Brazilian Journal of Pain
https://brjp.org.br/article/doi/10.5935/2595-0118.20220035-en
Brazilian Journal of Pain
Original Article

Effect of photobiomodulation therapy (660 nm and 830 nm) on carrageenan-induced edema and pain behavior in mice

Efeito da terapia por fotobiomodulação (660 nm e 830 nm) no comportamento da dor e edema induzidos por carragenina em camundongos

Alexandre Marcio Marcolino; Ketlyn Germann Hendler; Rafael Inacio Barbosa; Lais Mara Siqueira das Neves; Heloyse Uliam Kuriki; Rafael Cypriano Dutra

http://dx.doi.org/10.5935/2595-0118.20220035-en BrJP, vol.5, n3, p.206-212, 2022
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Abstract

BACKGROUND AND OBJECTIVES: Photobiomodulation (PBM) is an important therapeutic tool for inflammatory process modulation. In this study, the anti-inflammatory and analgesic effect of two different energies and two different wavelengths (660 nm and 830 nm) were investigate and compared through the model of carrageenan-induced paw edema in mice.

METHODS: Male Swiss mice, 36 animals (n=6 animals/group) were divided into six groups: Group 1 (saline-control), Group 2 (carrageenan), Group 3 (carrageenan + laser 660 nm, 5.88 J), Group 4 (carrageenan + laser 660 nm, 2.94 J), Group 5 (carrageenan + laser 830 nm, 5.88 J), and Group 6 (carrageenan + laser 830 nm, 2.94 J). PBM was applied 1h after the carrageenan injection which induced paw edema and hyperalgesia, which were measured by means of a plethysmometer and by flicker test using a water bath at 38ºC (±0.5ºC), respectively. Left paws of mice injected with carrageenan exhibited local edema that persisted for up to 6h after its administration. All animals were evaluated before, 1, 2, 3, 4, and 6 h after the injection of carrageenan.

RESULTS: PBM, specially the 830 nm wavelength with 2.94 J of energy, reduced the paw edema induced by carrageenan. In addition, the 660 nm wavelengths (5.88 J / 2.94 J) and 830 nm (2.94 J) inhibited thermal hyperalgesia induced by carrageenan after 4 h of paw injection.

CONCLUSION: There was evidence that the PBM 830 nm (2.94 J) produced a more pronounced anti-inflammatory effect, while the 660 nm (5.88 J / 2.94 J) energy laser was more effective to inhibit the hyperalgesia response induced by the carrageenan injection.

HIGHLIGHTS

  • The present study demonstrated that PBM was effective in minimizing pain and edema in the acute inflammatory process in an experimental model.
  • The 830 nm wavelength (5.88 J energy) was more effective in improving edema in the acute inflammatory process in an experimental model.
  • In pain analysis, the energy of 2.94 J was more effective regardless of the wavelength used in the acute inflammatory process in an experimental model.

Keywords

Edema, Hyperalgesia, Inflammation, Low level laser therapy, Pain.

Resumo

JUSTIFICATIVA E OBJETIVOS: A fotobiomodulação (FBM) é uma importante ferramenta terapêutica para modulação dos processos inflamatórios. Neste estudo, investigou-se o efeito anti-inflamatório e analgésico de duas energias e dois comprimentos de onda diferentes (660 nm e 830 nm) através do modelo de edema de pata induzido por carragenina em camundongos.

MÉTODOS: Trinta e seis camundongos Swiss machos (n=6 animais/grupo) foram divididos em seis grupos: Grupo 1 (controle salino), Grupo 2 (carragenina), Grupo 3 (carragenina + laser 660 nm, 5,88 J), Grupo 4 (carragenina + laser 660 nm, 2,94 J), Grupo 5 (carragenina + laser 830 nm, 5,88 J) e Grupo 6 (carragenina + laser 830 nm, 2,94 J). A FBM foi aplicada 1h após a injeção de carragenina que induziu o edema de pata e a hiperalgesia térmica, os quais foram medidos por meio de um pletismômetro e pelo flicker test em banho-maria a 38ºC (±0,5ºC), respectivamente. As patas esquerdas injetadas com carragenina apresentaram edema local que persistiu por até 6h após sua administração. Todos os animais foram avaliados antes, 1, 2, 3, 4, e 6 horas após a injeção de carragenina.

RESULTADOS: A FBM, principalmente o comprimento de onda 830 nm com 2,94 J de energia, reduziu o edema de pata induzido pela carragenina. Além disso, o comprimento de onda 660 nm (5,88 J / 2,94 J) e o 830 nm (2,94 J) inibiram a hiperalgesia térmica induzida pela carragenina após 4h da injeção na pata.

CONCLUSÃO: Evidenciou-se que a FBM 830 nm (2,94 J) produziu efeito anti-inflamatório mais pronunciado, enquanto o laser de 660 nm (5,88 J / 2,94 J) de energia foi mais eficaz para reduzir a resposta de hiperalgesia induzida pela injeção de carragenina.

DESTAQUES

  • O presente estudo demonstrou que a PBM foi eficaz minimizando a dor e o edema no processo inflamatório agudo em um modelo experimental. 
  • O comprimento de onda 830 nm (energia de 5,88 J) foi mais eficaz na melhora do edema no processo inflamatório agudo em um modelo experimental.
  • Na análise da dor, a energia de 2,94 J foi mais eficaz independente do comprimento de onda utilizado no processo inflamatório agudo em um modelo experimental.

Palavras-chave

Dor, Terapia a Laser de baixa intensidade, Edema, Hiperalgesia, Inflamação, Carragenina.

References

Geremia A, Biancheri P, Allan P, Corazza GR, Di Sabatino A. Innate and adaptive immunity in inflammatory bowel disease. Autoimmun Rev. 2014;13(1):3-10.

Noah TA, Zachary MW, Randy JN. Inflammation: mechanisms, costs, and natural variation. Ann Rev Ecology Evolut Systemat. 2012;43:385-406.

Janeway Jr CA. Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harbor Symp Quant Biol. 1989;54Pt:1-13.

Michel CC, Curry FE. Microvascular permeability. Physiol Rev. 1999;79(3):703-61.

Albertine R, Villaverde AB, Aimbire F, Salgado MA, Bjordal JM, Alves LP, Munin E, Costa MS. Anti-inflammatory effects of low-level laser therapy (LLLT) with two different red wavelengths (660 nm and 684 nm) in carrageenan-induced rat paw edema. J Photochem Photobiol B. 2007;89(1):50-5.

Albertini R, Villaverde AB, Aimbire F, Bjordal J, Brugnera A, Mittmann J, Silva M, Costa M. Cytokine mRNA expression is decreased in the subplantar muscle of rat paw subjected to carrageenan-induced inflammation after low-level laser therapy. Photomed Laser Surg. 2008;26(1):19-24.

Gomes RP, Bressan E, Silva TM, Gevaerd MS, Tonussi CR, Domenech SC. Efeitos de um minuto e dez minutos de deambulação em ratos com artrite induzida por adjuvante completo de Freund sobre os sintomas de dor e edema. Rev Bras Reumatol. 2014;54(2):83-9.

Chan CC, Boyce S, Brideau C, Ford-Hutchinson AW, Gordon R, Guay D, Hill RG, Li CS, Mancini J, Penneton M. Pharmacology of a selective cyclooxygenase-2 inhibitor, L-745,337: a novel nonsteroidal anti-inflammatory agent with an ulcerogenic sparing effect in rat and non human primate stomach. J Pharmacol Exp Ther. 1995;274(3):1531-7.

Khanna IK, Weier RM, Yu Y, Collins PW, Miyashiro JM, Koboldt CM, Veenhuizen AW, Currie JL, Seibert K, Isakson PC. 1,2-Diarylpyrroles as potent and selective inhibitors of cyclooxygenase-2. J Med Chem. 1997;40(11):1619-33.

Riendeau D, Percival MD, Boyce S, Brideau C, Charlston S, Cromlish W. Biochemical and pharmacological profile of a tetrasubstituted furanone as a highly selective COX-2 inhibitor. Br J Pharmacol. 1997;121(1):105-17.

Zhang Y, Shaffer A, Portanova J, Seibert K, Isakson PC. Inhibition of cyclooxygenase-2 rapidly reverses inflammatory hyperalgesia and prostaglandin E2 production. J Pharmacol Exp Ther. 1997;283(3):1069-75.

Cuzzocrea S, Sautebin L, De Sarro G, Costantino G, Rombolà L, Mazzon E, Ialenti A, De Sarro A, Ciliberto G, Di Rosa M, Caputi AP, Thiemermann C. Role of IL-6 in the pleurisy and lung injury caused by carrageenan. J Immunol. 1999;163(9):5094-104.

Morris CJ. Carrageenan-induced paw edema in the rat and mouse. Methods Mol Biol. 2003;225:115-21.

Abd El-Rahman RS, Suddek GM, Gameil NM, El-kashef HA. Protective potential of MMR vaccine against complete Freund’s adjuvant-induced inflammation in rats. Inflammopharmacology. 2011;19(6):343-8.

Bhalekar MR, Upadhaya PG, Nalawade SD, Madgulkar AR, Kshirsagar SJ. Anti-rheumatic activity of chloroquine-SLN gel on wistar rats using complete freund’s adjuvant (CFA) model. Indian J Rheumatol. 2015;10(1):58-64.

Seibert K, Zhang Y, Leahy K., Hauser S., Masferrer J, Perkins W, Lee L, Isakson P. Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain. Proc Natl Acad Sci USA. 1994;91(25):12013-7.

Portanova JP, Zhang Y, Anderson GD, Hauser SD, Masferrer JL, Seibert K, Gregory AS, Isakson PC. Selective neutralization of prostaglandin E2 blocks inflammation, hyperalgesia, and interleukin 6 production in vivo. J Exp Med. 1996;184(3):883-91.

Sun S, Yin Y, Yin X, Cao F, Luo D, Zhang T, Li Y, Nia L. Anti-nociceptive effects of Tanshinone IIA (TIIA) in a rat model of complete Freund’s adjuvant (CFA)-induced inflammatory pain. Brain Res Bull. 2012;88(6):581-8.

Barbosa RI, Marcolino AM, de Jesus Guirro RR, Mazzer N, Barbieri CH, de Cássia Registro Fonseca M. Comparative effects of wavelengths of low-power laser in regeneration of sciatic nerve in rats following crushing lesion. Lasers Med Sci. 2010;25(3):423-30.

Baroni BM, Rodrigues R, Freire BB, Franke RA, Geremia JM, Vaz MA. Effect of low-level laser therapy on muscle adaptation to knee extensor eccentric training. Eur J Appl Physiol. 2015;115(3):639-47.

Leal-Junior EC, Vanin AA, Miranda EF, de Carvalho Pde T, 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. 2015;30(2):925-39.

Marcolino AM, Barbosa RI, das Neves LM, Mazzer N, de Jesus Guirro RR, de Cássia Registro Fonseca M. Assessment of functional recovery of sciatic nerve in rats submitted to low-level laser therapy with different fluences. An experimental study: laser in functional recovery in rats. J Hand Microsurg. 2013;5(2):49-53.

das Neves LM, Marcolino AM, Prado RP, Ribeiro Tde S, Pinfildi CE, Thomazini JA. Low-level laser therapy on the viability of skin flap in rats subjected to deleterious effect of nicotine. Photomed Laser Surg. 2011;29(8):581-7.

Canever JB, Barbosa RI, Hendler KG, Neves LMSD, Kuriki HU, Aguiar Júnior AS, Fonseca MCR, Marcolino AM. Effects of photobiomodulation on different application points and different phases of complex regional pain syndrome type I in a experimental model. Korean J Pain. 2021;34(3):250-61.

Albertini R., Aimbire FS, Correa FI, Ribeiro W, Cogo JC, Antunes E, Teixeira SA, De Nucci G, Castro-Faria Neto HC, Zângaro RA, Lopes-Martins RA. Effects of different protocol doses of low power gallium-aluminum-arsenate (Ga-Al-As) laser radiation (650 nm) on carrageenan induced rat paw ooedema. J Photochem Photobiol B. 2004;74(2-3):101-7.

Fukuda TY, Tanji MM, Jesus JF, Sato MN, Duarte AJ, Plapler H. Single session to infrared low level diode laser on tnf-a and il-6 cytokines release by mononuclear spleen cells in mice: a pilot study. Lasers Surg Med. 2010;42(6):584-8.

Fukuda TY, Tanji MM, Silva SR, Sato MN, Plapler H. Infrared low-level diode laser on inflammatory process modulation in mice: pro and anti-inflammatory cytokines. Lasers Med Sci. 2013;28(5):1305-13.

Alves AC, Vieira R, Leal Junior E, dos Santos S, Ligeiro AP, Albertini R, Junior R, de Carvalho P. Effect of low-level laser therapy on the expression of inflammatory mediators and on neutrophils and macrophages in acute joint inflammation. Arthritis Res Ther. 2013;15(5):R116.

Oliveira RG, Ferreira AP, Côrtes AJ, Aarestrup BJ, Andrade LC, Aarestrup FM. Low-level laser reduces the production of TNF-a, IFN-γ, and IL-10 induced by OVA. Lasers Med Sci. 2013;28(6):1519-25.

Mantineo M, Pinheiro JP, Morgado AM. Low-level laser therapy on skeletal muscle inflammation: evaluation of irradiation parameters. J Biomed Opt. 2014;19(9):098002.

Farivar S, Malekshahabi T, Shiari R. Biological effects of low level laser therapy. J Lasers Med Sci. 2014;5(2):58-62.

Chow R. LLLT Treatment of Pain: Clinical Applications* Chap 17. 265 - 286. Low-Level Light Therapy: Photobiomodulation. Tutorial Texts in Optical Engineering Volume TT115; Ed. 2018:390.

Chow R, Armati P, Laakso L, Bjordal JM, Baxter GD. Inhibitory effects of laser irradiation on peripheral mammalian nerves and relevance to analgesic effects: a systematic review. Photomed Laser Surg. 2011;29(6):365-81.

Yan W, Chow R, Armati PJ. Inhibitory effects of visible 650-nm and infrared 808-nm laser irradiation on somatosensory and compound muscle action potentials in rat sciatic nerve: implications for laser-induced analgesia. J Peripher Nerv Syst. 2011;16(2):130-5.

Aimbire F, Albertini R, Pacheco MT, Castro-Faria-Neto HC, Leonardo PS, Iversen VV, Lopes Martins RA, Bjordal IM. Low-level laser therapy induces dose-dependent reduction of TNFalpha levels in acute inflammation. Photomed Laser Surg. 2006;24(1):33-7.

Bjordal JM, Johnson MI, Iversen V, Aimbire F, Lopes-Martins RA. Low-level laser therapy in acute pain: a systematic review of possible mechanisms of action and clinical effects in randomized placebo-controlled trials. Photomed Laser Surg. 2006;24(2):158-68.

Chagas LR, Silva Jr JA, de Almeida Pires J, Costa MS. Expression of mPGES-1 and IP mRNA is reduced by LLLT in both subplantar and brain tissues in the model of peripheral inflammation induced by carrageenan. Lasers Med Sci. 2015;30(1):83-8.

Bortone F, Santos HA, Albertini R, Pesquero JB, Costa MS, Silva Jr JA. Low level laser therapy modulates kinin receptors mRNA expression in the subplantar muscle of rat paw subjected to carrageenan-induced inflammation. Int Immunopharmacol. 2008;8(2):206-10.

Neves LMS, Gonçalves ECD, Cavalli J, Vieira G, Laurindo LR, Simões RR, Coelho IS, Santos ARS, Marcolino AM, Cola M, Dutra RC. Photobiomodulation therapy improves acute inflammatory response in mice: the role of cannabinoid receptors/ATP-sensitive K+ channel/p38-MAPK signalling pathway. Mol Neurobiol. 2018;55(7):5580-93.

Prianti Jr AC, Silva Jr JA, Dos Santos RF, Rosseti IB, Costa MS. Low-level laser therapy (LLLT) reduces the COX-2 mRNA expression in both subplantar and total brain tissues in the model of peripheral inflammation induced by administration of carrageenan. Lasers Med Sci. 2014;29(4):1397-403.

Laraia EM, Silva IS, Pereira DM, dos Reis FA, Albertini R, de Almeida P, Leal Junior EC, de Tarso Camillo de Carvalho P. Effect of low-level laser therapy (660 nm) on acute inflammation induced by tenotomy of achilles tendon in rats. Photochem Photobiol. 2012;88(6):1546-50.

Meneguzzo DT, Lopes LA, Pallota R, Soares-Ferreira L, Lopes-Martins RA, Ribeiro MS. Prevention and treatment of mice paw edema by near-infrared low-level laser therapy on lymph nodes. Lasers Med Sci. 2013;28(3):973-80.

Mazuqueli Pereira ESB, Basting RT, Abdalla HB, Garcez AS, Napimoga MH, Clemente-Napimoga JT. Photobiomodulation inhibits inflammation in the temporomandibular joint of rats. J Photochem Photobiol B. 2021;222:112281.

de Souza Costa M, de Brito TV, de Oliveira SB, Souza Brauna I, Mazulo Neto JCR, Teles RHG, Dutra YM, de Aguiar Magalhães D, Sousa SG, de Sousa JA, Branco CERC, Hazime FA, Reis Barbosa AL, Vasconcelos DFP, Medeiros JVR, de Carvalho Filgueiras M. Photobiomodulation exerts anti-inflammatory effects on the vascular and cellular phases of experimental inflammatory models. Lasers Med Sci. 2022;37(1):563-71.

Silva MP, Bortone F, Silva MP, Araújo TR, Costa MS, Silva Júnior JA. Inhibition of carrageenan-induced expression of tissue and plasma prekallikreins mRNA by low level laser therapy in a rat paw edema model. Rev Bras Fisioter. 2011;15(1):1-7.

de Vasconcelos DI, Leite JA, Carneiro LT, Piuvezam MR, de Lima MR, de Morais LC. Anti-inflammatory and antinociceptive activity of ouabain in mice. Mediators Inflamm. 2011;2011:912925.

Ferreira DM, Zângaro RA, Villaverde AB, Cury Y, Frigo L, Picolo G. Analgesic effect of he-ne (632.8 nm) low-level laser therapy on acute inflammatory pain. Photomed Laser Surg. 2005;23(2):177-81.

Pallotta RC, Bjordal JM, Frigo L, Leal Junior EC, Teixeira S, Marcos RL, Messias Fde M, Lopes-Martins RA. Infrared (810-nm) low-level laser therapy on rat experimental knee inflammation. Lasers Med Sci. 2012;27(1):71-8.

Assis L, Milares LP, Almeida T, Tim C, Magri A, Fernandes KR, Medalha C, Renno AC. Aerobic exercise training and low-level laser therapy modulate inflammatory response and degenerative process in an experimental model of knee osteoarthritis in rats. Osteoarthritis Cartilage. 2015;24(1):169-77.

Hochman B, Pinfildi CE, Nishioka MA, Furtado F, Bonatti S, Monteiro PK, Antunes AS, Quieregatto PR, Liebano RE, Chadi G, Ferreira FM. Low-level laser therapy and light-emitting diode effects in the secretion of neuropeptides SP and CGRP in rat skin. Lasers Med Sci. 2014;29(3):1203-8.

Dompe C, Moncrieff L, Matys J, Grzech-Lesniak K, Kocherova I, Bryja A, Bruska M, Dominiak M, Mozdziak P, Skiba THI, Shibli JA, Angelona Volponi A, Kempisty B, Dyszkiewicz-Konwinska M. Photobiomodulation - underlying mechanism and clinical applications. J Clin Med. 2020;9(6):1724.

Hamblin MR, Ferraresi C, Huang Y, de Freitas LF, Carroll JD. Low-Level Light Therapy: Photobiomodulation. Tutorial Texts in Optical Engineering Volume TT115; Ed. 2018:390.

Bjordal JM, Lopes-Martins RAB, Joensen J, Iversen VV. The anti-inflammatory mechanism of low level laser therapy and its relevance for clinical use in physiotherapy. Phys Ther Rev. 2010;15(4):286-93.

Submitted date:
02/03/2022

Accepted date:
07/13/2022

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