Impact of resveratrol in the reduction of the harmful effect of diabetes on peri-implant bone repair: bone-related gene expression, counter-torque and micro-CT analysis in rats

References

• Guariguata L, Whiting DR, Hambleton I, et al. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014;103(2):137–149.
   PubMed Web of Science ®Google Scholar
• Dannewitz B, Zeidler A, Hüsing J, et al. Loss of molars in periodontally treated patients: results 10 years and more after active periodontal therapy. J Clin Periodontol. 2016;43(1):53–62.
   PubMed Web of Science ®Google Scholar
• Ghiraldini B, Conte A, Casarin RC, et al. Influence of glycemic control on peri-implant bone healing: 12-month outcomes of local release of bone-related factors and implant stabilization in type 2 diabetics. Clin Implant Dent Relat Res. 2016;18(4):801–809.
   PubMed Web of Science ®Google Scholar
• Oates TW, Dowell S, Robinson M, et al. Glycemic control and implant stabilization in type 2 diabetes mellitus. J Dent Res. 2009;88(4):367–371.
   PubMed Web of Science ®Google Scholar
• Camargo WA, de Vries R, van Luijk J, et al. Diabetes mellitus and bone regeneration: a systematic review and meta-analysis of animal studies. Tissue Eng Part B Rev. 2017;23(5):471–479.
   PubMed Web of Science ®Google Scholar
• Monje A, Catena A, Borgnakke WS. Association between diabetes mellitus/hyperglycaemia and peri-implant diseases: systematic review and meta-analysis. J Clin Periodontol. 2017;44(6):636–648.
   PubMed Web of Science ®Google Scholar
• Conte A, Ghiraldini B, Casarin RC, et al. Impact of type 2 diabetes on the gene expression of bone-related factors at sites receiving dental implants. Int J Oral Maxillofac Surg. 2015;44(10):1302–1308.
   PubMed Web of Science ®Google Scholar
• Pino DS, Casarin RC, Pimentel SP, et al. Effect of resveratrol on critical-sized calvarial defects of diabetic rats: histometric and gene expression analysis. J Oral Maxillofac Surg. 2017;75(12):2561.e1–2561.e10.
   PubMed Web of Science ®Google Scholar
• Alkan A, Erdem E, Günhan O, et al. Histomorphometric evaluation of the effect of doxycycline on the healing of bone defects in experimental diabetes mellitus: a pilot study. J Oral Maxillofac Surg. 2002;60(8):898–904.
   PubMed Web of Science ®Google Scholar
• Yu M, Zhou W, Song Y, et al. Development of mesenchymal stem cell-implant complexes by cultured cells sheet enhances osseointegration in type 2 diabetic rat model. Bone. 2011;49(3):387–394.
   PubMed Web of Science ®Google Scholar
• Rybaczek T, Tangl S, Dobsak T, et al. The effect of parathyroid hormone on osseointegration in insulin-treated diabetic rats. Implant Dent. 2015;24(4):392–396.
   PubMed Web of Science ®Google Scholar
• Wang L, Hu X, Ma X, et al. Promotion of osteointegration under diabetic conditions by tantalum coating-based surface modification on 3-dimensional printed porous titanium implants. Colloids Surf B Biointerfaces. 2016; 148:440–452.
   PubMed Web of Science ®Google Scholar
• Altug HA, Tatli U, Coskun AT, et al. Effects of hyperbaric oxygen treatment on implant osseointegration in experimental diabetes mellitus. J Appl Oral Sci. 2018;26:e20180083.
   PubMed Web of Science ®Google Scholar
• Lu L, Zhijian H, Lei L, et al. Berberine in combination with insulin has additive effects on titanium implants osseointegration in diabetes mellitus rats. Evid Based Complement Alternat Med. 2015; 2015:824259.
   PubMed Web of Science ®Google Scholar
• Cirano FR, Pimentel SP, Casati MZ, et al. Effect of curcumin on bone tissue in the diabetic rat: repair of peri-implant and critical-sized defects. Int J Oral Maxillofac Surg. 2018;47(11):1495–1503.
   PubMed Web of Science ®Google Scholar
• Casati MZ, Algayer C, Cardoso da Cruz G, et al. Resveratrol decreases periodontal breakdown and modulates local levels of cytokines during periodontitis in rats. J Periodontol. 2013;84(10):e58–e64.
   PubMed Web of Science ®Google Scholar
• Corrêa MG, Pires PR, Ribeiro FV, et al. Systemic treatment with resveratrol and/or curcumin reduces the progression of experimental periodontitis in rats. J Periodont Res. 2017;52(2):201–209.
   PubMed Web of Science ®Google Scholar
• Lameira AG, Jr, Françoso BG, Absy S, et al. Resveratrol reverts epigenetic and transcription changes caused by smoke inhalation on bone-related genes in rats. DNA Cell Biol. 2018;37(8):670–679.
   PubMed Web of Science ®Google Scholar
• Wang D, Gao Z, Zhang X. Resveratrol induces apoptosis in murine prostate cancer cells via hypoxia-inducible factor 1-alpha (HIF-1α)/reactive oxygen species (ROS)/P53 signaling. Med Sci Monit. 2018;24:8970–8976.
   PubMed Web of Science ®Google Scholar
• Casarin RC, Casati MZ, Pimentel SP, et al. Resveratrol improves bone repair by modulation of bone morphogenetic proteins and osteopontin gene expression in rats. Int J Oral Maxillofac Surg. 2014;43(7):900–906.
   PubMed Web of Science ®Google Scholar
• Ornstrup MJ, Harsløf T, Sørensen L, et al. Resveratrol increases osteoblast differentiation in vitro independently of inflammation. Calcif Tissue Int. 2016;99(2):155–113.
   PubMed Web of Science ®Google Scholar
• Ribeiro FV, Pimentel SP, Corrêa MG, et al. Resveratrol reverses the negative effect of smoking on peri-implant repair in the tibia of rats. Clin Oral Impl Res. 2019;30(1):1–10.
   PubMed Web of Science ®Google Scholar
• Shakibaei M, Shayan P, Busch F, et al. Resveratrol mediated modulation of Sirt-1/Runx2 promotes osteogenic differentiation of mesenchymal stem cells: potential role of Runx2 deacetylation. PLoS One. 2012;7(4):e35712.
   PubMed Web of Science ®Google Scholar
• Zhao M, Ko SY, Garrett IR, et al. The polyphenol resveratrol promotes skeletal growth in mice through a sirtuin 1-bone morphogenic protein 2 longevity axis. Br J Pharmacol. 2018;175(21):4183–4192.
   PubMed Web of Science ®Google Scholar
• Khera A, Kanta P, Kalra J, et al. Resveratrol restores the level of key inflammatory cytokines and RANKL/OPG ratio in the femur of rat osteoporosis model. J Women Aging. 2018;21:1–13.
   Google Scholar
• Franck FC, Benatti BB, Andia DC, et al. Impact of resveratrol on bone repair in rats exposed to cigarette smoke inhalation: histomorphometric and bone-related gene expression analysis. Int J Oral Maxillofac Surg. 2018;47(4):541–548.
   PubMed Web of Science ®Google Scholar
• Zhu X, Wu C, Qiu S, et al. Effects of resveratrol on glucose control and insulin sensitivity in subjects with type 2 diabetes: systematic review and meta-analysis. Nutr Metab. 2017;14(1):60.
   Google Scholar
• Bo S, Togliatto G, Gambino R, et al. Impact of sirtuin-1 expression on H3K56 acetylation and oxidative stress: a double-blind randomized controlled trial with resveratrol supplementation. Acta Diabetol. 2018;55(4):331–340.
   PubMed Web of Science ®Google Scholar
• de Molon RS, Morais-Camilo JA, Verzola MH, et al. Impact of diabetes mellitus and metabolic control on bone healing around osseointegrated implants: removal torque and histomorphometric analysis in rats. Clin Oral Implants Res. 2013;24(7):831–837.
   PubMed Web of Science ®Google Scholar
• Pimentel SP, Casarin RC, Ribeiro FV, et al. Impact of micronutrients supplementation on bone repair around implants: microCT and counter-torque analysis in rats. J Appl Oral Sci. 2016;24(1):45–51.
   PubMed Web of Science ®Google Scholar
• Liu S, Broucek J, Virdi AS, et al. Limitations of using micro-computed tomography to predict bone-implant contact and mechanical fixation. J Microsc. 2012;245(1):34–42.
   PubMed Web of Science ®Google Scholar
• de Faria Vasconcelos KF, dos Santos Corpas L, da Silveira BM, et al. MicroCT assessment of bone microarchitecture in implant sites reconstructed with autogenous and xenogenous grafts: a pilot study. Clin Oral Implants Res. 2017;28(3):308–313.
   PubMed Web of Science ®Google Scholar
• Ozcan-Kucuk A, Alan H, Gul M, et al. Evaluating the effect of resveratrol on the healing of extraction sockets in cyclosporine a-treated rats. J Oral Maxillofac Surg. 2018;76(7):1404–1413.
   PubMed Web of Science ®Google Scholar
• Matsuda Y, Minagawa T, Okui T, et al. Resveratrol suppresses the alveolar bone resorption induced by artificial trauma from occlusion in mice. Oral Dis. 2018;24(3):412–421.
   PubMed Web of Science ®Google Scholar
• Gan L, Matsuura H, Ichiki T, et al. Improvement of neovascularization capacity of bone marrow mononuclear cells from diabetic mice by ex vivo pretreatment with resveratrol. Hypertens Res. 2009;32(7):542–547.
   PubMed Web of Science ®Google Scholar
• Belibasakis GN, Bostanci N. The RANKL-OPG system in clinical periodontology. J Clin Periodontol. 2012;39(3):239–248.
   PubMed Web of Science ®Google Scholar
• Ikebuchi Y, Aoki S, Honma M, et al. Coupling of bone resorption and formation by RANKL reverse signalling. Nature. 2018;561(7722):195–200.
   PubMed Web of Science ®Google Scholar
• Li X, Liu N, Gu B, et al. BMAL1 regulates balance of osteogenic-osteoclastic function of bone marrow mesenchymal stem cells in type 2 diabetes mellitus through the NF-κB pathway. Mol Biol Rep. 2018;45(6):1691–1704.
   PubMed Web of Science ®Google Scholar
• Stein GS, Lian JB, Van Wijen AJ, et al. Runx2 control of organization, assembly and activity of the regulatory machinery for skeletal gene expression. Oncogene. 2004;23(24):4315–4329.
   PubMed Web of Science ®Google Scholar
• Gennaro G, Claudino M, Cestari TM, et al. Green tea modulates cytokine expression in the periodontium and attenuates alveolar bone resorption in type 1 diabetic rats. PLoS One. 2015;10(8):e0134784
   PubMed Web of Science ®Google Scholar
• Hie M, Tsukamoto I. Increased expression of the receptor for activation of NF-KappaB and decreased runt-related transcription factor 2 expression in bone of rats with streptozotocin-induced diabetes. Int J Mol Med. 2010;26(4):611–618.
   PubMed Web of Science ®Google Scholar
• Serrão CR, Bastos MF, Cruz DF, et al. Role of metformin in reversing the negative impact of hyperglycemia on bone healing around implants inserted in type 2 diabetic rats. Int J Oral Maxillofac Implants. 2017;32(3):547–554.
   PubMed Web of Science ®Google Scholar