High energy photobiomodulation therapy in the early days of injury improves sciatic nerve regeneration in mice
Main Article Content
Abstract
Introduction: Different studies have evaluated the effects of electrophysical agents on regeneration after peripheral nerve injury. Among them, the most used in clinical and experimental research is photobiomodulation therapy (PBMT). Objective: To analyze the effect of standard energy (16.8 J) of PBMT on peripheral nerve regeneration, applied at different periods after sciatic nerve injury in mice. Methods: Thirty male Swiss mice were divided into six groups: naive; sham; control; LLLT-01 (660 nm, 16.8 J of total energy emitted in 1 day); LLLT-04 (660 nm, 4.2 J per day, 16.8 J of total energy emitted in 4 days); LLLT-28, (660 nm, 0.6 J per day, 16.8 J of total energy emitted over 28 days). The animals were evaluated using thermal hyperalgesia, Sciatic Functional Index (SFI), and Static Sciatic Index (SSI). Data were obtained at baseline and after 7, 14, 21, and 28 days after surgery. Results: For the SFI and SSI, all groups showed significant differences compared to the control group, and the LLLT-04 group presented the best results among those receiving PBMT. In the assessment of thermal hyperalgesia, there was a significant difference in the 14th day of evaluation in the LLLT-04 group. Conclusion: The application of 16.8 J was useful in sciatic nerve regeneration with an improvement of hyperalgesia, with higher efficacy when applied in four days (4.2 J/day).
Downloads
Article Details
Authors who publish with this journal agree to the following terms:
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY) that allows others to share and adapt the work with an acknowledgement of the work's authorship and initial publication in this journal.
Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.References
Taylor CA, Braza D, Rice JB, Dillingham T. The incidence of peripheral nerve injury in extremity trauma. Am J Phys Med Rehabil. 2008;87(5):381-5. http://doi.org/10.1097/PHM.0b013e31815e6370
Simon NG, Spinner RJ, Kline DG, Kliot M. Advances in the neurological and neurosurgical management of peripheral nerve trauma. J Neurol Neurosurg Psychiatry. 2016; 87(2):198-208. https://doi.org/10.1136/jnnp-2014-310175
Stratton JA, Kumar R, Sinha S, Shah P, Stykel M, Shapira Y, et al. Purification and characterization of Schwann cells from adult human skin and nerve. eNeuro. 2017; 4(3):307-16. https://doi.org/10.1523/ENEURO.0307-16.2017
Geuna S. The sciatic nerve injury model in pre-clinical research. J Neurosci Methods. 2015;243:39-46.
https://doi.org/10.1016/j.jneumeth.2015.01.021
Grinsell D, Keating C. Peripheral nerve reconstruction after injury: A review of clinical and experimental therapies. Biomed Res Int. 2014;2014:698256. http://dx.doi.org/10.1155/2014/698256
Xia B, Chen G, Zou Y, Yang L, Pan J, Lv Y. Low intensity pulsed ultrasound combination with induced pluripotent stem cells derived neural crest stem cells and growth differentiation factor 5 promotes sciatic nerve regeneration and functional recovery. J Tissue Eng Regen Med. 2019;13(4):625-36. http://doi.org/10.1002/term.2823
Ni XJ, Wang XD, Zhao YH, Sun HL, Hu YM, Yao J, et al. The Effect of Low-Intensity Ultrasound on Brain-Derived Neurotropic Factor Expression in a Rat Sciatic Nerve Crushed Injury Model. Ultrasound Med Biol. 2017;43(2):461-8. https://dx.doi.org/10.1016/j.ultrasmedbio.2016.09.0 17
Willand MP, Nguyen MA, Borschel GH, Gordon T. Electrical Stimulation to Promote Peripheral Nerve Regeneration. Neurorehabil Neural Repair. 2016;30(5):490-6. https://doi.org/10.1177/1545968315604399
Souza LG, Marcolino AM, Kuriki HU, Gonçalves ECD, Fonseca MCR, Barbosa RI. Comparative effect of photobiomodulation associated with dexamethasone after sciatic nerve injury model. Lasers Med Sci. 2018;33(6):1341-9. http://dx.doi.org/ 10.1007/s10103-018-2494-9
Barbosa RI, Marcolino AM, Guirro RRJ, Mazzer N, Barbieri CH, Fonseca MCR. Comparative effects of wavelengths of low-power laser in regeneration of sciatic nerve in rats following crushing lesion. Lasers Med Sci. 2010;25(3):423-30. https://doi.org/10.1007/s10103-009-0750-8
Barbosa RI, Marcolino AM, Guirro RRJ, Mazzer N, Barbieri CH, Fonseca MCR. Efeito do laser de baixa intensidade (660 nm) na regeneração do nervo isquiático lesado em ratos. Fisioter Pesqui. 2010;17(4):294-9.
http://dx.doi.org/10.1590/S1809-29502010000400002
Ziago EK, Fazan VP, Iyomasa MM, Sousa LG, Yamauchi PY, Silva EA, et al. Analysis of the variation in low-level laser energy density on the crushed sciatic nerves of rats: a morphological, quantitative, and morphometric study. Lasers Med Sci. 2017; 32(2):369-78. https://doi.org/10.1007/s10103-016-2126-1
Buchaim DV, Rodrigues AC, Buchaim RL, Barraviera B, Ferreira Junior RS, Rosa Junior GM, et al. The new heterologous fibrin sealant in combination with low-level laser therapy (LLLT) in the repair of the buccal branch of the facial nerve. Lasers Med Sci. 2016;31(5):965-72. https://doi.org/10.1007/s10103-016-1939-2
Fallah A, Mirzaei A, Gutknecht N, Demneh AS. Clinical effectiveness of low-level laser treatment on peripheral somatosensory neuropathy. Lasers Med Sci. 2017;32(3):721-8. https://doi.org/10.1007/s10103-016-2137-y
Barez MM, Tajziehchi M, Heidari MH, Bushehri A, Moayer F, Mansouri N, et al. Stimulation effect of low level laser therapy on sciatic nerve regeneration in rat. J Lasers Med Sci. 2017;8(Suppl 1):S32-7. https://doi.org/10.15171/jlms.2017.s7
Albuquerque-Pontes GM, Vieira RP, Tomazoni SS, Caires CO, Nemeth V, Vanin AA, et al. 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. 2015;30(1):59-66.
https://doi.org/10.1007/s10103-014-1616-2
Gupta A, Keshri GK, Yadav A, Gola S, Chauhan S, Salhan AK, et al. Superpulsed (Ga-As, 904 nm) low-level laser therapy (LLLT) attenuates inflammatory response and enhances healing of burn wounds. J Biophotonics. 2015;8(6):489-5. https://doi.org/10.1002/jbio.201400058
Karu T, Pyatibrat LV, Afanasyeva NI. A Novel mitochondria1 signaling pathway activated by visi ble-to-near infrared radiation. Photochem Photobiol. 2004;80(2)366-72. https://doi.org/10.1562/2004-03-25-RA-123
Karu TI. Critical review multiple roles of cytochrome c oxidase in mammalian cells under action of red and IR-A radiation. IUBMB Life. 2010;62(8):607-10. https://doi.org/10.1002/iub.359
Andrade ALM, Bossini PS, Souza ALMC, Sanchez AD, Parizotto NA. Effect of photobiomodulation therapy (808 nm) in the control of neuropathic pain in mice. Lasers Med Sci. 2017;32(4):865-72. https://doi.org/10.1007/s10103-017-2186-x
Rocha IR, Ciena AP, Rosa AS, Martins DO, Chacur M. Photobiostimulation reverses allodynia and peripheral nerve damage in streptozotocin-induced type 1 diabetes. Lasers Med Sci. 2017;32(3):495-501.
https://doi.org/10.1007/s10103-016-2140-3
Lee JH, Chiang MH, Chen PH, Ho ML, Lee HE, Wang YH. Anti-inflammatory effects of low-level laser therapy on human periodontal ligament cells: in vitro study. Lasers Med Sci. 2018;33(3):469-77. https://doi.org/10.1007/s10103-017-2376-6
Andreo L, Soldera CB, Ribeiro BG, Matos PRV, Bussadori SK, Fernandes KPS, et al. Effects of photobiomodulation on experimental models of peripheral nerve injury. Lasers Med Sci. 2017;32(9):2155-65.
https://doi.org/10.1007/s10103-017-2359-7
Al-Shammari AM, Syhood Y, Al-Khafaji AS. Use of low-power He-Ne laser therapy to accelerate regeneration processes of injured sciatic nerve in rabbit. Egypt J Neurol Psychiatry Neurosurg. 2019;55(1).
https://doi.org/10.1186/s41983-018-0047-6
Huang YY, Chen ACH, Carroll JD, Hamblin MR. Biphasic Dose response in low level light therapy. Dose Response. 2009;7(4):358-83. https://doi.org/10.2203/dose-response.09-027.Hamblin
Wolff AV, Wolff DVM, Smith PD. Office of Laboratory Animal Welfare. Compliance at the institutional and programmatic level. Lab Animal. 1994;23(8):28-9.
Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32(1):77-88. http://doi.org/10.1016/0304-3959(88)90026-7
Fernandes ES, Russell FA, Alawi KM, Sand C, Liang L, Salamon R, et al. Environmental cold exposure increases blood flow and affects pain sensitivity in the knee joints of CFA-induced arthritic mice in a TRPA1-dependent manner. Arthritis Res Ther. 2016;18:7. http://doi.org/10.1186/s13075-015-0905-x
Medinaceli L, Freed WJ, Wyatt RJ. An index of the functional condition of rat sciatic nerve based on measurements made from walking tracks. Exp Neurol. 1982;77(3):634-43. https://doi.org/10.1016/0014-4886(82)90234-5
Smit X, van Neck JW, Ebeli MJ, Hovius SE. Static footprint analysis: a time-saving functional evaluation of nerve repair in rats. Scand J Plast Reconstr Surg Hand Surg. 2004;38(6):321-5. https://doi.org/10.1080/02844310410034277
Bervar M. Video analysis of standing: an alternative footprint analysis to assess functional loss following injury to the rat sciatic nerve. J Neurosci Methods. 2000; 102(2):109-16. https://doi.org/10.1016/S0165-0270(00)00281-8
Monte-Raso VV, Moro CA, Mazzer N, Fonseca MCR, Fazan VPS, Barbieri G, et al. A new adjustable pinch designed for producing crush nerve injuries in the sciatic nerve of rats. Acta Ortop Bras. 2009;17(4):236-8.
http://dx.doi.org/10.1590/S1413-78522009000400009
Baptista AF, Gomes JR S, Oliveira JT, Santos SMG, Vannier-Santos MA, Martinez AMB. A new approach to assess function after sciatic nerve lesion in the mouse-adaptation of the sciatic static index. J Neurosci Methods. 2007;161(2):259-64. https://doi.org/10.1016/j.jneumeth.2006.11.016
Takhtfooladi M, Jahanbakhsh F, Takhtfooladi H, Yousefi K, Allahverdi A. 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. 2015;30(3):1047-52. https://doi.org/10.1007/s10103-015-1709-6
Seddon HJ. The use of autogenous grafts for the repair of large gaps in peripheral nerves. Br J Surg. 1947;35(138):151-67. https://doi.org/10.1002/bjs.18003513808
Wong KM, Babetto E, Beirowski B. Axon degeneration: make the Schwann cell great again. Neural Regen Res. 2017;12(4):518-24. https://doi.org/10.4103/1673-5374.205000
Marques CO, Faccioni-Heuser MC, Malysz T. Efeitos da vibração de corpo inteiro sobre a morfofuncionalidade do nervo isquiático em um modelo experimental de lesão por esmagamento. Dissertação (Mestrado) - Universidade Federal do Rio Grande do Sul. Porto Alegre: 2017.
Wang T, Ito A, T Aoyama, Nakahara R, Nakahata A, X Ji, et al. Functional evaluation outcomes correlate with histomorphometric changes in the rat sciatic nerve crush injury model: A comparison between sciatic functional index and kinematic analysis. PLoS One. 2018;13(12):e0208985. https://doi.org/10.1371/journal.pone.0208985
Lai HC, Lu CH, Wong CS, Lin BF, Chan SM, Kuo CY, et al. Baicalein attenuates neuropathic pain and improves sciatic nerve function recovery in rats with partial sciatic nerve transection. J Chin Med Assoc. 2018;81(11):955-63. https://doi.org/10.1016/j.jcma.2018.03.014
Almeida MMMM, Mangueira NM, Gama Filho OP, Oliveira MM, Heluy RA, Silveira Jr L, et al. Biochemical changes in injured sciatic nerve of rats after low-level laser therapy (660 nm and 808 nm) evaluated by Raman spectroscopy. Lasers Med Sci. 2019;34(3):525-35. https://doi.org/10.1007/s10103-018-2627-1