EFFECTS OF TRADITIONAL AND VASCULAR RESTRICTED
STRENGTH TRAINING PROGRAM WITH EQUALIZED
VOLUME ON ISOMETRIC AND DYNAMIC STRENGTH,
MUSCLE THICKNESS, ELECTROMYOGRAPHIC ACTIVITY,
AND ENDOTHELIAL FUNCTION ADAPTATIONS IN YOUNG
ADULTS
THIAGO ROZALES RAMIS,1 CARLOS HENRIQUE DE LEMOS MULLER,1 FRANCESCO PINTO BOENO,1
BRUNO COSTA TEIXEIRA,2 ANDERSON RECH,2 MARCELO GAVA POMPERMAYER,2
NIARA DA SILVA MEDEIROS,1 ÁLVARO REISCHAK DE OLIVEIRA,2 RONEI SILVEIRA PINTO,2 AND
JERRI LUIZ RIBEIRO1
1
IPA Methodist University Center, Porto Alegre, Rio Grande do Sul, Brazil; and 2Federal University of Rio Grande do Sul,
Porto Alegre, Brazil
ABSTRACT
Ramis, TR, Muller, CHdL, Boeno, FP, Teixeira, BC, Rech, A,
Pompermayer, MG, Medeiros, NdS, Oliveira, ÁRd, Pinto, RS,
and Ribeiro, JL. Effects of traditional and vascular restricted
strength training program with equalized volume on isometric
and dynamic strength, muscle thickness, electromyographic
activity, and endothelial function adaptations in young adults.
J Strength Cond Res XX(X): 000–000, 2018—The purpose of
the study was to evaluate and compare the acute and chronic
effects of partial vascular occlusion training in young, physically
active adults. Neuromuscular, morphological, and endothelial
function responses were compared between high-intensity
resistance training (HI-RT) and low-intensity resistance training
with partial vascular occlusion (LI-BFR), despite the same train-
ing volume. The 28 subjects (age, 23.96 6 2.67 years) were
randomly assigned into 2 groups: LI-BFR (n = 15) and HI-RT (n
= 13). Both groups performed unilateral exercise of elbow
flexion (EF) and knee extension (KE) 3 times per week for 8
weeks. This study was approved by the ethics committee.
Flow-mediated dilation showed a significant difference in base-
line and post-training in the LI-BFR group (4.44 6 0.51 vs.
6.35 6 2.08 mm, respectively). For nitrite/nitrate concentra-
tions only, there was a significant difference when comparing
pre- and post-acute exercise in both groups. The torque and
Address correspondence to Thiago Rozales Ramis, thiago.ramis@
yahoo.com.br.
00(00)/1–10
Journal of Strength and Conditioning Research

2018 National Strength and Conditioning Association
Copyright ª 2018 National Strength and Conditioning Association
rep. Sixty percent 1 repetition maximum had improvements in
both groups. There were differences between groups only in
isometric delta EF and isokinetic delta KE (EF 3.42 6 5.09 and
9.61 6 7.52 N$m; KE 12.78 6 25.61 and 42.69 6 35.68
N$m; LI-BFR and HI-RT groups, respectively). There was a sig-
nificant increase of muscle thickness in both groups. An
increase of both isokinetic and isometric electromyography
(EMG) of biceps of the HI-RT group was observed. The same
was observed for the LI-BFR group regarding isokinetic and
isometric EMG of vastus lateralis. Thus, in addition to strength
and hypertrophy gains, this study also shows benefits related
to vascular function. For practical applications, this study dem-
onstrates a clinical importance of LI-BFR training as an alter-
native methodology.
KEY WORDS exercise, resistance training, vascular occlusion
INTRODUCTION
S
trength training performed with vascular occlu-
sion, also known as blood flow restriction (BFR),
has been proposed as a novel method to improve
strength and hypertrophy, even in a short span
of time. There are some studies using strength exercises
with BFR that have shown improvements in strength,
muscle mass, reduction on cardiovascular preload, and
preventing disuse atrophy in orthopedic restrictions
(20,26,34).
In the BFR method, strength exercises are performed with
a very small load/intensity, which represents low mechan-
ical stress in both joint and muscular tissues. Pooling of
venous blood and reduced cardiac preload seem to be the
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Effects of Traditional and Blood Flow Restriction

myostatin (22) and secretion

of growth hormone (GH)
TABLE 1. Sample characterization and comparison of anthropometric
measurements.*† (35), among other things.
However, it is necessary to
LI-BFR HI-RT conduct more studies compar-
ing these different methods on
Pre-training Post-training Pre-training Post-training
the parameters of endothelial
Age (y) 23.52 6 2.77 — 24.46 6 2.56 — function. It is not known
Height (m) 1.73 6 0.06 — 1.75 6 0.05 — whether or not the occlusion
Body mass (Kg) 76.26 6 12.76 — 79.36 6 11.3 — is aggressive to the blood
Fat mass (%) 28.73 6 5.48 28.44 6 5.45 30.01 6 4.96 29.63 6 5.32
vessels.
Muscle mass (%) 44 6 4.16 44.3 6 3.97 43.38 6 3.96 43.8 6 4.26
Fat mass (Kg) 22.21 6 6.67 21.8 6 6.36 23.84 6 5.85 23.74 6 6.5 Thus, the aim of this study
Muscle mass (Kg) 33.4 6 5.91 33.88 6 5.45 34.42 6 5.57 34.77 6 5.83 was to evaluate and compare
the acute and chronic effects of
*Group LI-BFR = strength training with blood flow restriction; HI-RT group = high-intensity
strength training.
resistance training with and
Data presented as mean 6 SD without partial vascular occlu-
sion on neuromuscular adapta-
tions and morphological and
endothelial functions in young
main acute vascular responses induced by this method (34). physically active adults who undergo the same training
Moreover, acute and chronic hemodynamic changes volume, but with different intensities.
induced by strength exercises using the BFR method have
been associated with alterations in endothelial function, METHODS
although mechanisms supporting these changes are not Experimental Approach to the Problem
clear, especially when comparing different intensities and The subjects (n = 28) were randomly assigned into 2 groups:
volumes of training (10,16). the LI-BFR group (low-load resistance training with BFR; n
Changes in endothelial function are fully dependent on = 15) and the HI-RT group (high-load resistance training
the intensity of exercise; therefore, load and volume seem to without BFR n = 13). Both groups performed unilateral
directly affect these changes in response to a strength exercise of elbow flexion and knee extension for 8 weeks, 3
training program (19). Studies have compared the effects times per week and the volume was equalized. The groups
of different strength training programs on several variables, were assessed before and after training and the evaluators
especially comparing traditional exercises (i.e., without BFR) were blinded regarding the patients and the variables stud-
and BFR exercises (13,17,22,28,37). However, to the best of ied. The dependent variables were torque, muscle thickness
our knowledge, no studies have compared these different (MT), electromyography (EMG), and endothelial function.
exercises modes performed with equalized volumes. Thus, The independent variables were the training protocols and
to ensure that the differences between the protocols are only the variable intervening volume of training, which was
those of exercise intensity, whether BFR is or is not used, it is controlled.
very important that the next studies equalize the training
volumes for the protocols to be compared. Subjects
Evidence shows that hypertrophy and strength gains Twenty-eight male subjects (mean 6 SD: age, 23.96 6
occurred even with intensity between 20 and 50% of 1 2.67 years; body mass, 77.70 6 11.98 kg; and height,
repetition maximum (1RM) with BFR, thus demonstrating 1.74 6 0.05 m) were recruited. The subjects were healthy
similar adaptations to conventional training (22,26,30,37), and physically active, had not practiced strength training
but the intensity range for optimal endothelial function in the past 3 months, and were nonsmokers (Table 1). The
adaptation could not be reported yet. In this way, some sample size was determined using the study by Goldfarb
studies have shown that intensity of strength exercise could et al. (14) as a reference, in which the confidence level was
impair endothelial function in sedentary subjects (5,15). To 95%, the coefficient of variation was 7.98, and the standard
get overall results in neuromuscular adaptation similar to margin of error was 5%. The individuals who used ergo-
traditional strength training, a variety of molecular and met- genic aids or dietary resources, who had any disease that
abolic mechanisms need to occur with vascular restriction would restrict the practice of exercise, any type of meta-
training. For example, low oxygen availability induces the bolic disease that altered hemodynamic function, and who
recruitment of a motor unit with a high threshold, even at had any type of heart or circulatory disease were
low loads (25), causes cell swelling, activating muscle adap- excluded. The written informed consent (IC) was read
tation pathways to mTOR (24), and induces inhibition of and signed by subjects and this study was approved by

the TM

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taking into account all strength

training variables, the LI-BFR
TABLE 2. Assessment of endothelial function by flow-mediated dilation (FMD)
and concentration of nitrate and nitrite (NOx).*† group also held 4 sets, but the
number of repetitions in each
LI-BFR HI-RT set was calculated according
to the volume of training of
Pre-training Post-training Pre-training Post-training
the HI-RT group. For this pur-
FMD (mm) 4.44 6 0.51z 6.35 6 2.08z 5.16 6 2.41 6.41 6 1.88 pose, we used 4 steps: first, an
Nox 1.1 29.95 6 2.19§ 35.4 6 4.00§ 30.7 6 0.19§ 35.61 6 2.56§ average of 1RM of HI-RT for
(mmol$L21) the exercise of elbow flexors
Nox 1.2 29.97 6 4.59§ 34.56 6 3.01§ 30.04 6 1.33§ 35.08 6 4.18§
21 and knee extensors (12.36 6
(mmol$L )
2.42 and 64.49 6 11.78 kg,
*Group LI-BFR = strength training with blood flow restriction; HI-RT group = high-intensity respectively). Second, the over-
strength training. all mean of the 1RM was mul-
†The subjects performed an acute exercise protocol being NOx 1.1 before acute exercise
and 1.2 after acute exercise. Data presented as mean and SD. tiplied by 4 and multiplied by 8
zSignificant difference between pre-training and post-training. corresponding to the number
§Significant difference between pre- and post-acute exercise (p , 0.05).
of sets and repetitions that the
HI-RT group had to perform to
reach the training volume (the
elbow flexors volume was
the Ethics and Research Committee of Methodist Univer- 395.21 and the knee extensors volume was 2065.75). Third,
sity—IPA, by number 364.202. a mean of 30% of the 1RM of LI-BFR subjects for the exer-
cise of elbow flexors and knee extensors was performed (4.78
Procedures 6 1.01 and 21.82 6 5.22 kg, respectively). Finally, to obtain
The subjects came to the Exercise Physiology Laboratory of the number of LI-BFR repetitions, the following calculation
the Research Center in the Methodist University—IPA, for was performed: The general volume of the HI-RT group was
the explanation of study protocols and for signing the IC. divided by the multiplication between the general average of
Then, the medical history questionnaire (PAR-Q) was filled the load of 30% of 1RM and 4 sets, totaling approximately
to ensure that there were no risks to health, as well as filling 20.70 repetitions (rounded to 21) for elbow flexors and 23.64
out a questionnaire on the level of physical activity (IPAQ), repetitions (rounded to 23) for knee extensors. All subjects
the short version. Later, the anthropometric evaluation was were instructed to complete the repetitions and sets. The
based on the anatomical site markings and the technique of rest time between sets for both groups was 2 minutes (occlu-
measuring skinfolds following the standards of the Interna- sion was maintained during passive rest in the LI-BFR
tional Society for the Advancement of Kinanthropometry group) and execution of the movement was controlled using
(ISAK), body composition was calculated using a 5- a metronome (every 2 by 2 seconds).
component method (27), and flow-mediated dilation For partial occlusion determination, the subjects arrived at
(FMD) was performed. After that, 3 meetings were held the Laboratory of Physiology Exercise at the Methodist
for familiarization with exercises and machines. Subse- University Center—IPA and were placed in the supine posi-
quently, the 1 repetition maximum test (1RM) (7) and a num- tion to remain at absolute rest for 20 minutes. After this, the
ber of repetitions at 60% 1RM (rep. 60% 1RM) were resting blood pressure was measured, and it was later used in
performed, and the 60% load was adjusted at the end of the cuff fixing calculation for partial occlusion of the limb. In
training (2). At another moment, the subjects performed the exercise of biceps curls, the cuff was fixed in the upper
isokinetic and isometric tests in the upper and lower limbs, arm and for occlusion, cuff was inflated to 20 mm Hg below
the EMG signal was measured, and MT was assessed. systolic blood pressure (14). In knee extension exercises,
Finally, there was an acute exercise protocol in which sub- occlusion occurred 3 minutes after removing the cuffs of
jects performed the exercise protocol that was specific to the the upper limbs. Then, the occlusion protocol was deter-
training group (LI-BFR or HI-RT) and blood sampling was mined being 40 mm Hg above the value used to occlude
performed before and after acute exercise. All procedures the upper limb (14). In all cases, the cuff was fixed in the
were performed with an interval of 72 hours. At the end of upper arm or thigh. To ensure that the methodology used
the training, the subjects underwent the same procedures. for partial occlusion was reliable, an oximeter was used
The HI-RT performed high-intensity exercise (80% 1RM) (Nellcor NPB 195; Mallinckrodt, Inc., St. Louis, MO, USA)
without BFR (4 sets, 8 reps). The LI-BFR group performed after each set to ensure that the blood flow was not com-
low-intensity exercise (30% 1RM) with BFR. The training pletely disrupted (14). This occlusion methodology was cho-
volume was calculated by sets 3 reps 3 load (7). To ensure sen because the partial occlusion used in this study only
that the volumes of training for both groups were equal, prevents the venous flow, whereas total occlusion prevents

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Effects of Traditional and Blood Flow Restriction

TABLE 3. Absolute values of muscle torque, rep. 60% 1RM (pre-training and post-training), and muscle torque
delta.*†

LI-BFR HI-RT LI-BFR HI-RT

Pre-training Post-training Pre-training Post-training Delta Delta

EF, isokinetic 44.71 6 8.32z 49.14 6 7.89z 45.92 6 11.15z 51.15 6 10.13z 4.42 6 6.06 5.23 6 6.3
(N$m)
EF, isometric 61.5 6 11.81z 64.92 6 10.52z 56.76 6 12.47z 66.38 6 12.48z 3.42 6 5.09§ 9.61 6 7.52§
(N$m)
KE, isokinetic 191.13 6 45.58z 211.21 6 43.9z 198.23 6 35.9z 240.92 6 43.15z 12.78 6 25.61§ 42.69 6 35.68§
(N$m)
KE, isometric 240.07 6 59.04z 261.64 6 57.24z 261.3 6 48.61z 308.84 6 52.1z 21.57 6 23.1 47.38 6 25.95
(N$m)
EF, rep. 60% 11.57 6 3.65z 18.13 6 5.89z 12.07 6 3.17z 18.07 6 4.19z — —
1RM
KE, rep. 60% 10.71 6 2.1z 24.4 6 12.07z 10.61 6 1.66z 18.76 6 3.78z — —
1RM

*Group LI-BFR = strength training with blood flow restriction; HI-RT group = high-intensity strength training; EF = elbow flexion; KE
= knee extension; rep. 60% 1RM = number of repetitions at 60% 1RM.
†Data presented as mean and SD.
zSignificant difference between pre-training and post-training.
§Significant difference between groups (p , 0.05).

both the venous and arterial flow; therefore, we opted for the
less aggressive methodology. If the oximeter did not detect
the pulse on the finger, the cuff had pressure reduced in
increments of 5–10 mm Hg until the pulse was detected.
The cuff used for lower flow restriction limbs was 112 cm
long and 16 cm thick, whereas for the upper limbs, we used
a cuff that was 54 cm long and 14 cm thick.
Peak torque of elbow flexors and knee extensors was
assessed on a Cybex NORM dynamometer (Ronkonkoma,
NY, USA) in concentric (608$s21) and isometric (at 908 of
elbow flexion and 608 of knee flexion; 08: full joint extension)
conditions. For knee extension, subjects were seated on the
dynamometer chair (6), and for elbow flexion, a Scott bench
was attached to a dynamometer (12). Warm-up consisted of
10 submaximal concentric repetitions at 1208$s21. Before
each test, subjects performed a pre-test that simulated the
test condition, except for submaximal effort. The concentric
isokinetic test consisted of 5 maximal repetitions for both
elbow flexion and knee extension. After 2 minutes, 3 maxi-
mal isometric contractions were performed for both muscle
groups; each one sustained for 5 seconds, with a 2-minute
rest interval between them. Subjects were instructed to attain
physical exertion “as fast and hard as possible.” Pre- and
post-training tests followed the same evaluation order and
procedures. The greatest peak torque in each test provided
by the HUMAC 2009 software version 12.17.0 (HUMAC,
NY, USA) was used for further analysis. Intraclass correla-
tion coefficients for isokinetic and isometric tests were 0.91.
The collection of the EMG signal activity was recorded
from the biceps brachii (BB), rectus femoris (RF), and vastus
the TM
lateralis (VL) muscles during maximal isometric and iso-
kinetic strength testing. Before placing the electrodes,
shaving was performed using a disposable blade, and
abrasion of the skin with alcohol and cotton was performed
for the removal of oils and dead cells, thereby reducing skin
impedance. Bipolar electrodes (20-mm interelectrode dis-
tance) were placed at the muscle belly in the direction of
muscle fibers, according to SENIAM (http://www.seniam.
org). To ensure reliability of positioning of electrodes
between pre-training and post-training, an evaluation map
was used for each subject for proper placement (6).
A raw EMG signal was obtained using a Miotool 200, 2-
channel electromyograph (Miotool; Miotec, Porto Alegre,
Brazil) with sampling frequency of 2,000 Hz per channel and
amplified by a factor of 100. Analyses were performed using
SAD32 software. The EMG signal was Butterworth-filtered
using cutoff frequencies of 20 and 500 Hz for lower and
upper band-pass, respectively. Then, root mean square
(RMS) values were obtained from EMG data at 1-second
torque plateau for the best isometric trial (isometric RMS)
and from the best concentric repetition (isokinetic RMS) for
both elbow flexors and knee extensors. The evaluations were
conducted by experienced evaluators according to pre-
established and widely used techniques.
Assessment of MT was performed using ultrasound
imaging (Toshiba Model Nemio XG) being obtained in the
B-mode (32). Before image capture, the subjects were at rest
for 10 minutes in supine position, with limbs relaxed and
extended. To measure MT of BB muscles and brachialis
(BR) of the upper limbs and RF muscle, vastus medialis

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TABLE 4. Absolute values of hypertrophy and electromyography (EMG), pre-training and post-training.*†

LI-BFR HI-RT

Pre-training Post-training Pre-training Post-training

Thickness, biceps (mm) 31.65 6 3.19z 33.72 6 3.55z 31.14 6 3.43z 33.99 6 0.94z
Thickness, quadriceps (mm) 98.51 6 10.55z 101.67 6 10.94z 98.95 6 13.63z 102.49 6 13.14z
EMG, biceps isokinetic (mV) 859.3 6 185.67 988.53 6 303.29 793.12 6 221.19z 984.9 6 305z
EMG, biceps isometric (mV) 964.96 6 389.05 1,075.72 6 535.93 843.74 6 281.99z 1,066 6 324.5z
EMG, VL isokinetic (mV) 348.7 6 145.68z 443.63 6 219.15z 372.14 6 102.56 419.88 6 91.32
EMG, VL isometric (mV) 321.71 6 149.26z 416.69 6 178.5z 389.63 6 107.89 443.53 6 110.57

*Group LI-BFR = strength training with blood flow restriction; HI-RT group = high-intensity strength training; VL = vastus lateralis.
†Data presented as mean and SD.
zSignificant difference between pre-training and post-training.

(VM), vastus lateralis (VL) and vastus intermedius (VI) of the
lower limbs of each individual, a linear transducer frequency
was used (7.5 MHz), which was positioned perpendicularly
to the muscles evaluated. A water-soluble gel was used to
promote acoustic contact with the evaluated structure
and minimum pressure was applied over the transducer.
All ultrasound evaluations were performed by a qualified
experienced appraiser.
For the BB and BR, a measurement was used distally
corresponding to 60% of the distance between the lateral
epicondyle of the humerus and the acromion. The point for
assessing MT of RF, VI, and VL was half the distance from the
greater trochanter and the lateral epicondyle of the femur (21).
For the VM, it was captured the image at the location corre-
sponding to 30% of the distance between the lateral epicondyle
and the greater trochanter of the femur (18). A dermographic
pen was used for marking the points. In addition to these ref-
erence points mentioned above, for BB and VL 2 other points
were used: one proximal and one distal from the said reference
point (midpoint) for the evaluation of MT. The other 2 points
were assessed at BB 4 cm below and above the reference point
mentioned above and VL 5 cm below and above the reference.
Three images of each point were saved for posterior analyses
and mean thickness was calculated for future comparisons.
For the analysis of images and measurements of MT,
a perpendicular line was drawn to the inner edges, top, and
bottom of the fibrous sheath of each muscle evaluated in the
ImageJ (version 1:37, National Institutes of Health, USA)
software. For the analysis of the thickness of the VL and RF,
the distance between the subcutaneous fat and aponeurosis
VI was considered, as identified in the image. As for the
thickness of the VI and VM, the distance from the upper-
muscle aponeurosis and bone aponeurosis was considered.
To ensure capture of images at the same points, the pre-
training and post-training system was used for evaluation
maps as described above. All images were captured and
analyzed by the same evaluator.
For comparison, we used the summations of MT of the
reference points of each muscle evaluated in a muscle group
(average BB + BR and VL average + RF + VM + VI) with
the goal of full representation of the muscle group and the
aggregate MT. Intraclass correlation coefficient for MT was
0.83.
The FMD of the brachial artery in response to reactive
hyperemia was measured on an ultrasound device (Toshiba
model Nemio XG) as an indirect measure of endothelial
function adapted to the current guidelines (36). Assessments
occurred before and after performing each exercise protocol
in a warm room (21–248 C) always in the same period of the
day, after 15 minutes of rest in the supine position. A high-
frequency transducer (11.0 MHz) was used with water-based
gel to obtain images of the longitudinal upper and lower
walls of the brachial artery, with simultaneous electrocardio-
graphic tracing. In the period before occlusion, 5 baseline
images were analyzed and the average of them was used
as a basal diameter of the brachial artery value; then, a pres-
sure cuff placed on the forearms of the subjects was inflated
to 250 mm Hg and maintained for 5 minutes (9). After 5 mi-
nutes of occlusion, the cuff was removed and new images of
the brachial artery were obtained. The entire evaluation was
recorded on a DVD for later analysis in the software ImageJ.
To minimize the influence of the cardiac cycle in arterial
diameter, determination of the thicknesses was always in the
“R” wave of the electrocardiogram. Due to the inability to
perform a scan of the arterial diameter throughout the post-
closure period as proposed in the guidelines, evaluations of
arterial diameters were performed in fixed periods of 60 and
75 seconds after releasing the cuff. These periods were
selected because the peak dilation of the brachial artery
occlusion after 5 minutes varies significantly between periods
in different populations and levels of training. The highest
dilation value found was used for further analysis. The FMD
values were shown absolutely and as a percentage relative to
the increase in the brachial artery diameter after reactive

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Effects of Traditional and Blood Flow Restriction
hyperemia protocol. The calculation for determining the
percentage of vasodilation was as follows:
Vasodilatation% ¼ ð½EH2EB3100Þ=EB
Where EH is the thickness of the brachial artery after
reactive hyperemia and EB is the basal thickness of the
brachial artery (9,36). The evaluations were performed by
experienced evaluators according to pre-established and
widely used techniques.
Obtaining a Biological Sample. Venous blood samples were
collected (10 ml) without anticoagulant to obtain serum and
heparin to obtain plasma. This was done before and after
acute exercise in pre- and post-training. Serum was sepa-
rated by centrifugation for 10 minutes at 2,500 rpm. Shortly
afterward, it was aliquoted and frozen for later analysis.
Nitrite levels were determined by the method described
by Miranda (29). The Griess reagent was prepared by mixing
equal volumes of sulfanilamide (1%) dissolved in HCl (0.5
M) and N-naphthylethylenediamine (0.1%) in distilled water.
Volumes of 250 ml of plasma and 250 ml of trichloroacetic
acid 10% (TCA) were added in a test tube and centrifuged at
2,500 rpm for 10 minutes in order for the sample to lose
protein. By using the enzyme-linked immunosorbent assay
plate, 100 ml of deproteinized sample was added to 100 ml of
a saturated solution of vanadium chloride to reduce nitrate
to nitrite. Then, 100 ml of Griess reagent was added, leaving
the material for 30 minutes at room temperature protected
from light for reading at 540 nm in enzyme-linked immuno-
sorbent assay. A standard curve was obtained with different
volumes of sodium nitrite added to 100 ml of Griess reagent.
Statistical Analyses
For calculating the sample size, the study by Goldfarb et al.
(2008) was used as reference. The calculation was performed
using the WinPEPI program Version 4.0, in which confi-
dence level will be 95%, the coefficient of variation 7.98, and
a standard margin of error of 5%. Thus, each experimental
group consisted of 15 volunteers accounting for a 10%
sample loss.
Distributions of all variables to verify the normality by the
Shapiro-Wilk test was evaluated, assuming a homogeneous
normal distribution. It used analysis of variance for repeated
measures with the Bonferroni post hoc test. Significantly
different values were considered when p , 0.05. All data
were analyzed using the Statistical Package for Social Scien-
ces (SPSS) 17.0.
RESULTS
The 15 volunteers who started the resistance training with
BFR protocol completed all sessions of training, whereas in
the HI-RT group, 2 volunteers gave up due to personal
problems by the second week of training, ending with a total
of 13 subjects. Table 1 displays the baseline characteristics, in
mean and standard deviation. Moreover, the anthropometric
the TM
6 Journal of Strength and Conditioning Research
Copyright ª 2018 National Strength and Conditioning Association
measures did not show significant differences before and
after training and between groups.
Table 2 shows the mean of FMD and nitrite and nitrate
(NOx) measures. There was a significant difference between
pre-training and post-training at rest FMD in the LI-BFR
group (4.44 6 0.51 vs. 6.35 6 2.08 mm, respectively). For
NOx concentrations, there were no difference between
groups; however, there were significant differences in both
groups when comparing pre- and post-acute exercise (pre-
training—NOx 1.1 baseline 29.95 6 2.19 mmol$L21 and after
acute exercise 35.4 6 4.00 mmol$L21; baseline 30.7 6 0.19
mmol$L21 and after acute exercise 35.61 6 2.56 mmol$L21,
respectively, in the LI-BFR and HI-RT groups; post-training
—NOx 1.2 baseline 29.97 6 4.59 mmol$L21 and after acute
exercise 34.56 6 3.01 mmol$L21; baseline 30.04 6 1.33
mmol$L21 and after acute exercise 35.08 6 4.18 mmol$L21,
respectively, in the LI-BFR and HI-RT groups).
Table 3 shows the torque and rep. 60% 1RM improve-
ments and there was a rise in all parameters when compar-
ing baseline and post-training in both groups. There were
differences between groups only in isometric delta elbow
flexion and isokinetic delta knee extension (isometric delta
EF 3.42 6 5.09 and 9.61 6 7.52 N$m; isokinetic delta KE
12.78 6 25.61 and 42.69 6 35.68 N$m, respectively, in the
LI-BFR and HI-RT groups).
Table 4 shows the hypertrophy and EMG results. There
was an increase of MT in both groups when comparing the
baseline and post-training. An increase of both isokinetic and
isometric EMG of biceps of the HI-RT group was observed.
The same was observed for the LI-BFR group on isokinetic
and isometric EMG of VL.
DISCUSSION
This study compared the neuromuscular and morphological
adaptations after an 8-week training period with or without
vascular occlusion and the same training volumes. Further-
more, exercise-related and training-related changes in endo-
thelial function assessed by flow-mediated dilation and
nitrites/nitrates concentration were reported.
Strength training with BFR is now becoming an impor-
tant alternative training methodology for people who have
some kind of restriction regarding high mechanical loads.
For example, people with a high risk of cardiovascular events
could not withstand high mechanical loads. Vascular health
is a predictor of cardiovascular events and it is related to
endothelial function. It is well known that exercise and
hypoxia are factors that change endothelial function.
Because BFR decreases oxygen delivery to muscles, this
training methodology could change endothelial function. It
seems important to clarify that mechanism in healthy people
to better understand it so as to support future studies
involving subjects with endothelial dysfunction–related dis-
eases. Finally, to reliably compare both protocols, it is nec-
essary to control the volume of the methods used in the
study. Therefore, the only difference between groups was the

intensity and the occlusion of the limb. The importance of
this work is highlighted as there are few studies with con-
trolled volume of training that evaluate all of these
parameters.
The LI-BFR and HI-RT groups were homogeneous in
pre-training time as shown in Table 1. In addition, 8 weeks of
training was not able to generate significant changes in body
composition.
When evaluating endothelial function, at no time were
significant differences shown between groups at variable
FMD and NOx (Table 2). However, the LI-BFR group
showed a significant increase in FMD and NOx after train-
ing periods when compared with the baseline. The HI-RT
group showed a significant increase only in variable NOx.
Our data are innovative when analyzing the vascular
response evaluated by FMD and NOx for 8 weeks of
strength training. In this way, several factors have influenced
FMD, such as ischemia-reperfusion mechanism. Both
groups showed similar results for NOx, but FMD only
increased for the LI-BFR group. In addition, FMD was
similar between groups after training. The muscular con-
traction and relaxation during exercise could simulate the
ischemia-reperfusion mechanism, but intensity of exercise is
important. If there is no BFR, probably both groups would
have different FMD effects, because exercise intensity has
been showing a crucial role in FMD response (5). However,
BFR caused the same effect on low-intensity training com-
pared with high-intensity training without occlusion,
because both groups have no significant differences after
training.
Nitric oxide (NO) production is influenced by shear stress
mechanism and its bioavailability is altered by oxidative
stress (3,16). Because NOx concentration was equal between
groups, at all moments, it seems that the same effect of FMD
occurred. The BFR added to low intensity of training could
be able to generate the same biomarker increases compared
with high-intensity training without occlusion.
Partial vascular occlusion during exercise partially inter-
rupts arterial influx and blocks venous return; so, we can
hypothesize that shear stress could be increased. Therefore,
our results could be explained by the positive relationship of
shear stress and NO bioavailability causing FMD increase.
Thus, the adjustment of FMD with occlusion training must
be related to endothelial vasodilators but some other
endothelium-independent mechanism could also be related.
It is well established that low-intensity exercise with BFR
promotes strength gains and hypertrophy (22,30,33), even
showing similar benefits when compared with high-
intensity exercise without occlusion (22). According to
Abe et al. (2005), 2 weeks of low-intensity strength training
with BFR would already be enough for approximately 22%
of power increase in the leg-press exercise. In addition, there
was an increase of 7–8% of the thigh hypertrophy, evaluated
using magnetic resonance imaging, a result similar to a peri-
odization of 3–4 months of high-intensity training (1). Fur-
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Journal of Strength and Conditioning Research | www.nsca.com
thermore, Shionahara et al. (1998) conducted a study with
untrained subjects that presented, in thighs that underwent
occlusion, a 9% increase in maximum power in 2 weeks and
26% after 4 weeks of training. However, the thighs that only
underwent low-intensity training received no significant
gains (33).
In the study by Laurentino et al. (22), after 8 weeks of
training, the sample showed an approximately 40 and 36%
of 1RM increase at knee extension for occlusion and high-
intensity groups, respectively. In our study, the results
showed a significant increase in both groups evaluating the
basal values with the results after 8 weeks of training
(Table 3), which confirms the literature, again highlighting
this study with groups equalized by volume of training, dif-
fering only in intensity and occlusion.
Another important result in our study was the significant
increase in repetitions with 60% 1RM after training in both
groups (Table 3), with no significant difference between
them. Even with equal volumes of training between the 2
groups, repetitions and intensities were different, but theo-
retically according to Loenneke et al. (2010), the 2 groups
recruited the same type of fiber. The authors explain that
when oxygen availability decreases during occlusion, an
increasing recruitment of motor units occurs progressively
to make up for the power deficit (25). Moreover, there is an
increase in the EMG signal during occlusion, thereby sug-
gesting that there is an increase in the activation of fast fibers
(type 2) (23). According to the principle of activation of
motor units, when recruiting the fibers of type 2, type 1 fibers
were also recruited. If the 2 groups trained recruiting type 2
fibers, even with different intensities, the type 1 fibers must
have undergone some training effect, increasing resistance in
the test 60% of 1RM. Thus, the results presented in this work
that in repetitions with 60% 1RM can be explained by the
same fiber recruitment in both groups, indicating that occlu-
sion “decharacterizes” high-intensity and low-intensity dif-
ference as the results are similar.
Peak torque was evaluated in dynamic and isometric
forms in an isokinetic dynamometer. The 2 training groups
had a significant increase in peak torque both in elbow
flexion and knee extension. Furthermore, the delta results
were significantly higher in the HI-RT group for isometric
elbow flexion and isokinetic knee extension. Low-intensity
training with BFR has been shown to have similar results
compared with high-intensity training. However, the delta
results of this study showed significant differences between
groups, and it may be related to the control of training. It
seems that the equalized volume of training promoted
a greater strength gain for the high-intensity group. We
believe that this effect occurred because the equalized
volume makes the intensity the only difference between
groups, but these results can also be related to the theory
proposed by Loenneke et al. (26).
Loenneke et al. (2012) proposed a theory called “theoret-
ical reverse pattern of adaptations in traditional vs. low-
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Effects of Traditional and Blood Flow Restriction
intensity blood flow–restricted exercise” (reverse theory),
which may explain the delta differences between groups.
They proposed that the neural and hypertrophic adaptations
may occur in the opposite way to conventional strength
training proposed by Sale (1988) (26). Thus, we could
hypothesize that the greater strength gains for the high-
intensity training group takes place at the first 8 weeks as
a result of neural adaptations. Meanwhile, the low intensity
with BFR group would have hypertrophic adaptations and
the strength gains may occur after 8 weeks with neural adap-
tations (26).
In this work, muscle activation (EMG signal) did not differ
between the groups and these results could be explained by
the same recruitment pattern of fiber type II. Muscle
activation of elbow flexors increased only for the high-
intensity training group. Because elbow flexors activation
does not take place for the vascular occlusion group, it seems
that the “reverse theory” would be confirmed. However,
EMG for knee extensors showed opposed effects with the
only group increasing muscle activation being the vascular
occlusion group. Thus, neural adaptations could be different
between upper and lower limbs. In addition, MT increased
for both groups, contradicting the “reverse theory” (26).
Muscle thickness had baseline values that were similar
between groups and showed significantly different changes
after the intervention (Table 4). These results are in agree-
ment with many other studies showing similar hypertrophic
adaptations between high-intensity training and
low-intensity vascular occlusion training (8). So far, the
physiological mechanisms eliciting hypertrophy in strength
training with BFR are not entirely clear. A variety of molec-
ular and metabolic mechanisms for strength and hypertro-
phy adaptations, which will be discussed below, may explain
the results of low intensity with vascular occlusion training.
The low availability of oxygen and metabolic stress during
full or partial occlusion causes a progressive recruitment of
motor units, which may occur to offset the deficit strength
output. The activation of fast-twitch fibers (type II) after that
progressive recruitment would occur due to the activation of
high-threshold motor units (25). Furthermore, the increase
of water content in the muscle cell takes place with BFR and
exercise. This “swelling” would cause different intracellular
signals including activation of mTOR and MAPK pathways
increasing muscle adaptation (24).
Loenneke et al. (2010), in their review article, note that
several studies show an increased concentration of GH after
training with occlusion, appearing to be related to acidity of
intracellular environment. The low pH seems to cause
sympathetic activation through the afferent neurons type
III and IV (also sensitive to metabolite accumulation: K+, H+,
AMP, and hypoxia) that are related to the significant
increase in pituitary GH secretion (25).
In the same way, some researchers have been studying the
acute effect of this training to clarify the mechanisms that are
involved in its methodology. A study of young adult males,
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8 Journal of Strength and Conditioning Research
Copyright ª 2018 National Strength and Conditioning Association
which evaluated the acute effect of strength training with
vascular occlusion, showed an increase in GH levels
compared with resting levels (35). The research of Pierce
et al. (31) found that the group that underwent ischemia
and exercise (20% of maximal voluntary contraction)
increased GH levels approximately 9 times the baseline lev-
els, but no significant increases were shown by the group
that only performed ischemia. Abe et al. (1) demonstrated
that GH levels are related to circulating IGF-1 increases
stimulating protein synthesis. Therefore, the production of
IGF-1 stimulates an activation cascade, for example, of Akt
(also known as protein kinase B—PKB). The Akt promotes
the activation of mTOR and GSK-3B (glycogen synthase
kinase-3B) both inducing skeletal muscle hypertrophy (4).
A study performed at the University of Texas evaluated
another protein (S6K1—ribosomal S6 Kinase1) that has
a strong relationship with mTOR. The study demonstrated
that training with vascular occlusion stimulates the phos-
phorylation of S6K1, which is the key regulator of translation
initiation and protein synthesis in human skeletal muscle
(11). In addition, the increases of cross-sectional area and
strength gains with vascular occlusion training could be
related to myostatin, a potent inhibitor of muscle growth.
Laurentino et al. (22) found that physically active males can
have an approximately 40% expression decrease of myosta-
tin gene with occlusion and high-intensity training.
Finally, this study showed similar strength gains and
hypertrophy of the low-intensity strength training with
BFR compared with high-intensity resistance training with
controlled volume of training, and few studies equalize the
training volume of groups. It can be suggested that this
method may be a very important tool for people who cannot
undergo the mechanical stress caused by traditional strength
training. In addition, endothelium-dependent function seems
to change positively with vascular occlusion resistance
training. Thus, in addition to strength and hypertrophy
gains, this study also shows benefits related to vascular
function. This demonstrates a clinical importance of low-
intensity vascular occlusion training as an alternative
methodology.
PRACTICAL APPLICATIONS
Because of the low workloads, strength training with BFR
can be an alternative training method for individuals who
have some orthopedic, cardiovascular, or metabolic limita-
tion. Future studies can test this methodology for patients
who have endothelial dysfunction–related diseases, includ-
ing diabetes mellitus, hypertension, and heart failure. Vas-
cular occlusion could be an additional method for athletes to
increase strength and hypertrophy gains, like individuals
seeking body composition changes.
ACKNOWLEDGMENTS
This work was funded by the Higher Education Personnel
Training Coordination (CAPES) and the Foundation for

Support of Research of the State of Rio Grande do Sul
(FAPERGS). The authors thank the IPA Methodist Univer-
sity Center and Federal University of Rio Grande do Sul
(Porto Alegre, Brazil). They declare that there is no conflict
of interest. This work was funded by CAPES (Coordenação
de Aperfeiçoamento de Pessoal de Nı́vel Superior) and
FAPERS (Fundação de Amparo à Pesquisa do Rio Grande
do Sul).
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