Neuromuscular Electrical Stimulation (NMES) Reduces Structural

and Functional Losses of Quadriceps Muscle and Improves

Health Status in Patients with Knee Osteoarthritis
Marco Aurélio Vaz,1 Bruno Manfredini Baroni,1 Jeam Marcel Geremia,1 Fábio Juner Lanferdini,1 Alexandre Mayer,1
Adamantios Arampatzis,2 Walter Herzog3
1
Exercise Research Laboratory, School of Physical Education, Federal University of Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil,
2
Centre of Sport Science and Sport Medicine, Department of Training and Movement Sciences, Humboldt-Universität zu Berlin, Berlin, Germany,
3
Faculty of Kinesiology, Human Performance Laboratory, University of Calgary, Calgary, Alberta, Canada
Received 17 January 2012; accepted 11 October 2012
Published online 8 November 2012 in Wiley Online Library (wileyonlinelibrary.com). DOI 10.1002/jor.22264

ABSTRACT: Knee osteoarthritis (OA) is associated with quadriceps atrophy and weakness, so muscle strengthening is an important
point in the rehabilitation process. Since pain and joint stiffness make it often difficult to use conventional strength exercises, neuro-
muscular electrical stimulation (NMES) may be an alternative approach for these patients. This study was aimed at (1) identifying the
associations of knee OA with quadriceps muscle architecture and strength, and (2) quantifying the effects of a NMES training program
on these parameters. In phase 1, 20 women with knee OA were compared with 10 healthy female, asymptomatic, age-matched control
subjects. In phase 2, 12 OA patients performed an 8-week NMES strength training program. OA patients presented smaller vastus
lateralis thickness (11.9 mm) and fascicle length (20.5%) than healthy subjects (14.1 mm; 24.5%), and also had a 23% smaller knee
extensor torque compared to the control group. NMES training increased vastus lateralis thickness (from 12.6 to 14.2 mm) and fascicle
length (from 19.6% to 24.6%). Additionally, NMES training increased the knee extensor torque by 8% and reduced joint pain, stiffness,
and functional limitation. In conclusion, OA patients have decreased strength, muscle thickness, and fascicle length in the knee exten-
sor musculature compared to control subjects. NMES training appears to offset the changes in quadriceps structure and function, as
well as improve the health status in patients with knee OA. ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.
J Orthop Res 31:511–516, 2013

Keywords: osteoarthritis; muscle architecture; muscle strength; WOMAC; electrical stimulation

Osteoarthritis (OA) is one of the major degenerative dis-
eases and it affects elderly women more frequently than
elderly men.1,2 The prevalence of OA is expected to
increase dramatically in the near future due to the in-
creased life expectancy and an increasing rate of obesity
of the world population.3 The knee is the most affected
joint with 13.6% of women above 60 years showing ra-
diographic evidence of OA and/or clinical symptoms.2
OA causes erosion of articular cartilage, weakening of
subchondral bone, meniscal degeneration, inflammation
of the synovium, and intra-articular osteophytes.4 These
changes lead to a reduction in the range of motion,
and increase in joint stiffness and pain.5
In addition to the effects on the joint structure
and function, OA also has a negative effect on the mus-
culoskeletal system. Patients with knee OA have de-
creased knee extensor strength compared to healthy
subjects6–10 and compared to the healthy contralateral
limb.11,12 Evidence also suggests that the muscle weak-
ness is associated with a decrease in muscle mass.11,12
However, although a reduction in muscle thickness11
and anatomical cross-sectional area12 have been de-
scribed in OA patients, we were unable to find evidence
on how muscle weakness was related to changes in oth-
er muscle architecture parameters associated with
strength, such as fascicle length, and pennation angle.
Correspondence to: Marco Aurélio Vaz (T: þ5551-33085860;
F: þ5551-33085858; E-mail: marcovaz@esef.ufrgs.br)
ß 2012 Orthopaedic Research Society. Published by Wiley Periodicals, Inc.
Fascicle length is related to the number of sarcomeres
aligned in series in the muscle cells, which affects the
maximal contracting velocity and the optimal length
for force generation.13 Pennation angle has been associ-
ated with the amount of in parallel sarcomeres, which
is closely related to the maximal force capacity of a
muscle fiber.13 Therefore, determining the above
parameters allow for a better understanding on how
these intrinsic changes in muscle architecture affect
functionality in OA patients.
Knee extensor strength is a predictor of indepen-
dence in the elderly and an indicator for life span.14
Patients with knee OA often have significant
functional limitations,6 leading to a vicious cicle of
pain–weakness–pain. In addition, quadriceps weak-
ness has been related to decreases in proprioception,15
joint stabilization,16 and shock absorption,17 contribut-
ing to a progression of joint degeneration with a subse-
quent increase in joint pain.12,18 Epidemiological
studies have concluded that quadriceps muscle weak-
ness may lead to incident symptomatic knee OA, al-
though the results were not statistically significant
and contained body mass as a confounding factor.19
Moreover, studies in animal model demonstrated that
muscle weakness causes increased joint degenera-
tion,20 providing evidence that muscle weakness might
be a risk factor for the onset and progression of OA.21
Scientific evidence emphasizes the possible impor-
tance of quadriceps strengthening in the prevention
and rehabilitation of knee OA.3,18,21 However, pain
and joint stiffness make it often difficult to use

JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013 511

512 VAZ ET AL.
conventional strength training programs. Neuromus-
cular electrical stimulation (NMES) may be an alter-
native, low cost, efficient, and less painful approach
than voluntary knee extensor exercises for patients
with knee OA. NMES is considered an efficient tech-
nique for quadriceps strengthening22 and has been
used to treat patients with knee OA. Although previ-
ous studies found increases in health and knee
function after NMES training,23–28 the muscular adap-
tations of NMES in patients with knee OA have not
been described.
The present study had the following goals: (1) to
identify the associations of knee OA with structural
(muscle architecture) and functional (knee extensor
torque) parameters of the knee extensor muscles in el-
derly women; and (2) to quantify the possible effects of
an 8-week NMES strength training program on these
structural and functional parameters in this patient
population.
METHODS
Experimental Design
This study was approved by the University’s Research Ethics
Committe (Protocol #2007791) and all subjects signed an
informed consent form prior to participation. The study was
comprised of two parts. In phase 1, we quantified the effects
of knee OA on the structural and functional properties of
the knee extensor muscles, and in phase 2 we characterized
the effects of a NMES strength training program on these
properties.
Subjects
Patients with knee OA were recruited from a hospital and
two orthopaedic clinics. Subjects were chosen based on
the following inclusion criteria: (1) women, minimum age
of 50 years; (2) clinically diagnosed with knee OA; (3) no
contraindications to execute maximal knee extension tests
(e.g., cardiorespiratory complications); (4) no previous muscu-
loskeletal or joint injuries besides knee OA; (5) no hip or
knee surgery; and (6) no neurological problems.
All patients received an intial clinical assessment, includ-
ing knee X-rays to support the clinical diagnosis of OA. X-
rays included an axial patellar view obtained at 308 of knee
flexion (08 ¼ full extension), an antero-posterior monopodal
weightbearing (long view), a sagittal monopodal (long view);
and an antero-posterior Schuss incidence with 308 of knee
flexion (long view). X-ray images were used to determine the
degree of OA, according to the criteria proposed by Dejour
et al.29 Only patients diagnosed with a degree 2 or 3 of knee
OA were included in the study.
In phase 1 of this study, the structural and functional
properties of the quadriceps muscles of 20 women with knee
OA and 10 healthy female, asymptomatic, age-matched con-
trol subjects were assessed. The characteristics of the patient
and control groups subjects are presented in Table 1.
In phase 2, 12 of the 20 OA patients volunteered to partic-
ipate in the 8-week NMES strength training program
(age ¼ 58
8 years; height ¼ 1.55
0.08 m; body mass ¼
78
15 kg; body mass index ¼ 32
7 kg/m2). These OA
patients were submitted to clinical evaluation and assess-
ment of the structural and functional properties of the quad-
riceps muscles before and after the NMES strength training
program.
JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013
Table 1. Characteristics of the OA Patients Group and
Healthy Controls Group (Mean
SD)
Healthy
Subjects OA Patients
(n ¼ 10) (n ¼ 20) p-value
Age (years) 60
7 61
8 0.797
Height (cm) 157
1 156
7 0.116
Body mass (kg) 66
7 72
11 0.605
Body Mass 27
3 30
5 0.065
Index (kg/m2)
Testing Procedures
Muscle Architecture
An ultrassound system (SSD 4000, 51 Hz, ALOKA Inc.,
Japan) with a linear array probe (60 mm, 7.5 MHz), was
used to determine the thickness, fascicle length, and penna-
tion angle of the vastus lateralis muscle. Ultrassound images
were obtained at rest with the subject sitting on the chair of
an isokinetic dynamometer (Biodex System 3; Biodex Medical
Systems, Shirley, NY) with the hip and knee flexed at 858
and 908, respectively. All images were captured in the sagit-
tal plane of vastus lateralis (at midway between the lateral
condyle of the femur and the greater trochanter).30 The ul-
trasound probe was positioned in the approximate direction
of the vastus lateralis muscle fibers (long axis with respect to
the limb).30 The same experienced researcher made all evalu-
ations and this researcher was blinded to the study group.
Ultrasound images were analyzed off-line using ImageJ
software (National Institute of Health, Bethesda, MD).
Muscle thickness was defined as the distance between the
deep and the superficial aponeuroses. The pennation angle
was defined as the angle between the deep aponeurosis and
the fascicle orientation. Fascicle length was defined as the
length of the fascicular trajectory between the fascicle inser-
tions on the superficial and deep aponeuroses. Since this
length usually was greater than the probe surface, the fasci-
cle line was extrapolated and calculated through a mathe-
matical routine in MATLAB (MathWorks, Natick, MA).
Fascicle lengths were normalized to femur length (obtained
from the X-ray images) and are reported as percentage val-
ues. In a pilot study to test the intra-rater reliability of our
measurements, we found ICC values of 0.91 for muscle thick-
ness, 0.91 for pennation angle, and 0.90 for fascicle length.
Knee Extensor Torque
Maximal isometric knee extensor torques were obtained on
an isokinetic dynamometer (Biodex System 3; Biodex Medical
Systems). Participants were positioned on the dynamometer
according to the manufacturer’s recommendations. After a
warm-up and a familiarization session, each subject executed
three maximal isometric knee extensor contractions with the
knee fixed at a flexion angle of 608. Each contraction lasted
for 5 s and a 2-min interval was observed between consecu-
tive contractions. Peak torque values from each contraction
were obtained and an additional contraction was obtained if
a torque variation higher than 10% was observed between
consecutive contractions. The highest value from the three
maximal isometric contractions was used for data analysis.
Clinical Evaluation
The Western Ontario and McMaster Universities Arthritis
Index (WOMAC), including all three subscales (measured by
 NMES TRAINING FOR KNEE OSTEOARTHRITIS 513

a Likert version and the possible range of scores is 0 ¼ none (14.1
2.5 mm; 24.5
4.6%), while pennation angles
to 4 ¼ extreme)25 were used to determine the degree of func- were the same for the OA and control subject groups.
tionality of the OA patients before and after NMES strength Subjects in the OA group also had a 23% smaller knee
training program. extensor torque compared to the healthy control sub-
jects (Fig. 1).
Strength Training NMES Program
NMES training increased vastus lateralis thickness
A portable stimulator, designed for this study, was used for
(from 12.6
1.3 to 14.2
2.1 mm) and fascicle length
the strength training NMES program. The intervention was
performed with subjects seated on a regular chair (hip and (from 19.6
4.6% to 24.6
4.4%) from pre- to post-
knee angles maintained at approximately 908), 3 times/week training, but had no significant effect on the pennation
for a period of 8 weeks. Patients performed the 24 strength angle. Additionally, NMES training increased the maxi-
training sessions under the supervision of a member of the mal isometric knee extensor torque by 8% (Fig. 2).
research team. This researcher was responsible for the ade- OA patients showed improvements in WOMAC
quate positioning of the surface stimulation electrodes scores following the NMES training program (Table 3).
(5 cm  13 cm; Axelgaard Mfg. Co., Ltd., Fallbrook, CA) and The intervention program promoted a reduction of
for the control of the electrical stimulation intensity, which 38% in joint pain, 29% in joint stiffness, and 34% in
was set at the maximum that could be comfortably tolerated functional limitation.
by the patients. Subjects were instructed to relax and avoid
voluntary contractions of the knee extensors during the
training sessions.
DISCUSSION
NMES parameters included: rectangular biphasic sym- The primary results of this study are (1) that women
metric current, pulse duration of 400 ms and stimulation fre- with knee OA are weaker, have smaller muscles and
quency of 80 Hz. The first training session lasted 18 min and shorter fascicle length in VL compared to age- and
was comprised of 10 s of stimulation followed by 50 s of rest. sex-matched normal control subjects; (2) that NMES
Training progression was achieved by a gradual increase in strength training program in women aged 47–75 years
the total session time and a reduction of the resting period, with knee OA increases strength, muscle thickness,
resulting in an increased number of contractions per time and fibre lengths in VL; and (3) that these muscular
interval, and, therefore, greater exposure time of the knee changes following NMES training are associated with
extensor muscles to NMES (Table 2). improvements in clinical outcome scores.
Loss in quadriceps muscle mass in OA patients has
Statistical Analysis
been associated with decreases in muscle thickness11
Independent Student’s t-tests were used to quantify possible
differences in muscle thickness, fascicle length, angles of and cross-sectional area,12 and our results are in
pennation, and knee extensor torques between OA patients agreement with these previous findings. However,
and the healthy control group in part 1 of the study. Stu- Mairet et al.11 did not find decreases in fascicle
dent’s paired t-tests were used for the within group compar- lengths, as we found here.
isons between pre- and post-NMES intervention. A 5% Muscle atrophy is sometimes associated with a de-
(p < 0.05) significance value was adopted for all tests (SPSS crease in the pennation angle of muscles.13 However,
for Windows, 17.0 version, USA). All values are presented as we found no changes in the angles of pennation, nei-
means and
1 standard deviation in the text and means and ther between the normal and OA patient group nor

1 standard error in the figures. following the NMES training intervention, possibly
because of an accumulation of intramuscular fat
RESULTS and connective tissue sometimes found in atrophied
OA patients and healthy subjects presented similar muscles of OA patients.11,12 However, our results do
femur lengths (446
16 mm and 444
19 mm, not allow for evaluation of this hypothesis, as fat
respectively). Vastus lateralis thickness and fascicle content and possible fibrosis were not evaluated in our
length were smaller in OA patients (11.9
2.5 mm; patient group.
20.5
6.0%) compared to healthy subjects The smaller muscle thickness in the OA patients
compared to the control group subjects can be directly
explained with the smaller fascicle length as the pen-
Table 2. NMES Strength Training Program
nation angle was the same in OA patients and control
Total Contraction–Rest Contraction subjects. A muscle with shorter fascicle length will
Week Time (min) (s) Time (s) show a smaller capacity of force production at longer
lengths.13 As most studies comparing OA patients
1 18 10–50 180 with asymptomatic subjects6,7,9,10 evaluated the knee
2 20 10–50 200 extensor muscles with tests performed with the
3 22 10–40 264 knee at 908 of flexion (descending limb of the torque-
4 24 10–40 288 angle quadriceps relationship), the quadriceps muscle
5 26 10–30 390 of the OA patients was more distant from its optimal
6 28 10–30 420
length (or joint angle) for force production, which may
7 30 10–20 600
have contributed for the reduced levels of force pro-
8 32 10–20 640
duced at this specific joint angle.

JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013

514 VAZ ET AL.

Figure 1. Knee extensor torque and vastus lateralis muscle architecture from healthy and osteoarthritis patient groups (mean
SE).

p < 0.05.

The NMES strength training program was success-
ful in counteracting the deleterious effects of OA on
the knee extensor muscles. NMES reduced muscle
weakness and increased muscle thickness and fascicle
length. The post-NMES training values of the OA
patients were close to the values of the healthy control
group, suggesting that artificial electrical stimulation
offsets most of the OA-induced structural and func-
tional losses of the knee extensor muscles.
Our results for isometric knee extensor torque gains
are similar to the results reported by Talbot et al.23
following 12 weeks, 3 times/week, of NMES training in
OA patients. Durmus et al.26 found increments of
about 35% in the one maximal repetition test after 5

Figure 2. Knee extensor torque and vastus lateralis muscle architecture from OA patients before and after NMES strength training
(mean
SE). p < 0.05.

JOURNAL OF ORTHOPAEDIC RESEARCH APRIL 2013


Table 3. WOMAC Scores from OA Patients before and
after the 8-Week NMES Strength Training Program
(Mean
SD)
WOMAC Domain Baseline Post-Training p-value
Joint pain 11.7
3.2 7.2
3.5 0.005
Joint stiffness 5.1
1.6 3.6
1.7 0.075
Functional 44.9
7.8 29.7
12.8 0.001
limitation
weekly sessions of NMES training during 4 weeks,
while Rosemffet et al.25 did not observe any significant
gain in isometric force after 8 weeks of training with
three NMES sessions per week. These different out-
comes with apparently similar NMES stimulation
training protocols might be associated with the meth-
ods for evaluating maximal strength, to the level of
impairment of the OA patients, or the detailed param-
eters chosen for the NMES training programs (cur-
rent, duration, frequency, etc.). Since some NMES
interventions produce significant improvements in
knee extensor strength and muscle maintenance, it
seems important that NMES protocols are optimized
for each patient.
A reduced capacity for activating the knee extensor
muscles (muscle inhibition) is a well documented ad-
junct of knee OA.6–12 The mechanisms of this inhibi-
tion are unknown and need to be determined for
effective restoration of voluntary force and control of
the knee extensors. Improvements in voluntary activa-
tion of the quadriceps muscles after a period of a
NMES training program have been demonstrated in
young healthy subjects.31,32 Therefore, although the
mechanisms on how NMES reduces muscle inhibition
are not clear in the literature,33 the strength gains ob-
served in our study after NMES training may partly
be associated with an improvement in activation ca-
pacity of the quadriceps muscle. This possibility should
be addressed in future investigations.
There is strong evidence in the literature that
strength exercise has positive effects on pain scores
and functional outcomes in knee OA patients.34 Specif-
ically, OA patients have shown a significant decrease
in pain,23–28 a reduction in joint stiffness,26,27 an in-
crease in joint range of motion,28 and an improvement
in functional performance23,26 following NMES train-
ing. Although we cannot establish a direct causative
association between muscle strength and health sta-
tus, stronger knee extensor muscles are thought to de-
crease impact forces at the knee joint,16,17 and might
reduce the mechanical stimuli for pain,18 thereby re-
lieving the pain symptoms of the patients. Our find-
ings of improved WOMAC scores suggest that NMES
should be considered as a treatment option for the pre-
vention of ‘‘at risk’’ populations and/or the treatment
of patients with early OA in the knee. Nevertheless,
our results for the WOMAC scores might have been
biased due to the fact that all patients already knew
NMES TRAINING FOR KNEE OSTEOARTHRITIS 515
that they were in a treatment group, and is a limita-
tion of our study.
In conclusion, patients with knee OA have de-
creased strength, muscle thickness, and fascicle length
in the knee extensor musculature compared to age-
and sex-matched controls. NMES training of short du-
ration appears to offset the changes in quadriceps
structure and function, as well as reduces joint pain,
joint stiffness, and functional limitation in patients
with knee OA.
ACKNOWLEDGMENTS
The authors would like to acknowledge FINEP-Brazil,
CNPq-Brazil, and CAPES-Brazil for financial support. The
authors would also like to thank Cintia Helena Ritzel, Silvia
Helena Manfrin, Ângela Muraro, Rafael Fortuna, and Profs.
Fernando Aragão and Rafael Baptista for technical help in
different phases of the study, and Danton Pereira da Silva
Junior and Joel Machado dos Santos for the development of
the portable stimulator.
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