Introduction
Photobiomodulation therapy (PBMT), also known as phototherapy, involves the use of monochromatic light sources for therapeutic purposes throughout nonthermal effects. Physiological and therapeutic effects provided by PBMT are due to photophysical and photochemical events generated after absorption of light energy by specific chromophores on cell mitochondria (especially cytochrome c oxidase, unit IV in the mitochondrial respiratory chain) (23 14,21 13,24,55 6,35,44,49,54,57 3,6,10,48,51 16,30,38,43,45 7,16,56
Mechanisms involved in the installation of the muscular fatigue process are not fully understood, but it is known that both central and peripheral factors are associated with a reduction in the capacity to generate force (2,20 23 23
Previous studies focused in PBMT effects on muscular fatigue have used different exercise protocols, such as constant-load exercises until exhaustion (15,31,36 5,6,12,39,49,52 38,43 30 5,52,57 22,27,42,50,57 5,6,10,31 27 22,49,50
All the above mentioned studies applied PBMT immediately before exercise protocol (6,22,31,36,38,42,49,50,54,57 19 19
Methods
Experimental Approach to the Problem
To determine the best time to apply PBMT before exercise, we used a crossover, randomized, double-blind, and placebo-controlled trial. Subjects were submitted to the same protocol in 5 sessions with different treatments (Figure 1 ): (a) control (without any treatment, always at first week); (b) placebo (placebo treatment applied both 6 hours before and immediately before the test); (c) 6 hours before + immediately before (PBMT applied both 6 hours before and immediately before the test); (d) 6 hours before (PBMT applied 6 hours before and placebo applied immediately before the test); and (e) immediately before (placebo applied 6 hours before and PBMT applied immediately before the test). Except for the control session, treatment order was determined by lot.
Figure 1.: Flowchart describing the study design. PBMT = photobiomodulation therapy; MIVC = maximal isometric voluntary contraction.
Two researchers were responsible for all the testing sessions, and they were blinded to subject's allocation to treatment. A third researcher with proper training and sufficient experience with a PBMT device was responsible for randomization and treatment application. This researcher was instructed not to inform the subjects or the other researchers regarding PBMT or placebo application. Subjects used opaque goggles that blocked their view during treatment application. Because PBMT does not cause any sensitive stimulus (e.g., warm, cold, itching, skin irritation, and pain), subjects were completely blinded to treatment order. The experiment followed a 5-day evaluation with intervals of 7–10 days between the testing sessions. All tests were performed in the afternoon (15:00–18:00 hours), exactly 6 hours after the PBMT/placebo application in the morning (9:00–12:00 hours). Subjects were instructed to avoid any vigorous activities in the lower limbs, alcohol, and coffee ingestion, approximately 24 hours before the testing sessions.
Subjects
Nineteen volunteers (± SD 26 ± 6 years old, 81 ± 12 kg, and 181 ± 7 cm) were initially included in this study. The following inclusion criteria were adopted: (a) physically active men; (b) age ranging between 18 and 35 years; (c) resistance training routine with at least 2 sessions per week in the last 6 months; (d) availability to finish the protocol at least in 5 weeks; and (e) during the study protocol (5 weeks) did not perform resistance training in the lower limbs. The exclusion criteria were as follows: presenting injuries (knee) in the last 2 months and coefficient variation for maximal isometric voluntary contraction (MIVC) higher than 10% between control and placebo condition. We had 3 losses throughout the experiment, and thus, 16 subjects (26 ± 6.0 years, 81 ± 12 kg, and 181 ± 7.4 cm) completed accordingly the full study protocol and were considered for analysis.
Flowchart describing the phases of the study and the subjects' engagement is shown in Figure 1 . All subjects were informed of the benefits and risks of the research before signing an informed consent document to participate in the study. Ethical approval was obtained from the Federal University of Santa Catarina's Human Research Ethics Committee (CAAE: 61599116.1.0000.0121), and the protocol was written in accordance with the standards set by the Declaration of Helsinki.
Procedures
Isokinetic Tests Data collection was performed between the months of June and August of 2016. During all testing sessions, subjects performed a familiarization and a warm-up protocol (20 knee extension-flexion concentric submaximal repetitions at 120°·s−1 ) using an isokinetic dynamometer (Biodex System 4 Pro; Biodex Medical Systems, Shirley, NY, USA). The subjects were positioned on the dynamometer according to the manufacturer's recommendations for the evaluation of knee extension-flexion movements. The right knee was evaluated. After the warm-up, subjects performed 3 attempts of 5-second knee extension MIVC (MIVCPRE ) at 70° of knee extension (0° = full knee extension). A 2-minute rest period was respected between trials. The highest peak torque value obtained among the 3 MIVCs was considered as the maximal isometric strength. In sequence, subjects performed a fatigue protocol in maximal effort involving one attempt of 45 repetitions for knee extension-flexion at 180°·s−1 with the range of motion at 70° (30°–100°, considering 0° = full knee extension). This protocol was similar to previous studies (5,57 POST ). The flowchart describing the testing session is summarized in Figure 1 . Torque signal was sampled at 100 Hz and smoothed using a fifth-order, zero-phase, and recursive low-pass Butterworth filter with a cutoff frequency of 10 Hz.
Muscle activation was assessed by means of surface electromyography (EMG) from vastus lateralis (VL), rectus femoris (RF), and vastus medialis (VM). The skin surface was shaved, debrided, and cleaned, followed by attachment of Delsys Trigno wireless electrodes (Trigno Wireless EMG; Delsys, Inc., Natick, MA, USA) over 3 muscles of the right lower limb. Electrodes were placed at an estimated point midway between the muscle insertion and innervation zone, along the longitudinal axis of the muscle as described by Basmajian and DeLuca (8
The RMS values of VL, RF, and VM were calculated for all protocols (MIVC and fatigue protocol). For MIVC analysis, the RMS sum (VL + RF + VM) was used to represent muscle activation of the quadriceps (RMSQUAD ). For fatigue protocol, the RMSQUAD was normalized by the RMSQUAD obtained during MIVCPRE (100%) (41 QUAD ) was calculated during MIVCPRE and MIVCPOST (40
Photobiomodulation Therapy/Placebo
Photobiomodulation therapy and placebo were applied with the Chattanooga Intellect Advanced 2766 equipment (Chattanooga Group, Guildford, United Kingdom) on knee extensor muscles. Treatments were applied in 9 sites over the quadriceps muscular group (Figure 2 ) with the probe maintained stationary and perpendicularly to the skin. Placebo application was exactly the same way, however with the equipment turned off.
Figure 2.: Photobiomodulation therapy parameters and application sites (black circles at the muscle).
Statistical Analyses
Data normality was verified using the Shapiro-Wilk test. Two-way analysis of variance (ANOVA) (treatment [control, placebo, 6 hours before + immediately before, 6 hours before, and immediately before] × time [before and after fatigue protocol]) was used to compare the absolute peak torque, RMSQUAD , and MFQUAD obtained during MIVCs. Repeated-measures ANOVA was used to compare the percent changes (MIVCPRE to MIVCPOST ) in peak torque, RMSQUAD , and MFQUAD . The same procedure was used to compare the subject's performance during isokinetic fatigue protocol. The LSD post hoc was used for all analyses. All statistical analyses were performed using IBM SPSS Statistics for Windows, version 21.0 (IBM Corp., Armonk, NY, USA). The significance level was set at α = 0.05.
Magnitude-based inference analyses were also used to examine practical significances. The magnitude of differences between groups (placebo vs. 6 hours before + immediately before; placebo vs. 6 hours before, and placebo vs. immediately before) was calculated and expressed as standardized mean differences. We adopted the criteria of Cohen (1988) for the analysis (>0.2: small; >0.50: moderate; and >0.80: large). The chances that the true (unknown) mean changes being trivial, positive, or negative (i.e., greater than the smallest worthwhile change [0.2 multiplied by the between-subjects' SD ]) were determined. Quantitative chances of a positive or negative effect were assessed qualitatively, as follows: <1% = most unlikely; 1–5% = very unlikely; 5–25% = unlikely; 25–75% = possibly; 75–95% = likely; 95–99% = very likely; and >99% = most likely. If the chances of positive and negative effects were both >5%, then the true difference was assessed as unclear (9
Results
Subjects had similar exercise performance during isokinetic fatigue protocol throughout the 5 conditions of the study (Table 1 ). When we look at MIVCPRE and MIVCPOST fatigue protocols, there was no treatment × time interaction for peak torque, RMSQUAD , and MFQUAD (Figure 3A, C, E , respectively). However, it was observed a time effect for peak torque, RMSQUAD , and MFQUAD for all treatments. While treatment effect was identified only for peak torque, the 6 hours before + immediately before treatment presented higher values than control (p = 0.004) and placebo (p = 0.044) treatment. In addition, immediately before treatment presented higher peak torque than control treatment (p = 0.047). Regarding MIVCPOST , peak torque for 6 hours before + immediately before presented higher values than control (p = 0.001) and placebo (p = 0.004) treatments.
Table 1.: Mean and SD of peak torque, work, and quadriceps activation (RMSQUAD ) from the start, middle, end, and overall of the isokinetic fatigue protocol (n = 16).
Figure 3.: Absolute and percent change values for peak torque, quadriceps muscle activation (RMSQUAD ), and quadriceps median frequency (MFQUAD ) during premaximal and postmaximal isometric voluntary contractions at the 5 different treatments. a Different from 6 hours before + immediately before (p ≤ 0.05).
Peak torque percent change between MIVCPRE and MIVCPOST presented lower decrease for 6 hours before + immediately before treatment (26%) compared with control (33%; p = 0.018), placebo (29%; p = 0.034), and immediately before (32%; p = 0.024) treatments (Figure 3B ). No treatment effect was observed for percent change in RMSQUAD (F = 1.35, p = 0.260; Figure 3D ) and MFQUAD (F = 0.47, p = 0.884; Figure 3F ).
Figure 4 summarizes the effect sizes of PBMT treatments compared with placebo treatment. The magnitude-based inference reported a likely positive effect only for isometric peak torque when PBMT was applied 6 hours before + immediately before.
Figure 4.: Effects of different photobiomodulation therapy treatments compared with placebo treatment on isometric peak torque, quadriceps muscle activation (RMSQUAD ), and quadriceps median frequency (MFQUAD ).
Discussion
The main purpose of this study was to identify the effects of different times for PBMT application (6 hours before and immediately before fatigue protocol) on torque parameters and muscle activation of knee extensors. Human studies have applied PBMT immediately or up to 10 minutes before exercise protocols (5,6,15,22,27,30,36,38,42,43,49,50,52,54,57 18,19
The isokinetic exercise protocol used in this study successfully induced fatigue on knee extensor muscles, as evidenced by reduced muscle strength and activation after exercise, as well as the expressive fatigue index measured within the exercise protocol. Photobiomodulation therapy/placebo treatments did not affect the subject's performance in the isokinetic exercise protocol (Table 1 ), similar to previous studies that assessed the PBMT effects on muscle fatigue of knee extensors (5,57 3,5,6,32,39,49 PRE and MIVCPOST fatigue protocols. In our study, subjects were treated with 1 or 2 active sessions of PBMT before MIVCPRE . However, the previous PBMT treatments seem to have had no effects on maximal strength or neuromuscular activation.
Although PBMT presented no ergogenic effect on maximal strength capacity, the association of treatments performed 6 hours before and immediately before the exercise promoted a lower drop on isometric peak torque values compared with control, placebo, and immediately before treatments. Photobiomodulation therapy applied only immediately before exercise, as traditionally used by studies in this field, did not affect the strength decrement during MIVCs, which contradicts findings from the previous studies with knee extensors (3,5,6,32,39
This study did not provide evidence on mechanisms responsible for improvement in torque. However, according to previous studies, the interaction of light with biological tissue involves the absorption of photons by endogenous chromophores and a consequent transduction of light energy into chemical energy in cytoplasmic organelles (11,17,47 17,23,26 37 17 33
Commonly, the reduction in RMS values after fatigue protocol involving concentric contractions has been reported by other authors (4,28,46 + , Mg2+ , H+ , and lactate) (1 53 Figure 3C ), without differences among treatments (Figure 3D ). Likewise, other studies have also shown no changes in RMS values between PBMT and placebo treatments after fatigue protocols (31,49
Contradictory results have been observed in the literature for PBMT effect on median frequency. Although some studies reported minor drop on MF with application of PBMT (42,57 22,49,50,54 42,57 4,40 29 Figure 4 ), there is no clear evidence that PBMT was able to change a recruitment pattern among fast- and slow-twitch fibers.
Although the increase in ATP production related to the PBMT has been well established in the literature (25,37 18 19 34
In summary, this study shows for the first time that a combination of preconditioning sessions with PBMT (270 J per quadriceps muscle) applied 6 hours before and immediately before a high-intensity exercise protocol is able to reduce the strength fall related to muscle levels in healthy and physically active subjects.
Practical Applications
Our findings confirm the positive effects of PBMT (270 J per quadriceps muscle) and recommend that combined applications 6 hours and immediately before exercise reduce the fatigue level in knee extensors submitted to a resistance exercise protocol. Strength and conditioning trainers should consider the combined approach of PBMT applied 6 hours and immediately before resistance exercise to optimize the subjects' performance.
Acknowledgments
The authors thank the National Council for Scientific and Technological Development (CNPq, Brazil) and Amazonas State Research Support Foundation (FAPEAM) for the financial support. The authors have no conflicts of interest to disclose.
References
1. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: Cellular mechanisms. Physiol Rev 88: 287–332, 2008.
2. Ament W, Verkenke G. Exercise and fatigue. Sport Med 39: 389–422, 2009.
3. Antonialli FC, De Marchi T, Tomazoni SS, Vanin AA, dos Santos Grandinetti V, de Paiva PRV, Pinto HD, Miranda EF, De Carvalho PTC, Leal Junior ECP. 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, 2014.
4. Babault N, Desbrosses K, Fabre MS, Michaut A, Pousson M. Neuromuscular fatigue development during maximal concentric and isometric knee extensions. J Appl Physiol 100: 780–785, 2006.
5. Baroni BM, Leal Junior ECP, Geremia JM, Diefenthaeler F, Vaz MA. Effect of light-emitting diodes therapy (LEDT) on knee extensor muscle fatigue. Photomed Laser Surg 28: 653–658, 2010.
6. Baroni BM, Leal Junior ECP, De Marchi T, Lopes AL, Salvador M, Vaz MA. Low level laser therapy before eccentric exercise reduces muscle damage markers in humans. Eur J Appl Physiol 110: 789–796, 2010.
7. Baroni BM, Rodrigues R, Freire BB, Franke Rde A, Geremia JM, Vaz MA. Effect of low-level laser therapy on muscle adaptation to knee extensor eccentric training. Eur J Appl Physiol 115: 639–647, 2014.
8. Basmajian J, De Luca C. Muscle Alive (5th ed.). Baltimore, MD: Lippincott Williams & Wilkins, 1985.
9. Batterham AM, Hopkins WG. Making meaningful inferences about magnitudes. Int J Sports Physiol Perform 1: 50–57, 2006.
10. Borges LS, Cerqueira MS, Dos Santos Rocha JA, Conrado LAL, Machado M, Pereira R, Pinto Neto O. Light-emitting diode phototherapy improves muscle recovery after a damaging exercise. Lasers Med Sci 29: 1139–1144, 2014.
11. Borsa PA, Larkin KA, True JM. Does phototherapy enhance skeletal muscle contractile function and postexercise recovery? A systematic review. J Athl Train 48: 57–67, 2013.
12. De Brito Vieira WH, Ferraresi C, De Andrade Perez SE, Baldissera V, Parizotto NA. 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, 2012.
13. Enwemeka CS, Parker JC, Dowdy DS, Harkness EE, Sanford LE, Woodruff LD. The efficacy of low-power lasers in tissue repair and pain control: A meta-analysis study. Photomed Laser Surg 22: 323–329, 2004.
14. Enwemeka CS. Intricacies of dose in laser phototherapy for tissue repair and pain relief. Photomed Laser Surg 27: 1–7, 2009.
15. Ferraresi C, Beltrame T, Fabrizzi F, Nascimento ESP, Karsten M, Francisco CO, Borghi-Silva A, Catai AM, Cardoso DR, Ferreira AG, Hamblin MR, Bagnato VS, Parizotto NA. Muscular pre-conditioning using light-emitting diode therapy (LEDT) for high-intensity exercise: A randomized double-blind placebo-controlled trial with a single elite runner. Physiother Theor Pract 14: 1–8, 2015.
16. Ferraresi C, De Brito Oliveira T, De Oliveira Zafalon L, De Menezes Reiff RB, Baldissera V, De Andrade Perez SE, Júnior EM, Parizotto NA. Effects of low level laser therapy (808 nm) on physical strength training in humans. Lasers Med Sci 26: 349–358, 2011.
17. Ferraresi C, Hamblin MR, Parizotto NA. Low-level laser (light) therapy (LLLT) on muscle tissue: Performance, fatigue and repair benefited by the power of light. Photonics Lasers Med 1: 267–286, 2012.
18. Ferraresi C, Kaippert B, Avci P, Huang YY, De Sousa MVP, Bagnato VS, Parizotto NA, Hamblin MA. Low-level laser (light) therapy increases mitochondrial membrane potential and ATP synthesis in C2C12 myotubes with a peak response at 3–6 h. Photochem Photobiol 91: 411–416, 2015.
19. Ferraresi C, de Sousa MVP, Huang YY, Bagnato VS, Parizotto NA, Hamblin MR. Time response of increases in ATP and muscle resistance to fatigue after low-level laser (light) therapy (LLLT) in mice. Lasers Med Sci 30: 1259–1267, 2015.
20. Gandevia SC. Some central and peripheral factors affecting human motoneuronal output in neuromuscular fatigue. Sports Med 13: 93–98, 1992.
21. Hamblin M. Mechanisms and applications of the anti-inflammatory effects of photobiomodulation. AIMS Biophys 4: 337–361, 2017.
22. Higashi RH, Toma RL, Tucci HT, Pedroni CR, Ferreira PD, Baldini GS, Avairo MC, Borghi-Silva A, De Oliveira AS, Renno ACM. Effects of low-level laser therapy on biceps braquialis muscle fatigue in young women. Photomed Laser Surg 31: 586–594, 2013.
23. Huang Y-Y, Sharma SK, Carroll J, Hamblin MR. Biphasic dose response in low level light therapy—An update. Dose Response 9: 602–618, 2011.
24. Huang Z, Chen J, Ma J, Shen B, Pei F, Kraus VB. Effectiveness of low-level laser therapy in patients with knee osteoarthritis: A systematic review and meta-analysis. Osteoarthritis Cartilage 23: 1437–1444, 2015.
25. Karu T. Primary and secondary mechanisms of action of visible to near-IR radiation on cells. J Photochem Photobiol B 49: 1–17, 1999.
26. Karu TI. Multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life 62: 607–610, 2010.
27. Kelencz CA, Muñoz ISS, Amorim CF, Nicolau RA. Effect of low-power gallium-aluminum-arsenium noncoherent light (640 nm) on muscle activity: A clinical study. Photomed Laser Surg 28: 647–652, 2010.
28. Komi PV, Tesch P. EMG frequency spectrum, muscle structure, and fatigue during dynamic contractions in man. Eur J Appl Physiol Occup Physiol 42: 41–50, 1979.
29. Kupa EJ, Roy SH, Kandarian SC, De Luca CJ. Effects of muscle fiber type and size on EMG median frequency and conduction velocity. J Appl Physiol 79: 23–32, 1995.
30. Lanferdini FJ, Bini RR, Baroni BM, Klein KD, Carpes FP, Vaz MA. Low-level laser therapy improves performance and reduces fatigue in competitive cyclists. Int J Sports Physiol Perform 2017. Epub ahead of print.
31. Larkin-Kaiser KA, Borsa PA, Baweja HS, Moore MA, Tillman MD, George SZ, Christou EA. Photobiomodulation delays the onset of skeletal muscle fatigue in a dose-dependent manner. Lasers Med Sci 31: 1325–1332, 2016.
32. Larkin-Kaiser KA, Christou E, Tillman M, George S, Borsa PA. Near-infrared light therapy to attenuate strength loss after strenuous resistance exercise. J Athl Train 50: 45–50, 2015.
33. Larkin KA, Martin JS, Zeanah EH, True JM, Braith RW, Borsa PA. Limb blood flow after class 4 laser therapy. J Athl Train 47: 178–183, 2012.
34. Leal-Junior ECP, Vanin AA, Miranda EF, de Carvalho Pde TC, Dal Corso S, Bjordal JM. Effect of phototherapy (low-level laser therapy and light-emitting diode therapy) on exercise performance and markers of exercise recovery: A systematic review with meta-analysis. Lasers Med Sci 30: 925–939, 2015.
35. Leal ECP, Lopes-Martins RÁB, Rossi RP, De Marchi T, Baroni BM, De Godoi V, Marcos RL, Ramos L, Bjordal JM. Effect of cluster multi-diode light emitting diode therapy (LEDT) on exercise-induced skeletal muscle fatigue and skeletal muscle recovery in humans. Lasers Surg Med 41: 572–577, 2009.
36. Malta EDS, De Poli RAB, Brisola GMP, Milioni F, Miyagi WE, Machado FA, Zagatto AM. Acute LED irradiation does not change the anaerobic capacity and time to exhaustion during a high-intensity running effort: A double-blind, crossover, and placebo-controlled study: Effects of LED irradiation on anaerobic capacity and performance in running. Lasers Med Sci 31: 1473–1480, 2016.
37. Manteifel VM, Karu TI. Structure of mitochondria and activity of their respiratory chain in successive generations of yeast cells exposed to He-Ne laser light. Biol Bull 32: 556–566, 2005.
38. De Marchi T, Leal ECP, Bortoli C, Tomazoni SS, Lopes-Martins RÁB, Salvador M. Low-level laser therapy (LLLT) in human progressive-intensity running: Effects on exercise performance, skeletal muscle status, and oxidative stress. Lasers Med Sci 27: 231–236, 2012.
39. De Marchi T, Schmitt VM, Danúbia da Silva Fabro C, da Silva LL, Sene J, Tairova O, Salvador M, Leal-Junior ECP. Phototherapy for improvement of performance and exercise recovery: Comparison of 3 commercially available devices. J Athl Train 52: 429–438, 2017.
40. Merletti R, Lo Conte LR. Surface EMG signal processing during isometric contractions. J Electromyogr Kinesiol 7: 241–250, 1997.
41. Merletti R, Parker P. Electromyography: Physiology, Engineering, and Noninvasive Applications. Hoboken, NJ: Wiley-Interscience, 2004.
42. Miranda EF, Leal-Junior ECP, Marchetti PH, Dal Corso S. Acute effects of light emitting diodes therapy (LEDT) in muscle function during isometric exercise in patients with chronic obstructive pulmonary disease: Preliminary results of a randomized controlled trial. Lasers Med Sci 29: 359–365, 2014.
43. Miranda EF, Vanin AA, Tomazoni SS, Dos Santos Grandinetti V, De Paiva PRV, Dos Santos Monteiro Machado C, Monteiro KK, Casalechi HL, de Tarso P, de Carvalho C, Leal-Junior EC. Using pre-exercise photobiomodulation therapy combining super-pulsed lasers and light-emitting diodes to improve performance in progressive cardiopulmonary exercise tests. J Athl Train 51: 129–135, 2016.
44. Paolillo FR, Corazza AV, Paolillo AR, Borghi-Silva A, Arena R, Kurachi C, Bagnato VS. Phototherapy during treadmill training improves quadriceps performance in postmenopausal women. Climacteric 17: 285–293, 2014.
45. Paolillo FR, Corazza AV, Borghi-Silva A, Parizotto NA, Kurachi C, Bagnato VS. 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, 2013.
46. Pasquet B, Carpentier A, Duchateau J, Hainaut K. Muscle fatigue during concentric and eccentric contractions. Muscle Nerve 23: 1727–1735, 2000.
47. Reddy GK. Photobiological basis and clinical role of low-intensity lasers in biology and medicine. J Clin Laser Med Surg 22: 141–150, 2004.
48. Rizzi CF, Mauriz JL, Correa DSF, Moreira AJ, Zettler CG, Filippin LI, Marroni NP, González-Gallego J. Effects of low-level laser therapy (LLLT) on the nuclear factor (NF)-κB signaling pathway in traumatized muscle. Lasers Surg Med 38: 704–713, 2006.
49. Rossato M, Dellagrana RA, Lanferdini FJ, Sakugawa RL, Lazzari CD, Baroni BM, Diefenthaeler F. Effect of pre-exercise phototherapy applied with different cluster probe sizes on elbow flexor muscle fatigue. Lasers Med Sci 31: 1237–1244, 2016.
50. Dos Santos Maciel T, Muñoz ISS, Nicolau RA, Nogueira DV, Hauck LA, Osório RAL, de Paula Júnior AR. Phototherapy effect on the muscular activity of regular physical activity practitioners. Lasers Med Sci 29: 1145–1152, 2014.
51. Silveira PCL, Scheffer DDL, Glaser V, Remor AP, Pinho RA, Aguiar Junior AS, Latini A. Low-level laser therapy attenuates the acute inflammatory response induced by muscle traumatic injury. Free Radic Res 50: 503–513, 2016.
52. de Souza CGCG, Borges DT, de Brito Macedo L, Brasileiro JSS. Low-level laser therapy reduces the fatigue index in the ankle plantar flexors of healthy subjects. Lasers Med Sci 31: 1949–1955, 2016.
53. Taylor JL, Butler JE, Gandevia SC. Changes in muscle afferents, motoneurons and motor drive during muscle fatigue. Eur J Appl Physiol 83: 106–115, 2000.
54. Toma RL, Tucci HT, Antunes HKM, Pedroni CR, De Oliveira AS, Buck I, Ferreira PD, Vassão PG, Renno AC. Effect of 808 nm low-level laser therapy in exercise-induced skeletal muscle fatigue in elderly women. Lasers Med Sci 28: 1375–1382, 2013.
55. Tumilty S, Munn J, McDonough S, Hurley DA, Basford JR, Baxter GD. Low level laser treatment of tendinopathy: A systematic review with meta-analysis. Photomed Laser Surg 28: 3–16, 2010.
56. Vanin AA, Miranda EF, Machado CSM, de Paiva PRV, Albuquerque-Pontes GM, Casalechi HL, de Tarso CCP, Leal-Junior EC. What is the best moment to apply phototherapy when associated to a strength training program? A randomized, double-blinded, placebocontrolled trial: Phototherapy in association to strength training. Lasers Med Sci 31: 1555–1564, 2016.
57. Vassão PG, Toma RL, Antunes HKMM, Tucci HT, Renno ACMM. Effects of photobiomodulation on the fatigue level in elderly women: An isokinetic dynamometry evaluation. Lasers Med Sci 31: 275–282, 2016.
