Publications by authors named "Carlos Eduardo Pinfildi"

28 Publications

  • Page 1 of 1

Photobiomodulation Therapy (Light-Emitting Diode 630 nm) Favored the Oxidative Stress and the Preservation of Articular Cartilage in an Induced Knee Osteoarthritis Model.

Photobiomodul Photomed Laser Surg 2021 Apr 27;39(4):272-279. Epub 2021 Jan 27.

Department of Physical Therapy, School of Biological and Health Sciences, Universidade Federal dos Vales do Jequitinhonha e do Mucuri (UFVJM), Diamantina, Minas Gerais, Brazil.

To evaluate the effects of photobiomodulation (PBM) therapy on oxidative stress and histological aspects of knee osteoarthritis (OA) induced by sodium monoiodoacetate in Wistar rats. OA is a chronic degenerative disease. In addition to the inflammatory role, other factors, such as redox balance, appear to contribute to changes in the articular cartilage, the main articular structure affected. PBM therapy using light-emitting diode (LED) has been proposed to treat the disease by favoring anti-inflammatory effects and modulating markers of oxidative stress, acting on the degenerative process of cartilage. Twenty-seven male rats were separated into three groups: control (CG), OA (OAG), and LED treatment (LEDG). In the LED group, PBM (LED 630 nm, 300 mW, 9 J/cm, 0.3 W/cm, 30 sec) was applied, starting 24 h after induction, three times per week, for 8 weeks. Cartilage thickness, number of chondrocytes, enzymatic antioxidant defenses [superoxide dismutase (SOD) and catalase (CAT)], oxidative damage [thiobarbituric acid reactive substances (TBARS)], and nonenzymatic defense (ferric reducing antioxidant power) were analyzed. The LEDG had higher average cartilage thickness compared with the OAG and had similar thickness to the CG. Also, the number of chondrocytes was similar to the CG. In the oxidative stress analysis, the LEDG presented antioxidant enzymatic activity (SOD and CAT) higher than the CG, and presented concentration of TBARS lower than the CG and OAG groups. PBM therapy was effective in recovering oxidative stress and preserving the articular cartilage aspects in a knee OA animal model.
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http://dx.doi.org/10.1089/photob.2020.4926DOI Listing
April 2021

Acute Photobiomodulation Effects Through a Cluster Device on Skeletal Muscle Fatigue of Biceps Brachii in Young and Healthy Males: A Randomized Double-Blind Session.

Photobiomodul Photomed Laser Surg 2020 Dec;38(12):773-779

Department of Biosciences, Federal University of São Paulo (UNIFESP), Campus Baixada Santista, Santos, Brazil.

The aim of this study was to investigate and compare the acute effects of red and infrared photobiomodulation (PBM) using a cluster device on biceps brachii muscle fatigue in young and healthy males. Vigorous physical activity could lead to muscle fatigue, which compromises motor control and muscle strength and consequently impairs performance. The positive effects of PBM in reducing fatigue onset have been highlighted. However, the better wavelength with cluster devices is not yet established. A randomized double-blind session was used. Thirty-two young and healthy males were randomized into the control group (CG), red PBM group (RPG), and infrared PBM group (IPG). A PBM cluster device [7 visible diodes (630 nm), 7 infrared diodes (850 nm), 100 mW/diode, 2 W/cm power density, 91 J/cm energy density, 4 J per point, 28 J total energy, and 40 sec] was applied after muscle fatigue. Muscle fatigue was analyzed by surface electromyography (EMG) recorded from the long head of biceps brachii, blood lactate concentration, and evaluation of the rate of perceived exertion (RPE) using the Borg Scale. The fatigue protocol consisted of a maximum voluntary isotonic contraction of elbow flexion-extension with 75% of one-repetition maximum until exhaustion. The Borg Scale was applied before and at the end of the experiment to measure the RPE. The electromyography fatigue index (EMGFI) was calculated by windows of median frequency from EMG data. EMGFI, blood lactate concentration, and RPE showed no intergroup statistical difference, except the EMGFI delta value that showed a difference between IPG and CG, with a greater value in the CG. However, intragroup comparisons showed that EMGFI decreased in the CG and RPE and lactate concentration increased significantly in all groups. There was no difference between red and infrared PBM in reduction of biceps brachii fatigue. However, the EMGFI delta value was greater in the IPG compared with the CG, suggesting that infrared can be more effective in reducing biceps brachii fatigue.
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http://dx.doi.org/10.1089/photob.2019.4786DOI Listing
December 2020

Photobiomodulation Before Eccentric Fatigue Protocol in the Control of Pain and Muscle Damage Markers: A Double-Blind, Randomized Controlled Study.

Photobiomodul Photomed Laser Surg 2020 Dec;38(12):780-788

Department of Human Movement Science, University Federal of São Paulo-Campus Baixada Santista, Santos, Brasil.

Several strategies are used in the management of delayed-onset muscle soreness (DOMS), but there is not always evidence to justify its use. Photobiomodulation (PBM) is a noninvasive means, with promising previous results of its use in this outcome. This study aimed to identify the effects of PBM in the femoral quadriceps region to reduce DOMS in men undergoing a fatigue protocol. This is a double-blind, randomized controlled study. The sample consisted of 35 physically active men. The volunteers were divided into two groups: pre-fatigue PBM [Group 1 (G1)] and post-fatigue PMB [Group 2 (G2)]. The fatigue test was conducted at the same time of day. Given this was a crossover study of volunteers, we used at least a 1-week washout to avoid any residual interference from the previous intervention. PBM (active/placebo) was performed 5 min before the start of the fatigue protocol in G1 and immediately after the fatigue protocol in G2. PBM was applied at six points on the femoral quadriceps muscle (cluster laser/light emitting diodes 13, 415 mW, 30.2 J per point, 73 sec per application, and total dose of 181.2 J). In the data analysis, the primary endpoint was DOMS measured using a Numerical Pain Scale, and the secondary outcome was examined on the effects of PMB muscle damage, muscle contraction, and isometric horizontal jump. There were significant differences to PBM compared with the placebo group for DOMS, with no differences between the times of application. For muscle damage, there was significant difference ( > 0.05) when PBM was applied in pre-fatigue. G1 led to an increase of 14.9% in the creatine kinase level when active since the application of placebo PBM increased by 65% ( = 0.04). The PBM applied before eccentric fatigue protocol showed no significant results on DOMS, although there was a positive effect to control muscle damage. Brazilian Registry of Clinical Trials (RBR-7qhddz).
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http://dx.doi.org/10.1089/photob.2020.4866DOI Listing
December 2020

Investigation of different application techniques for Kinesio Taping® with an accompanying exercise protocol for improvement of pain and functionality in patients with patellofemoral pain syndrome: A pilot study.

J Bodyw Mov Ther 2020 Jan 22;24(1):47-55. Epub 2019 May 22.

Federal University of São Paulo (UNIFESP), Human Movement Sciences Department, Campus Baixada Santista, Santos, São Paulo, Brazil.

Background: Patellofemoral pain syndrome (PFPS), characterized by retropatellar and peripatellar pain, is a common disorder affecting young women. Treatment has included exercise-based therapy and taping techniques for rapid reduction of symptoms and pain. Although Kinesio Taping® (KT) has been studied as adjunctive therapy, evidence on its effectiveness is limited and conflicting.

Objective: To determine the feasibility of performing a double-blind randomized controlled trial (RCT) using KT® for PFPS treatment and to determine an ideal sample size.

Design: Double-blind, randomized, controlled pilot study.

Method: Forty-three women (aged 18-45 years) with at least a 3-month history of PFPS were randomized based on the mechanical correction techniques: using KT® for patellar medialization (KT-PM), using KT® for lateral rotation of the femur and tibia (KT-LRFT), and the control group (CG). All groups underwent the same muscle strengthening and motor control procedures for 12 weeks. Knee pain and function were evaluated at baseline, at 6 weeks, at treatment completion (12 weeks), and during the 12-week follow-up using the numerical pain rating scale (NPRS) at rest and during effort, Anterior Knee Pain Scale (AKPS), and single jump hop test.

Results: There were clinically significant differences between the KT-LRFT and the CG in terms of AKPS and NPRS scores during effort at the 6-week and 12-week follow-ups. All groups (within group) showed a significant improvement in pain and function.

Conclusions: A complete RCT using KT® for the treatment of PFPS is feasible with some changes regarding outcome measures and treatment protocols.
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http://dx.doi.org/10.1016/j.jbmt.2019.05.022DOI Listing
January 2020

High-energy dose of therapeutic ultrasound in the treatment of patellar tendinopathy: protocol of a randomized placebo-controlled clinical trial.

BMC Musculoskelet Disord 2019 Dec 27;20(1):624. Epub 2019 Dec 27.

Physical Agents and Rehabilitation Research Group GPRAE, Universidade Federal de São Paulo - UNIFESP, campus Baixada Santista, Santos, SP, 11015-029, Brazil.

Background: Patellar tendinopathy is an extremely debilitating condition and its treatment usually requires a combination of clinical approaches. Therapeutic ultrasound (TUS) is one of the most available electrophysical agent in rehabilitation settings; however, there is also a lack of high-quality studies that test different dosimetric aspects of TUS. Thus, the purpose of this study is to evaluate the short-, medium-, and long-term effects of the combination of high-energy TUS with a rehabilitation program for patellar tendinopathy.

Methods: This will be a randomized, placebo-controlled trial with blinding of patients, assessors, and therapist. The setting is an outpatient physical therapy clinic. We will recruit 66 participants (male and female) aged between 18 and 40 years and presenting with patellar tendinopathy. A treatment combining high-energy dose TUS and a rehabilitation program for patellar tendinopathy will be delivered twice a week for 8 weeks. The control group will receive the same treatment, but with a placebo TUS. The effectiveness of the intervention will be measured at the beginning (baseline), midpoint (4 weeks), and end of treatment (8 weeks), as well as at 3- and 6-months post-treatment. Primary outcomes will be pain intensity (visual analogue scale, VAS), and VISA-P questionnaire and primary time points will be baseline (T0) and the end of the program (T2). Also, IPAQ-short form questionnaire, muscle strength (manual dynamometry), 2D kinematics, pain pressure threshold (PPT) algometry, thermography, and magnetic resonance imaging (MRI) will be collected.

Discussion: TUS will be applied in an attempt to enhance the results obtained with the rehabilitation program proposed in this study, as well as stimulate some repair responses in individuals undergoing treatment for patellar tendinopathy, which in turn may optimize and improve treatment programs for patellar tendinopathy as well as to establish new guidelines for the application of TUS.

Trial Registration: This study was prospectively registered at April-3rd-2018 and updated at September-1st-2019 in the Brazilian Registry of Clinical Trials (REBEC) under the registration number: RBR-658n6w.
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http://dx.doi.org/10.1186/s12891-019-2993-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6933732PMC
December 2019

Hip and Knee Weakness and Ankle Dorsiflexion Restriction in Individuals Following Lateral Patellar Dislocation: A Case-Control Study.

Clin J Sport Med 2019 Dec 13. Epub 2019 Dec 13.

Human Movement Sciences Department, Federal University of São Paulo (UNIFESP), São Paulo, Brazil.

Objective: To explore the relationship between ankle dorsiflexion range of motion (ROM) and hip and knee muscle strength between patients with a history of patellar dislocation (PD) to healthy controls.

Design: Case-control study.

Setting: Orthopedical specialty outpatient clinic at a tertiary hospital.

Participants: Eighty-eight individuals were recruited; 44 individuals aged 16 years or older, of both sexes, with a history of at least one episode of atraumatic unilateral or bilateral PD requiring emergency care (14 men; 30 women; mean age 20 years) and 44 healthy (control) individuals (11 men; 33 women; mean age 21 years) matched for age, weight, and height to PD cases.

Intervention: Assessment of hip and knee strength and ankle dorsiflexion ROM.

Outcome Measures: Ankle dorsiflexion ROM was assessed through the lunge test with a goniometer. Hip and knee muscle strength was evaluated through isometric hand-held dynamometry. Differences between healthy and control individuals were assessed using Student t Tests and Mann-Whitney U Test.

Results: Patellar dislocation individuals presented with a reduced ankle dorsiflexion ROM [mean difference (MD): 9 degrees; effect size (ES): 1.39; P < 0.001] and generalized hip and knee weakness (MD range: 4.74 kgf to 31.4 kgf; ES range: 0.52-2.35; P < 0.05) compared with healthy subjects.

Conclusion: Individuals with a history of PD have reduced ankle dorsiflexion ROM and hip and knee muscle strength compared with healthy controls.
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http://dx.doi.org/10.1097/JSM.0000000000000815DOI Listing
December 2019

Photobiomodulation therapy and NMES improve muscle strength and jumping performance in young volleyball athletes: a randomized controlled trial study in Brazil.

Lasers Med Sci 2020 Apr 11;35(3):621-631. Epub 2019 Aug 11.

Departamento de Ortopedia e Traumatologia, Programa de Pós-Graduação em Ciências da Saúde Aplicada ao Esporte e à Atividade Física, Universidade Federal de São Paulo, São Paulo, Brazil.

The purpose of this study was to investigate the effectiveness of adding photobiomodulation therapy and neuromuscular electrical stimulation (NMES) to volleyball athletes' training, focusing on muscle strength and jumping skills. Thirty-six athletes were randomly placed into three groups: control, photobiomodulation therapy, and NMES. The athletes trained to improve their muscle strength and jumping skills. The athletes in the photobiomodulation therapy group were submitted to photobiomodulation therapy (850 nm, continuous, energy density 0.8 J/cm, radiant energy per point 6 J, total radiant energy 36 J) before undergoing strength and plyometric training. The NMES group additionally underwent NMES-based quadriceps femoris muscle strength training (base frequency 1 kHz, frequency modulation 70 Hz, intensity maximum tolerable). The variables analyzed were muscle strength, jumping ability, global impression, and jump frequency; they were measured at baseline and during follow-ups at 6 and 8 weeks. The statistical analysis was conducted on an intention-to-treat basis. The between-group differences and their respective 95% CIs were calculated using linear mixed models by using group, time, and group-versus-time interaction terms. Dominant lower limb strength improved the most in the NMES group compared to the control group (mean difference = 1.4, 95% CI = .5 to 2.4). Non-dominant lower limb strength increased in both the photobiomodulation therapy group (mean difference = 1.1, 95% CI = .3 to 2) and the NMES group (mean difference = 1.9, 95% CI = 1.1 to 2.8) compared to the control group, but the NMES group improved more than the photobiomodulation therapy group (mean difference = 0.8, 95% CI = 0.1 to 1.7). The NMES group had the greatest improvement in global perceived effect scale compared to the control group (mean difference = 1.1, 95% CI = 1 to 2.2). Dominant lower limb strength improved in the NMES group compared to the control group. Non-dominant lower limb strength increased in both the photobiomodulation therapy group and the NMES group compared to the control group, but the NMES group improved significantly more than the photobiomodulation therapy group; the NMES group also improved in the global perceived effect scale compared to the control group. This study found that, for volleyball athletes, photobiomodulation therapy and NMES both promoted benefits in terms of muscle-strength gain. In addition, these benefits were maintained for 2 weeks even after training was interrupted. Dominant lower limb strength improved in the NMES group compared to the control group. Non-dominant lower limb strength increased in both the photobiomodulation therapy group and the NMES group compared to the control group, but the NMES group improved significantly more than the photobiomodulation therapy group; the NMES group also improved in global impression of jumps compared to the control group.
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http://dx.doi.org/10.1007/s10103-019-02858-6DOI Listing
April 2020

Translation, cross-cultural adaptation and validation of the Norwich Patellar Instability score for use in Brazilian Portuguese.

Sao Paulo Med J 2019 Jul 15;137(2):148-154. Epub 2019 Jul 15.

PT, PhD. Professor, Department of Human Movement Sciences, Universidade Federal de São Paulo (UNIFESP), Baixada Santista Campus, Santos (SP), Brazil.

Background: The Norwich Patellar Instability (NPI) score is a tool for evaluating the impact of patellofemoral instability on joint function. It has not been translated or culturally adapted for the Brazilian population before.

Objective: This study had the aims of translating and culturally adapting the NPI score for use in Brazilian Portuguese and subsequently assessing its validity for this population.

Design And Setting: Translation, cross-cultural adaptation and validation study conducted at the State Public Servants' Institute of São Paulo, Brazil.

Methods: Sixty patients of both sexes (aged 16-40 years) with diagnoses of patellar dislocation were recruited. The translation and cultural adaptation were undertaken through translation into Brazilian Portuguese and back-translation to English by an independent translator. Face validity was assessed by a committee of experts and by 20 patients. Concurrent validity was assessed through comparing the Brazilian Portuguese NPI score with the Brazilian Portuguese versions of the Lysholm knee score and the Kujala patellofemoral disorder score among the other 40 patients. Correlation analysis between the three scores was performed using Pearson correlation coefficients with significance levels of P < 0.05.

Results: The Brazilian Portuguese version of the NPI score showed moderate correlation with the Brazilian Portuguese versions of the Lysholm score (r = -0.56; 95% confidence interval, CI: -0.74 to -0.30; P < 0.01) and Kujala score (r = -0.57; 95% CI: -0.75 to -0.31; P < 0.01).

Conclusion: The Brazilian Portuguese version of the NPI score is a validated tool for assessing patient-reported patellar instability for the Brazilian population.
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http://dx.doi.org/10.1590/1516-3180.2018.0393280119DOI Listing
July 2019

Photobiomodulation of Matrix Metalloproteinases in Rat Calcaneal Tendons.

Photobiomodul Photomed Laser Surg 2019 Jul 11;37(7):421-427. Epub 2019 Jun 11.

5 Surgery Department, Universidade Federal de São Paulo-UNIFESP, São Paulo, Brazil.

The main objective was to verify the modulatory effects of MMP-1, MMP-3, and MMP-13 levels on the partially injured calcaneal tendons of rat exposure to photobiomodulation. Photobiomodulation has been shown to have anti-inflammatory and regenerative effects on tendon injuries. However, there is still uncertainty regarding the beneficial effects in matrix metalloproteinase (MMP) levels, especially MMP-1, -3, and -13. Sixty-five male Wistar rats were used. Sixty were submitted to a direct trauma on the calcaneal tendons and were randomly distributed into the following six groups: LASER 1, 3, and 7 (10 partially injured calcaneal tendons in each group treated with photobiomodulation for 1, 3, and 7 days, respectively) and Sham 1, 3, and 7 (same injury, with simulated photobiomodulation). The remaining five animals were allocated to the normal group (no injury or treatment procedure). The 780 nm low-level laser was applied with 70 mW of mean power and 17.5 J/cm of fluency for 10 sec, once a day. The tendons were surgically removed and analyzed for MMP-1, MMP-3, and MMP-13 through immunohistochemistry. MMP-3 levels remained close to normal in all experimental groups ( > 0.05); however, reductions ( < 0.05) in MMP-1 and MMP-13 levels were detected in the groups submitted to one, three, and seven low level laser therapy applications. The photobiomodulation protocol was able to reduce MMP-1 and MMP-13 levels in injured calcaneal tendons.
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http://dx.doi.org/10.1089/photob.2019.4633DOI Listing
July 2019

NEUROMUSCULAR ELECTRICAL STIMULATION OF MEDIUM AND LOW FREQUENCY ON THE QUADRICEPS FEMORIS.

Acta Ortop Bras 2018 ;26(5):346-349

Universidade Federal de Goiás (UFG), Department of Physical Therapy, Jatai, GO, Brazil.

Objective: The purpose of this study was to investigate the effects of neuromuscular electrical stimulation (NMES) in different frequencies on the quadriceps femoris. A randomized, controlled, blind cross-sectional study.

Methods: Thirty subjects (12 men and 18 women), with an average age of 24.67 years, weight of 65.62 kg and height of 1.69 m were evaluated. Three random test conditions were applied: maximum voluntary isometric contraction (MVIC), maximum voluntary isometric contraction with medium frequency current (MVIC-MF) and maximum voluntary isometric contraction with low frequency current (MVIC-LF). Four MVICs were applied in each situation. The time between different isometric contraction types was 90 seconds while the time between the same conditions of contraction was 10 seconds.

Results: Two-way ANOVA test showed that MVIC-MF had higher values for peak torque than MVIC-LF (p=0.02). Significant statistical results were found when comparing MVIC-MF and MVIC (p=0.03), but not for MVIC and MVIC-LF (p=0.52).

Conclusion: Maximum voluntary isometric contraction associated with medium-frequency electrical stimulation was more effective than other NMES conditions.
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http://dx.doi.org/10.1590/1413-785220182605178164DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6220661PMC
January 2018

Prevalence of musculoskeletal injuries and a proposal for neuromuscular training to prevent lower limb injuries in Brazilian Army soldiers: an observational study.

Mil Med Res 2018 07 27;5(1):23. Epub 2018 Jul 27.

Human Movement Science and Rehabilitation, Department of Human Movement Science, Federal University of São Paulo-Physical Therapy, Campus Baixada Santista, Rua Silva Jardim, 136, Vila Mathias, Santos, SP, 11015-020, Brazil.

Background: The activities carried out by soldiers in the army involve great physical demands and require intense trainings to perform combat-specific tasks. Musculoskeletal injury is a potential threat to the health and physical integrity of the soldier. This study aimed to evaluate the prevalence of lower limb musculoskeletal injuries among soldiers and to propose a training protocol to prevent the most frequent injuries.

Methods: This observational (cross-sectional) study recruited a sample of 103 soldiers who required medical attention, from a total 202 new battalion soldiers. The medical records (paper and online) had a form of running text. All data collected were recorded by the registered physicians of the battalion medical post. The records were analyzed by the following variables: medical diagnosis, injury site, mechanism, type of treatment, time loss, existence of previous injury, and recurring injury.

Results: A total of 112 musculoskeletal injuries were diagnosed in 71 soldiers, and other types of diseases/injuries were diagnosed in the other soldiers. Joint pain accounted for 55.4% of the diagnoses. The knee was the most affected site, while trauma and overload were the most common mechanisms of injury. Drug treatment was used most frequently, accounting for 58% of the cases. The majority of the sample obtained a temporary leave of absence for 1 to 6 days or not at all. Previous injuries and recurrence were not presented as risk factors for injury. With the data received, a protocol for the prevention of injuries to the lower limbs was proposed.

Conclusion: This study indicated that the most frequent site of injury is the knee, and joint pain is the most common diagnosis. These results may support the necessity to develop a neuromuscular training protocol to prevent lower limb injuries, which we suggest to be applied in future studies.
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http://dx.doi.org/10.1186/s40779-018-0172-7DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6062882PMC
July 2018

Laser photobiomodulation (830 and 660 nm) in mast cells, VEGF, FGF, and CD34 of the musculocutaneous flap in rats submitted to nicotine.

Lasers Med Sci 2017 Feb 2;32(2):335-341. Epub 2016 Dec 2.

Post-Graduate Program in Rehabilitation and Functional Performance of Ribeirão Preto Medical School of the University of São Paulo (FMRP/USP), Av. dos Bandeirantes, 3900, Ribeirão Preto, SP, 14049-900, Brazil.

The aim of this study was to investigate the effect of laser photobiomodulation (PBM) on the viability of the transverse rectus abdominis musculocutaneous (TRAM) flap in rats subjected to the action of nicotine. We evaluated 60 albino Wistar rats, divided into six groups of ten animals. Group 1 (saline) underwent the surgical technique to obtain a TRAM flap; group 2 (laser 830 nm) underwent the surgical technique and was irradiated with a laser 830 nm; group 3 (laser 660 nm) underwent the surgical technique and was irradiated with a laser 660 nm; group 4 was treated with nicotine subcutaneously (2 mg/kg/2×/day/4 weeks) and underwent surgery; group 5 (nicotine + laser 830 nm) was exposed to nicotine, underwent the surgical technique, and was irradiated with a laser 830 nm; group 6 (nicotine + laser 660 nm) was exposed to nicotine, underwent the surgical technique, and was irradiated with a laser 660 nm. The application of PBM occurred immediately after surgery and on the two following days. The percentage of necrosis was assessed using the AxioVision® software. The number of mast cells (toluidine blue staining) was evaluated, and immunohistochemistry was performed to detect vascular endothelial growth factor expression (anti-VEGF-A), fibroblasts (anti-basic FGF), and neoformed vessels (anti-CD34). PBM with a wavelength of 830 nm increased the viability of the TRAM flap, with a smaller area of necrosis, increased number of mast cells, and higher expression of VEGF and CD34. PBM increases the viability of musculocutaneous flaps treated with to nicotine.
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http://dx.doi.org/10.1007/s10103-016-2118-1DOI Listing
February 2017

High voltage pulsed current in collagen realignment, synthesis, and angiogenesis after Achilles tendon partial rupture.

Braz J Phys Ther 2016 Jul-Aug;20(4):312-9. Epub 2016 Jun 16.

Departamento de Cirurgia Plástica, Universidade Federal de São Paulo (UNIFESP), São Paulo, SP, Brazil.

Objective: To verify the efficacy of high voltage pulsed current in collagen realignment and synthesis and in angiogenesis after the partial rupturing of the Achilles tendon in rats.

Method: Forty male Wistar rats were randomized into four groups of 10 animals each: sham, cathodic stimulation, anodic stimulation, and alternating stimulation. Their Achilles tendons were submitted to direct trauma by a free-falling metal bar. Then, the treatment was administered for six consecutive days after the injury. In the simulation group, the electrodes were positioned on the animal, but the device remained off for 30 minutes. The other groups used a frequency of 120 pps, sensory threshold, and the corresponding polarity. On the seventh day, the tendons were removed and sent for histological slide preparation for birefringence and Picrosirius Red analysis and for blood vessel quantification.

Results: No significant difference was observed among the groups regarding collagen realignment (types I or III collagen) or quantity of blood vessels.

Conclusion: High voltage pulsed current for six consecutive days was not effective in collagen realignment, synthesis, or angiogenesis after the partial rupturing of the Achilles tendon in rats.
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http://dx.doi.org/10.1590/bjpt-rbf.2014.0167DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5015677PMC
June 2017

Low-Level Laser Therapy (780 nm) on VEGF Modulation at Partially Injured Achilles Tendon.

Photomed Laser Surg 2016 Aug 26;34(8):331-5. Epub 2016 May 26.

5 Surgery Department, Universidade Federal de São Paulo-UNIFESP , São Paulo, Brazil .

Objective: The aim of this study was to analyze the modulatory effects of near infrared (780 nm) low-level laser therapy (LLLT) on the presence of the vascular endothelial growth factor (VEGF) in the partially injured Achilles tendons of rats.

Background: LLLT stimulates the healing process for Achilles tendon injuries, although the extent of the modulatory effect of LLLT on the VEGF levels found in the injured tendons remains unclear.

Methods: Sixty-five male Wistar rats were distributed in the following seven groups: LASER 1, 3, and 7 (10 partially injured Achilles tendons in each group, which were treated with LLLT for 1, 3, and 7 days, respectively); Sham 1, 3, and 7 (same injury, with simulated LLLT); Control group containing the five remaining animals and in which no procedures were performed. LLLT was applied once a day for 10 sec, with a mean power of 70 mW and fluency of 17.5 J/cm(2). After euthanasia, all of the Achilles tendons were surgically removed and the VEGF levels were analyzed using immunohistochemistry.

Results: The VEGF levels remained close to normal (p > 0.05) when comparing the experimental groups (LASER and Sham: 1, 3, and 7) with the Control group.

Conclusion: LLLT did not stimulate the expression of VEGF in the treated Achilles tendons.
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http://dx.doi.org/10.1089/pho.2016.4092DOI Listing
August 2016

Achilles Tendon Vascularization of Proximal, Medial, and Distal Portion Before and After Partial Lesion in Rats Treated with Phototherapy.

Photomed Laser Surg 2015 Dec;33(12):579-84

2 Department of Human Movement Science (DHMS)-University Federal of São Paulo-Campus Baixada Santista-Santos, SP, Brazil. Post-Graduation Interdisciplinary Health Science-Unifesp-Baixada Santista, Santos SP, Brazil .

Background: The Achilles tendon is one of the tendons most commonly injured by microtraumas and overuse during sports practice. This tendon is especially fragile because of the low blood supply in its central part. Nevertheless, the literature does not offer enough scientific support to explain the composition and vascular dynamic of animal tendons, despite the relevance of being able to observe if the animal tendon undergoes the same processes of vascularization in different regions, as occurs in humans.

Methods: We used 28 rats weighing 280 ± 20 g, which were divided into four groups with seven animals each (control, sham, 830 nm, 660 nm). The laser parameters were: power output 60 mW for both lasers, 40 J/cm(2) of energy density, total energy 1.1 J, power density 2.14 W/cm(2), and application time 18.6 sec. This study evaluated the vascular constitution of healthy and injured calcaneous tendons. The tendons of each animal were processed to be embedded in Paraplast and, after that, they were divided into three parts: proximal, medial, and distal. Afterwards, they were cut in slices of 6 μm were made, then they were stained with hematoxylin and eosin. Using an ocular lens reticulated with magnification × 400, we analyzed the number and the area density of the blood vessels using morphometric methods. Data were analyzed with the Shapiro-Wilk test, followed by Tukey, considering p as <0.05.

Results: The area density and the number of blood vessels in the proximal part were 36% and 42%, respectively, of the values found in the medial part. The distal part had 64% more vessels and 52.8% more area density (p < 0.05) than the medial part.

Conclusions: Low-level laser therapy (LLLT) had no effect on the studied parameters. The vascularization of rat tendon is similar to that of humans, which contributes to the studies of therapies that have been applied in humans.
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http://dx.doi.org/10.1089/pho.2015.3974DOI Listing
December 2015

Low-level laser therapy in IL-1β, COX-2, and PGE2 modulation in partially injured Achilles tendon.

Lasers Med Sci 2015 Jan 29;30(1):153-8. Epub 2014 Jul 29.

Interdisciplinary Surgical Science Program, Universidade Federal de São Paulo-UNIFESP, São Paulo, SP, 04021-001, Brazil,

This study evaluated IL-1β, COX-2, and PGE2 modulation in partially injured Achilles tendons treated with low-level laser therapy (LLLT). Sixty-five male Wistar rats were used. Sixty were submitted to a direct injury on Achilles tendon and then distributed into six groups: LASER 1 (a single LLLT application), LASER 3 (three LLLT applications), and LASER 7 (seven LLLT applications) and Sham 1, 3, and 7 (the same injury but LLLT applications were simulated). The five remaining animals were allocated at control group (no procedure performed). LLLT (780 nm) was applied with 70 mW of mean power and 17.5 J/cm(2) of fluency for 10 s, once a day. The tendons were surgically removed and assessed immunohistochemically for IL-1β, COX-2, and PGE2. In comparisons with control (IL-1β: 100.5 ± 92.5 / COX-2: 180.1 ± 97.1 / PGE2: 187.8 ± 128.8) IL-1β exhibited (mean ± SD) near-normal level (p > 0.05) at LASER 3 (142.0 ± 162.4). COX-2 and PGE2 exhibited near-normal levels (p > 0.05) at LASER 3 (COX-2: 176.9 ± 75.4 / PGE2: 297.2 ± 259.6) and LASER 7 (COX-2: 259.2 ± 190.4 / PGE2: 587.1 ± 409.7). LLLT decreased Achilles tendon's inflammatory process.
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http://dx.doi.org/10.1007/s10103-014-1636-yDOI Listing
January 2015

Acute effects of low-level laser therapy on physiologic and electromyographic responses to the cardiopulmonary exercise testing in healthy untrained adults.

Lasers Med Sci 2014 Nov 13;29(6):1945-51. Epub 2014 Jun 13.

Department of Human Movement Sciences, Federal University of São Paulo, Rua Silva Jardim, 136, Vila Mathias, Santos, São Paulo, 11015-020, Brazil,

Despite the positive effects of low-level laser therapy (LLLT) on muscle fatigue before exercises using a single muscle group, the acute effects of LLLT on performance in cardiopulmonary exercise testing (CPET) are poorly understood. We aimed to assess the acute effects of LLLT on physiologic and electromyographic responses to the CPET in healthy adults. A randomized, double-blind, placebo-controlled crossover trial was performed with 18 untrained participants (nine males, 22 ± 2 years). We applied LLLT or placebo on quadriceps and gastrocnemius 10 min before two rapidly incremental CPETs randomly performed in alternate days on a cycle ergometer. Participants received LLLT using a multidiode cluster, 20 s/site (850 nm, 100 mW/diode, 14 J/site). Physiological responses to the CPET were continuously monitored using a gas analyzer. The electromyographic fatigue threshold (EMGth) was assessed through surface electrodes on vastus lateralis. The root mean square (RMS) was plotted every 5 s against the exercise intensity, and its breakpoint values throughout the CPET was identified as EMGth. Compared to placebo, the LLLT significantly increased peak O2 uptake (V'O2 33 ± 10 vs. 31 ± 9 mL/min/kg). We observed a shallower slope of the Δheart rate/ΔV'O2 during the CPET after LLLT compared to placebo, i.e., increased cardiovascular efficiency (56 ± 24 vs. 66 ± 30 bpm/L/min). There were no LLLT-related changes in EMGth. The LLLT acutely increases exercise performance in healthy untrained adults probably due to increased O2 extraction by peripheral muscles without causing a significant impact on muscle fatigue.
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http://dx.doi.org/10.1007/s10103-014-1595-3DOI Listing
November 2014

Low-level laser therapy on tissue repair of partially injured achilles tendon in rats.

Photomed Laser Surg 2014 Jun 15;32(6):345-50. Epub 2014 May 15.

1 Interdisciplinary Surgical Science Program, Universidade Federal de São Paulo-UNIFESP , São Paulo, Brazil .

Objective: The aim of this study was to assess the alignment and type of collagen (I and III) in partially injured Achilles tendons of rats treated with low-level laser therapy (LLLT).

Background: Achilles tendons present high indices of injury and their regeneration process may take a long time. LLLT has been used to accelerate and enhance injured Achilles tendon repair.

Methods: Sixty-five male Wistar rats were distributed into seven groups: LASER 1, 3, and 7 (the rat's Achilles tendons were partially injured and submitted to treatment for 1, 3, or 7 days, respectively); a Sham group 1, 3, and 7 for each of LASER group (same injury, but the LLLT was only simulated), and five remaining animals were allocated to the control group (no procedures were performed). The 780 nm LLLT was applied once a day, with 70 mW of mean power, fluence of 17.5 J/cm(2) for 10 sec. After the rats were euthanized, the tendons were surgically removed and assessed by birefringence technique (collagen alignment) and picrosirius red (collagen I and III).

Results: Sham versus LASER analysis did not show differences (p>0.05) for collagen alignment. The collagen composition (median) was significantly different (p<0.05) for LASER 3 (I: 16.5; III: 83.5) versus Sham 3 (I: 12.5; III: 87.5) and LASER 7 (I: 20.2; III: 79.8) versus Sham 7 (I: 10.2; III: 89.8). LASER groups exhibited a higher percentage of type I collagen and a lower percentage of type III collagen.

Conclusions: LLLT stimulated collagen I proliferation, improving the injured Achilles tendons' healing process.
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http://dx.doi.org/10.1089/pho.2013.3694DOI Listing
June 2014

What is better in TRAM flap survival: LLLT single or multi-irradiation?

Lasers Med Sci 2013 May 22;28(3):755-61. Epub 2012 Jun 22.

Department of Science of Human Movement, University Federal of São Paulo-UNIFESP, Campus Baixada Santista, Santos, São Paulo, Brazil.

Low-level laser therapy (LLLT) has been used with the aim of improving vascular perfusion of the skin and musculocutaneous flaps. This study evaluated the effect of LLLT on transverse rectus abdominis musculocutaneous flap (TRAM) viability, vascular angiogenesis, and VEGF release. Eighty-four Wistar rats were randomly divided into seven groups with 12 rats in each group. Group 1 received sham laser treatment; group 2, 3 J/cm(2) at 1 point; group 3, 3 J/cm(2) at 24 points; group 4, 72 J/cm(2) at 1 point; group 5, 6 J/cm(2) at 1 point; group 6, 6 J/cm(2) at 24 points; and group 7, 144 J/cm(2) at 1 point. All experimental groups underwent LLLT immediately after the TRAM operation and on the following 2 days; thus, animals underwent 3 days of treatment. The percentage of skin flap necrosis area was calculated on the fourth postoperative day using the paper template method, and two skin samples were collected using a 1-cm(2) punch to evaluate alpha smooth muscle actin (1A4) and VEGF levels in blood vessels. Significant differences were found in necrosis percentage, and higher values were seen in group 1 than in the other groups. Statistically significant differences were not found among groups 3 to 7 (p<0.292). Groups 5 and 7 showed significantly higher VEGF levels compared to other groups. Groups 3 and 5 had an increase in levels of blood vessels compared to other groups. LLLT at energy densities of 6 to 144 J/cm(2) was efficient to increase angiogenesis and VEGF levels and promote viability in TRAM flaps in rats.
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http://dx.doi.org/10.1007/s10103-012-1130-3DOI Listing
May 2013

Different power settings of LLLT on the repair of the calcaneal tendon.

Photomed Laser Surg 2011 Oct 13;29(10):663-8. Epub 2011 Jun 13.

Department of Plastic Surgery, Universidade Federal de São Paulo, Rua Napoleão de Barros 715, São Paulo, Brazil.

Objective: The purpose of this study was to evaluate the effect of an 830-nm GaAlAs diode laser operating at output powers of 40, 60, 80, and 100 mW and energy density of 30 J/cm(2) on the repair of partial calcaneal tendon ruptures in rats.

Methods: A partial tendon rupture was induced in all animals, which were treated with laser irradiation for 5 consecutive days. Six days after injury, the injured tendons were removed and examined by polarized light microscopy. Collagen fiber organization was evaluated by birefringence measurements, and collagen content was determined by Picrosirius Red staining.

Results: It was observed that the higher the output power (60-100 mW) the greater the amount of type III collagen (p<0.01). The amount of type I collagen was significantly greater (p=0.05) in the 80 mW group than in the control group (sham stimulation). A non-statistically significant improvement in the realignment of collagen fibers was observed in the irradiated groups.

Conclusions: Low-level laser therapy resulted in significantly greater amounts of type III collagen (output powers of 60 mW or more) and type I collagen (output power of 80 mW), however, no significant differences between groups were found in the realignment of collagen fibers.
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http://dx.doi.org/10.1089/pho.2010.2919DOI Listing
October 2011

Low-level laser therapy on the viability of skin flap in rats subjected to deleterious effect of nicotine.

Photomed Laser Surg 2011 Aug 1;29(8):581-7. Epub 2011 Apr 1.

Department of Biomechanics, Medicine and Rehabilitation of the Locomotor System, University of São Paulo-FMRP/USP, Ribeirão Preto, Brazil.

Objective: The purpose of this study was to evaluate the effect of 830-nm laser in blocking the action of nicotine on the viability of skin flap.

Background Data: The authors have analyzed the deleterious effect of cigarette smoke or nicotine on the skin flap alone with evidence of increased skin necrosis in the flap.

Materials And Methods: Twenty-four Wistar-albino rats were divided into three groups of eight animals each: Group 1 (control), subjected to a surgical technique to obtain a flap for cranial base, laser irradiation simulation, and a subcutaneous injection of saline; Group 2, similar to Group 1, with subcutaneous injection of nicotine (2  mg/kg/day) for a period of 1 week before and 1 week after surgery; and Group 3, similar to Group 2, with skin flaps subjected to a λ 830-nm laser irradiation. The laser parameters used were: power 30 mW, beam area 0.07 cm(2), irradiance 429 mW/cm(2), irradiation time 84  sec, total energy 2.52  J, and energy density 36 J/cm(2). The laser was used immediately after surgery and for 4 consecutive days, in one point at 2.5  cm of the flap cranial base. The areas of necrosis were examined by two macroscopic analyses: paper template and Mini-Mop(®). The pervious blood vessels were also counted.

Results: The results were statistically analyzed by ANOVA and post-test contrast orthogonal method (multiple comparisons), showing that the laser decreased the area of necrosis in flaps subjected to nicotine, and consequently, increased the number of blood vessels (p < 0.05).

Conclusions: The laser proved to be an effective way to decrease the area of necrosis in rats subjected to nicotine, making them similar to the control group.
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http://dx.doi.org/10.1089/pho.2010.2883DOI Listing
August 2011

In vitro effect of 470 nm LED (Light Emitting Diode) in keloid fibroblasts.

Acta Cir Bras 2011 Feb;26(1):25-30

Department of Surgery, UNIFESP, Sao Paulo, SP, Brazil.

Purpose: To quantify keloid fibroblasts after irradiation with 470nm blue LED, in vitro.

Methods: Fibroblasts from keloid and adjacent skin have been obtained from 6 patients. Cells have been cultivated and maintained in DMEM culture medium. In Petri dishes, they were irradiated with energy doses of 6J, 12J and 18J. After 24 h, counting was done by the average of the triplicates for each sample.

Results: There were no significant differences in the number of irradiated keloid fibroblasts at the studied doses (p=0.261). In adjacent skin fibroblasts, differences were observed (p=0.025) concerning the doses of 18 J and 6 J (p=0.03).

Conclusions: There was a reduction in the number of adjacent skin fibroblasts irradiated with 470nm blue LED at the energy dose of 18 J compared to the ones irradiated at the energy dose of 6 J. There were no changes in keloid fibroblasts counting at any of the doses applied, 24 h after irradiation.
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http://dx.doi.org/10.1590/s0102-86502011000100006DOI Listing
February 2011

Mechanical stimulation improves survival in random-pattern skin flaps in rats.

Ultrasound Med Biol 2010 Dec 15;36(12):2048-56. Epub 2010 Oct 15.

Graduate Program, Federal University of Sao Paulo School of Medicine (UNIFESP-EPM), Sao Paulo, Brazil.

This was a study on the effects of 3-MHz ultrasound at 16- and 100-Hz pulse repetition frequencies on angiogenesis and viability of random-pattern skin flaps in rats. A cranially-based dorsal skin flap was raised in 60 EPM-Wistar rats, which were randomly divided into four groups: control, sham, 16-Hz and 100-Hz groups. The mean percentage of necrosis was as follows: control, 42% ± 13%; sham, 18% ± 13%; 16-Hz group, 13% ± 10%; and 100-Hz group, 15% ± 7%, with significant differences between the control and the other groups (p < 0.001). The mean vascular density was as follows: control, 5% ± 2%; sham, 7% ± 2%; 16-Hz group, 21% ± 4%; and 100-Hz group, 24% ± 10%, with significant differences between control and ultrasound groups, and between the sham and ultrasound groups (p < 0.001). Both ultrasound treatments (16- and 100-Hz PRFs) induced angiogenesis, and sham and ultrasound treatments improved viability of random-pattern skin flaps in rats.
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http://dx.doi.org/10.1016/j.ultrasmedbio.2010.07.020DOI Listing
December 2010

Effect of low level laser therapy (830 nm) with different therapy regimes on the process of tissue repair in partial lesion calcaneous tendon.

Lasers Surg Med 2009 Apr;41(4):271-6

Department of Plastic Surgery, São Paulo Federal University-UNIFESP, São Paulo, SP 04024-900, Brazil.

Background And Objective: Calcaneous tendon is one of the most damaged tendons, and its healing may last from weeks to months to be completed. In the search after speeding tendon repair, low intensity laser therapy has shown favorable effect. To assess the effect of low intensity laser therapy on the process of tissue repair in calcaneous tendon after undergoing a partial lesion.

Study Design/materials And Methods: Experimentally controlled randomized single blind study. Sixty male rats were used randomly and were assigned to five groups containing 12 animals each one; 42 out of 60 underwent lesion caused by dropping a 186 g weight over their Achilles tendon from a 20 cm height. In Group 1 (standard control), animals did not suffer the lesion nor underwent laser therapy; in Group 2 (control), animals suffered the lesion but did not undergo laser therapy; in Groups 3, 4, and 5, animals suffered lesion and underwent laser therapy for 3, 5, and 7 days, respectively. Animals which suffered lesion were sacrificed on the 8th day after the lesion and assessed by polarization microscopy to analyze the degree of collagen fibers organization.

Results: Both experimental and standard control Groups presented significant values when compared with the control Groups, and there was no significant difference when Groups 1 and 4 were compared; the same occurred between Groups 3 and 5.

Conclusion: Low intensity laser therapy was effective in the improvement of collagen fibers organization of the calcaneous tendon after undergoing a partial lesion.
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http://dx.doi.org/10.1002/lsm.20760DOI Listing
April 2009

Effect of application site of low-level laser therapy in random cutaneous flap viability in rats.

Photomed Laser Surg 2009 Jun;27(3):411-6

Master of Basic Sciences in Plastic Surgery, São Paulo Federal University, São Paulo, SP, Brazil.

Objective: This study aimed to investigate the effect of diode laser (830 nm) irradiation on the viability of ischemic random skin flaps in rats, as well as to determine the most effective site for applying laser radiation to speed healing.

Background Data: Low-level laser therapy (LLLT) has recently been used to improve the viability of ischemic random skin flaps in rats.

Materials And Methods: Seventy Wistar rats were used and divided into seven groups of 10 rats each: group 1, sham laser treatment; group 2, which received irradiation at 1 point 5 cm from the flap's cranial base; group 3, which received irradiation at 2 points (5 and 7.5 cm from the flap's base); group 4, which received irradiation at 3 points (2.5, 5 and 7.5 cm from the flap's base); group 5, which received irradiation at 1 point 2.5 cm from the flap's base; group 6, which received irradiation at 2 points (2.5 and 5 cm from the flap's base); and group 7, which received irradiation at 1 point 7.5 cm from the flap's base. The animals were subjected to laser therapy at an energy density of 36 J/cm(2) for 72 sec immediately after surgery, and one time on each of the four subsequent days. The percentage of necrotic skin flap area was calculated on the seventh postoperative day using a paper template.

Results: The results showed that the rats in group 5 had the highest increase in skin flap viability, with a statistically significant difference compared to the other groups. Statistically significant differences were not seen between any of the other groups.

Conclusion: The diode laser was effective in increasing skin flap viability in rats, and laser irradiation of a point 2.5 cm from the cranial base flap was found to be the most effective.
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http://dx.doi.org/10.1089/pho.2008.2320DOI Listing
June 2009

Effect of low-level laser therapy on mast cells in viability of the transverse rectus abdominis musculocutaneous flap.

Photomed Laser Surg 2009 Apr;27(2):337-43

Department of Plastic Surgery and IMES-FAFICA, São Paulo Federal University, São Paulo, SP, Brazil.

Objective: To assess the effect of low-level laser therapy (LLLT) on viability of mast cells of the transverse rectus abdominis musculocutaneous (TRAM) flap.

Background Data: LLLT has been recently used on the TRAM flap to stimulate mast cells.

Materials And Methods: Eighty-four Wistar rats were randomly divided into seven groups of 12 rats in each: group 1 (sham laser therapy); group 2 received 3 J/cm(2) at one point; group 3 received 3 J/cm(2) at 24 points; group 4 received 72 J/cm(2) at 1 point; group 5 received 6 J/cm(2) at 1 point; group 6 received 6 J/cm(2) at 24 points; and group 7 received 144 J/cm(2) at 1 point. All experimental groups underwent LLLT immediately after TRAM surgery and on the next two following days, for three sessions in total. The percentage of the area of skin flap necrosis was calculated on the fourth postoperative day and two samples of skin were collected from each rat with a 1-cm(2) punch to perform mast cell evaluations with toluidine blue dye.

Results: Statistically significant differences were found in the percentage of necrosis, and higher values were seen in group 1 than in all other groups. Among groups 3-7 no statistically significant differences were found (p < 0.292). For mast cells, when group 1 was compared to groups 5 (6 J/cm(2) at 1 point) and 7 (144 J/cm(2) at 1 point), it had fewer mast cells.

Conclusion: LLLT at a wavelength of 670 nm was effective at reducing the necrotic area, and we found that it can stimulate mast cells growth to increase vascular perfusion.
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http://dx.doi.org/10.1089/pho.2008.2295DOI Listing
April 2009

Experimental model for low level laser therapy on ischemic random skin flap in rats.

Acta Cir Bras 2006 Jul-Aug;21(4):258-62

Post-graduation Program in Plastic Surgery, Federal University of São Paulo, Rua Napoleão de Barros, 715/4 andar, 04024-900 São Paulo, SP, Brazil.

Purpose: To develop an experimental model to be used in the study of low level Laser therapy on viability of random skin flap in rats.

Methods: The sample was 24 Wistar-EPM rats. The random skin flap measured 10 x 4 cm and a plastic sheet was interposed between the flap and donor site. Group 1 (control) underwent sham irradiation with diode laser (830 nm). Group 2 was submitted to laser irradiation with diode laser (830 nm). The animals were submitted to Laser therapy with 36 J/cm(2) energy density (72 seconds) immediately after the surgery and on the four subsequent days. The probe was usually held in contact with the skin flap surface on a point at 2.5 cm cranial from the flap base. On the seventh postoperative day, the percentage of necrotic area was measured and calculated.

Results: Group 1 reached an average necrotic area of 48.86%, Group 2 - 23.14%. After the statistic analysis, compared with the control group, Group 2 showed a statistically significant increase in survival area (p<0.001).

Conclusion: The experimental model proved to be reliable to be used in the study of effects of low level laser therapy in random skin flap in rats.
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http://dx.doi.org/10.1590/s0102-86502006000400013DOI Listing
April 2007