Abstract
This study aimed to investigate the anti-inflammatory effects of different dosage of low-level laser therapy (LLLT) in an experimental model of temporomandibular joint (TMJ) arthritis. One hundred male Wistar rats were used and divided into the following groups: CG, control group; AG, animals group with left TMJ arthritis induced by intra-articular injection of Complete Freund’s adjuvant - CFA; LG5, LG10 and LG20 - animals with arthritis and treated with LLLT at doses 5, 10, and 20 J/cm2, respectively. Morphological analysis was performed by TMJ histological sections stained with hematoxylin-eosin (HE), picrosirius (PSR), and toluidine blue (TB), as well as histomorphometric evaluation of cartilage, articular disc, and masticatory muscles. The amount of feed consumed within 3 weeks was evaluated, and biochemical analysis of TMJ tissues included measurement of sulfated glycosaminoglycans (GAGs), matrix metalloproteinases (MMPs) 2 and 9 zymography, and ELISA for cytokines IL-6, TNF-α, and IL-1β. Only the 20 J/cm2 dose promoted higher feed intake compared to AG. On the other hand, all LLLT doses promoted better organization of articular disc collagen fibers, greater number of proteoglycans in articular cartilage, increased area and diameter of left lateral pterygoid fibers, reduced latent and active MMP 9 and 2 activity, and lower IL-1β concentration compared to AG. Considering the study limitations, it was observed that LLLT treatments were effective in protecting and tissue cleansing joint structures, accelerating tissue repair, especially at lower doses.
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de Leeuw R (2010) Orofacial pain: guidelines for assessment, diagnosis, and management, 4a. Quintessence Editora, São Paulo
Okeson JP (2008) Tratamento das Desordens Temporomandibulares e Oclusão, 6th edn. Elsevier, Rio de Janeiro
de Moura WP, da Silva PLP, Lemos GA et al (2017) Retrospective review of patients referred to a temporomandibular dysfunction care setting of a Brazilian public university. Rev Dor 18:128–134. https://doi.org/10.5935/1806-0013.20170026
Convissar RA (2011) Principles and practice of laser dentistry. Elsevier, Rio de Janeiro
Karu T (1989) Photobiology of low-power laser effects. Heulfh Physfrs 56:691–704
Farivar S, Malekshahabi T, Shiari R (2014) Biological effects of low level laser therapy. J Lasers Med Sci 5:58–62
Mazzetto MO, Hotta TH, Pizzo RCDA (2010) Measurements of jaw movements and TMJ pain intensity in patients treated with GaAlAs laser. Braz Dent J 21:356–360
Sayed N, Murugavel C, Gnanam A (2014) Management of temporomandibular disorders with low level laser therapy. J Maxillofac Oral Surg 13:444–450. https://doi.org/10.1007/s12663-013-0544-1
Hosgor H, Bas B, Celenk C (2017) A comparison of the outcomes of four minimally invasive treatment methods for anterior disc displacement of the temporomandibular joint. Int J Oral Maxillofac Surg 46:1403–1410. https://doi.org/10.1016/j.ijom.2017.05.010
Cetiner S, Kahraman SA, Yucetas S (2006) Evaluation of low-level laser therapy in the treatment of temporomandibular disorders. Photomed Laser Surg 24:637–641. https://doi.org/10.1089/pho.2006.24.637
de Carli ML, Guerra MB, Nunes TB et al (2013) Piroxicam and laser phototherapy in the treatment of TMJ arthralgia: a double-blind randomised controlled trial. J Oral Rehabil 40:171–178. https://doi.org/10.1111/joor.12022
Leal de Godoy CH, Motta LJ, Santos Fernandes KP et al (2015) Effect of low-level laser therapy on adolescents with temporomandibular disorder: a blind randomized controlled pilot study. J Oral Maxillofac Surg 73:622–629. https://doi.org/10.1016/j.joms.2014.09.018
Shobha R, Narayanan VS, Pai BJ et al (2017) Low-level laser therapy: a novel therapeutic approach to temporomandibular disorder – a randomized, double- blinded, placebo-controlled trial. Indian J Dent Res 28:380–387
Chen J, Huang Z, Ge M, Gao M (2015) Efficacy of low-level laser therapy in the treatment of TMDs: a meta-analysis of 14 randomised controlled trials. J Oral Rehabil 42:291–299. https://doi.org/10.1111/joor.12258
Bjordal JM, Couppé C, Chow RT et al (2003) A systematic review of low level laser therapy with location-specific doses for pain from chronic joint disorders. Aust J Physiother 49:107–116
Castano AP, Dai T, Yaroslavsky I et al (2007) Low-level laser therapy for zymosan-induced arthritis in rats: importance of illumination time. Lasers Surg Med 39:543–550. https://doi.org/10.1002/lsm.20516.Low-Level
Pallotta RC, Bjordal JM, Frigo L et al (2012) Infrared (810-nm) low-level laser therapy on rat experimental knee inflammation. Lasers Med Sci 27:71–78. https://doi.org/10.1007/s10103-011-0906-1
Alves ACA, Vieira RDP, Leal-Junior ECP et al (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 15:R116. https://doi.org/10.1186/ar4296
Alves ACA, De Carvalho PDTC, Parente M et al (2013) Low-level laser therapy in different stages of rheumatoid arthritis: a histological study. Lasers Med Sci 28:529–536. https://doi.org/10.1007/s10103-012-1102-7
Carlos FP, de Paula Alves da Silva M, de Lemos Vasconcelos Silva ME et al (2014) Protective effect of low-level laser therapy (LLLT) on acute zymosan-induced arthritis. Lasers Med Sci 29:757–763. https://doi.org/10.1007/s10103-013-1413-3
Santos SA, Alves ACA, Leal ECP et al (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. https://doi.org/10.1007/s10103-013-1467-2
Carvalho CM, Lacerda JA, dos Santos Neto FP et al (2011) Evaluation of laser phototherapy in the inflammatory process of the rat’s TMJ induced by carrageenan. Photomed Laser Surg 29:245–254. https://doi.org/10.1089/pho.2009.2685
Castro ICV, Rosa CB, Carvalho CM et al (2015) Assessment of different energy delivery settings in laser and LED phototherapies in the inflammatory process of rat’s TMJ induced by carrageenan. Lasers Med Sci 30:2105–2113. https://doi.org/10.1007/s10103-015-1748-z
Lemos GA, Rissi R, de Souza Pires IL et al (2016) Low-level laser therapy stimulates tissue repair and reduces the extracellular matrix degradation in rats with induced arthritis in the temporomandibular joint. Lasers Med Sci 31:1051–1059. https://doi.org/10.1007/s10103-016-1946-3
Barretto SR, de Melo GC, dos Santos JC et al (2013) Evaluation of anti-nociceptive and anti-inflammatory activity of low-level laser therapy on temporomandibular joint inflammation in rodents. J Photochem Photobiol B Biol 129:135–142. https://doi.org/10.1016/j.jphotobiol.2013.10.002
Desiderá AC, Nascimento GC, Gerlach RF, Leite-Panissi CRA (2015) Laser therapy reduces gelatinolytic activity in the rat trigeminal ganglion during temporomandibular joint inflammation. Oral Dis 21:652–658. https://doi.org/10.1111/odi.12330
Kucuk BB, Oral K, Selcuk NA et al (2010) The anti-inflammatory effect of low-level laser therapy on experimentally induced inflammation of rabbit temporomandibular joint retrodiscal tissues. J Orofac Pain 24:293–297
De Oliveira DWD, Lages FS, Guimarães RC et al (2017) Do TMJ symptoms improve and last across time after treatment with red (660 nm) and infrared (790 nm) low level laser treatment (LLLT)? a survival analysis. Cranio 35:372–378. https://doi.org/10.1080/08869634.2017.1292176
Tomazoni SS, Leal-Junior ECP, Pallotta RC et al (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. https://doi.org/10.1007/s10103-016-2091-8
Aimbire F, Albertini R, Pacheco MTT et al (2006) Low-level laser therapy induces dose-dependent reduction of TNFα levels in acute inflammation. Photomed Laser Surg 24:33–37. https://doi.org/10.1089/pho.2006.24.33
Oliveira VLC, Silva JA, Serra AJ et al (2017) Photobiomodulation therapy in the modulation of inflammatory mediators and bradykinin receptors in an experimental model of acute osteoarthritis. Lasers Med Sci 32:87–94. https://doi.org/10.1007/s10103-016-2089-2
Sokal RR, Rohlf FJ (2012) Biometry: the principles and practice of statistics in biological research, 4th edn. W. H. Freeman and Co, New York
Fontelles MJ, Simões MG, de Almeida JC, Fontelles RGS (2010) Scientific research methodology: guidelines for size sample calculation. Rev Para Med 24:57–64
Nascimento GC, Leite-Panissi CRA (2014) Physiology & behavior time-dependent analysis of nociception and anxiety-like behavior in rats submitted to persistent inflammation of the temporomandibular joint. Physiol Behav J 125:1–7
Paulino MR, Moreira VG, Lemos GA et al (2018) Prevalence of signs and symptoms of temporomandibular disorders in college preparatory students: associations with emotional factors, parafunctional habits, and impact on quality of life. Cienc e Saude Coletiva 23. https://doi.org/10.1590/1413-81232018231.18952015
Zhou Q, Imbe H, Dubner R, Ren K (1999) Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats : implications for. J Comp Neurol 291:276–291
Wang XD, Kou XX, Mao JJ et al (2012) Sustained inflammation induces degeneration of the temporomandibular joint. J Dent Res 91:499–505. https://doi.org/10.1177/0022034512441946
Rissi R, Lemos GA, Ide BN et al (2016) Joint immobilization: effects on muscular tissue of obese and malnourished mice. Rev Bras Cineantropometria Desempenho Hum 18:1–10. https://doi.org/10.5007/1980-0037.2015v17n5p50
Detamore MS, Orfanos JG, Almarza AJ et al (2005) Quantitative analysis and comparative regional investigation of the extracellular matrix of the porcine temporomandibular joint disc. Matrix Biol 24:45–57. https://doi.org/10.1016/j.matbio.2004.11.006
Kalpakci KN, Willard VP, Wong ME, Athanasiou KA (2011) An interspecies comparison of the temporomandibular joint disc. J Dent Res 90:193–198. https://doi.org/10.1177/0022034510381501
Lemos GA, da Silva PLP, Batista AUD, Palomari ET (2018) Experimental model of temporomandibular joint arthritis: evaluation of contralateral joint and masticatory muscles. Arch Oral Biol 95:79–88. https://doi.org/10.1016/j.archoralbio.2018.07.003
Issa JPM, Trawitzki BF, Ervolino E et al (2017) Low-intensity laser therapy efficacy evaluation in FVB mice subjected to acute and chronic arthritis. Lasers Med Sci 32:1269–1277. https://doi.org/10.1007/s10103-017-2235-5
Alves ACA, Albertini R, Dos Santos SA et al (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. https://doi.org/10.1007/s10103-013-1427-x
Kramer PR, Kerins CA, Schneiderman E, Bellinger LL (2010) Measuring persistent temporomandibular joint nociception in rats and two mice strains. Physiol Behav 99:669–678. https://doi.org/10.1016/j.physbeh.2010.01.037.Measuring
Bi RY, Ding Y, Gan YH (2016) Non-steroidal anti-inflammatory drugs attenuate hyperalgesia and block upregulation of trigeminal ganglionic sodium channel 1.7 after induction of temporomandibular joint inflammation in rats. Chin J Dent Res 19:35–42. https://doi.org/10.3290/j.cjdr.a35695
Al-Wattar WM, Abdulluh BH, Mahmmod AS (2013) The role of low level laser therapy on the expression of IL_1 beta in wound healing. J Bagh Coll Dent 25:108–113. https://doi.org/10.12816/0014941
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Lemos, G.A., Batista, A.U.D., da Silva, P.L.P. et al. Photobiostimulation activity of different low-level laser dosage on masticatory muscles and temporomandibular joint in an induced arthritis rat model. Lasers Med Sci 35, 1129–1139 (2020). https://doi.org/10.1007/s10103-019-02933-y
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DOI: https://doi.org/10.1007/s10103-019-02933-y