Enhanced antibacterial properties of nanomaterials such as TiO2 nanotubes (TNTs) and silver nanoparticles (AgNPs) have attracted much attention in biomedicine and industry. The antibacterial properties of nanoparticles depend, among others, on the functionalization layer of the nanoparticles. However, the more complex information about the influence of different functionalization layers on antibacterial properties of nanoparticle decorated surfaces is still missing. Here we show the array of ∼50 nm diameter TNTs decorated with ∼50 nm AgNPs having different functionalization layers such as polyvinylpyrrolidone, branched polyethyleneimine, citrate, lipoic acid, and polyethylene glycol. To assess the antibacterial properties, the viability of Gram-positive (Staphylococcus aureus) and Gram-negative bacteria (Escherichia coli and Pseudomonas aeruginosa) has been assessed. Our results showed that the functional layer of nanoparticles plays an important role in antibacterial properties and the synergistic effect such nanoparticles and TiO2 nanotubes have had different effects on adhesion and viability of G- and G+ bacteria. These findings could help researchers to optimally design any surfaces to be used as an antibacterial including the implantable titanium biomaterials.

Central European Institute of Technology Brno University of Technology Purkynova 123 Brno Czech Republic

Department of Biochemistry Faculty of Medicine Masaryk University Kamenice 753 5 625 00 Brno Czech Republic

Department of Chemistry and Biochemistry Mendel University in Brno Zemedelska 1 Brno Czech Republic

Department of Microelectronics Brno University of Technology Technicka 10 Brno Czech Republic

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Turner R. J. Metal-based antimicrobial strategies. J. Microb. Biotechnol. 2017;(10):1062–1065. PubMed PMC

Azam A. et al., Antimicrobial activity of metal oxide nanoparticles against Gram-positive and Gram-negative bacteria: a comparative study. Int. J. Nanomed. 2012;(7):6003. PubMed PMC

Różańska A. et al., Antimicrobial properties of selected copper alloys on Staphylococcus Aureus and Escherichia Coli in different simulations of environmental conditions: with vs. without organic contamination. Int. J. Environ. Res. Publ. Health. 2017;(14):813. PubMed PMC

Hasan J. et al., Antibacterial surfaces: the quest for a new generation of biomaterials. Trends Biotechnol. 2013;(31):295–304. PubMed

Lemire J. A. et al., Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat. Rev. Microbiol. 2013;(11):371–384. PubMed

Mahlapuu M. et al., Antimicrobial Peptides: An Emerging Category of Therapeutic Agents. Front. Cell. Infect. Microbiol. 2016;(6) PubMed PMC

Gkana E. N. et al., Anti-adhesion and Anti-biofilm Potential of Organosilane Nanoparticles against Foodborne Pathogens. Front. Microbiol. 2017;(8) PubMed PMC

Kamaruzzaman N. F. et al., Antimicrobial polymers: The potential replacement of existing antibiotics? Int. J. Mol. Sci. 2019;(20):2747. PubMed PMC

Likodimos V. Advanced Photocatalytic Materials. Materials. 2020;(13):821. PubMed PMC

Khezerlou A. et al., Nanoparticles and their antimicrobial properties against pathogens including bacteria, fungi, parasites and viruses. Microb. Pathog. 2018;(123):505526. PubMed

Buzea C. et al., Nanomaterials and nanoparticles: Sources and toxicity. Biointerphases. 2007;(2):MR17–MR71. PubMed

Wu S. et al., Antibacterial Au nanostructured surfaces. Nanoscale. 2016;(8):26202625. PubMed

Seil J. T. Webster T. J. Antimicrobial applications of nanotechnology: methods and literature. Int. J. Nanomed. 2012;(7):2767. PubMed PMC

Mohammadi G. et al., Development of azithromycin–PLGA nanoparticles: Physicochemical characterization and antibacterial effect against Salmonella typhi. Colloids Surf. B Biointerfaces. 2010;(80):34–39. PubMed

Fohlerova Z. Mozalev A. Anodic formation and biomedical properties of hafnium-oxide nanofilms. J. Mater. Chem. B. 2019;(7):2300–2310. PubMed

Tian A. et al., Nanoscale TiO2 nanotubes govern the biological behavior of human glioma and osteosarcoma cells. Int. J. Nanomed. 2015;(10):2423. PubMed PMC

Kummer K. M. et al., Biological applications of anodized TiO2 nanostructures: a review from orthopedic to stent applications. Nanosci. Nanotechnol. Lett. 2012;(4):483–493.

Zhang X. et al., A functionalized Sm/Sr doped TiO2 nanotube array on titanium implant enables exceptional bone-implant integration and also self-antibacterial activity. Ceram. Int. 2020;(46):14796–14807.

Cheng Y. et al., Progress in TiO 2 nanotube coatings for biomedical applications: a review. J. Mater. Chem. B. 2018;(6):1862–1886. PubMed

Mohan C. et al., In vitro hemocompatibility and vascular endothelial cell functionality on titania nanostructures under static and dynamic conditions for improved coronary stenting applications. Acta Biomater. 2013;(9):9568–9577. PubMed

Fohlerova Z. Mozalev A. Tuning the response of osteoblast-like cells to the porousalumina-assisted mixed-oxide nano-mound arrays. J. Biomed. Mater. Res. B Appl. Biomater. 2018;(106):1645–1654. PubMed

Wang Q. et al., TiO2 nanotube platforms for smart drug delivery: a review. Int. J. Nanomed. 2016;(11):4819. PubMed PMC

Zhang H. et al., Improved antibacterial activity and biocompatibility on vancomycin-loaded TiO2 nanotubes: in vivo and in vitro studies. Int. J. Nanomed. 2013;(8):4379. PubMed PMC

Popat K. C. et al., Decreased Staphylococcus epidermis adhesion and increased osteoblast functionality on antibiotic-loaded titania nanotubes. Biomaterials. 2007;(28):4880–4888. PubMed

Zhang X. et al., Synergistic effects of lanthanum and strontium to enhance the osteogenic activity of TiO2 nanotube biological interface. Ceram. Int. 2020;(46):13969–13979.

Li J. et al., Plasmonic gold nanoparticles modified titania nanotubes for antibacterial application. Appl. Phys. Lett. 2014;(104):261110.

Yang T. et al., Cytocompatibility and antibacterial activity of titania nanotubes incorporated with gold nanoparticles. Colloids Surf. B Biointerfaces. 2016;(145):597–606. PubMed

Liu W. et al., Synthesis of TiO 2 nanotubes with ZnO nanoparticles to achieve antibacterial properties and stem cell compatibility. Nanoscale. 2014;(6):9050–9062. PubMed

Bilek O. et al., Enhanced antibacterial and anticancer properties of Se-NPs decorated TiO2 nanotube film. PLoS One. 2019;(14):e0214066. PubMed PMC

Liu W. et al., Selenium nanoparticles incorporated into titania nanotubes inhibit bacterial growth and macrophage proliferation. Nanoscale. 2016;(8):15783–15794. PubMed

Lan M.-Y. et al., Both enhanced biocompatibility and antibacterial activity in Ag-decorated TiO2 nanotubes. PLoS One. 2013;(8):e75364. PubMed PMC

Mei S. et al., Antibacterial effects and biocompatibility of titanium surfaces with graded silver incorporation in titania nanotubes. Biomaterials. 2014;(35):4255–4265. PubMed

Guo Z. et al., Fabrication of silver-incorporated TiO2 nanotubes and evaluation on its antibacterial activity. Mater. Lett. 2014;(137):464–467.

Li H. et al., Antibacterial activity of TiO2 nanotubes: influence of crystal phase, morphology and Ag deposition. Appl. Surf. Sci. 2013;(284):179–183.

Gunputh U. F. et al., Anodised TiO2 nanotubes as a scaffold for antibacterial silver nanoparticles on titanium implants. Mater. Sci. Eng. C. 2018;(91):638644. PubMed

Roguska A. et al., Evaluation of the Antibacterial Activity of Ag-Loaded TiO2 Nanotubes. Eur. J. Inorg. Chem. 2012:5199–5206.

Yeniyol S. et al., Antibacterial activity of As-annealed TiO2 nanotubes doped with Ag nanoparticles against periodontal pathogens. Bioinorgan. Chem. Appl. 2014;(2014):829496. PubMed PMC

Esfandiari N. et al., Size tuning of Ag-decorated TiO2 nanotube arrays for improved bactericidal capacity of orthopedic implants. J. Biomed. Mater. Res. 2014;(102):2625–2635. PubMed

Burkowska-but A. et al., Influence of stabilizers on the antimicrobial properties of silver nanoparticles introduced into natural water. J. Environ. Sci. 2014;(26):542–549. PubMed

van Phu D. et al., Study on antibacterial activity of silver nanoparticles synthesized by gamma irradiation method using different stabilizers. Nanoscale Res. Lett. 2014;(9):162. PubMed PMC

Cinteza L. O. et al., Chitosan-stabilized Ag nanoparticles with superior biocompatibility and their synergistic antibacterial effect in mixtures with essential oils. Nanomaterials. 2018;(8):826. PubMed PMC

Bilek O. et al., Enhanced antibacterial and anticancer properties of Se-NPs decorated TiO2 nanotube film. PLoS One. 2019;(14):e0214066. PubMed PMC

Vazquez-muñoz R. et al., Enhancement of antibiotics antimicrobial activity due to the silver nanoparticles impact on the cell membrane. PLoS One. 2019;(14):e0224904. PubMed PMC

Yin I. X. et al., The Antibacterial Mechanism of Silver Nanoparticles and Its Application in Dentistry. Int. J. Nanomed. 2020;(15):2555–2562. PubMed PMC

Prabhu S. Poulose E. K. Silver nanoparticles: mechanism of antimicrobial action, synthesis, medical applications, and toxicity effects. Int. Nano Lett. 2012;(2):32.

Borowik A. et al., The Impact of Surface Functionalization on the Biophysical Properties of Silver Nanoparticles. Nanomaterials. 2019;(9):973. PubMed PMC

Juhna T. et al., Detection of Escherichia coli in biofilms from pipe samples and coupons in drinking water distribution networks. Appl. Environ. Microbiol. 2007;(73):7456–7464. PubMed PMC

Khatoon Z. et al., Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon. 2018;(4):e01067. PubMed PMC

Stocks S. M. Mechanism and use of the commercially available viability stain. BacLight. 2004;(61A):189–195. PubMed

Rosenberg M. et al., Propidium iodide staining underestimates viability of adherent bacterial cells. Sci. Rep. 2019;(9):6483. PubMed PMC

Ercan B. et al., Diameter of titanium nanotubes influences anti-bacterial efficacy. Nanotechnology. 2011;(22):295102. PubMed

Mazare A. et al., Corrosion, antibacterial activity and haemocompatibility of TiO2 nanotubes as a function of their annealing temperature. Corros. Sci. 2016;(103):215–222.

Huynh K. A. Chen K. L. Aggregation kinetics of citrate and polyvinylpyrrolidone coated silver nanoparticles in monovalent and divalent electrolyte solutions. Environ. Sci. Technol. 2011;(45):5564–5571. PubMed PMC

Qiao Z. et al., Silver nanoparticles with pH induced surface charge switchable properties for antibacterial and antibiofilm applications. J. Mater. Chem. B. 2019;(7):830–840. PubMed

Niska K. et al., Capping Agent-Dependent Toxicity and Antimicrobial Activity of Silver Nanoparticles: An In Vitro Study. Concerns about Potential Application in Dental Practice. Int. J. Med. Sci. 2016;(13):772–782. PubMed PMC

van Doorslaer X. et al., UV-A and UV-C induced photolytic and photocatalytic degradation of aqueous ciprofloxacin and moxifloxacin: Reaction kinetics and role of adsorption. Appl. Catal. B Environ. 2011;(101):540–547.

Crémet L. et al., Orthopaedic-implant infections by Escherichia coli: Molecular and phenotypic analysis of the causative strains. J. Infect. 2012;(64):169–175. PubMed

Maurice N. M. et al., Pseudomonas aeruginosa Biofilms: Host Response and Clinical Implications in Lung Infections. Am. J. Respir. Cell Mol. Biol. 2018;(58):428–439. PubMed PMC

Hunt P. R. et al., Bioactivity of nanosilver in Caenorhabditis elegans: Effects of size, coat, and shape. Toxicol. Rep. 2014;(1):923–944. PubMed PMC

Vasilev K. Nanoengineered antibacterial coatings and materials: A perspective. Coatings. 2019;9:654.

Lister J. L. Horswill A. R. Staphylococcus aureus biofilms: recent developments in biofilm dispersal. Front. Cell. Infect. Microbiol. 2014;(4):178. PubMed PMC

Modifications of Parylene by Microstructures and Selenium Nanoparticles: Evaluation of Bacterial and Mesenchymal Stem Cell Viability