Lasers Med Sci
DOI 10.1007/s10103-015-1858-7
ORIGINAL ARTICLE
Effects of photobiomodulation on the fatigue level in elderly
women: an isokinetic dynamometry evaluation
P. G. Vassão 1 & R. L. Toma 1 & H. K. M. Antunes 1 & H. T. Tucci 2 & A. C. M. Renno 1
Received: 19 March 2015 / Accepted: 15 December 2015
# Springer-Verlag London 2015
Abstract Aging is responsible by a series of morphological
and functional modifications that lead to a decline of muscle
function, particularly in females. Muscle tissue in elderly peo-
ple is more susceptible to fatigue and, consequently, to an in-
creased inability to maintain strength and motor control. In this
context, therapeutic approaches able of attenuating muscle fa-
tigue have been investigated. Among these, the
photobiomodulation demonstrate positive results to interacts
with biological tissues, promoting the increase in cell energy
production. Thus, the aim of this study was to investigate the
effects of photobiomodulation (808 nm, 250 J/cm2, 100 mW,
7 J each point) in the fatigue level and muscle performance in
elderly women. Thirty subjects entered a crossover randomized
double-blinded placebo-controlled trial. Photobiomodulation
was delivered on the rectus femoris muscle of the dominant
limb immediately before the fatigue protocol. In both sessions,
peripheral muscle fatigue was analyzed by surface electromy-
ography (EMG) and blood lactate analysis. Muscle perfor-
mance was evaluated using an isokinetic dynamometer. The
results showed that photobiomodulation was able of reducing
muscle fatigue by a significant increase of electromyographic
fatigue index (EFI) (p = 0.047) and decreasing significantly lac-
tate concentration 6 min after the performance of the fatigue
protocol (p = 0. 0006) compared the placebo laser session.
* P. G. Vassão
patriciavassao@gmail.com
1
Department of Biosciences, Federal University of São Paulo Campus
Baixada Santista, Rua Silva Jardim, 136, 11015-020 Santos, São
Paulo, Brazil
2
Department of Human Movement Science, Federal University of São
Paulo Campus Baixada Santista, Rua Silva Jardim, 136,
11015-020 Santos, São Paulo, Brazil
However, the photobiomodulation was not able of increasing
muscle performance measured by the isokinetic dynamometer.
Thus, it can be conclude that the photobiomodulation was ef-
fective in reducing fatigue levels. However, no effects of
photobiomodulation on muscle performance was observed.
Keywords Aged . Muscle fatigue . Photobiomodulation .
Electromyography . Muscle strength dynamometer .
Muscle changes . Surface electromyography
Introduction
The global proportion of people aged over 60 years is growing
faster than any other age groups as a result of a longer life
expectancy combined with decreased fertility rates [1, 2]. It is
well known that aging is characterized by a general decline in
the physiological function of all systems, including in the
musculoskeletal tissue [3]. The specific muscle changes found
in the elderly include a marked loss of muscle motor units and
muscle fibers, with a consequential decrease in muscle mass
and strength. The result of these alterations is a decrease of
muscular performance and an increase in fatigue levels during
daily activities [4–9]. As a consequence, a higher index of
intolerance to physical exercise and sedentary lifestyle is pre-
sented by this population [10–12].
Many clinical interventions have been developed with the
aim of attenuating the effects of muscle mass loss and increas-
ing the tolerance to exercises in elderly people, for instance,
physical exercise programs, cryotherapy, stretching [13], and
more recently, photobiomodulation [14–16].
Many authors have showed that photobiomodulation is ca-
pable of stimulating the metabolism of many biological tissues
mainly through the absorption of light energy by mitochon-
dria, stimulating the respiratory chain [14]. As a consequence,

this interaction alters the redox potential of the cytoplasm and
accelerates the flow of electrons in the mitochondrial electron
transport chain, increasing ATP synthesis [17, 18]. According-
ly, an acceleration in cellular metabolism is observed, which
leads to an increase in the syntheses of DNA, RNA, and pro-
teins and higher levels of energy [17, 19–22].
Based on these stimulatory effects, studies have reported
the positive effects of photobiomodulation in increasing mus-
cle performance and attenuating muscle fatigue during phys-
ical exercise in different populations [19–23]. It seems that a
decreased level of creatine kinase (CK), enhanced anti-
oxidative capacity, reduced inflammatory reaction, and cell
apoptosis in exercised muscles were observed after
photobiomodulation, resulting in an improvement of muscle
recovery and optimizing the beneficial effects of physical ex-
ercises in different populations [23–25]. In elderly people,
Toma et al. (2013) verified that photobiomodulation was ef-
fective in increasing the mean number of repetitions during
knee flexion–extension exercises in elderly women [16].
Despite the positive results demonstrated by laser irradia-
tion, some points should be further investigated, such as the
ideal dose, mechanisms of action, and long-term effects on
muscle recovery, mainly in particular groups such as elderly
people. In this context, the aim of the present study was to
investigate the effect of photobiomodulation on fatigue and
muscle performance in elderly women through electromyog-
raphy measurements, lactate concentration levels, and
isokinetic dynamometry. Thus, it was hypothesized that
photobiomodulation (808 nm) lessens the deleterious effects
of muscle fatigue induced by an isokinetic fatigue protocol,
thus increasing the electromyographic fatigue index and atten-
uating the increase in lactate concentration, with consequential
improvements in muscle performance.
Material and methods
Inclusion criteria
Healthy female aged between 60 and 70 years with a body
mass index of 22 to 27 kg/cm2 and classified as irregularly
active or active, who performed physical activity with a fre-
quency of at least five times a week, totaling a minimum of
150 min per week, according to International Physical Activ-
ity Questionnaire (IPAQ)–Short Version and reports by partic-
ipants were included.
Exclusion criteria
Those with previous musculoskeletal injury to the quadriceps
femoris; diagnosis of lung diseases; uncontrolled hypertension
or diabetes; and orthopedic or rheumatic diseases, fibromyal-
gia, or pain that may prevent physical exercise were excluded.
Lasers Med Sci
After entering the study, participants who developed any os-
seous, muscular, or articular injuries were excluded. All vol-
unteers submitted a medical statement (exercise testing Bruce
protocol) stating that they were capable of performing high-
intensity exercise.
Study design and randomization
This study was a randomized, double-blind, crossover trial
with placebo control. The randomization procedure was per-
formed by a simple drawing of lots (A or B) which determined
whether participants would receive the active laser or placebo
treatment in the first session, initial laser placebo (ILP) proto-
col (n = 15) and initial laser active (ILA) protocol (n = 15).
Thus, if the volunteer received active laser in the first session,
in the second session, they received placebo and vice versa.
The randomization procedure was performed through a com-
puter program (Microsoft Excel 2010) that created a random
table of numbers in which each number corresponded to the
ILP or ILA group. After that, participants were allocated ac-
cording to the corresponding number of their allocation code.
A researcher conducted the drawing procedures without
informing participants and evaluators, to determine which
photobiomodulation (active or placebo) would be applied on
muscle. Thus, both participants and researchers were blinded
to the allocation of treatment.
Participants
Eighty-nine volunteers were recruited through newspapers
and radio from 2013 to 2014 (São Paulo, SP, Brazil) and were
evaluated. From these, 34 were selected to participate accord-
ing to the inclusion criteria. However, during the period of the
study, four participants were excluded for the following rea-
sons: three participants missed the second session and one
participant had knee pain before the first session. Thus, the
final sample size was 30 volunteers, assessed in the following
groups:
Laser placebo (LP)—participants who received placebo
laser in experimental sessions (n = 30);
Laser active (LA)—participants who received active laser
in experimental sessions (n = 30).
Experimental procedures
The experimental procedures were composed of two sessions
of fatigue protocol using an isokinetic dynamometer. The fol-
lowing steps constituted the first session: baseline blood col-
lection (for lactate measurement), warm-up on the cycle er-
gometer, and familiarization with the isokinetic dynamometer.
Afterward, the placebo or active photobiomodulation was
Lasers Med Sci
applied (according to the randomization) and the isokinetic
fatigue protocol was performed simultaneously with surface
electromyography (SEMG). At the end, blood samples were
taken again. After 7 days, the second session was performed
following identical procedures to the first session. However,
an inverse mode of photobiomodulation from the first session
(placebo or active) was applied for each individual [15, 16, 25,
26]. The two sessions were held 7 days apart, either on a
Tuesday or Thursday. Procedures are summarized in Table 1.
The initial physical assessment consisted of collecting data
about the weight; height; body mass index (BMI); pain assess-
ment (visual analog scale (VAS) of pain); range of motion of
the hip, knee, and ankle of the dominant lower limb (using a
goniometer); and the application of specific orthopedic tests to
shorten the muscles involved (Kendal test). The dominant
lower limb test was used to elect the lower limb selected for
isokinetic dynamometer and electromyographic evaluation
[27]. The IPAQ was used as a tool to assess the level of phys-
ical activity of volunteers in this step.
Lactate measurement
Collections of blood samples were obtained in both sessions
for measurement of lactate. In each session, five samples were
taken at the following times: prior to the isokinetic fatigue
protocol; immediately afterward (0 min); and then 3, 6, and
30 min after completion of the protocol. Blood samples were
collected from the earlobe using a disposable lancet. The first
drop of blood was discarded to avoid contamination, and then,
25 μl of arterial blood was collected using a calibrated hepa-
rinized glass capillary. Blood samples were placed in tubes,
containing 50 μl of 1 % sodium fluoride, to prevent continued
glycolysis, and were stored in a freezer at −10 °C for further
analysis. The analyses were effected using a YSI 1500 Sport
Lactate Analyzer (YSI Inc., Yellow Springs, OH, USA),
which was calibrated according to the manufacturer’s instruc-
tions. This procedure was based on Higashi et al. [28].
SEMG
The equipment used was a MyosystemBr1 (DataHominis
Tecnologia Ltda, Uberlândia, Brazil), with a 4-kHz frequency
and bandwidth filtered to 10–1.5 kHz, three amplification
stages, input impedance of 10 GΩ, with a 12-bit A/D with
converter board, and common mode rejection ratio of 130 dB.
The EMG signal was captured by active electrode surface
differential with 2 bars of Ag-AgCl and with a 10-mm inter-
electrode distance. A circular electrode (3 cm2) attached to the
tibial tuberosity of the ipsilateral limb was used as a reference
electrode for reducing acquisition noise.
The active electrodes were positioned according to the Eu-
ropean Recommendations for Surface Electromyography, Re-
sults of the SENIAM Project [29], 50 % on the line between
the spina iliaca anterior superior and the superior part of the
patella in the dominant lower limb. The skin at the electrodes’
sites was shaved and cleaned with alcohol to reduce skin im-
pedance and achieve good fixation, before the attachment of
electrodes using adhesive tape. During fatigue protocol, par-
ticipants were verbally encouraged to maintain muscle con-
traction by the same examiner. The EMG signal was acquired
over two sessions. After 1 week, the same participants per-
formed the second stage following the same procedures as the
first session.
The electromyographic signal of the rectus femoris muscle
was obtained during 60 repetitions of flexion–extension of the
knee, performed on an isokinetic dynamometer. The visuali-
zation and digital signal processing EMG were analyzed using
MyosystemBr1 software, version 3.5 (DataHominis
Tecnologia Ltda, Uberlândia, Brazil). The raw signals were
digitally filtered to a frequency bandwidth of 20–1000 Hz.
After this, the signal obtained in each experimental session
from 60 contractions was divided into the following two parts:
the median frequency of the first 20 contractions and the me-
dian frequency of the last 20 contractions. Fast Fourier trans-
form (FFT) analysis was used to calculate the power spectral
density of the EMG signal, and the values of median frequen-
cy were used to calculate the electromyographic fatigue index
using the following formula: electromyographic fatigue index
(EFI) = median frequency of last 20 contractions/the median
frequency of first 20 contractions. The electromyographic fa-
tigue index was determined according to the formula used for
calculating the work fatigue index (%) of the knee extensor
muscles by isokinetic dynamometer (Biodex software). These
indices were obtained in the two experimental sessions and
were compared between groups.
Isokinetic dynamometry
The fatigue protocol in isokinetic dynamometry was based on
previous studies [24] and performed in two sessions. Prior to
protocol, the volunteers held a 5-min cycle ergometer warm-
up (speed in the range of 60–70 rpm and no load). After that,
participants were positioned on the previously calibrated
isokinetic dynamometer and were properly aligned and stabi-
lized with straps in order to avoid possible compensatory
movements. The dominant lower limb was tested for all par-
ticipants, and all evaluations were performed unilaterally [27].
Thus, the dominant knee axis (lateral epicondyle of the femur)
of each subject was adjusted to the dynamometer rotation axis.
The lever arm of the equipment was fixed approximately 2 cm
above the tibial malleolus. The chair height, backrest distance,
seat angle, and dynamometer base were adjusted for each
subject and noted for the second session. The dominant mem-
ber was weighed according to the instruction manual of the
Biodex Multi-Joint System 3 isokinetic dynamometer (Biodex
Medical System Inc., NY, USA). Before starting the recording

Table 1 Timeline for the period of evaluation of groups (ILP and ILA)
of isokinetic muscle performance, there was a familiarization
period with the apparatus consisting of five submaximal vol-
untary concentric muscle contractions in the full range of stan-
dardized and preprogrammed motion (90–20°) according to
the guideline procedures of the dynamometer, with a constant
angular velocity of 180°/s. After a 10-min rest, while
photobiomodulation was applied, the isokinetic protocol was
performed with a set of 60 concentric contractions and recip-
rocal contractions of quadriceps and hamstrings. The partici-
pants were visually and verbally encouraged throughout the
test protocol to achieve maximum effort from the beginning.
The muscle performance, in terms of work fatigue index, peak
torque, average power, and total work of the knee extensor
muscles, was evaluated by isokinetic dynamometry in accor-
dance with the guidelines of the equipment manufacturer
(Biodex Medical System Inc.).
Experimental protocol of laser photostimulation
Immediately before the fatigue protocol of each session, the
participants received placebo or active laser. An AsGaAl laser
(Photon Laser III; DMC Importação e Exportação de
Equipamentos Ltda, São Carlos, SP, Brazil) was used with
the following parameters: λ = 808 nm, continuous mode,
100 mW, 7 J per point, 56-J total energy, 0.028-cm2 spot size,
250-J/cm2 diode energy density or fluency, 35.7-W/cm2 diode
power density or irradiance, and 70 s at each point [28].
The laser was applied using the punctual contact technique
with the beam applied at eight points distributed over the belly
of the rectus femoris muscle of the dominant limb. In order to
standardize the laser application, the irradiation treatment
points (active or placebo) were placed at 25, 35, 50, and
75 % of the total measurement obtained between the anterior
superior iliac spine and superior border of patella, bilaterally,
with 2 cm between each point. Participants and researchers
Lasers Med Sci
used opaque goggles during photobiomodulation in order to
protect their eyes from the laser.
Sample size calculation
Sample size was calculated based on lactate concentration
collected during the isokinetic fatigue protocol. Statistical sig-
nificance level of 0.05 was set as satisfactory, using 208 R
Development Core Team software [30].
Statistical analysis
Participants were crossed over during the experiment to com-
pare the possible effects caused by the order of application of
placebo and active laser on muscle fatigue, for each subject.
To evaluate if the order of laser application (placebo and ac-
tive) had effects on the variables, the ANOVA model was used
with repeated measurements for experiments in crossover. The
data analysis demonstrated that there was no influence of pla-
cebo or active laser order of application among the two
groups. Intra- and inter-group comparisons of EFI, work fa-
tigue index, peak torque, average power, total work, and blood
lactate sample variables were made. The post hoc compari-
sons were made using Tukey’s test. The significance level
used for all comparisons was set at 5 % (p ≤ 0.05).
Results
The final sample was 30 participants. The anthropometric
characteristics of volunteers are shown in Table 2.
Figures 1 and 2 show the intra- and inter-group evaluations
of the lactate level measurements in both experimental situa-
tions (LP and LA) and in all the periods of time analyzed
(basal, 0, 3, 6, and 30 min).
Lasers Med Sci

Table 2 Anthropometric
characteristics of
volunteers
EMG analysis demonstrated that the EFI was significantly
Variables Means and SD
higher in the active laser experimental condition compared to
Age (years) 63,70 ± 3,02 the placebo (p = 0.011; Table 3). The isokinetic dynamometer
Body mass (kg) 60,34 ± 9,32 performance analysis demonstrated that no significant differ-
Height (m) 1,55 ± 0,07 ences for any of the variables measured were observed (work
BMI (kg/m2) 24,97 ± 3,21 fatigue index p = 0.796, peak torque p = 0.349, average power
p = 0.295, and total work p = 0.241) between both experimen-
BMI body mass index, kg kilograms, m tal conditions (Table 3).
meters, kg/m2 kilograms per square meter

The intra-group evaluation demonstrated that the basal lactate

levels for both experimental conditions were lower compared to
the levels measured after the fatigue protocol (0, 3, 6, and
30 min; Fig. 1). Furthermore, a statistically significant difference
was observed between the times 0 vs 3 min (p = 0.0083), 0 vs
6 min (p = 0.0004), 3 vs 30 min (p < 0.0001), and 6 vs 30 min
(p < 0.0001) for the placebo laser experimental condition. For
the active laser experimental condition, significant differences
were observed between the times 0 vs 3 min (p = 0.0139), 3 vs
6 min (p = 0.0232), and 3 vs 30 min (p < 0.0001).
Moreover, the behavior of the lactate concentration be-
tween the groups was also compared at each experimental
time point (Fig. 2). A significant difference between groups
was observed 6 min after the fatigue protocol, the concentra-
tion being higher in the placebo group compared to the active
group (p = 0.0006). No other significant difference in the other
periods analyzed was observed (for 0, 3, and 30 min after
fatigue protocol, p values of 0.17, 0.37, and 0.15,
respectively).
Discussion
The aim of this study was to investigate the influence of
photobiomodulation on fatigue and muscle performance of
quadriceps in elderly women submitted to a fatigue exercise
protocol using an isokinetic dynamometer. The hypothesis
was that photobiomodulation would stimulate muscle metab-
olism, consequently decreasing fatigue levels and increasing
performance. The results showed that the application of
photobiomodulation was effective in reducing muscle fatigue
by decreasing lactate concentration 6 min after the fatigue
protocol and increasing EFI. However, muscle performance,
as measured by the isokinetic dynamometer, was not im-
proved by photobiomodulation.
Recent studies have demonstrated the beneficial effects of
photobiomodulation on muscle fatigue levels in different pop-
ulations, mainly by the stimulation of cellular bioenergetics
and ATP synthesis, which contribute to an increase of cellular

Fig. 1 Mean and standard

deviations of intra-group lactate
concentrations over time, before
and after fatigue protocol for LP
and LA groups (*p < 0.05)
 Lasers Med Sci

Fig. 2 Mean and standard

deviations of inter-group lactate
concentrations over time before
and after fatigue protocol for LP
(gray) and LA (black) groups
(*p < 0.05)

energy [14, 16, 23, 25, 26, 31, 32]. Moreover, it seems that
photobiomodulation is capable of increasing tissue vasculari-
zation, which in turn accelerates blood flux and lactate remov-
al during exercise [15, 24, 26]. In addition, studies report that
the vasodilatation produced by photobiomodulation occurs
due to active nitric oxide in the endothelial smooth muscle
relaxation [33] and due to thermal effects [34].
In the present study, the intra-group lactate analysis showed,
for both groups, a significant increase in lactate concentration
after the isokinetic fatigue protocol. These findings demonstrate
that the isokinetic fatigue protocol used in this study was effec-
tive in inducing muscle fatigue in the volunteers. Furthermore,
the inter-group analysis demonstrated a positive effect of laser
on lactate removal 6 min after the fatigue protocol. Similar
results were observed in other clinical trials, in which laser
and light-emitting diode therapy were capable of maintaining
the blood lactate levels immediately after high-intensity exer-
cise protocols. This was probably due to its effects on energy
metabolism causing an increase in microcirculation and conse-
quently removing lactate [25, 31, 32].
It is well known that muscle fatigue leads to changes in
motor unit recruitment due to a deficiency in neuromuscular
Table 3 Mean and standard deviation values of isokinetic dynamometer
and electromyographic analysis
Variables LP LA
Work fatigue index (%) 58.37 ± 683 57.93 ± 6.56
Peak torque (Nm) 57.26 ± 989 59.72 ± 10.19
Average power (W) 55.5 ± 990 58.25 ± 10.05
Total work (J) 1794.34 ± 30022 1880.49 ± 280.65
EFI (score) 0.73 ± 0.07* 0.78 ± 0.09*
% percentage, Nm Newton meter, W watts, J joules, EFI electromyo-
graphic fatigue index
*p < 0.05
transmission or propagation of the action potential along the
muscle fibers [35]. This state may be reflected by electromyo-
graphic activity. Regarding the EMG data evaluated in the
present study, a higher EFI was identified in the active laser
group compared to the placebo laser group. Higher EFI indi-
cates a larger attenuation of muscle fatigue, suggesting that
photobiomodulation prevented the decrease in the excitation
of the muscle membrane potential, probably due to increased
electron transport and mitochondrial respiratory chain ATP
synthesis, which provided more energy for muscle contraction
[36, 37]. In a study by Vieira et al. [36], a higher EFI was
also observed in the group irradiated by laser (808 nm).
Thus, in this present study, photobiomodulation possibly
increased cellular metabolism with a consequent increase
in the production of ATP, providing more energy to the
rectus femoris muscle.
Furthermore, it was hypothesized that a decrease in muscle
fatigue would interfere with the increase in muscle perfor-
mance. However, in the present study, no difference was ob-
served between groups in the isokinetic dynamometer param-
eters. These findings do not corroborate studies that similarly
analyzed the effects of photobiostimulation on muscle tissue
using an isokinetic dynamometer. Baroni et al. [32] and dos
Santos Maciel et al. [31] found that the application of lasers
(810 and 780 nm, respectively) before a fatigue protocol was
effective in increasing the peak torque in healthy young males
and females.
In spite of the positive results of the present work, some
limitations should be considered. Although the 808-nm infra-
red laser used in this study demonstrated the capability of
penetrating deeply into tissues, the laser device used presented
a small spot size, which limited the area of irradiation in the
quadriceps and necessitated a long period of irradiation.
Therefore, further studies using other devices for irradiation,
such as clusters, should be performed with the aim of maxi-
mizing the effects of the irradiation.
Lasers Med Sci
Conclusion
The results of the present study showed that the application of
photobiomodulation in a single session was capable of atten-
uating muscle fatigue in elderly women when applied prior to
an isokinetic fatigue protocol. These findings open a clinical
window to the use of photobiomodulation on the elderly to
improve muscle performance and reduce muscle fatigue, in
association with a strength exercise program.
Acknowledgments The authors thank Mariane Stanev, Ph.D. from the
Comparative Literature Department, University of Michigan, and the
research subjects.
Compliance with ethical standard All procedures were approved by
the Ethics Committee of the Federal University of São Paulo (approval
number 528.166) and registered at ClinicalTrials.gov (RBR-28mjwb). All
participants were informed about the purpose and procedures of the study
and signed an informed consent declaration before their participation in
the experiment.
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