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Published in: Lasers in Medical Science 4/2017

01-05-2017 | Original Article

Histomorphologic and ultrastructural recovery of myopathy in rats treated with low-level laser therapy

Authors: Natalia Servetto, David Cremonezzi, Juan Carlos Simes, Antonio Di Pietro, Vilma R. Campana

Published in: Lasers in Medical Science | Issue 4/2017

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Abstract

The purpose of the present work was to study the effect of low-level laser therapy (LLLT): helium-neon (He-Ne) and gallium arsenide (Ga-As) laser on the histomorphology of muscle and mitochondria in experimental myopathy in rats. Thirty Suquía strain female rats were distributed in groups: (A) control (intact), (B) injured, (C) injured and treated with He-Ne laser, (D) injured and treated with Ga-As laser, (E) irradiated with He-Ne laser on the non-injured muscle, and (F) irradiated with Ga-As laser on the non-injured muscle. Myopathy was induced by injecting 0.05 mg/rat/day of adrenaline in the left gastrocnemius muscle at the same point on five consecutive days, in groups B, C, and D. LLLT was applied with 9.5 J cm−2 daily for seven consecutive days in groups C, D, E, and F. The muscles were examined with optic and electronic microscopy. The inflammation was classified as absent, mild, and intense and the degree of mitochondrial alteration was graded I, II, III, and IV. Categorical data were statistically analyzed by Chi-square and the Fisher-Irwin Bilateral test, setting significant difference at p < 0.05. The damage found in muscle and mitochondria histomorphology in animals with induced myopathy (B) was intense or severe inflammation with grade III or IV of mitochondrial alteration. They underwent significant regression (p < 0.001) compared with the groups treated with He-Ne (C) and Ga-As (D) laser, in which mild or moderate inflammation was seen and mitochondrial alteration grades I and II, recovering normal myofibrillar architecture. No differences were found between the effects caused by the two lasers, or between groups A, E, and F. Group A was found to be different from B, C, and D (p < 0.001). LLLT in experimental myopathy caused significant muscular and mitochondrial morphologic recovery.
Literature
1.
go back to reference Kumar V, Abbas AK, Fausto N, Aster JC (2010) Enfermedades del sistema inmunitario. In: Robbins C (ed) Patología estructural y funcional, 8vath edn. Elsevier Saunders, España, pp 183–257 Kumar V, Abbas AK, Fausto N, Aster JC (2010) Enfermedades del sistema inmunitario. In: Robbins C (ed) Patología estructural y funcional, 8vath edn. Elsevier Saunders, España, pp 183–257
2.
go back to reference Ciciliot S, Schiaffino S (2010) Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr Pharm Des 16:906–914CrossRefPubMed Ciciliot S, Schiaffino S (2010) Regeneration of mammalian skeletal muscle. Basic mechanisms and clinical implications. Curr Pharm Des 16:906–914CrossRefPubMed
3.
go back to reference Salomonsson S, Lundberg I (2006) Cytokines in idiopathic inflammatory myopathies. Autoimmunity 39:177–190CrossRefPubMed Salomonsson S, Lundberg I (2006) Cytokines in idiopathic inflammatory myopathies. Autoimmunity 39:177–190CrossRefPubMed
4.
go back to reference Astrin J (2008) Understanding the idiopathic inflammatory myopathies. JAAPA 21:42–47PubMed Astrin J (2008) Understanding the idiopathic inflammatory myopathies. JAAPA 21:42–47PubMed
5.
go back to reference Stadhouders AM, Sengers RC (1987) Morphological observations in skeletal muscle from patients with a mitochondrial myopathy. J Inherit Metab Dis 10:62–80CrossRefPubMed Stadhouders AM, Sengers RC (1987) Morphological observations in skeletal muscle from patients with a mitochondrial myopathy. J Inherit Metab Dis 10:62–80CrossRefPubMed
6.
go back to reference Rygiel KA, Miller J, Grady JP, Rocha MC, Taylor RW, Turnbull DM (2014) Mitochondrial and inflammatory changes in sporadic inclusion body myositis. Neuropathol Appl Neurobiol 41:288–303CrossRef Rygiel KA, Miller J, Grady JP, Rocha MC, Taylor RW, Turnbull DM (2014) Mitochondrial and inflammatory changes in sporadic inclusion body myositis. Neuropathol Appl Neurobiol 41:288–303CrossRef
7.
go back to reference Loell I, Lundberg IE (2011) Can muscle regeneration fail in chronic inflammation: a weakness in inflammatory myopathies? J Intern Med 269:243–257CrossRefPubMed Loell I, Lundberg IE (2011) Can muscle regeneration fail in chronic inflammation: a weakness in inflammatory myopathies? J Intern Med 269:243–257CrossRefPubMed
8.
go back to reference Distad BJ, Amato AA, Weiss MD (2011) inflammatory myopathies. Curr Treat Options Neurol 13:119–130CrossRefPubMed Distad BJ, Amato AA, Weiss MD (2011) inflammatory myopathies. Curr Treat Options Neurol 13:119–130CrossRefPubMed
9.
go back to reference Kandulski A, Venerito M, Malfertheiner P (2009) Non-steroidal anti-inflammatory drugs (NSAIDs)—balancing gastrointestinal complications and the cardiovascular risk. Dtsch Med Wochenschr 134:1635–1640CrossRefPubMed Kandulski A, Venerito M, Malfertheiner P (2009) Non-steroidal anti-inflammatory drugs (NSAIDs)—balancing gastrointestinal complications and the cardiovascular risk. Dtsch Med Wochenschr 134:1635–1640CrossRefPubMed
10.
go back to reference Ziltener JL, Leal S, Fournier PE (2010) Non-steroidal anti-inflammatory drugs for athletes: an update. Ann Phys Rehabil Med 53:278–288CrossRefPubMed Ziltener JL, Leal S, Fournier PE (2010) Non-steroidal anti-inflammatory drugs for athletes: an update. Ann Phys Rehabil Med 53:278–288CrossRefPubMed
13.
go back to reference Gigo-Benato D, Russo TL, Tanaka EH, Assis L, Salvini TF, Parizotto NA (2010) Effects of 660 and 780 nm low-level laser therapy on neuromuscular recovery after crush injury in rat sciatic nerve. Lasers Surg Med 42:673–682CrossRefPubMed Gigo-Benato D, Russo TL, Tanaka EH, Assis L, Salvini TF, Parizotto NA (2010) Effects of 660 and 780 nm low-level laser therapy on neuromuscular recovery after crush injury in rat sciatic nerve. Lasers Surg Med 42:673–682CrossRefPubMed
14.
go back to reference 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 28:125–129CrossRefPubMed 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 28:125–129CrossRefPubMed
15.
go back to reference Servetto N, Cremonezzi D, Simes JC, Soriano F, Palma JA, Campana VR (2010) Evaluation of inflammatory biomarkers associated with oxidative stress and histological assessment of low level laser therapy in experimental myopathy. Lasers Surg Med 42:577–583CrossRefPubMed Servetto N, Cremonezzi D, Simes JC, Soriano F, Palma JA, Campana VR (2010) Evaluation of inflammatory biomarkers associated with oxidative stress and histological assessment of low level laser therapy in experimental myopathy. Lasers Surg Med 42:577–583CrossRefPubMed
16.
go back to reference Iyomasa DM, Garavelo I, Iyomasa MM, Watanabe IS, Issa JP (2009) Ultraestructural analysis of the low level laser therapy effects on the lesioned anterior tibial muscle in the gerbil. Micron 40:413–418CrossRefPubMed Iyomasa DM, Garavelo I, Iyomasa MM, Watanabe IS, Issa JP (2009) Ultraestructural analysis of the low level laser therapy effects on the lesioned anterior tibial muscle in the gerbil. Micron 40:413–418CrossRefPubMed
17.
18.
go back to reference Carroll JD, Milward MR, Cooper PR, Hadis M, Palin WM (2014) Developments in low level light therapy (LLLT) for dentistry. Dent Mater 30:465–475CrossRefPubMed Carroll JD, Milward MR, Cooper PR, Hadis M, Palin WM (2014) Developments in low level light therapy (LLLT) for dentistry. Dent Mater 30:465–475CrossRefPubMed
19.
go back to reference Albuquerque-Pontes GM, Vieira RP, Tomazoni SS, Caires CO, Nemeth V, Vanin AA, Santos LA, Pinto HD, Marcos RL, Bjordal JM, de Carvalho PT, Leal-Junior EC (2015) Effect of pre-irradiation with different doses, wavelengths, and application intervals of low-level laser therapy on cytochrome c oxidase activity in intact skeletal muscle of rats. Lasers Med Sci 30:59–66CrossRefPubMed Albuquerque-Pontes GM, Vieira RP, Tomazoni SS, Caires CO, Nemeth V, Vanin AA, Santos LA, Pinto HD, Marcos RL, Bjordal JM, de Carvalho PT, Leal-Junior EC (2015) Effect of pre-irradiation with different doses, wavelengths, and application intervals of low-level laser therapy on cytochrome c oxidase activity in intact skeletal muscle of rats. Lasers Med Sci 30:59–66CrossRefPubMed
20.
go back to reference Baez MC, Táran MD, Campana V, Simes JC, Pons P, Palma JA, Moya M (2009) Marcadores de estrés oxidativo en aterogénesis inducida por hiperfibrinogenemia. Arch Cardiol Mex 79:85–90PubMed Baez MC, Táran MD, Campana V, Simes JC, Pons P, Palma JA, Moya M (2009) Marcadores de estrés oxidativo en aterogénesis inducida por hiperfibrinogenemia. Arch Cardiol Mex 79:85–90PubMed
21.
go back to reference Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A–138A Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A–138A
22.
go back to reference Massa EM, Aoki A (1971) Simple method for purification of glutaraldehyde. Acta Physiol Lat Am 21:161–163PubMed Massa EM, Aoki A (1971) Simple method for purification of glutaraldehyde. Acta Physiol Lat Am 21:161–163PubMed
23.
go back to reference Báez AL, Lo Presti MS, Fretes R, Díaz C, Pons P, Bazán PC, Strauss M, Rivarola HW, Paglini-Oliva P (2013) Chronic indeterminate phase of Chagas’ disease: mitochondrial involvement in infection with two strains. Parasitology 140:414–421CrossRefPubMed Báez AL, Lo Presti MS, Fretes R, Díaz C, Pons P, Bazán PC, Strauss M, Rivarola HW, Paglini-Oliva P (2013) Chronic indeterminate phase of Chagas’ disease: mitochondrial involvement in infection with two strains. Parasitology 140:414–421CrossRefPubMed
24.
go back to reference Osadchii OE, Norton GR, McKechnie R, Deftereos D, Woodiwiss AJ (2007) Cardiac dilatation and pump dysfunction without intrinsic myocardial systolic failure following chronic beta adrenoreceptor activation. Am J Physiol Heart Circ Physiol 292:H1898–H1905CrossRefPubMed Osadchii OE, Norton GR, McKechnie R, Deftereos D, Woodiwiss AJ (2007) Cardiac dilatation and pump dysfunction without intrinsic myocardial systolic failure following chronic beta adrenoreceptor activation. Am J Physiol Heart Circ Physiol 292:H1898–H1905CrossRefPubMed
25.
go back to reference Parra Lara R, Matamala Vargas F, Silva Mella H (2007) Morphological effect of As.Ga laser irradiation on rat skeletal muscle. Int J Morphol 25:43–50CrossRef Parra Lara R, Matamala Vargas F, Silva Mella H (2007) Morphological effect of As.Ga laser irradiation on rat skeletal muscle. Int J Morphol 25:43–50CrossRef
27.
go back to reference 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 29:11–17CrossRefPubMed 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 29:11–17CrossRefPubMed
28.
go back to reference Karu TI (2003) Low power laser therapy. In: Vo-Dinh T (ed) Biomedical photonics hand-book Ch 48. CRC Press, Boca Raton, pp 1–25 Karu TI (2003) Low power laser therapy. In: Vo-Dinh T (ed) Biomedical photonics hand-book Ch 48. CRC Press, Boca Raton, pp 1–25
29.
go back to reference Zhang CP, Hao TL, Chen P, Liang J, Wang CZ, Kang HX, Gao RL, Fu SB (2011) Effect of low level laser irradiation on the proliferation of myoblasts—the skeletal muscle precursor cells: an experimental in vitro study. Laser Phys 21:2122–2127CrossRef Zhang CP, Hao TL, Chen P, Liang J, Wang CZ, Kang HX, Gao RL, Fu SB (2011) Effect of low level laser irradiation on the proliferation of myoblasts—the skeletal muscle precursor cells: an experimental in vitro study. Laser Phys 21:2122–2127CrossRef
30.
go back to reference Boveris DL, Boveris A (2007) Oxygen delivery to the tissues and mitochondrial respiration. Front Biosci 12:1014–1023CrossRefPubMed Boveris DL, Boveris A (2007) Oxygen delivery to the tissues and mitochondrial respiration. Front Biosci 12:1014–1023CrossRefPubMed
31.
go back to reference Ghafourifar P, Cadenas E (2005) Mitochondrial nitric oxide synthase. Trends Pharmacol Sci 26:190–195CrossRefPubMed Ghafourifar P, Cadenas E (2005) Mitochondrial nitric oxide synthase. Trends Pharmacol Sci 26:190–195CrossRefPubMed
32.
go back to reference Desmet KD, Paz DA, Corry JJ, Eells JT, Wong-Riley MT, Henry MM, Buchmann EV, Connelly MP, Dovi JV, Liang HL, Henshel DS, Yeager RL, Millsap DS, Lim J, Gould LJ, Das R, Jett M, Hodgson BD, Margolis D, Whelan HT (2006) Clinical and experimental applications of NIR-LED photobiomodulation. Photomed Laser Surg 24:121–128CrossRefPubMed Desmet KD, Paz DA, Corry JJ, Eells JT, Wong-Riley MT, Henry MM, Buchmann EV, Connelly MP, Dovi JV, Liang HL, Henshel DS, Yeager RL, Millsap DS, Lim J, Gould LJ, Das R, Jett M, Hodgson BD, Margolis D, Whelan HT (2006) Clinical and experimental applications of NIR-LED photobiomodulation. Photomed Laser Surg 24:121–128CrossRefPubMed
33.
go back to reference Rezende SB, Ribeiro MS, Núñez SC, Garcia VG, Maldonado EP (2007) Effects of a single near-infrared laser treatment on cutaneous wound healing: biometrical and histological study in rats. J Photochem Photobiol B 87:145–153CrossRefPubMed Rezende SB, Ribeiro MS, Núñez SC, Garcia VG, Maldonado EP (2007) Effects of a single near-infrared laser treatment on cutaneous wound healing: biometrical and histological study in rats. J Photochem Photobiol B 87:145–153CrossRefPubMed
34.
go back to reference Shefer G, Partridge T, Heslop L, Gross JG, Oron U, Halevy O (2002) Low-energy laser irradiation promotes the survival and cell cycle entry of skeletal muscle satellite cells. J Cell Sci 115:1461–1469PubMed Shefer G, Partridge T, Heslop L, Gross JG, Oron U, Halevy O (2002) Low-energy laser irradiation promotes the survival and cell cycle entry of skeletal muscle satellite cells. J Cell Sci 115:1461–1469PubMed
35.
go back to reference 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 94:1005–1015CrossRefPubMed 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 94:1005–1015CrossRefPubMed
36.
go back to reference Emelyanov AN, Kiryanova VV (2015) Photomodulation of proliferation and differentiation of stem cells by the visible and infrared light. Photomed Laser Surg 33:164–174CrossRefPubMed Emelyanov AN, Kiryanova VV (2015) Photomodulation of proliferation and differentiation of stem cells by the visible and infrared light. Photomed Laser Surg 33:164–174CrossRefPubMed
37.
go back to reference Lindgard A, Hultén LM, Svensson L, Soussi B (2007) Irradiation at 634 nm releases nitric oxide from human monocytes. Lasers Med Sci 22:30–36CrossRefPubMed Lindgard A, Hultén LM, Svensson L, Soussi B (2007) Irradiation at 634 nm releases nitric oxide from human monocytes. Lasers Med Sci 22:30–36CrossRefPubMed
38.
go back to reference Karu TI, Pyatibrat LV, Afanasyeva NI (2005) Cellular effects of low power therapy can be mediated by nitric oxide. Lasers Surg Med 36:307–314CrossRefPubMed Karu TI, Pyatibrat LV, Afanasyeva NI (2005) Cellular effects of low power therapy can be mediated by nitric oxide. Lasers Surg Med 36:307–314CrossRefPubMed
39.
go back to reference Abdel S, Abdel-Meguid I, Korraa SE (2007) Markers of oxidative stress and aging in Duchene muscular dystrophy patients and the possible ameliorating affect of He:Ne laser. Acta Myol 26:14–21PubMed Abdel S, Abdel-Meguid I, Korraa SE (2007) Markers of oxidative stress and aging in Duchene muscular dystrophy patients and the possible ameliorating affect of He:Ne laser. Acta Myol 26:14–21PubMed
40.
go back to reference Leal-Junior EC, de Almeida P, Tomazoni SS, de Carvalho PT, Lopes-Martins RÁ, Frigo L, Joensen J, Johnson MI, Bjordal JM (2014) Superpulsed low-level laser therapy protects skeletal muscle of mdx mice against damage, inflammation and morphological changes delaying dystrophy progression. PLoS One 5:e89453CrossRef Leal-Junior EC, de Almeida P, Tomazoni SS, de Carvalho PT, Lopes-Martins RÁ, Frigo L, Joensen J, Johnson MI, Bjordal JM (2014) Superpulsed low-level laser therapy protects skeletal muscle of mdx mice against damage, inflammation and morphological changes delaying dystrophy progression. PLoS One 5:e89453CrossRef
41.
go back to reference de Almeida P, Tomazoni SS, Frigo L, de Carvalho PT, Vanin AA, Santos LA, Albuquerque-Pontes GM, De Marchi T, Tairova O, Marcos RL, Lopes-Martins RÁ, 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 29:653–658CrossRefPubMed de Almeida P, Tomazoni SS, Frigo L, de Carvalho PT, Vanin AA, Santos LA, Albuquerque-Pontes GM, De Marchi T, Tairova O, Marcos RL, Lopes-Martins RÁ, 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 29:653–658CrossRefPubMed
42.
go back to reference Hayworth CR, Rojas JC, Padilla E, Holmes GM, Sheridan EC, Gonzalez-Lima F (2010) In vivo low-level light therapy increases cytochrome oxidase in skeletal muscle. Photochem Photobiol 86:673–680CrossRefPubMed Hayworth CR, Rojas JC, Padilla E, Holmes GM, Sheridan EC, Gonzalez-Lima F (2010) In vivo low-level light therapy increases cytochrome oxidase in skeletal muscle. Photochem Photobiol 86:673–680CrossRefPubMed
43.
go back to reference Santos LA, Marcos RL, Tomazoni SS, Vanin AA, Antonialli FC, Grandinetti Vdos S, Albuquerque-Pontes GM, de Paiva PR, Lopes-Martins RÁ, de Carvalho PT, Bjordal JM, Leal-Junior EC (2014) Effects of pre-irradiation of low-level laser therapy with different doses and wavelengths in skeletal muscle performance, fatigue, and skeletal muscle damage induced by tetanic contractions in rats. Lasers Med Sci 29:1617–1626CrossRefPubMed Santos LA, Marcos RL, Tomazoni SS, Vanin AA, Antonialli FC, Grandinetti Vdos S, Albuquerque-Pontes GM, de Paiva PR, Lopes-Martins RÁ, de Carvalho PT, Bjordal JM, Leal-Junior EC (2014) Effects of pre-irradiation of low-level laser therapy with different doses and wavelengths in skeletal muscle performance, fatigue, and skeletal muscle damage induced by tetanic contractions in rats. Lasers Med Sci 29:1617–1626CrossRefPubMed
44.
go back to reference de Almeida P, Lopes-Martins RÁ, Tomazoni SS, Albuquerque-Pontes GM, Santos LA, Vanin AA, Frigo L, Vieira RP, Albertini R, de Carvalho PT, Leal-Junior EC (2013) Low-level laser therapy and sodium diclofenac in acute inflammatory response induced by skeletal muscle trauma: effects in muscle morphology and mRNA gene expression of inflammatory markers. Photochem Photobiol 89:501–507CrossRefPubMed de Almeida P, Lopes-Martins RÁ, Tomazoni SS, Albuquerque-Pontes GM, Santos LA, Vanin AA, Frigo L, Vieira RP, Albertini R, de Carvalho PT, Leal-Junior EC (2013) Low-level laser therapy and sodium diclofenac in acute inflammatory response induced by skeletal muscle trauma: effects in muscle morphology and mRNA gene expression of inflammatory markers. Photochem Photobiol 89:501–507CrossRefPubMed
45.
go back to reference de Almeida P, Lopes-Martins RÁ, Tomazoni SS, Silva JA Jr, de Carvalho PT, Bjordal JM, Leal Junior EC (2011) Low-level laser therapy improves skeletal muscle performance, decreases skeletal muscle damage and modulates mRNA expression of COX-1 and COX-2 in a dose-dependent manner. Photochem Photobiol 87:1159–1163CrossRefPubMed de Almeida P, Lopes-Martins RÁ, Tomazoni SS, Silva JA Jr, de Carvalho PT, Bjordal JM, Leal Junior EC (2011) Low-level laser therapy improves skeletal muscle performance, decreases skeletal muscle damage and modulates mRNA expression of COX-1 and COX-2 in a dose-dependent manner. Photochem Photobiol 87:1159–1163CrossRefPubMed
Metadata
Title
Histomorphologic and ultrastructural recovery of myopathy in rats treated with low-level laser therapy
Authors
Natalia Servetto
David Cremonezzi
Juan Carlos Simes
Antonio Di Pietro
Vilma R. Campana
Publication date
01-05-2017
Publisher
Springer London
Published in
Lasers in Medical Science / Issue 4/2017
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-017-2182-1

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