Bioadhesion in the oral cavity and approaches for biofilm management by surface modifications

Abstract

Background: All soft and solid surface structures in the oral cavity are covered by the acquired pellicle followed by bacterial colonization. This applies for natural structures as well as for restorative or prosthetic materials; the adherent bacterial biofilm is associated among others with the development of caries, periodontal diseases, peri-implantitis, or denture-associated stomatitis. Accordingly, there is a considerable demand for novel materials and coatings that limit and modulate bacterial attachment and/or propagation of microorganisms.

Objectives and findings: The present paper depicts the current knowledge on the impact of different physicochemical surface characteristics on bioadsorption in the oral cavity. Furthermore, it was carved out which strategies were developed in dental research and general surface science to inhibit bacterial colonization and to delay biofilm formation by low-fouling or "easy-to-clean" surfaces. These include the modulation of physicochemical properties such as periodic topographies, roughness, surface free energy, or hardness. In recent years, a large emphasis was laid on micro- and nanostructured surfaces and on liquid repellent superhydrophic as well as superhydrophilic interfaces. Materials incorporating mobile or bound nanoparticles promoting bacteriostatic or bacteriotoxic properties were also used. Recently, chemically textured interfaces gained increasing interest and could represent promising solutions for innovative antibioadhesion interfaces. Due to the unique conditions in the oral cavity, mainly in vivo or in situ studies were considered in the review.

Conclusion: Despite many promising approaches for modulation of biofilm formation in the oral cavity, the ubiquitous phenomenon of bioadsorption and adhesion pellicle formation in the challenging oral milieu masks surface properties and therewith hampers low-fouling strategies.

Clinical relevance: Improved dental materials and surface coatings with easy-to-clean properties have the potential to improve oral health, but extensive and systematic research is required in this field to develop biocompatible and effective substances.

Keywords: Biofilm management; Low-fouling surfaces; Nanostructured surfaces; Oral biofilms; Pellicle; Textured surfaces.

Fig. 1

Interaction and adsorption of proteins to surfaces. a Illustration of the Langmuir and RSA (random sequential adsorption) models (k_a adsorption constant, k_d desorption constant). b Depending on the state and properties, proteins can loosely, interchangeably, or irreversibly attach to surfaces. c Factors that influence protein adsorption are, among others, properties of the protein(s), pH of the surrounding medium, and surface properties like surface charge, surface energy, or topography

Fig. 2

Interactions influencing bioadhesion and biofilm formation in the oral cavity. Different short, medium, and long range forces influence adhesion of bacteria to surfaces. The pellicle masks some of these properties while also providing new ones. Providing receptors and metabolic substrates promote, while shear forces and antimicrobial activities counteract bacterial adhesion and biofilm formation (modified according to Hannig et al. [41])

Fig. 3

Initial bacterial adhesion to a pellicle-coated surface. a Initial bacterial approach and adhesion to surfaces is mediated by both attractive (green) and repulsive (red) short and long range forces [41]. b Depicted is the Stern layer surrounding the pellicle-coated surface and bacteria and the Gibbs free energy resulting from the sum of different forces (red curve) in relation to the distance between a bacterium and the surface. Small structures like fimbriae or flagella can overcome repulsive forces [43]. c The establishment of covalent, ionic, and hydrogen bonds establishes firm bonds between bacteria and the surface [44]

Fig. 4

Interaction of water with different surfaces. a Water contact angles on different surfaces. Contact angles on hydrophilic surfaces are below 90°, while hydrophobic surfaces have contact angles of more than 90°. b Depiction of Wenzel and Cassie–Baxter wetting regimes. In the Wenzel state, cavities are fully wetted, while in the Cassie–Baxter state, air is trapped within cavities. c Water roll-off angles on hydrophilic and superhydrophobic surfaces. Hydrophilic surfaces possess relatively high roll-off angles, while superhydrophobic surfaces have roll-off angles of less than 5°

Fig. 5

Overview of the acquired oral pellicle and biofilm formation in the oral cavity. a Depicted is the acquired oral pellicle on enamel composed of a thin basal pellicle and on top of it granular and globular structures. Early colonizers first adhere to lectins and other receptors on the acquired proteinaceous oral pellicle via specific adhesins in order to adhere tightly. b More microorganisms integrate into the developing biofilm structure by duplication or coadherence of further bacteria. c Depiction of a fully developed biofilm in the oral cavity. A multispecies biofilm is embedded into an extracellular matrix consisting among others of proteins, lipids, extracellular DNA, exopolysaccharides, and amyloid structures

Fig. 6

Interaction of bacteria with different surface properties. Rough surfaces increase the surface area (a) or offer protection against shear forces (b). c Since bacterial membranes are generally negatively charged, positively charged surfaces are generally attractant and negatively charged surfaces repellent. d Functionalized nanoparticles embedded into surfaces with anti-adhesive or antimicrobial properties can prevent attachment or proliferation of bacteria after surface contact or they are released into the surrounding environment. e Nanotextured superhydrophic surfaces are often bactericidal due to stretching of the membrane

Fig. 7

Interaction of bacteria and proteins with biphasic interfaces. a Bacteria can adhere to surfaces with various interfacial properties but might have problems to adapt to surfaces with alternating interfacial properties. b Protein adsorption transforms the synthetic textured identity into a biological alternating identity. c Nanotextures allow bioadhesion but might lead to easy removal