Skip to main content
Top
Published in: Lasers in Medical Science 7/2015

01-09-2015 | Review Article

The low level laser therapy (LLLT) operating in 660 nm reduce gene expression of inflammatory mediators in the experimental model of collagenase-induced rat tendinitis

Authors: Romildo Torres-Silva, Rodrigo Alvaro Brandão Lopes-Martins, Jan Magnus Bjordal, Lucio Frigo, Rachid Rahouadj, Gilles Arnold, Ernesto Cesar Pinto Leal-Junior, Jacques Magdalou, Rodney Pallotta, Rodrigo Labat Marcos

Published in: Lasers in Medical Science | Issue 7/2015

Login to get access

Abstract

Tendinopathy is a common disease with a variety of treatments and therapies. Laser therapy appears as an alternative treatment. Here, we investigate the effects of laser irradiation in an experimental model of tendinitis induced by collagenase injection on rats’ Achilles tendon, verifying its action in important inflammatory markers. Male Wistar rats were used and divided into five groups: control saline (C), non-treated tendinitis (NT) and tendinitis treated with sodium diclofenac (D) or laser (1 J) and (3 J). The tendinitis was induced by collagenase (100 μg/tendon) on the Achilles tendon, which was removed for further analyses. The gene expression for COX-2; TNF-α; IL-6; and IL-10 (RT-PCR) was measured. The laser irradiation (660 nm, 100 mW, 3 J) used in the treatment of the tendinitis induced by collagenase in Achilles tendon in rats was effective in the reduction of important pro-inflammatory markers such as IL-6 and TNF-α, becoming a promising tool for the treatment of tendon diseases.
Literature
2.
go back to reference Hast MW, Zuskov A, Soslowsky LJ (2014) The role of animal models in tendon research. Bone. Joint Res 3(6):193–202 Hast MW, Zuskov A, Soslowsky LJ (2014) The role of animal models in tendon research. Bone. Joint Res 3(6):193–202
3.
go back to reference Aittomaki A, Lahelma E, Rahkonen O, Leino-Arjas AMN, Olsen J (2006) The contribution of musculoskeletal disorders and physical workload to socioeconomic inequalities in health. Eur J Public Health 2:145–150 Aittomaki A, Lahelma E, Rahkonen O, Leino-Arjas AMN, Olsen J (2006) The contribution of musculoskeletal disorders and physical workload to socioeconomic inequalities in health. Eur J Public Health 2:145–150
4.
go back to reference Nguyen TH, Randolph DC (2007) Nonspecific low back pain and return to work. Am Fam Physician 10:1497–1502 Nguyen TH, Randolph DC (2007) Nonspecific low back pain and return to work. Am Fam Physician 10:1497–1502
5.
go back to reference Kjaer M, Langberg H, Bojsen-Møller J, Koskinen SO, Mackey A, Heinemeier K, Holm L, Skovgaard D, Døssing S, Hansen M, Hansen P, Haraldsson B, Carøe I, Magnusson SP (2008) Novel methods for tendon investigations. Disabil Rehabil 30(20–22):1514–1522CrossRefPubMed Kjaer M, Langberg H, Bojsen-Møller J, Koskinen SO, Mackey A, Heinemeier K, Holm L, Skovgaard D, Døssing S, Hansen M, Hansen P, Haraldsson B, Carøe I, Magnusson SP (2008) Novel methods for tendon investigations. Disabil Rehabil 30(20–22):1514–1522CrossRefPubMed
6.
go back to reference BARBE MF, BARR AE (2006) Inflammation and the pathophysiology of work-related musculoskeletal disorders. Brain Behav Immun 5:423–429CrossRef BARBE MF, BARR AE (2006) Inflammation and the pathophysiology of work-related musculoskeletal disorders. Brain Behav Immun 5:423–429CrossRef
7.
go back to reference Alfredson H, Lorentzon R (2000) Chronic Achilles tendinosis. Recommendations for treatment and prevention. Sports Med 29(2):135–146CrossRefPubMed Alfredson H, Lorentzon R (2000) Chronic Achilles tendinosis. Recommendations for treatment and prevention. Sports Med 29(2):135–146CrossRefPubMed
8.
go back to reference Lin TW, Cardenas L, Glaser DL, Soslowsky LJ (2006) Tendon healing in interleukin-4 and interleukin-6 knockout mice. J Biomech 39(1):61–69CrossRefPubMed Lin TW, Cardenas L, Glaser DL, Soslowsky LJ (2006) Tendon healing in interleukin-4 and interleukin-6 knockout mice. J Biomech 39(1):61–69CrossRefPubMed
9.
go back to reference Skutek M, Van Griensven M, Zeichen J et al (2001) Cyclic mechanical stretching enhances secretion of interleukin 6 in human tendon fibroblasts. Knee Surg Sports Traumatol Arthrosc 9(5):322–326CrossRefPubMed Skutek M, Van Griensven M, Zeichen J et al (2001) Cyclic mechanical stretching enhances secretion of interleukin 6 in human tendon fibroblasts. Knee Surg Sports Traumatol Arthrosc 9(5):322–326CrossRefPubMed
10.
go back to reference Fu SC, Wang W, Pau HM et al (2002) Increased expression of transforming growth factor-beta1 in patellar tendinosis. Clin Orthop Relat Res 400:174–183CrossRefPubMed Fu SC, Wang W, Pau HM et al (2002) Increased expression of transforming growth factor-beta1 in patellar tendinosis. Clin Orthop Relat Res 400:174–183CrossRefPubMed
11.
go back to reference Nakama K, Gotoh M, Yamada T et al (2006) Interleukin-6-induced activation of signal transducer and activator of transcription-3 in ruptured rotator cuff tendon. J Int Med Res 34(6):624–631CrossRefPubMed Nakama K, Gotoh M, Yamada T et al (2006) Interleukin-6-induced activation of signal transducer and activator of transcription-3 in ruptured rotator cuff tendon. J Int Med Res 34(6):624–631CrossRefPubMed
12.
go back to reference Hayer S, Redlich K, Korb A, Hermann S, Smolen J, Schett G (2007) Tenosynovitis and osteoclast formation as the initial preclinical changes in a murine model of inflammatory arthritis. Arthritis Rheum 56(1):79–88CrossRefPubMed Hayer S, Redlich K, Korb A, Hermann S, Smolen J, Schett G (2007) Tenosynovitis and osteoclast formation as the initial preclinical changes in a murine model of inflammatory arthritis. Arthritis Rheum 56(1):79–88CrossRefPubMed
13.
go back to reference Ricchetti ET, Reddy SC, Ansorge HL, Zgonis MH, VAN Kleunen JP, Liechty KW, Soslowsky LJ, Beredjiklian PK (2008) Effect of interleukin-10 overexpression on the properties of healing tendon in a murine patellar tendon model. J Hand Surg Eur 33A:1843–1852CrossRef Ricchetti ET, Reddy SC, Ansorge HL, Zgonis MH, VAN Kleunen JP, Liechty KW, Soslowsky LJ, Beredjiklian PK (2008) Effect of interleukin-10 overexpression on the properties of healing tendon in a murine patellar tendon model. J Hand Surg Eur 33A:1843–1852CrossRef
14.
go back to reference Alam R, Kumar D, Anderson-Walters D, Forsythe PA (1994) Macrophage inflammatory protein-1 alpha and monocyte chemoattractant peptide-1 elicit immediate and late cutaneous reactions and activate murine mast cells in vivo. J Immunol 2:1298–1303 Alam R, Kumar D, Anderson-Walters D, Forsythe PA (1994) Macrophage inflammatory protein-1 alpha and monocyte chemoattractant peptide-1 elicit immediate and late cutaneous reactions and activate murine mast cells in vivo. J Immunol 2:1298–1303
15.
go back to reference Hosaka Y, Kirisawa R, Ueda H, Yamaguchi M, Takehana K (2005) Differences in tumor necrosis factor (TNF)alpha and TNF receptor-1-mediated intracellular signaling factors in normal, inflamed and scar-formed horse tendons. J Vet Med Sci 67(10):985–991CrossRefPubMed Hosaka Y, Kirisawa R, Ueda H, Yamaguchi M, Takehana K (2005) Differences in tumor necrosis factor (TNF)alpha and TNF receptor-1-mediated intracellular signaling factors in normal, inflamed and scar-formed horse tendons. J Vet Med Sci 67(10):985–991CrossRefPubMed
16.
go back to reference Akesen B, Demirag B, Budak F (2009) Evaluation of intra-articular collagenase, TIMP-1, and TNF-alpha levels before and after anterior cruciate ligament reconstruction. Acta Orthop Traumatol Turc 43(3):214–218CrossRefPubMed Akesen B, Demirag B, Budak F (2009) Evaluation of intra-articular collagenase, TIMP-1, and TNF-alpha levels before and after anterior cruciate ligament reconstruction. Acta Orthop Traumatol Turc 43(3):214–218CrossRefPubMed
17.
go back to reference Fernandes MAL, Alves GES, Souza JCA (2003) Efeito do ultra-som terapêutico em tendinite experimental de eqüinos: estudo clínico, ultra-sonográfico e histopatológico de dois protocolos. Arq B Med Vet Zoot 55(1):27–34CrossRef Fernandes MAL, Alves GES, Souza JCA (2003) Efeito do ultra-som terapêutico em tendinite experimental de eqüinos: estudo clínico, ultra-sonográfico e histopatológico de dois protocolos. Arq B Med Vet Zoot 55(1):27–34CrossRef
18.
go back to reference Alves AC, Albertini R, dos Santos SA, Leal-Junior EC, Santana E, Serra AJ, Silva JA Jr, de Carvalho PD (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(3):911–919PubMed Alves AC, Albertini R, dos Santos SA, Leal-Junior EC, Santana E, Serra AJ, Silva JA Jr, de Carvalho PD (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(3):911–919PubMed
19.
go back to reference Alfredson H, Ohberg L, Forsgren S (2003) Is vasculo-neural ingrowth the cause of pain in chronic Achilles tendinosis? An investigation using ultrasonography and colour Doppler, immunohistochemistry, and diagnostic injections. Knee Surg Sports Traumatol Arthrosc 11(5):334–338CrossRefPubMed Alfredson H, Ohberg L, Forsgren S (2003) Is vasculo-neural ingrowth the cause of pain in chronic Achilles tendinosis? An investigation using ultrasonography and colour Doppler, immunohistochemistry, and diagnostic injections. Knee Surg Sports Traumatol Arthrosc 11(5):334–338CrossRefPubMed
20.
go back to reference Andres BM, Murrell GA (2008) Treatment of tendinopathy: what works, what does not, and what is on the horizon. Clin Orthop Relat Res 466(7):1539–1554PubMedCentralCrossRefPubMed Andres BM, Murrell GA (2008) Treatment of tendinopathy: what works, what does not, and what is on the horizon. Clin Orthop Relat Res 466(7):1539–1554PubMedCentralCrossRefPubMed
21.
go back to reference Bjordal JM, Klovning A, Lopes-Martins RA, Roland PD, Joensen J, Slørdal L (2008) Overviews and systematic reviews on low back pain. Ann Intern Med 10(148):789–790CrossRef Bjordal JM, Klovning A, Lopes-Martins RA, Roland PD, Joensen J, Slørdal L (2008) Overviews and systematic reviews on low back pain. Ann Intern Med 10(148):789–790CrossRef
22.
go back to reference Bjordal JM, Lopes-Martins RA (2013) Lack of adherence to the laser dosage recommendations from the World Association for Laser Therapy in Achilles study. Arch Phys Med Rehabil 94(2):408CrossRefPubMed Bjordal JM, Lopes-Martins RA (2013) Lack of adherence to the laser dosage recommendations from the World Association for Laser Therapy in Achilles study. Arch Phys Med Rehabil 94(2):408CrossRefPubMed
23.
go back to reference Marcos RL, Leal Junior EC et al (2011) Infrared (810 nm) low-level laser therapy in rat achilles tendinitis: a consistent alternative to drugs. Photochem Photobiol 87(6):1447–1452CrossRefPubMed Marcos RL, Leal Junior EC et al (2011) Infrared (810 nm) low-level laser therapy in rat achilles tendinitis: a consistent alternative to drugs. Photochem Photobiol 87(6):1447–1452CrossRefPubMed
24.
go back to reference 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(6):523–533CrossRefPubMed 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(6):523–533CrossRefPubMed
25.
go back to reference de Almeida P, Tomazoni SS, Frigo L, de Carvalho PD, Vanin AA, Santos LA, Albuquerque-Pontes GM, de Marchi T, Tairova O, Marcos RL, Lopes-Martins RA, Leal-Junior EC (2014) What is the best treatment to decrease pro-inflammatory cytokine release in acute skeletal muscle injury induced by trauma in rats: low-level laser therapy, diclofenac, or cryotherapy? Lasers Med Sci 29(2):653–658CrossRefPubMed de Almeida P, Tomazoni SS, Frigo L, de Carvalho PD, Vanin AA, Santos LA, Albuquerque-Pontes GM, de Marchi T, Tairova O, Marcos RL, Lopes-Martins RA, Leal-Junior EC (2014) What is the best treatment to decrease pro-inflammatory cytokine release in acute skeletal muscle injury induced by trauma in rats: low-level laser therapy, diclofenac, or cryotherapy? Lasers Med Sci 29(2):653–658CrossRefPubMed
26.
go back to reference Tsai WC, Hsu CC, Pang JH, Lin MS, Chen YH, Liang FC (2012) Low-level laser irradiation stimulates tenocyte migration with up-regulation of dynamin II expression. PLoS One 7(5):e38235PubMedCentralCrossRefPubMed Tsai WC, Hsu CC, Pang JH, Lin MS, Chen YH, Liang FC (2012) Low-level laser irradiation stimulates tenocyte migration with up-regulation of dynamin II expression. PLoS One 7(5):e38235PubMedCentralCrossRefPubMed
27.
go back to reference Tsai WC, Cheng JW, Chen JL, Chen CY, Chang HN, Liao YH, Lin MS, Pang JH (2014) Low-level laser irradiation stimulates tenocyte proliferation in association with increased NO synthesis and upregulation of PCNA and cyclins. Lasers Med Sci 29(4):1377–1384CrossRefPubMed Tsai WC, Cheng JW, Chen JL, Chen CY, Chang HN, Liao YH, Lin MS, Pang JH (2014) Low-level laser irradiation stimulates tenocyte proliferation in association with increased NO synthesis and upregulation of PCNA and cyclins. Lasers Med Sci 29(4):1377–1384CrossRefPubMed
28.
go back to reference Salate AC, Barbosa G, Gaspar P, Koeke PU, Parizotto NA, Benze BG, Foschiani D (2005) Effect of In-Ga-Al-P diode laser irradiation on angiogenesis in partial ruptures of Achilles tendon in rats. Photomed Laser Surg 23(5):470–475CrossRefPubMed Salate AC, Barbosa G, Gaspar P, Koeke PU, Parizotto NA, Benze BG, Foschiani D (2005) Effect of In-Ga-Al-P diode laser irradiation on angiogenesis in partial ruptures of Achilles tendon in rats. Photomed Laser Surg 23(5):470–475CrossRefPubMed
29.
go back to reference Barbosa D, de Souza RA, de Carvalho WR, Xavier M, de Carvalho PK, Cunha TC, Arisawa EÂ, Silveira LJR, Villaverde AB (2013) Low-level laser therapy combined with platelet-rich plasma on the healing calcaneal tendon: a histological study in a rat model. Lasers Med Sci 28(6):1489–1494CrossRefPubMed Barbosa D, de Souza RA, de Carvalho WR, Xavier M, de Carvalho PK, Cunha TC, Arisawa EÂ, Silveira LJR, Villaverde AB (2013) Low-level laser therapy combined with platelet-rich plasma on the healing calcaneal tendon: a histological study in a rat model. Lasers Med Sci 28(6):1489–1494CrossRefPubMed
30.
go back to reference Casalechi HL, de Farias Marques AC, da Silva EA, Aimbire F, Marcos RL, Lopes-Martins RA, de Carvalho PD, Albertini R (2014) Analysis of the effect of phototherapy in model with traumatic Achilles tendon injury in rats. Lasers Med Sci 29(3):1075–1081CrossRefPubMed Casalechi HL, de Farias Marques AC, da Silva EA, Aimbire F, Marcos RL, Lopes-Martins RA, de Carvalho PD, Albertini R (2014) Analysis of the effect of phototherapy in model with traumatic Achilles tendon injury in rats. Lasers Med Sci 29(3):1075–1081CrossRefPubMed
31.
go back to reference Marcos RL, Arnold G, Magnenet V, Rahouadj R, Magdalou J, Lopes-Martins RA (2014) Biomechanical and biochemical protective effect of low-level laser therapy for Achilles tendinitis. J Mech Behav Biomed Mater 29C:272–285CrossRef Marcos RL, Arnold G, Magnenet V, Rahouadj R, Magdalou J, Lopes-Martins RA (2014) Biomechanical and biochemical protective effect of low-level laser therapy for Achilles tendinitis. J Mech Behav Biomed Mater 29C:272–285CrossRef
32.
go back to reference Krasnouktsky S, Samuels J, Abramson SB (2007) Osteoarthritis in 2007. Bull NYU Hosp Jt Dis 65(3):222–228 Krasnouktsky S, Samuels J, Abramson SB (2007) Osteoarthritis in 2007. Bull NYU Hosp Jt Dis 65(3):222–228
34.
go back to reference Queiroz-Junior CM, Pacheco CMF, Maltos KLM, Caliari MV, Duarte IDG, Francischi JN (2009) Role of systemic and local administration of selective inhibitors of cyclo-oxygenase 1 and 2 in an experimental model of periodontal disease in rats. J Periodontal Res 44(2):153–160CrossRefPubMed Queiroz-Junior CM, Pacheco CMF, Maltos KLM, Caliari MV, Duarte IDG, Francischi JN (2009) Role of systemic and local administration of selective inhibitors of cyclo-oxygenase 1 and 2 in an experimental model of periodontal disease in rats. J Periodontal Res 44(2):153–160CrossRefPubMed
35.
go back to reference demos M, Joosten LA, Oppers-Walgreen B, van Schie JT, Jahr H, van Osch GJ, Verhaar JA (2009) Tendon degeneration is not mediated by regulation of Toll-like receptors 2 and 4 in human tenocytes. J Orthop Res 27(8):1043–1047CrossRef demos M, Joosten LA, Oppers-Walgreen B, van Schie JT, Jahr H, van Osch GJ, Verhaar JA (2009) Tendon degeneration is not mediated by regulation of Toll-like receptors 2 and 4 in human tenocytes. J Orthop Res 27(8):1043–1047CrossRef
36.
go back to reference Pingel J, Fredberg U, Mikkelsen LR, Schjerling P, Heinemeier KM, Kjaer M, Harisson A, Langberg H (2013) No inflammatory gene-expression response to acute exercise in human Achilles tendinopathy. Eur J Appl Physiol 113(8):2101–2109CrossRefPubMed Pingel J, Fredberg U, Mikkelsen LR, Schjerling P, Heinemeier KM, Kjaer M, Harisson A, Langberg H (2013) No inflammatory gene-expression response to acute exercise in human Achilles tendinopathy. Eur J Appl Physiol 113(8):2101–2109CrossRefPubMed
37.
go back to reference Kamimoto M, Mizuno S, Nakamura T (2009) Reciprocal regulation of IL-6 and IL-10 balance by HGF via recruitment of heme oxygenase-1 in macrophages for attenuation of liver injury in a mouse model of endotoxemia. Int J Mol Med 24(2):161–170PubMed Kamimoto M, Mizuno S, Nakamura T (2009) Reciprocal regulation of IL-6 and IL-10 balance by HGF via recruitment of heme oxygenase-1 in macrophages for attenuation of liver injury in a mouse model of endotoxemia. Int J Mol Med 24(2):161–170PubMed
38.
go back to reference Ortega E, Bote ME, Giraldo E, García JJ (2012) Aquatic exercise improves the monocyte pro- and anti-inflammatory cytokine production balance in fibromyalgia patients. Scand J Med Sci Sports 22(1):104–112CrossRefPubMed Ortega E, Bote ME, Giraldo E, García JJ (2012) Aquatic exercise improves the monocyte pro- and anti-inflammatory cytokine production balance in fibromyalgia patients. Scand J Med Sci Sports 22(1):104–112CrossRefPubMed
39.
go back to reference Biancofiore G, Bindi L, Miccoli M, Metelli MR, Panicucci E, Baggiani A, Filipponi F (2013) Balance of pro- and anti-inflammatory cytokines in cirrhotic patients undergoing liver transplantation. Transpl Immunol 28(4):193–197CrossRefPubMed Biancofiore G, Bindi L, Miccoli M, Metelli MR, Panicucci E, Baggiani A, Filipponi F (2013) Balance of pro- and anti-inflammatory cytokines in cirrhotic patients undergoing liver transplantation. Transpl Immunol 28(4):193–197CrossRefPubMed
40.
go back to reference John T, Lodka D, Kohl B, Ertel W, Jammrath J, Conrad C, Stoll C, Busch C, Schulze-Tanzil G (2010) Effect of pro-inflammatory and immunoregulatory cytokines on human tenocytes. J Orthop Res 28(8):1071–1077PubMed John T, Lodka D, Kohl B, Ertel W, Jammrath J, Conrad C, Stoll C, Busch C, Schulze-Tanzil G (2010) Effect of pro-inflammatory and immunoregulatory cytokines on human tenocytes. J Orthop Res 28(8):1071–1077PubMed
41.
go back to reference Keeble J, Blades M, Pitzalis C, Rocha FAC, Brain SD (2005) The role of substance P in microvascular responses in murine joint inflammation. Br J Pharmacol 144:1059–1066PubMedCentralCrossRefPubMed Keeble J, Blades M, Pitzalis C, Rocha FAC, Brain SD (2005) The role of substance P in microvascular responses in murine joint inflammation. Br J Pharmacol 144:1059–1066PubMedCentralCrossRefPubMed
Metadata
Title
The low level laser therapy (LLLT) operating in 660 nm reduce gene expression of inflammatory mediators in the experimental model of collagenase-induced rat tendinitis
Authors
Romildo Torres-Silva
Rodrigo Alvaro Brandão Lopes-Martins
Jan Magnus Bjordal
Lucio Frigo
Rachid Rahouadj
Gilles Arnold
Ernesto Cesar Pinto Leal-Junior
Jacques Magdalou
Rodney Pallotta
Rodrigo Labat Marcos
Publication date
01-09-2015
Publisher
Springer London
Published in
Lasers in Medical Science / Issue 7/2015
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-014-1676-3

Other articles of this Issue 7/2015

Lasers in Medical Science 7/2015 Go to the issue