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Bone repair assessment of critical size defects in rats treated with mineralized bovine bone (Bio-Oss®) and photobiomodulation therapy: a histomorphometric and immunohistochemical study

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Abstract

This study aimed to investigate the effects of administering photobiomodulation therapy (PBM) with bovine bone matrix on critical size defects in rats. Seventy-two adult male rats (albinus, Wistar), 90 days old, were used. Defect of 5 mm in diameter was made in their calvaria. The animals were divided into 4 groups: C-blood clot, B-Bio-Oss®, L-PBM, B+L-Bio-Oss®+PBM. Each group has been subdivided into 07, 30, and 60 days of observation. For PBM, a low GaAlAs energy of 660 nm was irradiated, total energy density of 45 J/cm2 . PBM was conducted in a trans-surgical form once only. For immunohistochemistry, a semi-quantitative analysis was made of expression of osteoprotegerin (OPG), nuclear kappa B-factor ligand receptor activator (RANKL), and tartrate-resistant acid phosphatase (TRAP). All histomorphometric data were statistically analyzed by ANOVA and Tukey test, significance level of 5%. The groups that showed the highest proportion of neoformation were L (0.39% ± 0.13) and C (0.37% ± 0.97), but groups B and B+L had larger defect size (C-1.75 mm2 ± 0.40, B-3.02 mm2 ± 0.63, L-2.45 mm2 ± 0.53, B+L-3.23 mm2 ± 1.01). In immunohistochemistry, groups B and B+L had higher immunostaining scores for OPG and RANKL at 60 days, and TRAP immunostaining increased in all groups at 30 days, but group L was the only one to present specimens with score 0. Although, at 60 days, groups L and C presented the highest proportion of bone neoformation, at 30 days group B+L had more than twice as much bone neoformation as group B, the choice of treatment application should depend on the aim of the treatment.

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References

  1. Khouri RK, Brown DM, Koudsi B, Deune EG, Gilula LA, Cooley BC, Reddi AH (1996 Jul) Repair of calvarial defects with flap tissue: role of bone morphogenetic proteins and competent responding tissues. Plast Reconstr Surg 98(1):103–109

    Article  CAS  Google Scholar 

  2. Springfield DS (1992 Oct) Autogenous bone grafts: nonvascular and vascular. Orthopedics. 15(10):1237–1241

    Article  CAS  Google Scholar 

  3. Chaushu G, Mardinger O, Calderon S, Moses O, Nissan J (2009 Mar) The use of cancellous block allograft for sinus floor augmentation with simultaneous implant placement in the posterior atrophic maxilla. J Periodontol 80(3):422–428

    Article  Google Scholar 

  4. Sbordone L, Toti P, Menchini-Fabris G, Sbordone C, Guidetti F (2009 Mar-Apr) Implant success in sinus-lifted maxillae and native bone: a 3-year clinical and computerized tomographic follow-up. Int J Oral Maxillofac Implants 24(2):316–324

    PubMed  Google Scholar 

  5. Shamsoddin E, Houshmand B, Golabgiran M. Biomaterial selection for bone augmentation in implant dentistry: a systematic review. J Adv Pharm Technol Res 2019 Apr-Jun;10(2):46–50. https://doi.org/10.4103/japtr.JAPTR_327_18. Review

  6. Stavropoulos A, Kostopoulos L, Nyengaard JR, Karring T (2003 Jul) Deproteinized bovine bone (Bio-Oss) and bioactive glass (Biogran) arrest bone formation when used as an adjunct to guided tissue regeneration (GTR): an experimental study in the rat. J Clin Periodontol 30(7):636–643

    Article  CAS  Google Scholar 

  7. Iezzi G, Scarano A, Mangano C, Cirotti B, Piattelli A (2008 Jan) Histologic results from a human implant retrieved due to fracture 5 years after insertion in a sinus augmented with anorganic bovine bone. J Periodontol 79(1):192–198

    Article  Google Scholar 

  8. Tapety FI, Amizuka N, Uoshima K, Nomura S, Maeda T (2004 Jun) A histological evaluation of the involvement of Bio-Oss in osteoblastic differentiation and matrix synthesis. Clin Oral Implants Res 15(3):315–324

    Article  Google Scholar 

  9. da Fonseca AS (2019 Feb) Is there a measure for low power laser dose? Lasers Med Sci 34(1):223–234. https://doi.org/10.1007/s10103-018-2676-5

    Article  PubMed  Google Scholar 

  10. Freitas NR, Guerrini LB, Esper LA, Sbrana MC, Dalben GDS, Soares S, et al. Evaluation of photobiomodulation therapy associated with guided bone regeneration in critical size defects. In vivo study. J Appl Oral Sci 2018;26:e20170244. https://doi.org/10.1590/1678-7757-2017-0244.

  11. Khadra M, Kasem N, Haanaes HR, Ellingsen JE, Lyngstadaas SP (2004 Jun) Enhancement of bone formation in rat calvarial bone defects using low-level laser therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 97(6):693–700

    Article  Google Scholar 

  12. Trelles MA, Mayayo E (1987) Bone fracture consolidates faster with low-power laser. Lasers Surg Med 7(1):36–45

    Article  CAS  Google Scholar 

  13. Garavello-Freitas I, Baranauskas V, Joazeiro PP, Padovani CR, Dal Pai-Silva M, da Cruz-Höfling MA (2003 May-Jun) Low-power laser irradiation improves histomorphometrical parameters and bone matrix organization during tibia wound healing in rats. J Photochem Photobiol B 70(2):81–89

    Article  CAS  Google Scholar 

  14. Rasouli Ghahroudi AA, Rokn AR, Kalhori KA, Khorsand A, Pournabi A, Pinheiro AL, Fekrazad R (2014 May) Effect of low-level laser therapy irradiation and Bio-Oss graft material on the osteogenesis process in rabbit calvarium defects: a double blind experimental study. Lasers Med Sci 29(3):925–932. https://doi.org/10.1007/s10103-013-1403-5

    Article  PubMed  Google Scholar 

  15. Pretel H, Lizarelli RF, Ramalho LT (2007 Dec) Effect of low level laser therapy on bone repair: histological study in rats. Lasers Surg Med 39(10):788–796

    Article  Google Scholar 

  16. Cunha MJ, Esper LA, Sbrana MC, de Oliveira PG, do Valle AL, de Almeida AL. Effect of low level laser on bone defects treated with bovine or autogenous bone grafts: in vivo study in rat calvaria. Biomed Res Int 2014;2014:104230. https://doi.org/10.1155/2014/104230.

  17. Percie du Sert N, Hurst V, Ahluwalia A, AlamS, AveyMT, BakerM, et al. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. PLoS Biol. 2020 18(7): e3000410. https://doi.org/10.1371/journal.pbio.300041014

  18. Sella VR, do Bomfim FR, Machado PC, da Silva Morsoleto MJ, Chohfi M, Plapler H (2015 Apr) Effect of low-level laser therapy on bone repair: a randomized controlled experimental study. Lasers Med Sci 30(3):1061–1068. https://doi.org/10.1007/s10103-015-1710-0

    Article  PubMed  Google Scholar 

  19. Calixto JC, Lima CE, Frederico L, Lima RP, Anbinder AL (2011 Apr) The influence of local administration of simvastatin in calvarial bone healing in rats. J Craniomaxillofac Surg 39(3):215–220

    Article  Google Scholar 

  20. Nagata MJ, Santinoni CS, Pola NM, de Campos N, Messora MR, Bomfim SR, Ervolino E, Fucini SE, Faleiros PL, Garcia VG, Bosco AF (2013 Apr 5) Bone marrow aspirate combined with low level laser therapy: a new therapeutic approach to enhance bone healing. J Photochem Photobiol B 121:6–14

    Article  CAS  Google Scholar 

  21. Garcia VG, Sahyon AS, Longo M, Fernandes LA, Gualberto Junior EC, Novaes VC, Ervolino E, de Almeida JM, Theodoro LH. Effect of LLLT on autogenous bone grafts in the repair of critical size defects in the calvaria of immunosuppressed rats. J Craniomaxillofac Surg 2014 Oct;42(7):1196–1202. https://doi.org/10.1016/j.jcms.2014.02.008. Epub 2014 Feb 25

  22. Nunes CMM, Ferreira CL, Bernardo DV, Oblack GB, Longo M, Santamaria MP, Jardini MAN (2019 Jun 13) The influence of LLLT applied on applied on calvarial defect in rats under effect of cigarette smoke. J Appl Oral Sci 27:e20180621. https://doi.org/10.1590/1678-7757-2018-0621

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Messora MR, Nagata MJ, Dornelles RC, Bomfim SR, Furlaneto FA, de Melo LG, Deliberador TM, Bosco AF, Garcia VG, Fucini SE (2008 Dec) Bone healing in critical-size defects treated with platelet-rich plasma activated by two different methods. A histologic and histometric study in rat calvaria. J Periodontal Res 43(6):723–729

    Article  CAS  Google Scholar 

  24. Buduneli E, Vardar-Sengül S, Buduneli N, Atilla G, Wahlgren J, Sorsa T (2007 Jan) Matrix metalloproteinases, tissue inhibitor of matrix metalloproteinase-1, and laminin-5 g2 chain immunolocalization in gingival tissue of endotoxin-induced periodontitis in rats: effects of low-dose doxycycline and alendronate. J Periodontol 78(1):127–134

    Article  CAS  Google Scholar 

  25. Brasilino MDS, Stringhetta-Garcia CT, Pereira CS, Pereira AAF, Stringhetta K, Leopoldino AM, Crivelini MM, Ervolino E, Dornelles RCM, de Melo Stevanato Nakamune AC, Chaves-Neto AH. Mate tea (Ilex paraguariensis) improves bone formation in the alveolar socket healing after tooth extraction in rats. Clin Oral Investig 2018 Apr;22(3):1449–1461. https://doi.org/10.1007/s00784-017-2249-1. Epub 2017 Oct 14

  26. Bosco AF, Faleiros PL, Carmona LR, Garcia VG, Theodoro LH, de Araujo NJ, Nagata MJ, de Almeida JM. Effects of low-level laser therapy on bone healing of critical-size defects treated with bovine bone graft. J Photochem Photobiol B 2016 Oct;163:303–310. https://doi.org/10.1016/j.jphotobiol.2016.08.040. Epub 2016 Aug 31

  27. de Oliveira GJPL, Aroni MAT, Medeiros MC, Marcantonio E Jr, Marcantonio RAC. Effect of low-level laser therapy on the healing of sites grafted with coagulum, deproteinized bovine bone, and biphasic ceramic made of hydroxyapatite and β-tricalcium phosphate. In vivo study in rats. Lasers Surg Med. 2018 Jan 13. https://doi.org/10.1002/lsm.22787

  28. Fan YP, Lu JF, Xu AT, He FM (2018 Oct) Physiochemical characterization and biological effect of anorganic bovine bone matrix and organic-containing bovine bone matrix in comparison with Bio-Oss in rabbits. J Biomater Appl 33(4):566–575. https://doi.org/10.1177/0885328218804926

    Article  PubMed  CAS  Google Scholar 

  29. Hassumi JS, Mulinari-Santos G, Fabris ALDS, Jacob RGM, Gonçalves A, Rossi AC, Freire AR, Faverani LP, Okamoto R (2018 Jun 18) Alveolar bone healing in rats: micro-CT, immunohistochemical and molecular analysis. J Appl Oral Sci 26:e20170326. https://doi.org/10.1590/1678-7757-2017-0326

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Tim CR, Pinto KN, Rossi BR, Fernandes K, Matsumoto MA, Parizotto NA, Rennó AC. Low-level laser therapy enhances the expression of osteogenic factors during bone repair in rats. Lasers Med Sci 2014 Jan;29(1):147–156. https://doi.org/10.1007/s10103-013-1302-9. Epub 2013 Mar 21

  31. Fabris ALDS, Faverani LP, Gomes-Ferreira PHS, Polo TOB, Santiago-Júnior JF, Okamoto R (2018 Jan 15) Bone repair access of Bone Ceramic™ in 5-mm defects: study on rat calvaria. J Appl Oral Sci 26:e20160531. https://doi.org/10.1590/1678-7757-2016-0531

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Elgali I, Igawa K, Palmquist A, Lennerås M, Xia W, Choi S, Chung UI, Omar O, Thomsen P. Molecular and structural patterns of bone regeneration in surgically created defects containing bone substitutes. Biomaterials. 2014 Mar;35(10):3229–3242. https://doi.org/10.1016/j.biomaterials.2013.12.084. Epub 2014 Jan 15

  33. Nicola RA, Jorgetti V, Rigau J, Pacheco MT, dos Reis LM, Zângaro RA (2003) Effect of low-power GaAlAs laser (660 nm) on bone structure and cell activity: an experimental animal study. Lasers Med Sci 18(2):89–94

    Article  Google Scholar 

Download references

Funding

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (420170/2016-2—research aid), Scientific Initiation Fellowship—PIBIC-EM-CNPq (4255, 5208, 6140), and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—CAPES (2018–2020: Graduate scholarship).

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Authors and Affiliations

  1. Department of Diagnosis and Surgery, São Paulo State University (UNESP), Institute of Science and Technology, Av. Eng. Francisco José Longo, n° 777 - Jardim São Dimas, São José dos Campos, SP, 12245-000, Brazil

    Letícia Cavassini Torquato, Eduardo Antonio Chelin Suárez & Daniella Viscensotto Bernardo

  2. São Paulo State University (UNESP), Institute of Science and Technology, São José dos Campos, SP, Brazil

    Isis Luzcybel Ribeiro Pinto, Ludmilla Oliveira Mantovani & Thiago Igor Lemes Silva

  3. Department of Diagnosis and Surgery – Division of Periodontology, São Paulo State University (UNESP), Institute of Science and Tecnology, São José dos Campos, SP, Brazil

    Maria Aparecida Neves Jardini, Mauro Pedrine Santamaria & Andrea Carvalho De Marco

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  1. Letícia Cavassini Torquato
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Correspondence to Letícia Cavassini Torquato.

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This study was submitted and approved by the Ethics Committee of Research in Animals of the Institute of Science and Technology of Sao Jose dos Campos/UNESP (002/2016-CEUA/ICT-UNESP).

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Torquato, L.C., Suárez, E.A.C., Bernardo, D.V. et al. Bone repair assessment of critical size defects in rats treated with mineralized bovine bone (Bio-Oss®) and photobiomodulation therapy: a histomorphometric and immunohistochemical study. Lasers Med Sci 36, 1515–1525 (2021). https://doi.org/10.1007/s10103-020-03234-5

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