Experimental Gerontology 114 (2018) 78–86

Contents lists available at ScienceDirect

Experimental Gerontology
journal homepage: www.elsevier.com/locate/expgero

Effect of 16 weeks of resistance exercise and detraining comparing two T

methods of blood flow restriction in muscle strength of healthy older
women: A randomized controlled trial
⁎
Rubens Vinícius Letieria,b, , Ana Maria Teixeirab, Guilherme Eustáquio Furtadob,
Carminda Goersch Lambogliac, Jordan L. Reesc, Beatriz Branquinho Gomesb
a
Multidisciplinary Research Nucleus in Physical Education (NIMEF), Federal University of Tocantins (UFT), Tocantinópolis, Brazil
b
Research Center for Sport and Physical Activity, CIDAF (UID/PTD/04213/2016), Faculty of Sports Sciences and Physical Education – University of Coimbra (FCDEF-
UC), Portugal
c
Faculty of Kinesiology, Sport, and Recreation, University of Alberta, Edmonton, Canada

A R T I C LE I N FO A B S T R A C T

Section Editor: Christiaan Leeuwenburgh Objective: The objective of this study was to compare the effect of 16 weeks of resistance training using different
Keywords: occlusion pressures, followed by 6 weeks of detraining on the muscular strength levels of older women.
Occlusion training Methods: This randomized-controlled trial included 56 recreationally active women (68.8 ± 5.09 years), ran-
Older adults domized into 5 groups: 1) Low-intensity with blood flow restriction “High” (LI + BFR_H): with higher occlusion
Isokinetic torque pressure, 2) Low-intensity with blood flow restriction “Low” (LI + BFR_L): with lower occlusion pressure, 3)
High-intensity (HI), 4) Low-intensity (LI), and 5) Control Group (CG). Participants completed 16 weeks of re-
sistance exercise training, followed by a 6-week detraining period. Maximal isokinetic torque (N.m) of right and
left knee extension (PTRE/PTLE) and flexion (PTRF/PTLF) was measured at pre-training, post-training and
immediately following the detraining period.
Results: Increased strength was observed in the LI + BFR_H, LI + BRF_L and HI groups post-training compared
to baseline in the PTRE (Δ% = 27.2, 15.75 and 13.81%, p < .05, respectively), PTLE (Δ% = 25.2, 18.95 and
30.39%, p < .05, respectively), PTRF (Δ% = 36.7, 22.79 and 34.97%, p < .05, respectively) and PTLF in the
groups (Δ% = 35.8, 24.93 and 26.14%, p < .05, respectively). Following the detraining period, the
LI + BFR_H, LI + BFR_L and HI groups had a decrease in strength levels, but values did not decrease below
baseline level.
Conclusion: Low intensity BFR resistance exercise increases muscle strength in older women similar to HI, with
higher occlusion pressures being more effective. Muscle strength was well preserved following a 6-week de-
training period, and although reductions were observed, some preservation of strength can be explained by
possible neural adaptations to exercise.

1. Introduction hospitalization, and mortality (Cook et al., 2017). Moreover, skeletal

The maintenance of muscle mass as we age is a factor of great re-
levance for overall health, quality of life and longevity (Seguin and
Nelson, 2003). Age-related reductions in muscle mass and strength may
be explained by a number of factors, such as the reduction in the ac-
tivation of motor units (Kamen et al., 1995), decrease in individual
muscle fiber size and fiber loss (Lexell et al., 1988) and the inability to
fully activate some muscle groups (Enoka, 1988). It has been demon-
strated that low levels of muscle strength of the knee extensor muscles
are associated with low physical function, increased disability,
muscle has a remarkable ability to withstand a wide variety of de-
mands, from rapid force production to sustaining overloads for long
periods of time (Brook et al., 2016).
The observed decline in strength and muscle mass are linked to the
loss of muscle contractile protein material (Kalyani et al., 2014), mainly
due to a decrease in the cross-sectional area of fast twitch fibers (i.e.,
type II) (Verdijk et al., 2014). Normally, men have more muscle mass
than women, especially in the upper body, but from the fifth decade,
regardless of gender, the reduction of muscle mass is more pronounced
in the lower limbs (Janssen et al., 2000), an influential factor in the

⁎
Corresponding author at: Universidade Federal do Tocantins (UFT), Avenida Nossa Senhora de Fátima, 1558 – Centro, Tocantinópolis, TO, Brazil.
E-mail address: rubens.letieri@gmail.com (R.V. Letieri).

https://doi.org/10.1016/j.exger.2018.10.017
Received 10 July 2018; Received in revised form 5 October 2018; Accepted 22 October 2018
Available online 01 November 2018
0531-5565/ © 2018 Elsevier Inc. All rights reserved.
R.V. Letieri et al.
impairment of age-related functional capacity (Janssen et al., 2002).
One of the auxiliary strategies in the treatment and prevention of
the deleterious effects of aging is the use of resistance exercise (RE). ER
has a potent effect in increasing skeletal muscle size and strength (Scott
et al., 2014). The effectiveness of an RE program is largely determined
by the manipulation of acute training variables such as muscle action,
load and volume, exercise selection and order, rest periods, repetition
rate, and training frequency (Bird et al., 2005).
Many resistance training (RE) studies in older adults have a dura-
tion ranging from 4 to 48 weeks, and most of them were designed fol-
lowing conventional exercise recommendations for older adults, and
included two to three non-consecutive sessions per week of one to three
sets of 10 to 15 repetitions (Nelson et al., 2007). These studies used
classic weight-lifting exercises such as leg press and leg squat. Other
interventions have included resistance training at high speed (e.g.,
focus on movement speed) (Earles et al., 2001) or explosive type heavy
resistance training, (e.g., 75%–80% of 1-repetition maximum (1RM)
performed with maximum intentional acceleration during the con-
centric movement phase) (Caserotti et al., 2008). However, part of the
elderly population is often unable to exercise at high intensities. The
intensity, frequency, and duration of training affect the training out-
come. Due to the risks associated with training, low motivation and/or
low functional capacity of the elderly, training duration may be the
main factor that improves the training result in these patients (Yoshiko
et al., 2017). However, long training can discourage participation and
adherence to exercise in the elderly. In terms of motivation and long-
term adherence, low-resistance exercises may be more appropriate for
the elderly than high-resistance exercises (Van Roie et al., 2015). Low
intensity (LI) resistance exercise (~20–30% 1RM) with peripheral
blood flow restriction (BFR) has been shown to be efficient in increasing
strength and muscle mass to a similar extent as high intensity (HI)
exercises (Karabulut et al., 2010; Laurentino et al., 2016). Blood flow
restriction in combination with LI exercise imposes less mechanical
load in joints compared to HI exercise and can increase strength and
muscle mass similarly (Slysz et al., 2016). If older adults achieve sa-
tisfactory levels of strength and muscle mass development through LI
BFR exercise, these adaptations may contribute to improved physical
function and quality of life (Cook et al., 2017). In addition, low in-
tensity training combined with BFR could reduce tensile forces in the
ligaments and joints when compared to resistance training of higher
intensity (> 60% of 1RM), decreasing the incidence of injury while still
promoting strength (Shinohara et al., 1998; Takarada et al., 2002).
Despite the clinical relevance of BFR, occlusion pressures considered
optimal for this population remain unknown. The occlusive pressure
used is a factor that must be individualized in the search for a safe and
effective application. Research in healthy individuals identified thigh
circumference as an important predictor of occlusion pressure
(Loenneke et al., 2012a, 2012b), with larger limbs requiring greater
pressure to achieve the same level of occlusion as in the smaller limbs
(Heitkamp, 2015). Therefore, setting pressures throughout a clinical
cohort may not restrict blood flow to the same extent in all individuals.
Fig. 1. Timeline of the study intervention; LI + BFR_H = Low-intensity exercise with blood flow restriction “High”; LI + BFR_L = Low-intensity exercise with blood
flow restriction “Low”; HI = High-intensity exercise; LI = Low-intensity exercise.
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Experimental Gerontology 114 (2018) 78–86
This may result in adverse cardiovascular outcomes, particularly if the
selected pressures result in complete arterial occlusion. This is the first
study with the BFR method to verify the effectiveness of occlusion
pressure based on limb circumference, systolic and diastolic blood
pressure in elderly women, which theoretically could induce higher
pressures without the risk of total arterial occlusion. Previous research
conducted by our laboratory with young individuals (Letieri et al.,
2016), revealed that the determination of pressures based on limb cir-
cumference, systolic and diastolic blood pressure, are usually more
intense. In this way, we hypothesized that the use of more intense
pressures could lead to greater activation of motor units in the elderly
and, consequently, greater strength development.
The present study aimed to compare the effect of 16 weeks of re-
sistance exercise and BFR followed by 6 weeks of detraining using 2
different occlusion pressures on muscle strength levels in older women.
In addition, after exercise withdrawal, we were interested in verifying
whether acquired strength levels tended to have less substantial de-
clines or if these were similar to the ones observed with high intensity
training without occlusion.
2. Methods
2.1. Initial procedures and ethical aspects
This study is a double-blind, randomized-controlled, parallel, five-
arm prevention trial. This study is enrolled in the Brazilian Registry of
Clinical Trials (ReBEC), number (RBR-2xfgdh).
Participants were recruited through a community exercise program
and were classified as “recreationally active” in that they were physi-
cally active but were not participating in structured resistance training.
Potential participants underwent initial screening to determine elig-
ibility for the study. This included a local interview to verify interest
and clinical condition. The study was approved by the ethics committee
of Quixadá Catholic University Center (n°1.175.175). All participants
were informed about the purpose and risks of the study and provided
written consent for voluntary participation according to Resolution
466/12 of the National Health Council (CNS/MS) in ethics for research
with humans, following the guidelines for ethics in scientific experi-
ments in exercise science research and in accordance with the guide-
lines for human research in the Declaration of Helsinki.
Eligibility criteria included females, 60 years or older with no
musculoskeletal limitations, no reported terminal illness or history of
acute myocardial infarction, peripheral cardiovascular disease, and
blood pressure < 130/80 mm Hg. Participants could not have partici-
pated in a resistance training program in the 6 months prior to the
study. Exclusion due to absence from training sessions only occurred for
participants who decided to voluntarily withdraw from the program for
personal reasons.
R.V. Letieri et al. Experimental Gerontology 114 (2018) 78–86

Fig. 2. CONSORT flow diagram.

Table 1
Baseline characteristics.
LI + BFR_H (N = 11) LI + BFR_L (N = 11) HI (N = 10) LI (N = 12) CON (N = 12) p value

Mean (SD) Mean (SD) Mean (SD) Mean (SD) Mean (SD)

Age (years) 68.0 (3.79) 69.4 (5.73) 66.75 (4.43) 71.27 (4.73) 69.0 (6.39) 0.298
Weight (kg) 68.0 (10.63) 64.35 (8.45) 69.5 (11.73) 65.17 (8.32) 67.24 (5.28) 0.692
Height (m) 1.55 (0.06) 1.53 (0.03) 1.52 (0.04) 1.51 (0.05) 1.5 (0.03) 0.183
BMI (kg/m2) 28 (3.03) 27.09 (2.58) 29.72 (4.75) 28.49 (3.65) 29.6 (1.76) 0.352

LI + BFR_H = Low-intensity exercise with blood flow restriction “High”; LI + BFR_L = LI + BFR_H = Low-intensity exercise with blood flow restriction “Low”,
HI = High-intensity exercise; LI = Low-intensity exercise; CON = Control Group.

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R.V. Letieri et al.
2.2. Study design
The total duration of the study was 26 weeks, and included 1 week
of familiarization testing, 1 week of pretesting, 16 weeks of direct in-
tervention (3 times per week for a total of 48 sessions), 1 week of post-
testing, 6 weeks of detraining, and 1 week of post-testing (Fig. 1).
2.3. Participants
The sample consisted of 56 women (68.8 ± 5.09 years) partici-
pating in a community exercise program. The participants were ran-
domized into 5 groups (Fig. 2): 1) Low-intensity exercise with blood
flow restriction “High” (LI + BFR_H), 2) Low-intensity exercise with
blood flow restriction “Low” (LI + BFR_L), 3) High-intensity exercise
(HI), 4) LI-intensity exercise (LI) and 5) Non-exercise Control Group
(CON). Baseline characteristics of participants are shown in Table 1.
2.3.1. Calculation of the sample, allocation of participants and “blinding
effect”
The sample size proposed for this study was based on an earlier
study including older adults who completed BFR training for femoral
quadriceps (Karabulut et al., 2010). Based on a power of analysis of the
record in knee extension strength after BFR (η2 = 0.15) or HI
(η2 = 0.34), the number of subjects required for each group was 8. The
alpha was set at 0.05 and power at 0.85 (G*Power 3.1.0, Universität
Kiel, Germany).
Participants were randomized in a ratio (1:1) by members of the
research team who were not involved in the assessments. A random
number generator was used (www.randomization.com) to allocate the
participants to the groups. Participants were not informed of the ex-
ercise intervention they would participate in and were instructed not to
discuss their experiences with other study participants. Interventions
were conducted individually and staggered to avoid interaction be-
tween participants. Before and after the intervention protocol, each
participant was assessed by the same evaluator who was not involved in
any of the phases of the exercise program and was not aware of the
allocation of participants in each group. All members of the research
team were trained in relation to study protocols and assessments.
2.4. Instruments and procedures
2.4.1. Body mass and height
Body mass (kg) and height (m) were evaluated using a mechanical
anthropometric scale with an accuracy of 0.100 g with coupled stadi-
ometer and 0.1 cm precision (Whelmy®, Brazil).
2.4.2. Assessment of muscle strength
In order to prescribe a relative training intensity for each partici-
pant, muscular strength was determined at baseline using the 1 re-
petition maximum (1RM) method described by (Brzycki, 1993). The
formula used to calculate 1RM was: 1RM = 100 ∗ charge in kilos /
(102.78–2.78 × number of repetitions). Relative intensity was then
prescribed as a percentage of 1RM (% RM). Reliability of this method
for the application in strength exercises for upper and lower limbs was
verified by (Abdul-Hameed et al., 2012).
2.4.2.1. Isokinetic test. The evaluation of lower limb muscle strength
was performed on a Biodex 3 System Pro® isokinetic dynamometer
(Biodex Biomedical Systems, Inc., Shirley, NY) and preliminary cycle
ergometer (Monark Ergomedic 828, Vansbro, Sweden). The maximal
isokinetic torque (N.m) was measured in the concentric-concentric
mode at 60°/s and five maximal repetitions of right/left knee extension
(PTRE/PTLE) and flexion (PTRF/PTLF) (de Amorim Aquino and Leme,
2006).
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Experimental Gerontology 114 (2018) 78–86
2.4.3. Determination of vascular occlusion pressure
Peripheral vascular occlusion pressure was determined by two
methods. For the LI + BFR_H group, pressure was determined using the
formula proposed by Loenneke et al. (2014) for the lower limbs.
Arterial occlusion (mm Hg) = 5.893 (thigh circumference cm)
+ 0.734 (Diastolic blood pressure)
+ 0.912 (Systolic blood pressure) − 220.046
For the LI + BFR_L group, after 5 min of rest, a vascular Doppler
(Martec DV601, São Paulo, SP, Brasil) was positioned on the posterior
aspect of the medial malleolus on the branches of the tibial artery. The
cuff was inflated until the Doppler sound interruption and the values
recorded in mm Hg. The cuff pressure used was set as 80% of the total
blood flow interruption pressure. For both groups, the cuffs were in-
flated shortly before the exercises and remained throughout the session.
After the initial evaluations, participants assigned to the LI + BFR_H
and LI + BFR_L group trained under the pressures of (185.75 ± 5.45
and 105.45 ± 6.5 mm Hg, respectively, p < .05).
2.4.4. Exercise protocol description
The study protocol consisted of a 16-week intervention with
training sessions three times a week. Each session had a maximum
duration of 40–50 min divided into three parts: a) 10 min of warm-up
with standing or sitting exercises of joint mobilization; b) 20 min of
direct intervention for the LI + BFR_H and LI + BFR_L groups and
30 min for the HI and LI groups; c) 10 min of cool down, with an em-
phasis on relaxation through seated or lying postures focusing on
breathing, body awareness, and static stretching. The groups that used
the BFR technique trained under the supervision of at least two tech-
nicians with technical knowledge in BFR training. Exercise prescription
for the BFR groups was 3–4 sets of 15 repetitions, (20–30% of 1RM),
with 30 s rest between sets. Ninety seconds rest was allocated between
different exercises. During the first two weeks, the participants per-
formed 3 sets (30, 15 and 15 repetitions) and increased to 4 sets in the
subsequent weeks. Pneumatic sleeves were inflated and maintained
during all series, including during rest intervals and were deflated
during the transition between exercises (90 s). The selected exercises
included: Squat, Leg Press, Knee Extension and Leg Curl. The HI group
performed the same exercises with 70–80% of 1RM, 3–4 sets of 6–8
repetitions and passive recovery of 60 s rest between sets and 90 s be-
tween exercises. The load was adjusted every 2 weeks. The control
group only participated in the evaluations and did not participate in
any training. All sessions were held in the morning between 7:00 a.m.
and 8:30 a.m. All interventions performed with exercises were recorded
and the participants had full follow-up during the period. To aid in the
adjustment of relative intensities, a perceived effort scale (OMNI) was
used for the exercise of strength (Robertson et al., 2003).
3. Statistical analysis
The normality of the data was verified by the Shapiro-Wilk test. One
Way ANOVA was conducted to examine between group differences at
baseline. Values are expressed as mean ± standard deviation and sta-
tistical significance for the specific comparisons. To compare the mean
changes over time between the groups, Repeated measures ANOVA
(5 × 3: group vs. time) was performed. Tukey Post hoc analysis was
performed for paired comparisons of means when significant interac-
tions were found in the dependent variables (i.e., PTRE, PTLE, PTRF
and PTLF). For all tests, the Huynh-Feldt correction was applied if the
sphericity assumption was violated. The percentage change (Δ%) was
determined by the formula: Δ% = ((post − pre) / pre) × 100. The level
of significance was p < .05. All statistical analysis was done using IBM
SPSS Statistics version 23.0 (Armonk, NY: IBM Corp, USA) and
GraphPad Prism 7 (GraphPad Software, Inc., La Jolla California, USA).
R.V. Letieri et al. Experimental Gerontology 114 (2018) 78–86

4. Results (−1.26%, −1.44%, −1.67%, −1.12% and −0.54%/week respec-

tively). In the PTRF, the values (−1.09%, −2.4%, −1.98%, −1.17%
Baseline characteristics can be found in Table 1. At baseline, there and −0.52%/week, respectively) were observed. In the PTLE
were no differences between groups for age, anthropometric measures (−1.15%, −1.84%, −2.53%, −0.89% and −0.84%/week, respec-
(body mass, height and BMI). There were no differences in peak right/ tively), and in the PTLF variable (−1.15%, −1.84%, −2.53%,
left leg extension/flexion torque (PTRE, p = .093 PTFE, p = .053, −0.89% and −0.84%/week, respectively) (Table 3).
PTRF, p = .09 and PTLF, p = .085). In post-training, when comparing only the groups submitted to BFR
The groups attendance rate was: 84.6% for both the LI + BFR_H and training, the LI + BFR_H group presented values of 8.91% and 7.19%
LI + BFR_L, 76.9% for the HI and 92.3% for both LI and CG. higher in PTRE and PTLE, respectively in relation to LI + BFR_L. In
A group × time interaction condition was observed in the PTRE PTRF and PTLF, the values were 0.33% and 4.29%, respectively, in
(F = 2.34, p = .021), explaining 6.1% of the total variation, PTLE favor of the LI + BFR_L group (Figs. 4, 5).
(F = 2.12, p = .0037), explaining 5.46% of the total variation,
PTRF = 3.80, p < .001, explaining 8.76% of the total variation and 5. Discussion
PTLF (F = 4.37, p < .001), 9.72% explains the total variation. For the
time condition, significant differences were found for PTRE variables To our knowledge, this is the first study examining the effect of
(F = 12.25, p < .001, 8.06% of the total variation), PTLE (F = 14.63, 16 weeks of resistance training and 6 weeks of detraining using two
p < .0001, 9.41% F = 19.24, p < .001, 11.08% of total variation) methods of BFR on muscle strength in healthy older women. The initial
and PTLF (F = 25.31, p < .001, 14.07% of total variation). The hypothesis was that training with individualized occlusion pressure
highest variations were in terms of the groups, where significant values based on limb circumference and systolic/diastolic blood pressure
were verified for the PTRE variables (F = 27.67, p < .001, 36.42% of could generate greater force increases after the 16-week period. Our
the total variation), PTLE (F = 27.92, p .001), 35.92% of F = 30.28, study confirmed this hypothesis, increased occlusion pressures lead to
p < .001, 33.67% of the total variation. Table 2 demonstrates the muscle strength levels similar to traditional training. Results from this
mean difference and the confidence intervals within the groups at the study suggest that moderate and high levels of BFR pressures, in com-
different moments of the intervention. bination with LI resistance exercise, provide similar increases in
Fig. 3 shows the percentage of strength levels achieved after strength to those observed with traditional HI resistance training with
16 weeks of intervention and 6 weeks of detraining. The percentage no BFR in older women. Additionally, after 6 weeks of exercise de-
decline rate was verified by the ratio: %total reduction in detraining/ training the BFR groups and traditional HI group showed sustained
number of weeks of detraining. In the LI + BFR_H, LI + BFR_L, HI, LI muscle strength compared to the LI and CON groups. It is also im-
and CON groups, the mean reduction in the PTRE variable was portant to note that in the group with more intense vascular occlusion
(LI + BFR_H), the percentage values of strength reduction were smaller
Table 2 than traditional HI and LI + BFR_L. In addition, the LI and CON groups
Isokinetic peak torque (N.m) of knee extension. showed no increase in strength and also showed a decrease in strength
PTRE (N.m) PTLE (N.m) levels after the detraining period.
Although previous research has reported low load exercise inter-
Mean (SD) 95% CI Mean (SD) 95% CI ventions combined with BFR to increase strength and lower limb
muscle mass in healthy young (Laurentino et al., 2012; Martín-
LI + BFR_H
Baseline 93.51 (17.43) 84.74–102.27 94.35 (16.08) 85.61–103.08
Hernández et al., 2013), and in older adults (Vechin et al., 2015), there
Post 119.47 110.99–127.95 118.13 109.34–126.93 has been no study to date comparing the effects of more intense oc-
(14.4)a,⁎⁎ (15.02)a,⁎⁎ clusion pressures with lower pressures in older women. It is speculated
Detraining 110.42 101.95–118.88 107.55 99.34–115.75 that protocols with increased peripheral vascular occlusion pressure
(14.2)b,⁎ (12.72)b,⁎
and/or increased exercise intensity may increase anabolic response to
LI + BFR_L
Baseline 94.77 (14.97) 85.57–103.96 92.65 (16.16) 83.49–101.81 exercise (Abe et al., 2012; Loenneke et al., 2015; Sugaya et al., 2011).
Post 109.7 (14.2) 100.80–118.59 110.21 100.99–119.43 This is based on acute findings where increases in occlusion pressure,
(15.21)a,⁎ which may induce increased metabolic stress, were associated with
Detraining 100.25 91.37–109.12 94.34 (13.53) 90.73–107.94
increased motor unit recruitment (Loenneke et al., 2015; Yasuda et al.,
(14.52)
HI
2008). This increased occlusion pressure reduces blood flow to the
Baseline 91.7 (13.48) 83.3–100.09 89.4 (13.04) 81.04–97.76 active muscle, leading to considerable increases in inorganic phosphate,
Post 116.01 107.89–124.13 116.57 108.15–124.99 an indicator of muscle fatigue (Sugaya et al., 2011). Consequently, in
(14.5)a,⁎⁎ (13.7)a,⁎⁎ order to maintain the production of strength, additional motor unit
Detraining 104.36 (13.3) 96.25–112.46 102.73 94.88–110.59
recruitment is required, especially fast twitch motor units (Lixandrão
(12.54)b,⁎
LI et al., 2015). Possible increases in recruitment of motor units, as ob-
Baseline 84.39 (15.22) 75.62–93.15 84.11 (15.49) 75.37–92.84 served in high pressure BRF protocols (Loenneke et al., 2015), may help
Post 85.88 (15.03) 77.39–94.35 86.69 (16.05) 77.89–95.48 explain our findings. Interestingly it has also been observed that BFR
Detraining 80.10 (16.45) 71.64–88.56 80.63 (17.08) 72.43–88.84 with light resistance training may stimulate increased secretion of
CON
Baseline 80.54 (9.86) 71.35–89.73 77.48 (10.38) 68.32–86.64
anabolic hormones such as growth hormone (Takarada et al., 2000).
Post 80.07 (10.96) 71.17–88.96 78.35 (12.09) 69.13–87.58 In the present study, the LI + BFR_H, LI + BFR_L and the HI group
Detraining 77.47 (10.43) 68.59–86.34 75.91 (10.88) 67.31–84.52 showed a significant increase in strength after 16 weeks of direct in-
tervention. A meta-analysis conducted by Loenneke et al. (2012) ex-
LI + BFR_H = Low-intensity exercise with blood flow restriction “High”; amined the effects of BFR exercise on muscle strength, but no study
LI + BFR_L = LI + BFR_H = Low-intensity exercise with blood flow restriction
reached 16 weeks in duration. Interestingly, the authors point out that
“Low”, HI = High-intensity exercise; LI = Low-intensity exercise;
studies with a longer duration (i.e., 9–10 weeks) have greater increases
CON = Control Group. PTRE = Peak Torque Right Extension; PTLE = Peak
Torque Left Extension. in strength. Supporting this, Slysz et al. (2016) point out that BFR in-
⁎⁎
p ≤ .01. terventions longer than 8 weeks were more effective than those
⁎ with < 8 weeks and 30% 1RM exercises were more effective in muscle
p ≤ .05.
a
Different from baseline. strength gains when compared to training performed at intensities of
b
Different from post. 20% of 1RM.

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R.V. Letieri et al. Experimental Gerontology 114 (2018) 78–86

Fig. 3. Δ% values of Peak of torque (N.m) within groups at different moments (post-training and wash-out) in relation to the baseline. a) Δ% of PTRE = Percent of
change of Peak Torque Right Extension, b) Δ% of PTLE = Percent of change of Peak Torque Left Extension; c) Δ% of PTRF = Percent of change of Peak Torque Right
Flexion d) Δ% of PTLF = Percent of change of Peak Torque Left Flexion. LI + BFR_H = low-intensity with blood flow restriction “high”; LI + BFR_L = low-intensity
with blood flow restriction “low”; HI = High-intensity exercise; LI = Low-intensity exercise; CG = Control group. **p ≤ .01; *p ≤ .05.

Table 3 Older women undergoing traditional high-intensity training in-

Isokinetic peak torque (N.m) of knee flexion. creased muscle strength levels to a similar extent as those undergoing
PTRF (N.m) PTLF (N.m)
the BFR interventions. It has been demonstrated that with traditional
resistance training, older adults can increase levels of strength and
Mean (SD) 95% CI Mean (SD) 95% CI muscle mass (Roth et al., 2001), although the rates of this increase are
lower in comparison with younger individuals. Such increases are ex-
LI + BFR_H
plained in part by the neural adaptations resulting from strength
Baseline 55.06 (9.19) 50.13–59.99 53.05 (8.01) 48.44–57.67
Post 75.29 (11.67)a,⁎⁎ 69.00–81.57 72.04 (9.43)a,⁎⁎ 66.70–77.38 training (Häkkinen et al., 1998). Metabolic changes induced by re-
Detraining 70.78 (12.17)a,⁎⁎ 64.44–77.12 67.06 (10.03)a,⁎⁎ 61.44–72.67 striction of blood flow may play an important role in muscle activation
LI + BFR_L (Yasuda et al., 2008). With the external compression induced by BFR
Baseline 61.52 (8.83) 56.35–66.69 60.25 (8.11) 55.41–65.09
training, significant changes occur in oxygen saturation in the venous
Post 75.54 (12.49)a,⁎⁎ 70.94–84.13 75.27 (9.29)a,⁎⁎ 69.66–80.87
Detraining 69.62 (13.7) 62.96–76.27 66.98 (11.37) 61.08–72.15
blood, partial pressure of oxygen, accumulation of hydrogen ions and
HI lactate, thus inducing a greater recruitment of motor units (Takarada
Baseline 59.05 (7.27) 54.33–63.78 57.81 (6.78) 53.39–62.23 et al., 2000).
Post 79.7 (10.53)a,⁎⁎ 73.68–85.72 78.7 (8.26)a,⁎⁎ 73.58–83.81 In the present study, the participants had a detraining period of
Detraining 69.25 (8.57)a,b,⁎ 63.17–75.32 66.77 (7.15)a,b,⁎ 61.39–72.15
6 weeks. It was observed that in the higher intensity group, muscle
LI
Baseline 53.65 (9.59) 48.72–58.58 53.43 (9.67) 48.81–58.05 strength did not decline to baseline values. These results are similar to
Post 55.51 (9.55) 49.22–61.80 54.61 (9.53) 49.27–59.95 results observed previously by Tokmakidis et al. (2009), who observed
Detraining 52.3 (9.83) 45.95–58.64 51.71 (10.41) 46.09–57.33 that the muscular strength reached by older adults following traditional
CON
HI and moderate intensity training tended to decline with detraining,
Baseline 51.74 (4.66) 46.57–56.46 52.03 (4.32) 47.19–56.87
Post 49.83 (6.45) 43.27–56.46 52.14 (4.55) 44.15–55.35
but levels remained higher than pre-training values. The authors report
Detraining 47.89 (6.86) 41.23–54.54 49.51 (3.84) 41.75–53.53 that gains obtained during the training period likely contribute to the
maintenance of strength and muscle mass. In a study by Yasuda et al.
LI + BFR_H = Low-intensity exercise with blood flow restriction “High”; (2014), it was found that after 12 weeks of exercise intervention using
LI + BFR_L = LI + BFR_H = Low-intensity exercise with blood flow restriction BFR and 24 weeks of detraining there was no sufficient decline of
“Low”, HI = High-intensity exercise; LI = Low-intensity exercise; muscle strength obtained with the training. This may be due to greater
CON = Control Group. PTRF = Peak Torque Right Flexion; PTLF = Peak
increases in muscular size accompanied by exercise with BFR and
Torque Left Flexion.
⁎⁎ neural adaptations, by increasing in recruitment of motor units. Simi-
p ≤ .01.
⁎
p ≤ .05. larly, Yasuda et al. (2012) found that increases in muscle strength in
a
Different from baseline. young men undergoing concentric and eccentric exercise with BFR,
b
Different from post. were well preserved after 6 weeks of detraining in the exercise with BFR
group. The authors of this study point out that the maintenance of
strength achieved after detraining was likely due to muscle hyper-
trophy.

83
R.V. Letieri et al.
Fig. 4. Tukey's post hoc test of Peak of torque (N.m) in post training. LI + BFR_H = low-intensity with blood flow restriction “high”; LI + BFR_L = low-intensity with
blood flow restriction “low”; HI = High-intensity exercise; LI = Low-intensity exercise; CG = Control group. **p ≤ .01; *p ≤ .05.
Similar results were observed by Yasuda et al. (2015) who examined
the effect of resistance band exercise and BFR on muscular strength of
older women after 12 weeks of intervention and 12 weeks of detraining.
The authors found that values of Maximal Voluntary Contractions
(MVC) observed after detraining of elbow flexors and extensors were
higher than baseline values, although a weekly muscular strength de-
cline of −0.29% per week for flexion and −0.20% for elbow extension,
respectively, was observed. Corroborating in parts, in our study, the
maintenance in the strength levels also well preserved after the washout
when compared to the strength levels achieved after the 16 weeks of
intervention. The rate of weekly decline was higher than in the study of
Yasuda et al. (2015), however, the total percentage achieved with the
intervention and the difference in muscle groups analyzed should be
considered.
Limitations of the present study include the absence of hormonal
and immunological blood parameters, such as growth hormone, IGF-1,
IL-6 and testosterone that may allow for a greater understanding of the
factors contributing to strength gains and declines. Another limitation
was that the study did not use functional measures, such as climbing
stairs or walking. Also, the detraining period was shorter than the in-
tervention period, which makes it difficult to understand whether the
rate of strength decline changes after this period. A longer detraining
period would allow us to better understand this relationship. In addi-
tion, the sample of this study included only women, which does not
allow for the comparison of sex differences or the ability to extrapolate
results to the general population. It should be noted though, that pre-
vious studies have generally included a combination of men and
women.
No adverse effects were observed in this study. However, for safety
reasons, the authors do not recommend extrapolating to people with
84
Experimental Gerontology 114 (2018) 78–86
high blood pressure and/or muscle and joint limitations.
This study presents promising results as it is the first study to
compare the effect of different BFR pressures and exercise intensities on
strength levels following 16 weeks of resistance exercise in older
women. The randomized controlled design of this study allowed for
good internal validity, and therefore an effective evaluation of possible
benefits or adverse effects of exercise intervention with BFR. Exercise
with BFR can be understood as an emerging clinical modality for the
elderly population, since it can achieve important physiological adap-
tations in individuals who cannot safely tolerate exercise with high
muscular tensions or for those with chronic limitations, such as for
example rheumatoid arthritis and osteoarthritis, or even those in the
process of post-surgical rehabilitation that need to minimize the dele-
terious effects of loss of strength and muscle mass.
This research line can have a positive impact on public health,
especially with the elderly population, through the use of alternative
methods to traditional exercise, with relatively low cost and well tol-
erated. Although no adverse effects were observed with the interven-
tion, it is suggested that the follow-up of this type of method be per-
formed by well-trained professionals in exercise with BFR for greater
patient safety.
6. Conclusion
Resistance exercise and BFR in older women increases muscle
strength levels to a similar extent as HI exercise without occlusion, after
16 weeks of intervention, especially with the higher occlusion pres-
sures. Muscle strength gains were well preserved after 6 weeks of de-
training, especially in the higher intensity groups and although reduc-
tions were observed, the preservation of strength in the BFR and HI
R.V. Letieri et al.
Fig. 5. Tukey's post hoc test of Peak of torque (N.m) in detraining. LI + BFR_H = low-intensity with blood flow restriction “high”; LI + BFR_L = low-intensity with
blood flow restriction “low”; HI = High-intensity; LI = Low-intensity; CG = Control group. **p ≤ .01; *p ≤ .05.
groups may be explained by possible neural adaptations to exercise.
Therefore, BFR methods can be considered an effective method in
promoting and retaining muscle strength in older women and it can be
an alternative to traditional exercise, with relatively low cost and well
tolerated, in individuals who cannot safely tolerate exercise with high
muscular tensions or for those with chronic limitations, such as for
example rheumatoid arthritis and osteoarthritis, or even for those in the
process of post-surgical rehabilitation that need to minimize the dele-
terious effects of loss of strength and muscle mass. Further studies of
longer intervention and detraining times are recommended for a better
understanding of what intensity and occlusion pressures are ideal to
elicit the greatest strength gains.
Conflicts of interest
The authors declare that there are no conflicts of interest.
Acknowledgements
The authors thank the University of Fortaleza (UNIFOR) and also
the professionals who participated in the process of daily interventions
and evaluations: Diane Nocrato, Messias Bezerra de Oliveira, Antônio
Evanildo Cardoso de Medeiros Filho, Kaio Breno Belizario de Oliveira,
Francisco Iran da Silva Junior, Gabriel Augusto Rangel de Oliveira, and
85
Experimental Gerontology 114 (2018) 78–86
Laís Aguiar de Lima.
Author contributions
RL designed and implemented the study protocol, performed the
statistical analysis and contributed to the drafting of the manuscript. GF
participated together with RL in the design of the study design and
drafting of the manuscript. AT and BG guided the work and contributed
to the critical and technical revision of the work. RL, GF, AT, JR & CL all
contributed to the drafting and critical revision of intellectual content.
Funds
UNIFOR provided part of the structure necessary for the develop-
ment of the research. Guilherme Furtado was financed by a grant from
CAPES/CNPQ – Brazilian Ministry of Education (BEX: 11929/13-8).
Ana Teixeira and Guilherme Furtado are registered at CIDAF (UID/
PTD/04213/2016).
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