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ORIGINAL ARTICLE
Phototherapy with combination of super-pulsed laser
and light-emitting diodes is beneficial in improvement
of muscular performance (strength and muscular endurance),
dyspnea, and fatigue sensation in patients with chronic
obstructive pulmonary disease
Eduardo Foschini Miranda &Luís Vicente Franco de Oliveira &
Fernanda Colella Antonialli &Adriane Aver Vanin &
Paulo de Tarso Camillo de Carvalho &Ernesto Cesar Pinto Leal-Junior
Received: 5 August 2014 /Accepted: 5 November 2014
#Springer-Verlag London 2014
Abstract Phototherapy is an electrophysical intervention be-
ing considered for the retardation of peripheral muscular fatigue
usually observed in chronic obstructive pulmonary disease
(COPD). The objective of this study was to evaluate the acute
effects of combination of super-pulsed laser and light-emitting
diodes phototherapy on isokinetic performance in patients with
COPD. Thirteen patients performed muscular endurance tests
in an isokinetic dynamometer. The maximum voluntary iso-
metric contraction (MVIC), peak torque (PT), and total work
(TW) of the non-dominant lower limb were measured in two
visits. The application of phototherapy or placebo (PL) was
conducted randomly in six locations of femoral quadriceps
muscle by using a cluster of 12 diodes (4 of 905 nm super-
pulsed lasers, 0.3125 mW each; 4 of 875 nm LEDs, 17.5 mW
each; and 4 of 640 nm LEDs, 15 mW each, manufactured by
Multi Radiance Medical™). We found statistically significant
increases for PT (174.7±35.7 N·m vs. 155.8±23.3 N·m, p=
0.003) and TW after application of phototherapy when com-
pared to placebo (778.0±221.1 J vs. 696.3±146.8 J, p=0.005).
Significant differences were also found for MVIC (104.8±
26.0 N·m vs. 87.2±24.0 N·m, p=0.000), sensation of dyspnea
(1 [0–4] vs. 3 [0–6], p=0.003), and fatigue in the lower limbs (2
[0–5] vs. 5 [0.5–9], p=0.002) in favor of phototherapy. We
conclude that the combination of super-pulsed lasers and LEDs
administered to the femoral quadriceps muscle of patients with
COPDincreasedthePTby20.2%andtheTWby12%.
Phototherapy with a combination of super-pulsed lasers and
LEDs prior to exercise also led to decreased sensation of
dyspnea and fatigue in the lower limbs in patients with COPD.
Keywords Chronic obstructive pulmonary disease .
Phototherapy .Fatigue
Introduction
Chronic obstructive pulmonary disease (COPD) is a pulmo-
nary pathological disorder that evolves with systemic mani-
festations including significant adverse effects on peripheral
muscle function and changes to the structure and metabolism
of the peripheral muscles, leading to decreased muscle
strength and endurance [1]. Factors that may be responsible
for premature muscle fatigue in this population include the
reduction of muscle strength, decrease in aerobic capacity,
dependence on glycolytic metabolism, and the fast buildup
of lactate during exercise [2]. Therefore, eletrophysical inter-
ventions such as phototherapy with lasers, light-emitting di-
odes (LEDs), or the combination of both are being studied to
minimize or delay muscle fatigue.
Several studies have used phototherapy as a non-invasive
therapeutic modality to increase muscle vasodilation [3], im-
prove collateral circulation, increase the level of oxygen in the
E. F. Miranda :P. C. de Carvalho :E. P. Leal-Junior
Post-Graduate Program in Biophotonics Applied to Health Sciences,
Nove de Julho University, Rua Vergueiro, 235, 01504-001
São Paulo, SP, Brazil
L. V. F. de Oliveira :F. C. Antonialli :A. A. Vanin :
P. C. de Carvalho :E. P. Leal-Junior (*)
Post-Graduate Program in Rehabilitation Sciences,
Nove de Julho University, São Paulo, Brazil
e-mail: ernesto.leal.junior@gmail.com
Lasers Med Sci
DOI 10.1007/s10103-014-1690-5
tissue, and increase adenosine triphosphate (ATP) in periph-
eral muscle mitochondria [4–7]. Many studies have used
phototherapy in the treatment of muscular disorders such as
fatigue in postmenopausal women during endurance training
[8]andforneckpain[9,10]. In addition, the ability of
phototherapy to reduce inflammatory processes and decrease
oxidative stress is also beneficial in muscular and sports-
related injuries [11,12]. The physiological changes caused
by phototherapy therefore have an important role in the pre-
vention and recovery of muscular fatigue.
In a previous study, Miranda et al. [13] were the first to study
the effect of phototherapy with LEDs in patients with COPD.
The authors found a decrease in the median frequency of
electromyographic outcome for evaluation of muscle fatigue
after isometric endurance testing and an increase in a muscular
endurance time test in ten patients with COPD after application
of LED phototherapy in the femoral quadriceps muscle.
As previous studies have shown beneficial effects by using
different wavelengths for enhancing muscle performance in
animal experiments [7,14,15], we hypothesized that a combi-
nation of super-pulsed lasers and LEDs could be a promising
alternative in preventing muscular fatigue induced by exercise in
patients with COPD. Furthermore, this is an innovative, non-
invasive, and non-pharmacological therapy. The purpose of this
study was to evaluate the acute effects of combined super-pulsed
laser and LED phototherapy on the isokinetic performance
(strength and muscular endurance) of patients with COPD.
Methods
Thirteen patients were consecutively recruited from the out-
patient chronic pulmonary diseases clinic at the Nove de Julho
University. All patients had a diagnosis of COPD according to
the global initiative for chronic obstructive lung disease
(GOLD) criteria [16]. The patients were at a stable phase of
the disease indicated by no change in the medical therapy
(including oral steroids) or exacerbation of symptoms in the
preceding 4 weeks. Patients with other known severe chronic
diseases, including cardiac, neuromuscular, or orthopedic dis-
orders, were excluded. The study was approved by the insti-
tutional ethics committee (process 632.222), and written in-
formed consent was obtained from all patients.
Randomization and blinding procedures
Randomization was performed by simple drawing of lots,
which was used to determine whether the active combination
of super-pulsed laser and LEDs phototherapy or placebo
would be given at the first session. Participants were crossed
over to receive whichever treatment was not given at the first
session. Randomization labels were created by using a ran-
domization table at a central office where a series of sealed,
opaque, and numbered envelopes were used to ensure
confidentiality. A participating researcher who had the func-
tion of programming the phototherapy device based on the
randomization results conducted randomization. This re-
searcher was instructed not to inform the participants or
other researchers regarding the phototherapy dose. Thus,
the researcher in charge of the administration of the pho-
totherapy was blinded to the dose applied to the volunteers.
Blinding was further maintained by the use of opaque
goggles by the participants.
Study design and protocol
A crossover, double-blinded, placebo-controlled, and ran-
domized clinical trial was carried out. The study was
conducted in the Laboratory of Phototherapy in Sport and
Exercise at the Nove de Julho University, São Paulo,
Brazil. Patients were administered either phototherapy or
placebo treatments on two visits, 1 week apart. Immediate-
ly after the application, the maximum voluntary isometric
contraction (MVIC) was determined and the endurance
test—total work (TW). A summary of the protocol is
presented in Fig. 1.
Procedures
Spirometry
Spirometry (Koko Spirometer, AL, USA) was performed as
per the American Thoracic Society/European Respiratory So-
ciety criteria [17]; FVC, FEV
1
,andFEV
1
/FVC are expressed as
absolute values and percent of predicted [18].
Fig. 1 CONSORT flow chart
Lasers Med Sci
Isokinetic protocol
An isokinetic dynamometer (System 4, Biodex®, USA)
was used for the evaluation of muscle function and the
execution of the exercise protocol. This is currently con-
sidered the method with the greatest reliability for the
measure of musculoskeletal performance. For the MVIC
test, the volunteers sat at an angle of 100° between the
trunk and hips with the non-dominant leg positioned with
the knee at 60° of flexion (0° corresponds to complete
knee extension) and were strapped to the dynamometer
seat. The dominant leg was positioned at 100° of hip
flexion and was strapped to the seat. The volunteers were
fastened to the seat of the dynamometer by using two
additional straps crossing the trunk. The volunteers were
instructed to cross their arms over their trunk, and the axis of
the dynamometer was positioned parallel to the center of the
knee.
The MVIC test consisted of three 5-s isometric con-
tractions of the knee extensors of the non-dominant leg.
The highest torque value of the three contractions (peak
torque [PT]) was used for the statistical analysis. This
parameter was chosen because it reflects the maximum
generation of force by the muscle. Instructions on how
to execute the test were given prior to testing, and the volun-
teers received verbal encouragement during the execution of
the test.
A resting period of 60 s was allowed, followed the
MVIC test after which volunteers performed a familiar-
ization isokinetic protocol. The familiarization consisted
of five submaximal voluntary repetitions of knee
flexion-extension in an eccentric contraction protocol,
followed by a resting period of 60 s. The eccentric
contraction protocol consisted of 20 eccentric, isokinetic
contractions of the knee extensor musculature in the
non-dominant leg (two sets of ten repetitions, 30 s rest
intervals between sets) at a velocity of 60° seg
−1
in
both the eccentric and concentric movements with a
60° range of motion (between 90° and 30° of knee
flexion). At each contraction, the dynamometer automat-
ically (passively) positioned the knee at 30°; the dyna-
mometer then flexed the knee until reaching 90°. The
volunteers were instructed to resist against knee flexion
movement imposed by the dynamometer with maximum
force. Despite the diversity of protocols proposed for
the execution of eccentric exercises on isokinetic dyna-
mometers, we used a modified protocol based on a
previous study carried out by our research group [19]
in which this method proved effective and reproducible
for the exercise-induced muscle damage. The researcher
in charge of the eccentric contractions protocol was
blinded to randomization and allocation of volunteers
to experimental groups.
Before and after the endurance test, the perceived effort
(dyspnea and leg fatigue) was assessed by using the modified
Borg scale [20].
Phototherapy
Patients received a single application of combined super-
pulsed laser and LED phototherapy or placebo 1 week
apart. The phototherapy combining super-pulsed laser
and LEDs or placebo was administered immediately be-
fore the testing of lower limb isokinetic dynamometry. A
12-diode cluster of super-pulsed laser and LEDs was
used. Each cluster consisted of four diodes of super-
pulsed laser (905 nm, 0.3125 mW average power and
12.5 W peak power for each diode), four diodes of
infrared LEDs (875 nm, 17.5 mW average power for
each diode), and four diodes of red LEDs (640 nm,
15 mW average power for each diode); they were
manufactured by Multi Radiance Medical™(Solon,
OH, USA). In view of the extensive area of radiation
employed in this project, the use of clusters becomes
fundamental to the application of the therapy. The appli-
cation of phototherapy was held with the cluster in direct
contact with the skin, at six sites of the quadriceps
femoris (two centrally, rectus femoris and vastus
intermedius; two laterally, vastus lateralis; and two me-
dially, vastus medialis). For placebo, the same proce-
dures were performed, but without irradiation. During
the application of combined super-pulsed laser and LEDs
phototherapy or placebo, the patient wore protective
goggles to prevent them from seeing whether or not there
was light being radiated.
Since the cluster has 12 diodes that were used to irradiate
six different locations of the extensor muscles of the knee (as
illustrated in Fig. 2), a total of 72 points in the musculature
were irradiated. Phototherapy parameters were chosen based
on a previous study performed by our research group [15].
Table 1provides a full description of the phototherapy
parameters.
Statistical analysis
The intention-to-treat analysis was followed. The Kol-
mogorov–Smirnovtestwasusedtoverifythenormal
distribution of data. Parametric data were expressed as
mean and standard deviation. Non-parametric data were
expressed as median and interquartile intervals. Differ-
ences in the variables of muscle function between com-
bined phototherapy and placebo treatments were com-
pared by using paired, two-sided Student’sttests, and
the differences of Borg scale were compared by using
the Wilcoxon test. The level of statistical significance was set
at p<0.05.
Lasers Med Sci
Results
Our volunteer population was formed mostly by patients with
moderate COPD according to the GOLD [16]criteria(GOLD
2, n=7), with the remaining patients classified as having mild
(GOLD 1, n=1), severe (GOLD 3, n=4), and very severe
(GOLD 4, n=1) COPD. Table 2summarizes the characteris-
tics of the patients.
A statistically significant difference was found for the
increase of PT after the application of combined super-
pulsed laser and LED phototherapy when compared with the
placebo (174.7 ±35.7 N· m vs. 155.8 ±23.3 N·m, respectively;
p=0.003). A similar finding was found for MVIC, with values
of 104.8±26.0 N·m vs. 87.2±24.0 N· m for the phototherapy
treatment and placebo, respectively (p= 0.000). Fig. 3a, b sum-
marizes the outcomes.
A greater value in the TW was observed during endurance
testing with the combination of super-pulsed laser and LED
phototherapy when compared to the placebo (778.0±221.1 J
vs. 696.3±146.8 J, respectively; p=0.005—Fig. 4).
The dyspnea score after the combination of super-pulsed laser
and LED phototherapy was lower in comparison with the place-
bo (1 [0–4] vs. 3 [0–6], p=0.003), and a similar result was seen in
the fatigue score for the lower limbs (2 [0–5] vs. 5 [0.5–9],
respectively; p=0.002). The findings are summarized in Fig. 5.
Discussion
To the best of our knowledge, this is the first study to analyze
the acute effects of the combination of super-pulsed laser and
LED phototherapy on isokinetic performance in patients with
Fig. 2 Illustration of irradiation areas of phototherapy
Tabl e 1 Phototherapy parameters
Number of lasers 4 super-pulsed infrared
Wavelength (nm) 905
Frequency (Hz) 250
Peak power (W)—each 12.5
Average optical output (mW)—each 0.03125
Power density (mW/cm
2
)—each 0.07
Dose (J)—each 0.07125
Spot size of laser (cm
2
)—each 0.44
Number of red LEDs 4 red
Wavelength of red LEDs (nm) 640
Frequency (Hz) 2
Average optical output (mW)—each 15
Power density (mW/cm
2
)—each 16.66
Dose (J)—each 3.42
Spot size of red LED (cm
2
)—each 0.9
Number of infrared LEDs 4 infrared
Wavelength of infrared LEDs (nm) 875
Frequency (Hz) 16
Average optical output (mW)—each 17.5
Power density (mW/cm
2
)—each 19.44
Dose (J)—each 3.99
Spot size of LED (cm
2
)—each 0.9
Magnetic field (mT) 35
Irradiation time per site (sec) 228
Total dose per si te (J ) 30
Total dose applied in muscular group (J) 180
Aperture of device (cm
2
)20
Tabl e 2 Vol u n tee r s ’characteristics
Va ri ab le s M ea n ± SD
Age, years 61±6
BMI, kg/m
2
24.3±4.1
FVC, L (% predicted) 2.5±0.7 (74±15)
FEV
1
, L (% predicted) 1.2±0.4 (53±16)
FEV
1
/FVC ratio, % 60.3±12.2
BMI body mass index, FVC forced vital capacity, FEV
1
forced expiratory
volume in 1 s in liters and in percentage of predicted, L (% predicted) in
liters and in percentage of predicted
Lasers Med Sci
COPD. Briefly, we found that combining lasers and LEDs
significantly increased the PT, TW, and MVIC, and decreased
dyspnea and lower limb fatigue in patients with COPD.
The beneficial use of phototherapy with a combination of
lasers and LEDs has been described recently in the literature.
Antonialli et al. [15] used phototherapy with a combination of
lasers and LEDs to test muscle performance and recovery after
exercise. The authors found an increased MVIC, decreased
biochemical levels of CK, and a decrease in the pain assess-
ment scale, when compared to placebo after an eccentric
protocol in an isokinetic dynamometer. In our study,
we did not evaluate biochemical markers and muscle
pain. However, we found a decreased sensation of dyspnea
and fatigue in the lower limbs assessed by using the Borg
scale, suggesting that the phototherapy with the combination
of lasers and LEDs was able to improve these parameters after
isokinetic exercise.
The combination of lasers and LEDs has also been used to
investigate the effects of phototherapy on non-specific knee
pain. The outcomes evaluated in this study were pain (evalu-
ated by using the visual analog scale) and quality of life
(measured by using the quality of life questionnaire SF-
36®). Phototherapy significantly decreased pain and im-
proved quality of life when compared with the placebo in
patients with knee pain [21]. In our study, the outcomes
evaluated were the variables obtained during an isokinetic
protocol and assessment of dyspnea and fatigue in the lower
limbs by using the Borg scale. We believe that a low score on
the Borg scale after application of phototherapy can be a good
indicator of improvement in the physical capacity of individ-
uals with COPD.
Miranda et al. [13] were the first to evaluate the
acute effect of phototherapy on quadriceps femoris mus-
cle function during isometric exercise in patients with
COPD. Phototherapy treatment was found to increase endur-
ance by 18 % and had a smaller decline on the median
Fig. 3 a,bComparison values of isokinetic protocol (PT and MVIC)
Fig. 4 Total work (TW) with combination of super-pulsed laser and
light-emitting diodes phototherapy compared to placebo
Fig. 5 Comparison of the Borg scale after phototherapy or placebo
Lasers Med Sci
frequency ofelectromyographic outcome for the evaluation of
muscle fatigue when contrasted with placebo. Corroborating
our previous findings, we observed a 20.2 % increase in
MVIC after application of phototherapy when compared with
placebo.
Similar to our study, Paolillo et al. [22]reportedan8.5%
increase in TWassessed by using an isokinetic dynamometer
in 20 postmenopausal women after application of photother-
apy when compared with the control group. We found a 12 %
increase in TW in our study that may be attributable to
differences in the study populations and the isokinetic proto-
col used by Paolillo et al. [22].
Although the present study is the first to use the combina-
tion of lasers and LEDs in patients with COPD, our findings
indicated that the magnitude of effect observed was higher
than that observed in other studies [13,15,21,22]. We believe
the best results were obtained owing to the combination of
different wavelengths (905, 875, and 640 nm) and different
sources of light (super-pulsed-laser and LEDs) used in our
study.
In animal studies, Albuquerque-Pontes et al. [7]radiated
the tibialis anterior muscle of rats with different wavelengths
(660, 830, and 905 nm). The authors found a significant
increase of cytochrome c oxidase. This finding contributes
to the understanding of how phototherapy can increase mus-
cular performance and protect against the development of
skeletal muscle fatigue and damage tissue [7].
The use of different wavelengths (660, 830, and 905 nm)
was investigated by Santos et al. [14] to evaluate the effects of
phototherapy immediately before tetanic contractions in the
development of skeletal muscle fatigue and possible tissue
damage in rats. The study showed that optimal doses of
phototherapy could slow the development of muscle fatigue
and protect against muscle tissue damage. The optimal doses
were, in part, dependent on specific wavelengths, and there-
fore must be differentiated to obtain the optimal effects for
tissue preservation and muscular fatigue.
The simultaneous use of different wavelengths may in-
crease the effects of phototherapy on skeletal muscle perfor-
mance and may represent a therapeutic advantage in clinical
situations, which was observed in the present study and in
previous studies [15,21]. One of the possible explanations for
the increase in isokinetic variables after applying the combi-
nation of lasers and LEDs is increased microcirculation
around the irradiated area. According to some authors
[23–26], increased local blood flow is able to reduce the
buildup of blood lactate and increase the supply of oxygen
to muscle tissues, thereby reducing muscle fatigue.
Based on these findings and previous studies, photo-
therapy with the combination of laser super-pulsed and
LEDs can be considered as a new and non-invasive
treatment to reduce fatigue and increase muscle strength in
patients with COPD.
Conclusion
In this study, we demonstrate that a combination of super-
pulsed laser and LED phototherapy on the femoral quadriceps
muscle in patients with COPD was able to increase PT by
20.2 % and TW by 12 %. Furthermore, combined photother-
apy prior to exercise still led to a decreased sensation of
dyspnea and lower limb fatigue in patients with COPD.
Funding Professor Ernesto CesarPinto Leal-Junior would like tothank
the São Paulo Research Foundation—FAPESP (grant number
2010/52404-0) and Brazilian Council of Science and Technology Devel-
opment—CNPq (grant number 472062/2013-1).
Conflict of interest Professor Ernesto Cesar Pinto Leal-Junior receives
a research support from Multi Radiance Medical (Solon, OH, USA), a
laser device manufacturer. The remaining authors declare that they have
no conflict of interest.
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