Ferraz Et Al. 2017 PDF

. . .
Published ahead of Print
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Benefits of Resistance Training with Blood Flow Restriction
in Knee Osteoarthritis
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Rodrigo Branco Ferraz2, Bruno Gualano1,2, Reynaldo Rodrigues1, Ceci Obara Kurimori1,
Ricardo Fuller1, Fernanda Rodrigues Lima1, Ana Lúcia de Sá-Pinto1, and Hamilton Roschel1,2
1
Rheumatology Division; Faculdade de Medicina FMUSP, Universidade de Sao Paulo, Sao
Paulo, SP, BR, University of São Paulo, SP, Brazil; 2Applied Physiology and Nutrition Research
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Group - School of Physical Education and Sport, University of São Paulo, SP, Brazil
Accepted for Publication: 14 December 2017

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Copyright © 2018 American College of Sports Medicine

Medicine & Science in Sports & Exercise, Publish Ahead of Print
DOI: 10.1249/MSS.0000000000001530
Benefits of Resistance Training with Blood Flow Restriction in Knee
Osteoarthritis
Rodrigo Branco Ferraz2, Bruno Gualano1,2, Reynaldo Rodrigues1, Ceci Obara Kurimori1,
Ricardo Fuller1, Fernanda Rodrigues Lima1, Ana Lúcia de Sá-Pinto1, and Hamilton Roschel1,2
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1
Rheumatology Division; Faculdade de Medicina FMUSP, Universidade de Sao Paulo, Sao
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Paulo, SP, BR, University of São Paulo, SP, Brazil
2
Applied Physiology and Nutrition Research Group - School of Physical Education and Sport,
University of São Paulo, SP, Brazil

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Corresponding Author:
Dr. Hamilton Roschel, Ph.D.
Escola de Educação Física e Esporte – Universidade de São Paulo

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Av. Melo de Moraes, 65, Butantã – São Paulo, SP - Brazil
Postal code: 05508-030

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E-mail: hars@usp.br
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Disclosure of funding received for this work: Fundação do Amparo à Pesquisa do Estado de São
Paulo (FAPESP) and Conselho Nacional de Pesquisa e Desenvolvimento (CNPq). The authors
declare that they have no competing interests. The results of the present study do not constitute
endorsement by ACSM. The results of the present study are presented clearly, honestly, and
without fabrication, falsification, or inappropriate data manipulation.
Copyright © 2017 by the American College of Sports Medicine. Unauthorized reproduction of this article is prohibited.
ABSTRACT
Purpose: Evaluate the effects of a low-intensity resistance training program associated with
partial blood flow restriction on selected clinical outcomes in patients with knee osteoarthritis
(OA). Methods: Forty-eight women with knee OA were randomized into one of the three
groups: low-intensity resistance training (30% one repetition maximum 1-RM) associated
(BFRT) or not (LI-RT) with partial blood flow restriction, and high-intensity resistance training
(HI-RT: 80% 1-RM). Patients underwent a 12-week supervised training program and were
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assessed for lower-limb 1-RM, quadriceps cross-sectional area (CSA), functionality (timed-
stands test - TST and timed-up-and-go test - TUG), and disease-specific inventory (Western
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Ontario and McMaster Universities Osteoarthritis Index - WOMAC) before (PRE) and after the
protocol (POST). Results: Similar within-group increases were observed in leg-press (26% and
33%, all p<0.0001), knee-extension 1-RM (23% and 22%; all p<0.0001) and CSA (7% and 8%;
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all p<0.0001) in BFRT and HI-RT, respectively, and these were significantly greater (all p<0.05)
than those of LI-RT. BFRT and HI-RT showed comparable improvements in TST (7% and 14%,
respectively), with the latter showing greater increases than LI-RT. TUG scores were not
significantly changed within or between groups. WOMAC physical function was improved in
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BFRT and HI-RT (-49% and -42%, respectively; all p<0.05), and WOMAC pain was improved
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in BFRT and LI-RT (-45% and -39%, respectively; all p<0.05). Four patients (out of 16) were
excluded due to exercise-induced knee pain in HI-RT. Conclusion: BFRT and HI-RT were
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similarly effective in increasing muscle strength, quadriceps muscle mass, and functionality in
knee OA patients. Importantly, BFRT was also able to improve pain while inducing less joint
stress, emerging as a feasible and effective therapeutic adjuvant in OA management. KEY-
WORDS: Arthritis; cartilage; rehabilitation; WOMAC; hypoxia; KAATSU.
INTRODUCTION
Osteoarthritis (OA) is the most common form of arthritis and is considered a major cause
of musculoskeletal pain, functional impairment, and reduced independence in older adults
worldwide (1). For instance, OA-related knee and hip pain are considered direct causes of
impaired walking and stairs climbing in the elderly in Europe and USA, being present in nearly
40% of individuals over the age of 60 (2, 3). OA is a heterogeneous chronic disease traditionally
characterized by cartilage involvement; currently, however, it is considered to involve the whole
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joint, including cartilage, subchondral bone, ligament, muscle, and periarticular soft tissues such
as synovial membrane and menisci. The disease encompasses changes in cartilage metabolism
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and synovial inflammation such as cartilage deterioration, joint space narrowing, osteophytes
formation, and sclerosis of the subchondral bone (4).
Quadriceps muscle weakness is considered not only as an important risk factor for OA (5)
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but also as a main determinant of physical functioning in women with knee OA (6), with
repercussions on proprioception (7) and tendency to falls (8). Additionally, a greater loss in
lower extremity lean mass have been observed in women with knee OA when compared with
healthy controls (9). This reduction in muscle mass is also associated with disease progression
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(10), pain (11) and with both presence and severity of age-related OA (12, 13). Therefore,
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quadriceps strengthening and hypertrophy is thought as a first-line therapy (14), making
resistance training (RT) a common practice within OA management (15, 16).

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In this respect, it has been postulated that the mechanical overload imposed on the muscle
should be between > 65% of the one repetition maximum (1-RM) in order to improve muscle
mass and strength (17). Importantly, patients with OA are often unable to exercise at such high-
intensities, limiting the application of conventional high-intensity RT (HI-RT) in OA not only
due to pain but also to the pathophysiology of the disease (18, 19), thus warranting the
investigation on new and viable strategies to mitigate OA-related symptoms.
Recently, a great deal of attention has been drawn to blood flow restriction training
(BFRT). It generally combines low-intensity (~20-40% 1-RM) RT with partial blood flow
restriction to the working muscles via inflatable air cuffs fixed in the proximal region of the
limbs exercised (20-22). Interestingly, despite the very low intensities adopted in BFRT, it has
been shown to promote increases in muscle size and strength comparable to those observed after
conventional HI-RT (21, 22), constituting a promising strategy for non-pharmacological
intervention in OA. In fact, previous work has demonstrated BFRT to be effective in increasing
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muscle strength in both women at risk for knee OA (23); however, evidence of BFRT efficacy
on OA is still scarce. Bryk et al (24) have provided initial insight into the matter, with data
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showing BFRT to significantly improve muscle strength. It is worth noting that the authors did
not include a control group (i.e. an intensity-matched -30% 1RM - non-occlusion group),
limiting the conclusion regarding possible differential effects of BFRT to those of training
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intensity per se. More importantly, its effects on muscle mass are currently unknown in
individuals with knee OA. Given the association between muscle mass and disease progression
and other clinical features in OA (10-13), specially in older patients, investigating the effects of
BFRT on quadriceps muscle mass constitutes an important clinical question in OA management.

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Therefore, the aim of this study was to compare the effects of BFRT to more traditional
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RT on lower-limb muscle strength and mass, functionally, pain and quality of life in women with
OA. We hypothesized that BFRT would result in similar benefits as compared to conventional
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high-intensity RT while inducing less pain.
METHODS
Study design
This is a randomized controlled trial conducted between January 2011 and July 2013 in
Sao Paulo, Brazil. This study was approved by the local ethical committee and all participants
signed an informed consent form before participation. All of the procedures were in accordance
with the Helsinki Declaration revised in 2008. The trial was registered at clinicaltrials.gov as
NTCT01483131. This manuscript was reported according to CONSORT guidelines (25).
Patients were ranked in tertiles according to their 1-RM in the leg press exercise, then they
were randomized by a computer-generated code into one of the following conditions: (i) high-
intensity resistance training (HI-RT); (ii) low-intensity resistance training (LI-RT), and (iii) low-
intensity resistance training with blood flow restriction (BFRT).
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At baseline (PRE) and after 12 weeks of training (POST), we assessed 1-RM leg press and
knee extension, physical function (as assessed by timed-stands [TST] and timed-up-and-go
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[TUG] tests), quadriceps cross-sectional area (CSA), and self-reported quality of life (as assessed
by Short Form Health Survey [SF-36] and Western Ontario and McMaster Universities
Osteoarthritis Index [WOMAC]). Self-reported adverse events were recorded throughout the
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protocol. Experimental design is illustrated elsewhere (see Supplemental Digital Content 1,
Experimental design, http://links.lww.com/MSS/B161).
Patients
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Women (aged between 50 and 65 years) diagnosed with knee OA according to the
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American College of Rheumatology criteria (26) were selected to participate in the study.
Exclusion criteria were as follows: (i) participation in physical exercise training over the past
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year; (ii) cardiovascular diseases and/or musculoskeletal disturbances which precluded exercise
participation; (iii) Kellgren-Lawrence radiographic grade of 1 or 4; (iv) knee pain numeric visual
scale (VAS) less than 1 or greater than 8; (v) use of nonsteroidal anti-inflammatory drugs over
the past three months; (vi) intra-articular infiltration with hyaluronic acid and corticosteroids
infiltration over the past six months. We decided to include female patients only in this trial, as
knee OA is more prevalent in women than in men (1) and to account for sex variability in
important variables such as muscle strength and mass. Table 1 shows the patients’ main features.
Resistance training programs
RT was performed in an intrahospital gymnasium (Laboratory of Assessment and
Conditioning in Rheumatology, School of Medicine, University of São Paulo). Exercise sessions
occurred two times a week and were monitored by a fitness professional. RT program was
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comprised of bilateral leg press and knee extension exercises using conventional strength
training machines (Nakagym, São Paulo, Brazil).
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In order to acquaint the subjects to their training protocols, the first week of training was
performed as follows: HI-RT performed four sets of 10 repetitions at 50% 1-RM, whereas LI-RT
performed four sets of 15 repetitions at 20% 1-RM. From the second week on, training intensity
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was increased to 80% and 30% 1-RM for HI-RT and LI-RT, respectively, and from the fifth
week on, all groups increased the number of sets performed for each exercise from four to five.
Training intensity and load progression for BFRT was exactly the same as those of LI-RT,
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however, BFRT trained with an air cuff placed at the inguinal fold (width 175 mm x length 920
mm - inflated to 70% of the pressure needed to provide complete blood flow restriction, see
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description below) in order to provide partial blood flow restriction. Importantly, the air cuff and,
hence, blood flow restriction, was sustained throughout the entire training sessions, including
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rest intervals, and was released immediately after the end of the session.
A one-minute rest period was allowed between sets for all groups. Exercise load was
adjusted every four weeks by reassessing patients’ 1-RM. Training intensity and blood flow
restriction increments are comprehensively described elsewhere (Supplemental Digital Content
2, Progression of training loads, http://links.lww.com/MSS/B162). A member of the research
staff monitored the adherence to the exercise program on a session basis.
Determination of the blood flow restriction pressure
Patients were asked to lie on a supine position while resting comfortably. A vascular
Doppler probe (DV-600, Marted, São Paulo, Brazil) was placed over the tibial artery to capture
its auscultatory pulse. For the determination of the cuff pressure (mm Hg) necessary for a
complete blood flow restriction (i.e., pulse elimination pressure), an air cuff was attached to the
patient’s thigh (i.e., inguinal fold region), and then inflated up to the point in which the
auscultatory pulse was interrupted. Cuff pressure utilized during the training protocol was
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determined as 70% of the necessary pressure for complete blood flow restriction in a resting
condition. The average cuff pressure necessary for complete blood flow restriction was 139.2 ±
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10.8 mm Hg, and average cuff pressure used throughout the training protocol was 97.4 ± 7.6 mm
Hg.
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Strength and functional tests
Prior to the 1-RM test, two light warm-up sets interspaced by two minutes were
performed. Afterwards, patients had up to five attempts to achieve the 1-RM load with a three-
minute interval between attempts. 1-RM tests were conducted for the leg press and knee
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extension exercises according to previous description (27).

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Physical function was measured by the TST and the TUG tests. TST evaluates the
number of stand-ups that a subject can perform from a standard armless chair (45 cm of height)
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in 30 seconds (28), whereas TUG assesses the time that a subject requires to rise from a standard
arm chair (45 cm of height), walk to a line on the floor three meters away, turn, return, and sit
down again (29). Testing sessions were conducted without assistive devices.
To avoid learning effects, patients underwent three familiarization sessions (30), at least 48
hours apart, for all strength and functional tests. Coefficients of variation (CV) for 1-RM leg
press, 1-RM knee extension, TST and TUG test-retest were 5.86%, 3.78%, 8.28%, and 3.97%,
respectively.
Quadriceps CSA
Computed tomography imaging (Brilliance CT, 64-slice, Philips Medical System
Technologies LTD) was used to obtain quadriceps CSA. Patients laid in a supine position with
their knees extended and legs straight. A bandage was used to restrain leg movements during the
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test. An initial reference image was obtained to determine the perpendicular distance from the
greater trochanter of the femur to the inferior border of the lateral epicondyle of the femur, which
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was defined as the segment length. Quadriceps CSA was measured at 50% of the segment length
with 0.8 cm slices. Scanning characteristics were as follows: 120 kV, 300 mA, rotation time of
0.75 s, and a field of view of 500 mm. Quadriceps images were traced in triplicates by a
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specialized researcher who was blinded to the treatment, and their mean values were used for
further analysis. Quadriceps CSA measurement’s CV was 0.73 %.
Self-reported quality of life assessment

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Pain, stiffness, and physical function were measured by WOMAC. This instrument is
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validated and recommended by the Osteoarthritis Research Society as the measure of choice
when assessing health status in older adults with knee OA (31). Rating scale ranges from 0
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(none) to 4 (extreme), with higher total scores indicating greater dysfunction. Quality of life was
also assessed through SF-36, which is a multi-purpose, short-form health survey with 36
questions. It yields a profile of functional health and well-being scores as well as
psychometrically-based physical and mental health summary measures, with the higher total
scores indicating better health condition (32).
Sample size calculation and statistical analysis
Sample size was estimated with the assistance of the G-Power® software (version 3.1.2).
Based on data from a previous meta-analysis reporting effects of BFRT on muscle strength in
untrained individuals (20), we determined that 12 patients would be needed to provide 95%
power (α = 0.05) for muscle strength in our untrained population of OA patients. As muscle
strength was our primary outcome and the most reported adaptation to BFRT, sample size
calculation was based on this parameter.
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Data were analyzed using intention-to-treat principles. Dependent variables were tested
by mixed models with repeated measures using the software SAS® version 9.3. Tukey post-hoc
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was used for multicomparisons purporse. Additionally, a secondary per protocol analysis was
conducted using delta scores (i.e., changes from PRE to POST tests). Groups baseline (PRE)
values were compared and found similar (p > 0.05). Additionally, PRE values influence on
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change scores (PRE to POST) were tested and no significant effects were found, possible
between-group differences in delta changes were tested by a one-way ANOVA. Tukey post-hoc
was used when necessary. Effect sizes (ES) (per protocol approach) were calculated according to
Cohen (1992). Fisher's test was applied to assess the possible between-group differences in the
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proportion of patients who dropped out due to reasons potentially attributed to the interventions
Finally, an exploratory analysis (Pearson’s r) was

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(e.g., persistent pain, injuries, fatigue).
conducted on any possible associations between training-induced changes in quadriceps muscle

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CSA or increases in strength with the remaining clinical variables (e.g.; functionality, pain,
quality of life, stiffness). Significance level was previously set at p < 0.05. Data are presented as
mean ± standard deviation, except when stated otherwise.
RESULTS
Patients
The flow of patients is illustrated in Figure 1. Out of the 379 patients who were screened
for participation, 48 met the inclusion criteria. These patients were ranked into tertiles according
to their 1-RM leg press and then randomly assigned to either HI-RT (n = 16), LI-RT (n = 16), or
BFRT (n = 16). Throughout the trial, six patients were excluded from HI-RT due to both
intervention-related and non-intervention related reasons (exercise-induced keen pain: n = 4;
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personal reasons: n = 2). Four patients were excluded from LI-RT due to non-intervention-
related reasons (inguinal hernia: n = 1; personal reasons: n = 3), and four patients were excluded
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from BFRT due to non-intervention-related reasons (rectal nodule: n = 1; upper-respiratory tract
infection: n = 1; personal reasons: n = 2). Adherence rate to training protocol were 90, 85, and
91% for HI-RT, LI-RT, and BFRT, respectively (considering completed case data).
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Muscle strength and functional tests
1-RM leg press and 1-RM knee extension were similar between HI-RT, LI-RT and BFRT
at baseline (p = 0.94 and p = 0.72 for leg press and knee extension, respectively). Within-group
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increases in 1-RM leg press (Figure 2 Panel A) and 1-RM knee extension (Figure 2 Panel C)
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were found only in HI-RT (+ 33%, ES = 0.82, p < 0.0001; + 22%, ES = 0.83, p < 0.0001,
respectively) and BFRT (+ 26%, ES = 1.01, p < 0.0001; + 23%, ES: 0.86, p < 0.0001). In
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contrast, 1-RM leg press (+ 8%, ES = 0.23, p = 0.22) and 1-RM knee extension (+ 7%, ES =
0.21, p = 0.23) remained unaltered after the intervention in LI-RT. Despite significant within-
group effects, both leg-press and knee-extension 1RM were similar across groups at POST (p >
0.05).
Importantly, delta analysis revealed that HI-RT (p < 0.0001) and BFRT (p = 0.0004) had
significantly greater increases in 1-RM leg press when compared with LI-RT (Figure 2 Panel B).
Similarly, HI-RT and BFRT had greater increases in 1-RM knee extension (p = 0.0004 and p =
0.0005, respectively) when compared with LI-RT (Figure 2 Panel D). Of note, no significant
differences between HI-RT and BFRT were observed (p > 0.05), indicating a similar effect
between treatments.
Baseline scores in TST and TUG tests were comparable between groups (p = 0.61 and p =
0.71, respectively). Within-group comparisons revealed significant improvements in TST in HI-
RT and BFRT (+ 14%, ES = 0.52, p < 0.0001 and + 7%, ES = 0.43, p = 0.01, respectively) after
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the intervention, whereas LI-RT showed no significant change (+ 5%, ES = 0.32, p = 0.31)
(Figure 3 Panel A). Despite significant within-group effects, no interaction effects were found
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and groups were comparable at POST (p > 0.05). Delta analysis demonstrated that HI-RT had
greater performance in TST than LI-RT (p = 0.04); no significant differences were noted
between BFRT and LI-RT and BFRT and HI-RT (all p > 0.05) (Figure 3 Panel B).
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In respect of the TUG, no within- or between-group differences were noted (all p > 0.05)
(Figure 3 Panel C). Additionally, delta analysis did not show any significant difference between
the three groups (all p > 0.05) (Figure 3 Panel D).

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Quadriceps CSA
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There were no significant differences between groups at PRE (p = 0.77). Importantly,
significant within-group increases in CSA were observed only in HI-RT (+ 8%, ES = 0.54, p <
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0.0001) and BFRT (+ 7%, ES = 0.39, p < 0.0001), but not in LI-RT (+ 2%, ES = 0.12, p = 0.52)
(Figure 4 Panel A). Despite this, groups were not significantly different at POST (p > 0.05);
importantly, delta analysis showed significantly greater increases in CSA in HI-RT and BFRT
when compared with LIRT (p = 0.007 and p = 0.02) (Figure 4 Panel B). Finally, no significant
difference was noted between HI-RT and BFRT (p > 0.05), evidencing a comparable effect
between treatments for this variable.
Pain and Self-reported quality of life
WOMAC and SF-36 data can be found in Table 2. All groups were comparable at PRE for
all WOMAC subscales (i.e., pain, stiffness, physical function, and total) (all p > 0.05). WOMAC
pain score was significantly reduced in LI-RT and BFRT (- 45%, ES = - 0.79, p = 0.001 and -
39%, ES = - 0.79, p = 0.02, respectively), but not in HI-RT (- 31%, ES = - 0.54, p = 0.19).
WOMAC stiffness score was significantly reduced in BFRT (- 44%, ES = - 1.12, p = 0.013), but
not in HI-RT and LI-RT (- 41%, ES = - 1.11, p = 0.53 and - 32%, ES = - 0.55, p = 0.286,
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respectively). WOMAC physical function score was significantly improved in BFRT and HI-RT
(- 49%, ES = - 1.30, p = 0.019 and - 42%, ES = - 1.18, p = 0.02), but not in LI-RT (-42%, ES = -
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0.69, p = 0.09). WOMAC total score was significantly improved from PRE- to POST-test in all
groups (HI-RT: - 39%, ES = - 1.23, p = 0.016; LI-RT: -42%, ES = - 0.79, p = 0.005; BFRT: -
46%, ES = - 1.3, p = 0.008).

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There were no significant difference within or between groups for any domain from SF-36,
nor any significant differences between delta scores (all p > 0.05).
Finally, we found significant associations between changes in leg-extension 1-RM and
change scores in stiffness and physical function subscales (r = 0.4, p = 0.02 and r = 0.37, p =
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0.03, respectively) and total score in WOMAC (r = 0.37, p = 0.03), and a trend towards
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significance in its association with changes in TST scores (r = 0.31, p = 0.07). Changes in CSA
were significantly associated with changes in TST scores (r = 0.5, p = 0.002) and a trend towards
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significance was found between changes in CSA and changes in stiffness subscale in WOMAC
(r = 0.3, p = 0.09). No significant associations were found between changes in leg-press 1-RM
and any of the parameters; however, a trend towards significance was found in its association
with changes in scores in stiffness and physical function subscales (r = 0.3, p = 0.09 and r = 0.3,
p = 0.09) and total score in WOMAC (r = 0.3, p = 0.08).
Adverse events
Four patients (out of 16) from HI-RT were excluded throughout the follow-up due to
exercise-induced knee pain. Fischer´s exact test revealed that this incidence was significantly
superior to that of either BFRT (p = 0.03) or LI-RT (p = 0.03) (none in either group). No other
adverse events were self-reported.
Discussion
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The main findings of this study are that BFRT was similarly effective as HI-RT in
increasing lower-limb maximum dynamic strength, quadriceps CSA, and functionality in knee
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OA patients. Additionally, both training methods were able to improve WOMAC physical
function subscale whereas BFRT, but not HI-RT, significantly improved WOMAC pain and
stiffness subscales. Importantly, HI-RT resulted in a significant number of withdrawals.

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Knee OA often encompasses diminished muscle strength and mass, which is
accompanied by pain and reduced quality of life. Therefore, given the importance of quadriceps
muscle strength and mass on disease progression, functionality, and quality of life (5, 6, 8, 9, 15,
19), both the American College of Rheumatology (33) and the European League Against
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Rheumatism (34) consider RT a first-line therapy in OA management. In order to maximize

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training-induced adaptations, the American College of Sports Medicine recommends moderate-
to high-load RT (> 65% 1-RM) (17), which constitutes an important drawback when dealing
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with knee OA patients, as pain is often a limitation while attempting to exercise at higher-
intensities (18). In this respect, BFRT has emerged as a potential alternative to HI-RT, as it
allegedly allows patients to exercise at much lower intensities (~20-40% 1-RM) while
experiencing similar muscle adaptations (20, 22).
In the present study, lower-limb maximum dynamic strength, as measured by leg press
and knee extension 1-RM, and functionality were increased to a similar extent with BFRT and
HI-RT, while no changes were found in LI-RT. This is in line with previous studies in different
populations (20, 21). For instance, we and others have shown BFRT to be equally effective as
HI-RT in increasing lower-limb 1-RM in young (22) and healthy elderly (21, 35) individuals. In
diseased populations, we have also shown BFRT to be a promising adjuvant therapy in
dermatomyositis and polimyositis (36), as well as in a patient with inclusion body myositis (37),
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which corroborates our findings.
Regarding OA management, there is preliminary evidence showing that BFRT was able
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to induce gains in muscle strength in women with risk factor for knee OA (23). However, no
comparison to an HI-RT group was provided, hampering further inferences on BFRT efficacy.
The only study to investigate BFRT on OA patients also reported comparable increases in
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muscle strength between BFRT and HI-RT, with slightly greater relative changes than those
found herein (24). It is important to note that only isometric strength was assessed, which
although informative, is less complex than a more physiological test such as the maximum
dynamic muscle strength test employed in our study. This, in association with the apparent lack
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of familiarization procedure in the study by Bryk et al. (2016) may, at least partially, explain the
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difference in magnitude between studies (despite a similar response pattern between training
protocols). Additionally, the authors included neither an intensity-matched non-occlusion group

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nor muscle mass assessments, limiting their conclusions.
In this respect, BFRT has been suggested as an effective method for increasing lower-
limb lean mass. In fact, similar muscle mass accrual has been shown after BFRT when compared
with HI-RT in both young (22) and elderly (21). Additionally, we have previously shown BFRT
to be able to induce increases in muscle mass in severely diseased individuals (36, 37), which is
now extended to OA patients. In the present study, we found comparable increases in quadriceps
CSA between BFRT and HI-RT, with no change in LI-RT. This novel finding is of substantial
clinical relevance and advances the literature significantly as quadriceps muscle mass is an
important feature in knee OA. In fact, a greater loss in lower extremity lean mass has been
observed in women with knee OA when compared with healthy controls (9). This reduction in
muscle mass is also associated with disease progression (10), pain (11), and with both presence
and severity of age-related OA (12). Finally, thigh lean muscle mass is related to knee extensor
and flexor power in women with knee OA (38), which has direct implications for strength and
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functionality (6, 7, 9); therefore, targeting not only quadriceps strengthening, but also lean mass,
is key in OA management.
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In line with our findings regarding muscle strength and mass, functionality was
significantly improved after training in both BFRT and HI-RT (as measured by TST).
Maintaining functionality is one of the main goals in OA treatment. Impaired physical function is
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associated with restrictions in physical performance of daily activities for independent living and
is considered a predictor of disability (39). The findings of the present study support the use of
BFRT interventions in knee OA, as it favors preservation of independence and, thus, quality of
life in these patients while inducing less strain in the affected joints and, consequently, less pain.
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In fact, whilst WOMAC scores for physical function were significantly improved in both BFRT
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and HI-RT, subscale WOMAC pain was significant and positively changed only after BFRT,
supporting our contention. Another relevant finding was that 25% of the sample enrolled in the
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conventional HI-RT intervention protocol withdrew from study due to exercise-related pain,
whereas no adverse events were noted during BFRT. It is likely that lower joint stress and lesser
pain may exert a differential effect on the long-term adherence to exercise in knee OA patients,
which would be of clinical significance though proper investigation is currently lacking.
Additionally, arterial blood pressure was monitored prior to and after each training session and
no clinically relevant alterations were observed (data not shown). Similarly, resting blood
pressure was not affected by the 12-week intervention (data not shown), adding to the safety
argument of BFRT for this population. In fact, BFRT has previously been deemed safe in a
variety of populations, with minimal incidence of adverse events (40), though professional
assistance and proper control of training variables are necessary. Data on the safety of BFRT in
patients with cardiovascular disease are still scarce.
Given the effect increases in muscle strength and/or mass may have on clinical
parameters in knee OA, we decided to investigate any possible associations between these
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variables. Importantly, these results are exploratory and limited by the low sample size;
nonetheless, it is interesting to observe positive associations between physiological and clinical
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variables in a population of knee OA patients. This is somehow expected, as previous studies
have indicated positive associations between muscle mass and strength with pain and
functionality (6-8, 10,11).

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Finally, it is imperative to emphasize that the discussion of our findings is based upon
within-group changes and between-group comparisons in delta scores, the latter being a
secondary analysis in our model. Even though no significant between-group differences were
found, this is mitigated by the much larger ES observed in both BFRT and HI-RT when
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compared with LI-RT, and the observable similarity in data behavior pattern over time, with
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BFRT and HI-RT presenting very similar response patterns. Moreover, although we ran a priori
power analysis for sample size calculation, it is very likely that the study is actually
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underpowered based on a posteriori power analysis, which may explain the lack of interaction
effects.
In conclusion, the present study demonstrated similar effects between BFRT and HI-RT
in increasing muscle strength, quadriceps muscle mass, and functionality in older female knee
OA patients. Importantly, BFRT was also able to improve pain while using lower loads and
inducing less joint stress, emerging as a feasible and effective therapeutic adjuvant in OA
management.
Acknowledgements
The authors thank Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP),
Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and Coordenadoria
de Aperfeiçoamento de Pessoal de Nível Superior - Programa de Excelência Acadêmica
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(CAPES/PROEX) for the financial support. HR is supported by CNPq and FAPESP
(307023/2014-1 and 2016/10993-5, respectively).
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Conflict of interest statement
The authors declare that they have no competing interests. The results of the present study do not
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constitute endorsement by ACSM. The results of the present study are presented clearly,
honestly, and without fabrication, falsification, or inappropriate data manipulation.
Authors’ contributions
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Significant manuscript writer – HR, RBF, BG

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Significant manuscript reviewer/reviser - HR, ALSP, BG, RBF, RF, COB, FRL, RR
Concept and design – HR, BG, RBF

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Data acquisition – RBF, RF, ALSP, FRL, RR, COB
Data analysis and interpretation – HR, BG, RBF, ALSP, FRL, COB, RF
Statistical Expertise – HR, RBF
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Figure legends.
Figure 1. Flowchart of patients.
URTI: upper respiratory tract infection.
Figure 2. Lower-limb maximum dynamic strength.
Panels A and C show leg-press and knee extension 1-RM, respectively, before (PRE) and after
(POST) the exercise training protocol. * indicates p < 0.05 for within-group comparisons. Panels
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B and D show delta changes (pre- to post-training) in leg press and knee extension 1-RM,
respectively. * indicates p < 0.05 when compared with LI-RT. Data are presented as mean ± SD.
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HI-RT: high-intensity resistance training; LI-RT: low-intensity resistance training; BFRT: low-
intensity resistance training with blood flow restriction.
Figure 3. Functional tests.

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Panels A and C show data from timed-stands and timed-up-and-go tests, respectively, before
(PRE) and after (POST) the exercise training protocol. * indicates p < 0.05 for within-group
comparisons. Panels B and D show delta changes (pre- to post-training) in timed-stands and
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timed-up-and-go, respectively. * indicates p < 0.05 when compared with LI-RT. Data are
presented as mean and ± SD. HI-RT: high-intensity resistance training; LI-RT: low-intensity
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resistance training; BFRT: low-intensity resistance training with blood flow restriction.
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Figure 4. Quadriceps CSA.
Panel A shows quadriceps cross-sectional area before (PRE) and after (POST) the exercise
training protocol. * indicates p < 0.05 for within-group comparisons. Panel B shows delta
changes in quadriceps cross-sectional area (pre- to post-training). * indicates p < 0.05 when
compared with LI-RT. Data are presented as mean and ± SD. HI-RT: high-intensity resistance
training; LI-RT: low-intensity resistance training; BFRT: low-intensity resistance training with
blood flow restriction.
List of Supplement Digital Content:
Supplemental Digital Content 1. TIFF – Figure. Experimental design. 1-RM, one repetition
maximum; CSA, cross-sectional area; WOMAC, Western Ontario and McMaster Universities
Osteoarthritis Index; SF-36, Short Form Health Survey.
Supplemental Digital Content 2. DOCX – Table. Progression of training load
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Table 1. Patients’ baseline characteristics and drug regimen.
Groups
HI-RT LI-RT BFRT

p
(n=16) (n=16) (n=16)
Age (yr) 59.9 ± 4 60.7 ± 4 60.3 ± 3 0.8672
Weight (kg) 74.2 ± 16 71.0 ± 13 77.9 ± 7 0.3021
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Height (cm) 159.9 ± 5 157.0 ± 8 160.8 ± 6 0.2553
BMI (kg/m²) 30.3 ± 5 29.9 ± 3 30.2 ± 3 0.8944
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VAS (cm) 5.3 ± 1 5.1 ± 1 5.2 ± 1 0.9323
Disease duration, years since diagnosis 4.4 ± 3 4.7 ± 3 4.4 ± 3 0.9594
Kellgren–Lawrence radiographic
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grade, n (%)
2 11 (69) 9 (56) 10 (62) 0.9154
3 5 (31) 7 (44) 6 (38) 0.8974
Drugs, n (%)
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Antithyroid 1 (6) 2 (12) 2 (12) 0.8278

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Antiulcer 1 (6) 1 (6) 1 (6) 0.9913
Antihypertensive 5 (31) 5 (31) 7 (44) 0.8679

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Antidepressant 2 (12) 1 (6) 4 (25) 0.6734
Antidiabetic 0 (0) 0 (0) 1 (6) 0.5889
Sympathomimetic 0 (0) 1 (6) 0 (0) 0.4970
Immunosuppressive 1 (6) 1 (6) 3 (19) 0.4529
Hypocholesterolemic 0 (0) 2 (12) 3 (19) 0.2243
Myorelaxant 0 (0) 0 (0) 2 (12) 0.1951
Antiarthritic 2 (12) 5 (31) 8 (50) 0.5740
Glucosamine 2 (12) 3 (19) 4 (25) 0.6377
Chondroitin 2 (12) 3 (19) 2 (12) 0.8228
Diacerein 0 (0) 2 (12) 7 (44) 0.3568
Data are expressed as mean ± SD and level of significance (p). No significant differences were
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observed between groups at baseline. HI-RT: high-intensity resistance training; LI-RT: low-
intensity resistance training; BFRT: low-intensity resistance training with blood flow restriction;
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BMI: Body Mass Index; VAS: Visual Analog Score.
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Table 2. Self-reported quality of life.
PRE POST
WOMAC - Pain
HI-RT 7.2 ± 2.2 4.6 ± 3.1
LI-RT 7.9 ± 3.9 4.0 ± 2.6*
BFRT 6.9 ± 3.3 4.0 ± 2.9*
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WOMAC - Stiffness
HI-RT 3.5 ± 1.2 2.0 ± 1.8
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LI-RT 2.8 ± 1.4 1.8 ± 1.7
BFRT 3.6 ± 1.5 2.1 ± 1.5*
WOMAC - Physical function

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HI-RT 25.9 ± 9.3 14.6 ± 9.2
LI-RT 24.4 ± 12.9 12.7 ± 7.7*
BFRT 21.0 ± 8.5 10.3 ± 6.9*
WOMAC – Total
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HI-RT 36.6 ± 11.1 21.2 ± 13.2*

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LI-RT 35.1 ± 16.2 18.4 ± 11.5*
BFRT 31.5 ± 12.0 17.1 ± 11.2*

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SF-36 – Mental Health
HI-RT 65.4 ± 20.7 71.1 ± 23.1
LI-RT 69.0 ± 15.7 78.5 ± 19.8
BFRT 68.0 ± 23.8 79.3 ± 12.0
SF-36 – Physical Health
HI-RT 55.7 ± 16.9 64.8 ± 15.5
LI-RT 57.0 ± 15.9 66.0 ± 20.3
BFRT 60.4 ± 16.1 73.4 ± 13.5
Data are expressed as mean ± SD. HI-RT: high-intensity resistance training; LI-RT: low-
intensity resistance training; BFRT: low-intensity resistance training with blood flow
restriction; WOMAC: Western Ontario and McMaster Universities index of osteoarthritis; SF-
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36: Short Form Health Survey. * indicates p < 0.05 for within-group comparisons.
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Supplemental Table. Progression of training loads.
Weeks Group Number of sets Number of repetitions % Restriction % 1-RM
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1 HI-RT 4 10 - 50
LI-RT 4 15 - 20
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BFRT 4 15 50 20
2 to 4 HI-RT 4 10 - 80
LI-RT 4 15 - 30
BFRT 4 15 70 30
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5 HI-RT 1-RM tests
LI-RT 1-RM tests
BFRT 1-RM tests

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5 to 8 HI-RT 5 10 - 80
LI-RT 5 15 - 30
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BFRT 5 15 70 30
9 HI-RT 1-RM tests

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LI-RT 1-RM tests
BFRT 1-RM tests
9 to 12 HI-RT 5 10 - 80
LI-RT 5 15 - 30
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BFRT 5 15 70 30
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% Restriction, percentage of blood flow restriction; % 1-RM, percentage of one repetition maximum; HI-RT, high-intensity resistance
training; LI-RT, low-intensity resistance training; BFRT, low-intensity resistance training with blood flow restriction
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Published ahead of Print

Accepted for Publication: 14 December 2017

Copyright © 2018 American College of Sports Medicine

Benefits of Resistance Training with Blood Flow Restriction in Knee

University of São Paulo, SP, Brazil

Dr. Hamilton Roschel, Ph.D.

Escola de Educação Física e Esporte – Universidade de São Paulo

Av. Melo de Moraes, 65, Butantã – São Paulo, SP - Brazil

Postal code: 05508-030

without fabrication, falsification, or inappropriate data manipulation.

stress, emerging as a feasible and effective therapeutic adjuvant in OA management. KEY-

WORDS: Arthritis; cartilage; rehabilitation; WOMAC; hypoxia; KAATSU.

of musculoskeletal pain, functional impairment, and reduced independence in older adults

characterized by cartilage involvement; currently, however, it is considered to involve the whole

formation, and sclerosis of the subchondral bone (4).

quadriceps strengthening and hypertrophy is thought as a first-line therapy (14), making

resistance training (RT) a common practice within OA management (15, 16).

intensities, limiting the application of conventional high-intensity RT (HI-RT) in OA not only

investigation on new and viable strategies to mitigate OA-related symptoms.

conventional HI-RT (21, 22), constituting a promising strategy for non-pharmacological

BFRT on quadriceps muscle mass constitutes an important clinical question in OA management.

high-intensity RT while inducing less pain.

NTCT01483131. This manuscript was reported according to CONSORT guidelines (25).

intensity resistance training with blood flow restriction (BFRT).

Experimental design, http://links.lww.com/MSS/B161).

Resistance training programs

RT was performed in an intrahospital gymnasium (Laboratory of Assessment and

Conditioning in Rheumatology, School of Medicine, University of São Paulo). Exercise sessions

training machines (Nakagym, São Paulo, Brazil).

restriction increments are comprehensively described elsewhere (Supplemental Digital Content

2, Progression of training loads, http://links.lww.com/MSS/B162). A member of the research

staff monitored the adherence to the exercise program on a session basis.

extension exercises according to previous description (27).

Computed tomography imaging (Brilliance CT, 64-slice, Philips Medical System

further analysis. Quadriceps CSA measurement’s CV was 0.73 %.

Self-reported quality of life assessment

questions. It yields a profile of functional health and well-being scores as well as

scores indicating better health condition (32).

calculation was based on this parameter.

Finally, an exploratory analysis (Pearson’s r) was

(e.g., persistent pain, injuries, fatigue).

conducted on any possible associations between training-induced changes in quadriceps muscle

mean ± standard deviation, except when stated otherwise.

intervention-related and non-intervention related reasons (exercise-induced keen pain: n = 4;

0.71, respectively). Within-group comparisons revealed significant improvements in TST in HI-

the three groups (all p > 0.05) (Figure 3 Panel D).

There were no significant differences between groups at PRE (p = 0.77). Importantly,

between treatments for this variable.

46%, ES = - 1.3, p = 0.008).

Finally, we found significant associations between changes in leg-extension 1-RM and

p = 0.09) and total score in WOMAC (r = 0.3, p = 0.08).

adverse events were self-reported.

stiffness subscales. Importantly, HI-RT resulted in a significant number of withdrawals.

Rheumatism (34) consider RT a first-line therapy in OA management. In order to maximize

training-induced adaptations, the American College of Sports Medicine recommends moderate-

experiencing similar muscle adaptations (20, 22).

diseased populations, we have also shown BFRT to be a promising adjuvant therapy in

protocols). Additionally, the authors included neither an intensity-matched non-occlusion group

nor muscle mass assessments, limiting their conclusions.

which would be of clinical significance though proper investigation is currently lacking.

patients with cardiovascular disease are still scarce.

nonetheless, it is interesting to observe positive associations between physiological and clinical