Titanium offers excellent biocompatibility and extraordinary mechanical properties. As a result, it is used as a material for dental implants. Implants infected by peri-implantitis can be cleaned for successful re-osseointegration. Optimal surface properties, such as roughness and wettability, have a significant impact on cell adhesion. The aim of this study was to evaluate the adhesion and proliferation of osteoblasts on the surface of repeatedly cleaned nanostructured titanium samples. Human osteoblast-like cells MG-63 were seeded on nanostructured titanium specimens manufactured from rods produced by the equal channel angular pressing. For surface characterization, roughness and wettability were measured. Cell adhesion after 2 h as well as cell proliferation after 48 h from plating was assessed. We have found that this repeated cleaning of titanium surface reduced cell adhesion as well as proliferation. These events depend on interplay of surface properties, such as wettability, roughness and topography. It is difficult to distinguish which factors are responsible for these events and further investigations will be required. However, even after the several rounds of repeated cleaning, there was a certain rate of adhesion and proliferation recorded. Therefore the attempts to save failing implants by using in situ cleaning are promising.

Department of Medical Chemistry and Biochemistry Faculty of Medicine in Pilsen Charles University Karlovarska 48 301 66 Pilsen Czech Republic

Department of Stomatology Faculty of Medicine in Pilsen University Hospital and Charles University alej Svobody 80 301 00 Pilsen Czech Republic

Timplant s r o Sjednoceni 77 1 72525 Ostrava Czech Republic

Zobrazit více v PubMed

Banerjee D., Williams J.C. Perspectives on Titanium Science and Technology. Acta Mater. 2013;61:844–879. doi: 10.1016/j.actamat.2012.10.043. DOI

Babuska V., Dobra J., Kulda V., Kripnerova M., Moztarzadeh A., Bolek L., Lahoda J., Hrusak D. Comparison of fibroblast and osteoblast response to cultivation on titanium implants with different grain sizes. J. Nanomater. 2015;2015:920893. doi: 10.1155/2015/920893. DOI

Özcan M., Hämmerle C. Titanium as a Reconstruction and Implant Material in Dentistry: Advantages and Pitfalls. Materials. 2012;5:1528–1545. doi: 10.3390/ma5091528. DOI

Valiev R.Z., Langdon T.G. Principles of equal-channel angular pressing as a processing tool for grain refinement. Prog. Mater. Sci. 2006;51:881–981. doi: 10.1016/j.pmatsci.2006.02.003. DOI

Qarni M.J., Sivaswamy G., Rosochowski A., Boczkal S. On the evolution of microstructure and texture in commercial purity titanium during multiple passes of incremental equal channel angular pressing (I-ECAP) Mater. Sci. Eng. A. 2017;699:31–47. doi: 10.1016/j.msea.2017.05.040. DOI

Novak Z. Periimplantitis, problems and solutions. Quintessenz. 2004;13:1–4.

Persson G.R., Renvert S. Cluster of Bacteria Associated with Peri-Implantitis: Pathogens in Peri-Implantitis. Clin. Implant Dent. Relat. Res. 2014;16:783–793. doi: 10.1111/cid.12052. PubMed DOI

de Waal Y.C., Eijsbouts H.V., Winkel E.G., van Winkelhoff A.J. Microbial Characteristics of Peri-Implantitis: A Case-Control Study. J. Periodontol. 2017;88:209–217. doi: 10.1902/jop.2016.160231. PubMed DOI

Abranches J., Zeng L., Kajfasz J.K., Palmer S.R., Chakraborty B., Wen Z.T., Richards V.P., Brady L.J., Lemos J.A. Biology of Oral Streptococci. Microbiol. Spectr. 2018;6:426–434. doi: 10.1128/microbiolspec.GPP3-0042-2018. PubMed DOI PMC

Khoury F., Keeve P.L., Ramanauskaite A., Schwarz F., Koo K.T., Sculean A., Romanos G. Surgical treatment of peri-implantitis—Consensus report of working group 4. Int. Dent. J. 2019;69:18–22. doi: 10.1111/idj.12505. PubMed DOI PMC

Koo K.T., Khoury F., Keeve P.L., Schwarz F., Ramanauskaite A., Sculean A., Romanos G. Implant Surface Decontamination by Surgical Treatment of Periimplantitis: A Literature Review. Implant Dent. 2019;28:173–176. doi: 10.1097/ID.0000000000000840. PubMed DOI

Levin L., Zigdon H., Coelho P.G., Suzuki M., Machtei E.E. Reimplantation of Dental Implants following Ligature-Induced Peri-Implantitis: A Pilot Study in Dogs: Reimplantation following Ligature-Induced Peri-Implantitis. Clin. Implant Dent. Relat. Res. 2013;15:1–6. doi: 10.1111/j.1708-8208.2011.00371.x. PubMed DOI

Persson L.G., Ericsson I., Berglundh T., Lindhe J. Osseintegration following treatment of peri-implantitis and replacement of implant components. An experimental study in the dog. J. Clin. Periodontol. 2001;28:258–263. doi: 10.1034/j.1600-051x.2001.028003258.x. PubMed DOI

Zhou W., Wang F., Monje A., Elnayef B., Huang W., Wu Y. Feasibility of Dental Implant Replacement in Failed Sites: A Systematic Review. Int. J. Oral Maxillofac. Implants. 2016;31:535–545. doi: 10.11607/jomi.4312. PubMed DOI

Duske K., Jablonowski L., Koban I., Matthes R., Holtfreter B., Sckell A., Nebe J.B., von Woedtke T., Weltmann K.D., Kocher T. Cold atmospheric plasma in combination with mechanical treatment improves osteoblast growth on biofilm covered titanium discs. Biomaterials. 2015;52:327–334. doi: 10.1016/j.biomaterials.2015.02.035. PubMed DOI

Renvert S., Polyzois I., Maguire R. Re-osseointegration on previously contaminated surfaces: A systematic review. Clin. Oral Implants Res. 2009;20:216–227. doi: 10.1111/j.1600-0501.2009.01786.x. PubMed DOI

Lin C.Y., Chen Z., Pan W.L., Wang H.L. The effect of supportive care in preventing peri-implant diseases and implant loss: A systematic review and meta-analysis. Clin. Oral Implants Res. 2019;30:714–724. doi: 10.1111/clr.13496. PubMed DOI

Valiev R.Z., Estrin Y., Horita Z., Langdon T.G., Zehetbauer M.J., Zhu Y. Producing Bulk Ultrafine-Grained Materials by Severe Plastic Deformation: Ten Years Later. JOM. 2016;68:1216–1226. doi: 10.1007/s11837-016-1820-6. DOI

Nazarov D., Zemtsova E., Solokhin A., Valiev R., Smirnov V. Modification of the Surface Topography and Composition of Ultrafine and Coarse Grained Titanium by Chemical Etching. Nanomaterials. 2017;7:15. doi: 10.3390/nano7010015. PubMed DOI PMC

Valente N.A., Andreana S. Peri-implant disease: What we know and what we need to know. J. Periodontal Implant Sci. 2016;46:136–151. doi: 10.5051/jpis.2016.46.3.136. PubMed DOI PMC

Kulkarni M., Mazare A., Gongadze E., Perutkova S., Kralj-Iglič V., Milosev I., Schmuki P., Iglic A., Mozetic M. Titanium nanostructures for biomedical applications. Nanotechnology. 2015;26:062002. doi: 10.1088/0957-4484/26/6/062002. PubMed DOI

Babuska V., Palan J., Kolaja Dobra J., Kulda V., Duchek M., Cerny J., Hrusak D. Proliferation of Osteoblasts on Laser-Modified Nanostructured Titanium Surfaces. Materials. 2018;11:1827. doi: 10.3390/ma11101827. PubMed DOI PMC

Lavenus S., Pilet P., Guicheux J., Weiss P., Louarn G., Layrolle P. Behaviour of mesenchymal stem cells, fibroblasts and osteoblasts on smooth surfaces. Acta Biomater. 2011;7:1525–1534. doi: 10.1016/j.actbio.2010.12.033. PubMed DOI

Shi X., Xu L., Munar M.L., Ishikawa K. Hydrothermal treatment for TiN as abrasion resistant dental implant coating and its fibroblast response. Mater. Sci. Eng. C. 2015;49:1–6. doi: 10.1016/j.msec.2014.12.059. PubMed DOI

Zhao G., Schwartz Z., Wieland M., Rupp F., Geis-Gerstorfer J., Cochran D.L., Boyan B.D. High surface energy enhances cell response to titanium substrate microstructure. J. Biomed. Mater. Res. A. 2005;74A:49–58. doi: 10.1002/jbm.a.30320. PubMed DOI

Rupp F., Scheideler L., Eichler M., Geis-Gerstorfer J. Wetting behavior of dental implants. Int. J. Oral Maxillofac. Implants. 2011;26:1256–1266. PubMed

Massaro C., Rotolo P., De Riccardis F., Milella E., Napoli A., Wieland M., Textor M., Spencer N.D., Brunette D.M. Comparative investigation of the surface properties of commercial titanium dental implants. Part I: Chemical composition. J. Mater. Sci. Mater. Med. 2002;13:535–548. doi: 10.1023/A:1015170625506. PubMed DOI

Le Guéhennec L., Soueidan A., Layrolle P., Amouriq Y. Surface treatments of titanium dental implants for rapid osseointegration. Dent. Mater. 2007;23:844–854. doi: 10.1016/j.dental.2006.06.025. PubMed DOI

Herminghaus S. Roughness-induced non-wetting. Europhys. Lett. EPL. 2000;52:165–170. doi: 10.1209/epl/i2000-00418-8. DOI

Quéré D. Wetting and Roughness. Annu. Rev. Mater. Res. 2008;38:71–99. doi: 10.1146/annurev.matsci.38.060407.132434. DOI

Marmur A. Contact Angle Wettability and Adhesion. Volume 6. CRC Press; Boca Raton, FL, USA: 2009. A guide to the equilibrium contact angles maze; pp. 3–18.

Rupp F., Liang L., Geis-Gerstorfer J., Scheideler L., Hüttig F. Surface characteristics of dental implants: A review. Dent. Mater. 2018;34:40–57. doi: 10.1016/j.dental.2017.09.007. PubMed DOI

Eriksson C., Nygren H., Ohlson K. Implantation of hydrophilic and hydrophobic titanium discs in rat tibia: Cellular reactions on the surfaces during the first 3 weeks in bone. Biomaterials. 2004;25:4759–4766. doi: 10.1016/j.biomaterials.2003.12.006. PubMed DOI

Bornstein M.M., Valderrama P., Jones A.A., Wilson T.G., Seibl R., Cochran D.L. Bone apposition around two different sandblasted and acid-etched titanium implant surfaces: A histomorphometric study in canine mandibles. Clin. Oral Implants Res. 2008;19:233–241. doi: 10.1111/j.1600-0501.2007.01473.x. PubMed DOI

Areid N., Peltola A., Kangasniemi I., Ballo A., Närhi T.O. Effect of ultraviolet light treatment on surface hydrophilicity and human gingival fibroblast response on nanostructured titanium surfaces. Clin. Exp. Dent. Res. 2018;4:78–85. doi: 10.1002/cre2.108. PubMed DOI PMC

Kim T.N., Balakrishnan A., Lee B.C., Kim W.S., Smetana K., Park J.K., Panigrahi B.B. In vitro biocompatibility of equal channel angular processed (ECAP) titanium. Biomed. Mater. 2007;2:S117–S120. doi: 10.1088/1748-6041/2/3/S06. PubMed DOI

Le Guehennec L., Lopez-Heredia M.-A., Enkel B., Weiss P., Amouriq Y., Layrolle P. Osteoblastic cell behaviour on different titanium implant surfaces. Acta Biomater. 2008;4:535–543. doi: 10.1016/j.actbio.2007.12.002. PubMed DOI

van Wachem P.B., Beugeling T., Feijen J., Bantjes A., Detmers J.P., van Aken W.G. Interaction of cultured human endothelial cells with polymeric surfaces of different wettabilities. Biomaterials. 1985;6:403–408. doi: 10.1016/0142-9612(85)90101-2. PubMed DOI

Bacakova L., Filova E., Parizek M., Ruml T., Svorcik V. Modulation of cell adhesion, proliferation and differentiation on materials designed for body implants. Biotechnol. Adv. 2011;29:739–767. doi: 10.1016/j.biotechadv.2011.06.004. PubMed DOI

Webb K., Hlady V., Tresco P.A. Relative importance of surface wettability and charged functional groups on NIH 3T3 fibroblast attachment, spreading, and cytoskeletal organization. J. Biomed. Mater. Res. 1998;41:422–430. doi: 10.1002/(SICI)1097-4636(19980905)41:3<422::AID-JBM12>3.0.CO;2-K. PubMed DOI PMC

Babuska V., Moztarzadeh O., Kubikova T., Moztarzadeh A., Hrusak D., Tonar Z. Evaluating the osseointegration of nanostructured titanium implants in animal models: Current experimental methods and perspectives (Review) Biointerphases. 2016;11:030801. doi: 10.1116/1.4958793. PubMed DOI

Gittens R.A., Scheideler L., Rupp F., Hyzy S.L., Geis-Gerstorfer J., Schwartz Z., Boyan B.D. A review on the wettability of dental implant surfaces II: Biological and clinical aspects. Acta Biomater. 2014;10:2907–2918. doi: 10.1016/j.actbio.2014.03.032. PubMed DOI PMC

In Situ Hydroxyapatite Synthesis Enhances Biocompatibility of PVA/HA Hydrogels

Biological Evaluation of Polyvinyl Alcohol Hydrogels Enriched by Hyaluronic Acid and Hydroxyapatite