Abstract

Bacterial infection of implants and prosthetic devices is one of the most common causes of implant failure. The nanostructured surface of biocompatible materials strongly influences the adhesion and proliferation of mammalian cells on solid substrates. The observation of this phenomenon has led to an increased effort to develop new strategies to prevent bacterial adhesion and biofilm formation, primarily through nanoengineering the topology of the materials used in implantable devices. While several studies have demonstrated the influence of nanoscale surface morphology on prokaryotic cell attachment, none have provided a quantitative understanding of this phenomenon. Using supersonic cluster beam deposition, we produced nanostructured titania thin films with controlled and reproducible nanoscale morphology respectively. We characterized the surface morphology; composition and wettability by means of atomic force microscopy, X-ray photoemission spectroscopy and contact angle measurements. We studied how protein adsorption is influenced by the physico-chemical surface parameters. Lastly, we characterized Escherichia coli and Staphylococcus aureus adhesion on nanostructured titania surfaces. Our results show that the increase in surface pore aspect ratio and volume, related to the increase of surface roughness, improves protein adsorption, which in turn downplays bacterial adhesion and biofilm formation. As roughness increases up to about 20 nm, bacterial adhesion and biofilm formation are enhanced; the further increase of roughness causes a significant decrease of bacterial adhesion and inhibits biofilm formation. We interpret the observed trend in bacterial adhesion as the combined effect of passivation and flattening effects induced by morphology-dependent protein adsorption. Our findings demonstrate that bacterial adhesion and biofilm formation on nanostructured titanium oxide surfaces are significantly influenced by nanoscale morphological features. The quantitative information, provided by this study about the relation between surface nanoscale morphology and bacterial adhesion points towards the rational design of implant surfaces that control or inhibit bacterial adhesion and biofilm formation.

Highlights

  • Biomedical implants and smart prosthetics increasingly incorporate engineered surfaces at the nanoscale in order to modulate and control the interaction between biomaterials and biological systems [1,2,3]

  • As we already demonstrated in previous studies, the increase of the amount of adsorbed proteins on cluster-assembled titania is tailored by surface morphology that promotes protein nucleation on the surface in correspondence of nanometric surface pores with aspect ratio higher than a specific threshold value [15]

  • We characterized the interaction of E.coli and S.aureus with cluster-assembled titania surfaces demonstrating a precise and quantitative relationship between surface nano-morphology and bacterial adhesion

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Summary

Introduction

Biomedical implants and smart prosthetics increasingly incorporate engineered surfaces at the nanoscale in order to modulate and control the interaction between biomaterials and biological systems [1,2,3]. A large number of studies qualitatively demonstrate that nanostructures on titanium oxide surface can enhance cell adhesion and proliferation [8,9,10]. When a biomaterial surface comes into contact with biological fluids, such as blood or serum, it is immediately coated by the proteins present in the media. This protein layer strongly influences cell adhesion and proliferation on implants. Protein-surface interaction is determined by the complex interplay between morphological and chemical features. These include surface charge, hydrophobicity, roughness and chemical composition [14,15]. The quantitative study of protein adsorption on nanostructured surfaces, in terms of separating the role of parameters, such as surface chemistry and surface nanotopography, has been a recent development [15]

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