Lasers in Surgery and Medicine 42:584–588 (2010)

Single Session to Infrared Low Level Diode Laser on TNF-a

and IL-6 Cytokines Release by Mononuclear Spleen Cells in
Mice: A Pilot Study
Thiago Y. Fukuda, PhD student,1* Maury M. Tanji, PhD,2 Julio F. Jesus, MSc student,3 Maria N. Sato, PhD,4
Alberto J.S. Duarte, PhD,5 and Hélio Plapler, PhD6
1
Experimental Surgery, Federal University of São Paulo (UNIFESP), São Paulo, SP 04023-062, Brazil
2
Laboratory of Medical Investigation in Dermatology and Immunodeficiencies, LIM-56, FMUSP, São Paulo, SP, Brazil;
Universidade do Grande ABC, SP, Brazil
3
Experimental Surgery, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil
4
Laboratory of Medical Investigation in Dermatology and Immunodeficiencies, LIM-56, FMUSP, São Paulo, SP, Brazil
5
Laboratory of Medical Investigation in Dermatology and Immunodeficiencies, LIM-56, FMUSP, São Paulo, SP, Brazil
6
Experimental Surgery, Federal University of São Paulo (UNIFESP), São Paulo, SP, Brazil

Background and Objective: The results of low-level
infrared laser (LLL) systemic action on inflamma-
tory modulation process, specifically diminishing pro-
inflammatory and producing anti-inflammatory cytokines
are extremely controversial in the literature. More studies
are necessary to clarify the biomodulation process. The
main objective was to investigate the effect of a single
session of an AsGaAl laser on spleen cells interleukin-6
(IL-6) and tumor necrosis factor - alpha (TNF-a) release, in
vivo, in mice.
Study Design/Materials and Methods: In a pilot study,
18 isogenic mice were distributed in three groups: control
(no surgical procedure, n ¼ 6), sham (surgical procedure
with three standard cutaneous incisions, followed by
abdominal muscle incision followed by suture, n ¼ 6) and
LLL (same procedure followed by a single LLL exposure
12 hours after the procedure, n ¼ 6). The animals in the LLL
group received a single infrared continuous laser session
(780 nm wavelength, power of 20 mW, energy density of
10 J/cm2) on three points (20 seconds per point), and final
energy of 0.4 J. All animals of the sham and LLL groups
were sacrificed 36 hours after surgical procedure; the
spleen mononuclear cells were isolated and cultivated for
48 hours. The IL-6 and TNF-a were measured by the ELISA
method.
Results: IL-6 and TNF-a concentrations released by the
mononuclear cells showed significant differences between
the control and sham group (P<0.07). However, there were
no differences between the control and LLL group and
between the sham and LLL groups (P > 0.07).
Conclusion: The single session of infrared LLL showed
a tendency of decreasing the IL-6 and TNF-a release
by mononuclear spleen cells in mice after application,
although there was not a significant difference between the
sham and LLL group. Conclusions regarding effectiveness
of a single session procedure cannot be made due to the low
statistical power of this pilot study. Lasers Surg. Med.
42:584–588, 2010. ß 2010 Wiley-Liss, Inc.
Key words: cytokines; inflammation; low-level laser
therapy
INTRODUCTION
The low level laser (LLL) has been widely used in several
clinical situations due to its therapeutic effects without
heat production risks and damage to the irradiated
tissue. The LLL promotes cell changes by biostimulation,
accelerating tissue repair and decreasing inflammatory
processes [1–5].
The LLL cell effects may be classified as primary (photon
absorption induced by tissue cells); secondary (which
depends of the phototherapy and also on the cell reactions
that occurred before); and tertiary (which are influenced by
the internal and external environment, as well as cell
interactions). These tertiary effects are known as systemic
effects [6,7]. However, there is a lack of evidence in the
literature regarding this systemic effect.
One session of LLL has proven to be effective in some
biological phenomena, but there are few studies showing
these immediate effects on the modulation of inflammatory
processes [8–11]. As the inflammatory process reacts as a
local defense against agents such as an irritation after a
certain traumatic process, the body produces few proteins
which allow communication among cells and other organs,
including cytokines [12].
No competing financial interests exist.
Contract grant sponsor: Fundação de Amparo à Pesquisa do
Estado de São Paulo (FAPESP), Brazil; Contract grant number:
2007/04479-8.
Current address: Cirurgia experimental, UNIFESP, Rua
Botucatu, 740, Vila Clementino, São Paulo, SP 04023-062, Brazil.
*Correspondence to: Thiago Y. Fukuda, PhD student, Physical
Therapy Sector, Santa Casa de São Paulo, Rua Dr. Cesário Motta
Jr., 112, CEP: 01221-020, São Paulo, SP, Brazil.
E-mail: tfukuda10@yahoo.com.br
Accepted 4 June 2010
Published online 15 July 2010 in Wiley InterScience
(www.interscience.wiley.com).
DOI 10.1002/lsm.20949

ß 2010 Wiley-Liss, Inc.

 LLL ON CYTOKINE SPLEEN CELLS RELEASE 585

Cytokine is the generic term used to assign a group of

molecules (proteins) involved in the signals emission
between the cells during the development of immune and
repair responses. The cytokines can be allocated in several
categories: interleukins (IL), interferon (IFN), transform-
ing growth factor (TGF), tumor necrosis factor (TNF) and
others [13].
The TNF-a and some IL’s are known as proinflammatory
cytokines. These have an important role as mediators in
inflammatory and immunological processes, proteolysis,
cell recruitment, and healing. The TNF-a has an essential
position in the cytokines release cascade, therefore it also
promotes stimulation of other cytokines release such as IL-
6. The IL-6 has been associated with several diseases that
unchain inflammatory processes such as rheumatoid Fig. 1. A: Planning of the surgery with three standardized
arthritis, acute pancreatitis, viral infections, bacterial cutaneous incision and posterior 1 cm incision in the abdo-
meningitis, and Alzheimer disease [14]. Moreover, these minal muscle; (B) LLL exposure points after surgical
inflammatory mediators sensitize the primary afferent procedure.
nociceptors, increasing pain sensitivity [15].
Several studies in the literature show the LLL irradia-
tion effects in cells associated to inflammatory reply as in
lymphocytes, fibroblasts, macrophages, endothelial cells. The animals were positioned on a plane surface with
Furthermore, there are blood plasma components such as their limbs in extension position and shaved. A skin square
platelets, red blood cells, hemoglobin, immunoglobulin flap measuring 2 cm each side was created, the cranial base
and plasmatic proteins, cell growth factors, and cytokines of the flap was kept intact. The abdominal muscle under the
[5,12,16–18]. flap was exposed and incised in a 1 cm extension; both
However, there is still a lack of research to validate the muscle and skin flap were sutured with a monofilamentar
LLL systemic effects due to a single laser application on thread (mononylon 6–0) (Fig. 1A).
cytokines release. Similarly, there is not a consensus From the 18 animals studied, 12 were submitted to this
regarding to the dosage to be used in the clinical practice. surgical procedure and afterwards they were randomly
There are studies showing that, after using the red LLL assessed to a sham or to a LLL group. The six remaining
with energy density below 18.9 J/cm2, the cytokine levels animals served as a control group.
decreased, and others with the same result with approxi-
mately 38.0 J/cm2 [16,19–21]; infrared laser irradiation * Control group: 06 animals without surgical procedure.
(850 nm, energy of 0.3 a 1.5 J) should also control the * LLL group: 06 animals with laser exposure 12 hours
induction of proinflammatory cytokines [22]. However, after surgical procedure.
other studies did not find inflammatory modulation when * Sham group: 06 animals with the same surgical
using 904 nm LLL and energy density of 9.0 J/cm2 [17]. procedure, but without laser exposure.
Therefore the purpose of this article was to analyze the
role of one single session of a low level infrared laser on the
IL-6 and TNF-a proinflammatory cytokines release from LLL Irradiation
spleen mononuclear cells in mice, in vivo. An infrared AsGaAl diode laser (model Twin Laser) with
l of 780 nm, spot size of 0.04 cm2 and an output power of
METHODS 20 mW was used.
Three punctual laser applications were performed on
This study was approved by the Research Ethics
the exposed area 12 hours after the surgical procedure
Committee of the Federal University of São Paulo accord-
(Fig. 1B). A laser exposure simulation was performed with
ing to protocol 2038/07.
the equipment in ‘‘stand by’’ for the sham group. The
The experiments were performed on 18 Balb-C isogenic
contact technique was used in all exposures [23,24].
male mice weighing 25–30 g each. The animals were
The single exposure to the LLL group was continuous
maintained in appropriate cages with a 12-hour light/dark
with an energy density of 10 J/cm2, an application time of
cycle, with a temperature around 208C, with a relative
20 seconds, and a final energy of 0.4 J per point.
humidity of (65%), and with access to food and water ad
libitum. Separation of Mononuclear Cells
The animals were euthanized 36 hours after the surgical
Surgical Procedure procedure in the sham and LLL groups, the spleen was
Anesthesia protocol consisted of ketamine (0.06 ml) dissected and macerated and later mononuclear cells were
and xylazine 2% (0.015 ml) application by intraperitoneal isolated using Ficoll-Hypaque at a density of 1.095. These
injection. cells were counted in hematologic automated equipment
586 FUKUDA ET AL.
6
and the concentration was adjusted to 210 cells/ml. The
cells were incubated in 48 culture plate wells and
stimulated with concanavalin mitogen (ConA) for 48 hours.
After this period, the supernatant was removed and
frozen to 808C until the dosage of cytokine was made.
Results from the control group were considered as baseline
standard.

Enzyme Linked Immunosorbent Assay

(ELISA) Method Analyze
Analyzes were carried out using specific antigens of
IL-6 and TNF-a cytokines dosage based on the ELISA test
(eBioscience, Inc., San Diego, CA) in the Laboratory of
Medical Investigation in Dermatology and Immuno-
deficiency—LIM-56, FMUSP, São Paulo, Brazil.
The plates were coated with capture antibody and Fig. 2. Average (  SEM) of the IL-6 concentration in pg/ml
incubated overnight at 48C. The wells were blocked with released by the mononuclear spleen cells of the control, sham,
assay diluent. All samples were incubated overnight at 48C. and LLL groups.
The wells were washed out and the detection antibody was
added and incubated at room temperature for 1 hour. The
wells were washed out and avidin-HRP complex was added produces signaling factors that, after irradiation, will
and incubated at room temperature for 30 minutes. After circulate into the blood vessels and lymphatic system [6].
that, the substrate solution was added and incubated at According to Rochkind et al. [23] the LLL systemic effects
room temperature for 15 minutes. The stop solution was in the repair of the nervous system injuries, as well as the
added and the plate read at 450 nm. wound healing and repair of bilateral cutaneous burns
induced in rat paws, demonstrated that the LLL irradiation
Analyzes of the Data
accelerated the repair of the irradiated limb as well as the
The Graph Pad statistical program was used for contralateral limb.
data processing. In the beginning, a normality test Still among these probable systemic effects, there are
(Kolmogorov–Smirnov) was performed followed by ana- theories of a significant decrease in the hemosedimentation
lysis of variance (ANOVA) with the Kruskal–Wallis speed (HSS) with the LLL action after 12 exposures, but
multiple comparison test. The data demonstrate a mean changes in the hemoglobin rate had not been noticed [24].
(  SEM) and the statistical significance was considerate at However, some studies did not observe systemic effects,
P<0.07. such as modifications of HSS, hemoglobin rate, leukocytes,
and platelets counting [25,26]. This divergence in the
RESULTS obtained results can be associated with the standardization
Regarding to the IL-6 concentration in pg/ml, the of LLL irradiation, beyond methodological problems of the
averages (  SEM) of the studied groups were: control of studies that were performed with different samples, types
38.0 (  4.7), sham of 57.8 (  8.8), and LLL of 53.1 (  8.2).
The TNF-a concentration in pg/ml were: control of
51.3 (  6.1), sham of 64.6 (  6.3), and LLL of 54.8 (  4.2).
The results observed in the IL-6 and TNF-a concen-
tration among the three groups were similar. The sham
group showed significant difference when compared to
control group (P<0.07), meaning that there was expressive
proinflammatory cytokines release by mononuclear spleen
cells in mice with the surgical proceeding. The difference
between LLL group compared to control and sham groups
was not significant (P > 0.07) (Figs. 2 and 3).

DISCUSSION
The LLL generates photochemical, photophysical and
photobiological effects, affecting not only the application
area, but also the surrounding region. Thus, the effect of a
laser beam is not only limited to the diffusion optic area.
The effect of the metabolic mediators can reach the most
distant areas of the body, generating systemic effects [23], Fig. 3. Average (  SEM) of the TNF-a concentration in pg/ml
however few studies prove this hypothesis. A possible released by the mononuclear spleen cells of the control, sham,
explanation is the fact that the tissue submitted to laser and LLL groups.
 LLL ON CYTOKINE SPLEEN CELLS RELEASE
of laser, wave lengths, mean power, and non-specified
energy doses [27,28].
The ELISA assay was employed for analysis of the IL-6
and TNF-a levels, according to Yamaura et al. [15] and
Aimbire et al. [29]. These studies showed decrease of
the proinflammatory cytokines with the laser application
immediately after intervention. The ELISA is a stand-
ardized and reliable method to measure the cytokine
concentration and for this reason, it was employed in the
present study. Our preliminary results showed that
the surgical proceeding generates increase of cytokines
release because the sham group showed significant
increase of the IL-6 and TNF-a concentration when
compared to control. The LLL probably can modulate this
process because changes in the cytokine levels release by
spleen mononuclear cells in mice were not observed
compared to the control group.
Thus, we looked for evidence of the laser effects after
single or multiple treatment sessions. Studies have shown
the effectiveness of a single laser exposure for pain relief [8],
creatine kinase (CK) levels decrease and cell apoptosis [9],
repair of ligament injuries [11] and prevention of muscle
tissue damage [10], but others did not state the same
conclusions for the healing of ligament injuries [30,31].
Then, the present study is justified by the lack of evidence of
a single LLL session for the proinflammatory cytokines
control.
According to the literature, the peak of inflammatory
process maybe occurs around 4 hours after injury [29]. In
the study conducted by Aimbire et al. [29] the laser was
employed immediately after induced inflammation and,
therefore, the animals did not suffer traumatic injury and
probably vascular damage. The experimental model of the
present study was applied trying to simulate surgical
proceedings with strong vascular damages in humans.
We hypothesized that the LLL application in the peak of
inflammatory process could increase the hemorrhage.
The decrease of the TNF-a release can be promoted by
several kinds of treatment. Among these, the LLL have
characteristics favorable to its use, as a simple application
and a non-invasive method of inflammation control [32].
The IL-6 is a pleiotropic cytokine with a wide field of
biological activities. Therefore, this helps the erythro-
poietic function, controls the immune system response,
and the production of acute phase reactions, such as the
stimulation of C-reactive protein release. This cytokine also
has an inductive metabolic role in the cortisol contra-
regulator hormone [33]. For these important functions,
both the IL-6 as well as the TNF-a were analyzed from a
single LLL session during a 12-hour period after the
surgical procedure. Because they are proinflammatory
cytokines, there is a probability of a higher release in the
initial stages of the healing process.
There are no standard values regarding to laser param-
eters in the modulation of inflammatory processes, partic-
ularly for the infrared laser, which is widely used in clinical
practice due to its greater tissue penetration [34]. There are
some studies demonstrating that the application of infrared
LLL can inhibit the TNF-a with doses between 5 and
587
2
25 J/cm [32]. Correa et al. [34] showed a migration control
of the inflammatory cells with energy of 0.24 J. In the
present article, the continuous infrared LLL (780 nm) with
an output power of 20 mW and dose equal to 10 J/cm2 was
utilized. Based on these parameters, an application time of
20 seconds was added, which generated a final energy of
0.4 J per point. Therefore, the total exposure time of
60 seconds was equal to that used by Correa et al. [34].
We did not find strong modulation of one single session
laser application when compared to sham group but the
laser probably decreased the proinflammatory cytokines
because there was not significant difference between LLL
and control group in this experimental model.
Some factors probably influenced these results, such as
an insufficient injury of the abdominal muscle of mice in
order to generate a strong inflammatory process that could
provide control of the cytokines release in circulating
spleen cells. Perhaps a more aggressive injury with a
stronger inflammatory stimulus could induce more evident
systemic changes. Finally, it is important to highlight that
we used a single laser session, and maybe 2 or 3 sessions
could unchain a stronger healing response, once the IL-6
and TNF-a expression was already lower after a single laser
pass.
CONCLUSION
According to the obtained results, we concluded that a
single session of infrared LLL showed a tendency of
decreasing the IL-6 and TNF-a release by the spleen
mononuclear cells in mice despite the low statistical power
of this pilot study. Thus, further studies are necessary with
a larger sample to test our hypothesis. Another possibility
is to study how the cumulative effect of the LLL might
influence the cytokine release and the inflammatory
process.
ACKNOWLEDGMENTS
The authors are grateful to the Research Support
Foundation of the State of São Paulo (FAPESP), Brazil,
for providing financial support (grant #2007/04479-8), and
to Vanessa Ovanessian for her help during the experimen-
tal phase, Research Group in Laser in Experimental
Surgery, Federal University of São Paulo, UNIFESP,
Brazil and Laboratory of Medical Investigation in Derma-
tology and Immunodeficiencies – LIM-56, FMUSP, Brazil.
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