Effect of photobiomodulation therapy on oxidative stress markers of gastrocnemius muscle of diabetic rats subjected to high-intensity exercise
This study aimed to determine whether photobiomodulation therapy (PBMT) in diabetic rats subjected to high-intensity exercise interferes with the expression of the oxidative stress marker in the gastrocnemius muscle. Twenty-four male Wistar rats were included in this study comprising 16 diabetic and eight control rats. The animals were allocated into three groups—control, diabetic fatigue, and diabetic PBMT fatigue groups. Diabetes was induced via the intraperitoneal administration of streptozotocin (50 mg/kg). We subsequently assessed blood lactate levels and PBMT. The animals of the diabetic fatigue group PBMT were irradiated before the beginning of the exercises, with dose of 4 J and 808 nm, were submitted to treadmill running with speed and gradual slope until exhaustion, as observed by the maximum volume of oxygen and lactate level. The animals were euthanized and muscle tissue was removed for analysis of SOD markers, including catalase (CAT), glutathione peroxidase (GPx), and 2-thiobarbituric acid (TBARS) reactive substances. CAT, SOD, and GPx activities were significantly higher in the diabetic PBMT fatigue group (p < 0.05) than in the diabetic fatigue group. Outcomes for the diabetic PBMT fatigue group were similar to those of the control group (p > 0.05), while their antioxidant enzymes were significantly higher than those of the diabetic fatigue group. PBMT mitigated the TBARS concentration (p > 0.05). PBMT may reduce oxidative stress and be an alternative method of maintaining physical fitness when subjects are unable to perform exercise. However, this finding requires further testing in clinical studies.
KeywordsType 1 diabetes Photobiomodulation therapy Oxidative stress High-intensity exercise
Role of the funding source
This work was supported by grants from the São Paulo Research Foundation (FAPESP, grant number (2015/13677-4) and the National Council for Scientific and Technological (grant number 309065/2015-1).
Compliance with ethical standards
All experimental procedures were performed in accordance with the standards established by the Brazilian College for Animal Experimentation. The animals were handled in compliance with the national guidelines for the humane treatment of laboratory animals, and the UNINOVE Research Ethics Committee approved all experimental procedures (approval number CEUA-AN0035.2014).
Conflict of interest
No competing financial interests exist. Professor Ernesto Cesar Pinto Leal-Junior receives research support from Multi Radiance Medical (Solon, OH-USA), a laser device manufacturer. Multi Radiance Medical had no role in the planning of this study, and the laser device used was not theirs. They had no influence on study design, data collection and analysis, decision to publish, or preparation of the manuscript. The remaining authors declare that they have no conflict of interests.
- 14.Vanin AA, Verhagen E, Barboza SD, Oliveira Pena Costa L, Leal-Junior ECP (2017) Photobiomodulation therapy for the improvement of muscular performance and reduction of muscular fatigue associated with exercise in healthy people: a systematic review and meta-analysis. Lasers Med Sci 33(1):181–214CrossRefGoogle Scholar
- 15.Machado AF, Micheletti JK, Vanderlei FM, Nakamura FY, Leal-Junior ECP, Netto J Jr, Pastre CM (2017) Effect of low-level laser therapy (LLLT) and light-emitting diodes (LEDT) applied during combined training on performance and post-exercise recovery: protocol for a randomized placebo-controlled trial. Braz J Phys Ther 21:296–304CrossRefGoogle Scholar
- 16.De Paiva PRV, Tomazoni SS, Johnson DS, Vanin AA, Albuquerque-Pontes GM, dos Santos Monteiro Machado C et al (2016) Photobiomodulation therapy (PBMT) and/or cryotherapy in skeletal muscle restitution, what is better? A randomized, double-blinded, placebo-controlled clinical trial. Lasers Med Sci 31:1925–1933CrossRefGoogle Scholar
- 17.Vanin AA, De Marchi T, Tomazoni SS, Tairova O, Casalechi HL, de Carvalho P d C et al (2016) Pre-exercise infrared low-level laser therapy (810 nm) in skeletal muscle performance and post exercise recovery in humans. What is the optimal dose? A randomized, double-blind, placebo-controlled clinical trial. Photomed Laser Surg 34:473–482CrossRefGoogle Scholar
- 18.Pinto HD, Vanin AA, Miranda EF, Tomazoni SS, Johnson DS, Albuquerque-Pontes GM et al (2016) Photobiomodulation therapy improves performance and accelerates recovery of high-level rugby players in field test: a randomized, crossover, double-blind, placebo controlled clinical study. J Strength Cond Res 30:3329–3338CrossRefGoogle Scholar
- 19.Miranda EF, Vanin AA, Tomazoni SS, dos Santos GV, de Paiva PRV, dos Santos Monteiro Machado C et al (2016) Using pre-exercise photobiomodulation therapy combining super-pulsed lasers and light-emitting diodes to improve performance in progressive cardiopulmonary exercise tests. J Athl Train 51:129–135CrossRefGoogle Scholar
- 22.de Oliveira AR, Vanin AA, Tomazoni SS, Miranda EF, Albuquerque-Pontes GM, De Marchi T et al (2017) Pre-exercise infrared photobiomodulation therapy (810nm) in skeletal muscle performance and postexercise recovery in humans: what is the optimal power output? Photomed Laser Surg 35(11):595–603. https://doi.org/10.1089/pho.2017.4343 CrossRefPubMedGoogle Scholar
- 23.De Marchi T, Schmitt VM, Machado GP, Sene JS, de Col CD, Tairova O et al (2017) Does photobiomodulation therapy is better than cryotherapy in muscle recovery after a high-intensity exercise? A randomized, double-blind, placebo-controlled clinical trial. Lasers Med Sci 32:429–437CrossRefGoogle Scholar
- 25.Aparecida Da Silva A, Leal-Junior EC, Alves AC, Rambo CS, Dos Santos SA, Vieira RP et al (2013) Wound-healing effects of low-level laser therapy in diabetic rats involve the modulation of MMP-2 and MMP-9 and the redistribution of collagen types I and III. J Cosmet Laser Ther 15:210–216CrossRefGoogle Scholar
- 29.Amadio EM, Serra AJ, Guaraldo SA, Silva JA Jr, Antônio EL, Silva F et al (2015) The action of pre-exercise low-level laser therapy (LLLT) on the expression of IL-6 and TNF-α proteins and on the functional fitness of elderly rats subjected to aerobic training. Lasers Med Sci 30(3):1127–1134CrossRefGoogle Scholar
- 37.Miranda EF, Tomazoni SS, de Paiva PRV, Pinto HD, Smith D, Santos LA, de Carvalho P d C, Leal-Junior ECP (2017) When is the best moment to apply photobiomodulation therapy (PBMT) when associated to a treadmill endurance-training program? A randomized, triple-blinded, placebo-controlled clinical trial. Lasers Med Sci 29. https://doi.org/10.1007/s10103-017-2396-2 CrossRefGoogle Scholar
- 38.Vanin AA, Miranda EF, Machado CS, de Paiva PR, Albuquerque-Pontes GM, Casalechi HL, de Carvalho P d C, Leal-Junior EC (2016) What is the best moment to apply phototherapy when associated to a strength training program? A randomized, double-blinded, placebo-controlled trial: Phototherapy in association to strength training. Lasers Med Sci 31:1555–1564 Erratum: 2017 Lasers Med Sci 32:253CrossRefGoogle Scholar
- 39.Leal Junior EC, Lopes-Martins RA, Frigo L, De Marchi T, Rossi RP, de Godoi V et al (2010) Effects of low-level laser therapy (LLLT) in the development of exercise-induced skeletal muscle fatigue and changes in biochemical markers related to postexercise recovery. J Orthop Sports Phys Ther 40:524–532CrossRefGoogle Scholar
- 40.Santos LA, Marcos RL, Tomazoni SS, Vanin AA, Antonialli FC, Grandinetti Vdos S, Albuquerque-Pontes GM, de Paiva PR, Lopes-Martins RÁ, de Carvalho PT, Bjordal JM, Leal-Junior EC (2014) Effects of pre-irradiation of low-level laser therapy with different doses and wavelengths in skeletal muscle performance, fatigue, and skeletal muscle damage induced by tetanic contractions in rats. Lasers Med Sci 29(5):1617–1626. https://doi.org/10.1007/s10103-014-1560-1 CrossRefPubMedGoogle Scholar
- 46.Albuquerque-Pontes GM, Vieira Rde P, Tomazoni SS, Caires CO, Nemeth V, Vanin AA et al (2015) Effect of pre-irradiation with different doses, wavelengths, and application intervals of low-level laser therapy on cytochrome C oxidase activity in intact skeletal muscle of rats. Lasers Med Sci 30:59–66CrossRefGoogle Scholar
- 48.Silva AA, Leal-Junior EC, D'Avila Kde A, Serra AJ, Albertini R, França CM, Nishida JA, de Carvalho Pde T (2015) Pre-exercise low-level laser therapy improves performance and levels of oxidative stress markers in mdx mice subjected to muscle fatigue by high-intensity exercise. Lasers Med Sci 30(6):1719–1727. https://doi.org/10.1007/s10103-015-1777-7 CrossRefPubMedGoogle Scholar