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JEPonline
Chronic Effect of Strength Training with Blood Flow
Restriction on Muscular Strength among Women with
Osteoporosis
Júlio Silva1, Gabriel Rodrigues Neto1, Eduardo Freitas1, Elísio Neto1,
Gilmário Batista1, Mônica Torres2, Maria do Socorro Sousa1
1Physical Education Graduate Program, Federal University of Paraíba
(UFPB), Paraíba, PB, Brazil, 2State University of Rio de Janeiro
(UERJ), Rio de Janeiro, RJ, Brazil
ABSTRACT
Silva J, Neto GR, Freitas E, Pereira Neto E, Batista G, Torres M,
Sousa MS. Chronic Effect of Strength Training with Blood Flow
Restriction on Muscular Strength among Women with Osteoporosis.
JEPonline 2015;18(4):33-41. The aim of this study was to analyze the
chronic effect of strength training (ST) combined with blood flow
restriction (BFR) on maximal dynamic strength (MDS) in osteoporotic
women. Fifteen elderly women with osteoporosis, aged 62.2 ± 4.53
yrs, took part in the study. They were proportionally randomized into
three groups: (a) low-intensity strength training with BFR (LI+BFR); (b)
high intensity exercise (HI); and (c) control (CON). Experimental
groups performed knee extensions for 12 wks, 2 times·wk-1. The CON
subjects maintained their normal daily activities. They did not perform
any type of exercise during the study period. The one-repetition
maximum (1-RM) test was performed to assess MDS pre-test and at
6th- and 12th-wks. Outcomes showed significant increases in the
MDS when the pre-test and the 12th-wk values were compared for the
HI and LI+BFR groups (P<0.001; P=0.004), respectively. The ES of
LI+BFR was also effective in improving MDS levels. Therefore, this
method of intervention might be an effective alternative for special
groups, particularly osteoporotic women.
Keywords: Strength Training, Osteoporosis, Women, Kaatsu
Journal of Exercise Physiology
online
August 2015
Volume 18 Number 4
Editor-in-Chief
Tommy Boone, PhD, MBA
Review Board
Todd Astorino, PhD
Julien Baker, PhD
Steve Brock, PhD
Lance Dalleck, PhD
Eric Goulet, PhD
Robert Gotshall, PhD
Alexander Hutchison, PhD
M. Knight-Maloney, PhD
Len Kravitz, PhD
James Laskin, PhD
YitAun Lim, PhD
Lonnie Lowery, PhD
Derek Marks, PhD
CristineMermier, PhD
Robert Robergs, PhD
Chantal Vella, PhD
Dale Wagner, PhD
Frank Wyatt, PhD
Ben Zhou, PhD
Official Research Journal
of the American Society of
Exercise Physiologists
ISSN 1097-9751
Official Research Journal of
the American Society of
Exercise Physiologists
ISSN 1097-9751
34
INTRODUCTION
In Brazil, it is estimated that ~10 million people suffer from osteoporosis (9). According to the World
Health Organization (22), this disease is the second-largest health care problem in the world followed
by cardiovascular disorders. Osteoporosis is a metabolic bone disorder characterized by decreased
bone mineral density (BMD) with deterioration of the bone microarchitecture. The disorder occurs
most frequently after menopause (20). Combined with the decrease in muscle mass, BMD decreases
the capacity to produce strength that leads to increased skeletal fragility and fractures due to falls
(13). On the other hand, strength training (ST) is an excellent treatment to increase the size and
strength of the muscles to help maintain and/or increase BMD in people with osteoporosis (2). As a
result, there is anticipated reduction in the risk of falls along with an increase in functional capacity
(8).
Thus, high-intensity ST improves the performance of daily activities among older adults and people
with osteoporosis (21,28,26). The physiological mechanisms associated with high-intensity ST (≥
70% of one-repetition maximum, 1-RM) and improvements in BMD are attributed to the stress
imposed on the joints, the muscles, and the skeletal structures in which the muscles originate and
insert (6). Yet, several studies show that low-intensity ST (20 to 50% of 1-RM) combined with blood
flow restriction (BFR) produces similar strength and muscle mass gains without causing great stress
to the joints resulting from high-intensity ST (1,11,16). This means the combination of ST with BFR
may be a better alternative, especially at the beginning of the training sessions to increase muscle
strength and muscle mass in older adults.
The low-intensity ST with BFR method is carried out with the use of an inflatable cuff to restrict blood
flow to and from the muscles. The BFR results in significant intramuscular changes and neural activity
(25,27) that is associated with a rapid recruitment of type II motor units (18). These are also changes
observed in high-intensity ST that are important for developing strength, increasing muscle mass, and
improving functional capacity.
While the benefits of performing ST with BFR among older adults without osteoporosis are already
documented [e.g., increased muscle strength (10,30), improved bone markers (4,11,17), and
improved hormonal response (7,23)], the purpose of this study was to analyze the chronic effect of
strength training (ST) combined with BFR on maximal dynamic strength (MDS) in osteoporotic
women.
METHODS
Subjects
Fifteen osteoporotic women agreed to participate as subjects in this study. They were proportionally
randomized into three groups: (a) low-intensity ST group with blood flow restriction (LI+BFR); (b)
high-intensity ST group (HI); and (c) control group (CON), which was not exposed to exercise (refer to
Table 1 for subject characteristics). The sample size was calculated using G*Power 3.1® software
(Ausseldorf, Bundesland, Germany). Based on a post-hoc analysis, an alpha level of P≤0.05, a
correlation coefficient of 0.5, and an effect size of 0.80 were used for n = 15 subjects. We found that
the sample size was sufficient to provide 80.9% statistical power. To calculate the sample size, the
procedures suggested by Beck were adopted (3).
35
Table 1. Sample Characteristics.
Variables
Control
(n=5)
HI
(n=5)
LI+BFR
(n=5)
Age (yrs)
62.20 ± 4.08
61.80 ± 6.01
62.60 ± 4.33
Height (cm)
152.96 ± 6.59
150.56 ± 4.85
151.78 ± 5.99
Body Mass (kg)
58.52 ± 12
57.32 ± 8.56
63.98 ± 11.91
Note: Values are expressed as the means ± standard deviations; HI = high-intensity group; LI+BFR = low-
intensity group combined with blood flow restriction.
Women with the following characteristics were included in the study: (a) chronological age greater
than 50 yrs; (b) six months without performing lower-limb strengthening activities; and (c) previous
diagnosis of osteoporosis with a T-score lower than -2.5 SD. After the study’s possible risks and
benefits were explained, the subjects signed an informed consent form prepared in accordance with
the Declaration of Helsinki. The study was approved by the Human Research Ethics Committee
under protocol no. 100/13.
Instruments
Determination of BFR
The BFR procedure was performed by vascular Doppler (MedPej® DV-2001, Ribeirão Preto, State of
São Paulo - SP, Brazil), in which the transducer was placed on the posterior tibial artery. A blood
pressure cuff (18 cm in width and 80 cm in length) was secured to the thigh (inguinal fold) and inflated
to the point that the auscultatory pulse of the tibial artery was interrupted (15). The tourniquet
pressure used during the training protocol was set as 80% of the pressure required for complete BFR
in the resting state (15). The cuff was deflated between the series. The mean pressure used
throughout the exercise protocol was 104.20 ± 7.88 mm Hg.
Maximum Strength Measure (1-RM)
The MDS (1-RM) was determined following the recommendations of the American Society of
Exercise Physiologists (5) and was performed using a leg extension machine (Body Fitness, Brazil)
unilaterally (right lower limb). The sample subjects were instructed not to perform physical activities or
strenuous efforts for at least 24 hrs prior to the tests. To warm up, a series of 5 to 10 repetitions of
knee extensions were performed on the same machine on which the test was performed, with a load
of 40% of the perceived 1-RM. After 1-min of rest, the subjects performed a second series of 3 to 5
repetitions with 60 to 80% of the perceived 1-RM load. Subsequently, the subjects tried to perform a
maximum repetition. The load was measured regardless of the goal being achieved or not. The
subjects had at most five attempts with 5-min intervals between them to allow for measurement of the
1-RM. In case the 1-RM could not be measured in these five attempts, this process was repeated
after 72 hrs. No pause was allowed between the concentric and the eccentric phase of a repetition or
between repetitions. The maximum strength was evaluated pre-test and at the 6th-wk and the 12th-
wk.
36
Procedures
ST Program
The ST program lasted 12 wks. It was designed with two weekly sessions separated by a 48-hr
interval (totaling 24 sessions). The exercise used was unilateral knee extension (right leg). The
experimental groups performed a 3-min warm-up on a stationary bicycle. The HI group performed the
exercise with four series until concentric failure with a load corresponding to 80% of 1-RM and a 2-
min rest interval between series (mean of 8.0 ± 2.01 repetitions per series; Figure 1A). The LI+BFR
group performed four series, until concentric failure, with a load corresponding to 30% of 1-RM, a 30-
sec rest interval between series (mean of 7.0 ± 3.38 repetitions per series), and the BFR using an
inflatable cuff (Figure 1B). The CON subjects maintained their normal daily activities without a
commitment to any type of physical exercise or strenuous activity involving the lower limbs throughout
the study’s intervention period and until the post-test was performed.
Statistical Analyses
The descriptive results are expressed as the means ± standard deviations. The effect size was used
to determine the magnitude of changes between the assessed time-points (24), and the percentage
variation (Δ%) was used to express possible differences in muscle strength between the first and the
third evaluations (post-test). Analysis of variance of repeated measures [3 x 3; protocols (BRF vs. HI
vs. CON) x time (pre-test vs. 6th-wk vs. 12th-wk)] followed by the Bonferroni’s post hoc test were
used to evaluate the effects of exercise for all dependent variables. The significance level adopted
was P≤0.05. No assumption of the use of the parametric statistics was violated. All analyses were
37
performed in the statistical software Statistical Package for the Social Sciences (SPSS) version 20.0
(SPSS Inc., Chicago, IL, USA).
RESULTS
In the intergroup comparison of the MDS, significant differences were observed at the 6th-wk when
evaluating LI+BFR vs.CON groups (P=0.004) and at the 12th-wk when evaluating LI+BFR vs. CON
and HI vs. CON groups (P=0.004 and P=0.017, respectively) (Table 2). In the intragroup analysis,
the HI group exhibited a significant difference when comparing pre- vs. 6th-wk, pre- vs. 12th-wk and
6th-wk vs. 12th-wk (P<0.001, ES = 1.44, ∆%= 18.35; P<0.001, ES= 2.77, ∆% = 34.5; P=0.002, ES =
1.39, ∆%= 13.65, respectively). For the LI+BFR group, there was a significant difference when
comparing pre- vs. 6th-wk and pre- vs. 12th-wk (P=0.006, ES = 5.71, ∆%= 0.30; P=0.004, ES = 0.63,
∆%= 10.59). The CON group did not exhibit significant differences between the three assessed time-
points (P>0.05).
Table 2. Comparative Analysis of Maximum Dynamic Strength (1-RM) between the Study
Groups.
RM
Control
HI
LI+BFR
Pre-
27.98 ± 3.74
27.78 ± 3.45
35.85 ± 6.72
6th- WK
27.94 ± 3.76
32.88 ± 3.21*
37.90 ± 5.71*
12th-WK
27.83 ± 3.58
37.37 ± 4.58*
40.10 ± 7.39*
Note: *Significant differences between pre- and 6th-wk, pre- and 12th-wk and 6th-wk and 12th-wk (P<0.05); HI
= high-intensity group; LI+BFR = low-intensity group combined with blood flow restriction.
DISCUSSION
This study analyzed the chronic effect of ST combined with BFR on the MDS of women with
osteoporosis. The data from this study show significant increases in MDS in the two assessment
time-points after the intervention program started in both experimental groups, but with no significant
differences between them. These results corroborate those obtained by Mosti et al. (19), who
observed increased maximum strength levels after a high-intensity intervention period (85 to 90% of
1-RM) over 12 wks. The same authors also observed improved BMD levels. In the study by Mosti et
al. (19), the exercises were performed 3 times·wk-1, while in the present study, the exercises were
performed 2 times·wk-1 without BFR. In the present study, considering that significant increases in
MDS were observed with and without BFR, we can infer that performing the exercises 2 times·wk-1
with and without BFR seems to be sufficient to observe increased MDS in the analyzed periods and
in the studied population. Thus, ST with BFR may be an alternative for improving MDS levels
provided that a high volume of exercise is performed (greater than or equal to 2 times·wk-1).
The effects of exercise with BFR for increasing muscle strength (11,29) are well known. This
improvement is justified by increased muscle hypertrophy and neuromuscular adaptations (29).
Several studies have also observed increased muscle strength when using ST with BFR in older
adults (10,12,30). However, to the best of our knowledge, the present study is the first to study the
effects of ST with BFR in a population of subjects with osteoporosis.
38
Based on studies by Karabulut et al. (10) and Yasuda et al. (30), it seems that performing ST with
BFR promotes increased muscle strength in older adults whether or not they have osteoporosis.
When analyzing the studies by Karabulut et al. (10) and Yasuda et al. (30) and comparing them to the
present study, one observes that even when exercises are performed unilaterally, strength gains may
be similar to those obtained when exercises are performed bilaterally (i.e., ST with BFR can be
performed both unilaterally and bilaterally to increase the strength of older adults). Thus, we
speculate that there was an increase in muscle strength levels for the LI with BFR and HI groups and
that a consequent increase in MDS would occur. This result would be a counterpoint for the assertion
that high-intensity and high-impact ST would be the only effective way of increasing levels of strength,
hypertrophy, and gain in the formation or maintenance of bone mass (21,26,28).
Several studies have observed positive effects of ST with BFR on bone markers (4,11,17). Although
ST with BFR has shown positive effects for bone metabolism, and its contribution for the recovery of
bone trauma has been reported (17), it is not yet clear how this training affects bone metabolism. In a
study conducted with a population of elderly men (11) that used the knee extension exercise with
BFR, positive responses were observed in osteoblast activity and muscle strength. Similarly, Kim et
al. (14) reported positive increases in both bone turnover markers and muscle cross-sectional area in
older adults who trained with and without BFR. However, subjects who performed high-intensity
training exhibited the greatest gains and showed improved bone turnover, based on higher responses
of the bone anabolic marker for that type of exercise. Similarly, Bemben et al. (4) observed that, after
a session of ST with BFR, the analyses of bone markers of absorption and reabsorption indicated an
increase in osteoblast activity and a decrease in osteoclast activity. Thus, ST with BFR seems to be
effective for developing bone tissue because it indicates a positive response in bone rehabilitation
(14). Based on the above and on the articles mentioned previously, it seems that similarly to high-
intensity ST, ST with BFR can improve bone markers.
Thus, based on the abovementioned findings and the data from the present study, ST performed in
combination with BFR is effective for increasing MDS in the elderly population with osteoporosis.
Because improvements in bone markers were observed in other studies with the use of BFR, it is
reasonable to expect that this method will be an alternative intervention in this population. However,
further studies are needed to assess the efficacy of using ST with BFR in the BMD of elderly
populations with osteoporosis. Therefore, we recommend that high- and low-intensity training with
BFR be used to prevent and control osteoporosis.
CONCLUSIONS
Low-intensity ST combined with BFR seems to be effective for increasing MDS in elderly women with
osteoporosis. Thus, this method seems to be an effective alternative for special population groups,
especially in women with osteoporosis.
Address for correspondence: Neto GR, MD, Department of Physical Education - Associate
Graduate Program in Physical Education UPE / UFPB, Federal University of Paraíba, University City,
Research Center for Human Movement Sciences, Kinanthropometry Laboratory, Room 06 and 08.
Castelo Branco. João Pessoa – 58051-900, Brazil. / Phone: 55 083 9612-2726 E-mail:
gabrielrodrigues_1988@hotmail.com
39
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