Insight into antibacterial effect of titanium nanotubular surfaces with focus on Staphylococcus aureus and Pseudomonas aeruginosa
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
GA20-11321S
Grantová Agentura České Republiky
PubMed
39068252
PubMed Central
PMC11283573
DOI
10.1038/s41598-024-68266-1
PII: 10.1038/s41598-024-68266-1
Knihovny.cz E-zdroje
- Klíčová slova
- Anodization, Bacterial behavior, Diameter, Nanotubes, Roughness, Ti ion release, Titanium,
- MeSH
- antibakteriální látky * farmakologie chemie MeSH
- biofilmy účinky léků růst a vývoj MeSH
- lidé MeSH
- mikrobiální testy citlivosti MeSH
- nanotrubičky * chemie MeSH
- povrchové vlastnosti * MeSH
- Pseudomonas aeruginosa * účinky léků MeSH
- Staphylococcus aureus * účinky léků MeSH
- titan * chemie farmakologie MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- antibakteriální látky * MeSH
- titan * MeSH
Materials used for orthopedic implants should not only have physical properties close to those of bones, durability and biocompatibility, but should also exhibit a sufficient degree of antibacterial functionality. Due to its excellent properties, titanium is still a widely used material for production of orthopedic implants, but the unmodified material exhibits poor antibacterial activity. In this work, the physicochemical characteristics, such as chemical composition, crystallinity, wettability, roughness, and release of Ti ions of the titanium surface modified with nanotubular layers were analyzed and its antibacterial activity against two biofilm-forming bacterial strains responsible for prosthetic joint infection (Staphylococcus aureus and Pseudomonas aeruginosa) was investigated. Electrochemical anodization (anodic oxidation) was used to prepare two types of nanotubular arrays with nanotubes differing in dimensions (with diameters of 73 and 118 nm and lengths of 572 and 343 nm, respectively). These two surface types showed similar chemistry, crystallinity, and surface energy. The surface with smaller nanotube diameter (TNT-73) but larger values of roughness parameters was more effective against S. aureus. For P. aeruginosa the sample with a larger nanotube diameter (TNT-118) had better antibacterial effect with proven cell lysis. Antibacterial properties of titanium nanotubular surfaces with potential in implantology, which in our previous work demonstrated a positive effect on the behavior of human gingival fibroblasts, were investigated in terms of surface parameters. The interplay between nanotube diameter and roughness appeared critical for the bacterial fate on nanotubular surfaces. The relationship of nanotube diameter, values of roughness parameters, and other surface properties to bacterial behavior is discussed in detail. The study is believed to shed more light on how nanotubular surface parameters and their interplay affect antibacterial activity.
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VanEpps, J. S. & Younger, J. G. Implantable device-related infection. Shock46, 597–608 (2016). 10.1097/SHK.0000000000000692 PubMed DOI PMC
Esteban, J. & Gómez-Barrena, E. An update about molecular biology techniques to detect orthopaedic implant-related infections. EFORT Open Rev.6, 93–100 (2021). 10.1302/2058-5241.6.200118 PubMed DOI PMC
Cyphert, E. L., Zhang, N., Learn, G. D., Hernandez, C. J. & von Recum, H. A. Recent advances in the evaluation of antimicrobial materials for resolution of orthopedic implant-associated infections in vivo. ACS Infect. Dis.7, 3125–3160 (2021). 10.1021/acsinfecdis.1c00465 PubMed DOI PMC
Natsuhara, K. M., Shelton, T. J., Meehan, J. P. & Lum, Z. C. Mortality during total hip periprosthetic joint infection. J. Arthroplasty34, S337–S342 (2019). 10.1016/j.arth.2018.12.024 PubMed DOI
Drain, N. P. et al. High mortality after total knee arthroplasty periprosthetic joint infection is related to preoperative morbidity and the disease process but not treatment. J. Arthroplasty37, 1383–1389 (2022). 10.1016/j.arth.2022.03.046 PubMed DOI
Fischbacher, A. & Borens, O. Prosthetic-joint Infections: Mortality over the last 10 years. J. Bone Jt. Infect.4, 198–202 (2019). 10.7150/jbji.35428 PubMed DOI PMC
Pirisi, L., Pennestrì, F., Viganò, M. & Banfi, G. Prevalence and burden of orthopaedic implantable-device infections in Italy: A hospital-based national study. BMC Infect. Dis.20, 337 (2020). 10.1186/s12879-020-05065-9 PubMed DOI PMC
Mponponsuo, K. et al. Economic burden of surgical management of prosthetic joint infections following hip and knee replacements in Alberta, Canada: An analysis and comparison of two major urban centers. J. Hosp. Infect.S0195–6701(22), 00132–00133 (2022). PubMed
Premkumar, A. et al. Projected economic burden of periprosthetic joint infection of the hip and knee in the United States. J. Arthroplasty36, 1484-1489.e3 (2021). 10.1016/j.arth.2020.12.005 PubMed DOI
Shichman, I. et al. Projections and epidemiology of primary hip and knee arthroplasty in medicare patients to 2040–2060. JB JS Open Access8, e22.00112 (2023). PubMed PMC
Matsuoka, H., Nanmo, H., Nojiri, S., Nagao, M. & Nishizaki, Y. Projected numbers of knee and hip arthroplasties up to the year 2030 in Japan. J. Orthop. Sci.28, 161–166 (2023). 10.1016/j.jos.2021.09.002 PubMed DOI
Blüher, M. Obesity: Global epidemiology and pathogenesis. Nat. Rev. Endocrinol.15, 288–298 (2019). 10.1038/s41574-019-0176-8 PubMed DOI
Powell, A., Teichtahl, A. J., Wluka, A. E. & Cicuttini, F. M. Obesity: A preventable risk factor for large joint osteoarthritis which may act through biomechanical factors. Br. J. Sports Med.39, 4–5 (2005). 10.1136/bjsm.2004.011841 PubMed DOI PMC
Hernigou, P. & Scarlat, M. M. Growth in musculoskeletal pathology worldwide: The role of Société Internationale de Chirurgie Orthopédique et de Traumatologie and publications. Int. Orthop.46, 1913–1920 (2022). 10.1007/s00264-022-05512-z PubMed DOI
Izakovicova, P., Borens, O. & Trampuz, A. Periprosthetic joint infection: Current concepts and outlook. EFORT Open Rev.4, 482–494 (2019). 10.1302/2058-5241.4.180092 PubMed DOI PMC
Rakow, A., Perka, C., Trampuz, A. & Renz, N. Origin and characteristics of haematogenous periprosthetic joint infection. Clin. Microbiol. Infect.25, 845–850 (2019). 10.1016/j.cmi.2018.10.010 PubMed DOI
Staats, A., Li, D., Sullivan, A. C. & Stoodley, P. Biofilm formation in periprosthetic joint infections. Ann. Jt.6, 43 (2021). 10.21037/aoj-20-85 PubMed DOI PMC
Davidson, D. J., Spratt, D. & Liddle, A. D. Implant materials and prosthetic joint infection: The battle with the biofilm. EFORT Open Rev.4, 633–639 (2019). 10.1302/2058-5241.4.180095 PubMed DOI PMC
Visperas, A., Santana, D., Klika, A. K., Higuera-Rueda, C. A. & Piuzzi, N. S. Current treatments for biofilm-associated periprosthetic joint infection and new potential strategies. J. Orthop. Res.40, 1477–1491 (2022). 10.1002/jor.25345 PubMed DOI PMC
Peng, H.-M. et al. Microbiology of periprosthetic hip and knee infections in surgically revised cases from 34 centers in Mainland China. Infect. Drug Resist.14, 2411–2418 (2021). 10.2147/IDR.S305205 PubMed DOI PMC
Benito, N. et al. The different microbial etiology of prosthetic joint infections according to route of acquisition and time after prosthesis implantation, including the role of multidrug-resistant organisms. J. Clin. Med.8, 673 (2019). 10.3390/jcm8050673 PubMed DOI PMC
Fröschen, F. S., Randau, T. M., Franz, A., Molitor, E. & Hischebeth, G. T. R. Microbiological profiles of patients with periprosthetic joint infection of the hip or knee. Diagnostics12, 1654 (2022). 10.3390/diagnostics12071654 PubMed DOI PMC
Papalini, C. et al. Prosthetic joint infection diagnosis applying the three-level European Bone and Joint Infection Society (EBJIS) approach. Eur. J. Clin. Microbiol. Infect. Dis.41, 771–778 (2022). 10.1007/s10096-022-04410-x PubMed DOI PMC
Arciola, C. R., Campoccia, D. & Montanaro, L. Implant infections: Adhesion, biofilm formation and immune evasion. Nat. Rev. Microbiol.16, 397–409 (2018). 10.1038/s41579-018-0019-y PubMed DOI
Seebach, E. & Kubatzky, K. F. Chronic implant-related bone infections—Can immune modulation be a therapeutic strategy?. Front. Immunol.10, 1724 (2019). 10.3389/fimmu.2019.01724 PubMed DOI PMC
Shiels, S. M., Mangum, L. H. & Wenke, J. C. Revisiting the “race for the surface” in a pre-clinical model of implant infection. Eur. Cell Mater.39, 77–95 (2020). 10.22203/eCM.v039a05 PubMed DOI
Chu, L. et al. Preferential colonization of osteoblasts over co-cultured bacteria on a bifunctional biomaterial surface. Front. Microbiol.9, 2219 (2018). 10.3389/fmicb.2018.02219 PubMed DOI PMC
Gobbi, S. J., Gobbi, V. J. & Rocha, Y. Requirements for selection/development of a biomaterial. Biomed. J. Sci. Tech. Res.14, 10674–10679 (2019).
Huzum, B. et al. Biocompatibility assessment of biomaterials used in orthopedic devices: An overview (Review). Exp. Ther. Med.22, 1315 (2021). 10.3892/etm.2021.10750 PubMed DOI PMC
Ma, C., Du, T., Niu, X. & Fan, Y. Biomechanics and mechanobiology of the bone matrix. Bone Res.10, 59 (2022). 10.1038/s41413-022-00223-y PubMed DOI PMC
Bohara, S. & Suthakorn, J. Surface coating of orthopedic implant to enhance the osseointegration and reduction of bacterial colonization: A review. Biomater. Res.26, 26 (2022). 10.1186/s40824-022-00269-3 PubMed DOI PMC
Han, X. et al. Surface modification techniques of titanium and titanium alloys for biomedical orthopaedics applications: A review. Colloids Surf. B: Biointerfaces227, 113339 (2023). 10.1016/j.colsurfb.2023.113339 PubMed DOI
Zhu, G., Wang, G. & Li, J. J. Advances in implant surface modifications to improve osseointegration. Mater. Adv.2, 6901–6927 (2021).10.1039/D1MA00675D DOI
Uneputty, A. et al. Strategies applied to modify structured and smooth surfaces: A step closer to reduce bacterial adhesion and biofilm formation. Colloid Interface Sci. Commun.46, 100560 (2022).10.1016/j.colcom.2021.100560 DOI
Zhang, L. et al. Infection-responsive long-term antibacterial bone plates for open fracture therapy. Bioact. Mater.25, 1–12 (2023). PubMed PMC
Sun, T. et al. Simvastatin-hydroxyapatite coatings prevent biofilm formation and improve bone formation in implant-associated infections. Bioact. Mater.21, 44–56 (2023). PubMed PMC
Chopra, D., Gulati, K. & Ivanovski, S. Understanding and optimizing the antibacterial functions of anodized nano-engineered titanium implants. Acta Biomater.127, 80–101 (2021). 10.1016/j.actbio.2021.03.027 PubMed DOI
Ge, X. et al. Cicada-inspired fluoridated hydroxyapatite nanostructured surfaces synthesized by electrochemical additive manufacturing. Mater. Des.193, 108790 (2020).10.1016/j.matdes.2020.108790 DOI
Jenkins, J. et al. Antibacterial effects of nanopillar surfaces are mediated by cell impedance, penetration and induction of oxidative stress. Nat. Commun.11, 1626 (2020). 10.1038/s41467-020-15471-x PubMed DOI PMC
Ge, X. et al. Bacterial responses to periodic micropillar array: Bacterial responses to periodic micropillar array. J. Biomed. Mater. Res.103, 384–396 (2015).10.1002/jbm.a.35182 PubMed DOI
Ge, X. et al. Micro/nano-structured TiO2 surface with dual-functional antibacterial effects for biomedical applications. Bioact. Mater.4, 346–357 (2019). PubMed PMC
Georgakopoulos-Soares, I., Papazoglou, E. L., Karmiris-Obratański, P., Karkalos, N. E. & Markopoulos, A. P. Surface antibacterial properties enhanced through engineered textures and surface roughness: A review. Colloids Surf. B: Biointerfaces231, 113584 (2023). 10.1016/j.colsurfb.2023.113584 PubMed DOI
Linklater, D. P. et al. High aspect ratio nanostructures kill bacteria via storage and release of mechanical energy. ACS Nano12, 6657–6667 (2018). 10.1021/acsnano.8b01665 PubMed DOI
Sarraf, M., Rezvani Ghomi, E., Alipour, S., Ramakrishna, S. & Liana, S. N. A state-of-the-art review of the fabrication and characteristics of titanium and its alloys for biomedical applications. Bio-des Manuf.5, 371–395 (2022).10.1007/s42242-021-00170-3 PubMed DOI PMC
Szczęsny, G. et al. A review on biomaterials for orthopaedic surgery and traumatology: From past to present. Materials15, 3622 (2022). 10.3390/ma15103622 PubMed DOI PMC
Kaur, M. & Singh, K. Review on titanium and titanium based alloys as biomaterials for orthopaedic applications. Mater. Sci. Eng. C.102, 844–862 (2019).10.1016/j.msec.2019.04.064 PubMed DOI
Kim, K. T., Eo, M. Y., Nguyen, T. T. H. & Kim, S. M. General review of titanium toxicity. Int. J. Implant Dent.5, 10 (2019). 10.1186/s40729-019-0162-x PubMed DOI PMC
Hanawa, T. Titanium-tissue interface reaction and its control with surface treatment. Front. Bioeng. Biotechnol.7, 170 (2019). 10.3389/fbioe.2019.00170 PubMed DOI PMC
Wu, B., Tang, Y., Wang, K., Zhou, X. & Xiang, L. Nanostructured titanium implant surface facilitating osseointegration from protein adsorption to osteogenesis: The example of TiO2 NTAs. IJN17, 1865–1879 (2022). 10.2147/IJN.S362720 PubMed DOI PMC
Su, E. P. et al. Effects of titanium nanotubes on the osseointegration, cell differentiation, mineralisation and antibacterial properties of orthopaedic implant surfaces. Bone Jt. J.100-B, 9–16 (2018).10.1302/0301-620X.100B1.BJJ-2017-0551.R1 PubMed DOI PMC
Zheng, S. et al. Implication of surface properties, bacterial motility, and hydrodynamic conditions on bacterial surface sensing and their initial adhesion. Front. Bioeng. Biotechnol.9, 643722 (2021). 10.3389/fbioe.2021.643722 PubMed DOI PMC
Zhai, S. et al. Overview of strategies to improve the antibacterial property of dental implants. Front. Bioeng. Biotechnol.11, 1267128 (2023). 10.3389/fbioe.2023.1267128 PubMed DOI PMC
Singhatanadgit, W., Toso, M., Pratheepsawangwong, B., Pimpin, A. & Srituravanich, W. Titanium dioxide nanotubes of defined diameter enhance mesenchymal stem cell proliferation via JNK- and ERK-dependent up-regulation of fibroblast growth factor-2 by T lymphocytes. J. Biomater. Appl.33, 997–1010 (2019). 10.1177/0885328218816565 PubMed DOI
Oh, S. et al. Stem cell fate dictated solely by altered nanotube dimension. Proc. Natl. Acad. Sci. USA106, 2130–2135 (2009). 10.1073/pnas.0813200106 PubMed DOI PMC
Voltrova, B. et al. Different diameters of titanium dioxide nanotubes modulate Saos-2 osteoblast-like cell adhesion and osteogenic differentiation and nanomechanical properties of the surface. RSC Adv.9, 11341–11355 (2019). 10.1039/C9RA00761J PubMed DOI PMC
Wang, F., Li, C., Zhang, S. & Liu, H. Role of TiO2 nanotubes on the surface of implants in osseointegration in animal models: A systematic review and meta-analysis. J. Prosthodont.29, 501–510 (2020). 10.1111/jopr.13163 PubMed DOI
Wang, N. et al. Effects of TiO2 nanotubes with different diameters on gene expression and osseointegration of implants in minipigs. Biomaterials32, 6900–6911 (2011). 10.1016/j.biomaterials.2011.06.023 PubMed DOI
Lv, L. et al. The nanoscale geometry of TiO2 nanotubes influences the osteogenic differentiation of human adipose-derived stem cells by modulating H3K4 trimethylation. Biomaterials39, 193–205 (2015). 10.1016/j.biomaterials.2014.11.002 PubMed DOI
Alves-Rezende, M. C. R. et al. The role of TiO2 nanotube surface on osseointegration of titanium implants: Biomechanical and histological study in rats. Microscopy Res. Tech.83, 817–823 (2020).10.1002/jemt.23473 PubMed DOI
Sterzenbach, T., Helbig, R., Hannig, C. & Hannig, M. Bioadhesion in the oral cavity and approaches for biofilm management by surface modifications. Clin. Oral Invest.24, 4237–4260 (2020).10.1007/s00784-020-03646-1 PubMed DOI PMC
Verran, J., Packer, A., Kelly, P. J. & Whitehead, K. A. Use of the atomic force microscope to determine the strength of bacterial attachment to grooved surface features. J. Adhes. Sci. Technol.24, 2271–2285 (2010).10.1163/016942410X508019 DOI
Crawford, R. J., Webb, H. K., Truong, V. K., Hasan, J. & Ivanova, E. P. Surface topographical factors influencing bacterial attachment. Adv. Colloid Interface Sci.179–182, 142–149 (2012). 10.1016/j.cis.2012.06.015 PubMed DOI
Wu, S., Zhang, B., Liu, Y., Suo, X. & Li, H. Influence of surface topography on bacterial adhesion: A review (Review). Biointerphases13, 060801 (2018). 10.1116/1.5054057 PubMed DOI
Wassmann, T., Kreis, S., Behr, M. & Buergers, R. The influence of surface texture and wettability on initial bacterial adhesion on titanium and zirconium oxide dental implants. Int. J. Implant Dent.3, 32 (2017). 10.1186/s40729-017-0093-3 PubMed DOI PMC
Kingsak, M., Maturavongsadit, P., Jiang, H. & Wang, Q. Cellular responses to nanoscale substrate topography of TiO2 nanotube arrays: Cell morphology and adhesion. Biomater. Transl.3, 221–233 (2022). PubMed PMC
Kummer, K. M. et al. Effects of different sterilization techniques and varying anodized TiO2 nanotube dimensions on bacteria growth. J. Biomed. Mater. Res.101B, 677–688 (2013).10.1002/jbm.b.32870 PubMed DOI
Stolzoff, M. et al. Decreased bacterial growth on titanium nanoscale topographies created by ion beam assisted evaporation. IJN12, 1161–1169 (2017). 10.2147/IJN.S119750 PubMed DOI PMC
Sbricoli, L. et al. Bacterial adhesion to grade 4 and grade 5 turned and mildly acid-etched titanium implant surfaces: An in vitro and ex vivo study. Appl. Sci.11, 7185 (2021).10.3390/app11167185 DOI
Fu, Y. & Mo, A. A review on the electrochemically self-organized titania nanotube arrays: Synthesis, modifications, and biomedical applications. Nanoscale Res. Lett.13, 187 (2018). 10.1186/s11671-018-2597-z PubMed DOI PMC
Zakir, O. et al. A review on TiO2 nanotubes: Synthesis strategies, modifications, and applications. J. Solid State Electrochem.27, 2289–2307 (2023).10.1007/s10008-023-05538-2 DOI
Khudhair, D. et al. Anodization parameters influencing the morphology and electrical properties of TiO2 nanotubes for living cell interfacing and investigations. Mater. Sci. Eng.: C59, 1125–1142 (2016).10.1016/j.msec.2015.10.042 PubMed DOI
Aguirre Ocampo, R. et al. Effect of surface characteristics on the antibacterial properties of titanium dioxide nanotubes produced in aqueous electrolytes with carboxymethyl cellulose. J. Biomed. Mater. Res.109, 104–121 (2021).10.1002/jbm.a.37010 PubMed DOI
Vrchovecká, K., Kuta, J., Uher, M., Přibyl, J. & Pávková, G. M. Effect of titanium nanostructured surface on fibroblast behavior. J. Biomed. Mater. Res.111, 1333–1343 (2023).10.1002/jbm.a.37531 PubMed DOI
Vrchovecká, K. et al. A release of Ti-ions from nanostructured titanium oxide surfaces. Surf. Interfaces29, 101699 (2022).10.1016/j.surfin.2021.101699 DOI
Pesode, P. A. & Barve, S. B. Recent advances on the antibacterial coating on titanium implant by micro-Arc oxidation process. Mater. Today: Proc.47, 5652–5662 (2021).
Liu, J. et al. Nano-modified titanium implant materials: A way toward improved antibacterial properties. Front. Bioeng. Biotechnol.8, 576969 (2020). 10.3389/fbioe.2020.576969 PubMed DOI PMC
Li, Y. et al. Enhanced antibacterial properties of orthopedic implants by titanium nanotube surface modification: A review of current techniques. IJN14, 7217–7236 (2019). 10.2147/IJN.S216175 PubMed DOI PMC
Ivanova, E. P. et al. Impact of nanoscale roughness of titanium thin film surfaces on bacterial retention. Langmuir26, 1973–1982 (2010). 10.1021/la902623c PubMed DOI
Kreve, S. & Reis, A. C. D. Bacterial adhesion to biomaterials: What regulates this attachment? A review. Jpn. Dent. Sci. Rev.57, 85–96 (2021). 10.1016/j.jdsr.2021.05.003 PubMed DOI PMC
Ramachandran, B., & Muthuvijayan, V. Surface engineering approaches for controlling biofilms and wound infections. In ACS Symposium Series (eds Rathinam, N. K., Sani, R. K.) 101–123 (American Chemical Society, 2019) [cited 2023 Dec 18]. 10.1021/bk-2019-1323.ch005
Yang, X. et al. Antibacterial surfaces: Strategies and applications. Sci. China Technol. Sci.65, 1000–1010 (2022). 10.1007/s11431-021-1962-x PubMed DOI PMC
Puckett, S. D., Taylor, E., Raimondo, T. & Webster, T. J. The relationship between the nanostructure of titanium surfaces and bacterial attachment. Biomaterials31, 706–713 (2010). 10.1016/j.biomaterials.2009.09.081 PubMed DOI
Li, H. et al. Antibacterial activity of TiO2 nanotubes: Influence of crystal phase, morphology and Ag deposition. Appl. Surf. Sci.284, 179–183 (2013).10.1016/j.apsusc.2013.07.076 DOI
Mazare, A. et al. Corrosion, antibacterial activity and haemocompatibility of TiO2 nanotubes as a function of their annealing temperature. Corros. Sci.103, 215–222 (2016).10.1016/j.corsci.2015.11.021 DOI
Xue, J. et al. The surface wettability of TiO2 nanotube arrays: Which is more important—Morphology or chemical composition?. J. Porous Mater.26, 91–98 (2019).10.1007/s10934-018-0616-1 DOI
Ercan, B., Taylor, E., Alpaslan, E. & Webster, T. J. Diameter of titanium nanotubes influences anti-bacterial efficacy. Nanotechnology22, 295102 (2011). 10.1088/0957-4484/22/29/295102 PubMed DOI
Zhang, X. et al. Quantitatively predicting bacterial adhesion using surface free energy determined with a spectrophotometric method. Environ. Sci. Technol.49, 6164–6171 (2015). 10.1021/es5050425 PubMed DOI PMC
Ji, X. et al. Different antibacterial mechanisms of titania nanotube arrays at various growth phases of E. coli. Trans. Nonferrous Met. Soc. China31, 3821–3830 (2021).10.1016/S1003-6326(21)65767-9 DOI
Yu, J., Zhou, M., Zhang, L. & Wei, H. Antibacterial adhesion strategy for dental titanium implant surfaces: From mechanisms to application. JFB13, 169 (2022). 10.3390/jfb13040169 PubMed DOI PMC
Pacha-Olivenza, M. Á. et al. Relevance of topographic parameters on the adhesion and proliferation of human gingival fibroblasts and oral bacterial strains. BioMed Res. Int.2019, 1–13 (2019). PubMed PMC
Wiessner, A. et al. In vivo biofilm formation on novel PEEK, titanium, and zirconia implant abutment materials. IJMS24, 1779 (2023). 10.3390/ijms24021779 PubMed DOI PMC
Annunziata, M. et al. Bacterial adhesion to direct laser metal formed and mildly acid etched implant surfaces. Surf. Coat. Technol.328, 390–397 (2017).10.1016/j.surfcoat.2017.09.011 DOI
Pawlus, P., Reizer, R. & Wieczorowski, M. Functional importance of surface texture parameters. Materials14, 5326 (2021). 10.3390/ma14185326 PubMed DOI PMC
Souza, J. G. S. et al. Targeting implant-associated infections: Titanium surface loaded with antimicrobial. iScience24, 102008 (2021). 10.1016/j.isci.2020.102008 PubMed DOI PMC
Lüdecke, C. et al. Nanorough titanium surfaces reduce adhesion of Escherichia coli and Staphylococcus aureus via nano adhesion points. Colloids Surf. B: Biointerfaces145, 617–625 (2016). 10.1016/j.colsurfb.2016.05.049 PubMed DOI
Świercz, R. & Oniszczuk-Świercz, D. Experimental investigation of surface layer properties of high thermal conductivity tool steel after electrical discharge machining. Metals7, 550 (2017).10.3390/met7120550 DOI
Pawlus, P., Reizer, R. & Zelasko, W. Prediction of parameters of equivalent sum rough surfaces. Materials13, 4898 (2020). 10.3390/ma13214898 PubMed DOI PMC
Dudás, I. & Varga, G. 3D topography for environmentally friendly machined surfaces. J. Phys.: Conf. Ser.13, 24–27 (2005).
D’Ercole, S. et al. A novel 3D titanium surface produced by selective laser sintering to counteract Streptococcus oralis Biofilm Formation. Appl. Sci.11, 11915 (2021).10.3390/app112411915 DOI
Cheng, Y., Feng, G. & Moraru, C. I. Micro- and nanotopography sensitive bacterial attachment mechanisms: A review. Front. Microbiol.10, 191 (2019). 10.3389/fmicb.2019.00191 PubMed DOI PMC
Whitehead, K. A. & Verran, J. The effect of surface topography on the retention of microorganisms. Food Bioproducts Process.84, 253–259 (2006).10.1205/fbp06035 DOI
Whitehead, K. A., Colligon, J. & Verran, J. Retention of microbial cells in substratum surface features of micrometer and sub-micrometer dimensions. Colloids Surf. B: Biointerfaces41, 129–138 (2005). 10.1016/j.colsurfb.2004.11.010 PubMed DOI
Lorenzetti, M. et al. The influence of surface modification on bacterial adhesion to titanium-based substrates. ACS Appl. Mater. Interfaces7, 1644–1651 (2015). 10.1021/am507148n PubMed DOI
Seddiki, O., Harnagea, C., Levesque, L., Mantovani, D. & Rosei, F. Evidence of antibacterial activity on titanium surfaces through nanotextures. Appl. Surf. Sci.308, 275–284 (2014).10.1016/j.apsusc.2014.04.155 DOI
Katsikogianni, M. & Missirlis, Y. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria-material interactions. ECM8, 37–57 (2004). 10.22203/eCM.v008a05 PubMed DOI
Meinshausen, A.-K. et al. Aspect ratio of nano/microstructures determines Staphylococcus aureus adhesion on PET and titanium surfaces. J. Appl. Microbiol.131, 1498–1514 (2021). 10.1111/jam.15033 PubMed DOI
Akanbi, O. E., Njom, H. A., Fri, J., Otigbu, A. C. & Clarke, A. M. Antimicrobial susceptibility of Staphylococcus aureus isolated from recreational waters and beach sand in Eastern Cape Province of South Africa. IJERPH14, 1001 (2017). 10.3390/ijerph14091001 PubMed DOI PMC
Diggle, S. P. & Whiteley, M. Microbe profile: Pseudomonas aeruginosa: Opportunistic pathogen and lab rat: This article is part of the Microbe Profiles collection. Microbiology166, 30–33 (2020). 10.1099/mic.0.000860 PubMed DOI PMC
Whitehead, K. A. & Verran, J. The effect of surface properties and application method on the retention of Pseudomonas aeruginosa on uncoated and titanium-coated stainless steel. Int. Biodeterior. Biodegrad.60, 74–80 (2007).10.1016/j.ibiod.2006.11.009 DOI
Pellegrino, L., Kriem, L. S., Robles, E. S. J. & Cabral, J. T. Microbial response to micrometer-scale multiaxial wrinkled surfaces. ACS Appl. Mater. Interfaces14, 31463–31473 (2022). 10.1021/acsami.2c08768 PubMed DOI PMC
Whitehead, K. A. & Verran, J. Formation, architecture and functionality of microbial biofilms in the food industry. Curr. Opin. Food Sci.2, 84–91 (2015).10.1016/j.cofs.2015.02.003 DOI
Flausino, J. S. et al. Biofilm formation on different materials for tooth restoration: Analysis of surface characteristics. J. Mater. Sci.49, 6820–6829 (2014).10.1007/s10853-014-8384-z DOI
Gross, M., Cramton, S. E., Götz, F. & Peschel, A. Key role of teichoic acid net charge in Staphylococcus aureus colonization of artificial surfaces. Infect. Immun.69, 3423–3426 (2001). 10.1128/IAI.69.5.3423-3426.2001 PubMed DOI PMC
Whitehead, S. A., Shearer, A. C., Watts, D. C. & Wilson, N. H. F. Comparison of methods for measuring surface roughness of ceramic. J. Oral Rehabilit.22, 421–427 (1995).10.1111/j.1365-2842.1995.tb00795.x PubMed DOI
Whitehead, S. A., Shearer, A. C., Watts, D. C. & Wilson, N. H. F. Comparison of two stylus methods for measuring surface texture. Dent. Mater.15, 79–86 (1999). 10.1016/S0109-5641(99)00017-2 PubMed DOI
Braz, J. K. F. S. et al. Plasma nitriding under low temperature improves the endothelial cell biocompatibility of 316L stainless steel. Biotechnol. Lett.41, 503–510 (2019). 10.1007/s10529-019-02657-7 PubMed DOI
Nunes Filho, A. et al. Titanium surface chemical composition interferes in the Pseudomonas aeruginosa biofilm formation. Artif. Organs42, 193–199 (2018). 10.1111/aor.12983 PubMed DOI
Peng, Z. et al. Dual effects and mechanism of TiO2 nanotube arrays in reducing bacterial colonization and enhancing C3H10T1/2 cell adhesion. IJN8, 3093 (2013). PubMed PMC
Liu, P. et al. Early antimicrobial evaluation of nanostructured surfaces based on bacterial biological properties. ACS Biomater. Sci. Eng.8, 4976–4986 (2022). 10.1021/acsbiomaterials.2c00559 PubMed DOI
Anitha, V. C. et al. Biofilm formation on a TiO2 nanotube with controlled pore diameter and surface wettability. Nanotechnology26, 065102 (2015). 10.1088/0957-4484/26/6/065102 PubMed DOI
Xu, Z. et al. Enhanced human gingival fibroblast response and reduced Porphyromonas gingivalis adhesion with titania nanotubes. BioMed Res. Int.2020, 1–10 (2020).10.1155/2020/2094320 PubMed DOI PMC
Simi, V. S. & Rajendran, N. Influence of tunable diameter on the electrochemical behavior and antibacterial activity of titania nanotube arrays for biomedical applications. Mater. Charact.129, 67–79 (2017).10.1016/j.matchar.2017.04.019 DOI
Kobayashi, M. et al. The effect of ultraviolet treatment on TiO2 nanotubes: A study of surface characteristics, bacterial adhesion, and gingival fibroblast response. Metals12, 80 (2022).10.3390/met12010080 DOI
Shin, D. H., Shokuhfar, T., Choi, C. K., Lee, S.-H. & Friedrich, C. Wettability changes of TiO2 nanotube surfaces. Nanotechnology22, 315704 (2011). 10.1088/0957-4484/22/31/315704 PubMed DOI
Draghi, L., Preda, V., Moscatelli, M., Santin, M. & Chiesa, R. Gentamicin-loaded TiO2 nanotubes as improved antimicrobial surfaces for orthopedic implants. Front. Mater.7, 233 (2020).10.3389/fmats.2020.00233 DOI
Rajeswari, S., Nandini, V., Perumal, A. & Gowda, T. Influence of titania nanotubes diameter on its antibacterial efficacy against periodontal pathogens: An In vitro analysis. J. Pharm. Bioallied Sci.13, 284 (2021).10.4103/jpbs.JPBS_743_20 PubMed DOI PMC
Lin, W. et al. Inhibited bacterial biofilm formation and improved osteogenic activity on gentamicin-loaded titania nanotubes with various diameters. IJN9, 1215–1230 (2014). PubMed PMC
Xu, Z. et al. Increased mesenchymal stem cell response and decreased Staphylococcus aureus adhesion on titania nanotubes without pharmaceuticals. BioMed Res. Int.2015, 1–9 (2015). PubMed PMC
İzmir, M. & Ercan, B. Anodization of titanium alloys for orthopedic applications. Front. Chem. Sci. Eng.13, 28–45 (2019).10.1007/s11705-018-1759-y DOI
Narendrakumar, K. et al. Adherence of oral streptococci to nanostructured titanium surfaces. Dent. Mater.31, 1460–1468 (2015). 10.1016/j.dental.2015.09.011 PubMed DOI
Kulkarni, M. et al. Interaction of nanostructured TiO2 biointerfaces with stem cells and biofilm-forming bacteria. Mater. Sci. Eng.: C.77, 500–507 (2017).10.1016/j.msec.2017.03.174 PubMed DOI
Shi, X. et al. Antibacterial activities of TiO2 nanotubes on Porphyromonas gingivalis. RSC Adv.5, 34237–34242 (2015).10.1039/C5RA00804B DOI
Lewandowska, Ż et al. The evaluation of the impact of titania nanotube covers morphology and crystal phase on their biological properties. J. Mater. Sci.: Mater. Med.26, 163 (2015). PubMed PMC
Zhao, C. et al. Preparation and antibacterial activity of titanium nanotubes loaded with Ag nanoparticles in the dark and under the UV light. Appl. Surf. Sci.280, 8–14 (2013).10.1016/j.apsusc.2013.04.057 DOI
Song, R. et al. Facile construction of structural gradient of TiO2 nanotube arrays on medical titanium for high throughput evaluation of biocompatibility and antibacterial property. ACS Appl. Bio Mater.1, 1056–1065 (2018). 10.1021/acsabm.8b00288 PubMed DOI
Feng, E. et al. Improved osteogenic activity and inhibited bacterial biofilm formation on andrographolide-loaded titania nanotubes. Ann. Transl. Med.8, 987–987 (2020). 10.21037/atm-20-4901 PubMed DOI PMC
Li, W., Thian, E. S., Wang, M., Wang, Z. & Ren, L. Surface design for antibacterial materials: From fundamentals to advanced strategies. Adv. Sci.8, 2100368 (2021).10.1002/advs.202100368 PubMed DOI PMC
Wandiyanto, J. V. et al. Outsmarting superbugs: Bactericidal activity of nanostructured titanium surfaces against methicillin- and gentamicin-resistant Staphylococcus aureus ATCC 33592. J. Mater. Chem. B7, 4424–4431 (2019).10.1039/C9TB00102F DOI
Lee, S. W., Phillips, K. S., Gu, H., Kazemzadeh-Narbat, M. & Ren, D. How microbes read the map: Effects of implant topography on bacterial adhesion and biofilm formation. Biomaterials268, 120595 (2021). 10.1016/j.biomaterials.2020.120595 PubMed DOI
Yang, X. et al. Recent progress on bioinspired antibacterial surfaces for biomedical application. Biomimetics7, 88 (2022). 10.3390/biomimetics7030088 PubMed DOI PMC
Song, F., Koo, H. & Ren, D. Effects of material properties on bacterial adhesion and biofilm formation. J. Dent. Res.94, 1027–1034 (2015). 10.1177/0022034515587690 PubMed DOI
San-Martin-Galindo, P. et al. Modulation of virulence factors of Staphylococcus aureus by nanostructured surfaces. Mater. Des.208, 109879 (2021).10.1016/j.matdes.2021.109879 DOI
Ghilini, F., Pissinis, D. E., Miñán, A., Schilardi, P. L. & Diaz, C. How functionalized surfaces can inhibit bacterial adhesion and viability. ACS Biomater. Sci. Eng.5, 4920–4936 (2019). 10.1021/acsbiomaterials.9b00849 PubMed DOI
Harper, C. E. & Hernandez, C. J. Cell biomechanics and mechanobiology in bacteria: Challenges and opportunities. APL Bioeng.4, 021501 (2020). 10.1063/1.5135585 PubMed DOI PMC
Morales-García, A. L. et al. The role of extracellular DNA in microbial attachment to oxidized silicon surfaces in the presence of Ca2+ and Na+. Langmuir37, 9838–9850 (2021). 10.1021/acs.langmuir.1c01410 PubMed DOI PMC
Desai, S., Sanghrajka, K. & Gajjar, D. High adhesion and increased cell death contribute to strong biofilm formation in Klebsiella pneumoniae. Pathogens8, 277 (2019). 10.3390/pathogens8040277 PubMed DOI PMC
Biguetti, C. C. et al. Effects of titanium corrosion products on in vivo biological response: A basis for the understanding of osseointegration failures mechanisms. Front. Mater.8, 651970 (2021).10.3389/fmats.2021.651970 DOI
Weller, J. et al. The role of bacterial corrosion on recolonization of titanium implant surfaces: An in vitro study. Clin. Implant Dent. Relat. Res.24, 664–675 (2022). 10.1111/cid.13114 PubMed DOI
Vaidya, M., McBain, A. J., Banks, C. E. & Whitehead, K. A. Single and combined antimicrobial efficacies for nine metal ion solutions against Klebsiella pneumoniae, Acinetobacter baumannii and Enterococcus faecium. Int. Biodeterior. Biodegrad.141, 39–43 (2019).10.1016/j.ibiod.2018.06.017 DOI
Yu, T. S. Effect of titanium-ion on the growth of various bacterial species. J. Microbiol.42, 47–50 (2004). PubMed
Park, S. M., Kim, H. S. & Yu, T. S. Effect of titanium ion and resistance encoding plasmid of Pseudomonas aeruginosa ATCC 10145. J. Microbiol.44, 255–262 (2006). PubMed
Punset, M. et al. Citric acid passivation of titanium dental implants for minimizing bacterial colonization impact. Coatings11, 214 (2021).10.3390/coatings11020214 DOI
Gil, F. J., Sánchez, L. A., Espías, A. & Planell, J. A. In vitro corrosion behaviour and metallic ion release of different prosthodontic alloys. Int. Dent. J.49, 361–367 (1999). 10.1111/j.1875-595X.1999.tb00538.x PubMed DOI
Joseph, L. A., Israel, O. K. & Edet, E. J. Comparative evaluation of metal ions release from titanium and Ti–6Al–7Nb into bio-fluids. Dent. Res. J.6, 7–11 (2009). PubMed PMC
Mutlu-Sagesen, L., Ergun, G. & Karabulut, E. Ion release from metal-ceramic alloys in three different media. Dent. Mater. J.30, 598–610 (2011). 10.4012/dmj.2011-031 PubMed DOI
Fage, S. W., Muris, J., Jakobsen, S. S. & Thyssen, J. P. Titanium: A review on exposure, release, penetration, allergy, epidemiology, and clinical reactivity. Contact Dermat.74, 323–345 (2016).10.1111/cod.12565 PubMed DOI
Hirayama, T. et al. Ion release from casts of commercially pure titanium in mixed solutions of organic acids contained in human saliva. J. Jpn. Prosthodont. Soc.52, 501–506 (2008).10.2186/jjps.52.501 PubMed DOI
Strietzel, R., Hösch, A., Kalbfleisch, H. & Buch, D. In vitro corrosion of titanium. Biomaterials19, 1495–1499 (1998). 10.1016/S0142-9612(98)00065-9 PubMed DOI
Koike, M. & Fujii, H. The corrosion resistance of pure titanium in organic acids. Biomaterials22, 2931–2936 (2001). 10.1016/S0142-9612(01)00040-0 PubMed DOI
Koike, M. & Fujii, H. In vitro assessment of corrosive properties of titanium as a biomaterial. J. Oral Rehabilit.28, 540–548 (2001).10.1046/j.1365-2842.2001.00690.x PubMed DOI
Nakagawa, M., Matsuya, S. & Udoh, K. Corrosion behavior of pure titanium and titanium alloys in fluoride-containing solutions. Dent. Mater. J.20, 305–314 (2001). 10.4012/dmj.20.305 PubMed DOI
Okazaki, Y. & Gotoh, E. Comparison of metal release from various metallic biomaterials in vitro. Biomaterials26, 11–21 (2005). 10.1016/j.biomaterials.2004.02.005 PubMed DOI
Yu, F., Addison, O., Baker, S. J. & Davenport, A. J. Lipopolysaccharide inhibits or accelerates biomedical titanium corrosion depending on environmental acidity. Int. J. Oral Sci.7, 179–186 (2015). 10.1038/ijos.2014.76 PubMed DOI PMC
Yu, X. et al. Osteoclast-mediated biocorrosion of pure titanium in an inflammatory microenvironment. Mater. Sci. Eng.: C.119, 111610 (2021).10.1016/j.msec.2020.111610 PubMed DOI
Noumbissi, S., Scarano, A. & Gupta, S. A literature review study on atomic ions dissolution of titanium and its alloys in implant dentistry. Materials12, 368 (2019). 10.3390/ma12030368 PubMed DOI PMC
Dini, C. et al. Progression of bio-tribocorrosion in implant dentistry. Front. Mech. Eng.6, 1 (2020).10.3389/fmech.2020.00001 DOI
Xu, L., Yu, X., Chen, W., Zhang, S. & Qiu, J. Biocorrosion of pure and SLA titanium surfaces in the presence of Porphyromonas gingivalis and its effects on osteoblast behavior. RSC Adv.10, 8198–8206 (2020). 10.1039/D0RA00154F PubMed DOI PMC
Costa, R. C. et al. Correction to: Microbial corrosion in titanium-based dental implants: How tiny bacteria can create a big problem?. J. Bio Tribo. Corros.7, 151 (2021).10.1007/s40735-021-00590-9 DOI
Kulkarni, M. et al. Wettability studies of topologically distinct titanium surfaces. Colloids Surf. B: Biointerfaces129, 47–53 (2015). 10.1016/j.colsurfb.2015.03.024 PubMed DOI
Kulkarni, M. et al. Protein interactions with layers of TiO2 nanotube and nanopore arrays: Morphology and surface charge influence. Acta Biomater.45, 357–366 (2016). 10.1016/j.actbio.2016.08.050 PubMed DOI
Kulkarni, M. et al. Binding of plasma proteins to titanium dioxide nanotubes with different diameters. IJN10, 1359 (2015). PubMed PMC