Skip to main content
Erschienen in: Lasers in Medical Science 6/2015

01.08.2015 | Original Article

Effect of low-level laser therapy on lung injury induced by hindlimb ischemia/reperfusion in rats

verfasst von: Mohammad Ashrafzadeh Takhtfooladi, Hamed Ashrafzadeh Takhtfooladi, Hamidreza Sedaghatfar, Samaneh Shabani

Erschienen in: Lasers in Medical Science | Ausgabe 6/2015

Einloggen, um Zugang zu erhalten

Abstract

To investigate the effect of low-level laser therapy (LLLT 650 nm) on the lung remote organ injury induced by hindlimb ischemia/reperfusion (I/R). The experiments were performed on 50 healthy mature male Wistar rats weighing mean 230 ± 20 g. The rats were randomly allocated into five equal groups as follows: normal group (animals nonmanipulated), sham group (operated with no ischemia), laser group (animals nonmanipulated and irradiated with laser), I/R group, and I/R + LLLT group. Rats were prepared for sterile surgery, and then, right hindlimbs were subjected to I/R induced by the femoral artery occlusion for duration of 120 min, followed by a 60-min reperfusion. The LLLT (K30 handheld probe, AZOR, Technica, Russia, 650 nm, 30 mW, surface area = 1 cm2, 60 S/cm2, energy density = 1.8 J/cm2) was carried out by irradiating the rats over a unique point on the skin over the right upper bronchus for 5 and 15 min after initiating reperfusion for 3 min. At the end of the trial, rats were euthanized under deep anesthesia and the right lung tissues were removed. Myeloperoxidase (MPO) and superoxide dismutase (SOD) activities and nitric oxide (NO), malondialdehyde (MDA), and glutathione (GSH) levels were measured in the lung tissues. The tissue samples were further examined histopathologically under light microscopy. It was found that I/R elevated MPO activity, MDA, and NO levels accompanied by a reduction in SOD activities and GSH levels (P < 0.05). LLLT restored MDA and NO levels, MPO and SOD activity, GSH levels, and lung injury scores (P < 0.05). In light of these findings, the LLLT has alleviated the lung tissue injuries after skeletal muscle I/R in this experimental model.
Literatur
1.
Zurück zum Zitat Haapaniemi T, Sirsjo A, Nylander G, Larsson J (1995) Hyperbaric oxygen treatment attenuates glutathione depletion and improves metabolic restitution in postischemic skeletal muscle. Free Radic Res 23(2):91–101PubMedCrossRef Haapaniemi T, Sirsjo A, Nylander G, Larsson J (1995) Hyperbaric oxygen treatment attenuates glutathione depletion and improves metabolic restitution in postischemic skeletal muscle. Free Radic Res 23(2):91–101PubMedCrossRef
2.
Zurück zum Zitat Blaisdell FW (2002) The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc Surg 10(6):620–630PubMedCrossRef Blaisdell FW (2002) The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc Surg 10(6):620–630PubMedCrossRef
3.
Zurück zum Zitat Esme H, Fidan H, Koken T, Solak O (2006) Effect of lung ischemia reperfusion on oxidative stress parameters of remote tissues. Eur J Cardiothorac Surg 29(3):294–298PubMedCrossRef Esme H, Fidan H, Koken T, Solak O (2006) Effect of lung ischemia reperfusion on oxidative stress parameters of remote tissues. Eur J Cardiothorac Surg 29(3):294–298PubMedCrossRef
4.
Zurück zum Zitat Ben-Abraham R, Guttman M, Flaishon R, Marouani N, Niv D, Weinbroum AA (2006) Mesenteric artery clamping/unclamping-induced acute lung injury is attenuated by N-methyl-D-aspartate antagonist dextromethorphan. Lung 184(6):309–317PubMedCrossRef Ben-Abraham R, Guttman M, Flaishon R, Marouani N, Niv D, Weinbroum AA (2006) Mesenteric artery clamping/unclamping-induced acute lung injury is attenuated by N-methyl-D-aspartate antagonist dextromethorphan. Lung 184(6):309–317PubMedCrossRef
5.
Zurück zum Zitat McCord JM (1985) Oxygen-derived free radicals in post ischemic tissue injury. N Engl J Med 312(8):159–160PubMed McCord JM (1985) Oxygen-derived free radicals in post ischemic tissue injury. N Engl J Med 312(8):159–160PubMed
6.
Zurück zum Zitat Abergel RP, Lyons RF, Castel JC, Dwyer RM, Uitto J (1987) Biostimulation of wound healing by laser: experimental approaches in animal models and in fibroblast cultures. Dermatol Surg Oncol 13:127–133CrossRef Abergel RP, Lyons RF, Castel JC, Dwyer RM, Uitto J (1987) Biostimulation of wound healing by laser: experimental approaches in animal models and in fibroblast cultures. Dermatol Surg Oncol 13:127–133CrossRef
7.
Zurück zum Zitat Takhtfooladi MA, Jahanbakhsh F, Takhtfooladi HA, Yousefi K, Allahverdi A (2015) Effect of low-level laser therapy (685 nm, 3 J/cm2) on functional recovery of the sciatic nerve in rats following crushing lesion. Lasers Med Sci 30:1047–1052PubMedCrossRef Takhtfooladi MA, Jahanbakhsh F, Takhtfooladi HA, Yousefi K, Allahverdi A (2015) Effect of low-level laser therapy (685 nm, 3 J/cm2) on functional recovery of the sciatic nerve in rats following crushing lesion. Lasers Med Sci 30:1047–1052PubMedCrossRef
8.
Zurück zum Zitat Ivaniuta OM, Dziublik AI, Skopichenko VN (1992) Optimal effectiveness of complex treatment of patients with chronic obstructive bronchitis by intravascular laser irradiation of blood. Probl Tuberk 6:21–24 Ivaniuta OM, Dziublik AI, Skopichenko VN (1992) Optimal effectiveness of complex treatment of patients with chronic obstructive bronchitis by intravascular laser irradiation of blood. Probl Tuberk 6:21–24
9.
Zurück zum Zitat Vasil’ev AP, Strel’tsova NN, Shakhov GG, Nikitina VI (1992) The effect of laser irradiation of the blood on the adenosine triphosphatase activity of the erythrocyte membranes and on the cardiac activity indices in patients with ischemic heart disease. Vrach Delo 6:61–64 Vasil’ev AP, Strel’tsova NN, Shakhov GG, Nikitina VI (1992) The effect of laser irradiation of the blood on the adenosine triphosphatase activity of the erythrocyte membranes and on the cardiac activity indices in patients with ischemic heart disease. Vrach Delo 6:61–64
10.
Zurück zum Zitat Gourgouliatos ZF, Welch AJ, Diller KR, Aggarwal SJ (1990) Laser irradiation-induced relaxation of blood vessels in vivo. Lasers Surg Med 10:524–532PubMedCrossRef Gourgouliatos ZF, Welch AJ, Diller KR, Aggarwal SJ (1990) Laser irradiation-induced relaxation of blood vessels in vivo. Lasers Surg Med 10:524–532PubMedCrossRef
11.
Zurück zum Zitat Morimoto Y, Arai T, Kikuchi M, Nakajima S, Nakamura H (1994) Effect of low-intensity argon laser irradiation on mitochondrial respiration. Lasers Surg Med 15:191–199PubMedCrossRef Morimoto Y, Arai T, Kikuchi M, Nakajima S, Nakamura H (1994) Effect of low-intensity argon laser irradiation on mitochondrial respiration. Lasers Surg Med 15:191–199PubMedCrossRef
12.
Zurück zum Zitat Yu W, Naim JO, Lanzafame RJ (1995) The effect of photo-irradiation (laser) on lymphocyte proliferation and ATP production in vitro. FASEB J 9(3 Pt I):A239 Yu W, Naim JO, Lanzafame RJ (1995) The effect of photo-irradiation (laser) on lymphocyte proliferation and ATP production in vitro. FASEB J 9(3 Pt I):A239
13.
Zurück zum Zitat Pacholewicz JK, Ianuzzo CD, Bokhua MR, Ianuzzo SE, Daloisio C, McGrath LB (1994) A novel method for myocardial infarction modification utilizing a helium-neon laser. Lasers Surg Med Suppl 6:65 Pacholewicz JK, Ianuzzo CD, Bokhua MR, Ianuzzo SE, Daloisio C, McGrath LB (1994) A novel method for myocardial infarction modification utilizing a helium-neon laser. Lasers Surg Med Suppl 6:65
14.
Zurück zum Zitat Salansky N, Brill G, Filonenko N (1994) Blood indexes changes under low energy photon (LEP) irradiation in vivo experiments. Lasers Surg Med Suppl 6:9 Salansky N, Brill G, Filonenko N (1994) Blood indexes changes under low energy photon (LEP) irradiation in vivo experiments. Lasers Surg Med Suppl 6:9
15.
Zurück zum Zitat Chi LH, Yu W, Naim JO, Lanzafame RJ (1995) Increased synthesis of nitric oxide by laser irradiation in sepsis. Lasers Surg Med Suppl 7:19 Chi LH, Yu W, Naim JO, Lanzafame RJ (1995) Increased synthesis of nitric oxide by laser irradiation in sepsis. Lasers Surg Med Suppl 7:19
16.
Zurück zum Zitat Takhtfooladi MA, Takhtfooladi HA, Khansari M (2014) The effects of low-intensity laser therapy on hepatic ischemia-reperfusion injury in a rat model. Lasers Med Sci 29(6):1887–1893PubMedCrossRef Takhtfooladi MA, Takhtfooladi HA, Khansari M (2014) The effects of low-intensity laser therapy on hepatic ischemia-reperfusion injury in a rat model. Lasers Med Sci 29(6):1887–1893PubMedCrossRef
17.
Zurück zum Zitat de Lima FM, Vitoretti L, Coelho F, Albertini R, Breithaupt-Faloppa AC, de Lima WT, Aimbire F (2013) Suppressive effect of low-level laser therapy on tracheal hyperresponsiveness and lung inflammation in rat subjected to intestinal ischemia and reperfusion. Lasers Med Sci 28(2):551–564PubMedCrossRef de Lima FM, Vitoretti L, Coelho F, Albertini R, Breithaupt-Faloppa AC, de Lima WT, Aimbire F (2013) Suppressive effect of low-level laser therapy on tracheal hyperresponsiveness and lung inflammation in rat subjected to intestinal ischemia and reperfusion. Lasers Med Sci 28(2):551–564PubMedCrossRef
18.
Zurück zum Zitat Koksel O, Yildirim C, Cinel L, Tamer L, Ozdulger A, Bastürk M, Degirmenci U, Kanik A, Cinel I (2005) Inhibition of poly (ADP-ribose) polymerase attenuates lung tissue damage after hind limb ischemia-reperfusion in rats. Pharmacol Res 51(5):453–462PubMedCrossRef Koksel O, Yildirim C, Cinel L, Tamer L, Ozdulger A, Bastürk M, Degirmenci U, Kanik A, Cinel I (2005) Inhibition of poly (ADP-ribose) polymerase attenuates lung tissue damage after hind limb ischemia-reperfusion in rats. Pharmacol Res 51(5):453–462PubMedCrossRef
19.
Zurück zum Zitat Wei H, Frenkel K (1993) Relationship of oxidative events and DNA oxidation in SENCAR mice to in vivo promoting activity of phorbol ester-type tumor promoters. Carcinogenesis 14:1195–1201PubMedCrossRef Wei H, Frenkel K (1993) Relationship of oxidative events and DNA oxidation in SENCAR mice to in vivo promoting activity of phorbol ester-type tumor promoters. Carcinogenesis 14:1195–1201PubMedCrossRef
20.
Zurück zum Zitat Cortas NK, Wakid NW (1990) Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction method. Clin Chem 36:1440–1443PubMed Cortas NK, Wakid NW (1990) Determination of inorganic nitrate in serum and urine by a kinetic cadmium-reduction method. Clin Chem 36:1440–1443PubMed
21.
Zurück zum Zitat Winterbourn CC, Hawkins RE, Brian M, Carrell RW (1975) The estimation of red cell superoxide dismutase activity. J Lab Clin Med 85:337–341PubMed Winterbourn CC, Hawkins RE, Brian M, Carrell RW (1975) The estimation of red cell superoxide dismutase activity. J Lab Clin Med 85:337–341PubMed
22.
Zurück zum Zitat Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358PubMedCrossRef Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358PubMedCrossRef
23.
Zurück zum Zitat Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582:67–78PubMedCrossRef Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582:67–78PubMedCrossRef
24.
Zurück zum Zitat Granger DN (1988) Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 255:H1269–H1275PubMed Granger DN (1988) Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 255:H1269–H1275PubMed
25.
Zurück zum Zitat Granger DN, Korthuis RJ (1995) Physiologic mechanisms of post ischemic tissue injury. Annu Rev Physiol 57:311–332PubMedCrossRef Granger DN, Korthuis RJ (1995) Physiologic mechanisms of post ischemic tissue injury. Annu Rev Physiol 57:311–332PubMedCrossRef
26.
Zurück zum Zitat Klausner JM, Anner H, Paterson ÝS, Kobzik L, Valeri CR, Shepro D, Hechtman HB (1988) Lower torso ischemic-induced lung injury is leukocyte dependent. Ann Surg 208:761–767PubMedCentralPubMedCrossRef Klausner JM, Anner H, Paterson ÝS, Kobzik L, Valeri CR, Shepro D, Hechtman HB (1988) Lower torso ischemic-induced lung injury is leukocyte dependent. Ann Surg 208:761–767PubMedCentralPubMedCrossRef
27.
Zurück zum Zitat Takhtfooladi MA, Jahanshahi A, Sotoudeh A, Jahanshahi G, Takhtfooladi HA, Aslani K (2013) Effect of tramadol on lung injury induced by skeletal muscle ischemia-reperfusion: an experimental study. J Bras Pneumol 39(4):434–439PubMedCentralPubMedCrossRef Takhtfooladi MA, Jahanshahi A, Sotoudeh A, Jahanshahi G, Takhtfooladi HA, Aslani K (2013) Effect of tramadol on lung injury induced by skeletal muscle ischemia-reperfusion: an experimental study. J Bras Pneumol 39(4):434–439PubMedCentralPubMedCrossRef
28.
Zurück zum Zitat Sotoudeh A, Takhtfooladi MA, Jahanshahi A, Khiabanian Asl AH, Takhtfooladi HA, Khansari M (2012) Effect of N-acetylcysteine on lung injury induced by skeletal muscle ischemia-reperfusion. Histopathological study in rat model. Acta Cir Bras 27(2):168–171PubMedCrossRef Sotoudeh A, Takhtfooladi MA, Jahanshahi A, Khiabanian Asl AH, Takhtfooladi HA, Khansari M (2012) Effect of N-acetylcysteine on lung injury induced by skeletal muscle ischemia-reperfusion. Histopathological study in rat model. Acta Cir Bras 27(2):168–171PubMedCrossRef
29.
Zurück zum Zitat Takhtfooladi H, Takhtfooladi M, Moayer F, Mobarakeh S (2015) Melatonin attenuates lung injury in a hind limb ischemia-reperfusion rat model. Rev Port Pneumol 21(1):30–35PubMed Takhtfooladi H, Takhtfooladi M, Moayer F, Mobarakeh S (2015) Melatonin attenuates lung injury in a hind limb ischemia-reperfusion rat model. Rev Port Pneumol 21(1):30–35PubMed
30.
Zurück zum Zitat Stallone RJ, Lim RC, Blaisdell FW (1969) Pathogenesis of the pulmonary changes following ischemia of the lower extremities. Ann Thorac Surg 7:539–549PubMedCrossRef Stallone RJ, Lim RC, Blaisdell FW (1969) Pathogenesis of the pulmonary changes following ischemia of the lower extremities. Ann Thorac Surg 7:539–549PubMedCrossRef
31.
Zurück zum Zitat Albertini R, Aimbire FS, Correa FI, Ribeiro W, Cogo JC, Antunes E, Teixeira SA, De Nucci G, Castro-Faria-Neto HC, Zângaro RA, Lopes-Martins RA (2006) Effects of different protocol doses of low power gallium-aluminum arsenate (Ga-Al-As) laser radiation (650nm) on carrageenan induced rat paw oedema. J Photochem Photobiol B 74(2–3):101–107 Albertini R, Aimbire FS, Correa FI, Ribeiro W, Cogo JC, Antunes E, Teixeira SA, De Nucci G, Castro-Faria-Neto HC, Zângaro RA, Lopes-Martins RA (2006) Effects of different protocol doses of low power gallium-aluminum arsenate (Ga-Al-As) laser radiation (650nm) on carrageenan induced rat paw oedema. J Photochem Photobiol B 74(2–3):101–107
32.
Zurück zum Zitat Xavier M, David DR, de Souza RA, Arrieiro AN, Miranda H, Santana ET, Silva JA Jr, Salgado MA, Aimbire F, Albertini R (2010) Anti-inflammatory effect of low level light emitting diode therapy on Achilles tendinitis in rats. Lasers Surg Med 42(6):553–558PubMedCrossRef Xavier M, David DR, de Souza RA, Arrieiro AN, Miranda H, Santana ET, Silva JA Jr, Salgado MA, Aimbire F, Albertini R (2010) Anti-inflammatory effect of low level light emitting diode therapy on Achilles tendinitis in rats. Lasers Surg Med 42(6):553–558PubMedCrossRef
33.
Zurück zum Zitat Landyshev IS, Avdeeva NV, Goborov ND, Krasavina NP, Tikhonova GA, Tkacheva SI (2002) Efficacy of low intensity laser irradiation and sodium nedocromil in the complex treatment of patients with bronchial asthma. Ter Arkh 74(3):25–28PubMed Landyshev IS, Avdeeva NV, Goborov ND, Krasavina NP, Tikhonova GA, Tkacheva SI (2002) Efficacy of low intensity laser irradiation and sodium nedocromil in the complex treatment of patients with bronchial asthma. Ter Arkh 74(3):25–28PubMed
34.
Zurück zum Zitat de Lima FM, Aimbire F, Miranda H, Vieira Rde P, de Oliveira AP, Albertini R (2014) Low-level laser therapy attenuates the myeloperoxidase activity and inflammatory mediator generation in lung inflammation induced by gut ischemia and reperfusion: a dose–response study. J Lasers Med Sci 5(2):63–70PubMedCentralPubMed de Lima FM, Aimbire F, Miranda H, Vieira Rde P, de Oliveira AP, Albertini R (2014) Low-level laser therapy attenuates the myeloperoxidase activity and inflammatory mediator generation in lung inflammation induced by gut ischemia and reperfusion: a dose–response study. J Lasers Med Sci 5(2):63–70PubMedCentralPubMed
35.
Zurück zum Zitat de Lima FM, Albertini R, Dantas Y, Maia-Filho AL, Santana Cde L, Castro-Faria-Neto HC, França C, Villaverde AB, Aimbire F (2013) Low-level laser therapy restores the oxidative stress balance in acute lung injury induced by gut ischemia and reperfusion. Photochem Photobiol 89(1):179–188PubMedCrossRef de Lima FM, Albertini R, Dantas Y, Maia-Filho AL, Santana Cde L, Castro-Faria-Neto HC, França C, Villaverde AB, Aimbire F (2013) Low-level laser therapy restores the oxidative stress balance in acute lung injury induced by gut ischemia and reperfusion. Photochem Photobiol 89(1):179–188PubMedCrossRef
36.
Zurück zum Zitat Seekamp A, Ward PA (1993) Ischemia-reperfusion injury. Agents Actions Suppl 41:137–152PubMed Seekamp A, Ward PA (1993) Ischemia-reperfusion injury. Agents Actions Suppl 41:137–152PubMed
37.
Metadaten
Titel
Effect of low-level laser therapy on lung injury induced by hindlimb ischemia/reperfusion in rats
verfasst von
Mohammad Ashrafzadeh Takhtfooladi
Hamed Ashrafzadeh Takhtfooladi
Hamidreza Sedaghatfar
Samaneh Shabani
Publikationsdatum
01.08.2015
Verlag
Springer London
Erschienen in
Lasers in Medical Science / Ausgabe 6/2015
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-015-1786-6

Weitere Artikel der Ausgabe 6/2015

Lasers in Medical Science 6/2015 Zur Ausgabe