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01-11-2018 | Original Article

Effect of photobiomodulation therapy on oxidative stress markers of gastrocnemius muscle of diabetic rats subjected to high-intensity exercise

Authors: Marcelo Frigero, Solange Almeida dos Santos, Andrey Jorge Serra, Caroline dos Santos Monteiro Machado, Leslie Andrews Portes, Paulo José Ferreira Tucci, Flavio Silva, Ernesto Cesar Leal-Junior, Paulo de Tarso Camillo de Carvalho

Published in: Lasers in Medical Science | Issue 8/2018

Abstract

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.

Gerasimou P, Nicolaidou V, Skordis N, Picolos M, Monos D, Costeas PA (2018) Combined effect of glutamine at position 70 of HLA-DRB1 and alanine at position 57 of HLA-DQB1 in type 1 diabetes: an epitope analysis. PLoS One 13:e0193684CrossRef

Pękala-Wojciechowska A, Poznański M, Szyszow K, Antczak A (2018) Concentration of 8-isoprostanes in the exhaled breath condensate as a marker of oxidative stress in patients with type 1 diabetes. Adv Respir Med 86:3–6CrossRef

Pouvreau C, Dayre A, Butkowski EG, de Jong B, Jelinek HF (2018) Inflammation and oxidative stress markers in diabetes and hypertension. J Inflamm Res 11:61–68CrossRef

Farinha JB, Krause M, Rodrigues-Krause J, Reischak-Oliveira A (2017) Exercise for type 1 diabetes mellitus management: general considerations and new directions. Med Hypotheses 104:147–153CrossRef

Finaud J, Lac G, Filaire E (2006) Oxidative stress: relationship with exercise and training. Sports Med 36:327–358CrossRef

Kennedy G, Spence VA, McLaren M, Hill A, Underwood C, Belch JJ (2005) Oxidative stress levels are raised in chronic fatigue syndrome and are associated with clinical symptoms. Free Radic Biol Med 39:584–589CrossRef

Allen MD, Kimpinski K, Doherty TJ, Rice CL (2015) Decreased muscle endurance associated with diabetic neuropathy may be attributed partially to neuromuscular transmission failure. J Appl Physiol 118:1014–1022CrossRef

Dos Santos SA, Dos Santos MAV, Simões MCB, Serra AJ, Leal-Junior EC, De Carvalho PTC (2017) Photobiomodulation therapy associated with treadmill training in the oxidative stress in a collagen-induced arthritis model. Lasers Med Sci 32:1071–1079CrossRef

Tuna Z, Duger T, Atalay-Guzel N, Aral A, BasTurk B, Haznedaroglu S, Goker B (2015) Aerobic exercise improves oxidant-antioxidant balance in patients with rheumatoid arthritis. J Phys Ther Sci 27:1239–1242CrossRef

10.

De Marchi T, Leal Junior ECP, Bortoli C, Tomazoni SS, Lopes-Martins RÁB, Salvador M (2012) Low-level laser therapy (LLLT) in human progressive-intensity running: effects on exercise performance, skeletal muscle status, and oxidative stress. Lasers Med Sci 27:231–236CrossRef

11.

Nonato LF, Rocha-Vieira R, Tossige-Gomes R, Soares AA, Soares BA, Freitas DA et al (2016) Swimming training attenuates oxidative damage and increases enzymatic but not non-enzymatic antioxidant defenses in the rat brain. Braz J Med Biol Res 49:e5310CrossRef

12.

Guaraldo SA, Serra AJ, Amadio EM, Antônio EL, Silva F, Portes LA, Tucci PJ, Leal-Junior EC, de Carvalho PT (2016) The effect of low-level laser therapy on oxidative stress and functional fitness in aged rats subjected to swimming: an aerobic exercise. Lasers Med Sci 31:833–840CrossRef

13.

Leal-Junior ECP (2015) Photobiomodulation therapy in skeletal muscle: from exercise performance to muscular dystrophies. Photomed Laser Surg 33:53–54CrossRef

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):181–214CrossRef

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 21:296–304CrossRef

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 31:1925–1933CrossRef

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 34:473–482CrossRef

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 30:3329–3338CrossRef

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 51:129–135CrossRef

20.

Hamblin MR (2017) Mechanisms and applications of the anti-inflammatory effects of photobiomodulation. AIMS Biophys 4:337–361CrossRef

21.

Tatmatsu-Rocha JC, Ferraresi C, Hamblin MR, Damasceno Maia F, do Nascimento NR, Driusso P, Parizotto NA (2016) Low-level laser therapy (904 nm) can increase collagen and reduce oxidative and nitrosative stress in diabetic wounded mouse skin. J Photochem Photobiol B 164:96–102CrossRef

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 CrossRefPubMed

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 32:429–437CrossRef

24.

Berkowitz BA, Luan H, Gupta RR, Pacheco D, Seidner A, Roberts R, Liggett J, Knoerzer DL, Connor JR, Du Y, Kern TS, Ito Y (2004) Regulation of the early subnormal retinal oxygenation response in experimental diabetes by inducible nitric oxide synthase. Diabetes 53:173–178CrossRef

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 15:210–216CrossRef

26.

Ho YJ, Lee AS, Chen WP, Chang WL, Tsai YK, Chiu HL et al (2014) Caffeic acid phenethyl amide ameliorates ischemia/reperfusion injury and cardiac dysfunction in streptozotocin-induced diabetic rats. Cardiovasc Diabetol 13:98CrossRef

27.

Baldari C, Bonavolontà V, Emerenziani GP, Gallotta MC, Silva AJ, Guidetti L (2009) Accuracy, reliability, linearity of Accutrend and Lactate Pro versus EBIO plus analyzer. Eur J Appl Physiol 107:105–111CrossRef

28.

Rocha RE, Coelho I, Pequito DC, Yamagushi A, Borghetti G, Yamazaki RK et al (2013) Interval training attenuates the metabolic disturbances in type 1 diabetes rat model. Arq Bras Endocrinol Metab 57:594–602CrossRef

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):1127–1134CrossRef

30.

De Melo BL, Vieira SS, Antônio EL, dos Santos LFN, Portes LA, Feliciano RS et al (2016) Exercise training attenuates right ventricular remodeling in rats with pulmonary arterial stenosis. Front Physiol 7:541CrossRef

31.

Weydert CJ, Cullen JJ (2010) Measurement of superoxide dismutase, catalase and glutathione peroxidase in cultured cells and tissue. Nat Protoc 5:51–66CrossRef

32.

Maritim AC, Sanders RA, Watkins JB 3rd. Diabetes, oxidative stress, and antioxidants: a review. J Biochem Mol Toxicol 17:24–38CrossRef

33.

Carolo dos Santos K, Pereira Braga C, Octavio Barbanera P, Seiva FR, Fernandes Junior A et al (2014) Cardiac energy metabolism and oxidative stress biomarkers in diabetic rat treated with resveratrol. PLoS One 9:e102775CrossRef

34.

Wohl P, Wohl P, Girman P, Pelikánová T (2004) Inflexibility of energy substrate oxidation in type 1 diabetic patients. Metabolism 53:655–659CrossRef

35.

Patrocinio T, Sardim AC, Assis L, Fernandes KR, Rodrigues N, Renno AC (2013) Effect of low-level laser therapy (808 nm) in skeletal muscle after resistance exercise training in rats. Photomed Laser Surg 31:492–498CrossRef

36.

Assis L, Yamashita F, Magri AM, Fernandes KR, Yamauchi L, Renno AC (2015) Effect of low-level laser therapy (808 nm) on skeletal muscle after endurance exercise training in rats. Braz J Phys Ther 19(6):457–465CrossRef

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 CrossRef

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 32:253CrossRef

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 40:524–532CrossRef

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 CrossRefPubMed

41.

Liu XG, Zhou YJ, Liu TC, Yuan JQ (2009) Effects of low-level laser irradiation on rat skeletal muscle injury after eccentric exercise. Photomed Laser Surg 27(6):863–869. https://doi.org/10.1089/pho.2008.2443 CrossRefPubMed

42.

Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O (2012) Oxidative stress and antioxidant defense. World Allergy Organ J 5:9–19CrossRef

43.

Biasibetti M, Rojas DB, Hentschke VS, Moura DJ, Karsten M, Wannmacher CM, Saffi J, Dal LP (2014) The influence of low-level laser therapy on parameters of oxidative stress and DNA damage on muscle and plasma in rats with heart failure. Lasers Med Sci 29:1895–1906CrossRef

44.

Leal-Junior EC, Lopes-Martins RA, de Almeida P, Ramos L, Iversen VV, Bjordal JM (2010) Effect of low-level laser therapy (GaAs 904 nm) in skeletal muscle fatigue and biochemical markers of muscle damage in rats. Eur J Appl Physiol 108:1083CrossRef

45.

Vieira Junior RC, Silva CMS, MBD A, Garcia A, Voltarelli VA, Reis Filho AD et al (2013) Aerobic swimming training increases the activity of antioxidant enzymes and the glycogen content in the skeletal muscle of rats. Rev Bras Med Esporte 19:204–208CrossRef

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 30:59–66CrossRef

47.

da Fonseca AS, Presta GA, Geller M, de Paoli F, Valença SS (2012) Low-intensity infrared laser increases plasma proteins and induces oxidative stress in vitro. Lasers Med Sci 27:211–217CrossRef

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 CrossRefPubMed

49.

Fillipin LI, Mauriz JL, Vedovelli K, Moreira AJ, Zettler CG, Lech O, Marroni NP, González-Gallego J (2005) Low-level laser therapy (LLLT) prevents oxidative stress and reduces fibrosis in rat traumatized Achilles tendon. Lasers Surg Med 37:293–300CrossRef

Title: Effect of photobiomodulation therapy on oxidative stress markers of gastrocnemius muscle of diabetic rats subjected to high-intensity exercise
Authors: Marcelo Frigero
Solange Almeida dos Santos
Andrey Jorge Serra
Caroline dos Santos Monteiro Machado
Leslie Andrews Portes
Paulo José Ferreira Tucci
Flavio Silva
Ernesto Cesar Leal-Junior
Paulo de Tarso Camillo de Carvalho
Publication date: 01-11-2018
Publisher: Springer London
Published in: Lasers in Medical Science / Issue 8/2018
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-018-2540-7

At a glance: The STEP trials

Springer Medicine

Effect of photobiomodulation therapy on oxidative stress markers of gastrocnemius muscle of diabetic rats subjected to high-intensity exercise

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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