International Journal of Applied Exercise Physiology

2322-3537 www.ijaep.com
Vol.6 No.4
Received: August 2017 , Accepted: November 2017 , Available online: December 2017

Effects of low-load resistance training with blood flow restriction on muscle size and
strength of professional soccer players with muscle imbalance

Benedito S Denadai, Felipe BD Oliveira, Sérgio RA Camarda, Leandro Ribeiro, Camila C Greco
Human Performance Laboratory, UNESP – Rio Claro, SP

DOI: https://doi.org/10.22631/ijaep.v6i4.194

ABSTRACT:

The purposes of this study were: 1) to determine whether low intensity resistance training combined with blood flow restriction (LI-BFR) could
affect the concentric hamstrings/quadriceps muscle strength ratio (Hcon:Qcon) of professional soccer players with Hcon:Qcon imbalance (Study
1), and; 2) whether hamstrings strength response observed after LI-BFR is associated with muscle hypertrophy (Study 2). In the Study 1, athletes
were randomly divided into a training group (n = 6) and a control group (n = 5). In the Study 2, all athletes (n = 11) performed a LI-BFR training
program. The athletes participated of a 6-week (twice a week) supervised training program (unilateral knee flexion at 30% 1RM) totalizing 12
training sessions. The concentric peak torque of knee flexors (+8%; P < 0.001) and Hcon:Qcon (+9%; P < 0.01) were significantly increased after
LI-BFR. Moreover, the cross-sectional area (CSA) of the hamstrings was significantly increased (+10%; P < 0.001) after LI-BFR. Thus, the addition
of hamstrings strength training program using LI-BFR during preseason is able to enhance both Hcon:Qcon and hamstrings CSA of professional
soccer players with Hcon:Qcon imbalance.

KEY WORDS Isokinetic torque; cross sectional area; magnetic resonance imaging; asymmetry

INTRODUCTION different interventions programs have been proposed to restore the

There are several lines of evidence indicating that playing and training
for soccer can improve the reciprocal balance of strength between the
hamstrings and quadriceps muscles (H/Q)[1-3]. Hoshikawa et al.[4] have
demonstrated that the increase of cross sectional area (CSA) seems to
explain, at least in part, the superior enhancement of strength in
hamstrings when compared to quadriceps femoris in soccer players.
However, some studies have found that concentric H/Q muscle strength
(Hcon:Qcon) imbalance is highly prevalent in both professional and
junior elite soccer players[5,6]. It is important to note that
epidemiological studies have indicated that poor eccentric muscular
strength and Hcon:Qcon strength imbalance play a central role in acute
hamstrings strain as well as anterior cruciate ligament injury[7]. Thus,
reciprocal balance of strength about the knee, aiming to minimize the
impact of injuries on both the health and performance of soccer players.
Askling et al.[8] verified that the addition of strength training exercise
with eccentric overload for hamstrings can reduce the occurrence of
hamstrings strain injuries when compared to ordinary training (i.e.,
without eccentric overloading) in elite male soccer players. However,
this intervention is not easily implemented in soccer teams, since a
special device (YoYo flywheel – YoYo Technology AB, Stockholm,
Sweden) was used to increase the muscle strength level during eccentric
muscle action. Using a different approach, Mjølsnes et al.[9] verified that
twenty-seven Nordic hamstring training (NHT) sessions during a 10-wk
training period have improved both eccentric (11%) and isometric (7%)

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 BLOOD FLOW RESTRICTION AND MUSCLE STRENGTH IMBALANCE
strength of hamstring in well-trained soccer players. Moreover, Arnason
et al.[10] reported a 60–70 % reduction in hamstrings injury rate
compared to control groups after the eccentric exercise protocol (i.e.,
NHT). However, NHT entails some disadvantages to be implemented in
soccer teams. Firstly, two or even three partners might be necessary to
provide adequate support to perform the NHT correctly[9]. Moreover,
during initial phase of training, only few repetitions and sets should be
performed, since NHT results in delayed onset muscle soreness (DOMS).
The DOMS can inhibit the players’ ability to perform subsequent training
sessions, decreasing adherence to NHT. Indeed, Gabbe et al.[11] verified
that Australian Football players experienced DOMS, resulting in
extremely poor compliance (50% reduction in participation from the first
to second sessions) to NHT.
Recently, many studies have found that low intensity resistance
training (20–30% 1RM) combined with moderate blood flow restriction
(LI-BFR) can induce muscle hypertrophy and strength increase similar
to those found after high-intensity resistance training (i.e., > 70% 1-
RM)[12,13]. Additionally, reviews studies have pointed that LI-BFR
seems to be safe and that there is no substantial muscle damage after the
practice of this type of exercise[14,15]. Indeed, LI-BFR is well tolerable,
allowing a greater number of sessions in a relatively short period (e.g.,
23 training sessions within 19 days)[16]. However, few studies have
analyzed the effect of a LI-BFR training program in highly trained
professional athletes. Muscle strength and anaerobic power are crucial in
many playing actions in soccer (e.g., sprints, jumping and tackles)[17].
Aerobic metabolism is also important to soccer performance, since
aerobic training status is correlated with both total distance covered
during the match and the amount of high-intensity running in the last 15-
minute period[18]. Thus, in an attempt to improve physical performance
of soccer players, strength and endurance training have been performed
concurrently (i.e., concurrent training). A smaller change in muscle fiber
size and different changes in fiber type have been observed after
concurrent training than after strength training[19]. Thus, it could be
interesting to analyze the effect of LI-BFR in this population.
Therefore, the purpose of this study was twofold: 1) to determine
whether a preseason strength training programme using LI-BFR for
hamstrings could affect the Hcon:Qcon of professional soccer players
with Hcon:Qcon imbalance, and; 2) to determine whether the increase of
muscle strength of hamstrings after LI-BFR is associated with muscle
hypertrophy.
METHODS
Participants
Twenty-two male professional soccer players (24.5 ± 3.1 years, 75.2 ±
10.1 kg, 179.5 ± 8.5 cm), with at least seven years of experience in the
sport, volunteered for the study. In the Study 1, the athletes were
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VOL. 6 (4)
randomly divided into a training group (TG, n = 6) and a control group
(CG, n = 5). In the Study 2, all athletes (n = 11) have performed the
training programme. Forty-eight soccer players were screened for
muscular strength imbalance and only players with Hcon:Qcon < 0.60
(range: 0.43 - 0.59) in dominant limb were included in the study[20]. An
injury report form was used to identify previous injuries of both
dominant and non-dominant knee in the last 12 months before the study.
Subjects who presented an injury during this period were excluded from
the study. The subjects completed a written informed consent to
participate of the study, and all procedures were evaluated and approved
by the local ethics committee. The experiments were conducted
according to the Helsinki Declaration for human experimentation.
Experimental Design
The intervention period was carried out directly after the off-season
period, encompassing the four preseason weeks of the preparation
period, and the first four weeks of the competitive season. The Study 1
and Study 2 were conducted in two different moments, separated by one
year. The participants were instructed to report to the laboratory at the
same time of the morning (± 2 h) on two (Study 1) or three (Study 2)
separate days within a period of 1-2 weeks. Each participant was required
to attend an isokinetic familiarisation session to lessen the effects of
learning on subsequent strength testing. During this session, each
participant completed five maximal concentric actions for knee extensors
(KE) and knee flexors (KF) at 60°•s-1 on an isokinetic dynamometer
(Biodex System 3, Biodex Medical Systems, Shirley, N.Y.). Moreover,
the maximum load that could be lifted through a full range of motion
with proper form during unilateral knee flexion was assessed and
recorded as the one repetition maximum (1RM). On the second visit, the
athletes performed maximal isokinetic concentric actions at 60°•s-1[20].
A standardized warm-up, consisting of 8-min running at 10 km/h
followed by 3 continuous reciprocal knee extensions–flexions
contractions progressing to maximum preceded both the familiarisation
and testing sessions. The determination of cross sectional area (CSA)
was performed in a third session (Study 2). All measurements were
completed before (Pre) and 3-5 days following training (Post) the
training period.
Training intervention
The usual soccer training sessions were conducted nine times a week
and included: strength/speed training (twice a week); aerobic training
(twice a week) and; soccer-specific technical-tactical skills (5 times a
week). Importantly, the soccer training sessions were similar between
groups (i.e., Study 1 - TG vs. CG) and studies (i.e., Study 1 vs. Study 2).
The subjects participated in a 6-week (twice a week) supervised training
program, totalizing 12 training sessions. During the training sessions, the
pressure cuffs [170 mm (width) × 650 mm (length)] was positioned near
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 BLOOD FLOW RESTRICTION AND MUSCLE STRENGTH IMBALANCE
the inguinal fold region of dominant limb and inflated to the training
pressure (140 mm/Hg). Resistance training consisted of unilateral knee
flexion at 30% 1RM. The athletes performed four sets to concentric
failure, with 30 s of rest between sets. The cuff’s pressure was maintained
during the whole session, including intervals and was released
immediately upon completion of the fourth set.
Procedures
Isokinetic testing
Participants were placed in a sitting position and securely strapped into
the test chair. Extraneous movement of the upper body was limited by
two cross-shoulder harnesses and an abdomen belt. The trunk/thigh angle
was set at 85°. The axis of the dynamometer was aligned with the right
knee flexion-extension axis, and the lever arm was attached to the
participant’s shank with a strap. Participants were asked to relax their leg
so that the effects of gravity on the passive limb and lever arm could be
measured. The range of motion (ROM) for the knee test was 70° [from
90° to 20° knee flexion (0° = full extension)]. Anatomical 90° knee
angle was determined by manual measurement using a handheld
goniometer. Concentric torque measurements involved five continuous,
reciprocal (maximal) knee extensions–flexions at 60°•s-1. This test was
performed using only the dominant (preferred kicking) limb. Instructions
were given to the subjects to perform all actions as fast and forcefully as
possible to obtain maximal torque.
Data processing
The isokinetic data were analyzed using specific algorithms created in
the MatLab Environment (The MathWorks, Natick, Massachusetts,
USA). Torque curves were smoothed using a 10 Hz Butterworth fourth-
order zero-lag filter. The action yielding the highest torque value
produced from five individual efforts was used for further analysis. The
peak torque was calculated as the average torque achieved over a range
of 10° around the angle at which the highest torque value was
reached[21]. The following parameters were obtained: peak torque of the
quadriceps and hamstrings and the Hcon:Qcon ratio.
Magnetic resonance images were obtained for dominant limb (GE
Signa EXCITE 1.5T) to determine the CSA of the hamstrings. Every
measure was obtained at least 72 hours after the last training session.
Immediately before each measure, the volunteers remained lying down
in supine position for 15 minutes to maintain blood flow stable avoiding
changes in muscle CSA due to hyperemia. Four consecutive slices (10
Table 1. Mean ± SD values of concentric peak torque of knee extensors (KE) and knee flexors (KF) and
hamstrings-to-quadriceps ratio (Hcon:Qcon) for trained group (TG) and control group (CG) before (Pre)
and after (Post) the training period.
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VOL. 6 (4)
mm) with 0 mm intersection gap between then were acquired, two slices
before and two after thigh mid-point from the greater trochanter to the
lateral condyle of the femur[4]. Data were exported and then analyzed
using an image analyzing software (Synedra View Personal Version
3.2.0.3). The CSA (cm2) was determined as the average value of the area
of the four slices.
Statistical analysis
Data are presented as the mean ± SD values. The distribution of
dependent variables was examined by the Shapiro-Wilk test. In the Study
1, a repeated measures 2 x 2 factorial analysis of variance (SPSS v18,
SPSS Inc., Chicago, IL, USA) was used to detect differences between
groups (TG vs. CG) over time (Pre-training vs. Post-training). Paired t-
tests were then used to determine within-group differences between pre-
and post training measures. In the Study 2, all pre- to post-training
changes were evaluated with paired t-tests. Statistical significance was
set at p < 0.05.
STATISTICAL RESULTS
The mean training load (30% 1RM) attained for all athletes performing
LI-BFR (i.e., Study 1 + Study 2, n = 17), was 22.9 ± 2.4 Kg. The average
values of the repetitions in the first, second, third and fourth set over the
intervention period were 58.4 ± 27.3, 28.6 ± 12.9, 17.3 ± 8.9 and 10.5 ±
4.5, respectively.
Table 1 presents the mean ± SD values of the variables obtained during
the Study 1. No significant group vs. time interaction was identified for
peak concentric torque of KE (F = 2.2; p = 0.17). A significant group vs.
time interaction was identified for peak concentric torque of KF (F =
43.8; p < 0.001). Paired comparisons revealed that peak concentric
torque of KE increased in the TG (+9%; p <0.001), but were unchanged
in the CG. The Hcon:Qcon increased in the TG (+12%; p < 0.001), but
not in the CG, reflecting a group-by-time interaction effect (F = 19.0; p
< 0.001).
The variables obtained during the Study 2 are shown in Table 2. Peak
concentric torque of KE was not significantly changed after LI-BFR.
Peak concentric torque of KF (+8%; p < 0.001) and Hcon:Qcon (+9%; p
< 0.01) were significantly increased after LI-BFR. Moreover, the CSA
of the hamstrings was significantly increased (Pre = 37.6 + 5.0 vs. Post
= 41.6 + 6.1 cm2, p < 0.001) after LI-BFR.
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TG (n = 6) CG (n = 5)
Pre Post Pre Post
KE (Nm) 310.3 ± 46.5 322.8 ± 55.5 285.8 ± 22.6 286.0 ± 26.9
KF (Nm) 151.0 ± 25.7 175.6 ± 32.9* 155.6 ± 10.7 153.0 ± 11.4
Hcon:Qcon 0.48 ± 0.03 0.54 ± 0.04* 0.53 ± 0.04 0.53 ± 0.03
*p < 0.01 in relation to pre.

Table 2. Mean ± SD values of concentric peak torque of knee extensors (KE) and knee flexors (KF) and
hamstrings-to-quadriceps ratio (Hcon:Qcon) before (Pre) and after (Post) the training period. N = 11.
Pre Post
KE (Nm) 286.0 ± 37.0 283.2 ± 41.13
KF (Nm) 152.3 ± 22.4 164.8 ± 26.6*
Hcon:Qcon 0.53 ± 0.04 0.58 ± 0.06*
*p < 0.01 in relation to pre.

DISCUSSION respectively) generated a significant increase (9-12%) in muscular

strength following 4-5 weeks (3 times a week) of knee extension
The main objective of this study was to determine the effects of LI-
exercises. Thus, 12-15 LI-BFR sessions performed during a relatively
BFR on strength (Studies 1 and 2) and muscle hypertrophy (Study 2) of
short period of time (5-6 weeks) led to large gains in maximal strength
professional soccer players with Hcon:Qcon imbalance. The main and
for already-trained athletes.
novel finding of the present study was that the addition of strength
Neural (i.e., agonist activation level and antagonist co-activation
training program using LI-BFR for the hamstrings during preseason
level)[25] and peripheral muscle properties (i.e., CSA, fibre type,
enhanced peak concentric torque of KF. No change was observed in peak
architecture, and tendon/aponeurosis stiffness)[26] have been implicated
concentric torque of KE in any group. Consequently, there was a
in the maximal strength production. Few studies have investigated the
significant increase in Hcon:Qcon ratio in the TG, but not in the CG.
neural adaptations promoted by LI-BFR, particularly in already-trained
Moreover, we have demonstrated that CSA of the hamstrings was
athletes. Recently, Manimmanakorn et al.[24] found that LI-BFR
significantly increased after a 6-week LI-BFR training program. Thus,
enhanced voluntary neural activation (i.e., root mean square of the
LI-BFR seems to be a practical and efficient intervention to improve
electromyographic signal) during maximal dynamic leg extension in
Hcon:Qcon of professional soccer players during the preseason.
female netballers. Besides changes in neural control, several studies have
Many studies, using different experimental designs (i.e., width and
demonstrated that short period (i.e., 3-4 weeks) of LI-BFR improves
pressure of the cuff, training intensity, volume, and type of exercise),
CSA of untrained individuals[16,27]. In the present study, we have
have found that LI-BFR induces increased muscle strength in both
demonstrated, for the first time, that CSA of the hamstrings was
untrained[12,13] and trained athletes[22,23]. In untrained individuals,
improved after LI-BFR in soccer players with Hcon:Qcon imbalance.
LI-BFR is able to promote gains in muscle strength (1RM) similar to
The mean muscle hypertrophy per session (~ 0.88%) found in our study
those observed after traditional high-load training programs[12,13]. In
is apparently superior (~ 0.38% and 0.44%) to those found in both
the present study, the addition of twelve LI-BFR sessions during a 6-wk
untrained individuals[13] and trained athletes[22] after LI-BFR,
training period improved concentric hamstring strength (8-9%) of well-
respectively. Thus, the muscle hypertrophy response to LI-BFR seems
trained soccer players. Similar findings were reported by
not be attenuated in soccer players with Hcon:Qcon imbalance.
Manimmanakorn et al.[24] and Yamanaka et al.[23], where LI-BFR
(20% 1RM) performed by athletes (football and netball players,

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 BLOOD FLOW RESTRICTION AND MUSCLE STRENGTH IMBALANCE VOL. 6 (4)

Although the soccer practice can improve the reciprocal balance of in hamstrings CSA, suggesting that the muscle hypertrophy response to
strength about the knee, many studies have found that Hcon:Qcon LI-BFR seems not to be attenuated in already-trained athletes.
imbalance is highly prevalent in professional soccer players[5,6]. The
neuromuscular characteristics [e.g., neural drive, fiber-type (MHC
isoform) composition, tendon/aponeurosis stiffness] that can explain the
muscle strength imbalance found in soccer players are poorly
understood. Recently, Denadai et al.[28] have found in professional
soccer players with muscular imbalance (Hcon:Qcon = 0.53) that the
ratio of torque to CSA for KF (4.3 + 0.7 Nm/cm2) was significantly
greater (~ 43%) than for KE (3.0 + 0.3 Nm/cm2). These values (absolute
and percentage difference) are apparently higher than those found in
professional soccer players (KE ~ 2.6 Nm/cm2; KF ~ 3.0 Nm/cm2 and ~
15%, respectively) with higher Hcon:Qcon (0.56-0.57) [4]. Thus, is
unlikely that neural deficit can explain the Hcon:Qcon imbalance found
in professional soccer players. In untrained individuals, muscle
hypertrophy can be observed after 4–6 weeks of intensive resistance
training (75%–85% 1RM)[29]. However, in already-trained athletes,
training-induced muscle hypertrophy is much more limited than in
untrained individuals[30]. Thus, LI-BFR seems to be an alternative
training method to improve hamstrings CSA of athletes, and
consequently increase the Hcon:Qcon of professional soccer players.
Indeed, we have demonstrated that twelve LI-BFR sessions during a 6-
wk training period improved Hcon:Qcon of already-trained athletes.
Despite the interesting findings presented herein, some important
limitation needs to be highlighted in the present study. Firstly, we have
analysed only 11 professional soccer players (Study 1). The small
number of volunteers reflects our inclusion / exclusion criteria aiming to
obtain a representative and homogeneous sample of professional players
with Hcon:Qcon imbalance in dominant leg from the same professional
club. Thus, the players were performing similar training program and
competition during the period of data collection. Secondly, no control
group was analysed in the Study 2. In addition to the reasons cited above,
we also considered the ethical / professionals aspects present in this
situation. As LI-BFR was able to promote gains in Hcon:Qcon (Study 1),
we have considered that it would not be appropriate not offering this
strength training for all athletes with Hcon:Qcon imbalance. Future
studies should further investigate the effects of LI-BFR on H:Q obtained
at different angular velocity and contraction mode (concentric and
eccentric). Moreover, prospective studies should be performed to analyze
whether a preseason hamstrings strength-training program using LI-BFR
could significantly reduce the incidence of hamstring injury.

CONCLUSION
Based on our findings, it can be concluded that the addition of a
strength training program using LI-BFR for hamstrings during preseason
enhanced Hcon:Qcon of professional soccer players with Hcon:Qcon
imbalance. Furthermore, our data indicate that LI-BFR induced increase

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 BLOOD FLOW RESTRICTION AND MUSCLE STRENGTH IMBALANCE VOL. 6 (4)

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