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ORIGINAL ARTICLE
When is the best moment to apply photobiomodulation therapy (PBMT)
when associated to a treadmill endurance-training program? A
randomized, triple-blinded, placebo-controlled clinical trial
Eduardo Foschini Miranda
1
&Shaiane Silva Tomazoni
2
&Paulo Roberto Vicente de Paiva
1,3
&Henrique Dantas Pinto
1,3
&
Denis Smith
3
&Larissa Aline Santos
3
&Paulo de Tarso Camillo de Carvalho
3
&Ernesto Cesar Pinto Leal-Junior
1,3
Received: 18 June 2017 / Accepted: 20 November 2017
#Springer-Verlag London Ltd., part of Springer Nature 2017
Abstract
Photobiomodulation therapy (PBMT) employing low-level laser therapy (LLLT) and/or light emittingdiode therapy (LEDT) has
emerged as an electrophysical intervention that could be associated with aerobic training to enhance beneficial effects of aerobic
exercise. However, the best moment to perform irradiation with PBMT in aerobic training has not been elucidated. The aim of this
study was to assess the effects of PBMT applied before and/or after each training session and to evaluate outcomes of the
endurance-training program associated with PBMT. Seventy-seven healthy volunteers completed the treadmill-training protocol
performed for 12 weeks, with 3 sessions per week. PBMT was performed before and/or after each training session (17 sites on
each lower limb, using a cluster of 12 diodes: 4 × 905 nm super-pulsed laser diodes, 4 × 875 nm infrared LEDs, and 4 × 640 nm
red LEDs, doseof 30 J per site). Volunteers were randomized in four groups according to the treatment they would receive before
and after each training session: PBMT before + PBMT after, PBMT before + placebo after, placebo before + PBMT after, and
placebo before + placebo after. Assessments were performed before the start of the protocol and after 4, 8, and 12 weeks of
training. Primary outcome was time until exhaustion; secondary outcome measures were oxygen uptake and body fat. PBMT
applied before and after aerobic exercise training sessions (PBMT before + PBMT after group) significantly increased (p<0.05)
the percentage of change oftime until exhaustion and oxygenuptake compared tothe group treated with placebo before and after
aerobic exercise training sessions (placebo before + placebo after group) at 4th, 8th, and 12th week. PBMT applied before and
after aerobic exercise training sessions (PBMT before + PBMTafter group) also significantly improved(p< 0.05) the percentage
of change of body fat compared to the group treated with placebo before and after aerobic exercise training sessions (placebo
before + placebo after group) at 8th and 12th week. PBMT applied before and after sessions of aerobic training during 12 weeks
can increase the time-to-exhaustion and oxygen uptake and also decrease the body fat in healthy volunteers when compared to
placebo irradiation before and after exercise sessions. Our outcomes showthat PBMTapplied beforeand after endurance-training
exercise sessions lead to improvement of endurance three times faster than exercise only.
Keywords Low-level laser therapy .Light emitting diode therapy .Phototherapy .Fatigue .Exercise .Aerobic training
Introduction
Physical activity is recommended and beneficial for both
asymptomatic persons and individuals with chronic diseases
[1,2]. Aerobic endurance is considered a useful tool for the
assessment of physical fitness and the detection of changes in
aerobic fitness resulting from systematic training [3].
Regular aerobic exercise has various beneficial metabolic,
vascular, and cardiorespiratory effects [4]. Additionally, it de-
creases body fat and increases muscle mass, muscle strength,
and bone density [5]. Moreover, it improves self-esteem and
*Ernesto Cesar Pinto Leal-Junior
ernesto.leal.junior@gmail.com
1
Laboratory of Phototherapy in Sports and Exercise, Nove de Julho
University, Sao Paulo, SP, Brazil
2
Masters and Doctoral Programs in Physical Therapy, Universidade
Cidade de São Paulo (UNICID), Sao Paulo, SP, Brazil
3
Post-Graduate Program in Rehabilitation Sciences, Nove de Julho
University, Rua Vergueiro, 235/249, Sao Paulo, SP 01504-001,
Brazil
Lasers in Medical Science
https://doi.org/10.1007/s10103-017-2396-2
physical and mental health and reduces the incidence of anx-
iety and depression [4,6].
Various ergogenic agents, such as whey protein [7], caffeine
[8], creatine [9], and neuromuscular electrical stimulation [10],
are currently used to increase the benefits of aerobic training.
Photobiomodulation therapy (PBMT) has emerged as an
electrophysical intervention that could be associated with aero-
bic training to enhance beneficial effects of aerobic exercise,
since several studies used PBMT to improve physical perfor-
mance when associated with different kinds of exercise [11–14].
Several studies have recently used PBMT to improve muscle
performance during aerobic activities in healthy adults [15–18]
and postmenopausal women [19,20]. However, to the best of
our knowledge, the best moment to perform irradiation with
PBMT in aerobic training has not been yet elucidated.
For instance, the current literature shows that the applica-
tion of PBMT before progressive aerobic exercise has ergo-
genic effects and acutely increases the time until exhaustion,
covered distance, and pulmonary ventilation and decreases the
score of dyspnea during progressive cardiopulmonary test
[15]. In addition, PBMTirradiation performed prior toaerobic
exercises improves the exercise performance by decreasing
the exercise-induced oxidative stress and muscle damage
[18] and increasing the oxygen extraction by peripheral mus-
cles [16]. When performed during aerobic training sessions,
PBMT improves the quadriceps power and reduces the pe-
ripheral fatigue in postmenopausal women [19,20].
Additionally, when applied after the sessions of endurance-
training program, PBMT leads to a greater fatigue reduction
than endurance training without PBMT irradiation [17].
Therefore, the optimal moment to perform PBMT in aero-
bic training is still open to discussion. With this perspective in
mind, we aimed to assess the effects of PBMT applied at
different time points (before and/or after) of each training ses-
sion and its potential effects on the outcomes of an endurance-
training program (aerobic exercise).
Materials and methods
Study design and protocol
We performed a triple-blind (assessors, therapists, and volun-
teers), placebo-controlled, randomized clinical trial. The study
was conducted in the Laboratory of Phototherapy in Sports
and Exercise.
Ethical aspects
All participants signed informed consent prior to enrollment
and the study was approved by the research ethics committee
of Nove de Julho University (process 553.831) and registered
at Clinical Trials.gov (NCT02874976).
Sample
The sample size was calculated assuminga type I error of 0.05
and a type II error of 0.2, based on previous study [21], and the
primary established outcome was the time until exhaustion.
Inclusion and exclusion criteria
We recruited 96 healthy volunteers (48 men and 48 women)
between 18 and 35 years of age and without training or in-
volvement in a regular exercise program (i.e., exercise more
than once per week) [22,23]. Volunteers were excluded if they
had any skeletal muscle injury, used any nutritional supple-
ment or pharmacologic agent, presented with signs or symp-
toms of any disease (i.e., neurologic, inflammatory, pulmo-
nary, metabolic, oncologic), or had a history of cardiac arrest
that might limit performance of high-intensity exercises.
Volunteers that were unable to attend a minimum rate of
80% of the training sessions and volunteers with immune
diseases that require continuous use of anti-inflammatory
drugs were also excluded.
Randomization and blinding procedures
Volunteers were distributed in four experimental groups (24
volunteers in each group) through a simple drawing of lots (A,
B, C, or D) that determined the moment they would receive
active and/or placebo PBMT treatment:
–PBMT + PBMT: volunteers were treated with active
PBMT before and after each training session.
–PBMT + placebo: volunteers were treated with active
PBMT before and placebo PBMT after each training
session.
–Placebo + PBMT: volunteers were treated with placebo
PBMT before and active PBMT after each training
session.
–Placebo + placebo: volunteers were treated with placebo
PBMT before and after each training session.
Randomization labels were created by using a randomiza-
tion table at a central office where a series of sealed, opaque,
and numbered envelopes ensured confidentiality. The re-
searcher who programmed the PBMT device (manufactured
by Multi Radiance Medical™, Solon, OH, USA) based on the
randomization results was not involved in any other procedure
of the study. He was instructed not to inform the participants
or other researchers of the PBMT program (active or placebo).
None of the researchers involved in aerobic endurance-
training assessments and data collection knew which program
corresponded to active or placebo PBMT.
Identical PBMT devices were used in both programs (ac-
tive or placebo) by a researcher who was not involved in any
Lasers Med Sci
phase of the projected data collection to ensure the study
blinding. All displays and sounds emitted were identical re-
gardless of the selected program. The active PBMT treatment
did not demonstrate discernable amounts of heat [24].
Therefore, volunteers were unable to differentiate between
active or placebo treatments. All volunteers were required to
wear opaque goggles during treatments to safety and to main-
tain the triple-blind design.
Procedures
The study included three sessions of aerobic endurance train-
ing per week performed over 12 weeks, and each session
lasted 30 min; the load for each exercise session (treadmill
speed) progressed constantly in order to keep subjects’heart
rate between 70 and 80% from maximum heart rate. The as-
sessments were conducted before the start of the training pro-
tocol and after 4, 8, and 12 weeks of training. A summary of
the study design is presented in Fig. 1.
Cardiopulmonary exercise test
Participants performed a standardized progressive cardiopul-
monary exercise test on a treadmill with a fixed inclination of
1% until exhaustion. They began the test with a 3-min warm-
up at a velocity of 3 km/h. Next, the treadmill velocity was
increased by 1 km/h at 1-min intervals until the velocity of
16 km/h was reached. Participants were instructed to use hand
signals to request termination of the test at any time. A 3-min
recovery phase at a velocity of 6 km/h was allowed after each
test [18]. During testing, we monitored the rates of oxygen
uptake (VO
2
), carbon dioxide production measured with a
VO 2000 gas analyzer (Inbrasport, Indústria Brasileira de
Equipamentos Médico-Desportivos LTDA, Porto Alegre,
RS, Brazil), total time until exhaustion, and heart rate mea-
suredwithadigitalelectrocardiograph (Medical Graphs
Ergomet, São Paulo, SP, Brazil).
These data were used to evaluate the performance of par-
ticipants during progressive cardiopulmonary exercise testing,
because this test is currently the most widely used in the liter-
ature for this purpose [25]. The entire test was monitored by
electrocardiogram and blood pressure measurement. If any
abnormal heart rate or blood pressure changes were observed
or if the test was terminated prematurely on request, the test
was stopped, and the volunteer’s data were deleted.
Body composition assessment
Body composition was assessed by the same technician
(blinded to volunteer’s allocation in different experimental
groups) using the procedures established by ISAK [26].
Measurements of height, body mass, and skinfolds were used
to establish the percentage of fat [26].
Aerobic training protocol
Aerobic treadmill training, associated or not with PBMT, was
performed three times a week for 12 weeks, each session
lasting 30 min, with training intensity kept between 70 and
80% of maximum heart rate [27]; changes in running speed
(training load) were constantly performed to achieve the 70–
80% heart rate.
Training was interrupted based on the criteria established
by the guidelines of the American Heart Association. Training
intensity was monitored by a heart rate monitor manufactured
by Polar®.
Fig. 1 CONSORT flowchart
Lasers Med Sci
Photobiomodulation therapy
PBMT was applied employing MR4 Laser Therapy Systems
outfitted with LaserShower 50 4D emitters (both
manufactured by Multi Radiance Medical, Solon, OH,
USA). The cluster style emitter contains 12 diodes composing
of four super-pulsed laser diodes (905 nm, 0.3125 mW aver-
age power, and 12.5 W peak power for each diode), four red
LED diodes (640 nm, 15 mW average power for each diode),
and four infrared LEDs diodes (875 nm, 17.5 mW average
power for each diode).
The cluster probe was selected due to the available cover-
age area and to reduce the number of sites needing treatment.
Treatment was applied in direct contact with the skin with a
slight applied overpressure to nine sites on extensor muscles
of the knee (Fig. 2a), six sites on kneeflexors of the knee, and
two sites on the calf (Fig. 2b) of both lower limbs [15,28]. To
ensure blinding, the device emitted the same sounds and re-
gardless of the programmed mode (active or placebo). The
researcher, who was blinded to randomization and the pro-
gramming of PBMT device, performed the PBMT.
PBMT parameters and irradiation sites were selected based
upon previous positive outcomes demonstrated with the same
family of device [13,15,28,29]. Table 1provides a full
description of the PBMT parameters. The volunteers received
PBMTor placebo from 5 to 10 min before and/or after aerobic
training sessions.
Statistical analysis
The obtained results were tested for their normality through
the Shapiro-Wilk test. Since the data showed a normal
distribution, two-way ANOVA test with Bonferroni post hoc
analysis was applied. The data were described as mean values
with the respective standard deviations and both absolute and
percentage values were analyzed. Graphical data are described
as mean and standard errors of mean (SEM). The level of
statistical significance was p<0.05.
Results
After data collection, we analyzed the results of 77 volunteers
of both genders (PBMT + PBMT: 18 volunteers; PBMT +
placebo: 21 volunteers; placebo + PBMT: 18 volunteers; and
placebo + placebo: 20 volunteers) that had completed the aer-
obic training protocol after 12 weeks (Fig. 1). None of the
recruited volunteers were excluded due abnormal heart rate or
Fig. 2 aTreatment sites at knee extensor muscles. bTreatment sites at
knee flexor and ankle plantar flexor muscles
Table 1 PBMT parameters
Number of lasers 4 Super-pulsed infrared
Wavelength (nm) 905 (± 1)
Frequency (Hz) 250
Peak power (W)—each 12.5
Average mean optical output (mW)—each 0.3125
Power density (mW/cm
2
)—each 0.71
Energy density (J/cm
2
)—each 0.162
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 (± 10)
Frequency (Hz) 2
Average optical output (mW)—each 15
Power density (mW/cm
2
)—each 16.66
Energy density (J/cm
2
)—each 3.8
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 (± 10)
Frequency (Hz) 16
Average optical output (mW)—each 17.5
Power density (mW/cm
2
)—each 19.44
Energy density (J/cm
2
)—each 4.43
Dose (J)—each 3.99
Spot size of LED (cm
2
)—each 0.9
Magnetic field (mT) 35
Irradiation time per site (s) 228
Total dose per site (J) 30
Total dose applied per lower limb (J) 510
Aperture of device (cm
2
)20
Application mode Cluster probe held stationary
in skin contact with a 90°
angle and slight pressure
Lasers Med Sci
blood pressure during the execution of procedures of this study.
The characteristics of the volunteers are summarized in Table 2.
As shown in Table 2, no statistically significant differences
(p> 0.05) were found for anthropometric variables and base-
line data among the different experimental study groups.
Table 3shows all results of cardiopulmonary progressive
test in absolute values for different variables analyzed in all
experimental groups of this study. We observed a statistically
significant improvement in oxygen uptake when PBMT was
performed before and after training sessions (PBMT + PBMT
group), comparing baseline values vs 4-, 8-, and 12-week
values (p< 0.001). The same was observed for pulmonary
ventilation, comparing baseline values vs 8- and 12-week
values (p=0.0018and p= 0.003, respectively), and for time
until exhaustion, comparing baseline values vs 4-, 8-, and 12-
week values (p<0.001).
Furthermore, PBMT applied before and after each aerobic
exercise training session (PBMT + PBMT group) significant-
ly increased (p< 0.05) the percentage change of oxygen con-
sumption and time-to-exhaustion compared to the group treat-
ed with placebo before and after each aerobic exercise training
session (placebo + placebo group) from 4th to 12th week.
Similarly, PBMT applied before and after each aerobic exer-
cise training session (PBMT + PBMT group) significantly
improved (p< 0.05) the percentage change of body fat com-
pared to group treated with placebo before and after each
aerobic exercise training session (placebo + placebo group).
The outcomes are summarized in Figs. 3,4,and5,
respectively.
Discussion
To the best of our knowledge, this is the first study aiming to
test the optimal moment to perform PBMT in an aerobic train-
ing protocol (before, after, or before and after training). Few
studies have assessed chronic effects of PBMT [17,20,21];
however, PBMT has been applied at different moments (be-
fore, after, or during exercise) of the aerobic training program.
Briefly, we observed that the combination of super-pulsed
lasers and LEDs applied before and after exercise sessions
increased the oxygen uptake, time-to-exhaustion, and reduced
body fat in healthy sedentary volunteers after 12 weeks of
aerobic training.
Paolillo et al. [20] investigated the effects of PBMT applied
during the sessions of aerobic training on the treadmill in 20
postmenopausal women. The training was performed twice a
week for 3 months, with an intensity of 85–90% of maximum
heart rate. The volunteers received LEDtherapy with 850 nm,
31 mW/cm
2
, 30 min irradiation, and 14,400 J applied bilater-
ally to the tight regions. PBMT increased the exercise toler-
ance time when compared to the control group. These data
corroborate with the results of our study, however, we used
different light sources and wavelengths simultaneously (4×
905 nm super-pulsed lasers, 4 × 875 nm infrared LEDs, and
4 × 640 nm red LEDs) to irradiate the volunteersand we found
an increase in exercise tolerance of 13.4%. The magnitude of
the difference in outcomes between studies might be related to
the used irradiation protocol (in our study, the volunteers were
irradiated before and after the aerobic training sessions, while
Paolillo et al. [20] irradiated volunteers during the training
sessions).
The same authors [21] also investigated the effects of
PBMT (infrared LEDs—850 nm) when applied during tread-
mill training in 45 postmenopausal women. The training was
performed twice a week for 6 months, and each training ses-
sion lasted 45 min. The authors found a significant increase in
exercise tolerance, and metabolic equivalents, and a longer
duration of Bruce test. In our study, the association of
PBMT before and after sessions of the aerobic training pro-
gram was able to increase the oxygen consumption (with
18.7%) and time-to-exhaustion (with 13.4%) and improve
the percentage of change of body fat (with 13.9%) after only
12 weeks of aerobic training.
Table 2 Baseline assessment data in absolute values
PBMT + PBMT PBMT + placebo Placebo + PBMT Placebo + placebo
Age (years) 24.7 ± 4.7 26.1 ± 5.2 26 ± 5.3 25.1 ± 4.6
Body mass index
a
26.0 ± 3.6 25.3 ± 2.8 24.9 ± 2.7 25.2 ± 1.9
Heart rate (beats per minute) 94.2± 15.0 87.8 ± 13.5 89.9 ± 11.9 95.1 ± 14.7
Systolic blood pressure (mmHg) 117.1 ± 12.1 118.4 ± 13.8 118.0 ± 10.1 111.2 ± 13.5
Diastolic blood pressure (mmHg) 84.7 ± 10.1 84.2 ± 8.4 84.7 ± 6.4 81.2 ± 10.1
Time until exhaustion (s) 681.5 ± 111.9 698.7 ± 131.3 693.1 ± 106.9 699.5 ± 137.3
VO
2
max (mL/kg/min) 35.8 ± 9.5 34.8 ± 6.9 35.2 ± 8.9 36.2 ± 7.7
Fat percentage 31.8 ± 10.4 29.5 ± 14.4 28.9 ± 11.1 30.1 ± 13.7
Data is expressed in average and standard deviation (±)
VO
2
max oxygen uptake
a
Calculated as kilograms per square meter
Lasers Med Sci
Duarte et al. [30] evaluated the effects of PBMT (808 nm)
associated with aerobic and resistance training performed
three times a week for 16 weeks in obese women. The authors
found a significant decrease in the percentage of fat and in
neck and waist circumference. It is important to highlight that
in our study, we observed statistically significant improve-
ment in the percentage of change of body fat (13.9%) after
only 12 weeks of aerobic training when associated with
PBMT before and after the training sessions. We believe that
the association of PBMT before and after training was able to
enhance the performance and the tolerance of the volunteers
during the aerobic training protocol, favoring the reduction of
the body fat at the end of the 12 weeks of training.
It is interesting how outcomes in the fourth week for PBMT
+ PBMT group were similar to those of placebo + placebo
group (or exercise alone) in the 12th week. This means that
PBMT with optimal irradiation protocol (before and after ex-
ercise training sessions) can increase the endurance capacity
of volunteers three times faster than exercise alone.
Regarding the mechanisms of the observed effects, we
strongly believe that mitochondrial activity modulation is the
key mechanism, despite the fact that our study only focused
on clinical and functional aspects and not on mechanisms.
Hayworth et al. [31] demonstrated that the activity of cyto-
chrome c oxidase is enhanced by PBMT with a single wave-
length in skeletal muscle fibers of rats. More recently,
Albuquerque-Pontes et al. [32] showed that PBMT with dif-
ferent wavelengths (660, 830, or 905 nm) was able to increase
the expression of cytochrome c oxidase in the intact skeletal
Table 3 Progressive endurance test variables
Baseline 4 weeks 8 weeks 12 weeks
VO
2
(mL/kg/min) PBMT + PBMT 35.8 ± 9.5 40.2 ± 10.2* 41.5 ± 10.4* 42.5 ± 11.2*
PBMT + Placebo 34.8 ± 7.0 37.6 ± 7.0 38.6 ± 8.0 38.2 ± 7.0
Placebo + PBMT 35.2 ± 8.9 36.6 ± 8.1 38.6 ± 8.3 38.5 ± 8.3
Placebo + placebo 36.2 ± 7.7 36.8 ± 8.0 37.6 ± 7.5 38.4 ± 10.1
VCO
2
(mL/kg/min) PBMT + PBMT 38.7 ± 7.0 40.4 ± 8.6 41.3 ± 7.8 41.4 ± 8.7
PBMT + placebo 38.,5 ± 7.8 39.5 ± 6.6 41.7 ± 7.9 41.9 ± 6.8
Placebo + PBMT 38.5 ± 9.5 38.2 ± 9.5 41.5 ± 8.4 40.7 ± 9.6
Placebo + placebo 38.8 ± 10.6 40.7 ± 9.4 43.1 ± 13.4 40.9 ± 10.5
VE (mL/kg/min) PBMT + PBMT 73.6 ± 22.8 77.9 ± 21.5 83.5 ± 24.5* 85.3 ± 22.5*
PBMT + Placebo 70.6 ± 20.3 71.0 ± 23.1 78.1 ± 23.0 77.2 ± 22.1
Placebo + PBMT 66.2 ± 25.3 70.6 ± 24.2 73.9 ± 20.6 73.4 ± 20.7
Placebo + placebo 69.9 ± 17.9 70.8 ± 18.8 70.3 ± 22.4 77.1 ± 18.3
Time until exhaustion (s) PBMT + PBMT 681.5 ± 111.9 752.1 ± 111.7* 787.7 ± 114.2* 808.5 ± 124.5*
PBMT + placebo 698.7 ± 131.1 739.3 ± 142.2 773.4 ± 165.9 792.1 ± 186.9
Placebo + PBMT 693.1 ± 106.9 738.4 ± 116.6 766.1 ± 121.0 797.0 ± 139.0
Placebo + placebo 699.5 ± 137.3 720.2 ± 150.0 741.3 ± 154.3* 766.1 ± 159.8*
Data is expressed in average and standard deviation (±)
VO
2
oxygen uptake, VCO
2
carbon dioxide production, VE pulmonary ventilation
*Statistically significant difference compared to baseline (p<0.05)
Fig. 4 Percentage of change in maximum oxygen uptake. The data are
presented in mean and SEM. Letter a indicates statistical significance
between PBMT + PBMT and placebo + placebo (p<0.05)
Fig. 3 Percentage of change in time-to-exhaustion. The data are
presented in mean and SEM. Letter a indicates statistical significance
between PBMT + PBMT and placebo + placebo (p<0.05)
Lasers Med Sci
muscle tissue in different time windows (5 min to 24 h after
irradiation), which means that the muscle metabolism can be
improved through the action of PBMT. These findings help us
to explain the increase in performance observed by the use of
PBMT associated with an aerobic training protocol and pro-
vide the rationale for the concurrent use of different wave-
lengths at the same time, which can represent a therapeutic
advantage in various clinical situations.
In fact, different studies have shown that the concurrent use
of different light sources and wavelengths enhances muscular
performance [13–15,28,29,33] decreases pain [34], in-
creases cytochrome c oxidase activity [32], decreases fatigue
development [35], and protects muscles against gradually
worsening damage [35].
In a previous study from our research group with a similar
purpose [36], it was observed that the best moment to perform
PBMT associated to strength training is before each exercise
session. As mentioned before, the current study showed that the
optimal moment to perform PBMT is before and after each
treadmill endurance-training exercise session. It clearly demon-
strates that not only doses [13,37] and power output [42], but
also the moment to apply PBMT should be optimized, since
different types of exercises [38] may need different optimal
moments to perform PBMT for achieving the best outcome.
We believe that our study results are interesting because
they show thatPBMT can chronically enhance aerobic perfor-
mance (endurance) and demonstrate that optimal moment to
perform PBMT associated with aerobic treadmill exercise is
before and after each exercise session. These outcomes can be
helpful to improve the scientific evidence [39–41] in this
promising and growing area.
Conclusion
PBMT (with simultaneous combination of super-pulsed la-
sers, infrared, and red LEDs) applied before and after sessions
of aerobic training during 12 weeks can increase oxygen up-
take and time-to-exhaustion and decrease body fat in healthy
volunteers when compared to placebo irradiation before and
after exercise sessions.
Funding information This study was supported by research grants 2010/
52404-0 from São Paulo Research Foundation—FAPESP (Professor
Ernesto Cesar Pinto Leal-Junior), 472062/2013-1 and 307717/2014-3
from Brazilian Council of Science and Technology Development—
CNPq (Professor Ernesto Cesar Pinto Leal-Junior), and 2014/01279-1
from São Paulo Research Foundation—FAPESP for Ph.D. scholarship
(Larissa Aline Santos).
Compliance with ethical standards
Competing interests Professor Ernesto Cesar Pinto Leal-Junior re-
ceived research support from Multi Radiance Medical (Solon, OH,
USA), a laser device manufacturer. The remaining authors declare that
they have no conflict of interest.
Ethical aspects All experimental procedures were submitted and ap-
proved by the Research Ethics Committee of Nove de Julho University
(process number 553.831) and registered at Clinical Trials.gov
(NCT02874976).
References
1. Warburton DE, Nicol CW, Bredin SS (2006) Health benefits of
physical activity: the evidence. CMAJ 174:801–809
2. Warburton DE, Katzmarzyk PT, Rhodes RE, Shephard RJ (2007)
Evidence-informed physical activity guidelines for Canadian
adults. Can J Public Health 98:S16–S68
3. Goodman JM, Thomas SG, Burr J (2011) Evidence-based risk as-
sessment and recommendations for exercise testing and physical
activity clearance in apparently healthy individuals. Appl Physiol
Nutr Metab 36:S14–S32
4. Chou CH, Hwang CL, Wu YT (2012) Effect of exercise on physical
function, daily living activities, and quality of life in the frail older
adults: a meta-analysis. Arch Phys Med Rehabil 93:237–244
5. Jacobson BH, Smith D, Fronterhouse J, Kline C, Boolani A (2012)
Assessment of the benefit of powered exercises for muscular en-
durance and functional capacity in elderly participants. J Phys Act
Health 9:1030–1035
6. de Vries NM, van Ravensberg CD, Hobbelen JS, Olde Rikkert MG,
Staal JB, Nijhuis-van der Sanden MW (2012) Effects of physical
exercise therapy on mobility, physical functioning, physical activity
and quality of life in community-dwelling older adults with im-
paired mobility, physical disability and/or multi-morbidity: a me-
ta-analysis. Ageing Res Rev 11:136–149
7. MacKenzie-Shalders KL, Byrne NM, Slater GJ, King NA (2015)
The effect of a whey protein supplement dose on satiety and food
intake in resistance training athletes. Appetite 92:178–184
8. Higgins S, Straight CR, Lewis RD (2016) The effects of preexercise
caffeinated coffee ingestion on endurance performance: an
evidence-based review. Int J Sport Nutr Exerc Metab 26:221–239
9. Lanhers C, Pereira B, Naughton G, Trousselard M, Lesage FX,
Dutheil F (2015) Creatine supplementation and lower limb strength
performance: a systematic review and meta-analyses. Sports Med
45:1285–1294
10. De Brandt J, Spruit MA, Derave W, Hansen D, Vanfleteren LE,
Burtin C (2016) Changes in structural and metabolic muscle char-
acteristics following exercise-based interventions in patients with
COPD: a systematic review. Expert Rev Respir Med 10:521–545
Fig. 5 Percentage of change in body fat. The data are presented in mean
and SEM. Letter a indicates statistical significance between PBMT +
PBMT and placebo + placebo (p<0.05)
Lasers Med Sci
11. Leal Junior EC, Lopes-Martins RA, Vanin AA, Baroni BM,
Grosselli D, De Marchi T, Iversen VV, Bjordal JM (2009) Effect
of 830 nm low-level laser therapy in exercise-induced skeletal mus-
cle fatigue in humans. Lasers Med Sci 24:425–431
12. Leal Junior EC, Lopes-Martins RA, Baroni BM, De Marchi
T, Taufer D, Manfro DS, Rech M, Danna V, Grosselli D,
Generosi RA, Marcos RL, Ramos L, Bjordal JM (2009)
Effect of 830 nm low-level laser therapy applied before
high-intensity exercises on skeletal muscle recovery in ath-
letes. Lasers Med Sci 24:857–863
13. Antonialli FC, De Marchi T, Tomazoni SS, Vanin AA, dos Santos
GV, de Paiva PR, Pinto HD, Miranda EF, de Tarso Camillo de
Carvalho P, Leal-Junior EC (2014) Phototherapy in skeletal muscle
performance and recovery after exercise: effect of combination of
super-pulsed laser and light-emitting diodes. Lasers Med Sci 29:
1967–1976
14. Miranda EF, deOliveira LV, Antonialli FC, Vanin AA, de Carvalho
PT, Leal-Junior EC (2015) Phototherapy with combination of
super-pulsed laser and light-emitting diodes is beneficial in im-
provement of muscular performance (strength and muscular endur-
ance), dyspnea, and fatigue sensation in patients with chronic ob-
structive pulmonary disease. Lasers Med Sci 30:437–443
15. Miranda EF, Vanin AA, Tomazoni SS, Grandinetti Vdos S, de Paiva
PR, Machado Cdos S, Monteiro KK, Casalechi HL, de Tarso P, de
Carvalho C, Leal-Junior EC (2016) Using pre-exercise
photobiomodulation therapy combining super-pulsed lasers and
light-emitting diodes to improve performance in progressive cardio-
pulmonary exercise tests. J Athl Train 51:129–135
16. Da Silva Alves MA, Pinfildi CE, Neto LN, Lourenço RP, de
Azevedo PH, Dourado VZ (2014) Acute effects of low-level laser
therapy on physiologic and electromyographic responses to the
cardiopulmonary exercise testing in healthy untrained adults.
Lasers Med Sci 29:1945–1951
17. Vieira WH, Ferraresi C, Perez SE, Baldissera V, Parizotto NA
(2012) Effects of low-level laser therapy (808 nm) on
isokinetic muscle performance of young women submitted to
endurance training: a randomized controlled clinical trial.
Lasers Med Sci 27:497–504
18. De Marchi T, Leal Junior EC, Bortoli C, Tomazoni SS, Lopes-
Martins RA, Salvador M (2012) Low-level laser therapy (LLLT)
in human progressive-intensity running: effects on exercise perfor-
mance, skeletal muscle status, and oxidative stress. Lasers Med Sci
27:231–236
19. Paolillo FR, Corazza AV, Paolillo AR, Borghi-Silva A, Arena R,
Kurachi C, Bagnato VS (2014) Phototherapy during treadmill train-
ing improves quadriceps performance in postmenopausal women.
Climacteric 17:285–293
20. Paolillo FR, Milan JC, Aniceto IV, Barreto SG, Rebelatto JR,
Borghi-Silva A, Parizotto NA, Kurachi C, Bagnato VS (2011)
Effects of infrared-LED illumination applied during high-intensity
treadmill training in postmenopausal women. Photomed Laser Surg
29:639–645
21. Paolillo FR, Corazza AV, Borghi-Silva A, Parizotto NA, Kurachi C,
Bagnato VS (2013) Infrared LED irradiation applied during high-
intensity treadmill training improves maximal exercise tolerance in
postmenopausal women: a 6-month longitudinal study. Lasers Med
Sci 28:415–422
22. American College of Sports Medicine, Chodzko-Zajko WJ, Proctor
DN, Fiatarone Singh MA, Minson CT, Nigg CR, Salem GJ,
Skinner JS (2009) American College of Sports Medicine position
stand. Exercise and physical activity for older adults. Med Sci
Sports Exerc 41:1510–1530
23. Song M, Carroll DD, Fulton JE (2013) Meeting the 2008 physical
activity guidelines for Americans among U.S. youth. Am J Prev
Med 44:216–222
24. Grandinétti Vdos S, Miranda EF, Johnson DS, de Paiva PR,
Tomazoni SS, Vanin AA, Albuquerque-Pontes GM, Frigo L,
Marcos RL, de Carvalho PT, Leal-Junior EC (2015) The thermal
impact of phototherapy with concurrent super-pulsed lasers and red
and infrared LEDs on human skin. Lasers Med Sci 30:1575–1581
25. Powers SK, Howley ET (2015) Exercise physiology: theory and
application to fitness and performance, 9th edn. McGraw-Hill,
New York
26. Marfell-Jones M, Olds T, Stewart A, Carter L (2006) International
standards for anthropometric assessment. ISAK, Potchefstroom
27. Borghi-Silva A, Arena R, Castello V, Simões RP, Martins LE,
Catai AM, Costa D (2009) Aerobic exercise training improves
autonomic nervous control in patients with COPD. Respir Med
103:1503–1510
28. Pinto HD, Vanin AA, Miranda EF, Tomazoni SS, Johnson DS,
Albuquerque-Pontes GM, Aleixo IO Jr, Grandinetti VD,
Casalechi HL, de Carvalho PT, Leal-Junior EC (2016)
Photobiomodulationtherapy improves performance and accelerates
recovery of high-level rugby players in field test: a randomized,
crossover, double-blind, placebo-controlled clinical study. J
Strength Cond Res 30:3329–3338
29. de Paiva PR, Tomazoni SS, Johnson DS, Vanin AA, Albuquerque-
Pontes GM, Machado CD, Casalechi HL, de Carvalho PT, Leal-
Junior EC (2016) Photobiomodulation therapy (PBMT) and/or
cryotherapy in skeletal muscle restitution, what is better? A ran-
domized, double-blinded, placebo-controlled clinical trial. Lasers
Med Sci 31:1925–1933
30. Duarte FO, Sene-Fiorese M, de Aquino Junior AE, da Silveira
Campos RM, Masquio DC, Tock L, Garcia de Oliveira Duarte
AC, Dâmaso AR, Bagnato VS, Parizotto NA (2015) Can low-
level laser therapy (LLLT) associated with an aerobic plus resis-
tance training change the cardiometabolic risk in obese women? A
placebo-controlled clinical trial. J Photochem Photobiol B 153:
103–110
31. Hayworth CR, Rojas JC, Padilla E, Holmes GM, Sheridan EC,
Gonzalez-Lima F (2010) In vivo low-level light therapy increases
cytochrome oxidase in skeletal muscle. Photochem Photobiol 86:
673–680
32. Albuquerque-Pontes GM, Vieira RP, Tomazoni SS, Caires CO,
Nemeth V, Vanin AA, Santos LA, Pinto HD, Marcos RL, Bjordal
JM, de Carvalho PT, Leal-JuniorEC (2015) Effect of pre-irradiation
with different doses, wavelengths, and application intervals of low-
level laser therapy on cytochrome c oxidase activity in intact skel-
etal muscle of rats. Lasers Med Sci 30:59–66
33. De Marchi T, Schmitt VM, Danúbia da Silva Fabro C, da Silva LL,
Sene J, Tairova O, Salvador M (2017) Phototherapy for improve-
ment of performance and exercise recovery: comparison of 3 com-
mercially available devices. J Athl Train 52:429–438
34. Leal-Junior EC, Johnson DS, Saltmarche A, Demchak T (2014)
Adjunctive use of combination of super-pulsed laser and light-
emitting diodes phototherapy on nonspecific knee pain: double-
blinded randomized placebo-controlled trial. Lasers Med Sci 29:
1839–1847
35. Santos LA, Marcos RL, Tomazoni SS, Vanin AA, Antonialli FC,
Grandinetti Vdos S, Albuquerque-Pontes GM,de Paiva PR, Lopes-
Martins RÁ, de Carvalho PT, Bjordal JM, Leal-Junior EC (2014)
Effects of pre-irradiation of low-level laser therapy with different
doses and wavelengths in skeletal muscle performance, fatigue, and
skeletal muscle damage induced by tetanic contractions in rats.
Lasers Med Sci 29:1617–1626
36. Vanin AA, Miranda EF, Machado CS, de Paiva PR, Albuquerque-
Pontes GM, Casalechi HL, de Tarso Camillo de Carvalho P, Leal-
Junior EC (2016) What is the best moment to apply phototherapy
when associated to a strength training program? A randomized,
double-blinded, placebo-controlled trial: phototherapy in associa-
tion to strength training. Lasers Med Sci 31:1555–1564
Lasers Med Sci
37. Aver Vanin A, De Marchi T, Tomazoni SS, Tairova O, Leão
Casalechi H, de Tarso Camillo de Carvalho P, Bjordal JM,
Leal-Junior EC (2016) Pre-exercise infrared low-level laser
therapy (810 nm) in skeletal muscle performance and postexer-
cise recovery in humans, what is the optimal dose? A random-
ized, double-blind, placebo-controlled clinical trial. Photomed
Laser Surg 34:473–482
38. Machado AF, Micheletti JK, Vanderlei FM, Nakamura FY, Leal-
Junior ECP, Netto Junior J, Pastre CM (2017) Effect of low-level
laser therapy (LLLT) and light-emitting diodes (LEDT) applied
during combined training on performance and post-exercise recov-
ery: protocol for a randomized placebo-controlled trial.Braz J Phys
Ther 21:296–304
39. Leal-Junior EC, Vanin AA, Miranda EF, de Carvalho PT, Dal Corso
S, Bjordal JM (2015) Effect of phototherapy (low-level laser ther-
apy and light-emitting diode therapy) on exercise performance and
markers of exercise recovery: a systematic review with meta-anal-
ysis. Lasers Med Sci 30:925–939
40. Leal-Junior EC (2015) Photobiomodulation therapy in skeletal
muscle: from exercise performance to muscular dystrophies.
Photomed Laser Surg 33:53–54
41. Vanin AA, Verhagen E, Barboza SD, Costa LOP, Leal-Junior ECP
(2017) Photobiomodulation therapy for the improvement of mus-
cular performance and reduction of muscular fatigue associated
with exercise in healthypeople: a systematic review and meta-anal-
ysis. Lasers Med Sci. https://doi.org/10.1007/s10103-017-2368-6
42. de Oliveira AR, Vanin AA, Tomazoni SS, Miranda EF,
Albuquerque-Pontes GM, De Marchi T, Dos Santos Grandinetti
V, de Paiva PRV, Imperatori TBG, de Carvalho PTC, Bjordal JM,
Leal-Junior ECP (2017) Pre-exercise infrared photobiomodulation
therapy (810 nm) in skeletal muscle performance and postexercise
recovery in humans: what is the optimal power output? Photomed
Laser Surg 35:595–603
Lasers Med Sci
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