Implant surface modifications and their impact on osseointegration and peri-implant diseases through epigenetic changes: A scoping review.
bioactive surfaces
biomaterials
biomedical implants
bone‐implant interface
epigenomics
surface properties
Journal
Journal of periodontal research
ISSN: 1600-0765
Titre abrégé: J Periodontal Res
Pays: United States
ID NLM: 0055107
Informations de publication
Date de publication:
15 May 2024
15 May 2024
Historique:
revised:
09
04
2024
received:
03
01
2024
accepted:
11
04
2024
medline:
15
5
2024
pubmed:
15
5
2024
entrez:
15
5
2024
Statut:
aheadofprint
Résumé
Dental implant surfaces and their unique properties can interact with the surrounding oral tissues through epigenetic cues. The present scoping review provides current perspectives on surface modifications of dental implants, their impact on the osseointegration process, and the interaction between implant surface properties and epigenetics, also in peri-implant diseases. Findings of this review demonstrate the impact of innovative surface treatments on the epigenetic mechanisms of cells, showing promising results in the early stages of osseointegration. Dental implant surfaces with properties of hydrophilicity, nanotexturization, multifunctional coatings, and incorporated drug-release systems have demonstrated favorable outcomes for early bone adhesion, increased antibacterial features, and improved osseointegration. The interaction between modified surface morphologies, different chemical surface energies, and/or release of molecules within the oral tissues has been shown to influence epigenetic mechanisms of the surrounding tissues caused by a physical-chemical interaction. Epigenetic changes around dental implants in the state of health and disease are different. In conclusion, emerging approaches in surface modifications for dental implants functionalized with epigenetics have great potential with a significant impact on modulating bone healing during osseointegration.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Hjalmar Svensson Foundation
ID : HJSV2022048
Informations de copyright
© 2024 The Authors. Journal of Periodontal Research published by John Wiley & Sons Ltd.
Références
Esposito M, Coulthard P, Thomsen P, Worthington HV. The role of implant surface modifications, shape and material on the success of osseointegrated dental implants. A Cochrane systematic review. Eur J Prosthodont Restor Dent. 2005;13(1):15‐31.
Jemt T, Olsson M, Franke SV. Incidence of first implant failure: a retroprospective study of 27 years of implant operations at one specialist clinic. Clin Implant Dent Relat Res. 2015;17 Suppl 2:e501‐e510. doi:10.1111/cid.12277
Dini C, Nagay BE, Cordeiro JM, et al. UV‐photofunctionalization of a biomimetic coating for dental implants application. Mater Sci Eng C Mater Biol Appl. 2020;110:110657. doi:10.1016/j.msec.2020.110657
Kunrath MF, Hubler R. A bone preservation protocol that enables evaluation of osseointegration of implants with micro‐ and nanotextured surfaces. Biotech Histochem. 2019;94(4):261‐270. doi:10.1080/10520295.2018.1552017
Kunrath MF, Hubler R, Shinkai RSA, Teixeira ER. Application of TiO2 nanotubes as a drug delivery system for biomedical implants: a critical review. ChemistrySelect. 2018;3:11180‐11189. doi:10.1002/slct.201801459
Rosales‐Leal JI, Rodriguez‐Valverde MA, Mazzaglia G, et al. Effects of roughness, wettability and morphology of engineered titanium surfaces on osteoblast‐like cell adhesion. Colloids Surf A Physicochem Eng Asp. 2010;365(1–3):222‐229. doi:10.1016/j.colsurfa.2009.12.017
Cunha A, Zouani OF, Plawinski L, et al. Human mesenchymal stem cell behavior on femtosecond laser‐textured Ti‐6Al‐4V surfaces. Nanomedicine (Lond). 2015;10(5):725‐739. doi:10.2217/nnm.15.19
Mathew A, Abraham S, Stephen S, et al. Superhydrophilic multifunctional nanotextured titanium dental implants: in vivo short and long‐term response in a porcine model. Biomater Sci. 2022;10(3):728‐743. doi:10.1039/d1bm01223a
Zambuzzi WF, Bonfante EA, Jimbo R, et al. Nanometer scale titanium surface texturing are detected by signaling pathways involving transient FAK and Src activations. PLoS One. 2014;9(7):e95662. doi:10.1371/journal.pone.0095662
Lv L, Liu Y, Zhang P, et al. The nanoscale geometry of TiO2 nanotubes influences the osteogenic differentiation of human adipose‐derived stem cells by modulating H3K4 trimethylation. Biomaterials. 2015;39:193‐205. doi:10.1016/j.biomaterials.2014.11.002
Rabineau M, Flick F, Mathieu E, et al. Cell guidance into quiescent state through chromatin remodeling induced by elastic modulus of substrate. Biomaterials. 2015;37:144‐155. doi:10.1016/j.biomaterials.2014.10.023
Lorden ER, Levinson HM, Leong KW. Integration of drug, protein, and gene delivery systems with regenerative medicine. Drug Deliv Transl Res. 2015;5(2):168‐186. doi:10.1007/s13346-013-0165-8
Larsson L, Pilipchuk SP, Giannobile WV, Castilho RM. When epigenetics meets bioengineering‐a material characteristics and surface topography perspective. J Biomed Mater Res B Appl Biomater. 2018;106(5):2065‐2071. doi:10.1002/jbm.b.33953
Asa'ad F, Pelanyte G, Philip J, Dahlin C, Larsson L. The role of epigenetic functionalization of implants and biomaterials in osseointegration and bone regeneration‐a review. Molecules. 2020;25(24):5879. doi:10.3390/molecules25245879
Monje A, Asa'ad F, Larsson L, Giannobile WV, Wang HL. Editorial epigenetics: a missing link between periodontitis and peri‐implantitis? Int J Periodontics Restorative Dent. 2018;38(4):476‐477. doi:10.11607/prd.2018.4.e
De Bruyn H, Christiaens V, Doornewaard R, et al. Implant surface roughness and patient factors on long‐term peri‐implant bone loss. Periodontol 2000. 2000;73(1):218‐227. doi:10.1111/prd.12177
Ichioka Y, Asa'ad F, Malekzadeh BO, Westerlund A, Larsson L. Epigenetic changes of osteoblasts in response to titanium surface characteristics. J Biomed Mater Res A. 2021;109(2):170‐180. doi:10.1002/jbm.a.37014
Kunrath MF, Muradas TC, Penha N, Campos MM. Innovative surfaces and alloys for dental implants: what about biointerface‐safety concerns? Dent Mater. 2021;37(10):1447‐1462. doi:10.1016/j.dental.2021.08.008
Shah FA, Thomsen P, Palmquist A. Osseointegration and current interpretations of the bone‐implant interface. Acta Biomater. 2019;84:1‐15. doi:10.1016/j.actbio.2018.11.018
Kunrath MF, Vargas ALM, Sesterheim P, Teixeira ER, Hubler R. Extension of hydrophilicity stability by reactive plasma treatment and wet storage on TiO2 nanotube surfaces for biomedical implant applications. J R Soc Interface. 2020;17(170):20200650. doi:10.1098/rsif.2020.0650
Xia L, Xie Y, Fang B, Wang X, Lin K. In situ modulation of crystallinity and nano‐structures to enhance the stability and osseointegration of hydroxyapatite coatings on Ti‐6Al‐4V implants. Chem Eng J. 2018;347(1):711‐720. doi:10.1016/j.cej.2018.04.045
Kunrath MF, Dos Santos RP, de Oliveira SD, Hubler R, Sesterheim P, Teixeira ER. Osteoblastic cell behavior and early bacterial adhesion on macro‐, micro‐, and nanostructured titanium surfaces for biomedical implant applications. Int J Oral Maxillofac Implants. 2020;35(4):773‐781. doi:10.11607/jomi.8069
Zöllner A, Ganeles J, Korostoff J, Guerra F, Krafft T, Brägger U. Immediate and early non‐occlusal loading of Straumann implants with a chemically modified surface (SLActive) in the posterior mandible and maxilla: interim results from a prospective multicenter randomized‐controlled study. Clin Oral Implants Res. 2008;19(5):442‐450. doi:10.1111/j.1600-0501.2007.01517.x
Albrektsson T, Wennerberg A. Oral implant surfaces: part 1‐review focusing on topographic and chemical properties of different surfaces and in vivo responses to them. Int J Prosthodont. 2004;17(5):536‐543.
Albrektsson T, Sennerby L, Wennerberg A. State of the art of oral implants. Periodontol 2000. 2000;2008(47):15‐26. doi:10.1111/j.1600-0757.2007.00247.x
Lemmerman KJ, Lemmerman NE. Osseointegrated dental implants in private practice: a long‐term case series study. J Periodontol. 2005;76(2):310‐319. doi:10.1902/jop.2005.76.2.310
Kunrath MF, Correia A, Teixeira ER, Hubler R, Dahlin C. Superhydrophilic nanotextured surfaces for dental implants: influence of early saliva contamination and wet storage. Nanomaterials (Basel). 2022;12(15):2603. doi:10.3390/nano12152603
Albrektsson T, Wennerberg A. On osseointegration in relation to implant surfaces. Clin Implant Dent Relat Res. 2019;21 Suppl 1:4‐7. doi:10.1111/cid.12742
Gao Y, Li Y, Xiao J, Xu L, Hu K, Kong L. Effects of microrough and hierarchical hybrid micro/nanorough surface implants on osseointegration in ovariectomized rats: a longitudinal in vivo microcomputed tomography evaluation. J Biomed Mater Res A. 2012;100(8):2159‐2167. doi:10.1002/jbm.a.34129
Aboushelib MN, Salem NA, Taleb AL, El Moniem NM. Influence of surface nano‐roughness on osseointegration of zirconia implants in rabbit femur heads using selective infiltration etching technique. J Oral Implantol. 2013;39(5):583‐590. doi:10.1563/AAID-JOI-D-11-00075
Kunrath MF, Monteiro MSG, Gupta S, Hubler R, de Oliveira SD. Influence of titanium and zirconia modified surfaces for rapid healing on adhesion and biofilm formation of Staphylococcus epidermidis. Arch Oral Biol. 2020;117:104824. doi:10.1016/j.archoralbio.2020.104824
Bermejo P, Sanchez MC, Llama‐Palacios A, Figuero E, Herrera D, Sanz AM. Biofilm formation on dental implants with different surface micro‐topography: an in vitro study. Clin Oral Implants Res. 2019;30(8):725‐734. doi:10.1111/clr.13455
Hirakawa Y, Jimbo R, Shibata Y, Watanabe I, Wennerberg A, Sawase T. Accelerated bone formation on photo‐induced hydrophilic titanium implants: an experimental study in the dog mandible. Clin Oral Implants Res. 2013;24 Suppl A100:139‐144. doi:10.1111/j.1600-0501.2011.02401.x
Toffoli A, Parisi L, Tatti R, et al. Thermal‐induced hydrophilicity enhancement of titanium dental implant surfaces. J Oral Sci. 2020;62(2):217‐221. doi:10.2334/josnusd.19-0235
Rupp F, Scheideler L, Olshanska N, de Wild M, Wieland M, Geis‐Gerstorfer J. Enhancing surface free energy and hydrophilicity through chemical modification of microstructured titanium implant surfaces. J Biomed Mater Res A. 2006;76(2):323‐334. doi:10.1002/jbm.a.30518
Rupp F, Gittens RA, Scheideler L, et al. A review on the wettability of dental implant surfaces I: theoretical and experimental aspects. Acta Biomater. 2014;10(7):2894‐2906. doi:10.1016/j.actbio.2014.02.040
Schwarz F, Wieland M, Schwartz Z, et al. Potential of chemically modified hydrophilic surface characteristics to support tissue integration of titanium dental implants. J Biomed Mater Res B Appl Biomater. 2009;88(2):544‐557. doi:10.1002/jbm.b.31233
Hicklin SP, Schneebeli E, Chappuis V, Janner SF, Buser D, Bragger U. Early loading of titanium dental implants with an intra‐operatively conditioned hydrophilic implant surface after 21 days of healing. Clin Oral Implants Res. 2016;27(7):875‐883. doi:10.1111/clr.12706
Bierbaum S, Mulansky S, Bognar E, et al. Osteogenic nanostructured titanium surfaces with antibacterial properties under conditions that mimic the dynamic situation in the oral cavity. Biomater Sci. 2018;6(6):1390‐1402. doi:10.1039/c8bm00177d
Gulati K, Moon HJ, Kumar PTS, Han P, Ivanovski S. Anodized anisotropic titanium surfaces for enhanced guidance of gingival fibroblasts. Mater Sci Eng C Mater Biol Appl. 2020;112:110860. doi:10.1016/j.msec.2020.110860
Gnilitskyi I, Pogorielov M, Viter R, et al. Cell and tissue response to nanotextured Ti6Al4V and Zr implants using high‐speed femtosecond laser‐induced periodic surface structures. Nanomedicine. 2019;21:102036. doi:10.1016/j.nano.2019.102036
Svensson S, Suska F, Emanuelsson L, et al. Osseointegration of titanium with an antimicrobial nanostructured noble metal coating. Nanomedicine. 2013;9(7):1048‐1056. doi:10.1016/j.nano.2013.04.009
Bright R, Fernandes D, Wood J, et al. Long‐term antibacterial properties of a nanostructured titanium alloy surface: an in vitro study. Materials Today Bio. 2022;13:100176. doi:10.1016/j.mtbio.2021.100176
Salou L, Hoornaert A, Louarn G, Layrolle P. Enhanced osseointegration of titanium implants with nanostructured surfaces: an experimental study in rabbits. Acta Biomater. 2015;11:494‐502. doi:10.1016/j.actbio.2014.10.017
Giro G, Tovar N, Witek L, et al. Osseointegration assessment of chairside argon‐based nonthermal plasma‐treated Ca‐P coated dental implants. J Biomed Mater Res A. 2013;101(1):98‐103. doi:10.1002/jbm.a.34304
Schliephake H, Scharnweber D, Roesseler S, Dard M, Sewing A, Aref A. Biomimetic calcium phosphate composite coating of dental implants. Int J Oral Maxillofac Implants. 2006;21(5):738‐746.
Binahmed A, Stoykewych A, Hussain A, Love B, Pruthi V. Long‐term follow‐up of hydroxyapatite‐coated dental implants‐a clinical trial. Int J Oral Maxillofac Implants. 2007;22(6):963‐968.
Moore B, Asadi E, Lewis G. Deposition methods for microstructured and nanostructured coatings on metallic bone implants: a review. Adv Mater Sci Eng. 2017;2017:1‐9. doi:10.1155/2017/5812907
Ke D, Vu AA, Bandyopadhyay A, Bose S. Compositionally graded doped hydroxyapatite coating on titanium using laser and plasma spray deposition for bone implants. Acta Biomater. 2019;84:414‐423. doi:10.1016/j.actbio.2018.11.041
Suarez‐Lopez Del Amo F, Garaicoa‐Pazmino C, Fretwurst T, Castilho RM, Squarize CH. Dental implants‐associated release of titanium particles: a systematic review. Clin Oral Implants Res. 2018;29(11):1085‐1100. doi:10.1111/clr.13372
Asa'ad F, Thomsen P, Kunrath MF. The role of titanium particles and ions in the pathogenesis of peri‐Implantitis. J Bone Metab. 2022;29(3):145‐154. doi:10.11005/jbm.2022.29.3.145
Civantos A, Martínez‐Campos E, Ramos V, Elvira C, Gallardo A, Abarrategi A. Titanium coatings and surface modifications: toward clinically useful bioactive implants. ACS Biomater Sci Eng. 2017;3(7):1245‐1261. doi:10.1021/acsbiomaterials.6b00604
Kunrath MF, Rubensam G, Rodrigues FVF, et al. Nano‐scaled surfaces and sustainable‐antibiotic‐release from polymeric coating for application on intra‐osseous implants and trans‐mucosal abutments. Colloids Surf B Biointerfaces. 2023;228:113417. doi:10.1016/j.colsurfb.2023.113417
Kunrath MF, Diz FM, Magini R, Galarraga‐Vinueza ME. Nanointeraction: the profound influence of nanostructured and nano‐drug delivery biomedical implant surfaces on cell behavior. Adv Colloid Interface Sci. 2020;284:102265. doi:10.1016/j.cis.2020.102265
de Avila ED, Castro AGB, Tagit O, et al. Anti‐bacterial efficacy via drug‐delivery system from layer‐by‐later coating for percutaneous dental implant components. Appl Surf Sci. 2019;488:194‐204. doi:10.1016/j.apsusc.2019.05.154
Zhang W, Cao H, Zhang X, et al. A strontium‐incorporated nanoporous titanium implant surface for rapid osseointegration. Nanoscale. 2016;8(9):5291‐5301. doi:10.1039/c5nr08580b
Hasani‐Sadrabadi MM, Pouraghaei S, Zahedi E, et al. Antibacterial and Osteoinductive implant surface using layer‐by‐layer assembly. J Dent Res. 2021;100(10):1161‐1168. doi:10.1177/00220345211029185
Alenezi A, Chrcanovic B, Wennerberg A. Effects of local drug and chemical compound delivery on bone regeneration around dental implants in animal models: a systematic review and meta‐analysis. Int J Oral Maxillofac Implants. 2018;33(1):e1‐e18. doi:10.11607/jomi.6333
Kazek‐Kesik A, Nosol A, Plonka J, et al. PLGA‐amoxicillin‐loaded layer formed on anodized Ti alloy as a hybrid material for dental implant applications. Mater Sci Eng C Mater Biol Appl. 2019;94:998‐1008. doi:10.1016/j.msec.2018.10.049
Eawsakul K, Tancharoen S, Nasongkla N. Combination of dip coating of BMP‐2 and spray coating of PLGA on dental implants for osseointegration. J Drug Deliv Sci Technol. 2021;61:102296. doi:10.1016/j.jddst.2020.102296
Kunrath MF, Shah FA, Dahlin C. Bench‐to‐bedside: Feasibility of nano‐engineered and drug‐delivery biomaterials for bone‐anchored implants and periodontal applications. Materials Today Bio. 2023;18:100540. doi:10.1016/j.mtbio.2022.100540
Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16(1):6‐21. doi:10.1101/gad.947102
Adcock IM, Tsaprouni L, Bhavsar P, Ito K. Epigenetic regulation of airway inflammation. Curr Opin Immunol. 2007;19(6):694‐700. doi:10.1016/j.coi.2007.07.016
Alaskhar Alhamwe B, Khalaila R, Wolf J, et al. Histone modifications and their role in epigenetics of atopy and allergic diseases. Allergy Asthma Clin Immunol. 2018;14:39. doi:10.1186/s13223-018-0259-4
Filipowicz W, Bhattacharyya SN, Sonenberg N. Mechanisms of post‐transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 2008;9(2):102‐114. doi:10.1038/nrg2290
Larsson L, Kavanagh NM, Nguyen TVN, Castilho RM, Berglundh T, Giannobile WV. Influence of epigenetics on periodontitis and peri‐implantitis pathogenesis. Periodontol 2000. 2022;90(1):125‐137. doi:10.1111/prd.12453
Crowder SW, Leonardo V, Whittaker T, Papathanasiou P, Stevens MM. Material cues as potent regulators of epigenetics and stem cell function. Cell Stem Cell. 2016;18(1):39‐52. doi:10.1016/j.stem.2015.12.012
Vermeulen S, Van Puyvelde B, Bengtsson Del Barrio L, et al. Micro‐topographies induce epigenetic reprogramming and quiescence in human mesenchymal stem cells. Adv Sci (Weinh). 2022;10(1):e2203880. doi:10.1002/advs.202203880
Hulsman M, Hulshof F, Unadkat H, et al. Analysis of high‐throughput screening reveals the effect of surface topographies on cellular morphology. Acta Biomater. 2015;15:29‐38. doi:10.1016/j.actbio.2014.12.019
Palmieri A, Pezzetti F, Brunelli G, et al. Short‐period effects of zirconia and titanium on osteoblast microRNAs. Clin Implant Dent Relat Res. 2008;10(3):200‐205. doi:10.1111/j.1708-8208.2007.00078.x
Palmieri A, Pezzetti F, Brunelli G, et al. Zirconium oxide regulates RNA interfering of osteoblast‐like cells. J Mater Sci Mater Med. 2008;19(6):2471‐2476. doi:10.1007/s10856-008-3386-5
Chakravorty N, Ivanovski S, Prasadam I, Crawford R, Oloyede A, Xiao Y. The microRNA expression signature on modified titanium implant surfaces influences genetic mechanisms leading to osteogenic differentiation. Acta Biomater. 2012;8(9):3516‐3523. doi:10.1016/j.actbio.2012.05.008
Iaculli F, Di Filippo ES, Piattelli A, Mancinelli R, Fulle S. Dental pulp stem cells grown on dental implant titanium surfaces: an in vitro evaluation of differentiation and microRNAs expression. J Biomed Mater Res B Appl Biomater. 2017;105(5):953‐965. doi:10.1002/jbm.b.33628
Wimmers Ferreira MR, Rodrigo Fernandes R, Freire Assis A, et al. Oxidative nanopatterning of titanium surface influences mRNA and MicroRNA expression in human alveolar bone osteoblastic cells. Int J Biomater. 2016;2016:9169371. doi:10.1155/2016/9169371
Zheng G, Guan B, Hu P, et al. Topographical cues of direct metal laser sintering titanium surfaces facilitate osteogenic differentiation of bone marrow mesenchymal stem cells through epigenetic regulation. Cell Prolif. 2018;51(4):e12460. doi:10.1111/cpr.12460
Lyu M, Zheng Y, Jia L, et al. Genome‐wide DNA‐methylation profiles in human bone marrow mesenchymal stem cells on titanium surfaces. Eur J Oral Sci. 2019;127(3):196‐209. doi:10.1111/eos.12607
Zhuang XM, Zhou B, Yuan KF. Role of p53 mediated miR‐23a/CXCL12 pathway in osteogenic differentiation of bone mesenchymal stem cells on nanostructured titanium surfaces. Biomed Pharmacother. 2019;112:108649. doi:10.1016/j.biopha.2019.108649
Cho YD, Kim WJ, Kim S, Ku Y, Ryoo HM. Surface topography of titanium affects their osteogenic potential through DNA methylation. Int J Mol Sci. 2021;22(5):2406. doi:10.3390/ijms22052406
Bighetti‐Trevisan RL, Almeida LO, Castro‐Raucci LMS, et al. Titanium with nanotopography attenuates the osteoclast‐induced disruption of osteoblast differentiation by regulating histone methylation. Biomater Adv. 2022;134:112548. doi:10.1016/j.msec.2021.112548
Fernandes C, da Silva RAF, Wood PF, et al. Titanium‐enriched medium promotes environment‐induced epigenetic machinery changes in human endothelial cells. J Funct Biomater. 2023;14(3):131. doi:10.3390/jfb14030131
Palmieri A, Pezzetti F, Brunelli G, et al. Anatase nanosurface regulates microRNAs. J Craniofac Surg. 2008;19(2):328‐333. doi:10.1097/SCS.0b013e3181534ab3
Asa'ad F, Monje A, Larsson L. Role of epigenetics in alveolar bone resorption and regeneration around periodontal and peri‐implant tissues. Eur J Oral Sci. 2019;127(6):477‐493. doi:10.1111/eos.12657
Suarez‐Lopez Del Amo F, Rudek I, Wagner VP, et al. Titanium activates the DNA damage response pathway in Oral epithelial cells: a pilot study. Int J Oral Maxillofac Implants. 2017;32(6):1413‐1420. doi:10.11607/jomi.6077
Voigt P, Tee WW, Reinberg D. A double take on bivalent promoters. Genes Dev. 2013;27(12):1318‐1338. doi:10.1101/gad.219626.113
Hsu CC, Serio A, Gopal S, et al. Biophysical regulations of epigenetic state and notch signaling in neural development using microgroove substrates. ACS Appl Mater Interfaces. 2022;14(29):32773‐32787. doi:10.1021/acsami.2c01996
Goetzke R, Sechi A, De Laporte L, Neuss S, Wagner W. Why the impact of mechanical stimuli on stem cells remains a challenge. Cell Mol Life Sci. 2018;75(18):3297‐3312. doi:10.1007/s00018-018-2830-z
Wu X, Chen X, Mi W, Wu T, Gu Q, Huang H. MicroRNA sequence analysis identifies microRNAs associated with peri‐implantitis in dogs. Biosci Rep. 2017;37(5):BSR20170768. doi:10.1042/BSR20170768
Wu X, Gu Q, Chen X, Mi W, Wu T, Huang H. MiR‐27a targets DKK2 and SFRP1 to promote reosseointegration in the regenerative treatment of peri‐implantitis. J Bone Miner Res. 2019;34(1):123‐134. doi:10.1002/jbmr.3575
Menini M, Dellepiane E, Baldi D, Longobardi MG, Pera P, Izzotti A. Microarray expression in peri‐implant tissue next to different titanium implant surfaces predicts clinical outcomes: a split‐mouth study. Clin Oral Implants Res. 2017;28(9):e121‐e134. doi:10.1111/clr.12943
Menini M, Pesce P, Baldi D, Coronel Vargas G, Pera P, Izzotti A. Prediction of titanium implant success by analysis of microRNA expression in peri‐implant tissue. a 5‐year follow‐up study. J Clin Med. 2019;8(6):888. doi:10.3390/jcm8060888
Khouly I, Pardinas Lopez S, Diaz Prado SM, et al. Global DNA methylation in dental implant failure due to peri‐Implantitis: an exploratory clinical pilot study. Int J Environ Res Public Health. 2022;19(2):1020. doi:10.3390/ijerph19021020
Kadkhodazadeh M, Jafari AR, Amid R, et al. MiR146a and MiR499 gene polymorphisms in Iranian periodontitis and peri‐implantitis patients. J Long Term Eff Med Implants. 2013;23(1):9‐16. doi:10.1615/jlongtermeffmedimplants.2013007073
Daubert DM, Pozhitkov AE, Safioti LM, Kotsakis GA. Association of Global DNA methylation to titanium and peri‐Implantitis: a case‐control study. JDR Clin Trans Res. 2019;4(3):284‐291. doi:10.1177/2380084418822831
Bai L, Du Z, Du J, et al. A multifaceted coating on titanium dictates osteoimmunomodulation and osteo/angio‐genesis towards ameliorative osseointegration. Biomaterials. 2018;162:154‐169. doi:10.1016/j.biomaterials.2018.02.010
Zhang H, Yuan Y, Xue H, et al. Reprogramming mitochondrial metabolism of macrophages by miRNA‐released microporous coatings to prevent peri‐implantitis. J Nanobiotechnology. 2023;21(1):485. doi:10.1186/s12951-023-02244-z
Geng Z, Yu Y, Li Z, et al. miR‐21 promotes osseointegration and mineralization through enhancing both osteogenic and osteoclastic expression. Mater Sci Eng C Mater Biol Appl. 2020;111:110785. doi:10.1016/j.msec.2020.110785
Geng Z, Wang X, Zhao J, et al. The synergistic effect of strontium‐substituted hydroxyapatite and microRNA‐21 on improving bone remodeling and osseointegration. Biomater Sci. 2018;6(10):2694‐2703. doi:10.1039/c8bm00716k
Song W, Yang C, Svend Le DQ, Zhang Y, Kjems J. Calcium‐MicroRNA complex‐functionalized nanotubular implant surface for highly efficient transfection and enhanced osteogenesis of mesenchymal stem cells. ACS Appl Mater Interfaces. 2018;10(9):7756‐7764. doi:10.1021/acsami.7b18289
Yan J, Chang B, Hu X, Cao C, Zhao L, Zhang Y. Titanium implant functionalized with antimiR‐138 delivered cell sheet for enhanced peri‐implant bone formation and vascularization. Mater Sci Eng C Mater Biol Appl. 2018;89:52‐64. doi:10.1016/j.msec.2018.03.011
Shao D, Wang C, Sun Y, Cui L. Effects of oral implants with miR‐122‐modified cell sheets on rat bone marrow mesenchymal stem cells. Mol Med Rep. 2018;17(1):1537‐1544. doi:10.3892/mmr.2017.8094
Meng Y, Li X, Li Z, et al. Surface functionalization of titanium alloy with miR‐29b nanocapsules to enhance bone regeneration. ACS Appl Mater Interfaces. 2016;8(9):5783‐5793. doi:10.1021/acsami.5b10650
Liu X, Tan N, Zhou Y, et al. Delivery of antagomiR204‐conjugated gold nanoparticles from PLGA sheets and its implication in promoting osseointegration of titanium implant in type 2 diabetes mellitus. Int J Nanomedicine. 2017;12:7089‐7101. doi:10.2147/IJN.S124584
Wang Z, Wu G, Feng Z, et al. Microarc‐oxidized titanium surfaces functionalized with microRNA‐21‐loaded chitosan/hyaluronic acid nanoparticles promote the osteogenic differentiation of human bone marrow mesenchymal stem cells. Int J Nanomedicine. 2015;10:6675‐6687. doi:10.2147/IJN.S94689
Wu K, Song W, Zhao L, et al. MicroRNA functionalized microporous titanium oxide surface by lyophilization with enhanced osteogenic activity. ACS Appl Mater Interfaces. 2013;5(7):2733‐2744. doi:10.1021/am400374c
Singh A, Ali S, Mahdi AA, Srivastava RN. MicroRNAs and their role in bone remodeling and pathogenesis. JAMMR. 2012;2(4):727‐749. doi:10.9734/BJMMR/2012/1543
Suh JS, Lee JY, Choi YS, Chung CP, Park YJ. Peptide‐mediated intracellular delivery of miRNA‐29b for osteogenic stem cell differentiation. Biomaterials. 2013;34(17):4347‐4359. doi:10.1016/j.biomaterials.2013.02.039
Fang S, Deng Y, Gu P, Fan X. MicroRNAs regulate bone development and regeneration. Int J Mol Sci. 2015;16(4):8227‐8253. doi:10.3390/ijms16048227
Rossi M, Pitari MR, Amodio N, et al. miR‐29b negatively regulates human osteoclastic cell differentiation and function: implications for the treatment of multiple myeloma‐related bone disease. J Cell Physiol. 2013;228(7):1506‐1515. doi:10.1002/jcp.24306
Bushati N, Cohen SM. microRNA functions. Annu Rev Cell Dev Biol. 2007;23:175‐205. doi:10.1146/annurev.cellbio.23.090506.123406
Krichevsky AM, Gabriely G. miR‐21: a small multi‐faceted RNA. J Cell Mol Med. 2009;13(1):39‐53. doi:10.1111/j.1582-4934.2008.00556.x
Bhagat TD, Zhou L, Sokol L, et al. miR‐21 mediates hematopoietic suppression in MDS by activating TGF‐beta signaling. Blood. 2013;121(15):2875‐2881. doi:10.1182/blood-2011-12-397067
Gamez B, Rodriguez‐Carballo E, Ventura F. MicroRNAs and post‐transcriptional regulation of skeletal development. J Mol Endocrinol. 2014;52(3):R179‐R197. doi:10.1530/JME-13-0294
Meng YB, Li X, Li ZY, et al. microRNA‐21 promotes osteogenic differentiation of mesenchymal stem cells by the PI3K/beta‐catenin pathway. J Orthop Res. 2015;33(7):957‐964. doi:10.1002/jor.22884
Eskildsen T, Taipaleenmaki H, Stenvang J, et al. MicroRNA‐138 regulates osteogenic differentiation of human stromal (mesenchymal) stem cells in vivo. Proc Natl Acad Sci U S A. 2011;108(15):6139‐6144. doi:10.1073/pnas.1016758108
Young SR, Gerard‐O'Riley R, Kim JB, Pavalko FM. Focal adhesion kinase is important for fluid shear stress‐induced mechanotransduction in osteoblasts. J Bone Miner Res. 2009;24(3):411‐424. doi:10.1359/jbmr.081102