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ORIGINAL ARTICLE
Effects of low-level laser therapy (808 nm) on isokinetic
muscle performance of young women submitted
to endurance training: a randomized controlled clinical trial
Wouber Hérickson de Brito Vieira &Cleber Ferraresi &
Sérgio Eduardo de Andrade Perez &Vilmar Baldissera &
Nivaldo Antônio Parizotto
Received: 12 April 2011 / Accepted: 3 August 2011
#Springer-Verlag London Ltd 2011
Abstract Low-level laser therapy (LLLT) has shown
efficacy in muscle bioenergetic activation and its effects
could influence the mechanical performance of this tissue
during physical exercise. This study tested whether endur-
ance training associated with LLLT could increase human
muscle performance in isokinetic dynamometry when
compared to the same training without LLLT. The primary
objective was to determine the fatigue index of the knee
extensor muscles (FIext) and the secondary objective was
to determine the total work of the knee extensor muscles
(TWext). Included in the study were 45 clinically healthy
women (21±1.78 years old) who were randomly distributed
into three groups: CG (control group), TG (training group)
and TLG (training with LLLT group). The training for the
TG and TLG groups involved cycle ergometer exercise
with load applied to the ventilatory threshold (VT) for 9
consecutive weeks. Immediately after each training session,
LLLT was applied to the femoral quadriceps muscle of both
lower limbs of the TLG subjects using an infrared laser
device (808 nm) with six 60-mW diodes with an energy of
0.6 J per diode and a total energy applied to each limb of
18 J. VT was determined by ergospirometry during an
incremental exercise test and muscle performance was
evaluated using an isokinetic dynamometer at 240°/s. Only
the TLG showed a decrease in FIext in the nondominant lower
limb (P=0.016) and the dominant lower limb (P=0.006).
Both the TLG and the TG showed an increase in TWext in
the nondominant lower limb (P<0.001 and P=0.011,
respectively) and in the dominant lower limb (P<0.000 and
P<0.000, respectively). The CG showed no reduction in
FIext or TWext in either lower limb. The results suggest that
an endurance training program combined with LLLT leads to
a greater reduction in fatigue than an endurance training
program without LLLT. This is relevant to everyone involved
in sport and rehabilitation.
Keywords Low-level laser therapy (LLLT) .Endurance
training .Fatigue index .Isokinetic dynamometer
Introduction
The radiation from low-level laser therapy (LLLT) interacts
with biological tissues triggering several physiological and/
or therapeutics effects [1,2], and LLLT has been shown to
enhance muscle performance in animal experiments [3–6],
in strength training in humans [7] and in maximum tests of
effort in isokinetic dynamometry also in humans [7,8].
LLLT seems to act on cellular energy metabolism, stimulat-
ing photochemical and photophysical events in the mito-
chondria [2,9,10]. It also promotes structural and
metabolic changes in the organelles of different cells and/
or tissues [9,11] that may be involved in the membrane
W. H. de Brito Vieira (*)
Department of Physical Therapy, Federal University of Rio
Grande do Norte (Campus Universitário Lagoa Nova),
Av. Senador Salgado Filho, 3000,
59072-970 Natal, RN, Brazil
e-mail: hericksonfisio@yahoo.com.br
C. Ferraresi :N. A. Parizotto
Department of Physical Therapy, Laboratory of
Eletrothermophototherapy, Federal University of São Carlos,
Rodovia Washington Luís, km 235,
13565-905 São Carlos, SP, Brazil
S. E. de Andrade Perez :V. Baldissera
Department of Physiological Sciences, Laboratory of Physiology
of Exercise, Federal University of São Carlos,
Rodovia Washington Luís, km 235,
13565-905 São Carlos, SP, Brazil
Lasers Med Sci
DOI 10.1007/s10103-011-0984-0
potential [12] and enzymatic activity [11,13]. The
structural changes in mitochondria promoted by LLLT
include the formation of giant mitochondria through the
merging of membranes of smaller and neighboring mito-
chondria [14]. This structural adaptation (larger mitochon-
dria) possibly results in the ability to provide higher levels
of respiration and energy (ATP) to cells, characteristic of a
metabolic adaptation (higher enzymatic machinery) [14].
Endurance training is a kind of training that can possibly
be modulated by LLLT. This training leads to an increase in
aerobic capacity [15,16] and stimulates type I muscle fibers
(oxidative) or type II fibers (oxidative and glycolytic) to
develop more mitochondria for metabolizing energy sub-
strates through oxidative phosphorylation [17,18]. The
highest aerobic capacity acquired from endurance training
can be assessed and/or monitored by an incremental and
dynamic physical test of effort on a cycle ergometer [19].
This evaluation utilizes a gas analyzer to measuring
inspired and expired gases during exercise and identifies,
for example, the ventilatory threshold (VT, the point that
indicates an exponential increase in ventilation to counter
the metabolic acidosis that occurs as a result of the
accumulation of H
+
ions from anaerobic glycolysis, which
supplements aerobic ATP production in high-intensity
exercise) [19]. Furthermore, endurance training increases
the expression of mitochondrial genes that are associated
with structural (number of mitochondria) and metabolic
adjustments (higher enzymatic machinery), which favors
aerobic metabolism and muscular endurance, i.e. fatigue
reduction during exercise [17,18].
Muscle fatigue promoted by repeated muscle contractions
is associated with the accumulation of inorganic phosphate,
ADP, magnesium ions, hydrogen ions and reactive oxygen
species in the muscle cells. In addition, muscle fatigue also
decreases sources of ATP such as muscle glycogen and
phosphocreatine [20]. Thus, muscle performance quantifica-
tion (torque, number of muscle contractions and fatigue) can
demonstrate indirectly the adaptation of skeletal muscle to
metabolic stress from exercise and can also identify muscle
responses to exercise with phototherapy stimulation [3,4,7,
8,21]. Isokinetic dynamometry has been used to evaluate
muscle performance in subjects submitted to phototherapy
before or after intense exercise [7,8,21]. The isokinetic
dynamometer is considered gold-standard equipment to
measure muscle performance and consequently muscle
fatigue, because the angular velocity (or the muscle-
shortening velocity) is always controlled (isokinetic) during
articular movement [21,22]. Thus, the force–velocity
relationship does not affect muscle torque or work produc-
tion or the muscle fatigue index [21].
The purpose of this study was to determine if a chronic
endurance training program with LLLT would enhance the
effects of chronic endurance training without LLLT. The
considered hypothesis was that a program of chronic
endurance training with LLLT could promote a greater
increase in muscle performance than endurance training only.
The study was a randomized controlled clinical trial to
determine the fatigue index (primary objective) and the total
work (secondary objective) of the knee extensor muscles
(FIext and TWext, respectively) by isokinetic dynamometry.
Methods
The study was designed as a randomized controlled clinical
trial. All procedures were approved by the Ethics in Human
Research Committee of the Federal University of São
Carlos and the study was registered with NIH Clinical
Trials (NCT01391195). The subjects were recruited from
among graduate students at the Federal University of São
Carlos. All subjects were informed about purposes proce-
dures of the study and signed a consent form.
Subjects
The subjects were 45 female students who reported being
clinically healthy.
Inclusion criteria
The inclusion criteria were: healthy female aged between
18 and 28 years with a body mass index between 18 and 25
kg/m
2
, and with a beginner or moderately trained pattern of
physical activity, i.e. performed some physical activity with
a noncompetitive aim one to three times a week, as
described previously [23].
Exclusion criteria
The exclusion criteria were: previous injury to the femoral
quadriceps or hamstring muscles (within 6 months prior to
the study), osseous or articular disorder of the lower limbs,
cardiovascular system disorder or systemic disease such as
those in a previous study [7].
Randomization
Randomization was performed by a simple drawing
procedure and the subjects were distributed equally into
three groups: training with LLLT group (TLG), training
alone group (TG) and control group (CG).
Study groups
TG and TLG subjects were submitted to a program of
chronic endurance training involving cycle ergometer
Lasers Med Sci
exercise three times a week for 9 consecutive weeks. Soon
after the end of each training session, the TLG subjects
underwent LLLT to both femoral quadriceps muscles. CG
subjects did not carry out any form of intervention and did
not receive any treatment. Thus, this group was evaluated
only at the beginning and at the end of the study.
Instruments
The following instruments were used: a computerized
isokinetic dynamometer (Multi-Joint System 3; Biodex,
New York, NY) to record the isokinetic variables of muscle
performance (FIext and TWext); a gas analyzer (VO2000;
MedGraphics, St. Paul, MN USA) for determination of VT
and an electromagnetic brake cycle ergometer (Ergo Cycle
167; Ergo-FIT, Pirmasens, Germany).
Procedures
The subjects were submitted to physiotherapeutic, nutri-
tional and medical evaluations during the morning in order
to ensure acceptable clinical and procedural conditions for
participation in the study. Next, a dynamic and incremental
test was performed on the cycle ergometer with respiratory
gas uptake (cardiopulmonary exercise test) to determine the
VT, which was used as the training load. This assessment
was repeated every 3 weeks to adjust the training load. In
the afternoon of the same day, the subjects’muscle
performance was evaluated by isokinetic dynamometry in
which FIext and TWext values were determined. All
subjects were instructed to keep to their normal physical
routine and eating habits during the study, to sleep for about
8 h per night, and not to consume alcohol or drugs.
Assessment protocols
All protocols for muscle performance assessment and
workload adjustment were performed by the same evalu-
ator. It is important to note that the assessments at baseline
and after 9 weeks were conducted on different training
days.
Protocol I (isokinetic dynamometry) A brief 5-min warm-
up was carried out on a cycle ergometer with a load of
50 W and a speed in the range 60–70 rpm. Next, the
subjects were positioned on the isokinetic dynamometer
which had been previously calibrated. The subjects stood
properly aligned and stabilized with straps in order to avoid
possible compensatory movements in accordance with the
guidelines for the device. Both lower limbs were evaluated
in a random order for each subject. The dynamometer
rotation axis was adjusted to the knee axis of the subject at
the lateral epicondyle of the femur. The hip was stabilized
at 80° and the lever arm of the equipment was set
approximately 1 cm above the tibial malleolus. Parameters
such as chair height, back-rest distance, seat angle and
dynamometer base were adjusted for each subject (Fig. 1a).
Before starting the recording of isokinetic muscle
performance, there was a familiarization period with the
apparatus that consisted of three submaximal voluntary
concentric muscle contractions in the full range of
standardized and preprogrammed motion (90–15º), with a
constant angular velocity at 240º/s. After a 3-min rest, the
test began with one set of 60 concentric and reciprocal
quadriceps and hamstring contractions in all ranges of
standardized and preprogrammed knee motion in flexion
and extension. The subjects were encouraged verbally and
visually to achieve maximum effort. FIext was calculated
as: 100 −[(work last third/work first third) × 100]. TWext
was calculated as the graphical area of all repetitions (torque
curve versus displacement) of the test in accordance with the
guidelines of the equipment manufacturer (BIODEX).
Protocol II (incremental and dynamic test of effort on the
cycle ergometer) The subjects remained for 2 min at rest on
the cycle ergometer to capture baseline values of the
inspired and expired gases (Fig. 1b). The protocol was
then started with load (power) of 25 W and a load increment
of 25 W every 2 min of activity (Balke’s protocol). The test
was always taken to the maximum (until volitional
exhaustion) or until the appearance of signs and limiting
symptoms, such as dyspnea, limiting pain in the legs or
chest pain. The volunteers were instructed to keep the speed
always around 60–70 rpm. VT was determined by an
experienced examiner through visual inspection of ventila-
tion curves, oxygen equivalent and/or expired fraction of
oxygen. For each block of effort, the volunteer pointed to
their perceived level of subjective effort on the Borg scale
(6–20 points) [24]. The heart rate of the subjects, room
temperature (22–25°C) and relative humidity (40–60%)
were also monitored.
Protocol III (training on the cycle ergometer) The TG and
TLG training was always conducted in the afternoon three
times a week for 9 consecutive weeks, with an effort load
corresponding to VT obtained in protocol II. The volunteers
were instructed to keep their speed around 60–70 rpm
during the training sessions. Each training session started
with 5 min of warm-up and ended with 5 min of cooling,
both with a load below the VT. The training sessions lasted
for 40 min in the 1st, 4th and 7th week, 50 min in the 2nd,
5th and 8th week, and 60 min in the 3rd, 6th and 9th week.
The loads were increased at the end of the 3rd and 6th
weeks of training in accordance with the VT obtained in a
new incremental effort test (protocol II). Each training
session was supervised by an instructor and all parameters
Lasers Med Sci
followed all the recommendations of the American College
of Sports Medicine [15].
Protocol IV (LLLT application) TLG subjects underwent
LLLT immediately after each training session while the
physiological stress and the consequent metabolic changes
were still present, since the efficacy of LLLT is known to be
increased under these conditions [25]. Using a contact
technique, the infrared laser beam was kept stationary and
perpendicular to the skin during 27 sessions in five different
areas distributed uniformly over the belly of the femoral
quadriceps muscle of each lower limb [26] giving in total 30
irradiated points per session (Fig. 1c). A near-infrared Ga-Al-
As laser (808 nm) with six obliquely arranged diodes
was used operating in continuous mode. The equipment
and LLLT parameters used were as follows: six diodes of
60 mW radiant power each; 10 s application time in each area;
0.6 J radiant energy per point (diode); 0.0028 cm
2
beam area;
214.28 J/cm
2
diode energy density or fluency; and 21.42 W/
cm
2
diode power density or irradiance. Thus, the total
application time for each lower limb was 50 s per session
(for a total of 100 s for the two limbs), the total energy
applied to each lower limb per session was 18 J (for a total of
36 J for the two limbs), and there were 30 application points
(for a total of 60 points for the two limbs).
Statistical analysis
The normality of the data distribution was analyzed using
the Shapiro-Wilk test and the homogeneity of variances
using Levene’s test. The effect of training on muscle
performance in isokinetic dynamometry was evaluated by
two-way analysis of variance with repeated measures only
on one factor. The independent factors were group (with
three levels: TLG, TG and CG) and time (with two levels:
baseline and after 12 weeks), which was also considered as
a repeated measurement. When significant differences were
found, Tukey’s post-hoc test was applied. Significance was
set at P<0.05.
Results
Table 1shows the demographic data of all the groups.
The TLG was the only group that showed a decrease in
FIext (the primary objective) for the nondominant (P=0.016)
and the dominant lower limb (P=0.006) after training. The
TG showed a decrease in FIext in both lower limbs (but
without statistical significance, P>0.05), and the CG showed
no change in FIext from the baseline values. Among the
groups no statistical differences were observed (P>0.05).
The detailed FIext results for both lower limbs of all groups
(CG, TG and TLG) are presented in Tables 2and 3,and
these results are presented graphically in Fig. 2.
The TG and TLG showed an increase in TWext (the
secondary objective) for the nondominant lower limb
(P=0.011 and P< 0.001, respectively) and for the domi-
nant lower limb (P<0.001 and P< 0.001, respectively)
after training. However, there were no significant differ-
ences between the groups (P>0.05). The detailed TWext
results for both lower limbs of all groups (CG, TG and
Fig. 1 Subject positioning for
the isokinetic dynamometry test
(a) and the ergospirometry test
(b). Application points for LLLT
on the knee extensor muscles (c)
Table 1 Anthropometric
characteristics of the three study
groups before and after
endurance training. Values are
means and standard deviations
Variable CG TG TLG
Before After Before After Before After
Age (years) 21.2± 2.1 –20.5± 1.3 –21.2 ± 1.7 –
Height (m) 1.63± 0.04 –1.60± 0.04 –1.64 ± 0.05 –
Body mass (kg) 54.5±5.2 55.3± 5.3 56.3± 6.2 57.1 ± 6.7 55.1± 6.8 55.7±6.5
BMI (kg/m
2
) 20.5± 1.8 20.8 ± 1.7 21.8± 2.1 22.2±2.3 20.6±1.8 20.7± 1.7
Lasers Med Sci
TLG) are presented in Tables 2and 3, and these results
are presented graphically in Fig. 3.
Discussion
With regard to the primary objective, the TLG was the only
group that showed a decrease in FIext after training, demon-
strating a beneficial effect of LLLTon muscle performance. The
TG also showed a decrease FIext but without statistical
significance, and the CG showed no change in FIext from the
baseline values (Fig. 2).TheFIexthasbeenusedtoassessthe
muscle endurance of subjects under fatigue protocols after
phototherapy [21], and this index, obtained by isokinetic
dynamometry, is a reliable measure of muscle response in the
evaluation of physical exercise to exhaustion [27]. With regard
to previous studies in which FIext was determined, some did
not evaluate fatigue reduction [21,28], while others corrob-
orate the results of this study in showing that LLLT promotes
a reduction in human muscle fatigue by increasing the number
of maximal voluntary contractions [29,30]. The total energy
used in previous studies that found significant differences
were 20 J for each member irradiated, similar to that found in
the present study (18 J). Furthermore, the muscle groups
irradiated were different (biceps brachial versus femoral
quadriceps) as well as the fluency (500 J/cm
2
and 1,785 J/
cm
2
versus 214.28 J/cm
2
) and the number of points irradiated
per limb (4 points versus 30 points). Compared with a more
recent study that also found better muscle performance of
subjects following LLLT [7], the parameters used were very
similar: irradiated limb, distribution of application points,
fluency, power density and total energy per member during
1weekoftraining(50.4Jversus54J).
With regard to the secondary objective, the TG and TLG
showed a significant increase in TWext after training (9 weeks),
but no differences were observed between the groups (Fig. 3).
These results demonstrate that the training was effective in
increasing the energy expended by subjects submitted to
endurance training during the fatigue test. TWext represents
the amount of energy (in Joules) that the knee extensor
muscles are able to produce during muscle contractions
(repetitions) in the performance test [27]. This energy is
calculated in terms of the graphical area of torque curves
versus displacement [27]. If the torque curves and time of
muscle contraction (displacement) are smaller, the total work
will also be lower [27]. Thus, the analysis of TWext associated
with FIext determines how torque curves versus displacement
ranged during fatigue testing and consequently it quantifies
decreases in torque production [27]. The present results do not
agree with those reported by Baroni et al. [21] who similarly
evaluated TWext and the FIext and found no improvement in
TWext or FIext in irradiated subjects. One possible reason is
related to the number of photostimulation application points
on the femoral quadriceps (3 points versus 30) and the
number of application sessions (1 versus 27 days).
After comparing the results found in this study with the
results already reported in the scientific literature, there
remains a gap in our understanding as to how LLLT can
improve muscle performance. This study was not designed to
identify the biochemical (energy metabolism) and genetic
(gene expression) effects of laser irradiation on skeletal muscle,
but to raise hypotheses that might elucidate these effects:
Table 2 FIext and TWext for the nondominant lower limbs. Values are means and standard deviations
Variable CG TG TLG
Before After PBefore After PBefore After P
FIext 65.1± 4.4 64.2 ± 5.5 0.992 66.5 ±4.5 62.9±5.9 0.201 63.8± 9.2 58.3 ± 7.6 0.016*
TWext 2,309.8± 255.6 2,403.4 ± 205.6 0.568 2,435.8±379.6 2,636.6 ± 477.2 0.011* 2,340.1± 484.2 2,644.3 ±473.2 <0.001*
*P<0.05, before vs after endurance training.
Table 3 FIext and TWext for the dominant lower limbs. Values are means and standard deviations
Variable CG TG TLG
Before After PBefore After PBefore After P
FIext 64.8±4.2 63.3± 2.9 0.760 64.5± 5.8 61.7±3.1 0.173 62.1 ± 6.8 57.7 ±5.4 0.006*
TWext 2,350.5 ± 316.3 2,417.4 ±230.5 0.798 2,501.3±433.6 2,813.0 ± 435.5 <0.001* 2,373.1 ±409.8 2,682.5± 490,2 <0.001*
*P<0.05, before vs after endurance training.
Lasers Med Sci
First hypothesis Structural changes in mitochondria of
tissues under laser therapy have been
reported, mainly involving the formation
of giant mitochondria through the merg-
ing of the membranes of smaller and
neighboring mitochondria [14]. These
organelles have receptors for laser pho-
tons such as the enzyme cytochrome c
oxidase [2,10,11,13]. The enzyme
cytochrome coxidase is a mitochondrial
enzyme responsible for the transfer of
electrons from complex III to complex
IVof the electron transport chain, direct-
ly involved in ATP synthesis (ATP) [13].
Thus, LLLT can increase muscle ATP
synthesis both by increasing the amount
of cytochrome coxidase and its activity
[13] or by increasing the activity of the
four complexes of the mitochondrial
electron transport chain, featuring a
metabolic adaptation (more ATP) for
cellular activity [11].
Second hypothesis The alactic anaerobic metabolism (phos-
phocreatine) provides ATP to skeletal
muscle during the first seconds of high-
intensity physical activity. This mecha-
nism requires resynthesis of creatine to
phosphocreatine to continue to supply
AT P d u r i n g e x e r c i s e [ 16]. This ATP
synthesis depends on ATP produced
aerobically by mitochondria via a mech-
anism called the mitochondrial creatine
shuttle, described by Tonkonogi and
Sahlin [16] and recently studied by
Ferraresi et al. [7]. Thus, the better
fatigue resistance of the TLG group in
the fatigue test may have been related
to higher amounts of alactic energy
(phosphocreatine), which may have
been a result of training and laser
photostimulation.
Third hypothesis Muscle fatigue has been related to accu-
mulation of hydrogen ions inferred from
lactate levels in the blood [31] and with
subjectively perceived increases in effort
[32]. Accordingly, Brooks et al. [31]and
Hashimoto et al. [33] have described a
mechanism for conversion of pyruvate to
lactate in the intermembrane space and in
the mitochondrial matrix of muscle cells,
contributing to lower lactate accumula-
tion and increased energy availability
during exercise, as discussed by Ferraresi
et al. [7].
Fig. 2 FIext for both lower
limbs. *P<0.05, before vs after
endurance training (TLG
dominant limb P=0.006, TLG
nondominant limb P=0.016)
Fig. 3 TWext for both lower
limbs. *P<0.05, before vs after
endurance training (TG and
TLG dominant limb P<0.001,
TG nondominant limb P=0.011,
TLG nondominant limb
P<0.001)
Lasers Med Sci
Fourth hypothesis In the TLG subjects the concentra-
tion of the cytosolic enzyme lactate
dehydrogenase (LDH) probably de-
creased [8], specifically the LDHA4
isoform which is considered a pyru-
vate reductase and has a greater
abilitytotransformpyruvicacidinto
lactic acid [34]. Thus, a lower con-
centration of LDHA4 leads to lower
levels of lactic acid production and
possibly decreases or delays the onset
of fatigue [31,32,35].
Fifth hypothesis Perhaps TLG subjects had an increase in
the expression of mitochondrial genes,
such as PPARCG-1α(peroxisome
proliferator-activated receptor gamma,
coactivator 1 alpha), or NRF-1 and NRF-
2 (nuclear respiratory factory 1 and 2)
during and after training followed by
LLLT [7]. In addition, other genes in-
volved in energy metabolism, such as
LDHC (encoding the LDH cytosolic
enzyme) or COX (encodes the cyto-
chrome coxidase enzyme) were possibly
modulated by training followed by LLLT.
The study had some limitations. TG subjects did not
receive a placebo laser treatment as performed in previous
studies [8,21,29,30], blood chemistry was not assessed
(immunological and inflammatory responses), and myo-
genic enzyme (creatine kinase) and metabolic enzymes
(such as LDH) were not assessed before and after exercise
training [8,29,30]. Another limitation is that possible
increases in body temperature, mainly of the femoral
quadriceps and the whole lower limb, following laser
therapy were not assessed although TLG subjects did not
report any warming.
Conclusion
The study results suggest that endurance training combined
with LLLT might be superior to endurance training only. We
emphasize that care is needed in generalizing the results.
Further studies, investigating in particular LLLT, myogenic
enzymes, blood chemistry and gene expression, are
necessary to elucidate the interaction between laser radia-
tion and metabolic and molecular mechanisms of recovery
and muscle performance.
Acknowledgments The authors would like to thank the Department of
Physical Therapy and the Department of Physiological Sciences of the
Federal University of São Carlos for assistance with this study, the
research volunteers, the Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq) for partial funding of the research, and
the DMC Equipamentos for manufacturing and lending the laser device.
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