Abstract
The presence of intra-articular crystals is detected in different articular pathologies of acute or chronic nature. The aim of this work was to analyze the action of the indium gallium aluminum and phosphorus (InGaAlP) (λ = 670 nm) laser on the synovial membrane present in the knee joint in experimentally induced microcrystalline arthritis in male adult Wistar rats. The animals were divided into three experimental groups (n = 24): control (A), experimentally induced arthritis (B), experimentally induced arthritis+InGaAlP laser therapy (C). The laser treatment was made daily in the patellar region of the right knee after 48 h of the experimental induction. After 7, 14, and 21 days of therapy, the rats were euthanized and the right knees were removed and processed for histomorphometric, immunohistochemical, ultrastructural, and biochemical investigation of the synovium. The number of granulocytes on the 14th and 21st days was higher in B and lower in C and, lastly, in A. The number of fibroblasts on the 14th and 21st days was similar between A and C and below B. The number of blood vessels on the 21st day was higher in B than in the other groups. The positive number of cells for the TUNEL test was higher on the 14th and 21st days in B compared to the others. The percentage of tissue area occupied by birefringent collagen fibers was higher in B on the 21st day than in the others. The ultrastructure of cells showed fibroblast-like morphology in all groups and periods evaluated. The quantification of glycosaminoglycans did not present significant differences between the groups in all the experimental periods. The amount of hydroxyproline was higher in B compared to the other groups on the 14th and 21st days. The content of non-collagen proteins was higher in B on the 21st day in relation to the other groups. Quantification of TNF-α on the 21st day was higher in A and B than in C. For TGF-β on the 21st day, groups B and C presented similar and higher values than A. For MMP-13, groups A and B presented data similar to and above C. In relation to ADAMT-S4, on the 21st day, groups B and C presented data similar to and lower than A. InGaAlP-670 nm therapy reduced the inflammatory process and tissue injuries of the synovial membrane in comparison to the untreated group, indicating its potential utilization in clinical studies aiming in the recovery of acute arthritis in patients.
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References
Bencardino J, Hassankhani A (2003) Calcium pyrophosphate dihydrate crystal deposition disease. Semin Musculoskelet Radiol 7:175–185
Pay S, Terkeltaub R (2003) Calcium pyrophosphate dehydrate and hydroxyapatite crystal deposition in the joint: new developments relevant to the clinician. Curr Rheumatol Rep 5:235–243
Dalbeth N, Haskard D (2005) Inflammation and tissue damage in crystal deposition diseases. Curr Opin Rheumatol 17:314–318
Cassetta M, Gorevic P (2004) Crystal arthritis. Gout and pseudogout in the geriatric patient. Geriatrics 59:25–30
Suresh E (2005) Diagnosis and management of gout: a rational approach. Postgrad Med J 81:572–579
Stancker TG, Vieira SS, Serra AJ, do Nascimento Lima R, Dos Santos Feliciano R, Silva JA Jr, Dos Santos SA, Dos Santos Vieira MA, Simões MCB, Leal-Junior EC, de Tarso Camillo de Carvalho P (2018) Can photobiomodulation associated with implantation of mesenchymal adipose-derived stem cells attenuate the expression of MMPs and decrease degradation of type II collagen in an experimental model of osteoarthritis? Lasers Med Sci 33:1073–1084
Tomazoni SS, Leal-Junior EC, Frigo L, Pallotta RC, Teixeira S, de Almeida P, Bjordal JM, Lopes-Martins RA (2016) Isolated and combined effects of photobiomodulation therapy, topical nonsteroidal anti-inflammatory drugs, and physical activity in the treatment of osteoarthritis induced by papain. J Biomed Opt 21:108001
Tomazoni SS, Leal-Junior EC, Pallotta RC, Teixeira S, de Almeida P, Lopes-Martins RA (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
Looney AL, Huntingford JL, Blaeser LL, Mann S (2018) A randomized blind placebo-controlled trial investigating the effects of photobiomodulation therapy (PBMT) on canine elbow osteoarthritis. Can Vet J 59:959–966
Morais NC, Barbosa AM, Vale ML, Llaverde AB, de Lima CJ, Cogo JC, Zamuner SR (2010) Anti-inflammatory effect of low-level laser and light-emitting diode in zymosan-induced arthritis. Photomed Laser Surg 28:227–232
Renno AC, McDonnell PA, Parizotto NA, Laakso EL (2007) The effects of laser irradiation on osteoblast and osteosarcoma cell proliferation and differentiation in vitro. Photomed Laser Surg 25:275–280
Castano AP, Dai T, Yaroslavsky I, Cohen R, Apruzzese WA, Smotrich MH, Hamblin MR (2007) Low-level laser therapy for zymosan-induced arthritis in rats: importance of illumination time. Lasers Surg Med 39:543–550
Soriano F, Campana V, Moya M, Gavotto A, Simes J, Soriano M, Soriano R, Spitale L, Palma J (2006) Photobiomodulation of pain and inflammation in microcrystalline arthropathies: experimental and clinical results. Photomed Laser Surg 24:140–150
Moscardi LC, Espíndola TP, Ferreira AA, Alves N, Amaral MEC, Aro AA, Dalia RA, Esquisatto MAM, Mendonça FAS, Santos GMT, Andrade TAM (2018) Lasertherapy as a strategy for tratament healing under caloric restriction – study in rats. J Pharm Pharmacol 6:647–658
Campana V, Moya M, Gavotto A, Simes JC, Spitale L, Soriano F, Palma JA (2003) He-ne laser on microcrystalline arthropathies. J Clin Laser Med Surg 21:99–103
Campana VR, Moya M, Gavotto A, Spitale L, Soriano F, Palma JA (2004) Laser therapy on arthritis induced by urate crystals. Photomed Laser Surg 22:499–503
Cotler HB, Chow RT, Hamblin MR, Carroll J (2015) The use of low level laser therapy (LLLT) for musculoskeletal pain. MOJ Orthop Rheumatol 2:00068
Rayegani SM, Raeissadat SA, Heidari S, Moradi-Joo M (2017) Safety and effectiveness of low-level laser therapy in patients with knee osteoarthritis: a systematic review and meta-analysis. J Lasers Med Sci 8:S12–S19
Felizatti AL, do Bomfim FRC, Bovo JL, de Aro AA, do Amaral MEC, Esquisatto MAM (2019) Effects of low-level laser therapy on the organization of articular cartilage in an experimental microcrystalline arthritis model. Lasers Med Sci 34:1401–1412
Zotti TCM, Peixoto J, Santucci J, Bezzan MB, Bomfim FRC (2014) Morphological aspects of induced acute synovitis after low-level laser therapy. Rev Bras Laser 3:30–33
Farndale RW, Buttle DJ, Barrett AJ (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 883:173–177
Stegemann H, Stalder K (1967) Determination of hydroxyproline. Clin Chim Acta 18:267–273
Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Ellman MH, Becker MA (2006) Crystal-induced arthropathies: recent investigative advances. Curr Opin Rheumatol 18:249–255
McQueen FM, Chhana A, Dalbeth N (2012) Mechanisms of joint damage in gout: evidence from cellular and imaging studies. Nat Rev Rheumatol 10:173–181
Reginato AM, Olsen BR (2007) Genetics and experimental models of crystal-induced arthritis. Lessons learned from mice and men: is it crystal clear? Curr Opin Rheumatol 19:134–145
Müller-Ladner U, Pap T, Gay RE, Neidhart M, Gay S (2005) Mechanisms of disease: the molecular and cellular basis of joint destruction in rheumatoid arthritis. Nat Clin Pract Rheumatol 1:102–110
Hsieh YL, Cheng YJ, Huang FC, Yang CC (2014) The fluence effects of low-level laser therapy on inflammation, fibroblast-like synoviocytes, and synovial apoptosis in rats with adjuvant-induced arthritis. Photomed Laser Surg 32:669–677
Wang M, Sampson ER, Jin H, Li J, Ke QH, Im HJ, Chen D (2013) MMP13 is a critical target gene during the progression of osteoarthritis. Arthritis Res Ther 15:R5
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 15:R116
Rubio CR, Cremonezzi D, Moya M, Soriano F, Palma J, Campana V (2010) Helium-neon laser reduces the inflammatory process of arthritis. Photomed Laser Surg 28:125–129
da Rosa AS, dos Santos AF, da Silva MM, Facco GG, Perreira DM, Alves AC, Leal Junior EC, de Carvalho PT (2012) Effects of low-level laser therapy at wavelengths of 660 and 808 nm in experimental model of osteoarthritis. J Photochem Photobiol B 88:161–166
Carlos FP, Silva MPA, Melo ELVS, Costa MS, Zamuner SR (2014) Protective effect of low-level laser therapy (LLLT) on acute zymosan-induced arthritis. Lasers Med Sci 29:757–763
Prindeze NJ, Moffatt LT, Shupp JW (2012) Mechanisms of action for light therapy: a review of molecular interactions. Exp Biol Med 237:1241–1248
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
Bartok B, Firestein GS (2010) Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev 233:233–255
Noss EH, Brenner MB (2008) The role and therapeutic implications of fibroblast-like synoviocytes in inflammation and cartilage erosion in rheumatoid arthritis. Immunol Rev 223:252–270
Aungier SR, Cartwright AJ, Schwenzer A, Marshall JL, Dyson MR, Slavny P, Parthiban K, Karatt-Vellatt A, Sahbudin I, Culbert E, Hextall P, Clanchy FI, Williams R, Marsden BD, Raza K, Filer A, Buckley CD, McCafferty J, Midwood KS (2019) Targeting early changes in the synovial microenvironment: a new class of immunomodulatory therapy? Ann Rheum Dis 78:186–191
Iozzo RV, Schaefer L (2015) Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol 42:11–55
Arner EC (2002) Aggrecanase-mediated cartilage degradation. Curr Opin Pharmacol 2:322–329
Caterson B, Flannery CR, Hughes CE, Little CB (2000) Mechanisms involved in cartilage proteoglycan catabolism. Matrix Biol 19:333–344
Guerino MR, Baranauskas V, Guerino AC (2000) Laser treatment of experimentally induced chronic arthritis. Appl Surf Sci 154:561–564
Gottlieb T, Jorgensen B, Rohde E, Muller G, Scheller E (2006) The influence of irradiation low-level diode laser on the proteoglycan content in arthrotically cartilage in rabbits. Med Laser Appl 21:53–59
Lin YS, Huang MH, Chai CY (2006) Effects of helium-neon laser on the mucopolysaccharide induction in experimental osteoarthritic cartilage. Osteoarth Cart 14:377–383
Lemos GA, Rissi R, de Souza Pires IL, de Oliveira LP, de Aro AA, Pimentel ER, Palomari ET (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
Pacifici M, Koyama E, Shibukawa Y, Wu C, Tamamura Y, Enomoto-Iwamoto M, Iwamoto M (2006) Cellular and molecular mechanisms of synovial joint and articular cartilage formation. Annals NY Acad Sci 1068:74–86
De Oliveira RF, Oliveira DA, Monteiro W, Zangaro RA, Magini M, Soares CP (2008) Comparison between the effect of low-level laser therapy and low-intensity pulsed ultrasonic irradiation in vitro. Photomed Laser Surg 26:6–9
Yamaura M, Yao M, Yaroslavsky I, Cohen R, Smotrich M, Kochevar IE (2009) Low level light effects on inflammatory cytokine production by rheumatoid arthritis synoviocytes. Lasers Surg Med 41:282–290
Alfredo PP, Bjordal JM, Dreyer SH, Meneses SR, Zaguetti G, Ovanessian V, Fukuda TY, Junior WS, Lopes Martins RÁ, Casarotto RA, Marques AP (2012) Efficacy of low level laser therapy associated with exercises in knee osteoarthritis: a randomized double-blind study. Clin Rehabil 26:523–533
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
Bondeson J, Wainwright SD, Lauder S, Amos N, Hughes CE (2006) The role of synovial macrophages and macrophage-produced cytokines in driving aggrecanases, matrix metalloproteinases, and other destructive and inflammatory responses in osteoarthritis. Arthritis Res Ther 8:R187
Takahashi T, Muneta T, Tsuji K, Sekiya I (2011) BMP-7 inhibits cartilage degeneration through suppression of inflammation in rat zymosan-induced arthritis. Cell Tissue Res 344:321–332
Tanimoto K, Suzuki A, Ohno S, Honda K, Tanaka N, Doi T, Yoneno K, Ohno-Nakahara M, Nakatani Y, Ueki M, Tanne K (2004) Effects of TGF-β1 on hyaluronan anabolism in fibroblasts derived from the synovial membrane of the rabbit temporomandibular joint. J Dent Res 83:40–44
Yamane S, Reddi AH (2008) Induction of chondrogenesis and superficial zone protein accumulation in synovial side population cells by BMP-7 and TGF-β1. J Orthop Res 26:485–492
Malemud CJ (2006) Matrix metalloproteinases (MMPs) in health and disease: an overview. Front Biosci 11:1696–1701
Moore BA, Aznavoorian S, Engler JA, Windsor LJ (2000) Induction of collagenase-3 (MMP-13) in rheumatoid arthritis synovial fibroblasts. Bioch Bioph Acta 1502:307–318
Bondeson J, Wainwright S, Hughes C, Caterson B (2008) The regulation of the ADAMT-S4 and ADAMT-S5 aggrecanases in osteoarthritis: a review. Clin Exp Rheumatol 26:139–145
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This study received financial support of the Hermínio Ometto Foundation.
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This study met the Guidelines for Care and Use of Animal Models and was approved by the Ethics Committee in Animal Experimentation of the FHO (Protocol no. 048/2015).
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Bartoli, D.M.F., Felizatti, A.L., do Bomfim, F.R.C. et al. Laser treatment of synovial inflammatory process in experimentally induced microcrystalline arthritis in Wistar rats. Lasers Med Sci 36, 529–540 (2021). https://doi.org/10.1007/s10103-020-03055-6
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DOI: https://doi.org/10.1007/s10103-020-03055-6