Advertisement

Lasers in Medical Science

, 26:803 | Cite as

Phototherapy with low-level laser affects the remodeling of types I and III collagen in skeletal muscle repair

  • Thais Oricchio Fedri de Souza
  • Dayane Aparecida Mesquita
  • Raquel Agnelli Mesquita Ferrari
  • Décio dos Santos PintoJr
  • Luciana Correa
  • Sandra Kalil Bussadori
  • Kristianne Porta Santos Fernandes
  • Manoela Domingues MartinsEmail author
Original Article

Abstract

The purpose of this article was to analyze the photobiomodulator role of low-level laser therapy (LLLT) on the skeletal muscle remodeling following cryoinjury in rats, focusing the types I and III collagen proteins. Laser phototherapy has been employed to stimulate repair in different tissues. However, its role in skeletal muscle remodeling is not yet well clarified, especially its effect on the collagen component of the extracellular matrix. Fifty adult Wistar rats were divided into four groups: control, sham, cryoinjury, and laser-treated cryoinjury. Laser irradiation was performed three times a week on the injured region using the InGaAlP (indium-gallium-aluminum-phosphorous) laser (660 nm; beam spot of 0.04 cm2, output power of 20 mW, power density of 0.5 mW/cm2, energy density of 5 J/cm2, 10-s exposure time, with a total energy dose of 0.2 J). Five animals were killed after short-term (days 1 and 7) and long-term (14 and 21) durations following injury. The muscles were processed and submitted to hematoxylin and eosin (H&E) and immunohistochemical staining. The histological slices were analyzed qualitatively, semi-quantitatively, and quantitatively. The data were submitted to statistical analysis using the Kruskal-Wallis test. The qualitative analysis of morphological aspects revealed that the muscle repair were very similar in cryoinjury and laser groups on days 1, 14 and 21. However, at 7 days, differences could be observed because there was a reduction in myonecrosis associated to formation of new vessels (angiogenesis) in the laser-treated group. The analysis of the distribution of types I and III collagen, on day 7, revealed a significant increase in the depositing of these proteins in the laser-treated group when compared to the cryoinjury group. InGaAlP diode laser within the power parameters and conditions tested had a biostimulatory effect at the regenerative and fibrotic phases of the skeletal muscle repairs, by promoting angiogenesis, reducing myonecrosis, and inducing types I and III collagen synthesis, following cryoinjury in rat.

Keywords

Skeletal muscle Remodeling Low-level laser therapy Muscle repair Collagen 

Notes

Acknowledgments

The authors are grateful to the Brazilian fostering agency Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) (process no 07/55439-6). We thank Richard Boike for his helpful comments and expertise with the English grammar.

Author disclosure statement

The authors declare that there are no competing financial interests.

References

  1. 1.
    Huard J, Li Y, Fu FH (2002) Muscle injuries and repair: current trends in research. J Bone Joint Surg Am 84-A:822–32PubMedGoogle Scholar
  2. 2.
    Carmeli E, Moas M, Reznick AZ, Coleman R (2004) Matrix metalloproteinases and skeletal muscle: a brief review. Muscle Nerve 29:191–197PubMedCrossRefGoogle Scholar
  3. 3.
    Kjaer M (2004) Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol Rev 84:649–98PubMedCrossRefGoogle Scholar
  4. 4.
    Chiquet M, Matthison M, Koch M, Tannheimer M, Chiquet-Ehrismann R (1996) Regulation of extracellular matrix synthesis by mechanical stress. Biochem Cell Biol 74:737–744PubMedCrossRefGoogle Scholar
  5. 5.
    Myllyla R, Myllyla VV, Tolonen U, Kivirikko KI (1982) Changes in collagen metabolism in diseased muscle. I. Biochemical studies. Arch Neurol 39:752–755PubMedGoogle Scholar
  6. 6.
    Han XY, Wang W, Komulainen J, Koskinen SO, Kovanen V (1999) VihkoV, Trackman PC, Takala TE. Increased mRNAs for procollagens and key regulating enzymes in rat muscle following downhill running. Pflugers Arch 437:857–864PubMedCrossRefGoogle Scholar
  7. 7.
    Kovanen V, Suominen H, Risteli J, Risteli L (1988) Type IV collagen and laminin in slow and fast skeletal muscle in rats–effects of age and life-time endurance training. Coll Relat Res 8:145–53PubMedGoogle Scholar
  8. 8.
    Koskinen SOA, Wang W, Ahtikoski AM, Kjaer M, Han XY, Komulainen J, Kovanen V, Takala TES (2001) Acute exercise induced changes in rat skeletal muscle mRNAs and proteins regulating type IV collagen content. Am J Physio Regul Integr Comp Physiol 280:R1292–R1300Google Scholar
  9. 9.
    Ahtikoski AM, Tuominen H, Korpelainen JT, Takala TE, Oikarinen A (2004) Collagen synthesis and degradation in polyneuropathy and myopathies. Muscle Nerve 30:602–8PubMedCrossRefGoogle Scholar
  10. 10.
    Almeida-Lopes L, Rigau J, Zângaro RA, Guiduli-Neto J, Jaeger MMM (2001) Comparison of the low level therapy effects on cultured gingival fibroblasts proliferation using different irradiance and fluence. Lasers Surg Med 29:179–184PubMedCrossRefGoogle Scholar
  11. 11.
    Pereira AN, Eduardo CP, Matson E, Marques MM (2002) Effect of low-power laser irradiation on cell growth and procollagen synthesis of cultured fibroblasts. Lasers Surg Med 31:263–267PubMedCrossRefGoogle Scholar
  12. 12.
    Marques MM, Pereira AN, Fujihara NA, Nogueira FN, Eduardo CP (2004) Effect of low-power laser irradiation on protein synthesis and ultrastructure of human gingival fibroblasts. Lasers Surg Med 34:260–265PubMedCrossRefGoogle Scholar
  13. 13.
    Longo L, Evangelista S, Tinacci G, Sesti AG (1987) Effect of diodes-laser silver arsenide–aluminium (Ga–Al–As) 904 nm on healing of experimental wounds. Lasers Surg Med 7:444–447PubMedCrossRefGoogle Scholar
  14. 14.
    Liu XG, Zhou YJ, Liu TC, Yuan JQ (2009) Effects of low-level laser irradiation on rat skeletal muscle injury after eccentric exercise. Photomed Laser Surg Aug 21Google Scholar
  15. 15.
    Lopes-Martins RA, Marcos RL, Leonardo PS, Prianti AC Jr (2006) Muscará MN, Aimbire F, Frigo L, Iversen VV, Bjordal JM Effect of low-level laser (Ga-Al-As 655 nm) on skeletal muscle fatigue induced by electrical stimulation in rats. J Appl Physiol 101:283–8PubMedCrossRefGoogle Scholar
  16. 16.
    Sussai DA, Carvalho Pde T, Dourado DM, Belchior AC, dos Reis FA (2010) Low-level laser therapy attenuates creatine kinase levels and apoptosis during forced swimming in rats. Lasers Med Sci 25:115–20PubMedCrossRefGoogle Scholar
  17. 17.
    Reinoso C, Cremonezzi D, Moya M, Soriano F, Palma J, Campana V (2010) Helium–neon laser reduces the inflammatory process of arthritis. Photomed Laser Surg 28:125–129CrossRefGoogle Scholar
  18. 18.
    Giuliani A, Fernandez M, Farinelli M, Baratto L, Capra R, Rovetta G, Monteforte P, Giardino L, Calzà L (2004) Very low level laser therapy attenuates edema and pain in experimental models. Int J Tissue React 26:29-37.PubMedGoogle Scholar
  19. 19.
    Brosseau L, Wells G, Marchand S, Gaboury I, Stokes B, Morin M, Casimiro L, Yonge K, Tugwell P (2005) Randomized controlled trial on low level laser therapy (LLLT) in the treatment of osteoarthritis (OA) on the hand. Laser Surg Med 36:210–219CrossRefGoogle Scholar
  20. 20.
    Miyabara EH, Aoki MS, Soares AG, Moriscot AS (2005) Expression of tropism-related genes in regenerating skeletal muscle of rats treated with cyclosporin-A. Cell Tissue Res 319:479–489PubMedCrossRefGoogle Scholar
  21. 21.
    Baptista J, Martins MD, Pavesi VC, Bussadori SK, Fernandes KP, Pinto Júnior Ddos S, Ferrari RA (2011) Influence of laser photobiomodulation on collagen IV during skeletal muscle tissue remodeling after injury in rats. Photomed Laser Surg 29:11–7PubMedCrossRefGoogle Scholar
  22. 22.
    Mesquita-Ferrari RA, Martins MD, Silva JA Jr, da Silva TD, Piovesan RF, Pavesi VC, Bussadori SK, Fernandes KP (2011) Effects of low-level laser therapy on expression of TNF-α and TGF-β in skeletal muscle during the repair process. Lasers Med Sci 26:335–40PubMedCrossRefGoogle Scholar
  23. 23.
    Walker RA (2006) Quantification of immunohistochemistry-issues concerning methods, utility and semiquantitative assessment I. Histochemistry 49:406–410Google Scholar
  24. 24.
    Reilly T, Ekblom B (2005) The use of recovery methods post-exercise. J Sports Sci 23:619–627PubMedCrossRefGoogle Scholar
  25. 25.
    Bibikova A, Oron U (1995) Regeneration in denervated toad (bufoviridis) gastrocnemius muscle and the promotion of the process by low energy laser irradiation. Anat Rec 241:123–128PubMedCrossRefGoogle Scholar
  26. 26.
    Barbosa AM, Villaverde AB, Sousa LG, Munin E, Fernandez CM, Cogo JC, Zamuner SR (2009) Effect of low-level laser therapy in the myonecrosis induced by Bothrops jararacussu snake venom. Photomed Laser Surg 27:591–7PubMedCrossRefGoogle Scholar
  27. 27.
    Dourado DM, Favero S, Baranauskas V, Cruz-Hofling MA (2003) Effects of the GaAs laser irradiation on myonecrosis caused by Bothrops moojeni snake venom. Lasers Surg Med 33:352–357PubMedCrossRefGoogle Scholar
  28. 28.
    Deveci D, Marshall JM, Egginton S (2002) Chronic hypoxia induces prolonged angiogenesis in skeletal muscles of rat. Exp Physiol 87:287–291PubMedCrossRefGoogle Scholar
  29. 29.
    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 23:470–5PubMedCrossRefGoogle Scholar
  30. 30.
    Nakano J, Kataoka H, Sakamoto J, Origuchi T, Okita M, Yoshimura T (2009) Low-level laser irradiation promotes the recovery of atrophied gastrocnemius skeletal muscle in rats. Exp Physiol 94:1005–15PubMedCrossRefGoogle Scholar
  31. 31.
    Smith LE, Shen W, Perruzzi C, Soker S, Kinose F, Xu X, Robinson G, Driver S, Bischoff J, Zhang B, Schaeffer JM, Senger DR (1999) Regulation of vascular endothelial growth factor-dependent retinal neovascularization by insulin-like growth factor-1 receptor. Nat Med 5:1390–1395PubMedCrossRefGoogle Scholar
  32. 32.
    Weiss N, Oron U (1992) Enhancement of muscle regeneration in the rat gastrocnemius by low energy laser irradiation. Anat Embryol 186:497–503PubMedCrossRefGoogle Scholar
  33. 33.
    Amaral AC, Parizotto NA, Salvini TF (2001) Dose-dependency of low-energy HeNe laser effect in regeneration of skeletal muscle in mice. Lasers Med Sci 16:44–51PubMedCrossRefGoogle Scholar
  34. 34.
    Gallegly JC, Turesky NA, Strotman BA, Gurley CM, Peterson CA, Dupont-Versteegden EE (2004) Satellite cell regulation of muscle mass is altered at old age. J Appl Physiol 97:1082–1090PubMedCrossRefGoogle Scholar
  35. 35.
    Yu W, Naim JO, McGowan M, Ippolito K, Lanzafame RJ (1997) Photomodulation of oxidative metabolism and electron chain enzymes in rat liver mitochondria. Photochem Photobiol 66:866–871PubMedCrossRefGoogle Scholar
  36. 36.
    Leal Junior EC, Lopes-Martins RA, de Almeida P, Ramos L, Iversen VV, Bjordal JM (2010) Effect of low-level laser therapy (GaAs 904 nm) in skeletal muscle fatigue and biochemical markers of muscle damage in rats. Eur J Appl Physiol 108:1083–1088PubMedCrossRefGoogle Scholar
  37. 37.
    Cressoni MD, Dib Giusti HH, Casarotto RA, Anaruma CA (2008) The effects of a 785-nm AlGaInP laser on the regeneration of ratanterior tibialis muscle after surgically-induced injury. Photomed Laser Surg (Ahead of print). doi: 10.1089/pho.2007.2150
  38. 38.
    Iyomasa DM, Garavelo I, Iyomasa MM, Watanabe IS, Issa JP (2009) Ultrastructural analysis of the low level laser therapy effects on the lesioned anterior tibial muscle in the gerbil. Micron 40:413–8PubMedCrossRefGoogle Scholar
  39. 39.
    Youn SR, Dyson M (1990) The effect of therapeutic ultrasound on angiogenesis. Ultrasound Med Biol 16:261–269CrossRefGoogle Scholar
  40. 40.
    Silveira PC, Silva LA, Fraga DB, Freitas TP, Streck EL, Pinho R (2009) Evaluation of mitochondrial respiratory chain activity in muscle healing by low-level laser therapy. J Photochem Photobiol B 95:89–92PubMedCrossRefGoogle Scholar
  41. 41.
    Pugliese LS, Medrado AP, Reis SR, Andrade Zde A (2003) The influence of low-level laser therapy on biomodulation of collagen and elastic fibers. Pesqui Odontol Bras 17:307–13PubMedCrossRefGoogle Scholar
  42. 42.
    Yamamoto Y, Kono T, Kotani H, Kasai S, Mito M (1996) Effect of low-power laser irradiation on procollagen synthesis in human fibroblasts. J Clin Laser Med Surg 14:129–32PubMedGoogle Scholar
  43. 43.
    Purslow PP (1989) Strain-induced reorientation of an intramuscular connective tissue network: implications for passive muscle elasticity. J Biomech 22:21–31PubMedCrossRefGoogle Scholar
  44. 44.
    Yew DT, Li WW, Pang KM, Mok YC, Au C (1989) Stimulation of collagen formation in the intestinal anastomosis by low dose He-Ne laser. Scanning Microsc 3:379–85PubMedGoogle Scholar
  45. 45.
    Reddy GK, Stehno-Bittel L, Enwemeka CS (1998) Laser photostimulation of collagen production in healing rabbit Achilles tendons. Lasers Surg Med 22:281–7PubMedCrossRefGoogle Scholar
  46. 46.
    Fillipin LI, Mauriz JL, Vedovelli K, Moreira AJ, Zettler CG, Lech O, Marroni NP, Gonzalez-Gallego J (2005) Low-level laser therapy (LLLT) prevents oxidative stress and reduces fibrosis in rat traumatized Achilles tendon. Lasers Surg Med 37:293–300PubMedCrossRefGoogle Scholar
  47. 47.
    Morrone G, Guzzardella Ga, Orienti L, Giavaresi G, Fini M, Rocca M, Torricelli P, Martini L, Giardino R (1998) Muscular trauma treated with a Ga-Al-As diode laser: In vivo experimental study. Lasers Med Sci 13:293–298CrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Ltd 2011

Authors and Affiliations

  • Thais Oricchio Fedri de Souza
    • 1
  • Dayane Aparecida Mesquita
    • 1
  • Raquel Agnelli Mesquita Ferrari
    • 1
  • Décio dos Santos PintoJr
    • 2
  • Luciana Correa
    • 2
  • Sandra Kalil Bussadori
    • 1
  • Kristianne Porta Santos Fernandes
    • 1
  • Manoela Domingues Martins
    • 3
    Email author
  1. 1.Rehabilitation SciencesUniversidade Nove de Julho - UNINOVESão PauloBrazil
  2. 2.Oral Pathology, School of DentistryUniversidade de São Paulo-FOUSPSão PauloBrazil
  3. 3.Oral Pathology, School of DentistryUniversidade Federal do Rio Grande do SulSantana, Porto AlegreBrazil

Personalised recommendations