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14-04-2022 | Osteoporosis | Original Article

Photobiomodulation stimulates surrounding bone formation and increases stability of titanium alloy miniscrews in ovariectomized rats

Authors: Bruna Guimarães Martins, Vanessa Santos de Moura, Denise Nami Fujii, Aguinaldo Silva Garcez, Selly Sayuri Suzuki

Published in: Lasers in Medical Science | Issue 7/2022

Abstract

The number of older individuals (> 60 years) treated in orthodontic dental practice is constantly growing, and osteoporosis is a common disease within this age range. Orthodontic treatment for this group tends to be challenging, often requiring the use of mini-implants. Mini-implants are important accessories in orthodontic treatment that provide solutions to complex cases. Despite the high level of success, these devices are prone to failure if insufficient bone stability is achieved. This study aimed to evaluate the effects of photobiomodulation on bone neoformation around mini-implants using fluorescence analysis in ovariectomized rats. A total of 12 female rats (Wistar) were ovariectomized and divided into three groups: two groups of low-level laser therapy irradiation in two different protocols, as follows: in the PBM1 group, applications were performed using 2 J, for 20 s each for 48 h, 6 irradiations in total, and in the PBM2 group, a single application of 4 J was performed for 40 s, and the third group represented the control group, and no laser therapy was applied. Each rat received two mini-implants placed immediately behind the upper incisors, and 0 g of force was applied using a NiTi spring. All rats received two bone markers, tetracycline (days 0–4) and alizarin (days 7–10), for 5 days each. Both markers were bound to calcium, allowing visualization of bone neoformation through fluorescence microscopy. After 12 days, euthanasia was performed; the results revealed that both irradiated groups showed significantly greater bone neoformation compared to the control group (p < 0.05). Mini-implant stability was measured in all animals using the Periotest device on day 0 and on the day of euthanasia. A significant increase in stability was observed in the group that received more laser application (p < 0.05). Photobiomodulation had a positive effect on bone neoformation around mini-implants in ovariectomized rats, with an increase in stability when more irradiation was performed.

Valle-Corotti KM, Valle CVM, Neves LS, Henriques JFC, Pinzan A (2008) A Ortodontia na atuação odontogeriátrica. R Dental Press Ortodon Ortop Facial 13:84–93. https://doi.org/10.1590/S1415-54192008000200010CrossRef

Araújo ACL, Faria EA, Stafocher JU (2017) Pé diabético: a atuação do profissional de enfermagem na prevenção e tratamento. Rev Saúde em Foco 9:621–641

Kulak CAM, Mañas NCP, Kulak Júnior J, Ramos CS, Borba VZC (2011) Osteoporose. Rev Bras Med 68:88–96

Santos SHB (2015) Índice de sucesso e fatores clínicos associados à estabilidade de mini-implantes ortodônticos: revisão sistemática e meta-análise. Faculdade de Odontologia da Universidade Federal de Pelotas, Tese

Namiuchi Junior OK, HerdyJL FFM, Motta RHL (2013) Utilização do mini-implantes no tratamento ortodôntico. RGO - Rev Gaúch Odontol 61:453–460

Melsen B (2005) Mini-implants: where are we? J Clin Orthod 39:539–547PubMed

Garcez AS, Suzuki SS, Martinez EF, Iemini MG, Suzuki H (2015) Effects of low-intensity laser therapy over mini-implant success rate in pigs. Lasers Med Sci 30:727–732. https://doi.org/10.1007/s10103-013-1367-5CrossRefPubMed

Ure DS, Oliver DR, Kim KB, Melo ACM, Buschang PH (2011) Stability changes of miniscrew implants over time: a pilot resonance frequency analysis. Angle Orthod 81:994–1000. https://doi.org/10.2319/120810-711.1CrossRefPubMedPubMedCentral

Mayer L, Gomes FV, de Oliveira MG, Moraes JF, Carlsson L (2016) Peri-implant osseointegration after low-level laser therapy: micro-computed tomography and resonance frequency analysis in an animal model. Lasers Med Sci 31:1789–1795. https://doi.org/10.1007/s10103-016-2051-3CrossRefPubMed

10.

Chen Y, Liu C, Chen X, Mo A (2019) Clinical evidence of photobiomodulation therapy (PBMT) on implant stability and success: a systematic review and meta-analysis. BMC Oral Health 19:77. https://doi.org/10.1186/s12903-019-0779-4CrossRefPubMedPubMedCentral

11.

Matys J, Świder K, Grzech-Leśniak K, Dominiak M, Romeo U (2019) Photobiomodulation by a 635nm diode laser on peri-implant bone: primary and secondary stability and bone density analysis - a randomized clinical trial. Biomed Res Int 2019:2785302. https://doi.org/10.1155/2019/2785302CrossRefPubMedPubMedCentral

12.

Pretel H, Lizarelli RF, Ramalho LT (2007) Effect of low-level laser therapy on bone repair: histological study in rats. Lasers Surg Med 39(10):788–796. https://doi.org/10.1002/lsm.20585CrossRefPubMed

13.

Zhou S, Wang G, Qiao L, Ge Q, Chen D, Xu Z, Shi D, Dai J, Qin J, Teng H, Jiang Q (2018) Age-dependent variations of cancellous bone in response to ovariectomy in C57BL/6J mice. Exp Ther Med 15:3623–3632. https://doi.org/10.3892/etm.2018.5839CrossRefPubMedPubMedCentral

14.

Oliveira GR, Vargas-Sanchez PK, Fernandes RR, Ricoldi MST, Semeghini MS, Pitol DL, de Sousa LG, Siessere S, Bombonato-Prado KF (2019) Lycopene influences osteoblast functional activity and prevents femur bone loss in female rats submitted to an experimental model of osteoporosis. J Bone Miner Metab 37:658–667. https://doi.org/10.1007/s00774-018-0970-8CrossRefPubMed

15.

Fernandes RR, Sanchez PKV, Sório ALR, Oliveira CAF, Ricoldi MST, Sousa LG, Rosa AL, Siéssere S, Bombonato-Prado KF (2019) Caffeine influences functional activity and gene expression of bone marrow osteoblastic cells from osteoporotic rats. J Caffeine Adenosine Res 9:53–59. https://doi.org/10.1089/caff.2019.0002CrossRef

16.

Oliveira EM (2016) Avaliação histológica dos efeitos do laser de baixa potência no processo inflamatório dos tecidos ao redor dos mini-implantes ortodônticos. Dissertação, Centro de Pesquisas Odontológicas São Leopoldo Mandic.

17.

Suzuki SS, Garcez AS, Reese PO, Suzuki H, Ribeiro MS, Moon W (2018) Effects of corticopuncture (CP) and low-level laser therapy (LLLT) on the rate of tooth movement and root resorption in rats using micro-CT evaluation. Lasers Med Sci 33:811–821. https://doi.org/10.1007/s10103-017-2421-5CrossRefPubMed

18.

Taddei SRA, Moura AP, Andrade Júnior I, Garlet GP, Garlet TP, Teixeira MM, Silva TA (2012) Experimental model of tooth movement in mice: a standardized protocol for studying bone remodeling under compression and tensile strains. J Biomech 45:2729–2735. https://doi.org/10.1016/j.jbiomech.2012.09.006CrossRefPubMed

19.

Carvalho FJLC (2014) Efeitos da laserterapia sobre a movimentação ortodôntica em ratos. Universidade Estadual Paulista, Dissertação

20.

Souza JMS (2014) Avaliação da influência do laser de baixa intensidade na movimentação ortodôntica e supressão da dor. Faculdade de Odontologia de Bauru da Universidade de São Paulo, TeseCrossRef

21.

Oh J-S, Kim S-G (2012) Clinical study of the relationship between implant stability measurements using Periotest and Osstell mentor and bone quality assessment. Oral Surg Oral Med Oral Pathol Oral Radiol 113:e35-40. https://doi.org/10.1016/j.tripleo.2011.07.003CrossRefPubMed

22.

Goia TS (2008) Avaliação in vitro e in vivo de ligas porosas de ti-13nb-13zr obtidas por metalurgia do pó. Instituto de Pesquisas Energéticas e Nucleares da Universidade de São Paulo, DissertaçãoCrossRef

23.

Atmaca H, Aydın A, Musaoğlu R (2013) Experimental model of osteoporosis: comparison between ovariectomy and botulinum toxin A. Acta Ortop Bras 21:340–343. https://doi.org/10.1590/S1413-78522013000600009CrossRefPubMedPubMedCentral

24.

Tzaphlidou M, Kafantari H (2000) Influence of nutritional factors on bone collagen fibrils in ovariectomized rats. Bone 27:635–638. https://doi.org/10.1016/s8756-3282(00)00382-3CrossRefPubMed

25.

Kim T-W, Baek S-H, Kim J-W, Chang Y-I (2008) Effects of microgrooves on the success rate and soft tissue adaptation of orthodontic miniscrews. Angle Orthod 78:1057–1064. https://doi.org/10.2319/101707-496.1CrossRefPubMed

26.

Hembree M, Buschang PH, Carrillo R, Spears R, Rossouw PE (2009) Effects of intentional damage of the roots and surrounding structures with miniscrew implants. Am J Orthod Dentofacial Orthop 135:280.e1-281. https://doi.org/10.1016/j.ajodo.2008.06.022CrossRef

27.

Kim H, Kim TW (2011) Histologic evaluation of root-surface healing after root contact or approximation during placement of mini-implants. Am J Orthod Dentofacial Orthop 139:752–760. https://doi.org/10.1016/j.ajodo.2009.06.042CrossRefPubMed

28.

Myers HM (1968) Alizarin and tetracycline binding by bone mineral. Am J Phys Anthropol 29:179–182. https://doi.org/10.1002/ajpa.1330290211CrossRefPubMed

29.

Pinto MR, Santos RL, Pithon MM, Araújo MTS, Braga JPV, Nojima LI (2013) Influence of low-intensity laser therapy on the stability of orthodontic mini-implants: a study in rabbits. J Oral Maxillofac Surg 115:e26-30. https://doi.org/10.1016/j.oooo.2011.09.036CrossRef

30.

Gomes FV, Mayer L, Massotti FP, Baraldi CE, Ponzoni D, Webber JBB, Oliveira MG (2015) Low-level laser therapy improves peri-implant bone formation: resonance frequency, electron microscopy, and stereology findings in a rabbit model. Int J Oral Maxillofac Surg 44:245–251. https://doi.org/10.1016/j.ijom.2014.09.010CrossRefPubMed

31.

Babuccu C, Keklikoğlu N, Baydoğan M, Kaynar A (2014) Cumulative effect of low-level laser therapy and low-intensity pulsed ultrasound on bone repair in rats. Int J Oral Maxillofac Surg 43:769–776. https://doi.org/10.1016/j.ijom.2013.12.002CrossRefPubMed

32.

Monea A, Beresescu G, Tibor M, Popsor S, Antonescu DM (2015) Bone healing after low-level laser application in extraction sockets grafted with allograft material and covered with a resorbable collagen dressing: a pilot histological evaluation. BMC Oral Health 15:134. https://doi.org/10.1186/s12903-015-0122-7CrossRefPubMedPubMedCentral

33.

Chen Y, Kyung HM, Zhao WT, Yu WJ (2009) Critical factors for the success of orthodontic mini-implants: a systematic review. Am J Orthod Dentofacial Orthop 135:284–291. https://doi.org/10.1016/j.ajodo.2007.08.017CrossRefPubMed

34.

Marañón-Vásquez GA, Lagravère MO, Borsatto MC, Souza SS, Watanabe PCA, Matsumoto MAN, Saraiva MCP, Romano FL (2019) Effect of photobiomodulation on the stability and displacement of orthodontic mini-implants submitted to immediate and delayed loading: a clinical study. Lasers Med Sci

35.

Kim YD, Kim SS, Hwang DS, Kim SG, Kwon YH, Shin SH, Kim UK, Kim JR, Chung IK (2007) Effect of low-level laser treatment after installation of dental titanium implant-immunohistochemical study of RANKL, RANK, OPG: an experimental study in rats. Lasers Surg Med 39(5) 441–450. 34, 1705–1715. https://doi.org/10.1007/s10103-019-02818-0

36.

Omasa S, Motoyoshi M, Arai Y, Ejima K, Shimizu N (2012) Low-level laser therapy enhances the stability of orthodontic mini-implants via bone formation related to BMP-2 expression in a rat model. Photomed Laser Surg 30:255–261. https://doi.org/10.1089/pho.2011.3157CrossRefPubMed

37.

de Vasconcellos LM, Barbara MA, Deco CP, Junqueira JC, do Prado RF, Anbinder AL, de Vasconcellos LG, Cairo CA, Carvalho YR (2014) Healing of normal and osteopenic bone with titanium implant and low-level laser therapy (GaAlAs): a histomorphometric study in rats. Lasers Med Sci 29(2) 575–580https://doi.org/10.1007/s10103-013-1326-1

38.

e Vasconcellos LM, Barbara MA, Rovai ES, de Oliveira França M, Ebrahim ZF, de Vasconcellos LG, Porto CD, Cairo CA (2016) Titanium scaffold osteogenesis in healthy and osteoporotic rats is improved by the use of low-level laser therapy (GaAlAs). Lasers Med Sci 31(5) 899–905https://doi.org/10.1007/s10103-016-1930-y

39.

Costa A, Maia T, de Barros Silva PG, Abreu LG, Gondim DV, Santos P (2021) Effects of low-level laser therapy on the orthodontic mini-implants stability: a systematic review and meta-analysis. Prog Orthod 22(1):6. https://doi.org/10.1186/s40510-021-00350-yCrossRefPubMedPubMedCentral

40.

Zhang B, Huang X, Huo S, Zhang C, Cen X, Zhao Z (2021) Effect of photobiomodulation therapy on mini-implant stability: a systematic review and meta-analysis. Lasers Med Sci. https://doi.org/10.1007/s10103-021-03281-6.Advanceonlinepublication.10.1007/s10103-021-03281-6CrossRefPubMedPubMedCentral

41.

Bilhan H, Cilingir A, Bural C, Bilmenoglu C, Sakar O, Geckili O (2015) The evaluation of the reliability of Periotest for implant stability measurements: an in vitro study. J Oral Implantol 41:e90–e95. https://doi.org/10.1563/aaid-joi-D-13-00303CrossRefPubMed

42.

Watanabe T, Miyazawa K, Fujiwara T, Kawaguchi M, Tabuchi M, Goto S (2017) Insertion torque and Periotest values are important factors predicting outcome after orthodontic miniscrew placement. Am J Orthod Dentofacial Orthop 152:483–488. https://doi.org/10.1016/j.ajodo.2017.01.026CrossRefPubMed

43.

Yano S, Motoyoshi M, Inaba M, Yano S, Takenouchi H, Son S, Arai Y, Shimizu N (2014) A healing period increases mini-implant stability in growing rats. J Oral Sci 56:113–118. https://doi.org/10.2334/josnusd.56.113CrossRefPubMed

Title: Photobiomodulation stimulates surrounding bone formation and increases stability of titanium alloy miniscrews in ovariectomized rats
Authors: Bruna Guimarães Martins
Vanessa Santos de Moura
Denise Nami Fujii
Aguinaldo Silva Garcez
Selly Sayuri Suzuki
Publication date: 14-04-2022
Publisher: Springer London
Keywords: Osteoporosis
Osteoporosis
Tetracyclines
Laser
Published in: Lasers in Medical Science / Issue 7/2022
Print ISSN: 0268-8921
Electronic ISSN: 1435-604X
DOI: https://doi.org/10.1007/s10103-022-03560-w

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Photobiomodulation stimulates surrounding bone formation and increases stability of titanium alloy miniscrews in ovariectomized rats

Abstract

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