Modification of the surfaces of medical devices to prevent microbial adhesion and biofilm formation

Journal of Hospital Infection 85 (2013) 87e93 Available online at www.sciencedirect.com

Journal of Hospital Infection journal homepage: www.elsevierhealth.com/journals/jhin

Review

Modification of the surfaces of medical devices to prevent microbial adhesion and biofilm formation ´ d, e, * C. Desrousseaux a, d, V. Sautou a, b, S. Descamps a, c, O. Traore a

Clermont Universite´, Universite´ d’Auvergne, C-BIOSENSS, Clermont-Ferrand, France CHU Clermont-Ferrand, Service Pharmacie, Clermont-Ferrand, France c CHU Clermont-Ferrand, Service de Chirurgie Orthope´dique, Clermont-Ferrand, France d LMGE «Laboratoire Micro-organismes: Ge´nome et Environnement», Clermont Universite´, Universite´ Blaise Pascal et Universite´ d’Auvergne, Clermont-Ferrand, France e CHU Clermont-Ferrand, Service d’Hygie`ne Hospitalie`re, Clermont-Ferrand, France b

A R T I C L E

I N F O

Article history: Received 8 February 2013 Accepted 27 June 2013 Available online 2 September 2013 Keywords: Medical devices Microbial adhesion Nanostructures

S U M M A R Y

Background: The development of devices with surfaces that have an effect against microbial adhesion or viability is a promising approach to the prevention of device-related infections. Aim: To review the strategies used to design devices with surfaces able to limit microbial adhesion and/or growth. Methods: A PubMed search of the published literature. Findings: One strategy is to design medical devices with a biocidal agent. Biocides can be incorporated into the materials or coated or covalently bonded, resulting either in release of the biocide or in contact killing without release of the biocide. The use of biocides in medical devices is debated because of the risk of bacterial resistance and potential toxicity. Another strategy is to modify the chemical or physical surface properties of the materials to prevent microbial adhesion, a complex phenomenon that also depends directly on microbial biological structure and the environment. Anti-adhesive chemical surface modifications mostly target the hydrophobicity features of the materials. Topographical modifications are focused on roughness and nanostructures, whose size and spatial organization are controlled. The most effective physical parameters to reduce bacterial adhesion remain to be determined and could depend on shape and other bacterial characteristics. Conclusions: A prevention strategy based on reducing microbial attachment rather than on releasing a biocide is promising. Evidence of the clinical efficacy of these surfacemodified devices is lacking. Additional studies are needed to determine which physical features have the greatest potential for reducing adhesion and to assess the usefulness of antimicrobial coatings other than antibiotics. ª 2013 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.

Introduction * Corresponding author. Address: Service d’Hygie `ne Hospitalie `re, Ho ˆpital G. Montpied, rue Montalembert, BP 69, 63003 Clermont Ferrand Cedex 1, France. Tel.: þ33 473 754 870; fax: þ33 473 754 871. E-mail address: [email protected] (O. Traore ´).

Invasive medical devices are widely used for diagnostic and therapeutic purposes in most medical specialties. Infectious risk is one of the most frequent complications related to the

0195-6701/$ e see front matter ª 2013 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jhin.2013.06.015

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use of indwelling medical devices such as orthopaedic or cardiac prostheses, vascular catheters, urinary catheters and endotracheal tubes. Medical device-related infections are a public health concern and an economic burden. For example, more than 5 million central venous catheters are implanted annually in the USA, of which more than 80,000 lead to catheter-related bacteraemia.1 In a study conducted in four European countries, catheter-related bloodstream infections accounted for more than 1000 deaths per year and per country, and entailed associated costs of V35 to V164 million per year and per country.2 The role of biofilms in medical device-related infections is clearly established.3 Biofilms are structured communities of micro-organisms that adhere to one another on a living or abiotic surface and produce extracellular polymeric substances which protect them from the external environment. Sessile bacteria in biofilm express phenotypic and genotypic characteristics different from their planktonic form.3 They become more resistant to antimicrobial stress and to the immune system; hence biofilms constitute a significant virulence factor.3,4 Because it is difficult to eliminate biofilm, removal of the contaminated device is often the only way to treat infections. One promising way of preventing invasive device-related infections is the development of medical devices with surfaces or materials that have an action against microbial adhesion or viability.5 The first strategy to be explored was the use of biocides, with the development of coatings that release antimicrobials or kill micro-organisms by contact.6e10 Many clinical trials have been performed, yielding conflicting results.3 Some authors fear that long-term extensive use of biocides on coatings and the release of subinhibitory concentrations could lead to increased antibiotic resistance.11 However, this risk remains mainly theoretical. The other strategy consists in developing anti-adhesive materials against bacteria. With less bacterial adhesion, the risk of biofilm formation could be reduced or delayed. Depending on the clinical application, even a slight delay in biofilm development could be beneficial, for example when indwelling time is short and the risk of device-related infection appears soon after the device is implanted. This review focuses on the anti-adhesive strategies used to design medical device surfaces that could potentially limit microbial growth, biofilm formation, and, in particular, the initial stage of microbial adhesion.

Mechanisms of bacterial adhesion Bacterial adhesion is a complex, multifactorial phenomenon. The properties of the surface material and those of the bacteria and the environment where the adhesion takes place are all factors that interfere with adhesion.12 Different theories have been developed to model the physicochemical interactions that determine bacterial adhesion. The classical DLVO theory (Derjaguin, Landau, Verwey, Overbeek) assimilates bacteria to inert colloidal particles, and in the thermodynamic theory bacterial attachment is interpreted as a spontaneous decrease in the free energy in a system. These models are detailed in the article by Hermansson.13 However, these models are limited because they are based on physicochemical interactions between surfaces and neglect the biological aspects of adhesion such as the role of specific bacterial structures called adhesins, which are involved in adhesion to another cell or to an abiotic surface.14 The medium in which adhesion takes place is also a

major factor. The ionic strength and pH of the solution influence the charge of the cell wall and of the substrate and hence the interactions between them. The presence of proteins can promote (fibronectin) or limit (albumin) bacterial adhesion. Finally, flow conditions can also influence the attachment of bacteria, with shear stress being a critical factor.12

Anti-adhesive chemical strategy Hydrophobicity and surface charge Bacterial adhesion depends on the hydrophobicity of the surface of cells and material. The most widely studied surface chemical properties of bacteria are hydrophobicity and surface charge, both of which depend on the composition of the bacterium’s external structure.12,15,16 A classical differentiation is made between Gram-negative and Gram-positive bacteria. The surface of Gram-negative bacteria is composed of an outer membrane with lipids and lipopolysaccharides, whereas Gram-positive bacteria have a cell wall with peptidoglycans and teichoic acids. These different structures explain the variety in the chemical properties of the bacterial surfaces. Bacterial surfaces with a high nitrogen:carbon ratio due to the presence of proteins are more hydrophobic. Hydrophilic surfaces have a high oxygen:carbon ratio.17,18 Hydrophobicity/hydrophilicity depends on the strain but also on the age of the micro-organisms or the environment.19 Materials can also be characterized by their hydrophobicity and their surface charge. Metallic materials are generally hydrophilic and negatively charged whereas for polymers these characteristics depend on their composition. Surface hydrophobicity or hydrophilicity is characterized by surface wettability, which can be measured by the contact angle. There is also a correlation between cell surface wettability and adhesion.20 It is generally accepted that hydrophobic cells attach more strongly to a surface and that all bacteria tend to adhere more strongly to hydrophobic material.16,21 Attachment between two hydrophobic elements is favoured because their interactions are strong. However, the process is perhaps more complicated. Adhesion might be more extensive to hydrophilic materials than to hydrophobic materials when the surface tension of the bacteria is larger than that of the suspending medium. The opposite pattern might prevail when the surface tension of the suspending liquid is larger than that of the bacteria.20 These results have been confirmed experimentally by selfautoassembled monolayers (SAMs). SAMs can modulate the different moieties exposed on a surface, and are used for bacterial adhesion studies as a model of surfaces with controlled chemical properties.22,23 SAMs functionalized with hydrophilic moieties (OH, NH2) tend to reduce bacterial adhesion compared with hydrophobic surfaces functionalized with methylated groups (CH3).24e27 Several hydrophilic coatings, such as hydrogels or chemically modified surfaces of medical devices, have been developed to limit biofilm development. Heparin or hyaluronic acid may be added to hydrophilic coatings.28 Heparin has not only an anticoagulant activity but also an anti-adhesive activity due to its hydrophilic characteristics. Clinical studies have reported that heparin-coated urinary catheters can reduce biofilm and organic and inorganic encrustation by Proteus mirabilis.29,30 In an experimental model mimicking catheter lock, others have shown that

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heparin in solution can stimulate the kinetics of biofilm formation by several strains of Staphylococcus aureus by increasing cellecell interactions without affecting primary adhesion.31 This example demonstrates that parameters other than initial adhesion could influence biofilm formation. In certain cases, fighting against initial adhesion is not always sufficient to avoid biofilm development. Plasma treatments can also create hydrophilic moieties at the surface of the medical device, resulting in antifouling and antimicrobial activity.32,33 With regard to surface charge, as bacteria are negatively charged in a neutral medium it is thought that they adhere preferentially to positively charged materials (attractive forces) and less to negatively charged surfaces (repulsive forces).34,35 However, opinions differ on the influence of the surface charge on adhesion.

circuits common to Gram-positive and -negative bacteria.49 Substances that interfere with the communication between cells are less likely to cause bacterial resistance than bactericidal or bacteriostatic substances. Another way to avoid the development of biofilm could be to limit initial microbial adhesion by disrupting the biofilm.50,51 Coatings with enzymes such as dispersin-B, which hydrolyses poly-N-acetylglucosamine, a polysaccharide very frequently found in the extracellular matrix of biofilm, can effectively prevent the formation of a biofilm. Coatings with dispersin-B enzymes in combination with antimicrobials such as triclosan or cefamandole nafate are being developed.52e54 The in vitro synergistic activity of the combination of antimicrobials and dispersin-B could be due to the fact that dispersin-B makes biofilm-embedded bacteria more susceptible to antimicrobial action.52

Steric barrier Chemical modifications of surfaces can also consist in grafting long chain polymers to form a brush-like structure on the surface. The density of the chains provides a steric barrier that repels bacterial adhesion by minimizing covalent interactions. The most widely studied brush polymers are polyethylene oxide derivatives. Polyethylene glycol (PEG) has been shown to be effective against protein fouling.36,37 Indeed, SAMs functionalized with ethylene glycol (4EG and 3EG) have lower bacterial adhesion than even hydrophilic surfaces.24,25 However, several authors have demonstrated that the hypothesis that surfaces resistant to protein adsorption are also resistant to the adhesion of bacteria cannot always be verified because the mechanisms of adsorption/adhesion vary.38,39 Nevertheless, brush-like structures are used to fix other compounds such as peptides or enzymes, for example, or to compose copolymer coatings in order to create a coating combining anti-adhesive and antimicrobial properties.40e43 Recent reports have identified after screening of different polymers new classes of polymers with reduced bacterial adhesion. The results, which could not have been predicted from the current theories of bacterial adhesion, show that polymers with ester moieties ðCHO2  Þ or cyclic hydrocarbon moieties (C4H, C6H) afford less strong bacterial attachment than materials with ethyl glycol (C2H3Oþ, C2H3O) and hydroxyl fragment groups ðC4 H2 O2  ; C6 H11 O3  Þ.5

Anti-adhesive strategy based on surface topographic modifications

Coatings with bioinspired molecules In the search for new molecules with anti-adhesive properties, workers have tried to identify the mechanisms that render living organisms resistant to micro-organism colonization.44 The chemical composition of the external surfaces of bacteria could be of interest in future research. For example, studies have shown that secreted bacterial polysaccharides have anti-adhesive characteristics.45,46 One current trend is the development of antimicrobial coatings that interfere with quorum-sensing (QS) mechanisms. It has been found that halogenated furanones synthesized by the red alga Delisea pulchra have anti-adhesive properties against a wide range of bacteria.47 Furanones have structural similarities with AHLs (N-acyl homoserine lactones), which are the main molecules of the quorum sensing for Gram-negative bacteria. Furanones interfere with the QS by fixing on the binding site of AHLs.48 It seems that furanones can also disrupt other communication

The physical aspect of the material surface has long been neglected in the theories of bacterial adhesion. The relief of a surface is dependent on the scale at which it is examined. For bacterial adhesion, the small scale level of defaults on the surface, i.e. the submicron level, is studied. Among the different reliefs, two groups can be distinguished: (i) surfaces with random or irregular features defined as roughness; (ii) surfaces with organized features, frequently made by an engineered process, defined by the term surface topography.

Surface roughness A surface can be considered as a succession of peaks and valleys with various heights and spacings in a plane. The profile of a surface with submicron features is measured with an atomic force microscope (AFM).55 The roughness parameter most frequently studied is an amplitude parameter: the roughness average (Ra) that describes the typical height variation of the surface.56 Attempts have been made to find an association between bacterial adhesion and surface roughness. Many roughness studies concern metallic surfaces such as titanium used for biomaterials but data on polymers are scarce. It is generally accepted that the smoother a surface is, the lower the probability of bacterial adhesion, but some studies have suggested otherwise. Whitehead and Verran showed in their review that, in many studies which assume that smooth stainless steel is more hygienic, no firm evidence of the assumption is provided.57 One study showed that Staphylococcus epidermidis adhesion was similar on titanium surfaces with different roughnesses.58 Wu et al. obtained a coverage by S. epidermidis of about 59% for a satin-finished titanium surface (Ra ¼ 0.83 mm) and 52% for a grit-blasted surface (Ra ¼ 11 mm) whereas polished surfaces (Ra ¼ 0.006 mm) and plasma-sprayed titanium (Ra ¼ 33 mm) surfaces had a coverage of around 10%.59 SEM observations show that this strain tends to adhere to grooves and depressions whose dimensions are similar to those of bacteria.59 Taylor et al. compared the adhesion of Pseudomonas aeruginosa and S. epidermidis to polymethylmethacrylate surfaces within a range of roughness states (Ra between 0.04 and 7.89 mm). The smallest increase in roughness from 0.04 to 1.86 mm increased bacterial adhesion

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nearly twofold. However, the other surfaces with higher Ra values had a bacterial coverage similar to that of the smooth surface (Ra ¼ 0.04 mm).60 Thus, in these cases, adhesion is not greater on the surface with the highest Ra value, suggesting that the relationship between roughness and bacterial adhesion is not linear. It seems that bacterial adhesion is enhanced when the features of the surface have dimensions or spacing similar to bacterial size (the micrometer scale).57,59,61 This type of surface configuration could increase adhesion because of increased surface contact and because bacteria may be protected against shear stress. With submicron roughness, bacterial adhesion is less well understood. Some studies showed an increase in bacterial adhesion on nanorough surfaces whereas others showed greater adhesion on nanosmooth surfaces.62e65 Studies on the impact of surface roughness on bacterial adhesion are often limited to amplitude parameters.62,63 Crawford et al. recommend that spatial parameters, which describe the distance between two points of the same height, and hybrid parameters, which combine amplitude and spacing parameters, should be used to characterize a surface in relation to bacterial adhesion.56

Surface topography There exist few studies on the effect on bacteria of surface topography with topographical features around or below the size of bacteria. Whether bacteria can ‘sense’ the dimensions of nanoscale is debated. As bacteria have a rigid wall it could be postulated that they are less sensitive to nanofeatures than eukaryotic cells. Bacterial structures such as pili might play the main role in adhesion at the nanoscale level, and nanostructures could afford them a stronger point of attachment.66,67 However, experiments comparing mutant bacteria without pili or fimbriae and their wild type showed the same pattern of adhesion on nanostructured surfaces.68 Nano- or microfeatures are multiple and are mostly characterized by their size (usually from 10 nm to 3 mm), shape or spatial organization. These parameters can be variably controlled depending on the manufacturing technique.66 It will be crucial to determine which parameters of nanofeatures are most effective in reducing the adhesion of bacteria. Topographic or nanoroughness modifications can change surface properties such as wettability.69 For example, the surface of titania nanotubes is more hydrophilic than a conventional titanium surface.70e72 These properties have biomedical applications in orthopaedics, improving osteointegration and decreasing bacterial adhesion.73,74 In addition, nanotubes could be filled with biocide to improve their action against biofilm.74,75 Superhydrophobic surfaces are also being developed with nano- or microfeatures to create auto-cleaning devices.76,77 In conditions of circulating media, the modified surface features could create modified nanoforce conditions, which, in turn, could have an impact on microbial attachment.78

Influence of physical structuring of nanofeatures on bacterial response Nanofeatures can have very different shapes: nanotubes, grooves, channels or ridges, pits or pillars.59,67,68,70,71,73,75,79e87 A few nanostructured surfaces are illustrated in Figure 1.

Figure 1. Scanning electron microscopic images of nanostructured surfaces: (A) nanopores in aluminium anodized; (B) titanium dioxide nanotubes; (C) 200 nm high polymethylmethacrylate nanopillars; (D) 70 nm high polymethylmethacrylate nanopillars. Scale bars are 200 nm.

No study has compared the adhesion of micro-organisms according to shape, and it is difficult to find a common parameter by which to compare all surfaces. The influence of size has been studied for given shapes of nanofeatures. For example, Ercan et al. compared the adhesion of S. aureus and S. epidermidis to commercial titanium surfaces and to nanotube surfaces with a diameter between 20 and 80 nm. A decrease in bacterial adhesion was observed for the largest diameters (60 and 80 nm).70 However, the study of Yu et al. yielded conflicting results: staphylococci adhesion increased in proportion to the diameter of the nanotubes (30, 70 and 120 nm).73 The spatial organization of the nanofeatures, especially the distance between them, is also an important parameter that can influence bacterial adhesion. Hochbaum and Aizenberg worked on nanostructured surfaces with posts arranged with square symmetry. The adhesion of P. aeruginosa was extremely sensitive to the distance between two adjacent posts on the side length of the square (called pitch), which varied from 0.9 to 4 mm. Adhesion increased with the reduction in this spacing. When this spacing was greater than the length of P. aeruginosa, adhesion was random. When it was between 1.2 and 1.5 mm (about the length of the bacterium), P. aeruginosa adhered along the plots (direction of the square side then the diagonal square). At 0.9 mm spacing, bacteria were perpendicular to the substrate and parallel to the axis of the posts.68 The arrangement of nanostructures can form larger patterns that may have various effects on microbial adhesion. For example, the positioning of the ridges on polymers with these types of nanofeatures can enhance or inhibit bacterial adhesion. Zhang et al. developed several imprinted polystyrene substrates with surfaces including either single-level 2 mm or 250 nm gratings, or hierarchical surfaces with both gratings (2 mm and 250 nm) arranged in parallel or perpendicularly.67 They showed that the hierarchical substrates enhance the adhesion of Escherichia coli compared with that of single-level surfaces.67 Another motif composed of ridges (2 mm width, 3 mm spacing and different lengths) in polydimethyl siloxane elastomer was bioinspired from shark skin. This structured elastomer presented no sign of biofilm formation of S. aureus after 14 days, unlike the smooth surface, which allowed mature biofilm to form.81

C. Desrousseaux et al. / Journal of Hospital Infection 85 (2013) 87e93 Finally, the interpretation of the effect of physical features may be even more complicated by the fact that the chemistry of the surface, if not characterized in parallel, can interfere with microbial adhesion. This could explain why different studies have yielded conflicting results.

3.

Influence of test micro-organisms

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As seen above, at the nanoscale level, the size and the shape of bacteria in relation to the dimensions of nanofeatures play an important role. Bacterial characteristics (adhesins, charge surface) are also important in the adhesion process. A nanostructured surface should be tested with various strains of different bacterial species because they exhibit different adhesion behaviours. For example, titanium surfaces nanostructured by femtosecond laser ablation, mimicking the superhydrophobic surface of a lotus leaf, were not colonized at 18 h by P. aeruginosa whereas adhesion of S. aureus was greater than on a polished surface.77 Such a result suggests that some nanostructured surfaces might not be suitable for medical applications in which the micro-organisms are unknown and very diverse.

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Conclusion The development of micro-organisms on medical devices involves multiple physicochemical and biological parameters depending on the properties of the micro-organisms and of the materials, and on the environment. To control medical devicerelated infections, strategies aimed at reducing microbial attachment could be an interesting complement to those based on the release of biocides. The efficacy of surface-modified medical devices in reducing infection without biocide molecules has so far been assessed mainly in vitro and only rarely in clinical studies. Furthermore, most studies take into account only one or two parameters of microbial adhesion whereas the process is multifactorial. This could explain the conflicting results observed. Further studies are needed to determine the physical nanostructures most likely to reduce adhesion. Depending on the size and shape of the micro-organisms, these structures may differ. The association of these structures with bio-inspired non-antibiotic antimicrobial coating is also an interesting approach that warrants further investigation.

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Acknowledgement

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The authors thank J. Watts for his help in preparing the manuscript and A.-M. Gelinaud of the technological platform Casimir for SEM observations.

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Conflict of interest statement C. Desrousseaux is supported by Cair LGL, manufacturer of medical devices.

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Funding sources None.

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