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Acute effect of photobiomodulation using light-emitting diodes (LEDs) on baroreflex sensitivity during and after constant loading exercise in patients with type 2 diabetes mellitus

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Abstract

To evaluate the photobiomodulation (PBM) effect on the cardiovascular autonomic control, analyzed by baroreflex sensitivity (sequence method), during constant load exercise and recovery in diabetic men, we evaluated 11 men with type 2 diabetes (DM2) (40–64 years). The constant workload exercise protocol (TECC) was performed on two different days, 14 days apart from each other, to guarantee PBM washout period. After PBM by light-emitting diode (LED) irradiation (150 J or 300 J or placebo), 10 min of rest (REST) was performed. After this period, the volunteer was positioned on a cycloergometer to start the test (1-min rest, 3-min free-load heating, 6-min constant workload–EXERCISE, 6-min free-load cool-down, 1-min rest) followed by a sitting period of 10 min (RECOVERY). The constant workload corresponded to 80%VO2GET (gas exchange threshold) identified by a previous cardiopulmonary exercise test (CPET). PBM was applied in continuous mode, contact technique, bilaterally, on both femoral quadriceps and gastrocnemius muscle groups. The electrocardiogram R-R intervals (BioAmp FE132) and the peripheral pulse pressure signals (Finometer PRO) were collected continuously throughout the protocol. Stable sequences of 256 points were chosen at REST, EXERCISE, and RECOVERY. The baroreflex sensitivity (BRS) was computed in time domain according to the sequence method (αseq). The comparison between therapies (150 J/300 J/placebo) and condition (REST, EXERCISE, and RECOVERY) was performed using the ANOVA two-way repeated measures test. There was no interaction between therapy and conditions during the TECC. There was only the condition effect (p < 0.001), showing that the behavior of αseq was similar regardless of the therapy. Photobiomodulation with 150 J or 300 J applied previously to a moderate-intensity TECC in DM2 was not able to promote cardiovascular autonomic control changes leading to an improvement in BRS.

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References

  1. 1.

    Marwick TH, Hordern MD, Miller T et al (2009) Exercise training for type 2 diabetes mellitus: impact on cardiovascular risk: a scientific statement from the American Heart Association. Circulation 119:3244–3262. https://doi.org/10.1161/CIRCULATIONAHA.109.192521

  2. 2.

    Azmi S, Petropoulos IN, Ferdousi M et al (2019) An update on the diagnosis and treatment of diabetic somatic and autonomic neuropathy. F1000Research 8. https://doi.org/10.12688/f1000research.17118.1

  3. 3.

    Pop-Busui R, Boulton AJM, Feldman EL et al (2017) Diabetic neuropathy: a position statement by the American Diabetes Association. Diabetes Care 40:136–154. https://doi.org/10.2337/dc16-2042

  4. 4.

    de Moura-Tonello SCG, Porta A, Marchi A et al (2016) Cardiovascular variability analysis and baroreflex estimation in patients with type 2 diabetes in absence of any manifest neuropathy. PLoS One 11:e0148903. https://doi.org/10.1371/journal.pone.0148903

  5. 5.

    de Oliveira GM, Porta A, Simões RP et al (2019) The additional impact of type 2 diabetes on baroreflex sensitivity of coronary artery disease patients might be undetectable in presence of deterioration of mechanical vascular properties. Med Biol Eng Comput. https://doi.org/10.1007/s11517-019-01966-3

  6. 6.

    Frattola A, Parati G, Gamba P et al (1997) Time and frequency domain estimates of spontaneous baroreflex sensitivity provide early detection of autonomic dysfunction in diabetes mellitus. Diabetologia 40:1470–1475. https://doi.org/10.1007/s001250050851

  7. 7.

    Davies MJ, D’Alessio DA, Fradkin J et al (2018) Management of hyperglycaemia in type 2 diabetes, 2018. A consensus report by the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD). Diabetologia 61:2461–2498. https://doi.org/10.1007/s00125-018-4729-5

  8. 8.

    Pagkalos M, Koutlianos N, Kouidi E et al (2007) Heart rate variability modifications following exercise training in type 2 diabetic patients with definite cardiac autonomic neuropathy. Br J Sports Med 42:47–54. https://doi.org/10.1136/bjsm.2007.035303

  9. 9.

    Colberg SR, Sigal RJ, Fernhall B et al (2010) Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement executive summary. Diabetes Care 33:2692–2696. https://doi.org/10.2337/dc10-1548

  10. 10.

    Francisco C d O, Beltrame T, Hughson RL et al (2019) Effects of light-emitting diode therapy (LEDT) on cardiopulmonary and hemodynamic adjustments during aerobic exercise and glucose levels in patients with diabetes mellitus: a randomized, crossover, double-blind and placebo-controlled clinical trial. Complement Ther Med 42:178–183. https://doi.org/10.1016/j.ctim.2018.11.015

  11. 11.

    de Sousa MVP, Kawakubo M, Ferraresi C et al (2018) Pain management using photobiomodulation: mechanisms, location, and repeatability quantified by pain threshold and neural biomarkers in mice. J Biophotonics 11:e201700370. https://doi.org/10.1002/jbio.201700370

  12. 12.

    Pires de Sousa MV, Ferraresi C, Kawakubo M et al (2016) Transcranial low-level laser therapy (810 nm) temporarily inhibits peripheral nociception: photoneuromodulation of glutamate receptors, prostatic acid phophatase, and adenosine triphosphate. Neurophotonics 3:015003. https://doi.org/10.1117/1.NPh.3.1.015003

  13. 13.

    Leal-Junior ECP, Vanin AA, Miranda EF et al (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 30:925–939. https://doi.org/10.1007/s10103-013-1465-4

  14. 14.

    Ferraresi C, Huang Y-Y, Hamblin MR (2016) Photobiomodulation in human muscle tissue: an advantage in sports performance? J Biophotonics 9:1273–1299. https://doi.org/10.1002/jbio.201600176

  15. 15.

    Ferraresi C, Hamblin MR, Parizotto NA (2012) Low-level laser (light) therapy (LLLT) on muscle tissue: performance, fatigue and repair benefited by the power of light. Photonics Lasers Med 1:267–286. https://doi.org/10.1515/plm-2012-0032

  16. 16.

    Maegawa Y, Itoh T, Hosokawa T et al (2000) Effects of near-infrared low-level laser irradiation on microcirculation. Lasers Surg Med 27:427–437. https://doi.org/10.1002/1096-9101(2000)27:5<427::AID-LSM1004>3.0.CO;2-A

  17. 17.

    Paolillo FR, Arena R, Dutra DB et al (2014) Low-level laser therapy associated with high intensity resistance training on cardiac autonomic control of heart rate and skeletal muscle remodeling in wistar rats. Lasers Surg Med 46:796–803. https://doi.org/10.1002/lsm.22298

  18. 18.

    Raczak G, Pinna GD, La Rovere MT et al (2005) Cardiovagal response to acute mild exercise in young healthy subjects. Circ J Off J Jpn Circ Soc 69:976–980

  19. 19.

    Peçanha T, Forjaz CLM (1985) Low DA (2017) additive effects of heating and exercise on baroreflex control of heart rate in healthy males. J Appl Physiol Bethesda Md 123:1555–1562. https://doi.org/10.1152/japplphysiol.00502.2017

  20. 20.

    Porta A, Bari V, Maria BD et al (2018) Peripheral resistance Baroreflex during incremental bicycle ergometer exercise: characterization and correlation with cardiac Baroreflex. Front Physiol 9. https://doi.org/10.3389/fphys.2018.00688

  21. 21.

    Peçanha T, Silva-Júnior ND, Forjaz CL d M (2014) Heart rate recovery: autonomic determinants, methods of assessment and association with mortality and cardiovascular diseases. Clin Physiol Funct Imaging 34:327–339. https://doi.org/10.1111/cpf.12102

  22. 22.

    Pinna GD, Porta A, Maestri R et al (2017) Different estimation methods of spontaneous baroreflex sensitivity have different predictive value in heart failure patients. J Hypertens 35:1666–1675. https://doi.org/10.1097/HJH.0000000000001377

  23. 23.

    Barthel P, Bauer A, Müller A et al (2012) Spontaneous baroreflex sensitivity: prospective validation trial of a novel technique in survivors of acute myocardial infarction. Heart Rhythm 9:1288–1294. https://doi.org/10.1016/j.hrthm.2012.04.017

  24. 24.

    American Diabetes Association (2018) 2. Classification and diagnosis of diabetes: standards of medical Care in Diabetes-2018. Diabetes Care 41:S13–S27. https://doi.org/10.2337/dc18-S002

  25. 25.

    Boulton AJM, Vinik AI, Arezzo JC et al (2005) Diabetic neuropathies: a statement by the American Diabetes Association. Diabetes Care 28:956–962

  26. 26.

    American Heart Association, Committee on Exercise, Kattus A (1972) Exercise testing and training of apparently healthy individuals : a handbook for physicians. AHA, Dallas, Tex. ; New York

  27. 27.

    Wasserman K, Hansen J (2005) Principles of exercise testing and interpretation, 4th ed

  28. 28.

    Novais L, Silva E, Simões R et al (2015) Anaerobic threshold by mathematical model in healthy and post-myocardial infarction men. Int J Sports Med 37:112–118. https://doi.org/10.1055/s-0035-1555776

  29. 29.

    Catai AM, Chacon-Mikahil MPT, Martinelli FS et al (2002) Effects of aerobic exercise training on heart rate variability during wakefulness and sleep and cardiorespiratory responses of young and middle-aged healthy men. Braz J Med Biol Res Rev Bras Pesqui Medicas E Biol 35:741–752

  30. 30.

    Ferraresi C, Beltrame T, Fabrizzi F et al (2015) Muscular pre-conditioning using light-emitting diode therapy (LEDT) for high-intensity exercise: a randomized double-blind placebo-controlled trial with a single elite runner. Physiother Theory Pract 31:354–361. https://doi.org/10.3109/09593985.2014.1003118

  31. 31.

    Porta A, Bari V, Bassani T et al (2013) Model-based causal closed-loop approach to the estimate of baroreflex sensitivity during propofol anesthesia in patients undergoing coronary artery bypass graft. J Appl Physiol 115:1032–1042. https://doi.org/10.1152/japplphysiol.00537.2013

  32. 32.

    Catai AM, Pastre CM, de Godoy MF et al (2019) Heart rate variability: are you using it properly? Standardisation checklist of procedures. Braz J Phys Ther. https://doi.org/10.1016/j.bjpt.2019.02.006

  33. 33.

    Bertinieri G, di Rienzo M, Cavallazzi A et al (1985) A new approach to analysis of the arterial baroreflex. J Hypertens Suppl Off J Int Soc Hypertens 3:S79–S81

  34. 34.

    Milan-Mattos JC, Porta A, Perseguini NM et al (2017) Influence of age and gender on the phase and strength of the relation between heart period and systolic blood pressure spontaneous fluctuations. J Appl Physiol 124:791–804. https://doi.org/10.1152/japplphysiol.00903.2017

  35. 35.

    Machado FA, Peserico CS, Mezzaroba PV et al (2017) Light-emitting diodes (LED) therapy applied between two running time trials has a moderate effect on attenuating delayed onset muscle soreness but does not change recovery markers and running performance. Sci Sports 32:286–294. https://doi.org/10.1016/j.scispo.2016.06.010

  36. 36.

    Lellamo F, Legramante M, Raimondi G et al (1996) Evaluation of reproducibility of spontaneous baroreflex sensitivity at rest and during laboratory tests. J Hypertens 14:1099–1104

  37. 37.

    DiCarlo SE, Bishop VS (1992) Onset of exercise shifts operating point of arterial baroreflex to higher pressures. Am J Phys 262:H303–H307. https://doi.org/10.1152/ajpheart.1992.262.1.H303

  38. 38.

    Purkayastha S, Maffuid K, Zhu X et al (2018) The influence of the carotid baroreflex on dynamic regulation of cerebral blood flow and cerebral tissue oxygenation in humans at rest and during exercise. Eur J Appl Physiol 118:959–969. https://doi.org/10.1007/s00421-018-3831-1

  39. 39.

    Halliwill JR (2001) Mechanisms and clinical implications of post-exercise hypotension in humans. Exerc Sport Sci Rev 29:65–70

  40. 40.

    Ferreira Junior A, Schamne JC, de Moraes SMF, Okuno NM (2018) Cardiac autonomic responses and number of repetitions maximum after LED irradiation in the ipsilateral and contralateral lower limb. Lasers Med Sci 33:353–359. https://doi.org/10.1007/s10103-017-2391-7

  41. 41.

    Ash C, Dubec M, Donne K, Bashford T (2017) Effect of wavelength and beam width on penetration in light-tissue interaction using computational methods. Lasers Med Sci 32:1909–1918. https://doi.org/10.1007/s10103-017-2317-4

  42. 42.

    Karu TI, Pyatibrat LV, Kolyakov SF, Afanasyeva NI (2008) Absorption measurements of cell monolayers relevant to mechanisms of laser phototherapy: reduction or oxidation of cytochrome c oxidase under laser radiation at 632.8 nm. Photomed Laser Surg 26:593–599. https://doi.org/10.1089/pho.2008.2246

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Acknowledgments

The study was supported by the São Paulo Research Foundation (FAPESP) (grant no. 2013/07953-3), National Council for Scientific and Technological Development (CNPq) (grant no. 140164/2015 and 169796/2018-3), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brasil (CAPES) (Finance Code 001).

Author information

Correspondence to Juliana Cristina Milan-Mattos.

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The crossover, double-blind, randomized, placebo-controlled clinical trial study was performed according to the principles of the Declaration of Helsinki for medical research involving humans.

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The authors declare that they have no conflict of interest.

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The founders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Milan-Mattos, J.C., de Oliveira Francisco, C., Ferroli-Fabrício, A.M. et al. Acute effect of photobiomodulation using light-emitting diodes (LEDs) on baroreflex sensitivity during and after constant loading exercise in patients with type 2 diabetes mellitus. Lasers Med Sci 35, 329–336 (2020). https://doi.org/10.1007/s10103-019-02815-3

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Keywords

  • Phototherapy
  • Physical exercise
  • Type 2 diabetes mellitus
  • Cardiovascular autonomic control
  • Baroreflex sensitivity
  • Sequence method