Abstract
Objective:
The aim of this study was to evaluate the effects of low level laser therapy (LLLT) on the degenerative process in the articular cartilage after an anterior cruciate ligament transection (ACLT) model in rats.
Methods:
Eighty male rats (Wistar) were divided into four groups: 1.) intact control group (CG), 2.) injured control group (ICG), 3.) injured laser-treated group at 10 J/cm2 (L10) and 4.) injured laser-treated group at 50 J/cm2 (L50). Animals were divided into 2 subgroups, with different periods of sacrifice (5 and 8 weeks post-surgery). The ACLT was used to induce osteoarthritis (OA) in the knees of the rats. LLLT started 2 weeks after the surgery and it was performed for 15 and 30 sessions, respectively using a 685-nm laser, at 10 and 50 J/cm2. Qualitative and semi-quantitative histologic, morphometric and immunohistochemistry analyses were performed.
Results:
Initial signs of tissue degradation could be observed 5 weeks post-ACLT, evidenced by the decrease of proteoglycan concentration and increase in cartilage thickness of the ICG. After 8 weeks post-surgery, analysis showed a progression of the degenerative processes in the ICG revealed by the increased cellularity and higher TNF-α, IL1-β and MMP-13 immunoexpression. LLLT was able to modulate some of the aspects relating to the degradative process, such as biomodulation of the number of chondrocyte proliferation, prevention of proteoglycan loss, and decrease of MMP-13 immunoexpression.
Conclusion:
This study showed that the 685-nm laser irradiation, especially at 10 J/cm2, prevented features related to the articular degenerative process in the knees of rats.
Zusammenfassung
Ziel:
Das Ziel dieser Studie war es, die Effekte der Low-Level-Lasertherapie (LLLT) auf den degenerativen Prozess im Gelenkknorpel von Ratten nach vorderer Kreuzbanddurchtrennung zu evaluieren.
Methoden:
Achtzig männliche Wistar-Ratten wurden in vier Versuchsgruppen unterteilt: 1.) intakte Kontrollgruppe (CG), 2.) verletzte Kontrollgruppe (ICG), 3.) verletzte Laser-behandelte Gruppe bei 10 J/cm2 (L10) und 4.) verletzte Laser-behandelte Gruppe bei 50 J/cm2 (L50). Die Tiere wurden in zwei Untergruppen aufgeteilt und entweder 5 oder 8 Wochen nach der Operation eingeschläfert. Die vordere Kreuzbanddurchtrennung wurde verwendet, um in den Kniegelenken der Ratten Osteoarthritis (OA) zu induzieren. Die LLLT begann 2 Wochen nach der Operation und wurde für 15 bzw. 30 Sitzungen bei 10 und 50 J/cm2 mit einem 685 nm-Laser durchgeführt. Qualitative und semi-quantitative histologische, morphometrische und immunhistochemische Analysen wurden durchgeführt.
Ergebnisse:
Erste Anzeichen von Gewebeabbau wurden 5 Wochen nach der vorderen Kreuzbanddurchtrennung beobachtet und durch die Abnahme der Proteoglycan-Konzentration und die Erhöhung der Knorpeldicke in der verletzten Kontrollgruppe (ICG) belegt. Acht Wochen nach der Operation zeigte sich in der ICG ein Fortschreiten der degenerativen Prozesse durch eine erhöhte Zellularität und eine höhere TNF-α-, IL1-β- und MMP-13-Immunexpression. Mittels LLLT war es möglich, einige der mit dem Abbauprozess in Zusammenhang stehenden Aspekte, wie die Proliferationsrate der Chondrozyten, die Vermeidung des Proteoglycan-Verlustes und die Abnahme der MMP-13-Immunexpression zu modulieren.
Fazit:
Die vorliegende Studie hat gezeigt, dass eine 685 nm-Laserbestrahlung vor allem bei 10 J/cm2, Vorgänge verhindern kann, die zu degenerativen Prozessen in den Kniegelenken von Ratten führen.
Acknowledgments
We thank to Brazilian funding agencies FAPESP and CNPq for the financial support of this research (grant number: FAPESP-2010-16822-5).
Conflict of interest statement
The authors have no competing financial interests.
References
[1] Jin SY, Hong SJ, Yang HI, Park SD, Yoo MC, Lee HJ, Hong MS, Park HJ, Yoon SH, Kim BS, Yim SV, Park HK, Chung JH. Estrogen receptor-alpha gene haplotype is associated with primary knee osteoarthritis in Korean population. Arthritis Res Ther 2004;6(5):R415–21.10.1186/ar1207Search in Google Scholar PubMed PubMed Central
[2] Gupta S, Hawker GA, Laporte A, Croxford R, Coyte PC. The economic burden of disabling hip and knee osteoarthritis (OA) from the perspective of individuals living with this condition. Rheumatology (Oxford) 2005;44(12):1531–7.10.1093/rheumatology/kei049Search in Google Scholar PubMed
[3] Vincent KR, Conrad BP, Fregly BJ, Vincent HK. The pathophysiology of osteoarthritis: a mechanical perspective on the knee joint. PM R 2012;4(5 Suppl):S3–9.10.1016/j.pmrj.2012.01.020Search in Google Scholar PubMed PubMed Central
[4] Walker ER, Boyd RD, Wu DD, Lukoschek M, Burr DB, Radin EL. Morphologic and morphometric changes in synovial membrane associated with mechanically induced osteoarthrosis. Arthritis Rheum 1991;34(5):515–24.10.1002/art.1780340503Search in Google Scholar PubMed
[5] van Valburg AA, van Roermund PM, Marijnissen AC, Wenting MJ, Verbout AJ, Lafeber FP, Bijlsma JW. Joint distraction in treatment of osteoarthritis (II): effects on cartilage in a canine model. Osteoarthritis Cartilage 2000;8(1):1–8.10.1053/joca.1999.0263Search in Google Scholar PubMed
[6] Buckwalter JA, Martin JA. Osteoarthritis. Adv Drug Deliv Rev 2006;58(2):150–67.10.1016/j.addr.2006.01.006Search in Google Scholar PubMed
[7] Bayat M, Ansari E, Gholami N, Bayat A. Effect of low-level helium-neon laser therapy on histological and ultrastructural features of immobilized rabbit articular cartilage. J Photochem Photobiol B 2007;87(2):81–7.10.1016/j.jphotobiol.2007.02.002Search in Google Scholar PubMed
[8] Wong BJ, Pandhoh N, Truong MT, Diaz S, Chao K, Hou S, Gardiner D. Identification of chondrocyte proliferation following laser irradiation, thermal injury, and mechanical trauma. Lasers Surg Med 2005;37(1):89–96.10.1002/lsm.20180Search in Google Scholar PubMed
[9] Gur A, Sarac AJ, Cevik R, Altindag O, Sarac S. Efficacy of 904 nm gallium arsenide low level laser therapy in the management of chronic myofascial pain in the neck: a double-blind and randomize-controlled trial. Lasers Surg Med 2004;35(3):229–35.10.1002/lsm.20082Search in Google Scholar PubMed
[10] Soriano F, Campana V, Moya M, Gavotto A, Simes J, Soriano M, Soriano R, Spitale L, Palma J. Photobiomodulation of pain and inflammation in microcrystalline arthropathies: experimental and clinical results. Photomed Laser Surg 2006;24(2):140–50.10.1089/pho.2006.24.140Search in Google Scholar PubMed
[11] Renno AC, McDonnell PA, Parizotto NA, Laakso EL. The effects of laser irradiation on osteoblast and osteosarcoma cell proliferation and differentiation in vitro. Photomed Laser Surg 2007;25(4):275–80.10.1089/pho.2007.2055Search in Google Scholar
[12] da Rosa AS, dos Santos AF, da Silva MM, Facco GG, Perreira DM, Alves AC, Leal Junior EC, de Carvalho Pde T. Effects of low-level laser therapy at wavelengths of 660 and 808 nm in experimental model of osteoarthritis. Photochem Photobiol 2012;88(1):161–6.10.1111/j.1751-1097.2011.01032.xSearch in Google Scholar
[13] Karu TI, Kolyakov SF. Exact action spectra for cellular responses relevant to phototherapy. Photomed Laser Surg 2005;23(4):355–61.10.1089/pho.2005.23.355Search in Google Scholar
[14] Cho HJ, Lim SC, Kim SG, Kim YS, Kang SS, Choi SH, Cho YS, Bae CS. Effect of low-level laser therapy on osteoarthropathy in rabbit. In Vivo 2004;18(5):585–91.Search in Google Scholar
[15] Kushibiki T, Tajiri T, Ninomiya Y, Awazu K. Chondrogenic mRNA expression in prechondrogenic cells after blue laser irradiation. J Photochem Photobiol B 2010;98(3):211–5.10.1016/j.jphotobiol.2010.01.008Search in Google Scholar
[16] Guerino MR, Baranauskas V, Guerino AC, Parizotto N. Laser treatment of experimentally-induced chronic arthritis. Appl Surf Sci 2000;154:561–4.10.1016/S0169-4332(99)00460-2Search in Google Scholar
[17] Castano AP, Dai T, Yaroslavsky I, Cohen R, Apruzzese WA, Smotrich MH, Hamblin MR. Low-level laser therapy for zymosan-induced arthritis in rats: Importance of illumination time. Lasers Surg Med 2007;39(6):543–50.10.1002/lsm.20516Search in Google Scholar PubMed PubMed Central
[18] Lin HD, He CQ, Luo QL, Zhang JL, Zeng DX. The effect of low-level laser to apoptosis of chondrocyte and caspases expression, including caspase-8 and caspase-3 in rabbit surgery-induced model of knee osteoarthritis. Rheumatol Int 2012;32(3):759–66.10.1007/s00296-010-1629-5Search in Google Scholar PubMed
[19] Oliveira P, Santos AA, Rodrigues T, Tim CR, Pinto KZ, Magri AMP, Fernandes KR, Mattiello SM, Parizotto NA, Anibal FF, Renno ACM. Effects of phototherapy on cartilage structure and inflammatory markers in an experimental model of osteoarthritis. J Biomed Opt 2013;18(12):128004.10.1117/1.JBO.18.12.128004Search in Google Scholar PubMed
[20] Delfino GB, Peviani SM, Durigan JL, Russo TL, Baptista IL, Ferretti M, Moriscot AS, Salvini TF. Quadriceps muscle atrophy after anterior cruciate ligament transection involves increased mRNA levels of atrogin-1, muscle ring finger 1, and myostatin. Am J Phys Med Rehabil 2013;92(5):411–9.10.1097/PHM.0b013e3182643f82Search in Google Scholar PubMed
[21] Renner AF, Carvalho E, Soares E, Mattiello-Rosa S. The effect of a passive muscle stretching protocol on the articular cartilage. Osteoarthritis Cartilage 2006;14(2):196–202.10.1016/j.joca.2005.08.011Search in Google Scholar PubMed
[22] Mankin HJ, Dorfman H, Lippiello L, Zarins A. Biochemical and metabolic abnormalities in articular cartilage from osteo-arthritic human hips. II. Correlation of morphology with biochemical and metabolic data. J Bone Joint Surg Am 1971;53(3):523–37.10.2106/00004623-197153030-00009Search in Google Scholar
[23] Pritzker KP, Gay S, Jimenez SA, Ostergaard K, Pelletier JP, Revell PA, Salter D, van den Berg WB. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage 2006;14(1):13–29.10.1016/j.joca.2005.07.014Search in Google Scholar
[24] Junqueira LC, Montes GS, Sanchez EM. The influence of tissue section thickness on the study of collagen by the Picrosirius-polarization method. Histochemistry 1982;74(1):153–6.10.1007/BF00495061Search in Google Scholar
[25] Montes GS. Structural biology of the fibres of the collagenous and elastic systems. Cell Biol Int 1996;20(1):15–27.10.1006/cbir.1996.0004Search in Google Scholar
[26] Andrade GB, Montes GS, Conceição GM, Saldiva PH. Use of the Picrosirius-polarization method to age fibrotic lesions in the hepatic granulomas produced in experimental murine schistosomiasis. Ann Trop Med Parasitol 1999;93(3):265–72.10.1080/00034983.1999.11813422Search in Google Scholar
[27] Garavello-Freitas I, Baranauskas V, Joazeiro PP, Padovani CR, Dal Pai-Silva M, da Cruz-Höfling MA. Low-power laser irradiation improves histomorphometrical parameters and bone matrix organization during tibia wound healing in rats. J Photochem Photobiol B 2003;70(2):81–9.10.1016/S1011-1344(03)00058-7Search in Google Scholar
[28] Vasilceac FA, Renner AF, Teodoro WR, Mattiello-Rosa SM. The remodeling of collagen fibers in rats ankles submitted to immobilization and muscle stretch protocol. Rheumatol Int 2011;31(6):737–42.10.1007/s00296-010-1371-zSearch in Google Scholar
[29] Torricelli P, Giavaresi G, Fini M, Guzzardella GA, Morrone G, Carpi A, Giardino R. Laser biostimulation of cartilage: in vitro evaluation. Biomed Pharmacother 2001;55(2):117–20.10.1016/S0753-3322(00)00025-1Search in Google Scholar
[30] Carter DR, Beaupré GS, Wong M, Smith RL, Andriacchi TP, Schurman DJ. The mechanobiology of articular cartilage development and degeneration. Clin Orthop Relat Res 2004;(427 Suppl):S69–77.10.1097/01.blo.0000144970.05107.7eSearch in Google Scholar PubMed
[31] Alfredo PP, Bjordal JM, Dreyer SH, Meneses SR, Zaguetti G, Ovanessian V, Fukuda TY, Junior WS, Lopes Martins RÁ, Casarotto RA, Marques AP. Efficacy of low level laser therapy associated with exercises in knee osteoarthritis: a randomized double-blind study. Clin Rehabil 2012;26(6):523–33.10.1177/0269215511425962Search in Google Scholar PubMed
[32] Fujita I, Hirata S, Ishikawa H, Mizuno K, Itoh H. Apoptosis of hypertrophic chondrocytes in rat cartilaginous growth plate. J Orthop Sci 1997;2:328–33.10.1007/BF02488917Search in Google Scholar
[33] Kühn K, D’Lima DD, Hashimoto S, Lotz M. Cell death in cartilage. Osteoarthritis Cartilage 2004;12(1):1–16.10.1016/j.joca.2003.09.015Search in Google Scholar
[34] Thomas CM, Fuller CJ, Whittles CE, Sharif M. Chondrocyte death by apoptosis is associated with cartilage matrix degradation. Osteoarthritis Cartilage 2007;15(1):27–34.10.1016/j.joca.2006.06.012Search in Google Scholar
[35] Narmoneva DA, Cheung HS, Wang JY, Howell DS, Setton LA. Altered swelling behavior of femoral cartilage following joint immobilization in a canine model. J Orthop Res 2002;20(1):83–91.10.1016/S0736-0266(01)00076-6Search in Google Scholar
[36] Gottlieb T, Jorgensen B, Rohde E, Müller G, Scheller EE. The influence of irradiation low-level diode laser on the proteoglycan content in arthritically cartilage in rabbits. Med Laser Appl 2006;21(1):53–59.10.1016/j.mla.2005.12.004Search in Google Scholar
[37] Lin YS, Huang MH, Chai CY. Effects of helium-neon laser on the mucopolysaccharide induction in experimental osteoarthritic cartilage. Osteoarthritis Cartilage 2006;14(4):377–83.10.1016/j.joca.2005.10.010Search in Google Scholar
[38] O’Connor KM. Unweighting accelerates tidemark advancement in articular cartilage at the knee joint of rats. J Bone Miner Res 1997;12(4):580–9.10.1359/jbmr.1997.12.4.580Search in Google Scholar
[39] Leroux MA, Cheung HS, Bau JL, Wang JY, Howell DS, Setton LA. Altered mechanics and histomorphometry of canine tibial cartilage following joint immobilization. Osteoarthritis Cartilage 2001;9(7):633–40.10.1053/joca.2001.0432Search in Google Scholar
[40] Setton LA, Mow VC, Müller FJ, Pita JC, Howell DS. Mechanical behavior and biochemical composition of canine knee cartilage following periods of joint disuse and disuse with remobilization. Osteoarthritis Cartilage 1997;5(1):1–16.10.1016/S1063-4584(97)80027-1Search in Google Scholar
[41] Velosa AP, Teodoro WR, Yoshinari NH. Colágeno na cartilagem osteoartrósica. Rev Bras Reumatol 2003;43:160–6.10.1590/S0482-50042003000300006Search in Google Scholar
[42] Dias CN, Renner AF, dos Santos AA, Vasilceac FA, Mattiello SM. Progression of articular cartilage degeneration after application of muscle stretch. Connect Tissue Res 2012;53(1):39–47.10.3109/03008207.2011.610476Search in Google Scholar
[43] Abramson SB, Attur M. Developments in the scientific understanding of osteoarthritis. Arthritis Res Ther 2009;11(3):227–35.10.1186/ar2655Search in Google Scholar
[44] Tang BL. ADAMTS: a novel family of extracellular matrix proteases. Int J Biochem Cell Biol 2001;33(1):33–44.10.1016/S1357-2725(00)00061-3Search in Google Scholar
[45] Arner EC. Aggrecanase-mediated cartilage degradation. Curr Opin Pharmacol 2002;2(3):322–9.10.1016/S1471-4892(02)00148-0Search in Google Scholar
[46] Glasson SS, Askew R, Sheppard B, Carito B, Blanchet T, Ma HL, Flannery CR, Peluso D, Kanki K, Yang Z, Majumdar MK, Morris EA. Deletion of active ADAMTS5 prevents cartilage degradation in a murine model of osteoarthritis. Nature 2005;434(7033):644–8.10.1038/nature03369Search in Google Scholar PubMed
[47] Peter WF, Jansen MJ, Hurkmans EJ, Bloo H, Dekker J, Dilling RG, Hilberdink W, Kersten-Smit C, de Rooij M, Veenhof C, Vermeulen HM, de Vos RJ, Schoones JW, Vliet Vlieland TP; Guideline Steering Committee-Hip and Knee Osteoarthritis. Physiotherapy in hip and knee osteoarthritis: development of a practice guideline concerning initial assessment, treatment and evaluation. Acta Reumatol Port 2011;36(3):268–81.Search in Google Scholar
[48] Guo H, Luo Q, Zhang J, Lin H, Xia L, He C. 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 2011;78(6):604–10.10.1016/j.jbspin.2011.01.009Search in Google Scholar PubMed
©2014 Walter de Gruyter GmbH, Berlin/Boston