Abstract
To evaluate whether acute photobiomodulation can elicit a hypotensive effect in spontaneously hypertensive rats (SHR). Male SHR were submitted to the implantation of a polyethylene cannula into the femoral artery. After 24 h, baseline measurements of the hemodynamic parameters: systolic, diastolic, and mean arterial pressure, and heart rate were accomplished for 1 h. Afterwards, laser application was simulated, and the hemodynamic parameters were recorded for 1 h. In the same animal, the laser was applied at six different positions of the rat’s abdomen, and the hemodynamic parameters were also recorded until the end of the hypotensive effect. The irradiation parameters were red wavelength (660 nm); average optical power of 100 mW; 56 s per point (six points); spot area of 0.0586 cm2; and irradiance of 1.71 W/cm2 yielding to a fluency of 96 J/cm2 per point. For measuring plasma NO levels, blood was collected before the recording, as well as immediately after the end of the mediated hypotensive effect. Photobiomodulation therapy was able to reduce the systolic arterial pressure in 69% of the SHR submitted to the application, displaying a decrease in systolic, diastolic, and mean arterial pressure. No change in heart rate was observed. Nevertheless, there was an increase in serum nitric oxide levels in the SHR responsive to photobiomodulation. Our results suggest that acute irradiation with a red laser at 660 nm can elicit a hypotensive effect in SHR, probably by a mechanism involving the release of NO, without changing the heart rate.
Similar content being viewed by others
References
Yusuf S, Hawkins S, Ounpuu S et al (2004) Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 364:937–952. https://doi.org/10.1016/S0140-6736(04)17018-9
Kannel WB (1996) Blood pressure as a cardiovascular risk factor: prevention and treatment. JAMA 275:1571–1576
Jung O, Gechter JL, Wunder C et al (2013) Resistant hypertension? Assessment of adherence by toxicological urine analysis. J Hypertens 31:766–774. https://doi.org/10.1097/HJH.0b013e32835e2286
Oishi JC, De Moraes TF, Buzinari TC, Cárnio EC, Parizotto NA, Rodrigues GJ (2017) Hypotensive acute effect of photobiomodulation therapy on hypertensive rats. Life Sci 178:56–60. https://doi.org/10.1016/j.lfs.2017.04.011
Yetik-Anacak G, Catravas JD (2006) Nitric oxide and the endothelium: history and impact on cardiovascular disease. Vasc Pharmacol 45:268–276. https://doi.org/10.1016/j.vph.2006.08.002
Furchgott RF, Ehrreich SJ, Greenblatt E (1961) The photoactivated relaxation of smooth muscle of rabbit aorta. J Gen Physiol 44:499–519
Kubaszewski E, Peters A, McClain S, Bohr D, Malinski T (1994) Light-activated release of nitric oxide from vascular smooth muscle of normotensive and hypertensive rats. Biochem Biophys Res Commun 200:213–218. https://doi.org/10.1006/bbrc.1994.1436
Plass CA, Loew HG, Podesser BK, Prusa AM (2012) Light-induced vasodilation of coronary arteries and its possible clinical implication. Ann Thorac Surg 93:1181–1186. https://doi.org/10.1016/j.athoracsur.2011.12.062
Vladimirov Y, Borisenko G, Boriskina N, Kazarinov K, Osipov A (2000) NO-hemoglobin may be a light-sensitive source of nitric oxide both in solution and in red blood cells. J Photochem Photobiol B 59:115–22. https://doi.org/10.1016/S1011-1344(00)00148-2
Huang YY, Chen AC, Carroll JD, Hamblin MR (2009) Biphasic dose response in low level light therapy. Dose Response 7:358–383. https://doi.org/10.2203/dose-response.09-027.Hamblin
Albertini R, Aimbire FSC, Correa FI et al (2004) Effects of different protocol doses of low Power gallium–aluminum–arsenate (Ga–Al–As) laser radiation (650 nm) on carrageenan induced rat paw oedema. Journal of Photochemistry and Photobiology 74:101–107. https://doi.org/10.1016/j.jphotobiol.2004.03.002
Vinck EM, Cagnie BJ, Cornelissen MJ, Declercq HA, Cambier DC (2003) Increased fibroblast proliferation induced by light emitting diode and low power laser irradiation. Lasers Med Sci 18:95–99. https://doi.org/10.1007/s10103-003-0262-x
Mezawa S, Iwata K, Naito K, Kamogawa H (1988) The possible analgesic effect of soft-laser irradiation on heat nociceptors in the cat tongue. Arch Oral Bio. 33:693–694
Oron U, Yaakobi T, Oron A et al (2001) Low energy laser irradiation reduces formation of scar tissue following myocardial infarction in dogs. Circulation 103:296–301
Tuby H, Maltz L, Oron U (2007) Low-Level Laser Irradiation (LLLI) promotes proliferation of mesenchymal and cardiac stem cells in culture. Lasers Surg Med 39:373-378. https://doi.org/10.1002/lsm.20492
Tomimura S, Silva BP, Sanches IC et al (2014) Hemodynamic effect of laser therapy in spontaneously hypertensive rats. Arq Bras Cardiol. 103:161-164. https://doi.org/10.5935/abc.20140117
Archer S (1993) Measurement of nitric oxide in biological models. FASEB Journal 7:349–360
Sim JJ, Bhandari SK, Shi J et al (2013) Characteristics of resistant hypertension in a large, ethnically diverse hypertension population of an integrated health system. Mayo Clin Proc 88:1099-1107. https://doi.org/10.1016/.mayocp.2013.06.017
Siddiqui M, Dudenbostel T, Calhoun DA (2016) Resistant and Refractory Hypertension: Antihypertensive Treatment Resistance vs Treatment Failure. Can J Cardiol 32:603–606. https://doi.org/10.1016/j.cjca.2015.06.033
Cook NR, Cohen J, Hebert PR, Taylor JO, Hennekens CH (1995) Implications of small reductions in diastolic blood pressure for primary prevention. Arch Intern Med 155:701–709. https://doi.org/10.1001/archinte.1995.00430070053006
Trippodo NC, Frohlich ED (1981) Similarities of genetic (spontaneous) hypertension. Circ Res 48:309–319
Keszler A, Lindemer B, Weihrauch D et al (1995) Red/near infrared light stimulates release of an endothelium dependent vasodilator and rescues vascular dysfunction in a diabetes model. Free Radical Biology and Medicine 113:157–164. https://doi.org/10.1016/j.freeradbiomed.2017.09.012
Keszler A, Lindemer B, Hogg N et al (2018) Wavelength-dependence of vasodilation and NO release from S-nitrosothiols and dinitrosyl iron complexes by far red/near infrared light. Arch Biochem Biophys. 649:47–52. https://doi.org/10.1016/j.abb.2018.05.006
Ball KA, Castello PR, Poyton RO (2011) Low intensity light stimulates nitrite-dependent nitric oxide synthesis but not oxygene consumption by cytochrome c oxidase: implications for phototherapy. J Photochem Photobiol B Biol 102:182–191. https://doi.org/10.1016/j.jphotobiol.2010.12.002
Lohr NL, Keszler A, Pratt P et al (2009) Enhancement of nitric oxide release from nitrosyl hemoglobin and nitrosyl myoglobin by red/near infrared radiation: potential role in cardioprotection. J Mol Cell Cardiol 47:256–263. https://doi.org/10.1016/j.yjmcc.2009.03.009
Rapoport RM, Draznin MB, Murad F (1983) Endothelium-dependent relaxation in rat aorta may be mediated through cyclic GMP-dependent protein phosphorylation. Nature 306:174–176
Munzel T, Hink U, Ygit H, Macharzina R, Harrison DG, Mulsch A (1999) Role of superoxide dismutase “in vivo” and “in vitro” nitrate tolerance. Br J Pharmacol 127:1224–1230. https://doi.org/10.1038/sj.bjp.0702622
Feelish M, Kelm M (1991) Biotrasformation of organic nitrates to nitric oxide by vascular smooth muscle and endothelial cells. Biochem Biophys Res Commun 180:286–293. https://doi.org/10.1016/S0006-291X(05)81290-2
Bates JN, Baker MT, Guerra R Jr, Harrison DG (1991) Nitric oxide generation from nitroprusside by vascular tissue. Evidence that reduction of the nitroprusside anion and cyanide loss are required. Biochem Pharmacol 42:157–165. https://doi.org/10.1016/0006-2952(91)90406-U
Yakazu Y, Iwasawa K, Narita H et al (2001) Hemodynamic and sympathetic effects of feoldopam and sodium nitroprusside. Acta Anaesthesiol Scand 45:1176–1180. https://doi.org/10.1034/j.1399-6576.2001.450920.x
Munhoz FC, Potje SR, Pereira AC, Daruge MG, da Silva RS, Bendhack LM, Antoniali C (2012) Hypotensive and vasorelaxing effects of the new NO-donor [Ru(terpy)(bdq)NO+]3+ in spontaneously hypertensive rats. Nitric Oxide 26:111–117. https://doi.org/10.1016/j.niox.2011.12.008
Rodrigues GJ, Pereira AC, Vercesi JA, Lima RG, Silva RS, Bendhack LM (2012) Long-lasting hypotensive effect in renal hypertensive rats induced by nitric oxide released from a ruthenium complex 60:193–198. https://doi.org/10.1097/FJC.0b013e31825bacc4
Dyer AR, Persky V, Stamler J et al (1980) Heart rate as a prognostic factor for coronary heart disease and mortality: findings in three Chicago epidemiologic studies. Am J Epidemiol 112:736–749
Heidland UE, Strauer BE (2001) Left ventricular muscle mass and elevated heart rate are associated with coronary plaque disruption. Circulation 104:1477–1482
Sun JC, Huang XL, Deng XR et al (2014) Elevated resting heart rate is associated with dyslipidemia in middle-aged and elderly Chinese. Biomed Environ Sci 27:601–605. https://doi.org/10.3967/bes2014.092
Levine HJ (1997) Rest heart rate and life expectancy. J Am Coll Cardiol 30:1104–1106. https://doi.org/10.1016/S0735-1097(97)00246-5
Acknowledgments
We thank the DMC Equipment LTDA for providing the Photon Lase III.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—(Finance Code 001) and by the São Paulo Research Foundation (FAPESP 2018/10588-9 and 2013/20549-7).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
All experimental protocols were performed in accordance with the guidelines of the Brazilian College for Animal Experimentation (COBEA), and were approved by the Ethical Committee for Animal of the Federal University of São Carlos—UFSCAR (no. 7936070618).
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Buzinari, T.C., de Moraes, T.F., Cárnio, E.C. et al. Photobiomodulation induces hypotensive effect in spontaneously hypertensive rats. Lasers Med Sci 35, 567–572 (2020). https://doi.org/10.1007/s10103-019-02849-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10103-019-02849-7