10). For the average repetitions completed in sets 2–4, there was no significant interaction (P 5 0.416; Table 3); however, there was a significant main

FIGURE 3. Mean changes across applied pressures in muscle thickness at the 10-cm site (A), muscle thickness of the mid-upper arm (B), and isokinetic peak torque at 1808/s (C) and 608/s (D). Dagger (†) indicates a main effect of time. Time-points with different letters represent significant differences between time-points in (A) and (B). Variability is represented as standard deviations. To maintain sufficient statistical power, only pre-exercise, day 11, and post-exercise were compared. 442

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in exercise volume between pressures did not appear to affect muscle adaptation.

Table 2. Ratings of discomfort from experiment 2. Ratings of discomfort (0–101) Day 1 High Low Day 11 High Low Day 22 High Low

Set 1 2 (0.5–2.5) 0.5 (0.3–2) Set 1* 2 (1.5–3) 0.7 (0.5–1) Set 1 1.5 (1–2) 1 (0.3–1.5)

Set 2* 3 (3–4) 1 (0.3–2.5) Set 2* 2.5 (2–4) 1 (0.5–2) Set 2* 2 (1.5–3) 1 (0.5–2)

Set 3* 3.5 (3–5) 2 (0.3–3) Set 3* 3 (1.5–5) 1 (1–2) Set 3* 3 (2.5–3) 1 (0.7–2)

Set 4* 4 (3–7) 2.5 (0.5–5) Set 4* 3 (2–5) 1.5 (1–2) Set 4* 3 (3–3) 1.5 (1–2.5)

Data presented as 50th percentile (25th–75th percentiles). *Significant differences between pressures for that set (P  0.05).

effect for condition (P 5 0.004) and time (P < 0.001). For the average exercise volume completed in weeks 1, 4, or 8, a 2 3 3 repeatedmeasures ANOVA did not reveal a significant interaction (P 5 0.766) or main effect of condition (P 5 0.127), but there was a main effect for time (P < 0.001; Table 3). DISCUSSION

These findings suggest that relatively high pressures may not be needed to maximize the acute or chronic response to BFR exercise. For example, although a wide range of relative pressures were used in the acute experiment, the increase in fatigue and muscle activation across pressures was similar. Thus, we speculated that lower pressures may produce similar changes in muscle size and strength as higher pressures. To provide further insight, we completed a smallscale training study to determine if differences in muscle adaptation could be observed after exercise in combination with 2 different pressures (40% vs. 90% arterial occlusion). Our chronic data are in agreement with the acute experiment and suggests that both relative pressures increased muscle size and strength to a similar extent after low-load training in combination with BFR. Contrary to our hypothesis, the difference

Experiment 1. Previous studies in the upper body have identified increases in EMG amplitude during low-load resistance exercise in combination with BFR.7,17,20–23 The increase in EMG amplitude may be due to a metabolic “overload” (i.e., depletion of phosphocreatine stores and decrease in muscle pH) induced fatigue within the muscle.6 The metabolic accumulation in concert with a reduced oxygen environment from the restriction of blood flow may increase recruitment of higher threshold fibers through stimulation of group III and IV afferent fibers.7 The muscle activation of the last 3 repetitions marginally decreased in some of the sets. This is likely due to the participant “cheating the weight up” with muscles other than the biceps brachii. This occurred despite our efforts to make the exercise execution as strict as possible. To our knowledge, only 1 other study21 has addressed those changes across different pressures [80%, 100%, and 120% of brachial systolic blood pressure (bSBP)] in the upper body. In that study, the authors observed that muscle activation increased progressively in all groups. However, the amplitude was significantly greater with 120% bSBP than a work-matched non-BFR condition from the end of 30 repetitive contractions to the end of the second set of 15 contractions. In addition, previous data in the lower body suggested that EMG amplitude is increased from 40% to 50% estimated arterial occlusion, but no further increase was observed when the pressure was increased to 60% estimated arterial occlusion.12 Our finding of a lack of augmentation with increasing pressure is in contrast to the 2 previous studies. Possible reasons for this discrepancy may be related to the setting of restriction pressure. In our study we set the pressure relative to the actual cuff used during exercise, but the aforementioned investigation by Yasuda et al.21 did not. Second, the previous study in our laboratory was completed with narrow cuffs in the lower

Table 3. Exercise volume from experiment 2.

First set High Low Sets 2–4 High* Low† Volume (kg) High Low

Week 1

Week 2

Week 3

Week 4

Week 5

Week 6

Week 7

Week 8

27 (3) 29 (1) Week 1* 5 (2) 10 (4) Week 1* 151.7 (88.5) 185. 5 (81.9)

28 (2) 29 (1) Week 2 5 (2) 10 (4) Week 2 155.5 (76) 186.1 (74)

28 (1) 30 (0) Week 3 6 (2) 11 (3) Week 3 171.9 (86) 207.7 (97.1)

30 (0) 30 (0) Week 4† 9 (4) 13 (3) Week 4† 203.7 (99.7) 229.3 (117.9)

30 (0) 30 (0) Week 5 8 (3) 12 (2) Week 5 212.8 (107.8) 252.7 (124.8)

30 (0) 30 (0) Week 6 9 (4) 13 (2) Week 6 221.2 (107.9) 257.4 (122.4)

30 (0) 30 (0) Week 7 11 (4) 14 (1) Week 7 250.3 (119.5) 282.5 (131.8)

30 (0) 30 (0) Week 8‡ 11 (4) 14 (1) Week 8‡ 254.7 (115.5) 283.7 (132.8)

Weeks with different symbols represents significant differences between weeks. Conditions with different symbols represent significant differences between conditions. To maintain sufficient statistical power, only weeks 1, 4, and 8 were compared. Variability represented as standard deviation.

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body,12 thus arterial occlusion could only be estimated.24 It is possible that the estimated value in the lower body may have been less than 40% arterial occlusion. However, in the present study, we were able to determine arterial occlusion in every individual, thus we likely have a truer representation of 40% arterial occlusion in the upper body. It may also be that there are intrinsic differences between the upper and lower body musculature. Experiment 2. Although research has shown that low-load exercise with BFR increases muscle mass and strength,1,3 it was unknown whether the applied pressure affected the overall adaptive response. We found no difference in muscle size, strength, or endurance between pressures, despite differences in exercise volume. It has been previously hypothesized that one needs to surpass a certain volume threshold to maximize the hypertrophic response9; however, our results suggest that threshold may be lower than the commonly prescribed 75-repetition protocol. This finding coincides with a previous study suggesting that more volume does not always augment muscle size and strength.25 Given that both groups had similar volumes of work in the first set, this may suggest that, in this population, the first set of approximately 30 repetitions may be the most important with the following sets being of less importance, assuming the muscle reaches maximal fatigue. However, we also cannot rule out the possibility that high relative pressure has a physiologic effect on muscle, making the overall exercise volume of less importance. It has been hypothesized that a hypothetical range may exist for observing beneficial adaptations with low-load exercise in combination with BFR, and higher pressures increase the possibility of an adverse event.26 Our results show that muscle adaptions were similar, but there was an overall higher rating of discomfort during exercise with the higher applied pressure. Although the differences in discomfort were small, these differences were maintained throughout the training study. Further, peak ratings of discomfort for each session were almost always greater with higher applied pressures compared with lower applied pressures (see Fig. S1 online). It is important to note that our rating quantified discomfort during exercise and not the rest periods. Most participants reported anecdotally much greater discomfort during the rest period with high relative pressures, which suggests that our measurement time-point was inadequate to show the true differences between pressures. Taken together, 40% arterial occlusion may be all that is needed to maximize the anabolic response to low-load BFR training when compared with 90% arterial occlusion, with444

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out the greater discomfort that was observed with 90% arterial occlusion. Limitations. In view of the results presented, this study has some limitations. First, the training study had a relatively small sample size. However, mean changes in muscle size, strength, and endurance were similar between arms, which suggests that the similar change between pressures was unlikely due to a statistical power issue. Further, the acute data presented here, along with a previous study,12 corroborate the finding that higher relative pressures may not augment muscle adaptation. Our estimate of muscle growth was muscle thickness and not the “gold standard” estimate from magnetic resonance imaging, although previous studies indicated a strong relationship between ultrasound estimates and more sophisticated measures.27–29 Regardless, the significant increases in biceps brachii thickness exceeded the error of our blinded tester (minimal difference), which gives confidence to the results. In addition, post-exercise muscle thickness measurements were taken 48–72 h after exercise despite previous data suggesting that swelling from upper body exercise lasts less than 24 h.30 A final potential limitation could be the cross-education of strength from one limb to the other; however, it has been noted previously that the cross-education effect is minimal or nonexistent when both limbs are training with different protocols.14 In conclusion, these findings indicate that muscle activation is not affected to a large degree by relative differences in applied pressure. Furthermore, we found that low-load exercise in combination with either 40% or 90% arterial occlusion produced similar increases in muscle size, strength, and endurance. In addition, the higher pressure condition produced indicated higher ratings of discomfort throughout the training program. Based on these preliminary data, we suggest that higher relative pressures may not be necessary with lowload resistance training in combination with BFR. REFERENCES 1. Loenneke JP, Wilson JM, Marin PJ, Zourdos MC, Bemben MG. Low intensity blood flow restriction training: a meta-analysis. Eur J Appl Physiol 2012;112:1849–1859. 2. Loenneke JP, Abe T, Wilson JM, Thiebaud RS, Fahs CA, Rossow LM, et al. Blood flow restriction: an evidence based progressive model (review). Acta Physiol Hung 2012;99:235–250. 3. Scott BR, Loenneke JP, Slattery KM, Dascombe BJ. Exercise with blood flow restriction: an updated evidence-based approach for enhanced muscular development. Sports Med 2015;45:313–325. 4. Loenneke JP, Wilson JM, Wilson GJ, Pujol TJ, Bemben MG. Potential safety issues with blood flow restriction training. Scand J Med Sci Sports 2011;21:510–518. 5. Loenneke JP, Thiebaud RS, Abe T. Does blood flow restriction result in skeletal muscle damage? A critical review of available evidence. Scand J Med Sci Sports 2014;24:e415–422. 6. Suga T, Okita K, Takada S, Omokawa M, Kadoguchi T, Yokota T, et al. Effect of multiple set on intramuscular metabolic stress during low-intensity resistance exercise with blood flow restriction. Eur J Appl Physiol 2012;112:3915–3920.

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7. Yasuda T, Abe T, Brechue WF, Iida H, Takano H, Meguro K, et al. Venous blood gas and metabolite response to low-intensity muscle contractions with external limb compression. Metabolism 2010;59: 1510–1519. 8. Sugaya M, Yasuda T, Suga T, Okita K, Abe T. Change in intramuscular inorganic phosphate during multiple sets of blood flow-restricted low-intensity exercise. Clin Physiol Funct Imaging 2011;31:411–413. 9. Loenneke JP, Fahs CA, Wilson JM, Bemben MG. Blood flow restriction: the metabolite/volume threshold theory. Med Hypotheses 2011; 77:748–752. 10. Cook SB, Clark BC, Ploutz-Snyder LL. Effects of exercise load and blood-flow restriction on skeletal muscle function. Med Sci Sports Exerc 2007;39:1708–1713. 11. Fahs CA, Loenneke JP, Thiebaud RS, Rossow LM, Kim D, Abe T, et al. Muscular adaptations to fatiguing exercise with and without blood flow restriction. Clin Physiol Funct Imaging 2015;35:167–176. 12. Loenneke JP, Kim D, Fahs CA, Thiebaud RS, Abe T, Larson RD, et al. Effects of exercise with and without different degrees of blood flow restriction on torque and muscle activation. Muscle Nerve 2015;51:713–721. 13. Burd NA, West DW, Staples AW, Atherton PJ, Baker JM, Moore DR, et al. Low-load high volume resistance exercise stimulates muscle protein synthesis more than high-load low volume resistance exercise in young men. PLoS One 2010;5:e12033. 14. Mitchell CJ, Churchward-Venne TA, West DW, Burd NA, Breen L, Baker SK, et al. Resistance exercise load does not determine trainingmediated hypertrophic gains in young men. J Appl Physiol 2012;113: 71–77. 15. van Roie E, Delecluse C, Coudyzer W, Boonen S, Bautmans I. Strength training at high versus low external resistance in older adults: effects on muscle volume, muscle strength, and force-velocity characteristics. Exp Gerontol 2013;48:1351–1361. 16. Yasuda T, Fukumura K, Uchida Y, Koshi H, Iida H, Masamune K, et al. Effects of low-load, elastic band resistance training combined with blood flow restriction on muscle size and arterial stiffness in older adults. J Gerontol A Biol Sci Med Sci 2015;70:950–958. 17. Yasuda T, Loenneke JP, Thiebaud RS, Abe T. Effects of blood flow restricted low-intensity concentric or eccentric training on muscle size and strength. PLoS One 2012;7:e52843. 18. Baechle TR, Earle RW. Essentials of strength training and conditioning. Champaign, IL: Human Kinetics; 2000.

Relative BFR Pressure

19. Loenneke JP, Thiebaud RS, Fahs CA, Rossow LM, Abe T, Bemben MG. Blood flow rest iction does not result in prolonged decrements in torque. Eur J Appl Physiol 2013;113:923–931. 20. Takarada Y, Takazawa H, Sato Y, Takebayashi S, Tanaka Y, Ishii N. Effects of resitance exercise combined with moderate vascular occlusion on muscular function in humans. J Appl Physiol 2000;88:2097– 2106. 21. Yasuda T, Brechue WF, Fujita T, Sato Y, Abe T. Muscle activation during low-intensity mucle contractions with varying levels of external limb compression. J Sports Sci Med 2008;7:467–474. 22. Yasuda T, Loenneke JP, Ogasawara R, Abe T. Influence of continuous or intermittent blood flow restriction on muscle activation during low-intensity multiple sets of resistance exercise. Acta Physiol Hung 2013;100:419–426. 23. Yasuda T, Fukumura K, Iida H, Nakajima T. Effect of low-load resistance exercise with and without blood flow restriction to volitional fatigue on muscle swelling. Eur J Appl Physiol 2015;115:919–926. 24. Loenneke JP, Fahs CA, Rossow LM, Thiebaud RS, Mattocks KT, Abe T, et al. Blood flow restriction pressure recommendations: a tale of two cuffs. Front Physiol 2013;4:249. 25. Martin-Hernandez J, Marin PJ, Menendez H, Ferrero C, Loenneke JP, Herrero AJ. Muscular adaptations after two different volumes of blood flow-restricted training. Scand J Med Sci Sports 2013;23:e114– 120. 26. Loenneke JP, Thiebaud RS, Abe T, Bemben MG. Blood flow restriction pressure recommendations: the hormesis hypothesis. Med Hypotheses 2014;82:623–626. 27. Kawakami Y, Abe T, Fukunaga T. Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles. J Appl Physiol 1993;74:2740–2744. 28. Koskelo EK, Kivisaari LM, Saarinen UM, Siimes MA. Quantitation of muscles and fat by ultrasonography: a useful method in the assessment of malnutrition in children. Acta Paediatr Scand 1991;80:682– 687. 29. Dupont AC, Sauerbrei EE, Fenton PV, Shragge PC, Loeb GE, Richmond FJ. Real-time sonography to estimate muscle thickness: comparison with MRI and CT. J Clin Ultrasound 2001;29:230–236. 30. Thiebaud RS, Yasuda T, Loenneke JP, Abe T. Effects of low-intensity concentric and eccentric exercise combined with blood flow restriction on indices of exercise-induced muscle damage. Interv Med Appl Sci 2013;5:53–59.

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Influence of relative blood flow restriction pressure on muscle activation and muscle adaptation.

The aim of this study was to investigate the acute and chronic skeletal muscle response to differing levels of blood flow restriction (BFR) pressure...
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