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Lundberg Laboratory for Human Muscle Function and Movement Analysis, Department of Orthopaedics, the Sahlgrenska
Academy at University of Gothenburg, Gothenburg, Sweden

ABSTRACT rehabilitation settings when large forces are contraindicated.

Wernbom, M, Järrebring, R, Andreasson, MA, and Augustsson, J. However, similarly to fatiguing blood flow restricted exercise, this
Acute effects of blood flow restriction on muscle activity and method is associated with ischemic muscle pain, and thus its
endurance during fatiguing dynamic knee extensions at low applications may be limited to highly motivated individuals.
load. J Strength Cond Res 23(8): 2389–2395, 2009—The KEY WORDS strength training, ischemia, vascular occlusion,
purpose of this study was to investigate muscle activity and blood flow restricted exercise, muscle hypertrophy, muscle
endurance during fatiguing low-intensity dynamic knee extension activation
exercise with and without blood flow restriction. Eleven healthy
subjects with strength training experience performed 3 sets of
unilateral knee extensions with no relaxation between repetitions

to concentric torque failure at 30% of the 1 repetition maximum. n the last 8 to 10 years, low-load training with blood
One leg was randomized to exercise with cuff occlusion and the flow restriction has attracted a lot of attention, both as
other leg to exercise without occlusion. The muscle activity in the a possible alternative to heavy resistance exercise in
the rehabilitation setting and as a training method to
quadriceps was recorded with electromyography (EMG).
increase muscle strength and size in healthy individuals.
Ratings of perceived exertion (RPE) and acute pain were col-
Several studies have shown that blood flow restriction by
lected immediately, and delayed onset muscle soreness
pressure cuffs in combination with low-intensity resistance
(DOMS) was rated before and at 24, 48, and 72 hours after exercise induces muscle mass increases at rates comparable
exercise. The results demonstrated high EMG levels in both with those seen with conventional strength training (17,26–
experimental conditions, but there were no significant differ- 28) and sometimes at even higher rates (2,12). In the studies
ences regarding maximal muscle activity, except for a higher that have included control groups that have trained at the
EMG in the eccentric phase in set 3 for the nonoccluded same intensities and volumes but without cuff occlusion, the
condition (p = 0.005). Significantly more repetitions were per- nonoccluded groups have generally made little if any gains in
formed with the nonoccluded leg in every set (p , 0.05). The muscle size and strength (1,2,12,27,28).
RPE and acute pain ratings were similar, but DOMS was higher However, because vascular occlusion reduces the muscle
in the nonoccluded leg (p , 0.05). We conclude that blood flow endurance at the low-to-moderate loads typically used in
training with blood flow restriction (33), and because the
restriction during low-intensity dynamic knee extension de-
occlusion has usually been applied continuously (including
creases the endurance but does not increase the maximum
rest periods) throughout the training session, the effort
muscle activity compared with training without restriction when
required to complete a given amount of work in an exercise
both regimes are performed to failure. The high levels of muscle bout should be substantially less with free flow conditions.
activity suggest that performing low-load dynamic knee exten- Therefore, one might argue that previous studies have not
sions in a no-relaxation manner may be a useful method in knee controlled for the degree of effort when comparing training
with and without cuff occlusion. Furthermore, it has been
Address correspondence to Mathias Wernbom, mathias.wernbom@ reported that there was little difference in the acute pain ratings between the occluded and nonoccluded legs when
23(8)/2389–2395 dynamic knee extensions were performed in a continuous
Journal of Strength and Conditioning Research nonstop manner to fatigue, indicating that ischemic
Ó 2009 National Strength and Conditioning Association conditions were induced by the exercise itself (33). Therefore,

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Muscle Activity and Endurance During Fatiguing Dynamic Knee Extensions

the purpose of this study was to investigate whether there Procedures

were any differences in muscle activity, as measured by Strength Testing and Familiarization. One week before the main
electromyography (EMG), and endurance during low- test, the subjects were tested for their unilateral 1RM strength
intensity dynamic knee extension exercise performed to for each leg in a variable resistance knee extension machine
fatigue with and without cuff occlusion. (Leg Extension FL130, Competition Line, Borås, Sweden).
Because the participants were all familiar with the dynamic
METHODS knee extension exercise, only 1 session was devoted to
strength testing. The 1RM was determined according to the
Experimental Approach to the Problem
procedures of Staron et al. (22). After the 1RM for each leg
To examine the effects of blood flow restriction on muscle had been established, the subjects practiced maximum
activity and endurance during dynamic knee extensions, isometric efforts in the same knee-extension machine, with
a within-subjects study design was used in which 1 leg the lever arm of the machine fixed at an angle corresponding
(dominant or nondominant) was tested with cuff occlusion, to 70° of knee flexion (full knee extension is here defined as
and the other leg was tested without occlusion in a random- 0°). After 5 minutes of rest, a load of 30% of 1RM was chosen,
ized fashion. The order of the conditions (with or without and the subject was familiarized with the partial blood flow
cuff occlusion) was also randomized. All subjects participated restriction and the cadence of repetitions to be used during
in a familiarization session (1 repetition maximum [1RM] the main test. A curved tourniquet cuff of 135 mm in width
testing, practice of maximal isometric efforts for EMG with a 100 mm wide pneumatic bag inside of it was
normalization, and dynamic knee extensions combined with connected to a surgical tourniquet system (Zimmer A.T.S.
vascular occlusion) 1 week before the main experiment. 2000, Zimmer Patient Care, Dover, OH, USA) with
Normalization of the EMG amplitude with respect to the automatic regulation of the pressure. The cuff was wrapped
EMG obtained during a maximal isometric activation was around the proximal part of the thigh and inflated to
performed to provide an index of the level of neuromuscular a pressure of 100 mm Hg just before exercise with partial
activation during the exercises and also because this occlusion and kept inflated during the rest periods in between
procedure increases the reliability of the measurements (4). the sets. For each leg, 1 set of knee extensions to concentric
torque failure was performed with cuff occlusion, followed by
Subjects a second set of 5 repetitions after 45 seconds of rest, during
Eleven healthy persons (8 men and 3 women, 20–39 yr of age) which the partial occlusion was maintained. This was done to
volunteered for the study (Table 1). All participants had confirm that the subjects tolerated the pressure to be used
several years of experience with strength training. Some of during the main experiment 1 week later.
the subjects were track and field athletes (sprinters and
jumpers) and soccer players, and the others trained for their Endurance Testing. At a subsequent session after the 1RM
own strength and conditioning purposes, but none competed testing, with 6 to 10 days between the sessions, the subjects
in strength sports. From a strength point of view, the subjects were tested for their endurance in the unilateral knee
were classified as ‘‘trained’’ on the continuum between extension exercise at 30% of 1RM. The same tourniquet
untrained and elite, as outlined by Deschenes and Kraemer system as in the familiarization session was used and inflated
(10), and they were tested in the beginning of a new training to a pressure of 100 mm Hg just before exercise with cuff
year cycle. The participants were instructed not to train their occlusion, and this pressure was maintained for the occluded
quadriceps during the last 3 days before the main test. The leg during the exercise, including rest periods between sets.
subjects were informed of the experimental risks and signed After a warm-up, the subjects performed as many repetitions
an informed consent document before the investigation. The as possible for a total of 3 sets for each leg. The rest
study was approved by the Human Ethics Committee at the period between each set was 45 seconds for both the
Faculty of Medicine, University of Gothenburg, Sweden. nonoccluded and the occluded leg. The range of motion was
between 100° and 20° of knee flexion (0° = full extension), and
the cadence was 20 repetitions per minute (1.5 s each for the
TABLE 1. Subject characteristics. concentric and the eccentric muscle actions), which was
controlled with a metronome set at 40 beats per minute. No
n Mean SD rest was permitted between the repetitions, and the subjects
Men 8 were instructed to stop the eccentric phase just before
Women 3 the weight stack touched down to avoid relaxation of the
Age (yr) 25 5 quadriceps. The number of repetitions performed in each set
Height (cm) 178 10 was noted as a measure of endurance, and the muscle activity
Weight (kg) 77 13
during the exercise was measured by EMG, as described
below. After all 3 sets for the occluded leg had been
completed, the pressure cuff was deflated. The subjects
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remained seated in the machine during the rest periods other connected devices. The EMG was normalized to
between the sets. a maximum voluntary isometric activation (MVIA) using the
Continuous partial occlusion rather than intermittent normalization function of the MuscleLab unit. After a
severe occlusion was chosen because most of the previous warm-up with gradually increasing force developments, 2
studies have used a partial occlusion training model and MVIA trials were performed at a knee angle of 70°. The
because partial blood flow restriction is more tolerable than subjects were instructed to smoothly increase force, and once
severe or complete occlusion (8). Hoeger et al. (15) the maximum was reached, the effort was sustained for at
demonstrated a test-retest reliability of r = 0.86 to 0.96 for least 3 to 4 seconds, during which time EMG was collected
knee extension endurance tests at loads of between 40% and for normalization. Alkner et al. (3) reported a coefficient of
60% of 1RM when performed in a similar continuous fashion variation between trials for EMG to be in the range of
as in our study. Tagesson and Kvist (23) reported intraclass 4.7–9.2% for the MuscleLab system.
correlation coefficient values of 0.90 to 0.96 for the unilateral A display with the EMG RMS curve was placed in front
knee-extension 1RM test. of the leg extension machine for monitoring purposes and
to provide real-time feedback to the subject. Because the
Electromyography and Goniometry. The skin was shaved with normalization value was chosen automatically by the
a hand razor and carefully cleaned with ethanol before MuscleLab, the first of the 2 MVIA attempts was saved and
electrode placement. Bipolar surface self-adhesive Ag/AgCl used as the reference value (100%) if the 2 attempts did not
monitoring electrodes (model 2223, 3M Medical, Neuss, differ by more than approximately 5% in RMS amplitude, in
Germany) with a 4.0 cm interelectrode distance were placed which case further attempts were made until a plateau in
on the medial portion of the vastus lateralis (VL) and the amplitude was noted. During the 30% of 1RM endurance tests
vastus medialis (VM) muscles of the quadriceps femoris with and without occlusion, as in the MVIA trials, the EMG
muscle group approximately 15 and 10 cm above the RMS curve was displayed in real-time in front of the subject
proximal border of the patella. These placings were for motivation, and loud verbal encouragements were
somewhat similar to those used by Andersen et al. (4), and also used to motivate the subjects to continue to the point
they were chosen to avoid having the electrodes passing over of concentric torque failure. The average RMS values for
the innervation zones of the muscles during the exercise complete concentric and eccentric phases, respectively, were
movement while still leaving enough room for the used for analysis. The first repetition of each set was discarded
tourniquet. The approximate locations of the innervation because the subjects generally had not found the proper
zones were based on the anatomic guidelines provided by tempo. During the final 2 or 3 repetitions in each set, most
Rainoldi et al. (20). Knee joint angle was measured with an subjects also had difficulty following the correct tempo
electrogoniometer, which was positioned laterally to the because of the accumulating fatigue, but these repetitions
knee joint. Calibration of the goniometer signal was were considered for analysis as long as they were in the full
performed at anatomic knee joint angles of 0° and 90° using range of motion.
a geometric retractor. A linear encoder was used to measure
the position and displacement of the weight stack. The Ratings of Pain, Perceived Exertion, and Delayed Onset Muscle
goniometer and encoder data were used to identify the Soreness. The subjects were asked at the end of both the
concentric and eccentric
phases of each repetition.
The EMG and goniometer/
encoder data were collected
using the MuscleLab 3010e
recording and acquisition sys-
tem (Ergotest Technology,
Langesund, Norway), using
the accompanying software
program on a laptop computer
(3). The MuscleLab EMG leads
had built-in preamplifiers, and
the pre-amplified signal was
filtered through a 8 to 1,200
Hz band pass filter before it
was root mean square (RMS)
converted. The RMS converted Figure 1. Number of repetitions with and without partial occlusion. * = p , 0.05 between the nonoccluded and
signal was then sampled at 100 occluded conditions.
Hz and synchronized with the

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Muscle Activity and Endurance During Fatiguing Dynamic Knee Extensions

TABLE 2. Lowest and highest electromyographic (EMG) activation (% of maximum voluntary isometric activation [MVIA])
for complete concentric and eccentric phases for vastus medialis (VM) and vastus lateralis (VL) during occluded and
nonoccluded conditions, set 1 to 3 (means 6 SD).

Concentric EMG (% of MVIA) Eccentric EMG (% of MVIA)

Lowest Highest Lowest Highest Lowest Highest Lowest Highest

Occluded set 1 Nonoccluded set 1 Occluded set 1 Nonoccluded set 1

VM 34 6 10 101 6 22 37 6 12 107 6 24 24 6 8 50 6 13 26 6 8 57 6 18
VL 36 6 11 86 6 19 34 6 11 97 6 17 23 6 7 45 6 10 23 6 7 44 6 12
VM+VL 35 6 10 94 6 18 36 6 11 102 6 19 24 6 7 48 6 10 24 6 7 50 6 14
Occluded set 2 Nonoccluded set 2 Occluded set 2 Nonoccluded set 2
VM 73 6 18 98 6 27 72 6 22 107 6 27 29 6 9 52 6 16 32 6 9 61 6 16
VL 66 6 19 91 6 26 63 6 19 96 6 20 26 6 9 46 6 12 28 6 10 53 6 15
VM+VL 70 6 18 94 6 23 68 6 20 102 6 21 28 6 8 49 6 13 30 6 9 57 6 15
Occluded set 3 Nonoccluded set 3 Occluded set 3 Nonoccluded set 3
VM 77 6 21 93 6 23 78 6 21 102 6 20 34 6 11 47 6 12 37 6 12 64 6 17*
VL 70 6 19 85 6 24 67 6 19 93 6 24 31 6 10 40 6 11 33 6 13 53 6 15*
VM+VL 74 6 19 89 6 21 72 6 20 98 6 20 32 6 10 44 6 11 35 6 12 58 6 15*

*p , 0.05 between the nonoccluded and occluded conditions; n = 11.

occluded and the nonoccluded protocols to use the Borg RESULTS

CR-10 and ratings of perceived exertion (RPE) scales (6) to
Significant differences in the number of repetitions performed
rate the pain and perceived exertion in their quadriceps. The
were found between the occluded and the nonoccluded legs
10 on the Borg CR-10 pain scale was anchored as ‘‘the for each of the 3 sets and for all 3 sets combined (Figure 1). No
previously worst exercise-induced pain experienced in your differences in minimum and maximum muscle activity were
quadriceps,’’ and in line with the recommendations of Borg noted between the conditions, except for the third set, in
(6), the subjects were allowed to use even higher values (up to which the activation in the eccentric phase during the
12) if they thought that they had exceeded this during the repetitions with the highest activity was significantly greater
tests. Delayed onset muscle soreness (DOMS) was rated at in the nonoccluded leg (p = 0.005 for VL and VM combined)
24, 48, and 72 hours postexercise using the visual analog scale
(Table 2). Acute pain (Borg CR-10) and RPE ratings were not
(VAS). The 0 value for the VAS was designated as ‘‘no
soreness at all,’’ and the maximum value of 10 was ‘‘extreme
muscle soreness’’ (33).

Statistical Analyses TABLE 3. Median values and interquartile ranges for

Power analysis on data from pilot studies revealed that, to local perceived exertion (Borg rating of perceived
detect a 33% difference in the number of repetitions in the first exertion [RPE] 6–20 scale), pain (Borg CR-10), and
set, at least 7 participants were required to achieve a power delayed onset muscle soreness (DOMS; visual
analog 0–10 scale).
of 0.90. Differences in EMG activity and in the number of
repetitions between the occluded and the nonoccluded test Variables Occluded Nonoccluded
conditions were computed with paired t-tests, whereas
Borg RPE 18,9 (1,3) 19,0 (1,2)
comparisons regarding Borg RPE, Borg CR-10, and DOMS
CR-10 9,7 (2,1) 9,2 (1,5)
ratings were performed with the Wilcoxon signed rank test. DOMS (24 hr post) 2,9 (2,8) 4,0 (2,0)*
Means and SDs were calculated for EMG and for the number DOMS (48 hr post) 3,3 (2,8) 5,0 (2,5)*
of repetitions, whereas median and interquartile ranges were DOMS (72 hr post) 2,5 (2,4) 3,5 (4,1)*
computed for the Borg RPE, Borg CR-10, and DOMS ratings
*p , 0.05 between nonoccluded and occluded
(ordinal). Statistical Package for Social Science (SPSS, conditions; n = 11.
Chicago, IL, USA), version 14.0, was used for the analyses.
Significance was accepted at the alpha level of p # 0.05.
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significantly different between the conditions (Table 3). For occluded leg but also the nonoccluded leg were submitted to
DOMS, significantly greater ratings on the VAS scale were relative ischemia. We therefore suggest that because of the
noted for the nonoccluded leg (p , 0.05) (Table 3). ischemic conditions, the type I fibers became highly fatigued
during the first set, thus necessitating the recruitment of an
DISCUSSION increasing number of motor units containing type II fibers as
The major finding of the current study was that although the set progressed, as indicated by the increase in EMG
partial restriction of blood flow with a thigh tourniquet did (Table 2). In addition, the EMG data indicate that the type II
influence the endurance in the dynamic knee extension fibers were recruited earlier in the second and third sets
exercise at an intensity of 30% of 1RM, it did not increase the than in the first set, presumably because of residual fatigue in
maximum level of muscle activity in the quadriceps either in type I fibers.
the concentric or the eccentric phase compared with no cuff The gradual increase in the EMG during the eccentric
occlusion when both regimes were performed to the point of phase also deserves comment. During the first few repetitions
concentric torque failure. If anything, there was a tendency for of each set, the activity was low, as expected (approximately
greater activity in both of the vastus muscles during the 25–30% of MVIA), but as the point of concentric torque
nonoccluded condition for both the concentric and the failure drew nearer, the eccentric activity showed a marked
eccentric phases, which became significant for the eccentric increase, ending at levels of approximately 50–60% of MVIA,
phase in the third set. Generally, the lowest activity was seen which suggests the possibility that motor units containing fast
in the beginning of the sets and the highest during the last few fibers were increasingly recruited also during the eccentric
repetitions of each set, and this was true for both conditions phase. To the best of our knowledge, this increase in
and for both the concentric and the eccentric phases. Also, the activation during eccentric muscle actions has not been
muscle activity during the first repetitions, especially during reported before in the literature on training combined with
the concentric phases, was clearly greater during the second blood flow restriction. Therefore, we propose that fatiguing
and the third sets compared with the first set. low-intensity dynamic training during ischemic conditions
At first glance, our findings may appear to contradict includes a significant eccentric component and that this could
those of previous studies that have compared training with potentially contribute to the training effects observed with
and without cuff occlusion in terms of muscle activity and this type of training.
in which occlusion was demonstrated to yield higher levels of Not surprisingly, fatiguing low-load strength training was
muscle activation. However, in these studies (25,26,34,35), the associated with a significant degree of pain because of the
degree of effort most likely differed between the conditions, ischemia and accumulation of metabolites in the quadriceps.
in contrast with the current study where the effort was The Borg RPE values were also generally high, as expected,
maximal in both conditions. Furthermore, in the present considering that the subjects performed all-out sets. In-
study, high levels of activation (86–107% of MVIA) were seen terestingly, the pain ratings were similar between conditions.
in both conditions in the last few repetitions during the In contrast, in our previous study (33), occlusion was
concentric phases, and shorter bursts (lasting a few tenths of associated with greater pain levels. However, in that study
a second) of approximately 120–160% of MVIA were not (33), the pain levels were maximal in the moments
uncommon. Therefore, our results confirm the findings of immediately after the exercise, when the cuff had not yet
Takarada et al. (25,27) of high EMG levels during low- been deflated. The high pressure (200 mm Hg) used in
intensity (20–40% of 1RM) training with blood flow combination with the relatively wide cuff probably imposed
restriction. The novel finding in our study is that a high a nearly complete restriction of blood flow. In the current
level of activation is possible also without cuff occlusion if the study, the lower pressure used (100 mm Hg) most likely
repetitions are performed in a no-relaxation manner. allowed for some washout of metabolites, and therefore the
The high EMG levels suggest, but do not directly prove, pain did not increase in the rest periods between the sets.
type II fiber recruitment. However, Krustrup and colleagues Nevertheless, it is possible that metabolites accumulated to
(16) recently demonstrated that blood flow restriction during such a degree during and after the exercise with cuff
pure concentric knee extensor exercise at a low workload (29 occlusion that it may have impacted on the activation of
Watts) resulted in a lowered creatine phosphate content in the muscle, thus explaining the differences observed in the
93% of the fast-twitch fibers, which strongly supports that the third set.
majority of type II fibers can be recruited at low loads during Although we did not measure blood flow in this study, the
ischemic conditions. endurance data, along with feedback from the subjects,
It is well known that muscle blood flow during both static suggested that the occlusion was indeed affecting the muscle.
and dynamic exercise occurs mainly during the relaxation In fact, several of the subjects experienced difficulty in starting
period between contractions (5,18). By eliminating the the first repetition in the second and third sets with the
relaxation of the muscle between repetitions in our protocol, occluded leg, but once they had managed to do the first
the muscle blood flow likely became insufficient to meet the repetition, they were usually able to do several more.
metabolic demands, and consequently not only the cuff- Furthermore, we determined in separate pilot experiments

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Muscle Activity and Endurance During Fatiguing Dynamic Knee Extensions

that 100 mm Hg in combination with our relatively wide cuff factors and hormones in the blood flow restricted condition.
reduced blood flow in the femoral artery at rest by On the other hand, the greater amount of work and the
approximately 50–60% in the seated position, as measured slightly higher muscle activity during the eccentric phase
by Doppler ultrasound. Takano et al. (24) used a narrow could in theory lead to greater adaptations for the non-
tourniquet (33 mm in width) and pressures of 160 to 180 mm occluded regime. Finally, the findings of the present study
Hg and reported an approximately 70% reduction of the concern the dynamic knee extension exercise with variable
femoral blood flow at rest in the seated position. Wider cuffs resistance and may not necessarily be generalizable to other
are generally more effective in occluding the blood flow than exercises or other muscle groups.
are more narrow ones (9,14). Consequently, we were able to
use a relatively low pressure to minimize compressive and PRACTICAL APPLICATIONS

shear forces on soft tissues, in particular nerves and blood Cuff occlusion decreases the muscle endurance at low loads
vessels (9,14). but does not necessarily result in greater maximal muscle
As in our previous study (33), multiple sets of low-intensity activity in the quadriceps in the knee extension exercise if
training to fatigue induced DOMS. However, the soreness performed to the point of concentric torque failure. The knee
in the nonoccluded leg was significantly greater than for the extension exercise in a variable resistance machine appears to
occluded leg, which may be explained by the greater number be sufficient in itself to induce relative ischemia already at low
of repetitions completed for the leg that trained without loads if performed in a continuous manner without relaxation
blood flow restriction. An important underlying factor of the muscle between the repetitions. The high degree of
behind the DOMS may be the relatively high increase in muscle activation suggests that these methods may be useful
activation observed during the eccentric phases from the in rehabilitation (e.g., after sports injuries), in which large
beginning to the end of each set, as discussed previously. The loads sometimes may be contraindicated. However, because
ischemia-reperfusion and the formation of reactive oxygen it is rather painful to train close to concentric torque failure at
species (ROS) occurring during exercise could also play these low loads regardless of whether a pressure cuff is used or
a role (29–31). Intriguingly though, Goldfarb and colleagues not, the applicability of these methods may be limited to
(13) reported that plasma protein carbonyl levels, a marker of highly motivated individuals. Furthermore, because multiple
ROS-mediated damage, were significantly less elevated after sets of fatiguing dynamic knee extensions at these low loads
blood flow restricted exercise compared with conventional often lead to DOMS, the volume or level of effort should
resistance training. probably be limited initially.
Because studies have demonstrated hypertrophy
(1,2,12,17,28), and increases in muscle protein synthesis ACKNOWLEDGMENTS
(MPS) (11), with low-intensity (20% of 1RM) occlusion This study was supported by a grant from the Swedish
training, and because the femoral blood flow may become National Centre for Research in Sports. The authors thank
insufficient already at low loads during continuous dynamic the subjects for their time and effort and Zimmer Sweden for
knee extensions (21), we previously speculated that it is providing the automatic tourniquet system. The authors
possible to induce hypertrophy also without cuff occlusion have no conflicts of interest that are directly relevant to the
at low intensities (approximately 20–30% of 1RM) in this content of this study. The results of the present study do not
exercise if performed in a no-relaxation manner (32). In line constitute endorsement of the product by the authors or the
with this hypothesis, Burd et al. (7) recently reported in NSCA.
a preliminary study that 4 sets to failure at 30% of 1RM
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