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Low-level laser therapy (LLLT) improves alveolar bone healing in rats

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Abstract

The main objective of the present study was to evaluate the effect of low-level laser therapy (LLLT) in enhancing bone healing in irradiated alveolus post-tooth extraction. Sixty male Wistar rats (180 ± 10 g) were used in the present study. The left maxillary first molars were extracted, and the alveolar region was irradiated by diode laser device (GaAlAs) immediately after extraction and for more 3-day daily applications. The animals were randomly assigned into two groups: control group (n = 30, with left maxillary molar extraction—CG) and experimental group (n = 30, with tooth extraction and low-level laser therapy applied to the dental alveolus for 42 s—EG). These groups were divided into subgroups (five rats per subgroup) according to the observation time point—1, 2, 3, 5, 7, and 10 days—post-tooth extraction. The maxillary bone was separated, and the specimens were stained with hematoxylin and eosin, Masson’s trichrome, and picrosirius red and immunohistochemistry for RUNX-2. Parametric and nonparametric tests were used with a significance level of 5%. LLLT accelerated bone healing with mature collagen fiber bundles and early new bone formation. Histomorphometric analysis revealed an increase of osteoblast (RUNX-2) and osteoclast (TRAP) activity and in the area percentage of cancellous bone in the lased alveolus compared to the control group. This increase was statistically significant (p < 0.05). Application of LLLT with a GaAlAs diode laser device enhanced bone healing and mineralization on alveolar region.

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References

  1. Kawasaki K, Shimizu N (2000) Effects of low-energy laser irradiation on bone remodeling during experimental tooth movement in rats. Lasers Surg Med 26(3):282–291

    CAS  PubMed  Google Scholar 

  2. Khadra M, Kasem N, Haanæs HR, Ellingsen JE, Lyngstadaas SP (2004) Enhancement of bone formation in rat calvarial bone defects using low-level laser therapy. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontology 97(6):693–700

    PubMed  Google Scholar 

  3. Hall B (1994) Embryonic bone formation with special reference to epithelial-mesenchymal interactions and growth factors. Bone 8:137–192

    Google Scholar 

  4. Garant PR, Garant P (2003) Oral cells and tissues, vol 35. Quintessence Publishing Company Chicago,

  5. Yamada Y, Nakamura-Yamada S, Miki M, Nakajimaa Y, Babaa S Trends in clinical trials on bone regeneration in dentistry-towards an innovative development in dental implant treatment. In, 2020.

  6. Nie L, Yang X, Duan L, Huang E, Pengfei Z, Luo W, Zhang Y, Zeng X, Qiu Y, Cai T, Li C (2017) The healing of alveolar bone defects with novel bio-implants composed of Ad-BMP9-transfected rDFCs and CHA scaffolds. Sci Rep 7(1):6373. https://doi.org/10.1038/s41598-017-06548-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Sheikh Z, Hamdan N, Ikeda Y, Grynpas M, Ganss B, Glogauer M (2017) Natural graft tissues and synthetic biomaterials for periodontal and alveolar bone reconstructive applications a review. Biomater Res 21(1):9. https://doi.org/10.1186/s40824-017-0095-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Moreno Sancho F, Leira Y, Orlandi M, Buti J, Giannobile WV, D’Aiuto F (2019) Cell-based therapies for alveolar bone and periodontal regeneration concise review. Stem Cells Transl Med 8(12):1286–1295. https://doi.org/10.1002/sctm.19-0183

    Article  PubMed  PubMed Central  Google Scholar 

  9. Ribeiro LNS, Monteiro PM, Barretto GD, Luiz KG, Alves SYF, Stuani MBS (2020) The effect of cigarette smoking and low-level laser irradiation in RANK/RANKL/OPG expression. Braz Dent J 31:57–62

    PubMed  Google Scholar 

  10. Kana JS, Hutschenreiter G (1981) Effect of low—power density laser radiation on healing of open skin wounds in rats. Arch Surg 116(3):293–296

    CAS  PubMed  Google Scholar 

  11. Mester E, Nagylucskay S, Tisza S, Mester A (1978) Stimulation of wound healing by means of laser rays Part III-investigation of the effect on immune competent cells. Acta Chir Acad Sci Hung 19(2):163–170

    CAS  PubMed  Google Scholar 

  12. Colls J (1984) La terapia laser actual. Centro de Documentación Laser-Medtec, Barcelona

    Google Scholar 

  13. Chomette G, Auriol M, Zeitoun R, Mousques T (1987) Effect of the soft laser on gingival connective tissue I-effect on fibroblasts Histoenzymology and electron microscopy study. J Biol Buccale 15(1):45–49

    CAS  PubMed  Google Scholar 

  14. Chomette G, Auriol M, Zeitoun R, Mousques T (1987) Effect of the soft laser on gingival connective tissue II-effect on wound healing Optical microscopy histoenzymology and electron microscopy studies. J Biol Buccale 15(1):51–57

    CAS  PubMed  Google Scholar 

  15. Khadra M, Rønold HJ, Lyngstadaas SP, Ellingsen JE, Haanæs HR (2004) Low-level laser therapy stimulates bone–implant interaction: an experimental study in rabbits. Clin Oral Implants Res 15(3):325–332

    PubMed  Google Scholar 

  16. Liu X, Lyon R, Meier HT, Thometz J, Haworth ST (2007) Effect of lower-level laser therapy on rabbit tibial fracture. Photomed Laser Surg 25(6):487–494

    PubMed  Google Scholar 

  17. Nissan J, Assif D, Gross M, Yaffe A, Binderman I (2006) Effect of low intensity laser irradiation on surgically created bony defects in rats. J Oral Rehabil 33(8):619–924

    CAS  PubMed  Google Scholar 

  18. Ueda Y, Shimizu N (2003) Effects of pulse frequency of low-level laser therapy (LLLT) on bone nodule formation in rat calvarial cells. J Clin Laser Med Surg 21(5):271–277

    PubMed  Google Scholar 

  19. Dörtbudak O, Haas R, Mailath-Pokorny G (2000) Biostimulation of bone marrow cells with a diode soft laser. Clin Oral Implants Res 11(6):540–545

    PubMed  Google Scholar 

  20. Santinoni CdS, Oliveira HFF, Batista VEdS, Lemos CAA, Verri FR (2017) Influence of low-level laser therapy on the healing of human bone maxillofacial defects: a systematic review. J Photochem Photobiol, B 169:83–89. https://doi.org/10.1016/j.jphotobiol.2017.03.004

    Article  CAS  Google Scholar 

  21. da Silva APRB, Petri AD, Crippa GE, Stuani AS, Stuani AS, Rosa AL, Stuani MBS (2012) Effect of low-level laser therapy after rapid maxillary expansion on proliferation and differentiation of osteoblastic cells. Lasers in Medical Science 27(4):777–783. https://doi.org/10.1007/s10103-011-0968-0

    Article  PubMed  Google Scholar 

  22. Junqueira L, Carneiro J (1982) Tecido Ósseo. Histologia Básica. Editora Guanabara Koogan, Rio de Janeiro

    Google Scholar 

  23. César-Neto JB, Benatti BB, Sallum EA, Casati MZ, Nociti FH Jr (2006) The influence of cigarette smoke inhalation and its cessation on the tooth-supporting alveolar bone a histometric study in rats. J Periodontal Res 41(2):118–123

    PubMed  Google Scholar 

  24. de Figueiredo FA, Shimano RC, Ervolino E, Pitol DL, Gerlach RF, Issa JPM (2019) Doxycycline reduces osteopenia in female rats. Sci Rep 9(1):1–14

    Google Scholar 

  25. Ribeiro LNS Avaliação da remodelação óssea em alvéolos dentários, após a aplicação do laser de baixa potência. Universidade de São Paulo,

  26. Wolfson EM, Seltzer S (1975) Reaction of rat connective tissue to some gutta-percha formulations. J Endod 1(12):395–402

    CAS  PubMed  Google Scholar 

  27. Dahlin C, Sennerby L, Lekholm U, Linde A, Nyman S (1989) Generation of new bone around titanium implants using a membrane technique an experimental study in rabbits. Int J Oral Maxillofac Implants 4:1

    Google Scholar 

  28. Lindhe J, Meyle J (2008) Peri-implant diseases: consensus report of the sixth European workshop on periodontology. J Clin Periodontol 35(8 Suppl):282–285. https://doi.org/10.1111/j.1600-051X.2008.01283.x

    Article  PubMed  Google Scholar 

  29. Hedner E, Linde A (1995) Efficacy of bone morphogenetic protein (BMP) with osteopromotive membranes–an experimental study in rat mandibular defects. Eur J Oral Sci 103(4):236–241

    CAS  PubMed  Google Scholar 

  30. Holland R, Mazuqueli L, de Souza V, Murata SS, Júnior ED, Suzuki P (2007) Influence of the type of vehicle and limit of obturation on apical and periapical tissue response in dogs’ teeth after root canal filling with mineral trioxide aggregate. J Endod 33(6):693–697

    PubMed  Google Scholar 

  31. Markel MD, Wikenheiser M, Chao E (1991) Formation of bone in tibial defects in a canine model Histomorphometric and biomechanical studies. J Bone Joint Surg Am 73(6):914–923

    CAS  PubMed  Google Scholar 

  32. da Silva RV, Camilli JA (2006) Repair of bone defects treated with autogenous bone graft and low-power laser. J Craniofac Surg 17(2):297–301

    PubMed  Google Scholar 

  33. Miloro M, Miller JJ, Stoner JA (2007) Low-level laser effect on mandibular distraction osteogenesis. J Oral Maxillofac Surg 65(2):168–176

    PubMed  Google Scholar 

  34. Freitas I, Baranauskas V, Cruz-Höfling M (2000) Laser effects on osteogenesis. Appl Surf Sci 154:548–554

    Google Scholar 

  35. Takeda Y (1988) Irradiation effect of low-energy laser on alveolar bone after tooth extraction Experimental study in rats. Int J Oral Maxillofac Surg 17(6):388–391

    CAS  PubMed  Google Scholar 

  36. Saito S, Shimizu N (1997) Stimulatory effects of low-power laser irradiation on bone regeneration in midpalatal suture during expansion in the rat. Am J Orthod Dentofacial Orthop 111(5):525–532

    CAS  PubMed  Google Scholar 

  37. Shibli JA, Martins MC, Ribeiro FS, Garcia VG, Nociti FH Jr, Marcantonio E Jr (2006) Lethal photosensitization and guided bone regeneration in treatment of peri-implantitis: an experimental study in dogs. Clin Oral Implants Res 17(3):273–281

    PubMed  Google Scholar 

  38. Dörtbudak O, Haas R, Mailath-Pokorny G (2002) Effect of low-power laser irradiation on bony implant sites. Clin Oral Implants Res 13(3):288–292

    PubMed  Google Scholar 

  39. Souza L, Cardoso R, Kuriki H, Marcolino A, Fonseca M, Barbosa R (2020) High energy photobiomodulation therapy in the early days of injury improves sciatic nerve regeneration in mice. ABCS Health Sciences 45:e020016. https://doi.org/10.7322/abcshs.45.2020.1345

    Article  Google Scholar 

  40. Lizarelli RF, Lamano-Carvalho TL, Brentegani LG Histometric evaluation of the healing of the dental alveolus in rats after irradiation with a low-powered GaA1As laser. In: Lasers in Dentistry V, 1999. International Society for Optics and Photonics, pp 49-56

  41. Ferraresi C, Kaippert B, Avci P, Huang Y-Y, de Sousa MVP, Bagnato VS, Parizotto NA, Hamblin MR (2015) Low-level laser (light) therapy increases mitochondrial membrane potential and ATP synthesis in C2C12 myotubes with a peak response at 3–6 h. Photochem Photobiol 91(2):411–416. https://doi.org/10.1111/php.12397

    Article  CAS  PubMed  Google Scholar 

  42. Houreld N, Abrahamse H (2007) Effectiveness of helium-neon laser irradiation on viability and cytotoxicity of diabetic-wounded fibroblast cells. Photomed Laser Surg 25(6):474–481

    CAS  PubMed  Google Scholar 

  43. Medrado AR, Pugliese LS, Reis SRA, Andrade ZA (2003) Influence of low level laser therapy on wound healing and its biological action upon myofibroblasts. Lasers Surg Med 32(3):239–244

    PubMed  Google Scholar 

  44. Surinchak JS, Alago ML, Bellamy RF, Stuck BE, Belkin M (1983) Effects of low-level energy lasers on the healing of full-thickness skin defects. Lasers Surg Med 2(3):267–274

    CAS  PubMed  Google Scholar 

  45. Al-Watban FA, Zhang XY (1997) Comparison of wound healing process using argon and krypton lasers. J Clin Laser Med Surg 15(5):209–215. https://doi.org/10.1089/clm.1997.15.209

    Article  CAS  PubMed  Google Scholar 

  46. Matsumoto MA, Ferino RV, Monteleone GF, Ribeiro DA (2009) Low-level laser therapy modulates cyclo-oxygenase-2 expression during bone repair in rats. Lasers Med Sci 24(2):195–201

    PubMed  Google Scholar 

  47. Garcia VG (1992) Comportamento de feridas cutaneas submetidas a acao do raio laser: estudo clinico, biometrico e histologico em ratos.

  48. Garcia VG, Carvalho PSPd, Oliveira JAGPd (1995) Ação da radiação laser na reparação de feridas de extração dental infectadas estudo histológico em ratos. RGO 43(4):191–194

    Google Scholar 

  49. Garcia VG, Okamoto T, Kina JR, Fonseca RG, Theodoro LH (1996) Reparação de feridas de extração dental submetidas ao tratamento com raio laser estudo histológico em ratos. Rev Fac Odontol Lins (Impr) 9(1):33–42

    Google Scholar 

  50. Niccoli-Filho W, Okamoto T (1994) Effect of the helium–neon laser on the healing of extraction wounds a histological study in rats. J Laser Appl 6(4):237–240

    Google Scholar 

  51. Rosero KAV, Sampaio RMF, Deboni MCZ, Corrêa L, Marques MM, Ferraz EP, da Graça N-H (2020) Photobiomodulation as an adjunctive therapy for alveolar socket preservation a preliminary study in humans. Lasers Med Sci 35(8):1711–1720. https://doi.org/10.1007/s10103-020-02962-y

    Article  PubMed  Google Scholar 

  52. Dominguez A, León P, Aristizábal J (2016) Effect of low level laser therapy on local bone resorption during orthodontic treatment: a randomized controlled trial. Int J Odontostomatol 10:483–490. https://doi.org/10.4067/S0718-381X2016000300016

    Article  Google Scholar 

  53. Özyurt A, Elmas Ç, Seymen CM, Peker VT, Altunkaynak B, Güngör MN (2018) Effects of low-level laser therapy with a herbal extract on alveolar bone healing. J Oral Maxillofac Surg 76(2):287.e281-287.e210. https://doi.org/10.1016/j.joms.2017.10.014

    Article  Google Scholar 

  54. de Assis Limeira Jr F, Pinheiro ALB, de Martinez Gerbi MEM, Ramalho LMP, Marzola C, Ponzi EAC, Soares AO, de Carvalho LCB, Lima HCV, Gonçalves TO Assessment of bone repair following the use of anorganic bone graft and membrane associated or not to 830-nm laser light. In: Lasers in dentistry IX, 2003. International Society for Optics and Photonics, pp 30–36

  55. Dube A, Bansal H, Gupta P (2003) Modulation of macrophage structure and function by low level He–Ne laser irradiation. Photochem Photobiol Sci 2(8):851–855

    CAS  PubMed  Google Scholar 

  56. Vladimirov YA, Osipov A, Klebanov G (2004) Photobiological principles of therapeutic applications of laser radiation. Biochem Mosc 69(1):81–90

    CAS  Google Scholar 

  57. Correa F, Martins RABL, Correa JC, Iversen VV, Joenson J, Bjordal JM (2007) Low-level laser therapy (GaAs λ= 904 nm) reduces inflammatory cell migration in mice with lipopolysaccharide-induced peritonitis. Photomed Laser Surg 25(4):245–249

    PubMed  Google Scholar 

  58. Houreld N, Abrahamse H (2007) In vitro exposure of wounded diabetic fibroblast cells to a helium-neon laser at 5 and 16 J/cm2. Photomed Laser Surg 25(2):78–84

    CAS  PubMed  Google Scholar 

  59. Mirzaei M, Bayat M, Mosafa N, Mohsenifar Z, Piryaei A, Farokhi B, Rezaei F, Sadeghi Y, Rakhshan M (2007) Effect of low-level laser therapy on skin fibroblasts of streptozotocin-diabetic rats. Photomed Laser Surg 25(6):519–525

    PubMed  Google Scholar 

  60. Chen CH, Hung HS, Hsu Sh (2008) Low-energy laser irradiation increases endothelial cell proliferation, migration, and eNOS gene expression possibly via PI3K signal pathway. Lasers Surg Med 40(1):46–54

    PubMed  Google Scholar 

  61. Pires Oliveira DA, de Oliveira RF, Zangaro RA, Soares CP (2008) Evaluation of low-level laser therapy of osteoblastic cells. Photomed Laser Surg 26(4):401–404

    PubMed  Google Scholar 

  62. Agoston DV (2017) How to translate time? The temporal aspect of human and rodent biology. Front Neurol 8:92–92. https://doi.org/10.3389/fneur.2017.00092

    Article  PubMed  PubMed Central  Google Scholar 

  63. Lelovas PP, Xanthos TT, Thoma SE, Lyritis GP, Dontas IA (2008) The laboratory rat as an animal model for osteoporosis research. Comp Med 58(5):424–430

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Amaroli A, Colombo E, Zekiy A, Aicardi S, Benedicenti S, De Angelis N (2020) Interaction between laser light and osteoblasts photobiomodulation as a trend in the management of socket bone preservation-a review. Biology 9:11. https://doi.org/10.3390/biology9110409

    Article  CAS  Google Scholar 

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Funding

Coordenação de Aperfeiçoamento de Pessoal de Nivel Superior (CAPES) had the role on funding the first author on the development of the present study. Fundaçao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP) had the role on funding the manufacturer’s materials used by the authors on the present study.

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Correspondence to Fellipe Augusto Tocchini de Figueiredo.

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Animal Ethics Committee at the University of Sao Paulo (CEUA-FORP), Ribeirao Preto, Sao Paulo, Brazil (Protocol No.—09.1.1449.53.2).

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Ribeiro, L.N.S., de Figueiredo, F.A.T., da Silva Mira, P.C. et al. Low-level laser therapy (LLLT) improves alveolar bone healing in rats. Lasers Med Sci 37, 961–969 (2022). https://doi.org/10.1007/s10103-021-03340-y

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