Investigating the role of Rubus coreanus in enhancing peri-implant bone healing in healthy and estrogen-deficient rats

investigating-the-role-of-rubus-coreanus-in-enhancing-peri-implant-bone-healing-in-healthy-and-estrogen-deficient-rats
Investigating the role of Rubus coreanus in enhancing peri-implant bone healing in healthy and estrogen-deficient rats

References

  1. Tella, S. H. & Gallagher, J. C. Prevention and treatment of postmenopausal osteoporosis. J. Steroid Biochem. Mol. Biol. 142, 155–170 (2014).

    Google Scholar 

  2. Kanis, J. A. et al. A new approach to the development of assessment guidelines for osteoporosis. Osteoporos. Int. J. Establ Result Coop. Eur. Found. Osteoporos. Natl. Osteoporos. Found. USA. 13, 527–536 (2002).

    Google Scholar 

  3. Temmerman, A., Rasmusson, L., Kübler, A., Thor, A. & Quirynen, M. An open, prospective, non-randomized, controlled, multicentre study to evaluate the clinical outcome of implant treatment in women over 60 years of age with osteoporosis/osteopenia: 1-year results. Clin. Oral Implants Res. 28, 95–102 (2017).

    Google Scholar 

  4. Eastell, R. Management of osteoporosis due to ovarian failure. Med. Pediatr. Oncol. 41, 222–227 (2003).

    Google Scholar 

  5. Armas, L. A. G. & Recker, R. R. Pathophysiology of osteoporosis: new mechanistic insights. Endocrinol. Metab. Clin. North. Am. 41, 475–486 (2012).

    Google Scholar 

  6. Lemos, C. A. A. et al. 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-analysis. Clin. Oral Investig. 27, 2483–2493 (2023).

    Google Scholar 

  7. Giro, G. et al. Impact of osteoporosis in dental implants: A systematic review. World J. Orthop. 6, 311–315 (2015).

    Google Scholar 

  8. Merheb, J., Vercruyssen, M., Coucke, W. & Quirynen, M. Relationship of implant stability and bone density derived from computerized tomography images. Clin. Implant Dent. Relat. Res. 20, 50–57 (2018).

    Google Scholar 

  9. Song, S., Guo, Y., Yang, Y. & Fu D. Advances in pathogenesis and therapeutic strategies for osteoporosis. Pharmacol. Ther. 237, 108168 (2022).

    Google Scholar 

  10. McClung, M. R. Romosozumab for the treatment of osteoporosis. Osteoporos. Sarcopenia. 4, 11–15 (2018).

    Google Scholar 

  11. Sibai, T., Morgan, E. F. & Einhorn, T. A. Anabolic agents and bone quality. Clin. Orthop. 469, 2215–2224 (2011).

    Google Scholar 

  12. Anil, S., Preethanath, R. S., AlMoharib, H. S., Kamath, K. P. & Anand, P. S. Impact of osteoporosis and its treatment on oral health. Am. J. Med. Sci. 346, 396–401 (2013).

    Google Scholar 

  13. Ruggiero, S. L. et al. American association of oral and maxillofacial surgeons’ position paper on Medication-Related osteonecrosis of the Jaws-2022 update. J. Oral Maxillofac. Surg. Off J. Am. Assoc. Oral Maxillofac. Surg. 80, 920–943 (2022).

    Google Scholar 

  14. Li, Z. et al. Cell death regulation: A new way for natural products to treat osteoporosis. Pharmacol. Res. 187, 106635 (2023).

    Google Scholar 

  15. Martiniakova, M., Babikova, M. & Omelka, R. Pharmacological agents and natural compounds: available treatments for osteoporosis. J. Physiol. Pharmacol. Off J. Pol. Physiol. Soc. https://doi.org/10.26402/jpp.2020.3.01 (2020).

    Google Scholar 

  16. Choi, C. et al. Effect of rubus Coreanus extracts on diabetic osteoporosis by simultaneous regulation of osteoblasts and osteoclasts. Menopause N Y N. 19, 1043–1051 (2012).

    Google Scholar 

  17. Hong, S. et al. Suppressive effects of Geoje raspberry (Rubus Tozawae Nakai ex J.Y. Yang) on Post-Menopausal osteoporosis via its osteogenic activity on osteoblast differentiation. Nutrients 16, 3856 (2024).

    Google Scholar 

  18. Meng, Q., Manghwar, H. & Hu, W. Study on supergenus rubus L.: Edible, Medicinal, and phylogenetic characterization. Plants 11, 1211 (2022).

    Google Scholar 

  19. Lee, M. Y. et al. Metabolite profiling reveals the effect of dietary rubus Coreanus vinegar on Ovariectomy-Induced osteoporosis in a rat model. Mol. Basel Switz. 21, 149 (2016).

    Google Scholar 

  20. Jung Koo, H. et al. Effect of the combinatory mixture of rubus Coreanus Miquel and astragalus Membranaceus bunge extracts on ovariectomy-induced osteoporosis in mice and anti-RANK signaling effect. J. Ethnopharmacol. 151, 951–959 (2014).

    Google Scholar 

  21. Lee, K. H. & Choi, E. M. Rubus Coreanus Miq. Extract promotes osteoblast differentiation and inhibits bone-resorbing mediators in MC3T3-E1 cells. Am. J. Chin. Med. 34, 643–654 (2006).

    Google Scholar 

  22. Do, S. H. et al. Bone-protecting effect of rubus Coreanus by dual regulation of osteoblasts and osteoclasts. Menopause N Y N. 15, 676–683 (2008).

    Google Scholar 

  23. Valencia-Llano, C. H., Solano, M. A. & Grande-Tovar, C. D. Nanocomposites of Chitosan/Graphene Oxide/Titanium dioxide Nanoparticles/Blackberry waste extract as potential bone substitutes. Polymers 13, 3877 (2021).

    Google Scholar 

  24. Kaume, L., Howard, L. R. & Devareddy, L. The blackberry fruit: a review on its composition and chemistry, metabolism and bioavailability, and health benefits. J. Agric. Food Chem. 60, 5716–5727 (2012).

    Google Scholar 

  25. Srivichit, B., Thonusin, C., Chattipakorn, N. & Chattipakorn, S. C. Impacts of bisphosphonates on the bone and its surrounding tissues: mechanistic insights into medication-related osteonecrosis of the jaw. Arch. Toxicol. 96, 1227–1255 (2022).

    Google Scholar 

  26. Duarte, P. M., César Neto, J. B., Gonçalves, P. F. & Sallum, E. A. Nociti, júnior F. H. Estrogen deficiency affects bone healing around titanium implants: a histometric study in rats. Implant Dent. 12, 340–346 (2003).

    Google Scholar 

  27. Tsao, Y. T. et al. Osteocalcin mediates biomineralization during osteogenic maturation in human mesenchymal stromal cells. Int. J. Mol. Sci. 18, 159 (2017).

    Google Scholar 

  28. Lamp, E. C. & Drexler, H. G. Biology of tartrate-resistant acid phosphatase. Leuk. Lymphoma. 39, 477–484 (2000).

    Google Scholar 

  29. Shah, F. A., Johansson, B. R., Thomsen, P. & Palmquist, A. Ultrastructural evaluation of shrinkage artefacts induced by fixatives and embedding resins on osteocyte processes and pericellular space dimensions. J. Biomed. Mater. Res. A. 103, 1565–1576 (2015).

    Google Scholar 

  30. Grandfield, K., Vuong, V. & Schwarcz, H. P. Ultrastructure of bone: hierarchical features from nanometer to micrometer scale revealed in focused ion beam sections in the TEM. Calcif Tissue Int. 103, 606–616 (2018).

    Google Scholar 

  31. Schwarcz, H. P., Abueidda, D. & Jasiuk, I. The Ultrastructure of Bone and Its Relevance to Mechanical Properties. Front Phys https://doi.org/10.3389/fphy.2017.00039 (2017).

    Google Scholar 

  32. Okada, H. et al. Ultrastructure of cement lines. J. Hard Tissue Biol. 22, 445–450 (2013).

    Google Scholar 

  33. Göttlicher, M. et al. Functionalization of Ti-40Nb implant material with strontium by reactive sputtering. Biomater. Res. 21, 18 (2017).

    Google Scholar 

  34. Trino, L. D. et al. Titanium surface Bio-functionalization using osteogenic peptides: surface Chemistry, Biocompatibility, corrosion and tribocorrosion aspects. J. Mech. Behav. Biomed. Mater. 81, 26–38 (2018).

    Google Scholar 

  35. Monteiro, N. G. et al. Rubus Coreanus enhances Peri-Implant bone healing and biomineralization in ovariectomized and healthy rats. Biology 14, 139 (2025).

    Google Scholar 

  36. International Organization for Standardization. ISO 10993-5: Biological Evaluation of Medical Devices – Part 5: Tests for in Vitro Cytotoxicity. (Geneva, 2009).

  37. Song, Y., Ju, Y., Song, G. & Morita, Y. In vitro proliferation and osteogenic differentiation of mesenchymal stem cells on nanoporous alumina. Int. J. Nanomed. 8, 2745–2756 (2013).

    Google Scholar 

  38. Li, Z., Müller, R. & Ruffoni, D. Bone remodeling and mechanobiology around implants: insights from small animal imaging. J. Orthop. Res. Off Publ Orthop. Res. Soc. 36, 584–593 (2018).

    Google Scholar 

  39. Fiorin, L. G. et al. Tamoxifen improves homeostasis in the peri-implant bone remodeling of osseointegrated titanium implants. J. Periodontal Res. 57, 880–890 (2022).

    Google Scholar 

  40. Gomes-Ferreira, P. H. S. et al. Teriparatide improves microarchitectural characteristics of peri-implant bone in orchiectomized rats. Osteoporos. Int. J. Establ Result Coop. Eur. Found. Osteoporos. Natl. Osteoporos. Found. USA. 31, 1807–1815 (2020).

    Google Scholar 

  41. Duarte, N. D. et al. Sonification of deproteinized bovine bone functionalized with genistein enhances bone repair in Peri-Implant bone defects in ovariectomized rats. J. Funct. Biomater. 15, 328 (2024).

    Google Scholar 

  42. Micheletti, C. et al. Mesoscale characterization of osseointegration around an additively manufactured genistein-coated implant. Sci. Rep. 14, 15339 (2024).

    Google Scholar 

  43. Gomes-Ferreira, P. H. S. et al. Evaluation of vitamin D isolated or associated with teriparatide in Peri-Implant bone repair in tibia of orchiectomized rats. Biology 12, 228 (2023).

    Google Scholar 

  44. Fernandes, E. et al. Strontium-containing mineralized phospholipid coatings improve osseointegration in osteoporotic rats. J. Biomed. Mater. Res. A. 113, e37782 (2025).

    Google Scholar 

  45. Freire, A. R. et al. Histometric analysis of bone repair in bone-implant interface using a polylactic/polyglycolic acid copolymer associated with implants in rabbit tibia. J. Oral Implantol. 38 (Spec No), 449–457 (2012).

    Google Scholar 

  46. Glösel, B., Kuchler, U., Watzek, G. & Gruber, R. Review of dental implant rat research models simulating osteoporosis or diabetes. Int. J. Oral Maxillofac. Implants. 25, 516–524 (2010).

    Google Scholar 

  47. Alfaiate, D. et al. Surgical bone implantation technique for rat tibia models of diabetes and osteoporosis. J. Vis. Exp. JoVE. https://doi.org/10.3791/66591 (2024).

    Google Scholar 

  48. Galvao, J. et al. Unexpected low-dose toxicity of the universal solvent DMSO. FASEB J. Off Publ Fed. Am. Soc. Exp. Biol. 28, 1317–1330 (2014).

    Google Scholar 

  49. Paludetto, L. V. et al. Smart delivery of biomolecules interfering with Peri-Implant repair in osteoporotic rats. Int. J. Mol. Sci. 25, 8963 (2024).

    Google Scholar 

  50. Park, J. W. et al. Osteoblast response and osseointegration of a Ti-6Al-4V alloy implant incorporating strontium. Acta Biomater. 6, 2843–2851 (2010).

    Google Scholar 

  51. Parent, M. et al. PLGA in situ implants formed by phase inversion: critical physicochemical parameters to modulate drug release. J. Control Release Off J. Control Release Soc. 172, 292–304 (2013).

    Google Scholar 

  52. Hernandez-Montelongo, J. et al. Electrostatic immobilization of antimicrobial peptides on polyethylenimine and their antibacterial effect against Staphylococcus epidermidis. Colloids Surf. B Biointerfaces. 164, 370–378 (2018).

    Google Scholar 

  53. Rosa, M. L. et al. Chronic ethanol intake inhibits in vitro osteogenesis induced by osteoblasts differentiated from stem cells. J. Appl. Toxicol. JAT. 28, 205–211 (2008).

    Google Scholar 

  54. Health, C. D. and R. Use of International Standard ISO 10993-1. Biological evaluation of medical devices – Part 1: Evaluation and testing within a risk management process. https://www.fda.gov/regulatory-information/search-fda-guidance-documents/use-international-standard-iso-10993-1-biological-evaluation-medical-devices-part-1-evaluation-and (2023).

  55. de Andrade, D. P. et al. Titanium–35niobium alloy as a potential material for biomedical implants: in vitro study. Mater. Sci. Eng. C. 56, 538–544 (2015).

    Google Scholar 

  56. do Prado, R. F. et al. Porous titanium and Ti-35Nb alloy: effects on gene expression of osteoblastic cells derived from human alveolar bone. J. Mater. Sci. Mater. Med. 26, 259 (2015).

    Google Scholar 

  57. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265–275 (1951).

    Google Scholar 

  58. Percie du Sert. The ARRIVE guidelines 2.0: updated guidelines for reporting animal research. BMJ Open. Sci. 4, e100115 (2020).

    Google Scholar 

  59. Lagari, V. S. & Levis, S. Phytoestrogens for menopausal bone loss and climacteric symptoms. J. Steroid Biochem. Mol. Biol. 139, 294–301 (2014).

    Google Scholar 

  60. The oestrous cycle in the rat and its associated phenomena – Digital. Collections – National Library of Medicine. https://collections.nlm.nih.gov/catalog/nlm:nlmuid-06120800R-bk (1922).

  61. Ramalho-Ferreira, G., Faverani, L. P., Prado, F. B., Garcia, I. R. & Okamoto, R. Raloxifene enhances peri-implant bone healing in osteoporotic rats. Int. J. Oral Maxillofac. Surg. 44, 798–805 (2015).

    Google Scholar 

  62. Luvizuto, E. R. et al. Osteocalcin Immunolabeling during the alveolar healing process in ovariectomized rats treated with Estrogen or raloxifene. Bone 46, 1021–1029 (2010).

    Google Scholar 

  63. dos Santos, P. L. et al. Guided implant surgery: what is the influence of this new technique on bone cell viability? J. Oral Maxillofac. Surg. 71, 505–512 (2013).

    Google Scholar 

  64. Bouxsein, M. L. et al. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Min. Res. Off J. Am. Soc. Bone Min. Res. 25, 1468–1486 (2010).

    Google Scholar 

  65. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 9, 676–682 (2012).

    Google Scholar 

  66. Gomes, F. V. et al. 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 (2015).

    Google Scholar 

  67. Jarmar, T. et al. Technique for Preparation and characterization in cross-section of oral titanium implant surfaces using focused ion beam and transmission electron microscopy. J. Biomed. Mater. Res. A. 87, 1003–1009 (2008).

    Google Scholar 

  68. Thorfve, A., Palmquist, A. & Grandfield, K. Three-dimensional analytical techniques for evaluation of osseointegrated titanium implants. Mater. Sci. Technol. 31, 174–179 (2015).

    Google Scholar 

Download references