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Published in: Lasers in Medical Science 1/2017

01-01-2017 | Original Article

Maximal oxygen uptake and exercise tolerance are improved in rats with heart failure subjected to low-level laser therapy associated with resistance training

Authors: Vítor Scotta Hentschke, Lucas Capalonga, Douglas Dalcin Rossato, Júlia Luíza Perini, Jadson Pereira Alves, Giuseppe Potrick Stefani, Marlus Karsten, Mauro Pontes, Pedro Dal Lago

Published in: Lasers in Medical Science | Issue 1/2017

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Abstract

Exercise tolerance and maximal oxygen uptake (VO2max) are reduced in heart failure (HF). The influence of combined resistance training (RT) and low-level laser therapy (LLLT) on exercise tolerance and VO2max in HF has not yet been explored. The aim of this study was to evaluate the influence of combined RT and LLLT on VO2max and exercise tolerance in rats with HF induced by myocardial infarction (MI). Rats were allocated to sedentary sham (Sed-Sham, n = 12), sedentary heart failure (Sed-HF, n = 9), RT heart failure (RT-HF, n = 7) and RT associated with LLLT heart failure (RT + LLLT-HF, n = 7) groups. After MI or sham surgery, rats underwent a RT and LLLT protocol (applied immediately after RT) for 8 weeks. VO2max and exercise tolerance were evaluated at the end of protocol. HF rats subjected to LLLT combined with RT showed higher VO2basal (41 %), VO2max (40 %), VO2reserve (39 %), run distance (46 %), time to exhaustion (30 %) and maximal velocity (22 %) compared with HF rats that underwent RT alone. LLLT associated with RT improved oxygen uptake and exercise tolerance compared with RT alone in HF rats.
Literature
1.
go back to reference Conraads VM, Van Craenenbroeck EM, De Maeyer C, Van Berendoncks AM, Beckers PJ, Vrints CJ (2013) Unraveling new mechanisms of exercise intolerance in chronic heart failure: role of exercise training. Heart Fail Rev 18(1):65–77. doi:10.1007/s10741-012-9324-0 CrossRefPubMed Conraads VM, Van Craenenbroeck EM, De Maeyer C, Van Berendoncks AM, Beckers PJ, Vrints CJ (2013) Unraveling new mechanisms of exercise intolerance in chronic heart failure: role of exercise training. Heart Fail Rev 18(1):65–77. doi:10.​1007/​s10741-012-9324-0 CrossRefPubMed
2.
go back to reference Francis DP, Shamim W, Davies LC, Piepoli MF, Ponikowski P, Anker SD, Coats AJ (2000) Cardiopulmonary exercise testing for prognosis in chronic heart failure: continuous and independent prognostic value from VE/VCO(2)slope and peak VO(2). Eur Heart J 21(2):154–161. doi:10.1053/euhj.1999.1863 CrossRefPubMed Francis DP, Shamim W, Davies LC, Piepoli MF, Ponikowski P, Anker SD, Coats AJ (2000) Cardiopulmonary exercise testing for prognosis in chronic heart failure: continuous and independent prognostic value from VE/VCO(2)slope and peak VO(2). Eur Heart J 21(2):154–161. doi:10.​1053/​euhj.​1999.​1863 CrossRefPubMed
4.
go back to reference Piepoli MF, Guazzi M, Boriani G, Cicoira M, Corra U, Dalla Libera L, Emdin M, Mele D, Passino C, Vescovo G, Vigorito C, Villani GQ, Agostoni P, Working Group 'Exercise Physiology SC, Cardiac Rehabilitation ISoC (2010) Exercise intolerance in chronic heart failure: mechanisms and therapies. Part I Eur J Cardiovasc Prev Rehabil 17(6):637–642CrossRefPubMed Piepoli MF, Guazzi M, Boriani G, Cicoira M, Corra U, Dalla Libera L, Emdin M, Mele D, Passino C, Vescovo G, Vigorito C, Villani GQ, Agostoni P, Working Group 'Exercise Physiology SC, Cardiac Rehabilitation ISoC (2010) Exercise intolerance in chronic heart failure: mechanisms and therapies. Part I Eur J Cardiovasc Prev Rehabil 17(6):637–642CrossRefPubMed
6.
go back to reference Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Drazner MH, Fonarow GC, Geraci SA, Horwich T, Januzzi JL, Johnson MR, Kasper EK, Levy WC, Masoudi FA, McBride PE, McMurray JJ, Mitchell JE, Peterson PN, Riegel B, Sam F, Stevenson LW, Tang WH, Tsai EJ, Wilkoff BL, American College of Cardiology F, American Heart Association Task Force on Practice G (2013) 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 62(16):e147–e239. doi:10.1016/j.jacc.2013.05.019 CrossRefPubMed Yancy CW, Jessup M, Bozkurt B, Butler J, Casey DE Jr, Drazner MH, Fonarow GC, Geraci SA, Horwich T, Januzzi JL, Johnson MR, Kasper EK, Levy WC, Masoudi FA, McBride PE, McMurray JJ, Mitchell JE, Peterson PN, Riegel B, Sam F, Stevenson LW, Tang WH, Tsai EJ, Wilkoff BL, American College of Cardiology F, American Heart Association Task Force on Practice G (2013) 2013 ACCF/AHA guideline for the management of heart failure: a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 62(16):e147–e239. doi:10.​1016/​j.​jacc.​2013.​05.​019 CrossRefPubMed
8.
go back to reference Piepoli MF, Conraads V, Corra U, Dickstein K, Francis DP, Jaarsma T, McMurray J, Pieske B, Piotrowicz E, Schmid JP, Anker SD, Solal AC, Filippatos GS, Hoes AW, Gielen S, Giannuzzi P, Ponikowski PP (2011) Exercise training in heart failure: from theory to practice. A consensus document of the Heart Failure Association and the European Association for Cardiovascular Prevention and Rehabilitation. Eur J Heart Fail 13(4):347–357. doi:10.1093/eurjhf/hfr017 CrossRefPubMed Piepoli MF, Conraads V, Corra U, Dickstein K, Francis DP, Jaarsma T, McMurray J, Pieske B, Piotrowicz E, Schmid JP, Anker SD, Solal AC, Filippatos GS, Hoes AW, Gielen S, Giannuzzi P, Ponikowski PP (2011) Exercise training in heart failure: from theory to practice. A consensus document of the Heart Failure Association and the European Association for Cardiovascular Prevention and Rehabilitation. Eur J Heart Fail 13(4):347–357. doi:10.​1093/​eurjhf/​hfr017 CrossRefPubMed
9.
go back to reference Pu CT, Johnson MT, Forman DE, Hausdorff JM, Roubenoff R, Foldvari M, Fielding RA, Singh MA (2001) Randomized trial of progressive resistance training to counteract the myopathy of chronic heart failure. J Appl Physiol (1985) 90(6):2341–2350 Pu CT, Johnson MT, Forman DE, Hausdorff JM, Roubenoff R, Foldvari M, Fielding RA, Singh MA (2001) Randomized trial of progressive resistance training to counteract the myopathy of chronic heart failure. J Appl Physiol (1985) 90(6):2341–2350
10.
go back to reference Arena R, Pinkstaff S, Wheeler E, Peberdy MA, Guazzi M, Myers J (2010) Neuromuscular electrical stimulation and inspiratory muscle training as potential adjunctive rehabilitation options for patients with heart failure. J Cardiopulm Rehabil Prev 30(4):209–223. doi:10.1097/HCR.0b013e3181c56b78 CrossRefPubMed Arena R, Pinkstaff S, Wheeler E, Peberdy MA, Guazzi M, Myers J (2010) Neuromuscular electrical stimulation and inspiratory muscle training as potential adjunctive rehabilitation options for patients with heart failure. J Cardiopulm Rehabil Prev 30(4):209–223. doi:10.​1097/​HCR.​0b013e3181c56b78​ CrossRefPubMed
11.
go back to reference Sbruzzi G, Ribeiro RA, Schaan BD, Signori LU, Silva AM, Irigoyen MC, Plentz RD (2010) Functional electrical stimulation in the treatment of patients with chronic heart failure: a meta-analysis of randomized controlled trials. Eur J Cardiovasc Prev Rehabil 17(3):254–260PubMed Sbruzzi G, Ribeiro RA, Schaan BD, Signori LU, Silva AM, Irigoyen MC, Plentz RD (2010) Functional electrical stimulation in the treatment of patients with chronic heart failure: a meta-analysis of randomized controlled trials. Eur J Cardiovasc Prev Rehabil 17(3):254–260PubMed
13.
go back to reference Leal-Junior EC, Vanin AA, Miranda EF, de Carvalho PT, Dal Corso S, Bjordal JM (2015) Effect of phototherapy (low-level laser therapy and light-emitting diode therapy) on exercise performance and markers of exercise recovery: a systematic review with meta-analysis. Lasers Med Sci 30(2):925–939. doi:10.1007/s10103-013-1465-4 CrossRefPubMed Leal-Junior EC, Vanin AA, Miranda EF, de Carvalho PT, Dal Corso S, Bjordal JM (2015) Effect of phototherapy (low-level laser therapy and light-emitting diode therapy) on exercise performance and markers of exercise recovery: a systematic review with meta-analysis. Lasers Med Sci 30(2):925–939. doi:10.​1007/​s10103-013-1465-4 CrossRefPubMed
14.
go back to reference De Marchi T, Leal Junior EC, Bortoli C, Tomazoni SS, Lopes-Martins RA, Salvador M (2012) Low-level laser therapy (LLLT) in human progressive-intensity running: effects on exercise performance, skeletal muscle status, and oxidative stress. Lasers Med Sci 27(1):231–236. doi:10.1007/s10103-011-0955-5 CrossRefPubMed De Marchi T, Leal Junior EC, Bortoli C, Tomazoni SS, Lopes-Martins RA, Salvador M (2012) Low-level laser therapy (LLLT) in human progressive-intensity running: effects on exercise performance, skeletal muscle status, and oxidative stress. Lasers Med Sci 27(1):231–236. doi:10.​1007/​s10103-011-0955-5 CrossRefPubMed
15.
go back to reference Amadio EM, Serra AJ, Guaraldo SA, Silva JA Jr, Antonio EL, Silva F, Portes LA, Tucci PJ, Leal-Junior EC, de Carvalho PT (2015) The action of pre-exercise low-level laser therapy (LLLT) on the expression of IL-6 and TNF-alpha proteins and on the functional fitness of elderly rats subjected to aerobic training. Lasers Med Sci. doi:10.1007/s10103-015-1713-x PubMed Amadio EM, Serra AJ, Guaraldo SA, Silva JA Jr, Antonio EL, Silva F, Portes LA, Tucci PJ, Leal-Junior EC, de Carvalho PT (2015) The action of pre-exercise low-level laser therapy (LLLT) on the expression of IL-6 and TNF-alpha proteins and on the functional fitness of elderly rats subjected to aerobic training. Lasers Med Sci. doi:10.​1007/​s10103-015-1713-x PubMed
16.
17.
go back to reference Biasibetti M, Rojas DB, Hentschke VS, Moura DJ, Karsten M, Wannmacher CM, Saffi J, Dal Lago P (2014) The influence of low-level laser therapy on parameters of oxidative stress and DNA damage on muscle and plasma in rats with heart failure. Lasers Med Sci 29(6):1895–1906. doi:10.1007/s10103-014-1597-1 CrossRefPubMed Biasibetti M, Rojas DB, Hentschke VS, Moura DJ, Karsten M, Wannmacher CM, Saffi J, Dal Lago P (2014) The influence of low-level laser therapy on parameters of oxidative stress and DNA damage on muscle and plasma in rats with heart failure. Lasers Med Sci 29(6):1895–1906. doi:10.​1007/​s10103-014-1597-1 CrossRefPubMed
20.
go back to reference Pfeifer PC, Musch TI, McAllister RM (2001) Skeletal muscle oxidative capacity and exercise tolerance in rats with heart failure. Med Sci Sports Exerc 33(4):542–548CrossRefPubMed Pfeifer PC, Musch TI, McAllister RM (2001) Skeletal muscle oxidative capacity and exercise tolerance in rats with heart failure. Med Sci Sports Exerc 33(4):542–548CrossRefPubMed
21.
go back to reference Krisan AD, Collins DE, Crain AM, Kwong CC, Singh MK, Bernard JR, Yaspelkis BB 3rd (2004) Resistance training enhances components of the insulin signaling cascade in normal and high-fat-fed rodent skeletal muscle. J Appl Physiol (1985) 96(5):1691–1700. doi:10.1152/japplphysiol.01054.2003 CrossRef Krisan AD, Collins DE, Crain AM, Kwong CC, Singh MK, Bernard JR, Yaspelkis BB 3rd (2004) Resistance training enhances components of the insulin signaling cascade in normal and high-fat-fed rodent skeletal muscle. J Appl Physiol (1985) 96(5):1691–1700. doi:10.​1152/​japplphysiol.​01054.​2003 CrossRef
23.
go back to reference Tamaki T, Uchiyama S, Nakano S (1992) A weight-lifting exercise model for inducing hypertrophy in the hindlimb muscles of rats. Med Sci Sports Exerc 24(8):881–886CrossRefPubMed Tamaki T, Uchiyama S, Nakano S (1992) A weight-lifting exercise model for inducing hypertrophy in the hindlimb muscles of rats. Med Sci Sports Exerc 24(8):881–886CrossRefPubMed
24.
go back to reference Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, Nieman DC, Swain DP, American College of Sports M (2011) American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 43(7):1334–1359. doi:10.1249/MSS.0b013e318213fefb CrossRefPubMed Garber CE, Blissmer B, Deschenes MR, Franklin BA, Lamonte MJ, Lee IM, Nieman DC, Swain DP, American College of Sports M (2011) American College of Sports Medicine position stand. Quantity and quality of exercise for developing and maintaining cardiorespiratory, musculoskeletal, and neuromotor fitness in apparently healthy adults: guidance for prescribing exercise. Med Sci Sports Exerc 43(7):1334–1359. doi:10.​1249/​MSS.​0b013e318213fefb​ CrossRefPubMed
26.
go back to reference Louzada RA, Oliveira PF, Cavalcanti-de-Albuquerque JP, Cunha-Carvalho L, Baldanza MR, Kasai-Brunswick TH, Goldenberg RC, Campos-de-Carvalho AC, Werneck-de-Castro JP (2010) Granulocyte-colony stimulating factor treatment of chronic myocardial infarction. Cardiovasc Drugs Ther 24(2):121–130. doi:10.1007/s10557-010-6215-2 CrossRefPubMed Louzada RA, Oliveira PF, Cavalcanti-de-Albuquerque JP, Cunha-Carvalho L, Baldanza MR, Kasai-Brunswick TH, Goldenberg RC, Campos-de-Carvalho AC, Werneck-de-Castro JP (2010) Granulocyte-colony stimulating factor treatment of chronic myocardial infarction. Cardiovasc Drugs Ther 24(2):121–130. doi:10.​1007/​s10557-010-6215-2 CrossRefPubMed
27.
go back to reference Rondon E, Brasileiro-Santos MS, Moreira ED, Rondon MU, Mattos KC, Coelho MA, Silva GJ, Brum PC, Fiorino P, Irigoyen MC, Krieger EM, Middlekauff HR, Negrao CE (2006) Exercise training improves aortic depressor nerve sensitivity in rats with ischemia-induced heart failure. Am J Physiol Heart Circ Physiol 291(6):H2801–H2806. doi:10.1152/ajpheart.01352.2005 CrossRefPubMed Rondon E, Brasileiro-Santos MS, Moreira ED, Rondon MU, Mattos KC, Coelho MA, Silva GJ, Brum PC, Fiorino P, Irigoyen MC, Krieger EM, Middlekauff HR, Negrao CE (2006) Exercise training improves aortic depressor nerve sensitivity in rats with ischemia-induced heart failure. Am J Physiol Heart Circ Physiol 291(6):H2801–H2806. doi:10.​1152/​ajpheart.​01352.​2005 CrossRefPubMed
28.
go back to reference Werneck-de-Castro JP, Costa ESRH, de Oliveira PF, Pinho-Ribeiro V, Mello DB, Pecanha R, Mattos E, Olivares EL, Maia AC, Mill JG, Dos Santos Goldenberg RC, Campos-de-Carvalho AC (2006) G-CSF does not improve systolic function in a rat model of acute myocardial infarction. Basic Res Cardiol 101(6):494–501. doi:10.1007/s00395-006-0605-4 CrossRefPubMed Werneck-de-Castro JP, Costa ESRH, de Oliveira PF, Pinho-Ribeiro V, Mello DB, Pecanha R, Mattos E, Olivares EL, Maia AC, Mill JG, Dos Santos Goldenberg RC, Campos-de-Carvalho AC (2006) G-CSF does not improve systolic function in a rat model of acute myocardial infarction. Basic Res Cardiol 101(6):494–501. doi:10.​1007/​s00395-006-0605-4 CrossRefPubMed
29.
go back to reference Batista ML Jr, Santos RV, Oliveira EM, Seelaender MC, Costa Rosa LF (2007) Endurance training restores peritoneal macrophage function in post-MI congestive heart failure rats. J Appl Physiol (1985) 102(5):2033–2039. doi:10.1152/japplphysiol.00871.2006 CrossRef Batista ML Jr, Santos RV, Oliveira EM, Seelaender MC, Costa Rosa LF (2007) Endurance training restores peritoneal macrophage function in post-MI congestive heart failure rats. J Appl Physiol (1985) 102(5):2033–2039. doi:10.​1152/​japplphysiol.​00871.​2006 CrossRef
30.
go back to reference Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ, Chamber Quantification Writing G, American Society of Echocardiography’s G, Standards C, European Association of E (2005) Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18(12):1440–1463. doi:10.1016/j.echo.2005.10.005 CrossRefPubMed Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA, Picard MH, Roman MJ, Seward J, Shanewise JS, Solomon SD, Spencer KT, Sutton MS, Stewart WJ, Chamber Quantification Writing G, American Society of Echocardiography’s G, Standards C, European Association of E (2005) Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18(12):1440–1463. doi:10.​1016/​j.​echo.​2005.​10.​005 CrossRefPubMed
32.
go back to reference Martinez PF, Okoshi K, Zornoff LA, Oliveira SA Jr, Campos DH, Lima AR, Damatto RL, Cezar MD, Bonomo C, Guizoni DM, Padovani CR, Cicogna AC, Okoshi MP (2011) Echocardiographic detection of congestive heart failure in postinfarction rats. J Appl Physiol (1985) 111(2):543–551. doi:10.1152/japplphysiol.01154.2010 CrossRef Martinez PF, Okoshi K, Zornoff LA, Oliveira SA Jr, Campos DH, Lima AR, Damatto RL, Cezar MD, Bonomo C, Guizoni DM, Padovani CR, Cicogna AC, Okoshi MP (2011) Echocardiographic detection of congestive heart failure in postinfarction rats. J Appl Physiol (1985) 111(2):543–551. doi:10.​1152/​japplphysiol.​01154.​2010 CrossRef
33.
go back to reference Moreira JB, Bechara LR, Bozi LH, Jannig PR, Monteiro AW, Dourado PM, Wisloff U, Brum PC (2013) High- versus moderate-intensity aerobic exercise training effects on skeletal muscle of infarcted rats. J Appl Physiol (1985) 114(8):1029–1041. doi:10.1152/japplphysiol.00760.2012 CrossRef Moreira JB, Bechara LR, Bozi LH, Jannig PR, Monteiro AW, Dourado PM, Wisloff U, Brum PC (2013) High- versus moderate-intensity aerobic exercise training effects on skeletal muscle of infarcted rats. J Appl Physiol (1985) 114(8):1029–1041. doi:10.​1152/​japplphysiol.​00760.​2012 CrossRef
34.
go back to reference Schenkel PC, Tavares AM, Fernandes RO, Diniz GP, Bertagnolli M, da Rosa Araujo AS, Barreto-Chaves ML, Ribeiro MF, Clausell N, Bello-Klein A (2010) Redox-sensitive prosurvival and proapoptotic protein expression in the myocardial remodeling post-infarction in rats. Mol Cell Biochem 341(1–2):1–8. doi:10.1007/s11010-010-0431-8 CrossRefPubMed Schenkel PC, Tavares AM, Fernandes RO, Diniz GP, Bertagnolli M, da Rosa Araujo AS, Barreto-Chaves ML, Ribeiro MF, Clausell N, Bello-Klein A (2010) Redox-sensitive prosurvival and proapoptotic protein expression in the myocardial remodeling post-infarction in rats. Mol Cell Biochem 341(1–2):1–8. doi:10.​1007/​s11010-010-0431-8 CrossRefPubMed
35.
go back to reference Tavares AM, da Rosa Araujo AS, Baldo G, Matte U, Khaper N, Bello-Klein A, Rohde LE, Clausell N (2010) Bone marrow derived cells decrease inflammation but not oxidative stress in an experimental model of acute myocardial infarction. Life Sci 87(23–26):699–706. doi:10.1016/j.lfs.2010.10.008 CrossRefPubMed Tavares AM, da Rosa Araujo AS, Baldo G, Matte U, Khaper N, Bello-Klein A, Rohde LE, Clausell N (2010) Bone marrow derived cells decrease inflammation but not oxidative stress in an experimental model of acute myocardial infarction. Life Sci 87(23–26):699–706. doi:10.​1016/​j.​lfs.​2010.​10.​008 CrossRefPubMed
37.
go back to reference Reffelmann T, Kloner RA (2003) Transthoracic echocardiography in rats. Evalution of commonly used indices of left ventricular dimensions, contractile performance, and hypertrophy in a genetic model of hypertrophic heart failure (SHHF-Mcc-facp-Rats) in comparison with Wistar rats during aging. Basic Res Cardiol 98(5):275–284. doi:10.1007/s00395-003-0401-3 CrossRefPubMed Reffelmann T, Kloner RA (2003) Transthoracic echocardiography in rats. Evalution of commonly used indices of left ventricular dimensions, contractile performance, and hypertrophy in a genetic model of hypertrophic heart failure (SHHF-Mcc-facp-Rats) in comparison with Wistar rats during aging. Basic Res Cardiol 98(5):275–284. doi:10.​1007/​s00395-003-0401-3 CrossRefPubMed
39.
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(1):59–66. doi:10.1007/s10103-014-1616-2 CrossRefPubMed 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(1):59–66. doi:10.​1007/​s10103-014-1616-2 CrossRefPubMed
40.
go back to reference Nozawa E, Kanashiro RM, Murad N, Carvalho AC, Cravo SL, Campos O, Tucci PJ, Moises VA (2006) Performance of two-dimensional Doppler echocardiography for the assessment of infarct size and left ventricular function in rats. Braz J Med Biol Res 39(5):687–695CrossRefPubMed Nozawa E, Kanashiro RM, Murad N, Carvalho AC, Cravo SL, Campos O, Tucci PJ, Moises VA (2006) Performance of two-dimensional Doppler echocardiography for the assessment of infarct size and left ventricular function in rats. Braz J Med Biol Res 39(5):687–695CrossRefPubMed
41.
go back to reference Oh BH, Ono S, Rockman HA, Ross J Jr (1993) Myocardial hypertrophy in the ischemic zone induced by exercise in rats after coronary reperfusion. Circulation 87(2):598–607CrossRefPubMed Oh BH, Ono S, Rockman HA, Ross J Jr (1993) Myocardial hypertrophy in the ischemic zone induced by exercise in rats after coronary reperfusion. Circulation 87(2):598–607CrossRefPubMed
42.
go back to reference Perini JL, Hentschke VS, Sonza A, Dal Lago P (2016) Long-term low-level laser therapy promotes an increase in maximal oxygen uptake and exercise performance in a dose-dependent manner in Wistar rats. Lasers Med Sci 31(2):241–248. doi:10.1007/s10103-015-1849-8 CrossRefPubMed Perini JL, Hentschke VS, Sonza A, Dal Lago P (2016) Long-term low-level laser therapy promotes an increase in maximal oxygen uptake and exercise performance in a dose-dependent manner in Wistar rats. Lasers Med Sci 31(2):241–248. doi:10.​1007/​s10103-015-1849-8 CrossRefPubMed
43.
go back to reference Capalonga L, Karsten M, Hentschke VS, Rossato DD, Dornelles MP, Sonza A, Bagnato VS, Ferraresi C, Parizotto NA, Dal Lago P (2016) Light-emitting diode therapy (LEDT) improves functional capacity in rats with heart failure. Lasers Med Sci. doi:10.1007/s10103-016-1922-y Capalonga L, Karsten M, Hentschke VS, Rossato DD, Dornelles MP, Sonza A, Bagnato VS, Ferraresi C, Parizotto NA, Dal Lago P (2016) Light-emitting diode therapy (LEDT) improves functional capacity in rats with heart failure. Lasers Med Sci. doi:10.​1007/​s10103-016-1922-y
44.
go back to reference da Silva Alves MA, Pinfildi CE, Neto LN, Lourenco RP, de Azevedo PH, Dourado VZ (2014) Acute effects of low-level laser therapy on physiologic and electromyographic responses to the cardiopulmonary exercise testing in healthy untrained adults. Lasers Med Sci 29(6):1945–1951. doi:10.1007/s10103-014-1595-3 CrossRefPubMed da Silva Alves MA, Pinfildi CE, Neto LN, Lourenco RP, de Azevedo PH, Dourado VZ (2014) Acute effects of low-level laser therapy on physiologic and electromyographic responses to the cardiopulmonary exercise testing in healthy untrained adults. Lasers Med Sci 29(6):1945–1951. doi:10.​1007/​s10103-014-1595-3 CrossRefPubMed
45.
go back to reference Miranda EF, Vanin AA, Tomazoni SS, Grandinetti Vdos S, de Paiva PR, Machado Cdos S, Monteiro KK, Casalechi HL, de Tarso P, de Carvalho C, Leal-Junior EC (2016) Using pre-exercise photobiomodulation therapy combining super-pulsed lasers and light-emitting diodes to improve performance in progressive cardiopulmonary exercise tests. J Athl Train 51(2):129–135. doi:10.4085/1062-6050-51.3.10 CrossRefPubMed Miranda EF, Vanin AA, Tomazoni SS, Grandinetti Vdos S, de Paiva PR, Machado Cdos S, Monteiro KK, Casalechi HL, de Tarso P, de Carvalho C, Leal-Junior EC (2016) Using pre-exercise photobiomodulation therapy combining super-pulsed lasers and light-emitting diodes to improve performance in progressive cardiopulmonary exercise tests. J Athl Train 51(2):129–135. doi:10.​4085/​1062-6050-51.​3.​10 CrossRefPubMed
46.
go back to reference Miranda EF, de Oliveira LV, Antonialli FC, Vanin AA, de Carvalho PT, Leal-Junior EC (2015) Phototherapy with combination of super-pulsed laser and light-emitting diodes is beneficial in improvement of muscular performance (strength and muscular endurance), dyspnea, and fatigue sensation in patients with chronic obstructive pulmonary disease. Lasers Med Sci 30(1):437–443. doi:10.1007/s10103-014-1690-5 CrossRefPubMed Miranda EF, de Oliveira LV, Antonialli FC, Vanin AA, de Carvalho PT, Leal-Junior EC (2015) Phototherapy with combination of super-pulsed laser and light-emitting diodes is beneficial in improvement of muscular performance (strength and muscular endurance), dyspnea, and fatigue sensation in patients with chronic obstructive pulmonary disease. Lasers Med Sci 30(1):437–443. doi:10.​1007/​s10103-014-1690-5 CrossRefPubMed
47.
go back to reference Leal-Junior EC, de Almeida P, Tomazoni SS, de Carvalho PT, Lopes-Martins RA, 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 9(3), e89453. doi:10.1371/journal.pone.0089453 CrossRefPubMedPubMedCentral Leal-Junior EC, de Almeida P, Tomazoni SS, de Carvalho PT, Lopes-Martins RA, 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 9(3), e89453. doi:10.​1371/​journal.​pone.​0089453 CrossRefPubMedPubMedCentral
48.
go back to reference Cicoira M, Bolger AP, Doehner W, Rauchhaus M, Davos C, Sharma R, Al-Nasser FO, Coats AJ, Anker SD (2001) High tumour necrosis factor-alpha levels are associated with exercise intolerance and neurohormonal activation in chronic heart failure patients. Cytokine 15(2):80–86. doi:10.1006/cyto.2001.0918 CrossRefPubMed Cicoira M, Bolger AP, Doehner W, Rauchhaus M, Davos C, Sharma R, Al-Nasser FO, Coats AJ, Anker SD (2001) High tumour necrosis factor-alpha levels are associated with exercise intolerance and neurohormonal activation in chronic heart failure patients. Cytokine 15(2):80–86. doi:10.​1006/​cyto.​2001.​0918 CrossRefPubMed
49.
go back to reference Coirault C, Guellich A, Barbry T, Samuel JL, Riou B, Lecarpentier Y (2007) Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 292(2):H1009–H1017. doi:10.1152/ajpheart.00438.2006 CrossRefPubMed Coirault C, Guellich A, Barbry T, Samuel JL, Riou B, Lecarpentier Y (2007) Oxidative stress of myosin contributes to skeletal muscle dysfunction in rats with chronic heart failure. Am J Physiol Heart Circ Physiol 292(2):H1009–H1017. doi:10.​1152/​ajpheart.​00438.​2006 CrossRefPubMed
52.
53.
go back to reference Ferraresi C, de Brito OT, de Oliveira ZL, de Menezes Reiff RB, Baldissera V, de Andrade Perez SE, Matheucci Junior E, Parizotto NA (2011) Effects of low level laser therapy (808 nm) on physical strength training in humans. Lasers Med Sci 26(3):349–358. doi:10.1007/s10103-010-0855-0 CrossRefPubMed Ferraresi C, de Brito OT, de Oliveira ZL, de Menezes Reiff RB, Baldissera V, de Andrade Perez SE, Matheucci Junior E, Parizotto NA (2011) Effects of low level laser therapy (808 nm) on physical strength training in humans. Lasers Med Sci 26(3):349–358. doi:10.​1007/​s10103-010-0855-0 CrossRefPubMed
54.
go back to reference Ferraresi C, Parizotto NA, Pires de Sousa MV, Kaippert B, Huang YY, Koiso T, Bagnato VS, Hamblin MR (2015) Light-emitting diode therapy in exercise-trained mice increases muscle performance, cytochrome c oxidase activity, ATP and cell proliferation. J Biophotonics 8(9):740–754. doi:10.1002/jbio.201400087 CrossRefPubMed Ferraresi C, Parizotto NA, Pires de Sousa MV, Kaippert B, Huang YY, Koiso T, Bagnato VS, Hamblin MR (2015) Light-emitting diode therapy in exercise-trained mice increases muscle performance, cytochrome c oxidase activity, ATP and cell proliferation. J Biophotonics 8(9):740–754. doi:10.​1002/​jbio.​201400087 CrossRefPubMed
55.
go back to reference Vieira WH, Ferraresi C, Perez SE, Baldissera V, Parizotto NA (2012) Effects of low-level laser therapy (808 nm) on isokinetic muscle performance of young women submitted to endurance training: a randomized controlled clinical trial. Lasers Med Sci 27(2):497–504. doi:10.1007/s10103-011-0984-0 CrossRefPubMed Vieira WH, Ferraresi C, Perez SE, Baldissera V, Parizotto NA (2012) Effects of low-level laser therapy (808 nm) on isokinetic muscle performance of young women submitted to endurance training: a randomized controlled clinical trial. Lasers Med Sci 27(2):497–504. doi:10.​1007/​s10103-011-0984-0 CrossRefPubMed
56.
go back to reference Vanin AA, Miranda EF, Machado CS, de Paiva PR, Albuquerque-Pontes GM, Casalechi HL, de Tarso Camillo de Carvalho P, Leal-Junior EC (2016) What is the best moment to apply phototherapy when associated to a strength training program? A randomized, double-blinded, placebo-controlled trial: phototherapy in association to strength training. Lasers Med Sci. doi:10.1007/s10103-016-2015-7 Vanin AA, Miranda EF, Machado CS, de Paiva PR, Albuquerque-Pontes GM, Casalechi HL, de Tarso Camillo de Carvalho P, Leal-Junior EC (2016) What is the best moment to apply phototherapy when associated to a strength training program? A randomized, double-blinded, placebo-controlled trial: phototherapy in association to strength training. Lasers Med Sci. doi:10.​1007/​s10103-016-2015-7
57.
go back to reference Rolim NP, Mattos KC, Brum PC, Baldo MV, Middlekauff HR, Negrao CE (2006) The decreased oxygen uptake during progressive exercise in ischemia-induced heart failure is due to reduced cardiac output rate. Braz J Med Biol Res 39(2):297–304CrossRefPubMed Rolim NP, Mattos KC, Brum PC, Baldo MV, Middlekauff HR, Negrao CE (2006) The decreased oxygen uptake during progressive exercise in ischemia-induced heart failure is due to reduced cardiac output rate. Braz J Med Biol Res 39(2):297–304CrossRefPubMed
58.
go back to reference Fletcher PJ, Pfeffer JM, Pfeffer MA, Braunwald E (1981) Left ventricular diastolic pressure-volume relations in rats with healed myocardial infarction. Effects on systolic function. Circ Res 49(3):618–626CrossRefPubMed Fletcher PJ, Pfeffer JM, Pfeffer MA, Braunwald E (1981) Left ventricular diastolic pressure-volume relations in rats with healed myocardial infarction. Effects on systolic function. Circ Res 49(3):618–626CrossRefPubMed
Metadata
Title
Maximal oxygen uptake and exercise tolerance are improved in rats with heart failure subjected to low-level laser therapy associated with resistance training
Authors
Vítor Scotta Hentschke
Lucas Capalonga
Douglas Dalcin Rossato
Júlia Luíza Perini
Jadson Pereira Alves
Giuseppe Potrick Stefani
Marlus Karsten
Mauro Pontes
Pedro Dal Lago
Publication date
01-01-2017
Publisher
Springer London
Published in
Lasers in Medical Science / Issue 1/2017
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-016-2088-3

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