Osseointegration Properties of Titanium Implants Treated by Nonthermal Atmospheric-Pressure Nitrogen Plasma

Pure titanium is used in dental implants owing to its excellent biocompatibility and physical properties. However, the aging of the material during storage is detrimental to the long-term stability of the implant after implantation. Therefore, in this study, we attempted to improve the surface properties and circumvent the negative effects of material aging on titanium implants by using a portable handheld nonthermal plasma device capable of piezoelectric direct discharge to treat pure titanium discs with nitrogen gas. We evaluated the osteogenic properties of the treated samples by surface morphology and elemental analyses, as well as in vitro and in vivo experiments. The results showed that nonthermal atmospheric-pressure nitrogen plasma can improve the hydrophilicity of pure titanium without damaging its surface morphology while introducing nitrogen-containing functional groups, thereby promoting cell attachment, proliferation, and osseointegration to some extent. Therefore, nitrogen plasma treatment may be a promising method for the rapid surface treatment of titanium implants.

[1]  Cheng Lu,et al.  Comparing medium pressure dielectric barrier discharge (DBD) plasmas and classic methods of surface cleaning/activation of pure Mg for biomedical applications , 2021 .

[2]  S. Nettesheim,et al.  Atmospheric pressure plasma jet powered by piezoelectric direct discharge , 2020, Plasma Processes and Polymers.

[3]  F. Khan,et al.  Ultraviolet Photodetection Based on High-Performance Co-Plus-Ni Doped ZnO Nanorods Grown by Hydrothermal Method on Transparent Plastic Substrate , 2020, Nanomaterials.

[4]  C. Aparicio,et al.  Nano-scale modification of titanium implant surfaces to enhance osseointegration. , 2019, Acta biomaterialia.

[5]  Daiga Ujino,et al.  Effect of Plasma Treatment of Titanium Surface on Biocompatibility , 2019, Applied Sciences.

[6]  C. Canal,et al.  The effect of low temperature atmospheric nitrogen plasma on MC3T3-E1 preosteoblast proliferation and differentiation in vitro , 2019, Journal of Physics D: Applied Physics.

[7]  G. Schmidmaier,et al.  Insulin-Like Growth Factor-1 as a Possible Alternative to Bone Morphogenetic Protein-7 to Induce Osteogenic Differentiation of Human Mesenchymal Stem Cells in Vitro , 2018, International journal of molecular sciences.

[8]  M. Asadian,et al.  Surface Treatment of PEOT/PBT (55/45) with a Dielectric Barrier Discharge in Air, Helium, Argon and Nitrogen at Medium Pressure , 2018, Materials.

[9]  H. Sies On the history of oxidative stress: Concept and some aspects of current development , 2018 .

[10]  Jue Zhang,et al.  A novel cold atmospheric pressure air plasma jet for peri-implantitis treatment: An in vitro study. , 2018, Dental materials journal.

[11]  W. Zhu,et al.  Silicon nitride surface chemistry: A potent regulator of mesenchymal progenitor cell activity in bone formation , 2017 .

[12]  Shiqiang Chen,et al.  Nanopatterning of steel by one-step anodization for anti-adhesion of bacteria , 2017, Scientific Reports.

[13]  W. Teughels,et al.  Synergistic interactions between corrosion and wear at titanium‐based dental implant connections: A scoping review , 2017, Journal of periodontal research.

[14]  Luyuan Chen,et al.  Synergistic effect of nanotopography and bioactive ions on peri-implant bone response , 2017, International journal of nanomedicine.

[15]  H. Sies Hydrogen peroxide as a central redox signaling molecule in physiological oxidative stress: Oxidative eustress☆ , 2017, Redox biology.

[16]  E. Choi,et al.  Time-dependent effects of ultraviolet and nonthermal atmospheric pressure plasma on the biological activity of titanium , 2016, Scientific Reports.

[17]  Mingqiang Li,et al.  Enhanced osteoblast adhesion on amino-functionalized titanium surfaces through combined plasma enhanced chemical vapor deposition (PECVD) method , 2016 .

[18]  M. Marcacci,et al.  Magnetic hydroxyapatite coatings as a new tool in medicine: A scanning probe investigation. , 2016, Materials science & engineering. C, Materials for biological applications.

[19]  A. Dejneka,et al.  The interplay between biological and physical scenarios of bacterial death induced by non-thermal plasma. , 2016, Biomaterials.

[20]  J. Liu,et al.  Enhanced cytocompatibility of silver-containing biointerface by constructing nitrogen functionalities , 2015 .

[21]  Paulo G Coelho,et al.  Assessment of Atmospheric Pressure Plasma Treatment for Implant Osseointegration , 2015, BioMed research international.

[22]  J. Yi,et al.  Ultraviolet irradiation enhanced bioactivity and biological response of mesenchymal stem cells on micro-arc oxidized titanium surfaces. , 2015, Dental materials journal.

[23]  S. L. Barbosa,et al.  How do titanium and Ti6Al4V corrode in fluoridated medium as found in the oral cavity? An in vitro study. , 2015, Materials science & engineering. C, Materials for biological applications.

[24]  Hideyuki Sakoda,et al.  Effect of surface roughness of biomaterials on Staphylococcus epidermidis adhesion , 2014, BMC Microbiology.

[25]  D. Egan,et al.  In vitro induction of alkaline phosphatase levels predicts in vivo bone forming capacity of human bone marrow stromal cells. , 2014, Stem cell research.

[26]  S. Kawata,et al.  In situ Raman imaging of osteoblastic mineralization , 2014 .

[27]  E. Pamuła,et al.  Increased reactivity and in vitro cell response of titanium based implant surfaces after anodic oxidation , 2013, Journal of Materials Science: Materials in Medicine.

[28]  E. Choi,et al.  The effects of non-thermal atmospheric pressure plasma jet on cellular activity at SLA-treated titanium surfaces , 2013 .

[29]  Yuquan Wei,et al.  Redox homeostasis: the linchpin in stem cell self-renewal and differentiation , 2013, Cell Death and Disease.

[30]  N. Keller,et al.  Chemistry of NOx on TiO2 Surfaces Studied by Ambient Pressure XPS: Products, Effect of UV Irradiation, Water, and Coadsorbed K(.). , 2013, The journal of physical chemistry letters.

[31]  P. Coelho,et al.  Plasma Treatment Maintains Surface Energy of the Implant Surface and Enhances Osseointegration , 2013, International journal of biomaterials.

[32]  Masahiro Tanaka,et al.  Bioactivity of nanostructure on titanium surface modified by chemical processing at room temperature. , 2012, Journal of prosthodontic research.

[33]  Lauren R. Clements,et al.  Assessing embryonic stem cell response to surface chemistry using plasma polymer gradients. , 2012, Acta biomaterialia.

[34]  B. Nebe,et al.  Atmospheric plasma enhances wettability and cell spreading on dental implant metals. , 2012, Journal of clinical periodontology.

[35]  T. Hanawa A comprehensive review of techniques for biofunctionalization of titanium , 2011, Journal of periodontal & implant science.

[36]  I. Turkyilmaz Implant Dentistry - A Rapidly Evolving Practice , 2011 .

[37]  T. Dufour,et al.  Long-term implant survival and success: a 10-16-year follow-up of non-submerged dental implants. , 2010, Clinical oral implants research.

[38]  Y. Sugita,et al.  Nonvolatile buffer coating of titanium to prevent its biological aging and for drug delivery. , 2010, Biomaterials.

[39]  A. Clyne,et al.  Endothelial Cell Proliferation is Enhanced by Low Dose Non-Thermal Plasma Through Fibroblast Growth Factor-2 Release , 2010, Annals of Biomedical Engineering.

[40]  Yang Yang,et al.  Time-dependent degradation of titanium osteoconductivity: an implication of biological aging of implant materials. , 2009, Biomaterials.

[41]  A. Singh,et al.  Ti based biomaterials, the ultimate choice for orthopaedic implants – A review , 2009 .

[42]  M. Anpo,et al.  The effect of ultraviolet functionalization of titanium on integration with bone. , 2009, Biomaterials.

[43]  P. Layrolle,et al.  Osteoblastic cell behaviour on different titanium implant surfaces. , 2008, Acta biomaterialia.

[44]  P. Layrolle,et al.  Surface treatments of titanium dental implants for rapid osseointegration. , 2007, Dental materials : official publication of the Academy of Dental Materials.

[45]  P. Favia,et al.  Plasma‐Treated Nitrogen‐Containing Surfaces for Cell Adhesion: The Role of the Polymeric Substrate , 2007 .

[46]  M. Mozetič,et al.  XPS study of the deposited Ti layer in a magnetron-type sputter ion pump , 2006 .

[47]  S. Pollack,et al.  Fibroblast growth factor 2 induced proliferation in osteoblasts and bone marrow stromal cells: a whole cell model. , 2006, Biophysical journal.

[48]  Z. Gugala,et al.  Attachment, growth, and activity of rat osteoblasts on polylactide membranes treated with various low-temperature radiofrequency plasmas. , 2006, Journal of biomedical materials research. Part A.

[49]  T. Tatsuma,et al.  Photocatalytic remote oxidation with various photocatalysts and enhancement of its activity , 2005 .

[50]  Tatsuya Kobayashi,et al.  Minireview: transcriptional regulation in development of bone. , 2005, Endocrinology.

[51]  P. Chu,et al.  Surface modification of titanium, titanium alloys, and related materials for biomedical applications , 2004 .

[52]  J. Weng,et al.  Characterization of surface oxide films on titanium and adhesion of osteoblast. , 2003, Biomaterials.

[53]  J. Pou,et al.  Micro- and nano-testing of calcium phosphate coatings produced by pulsed laser deposition. , 2003, Biomaterials.

[54]  A. J. Wagner,et al.  A Comparison of PE Surfaces Modified by Plasma Generated Neutral Nitrogen Species and Nitrogen Ions , 2003 .

[55]  Niklaus P Lang,et al.  De novo alveolar bone formation adjacent to endosseous implants. , 2003, Clinical oral implants research.

[56]  G. C. Allen,et al.  Photocatalytic oxidation of NOx gases using TiO2: a surface spectroscopic approach. , 2002, Environmental pollution.

[57]  Junying Chen,et al.  Plasma-surface modification of biomaterials , 2002 .

[58]  S. Hayakawa,et al.  Bioactive titania-gel layers formed by chemical treatment of Ti substrate with a H2O2/HCl solution. , 2002, Biomaterials.

[59]  Kozo Nakamura,et al.  Regulation of Osteoblast, Chondrocyte, and Osteoclast Functions by Fibroblast Growth Factor (FGF)-18 in Comparison with FGF-2 and FGF-10* , 2002, The Journal of Biological Chemistry.

[60]  Larry L Hench,et al.  Third-Generation Biomedical Materials , 2002, Science.

[61]  Kozo Nakamura,et al.  Regulation of Osteoclast Differentiation by Fibroblast Growth Factor 2: Stimulation of Receptor Activator of Nuclear Factor κB Ligand/Osteoclast Differentiation Factor Expression in Osteoblasts and Inhibition of Macrophage Colony‐Stimulating Factor Function in Osteoclast Precursors , 2001, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[62]  S. Moreau,et al.  Low-temperature sterilization using gas plasmas: a review of the experiments and an analysis of the inactivation mechanisms. , 2001, International journal of pharmaceutics.

[63]  C. Stanford,et al.  Osteoblast Integrin Adhesion and Signaling Regulate Mineralization , 2001, Journal of dental research.

[64]  N. Huang,et al.  Third-generation plasma immersion ion implanter for biomedical materials and research , 2001 .

[65]  J. Jacobs,et al.  Evaluation of metallic and polymeric biomaterial surface energy and surface roughness characteristics for directed cell adhesion. , 2001, Tissue engineering.

[66]  M. McKee,et al.  Chemical modification of titanium surfaces for covalent attachment of biological molecules. , 1998, Journal of biomedical materials research.

[67]  D. Brewis Plasma surface modification , 1997 .

[68]  R. C. King,et al.  Handbook of X Ray Photoelectron Spectroscopy: A Reference Book of Standard Spectra for Identification and Interpretation of Xps Data , 1995 .

[69]  Håkan Mattsson,et al.  Surface spectroscopic characterization of titanium implant materials , 1990 .

[70]  L. N. Wu,et al.  Correlation between loss of alkaline phosphatase activity and accumulation of calcium during matrix vesicle-mediated mineralization. , 1988, The Journal of biological chemistry.

[71]  D. H. Kaelble,et al.  Dispersion-Polar Surface Tension Properties of Organic Solids , 1970 .

[72]  J. Jansen,et al.  Dental Implant Surface Enhancement and Osseointegration , 2011 .

[73]  J. Souza,et al.  Tribocorrosion and bio-tribocorrosion in the oral environment : the case of dental implants , 2011 .

[74]  O. Trubiani,et al.  Nitric oxide production during the osteogenic differentiation of human periodontal ligament mesenchymal stem cells. , 2009, Acta histochemica.

[75]  C. Werner,et al.  Surface modification of poly(hydroxybutyrate) films to control cell-matrix adhesion. , 2007, Biomaterials.

[76]  Sandra Downes,et al.  Protein adsorption and human osteoblast-like cell attachment and growth on alkylthiol on gold self-assembled monolayers. , 2002, Journal of biomedical materials research.

[77]  J. Davies,et al.  Mechanisms of endosseous integration. , 1998, The International journal of prosthodontics.