587690

research-article2015

JDRXXX10.1177/0022034515587690Journal of Dental ResearchEffects of Material Properties

Critical Reviews in Oral Biology & Medicine

Effects of Material Properties on Bacterial Adhesion and Biofilm Formation

Journal of Dental Research 1­–8 © International & American Associations for Dental Research 2015 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0022034515587690 jdr.sagepub.com

F. Song1,2, H. Koo3, and D. Ren1,2,4,5

Abstract Adhesion of microbes, such as bacteria and fungi, to surfaces and the subsequent formation of biofilms cause multidrug-tolerant infections in humans and fouling of medical devices. To address these challenges, it is important to understand how material properties affect microbe-surface interactions and engineer better nonfouling materials. Here we review the recent progresses in this field and discuss the main challenges and opportunities. In particular, we focus on bacterial biofilms and review the effects of surface energy, charge, topography, and stiffness of substratum material on bacterial adhesion. We summarize how these surface properties influence oral biofilm formation, and we discuss the important findings from nondental systems that have potential applications in dental medicine. Keywords: bacteria, biomaterials, dental implants, infection control, dentistry, biofouling

Introduction More than 99% of bacteria on Earth live as surface-attached cells, and the sessile life form of detrimental bacteria is associated with many problems, such as chronic infections in humans and biofouling in industrial settings (Hall-Stoodley et al. 2004). Thus, understanding bacterial adhesion and the subsequent formation of biofilms (multicellular structures with microbial cells embedded in an extracellular matrix; Hall-Stoodley et al. 2004; Flemming and Wingender, 2010) is critical for the study of bacterial pathogenicity and for controlling biofilm-related infections. The human mouth provides a unique environment for the formation of complex biofilms; for example, it hosts >1,000 bacterial species with high cell density (109 cells/mL found in human saliva samples; Dewhirst et al. 2010). The fast turnover of oral lining epithelia (shedding 3 times per day) is an effective mechanism to reduce bacterial adhesion. In comparison, the nonshedding surfaces, such as teeth, dentures, and dental implants, are susceptible to biofilm formation, which can cause serious issues, such as dental caries, periodontitis, and dental implant failure (Marsh et al. 2011). Biotic and abiotic dental surfaces are constantly coated with saliva, which forms a conditioning film known as pellicle, consisting of glycoproteins (mucins), phosphoproteins, histidine-rich proteins, prolinerich proteins, α-amylase, and many other molecules, including bacterially derived glucosyltransferases (Siqueira et al. 2012). The formation and composition of pellicle appear to vary on different surfaces (Aroonsang et al. 2014), although the exact effects of material properties on pellicle formation and the underlying mechanisms are not well understood. Within the complex oral microbiome, early colonizers, such as oral streptococci (e.g., Streptococcus oralis and Streptococcus sanguinis), can adhere to pellicle-coated surfaces via adhesin receptor and charge interactions among other mechanisms

(Nobbs et al. 2009). This is followed by the formation of multispecies biofilms with further attachment of other bacteria, such as Fusobacterium nucleatum, Porphyromonas gingivalis, and Aggregatibacter actinomycetemcomitans (Kuramitsu et al. 2007; Kolenbrander et al. 2010). Depending on a variety of host and dietary factors, further bacterial accumulation, structural organization of the matrix, and microbial composition can be dynamically changed, forming highly complex oral biofilms (reviewed in Marsh et al. 2011). Frequent exposure to dietary sugars can dramatically affect the dynamics of bacterial adhesion and biofilm accumulation. For example, glucosyltransferases present in the pellicle can produce exopolysaccharides in situ from sucrose, modifying bacterial binding affinity/ selectivity and promoting cariogenic biofilm development (Bowen and Koo 2011). Biofilms can also be formed periapically and intracanally and on a variety of dental materials, such as restorative materials (composite resins, dental primers, and dental adhesives), endodontic materials (root canal sealers), and orthodontic and implanted materials (ceramics, resin composites, and metallic alloys), as recently reviewed (Wang et al. 2014). Other conditions, such as HIV, diabetes, smoking, and 1

Department of Biomedical and Chemical Engineering, Syracuse University, Syracuse, NY, USA 2 Syracuse Biomaterials Institute, Syracuse University, Syracuse, NY, USA 3 Department of Orthodontics and Divisions of Pediatric Dentistry & Community Oral Health, University of Pennsylvania, Philadelphia, PA, USA 4 Department of Civil and Environmental Engineering, Syracuse University, Syracuse, NY, USA 5 Department of Biology, Syracuse University, Syracuse, NY, USA Corresponding Author: D. Ren, Department of Biomedical and Chemical Engineering, 329 Link Hall, Syracuse, NY 13244, USA. Email: [email protected]

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Figure 1.  Schematic illustration of bacterial adhesion and the effects of material properties in complex environments. The effects of surface charge, hydrophobicity, roughness, topography, and stiffness are discussed in this review.

cancer, are known to change the host environment locally, often increasing the risk of biofilm development that may lead to oral diseases (Pihlstrom et al. 2005). Since adhesion is the first step of biofilm formation, understanding bacteria-surface interactions is essential for biofilm control. Bacterial cells approach surfaces by different means, including Brownian motion, sedimentation, movement with liquid flow, bacterial motility with cell surface appendages, and interaction with other cells to form aggregates (Teughels et al. 2006). None of the theoretical models developed to date can accurately describe the adhesion of all bacteria on different surfaces. This is mostly due to the complexity of bacteriasurface interactions and extracellular factors that cover the substratum surface (e.g., those in the salivary pellicle; Nobbs et al. 2009) and bacterial cell wall (e.g., adhesins and other membrane-associated structures). Furthermore, how bacteria adjust physiology and cell surface properties dynamically in response to the local surface environment remains to be fully elucidated. Such knowledge gaps and the need for better nonfouling materials have motivated researchers to investigate the effects of material properties on bacterial adhesion. In this review, we present an update on this research field. Because some related topics were well summarized in early reviews (Teughels et al. 2006; Busscher et al. 2010; Renner and Weibel 2011; Campoccia et al. 2013) and because the number of references of this article is limited to 60, we will not present a systematic review of the entire literature but rather focus on the recent progresses, especially those in the last 3 y (see Fig. 1 for an overview of the factors that affect bacteria-surface interactions). We also discuss the findings from non-dental systems that may be helpful for oral biofilm research and practical applications in the field of dentistry.

Surface Charge Surface charge plays an important role in determining the binding force between bacteria and the surface, and it has long been known to affect biofilm formation. Most bacterial cells are

negatively charged; thus, in general, a positively charged surface is more prone to bacterial adhesion, and a negatively charged surface is more resistant to bacterial adhesion. Meanwhile, surfaces presenting certain cationic groups, such as quaternary ammonium and polyethylenimines, have antimicrobial activities and thus can kill the attached cells (Campoccia et al. 2013). In principle, controlling bacterial adhesion with surface charge may not work in static systems since the dead cells present a barrier that reduces the charge and facilitates the adhesion of other bacterial cells. However, because shear force (rinsing and brushing) can be readily applied to remove dead cells from dental materials, this strategy may be effective in some oral applications. Interestingly, recent research showed that surface charge can also affect long-term biofilm structure. For example, Pseudomonas aeruginosa biofilms on negatively charged poly(3-sulphopropylmethacrylate) surfaces are mushroom shaped and have a higher level of cyclic diguanylate monophosphate (c-di-GMP) than the relatively uniform biofilms formed on positively charged poly(2-(methacryloyloxy)-ethyl trimethyl ammonium chloride) surfaces (Rzhepishevska et al. 2013). Because the increase in c-di-GMP level is known to induce the production of extracellular matrix, it was speculated that P. aeruginosa may be able to modify cell surfaces to better attach on negatively charged surfaces (Rzhepishevska et al. 2013). These findings emphasize that surface charge alone may not be sufficient to repel bacteria and prevent biofilm formation of some bacterial species. Further complications may arise in complex systems with conditioning films and other environmental factors. For example, the formation of salivary pellicle causes the surface to be negatively charged, which can attract Ca2+ ions and promote the adhesion of Streptococcus mutans and F. nucleatum to Ti surfaces (Badihi Hauslich et al. 2013). In addition, the physical and chemical nature of a dental material can affect the composition and physiochemical properties of pellicle, such as density and configuration (Teughels et al. 2006). Further research is needed to understand how surface charge affects the

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Effects of Material Properties property of pellicle and to determine if surface charge can be tailored to promote the integration of host cells but repel or kill bacterial pathogens that cause oral diseases.

Surface Energy The role of hydrophobicity in oral bacterial adhesion has been reviewed elsewhere (Busscher et al. 2008; Nobbs et al. 2009; Busscher et al. 2010) and will not be discussed in great detail here. In general, by tuning the hydrophobicity of a surface, bacterial adhesion can be either promoted or inhibited. In oral environments, the trend appears to be different between supragingival and subgingival surfaces. Supragingivally, less biofilm is formed on hydrophobic surfaces than hydrophilic ones, while no such difference was observed for subgingival biofilms. This difference was attributed to the fluctuating shear in supragingival environment, which can slough off bacterial biofilms more from hydrophobic surfaces (Quirynen et al. 1995). The preference of surface hydrophobicity differs among the bacterial species. The presence of salivary coating on bacterial cells and dental surfaces can also greatly affect how hydrophobicity influences the interaction between oral bacteria and dental materials. In addition to the surface energy of substratum, the property of bacterial cells is important. For example, the hydrophobic S. sanguinis attaches better to saliva-coated pure titanium grade 2 (cp-Ti) and Ti-6A-4V alloy than the hydrophilic Streptococcus constellatus (Mabboux et al. 2004). Hu et al. (2011) reported that demineralization of enamel by heating increased the apatite hydrophobicity, caused the zeta potential of enamel to be more negative, and reduced the adhesion of Streptococcus mitis but not S. oralis and S. sanguinis. This was attributed to the difference in the surface properties of bacterial cells, such as hydrophobicity, zeta potential, and the abundance of fibrils and fimbriae. In addition to conventional systems, recent research showed that superhydrophobic and superhydrophilic surfaces can both prevent biofilm formation. A naturally existing example is lotus leaf, which has a water contact angle of 170º and remarkable self-cleaning properties due to the low surface energy of waxes and the specific surface roughness presented by microprotrusions and nanohairs, the major factors for achieving superhydrophobicity (Zhang et al. 2013). According to the Cassie-Baxter model, when the surface roughness is in an appropriate range, the system reaches the Cassie state, in which air is trapped in the grooves between surface features and thus prevents wetting (Marmur 2003). A number of superhydrophobic materials have recently been developed on the basis of these principles (for a recent review, see Zhang et al. 2013). Besides superhydrophobic surfaces, superhydrophilic surfaces have good nonfouling properties due to the formation of a dense layer of water molecules, which weakens the interaction between cell surface and substratum material and thus reduces cell adhesion. This principle, known as water layer theory, has guided the design of nonfouling materials. For example, zwitterionic polymers—which are neutral molecules with a positive and a negative electrical charge in close

proximity—can be used to coat material surfaces to obtain superhydrophilicity and reduce fouling by proteins and bacteria (for a recent review, see Mi and Jiang 2014). The applicability of surperhydrophobic and superhydrophilic surfaces in the dental field remains to be investigated. Intriguingly, Venault et al. (2014) reported that coating of hydroxyapatite with a zwitterion polymer polyethyleneimine-g-SBMA inhibited the adsorption of bovine serum albumin and lysozyme, which was attributed to the entrapment of water by the zwitterionic molecules. Further tests of this material showed up to 70% inhibition of oral bacterial adhesion on human teeth (Venault et al. 2014). With the rapid advancements in material science and fabrication techniques, the coming years will witness more intriguing progresses in this area.

Roughness and Topography Among the surface properties, surface roughness and topography have been the primary topics in dental biofilm research. In general, an increase in surface roughness promotes bacterial attachment due to the increase in contact area between the material surface and bacterial cells (Anselme et al. 2010) and protection from shear forces (Teughels et al. 2006). Thus, smoothening the surface can reduce biofilm formation (Ionescu et al. 2012), and a roughness of Ra of 0.2 µm was reported to be the threshold for maximum reduction of bacterial adhesion on abutment surfaces (Quirynen et al. 1996). However, the exact effects of surface roughness on bacterial adhesion and biofilm formation vary with the size and shape of bacterial cells and other environmental factors. Thus, there is no universally optimum roughness that can repress adhesion of all bacterial species (Renner and Weibel 2011). For example, Xing et al. (2014) reported that microbial adhesion on TiZr dental implant abutment is positively correlated with nanoroughness (200 nm and a thickness of 60 to 80 µm coated with perfluorinated

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bacterial adhesion and biofilm formation have been investigated for many years. Generally, negatively charged surfaces, super hydrophobic surfaces, super hydrophilic surfaces, and nm-scale surface roughness have all been shown to reduce bacterial adhesion. Moreover, some positively charged surfaces exhibit antimicrobial properties, which can be obtained by coating appropriate materials on a substrate. However, bacteria have remarkable strategies to overcome these barriers and develop biofilms. In the mouth, the presence of acquired pellicle containing host and bacterially derived proteins poses a great challenge to the control of bacterial adhesion and Figure 5.  Schematic representation of a smart polymer coating that can kill bacteria under dry biofilm formation based on surface modconditions and repel bacteria under wet conditions. Reprinted with permission from Cao et al. ifications. Besides surface properties, (2012). other factors, such as dietary intake and complex oral microbiome, affect biofilm formation. For example, exoenzymes present in the pellicle lubricating fluid, which was named slippery liquid-infused porous can utilize diet sugar to produce exopolysaccharides in situ, surface, or SLIPS. It was shown to reduce P. aeruginosa attachdramatically modifying bacterial binding affinity/selectivity as ment by 99.6% for over 7 d (Fig. 3). well as surface topography. Thus, new materials and strategies Intriguingly, smart surfaces that combine multiple surface for dental applications should be evaluated under conditions properties or are capable of switching among different stages have mimicking the oral cavity. been developed and have exhibited promising nonfouling and antiCompared with the effects of surface charge, hydrophobicity, microbial properties. For example, Pranzetti et al. (2013) develand chemistry, how surface stiffness and topography (except for oped an electrically reversible switchable surface with roughness) affect bacterial adhesion and biofilm development is 11-mercaptoundecanoic acid and mercaptoethanol self-assembled still poorly understood. Furthermore, how changes in these surmonolayers. The surface can be switched between attractive and face properties affect the pellicle formation and composition repellant state by controlling the surface potential. When the sur(including protein/enzyme conformation; Fears et al. 2015) and face has negative potential, the long chain negative mercaptounhow pellicle modifies the surface properties of different dental decanoic acid polymer will stand on the surface, and bacterial cells materials deserve further study. Importantly, how the interplay (M. hydrocarbonoclasticus) are attracted by the hydrophilic between surface properties and pellicle formation affect the bactecharged self-assembled monolayers. If the surface has positive rial adhesion strength, as well as the mechanical stability and potential, the long polymer chain will fold to the bottom, and the detachment of biofilms, needs additional elucidation. Previous surface will repel attached bacteria by hydrophobic neutral selfresearch greatly advanced our understanding of the physicochemassembled monolayers (Fig. 4). Cao et al. (2012) designed another ical and mechanical interactions between microorganisms and switchable surface using a smart polymer that has 2 equilibrium material surfaces, as well as interactions between cell wall compostates: a cationic N,N-dimethyl-2-morpholinone (CB-ring) state nents (e.g., adhesins) and pellicle receptors. However, how bacteand a zwitterionic carboxy betaine (CB-OH) state. The 2 states can ria sense and respond to different surface properties at the genetic be switched by the wettability of surface. The CB-ring in the dry level is largely unknown. It is also important to understand how environment was shown to kill 99.9% of E. coli K12 cells attached bacterial adhesion affects the local microenvironment and the subby positive charges on the surface; the CB-OH in the wet environsequent impact on further biofilm development. For example, the ment can repel >90% of attached and dead cells due to the zwitinflammation caused by biofilm formed on dentures, mucous surterionic properties of the surface (Fig. 5). Although not all of these face, and acrylic resins could change the local pH, nutrients, the strategies are readily applicable to oral systems due to the presence composition of proteins, and gingival crevicular fluid flow, which of salivary coating and intermittent shear forces, the design prinsubsequently alter the composition of the microflora and may prociples are nevertheless intriguing. Further research in this area will mote distinctive bacterial adhesion pattern (Marsh et al. 2011). benefit from new technologies of material and surface engineering Better understanding of the mechanisms by which bacteria monithat can overcome biofilm challenges. tor the local surface properties and environmental changes and modulate their physiology and adhesion is critical for designing Conclusions and Perspective new nonfouling and antimicrobial surfaces. Effects of material/surface properties—such as surface charge, In summary, the recent advancements in material design hydrophobicity, roughness, topography, and chemistry—on and surface engineering have provided a plethora of

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Effects of Material Properties opportunities for creating exciting new materials for dental applications. However, some new technologies have been tested only for nondental biofilms—for example, those of E. coli and P. aeruginosa. Further development and evaluation are needed using in vitro conditions that better mimic the complex mouth environment, as well as in vivo models with oral bacteria to assess the clinical translatability of new surface modifications. This research field will also benefit from a better understanding of the bacterial systems involved in surface sensing, especially at the molecular level. Integration of these knowledge and technologies is necessary to guide rational design of smart dental materials to reduce fouling by overcoming the unique challenges in the oral environment, such as complex oral microbiome, the presence of salivary proteins and other host/bacterially derived factors, as well as external factors such as diet.

Author Contributions F. Song, contributed to data analysis and interpretation, drafted and critically revised the manuscript; H. Koo, D. Ren, contributed to conception, design, data analysis, and interpretation, drafted and critically revised the manuscript. All authors gave final approval and agree to be accountable for all aspects of the work.

Acknowledgments The research related to this topic in the Ren laboratory is supported by the U.S. National Science 1137186 Foundation (CAREER-1055644 and EFRI-1137186). Part of the work in the Koo laboratory discussed here is supported by U.S. National Science Foundation (EFRI-1137186). The authors declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

References Anselme K, Davidson P, Popa A, Giazzon M, Liley M, Ploux L. 2010. The interaction of cells and bacteria with surfaces structured at the nanometre scale. Acta Biomater. 6(10):3824–3846. Aroonsang W, Sotres J, El-Schich Z, Arnebrant T, Lindh L. 2014. Influence of substratum hydrophobicity on salivary pellicles: organization or composition? Biofouling. 30(9):1123–1132. Badihi Hauslich L, Sela MN, Steinberg D, Rosen G, Kohavi D. 2013. The adhesion of oral bacteria to modified titanium surfaces: role of plasma proteins and electrostatic forces. Clin Oral Implants Res. 24 Suppl A100:49–56. Bakker DP, Huijs FM, de Vries J, Klijnstra JW, Busscher HJ, van der Mei HC. 2003. Bacterial deposition to fluoridated and non-fluoridated polyurethane coatings with different elastic modulus and surface tension in a parallel plate and a stagnation point flow chamber. Colloids Surf B Biointerfaces. 32(3):179–190. Barrantes A, Arnebrant T, Lindh L. 2014. Characteristics of saliva films adsorbed onto different dental materials studied by QCM-D. Colloids Surf A Physicochem Eng Aspects. 442:56–62. Belas R. 2014. Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol. 22(9):517–527. Bowen WH, Koo H. 2011. Biology of Streptococcus mutans–derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res. 45(1):69–86. Busscher HJ, Norde W, van der Mei HC. 2008. Specific molecular recognition and nonspecific contributions to bacterial interaction forces. Appl Environ Microbiol. 74(9):2559–2564. Busscher HJ, Rinastiti M, Siswomihardjo W, van der Mei HC. 2010. Biofilm formation on dental restorative and implant materials. J Den Res. 89(7):657–665.

Campoccia D, Montanaro L, Arciola CR. 2013. A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials. 34(34):8533– 8554. Cao Z, Mi L, Mendiola J, Ella-Menye JR, Zhang L, Xue H, Jiang S. 2012. Reversibly switching the function of a surface between attacking and defending against bacteria. Angew Chem Int Ed. 51(11):2602–2605. Chebolu A, Laha B, Ghosh M. 2013. Investigation on bacterial adhesion and colonisation resistance over laser-machined micro patterned surfaces. Micro Nano Lett, IET. 8(6):280–283. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, Lakshmanan A, Wade WG. 2010. The human oral microbiome. J Bacteriol. 192(19):5002– 5017. Epstein AK, Hong D, Kim P, Aizenberg J. 2013. Biofilm attachment reduction on bioinspired, dynamic, micro-wrinkling surfaces. New J Phys. 15(9):095018. Epstein AK, Wong T-S, Belisle RA, Boggs EM, Aizenberg J. 2012. Liquidinfused structured surfaces with exceptional anti-biofouling performance. Proc Natl Acad Sci U S A. 109(33):13182–13187. Fears KP, Gonzalez-Begne M, Love CT, Day DE, Koo H. 2015. Surface-induced changes in the conformation and glucan production of glucosyltransferase adsorbed on saliva-coated hydroxyapatite. Langmuir. 31(16):4654–4662. Flemming HC, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol. 8(9):623–633. Friedlander RS, Vlamakis H, Kim P, Khan M, Kolter R, Aizenberg J. 2013. Bacterial flagella explore microscale hummocks and hollows to increase adhesion. Proc Natl Acad Sci U S A. 110(14):5624–5629. Gu H, Ren D. 2014. Materials and surface engineering to control bacterial adhesion and biofilm formation: a review of recent advances. Front Chem Sci Eng. 8(1):20–33. Guegan C, Garderes J, Le Pennec G, Gaillard F, Fay F, Linossier I, Herry JM, Bellon Fontaine MN, Vallée Réhel K. 2014. Alteration of bacterial adhesion induced by the substrate stiffness. Colloids Surf B Biointerfaces. 114(2014):193–200. Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2(2):95–108. Hannig M. 1997. Transmission electron microscopic study of in vivo pellicle formation on dental restorative materials. Eur J Oral Sci. 105(5 Pt 1):422– 433. Hickman JW, Harwood CS. 2008. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol. 69(2):376–389. Hou S, Gu H, Smith C, Ren D. 2011. Microtopographic patterns affect Escherichia coli biofilm formation on poly (dimethylsiloxane) surfaces. Langmuir. 27(6):2686–2691. Hu XL, Ho B, Lim CT, Hsu CS. 2011. Thermal treatments modulate bacterial adhesion to dental enamel. J Den Res. 90(12):1451–1456. Ionescu A, Wutscher E, Brambilla E, Schneider-Feyrer S, Giessibl FJ, Hahnel S. 2012. Influence of surface properties of resin-based composites on in vitro Streptococcus mutans biofilm development. Eur J Oral Sci. 120(5):458–465. Jansson T, Clare-Salzler ZJ, Zaveri TD, Mehta S, Dolgova NV, Chu B-H, Ren F, Keselowsky, BG. 2012. Antibacterial effects of zinc oxide nanorod surfaces. J Nanosci Nanotechnol. 12(9):7132–7138. Kolenbrander PE, Palmer RJ Jr, Periasamy S, Jakubovics NS. 2010. Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol. 8(7):471–480. Kuramitsu HK, He X, Lux R, Anderson MH, Shi W. 2007. Interspecies interactions within oral microbial communities. Microbiol Mol Bio Rev. 71(4):653–670. Lichter JA, Thompson MT, Delgadillo M, Nishikawa T, Rubner MF, Van Vliet KJ. 2008. Substrata mechanical stiffness can regulate adhesion of viable bacteria. Biomacromolecules. 9(6):1571–1578. Lin HY, Liu YL, Wismeijer D, Crielaard W, Deng DM. 2013. Effects of oral implant surface roughness on bacterial biofilm formation and treatment efficacy. Inter J Oral Maxillofacial Implants. 28(5):1226–1231. Mabboux F, Ponsonnet L, Morrier JJ, Jaffrezic N, Barsotti O. 2004. Surface free energy and bacterial retention to saliva-coated dental implant materials: an in vitro study. Colloids Surf B Biointerfaces. 39(4):199–205. Manabe K, Nishizawa S, Shiratori S. 2013. Porous surface structure fabricated by breath figures that suppresses Pseudomonas aeruginosa biofilm formation. ACS Appl Mater Interfaces. 5(22):11900–11905. Marmur A. 2003. Wetting on hydrophobic rough surfaces: to be heterogeneous or not to be? Langmuir. 19(20):8343–8348. Marsh PD, Moter A, Devine DA. 2011. Dental plaque biofilms: communities, conflict and control. Periodontology. 55(1):16–35.

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8

Journal of Dental Research 

Mi L, Jiang S. 2014. Integrated antimicrobial and nonfouling zwitterionic polymers. Angew Chem Int Ed Engl. 53(7):1746–1754. Nobbs AH, Lamont RJ, Jenkinson HF. 2009. Streptococcus adherence and colonization. Microbiol Mol Biol Rev. 73(3):407–450. Pan J, Sun K, Liang Y, Sun P, Yang X, Wang J, Zhang J, Zhu W, Fang J, Becker KH. 2013. Cold plasma therapy of a tooth root canal infected with Enterococcus faecalis biofilms in vitro. J Endod. 39(1):105–110. Perera-Costa D, Bruque JM, González-Martín MAL, Gómez-García AC, Vadillo-Rodriguez V. 2014. Studying the influence of surface topography on bacterial adhesion using spatially organized microtopographic surface patterns. Langmuir. 30(16):4633–4641. Perni S, Prokopovich P. 2013. Micropatterning with conical features can control bacterial adhesion on silicone. Soft Matter. 9(6):1844–1851. Pihlstrom BL, Michalowicz BS, Johnson NW. 2005. Periodontal diseases. Lancet. 366(9499):1809–1820. Pogodin S, Hasan J, Baulin VA, Webb HK, Truong VK, Phong Nguyen TH, Boshkovikj V, Fluke CJ, Watson GS, Watson JA, et al. 2013. Biophysical model of bacterial cell interactions with nanopatterned cicada wing surfaces. Biophys J. 104(4):835–840. Poncin-Epaillard F, Herry J, Marmey P, Legeay G, Debarnot D, BellonFontaine M. 2013. Elaboration of highly hydrophobic polymeric surface: a potential strategy to reduce the adhesion of pathogenic bacteria? Mater Sci Eng C. 33(3):1152–1161. Pranzetti A, Mieszkin S, Iqbal P, Rawson FJ, Callow ME, Callow JA, Koelsch P, Preece JA, Mendes PM. 2013. An electrically reversible switchable surface to control and study early bacterial adhesion dynamics in real-time. Adv Mater. 25(15):2181–2185. Quirynen M, Bollen CM.1995. The influence of surface roughness and surfacefree energy on supra- and subgingival plaque formation in man: a review of the literature. J Clin Periodontol. 22:1–14. Quirynen M, Bollen CM, Papaioannou W, Van Eldere J, van Steenberghe D. 1996. The influence of titanium abutment surface roughness on plaque accumulation and gingivitis: short-term observations. Int J Oral Maxillofac Implants. 11(2):169–178. Renner LD, Weibel DB. 2011. Physicochemical regulation of biofilm formation. MRS Bull. 36(5):347–355.

Rzhepishevska O, Hakobyan S, Ruhal R, Gautrot J, Barbero D, Ramstedt M. 2013. The surface charge of anti-bacterial coatings alters motility and biofilm architecture. Biomater Sci. 1(6):589–602. Saha N, Monge C, Dulong V, Picart C, Glinel K. 2013. Influence of polyelectrolyte film stiffness on bacterial growth. Biomacromolecules. 14(2):520–528. Scardino AJ, de Nys R. 2011. Mini review: biomimetic models and bioinspired surfaces for fouling control. Biofouling. 27(1):73–86. Siegismund D, Undisz A, Germerodt S, Schuster S, Rettenmayr M. 2014. Quantification of the interaction between biomaterial surfaces and bacteria by 3-D modeling. Acta Biomater. 10(1):267–275. Siqueira WL, Custodio W, McDonald EE. 2012. New insights into the composition and functions of the acquired enamel pellicle. J Dent Res. 91(12):1110–1118. Song F, Ren D. 2014. Stiffness of cross-linked poly (dimethylsiloxane) affects bacterial adhesion and antibiotic susceptibility of attached cells. Langmuir. 30(34):10354–10362. Teughels W, Van Assche N, Sliepen I, Quirynen M. 2006. Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res. 17 Suppl 2:68–81. Venault A, Yang HS, Chiang YC, Lee BS, Ruaan RC, Chang Y. 2014. Bacterial resistance control on mineral surfaces of hydroxyapatite and human teeth via surface charge-driven antifouling coatings. ACS Appl Mater Interfaces. 6(5):3201–3210. Wang Q, Suzuki A, Mariconda S, Porwollik S, Harshey RM. 2005. Sensing wetness: a new role for the bacterial flagellum. EMBO J. 24(11):2034–2042. Wang Z, Shen Y, Haapasalo M. 2014. Dental materials with antibiofilm properties. Dent Mater. 30(2):e1–e16. Xing R, Lyngstadaas SP, Ellingsen JE, Taxt-Lamolle S, Haugen HJ. 2014. The influence of surface nanoroughness, texture and chemistry of TiZr implant abutment on oral biofilm accumulation. Clin Oral Implants Res. 2014:1–8. Xu LC, Siedlecki CA. 2014. Staphylococcus epidermidis adhesion on hydrophobic and hydrophilic textured biomaterial surfaces. Biomed Mater. 9(3):035003. Zhang X, Wang L, Levanen E. 2013. Superhydrophobic surfaces for the reduction of bacterial adhesion. RSC Adv. 3:12003–12020.

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Effects of Material Properties on Bacterial Adhesion and Biofilm Formation.

Adhesion of microbes, such as bacteria and fungi, to surfaces and the subsequent formation of biofilms cause multidrug-tolerant infections in humans a...
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