journal article·2025-12-08Open access

Bioactive Glass Modified by Sonochemistry Improves Peri-Implant Bone Repair in Ovariectomized Rats

Marcelly Braga Gomes, Nathália Dantas Duarte, Gabriel Mulinari-Santos, Fábio Roberto de Souza Batista, Luy de Abreu Costa, Paulo Roberto Botacin, Paulo Noronha Lisboa-Filho, Roberta Okamoto

Biomimetics· Volume 10· Issue 12

Abstract

Estrogen deficiency is a primary cause of osteoporosis, compromising bone mineral density that may impair peri-implant healing. Given the compromised bone environment associated with estrogen deficiency, strategies such as particle reduction via sonochemistry are promising approaches to enhance regenerative outcomes. However, its effects in promoting bone formation remain insufficiently explored. Therefore, this study evaluated the potential of two sonicated biomaterials to improve peri-implant repair in ovariectomized rats. Fifty female rats were allocated into five groups: blood clot (CLOT), Biogran® (BGN), sonicated Biogran® (BGS), Bio-Oss® (BON), and sonicated Bio-Oss® (BOS). Tibial peri-implant defects were created 30 days after ovariectomy and analyzed 28 days later by removal torque, microcomputed tomography, and confocal microscopy. BGS exhibited the highest removal torque (6.28 Ncm), followed by BON (5.37 Ncm), BOS (3.92 Ncm), BGN (3.15 Ncm), and CLOT (2.58 Ncm). Micro-CT revealed bone volume fraction (BV/TV) values of 8.07% (CLOT), 6.47% (BOS), 6.02% (BGS), 5.55% (BGN), and 2.84% (BON). For the trabecular number (Tb.N), BGS (1.11 mm−1) showed a significant increase compared with BGN (0.69 mm−1), p < 0.05. These findings show that sonochemically modified bioactive glass improves mechanical stability and trabecular microarchitecture under estrogen-deficient conditions. However, further studies are needed to standardize sonication parameters for different biomaterials and expand their translational applicability.
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Research context

OpenAlex topics: Ultrasound and Hyperthermia Applications · Bone Tissue Engineering Materials · Ultrasound and Cavitation Phenomena

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

Affiliations

Department of Basic Sciences, School of Dentistry (FOA-UNESP), São Paulo State University “Júlio de Mesquita Filho”, Araçatuba 16015-050, SP, Brazil

Department of Diagnosis and Surgery, School of Dentistry (FOA-UNESP), São Paulo State University “Júlio de Mesquita Filho”, Araçatuba 16015-050, SP, Brazil

Division of Restorative and Prosthetic Dentistry, College of Dentistry, The Ohio State University, Columbus, OH 43210, USA

Department of Physics, School of Sciences (FC-UNESP), São Paulo State University “Júlio de Mesquita Filho”, Bauru 17033-360, SP, Brazil

Funding

São Paulo State Research Foundation · Research Productivity Scholarship

References (39)

Show source-provided references
1. Estrogen deficiency-mediated osteoimmunity in postmenopausal osteoporosis10.1002/med.22081 ↗
2. Does osteoporosis influence the marginal peri-implant bone level in female patients? A cross-sectional study in a matched collective10.1111/cid.12493 ↗
3. Osteoporosis’ effects on dental implants osseointegration and survival rate: A systematic review of clinical studies
4. Do dental implants placed in patients with osteoporosis have higher risks of failure and marginal bone loss compared to those in healthy patients? A systematic review with meta-analysis10.1007/s00784-023-05005-2 ↗
5. Comparison of Alveolar Bone Level around Osseointegrated Dental Implants among Premenopausal and Postmenopausal Women: A 2-Year Study10.1615/JLongTermEffMedImplants.2023047432 ↗
6. Role of RANK ligand in mediating increased bone resorption in early postmenopausal women10.1172/JCI200317215 ↗
7. Bone health and menopause: Osteoporosis prevention and treatment10.1016/j.beem.2023.101782 ↗
8. Pedroso, A.L., Canal, R., Gehrke, S.A., da Costa, E.M., Scarano, A., Zanelatto, F.B., and Pelegrine, A.A. (2025). The Validation of an Experimental Model in Wistar Female Rats to Study Osteopenia and Osteoporosis. Bioengineering, 12.10.3390/bioengineering12070702 ↗
9. Duarte, N.D., Mulinari-Santos, G., Batista, F.R.S., Gomes, M.B., Monteiro, N.G., Silva, A.C.E.D., Gruber, R., Lisboa-Filho, P.N., Gomes-Ferreira, P.H.S., and Okamoto, R. (2024). Sonification of Deproteinized Bovine Bone Functionalized with Genistein Enhances Bone Repair in Peri-Implant Bone Defects in Ovariectomized Rats. J. Funct. Biomater., 15.10.3390/jfb15110328 ↗
10. Sonochemical synthesis of carbon dots, mechanism, effect of parameters, and catalytic, energy, biomedical and tissue engineering applications10.1016/j.ultsonch.2020.105009 ↗
11. Sonochemical time standardization for bioactive materials used in periimplantar defects filling10.1016/j.ultsonch.2019.04.032 ↗
12. The Evolution of Sonochemistry: From the Beginnings to Novel Applications10.1002/cplu.202300660 ↗
13. Florencio-Silva, R., Sasso, G.R., Sasso-Cerri, E., Simões, M.J., and Cerri, P.S. (2015). Biology of Bone Tissue: Structure, Function, and Factors That Influence Bone Cells. BioMed Res. Int., 2015.10.1155/2015/421746 ↗
14. Deplaigne, V., and Rochefort, G.Y. (2023). Cell-Biomaterial Interactions. Bioengineering, 10.10.3390/bioengineering10020241 ↗
15. How sonochemistry contributes to green chemistry?10.1016/j.ultsonch.2017.03.029 ↗
16. Advances in Green Organic Sonochemistry10.1007/s41061-016-0074-7 ↗
17. de Souza Santos, A.M., Dos Santos Pereira, R., Montemezzi, P., Mello-Machado, R.C., Okamoto, R., Sacco, R., Noronha Lisboa-Filho, P., Messora, M.R., Mourão, C.F., and Hochuli-Vieira, E. (2023). The Interplay of Raloxifene and Sonochemical Bio-Oss in Early Maxillary Sinus Bone Regeneration: A Histological and Immunohistochemical Analysis in Rabbits. Medicina, 59.10.3390/medicina59091521 ↗
18. Gomes-Ferreira, P.H.S., Micheletti, C., Frigério, P.B., de Souza Batista, F.R., Monteiro, N.G., Bim-Júnior, O., Lisboa-Filho, P.N., Grandfield, K., and Okamoto, R. (2022). PTH 1-34-functionalized bioactive glass improves peri-implant bone repair in orchiectomized rats: Microscale and ultrastructural evaluation. Biomater. Adv., 134.10.1016/j.msec.2022.112688 ↗
19. Preventive effect of platelet-rich plasma/Bio-Oss granules composite on medication-related osteonecrosis of the jaw in a rat model10.1016/j.jdent.2025.105802 ↗
20. Percie du Sert, N., Hurst, V., Ahluwalia, A., Alam, S., Avey, M.T., Baker, M., Browne, W.J., Clark, A., Cuthill, I.C., and Dirnagl, U. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. PLoS Biol., 18.10.1371/journal.pbio.3000410 ↗
21. Long, J.A., and Evans, H.M. (1922). The Oestrus Cycle in the Rat and Its Related Phenomena, University of California Press. [1st ed.].
22. Marcantonio, C.C., Perles, G.H., Lopes, M.E.S., Soares, L.F.F., da Costa, P.I., Cerri, P.S., and Cirelli, J.A. (2024). Influence of anti-sclerostin monoclonal antibody in the repair of post-extraction sockets of ovariectomized rats. Arch. Oral Biol., 162.10.1016/j.archoralbio.2024.105962 ↗
23. Effect of ovariectomy induced osteoporosis on metaphysis and diaphysis repair process10.1016/j.injury.2021.02.020 ↗
24. Alveolar Bone Repair Dynamics in Rats Influenced by Coffee Ingestion: A Confocal Microscopy Analysis
25. Chen, M., Wang, Y., Yuan, P., Wang, L., Li, X., and Lei, B. (2024). Multifunctional bioactive glass nanoparticles: Surface–interface decoration and biomedical applications. Regen. Biomater., 11.10.1093/rb/rbae110 ↗
26. Pandey, C., Rokaya, D., and Bhattarai, B.P. (2022). Contemporary Concepts in Osseointegration of Dental Implants: A Review. BioMed Res. Int., 2022.10.1155/2022/6170452 ↗
27. de Araújo, J.C.R., Sobral Silva, L.A., de Barros Lima, V.A., Bastos Campos, T.M., Lisboa Filho, P.N., Okamoto, R., and de Vasconcellos, L.M.R. (2023). The Local Release of Teriparatide Incorporated in 45S5 Bioglass Promotes a Beneficial Effect on Osteogenic Cells and Bone Repair in Calvarial Defects in Ovariectomized Rats. J. Funct. Biomater., 14.10.3390/jfb14020093 ↗
28. Platelet-rich plasma enhances human osteoblast-like cell proliferation and differentiation10.1016/j.joms.2004.07.016 ↗
29. Regulation of angiogenesis during osseointegration by titanium surface microstructure and energy
30. Long-term stability of soft tissues following alveolar ridge preservation: 10-year results of a prospective study around nonsubmerged implants10.11607/prd.2133 ↗
31. Peri-implantitis Update: Risk Indicators, Diagnosis, and Treatment10.1055/s-0040-1715779 ↗
32. Duarte, N.D., Frigério, P.B., Chica, G.E.A., Okamoto, R., Buchaim, R.L., Buchaim, D.V., Messora, M.R., and Issa, J.P.M. (2025). Biomaterials for Guided Tissue Regeneration and Guided Bone Regeneration: A Review. Dent. J., 13.10.3390/dj13040179 ↗
33. Standardized nomenclature, symbols, and units for bone histomorphometry: A 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee10.1002/jbmr.1805 ↗
34. La Monaca, G., Iezzi, G., Cristalli, M.P., Pranno, N., Sfasciotti, G.L., and Vozza, I. (2018). Comparative Histological and Histomorphometric Results of Six Biomaterials Used in Two-Stage Maxillary Sinus Augmentation Model after 6-Month Healing. BioMed Res. Int., 2018.10.1155/2018/9430989 ↗
35. Xu, Y., Li, Y., Hou, Q., Hao, Y., and Ding, Z. (2024). Ball Milling Innovations Advance Mg-Based Hydrogen Storage Materials Towards Practical Applications. Materials, 17.10.3390/ma17112510 ↗
36. Micronization of a soft material: Air-jet and micro-ball milling10.1208/s12249-010-9542-5 ↗
37. Cryomilling for the fabrication of doxorubicin-containing silica-nanoparticle/polycaprolactone nanocomposite films10.1039/C5NR07287E ↗
38. Effects of high-energy ball-milling on injectability and strength of β-tricalcium-phosphate cement10.1016/j.jmbbm.2015.03.005 ↗
39. Review of dental implant rat research models simulating osteoporosis or diabetes