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CRE0010.1177/0269215514552082Clinical RehabilitationMelo et al.
CLINICAL
Article REHABILITATION
Clinical Rehabilitation
Abstract
Objectives: To determine the effects of low-level laser therapy in combination with neuromuscular
electrical stimulation on the muscle architecture and functional capacity of elderly patients with knee
osteoarthritis.
Design: A randomized, evaluator-blinded clinical trial with sequential allocation of patients to three
different treatment groups.
Setting: Exercise Research Laboratory.
Subjects: A total of 45 elderly females with knee osteoarthritis, 2-4 osteoarthritis degrees, aged 66–
75 years.
Intervention: Participants were randomized into one of the following three intervention groups:
electrical stimulation group (18–32 minutes of pulsed current, stimulation frequency of 80 Hz, pulse
duration of 200 μs and stimulation intensity fixed near the maximal tolerated), laser group (low-level laser
therapy dose of 4–6 J per point, six points at the knee joint) or combined group (electrical stimulation
and low-level laser therapy). All groups underwent a four-week control period (without intervention)
followed by an eight-week intervention period.
Main measures: The muscle thickness, pennation angle and fascicle length were assessed by
ultrasonography, and the functional capacity was assessed using the 6-minute walk test and the Timed Up
and Go Test.
Results: After intervention, only the electrical stimulation and combined groups exhibited significant
increases in the muscle thickness (27%–29%) and pennation angle (24%–34%) values. The three groups
exhibited increased performance on the walk test (5%–9%). However, no significant differences in terms
of functional improvements were observed between the groups.
Conclusions: Neuromuscular electrical stimulation reduced the deleterious effects of osteoarthritis on
the quadriceps structure. Low-level laser therapy did not potentiate the effects of electrical stimulation
on the evaluated parameters.
Keywords
Neuromuscular electrical stimulation, low-level laser therapy, knee osteoarthritis, elderly, vastus
lateralis muscle architecture, functional capacity
Introduction
Knee osteoarthritis is a chronic degenerative disease its effects on the release of neurotransmitters that are
that presents clinical symptoms, such as morning associated with pain modulation and the release of
stiffness, reduced range of motion, chronic joint pain anti-inflammatory agents,10,11 low-level laser therapy
and muscle weakness.1 Evidence also suggests that might improve the functionality of patients with knee
muscle weakness is associated with negative changes osteoarthritis.
in the muscle architecture, such as a decrease in the The efficacy of low-level laser therapy, in com-
muscle thickness and fascicle length.2,3 These bination with neuromuscular electrical stimulation
changes in the muscle structure have a negative to treat patients with knee osteoarthritis, has not
impact on the patient’s functionality because a been previously studied. The aim of the present
reduced fascicle length is related to a serial sarcomere study was to quantify the effects of neuromuscular
loss and reflects the muscle’s reduced shortening electrical stimulation and low-level laser therapy
velocity.3–5 Furthermore, reduced muscle thickness is on the muscle architecture parameters, pain and
associated with parallel sarcomere loss and ulti- functional capacity. Our main hypothesis was that
mately leads to a reduction in the maximum muscle the combination of low-level laser therapy with
fibre strength capacity.3–6 neuromuscular electrical stimulation should pro-
Neuromuscular electrical stimulation has been mote a greater decrease in pain and larger increases
recommended for quadriceps strengthening when in the functional capacity and muscle architecture
chronic pain and joint stiffness prevent patients from parameters than each therapy alone.
engaging in a voluntary exercise programme.7–9
Although previous studies found increases in quadri-
ceps strength and knee function,3,9 muscle architec- Methods
ture adaptations from neuromuscular electrical
Trial design
stimulation in patients with knee osteoarthritis have
not been completely described in randomized con- This randomized, single-blinded, clinical trial
trolled trials. (ClinicalTrials.gov Identifier: NCT02067871) was
Low-level laser therapy has been considered effec- approved by the University’s Ethics in Research
tive for treating knee osteoarthritis because of its cell Committee (Protocol number 20160). All patients
bio-stimulating action10 and its regenerative,11,12 anal- signed a written consent form prior to data
gesic,10 and anti-inflammatory effects.10,11 Because of collection.
Melo et al. 3
Table 2. Anthropometric and baseline clinical characteristics of the three experimental groups.
hoc test. The effect size (the difference between the electrical stimulation and combined groups showed
pre- and postintervention scores, divided by the an increased pennation angle (p < 0.001) and mus-
standard deviation of the preintervention score) cle thickness (p < 0.001) (Table 3) between the pre-
was calculated and interpreted using the following and postintervention tests. There were no
scale, which was proposed by Cohen23: trivial between-intervention effects on the fascicle length
effect (<0.10), small effect (0.30–0.10), medium (p = 0.67) (Table 3). Significant differences in the
effect (0.50–0.30) and large effect (above 0.50). muscle thickness (p = 0.003), but not in the penna-
The significance level was set to α < 0.05 for all tion angle (p > 0.05), were observed between
statistical analyses. All results are expressed as the groups for the per cent variation between pre- and
mean ± standard deviation. postintervention. The neuromuscular electrical
stimulation and combined groups showed the high-
Results est increases in the per cent values of muscle thick-
ness (p = 0.003) after the eight-week intervention,
Overall, 45 of 193 eligible participants underwent compared with the laser group (Table 3). Figure 2
randomization, and 44 out of 45 completed postint- illustrates the changes in the muscle architecture of
ervention testing (Figure 1). No significant differ- a representative subject from the neuromuscular
ences were found between the precontrol electrical stimulation group during the pre- and
anthropometric or clinical characteristics (p > 0.05; postintervention tests. The increased thickness
Table 2). after the eight-week electrical stimulation interven-
tion is visible. A similar increase was observed in
Muscle architecture the combined group.
Table 3. Time elapsed and pain scale during the Timed Up and Go Test, distance travelled and pain scale during
the 6-minute walk test and architectural variables during the study evaluation times.
Δ%: difference between the pre- and postintervention scores divided by the preintervention score; 6WT: 6-minute walk test; ES:
effect size; TUG: Timed Up and Go Test.
*Indicates significant differences between the pre- and postintervention tests (p < 0.01).
#Indicates significant differences between the neuromuscular electrical stimulation group or combined vs. the laser group in the
postintervention test (p < 0.001).
Figure 2. Ultrasonography images from a representative subject showing vastus lateralis muscles before
(preintervention) and after (postintervention) the neuromuscular electrical stimulation programme.
VI: vastus intermedius; VL: vastus lateralis.
present study was most likely responsible for the variable can explain the observed differences in
increased fascicle pennation angle and muscle parallel and serial hypertrophy. Nevertheless, the
thickness. A previous study from our group,3 using results of both studies confirm that neuromuscular
an identical neuromuscular electrical stimulation electrical stimulation treatment is an effective strat-
protocol, reported a similar increase in the muscle egy for restraining (and/or postponing) the charac-
thickness that was related to the increased fascicle teristic muscle atrophy associated with knee
length but not to the pennation angle in 12 elderly osteoarthritis. However, it is still unclear whether
patients with knee osteoarthritis after eight weeks neuromuscular electrical stimulation can change
of intervention. These results suggest that, despite the fascicle length or optimal angle for force pro-
using the same electrical stimulation protocol, a duction, and these issues require further
parallel increase in the number of sarcomeres was investigation.
responsible for the architectural changes in the The neuromuscular electrical stimulation proto-
vastus lateralis in our study. However, in the study col is critical for the induction of quadriceps mor-
by Vaz et al.,3 these changes were likely associated phological and functional changes. High-intensity
with an increase in the number of serial sarcom- electrical stimulation has been recommended when
eres. The reason for this different structural adap- the training is aimed at improving the strength;24,25
tation is yet unknown given that, with the exception a significant linear correlation between current
of the subject’s maximally tolerated stimulation intensity, the number of activated motor units and,
intensity, the neuromuscular electrical stimulation consequently, the measured external force has
parameters used during the interventions were the already been shown.26 However, progressive
same in both studies. increases in the intensity of neuromuscular electri-
Future investigations will try to identify whether cal stimulation are limited to the maximal discom-
the stimulation intensity is different between the fort tolerated by subjects, limiting our ability to
two groups of these studies, and whether this increase the mechanical overload on the muscle
Melo et al. 9
structures. The present study shows that, in addi- reduce muscle inhibition and muscle weakness,
tion to the electrical stimulation increase, when amplifying the effects of electrical stimulation on
aiming to promote muscle strengthening and to muscle strengthening. However, low-level laser
minimise muscle atrophy, neuromuscular electrical therapy did not potentiate the effects of neuromus-
stimulation protocols should ideally provide cular electrical stimulation as had been initially
increases in the treatment volume. expected. Although one could posit that combined
The fact that no between-group differences in neuromuscular electrical stimulation and low-level
terms of the functional and pain outcomes were laser treatment are not more effective than neuro-
observed was unexpected, because our hypothesis muscular electrical stimulation therapy alone, it is
was that low-level laser therapy should potentiate important to mention that pain is the main clinical
electrical stimulation effects owing to the anti- symptom used for assessing the severity of this
inflammatory and analgesic effects at the knee degenerative disease; therefore, low-level laser
joint. As no within-group differences were therapy should be considered an important clinical
observed during the control period, postinterven- tool for treating osteoarthritic patients. One of the
tion improvements seem to be related to the real possible limitations of this approach might be that
effects caused by the tested therapies. The neuro- only six points were used for the laser therapy
muscular electrical stimulation findings, regarding treatment. Perhaps additional points, or even higher
the functional and pain outcomes, are in accord- doses, might be necessary to affect the structural
ance with previous knee osteoarthritis studies per- outcomes. Additionally, the fact that participants
formed on elderly subjects.27,28. However, the were allowed to use analgesic or anti-inflammatory
low-level laser therapy effect observed on the func- drugs might have altered the effect of low-level
tional capacity of the osteoarthritic patients was laser therapy.17
reported for the first time. Another possibility is that the addition of low-
The improvements in the 6-minute walk test level laser therapy to neuromuscular electrical
performance associated with pain relief, suggest stimulation generated a false negative effect (Type
that reducing muscle weakness is not the only fac- II error), caused by the statistical test power
tor that produces functional improvement. The because the calculation used to determine the sam-
reduction in joint inflammation and pain owing to ple size considered a large effect size based on data
laser treatment might have been responsible for obtained from the use of neuromuscular electrical
this performance improvement. Furthermore, if stimulation alone in similar studies. However, even
muscle weakness associated with muscle atrophy if the above-stated possibilities are not confirmed,
has a unique influence on the progression of oste- it is important to note that the combined group
oarthritis,29 pain and inflammation at the initial patients might have obtained additional clinical
disease stages should accelerate the degenerative benefits (not evaluated via ultrasound or functional
process via muscle inhibition.30,31 Considering the tests) that patients receiving the isolated therapy
well-established analgesic effect of low-level did not obtain.
laser therapy,10–12,18 laser treatment most likely Despite the body of evidence on the positive
blocked the vicious cycle of pain, thereby decreas- effects of low-level laser therapy on cartilage,20,21 a
ing muscle inhibition and increasing physical placebo effect might have contributed to the
activity that had been reduced as a strategy to patients’ improved performance on the 6-minute
avoid pain. Ultimately, this will minimise muscle walk test. As an investigation of the real analge-
weakness. sic,19 anti-inflammatory11 and regenerative20,21
Our main hypothesis was that the combined use effects on cartilage is beyond the focus of the pre-
of low-level laser therapy and neuromuscular elec- sent study, future studies could use magnetic reso-
trical stimulation should have additional improve- nance imaging to evaluate the effect of low-level
ments on muscle structure and functional capacity, laser therapy on cartilage structure and inflamma-
because reduced pain and inflammation should tory markers in osteoarthritic patients, and to assess
10 Clinical Rehabilitation
the correlation of these effects with the clinical 3. Vaz MA, Baroni BM, Geremia JM, et al. Neuromuscular
findings of improved functionality. electrical stimulation (NMES) reduces structural and
functional losses of quadriceps muscle and improves
health status in patients with knee osteoarthritis. J Orthop
Res 2013; 31(4): 511–516.
Clinical messages 4. Lieber RL and Friden J. Functional and clinical signifi-
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muscle structure and function. muscle architecture, and muscle function in elderly post-
•• The combination of low-level laser ther- operative patients. J Appl Physiol 2008; 105: 180–186.
6. Bax L, Filip S and Verhagen A. Does neuromuscular elec-
apy and neuromuscular electrical stimula- trical stimulation strengthen the quadriceps femoris? A
tion did not produce any additional systematic review of randomized controlled trials. Sports
benefits in the muscle structure and Med 2005; 35(3): 191–212.
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trical stimulation and voluntary muscular contractions.
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8. MELO MO Aragão FA and Vaz MA. Neuromuscular
Contributors electrical stimulation for muscle strengthening in elderly
● MOM: Conception and design, training, data acqui- with knee osteoarthritis: A systematic review. Clin Compl
sition and data analysis, drafting, revising and final Ther Clin Prac 2013; 19: 27–31.
9. Durmus D, Alayli G and Cantürk F. Effects of quadri-
approval of the manuscript. BMB: Conception and
ceps electrical stimulation program on clinical parameters
design, revising and final approval of the manu-
in the patients with knee osteoarthritis. Clin Rheumatol
script. KP, GAB, DPSJ: Acquisition, analyses and 2007; 26(5): 674–678.
interpretation of data. MAV: Conception, design, 10. Bjordal JM, Klovning A, Ljunggren AE and Slørdal L.
training and supervision, data analysis and interpre- Photoradiation in acute pain: a systematic review of pos-
tation, English review and final approval of the sible mechanisms of action and clinical effects in rand-
manuscript. omized placebo-controlled trials. Photomed Laser Surg
2006; 24(2): 158–168.
11. Gur A, Cosut A, Sarac AJ, Cevik R, Nas K and Uyar A.
Acknowledgement
Efficacy of different therapy regimes of low-power laser
This work was supported by the Financiadora de in painful osteoarthritis of the knee: a double-blind and
Estudos e Projetos Ministério da Ciência e Tecnologia randomized-controlled trial. Lasers Surg Med 2003;
– FINEP [ 105074400], Fundação de Amparo e Ensino 33(5): 330–338.
à Pesquisa – PAPERGS [1015272 ] and Conselho 12. Hegedus B, Viharos L, Gervain M and Gálfi M. The effect
Nacional de Desenvolvimento Científico e Tecnológico of low-level laser in knee osteoarthritis: a double-blind,
randomized, placebo-controlled trial. Photomed Laser
– CNPq [ 304039/2012-8].
Surg 2009; 27(4): 577–584.
13. Kellgren JH and Lawrence JS. Radiological assessment of
Conflict of interest osteoarthrosis. Ann Rheum Dis 1957; 16: 494–501.
The authors report no conflict of interest. 14. Blazevich AJ. Effects of physical training and detrain-
ing, imobilization, growth and aging on human fascicule
geometry. Sports Med 2006; 36: 1003–1017.
Funding 15. Baroni BM, Geremia JM, Rodrigo R, Franke RDA,
This research received no specific grant from any funding Karamanidis K and Vaz MA. Muscle architecture adapta-
agency in the public, commercial, or not-for-profit sectors. tions to knee extensor eccentric training: rectus femoris
vs. vastus lateralis. Muscle Nerve 2013; 48: 498–506.
16. Terwee CB, Mokkink LB, Steutiens MP and Dekker J.
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