Associação de compósitos de colágeno marinho/biosilicato e fotobiomodulação no processo de consolidação óssea usando um modelo experimental de defeito na calvária
DOI:
https://doi.org/10.33448/rsd-v10i8.16498Palavras-chave:
Fotobiomodulação; Biomateriais; Engenharia tecidual.Resumo
O estudo comparou a capacidade regenerativa óssea em modelo experimental de defeitos ósseos cranianos em ratos, em 3 grupos: G1: defeitos ósseos irradiados com fotobiomodulação; G2: Biosilicato + fotobiomodulação e G3: Biosilicato e esponja marinha + fotobiomodulação. A histocompatibilidade e as respostas ósseas foram realizadas após 15 e 45 dias de implantação. A análise histológica demonstrou que os animais irradiados com fotobiomodulação apresentaram um aumento da quantidade de neoformados ao longo do tempo. A histomorfometria mostrou maiores valores de volume ósseo para G3 e G1, maiores valores de volume de osteóide e número de osteoblastos observados para G3 em relação ao G2. A imunomarcação de TGF-β foi maior para G2. Os valores encontrados para VEGF foram maiores para o biosilicato (com ou sem esponja marinha) 15 dias após o implante, com diferença aumentada sendo observada para o G1, 45 dias após a cirurgia. Em conclusão, o estímulo fornecido pela fotobiomodulação associada ao compósito biomimético aumentou a formação óssea no defeito ósseo craniano em ratos. Consequentemente, esses dados destacam o potencial da introdução da esponja marinha no biosilicato e irradiada com fotobiomodulação para melhorar o desempenho biológico para aplicações de regeneração óssea.
Referências
Bossini, P. S., Rennó, A. C. M., Ribeiro, D. A., Fangel, R., Peitl, O., Zanotto, E. D., & Parizotto, N. A. (2011). Biosilicate® and low-level laser therapy improve bone repair in osteoporotic rats. Journal of Tissue Engineering and Regenerative Medicine, 12:52-57. https://doi.org/10.1002/term.309
Bossini, P. S., Rennó, A.C., Ribeiro, D. A., Fangel, R., Ribeiro, A. C., Lahoz, M. A., & Parizotto, N. A. (2012). Low level laser therapy (830nm) improves bone repair in osteoporotic rats: similar outcomes at two different dosages. Experimental Gerontology, 47:136-42. https://doi.org/10.1016/j.exger.2011.11.005
Cury, V., Moretti, A. I., Assis, L., Bossini, P., Crusca, J. S., Neto, C. B., Fangel, R., Souza, H. P., Hamblin, M. R., & Parizotto, N. A. (2013). Low level laser therapy increases angiogenesis in a model of ischemic skin flap in rats mediated by VEGF, HIF-1α and MMP-2. Journal of photochemistry and photobiology. B, Biology, 125:164–170. https://doi.org/10.1016/j.jphotobiol.2013.06.004
D'Mello, S. R., Elangovan, S., Hong, L., Ross, R. D., Sumner, D. R., & Salem, A. K. (2015). A Pilot Study Evaluating Combinatorial and Simultaneous Delivery of Polyethylenimine-Plasmid DNA Complexes Encoding for VEGF and PDGF for Bone Regeneration in Calvarial Bone Defects. Current pharmaceutical biotechnology, 16(7), 655–660. https://doi.org/10.2174/138920101607150427112753
de Freitas, L. F., & Hamblin, M. R. (2016). Proposed Mechanisms of Photobiomodulation or Low-Level Light Therapy. IEEE journal of selected topics in quantum electronics : a publication of the IEEE Lasers and Electro-optics Society, 22(3), 7000417. https://doi.org/10.1109/JSTQE.2016.2561201
Einhorn, T. A., & Gerstenfeld, L. C. (2015). Fracture healing: mechanisms and interventions. Nature reviews. Rheumatology, 11(1), 45–54. https://doi.org/10.1038/nrrheum.2014.164
Exposito, J. Y., Cluzel, C., Garrone, R., & Lethias, C. (2002). Evolution of collagens. The Anatomical record, 268(3), 302–316. https://doi.org/10.1002/ar.10162
Fangel, R., Bossini, P. S., Renno, A. C., Ribeiro, D. A., Wang, C. C., Toma, R. L., Nonaka, K. O., Driusso, P., Parizotto, N. A., & Oishi, J. (2011). Low-level laser therapy, at 60 J/cm2 associated with a Biosilicate(®) increase in bone deposition and indentation biomechanical properties of callus in osteopenic rats. Journal of biomedical optics, 16(7), 078001. https://doi.org/10.1117/1.3598847
Fangel, R., Bossini, P. S., Renno, A. C., Granito, R. N., Wang, C. C., Nonaka, K. O., Driusso, P., Parizotto, N. A., & Oishi, J. (2014). Biomechanical properties: effects of low-level laser therapy and Biosilicate® on tibial bone defects in osteopenic rats. Journal of applied biomaterials & functional materials, 12(3), 271–277. https://doi.org/10.5301/jabfm.5000198
Farivar, S., Malekshahabi, T., & Shiari, R. (2014). Biological effects of low level laser therapy. Journal of lasers in medical sciences, 5(2), 58–62.
Fernandes, K. R., Ribeiro, D. A., Rodrigues, N. C., Tim, C., Santos, A. A., Parizotto, N. A., de Araujo, H. S., Driusso, P., & Rennó, A. C. (2013). Effects of low-level laser therapy on the expression of osteogenic genes related in the initial stages of bone defects in rats. Journal of biomedical optics, 18(3), 038002. https://doi.org/10.1117/1.JBO.18.3.038002
Fernandes, K. R., Magri, A., Kido, H. W., Ueno, F., Assis, L., Fernandes, K., Mesquita-Ferrari, R. A., Martins, V. C., Plepis, A. M., Zanotto, E. D., Peitl, O., Ribeiro, D., van den Beucken, J. J., & Renno, A. (2017a). Characterization and biological evaluation of the introduction of PLGA into biosilicate®. Journal of biomedical materials research. Part B, Applied biomaterials, 105(5), 1063–1074. https://doi.org/10.1002/jbm.b.33654
Fernandes, K. R., Magri, A., Kido, H. W., Parisi, J. R., Assis, L., Fernandes, K., Mesquita-Ferrari, R. A., Martins, V. C., Plepis, A. M., Zanotto, E. D., Peitl, O., & Renno, A. (2017b). Biosilicate/PLGA osteogenic effects modulated by laser therapy: In vitro and in vivo studies. Journal of photochemistry and photobiology. B, Biology, 173, 258–265. https://doi.org/10.1016/j.jphotobiol.2017.06.002
Fernandes, K. R., Parisi, J. R., Magri, A., Kido, H. W., Gabbai-Armelin, P. R., Fortulan, C. A., Zanotto, E. D., Peitl, O., Granito, R. N., & Renno, A. (2019). Influence of the incorporation of marine spongin into a Biosilicate®: an in vitro study. Journal of materials science. Materials in medicine, 30(6), 64. https://doi.org/10.1007/s10856-019-6266-2
Fortuna, T., Gonzalez, A. C., Sá, M. F., Andrade, Z. A., Reis, S., & Medrado, A. (2018). Effect of 670 nm laser photobiomodulation on vascular density and fibroplasia in late stages of tissue repair. International wound journal, 15(2), 274–282. https://doi.org/10.1111/iwj.12861
Gabbai-Armelin, P. R., Souza, M. T., Kido, H. W., Tim, C. R., Bossini, P. S., Magri, A. M., Fernandes, K. R., Pastor, F. A., Zanotto, E. D., Parizotto, N. A., Peitl, O., & Renno, A. C. (2015). Effect of a new bioactive fibrous glassy scaffold on bone repair. Journal of materials science. Materials in medicine, 26(5), 177. https://doi.org/10.1007/s10856-015-5516-1
Gabbai-Armelin, P. R., Souza, M. T., Kido, H. W., Tim, C. R., Bossini, P. S., Fernandes, K. R., Magri, A. M., Parizotto, N. A., Fernandes, K. P., Mesquita-Ferrari, R. A., Ribeiro, D. A., Zanotto, E. D., Peitl, O., & Renno, A. C. (2017). Characterization and biocompatibility of a fibrous glassy scaffold. Journal of tissue engineering and regenerative medicine, 11(4), 1141–1151. https://doi.org/10.1002/term.2017
Granito, R. N., Ribeiro, D. A., Rennó, A. C., Ravagnani, C., Bossini, P. S., Peitl-Filho, O., Zanotto, E. D., Parizotto, N. A., & Oishi, J. (2009). Effects of biosilicate and bioglass 45S5 on tibial bone consolidation on rats: a biomechanical and a histological study. Journal of materials science. Materials in medicine, 20(12), 2521–2526. https://doi.org/10.1007/s10856-009-3824-z
Granito, R. N., Rennó, A. C., Ravagnani, C., Bossini, P. S., Mochiuti, D., Jorgetti, V., Driusso, P., Peitl, O., Zanotto, E. D., Parizotto, N. A., & Oishi, J. (2011). In vivo biological performance of a novel highly bioactive glass-ceramic (Biosilicate®): A biomechanical and histomorphometric study in rat tibial defects. Journal of biomedical materials research. Part B, Applied biomaterials, 97(1), 139–147. https://doi.org/10.1002/jbm.b.31795
Green, D., Howard, D., Yang, X., Kelly, M., & Oreffo, R. O. (2003). Natural marine sponge fiber skeleton: a biomimetic scaffold for human osteoprogenitor cell attachment, growth, and differentiation. Tissue engineering, 9(6), 1159–1166. https://doi.org/10.1089/10763270360728062
Guo, Y., Xue, Y., Niu, W., Chen, M., Wang, M., Ma, P. X., & Lei, B. (2018). Monodispersed Bioactive Glass Nanoparticles Enhance the Osteogenic Differentiation of Adipose-Derived Stem Cells through Activating TGF-Beta/Smad3 Signaling Pathway. Particle & Particle Systems Characterization, 35(7), 1800087. https://doi.org/10.1002/ppsc.201800087
Haach, L. C. A., Purquerio, B. M., Silva Jr, N. F., Gaspar, A. M. M., & Fortulan, C. A. (2014). Comparison of Two Composites Developed to be Used as Bone Replacement – PMMA/Bioglass 45S5® Microfiber and PMMA/ Hydroxyapatite. Bioceramics Development and Applications, 4:071. https://doi.org/10.4172/2090-5025.1000071
Hamblin M. R. (2017). Mechanisms and applications of the anti-inflammatory effects of photobiomodulation. AIMS biophysics, 4(3), 337–361. https://doi.org/10.3934/biophy.2017.3.337
Hench, L. L., & Polak, J. M. (2002). Third-generation biomedical materials. Science (New York, N.Y.), 295(5557), 1014–1017. https://doi.org/10.1126/science.1067404
Iwatsubo, T., Kishi, R., Miura, T., Ohzono, T., & Yamaguchi, T. (2015). Formation of Hydroxyapatite Skeletal Materials from Hydrogel Matrices via Artificial Biomineralization. The journal of physical chemistry. B, 119(28), 8793–8799. https://doi.org/10.1021/acs.jpcb.5b03181
Johnson, K. E., & Wilgus, T. A. (2014). Vascular Endothelial Growth Factor and Angiogenesis in the Regulation of Cutaneous Wound Repair. Advances in wound care, 3(10), 647–661. https://doi.org/10.1089/wound.2013.0517
Karu T. I. (2008). Mitochondrial signaling in mammalian cells activated by red and near-IR radiation. Photochemistry and photobiology, 84(5), 1091–1099. https://doi.org/10.1111/j.1751-1097.2008.00394.x
Kido, H. W., Oliveira, P., Parizotto, N. A., Crovace, M. C., Zanotto, E. D., Peitl-Filho, O., Fernandes, K. P., Mesquita-Ferrari, R. A., Ribeiro, D. A., & Renno, A. C. (2013). Histopathological, cytotoxicity and genotoxicity evaluation of Biosilicate® glass-ceramic scaffolds. Journal of biomedical materials research. Part A, 101(3), 667–673. https://doi.org/10.1002/jbm.a.34360
Kido, H. W., Brassolatti, P., Tim, C. R., Gabbai-Armelin, P. R., Magri, A. M., Fernandes, K. R., Bossini, P. S., Parizotto, N. A., Crovace, M. C., Malavazi, I., da Cunha, A. F., Plepis, A. M., Anibal, F. F., & Rennó, A. C. (2017). Porous poly (D,L-lactide-co-glycolide) acid/biosilicate® composite scaffolds for bone tissue engineering. Journal of biomedical materials research. Part B, Applied biomaterials, 105(1), 63–71. https://doi.org/10.1002/jbm.b.33536
Kubota, T., Hasuike, A., Ozawa, Y., Yamamoto, T., Tsunori, K., Yamada, Y., & Sato, S. (2017). Regenerative capacity of augmented bone in rat calvarial guided bone augmentation model. Journal of periodontal & implant science, 47(2), 77–85. https://doi.org/10.5051/jpis.2017.47.2.77
Lin, Z., Solomon, K. L., Zhang, X., Pavlos, N. J., Abel, T., Willers, C., Dai, K., Xu, J., Zheng, Q., & Zheng, M. (2011). In vitro evaluation of natural marine sponge collagen as a scaffold for bone tissue engineering. International journal of biological sciences, 7(7), 968–977. https://doi.org/10.7150/ijbs.7.968
Lopez-Heredia, M. A., Sa, Y., Salmon, P., de Wijn, J. R., Wolke, J. G., & Jansen, J. A. (2012). Bulk properties and bioactivity assessment of porous polymethylmethacrylate cement loaded with calcium phosphates under simulated physiological conditions. Acta biomaterialia, 8(8), 3120–3127. https://doi.org/10.1016/j.actbio.2012.05.007
Luvizuto, E. R., Queiroz, T. P., Margonar, R., Panzarini, S. R., Hochuli-Vieira, E., Okamoto, T., & Okamoto, R. (2012). Osteoconductive properties of β-tricalcium phosphate matrix, polylactic and polyglycolic acid gel, and calcium phosphate cement in bone defects. The Journal of craniofacial surgery, 23(5), e430–e433. https://doi.org/10.1097/SCS.0b013e31825e4abf
Magri, A. M., Fernandes, K. R., Assis, L., Mendes, N. A., da Silva Santos, A. L., de Oliveira Dantas, E., & Rennó, A. C. (2015). Photobiomodulation and bone healing in diabetic rats: evaluation of bone response using a tibial defect experimental model. Lasers in medical science, 30(7), 1949–1957. https://doi.org/10.1007/s10103-015-1789-3
Matsumoto, M. A., Caviquioli, G., Biguetti, C. C., Holgado, L., Saraiva, P. P., Rennó, A. C., & Kawakami, R. Y. (2012). A novel bioactive vitroceramic presents similar biological responses as autogenous bone grafts. Journal of materials science. Materials in medicine, 23(6), 1447–1456. https://doi.org/10.1007/s10856-012-4612-8
Mokoena, D., Dhilip Kumar, S. S., Houreld, N. N., & Abrahamse, H. (2018). Role of photobiomodulation on the activation of the Smad pathway via TGF-β in wound healing. Journal of photochemistry and photobiology. B, Biology, 189, 138–144. https://doi.org/10.1016/j.jphotobiol.2018.10.011
Moura, J., Teixeira, L. N., Ravagnani, C., Peitl, O., Zanotto, E. D., Beloti, M. M., Panzeri, H., Rosa, A. L., & de Oliveira, P. T. (2007). In vitro osteogenesis on a highly bioactive glass-ceramic (Biosilicate). Journal of biomedical materials research. Part A, 82(3), 545–557. https://doi.org/10.1002/jbm.a.31165
Noba, C., Mello-Moura, A., Gimenez, T., Tedesco, T. K., & Moura-Netto, C. (2018). Laser for bone healing after oral surgery: systematic review. Lasers in medical science, 33(3), 667–674. https://doi.org/10.1007/s10103-017-2400-x
Oliveira, F. S., Pinfildi, C. E., Parizoto, N. A., Liebano, R. E., Bossini, P. S., Garcia, E. B., & Ferreira, L. M. (2009). Effect of low level laser therapy (830 nm) with different therapy regimes on the process of tissue repair in partial lesion calcaneous tendon. Lasers in surgery and medicine, 41(4), 271–276. https://doi.org/10.1002/lsm.20760
Parisi, J. R., Fernandes, K. R., Avanzi, I. R., Dorileo, B. P., Santana, A. F., Andrade, A. L., Gabbai-Armelin, P. R., Fortulan, C. A., Trichês, E. S., Granito, R. N., & Renno, A. (2019). Incorporation of Collagen from Marine Sponges (Spongin) into Hydroxyapatite Samples: Characterization and In Vitro Biological Evaluation. Marine biotechnology (New York, N.Y.), 21(1), 30–37. https://doi.org/10.1007/s10126-018-9855-z
Parisi, J. R., Fernandes, K. R., Aparecida do Vale, G. C., de França Santana, A., de Almeida Cruz, M., Fortulan, C. A., Zanotto, E. D., Peitl, O., Granito, R. N., & Rennó, A. (2020). Marine spongin incorporation into Biosilicate® for tissue engineering applications: An in vivo study. Journal of biomaterials applications, 35(2), 205–214. https://doi.org/10.1177/0885328220922161
Pinto, K. N., Tim, C. R., Crovace, M. C., Matsumoto, M. A., Parizotto, N. A., Zanotto, E. D., Peitl, O., & Rennó, A. C. (2013). Effects of biosilicate(®) scaffolds and low-level laser therapy on the process of bone healing. Photomedicine and laser surgery, 31(6), 252–260. https://doi.org/10.1089/pho.2012.3435
Pisani, P., Renna, M. D., Conversano, F., Casciaro, E., Di Paola, M., Quarta, E., Muratore, M., & Casciaro, S. (2016). Major osteoporotic fragility fractures: Risk factor updates and societal impact. World journal of orthopedics, 7(3), 171–181. https://doi.org/10.5312/wjo.v7.i3.171
Santinoni, C. D., Oliveira, H. F., Batista, V. E., Lemos, C. A., & Verri, F. R. (2017). Influence of low-level laser therapy on the healing of human bone maxillofacial defects: A systematic review. Journal of photochemistry and photobiology. B, Biology, 169, 83–89. https://doi.org/10.1016/j.jphotobiol.2017.03.004
Sarvestani, F. K., Dehno, N. S., Nazhvani, S. D., Bagheri, M. H., Abbasi, S., Khademolhosseini, Y., & Gorji, E. (2017). Effect of low-level laser therapy on fracture healing in rabbits. Laser therapy, 26(3), 189–193. https://doi.org/10.5978/islsm.17-OR-14
Shakouri, K., Eftekharsadat, B., Oskuie, M. R., Soleimanpour, J., Tarzamni, M. K., Salekzamani, Y., Hoshyar, Y., & Nezami, N. (2010). Effect of low-intensity pulsed ultrasound on fracture callus mineral density and flexural strength in rabbit tibial fresh fracture. Journal of orthopaedic science : official journal of the Japanese Orthopaedic Association, 15(2), 240–244. https://doi.org/10.1007/s00776-009-1436-6
Silva, T. H., Moreira-Silva, J., Marques, A. L., Domingues, A., Bayon, Y., & Reis, R. L. (2014). Marine origin collagens and its potential applications. Marine drugs, 12(12), 5881–5901. https://doi.org/10.3390/md12125881
Skondra, F. G., Koletsi, D., Eliades, T., & Farmakis, E. (2018). The Effect of Low-Level Laser Therapy on Bone Healing After Rapid Maxillary Expansion: A Systematic Review. Photomedicine and laser surgery, 36(2), 61–71. https://doi.org/10.1089/pho.2017.4278
Sousa, T. H. S., Fortulan, C. A., Antunes, E. S., & de M. Purquerio, B. (2008). Concept of a Bioactive Implant with Functional Gradient Structure. Key Engineering Materials, 396–398, 221–224. https://doi.org/10.4028/www.scientific.net/kem.396-398.221
Swatschek, D., Schatton, W., Kellermann, J., Müller, W. E., & Kreuter, J. (2002). Marine sponge collagen: isolation, characterization and effects on the skin parameters surface-pH, moisture and sebum. European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V, 53(1), 107–113. https://doi.org/10.1016/s0939-6411(01)00192-8
Tim, C. R., Bossini, P. S., Kido, H. W., Malavazi, I., von Zeska Kress, M. R., Carazzolle, M. F., Parizotto, N. A., & Rennó, A. C. (2015). Effects of low-level laser therapy on the expression of osteogenic genes during the initial stages of bone healing in rats: a microarray analysis. Lasers in medical science, 30(9), 2325–2333. https://doi.org/10.1007/s10103-015-1807-5
Ueno, F. R., Kido, H. W., Granito, R. N., Gabbai-Armelin, P. R., Magri, A. M., Fernandes, K. R., da Silva, A. C., Braga, F. J., & Renno, A. C. (2016). Calcium phosphate fibers coated with collagen: In vivo evaluation of the effects on bone repair. Bio-medical materials and engineering, 27(2-3), 259–273. https://doi.org/10.3233/BME-161581
Wu, M., Chen, G., & Li, Y. P. (2016). TGF-β and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone research, 4, 16009. https://doi.org/10.1038/boneres.2016.9
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Copyright (c) 2021 Giovanna Caroline Aparecida do Vale; Kelly Rossetti Fernandes; Julia Risso Parisi; Alan de França Santana; Matheus de Almeida Cruz; Carlos Alberto Fortulan; Edgar Dutra Zanotto; Oscar Peitl; Renata Neves Granito; Ana Claudia Muniz Rennó
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