Dual-function antibacterial surfaces for biomedical applications.

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Contents lists available at ScienceDirect

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Review

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Dual-function antibacterial surfaces for biomedical applications

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Qian Yu, Zhaoqiang Wu ⇑, Hong Chen

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College of Chemistry, Chemical Engineering and Materials Science, Soochow University, 199# Ren’ai Road, Suzhou 215123, China

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a r t i c l e

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Article history: Received 20 September 2014 Received in revised form 24 December 2014 Accepted 16 January 2015 Available online xxxx

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Keywords: Antibacterial Bactericidal Bacteria-resistant Bacteria-release Functional surface

a b s t r a c t Bacterial attachment and the subsequent formation of biofilm on surfaces of synthetic materials pose a serious problem in both human healthcare and industrial applications. In recent decades, considerable attention has been paid to developing antibacterial surfaces to reduce the extent of initial bacterial attachment and thereby to prevent subsequent biofilm formation. Briefly, there are three main types of antibacterial surfaces: bactericidal surfaces, bacteria-resistant surfaces, and bacteria-release surfaces. The strategy adopted to develop each type of surface has inherent advantages and disadvantages; many efforts have been focused on the development of novel antibacterial surfaces with dual functionality. In this review, we highlight the recent progress made in the development of dual-function antibacterial surfaces for biomedical applications. These surfaces are based on the combination of two strategies into one system, which can kill attached bacteria as well as resisting or releasing bacteria. Perspectives on future research directions for the design of dual-function antibacterial surfaces are also provided. Ó 2015 Published by Elsevier Ltd. on behalf of Acta Materialia Inc.

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1. Introduction

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Bacterial attachment and the subsequent proliferation and colonization of bacteria on the surfaces of synthetic materials usually result in the formation of a biofilm [1–4]. This bacterial biofilm poses a major problem in both human healthcare and industrial applications, including but not limited to public health settings, surgical equipment, biosensors, textiles, water purification systems, and packaging [5,6]. For medical implants and devices, bacterial attachment adversely affects the functionality and limits the lifetime of devices, and bacterial infections represent a common and substantial complication in the clinic, sometimes even leading to death [7,8]. For food processing and packaging materials, the accumulation of bacteria has a serious impact on processing efficiency, productivity, and food quality [9]. For marine equipment, microbial contamination on surfaces provides an easily accessible platform for other marine species to attach and proliferate, leading to an increase in the cost of operation and maintenance [10]. To solve these problems, considerable efforts have been directed toward developing antibacterial surfaces that can greatly reduce the extent of initial bacterial attachment and thereby prevent subsequent biofilm formation [11–16]. In recent decades, various antibacterial surfaces have been designed, which can be divided into three categories based on

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⇑ Corresponding author. E-mail address: [email protected] (Z. Wu).

the their operating mechanisms: (i) bactericidal surfaces for killing attached bacteria; (ii) bacteria-resistant surfaces for preventing the initial attachment of bacteria; and (iii) bacteria-release surfaces for reducing the adhesion between bacteria and material surfaces and facilitating the release of attached bacteria by an external force. Although remarkable progress has been made in the development of these antibacterial surfaces, each methodology has inherent advantages and disadvantages. For example, bactericidal surfaces can prevent the formation of viable biofilms, but these surfaces will still be contaminated by remaining dead bacteria, which may trigger immune responses or inflammation [17]. In addition, these surfaces suffer the problems of ecotoxicity of biocides toward nontargeted species and poor compatibility with mammalian cells. On the other hand, bacteria-resistant surfaces or bacteria-release surfaces can prevent or reduce the initial attachment of bacteria; however, to date, no such surfaces can achieve 100% prevention of bacterial attachment, inevitably becoming colonized by bacteria that are not killed once they attach themselves to the surfaces. Therefore, an ideal antibacterial surface that can perform the following functions is required: (i) first, prevent initial bacterial attachment; (ii) subsequently, kill all bacteria that manage to overcome this anti-adhesion barrier; and (iii) finally, remove dead bacteria. To achieve this goal, several groups have developed surfaces by combining two strategies into one system. Over the past decade, excellent reviews on the fabrication and application of antibacterial surfaces with a single functionality have been published [18–22]; however, to the best of our knowledge, few reviews on dual-function antibacterial surfaces have been published [23].

http://dx.doi.org/10.1016/j.actbio.2015.01.018 1742-7061/Ó 2015 Published by Elsevier Ltd. on behalf of Acta Materialia Inc.

Q1 Please cite this article in press as: Yu Q et al. Dual-function antibacterial surfaces for biomedical applications. Acta Biomater (2015), http://dx.doi.org/ 10.1016/j.actbio.2015.01.018

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In this review, we first briefly introduce three main strategies for designing antibacterial surfaces with a single functionality: bactericidal surfaces, bacteria-resistant surfaces and bacteriarelease surfaces. We then highlight recent developments in the creation of dual-function antibacterial surfaces based on the combination of two strategies (e.g., kill/resist or kill/release) into one system for biomedical applications. Finally, we conclude by presenting future research directions for developing dual-function antibacterial surfaces.

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2. Basic strategies for designing antibacterial surfaces

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2.1. Bactericidal surfaces

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Bactericidal surfaces refer to surfaces that are capable of killing bacteria. According to the killing mechanism, these surfaces can be divided into two main categories: contact-based bactericidal surfaces and release-based bactericidal surfaces.

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2.1.1. Contact-based bactericidal surfaces Contact-based bactericidal surfaces are surfaces that are coated with antibacterial agents by either covalent conjugation or physical adsorption to kill adhering bacteria. The antibacterial agents used in this respect range from synthetic chemicals such as quaternary ammonium compounds (QACs), polycations and various antibiotics to natural biomolecules such as chitosan, antimicrobial peptides (AMPs) and antimicrobial enzymes (AMEs). Herein, we introduce several typical examples. QACs with both long hydrophobic alkyl chains and positively charged quaternary ammonium groups have been demonstrated to show strong contact-killing activity toward both Gram-positive and Gram-negative bacteria. The ion exchange of QAC molecules with Ca2+ and Mg2+ ions in the cytoplasmic membrane destabilizes the intracellular matrix of a bacterium; additionally, the hydrophobic tail interdigitates into the hydrophobic bacterial membrane over the entire surface area of a bacterium, causing general perturbations in the cytoplasmic membrane and leakage of intracellular fluid containing essential molecules [24,25]. One typical QAC is the quaternary ammonium silane of 3-(trimethoxysilyl)-propyldimethyloctadecyl ammonium chloride (QAS, Fig. 1a), which can be easily immobilized onto OH-containing surfaces (such as

Fig. 1. Chemical structures of (a) 3-(trimethoxysilyl)-propyldimethyloctadecyl ammonium chloride (QAS), (b) quaternized poly(4-vinyl-N-alkylpyridinium bromide) (PVP), and (c) quaternized poly (2-(dimethylamino ethyl) methacrylate) (PDMAEMA).

silicone rubber [26], cotton [27], titanium [28], silica particle [29], and cellulose [30]) by covalent bonds. In addition to QAS, polymers with quaternary ammonium groups in their side chains have also been explored as polymeric biocides. Quaternized poly(4-vinyl-N-alkylpyridinium bromide) (PVP, Fig. 1b) [31,32] and quaternized poly(2-(dimethylamino ethyl) methacrylate) (PDMAEMA, Fig. 1c) [33–35] are two typical biocidal polymers. For more information on antibacterial polymers, readers may refer to other reviews [20,36,37]. AMPs and AMEs represent natural alternatives to traditional synthetic biocidal compounds for developing bactericidal coatings. AMPs form an integral part of the innate immune system in most organisms. The advantages of AMPs include limited immunogenicity, rapid bactericidal behavior, and less susceptibility to proteolysis [38]. AMEs refer to a group of enzymes with abilities to directly attack the microorganism, interfere with biofilm formation, and/or catalyze reactions which result in the production of antimicrobial compounds [39]. According to the antibacterial mechanism, they can be divided into three categories: proteolytic enzymes, polysaccharide-degrading enzymes, and oxidative enzymes [40]. AMPs and AMEs can be immobilized on supporting surfaces either physically (e.g., via adsorption or layer-by-layer assembly) or chemically (e.g., via covalent bonding) to fabricate bactericidal coatings with a broad spectrum of antibacterial activity, high efficacy even at low concentrations, and lack of susceptibility to bacterial resistance [39–41].

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2.1.2. Release-based bactericidal surfaces Release-based bactericidal surfaces are surfaces within which biocides are preloaded or embedded before being released slowly into the environment to kill bacteria. The most widely used biocides are silver nanoparticles (AgNPs) because of their strong and broad-spectrum antibacterial characteristics [8,15,42–44]. The main mechanism through which AgNPs exert their biocidal properties is through the release of Ag+ ions, which damage the bacterial membrane as well as disrupt the function of bacterial enzymes and/or nucleic acid groups in cellular protein and DNA [45]. There are also several types of release-based bactericidal surfaces that use antibiotics [46–48] or nitrogen oxide [49–51] as releasing biocides to avoid bacterial infection.

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2.1.3. Dual-contact- and release-based bactericidal surfaces Several bactericidal surfaces with two different biocides incorporated into one system operate through both contact-based and release-based mechanisms. These surfaces are of particular interest because they can minimize the selection and proliferation of resistant strains, providing long-term antibacterial efficiency. For example, a thin film coating composed of two distinct, layered functional regions (i.e., a polyelectrolyte multilayer reservoir for the loading and release of bactericidal AgNPs and a SiO2 surface cap with immobilized QAS, as shown in Fig. 2) was developed [52]. Dual-function coatings of this type show high initial

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Fig. 2. Schematic illustration of a two-level dual-function bactericidal coating with both QAS and AgNPs. Reprinted with permission from Ref. [52], Copyright 2006, American Chemical Society.


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bacteria-killing efficiency due to the release of Ag+ ions and retain significant antibacterial activity after the depletion of embedded AgNPs because of the immobilized QAS. In another report, dual-action antibacterial composites consisting of a cationic polymer matrix and embedded silver bromide (AgBr) nanoparticles were fabricated simply by the on-site precipitation of AgBr nanoparticles [53]. The water-insoluble composites formed good coatings on glass and exhibited long-lasting antibacterial properties toward both airborne and waterborne bacteria. Similarly, a composite antibacterial coating was generated by lysozyme-mediated AgNP synthesis and electrophoretic deposition, demonstrating the antibacterial activity of Ag+ ions and the muramidase activity of lysozyme [54].

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2.1.4. Bactericidal surfaces with switchable biocidal activity Recently, several surfaces with biocidal activity that can switch in response to environmental stimuli (usually changes in temperature) have been developed. For example, a thermo-responsive copolymer based on 2-(2-methoxyethoxy)ethyl methacrylate (MEO2MA), hydroxyl-terminated oligo(ethylene glycol) methacrylate (OEGMA) and 2-hydroxyethyl methacrylate (HEMA) was grown on silicon surfaces, followed by covalent conjugation of AMP magainin-I on the polymer [55]. When the temperature is below the polymer’s collapse transition temperature (Tcoll), the copolymer chains are swollen and adopt an extended conformation, promoting the accessibility of AMPs to approaching bacteria and thereby killing the bacteria. On other hand, at temperatures above Tcoll, the progressive collapse of the polymer brushes provides a more hydrophobic environment for burying the AMPs, resulting in the suppression of bactericidal activity as illustrated in Fig. 3. In another report, a copolymer composed of two functional monomers, thermo-responsive N-isopropylacrylamide (NIPAAm) and biocidal 2-aminoethyl methacrylate, was synthesized. By crosslinking the copolymers with poly(ethyleneglycol) diglycidyl ether (PEGDE) on cotton, a non-leaching surface with a thermo-switchable, Gram-selective biocidal effect was obtained due to the responsive change in conformation and hydrophilicity [56]. Thermo-responsive poly(N-isopropylacrylamide-co-allylamine) (PNIPAAm-co-ALA) nanogels were synthesized and grafted onto non-woven polypropylene, followed by incorporation of silver nitrate. The composite coatings exhibited temperature-dependent biocidal activity against Staphylococcus aureus and Pseudomonas aeruginosa. At 28 °C, both types of bacteria grew well and proliferated on the coating surface, but at 37 °C, there was a reduction in bacterial growth due to the collapse of nanogels, releasing the AgNPs. This coating may find potential applications in wound dressing systems considering that an infected wound or infected skin has a significantly elevated temperature compared with normal tissues.

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2.2. Bacteria-resistant surfaces

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Bacteria-resistant surfaces are capable of reducing the extent of initial bacterial attachment and thereby preventing the earliest

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stages of biofilm formation. Because it is well accepted that the initial attachment of bacteria is facilitated by a layer of adsorbed protein, it is natural to assume that nonfouling surfaces that prevent non-specific interactions with the biological environment, in particular the adsorption of proteins, also reduce the ability of planktonic bacteria to adhere. These surfaces are usually modified with hydrophilic polymers or oligomers, which can form a physical barrier known as a hydration layer in aqueous environments. Bacteriaresistant surfaces are divided into two main categories according to the formation mechanism of the hydration layer: ethylene glycol (EG)-based surfaces and zwitterion-based surfaces.

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2.2.1. EG-based surfaces The most commonly used nonfouling hydrophilic materials are polymers or oligomers based on the ethylene glycol (EG) repeat unit, such as poly(ethylene glycol) (PEG) [57] and oligo(ethylene glycol) (OEG) [58]. It is reported that self-assembled monolayers (SAMs) of OEG-terminated alkanethiolates resist 99.7% of attachment of two types of bacteria with different phylogenies and natural environments (D. marina and Staphylococcus epidermidis) [59], Q4 and as the number of EG moieties increases, the negative interfacial tension between the OEG SAMs and water increases, leading to enhanced bacterial resistance [60]. Many researchers have fabricated a series of substrates coated or covalently grafted with EG-containing linear polymers [61,62], comb-like polymers with EG-containing side chains such as PHEMA (Fig. 4a) and POEGMA (Fig. 4b) [63–66], hyperbranched polymers [67,68], or EG-based hydrogels [69–72], aiming at resisting bacterial attachment for various applications ranging from those in the marine industry to biomedical devices.

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2.2.2. Zwitterion-based surfaces An alternative strategy for developing bacteria-resistant surfaces is based on biomimetic nonfouling zwitterionic polymers, which have an equimolar number of homogenously distributed anionic and cationic groups on their polymer chains. In contrast to EG-based surfaces, in which the hydration layer is maintained by weak hydrogen bonds, the hydration layer in zwitterionic materials is more tightly bound through electrostatic interactions, making these materials more effective in resisting the adhesion of fouling agents [22]. Jiang and co-workers developed a series of surfaces modified with zwitterionic polymers such as poly(sulfobetaine methacrylate) (PSBMA, Fig. 5a) [73,74] and poly(carboxybetaine methacrylate) (PCBMA, Fig. 5b) [75], which showed effective resistance toward the short-term adhesion of marine bacteria or biomedical bacteria and prevented the formation of biofilm [23,76]. Similarly, materials with mixed-charge layers uniformly distributed at the molecular level are equivalent to zwitterionic materials in their ability to show high resistance toward bacterial adhesion [77–79]. One typical example is a copolymer polymerized with the two oppositely charged monomers [2-(methacryloyloxy)ethyl] trimethylammonium chloride (TM) and 3-sulfopropyl methacrylate potassium salt (SA) as shown in Fig. 5c.

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Fig. 3. Schematic illustration of the grafted P(MEO2MA50-HOEGMA20-HEMA30) copolymer brushes conjugated with magainin-I peptide below and above the Tcoll.


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Fig. 4. Chemical structures of two EG-based comb-like nonfouling polymers: (a) PHEMA and (b) POEGMA.

Fig. 5. Chemical structures of zwitterion-based nonfouling polymers: (a) PSBMA, (b) PCBMA, and (c) copolymer of TM/SA (P(TM/SA)).

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Polypropylene membranes grafted with this copolymer with TM:SA in a 1:1 ratio showed overall balanced charges and good resistance toward bacterial growth and biofilm formation [79]. To the best of our knowledge, no material developed to date is able to completely resist the adhesion of bacteria. In addition, although bacteria-resistant surfaces can mainly prevent the initial attachment of bacteria, they do not actively interact with or kill bacteria. Therefore, these surfaces may eventually become contaminated due to defects during preparation or handling and deterioration of the coating in physiological media.

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2.3. Bacteria-release surfaces

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Unlike bacteria-resistant surfaces, bacteria-release surfaces allow the initial adhesion of bacteria but are able to release them under proper conditions. This strategy is widely adopted to combat marine biofouling (e.g., the adhesion and settlement of marine

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organisms (bacteria, algae, molluscs)). Silicone- and fluorine-based polymers are two major polymeric materials exhibiting fouling-release properties. The low surface energy of these polymers reduces the extent of polar and hydrogen bonding interactions with organisms, effectively lowering the adhesion strength and causing macrofouling organisms to be ‘‘released’’ from the surfaces upon the application of shear [18]. In recent decades, amphiphilic block copolymers with both hydrophobic and hydrophilic side chains have been shown to inhibit settlement and improve the release (i.e., reduce adhesion strength) of a range of biofoulers [18,80,81]. Moreover, inspired by the hierarchical structures exhibited by natural materials, engineered surfaces with special microand/or nano-topographies also provide a way to combat biofouling [17,82–86,6,87]. Stimuli-responsive surfaces show rapid and reversible changes in their physicochemical properties in response to small changes in environmental stimuli (e.g., temperature, pH, ionic strength, and light) [88,89]. Because bacteria–surface interactions are highly dependent on the properties of surfaces (such as wettability, surface charge, and morphology), the responsive transition of surface properties from a bacteria-adhesive state to a bacteria-repellent state may lead to the release of attached bacteria to render the surface clean, making stimuli-responsive surfaces good candidates as bacterial release surfaces [78,90–92]. Poly(N-isopropylacrylamide) (PNIPAAm) is the most commonly used and best studied thermo-responsive polymer [93]. Surfaces modified by PNIPAAm exhibit reversible surface wettability and bioadhesion properties in response to temperature changes across the lower critical solution temperature (LCST) [94–99]. Lopez and co-workers pioneered the study of interfacial interactions between PNIPAAm-modified surfaces and microorganisms, demonstrating the use of PNIPAAm as a fouling-release material [90]. When the temperature is changed across the LCST, PNIPAAm-modified surfaces can release not only newly attached bacteria but also fully developed biofilms (as illustrated in Fig. 6a) [100–108]. Surfaces modified with pH-responsive polymers can also be used for triggered bacterial release. Electrostatic interaction is the main driving force for this type of surface to attract (with the opposite charge) or repel (with the same charge) bacteria. For example, a tunable, mixed-charge copolymer surface containing positively charged quaternary amine monomers and negatively charged carboxylic acid monomers showed pH-responsive changes in surface charge [78]. Under acidic conditions, the surface is positively charged due to the protonation of the carboxylic acid group, resulting in the attraction of negatively charged bacteria. These adhered bacteria can be easily released as the bulk pH increases because of the transition of the surface charge from positive to neutral (as illustrated in Fig. 6b). This tunable surface can be used to collect a contaminant and then be externally stimulated to release the contaminant to allow the analysis of its composition. Apart from temperature- and pH-responsive surfaces, which are usually targeted for the release of bacteria that adhere for short periods, there are several methods that are designed to remove microbial biofilms from substrates. Simple elastomer surfaces capable of dynamic deformation in response to external stimuli, including changes in electrical voltage, mechanical stretching, and changes in air pressure, have been reported to effectively detach microbial biofilms and macro-fouling organisms [92] (as illustrated in Fig. 6c). For example, more than 80% of C. marina and Escherichia coli biofilms can be detached from such elastomer surfaces when the applied strain exceeds critical values ranging from 2% to 14%. The same strategy has been extended to the on-demand detachment of infectious biofilms from the previously inaccessible main drainage lumen of urinary catheters [109]. Another method for removing biofilms is based on electrochemistry [110–112]. By operating at potentials or current densities that


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Fig. 6. Typical bacteria-release surfaces based on (a) thermo-responsive polymer, (b) pH-responsive polymer, and (c) electrical voltage-responsive polymer.

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promote hydrogen evolution from a biofouled surface, a 10-day old P. aeruginosa biofilm formed on stainless steel 316L substrates could be completely removed in a matter of seconds [112]. The removal mechanism is based predominantly on the electrochemical formation of hydrogen gas bubbles at the porous biofilm/substrate interface, which then mechanically detach the biofilm.

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3. Dual-function antibacterial surfaces

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There are three types of dual-functionality based on the combination of antibacterial surfaces with single functionality: resist and release, kill and resist, and kill and release. The first type of surfaces themselves do not exhibit biocidal activity and they have been widely used for combating marine biofouling; these surfaces can inhibit the settling stages of bacteria and other fouling organisms and/or reduce the adhesion strength of the organisms that have colonized the surface and release them under proper condition [25,113–115]. In contrast, the latter two types of surfaces are composed of antibacterial agents and bacteria-resistant or bacteria-release agents to realize the dual functionality via both ‘‘offensive’’ and ‘‘defensive’’ approaches, which are more suitable for biomedical applications. Therefore, in the following section, we focus on the recent developments of ‘‘kill and resist’’ and ‘‘kill and release’’ antibacterial surfaces.

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3.1. Kill and resist

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The first type of dual-function antibacterial surfaces is based on the combination of bactericidal and bacteria-resistant properties. These surfaces can be divided into three categories based on the method used to incorporate biocides into nonfouling materials. The biocides can be (i) tethered to nonfouling hydrophilic

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polymers, (ii) alternately deposited with an anti-adhesive layer, or (iii) stored in a nonfouling matrix and substantially released.

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3.1.1. Hydrophilic polymer as a spacer or a nonfouling agent Hydrophilic polymers are widely used as spacers for the immobilization of bioactive molecules to create biofunctional surfaces because (i) they are capable of resisting non-specific protein adsorption as well as bacteria and cell adhesion, thereby reducing unwanted biological responses; (ii) they can provide a hydrophilic microenvironment to maintain the bioactivity of biomolecules, and (iii) they can enhance the accessibility of end-immobilized active molecules to targets [116–119]. In recent years, several hydrophilic polymers have been used for the attachment of antibiotic molecules to create antibacterial surfaces with both bactericidal and bacterial-resistant properties. PEG is one of the best known nonfouling polymers. Using PEG with different terminal groups as spacers, several antibiotics, including penicillin [120,121], ampicillin [122] and gentamicin [123], can be immobilized on polymeric substrates (as shown in Fig. 7a). Specifically, the immobilization of randomly mixed PEG of two different molecular weights introduces molecular roughness and increases the effective surface area in contact with bacteria, resulting in enhanced antibacterial functionality [120]. Two different antibiotics—penicillin and gentamicin—can then be attached to the PEG-grafted polypropylene surfaces using two different types of conjugation chemistry, aiming at simultaneously resisting the growth of their target bacteria strains, Gram-positive S. aureus and Gram-negative Pseudomonas putida, respectively [123]. One main drawback of antibacterial surfaces based on PEG is that the concentration of biocidal groups available is quite limited because each grafted PEG chain has only one functional group at its free end. To increase the density of binding sites for active groups, more attention has been paid to the application of comb-like

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Fig. 7. Schematic of immobilization of biocides using hydrophilic polymers including (a) PEG and (b) comb-like polymers as spacers.

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polymers with side chains containing EG units. An effective way to endow stainless steel surfaces with both antifouling and antibacterial functionalities is illustrated in Fig. 7b. The surfaces are first grafted with PEG-derived polymers such as PHEMA [124] or POEGMA [125], followed by activation of the hydroxyl groups on the side-chain ends for the covalent binding of antibacterial biomolecules (chitosan [124] or lysozyme [125]). This non releasing approach to inducing these two important functions (antifouling and antibacteria) simultaneously are highly advantageous in combating biofilm-related infections for biomedical and biomaterial applications. In addition to PHEMA and POEGMA, other hydrophilic copolymers have been used for the conjugation of natural biocides (such as AMPs) to fabricate antibacterial coatings on implants to resist biofilm formation [126]. In addition to serving as a spacer, PEG can also be used as a nonfouling polymeric matrix to provide bacteria resistant ability. For example, a polymeric coating in which AgNPs were generated in situ and embedded in the polymeric matrix was developed. Additionally, the surface of the coating was modified with PEG chains [127]. This coating is capable of killing bacteria by the release of Ag+ ions from the matrix as well as at least inhibiting bacterial growth and repelling bacteria by the outermost PEG chains at the same time. Libera and co-workers explored the use of self-assembled PEG-based microgels to reduce the rate of biomaterial-associated infection [128]. In addition to their intrinsic bacteria-resistant properties, these microgels can also be used as reservoirs to load and locally release antimicrobial peptides, resulting in enhanced inhibition of bacterial colonization on synthetic surfaces. 3.1.2. Layer-by-layer deposition of nonfouling layer and antibacterial layer Layer-by-layer (LBL) deposition is a simple, low-cost and mild technique for fabrication of multilayers of polymers (usually polyQ5 electrolytes) highly tunable in both morphology and functionality. The deposited multilayers have been exploited as reservoirs for loading and triggered-releasing antibacterial agents [129–135]. This method also offers another approach to simultaneously reducing bacterial adhesion and killing bacteria adhered onto a surface, where antibacterial agents and anti-adhesive agents with opposite charges are physically adsorbed onto substrates alternately to form a multilayer film (Fig. 8). A typical dual-function antibacterial surface prepared by the LBL method is based on chitosan (a cationic antibacterial molecule)

and heparin (an anionic anti-adhesive molecule) [136,137]. Results concerning the initial adhesion of E. coli and those obtained from an in vitro antibacterial assay showed that the chitosan/heparin multilayer-modified surface reduced bacterial adhesion dramatically and killed the bacteria effectively. To enhance the antibacterial properties of surfaces of this type, a composite system containing a degradable poly(vinylpyrrolidone)/poly(acrylic acid) (PVP/PAA) multilayer film and a heparin/chitosan multilayer film was constructed by LBL self-assembly [138]. The dual functionality of this system is manifested by two processes (as illustrated in Fig. 9). During the first 24 h, the top PVP/PAA is continuously removed, maintaining the prevention of bacterial adhesion on the surface. After removal of the (PVP/PAA) film, the underlying heparin/chitosan multilayer film is subsequently exposed and provides contact-killing antibacterial properties as previously discussed. This system is specially designed to address the bacterial adhesion problem during the most decisive period of fouling, and may have potential applications in the field of medical devices, particularly in implants. In addition to electrostatic interaction, click chemistry based on Huisgen 1,3-dipolar cycloaddition provides an alternative method or the covalent LBL deposition of anti-adhesive and antibacterial polymers to form a multilayer film. For example, azido-functionalized poly(ethylene glycol) methyl ether methacrylate-based polymer chains(azido-PPEGMA) and alkynyl-functionalized 2-(methacryloyloxy)ethyl trimethylammonium chloride-based polymer chains (alkynyl-PMETA) were click deposited sequentially on a polydopamine-coated stainless steel substrate, yielding a

Fig. 8. Schematic of multilayer film containing antibacterial agents and antiadhesive agents prepared by the LBL method.


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Fig. 9. Schematic representation of construction, cross-linking, degradation, and antibacterial properties of the (PVP/PAA)10-(heparin/chitosan)10 multilayer film. Reprinted with permission from Ref. [139], Copyright 2013, American Chemical Society.

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bifunctional and robust polymer multilayer coating for combating marine biofouling [139]. The resulting surfaces showed high bactericidal efficiency against marine Pseudomonas sp. NCIMB 2021, as well as greatly reduced bacterial adhesion and barnacle cyprid settlement. The functionality of the multilayer polymer coatings were maintained after exposure to filtered natural seawater at 30 °C for 30 days, suggesting good stability and durability.

form. This polymer-drug complex hydrogel with a built-in antibacterial function is able to keep the surface free of bacteria and simultaneously inhibit bulk bacteria growth, holding great potential in applications such as wound dressing [142,143] and surface coatings for medical devices.

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3.1.3. Nonfouling matrix with releasable antibacterial agents Most antibacterial surfaces based on the contact-killing mechanism can effectively kill bacteria attached to surfaces, but they have limited antibacterial capacity against planktonic bacteria. On the other hand, the controlled release of antibacterial agents from surfaces can be used to reduce bacterial colonization on surfaces and inhibit the proliferation of planktonic bacteria. To achieve both bulk antibacterial and surface nonfouling properties, a series of zwitterionic hydrogels with releasable biocides were developed. One facile way to produce such gels is to use an antibacterial anionic molecule (e.g., salicylate) as the counterion of a positively zwitterionic ester precursor [140]. As the hydrolysis of the ester group and/or anion exchange proceeds, the antibacterial molecules are released to inhibit the growth of bacteria in the surrounding environment after 24 h, leaving a zwitterionic nonfouling surface to further reduce bacterial adhesion. Although this method is straightforward, the release of drugs under high salt conditions is uncontrollable due to the exchange of environmental ions. This drawback can be addressed by the covalent conjugation of antibacterial molecules into a polymer matrix via hydrolysable linkers, in which the release of drugs was not sensitive to the ion strength [141]. As shown in Fig. 10, before hydrolysis, the salicylate molecule behaved as an anionic moiety to balance the cationic quaternary ammonium group on the polymer matrix to yield nonfouling properties. During hydrolysis, the released salicylate molecule was replaced by a new carboxylate group to maintain overall charge neutrality. After the salicylate was completely released, the hydrogel finally transitions into a stable zwitterionic form, preventing further bacterial adhesion. Throughout the entire process, the hydrogel surface consistently maintained the zwitterionic

The second type of dual-function antibacterial surface is based on the combination of bactericidal and bacteria-release properties into one system. Common bactericidal surfaces suffer a serious problem associated with the accumulation of dead bacteria and other debris [23], which not only degrades biocidal activity but also provides nutrients for other colonizers. It is thus desired to remove or release bacteria once they are killed from surfaces to maintain long-term biocidal activity. So far, most reports on the ‘‘kill and release’’ antibacterial surfaces are based on either zwitterionic polymers or thermo-responsive polymers, which we will introduce in the following section. In addition, there are several reports on surfaces based on QAS integrated silicone-based polymers to reduce marine biofouling [72,144–146], but those are not the main scope of this review.

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3.2.1. pH-induced cationic-zwitterionic transformation (chemical change) The first ‘‘kill and release’’ dual-function antibacterial surfaces produced are capable of chemically switching from an antibacterial cationic form (to kill attached bacteria) to a nonfouling zwitterionic form (to repel dead bacteria). For example, a zwitterionic monomer derivative was designed by Jiang and co-workers to modify the surfaces by surface-initiated polymerization (Fig. 11a) [147]. The surface modified by a cationic precursor carried biocidal quaternary amine groups, which can efficiently kill bacteria that attach to the surface at an early stage. The cationic ester groups can later be readily hydrolyzed in neutral or basic aqueous environments, resulting in a transition to zwitterionic surfaces to release dead bacteria and to retain the nonfouling properties for resistance against further bacterial attachment and provide a biocompatible

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Fig. 10. Schematic illustration of a hydrogel made up of a zwitterionic polymer with built-in antibacterial properties that is able to keep the surface free from bacteria and inhibit bacterial growth in bulk. Reprinted with permission from Ref. [142], Copyright 2012, Elsevier.

Fig. 11. (a) A zwitterionic surface that kills and releases bacteria in response to the environmental pH value. (b) A bactericidal surface based on a zwitterionic ester precursor kills bacteria at the cationic state and then undergoes hydrolysis to release dead bacterial cells to provide long-term bacterial resistance. Reprinted with permission from Ref. [23], Copyright 2014, Wiley-VCH.

568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584

environment. Although this one-time transition between cationic and zwitterionic forms is adequate for disposable devices, for many applications renewable surfaces with a repeatable ‘‘kill and release’’ functionality are necessary. To meet this requirement, the same research group developed a new polymer that is capable of reversibly switching between a cationic ring structure (CB-ring) and a zwitterionic linear structure (CB-OH) in response to environmental pH (Fig. 11b) [148]. Surfaces modified by the polymer in the CB-ring form showed strong biocidal activity toward more than 99% bacteria sprayed on the surface in one hour under dry conditions. Exposure of the surfaces to water induced the quick hydrolysis of the CB-ring form to the CB-OH form, resulting in the release of dead bacteria and the prevention of further bacterial fouling. More importantly, the CB-OH form can be easily converted back to the CB-ring form under acidic conditions to regenerate the biocidal activity for repeated use. This strategy, based on pH-induced cationic–zwitterionic transformation, is effective in

both killing and releasing bacteria; however, there are several limitations that should be addressed. Bacteria must be attached to the surface while it is dry (a wet surface is resistant to bacterial attachment), suggesting that the surface only works for airborne bacteria and may not be suitable for waterborne bacteria. In addition, the requirements of changing pH and chemical speciation to actuate functionality may be disadvantageous and cumbersome in certain biomedical applications.

585

3.2.2. Temperature-induced changes of conformation and hydrophobicity (physical change) As previously discussed, surfaces modified by PNIPAAm are capable of reversibly altering their properties in response to changes in temperature. Therefore, it is promising to integrate biocides with PNIPAAm to achieve multifunctional surfaces with the capacity for the controllable attachment, killing and release of bacteria. Recently, Yu and co-workers developed a new platform exhibiting switchable bioactivity based on nanopatterned PNIPAAm brushes. The temperature-induced conformational changes of the nanopatterned PNIPAAm brushes provide the capacity to spatially control the conformation of biomolecules between brushes, leading to an ON/OFF switch for surface bioactivity [107,149–151]. Two common biocides, quaternary ammonium salt (QAS) [107] and bacteriolytic enzyme lysozyme [150], are immobilized in polymer-free regions between nanopatterned PNIPAAm brushes. Above the LCST, desolvated, collapsed PNIPAAm chains facilitate the attachment of bacteria and expose biocides that kill adhered bacteria. Upon decreasing the temperature below the LCST, swollen PNIPAAm chains promote the release of dead bacteria (as illustrated in Fig. 12). The biocidal efficacy and release properties of these surfaces can be maintained for at least two attach-kill-release cycles. Although nanopatterned PNIPAAm/biocides hybrid surfaces effectively exhibit both biocidal and fouling-release functionalities, the preparation of these surfaces involves multiple steps and may not be suitable for other non-silica-based substrates, limiting their broad application. Alternatively, the same research group adopted a simple and facile deposition method called resonant infrared, matrix-assisted pulsed laser evaporation (RIR-MAPLE), in which an organic thin film is gently deposited onto substrate surfaces by the infrared laser ablation of a host emulsion matrix without the degradation of structural or functional integrity [152]. In particular, RIR-MAPLE provides a facile, one-step method for depositing multi-component films of the constituent materials exhibiting domain sizes on nanoscale, regardless of the solubility characteristics of each component. Using this method, the researchers deposited two dual-function antibacterial films by blending PNIPAAm with biocides (cationic QAS [153] and oligo (p-phenylene-ethynylene) (OPE) with UV light-induced biocidal activity [152,154]), which accumulated and killed a large number of

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Fig. 12. (a) Schematic depicting the procedure for preparation of nanopatterned PNIPAAm/biocide surfaces. (Step 1: patterning of the SAM of initiators via interferometric lithography; step 2: surface-initiated polymerization of NIPAAm from the pre-patterned initiator SAM; step 3: adsorption of biocides into the intervals between nanopatterned PNIPAAm lines) (b) Schematic of attachment, killing and release of bacteria on nanopatterned PNIPAAm/biocide hybrid surfaces in response to temperature. Reprinted with permission from Ref. [151], Copyright 2014, The Royal Society of Chemistry.

bacteria above the LCST, and further released the biocides upon exposure to water below the LCST. The surface chemical composition, morphology and wettability as well as the killing and release properties of the films can be adjusted simply by changing the ratio of PNIPAAm to biocides.

634

4. Summary and perspective

639

Over the past few decades, a significant number of dual-function antibacterial surfaces have been developed for the prevention of initial bacterial attachment and biofilm formation (as summarized in Table 1). These surfaces combine the biocidal activity afforded by biocides and the bacteria-resistant or bacteria-release capability afforded by certain materials (usually functional polymers), yielding advanced properties compared with conventional antibacterial surfaces with a single functionality. Although considerable progress has been made in this area and the experimental results are promising, many challenges in both science and technology remain, and further efforts may be guided by the following points:

640

1. Optimization of the design and fabrication process. For most of the dual-function antibacterial surfaces introduced in this review, multifunctionality (kill and resist, or kill and release) is achieved by two or more functional components. However, biocidal activity and bacteria-resistance/bacteria-release properties usually compromise one another. Therefore, the composition of surfaces must be optimized to obtain the highest performance. Moreover, for real-world applications, the fabrication of surfaces should be facile, low-cost and reproducible.

652

Bacteria-resistant material

Biocide

Bacteria

Ref.

Kill and resistant dual functional antibacterial surfaces ePTFE PEG ePTFE PEG TiO2 PEG PP PEG Silica particles PMEO2MA based copolymer TiO2 P(DMA-APMA) Stainless steel PHEMA Stainless steel POEGMA Glass PEG PET Heparin PS Heparin Si and glass PVP/PAA Hydrogel PHEAA Hydrogel PCBMA-based Hydrogel PCBMA-based Glass PCBMA

Penicillin Ampicillin Vancomycin Penicillin, Gentamicin Magainin-I AMP Chitosan Lysozyme AgNPs Chitosan Chitosan HEP/CHI Salicylic acid Salicylic acid Salicylic acid AgNPs

S. aureus S. aureus, E. faecalis, B. thuringiensis B. subtilis S. aureus, P. putida L. ivanovi P. aeruginosa E. coli E. coli, S. aureus S. aureus E. coli E. coli S. aureus E. coli, S. epidermidis E. coli, S. epidermidis S. epidermidis E. coli

[120,121] [122] [155] [123] [156] [126] [124] [125] [127] [137] [136] [138] [157] [140] [141] [158]

Substrate

Biocide

Bacteria

Ref.

QAS Lysozyme QAS OPE

E. E. E. E. E. E.

[147] [148] [107] [150] [153] [154]

Bacteria-release material

Kill and release dual functional antibacterial surfaces Au Zwitterionic ester precursor Au Zwitterionic ester precursor Glass PNIPAAm Glass PNIPAAm Glass PNIPAAm Glass PNIPAAm

coli coli coli, coli, coli, coli,

S. S. S. S.

epidermidis epidermidis epidermidis epidermidis


636 637 638

641 642 643 644 645 646 647 648 649 650 651

653 654 655 656 657 658 659 660 661

2. Integration of surface micro- and nano-topography. Briefly, most of the above-described antibacterial strategies are based on chemical modification. From another point of view, it is suggested that micro- and nanoscale surface topographical features also play an important role in controlling bacterial attachment and biofilm

Table 1 Summary of dual-function antibacterial surfaces. Substrate

635

662 663 664 665 666

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698

formation. Mimicking nature to provide engineering solutions offers a model for the development of functional surfaces with special antibacterial properties. For example, bio-inspired structures that mimic shark skin and lotus leaves endow synthetic surfaces with effective bacteria-resistance properties. Furthermore, it is reported that the synergistic effects of surface topography and polymer chemistry impart to surface biological properties that are opposite those of the corresponding smooth surfaces and even other unexpected biological properties such as enhanced bioadhesion or bioresistance [159,160]. Therefore, it is interesting to explore whether the integration of surface topography, especially on the nanoscale, into existing multifunctional antibacterial surfaces yields novel properties. 3. Addition of other functionalities for various applications. The real biological environment is complex, and different fields of research require synthetic surfaces that exhibit specific properties besides antibacterial properties. For blood-contacting devices, characteristics indicative of good hemocompatibility such as platelet resistance and antithrombotic properties are a key requirement [161]. For orthopedic and dental implants, surfaces should inhibit bacterial colonization and concomitantly promote osteoblast adhesion to realize their functions [162]. For marine applications, it is required that surfaces exhibit enhanced corrosion resistance and durability as well as fouling-resistance against diverse organisms which could colonize any submerged surfaces [163]. To date, a few research groups have tried to incorporate other functional groups into antibacterial surfaces to improve other specific properties to achieve better performance in real-world applications [161–163]. It should be noted that, for in vivo biomedical applications, the toxicological effects of antibacterial surfaces should be determined first and that the biocompatibility of these surfaces must be improved.

699

Acknowledgements

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Q6 This work was supported by the National Natural Science FounQ7 dation of China (21174098, 21334004 and 21404076), the Natural Science Foundation of Jiangsu Province (BK20140316), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and the Project of Scientific and Technologic Infrastructure of Suzhou (SZS201207).

[9] [10] [11]

[12] [13] [14] [15]

[16]

[17] [18] [19]

[20] [21]

[22] [23] [24]

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Appendix A. Figures with essential color discrimination

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Certain figures in this article, particularly Figs. 2, 3, 6–12 are difficult to interpret in black and white. The full color images can be found in the on-line version, at http://dx.doi.org/10.1016/j.actbio. 2015.01.018.

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[31] [32]

References

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[33] 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728 729

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[1] Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004;2:95–108. [2] Tuson HH, Weibel DB. Bacteria–surface interactions. Soft Matter 2013;9:4368–80. [3] Pavithra D, Doble M. Biofilm formation, bacterial adhesion and host response on polymeric implants – issues and prevention. Biomed Mater 2008;3:1–13. [4] Katsikogianni M, Missirlis YF. Concise review of mechanisms of bacterial adhesion to biomaterials and of techniques used in estimating bacteria– material interactions. Eur Cell Mater 2004;8:37–57. [5] Banerjee I, Pangule RC, Kane RS. Antifouling coatings: recent developments in the design of surfaces that prevent fouling by proteins, bacteria, and marine organisms. Adv Mater 2011;23:690–718. [6] Grozea CM, Walker GC. Approaches in designing non-toxic polymer surfaces to deter marine biofouling. Soft Matter 2009;5:4088–100. [7] Harding JL, Reynolds MM. Combating medical device fouling. Trends Biotechnol 2014;32:140–6. [8] Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW. Biofilm formation in Staphylococcus implant infections. A review of molecular

[34]

[35]

[36] [37]

[38] [39]

mechanisms and implications for biofilm-resistant materials. Biomaterials 2012;33:5967–82. Mérian T, Goddard JM. Advances in nonfouling materials: perspectives for the food industry. J Agric Food Chem 2012;60:2943–57. Callow JA, Callow ME. Trends in the development of environmentally friendly fouling-resistant marine coatings. Nat Commun 2011;2:244. Salwiczek M, Qu Y, Gardiner J, Strugnell RA, Lithgow T, McLean KM, et al. Emerging rules for effective antimicrobial coatings. Trends Biotechnol 2014;32:82–90. Glinel K, Thebault P, Humblot V, Pradier CM, Jouenne T. Antibacterial surfaces developed from bio-inspired approaches. Acta Biomater 2012;8:1670–84. Hasan J, Crawford RJ, Ivanova EP. Antibacterial surfaces: the quest for a new generation of biomaterials. Trends Biotechnol 2013;31:295–304. Yang WJ, Neoh K-G, Kang E-T, Teo SL-M, Rittschof D. Polymer brush coatings for combating marine biofouling. Prog Polym Sci 2014;39:1017–42. Campoccia D, Montanaro L, Arciola CR. A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials 2013;34: 8533–54. Zhang H, Chiao M. Antifouling coatings of PDMS devices for biological/ biomedical applications. J Med Biol Eng 2014. http://dx.doi.org/10.5405/ jmbe.1758. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999;284:1318–22. Lejars M, Margaillan A, Bressy C. Fouling release coatings: a nontoxic alternative to biocidal antifouling coatings. Chem Rev 2012;112:4347–90. Kugel A, Stafslien S, Chisholm BJ. Antimicrobial coatings produced by ‘‘tethering’’ biocides to the coating matrix: a comprehensive review. Prog Org Coat 2011;72:222–52. Muñoz-Bonilla A, Fernández-García M. Polymeric materials with antimicrobial activity. Prog Polym Sci 2012;37:281–339. Neoh KG, Kang ET. Combating bacterial colonization on metals via polymer coatings: relevance to marine and medical applications. ACS Appl Mater Interfaces 2011;3:2808–19. Schlenoff JB. Zwitteration: coating surfaces with zwitterionic functionality to reduce nonspecific adsorption. Langmuir 2014;30:9625–36. Mi L, Jiang S. Integrated antimicrobial and nonfouling zwitterionic polymers. Angew Chem Int Ed 2014;53:1746–54. Jellali R, Campistron I, Pasetto P, Laguerre A, Gohier F, Hellio C, et al. Antifouling activity of novel polyisoprene-based coatings made from photocurable natural rubber derived oligomers. Prog Org Coat 2013;76:1203–14. Cheng L, Liu Q, Lei Y, Lin Y, Zhang A. The synthesis and characterization of carboxybetaine functionalized polysiloxanes for the preparation of antifouling surfaces. RSC Adv 2014;4:54372–81. Gottenbos B, van der Mei HC, Klatter F, Nieuwenhuis P, Busscher HJ. In vitro and in vivo antimicrobial activity of covalently coupled quaternary ammonium silane coatings on silicone rubber. Biomaterials 2002;23: 1417–23. Isquith AJ, Abbott EA, Walters PA. Surface-bonded antimicrobial activity of an organosilicon quaternary ammonium chloride. Appl Microbiol 1972;24: 859–63. Nikawa H, Ishida K, Hamada T, Satoda T, Murayama T, Takemoto T, et al. Immobilization of octadecyl ammonium chloride on the surface of titanium and its effect on microbial colonization in vitro. Dent Mater J 2005;24: 570–82. Song J, Kong H, Jang J. Bacterial adhesion inhibition of the quaternary ammonium functionalized silica nanoparticles. Colloids Surf B 2011;82: 651–6. Poverenov E, Shemesh M, Gulino A, Cristaldi DA, Zakin V, Yefremov T, et al. Durable contact active antimicrobial materials formed by a one-step covalent modification of polyvinyl alcohol, cellulose and glass surfaces. Colloids Surf B 2013;112:356–61. Tiller JC, Liao CJ, Lewis K, Klibanov AM. Designing surfaces that kill bacteria on contact. Proc Natl Acad Sci USA 2001;98:5981–5. Tiller JC, Lee SB, Lewis K, Klibanov AM. Polymer surfaces derivatized with poly(vinyl-N-hexylpyridinium) kill airborne and waterborne bacteria. Biotechnol Bioeng 2002;79:465–71. Lee SB, Koepsel RR, Morley SW, Matyjaszewski K, Sun YJ, Russell AJ. Permanent, nonleaching antibacterial surfaces. 1. Synthesis by atom transfer radical polymerization. Biomacromolecules 2004;5:877–82. Murata H, Koepsel RR, Matyjaszewski K, Russell AJ. Permanent, non-leaching antibacterial surfaces – 2: How high density cationic surfaces kill bacterial cells. Biomaterials 2007;28:4870–9. Cheng ZP, Zhu XL, Shi ZL, Neoh KG, Kang ET. Polymer microspheres with permanent antibacterial surface from surface-initiated atom transfer radical polymerization. Ind Eng Chem Res 2005;44:7098–104. Siedenbiedel F, Tiller JC. Antimicrobial polymers in solution and on surfaces: overview and functional principles. Polymers 2012;4:46–71. Timofeeva L, Kleshcheva N. Antimicrobial polymers: mechanism of action, factors of activity, and applications. Appl Microbiol Biotechnol 2011;89:475–92. Jeon G, Yang SY, Byun J, Kim JK. Electrically actuatable smart nanoporous membrane for pulsatile drug release. Nano Lett 2011;11:1284–8. Fuglsang CC, Johansen C, Christgau S, AdlerNissen J. Antimicrobial enzymes: applications and future potential in the food industry. Trends Food Sci Technol 1995;6:390–6.


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[40] Thallinger B, Prasetyo EN, Nyanhongo GS, Guebitz GM. Antimicrobial enzymes: an emerging strategy to fight microbes and microbial biofilms. Biotechnol J 2013;8:97–109. [41] Onaizi SA, Leong SSJ. Tethering antimicrobial peptides: current status and potential challenges. Biotechnol Adv 2011;29:67–74. [42] Regan F, Chapman J, Sullivan T. Nanoparticles in anti-microbial materials: their use and characterisation. RSC Publishing; 2012. [43] Knetsch MLW, Koole LH. New strategies in the development of antimicrobial coatings: the example of increasing usage of silver and silver nanoparticles. Polymers 2011;3:340–66. [44] Luk Y-Y, Kato M, Mrksich M. Self-assembled monolayers of alkanethiolates presenting mannitol groups are inert to protein adsorption and cell attachment. Langmuir 2000;16:9604–8. [45] Rizzello L, Pompa PP. Nanosilver-based antibacterial drugs and devices: mechanisms, methodological drawbacks, and guidelines. Chem Soc Rev 2014;43:1501–18. [46] Kim H-W, Knowles JC, Kim H-E. Hydroxyapatite/poly(e-caprolactone) composite coatings on hydroxyapatite porous bone scaffold for drug delivery. Biomaterials 2004;25:1279–87. [47] Stigter M, de Groot K, Layrolle P. Incorporation of tobramycin into biomimetic hydroxyapatite coating on titanium. Biomaterials 2002;23:4143–53. [48] Lawson MC, Shoemaker R, Hoth KB, Bowman CN, Anseth KS. Polymerizable vancomycin derivatives for bactericidal biomaterial surface modification: structure–function evaluation. Biomacromolecules 2009;10:2221–34. [49] Slomberg DL, Lu Y, Broadnax AD, Hunter RA, Carpenter AW, Schoenfisch MH. Role of size and shape on biofilm eradication for nitric oxide-releasing silica nanoparticles. ACS Appl Mater Interfaces 2013;5:9322–9. [50] Nablo BJ, Rothrock AR, Schoenfisch MH. Nitric oxide-releasing sol–gels as antibacterial coatings for orthopedic implants. Biomaterials 2005;26:917– 924. [51] Nablo BJ, Chen T-Y, Schoenfisch MH. Sol–gel derived nitric-oxide releasing materials that reduce bacterial adhesion. J Am Chem Soc 2001;123:9712–3. [52] Li Z, Lee D, Sheng X, Cohen RE, Rubner MF. Two-level antibacterial coating with both release-killing and contact-killing capabilities. Langmuir 2006;22:9820–3. [53] Sambhy V, MacBride MM, Peterson BR, Sen A. Silver bromide nanoparticle/ polymer composites: dual action tunable antimicrobial materials. J Am Chem Soc 2006;2006:9798–808. [54] Eby DM, Luckarift HR, Johnson GR. Hybrid antimicrobial enzyme and silver nanoparticle coatings for medical instruments. ACS Appl Mater Interfaces 2009;1:1553–60. [55] Laloyaux X, Fautré E, Blin T, Purohit V, Leprince J, Jouenne T, et al. Temperature-responsive polymer brushes switching from bactericidal to cell-repellent. Adv Mater 2010;22:5024–8. [56] Mattheis C, Zhang Y, Agarwal S. Thermo-switchable antibacterial activity. Macromol Biosci 2012;12:1401–12. [57] Chapman RG, Ostuni E, Liang MN, Meluleni G, Kim E, Yan L, et al. Polymeric thin films that resist the adsorption of proteins and the adhesion of bacteria. Langmuir 2001;17:1225–33. [58] Ostuni E, Chapman RG, Liang MN, Meluleni G, Pier G, Ingber DE, et al. Selfassembled monolayers that resist the adsorption of proteins and the adhesion of bacterial and mammalian cells. Langmuir 2001;17:6336–43. [59] Ista LK, Fan H, Baca O, Lopez GP. Attachment of bacteria to model solid surfaces: oligo(ethylene glycol) surfaces inhibit bacterial attachment. FEMS Microbiol Lett 1996;142:59–63. [60] Ista LK, Lopez GP. Interfacial tension analysis of oligo(ethylene glycol) terminated self-assembled monolayers and their resistance to bacterial attachment. Langmuir 2012;28:12844–50. [61] Kuroki H, Tokarev I, Nykypanchuk D, Zhulina E, Minko S. Stimuli-responsive materials with self-healing antifouling surface via 3D polymer grafting. Adv Funct Mater 2013;23:4593–600. [62] Saldarriaga Fernández IC, van der Mei HC, Lochhead MJ, Grainger DW, Busscher HJ. The inhibition of the adhesion of clinically isolated bacterial strains on multi-component cross-linked poly(ethylene glycol)-based polymer coatings. Biomaterials 2007;28:4105–12. [63] Zhao C, Li L, Wang Q, Yu Q, Zheng J. Effect of film thickness on the antifouling performance of poly(hydroxy-functional methacrylates) grafted surfaces. Langmuir 2011;27:4906–13. [64] Lin NJ, Yang HS, Chang Y, Tung KL, Chen WH, Cheng HW, et al. Surface selfassembled pegylation of fluoro-based PVDF membranes via hydrophobicdriven copolymer anchoring for ultra-stable biofouling resistance. Langmuir 2013;29:10183–93. [65] Li M, Neoh KG, Xu LQ, Wang R, Kang ET, Lau T, et al. Surface modification of silicone for biomedical applications requiring long-term antibacterial, antifouling, and hemocompatible properties. Langmuir 2012;28:16408–22. [66] Yang WJ, Cai T, Neoh KG, Kang ET, Teo SL, Rittschof D. Barnacle cement as surface anchor for ‘‘clicking’’ of antifouling and antimicrobial polymer brushes on stainless steel. Biomacromolecules 2013;14:2041–51. [67] Weber T, Gies Y, Terfort A. Bacteria-repulsive polyglycerol surfaces by grafting polymerization onto aminopropylated surfaces. Langmuir 2012;28: 15916–21. [68] Weber T, Bechthold M, Winkler T, Dauselt J, Terfort A. Direct grafting of antifouling polyglycerol layers to steel and other technically relevant materials. Colloids Surf B 2013;111C:360–6. [69] Ekblad T, Bergström G, Ederth T, Conlan SL, Mutton R, Clare AS, et al. Poly(ethylene glycol)-containing hydrogel surfaces for antifouling

[70]

[71]

[72]

[73]

[74]

[75]

[76]

[77]

[78]

[79]

[80] [81] [82]

[83] [84]

[85]

[86] [87] [88] [89] [90]

[91]

[92]

[93] [94]

[95]

[96]

[97]

[98]

[99]

11

applications in marine and freshwater environments. Biomacromolecules 2008;9:2775–83. Song A, Rane AA, Christman KL. Antibacterial and cell-adhesive polypeptide and poly(ethylene glycol) hydrogel as a potential scaffold for wound healing. Acta Biomater 2012;8:41–50. Lei J, Mayer C, Viatcheslav Freger V, Ulbricht M. Synthesis and characterization of poly(ethylene glycol) methacrylate based hydrogel networks for anti-biofouling applications. Macromol Mater Eng 2013;298:967–80. Lundberg P, Bruin A, Klijnstra JW, Nyström AM, Johansson M, Malkoch M, et al. Poly(ethylene glycol)-based thiol-ene hydrogel coatings curing chemistry, aqueous stability, and potential marine antifouling applications. ACS Appl Mater Interfaces 2010;2:903–12. Cheng G, Zhang Z, Chen S, Bryers JD, Jiang S. Inhibition of bacterial adhesion and biofilm formation on zwitterionic surfaces. Biomaterials 2007;28: 4192–9. Zhang Z, Finlay JA, Wang L, Gao Y, Callow JA, Callow ME, et al. Polysulfobetaine-grafted surfaces as environmentally benign ultralow fouling marine coatings. Langmuir 2009;25:13516–21. Cheng G, Li G, Xue H, Chen S, Bryers JD, Jiang S. Zwitterionic carboxybetaine polymer surfaces and their resistance to long-term biofilm formation. Biomaterials 2009;30:5234–40. Jiang S, Cao Z. Ultralow-fouling, functionalizable, and hydrolyzable zwitterionic materials and their derivatives for biological applications. Adv Mater 2010;22:920–32. Chang Y, Shu S-H, Shih Y-J, Chu C-W, Ruaan R-C, Chen W-Y. Hemocompatible mixed-charge copolymer brushes of pseudozwitterionic surfaces resistant to nonspecific plasma protein fouling. Langmuir 2010;26:3522–30. Mi L, Bernards MT, Cheng G, Yu Q, Jiang S. pH responsive properties of nonfouling mixed-charge polymer brushes based on quaternary amine and carboxylic acid monomers. Biomaterials 2010;31:2919–25. Zhao Y-H, Zhu X-Y, Wee K-H, Bai R. Achieving highly effective non-biofouling performance for polypropylene membranes modified by UV-induced surface graft polymerization of two oppositely charged monomers. J Phys Chem B 2010;114:2422–9. Krishnan S, Weinman CJ, Ober CK. Advances in polymers for anti-biofouling surfaces. J Mater Chem 2008;18:3405. Detty MR, Ciriminna R, Bright FV, Pagliaro M. Environmentally benign sol–gel antifouling and foul-releasing coatings. Acc Chem Res 2014;47:678–87. Sullivan T, Regan F. Designing sustainable antifouling based on biomimetic design principles for ocean sensing technology. J Ocean Technol 2011;6:42–54. Kirschner CM, Brennan AB. Bio-inspired antifouling strategies. Annu Rev Mater Res 2012;42:211–29. Callow ME, Jennings AR, Brennan AB, Seegert CE, Gibson A, Wilson L, et al. Microtopographic cues for settlement of zoospores of the green fouling alga Enteromorpha. Biofouling 2002;18:237–45. Chapman J, Regan F. Nanofunctionalized superhydrophobic antifouling coatings for environmental sensor applications—advancing deployment with answers from nature. Adv Eng Mater 2012;14:B175–84. Magin CM, Cooper SP, Brennan AB. Non-toxic antifouling strategies. Mater Today 2010;13:36–44. Yu Q, Liu H, Chen H. Vertical SiNWAs for biomedical and biotechnology applications. J Mater Chem B 2014;2:7849–60. Kuroki H, Tokarev I, Minko S. Responsive surfaces for life science applications. Annu Rev Mater Res 2012;42:343–72. Mendes PM. Stimuli-responsive surfaces for bio-applications. Chem Soc Rev 2008;37:2512–29. Ista LK, Mendez S, Balamurugan SS, Balamurugan S, Rama Rao VG, Lopez GP. Smart surfaces for the control of bacterial attachment and biofilm accumulation. ACS Symp Ser 2009;1002:95–110. Pernites RB, Santos CM, Maldonado M, Ponnapati RR, Rodrigues DF, Advincula RC. Tunable protein and bacterial cell adsorption on colloidally templated superhydrophobic polythiophene films. Chem Mater 2012;24:870–80. Shivapooja P, Wang Q, Orihuela B, Rittschof D, Lopez GP, Zhao X. Bioinspired surfaces with dynamic topography for active control of biofouling. Adv Mater 2013;25:1430–4. Schild HG. Poly(N-isopropylacrylamide): experiment, theory and application. Prog Polym Sci 1992;17:163–249. Sun TL, Wang GJ, Feng L, Liu BQ, Ma YM, Jiang L, et al. Reversible switching between superhydrophilicity and superhydrophobicity. Angew Chem Int Ed 2004;43:357–60. Yu Q, Zhang Y, Chen H, Wu Z, Huang H, Cheng C. Protein adsorption on poly(N-isopropylacrylamide)-modified silicon surfaces: effects of grafted layer thickness and protein size. Colloids Surf B 2010;76:468–74. Huber DL, Manginell RP, Samara MA, Kim B-I, Bunker BC. Programmed adsorption and release of proteins in a microfluidic device. Science 2003;301:352–4. Okano T, Yamada N, Okuhara M, Sakai H, Sakurai Y. Mechanism of cell detachment from temperature-modulated, hydrophilic–hydrophobic polymer surfaces. Biomaterials 1995;16:297–303. Reed JA, Love SA, Lucero AE, Haynes CL, Canavan HE. Effect of polymer deposition method on thermoresponsive polymer films and resulting cellular behavior. Langmuir 2012;28:2281–7. Yu Q, Chen H. Applications of regulation of protein adsorption using PNIPAAm modified surfaces. Prog Chem 2014;26:1275–84.


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[100] Ista LK, Lopez GP. Lower critical solubility temperature materials as biofouling release agents. J Ind Microbiol Biotechnol 1998;20:121–5. [101] Ista LK, Perez-Luna VH, Lopez GP. Surface-grafted, environmentally sensitive polymers for biofilm release. Appl Environ Microbiol 1999;65:1603–9. [102] Ista LK, Mendez S, Perez-Luna VH, Lopez GP. Synthesis of poly(Nisopropylacrylamide) on initiator-modified self-assembled monolayers. Langmuir 2001;17:2552–5. [103] Ista LK, Mendez S, Lopez GP. Attachment and detachment of bacteria on surfaces with tunable and switchable wettability. Biofouling 2010;26:111–8. [104] Shivapooja P, Ista LK, Canavan HE, Lopez GP. AGRET-ATRP synthesis and characterization of PNIPAAm brushes for quantitative cell detachment studies. Biointerphases 2012;7:32. [105] Cunliffe D, Smart CA, Tsibouklis J, Young S, Alexander C, Vulfson EN. Bacterial adsorption to thermoresponsive polymer surfaces. Biotechnol Lett 2000;22:141–5. [106] Alarcon CDH, Farhan T, Osborne VL, Huck WTS, Alexander C. Bioadhesion at micro-patterned stimuli-responsive polymer brushes. J Mater Chem 2005;15:2089–94. [107] Yu Q, Cho J, Shivapooja P, Ista LK, Lopez GP. Nanopatterned smart polymer surfaces for controlled attachment, killing, and release of bacteria. ACS Appl Mater Interfaces 2013;5:9295–304. [108] Cunliffe D, Alarcon CD, Peters V, Smith JR, Alexander C. Thermoresponsive surface-grafted poly(N-isopropylacrylamide) copolymers: effect of phase transitions on protein and bacterial attachment. Langmuir 2003;19: 2888–99. [109] Levering V, Wang Q, Shivapooja P, Zhao X, Lopez GP. Soft robotic concepts in catheter design: an on-demand fouling-release urinary catheter. Adv Health Mater 2014;3:1588–96. [110] van der Borden AJ, van der Werf H, van der Mei HC, Busscher HJ. Electric current-induced detachment of Staphylococcus epidermidis biofilms from surgical stainless steel. Appl Environ Microbiol 2004;70:6871–4. [111] Shim S, Hong SH, Tak Y, Yoon J. Prevention of Pseudomonas aeruginosa adhesion by electric currents. Biofouling 2011;27:217–24. [112] Dargahi M, Hosseinidoust Z, Tufenkji N, Omanovic S. Investigating electrochemical removal of bacterial biofilms from stainless steel substrates. Colloids Surf B 2014;117C:152–7. [113] Krishnan S, Ayothi R, Hexemer A, Finlay JA, Sohn KE, Perry R, et al. Antibiofouling properties of comblike block copolymers with amphiphilic side chains. Langmuir 2006;22:5075–86. [114] Gudipati CS, Finlay JA, Callow JA, Callow ME, Wooley KL. The antifouling and fouling-release performance of hyperbranched fluoropolymer (HBFP) poly(ethylene glycol) (PEG) composite coatings evaluated by adsorption of biomacromolecules and the green fouling alga ulva. Langmuir 2005;21:3044–53. [115] Yeh SB, Chen CS, Chen WY, Huang CJ. Modification of silicone elastomer with zwitterionic silane for durable antifouling properties. Langmuir 2014;30:11386–93. [116] Yuan L, Yu Q, Li D, Chen H. Surface modification to control protein–surface interaction. Macromol Biosci 2011;11:1031–40. [117] Chen H, Yuan L, Song W, Wu Z, Li D. Biocompatible polymer materials: role of protein–surface interactions. Prog Polym Sci 2008;33:1059–87. [118] Goddard JM, Hotchkiss JH. Polymer surface modification for the attachment of bioactive compounds. Prog Polym Sci 2007;32:698–725. [119] Yu Q, Zhang Y, Wang H, Brash JL, Chen H. Anti-fouling bioactive surfaces. Acta Biomater 2011;7:1550–7. [120] Aumsuwan N, Heinhorst S, Urban MW. Antibacterial surfaces on expanded polytetrafluoroethylene; penicillin attachment. Biomacromolecules 2007;8:713–8. [121] Aumsuwan N, Heinhorst S, Urban MW. The effectiveness of antibiotic activity of penicillin attached to expanded poly(tetrafluoroethylene) (ePTFE) surfaces: a quantitative assessment. Biomacromolecules 2007;8:3525–30. [122] Aumsuwan N, Danyus RC, Heinhorst S, Urban MW. Attachment of ampicillin to expanded poly(tetrafluoroethylene): surface reactions leading to inhibition of microbial growth. Biomacromolecules 2008;9:1712–8. [123] Aumsuwan N, McConnell MS, Urban MW. Tunable antimicrobial polypropylene surfaces: simultaneous attachment of penicillin (Gram+) and gentamicin (Gram ). Biomacromolecules 2009;10:623–9. [124] Yang WJ, Cai T, Neoh K-G, Kang E-T, Dickinson GH, Teo SL-M, et al. Biomimetic anchors for antifouling and antibacterial polymer brushes on stainless steel. Langmuir 2011;27:7065–76. [125] Yuan S, Wan D, Liang B, Pehkonen SO, Ting YP, Neoh KG, et al. Lysozymecoupled poly(poly(ethylene glycol) methacrylate) stainless steel hybrids and their antifouling and antibacterial surfaces. Langmuir 2011;27:2761–74. [126] Gao G, Lange D, Hilpert K, Kindrachuk J, Zou Y, Cheng JT, et al. The biocompatibility and biofilm resistance of implant coatings based on hydrophilic polymer brushes conjugated with antimicrobial peptides. Biomaterials 2011;32:3899–909. [127] Ho CH, Tobis J, Sprich C, Thomann R, Tiller JC. Nanoseparated polymeric networks with multiple antimicrobial properties. Adv Mater 2004;16:957–61. [128] Wang Q, Uzunoglu E, Wu Y, Libera M. Self-assembled poly(ethylene glycol)co-acrylic acid microgels to inhibit bacterial colonization of synthetic surfaces. ACS Appl Mater Interfaces 2012;4:2498–506. [129] Pavlukhina S, Lu Y, Patimetha A, Libera M, Sukhishvili S. Polymer multilayers with pH-triggered release of antibacterial agents. Biomacromolecules 2010;11:3448–56.

[130] Wong SY, Han L, Timachova K, Veselinovic J, Hyder MN, Ortiz C, et al. Drastically lowered protein adsorption on microbicidal hydrophobic/ hydrophilic polyelectrolyte multilayers. Biomacromolecules 2012;13:719–26. [131] Chuang HF, Smith RC, Hammond PT. Polyelectrolyte multilayers for tunable release of antibiotics. Biomacromolecules 2008;9:1660–8. [132] Zhuk I, Jariwala F, Attygalle AB, Wu Y, Libera MR, Sukhishvili SA. Selfdefensive layer-by-layer films with bacteria-triggered antibiotic release. ACS Nano 2014;8:7733–45. [133] Moskowitz JS, Blaisse MR, Samuel RE, Hsu H-P, Harris MB, Martin SD, et al. The effectiveness of the controlled release of gentamicin from polyelectrolyte multilayers in the treatment of Staphylococcus aureus infection in a rabbit bone model. Biomaterials 2010;31:6019–30. [134] Wong SY, Li Q, Veselinovic J, Kim B-S, Klibanov AM, Hammond PT. Bactericidal and virucidal ultrathin films assembled layer by layer from polycationic N-alkylated polyethylenimines and polyanions. Biomaterials 2010;31:4079–87. [135] Shukla A, Fleming KE, Chuang HF, Chau TM, Loose CR, Stephanopoulos GN, et al. Controlling the release of peptide antimicrobial agents from surfaces. Biomaterials 2010;31:2348–57. [136] Follmann HD, Martins AF, Gerola AP, Burgo TA, Nakamura CV, Rubira AF, et al. Antiadhesive and antibacterial multilayer films via layer-by-layer assembly of TMC/heparin complexes. Biomacromolecules 2012;13:3711–22. [137] Fu J, Ji J, Yuan W, Shen J. Construction of anti-adhesive and antibacterial multilayer films via layer-by-layer assembly of heparin and chitosan. Biomaterials 2005;26:6684–92. [138] Wang BL, Ren KF, Chang H, Wang JL, Ji J. Construction of degradable multilayer films for enhanced antibacterial properties. ACS Appl Mater Interfaces 2013;5:4136–43. [139] Yang WJ, Pranantyo D, Neoh KG, Kang ET, Teo SL, Rittschof D. Layer-by-layer click deposition of functional polymer coatings for combating marine biofouling. Biomacromolecules 2012;13:2769–80. [140] Cheng G, Xue H, Li G, Jiang S. Integrated antimicrobial and nonfouling hydrogels to inhibit the growth of planktonic bacterial cells and keep the surface clean. Langmuir 2010;26:10425–8. [141] Mi L, Jiang S. Synchronizing nonfouling and antimicrobial properties in a zwitterionic hydrogel. Biomaterials 2012;33:8928–33. [142] Mi L, Xue H, Li Y, Jiang S. A thermoresponsive antimicrobial wound dressing hydrogel based on a cationic betaine ester. Adv Funct Mater 2011;21:4028–34. [143] Ji F, Lin W, Wang Z, Wang L, Zhang J, Ma G, et al. Development of nonstick and drug-loaded wound dressing based on the hydrolytic hydrophobic poly(carboxybetaine) ester analogue. ACS Appl Mater Interfaces 2013;5:10489–94. [144] Ye S, Majumdar P, Chisholm B, Stafslien S, Chen Z. Antifouling and antimicrobial mechanism of tethered quaternary ammonium salts in a cross-linked poly(dimethylsiloxane) matrix studied using sum frequency generation vibrational spectroscopy. Langmuir 2010;26:16455–62. [145] Liu Y, Leng C, Chisholm B, Stafslien S, Majumdar P, Chen Z. Surface structures of PDMS incorporated with quaternary ammonium salts designed for antibiofouling and fouling release applications. Langmuir 2013;29:2897–905. [146] Majumdar P, Lee E, Gubbins N, Christianson DA, Stafslien SJ, Daniels J, et al. Combinatorial materials research applied to the development of new surface coatings XIII: an investigation of polysiloxane antimicrobial coatings containing tethered quaternary ammonium salt groups. J Comb Chem 2009;11:1115–27. [147] Cheng G, Xite H, Zhang Z, Chen SF, Jiang SY. A switchable biocompatible polymer surface with self-sterilizing and nonfouling capabilities. Angew Chem Int Ed 2008;47:8831–4. [148] Cao Z, Mi L, Mendiola J, Ella-Menye JR, Zhang L, Xue H, et al. Reversibly switching the function of a surface between attacking and defending against bacteria. Angew Chem Int Ed 2012;51:2602–5. [149] Yu Q, Johnson LM, Lopez GP. Nanopatterned polymer brushes for triggered detachment of anchorage-dependent cells. Adv Funct Mater 2014;24: 3751–9. [150] Yu Q, Ista LK, Lopez GP. Nanopatterned antimicrobial enzymatic surfaces combining biocidal and fouling release properties. Nanoscale 2014;6:4750–7. [151] Yu Q, Shivapooja P, Johnson LM, Tizazu G, Leggett GJ, Lopez GP. Nanopatterned polymer brushes as switchable bioactive interfaces. Nanoscale 2013;5:3632–7. [152] Ge W, Yu Q, Lopez GP, Stiff-Roberts AD. Antimicrobial oligo(p-phenyleneethynylene) film deposited by resonant infrared matrix-assisted pulsed laser evaporation. Colloids Surf B 2014;116:786–92. [153] Yu Q, Ge W, Atewologun A, Stiff-Roberts AD, Lopez GP. RIR-MAPLE deposition of multifunctional films combining biocidal and fouling release properties. J Mater Chem B 2014;2:4371–8. [154] Yu Q, Ge W, Atewologun A, Stiff-Roberts AD, Lopez GP. Antimicrobial and bacteria-releasing multifunctional surfaces: oligo (p-phenylene-ethynylene)/ poly (N-isopropylacrylamide) films deposited by RIR-MAPLE [in press]. [155] Wach JY, Bonazzi S, Gademann K. Antimicrobial surfaces through natural product hybrids. Angew Chem Int Ed 2008;47:7123–6. [156] Blin T, Purohit V, Leprince JRM, Jouenne T, Glinel K. Bactericidal microparticles decorated by an antimicrobial peptide for the easy disinfection of sensitive aqueous solutions. Biomacromolecules 2011;12: 1259–64.


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[157] Zhao C, Li X, Li L, Cheng G, Gong X, Zheng J. Dual functionality of antimicrobial and antifouling of poly(N-hydroxyethylacrylamide)/salicylate hydrogels. Langmuir 2013;29:1517–24. [158] Hu R, Li G, Jiang Y, Zhang Y, Zou JJ, Wang L, et al. Silver-zwitterion organic– inorganic nanocomposite with antimicrobial and antiadhesive capabilities. Langmuir 2013;29:3773–9. [159] Li D, Zheng Q, Wang Y, Chen H. Combining surface topography with polymer chemistry: exploring new interfacial biological phenomena. Polym Chem 2013;5:14–24. [160] Yu Q, Li X, Zhang Y, Yuan L, Zhao T, Chen H. The synergistic effects of stimuli– responsive polymers with nano-structured surfaces: wettability and protein adsorption. RSC Adv 2011;1:262–9.

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[161] Zhao J, Song L, Shi Q, Luan S, Yin J. Antibacterial and hemocompatibility switchable polypropylene nonwoven fabric membrane surface. ACS Appl Mater Interfaces 2013;5:5260–8. [162] Hu X, Neoh K-G, Shi Z, Kang E-T, Poh C, Wang W. An in vitro assessment of titanium functionalized with polysaccharides conjugated with vascular endothelial growth factor for enhanced osseointegration and inhibition of bacterial adhesion. Biomaterials 2010;31:8854–63. [163] Yuan SJ, Pehkonen SO, Ting YP, Neoh KG, Kang ET. Antibacterial inorganic– organic hybrid coatings on stainless steel via consecutive surface-initiated atom transfer radical polymerization for biocorrosion prevention. Langmuir 2010;26:6728–36.


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Metal-Based Antibacterial Substrates for Biomedical Applications.

Bio-Inspired Extreme Wetting Surfaces for Biomedical Applications.

Functional nanoparticles for biomedical applications.

Crosslinking biopolymers for biomedical applications.

Titanium nanostructures for biomedical applications.

Antibacterial Au nanostructured surfaces.

Two-dimensional graphene analogues for biomedical applications.

keratin composites for biomedical applications.

nano-structured superhydrophobic surfaces in the biomedical field: part II: applications overview.

Magnetic nanoparticles adapted for specific biomedical applications.

Fluorescent probes for biomedical applications (2009-2014).

Engineering Stem Cells for Biomedical Applications.

Stimuli-responsive nanomaterials for biomedical applications.

Dielectrophoresis for Biomedical Sciences Applications: A Review.

Carbon nanotubes reinforced composites for biomedical applications.

Biocompatible electrospun polymer blends for biomedical applications.

Designing fractal nanostructured biointerfaces for biomedical applications.

High-energy proton imaging for biomedical applications.

Functional supramolecular polymers for biomedical applications.

Design of Hydrogels for Biomedical Applications.

Biopolymeric formulations for biocatalysis and biomedical applications.

Photocontrolled nanoparticle delivery systems for biomedical applications.

A thermostatic system for biomedical applications.

Engineered magnetic nanoparticles for biomedical applications.