Neuromuscular Adaptations To Low-Load Blood Flow Restricted Resistance Training
Neuromuscular Adaptations To Low-Load Blood Flow Restricted Resistance Training
Neuromuscular Adaptations To Low-Load Blood Flow Restricted Resistance Training
http://www.jssm.org
` Research article
Summer B. Cook 1, Brendan R. Scott 2, Katherine L. Hayes 1 and Bethany G. Murphy 1
1
Department of Kinesiology, University of New Hampshire, Durham, NH, USA
2
School of Psychology and Exercise Science, Murdoch University, Perth, Western Australia
Received: 29 September 2017 / Accepted: 28 November 2017 / Published (online): 01 March 2018
Cook et al. 67
more novel and innovative studies directly comparing the neural adaptations were assessed via isometric knee exten-
neuromuscular effects of low-load BFR and moderate load sions, the LE was considered the primary training stimulus
(ML) training are warranted. Understanding how central in this study, while the leg press was used to provide sup-
activation and peripheral neuromuscular factors, such as plementary overload for the knee extensors.
twitch torque and rate of torque development and relaxa- At each training session, participants completed 3
tion, change after both types of training is needed to de- sets of bilateral LE and leg press in a random order, with
scribe the overall effects on muscular function. Therefore, 30 s of rest between sets and 180 s between exercises. Par-
the purpose of this study was to compare central and pe- ticipants in the ML group trained with a load of 70% 1-RM
ripheral neuromuscular adaptations and cross-sectional for 2 sets of 10 repetitions before performing the third set
area (CSA) changes following 6 weeks of ML or BFR to failure. Participants in the BFR group performed 2 sets
training on the knee extensor muscles and to evaluate the of 25 repetitions and a third set to failure using 20% 1-RM.
impact of these training regimens on muscular strength. It Exercise failure was defined as an inability to maintain the
was hypothesized that muscle strength and CSA would in- specified rate of contractions (2 s concentric and 2 s eccen-
crease in both types of training and that central neuromus- tric) or an inability to maintain full range of motion for two
cular adaptations would be more prominent in the HL train- consecutive contractions. In the BFR condition, partici-
ing regimen. pants performed the exercise with specially-designed tour-
niquet cuffs (54 mm wide; KAATSU Master Mini, Sato
Methods Sports Plaza, Tokyo, Japan) applied to the proximal thighs
at a suprasystolic pressure. The cuff pressure ranged from
Participants 180 mmHg to 200 mmHg. The BFR was maintained con-
Eighteen healthy, untrained men and women aged 18-22 tinuously throughout each exercise, including inter-set rest
years participated in this study (Table 1). They were clas- periods, but was released between the exercises. The par-
sified as moderately active according to the Lipid Research ticipants in the CON group were asked to not engage in any
Clinics Physical Activity Questionnaire (Ainsworth et al., exercise throughout the duration of the study. This was
1993) though they were not currently participating in re- confirmed through weekly visits with the researchers to en-
sistance training of the legs and did not report engaging in sure no other exercise was being undertaken.
structured exercise within the last three months. Partici- The loads used during training were determined
pants gave their written informed consent and the study during 1-RM testing (explained in detail below) and re-
was approved by the local Institutional Review Board. In- mained consistent throughout the training program, with
dividuals with orthopedic limitations of the legs, a history progressive overload achieved via increases in the number
of cardiovascular disease, a history or risk of abnormal of repetitions performed to failure. However, an unfore-
blood clotting or who were smokers were excluded from seen limitation of this exercise protocol was that several
participation. participants in the BFR condition did not reach volitional
failure in the leg press within 20 minutes, possibly because
Experimental design of contributions from the non-restricted gluteal muscles.
The duration of the study was 8 weeks, with pre- and post- To limit potential negative effects associated with pro-
training measurements collected one week prior to and fol- longed BFR such as bruising, numbness and lightheaded-
lowing 6 weeks of resistance training using bilateral leg ex- ness (Clark et al. 2011), these participants ceased exercise
tension (LE) and leg press exercises. Upon entering into after 20-minutes. Importantly though, all participants did
the study, the participants underwent familiarization ses- reach fatigue for all sessions with the primary LE exercise.
sions and baseline measures of leg strength, muscle vol-
ume, and neuromuscular function. Using a stratified ran- Neuromuscular measurements
domization based on sex, the participants were assigned to Knee extensor peak torque: Maximum isometric torque of
one of 3 groups: ML, BFR, or a non-exercising control the knee extensors on the dominant leg was measured from
group (CON). Measurements to quantify neuromuscular each subject on a HUMAC Norm dynamometer (CSMI,
adaptations to exercise were obtained at baseline and fol- Stoughton, MA, USA) with analog output that was sam-
lowing the intervention approximately 48 hours post-train- pled using the BIOPAC MP150 data acquisition system
ing. (AcqKnowledge 4.1 software; BIOPAC Systems Inc., CA,
USA). To obtain peak torque, participants were seated in
Training protocols the dynamometer at a hip angle of 85° with the torso se-
Resistance training was performed using seated LE and cured by a seat belt preventing hip movements during tri-
horizontal leg press machines (Nautilus Nitro, Med-Fit als. Participants’ knee angle was set at 60° and they were
Systems, Independence, VA). Considering that several instructed to extend the knee with as much force against an
Table 1. Descriptive statistics of the study sample. Values are means ± (SD).
ML BFR Control
Men (n =3) Women (n =3) Men (n =3) Women (n =3) Men (n =3) Women (n =3)
Age (yr) 19.3 (1.2) 21 (0.0) 19.0 (1.0) 19.7 (1.5) 19.7 (1.5) 21 (1.0)
Stature (m) 1.73 (.02) 1.62 (.10)* 1.79 (.12) 1.66 (.07)* 1.74 (.03) 163 (.10)*
Mass (kg) 74.5 (9.8) 54.6 (5.8)* 74.9 (6.9) 64.0 (13.1)* 67.0 (4.9) 67.9 (9.8)*
* indicates significant difference between men and women (p < 0.05). ML: moderate-load, BFR: blood flow restricted.
68 Blood flow restricted resistance training
immovable pad of the dynamometer for 3-5 s. This was using the National Institutes of Health ImageJ software
repeated 3-5 times until the difference in peak torque be- (Abramoff et al., 2004). The vasti muscles (lateralis, medi-
tween two trials was within 5%. Participants rested 1-2 alis, and intermedius) and the rectus femoris on the right
minutes between all attempts. Standardized and consistent leg were identified and traced. Slices between the identifi-
verbal encouragement was provided to all subjects. cation of the distal rectus femoris and the appearance of the
Electrically evoked torque: Measurements of elec- femoral neck were located and traced to quantify the quad-
trically evoked contraction torques were elicited on the riceps femoris. The same number of slices from the same
dominant leg by transcutaneous stimulation of the femoral anatomical locations was analyzed for each participant at
nerve using a hand-held cathode probe placed in the ingui- pre- and post-training by the same investigator. Volume
nal triangle. When the highest isometric twitch torque pro- was calculated as the sum of the measured slices with con-
duced from the stimulation with the probe was determined, sideration of interslice gaps.
a surface electrode (Ag-AgCl, 36 mm diameter; Kendall One repetition maximum (1-RM) testing: Bilateral
MediTrace 200) was placed over the skin and used for sub- 1-RM on the seated LE and leg press machines were meas-
sequent stimulations. An anode was placed on the skin over ured using the procedures described by Baechle and Earle
the greater trochanter (Ag-AgCl, 48 mm diameter; Kendall (2008). Two to four minutes of rest was given between at-
MediTrace 530). The stimulus consisted of a 1 ms rectan- tempts and the 1-RM measurements were determined
gular pulse with 400-V maximum voltage (Digitimer con- within 4-6 attempts. Six male participants were able to lift
stant current stimulator model DS7AH coupled with the the weight stack on the machines at pre-training and/or
train/delay generator, Hertfordshire, UK). Supramaximal post-training and in such instances, the number of repeti-
stimulation was achieved by increasing the stimulus inten- tions performed at the maximum weight of the machine
sity 10% beyond that required to elicit peak twitch torque. (116 kg) was performed and the 1-RM was then predicted
Doublet (interpulse duration was 6 ms apart) torques and using the Brzycki equation (Brzycki, 1993). The 1-RM
post activation potentiated torque were measured and rec- scores were used to prescribe exercise load for the training
orded on the HUMAC Norm dynamometer that was inter- protocols and the LE 1-RM was used to evaluate strength
faced with the BIOPAC MP150 data acquisition system. improvements from training.
Central activation: Voluntary activation of the knee
extensors was assessed using the interpolated twitch tech- Statistical analysis
nique as previously described (Clark et al., 2007). After Because of the paucity of data regarding the neuromuscular
evoked torque was measured, participants performed a 4-5 measurements assessed in this study, the sample size cal-
s isometric maximum voluntary contractions. During that culation was powered to detect significance between three
time, a supramaximal doublet was delivered to the femoral groups with respect to knee extension strength based on the
nerve and again within 1-2 s after the completion of the effect size determined from data presented by Karabulut et
isometric contraction. The last supramaximal stimulus was al. (2010). The parameters used for this model were an ef-
the post activation potentiated doublet. The increase in fect size = 0.53, at a power = 0.9 and a specified alpha =
torque following the initial doublet was expressed to the 0.05.
post activation potentiated doublet and expressed as fol- Data are expressed as means and standard devia-
lows: tions. Reliability of the dependent variables has been re-
ported previously with intraclass correlations ranging from
%Central Activation = 1 – (doublet torque during isometric contraction 0.7-0.99 (Cook et al. 2014). Box plots were used to exam-
÷ post activation potentiated double torques) x 100 ine the data distribution. Multivariate analysis of variance
(MANOVA) was used to compare the groups at pre-train-
Contractile properties: To identify changes in the ing for all dependent variables simultaneously. A two-way
functional contractile properties of the knee extensors, the repeated measures analysis of variance (ANOVA) proce-
torque-time curve from the post activation potentiated dure was used to detect differences in the dependent varia-
torque was evaluated. Peak torque, time to peak torque and bles with respect to the within-subjects independent varia-
time to half-relaxation was calculated. ble (pre-training vs post-testing) and the between subjects
factor (ML, BFR, CON). Significant interactions and main
Muscle size and dynamic strength effects were followed with appropriate post hoc tests, in-
Muscle volume: To quantify changes in muscle mass, serial cluding Tukey post hoc tests or paired t-tests with Bonfer-
axial plane magnetic resonance imaging scans (10 mm roni adjustments. Cohen’s d were computed and effect
slice thickness, 15 mm apart, 2120 ms repetition time) were sizes were categorized as small (0.10), medium (0.50), or
acquired from both upper legs using a 1.5 Tesla Siemens large (0.80) (Cohen, 1988). These values were used to
Espree Scanner (Siemens Medical Systems, Erlangen, Ger- compare the training adaptations between training groups.
many) with a receiver body array coil and a field of view An alpha level of ≤ 0.05 was required for statistical signif-
of 420 mm. These scans were obtained between 48 and 72 icance. Statistics were computed using SPSS Statistics ver-
hours after completion of any exercise and testing sessions. sion 22.0 (Chicago, IL).
After a 30 minute supine rest period to allow for fluid equi-
libration, cross-sectional images from the femoral greater Results
trochanter to the patella were obtained. An average of 11 ±
2 slices was used for analysis. The digitized images were The age, mass and stature of the men and women were sim-
transferred to a computer for calculation of muscle volume ilar within the three training groups (p > 0.05), but there
Cook et al. 69
was a significant main effect of sex indicating that the BFR condition and 3.4 ± 0.4 minutes for the ML condition
males were taller and heavier than the females (Table 1; p and was significantly different between the groups (p <
< 0.05). There were no significant differences between the 0.05).
groups at pre-training when all dependent variables were Figure 2 depicts box plots of percent change in iso-
simultaneously considered (p = 0.78). There was 100% metric torque, LE 1-RM and muscle volume following the
subject compliance in the training sessions. The partici- training regimens and Table 2 depicts corresponding effect
pants in the BFR training condition lifted an average load sizes. Isometric peak torque of the knee extensors was sta-
of 68 ± 41 kg on the LE at each session and always per- tistically similar among the three groups prior to training
formed significantly more repetitions in the exercise ses- (p = 0.15) and did not significantly change following 6-
sion than the participants in the ML training group (average weeks of resistance training (p = 0.13; d range = 0.09 -
load = 136 ± 50 kg; p < 0.01) (Figure 1). The ML training 0.44; Fig.2a, Table 2).There was a significant time x group
group significantly increased the average number of repe- interaction (p = 0.02) in the LE 1-RM that indicated signif-
titions per session performed in each exercise session from icant improvements in the ML (34%; p = 0.02; d = 0.78)
week 1 to weeks 4, 5 and 6 (p < 0.01) while the BFR group and BFR (13%; p = 0.01; d = 0.67) groups and no change
had greater variability in the average number of repetitions in the CON group (1.5%; p = 0.64; d = 0.07; Figure 2b,
per session completed and only experienced a significant Table 2). There was a significant time x group interaction
increase from week 1 to week 6 (p < 0.05). Accordingly, (p = 0.02) in knee extensor volume as there was an increase
LE exercise volume at the end of the study was signifi- of 5.6% in the ML group (p = 0.02; d = 0.19) and 2.5% in
cantly higher in the BFR group than the ML group (12,250 the BFR group (p = 0.03; d = 0.09) but no change in the
± 4971 kg vs 5466 ± 2201 kg, respectively) (p < 0.05). The CON group (p = 0.96; d = 0.00; Figure 2c, Table 2).
average duration of training was 11.6 ± 4.6 minutes for the
Figure 1. The mean+ standard deviation leg extension (LE) repetitions performed at the weekly sessions of moderate-load
(ML) and low-load blood flow restricted (BFR) resistance training. * denotes significant increase from Week 1 in the number of repeti-
tions performed (p < 0.05).
Table 2. Pre and post strength values and effect sizes for all training programs. Values are mean ± (SD).
ML BFR Control
Pre Post d Pre Post d Pre Post d
Isometric Torque (Nm) 203 (64) 238 (92) .44 273 (58) 267 (55) .11 227 (53) 232 (60) .09
LE 1-RM (kg) 88 (32) 118 (44)* .78 116 (21) 131 (24)* .67 124 (30) 126 (38) .07
Muscle Volume (cm3) 1690 (464) 1785 (528)* .19 1952 (539) 2001 (531)* .09 1945 (384) 1945 (389) .00
* indicates significant difference from Pre (p < 0.05). ML: moderate-load, BFR: blood flow restricted, d: Cohen’s d, LE 1-RM: leg extension
one repetition maximum
Table 3. Neuromuscular measurements before and after 6-weeks of moderate-load (ML) or low-load blood flow re-
stricted (BFR) resistance training. Values are means (±SD).
ML BFR Control
Pre Post d Pre Post d Pre Post d
Twitch Torque (Nm) 43 (11) 42 (5) -.35 55 (20) 55 (21) .00 41 (12) 43 (11) .17
Doublet Torque (Nm) 55 (11) 63 (9) .80 75 (26) 79(33) .13 62 (16) 65 (11) .22
PAP Torque (Nm) 67 (24) 66 (16) -.05 85 (31) 90 (38) .14 65 (22) 67 (17) .10
CAR (%) 86 (9) 89 (8) .35 97 (2) 95 (3) -.78 93 (12) 93 (8) .00
TPT (ms) 50 (8) 56 (9) .70 52 (11) 54 (8) .21 58 (16) 63 (20) .28
HRT (ms) 139 (54) 137 (58) -.04 143 (46) 192 (68) .84 125 (49) 104 (46) -.44
ML: moderate-load, BFR: blood flow restricted, d: Cohen’s d, CAR: central activation ratio, PAP: post-activation potentiated doublet
torque, TPT: time to peak torque, HRT: half-relaxation time. Pre is at 0 weeks of training and post is after 6 weeks of training.
70 Blood flow restricted resistance training
research, Clark et al. (2011) found no changes in nerve con- neural adaptations assessed through isometric contractions.
duction velocity before and after four weeks of BFR re- To illustrate, Sale et al. (1992) reported increases in 1-RM
sistance training and resistance training at 80% of maxi- strength and cross-sectional area following 10 weeks of el-
mum strength. Brandner et al. (2015) has recently reported bow flexor training despite no changes in isometric
on enhanced corticomotor excitability following one ses- strength and twitch torque. They attributed the improve-
sion of BFR training. It is important to consider that the ment in 1-RM to neural factors related to coordination and
present study was not powered for improvements in central learning, such as a decrease in agonist and antagonist acti-
activation and the participants in the study were healthy, vation, and suggested the possibility that early increases in
moderately-active, untrained, young adults that already muscle mass may not necessarily contribute significantly
possessed high levels of quadriceps muscle activation. to the enhanced strength.
Furthermore, there were no significant changes in There are some limitations to our study that should
peripheral nerve and contractile function observed in our be addressed. Firstly, the sample size for this study was
study with evoked torque, time to peak torque, and half- based on effect sizes from knee extension strength im-
relaxation time remaining constant across all groups. Sim- provements of a previous study as the neuromuscular as-
ilar to our findings, Ishida et al. (1990) reported strength sessments employed in this study have not previously been
improvements following 8-weeks of moderate-to-high load investigated. Because of the intricacies of measurements,
training on the plantar-flexors but could not attribute the we believe this small-scale study provides substantial in-
strength gains to enhanced contractile function as twitch sight and direction into future BFR studies. A second lim-
torque and rates of torque development and relaxation re- itation to this study is that the training loads were not pro-
mained constant. There was a tendency for half-relaxation gressed and it is likely that by the study’s conclusion par-
time to slow in the BFR group (34%; d=.84). This is an ticipants were exercising at lower relative load. However,
interesting finding to further explore as the muscle contrac- this was addressed by having all participants exercise to
tile processes depend on Ca2+ sensitivity and efficiency of volitional failure, which has been shown as a valid method
Ca2+ movement into and out of the sarcoplasmic reticulum. to induce progressive overload, particularly at light loads
It is known that fast-twitch and slow-twitch muscle fibers (Burd et al., 2012; Cook et al., 2007). A final limitation in
differ in the number and size of sarcoplasmic reticulum this study is that it assesses strength and hypertrophic ad-
Ca2+ pumps, such that the slow-twitch fibers have a lower aptations following ML and BFR resistance exercise in un-
rate of Ca2+ uptake, resulting in slower half-relaxation time trained males and females. While males and females en-
(Stephenson et al., 1998). Nielsen et al. (2017) reported a gage in BFR training, the inclusion of mixed-gender
delayed adaptation to BFR exercise as improvements in groups may have obscured some findings since women
muscle function were not apparent until twelve days upon have demonstrated greater endurance during BFR exercise
completion of a training program. It is possible that a tran- than males (LaBarbera, et al., 2013). Also, the magnitude
sient impairment in contractile function following BFR ex- of adaptations apparent in our study may not be as promi-
ercise persisted through the exercise testing 48 hours after nent in individuals that already possess high levels of mus-
the completion of training. cle strength and mass due to regular resistance training.
The current study was unable to replicate the find-
ings of Moore et al. (2004) who noted a depressed resting Conclusions
twitch torque and an augmented post activated potentiated
twitch torque following low-load BFR exercise in the bi- Our results demonstrate significant gains in muscular size
ceps. A decline in resting twitch torque following a training and strength following six weeks of ML and low-load BFR
regimen would indicate a negative adaptation that the au- training, with ML training appearing to show greater mag-
thors speculated could be related to low-frequency fatigue. nitudes of adaptation in a more efficient and timely manner
It is interesting to note that the ML training group showed in each exercise session. There were no significant changes
a non-significant increase in doublet torque accompanied in central and peripheral neuromuscular function yet mod-
by a high effect size (d = 0.80) perhaps signifying a possi- erate-to-large effect sizes in central activation and evoked
ble adaptation not evident following BFR training. Moore torque suggest that further study on the neuromuscular var-
et al. (2004) also suggested that the increase in post activa- iables is necessary. This study has implications for several
tion potentiated torque following BFR training, which can clinical populations who would benefit from gains in mus-
be considered a positive adaptation that allows muscles to cle size and strength but cannot tolerate the mechanical
generate more force during submaximal activities, was strain associated with lifting heavy loads. BFR resistance
possibly a compensatory mechanism in response to the de- training may be a suitable modality of resistance exercise
pressed twitch torque. In the present study, PAP increased until moderate-to-high load resistance training is achieva-
non-significantly with a small effect size (d = 0.14), sug- ble.
gesting more research into this concept.
It is important to note that the central and peripheral Acknowledgements
This work was supported by the American College of Sports Medicine
neuromuscular measurements in our study were conducted Foundation for KAATSU Research. This study was approved by the Uni-
during isometric contractions. The overall strength in- versity of New Hampshire Institutional Review Board (IRB #4738) and
creases observed in the present study are specific to the conforms to the Declaration of Helsinki. The experiments comply with
the current laws of the country in which they were performed. The authors
training mode of isotonic contractions and the lack of have no conflict of interest to declare.
significant change in isometric muscle strength may mask
72 Blood flow restricted resistance training
AUTHOR BIOGRAPHY
Summer B. COOK
Employment
Associate Professor, Department of Ki-
nesiology, University of New Hamp-
shire
Degree
PhD
Research interest
Neuromuscular function, aging and
blood flow restricted exercise.
E-mail: [email protected]
Brendan R. SCOTT
Employment
Lecturer in Strength and Conditioning,
School of Psychology and Exercise Sci-
ence, Murdoch University, AUS.
Degree
PhD
Research interest
Resistance training methods, athlete
monitoring
E-mail: Brendan.Scott@mur-
doch.edu.au
Katherine L. HAYES
Employment
Postdoctoral associate at the University
of Massachusetts Medical School
Degree
PhD
Research interest
Effect of exercise on stem cells in
healthy and diseased conditions
E-mail: [email protected]
Bethany G. MURPHY
Employment
Clinical Instructor at the Birchtree Cen-
ter, Portsmouth, NH
Degree
BSc
Research interest
Exercise and health
E-mail: [email protected]