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Erschienen in: Lasers in Medical Science 5/2017

21.04.2017 | Original Article

Photobiomodulation therapy associated with treadmill training in the oxidative stress in a collagen-induced arthritis model

verfasst von: Solange Almeida dos Santos, Marcia Ataize dos Santos Vieira, Maira Cécilia Brandão Simões, Andrey Jorge Serra, Ernesto Cesar Leal-Junior, Paulo de Tarso Camillo de Carvalho

Erschienen in: Lasers in Medical Science | Ausgabe 5/2017

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Abstract

Rheumatoid arthritis (RA) is a chronic inflammatory disease characterized by chronic and systemic inflammation, which leads to the destruction of the cartilage and bone and affects tissues in multiple joints. Oxidative stress has been implicated with regards to involvement in various disease conditions, such as diabetes mellitus and neurodegenerative, respiratory, cardiovascular, and RA diseases. In vivo experimental studies using photobiomodulation therapy (PBMT) have shown positive effects in reducing lipid peroxidation and in increasing antioxidant activity. The regular practice of physical exercise has also been reported to be a beneficial treatment capable of reducing oxidative damage. Thus, the aim of this study was to analyze the effects of photobiomodulation therapy at 2- and 4-J doses associated with physical exercise on oxidative stress in an experimental model of RA in protein expression involving superoxide dismutase (SOD), glutathione peroxidase (GPX), and/or catalase (CAT) on thiobarbituric acid reactive substances (TBARS). In this study, 24 male Wistar rats divided into four groups were submitted to an RA model (i.e., collagen-induced arthritis, CIA), with the first immunization performed at the base of the tail on days 0 and 7 were included. After 28 days, a third intraarticular dose was administered in both knees of the animals. After the last induction, PBMT was started immediately, transcutaneously at two points (i.e., the medial and lateral), with a total of 15 applications. Treadmill exercise was also started the day after the last induction, and lasted for 5 weeks. With respect to results, we obtained the decreases in the lipid peroxidation and the increases of the antioxidant activities of SOD, GPX and CAT, with physical exercise associated to PBMT in doses of 2 and 4 J. In conclusion, physical exercise associated with PBMT decreases lipid peroxidation and increases antioxidant activity.
Literatur
1.
Zurück zum Zitat Hadi V, Kheirouri S, Alizadeh M, Khabbazi A, Hosseini H (2016) Effects of Nigella sativa oil extract on inflammatory cytokine response and oxidative stress status in patients with rheumatoid arthritis: a randomized, double-blind, placebo-controlled clinical trial. Avicenna J Phytomed 6:34–43PubMedPubMedCentral Hadi V, Kheirouri S, Alizadeh M, Khabbazi A, Hosseini H (2016) Effects of Nigella sativa oil extract on inflammatory cytokine response and oxidative stress status in patients with rheumatoid arthritis: a randomized, double-blind, placebo-controlled clinical trial. Avicenna J Phytomed 6:34–43PubMedPubMedCentral
2.
Zurück zum Zitat Lu QY, Han QH, Li X, Li ZC, Pan YT, Liu L, Fu QG (2014) Analysis of differentially expressed genes between rheumatoid arthritis and osteoarthritis based on the gene co-expression network. Mol Med Rep 10:119–124. doi:10.3892/mmr.2014.2166 PubMed Lu QY, Han QH, Li X, Li ZC, Pan YT, Liu L, Fu QG (2014) Analysis of differentially expressed genes between rheumatoid arthritis and osteoarthritis based on the gene co-expression network. Mol Med Rep 10:119–124. doi:10.​3892/​mmr.​2014.​2166 PubMed
4.
Zurück zum Zitat Khojah HM, Ahmed S, Abdel-Rahman MS, Hamza AB (2016) Reactive oxygen and nitrogen species in patients with rheumatoid arthritis as potential biomarkers for disease activity and the role of antioxidants. Free Radic Biol Med S0891-5849:30308–30302. doi:10.1016/j.freeradbiomed.2016.06.020 Khojah HM, Ahmed S, Abdel-Rahman MS, Hamza AB (2016) Reactive oxygen and nitrogen species in patients with rheumatoid arthritis as potential biomarkers for disease activity and the role of antioxidants. Free Radic Biol Med S0891-5849:30308–30302. doi:10.​1016/​j.​freeradbiomed.​2016.​06.​020
8.
Zurück zum Zitat He F, Li J, Liu Z, Chuang CC, Yang W, Zuo L (2016) Redox mechanism of reactive oxygen species in exercise. Front Physiol 7:486PubMedPubMedCentral He F, Li J, Liu Z, Chuang CC, Yang W, Zuo L (2016) Redox mechanism of reactive oxygen species in exercise. Front Physiol 7:486PubMedPubMedCentral
9.
Zurück zum Zitat Ji LL (1999) Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med 222:283–292CrossRefPubMed Ji LL (1999) Antioxidants and oxidative stress in exercise. Proc Soc Exp Biol Med 222:283–292CrossRefPubMed
11.
Zurück zum Zitat 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 31:833–840. doi:10.1007/s10103-016-1882-2 CrossRefPubMed 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 31:833–840. doi:10.​1007/​s10103-016-1882-2 CrossRefPubMed
12.
Zurück zum Zitat Leal-Junior EC, Vanin AA, Miranda EF, de Carvalho PT, Dal Corso S, Bjordal JM (2015) 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. doi:10.1007/s10103-013-1465-4 CrossRefPubMed Leal-Junior EC, Vanin AA, Miranda EF, de Carvalho PT, Dal Corso S, Bjordal JM (2015) 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. doi:10.​1007/​s10103-013-1465-4 CrossRefPubMed
13.
Zurück zum Zitat Leal Junior EC, Lopes-Martins RA, Frigo L, De Marchi T, Rossi RP, de Godoi V, Tomazoni SS, Silva DP, Basso M, Filho PL, de Valls Corsetti F, Iversen VV, Bjordal JM (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 40:524–532. doi:10.2519/jospt.2010.3294 CrossRefPubMed Leal Junior EC, Lopes-Martins RA, Frigo L, De Marchi T, Rossi RP, de Godoi V, Tomazoni SS, Silva DP, Basso M, Filho PL, de Valls Corsetti F, Iversen VV, Bjordal JM (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 40:524–532. doi:10.​2519/​jospt.​2010.​3294 CrossRefPubMed
14.
Zurück zum Zitat de Almeida P, Lopes-Martins RA, De Marchi T, Tomazoni SS, Albertini R, Corrêa JC, Rossi RP, Machado GP, da Silva DP, Bjordal JM, Leal Junior EC (2012) Red (660 nm) and infrared (830 nm) low-level laser therapy in skeletal muscle fatigue in humans: what is better? Lasers Med Sci 27:453–458. doi:10.1007/s10103-011-0957-3 CrossRefPubMed de Almeida P, Lopes-Martins RA, De Marchi T, Tomazoni SS, Albertini R, Corrêa JC, Rossi RP, Machado GP, da Silva DP, Bjordal JM, Leal Junior EC (2012) Red (660 nm) and infrared (830 nm) low-level laser therapy in skeletal muscle fatigue in humans: what is better? Lasers Med Sci 27:453–458. doi:10.​1007/​s10103-011-0957-3 CrossRefPubMed
15.
Zurück zum Zitat Sussai DA, Carvalho Pde T, Dourado DM, Belchior AC, dos Reis FA, Pereira DM (2010) Low-level laser therapy attenuates creatine kinase levels and apoptosis during forced swimming in rats. Lasers Med Sci 25:115–120. doi:10.1007/s10103-009-0697-9 CrossRefPubMed Sussai DA, Carvalho Pde T, Dourado DM, Belchior AC, dos Reis FA, Pereira DM (2010) Low-level laser therapy attenuates creatine kinase levels and apoptosis during forced swimming in rats. Lasers Med Sci 25:115–120. doi:10.​1007/​s10103-009-0697-9 CrossRefPubMed
16.
Zurück zum Zitat 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 29:1617–1626. doi:10.1007/s10103-014-1560-1 CrossRefPubMed 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 29:1617–1626. doi:10.​1007/​s10103-014-1560-1 CrossRefPubMed
17.
Zurück zum Zitat 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(4):293–300CrossRefPubMed 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(4):293–300CrossRefPubMed
18.
Zurück zum Zitat Firat ET, Dağ A, Günay A, Kaya B, Karadede Mİ, Ersöz Kanay B, Ketani A, Evliyaoğlu O, Uysal E (2014) The effect of low-level laser therapy on the healing of hard palate mucosa and the oxidative stress status of rats. J Oral Pathol Med 43:103–110. doi:10.1111/jop.12106 CrossRefPubMed Firat ET, Dağ A, Günay A, Kaya B, Karadede Mİ, Ersöz Kanay B, Ketani A, Evliyaoğlu O, Uysal E (2014) The effect of low-level laser therapy on the healing of hard palate mucosa and the oxidative stress status of rats. J Oral Pathol Med 43:103–110. doi:10.​1111/​jop.​12106 CrossRefPubMed
19.
Zurück zum Zitat Servetto N, Cremonezzi D, Simes JC, Moya M, Soriano F, Palma JA, Campana VR (2010) Evaluation of inflammatory biomarkers associated with oxidative stress and histological assessment of low-level laser therapy in experimental myopathy. Lasers Surg Med 42:577–583. doi:10.1002/lsm.20910 CrossRefPubMed Servetto N, Cremonezzi D, Simes JC, Moya M, Soriano F, Palma JA, Campana VR (2010) Evaluation of inflammatory biomarkers associated with oxidative stress and histological assessment of low-level laser therapy in experimental myopathy. Lasers Surg Med 42:577–583. doi:10.​1002/​lsm.​20910 CrossRefPubMed
20.
Zurück zum Zitat Tomazoni SS, Leal-Junior EC, Frigo L, Pallotta RC, Teixeira S, de Almeida P, Bjordal JM, Lopes-Martins RÁ (2016) Isolated and combined effects of photobiomodulationtherapy, topical nonsteroidal anti-inflammatory drugs, and physical activity in the treatment of osteoarthritis induced by papain. J Biomed Opt 21:108001. doi:10.1117/1.JBO.21.10.108001 CrossRefPubMed Tomazoni SS, Leal-Junior EC, Frigo L, Pallotta RC, Teixeira S, de Almeida P, Bjordal JM, Lopes-Martins RÁ (2016) Isolated and combined effects of photobiomodulationtherapy, topical nonsteroidal anti-inflammatory drugs, and physical activity in the treatment of osteoarthritis induced by papain. J Biomed Opt 21:108001. doi:10.​1117/​1.​JBO.​21.​10.​108001 CrossRefPubMed
21.
Zurück zum Zitat Tomazoni SS, Leal-Junior EC, Pallotta RC, Teixeira S, de Almeida P, Lopes-Martins RÁ (2017) Effects of photobiomodulation therapy, pharmacological therapy, and physical exercise as single and/or combined treatment on the inflammatory response induced by experimental osteoarthritis. Lasers Med Sci 32:101–108. doi:10.1007/s10103-016-2091-8 CrossRefPubMed Tomazoni SS, Leal-Junior EC, Pallotta RC, Teixeira S, de Almeida P, Lopes-Martins RÁ (2017) Effects of photobiomodulation therapy, pharmacological therapy, and physical exercise as single and/or combined treatment on the inflammatory response induced by experimental osteoarthritis. Lasers Med Sci 32:101–108. doi:10.​1007/​s10103-016-2091-8 CrossRefPubMed
22.
Zurück zum Zitat Silva AA, Leal-Junior EC, D’Avila Kde A, Serra AJ, Albertini R, França CM, Nishida JA, de Carvalho PT (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 30:1719–1727. doi:10.1007/s10103-015-1777-7 CrossRefPubMed Silva AA, Leal-Junior EC, D’Avila Kde A, Serra AJ, Albertini R, França CM, Nishida JA, de Carvalho PT (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 30:1719–1727. doi:10.​1007/​s10103-015-1777-7 CrossRefPubMed
24.
Zurück zum Zitat dos Santos SA, Alves AC, Leal-Junior EC, Albertini R, Vieira RP, Ligeiro AP, Junior JA, de Carvalho PT (2014) Comparative analysis of two low-level laser doses on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Lasers Med Sci 29:1051–1058. doi:10.1007/s10103-013-1467-2 CrossRefPubMed dos Santos SA, Alves AC, Leal-Junior EC, Albertini R, Vieira RP, Ligeiro AP, Junior JA, de Carvalho PT (2014) Comparative analysis of two low-level laser doses on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Lasers Med Sci 29:1051–1058. doi:10.​1007/​s10103-013-1467-2 CrossRefPubMed
25.
Zurück zum Zitat Tang T, Muneta T, Young-Jin J, Nimura A, Miyazaki K, Masuda H, Mochizuki T, Sekiya I (2008) Serum keratan sulfate transiently increases in the early stage of osteoarthritis during strenuous running of rats: protective effect of intraarticular hyaluronan injection. Arthritis Res Ther 10:R13. doi:10.1186/ar2363 CrossRefPubMedPubMedCentral Tang T, Muneta T, Young-Jin J, Nimura A, Miyazaki K, Masuda H, Mochizuki T, Sekiya I (2008) Serum keratan sulfate transiently increases in the early stage of osteoarthritis during strenuous running of rats: protective effect of intraarticular hyaluronan injection. Arthritis Res Ther 10:R13. doi:10.​1186/​ar2363 CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Alves AC, Vieira R, Leal-Junior E, dos Santos S, Ligeiro AP, Albertini R, Junior J, de Carvalho P (2013) Effect of low-level laser therapy on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Arthritis Res Ther. doi:10.1186/ar4296 PubMedPubMedCentral Alves AC, Vieira R, Leal-Junior E, dos Santos S, Ligeiro AP, Albertini R, Junior J, de Carvalho P (2013) Effect of low-level laser therapy on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Arthritis Res Ther. doi:10.​1186/​ar4296 PubMedPubMedCentral
27.
Zurück zum Zitat Wang P, Liu C, Yang X, Zhou Y, Wei X, Ji Q, Yang L, He C (2014) Effects of low-level laser therapy on joint pain, synovitis, anabolic, and catabolic factors in a progressive osteoarthritis rabbit model. Lasers Med Sci 29:1875–1885. doi:10.1007/s10103-014-1600-x CrossRefPubMed Wang P, Liu C, Yang X, Zhou Y, Wei X, Ji Q, Yang L, He C (2014) Effects of low-level laser therapy on joint pain, synovitis, anabolic, and catabolic factors in a progressive osteoarthritis rabbit model. Lasers Med Sci 29:1875–1885. doi:10.​1007/​s10103-014-1600-x CrossRefPubMed
28.
Zurück zum Zitat Guo H, Luo Q, Zhang J, Lin H, Xia L, He C (2011) Comparing different physical factors on serum TNF-α levels, chondrocyte apoptosis, caspase-3 and caspase-8 expression in osteoarthritis of the knee in rabbits. Joint Bone Spine 78:604–610. doi:10.1016/j.jbspin.2011.01.009 CrossRefPubMed Guo H, Luo Q, Zhang J, Lin H, Xia L, He C (2011) Comparing different physical factors on serum TNF-α levels, chondrocyte apoptosis, caspase-3 and caspase-8 expression in osteoarthritis of the knee in rabbits. Joint Bone Spine 78:604–610. doi:10.​1016/​j.​jbspin.​2011.​01.​009 CrossRefPubMed
29.
Zurück zum Zitat Alves AC, Albertini R, dos Santos SA, Leal-Junior EC, Santana E, Serra AJ, Silva JA Jr, de Carvalho PT (2014) Effect of low-level laser therapy on metalloproteinase MMP-2 and MMP-9 production and percentage of collagen types I and III in a papain cartilage injury model. Lasers Med Sci 29:911–919. doi:10.1007/s10103-013-1427-x CrossRefPubMed Alves AC, Albertini R, dos Santos SA, Leal-Junior EC, Santana E, Serra AJ, Silva JA Jr, de Carvalho PT (2014) Effect of low-level laser therapy on metalloproteinase MMP-2 and MMP-9 production and percentage of collagen types I and III in a papain cartilage injury model. Lasers Med Sci 29:911–919. doi:10.​1007/​s10103-013-1427-x CrossRefPubMed
30.
32.
Zurück zum Zitat Alves AC, de Carvalho PT, Parente M, Xavier M, Frigo L, Aimbire F, Leal Junior EC, Albertini R (2013) Low-level laser therapy in different stages of rheumatoid arthritis: a histological study. Lasers Med Sci 28:529–536. doi:10.1007/s10103-012-1102-7 CrossRefPubMed Alves AC, de Carvalho PT, Parente M, Xavier M, Frigo L, Aimbire F, Leal Junior EC, Albertini R (2013) Low-level laser therapy in different stages of rheumatoid arthritis: a histological study. Lasers Med Sci 28:529–536. doi:10.​1007/​s10103-012-1102-7 CrossRefPubMed
33.
Zurück zum Zitat Ribeiro BG, Alves AN, dos Santos LA, Cantero TM, Fernandes KPS, Dias Dda S, Bernardes N, De Angelis K, Mesquita-Ferrari RA (2016) Red and infrared low-level laser therapy prior to injury with or without administration after injury modulate oxidative stress during the muscle repair process. PLoS One 11:e0153618. doi:10.1371/journal.pone.0153618 CrossRefPubMedPubMedCentral Ribeiro BG, Alves AN, dos Santos LA, Cantero TM, Fernandes KPS, Dias Dda S, Bernardes N, De Angelis K, Mesquita-Ferrari RA (2016) Red and infrared low-level laser therapy prior to injury with or without administration after injury modulate oxidative stress during the muscle repair process. PLoS One 11:e0153618. doi:10.​1371/​journal.​pone.​0153618 CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Biasibetti M, Rojas DB, Hentschke VS, Moura DJ, Karsten M, Wannmacher CM, Saffi J, Dal Lago P (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(6):1895–1906. doi:10.1007/s10103-014-1597-1 CrossRefPubMed Biasibetti M, Rojas DB, Hentschke VS, Moura DJ, Karsten M, Wannmacher CM, Saffi J, Dal Lago P (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(6):1895–1906. doi:10.​1007/​s10103-014-1597-1 CrossRefPubMed
35.
Zurück zum Zitat De Marchi T, Leal Junior EC, Bortoli C, Tomazoni SS, Lopes-Martins RA, 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 27:231–236. doi:10.1007/s10103-011-0955-5 CrossRefPubMed De Marchi T, Leal Junior EC, Bortoli C, Tomazoni SS, Lopes-Martins RA, 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 27:231–236. doi:10.​1007/​s10103-011-0955-5 CrossRefPubMed
36.
Zurück zum Zitat Nonato LF, Rocha-Vieira E, Tossige-Gomes R, Soares AA, Soares BA, Freitas DA, Oliveira MX, Mendonca VA, Lacerda AC, Massensini AR, Leite HR (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:e5310. doi:10.1590/1414-431X20165310 CrossRefPubMedPubMedCentral Nonato LF, Rocha-Vieira E, Tossige-Gomes R, Soares AA, Soares BA, Freitas DA, Oliveira MX, Mendonca VA, Lacerda AC, Massensini AR, Leite HR (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:e5310. doi:10.​1590/​1414-431X20165310 CrossRefPubMedPubMedCentral
37.
Zurück zum Zitat Yamazaki M, Kusano K, Ishibashi T, Kiuchi M, Koyama K (2015) Intravenous infusion of H2-saline suppresses oxidative stress and elevates antioxidant potential in thoroughbred horses after racing exercise. Sci Rep 5:15514 DOi: 10.1038/srep15514. Yamazaki M, Kusano K, Ishibashi T, Kiuchi M, Koyama K (2015) Intravenous infusion of H2-saline suppresses oxidative stress and elevates antioxidant potential in thoroughbred horses after racing exercise. Sci Rep 5:15514 DOi: 10.​1038/​srep15514.
38.
Zurück zum Zitat Mazzola PN, Terra M, Rosa AP, Mescka CP, Moraes TB, Piccoli B, Jacques CE, Dalazen G, Cortes MX, Coelho J, Dutra-Filho CS (2011) Regular exercise prevents oxidative stress in the brain of hyperphenylalaninemic rats. Metab Brain Dis 26:291–297CrossRefPubMed Mazzola PN, Terra M, Rosa AP, Mescka CP, Moraes TB, Piccoli B, Jacques CE, Dalazen G, Cortes MX, Coelho J, Dutra-Filho CS (2011) Regular exercise prevents oxidative stress in the brain of hyperphenylalaninemic rats. Metab Brain Dis 26:291–297CrossRefPubMed
39.
Zurück zum Zitat Pinho RA, Silveira PCL, Piazza M, Tuon T, Slva GA, Dal-Pizzol F, Moreira JCF (2006) Exercício físico regular diminui o estresse oxidativo pulmonar em ratos após exposição aguda ao carvão mineral. Rev Bras Med Esporte 12(2):81–84. doi:10.1590/S1517-86922006000200005 CrossRef Pinho RA, Silveira PCL, Piazza M, Tuon T, Slva GA, Dal-Pizzol F, Moreira JCF (2006) Exercício físico regular diminui o estresse oxidativo pulmonar em ratos após exposição aguda ao carvão mineral. Rev Bras Med Esporte 12(2):81–84. doi:10.​1590/​S1517-8692200600020000​5 CrossRef
40.
Zurück zum Zitat Pinho WL, Rebelo da Silva AP (2013) Efeitos do exercício físico sobre a formação de espécies reativas de oxigênio e os compostos antioxidantes da dieta. Revista Brasileira de Nutrição Esportiva, São Paulo 7:77–87 Pinho WL, Rebelo da Silva AP (2013) Efeitos do exercício físico sobre a formação de espécies reativas de oxigênio e os compostos antioxidantes da dieta. Revista Brasileira de Nutrição Esportiva, São Paulo 7:77–87
41.
Zurück zum Zitat Silveira PCL, Silva LA, Tuon T, Freitas TP, Streck EL, Pinho RA (2009) Effects of low-level laser therapy on epidermal oxidative response induced by wound healing. Rev Bras Fisioter 13:281–287CrossRef Silveira PCL, Silva LA, Tuon T, Freitas TP, Streck EL, Pinho RA (2009) Effects of low-level laser therapy on epidermal oxidative response induced by wound healing. Rev Bras Fisioter 13:281–287CrossRef
42.
Zurück zum Zitat Carvalho JL, de Brito AA, de Oliveira A, de Castro Faria Neto HC, Pereira TM, de Carvalho RA, Anatriello E, Aimbire F (2016) The chemokines secretion and the oxidative stress are targets of low-level laser therapy in allergic lung inflammation. J Biophotonics 9:1208–1221CrossRefPubMed Carvalho JL, de Brito AA, de Oliveira A, de Castro Faria Neto HC, Pereira TM, de Carvalho RA, Anatriello E, Aimbire F (2016) The chemokines secretion and the oxidative stress are targets of low-level laser therapy in allergic lung inflammation. J Biophotonics 9:1208–1221CrossRefPubMed
43.
Zurück zum Zitat Assis L, Moretti AI, Abrahão TB, Cury V, Souza HP, Hamblin MR, Parizotto NA (2012) Low-level laser therapy (808 nm) reduces inflammatory response and oxidative stress in rat tibialis anterior muscle after cryolesion. Lasers Surg Med 44:726–735CrossRefPubMedPubMedCentral Assis L, Moretti AI, Abrahão TB, Cury V, Souza HP, Hamblin MR, Parizotto NA (2012) Low-level laser therapy (808 nm) reduces inflammatory response and oxidative stress in rat tibialis anterior muscle after cryolesion. Lasers Surg Med 44:726–735CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Huang YY, Nagata K, Tedford CE, McCarthy T, Hamblin MR (2013) Low-level laser therapy (LLLT) reduces oxidative stress in primary cortical neurons in vitro. J Biophotonics 6:829–838PubMed Huang YY, Nagata K, Tedford CE, McCarthy T, Hamblin MR (2013) Low-level laser therapy (LLLT) reduces oxidative stress in primary cortical neurons in vitro. J Biophotonics 6:829–838PubMed
Metadaten
Titel
Photobiomodulation therapy associated with treadmill training in the oxidative stress in a collagen-induced arthritis model
verfasst von
Solange Almeida dos Santos
Marcia Ataize dos Santos Vieira
Maira Cécilia Brandão Simões
Andrey Jorge Serra
Ernesto Cesar Leal-Junior
Paulo de Tarso Camillo de Carvalho
Publikationsdatum
21.04.2017
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 5/2017
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-017-2209-7

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