Comparison of photobiomodulation in the treatment of skin injury with an open wound in mice

Abstract

This study aimed to investigate the effects of photobiomodulation at a wavelength of 660 and 830 nm at different numbers of application points in the healing of open wounds in mice. In total, 120 mice were divided into 10 groups. The animals were submitted to cutaneous lesion of the open wound type (1.5 × 1.5 cm). Photobiomodulation at a wavelength of 660 and 830 nm and total energy of 3.6 J were used, applied at 1, 4, 5, and 9 points, for 14 days. The animals were subjected to analysis of the lesion area, skin temperature, and histological analysis. Macroscopic analysis results showed a difference (p < 0.05) between the irradiated groups and the sham group at 14 days PO. There was no statistical difference in skin temperature. Histological analysis findings showed better results for the epidermis thickness. Regarding the number of blood vessels, a difference was found between the 1- and 5-point 830-nm photobiomodulation groups and between the 4-point 660-nm group and the naive group. A significant difference in the number of fibroblasts was observed between the 830- and 660-nm photobiomodulation groups and the naive and sham groups. When comparing photobiomodulation wavelength, the 830-nm groups were more effective, and we emphasize the groups irradiated at 5 points, which showed an improvement in macroscopic analysis and epidermis thickness, an increase in the number of vessels, and a lower number of fibroblasts on the 14th day after skin injury.

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References

  1. 1.

    Campos ACL, Borges-Branco A, Groth AK (2007) Cicatrização de feridas. Arq Bras Cir Dig 20:51–58

    Article  Google Scholar 

  2. 2.

    Shah A, Amini-Nik S (2017) The role of phytochemicals in the inflammatory phase of wound healing. Int J Mol Sci. 18(5):1068. https://doi.org/10.3390/ijms18051068

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Lanzafame RJ, Stadler I, Cunningham R, Muhlbauer A, Griggis J, Soltz R, Soltz BA (2013) Preliminary assessment of photoactivated antimicrobial collagen on bioburden in a murine pressure ulcer model. Photomed Laser Surg 31(11):539–546

    CAS  Article  Google Scholar 

  4. 4.

    das Neves LM, Leite GP, Marcolino AM, Pinfildi CE, Garcia SB, Araújo JE, Guirro ECO (2017) Laser photobiomodulation (830 and 660 nm) in mast cells, VEGF, FGF, and CD34 of the musculocutaneous flap in rats submitted to nicotine. Lasers Med Sci 32(2):335–341

    Article  Google Scholar 

  5. 5.

    Zielins ER, Brett EA, Luan A, Hu MS, Walmsley GG, Paik K, Senarath-Yapa K, Atashroo DA, Wearda T, Lorenz HP, Wan DC, Longaker MT (2015) Emerging drugs for the treatment of wound healing. Expert Opin Emerg Drugs 20(2):235–246

    CAS  Article  Google Scholar 

  6. 6.

    Norman G, Dumville JC, Moore ZE, Tanner J, Christie J, Goto S (2016) Antibiotics and antiseptics for pressure ulcers. Cochrane Database Syst Rev 4:Cd011586

    Google Scholar 

  7. 7.

    Reddy M, Gill SS, Kalkar SR, Wu W, Anderson PJ, Rochon PA (2008) Treatment of pressure ulcers: a systematic review. Jama. 300(22):2647–2662

    CAS  Article  Google Scholar 

  8. 8.

    Han G, Ceilley R (2017) Chronic wound healing: a review of current management and treatments. Adv Ther 34(3):599–610

    Article  Google Scholar 

  9. 9.

    Zhang L, Weng C, Zhao Z, Fu X (2017) Extracorporeal shock wave therapy for chronic wounds: a systematic review and meta-analysis of randomized controlled trials. Wound Repair Regen 25(4):697–706

    Article  Google Scholar 

  10. 10.

    Neves LM, Guirro EC, Albuquerque FL, Marcolino AM (2016) Effects of high-voltage electrical stimulation in improving the viability of musculocutaneous flaps in rats. Ann Plast Surg 77(4):e50–e54

    CAS  Article  Google Scholar 

  11. 11.

    Bora Karsli P, Gurcay E, Karaahmet OZ, Cakci A (2017) High-voltage electrical stimulation versus ultrasound in the treatment of pressure ulcers. Adv Skin Wound Care 30(12):565–570

    Article  Google Scholar 

  12. 12.

    Khouri C, Kotzki S, Roustit M, Blaise S, Gueyffier F, Cracowski JL (2017) Hierarchical evaluation of electrical stimulation protocols for chronic wound healing: an effect size meta-analysis. Wound Repair Regen 25(5):883–891

    Article  Google Scholar 

  13. 13.

    Chen B, Kao HK, Dong Z, Jiang Z, Guo L (2017) Complementary effects of negative-pressure wound therapy and pulsed radiofrequency energy on cutaneous wound healing in diabetic mice. Plast Reconstr Surg 139(1):105–117

    CAS  Article  Google Scholar 

  14. 14.

    Nicoletti G, Perugini P, Bellino S, Capra P, Malovini A, Jaber O, Tresoldi M, Faga A (2017) Scar remodeling with the association of monopolar capacitive radiofrequency, electric stimulation, and negative pressure. Photomed Laser Surg 35(5):246–258

    CAS  Article  Google Scholar 

  15. 15.

    Dungel P, Hartinger J, Chaudary S, Slezak P, Hofmann A, Hausner T, Strassl M, Wintner E, Redl H, Mittermayr R (2014) Low-level light therapy by LED of different wavelength induces angiogenesis and improves ischemic wound healing. Lasers Surg Med 46(10):773–780

    Article  Google Scholar 

  16. 16.

    Machado RS, Viana S, Sbruzzi G (2017) Low-level laser therapy in the treatment of pressure ulcers: systematic review. Lasers Med Sci 32(4):937–944

    Article  Google Scholar 

  17. 17.

    Karu TI, Pyatibrat LV, Afanasyeva NI (2005) Cellular effects of low power laser therapy can be mediated by nitric oxide. Lasers Surg Med 36:307–314

    Article  Google Scholar 

  18. 18.

    De Oliveira RF, Oliveira DA, Monteiro W, Zangaro RA, Magini M, Soares CP (2008) Comparison between the effect of low-level laser therapy and low-intensity pulsed ultrasonic irradiation in vitro. Photomed Laser Surg 26(1):6–9

    Article  Google Scholar 

  19. 19.

    Lins R, Dantas E, Lucena K, Catão M, Granville-Garcia A, Carvalho Neto L (2010) Efeitos bioestimulantes do laser de baixa potência no processo de reparo. An Bras Dermatol. 85(6):849–55. https://doi.org/10.1590/s0365-05962010000600011

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Andrade FS, Clark RM, Ferreira ML (2014) Effects of low-level laser therapy on wound healing. Rev Col Bras Cir 41(2):129–133

    Article  Google Scholar 

  21. 21.

    Sousa RC, Maia Filho AL, Nicolau RA, Mendes LM, Barros TL, Neves SM (2015) Action of AlGaInP laser and high-frequency generator in cutaneous wound healing. A comparative study. Acta Cir Bras 30(12):791–798

    Article  Google Scholar 

  22. 22.

    de Freitas LF, Hamblin MR (2016) Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron 22(3):1–17. https://doi.org/10.1109/JSTQE.2016.2561201

  23. 23.

    Freitas APP, Antiorio ATB, Seabra DI (2017) Anestesia e analgesia em animais de laboratório. In: UNICAMP

  24. 24.

    Guia anestesia e analgesia em animais de laboratório. In: (CEUA), 2017

  25. 25.

    Schoell AR, Heyde BR, Weir DE, Chiang PC, Hu Y, Tung DK (2009) Euthanasia method for mice in rapid time-course pulmonary pharmacokinetic studies. J Am Assoc Lab Anim Sci 48(5):506–511

  26. 26.

    Manual de normas do Laboratório de Técnica Operatória e Cirurgia Experimental. In: UFSC, Santa Catarina, ed. 2013

  27. 27.

    Solmaz H, Dervisoglu S, Gulsoy M, Ulgen Y (2016) Laser biostimulation of wound healing: bioimpedance measurements support histology. Lasers Med Sci 31(8):1547–1554

    Article  Google Scholar 

  28. 28.

    Uzeda-E-Silva VD, Rodriguez TT, Rocha IA, Xavier FCA, Santos JN, Cury PR, Ramalho LMP (2016) Laser phototherapy improves early stage of cutaneous wound healing of rats under hyperlipidic diet. Lasers Med Sci 31(7):1363–1370

    Article  Google Scholar 

  29. 29.

    Chiarotto GB, Neves LM, Esquisatto MA, do Amaral ME, dos Santos GM, Mendonca FA (2014) Effects of laser irradiation (670-nm InGaP and 830-nm GaAlAs) on burn of second-degree in rats. Lasers Med Sci 29(5):1685–1693

    Article  Google Scholar 

  30. 30.

    Rocha Júnior AM, Oliveira RG, Farias RE, Andrade LCF, Aarestrup FM (2006) Modulação da proliferação fibroblástica e da resposta inflamatória pela terapia a laser de baixa intensidade no processo de reparo tecidual. An Bras Dermatol 81:150–156

    Article  Google Scholar 

  31. 31.

    das Neves LM, Marcolino AM, Prado RP, Ribeiro TS, Pinfildi CE, Thomazini JA (2011) Low-level laser therapy on the viability of skin flap in rats subjected to deleterious effect of nicotine. Photomed Laser Surg 29(8):581–587

    Article  Google Scholar 

  32. 32.

    Neves LMS, Marcolino AM, Prado RP, Thomazini JA (2011) Laser 830nm na viabilidade do retalho cutâneo de ratos submetidos à nicotina. Acta Ortop Bras 19(6):342–345

    Article  Google Scholar 

  33. 33.

    Gupta A, Dai T, Hamblin MR (2014) Effect of red and near-infrared wavelengths on low-level laser (light) therapy-induced healing of partial-thickness dermal abrasion in mice. Lasers Med Sci 29(1):257–265

    Article  Google Scholar 

  34. 34.

    Rathnakar B, Rao BS, Prabhu V, Chandra S, Rai S, Rao ACK, Sharma M, Gupta PK, Mahato KK (2016) Photo-biomodulatory response of low-power laser irradiation on burn tissue repair in mice. Lasers Med Sci 31(9):1741–1750

    Article  Google Scholar 

  35. 35.

    Sommer AP, Pinheiro AL, Mester AR, Franke RP, Whelan HT (2001) Biostimulatory windows in low-intensity laser activation: lasers, scanners, and NASA’s light-emitting diode array system. J Clin Laser Med Surg 19(1):29–33

    CAS  Article  Google Scholar 

  36. 36.

    Hamblin MR (2018) Mechanisms and mitochondrial redox signaling in photobiomodulation. Photochem Photobiol 94(2):199–212

    CAS  Article  Google Scholar 

  37. 37.

    Carroll J (2008) A 3D dose model for low level laser/led therapy biostimulation and bioinhibition. 3 Chap; pp. 327 - 443. In: Hamblin MR, Waynant RW, Anders J. Mechanisms for Low-Light Therapy III. Proc. SPIE 6846. https://doi.org/10.1117/12.771183

  38. 38.

    Pinfildi CE, Liebano RE, Hochman BS, Ferreira LM (2005) Helium-neon laser in viability of random skin flap in rats. Lasers Surg Med 37(1):74–77

    Article  Google Scholar 

  39. 39.

    Prado RP, Pinfildi CE, Liebano RE, Hochman BS, Ferreira LM (2009) Effect of application site of low-level laser therapy in random cutaneous flap viability in rats. Photomed Laser Surg 27(3):411–416

    Article  Google Scholar 

  40. 40.

    Pinfildi CE, Hochman BS, Nishioka MA, Sheliga TR, Neves MAI, Liebano RE, Ferreira LM (2013) What is better in TRAM flap survival: LLLT single or multi-irradiation? Lasers Med Sci 28(3):755–761. https://doi.org/10.1007/s10103-012-1130-3

    Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Martignago CCS, Tim CR, Assis L, Neves LMG, Bossini PS, Renno AC, LIebano RE, Parizotto N (2018) Comparison of two different laser photobiomodulation protocols on the viability of random skin flap in rats. Lasers Med Sci 34:1041–1047. https://doi.org/10.1007/s10103-018-2694-3

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Goncalves RV, Novaes RD, Matta SL, Benevides GP, Faria FR, Pinto MV (2010) Comparative study of the effects of gallium-aluminum-arsenide laser photobiomodulation and healing oil on skin wounds in Wistar rats: a histomorphometric study. Photomed Laser Surg 28(5):597–602

    CAS  Article  Google Scholar 

  43. 43.

    Goncalves RV, Novaes RD, Cupertino Mdo C, Moraes B, Leite JPV, Peluzio MCG, Pinto MVM, Patta LP (2013) Time-dependent effects of low-level laser therapy on the morphology and oxidative response in the skin wound healing in rats. Lasers Med Sci 28(2):383–390. https://doi.org/10.1007/s10103-012-1066-7

    Article  Google Scholar 

  44. 44.

    Carneiro C, Schleder JC, Fischer SV, Zedebski RAM, Verner AF, Lipinski L (2015) Efeito de lasers de baixa potência no reparo de lesões cutâneas. Publicatio uepg Ciências biológicas e da saúde (online) 21:109–115

    Google Scholar 

  45. 45.

    Yadav A, Gupta A (2017) Noninvasive red and near-infrared wavelength-induced photobiomodulation: promoting impaired cutaneous wound healing. Photodermatol Photoimmunol Photomed 33(1):4–13

    Article  Google Scholar 

  46. 46.

    Gal P, Vidinsky B, Toporcer T, Mokrý M, Mozes S, Longauer F, Sabo J (2006) Histological assessment of the effect of laser irradiation on skin wound healing in rats. Photomed Laser Surg 24(4):480–488

    Article  Google Scholar 

  47. 47.

    Leite GP, das Neves LM, Silva CA, Guirro RRJ, Souza TR, Souza AK, Garcia SB, Guirro ECO (2017) Photobiomodulation laser and pulsed electrical field increase the viability of the musculocutaneous flap in diabetic rats. Lasers Med Sci 32(3):641–648. https://doi.org/10.1007/s10103-017-2160-7

    Article  Google Scholar 

  48. 48.

    Melo VA, Anjos DCS, Albuquerque Júnior R, Melo DB, Carvalho FUR (2011) Effect of low level laser on sutured wound healing in rats. Acta Cir Bras 26:129–134. https://doi.org/10.1590/s0102-86502011000200010

    Article  Google Scholar 

  49. 49.

    Wagner VP, Curra M, Webber LP, Nor C, Matte U, Meurer L, Martins MD (2016) Photobiomodulation regulates cytokine release and new blood vessel formation during oral wound healing in rats. Lasers Med Sci 31(4):665–671. https://doi.org/10.1007/s10103-016-1904-0

    Article  Google Scholar 

  50. 50.

    Medeiros AC, Dantas-Filho AM (2017) Cicatrização das feridas cirúrgicas. J Surg Clin Res 7(2):87–102. https://doi.org/10.20398/jscr.v7i2.11438

    Article  Google Scholar 

  51. 51.

    Gonçalves RV, Mezêncio JMS, Benevides GP, Matta SLP, Neves CA, Sarandy MM, Vilela EF (2010) Effect of gallium-arsenide laser, gallium-aluminum-arsenide laser and healing ointment on cutaneous wound healing in Wistar rats. Braz J Med Biol Res 43:350–355. https://doi.org/10.1590/S0100-879X2010007500022

    Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Sampaio SCPO, Monteiro JSC, Cangussu MCT, Santos GMP, Santos MAV, Santos JN, Pineiro ALB (2013) Effect of laser and LED phototherapies on the healing of cutaneous wound on healthy and iron-deficient Wistar rats and their impact on fibroblastic activity during wound healing. Lasers Med Sci 28(3):799–806. https://doi.org/10.1007/s10103-012-1161-9

    Article  Google Scholar 

  53. 53.

    Chaves ME, Araujo AR, Piancastelli AC, Pinotti M (2014) Effects of low-power light therapy on wound healing: LASER × LED. An Bras Dermatol 89(4):616–623

    Article  Google Scholar 

  54. 54.

    Solmaz H, Ulgen Y, Gulsoy M (2017) Photobiomodulation of wound healing via visible and infrared laser irradiation. Lasers Med Sci 32(4):903–910

    Article  Google Scholar 

  55. 55.

    Christensen J, Matzen LH, Vaeth M, Schou S, Wenzel A (2012) Thermography as a quantitative imaging method for assessing postoperative inflammation. Dentomaxillofac Radiol 41(6):494–499

    CAS  Article  Google Scholar 

  56. 56.

    Dostalova T, Kroulikova V, Podzimek S, Jelinkova H (2017) Low-level laser therapy after wisdom teeth surgery: evaluation of immunologic markers (secretory immunoglobulin a and lysozyme levels) and thermographic examination: placebo controlled study. Photomed Laser Surg 35(11):616–621

    CAS  Article  Google Scholar 

  57. 57.

    Carvalho A, Bizo MHA, Toma HS, Guedes KMR, Muraro LS, Musis C (2017) Effect of gallium arsenide low-level laser therapy on the inflammatory phase of skin wound healing in rats. Acta Vet Bras 11(4):226–230. https://doi.org/10.21708/avb.2017.11.4.7274

    Article  Google Scholar 

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Funding

This research was funded by the Coordination for Improvement of Higher Education Personnel (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES). Financial support was received for the master’s student.

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Correspondence to Alexandre Marcio Marcolino.

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This study was approved by the Ethics Committee (CEUA) under number 4017201117.

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Hendler, K.G., Canever, J.B., de Souza, L.G. et al. Comparison of photobiomodulation in the treatment of skin injury with an open wound in mice. Lasers Med Sci (2021). https://doi.org/10.1007/s10103-020-03216-7

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Keywords

  • Low-intensity laser therapy
  • Mice
  • Healing
  • Histology
  • Injuries