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Erschienen in: Lasers in Medical Science 4/2016

16.03.2016 | Original Article

Low-level laser therapy modulates pro-inflammatory cytokines after partial tenotomy

verfasst von: Flávia Da Ré Guerra, Cristiano Pedrozo Vieira, Letícia Prado Oliveira, Petrus Pires Marques, Marcos dos Santos Almeida, Edson Rosa Pimentel

Erschienen in: Lasers in Medical Science | Ausgabe 4/2016

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Abstract

Tendon injuries give rise to substantial morbidity, and current understanding of the mechanisms involved in tendon injury and repair is limited. This lesion remains a clinical issue because the injury site becomes a region with a high incidence of recurrent rupture and has drawn the attention of researchers. We already demonstrated that low-level laser therapy (LLLT) stimulates the synthesis and organization of collagen I, MMP-9, and MMP-2 and improved the gait recovery of the treated animals. The aim of this study was to evaluate the effects of LLLT in the nitric oxide and cytokines profile during the inflammatory and remodeling phases. Adult male rats were divided into the following groups: G1—intact, G2— injured, G3—injured + LLLT (4 J/cm2 continuous), G4—injured + LLLT (4 J/cm2–20 Hz—pulsed laser). According to the analysis, the animals were euthanized on different dates (1, 4, 8, or 15 days after injury). ELISA assay of TNF-α, IL-1β, IL-10, and TGF-β was performed. Western blotting of isoform of nitric oxide synthase (i-NOS) and nitric oxide dosage experiments was conducted. Our results showed that the pulsed LLLT seems to exert an anti-inflammatory effect over injured tendons, with reduction of the release of proinflammatory cytokines, such as TNF-α and the decrease in the i-NOS activity. Thanks to the pain reduction and the facilitation of movement, there was a stimulation in the TGF-β and IL-1β release. In conclusion, we believe that pulsed LLLT worked effectively as a therapy to reestablish the tendon integrity after rupture.
Literatur
1.
Zurück zum Zitat Latarjet M, Liard AR (1996) Anatomia Humana. 2ed. Editora Panamericana, pp.837-880 Latarjet M, Liard AR (1996) Anatomia Humana. 2ed. Editora Panamericana, pp.837-880
2.
Zurück zum Zitat Maffulli N, Renström P, Leadbetter WB (2005) Tendon Injuries: Basic Science and Clinical Medicine. Springer-Verlag London Limited Maffulli N, Renström P, Leadbetter WB (2005) Tendon Injuries: Basic Science and Clinical Medicine. Springer-Verlag London Limited
4.
Zurück zum Zitat Nourissat G, Berenbaum F, Duprez D (2015) Tendon injury: from biology to tendon repair. Nat Rev Rheumatol 11:223–233CrossRefPubMed Nourissat G, Berenbaum F, Duprez D (2015) Tendon injury: from biology to tendon repair. Nat Rev Rheumatol 11:223–233CrossRefPubMed
5.
Zurück zum Zitat Cribb AM, Scott JE (1995) Tendon response to tensile stress: an ultrastructural investigation of collagen:proteoglycan interactions in stressed tendon. J Anat 187:423–428PubMedPubMedCentral Cribb AM, Scott JE (1995) Tendon response to tensile stress: an ultrastructural investigation of collagen:proteoglycan interactions in stressed tendon. J Anat 187:423–428PubMedPubMedCentral
6.
Zurück zum Zitat Szaro P, Witkowski G, Smigielski R, Krajewski P, Ciszek B (2009) Fascicles of the adult human Achilles tendon - an anatomical study. Ann Anat 191(6):586–593CrossRefPubMed Szaro P, Witkowski G, Smigielski R, Krajewski P, Ciszek B (2009) Fascicles of the adult human Achilles tendon - an anatomical study. Ann Anat 191(6):586–593CrossRefPubMed
7.
Zurück zum Zitat Sharma P, Maffulli N (2006) Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact 6(2):181–190PubMed Sharma P, Maffulli N (2006) Biology of tendon injury: healing, modeling and remodeling. J Musculoskelet Neuronal Interact 6(2):181–190PubMed
8.
Zurück zum Zitat Vieira CP, de Aro AA, de Almeida Mdos S, de Mello GC, Antunes E, Pimentel ER (2011) Effects of acute inflammation induced in the rat paw on the deep digital flexor tendon. Connect Tissue Res 53(2):160–8CrossRefPubMed Vieira CP, de Aro AA, de Almeida Mdos S, de Mello GC, Antunes E, Pimentel ER (2011) Effects of acute inflammation induced in the rat paw on the deep digital flexor tendon. Connect Tissue Res 53(2):160–8CrossRefPubMed
9.
Zurück zum Zitat Molloy T, Wang Y, Murrell G (2003) The roles of growth factors in tendon and ligament healing. Sports Med 33(5):381–94CrossRefPubMed Molloy T, Wang Y, Murrell G (2003) The roles of growth factors in tendon and ligament healing. Sports Med 33(5):381–94CrossRefPubMed
10.
Zurück zum Zitat Houlred NN, Sekhejane PR, Abrahamse H (2010) Irradiation at 830nm Stimulates Nitric Oxide Production and Inhibits Pro-Inflammatory Cytokines in Diabetic Wounded Fibroblast Cells. Lasers Surg Med 42:494–502CrossRef Houlred NN, Sekhejane PR, Abrahamse H (2010) Irradiation at 830nm Stimulates Nitric Oxide Production and Inhibits Pro-Inflammatory Cytokines in Diabetic Wounded Fibroblast Cells. Lasers Surg Med 42:494–502CrossRef
11.
Zurück zum Zitat Jarvinen TA, Kannus P, Mafulli N et al (2005) Achilles tendon disorders: etiology and epidemiology. Foot Ankle Clin 10(2):255–266CrossRefPubMed Jarvinen TA, Kannus P, Mafulli N et al (2005) Achilles tendon disorders: etiology and epidemiology. Foot Ankle Clin 10(2):255–266CrossRefPubMed
12.
Zurück zum Zitat Chan HKF, Fung DT, Ng GY (2007) Effects of low-voltage microamperage stimulation on tendon healing in rats. J Orthop Sports Phys Ther 37(7):399–403CrossRefPubMed Chan HKF, Fung DT, Ng GY (2007) Effects of low-voltage microamperage stimulation on tendon healing in rats. J Orthop Sports Phys Ther 37(7):399–403CrossRefPubMed
13.
Zurück zum Zitat Oliveira FS, Pinfild CE, Parizoto NA et al (2009) Effect of low level laser therapy (830 nm) with different therapy regimes on the process of tissue repair in partial lesion calcaneous tendon. Lasers Surg Med 41:271–276CrossRefPubMed Oliveira FS, Pinfild CE, Parizoto NA et al (2009) Effect of low level laser therapy (830 nm) with different therapy regimes on the process of tissue repair in partial lesion calcaneous tendon. Lasers Surg Med 41:271–276CrossRefPubMed
14.
Zurück zum Zitat Aro AA, Simões GF, Esquisato MAM, Foglio MA, Carvalho JE, Oliveira ALR, Gomes L, Pimentel ER (2013) Arrabidaea chica extract improves gait recovery and changes collagen content during healing of the Achilles tendon. Injury 44(7):884–92CrossRefPubMed Aro AA, Simões GF, Esquisato MAM, Foglio MA, Carvalho JE, Oliveira ALR, Gomes L, Pimentel ER (2013) Arrabidaea chica extract improves gait recovery and changes collagen content during healing of the Achilles tendon. Injury 44(7):884–92CrossRefPubMed
15.
Zurück zum Zitat Kaux JF, Forthomme B, Goff CL, Crielaard JM, Croisier JL (2011) Current opinions on tendinopathy. J Sports Sci Med 10:238–253PubMedPubMedCentral Kaux JF, Forthomme B, Goff CL, Crielaard JM, Croisier JL (2011) Current opinions on tendinopathy. J Sports Sci Med 10:238–253PubMedPubMedCentral
16.
Zurück zum Zitat Pinfildi CE, Liebano RE, Hochman BS, Ferreira LM (2005) Heliumneon laser in viability of random skin flap in rats. Lasers Surg Med 37:89–91CrossRef Pinfildi CE, Liebano RE, Hochman BS, Ferreira LM (2005) Heliumneon laser in viability of random skin flap in rats. Lasers Surg Med 37:89–91CrossRef
17.
Zurück zum Zitat Chen M, Chun C, Meijuan Y et al (2008) Involvement of CAPON and Nitric Oxide Synthases in rat muscle regeneration after peripheral nerve injury. J Mol Neurosci 34:89–100CrossRefPubMed Chen M, Chun C, Meijuan Y et al (2008) Involvement of CAPON and Nitric Oxide Synthases in rat muscle regeneration after peripheral nerve injury. J Mol Neurosci 34:89–100CrossRefPubMed
18.
Zurück zum Zitat da Guerra FR, Vieira CP, Almeida MS, Oliveira LP, de Aro AA, Pimentel ER (2013) LLLT improves tendon healing through increase of MMP activity and collagen synthesis. Lasers Med Sci 28(5):1281–8CrossRef da Guerra FR, Vieira CP, Almeida MS, Oliveira LP, de Aro AA, Pimentel ER (2013) LLLT improves tendon healing through increase of MMP activity and collagen synthesis. Lasers Med Sci 28(5):1281–8CrossRef
19.
Zurück zum Zitat Pugliese LS, Medrado AP, Reis SR, Andrade ZA (2003) The influence of low-level laser therapy on biomodulation of collagen and elastic fibers. Pesqui Odontol Bras 17(4):307–313CrossRefPubMed Pugliese LS, Medrado AP, Reis SR, Andrade ZA (2003) The influence of low-level laser therapy on biomodulation of collagen and elastic fibers. Pesqui Odontol Bras 17(4):307–313CrossRefPubMed
20.
Zurück zum Zitat Guerra Fda R, Vieira CP, de dos Santos Almeida M, Oliveira LP, Claro AC, Simões GF, de Oliveira AL, Pimentel ER (2014) Pulsed LLLT improves tendon healing in rats: a biochemical, organizational, and functional evaluation. Lasers Med Sci 29(2):805–811CrossRefPubMed Guerra Fda R, Vieira CP, de dos Santos Almeida M, Oliveira LP, Claro AC, Simões GF, de Oliveira AL, Pimentel ER (2014) Pulsed LLLT improves tendon healing in rats: a biochemical, organizational, and functional evaluation. Lasers Med Sci 29(2):805–811CrossRefPubMed
21.
Zurück zum Zitat Enwemeka CS, Reddy GK (2000) The biological effects of laser therapy and other modalities on connective tissue repair processes. Laser Ther 12:22–30CrossRef Enwemeka CS, Reddy GK (2000) The biological effects of laser therapy and other modalities on connective tissue repair processes. Laser Ther 12:22–30CrossRef
22.
Zurück zum Zitat Wren TAL, Yerby SA, Beaupre GS et al (2001) Mechanical properties of human Achilles tendon. Clin Biomech 16:245–251CrossRef Wren TAL, Yerby SA, Beaupre GS et al (2001) Mechanical properties of human Achilles tendon. Clin Biomech 16:245–251CrossRef
23.
Zurück zum Zitat Chen CH, Tsai LL, Wang YH et al (2009) Low-level laser irradiation promotes cell proliferation and mRNA expression of type I collagen and decorin in porcine Achilles tendon fibroblasts in vitro. J Orthop Res 27:646–650CrossRefPubMed Chen CH, Tsai LL, Wang YH et al (2009) Low-level laser irradiation promotes cell proliferation and mRNA expression of type I collagen and decorin in porcine Achilles tendon fibroblasts in vitro. J Orthop Res 27:646–650CrossRefPubMed
24.
Zurück zum Zitat Demir H, Menku P, Kirnap M (2004) Comparison of the Effects of Laser, Ultrasound, and Combined Laser + Ultrasound Treatments in Experimental Tendon Healing. Lasers Surg Med 35:84–89CrossRefPubMed Demir H, Menku P, Kirnap M (2004) Comparison of the Effects of Laser, Ultrasound, and Combined Laser + Ultrasound Treatments in Experimental Tendon Healing. Lasers Surg Med 35:84–89CrossRefPubMed
25.
Zurück zum Zitat Request Privilege of Utility Model in Brazil, titled: Retainer of Rats For Laser Beam And Biocompounds Application, deposited inNational Institute Of Industrial Property–INPI, on 04.16.10, undern°MU9000622-4, authored by researchers Andrea Aparecida de Aro and Edson Rosa Pimentel, from Institute of Biology, UNICAMP Request Privilege of Utility Model in Brazil, titled: Retainer of Rats For Laser Beam And Biocompounds Application, deposited inNational Institute Of Industrial Property–INPI, on 04.16.10, undern°MU9000622-4, authored by researchers Andrea Aparecida de Aro and Edson Rosa Pimentel, from Institute of Biology, UNICAMP
26.
Zurück zum Zitat Bradford MM (1976) A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMed Bradford MM (1976) A rapid sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254CrossRefPubMed
27.
Zurück zum Zitat Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci 76(9):4350–4354CrossRefPubMedPubMedCentral Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: Procedure and some applications. Proc Natl Acad Sci 76(9):4350–4354CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Moro CF, Consonni SR, Rosa RG, Nascimento MA, Joazeiro PP (2012) High iNOS mRNA and protein localization during late pregnancy suggest a role for nitric oxide in mouse pubic symphysis relaxation. Mol Reprod Dev 79(4):272–82CrossRefPubMed Moro CF, Consonni SR, Rosa RG, Nascimento MA, Joazeiro PP (2012) High iNOS mRNA and protein localization during late pregnancy suggest a role for nitric oxide in mouse pubic symphysis relaxation. Mol Reprod Dev 79(4):272–82CrossRefPubMed
29.
Zurück zum Zitat Seibert K, Zhang Y, Leahy K et al (1994) Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain. Proc Natl Acad Sci U S A 91:12013–12017CrossRefPubMedPubMedCentral Seibert K, Zhang Y, Leahy K et al (1994) Pharmacological and biochemical demonstration of the role of cyclooxygenase 2 in inflammation and pain. Proc Natl Acad Sci U S A 91:12013–12017CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Schulze-Tanzil G, Al-Sadi O, Wiegand E, Ertel W, Busch C, Kohl B, Pufe T (2011) The role of pro-inflammatory and immunoregulatory cytokines in tendon healing and rupture: new insights. Scand J Med Sci Sports 21(3):337–51CrossRefPubMed Schulze-Tanzil G, Al-Sadi O, Wiegand E, Ertel W, Busch C, Kohl B, Pufe T (2011) The role of pro-inflammatory and immunoregulatory cytokines in tendon healing and rupture: new insights. Scand J Med Sci Sports 21(3):337–51CrossRefPubMed
31.
Zurück zum Zitat Sharma P, Maffulli N (2005) Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg 87:187–202CrossRefPubMed Sharma P, Maffulli N (2005) Tendon injury and tendinopathy: healing and repair. J Bone Joint Surg 87:187–202CrossRefPubMed
32.
Zurück zum Zitat Cao TV, Hicks MR, Campbell D, Standley PRJ (2013) Dosed myofascial release in three-dimensional bioengineered tendons: effects on human fibroblast hyperplasia, hypertrophy, and cytokine secretion. Manip Physiol Ther 36(8):513–21CrossRef Cao TV, Hicks MR, Campbell D, Standley PRJ (2013) Dosed myofascial release in three-dimensional bioengineered tendons: effects on human fibroblast hyperplasia, hypertrophy, and cytokine secretion. Manip Physiol Ther 36(8):513–21CrossRef
33.
Zurück zum Zitat Mobasheri A, Shakibaei M (2013) Is tendinitis an inflammatory disease initiated and driven by pro-inflammatory cytokines such as interleukin 1β? Histol Histopathol 28(8):955–64PubMed Mobasheri A, Shakibaei M (2013) Is tendinitis an inflammatory disease initiated and driven by pro-inflammatory cytokines such as interleukin 1β? Histol Histopathol 28(8):955–64PubMed
34.
Zurück zum Zitat Kersul AL, Iglesias A, Ríos Á, Noguera A, Forteza A, Serra E, Agustí A, Cosío BG (2011) Molecular mechanisms of inflammation during exacerbations of chronic obstructive pulmonary disease. Arch Bronconeumol 47(4):176–83CrossRefPubMed Kersul AL, Iglesias A, Ríos Á, Noguera A, Forteza A, Serra E, Agustí A, Cosío BG (2011) Molecular mechanisms of inflammation during exacerbations of chronic obstructive pulmonary disease. Arch Bronconeumol 47(4):176–83CrossRefPubMed
35.
Zurück zum Zitat Chan KM, Fu SC, Wong YP, Hui WC, Cheuk YC, Wong WN (2008) Expression of transforming growth factor b isoforms and their roles in tendon healing. Wound Rep Regen 16:399–407CrossRef Chan KM, Fu SC, Wong YP, Hui WC, Cheuk YC, Wong WN (2008) Expression of transforming growth factor b isoforms and their roles in tendon healing. Wound Rep Regen 16:399–407CrossRef
36.
Zurück zum Zitat Chen CH, Cao Y, Wu YF, Bais AJ, Gao JS, Tang JB (2008) Tendon healing in vivo: gene expression and production of multiple growth factors in early tendon healing period. Hand Surg 33A:1834–1842CrossRef Chen CH, Cao Y, Wu YF, Bais AJ, Gao JS, Tang JB (2008) Tendon healing in vivo: gene expression and production of multiple growth factors in early tendon healing period. Hand Surg 33A:1834–1842CrossRef
37.
Zurück zum Zitat Hou Y, Mao Z, Wei XL, Lin L, Chen LX, Wang HJ, Fu X, Zhang JY, Yu CL (2009) The roles of TGF-b1 gene transfer on collagen formation during Achilles tendon healing. Biochem Biophys Res Commun 383:235–239CrossRefPubMed Hou Y, Mao Z, Wei XL, Lin L, Chen LX, Wang HJ, Fu X, Zhang JY, Yu CL (2009) The roles of TGF-b1 gene transfer on collagen formation during Achilles tendon healing. Biochem Biophys Res Commun 383:235–239CrossRefPubMed
38.
Zurück zum Zitat Rocha Júnior AM, Vieira BJ, Andrade LCF, Monteiro F (2009) Low-level laser therapy increases transforming growth factor-_2 expression and induces apoptosis of epithelial cells during the tissue repair process. Photomed Laser Surg 27(2):303–307CrossRefPubMed Rocha Júnior AM, Vieira BJ, Andrade LCF, Monteiro F (2009) Low-level laser therapy increases transforming growth factor-_2 expression and induces apoptosis of epithelial cells during the tissue repair process. Photomed Laser Surg 27(2):303–307CrossRefPubMed
39.
Zurück zum Zitat Anaguchi Y, Yasuda K, Majima T, Tohyama H, Minami A, Hayashi K (2005) The effect of transforming growth factor-beta on mechanical properties of the fibrous tissue regenerated in the patellar tendon after resecting the central portion. Clin Biomech (Bristol, Avon) 20(9):959–965CrossRef Anaguchi Y, Yasuda K, Majima T, Tohyama H, Minami A, Hayashi K (2005) The effect of transforming growth factor-beta on mechanical properties of the fibrous tissue regenerated in the patellar tendon after resecting the central portion. Clin Biomech (Bristol, Avon) 20(9):959–965CrossRef
40.
Zurück zum Zitat Sporn MB (2006) The early history of TGF-beta, and a brief glimpse of its future. Cytokine Growth Factor Rev 17(1–2):3–7CrossRefPubMed Sporn MB (2006) The early history of TGF-beta, and a brief glimpse of its future. Cytokine Growth Factor Rev 17(1–2):3–7CrossRefPubMed
41.
Zurück zum Zitat Halikis MN, Manske PR, Kubota H, Aoki M (1997) Effect of immobilization, immediate mobilization, and delayed mobilization on the resistance to digital flexion using a tendon injury model. J Hand Surg [Am] 22(3):464–72CrossRef Halikis MN, Manske PR, Kubota H, Aoki M (1997) Effect of immobilization, immediate mobilization, and delayed mobilization on the resistance to digital flexion using a tendon injury model. J Hand Surg [Am] 22(3):464–72CrossRef
42.
Zurück zum Zitat Aoki M, Kubota H, Pruitt DL, Manske PR (1997) Biomechanical and histologic characteristics of canine flexor tendon repair using early postoperative mobilization. J Hand Surg [Am] 22(1):107–114CrossRef Aoki M, Kubota H, Pruitt DL, Manske PR (1997) Biomechanical and histologic characteristics of canine flexor tendon repair using early postoperative mobilization. J Hand Surg [Am] 22(1):107–114CrossRef
43.
Zurück zum Zitat Tomiosso TC, Nakagaki WR, Gomes L, Hyslop S, Pimentel ER (2009) Organization of collagen bundles during tendon healing in rats treated with L-NAME. Cell Tissue Res 337(2):235–342CrossRefPubMed Tomiosso TC, Nakagaki WR, Gomes L, Hyslop S, Pimentel ER (2009) Organization of collagen bundles during tendon healing in rats treated with L-NAME. Cell Tissue Res 337(2):235–342CrossRefPubMed
44.
Zurück zum Zitat Griffith OW, Stuehr DJ (1995) Nitric oxide synthases: properties and catalytic mechanism. Annu Rev Physiol 57:707–36CrossRefPubMed Griffith OW, Stuehr DJ (1995) Nitric oxide synthases: properties and catalytic mechanism. Annu Rev Physiol 57:707–36CrossRefPubMed
Metadaten
Titel
Low-level laser therapy modulates pro-inflammatory cytokines after partial tenotomy
verfasst von
Flávia Da Ré Guerra
Cristiano Pedrozo Vieira
Letícia Prado Oliveira
Petrus Pires Marques
Marcos dos Santos Almeida
Edson Rosa Pimentel
Publikationsdatum
16.03.2016
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 4/2016
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-016-1918-7

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