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Cite This: ACS Appl. Mater. Interfaces 2017, 9, 37511-37523

Smart Antibacterial Surfaces with Switchable Bacteria-Killing and Bacteria-Releasing Capabilities Ting Wei,† Zengchao Tang,‡ Qian Yu,*,† and Hong Chen† †

State and Local Joint Engineering Laboratory for Novel Functional Polymeric Materials, College of Chemistry, Chemical Engineering and Materials Science, Soochow University, 199 Ren’ai Road, Suzhou, 215123, PR China ‡ Jiangsu Biosurf Biotech Company Ltd., 218 Xinghu Street, Suzhou, 215123, PR China ABSTRACT: The attachment and subsequent colonization of bacteria on the surfaces of synthetic materials and devices lead to serious problems in both human healthcare and industrial applications. Therefore, antibacterial surfaces that can prevent bacterial attachment and biofilm formation have been a long-standing focus of considerable interest and research efforts. Recently, a promising “kill−release” strategy has been proposed and applied to construct so-called smart antibacterial surfaces, which can kill bacteria attached to their surface and then undergo on-demand release of the dead bacteria and other debris to reveal a clean surface under an appropriate stimulus, thereby maintaining effective long-term antibacterial activity. This Review focuses on the recent progress (particularly over the past 5 years) on such smart antibacterial surfaces. According to the different design strategies, these surfaces can be divided into three categories: (i) “K + R”-type surfaces, which have both a killing unit and a releasing unit; (ii) “K → R”-type surfaces, which have a surface-immobilized killing unit that can be switched to perform a releasing function; and (iii) “K + (R)”-type surfaces, which have only a killing unit but can release dead bacteria upon the addition of a release solution. In the end, a brief perspective on future research directions and the major challenges in this promising field is also presented. KEYWORDS: antibacterial surface, stimuli-responsive polymer, kill−release strategy, bactericidal surface, bacterial release into nonfouling materials via covalent binding20,21 or layer-bylayer (LBL) deposition.22,23 In principle, such surfaces will realize both passive and active functions simultaneously to improve the overall antibacterial efficacy. However, the bactericidal components usually actively attract and bind to bacteria to realize the killing functions, whereas the nonfouling components repel bacteria as they approach. This incompatibility results in reduced effectiveness compared to that of the individual components alone. Therefore, for an ideal antibacterial surface, the bacterialresistant function and bactericidal function should be separated such that the surface only performs one function at a time to avoid interference. Based on this idea, a promising “kill−release” strategy has been proposed and applied to prepare so-called smart antibacterial surfaces that can kill bacteria attached to the surface and then release dead bacteria and other debris under an appropriate stimulus to give a clean surface, thereby maintaining effective long-term antibacterial activity. In this Review, we summarize recent (particularly over the past 5 years) representative works on the development of smart antibacterial surfaces based on the “kill−release” strategy. We divide these surfaces into three categories as illustrated in Figure 1 (here, we use “K” and “R” to represent the functions of “killing bacteria” and “releasing bacteria”, respectively): (i) “K + R”-type surfaces, which possess both a killing unit and

1. INTRODUCTION Bacterial adhesion and colonization on surfaces can lead to serious problems, including the infection of implants, the failure of medical devices, and threats to public health.1−5 Therefore, antibacterial surfaces that can prevent bacterial attachment and biofilm formation have become an active field of research, particularly for biomedical applications.6−8 Traditional antibacterial surfaces are typically classified into two types according to their mechanism of operation: (i) passive-defense antibacterial surfaces use nonfouling materials, such as polyethylene glycol (PEG) and zwitterionic polymers, to prevent the initial attachment of bacteria,9,10 and (ii) active-attack antibacterial surfaces use synthetic or natural biocides to kill the attached bacteria.11−14 Despite their general effectiveness, neither of these surfaces is suitable for practical applications due to their respective inherent limitations. Without bactericidal capabilities, passive-defense surfaces are ineffective against bacteria once they adhere onto the surface, and even a few attached bacteria will ultimately grow into a biofilm. However, active-attack surfaces usually suffer from problems related to the accumulation of dead bacteria and debris, which not only shield the functional groups, thereby reducing the bactericidal efficacy, but also serve as a conditioning film to provide nutrients for subsequent bacterial adhesion, causing an immune response or inflammation. Therefore, increasing attempts have been made to combine these two complementary approaches to combine bacterial resistance and bactericidal functionality in one surface.15−19 These dual functional antibacterial surfaces are usually prepared by incorporating biocides © 2017 American Chemical Society

Received: September 7, 2017 Accepted: October 9, 2017 Published: October 9, 2017 37511

DOI: 10.1021/acsami.7b13565 ACS Appl. Mater. Interfaces 2017, 9, 37511−37523

Review

ACS Applied Materials & Interfaces a releasing unit (section 2); (ii) “K → R”-type surfaces, which possess a surface-immobilized killing unit that can be switched to perform a releasing function (section 3); and (iii) “K + (R)”-type surfaces, which possess only a killing unit but can release dead bacteria upon the addition of a release solution (section 4). In the end, we provide a brief perspective on the future research directions and major challenges in this promising field.

properties (e.g., wettability, charge, or topography) in response to an external stimulus when they are immobilized on a solid surface. These transitions cause the modified surfaces to switch from a bacteria-attractive state to a bacteria-resistant state, facilitating the release of attached bacteria. Therefore, the combination of these two components provides an efficient way to fabricate multifunctional antibacterial surfaces that can kill and release bacteria. In this section, we will introduce the development of these “K + R” antibacterial surfaces according to the different stimuli factors used to trigger the surface function transition (as summarized in Table 1). 2.1. Temperature-Triggered Function Switch. Temperature, one of the most-common stimuli, has been widely used to control bioadhesion on solid surfaces.35,36 Poly(N-isopropylacrylamide) (PNIPAAm) is a prototypical thermoresponsive polymer that displays solubility reversible changes in response to temperature changes across a lower critical solution temperature (LCST) of 32 °C in aqueous solution.37 Surfaces modified with PNIPAAm thus exhibit unique temperature-controlled surface wettability and bioadhesion properties such as protein adsorption and desorption and cell attachment and detachment.38−41 In particular, pioneering work by Lopez and co-workers exploited PNIPAAm-modified surfaces as promising fouling-release materials that can release not only newly attached bacteria but also fully developed biofilms.42−44 Therefore, the integration of biocides with PNIPAAm should yield hybrid surfaces with a switchable bacteria-killing and bacteria-releasing capability. These surfaces can be divided into three categories based on the (i) co-immobilization, (ii) co-polymerization, or (iii) co-deposition of biocides with PNIPAAm. 2.1.1. Surfaces with Co-Immobilized Biocides and PNIPAAm. In 2013, Lopez and co-workers prepared surfaces grafted with nanopatterned PNIPAAm brushes by combining interferometric lithography (IL) and surface-initiated polymerization (SIP), and they systematically investigated the surface properties under different temperatures.45 A significant change in surface topography

2. “K + R”-TYPE ANTIBACTERIAL SURFACES “K + R”-type antibacterial surfaces contain both bactericidal units and bacteria-releasing units to realize both specific functions. The bactericidal components range from synthetic chemicals, such as quaternary ammonium compounds (QACs), cationic polymers, and metal nanoparticles, to natural biomolecules, such as antimicrobial peptides and antimicrobial enzymes, imparting surfaces with the ability to kill attached bacteria.24−31 The bacteriareleasing components are usually stimuli-responsive polymers,32−34 which enable reversible transitions in the surface

Figure 1. Schematic illustration of three categories of smart antibacterial surfaces based on the “kill−release” strategy. “K” and “R” refer to the functions of “killing bacteria” and “releasing bacteria”, respectively.

Table 1. Summary of “K + R”-Type Antibacterial Surfacesa killing units (K)

releasing units (R)

methods for combination

QAS

PNIPAAm

adsorption of biocides on the polymer-free regions between nanopatterned PNIPAAm brushes

lysozyme PPE PPE PMT PDMAEMA PDMAEMA QAS OPE AgNP lysozyme AMP PDMAEMA AgNP CD-QAS

PNIPAAm PNIPAAm PNIPAAm PNIPAAm PNIPAAm PVCL PNIPAAm PNIPAAm PNIPAAm PMAA PMAA PSBMA PCBMA Azo

mechanisms of bacteria release temperature-induced changes in conformation and hydrophobicity of PNIPAAm (or PVCL) chains

SIP + LBL deposition co-incorporation of PMT and PNIPAAm co-polymerization via SIP co-deposition via RIR-MAPLE one-step photopolymerization loading lysozyme into SiNWAs-PMAA surface under pH 4 co-graft polymerization co-graft polymerization embedding AgNPs into PCBMA brushes incorporation of CD-QAS with Azo via host−guest interaction

pH-induced hydration of PMAA chains antifouling properties of zwitterionic polymers in wet conditions dissociation of CD-QAS/Azo complexes by UV irradiation

ref 48 49 50 51 52 56 57 60 61 62 71 70 77 78 81

a

Abbreviations: quaternary ammonium salts (QAS); poly(N-isopropylacrylamide) (PNIPAAm); poly(p-phenylene ethynylene) (PPE); surfaceinitiated polymerization (SIP); layer-by-layer (LBL); poly[2-(methacryloyloxy)-ethyl]trimethylammonium chloride (PMT); poly(N,Ndimethylaminoethyl methacrylate) (PDMAEMA); poly(N-vinylcaprolactam) (PVCL); oligo (p-phenylene-ethynylene) (OPE); resonant infrared, matrix-assisted pulsed laser evaporation (RIR-MAPLE); silver nanoparticle (AgNP); poly(methacrylic acid) (PMAA); silicon nanowire arrays (SiNWAs); antimicrobial peptide (AMP); poly(sulfobetaine methacrylate) (PSBMA); poly(carboxybetaine methacrylate) (PCBMA); β- cyclodextrin derivative containing seven QAS groups (CD-QAS); azobenzene (Azo). 37512


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ACS Applied Materials & Interfaces

host−guest interactions between β-cyclodextrin (β-CD) and adamantane (Ada).52 As shown in Figure 3, PNIPAAm with an Ada end group (PNIPAAm-Ada) and a biocidal polymer poly[2(methacryloyloxy)-ethyl]trimethylammonium chloride with an Ada end group (PMT-Ada) were co-incorporated onto the surface of a silicon wafer (SW) pregrafted with β-CD by simply immersing the surface in a mixed solution of PNIPAAm-Ada and PMT-Ada. The reversible bacterial killing and detachment switch was also induced by the collapsed-to-extended conformational transition of PNIPAAm chains across the LCST, allowing the transition from the exposure to concealment of PMT chains to realize the corresponding functions (high bacterial-killing efficiency (∼90%) and satisfactory bacterial-detachment efficiency (∼85%)). 2.1.2. Surfaces with Co-Polymerized Biocides and PNIPAAm. SIP is a powerful surface modification approach for the generation of polymer brushes by which to tailor the physicochemical properties of interfaces.53,54 In particular, it is facile to endow surfaces with dual or multifunctionality through the SIP of a mixture of two or more monomers to graft co-polymer brushes on surfaces.55 Therefore, the SIP of a thermoresponsive monomer and bactericidal monomer provides another useful method with which to prepare temperature-triggered, multifunctional bactericidal, and fouling-release antibacterial surfaces. Using a surface-initiated, reversible addition−fragmentation chain-transfer polymerization (SI-RAFT) technique, Wang and co-workers prepared polydimethylsiloxane (PDMS) surfaces modified with co-polymer brushes of poly(2-(dimethylamino)ethyl methacrylate-co-NIPAAm)) (P(DMAEMA+-co-NIPAAm)) (Figure 4).56 The positively charged PDMAEMA+ components displayed strong bactericidal efficiency against both Grampositive and Gram-negative bacteria via a contact killing mechanism. However, the PNIPAAm components behaved as an actuator to change the hydration of co-polymers and the surface wettability in response to the decrease in temperature

was observed when the temperature of the aqueous solution crossed the LCST. Above the LCST, the PNIPAAm brushes collapsed to produce a distinct parallel surface pattern, while below the LCST, the PNIPAAm brushes swelled and laterally spread to cover the adjacent regions. This temperature-triggered conformational change enabled the thermally regulated concealment and exposure of bioactive molecules that were preimmobilized between the nanoscopic lines of PNIPAAm brushes, allowing the reversible switching of the surface bioactivity.46,47 Later, this group extended this finding to develop a series of smart antibacterial surfaces with a switchable bactericidal and bacteria-releasing capability.48−50 The preparation and operational mechanism of such surfaces are illustrated in Figure 2. Diverse biocides (such as quaternary ammonium salts (QAS),48 antimicrobial enzymes,49 and singlet oxygen sensitizers)50 have been physisorbed on the polymer-free regions between PNIPAAm brush nanopatterns. At temperatures above the LCST, these nanopatterned PNIPAAm/biocide hybrid surfaces facilitate the attachment of bacteria, and the collapsed and dehydrated nanopatterned PNIPAAm chains expose biocide to kill the attached bacteria. Decreasing the temperature to below the LCST induces the hydration of PNIPAAm, which promotes the release of dead bacteria and debris from the surface upon mild shearing. These nanoengineered surfaces are effective model surfaces for realizing controllable bacterial attachment, antimicrobial action, and fouling release. Although the performance of nanopatterned PNIPAAm-based surfaces is effective, the preparation of such hybrid surfaces requires sophisticated equipment and involves multiple steps, which may limit broad application. To address these limitations, some simple and facile methods to integrate biocides with PNIPAAm have been developed.51,52 For example, Zhao and co-workers constructed a material that exhibits thermoresponsive switching between bacterial killing and detachment based on the

Figure 2. Schematic illustration of the preparation of the nanopatterned PNIPAAm/biocide hybrid surface using the combination of IL and SIP techniques (above) and the attachment, killing, and temperature-triggered release of bacteria on the resulted hybrid surface (below). Reproduced with permission from ref 49. Copyright 2014, The Royal Society of Chemistry. 37513


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ACS Applied Materials & Interfaces from 37 to 4 °C, releasing the killed bacteria for surface selfcleaning. This co-polymer-modified surface maintained this reversibly switchable bactericidal and fouling-release capability for at least four kill-and-release cycles, suggesting good durability for long-term use. In another report, the same group used a similar strategy to construct a multifunctional antibacterial surface modified with terpolymer brushes of poly(N-vinylcaprolactam-co-2-(dimethylamino)-ethyl methacrylate-co-2-methacryloyloxy-ethyl phosphorylcholine) (P(VCL-co-DMAEMA+-co-MPC)).57 Poly(Nvinylcaprolactam) (PVCL) is a thermoresponsive polymer and has lower overall cytotoxicity than PNIPAAm-based polymers. Poly(2-methacryloyloxy-ethyl phosphorylcholine) (PMPC) is a typical zwitterionic polymer that is favorable for increased antiadhesive and fouling release properties. The resulting

terpolymer-modified surfaces maintained the bactericidal and self-cleaning properties discussed above, and the replacement of PNIPAAm with PVCL improved the biocompatibility with mammalian cells. Although co-polymerization is an effective way to construct a multifunctional antibacterial surface, the specific functions of bacterial killing and release may compromise each other. Therefore, a thorough investigation of the impact of a range of co-polymer parameters (e.g., the ratio of functional components, polymer chain length, and graft density) on the final surface properties is required to achieve surfaces with optimal killing efficiency, release efficiency, and reusability. 2.1.3. Surfaces with Co-Deposited and Blended Biocides and PNIPAAm. For broad application to diverse substrate materials, it is desirable to find a simple and universal technique to deposit multifunctional films that combine biocidal and fouling release properties. In this regard, resonant infrared, matrix-assisted pulsed laser evaporation (RIR-MAPLE), a facile and widely applicable vacuum-based deposition technique, provides an easy way to deposit multicomponent films with nanoscale domain sizes of the constituent materials; the deposited organic materials retain their respective structural and functional integrity.58,59 Using this technique, Lopez and co-workers proposed a strategy to fabricate multifunctional antibacterial surfaces by depositing blended films of PNIPAAm and biocides on solid surfaces. In their two separate proof-of-concept reports, two bactericidal compounds, cationic QAS60 and oligo(p-phenylene-ethynylene) (OPE) with light-enhanced biocidal activity61 were co-deposited with PNIPAAm. The resultant blended films exhibited strong biocidal activity to kill a large number of attached bacteria when the temperature was above the LCST, and the dead bacteria were released upon subsequent exposure to water below the LCST. The overall bacteria-killing and bacteria-releasing performance could be further optimized by simply adjusting the biocide-to-PNIPAAm ratio.61 Notably, the bacteria-releasing mechanism of PNIPAAm films deposited by RIR-MAPLE is likely different from that of surface-anchored PNIPAAm brushes prepared by SIP. A decrease in temperature below the LCST promotes the hydration and potential dissolution of the PNIPAAm layer, and the dissolved PNIPAAm are easily washed away during rinsing because there are no covalent bonds between the PNIPAAm films and underlying substrates, which further leads to the loss of anchorage points for bacteria and to bacterial detachment. Using a similar blending strategy, a smart antibacterial film combining biocidal silver nanoparticles (AgNPs) with PNIPAAm was prepared in situ by a one-step photopolymerization method.62 The free radicals produced by the photoinitiators could promote the photopolymerization of an NIPAAm monomer and simultaneously reduce silver ions to silver metal, producing a

Figure 3. Schematic illustration of the synthesis of PNIPAAm-Ada and PMT-Ada (above), functionalization of the SW-CD surface with PNIPAAm-Ada and PMT-Ada via host−guest interaction (middle), and the reversible thermoresponsive switch for bacterial killing and detachment on the resulted surface (below). Adapted with permission from ref 52. Copyright 2016, American Chemical Society.

Figure 4. Schematic illustration of the preparation of thermoresponsive co-polymer brushes on PDMS surfaces and the different conformations of the co-polymer brushes under different temperatures. Inspired by refs 56 and 57. 37514


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ACS Applied Materials & Interfaces AgNPs/PNIPAAm blended film on the substrate surface. As a result of the synergy between the AgNPs and PNIPAAm, the resulting surfaces achieved smart antibacterial activity that killed a large number of Escherichia coli (E. coli) at 37 °C and released the killed bacteria at 4 °C (Figure 5). As the amount of silver was

Figure 6. Schematic illustration of a hierarchical antibacterial surface composed of an outer pH-responsive PMAA layer and an inner bactericidal AMP layer and the corresponding switch of surface function switch between killing bacteria to repelling bacteria in response to change of pH. Reprinted with permission from ref 70. Copyright 2016, American Chemical Society.

Figure 5. Schematic illustration of an AgNPs/PNIPAAm hybrid surface that can attach, kill, and detach bacteria in response to the change in environmental temperature. Adapted with permission from ref 62. Copyright 2016, American Chemical Society.

increased, the fouling-resistant and self-cleaning capability of the surface was progressively enhanced. In addition to temperature, other stimuli such as pH, light, ionic strength, and mechanical stretching could lead to changes in surface properties and switch the interfacial interactions from a bacteria-attractive state to bacteria-repellent state.63−66 Recently, several smart antibacterial surfaces exhibiting a “kill−release” strategy were developed using the combination of these stimuliresponsive components and bactericidal components, as discussed below. 2.2. pH-Responsive Antibacterial Surfaces. pH-responsive polymers are usually weak polyelectrolytes whose charge density and conformation depend on the pH. When they are immobilized on solid surfaces, changes in environmental pH lead to changes in surface properties, such as the wettability and surface charge, and, thereby, in changes in bioadhesion.67 For example, poly(methacrylic acid) (PMAA) is a typical pH-responsive polymer with a large number of carboxy (COOH) groups on its repeating units. The PMAA chains present a collapsed conformation in acidic aqueous solution and extensively swell in basic aqueous solution due to the ionization of COOH groups to carboxylate ions (COO−), which results in a high density of negative charges, strong electrostatic repulsion, and a high degree of hydration.68,69 Considering the advantages of the pH-responsiveness of PMAA, a bacteria-responsive antibacterial surface with a two-layered hierarchical architecture was developed.70 As shown in Figure 6, the inner layer, which is based on positively charged bactericidal antimicrobial peptide (AMP), is shielded by an outer negatively charged hydrophilic PMAA layer, protecting against possible cytotoxicity. When bacteria colonize the surface, the bacterial metabolism-triggered decrease in the local environmental pH triggers the collapse of the PMAA chains to expose the underlying AMP and activate the bactericidal function. The killed bacteria and related debris are then easily removed by increasing the pH to promote the hydration and swelling of the PMAA chains. Recently, we combined the pH-responsiveness of PMAA and the unique nanoscale topography of silicon nanowire arrays (SiNWAs) to develop a smart antibacterial surface with switchable functionalities in response to environmental pH for the on-demand killing and release of bacteria.71 As illustrated in Figure 7, the

Figure 7. Schematic illustration of a smart antibacterial surface based on PMAA-modified SiNWAs with switchable functionalities among loading biocides (under an acidic pH), killing bacteria (under a neutral pH), and releasing bacteria (under a basic pH). Adapted with permission from ref 71. Copyright 2016, John Wiley and Sons.

PMAA-modified SiNWAs surface is an effective dynamic antibacterial reservoir that not only exhibited a remarkably high capacity for binding an antimicrobial enzyme, lysozyme, at an acidic pH (pH 4) but also desorpted a majority of the adsorbed lysozyme when the pH was increased to a neutral value (pH 7). The desorpted lysozyme molecules maintained their enzymatic activity and thus served as biocides with which to kill bacteria both suspended in solution and attached to the surface. More importantly, after the killing process, the dead bacteria and debris attached to the SiNWAs-PMAA surface could be readily removed by further increasing the pH to a basic value (pH 10); the “cleaned” surface could then be used to load new lysozyme for repeated applications. In this system, the pH-responsive properties of the grafted PMAA chains endow the system with stepwise regulation of the interfacial interactions between the surface and the lysozyme/bacteria, and the unique nanoporous topography and high surface area of the SiNWAs enhance the responsiveness and binding of the system.72,73 Moreover, this design might be applicable to other combinations of porous nanomaterials and stimuli-responsive polymers. 37515


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the local environment or cause unwanted side effects.79,80 Considering these advantages, we recently reported a supramolecular antibacterial surface with photoswitchable kill and release functions.81 This system is composed of a surface immobilized with azobenzene (Azo) groups and a biocidal β-CD derivative containing seven QAS groups (CD-QAS). As illustrated in Figure 9, the switching between the bacteria-killing and

2.3. Dry- and Wet-Responsive Antibacterial Surfaces. Zwitterionic polymers refer to polymers with an equimolar number of homogeneously distributed anionic and cationic groups along the chains. Surfaces grafted with zwitterionic polymers strongly bind water molecules via electrostatic interactions to form a stable hydration layer in aqueous solution and show excellent nonfouling properties.74−76 Taking advantage of this feature, several groups combined antimicrobial agents with zwitterionic polymers to develop antibacterial surfaces with switchable functions in response to moisture changes. For example, hierarchical antibacterial surfaces with a zwitterionic outer layer (poly(sulfobetaine methacrylate) (PSBMA)) on a polycationic bactericidal inner layer (PDMAEMA) were prepared using a surface-initiated photoiniferter-mediated polymerization (SI-PIMP) technique.77 As illustrated in Figure 8, in dry conditions,

Figure 9. Schematic illustration of a supramolecular antibacterial surface capable of switchability between bactericidal activity and bacteriareleasing ability in response to light. The surface-immobilized Azo groups in trans form can specially incorporate CD-QAS to realize bactericidal activity. Upon irradiation with UV light, the Azo groups switch to cis form, resulting in the dissociation of the Azo/CD-QAS inclusion complex and the release of dead bacteria from the surface. The surface can be regenerated by irradiation with visible light and reincorporation of fresh CD-QAS. Reprinted with permission from ref 81. Copyright 2017, American Chemical Society.

Figure 8. Schematic illustration of a hierarchical antibacterial surface consisting of a zwitterionic outer layer and a polycationic bactericidal inner layer. In the dry state, the collapsed zwitterionic outer layer exposes the polycationic layer to kill attached bacteria, while in the wet state, the zwitterionic outer layer swells to release dead bacteria and to prevent bacterial adhesion. Adapted with permission from ref 77. Copyright 2016, American Chemical Society.

bacteria-releasing functions is based on the photoresponsive host−guest interactions between CD-QAS and Azo. CD-QAS and trans-Azo formed inclusion complexes to endow the surface with strong biocidal activity, killing more than 90% of the attached bacteria. Exposure of the surface to UV light converted Azo from the trans form to the cis form to dissociate the CD-QAS/Azo complexes, resulting in the removal of CD-QAS and the killed bacteria from the surface. Moreover, due to the high efficiency of the cis−trans isomerization of Azo, following the kill-and-release cycle, the surface can be easily regenerated for reuse by irradiation with visible light to recover trans-Azo for the reincorporation of fresh CD-QAS.

the outer PSBMA layer collapses to facilitate contact between the underlying polycationic layer and attached bacteria. In wet conditions, the strong hydration causes PSBMA to swell, and the resulting hydration layer promotes the release of dead bacteria and inhibits further bacterial attachment. In another report, a silver-zwitterion inorganic−organic hybrid surface was developed by embedding AgNPs into a surface grafted with poly(carboxybetaine methacrylate) (PCBMA) brushes. 78 The obtained hybrid surface killed more than 99.8% of the E. coli K12 present in 1 h and released more than 98.7% of the dead bacterial cells from the surface after incubation with phosphate-buffered saline (PBS) with gentle shaking for 30 min. These surfaces exhibit switchable antibacterial mechanisms that kill airborne bacteria on the surface during dry storage and repel dead bacteria and further attachment of planktonic bacteria in aqueous environments, making them extremely promising for applications in infection-resistant implants and medical devices. 2.4. Light-Responsive Antibacterial Surfaces. Among the available external stimuli, light is advantageous because it can be delivered to the surface from a remote source and can induce fast responses. Moreover, due to its noninvasive and intrinsically clean nature, using light as a trigger generally does not influence

3. “K → R”-TYPE ANTIBACTERIAL SURFACES Unlike “K + R”-type antibacterial surfaces, in which the killing and releasing functions are realized by two separate components, “K → R”-type antibacterial surfaces themselves can switch from a bactericidal state to a bacteria-releasing state in response to appropriate stimuli. Such surfaces are usually based on zwitterionic polymer derivatives, which can chemically change their structures from a cationic form to kill bacteria to a zwitterionic form to release dead bacteria.82−84 The chemical diversity and design flexibility enable the integration of bactericidal functionality into conventional zwitterionic polymers. Through rational molecular design, various cationic precursors of zwitterionic polymers were developed for surface modification to endow surfaces switchable antibacterial activity. Jiang and co-workers systemically investigated the nonfouling properties of zwitterionic materials.85−87 They confirmed that zwitterionic materials such as polycarboxybetaine (PCB) and polysulfobetaine (PSB) dramatically reduce nonspecific protein adsorption and bacterial attachment, even biofilm formation, through the formation of a hydration layer via electrostatic interactions.82,85 Considering that betaine is a quaternized zwitterionic alkaloid whose positive portion consists of QAS groups with bactericidal activity, changing the carboxylate anions 37516


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Figure 10. Chemical structures of several zwitterionic polymer derivatives that can change from bactericidal cationic forms to nonfouling zwitterionic forms under diverse external stimuli including pH, light, and electrical potential. Inspired by refs (a) 89, (b) 90, (c) 91, (d) 92, (e) 93, and (f) 94.

of PCB into esters can yield hydrolyzable PCB ester precursors to realize the hydrolysis-triggered switch from the cationic bactericidal function to the zwitterionic antifouling function.83,88

In 2008, this group reported a surface modified by a cationic precursor possessing biocidal quaternary amine groups (the chemical structure is shown in Figure 10a).89 The bactericidal 37517


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between the cationic antimicrobial and zwitterionic antifouling states.

performance was as good as the performance of the common permanently cationic polymers, which kill more than 99% of bacteria. 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, retain the nonfouling properties for resistance against further bacterial attachment and provide a biocompatible environment. However, the transition between cationic and zwitterionic forms in this design was irreversible, so the material was only effective for one-time use. To address this limitation, these authors developed a new polymer capable of reversibly switching between a cationic ring structure (CB-ring) and a zwitterionic linear structure (CB−OH) through a reversible lactonization reaction90 (Figure 10b). Surfaces modified by the polymer in the CB-ring form showed strong biocidal activity, killing more than 99% of the bacteria sprayed on the surface in 1 h under dry conditions. Exposure of the surfaces to water induced the rapid hydrolysis of the CB-ring form to the CB−OH form, resulting in the release of the 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. Recently, Luan and co-workers exploited a similar principle of cationic−zwitterionic transformation for antibacterial modification of common biomedical materials, including chitosan (CS) nonwoven wound dressing and styrenic thermoplastic elastomers (poly(styrene-b-isobutylene-b-styrene) (SIBS).91,92 The as-prepared, nonwoven surface and elastomer functionalized with cationic carboxybetaine esters (Q-CS and Q-SIBS) were able to kill bacteria effectively. Upon hydrolysis of the carboxybetaine esters, the resulting zwitterionic surface (Z-CS and Z-SIBS) could further suppress the attachment of proteins, platelets, erythrocytes, and bacteria (Figure 10c,d). These polymer materials that can switch from effective bactericidal activity during storage to antifouling activity before service have great potential in biomedical applications, and the modification strategy is generally applicable to other polymer materials. Although effective, the aforementioned surfaces have inherent limitations. For example, they are only effective against airborne bacteria in the dry state and may not be suitable for waterborne bacteria because the bactericidal activity is lost in wet environments. The hydrolysis is relatively time-consuming and difficult to accurately control, and the requirement of changing the pH to switch between the functions may not be tolerated in certain biomedical applications. Alternatively, other stimuli such as light and electrical potential have been used to trigger the cationic− zwitterionic transformation (Figure 10e,f).93,94 For example, an electroactive poly(sulfobetaine-3,4-ethylenedioxythiophene) (PSBEDOT) film was developed with poly(3,4-ethylenedioxythiophene) (PEDOT) as the conducting backbone and zwitterionic sulfobetaine as the side chain, showing electroswitchable antimicrobial and antifouling properties94 (Figure 10f). After the application of a 0.6 V potential for 1 h, the PEDOT backbone is in the oxidized state, and the overall polymer film is cationic, killing any attached bacteria. Decreasing the potential places the PEDOT backbone in its reduced state and the overall film in its zwitterionic form. Due to the repulsive force generated by the strong hydration of the zwitterionic side chains and the disappearance of the attractive force between the negatively charged bacteria and positively charged PSBEDOT surfaces, the killed bacterial cells are released. In this system, the oxidized− reduced state can be easily and accurately controlled by applying an electrical potential, allowing more rapid and active switching

4. “K + (R)”-TYPE ANTIBACTERIAL SURFACES For both “K + R”-type and “K − R”-type antibacterial surfaces, the killing and release functions are realized in a single system. Alternatively, in recent years, researchers have developed a third type of surface following the “kill-and-release” strategy: a “K + (R)”-type antibacterial surface, which is composed of only biocidal units that kill attached bacteria and requires an additional “releasing” reagent for the removal of killed bacteria and debris. According to the bacteria-releasing mechanisms, these “K + (R)”-type antibacterial surfaces can be divided into two categories based on the (i) direct and (ii) indirect weakening of the interfacial interactions between the bacteria and surface (as summarized in Table 2). Table 2. Summary of “K + (R)”-Type Antibacterial Surfacesa bactericidal components (K)

additional releasing solution (R)

PTMAEMA

0.1 M PP

PIL(Br) Lysozyme

0.2 M LiTf2N 4.0 M NaCl

TCS TRGO + NIR laser irradiation CD-QAS

1.0 M NaCl AdCNa 0.5% SDS

mechanisms of bacteria release hydration induced by ion exchange between counteranions salt-induced hydration of polymer brush dissociation of host−guest interaction between Ada and β-CD

ref 96 97 98 99 108 112

a

Abbreviations: poly((trimethylamino)ethyl methacrylate chloride), PTMAEMA; sodium hexametaphosphate, PP; poly(ionic) liquid, PIL; lithium bis(trifluoromethanesulfonyl)amide, LiTf2N; sodium chloride, NaCl; triclosan, TCS; thermally reduced graphene oxide, TRGO; near-infrared, NIR; sodium adamantine carboxylate, AdCNa; sodium dodecyl sulfate, SDS; adamantane, Ada; β-cyclodextrin, β-CD.

4.1. Directly Weakening the Interfacial Interactions between the Bacteria and Surface. Most contact-killing antibacterial surfaces rely on the surface-bound cationic compounds such as QACs, polycations, chitosan, and AMP; the main killing mechanism is based on the electrostatic attraction between these positively charged agents and the negatively charged bacterial cell membranes to cause membrane charge disruption and damage, leading to bacterial death.95 However, the strong electrostatic attraction always results in the accumulation of bacteria even after they have been killed, leading to serious problems. Because the interfacial electrostatic interaction can be regulated by changing the type and strength of environmental ions, it might be possible to remove the bacteria using ionic solutions as releasing reagents. Chang and co-workers developed a counterion-activated switchable antibacterial surface based on poly((trimethylamino)ethyl methacrylate chloride) (PTMAEMA) brushes.96 Under normal conditions, the cationic PTMAEMA attracted bacteria to the locally abundant QAC moieties, which killed the bacteria upon contact. The introduction of electrolyte solution containing a suitable counterion (polyphosphate anion (PP6−)) led to the collapse and hydration of the polymer chains and an increase in negative net charges, which together generated a repulsive force to repel the attached dead bacteria from the surface and recover the biocidal activity (Figure 11). 37518


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Figure 11. Schematic illustration of the contact killing and counterion-assisted release of bacteria on the surface modified with PTMAEMA polycation brushes. The repetitive killing and releasing actions of PTMAEMA was realized through the undocking and docking of counterions. Adapted with permission from ref 96. Copyright 2015, American Chemical Society.

4.2. Indirectly Weakening the Interfacial Interactions between the Bacteria and Surface. Instead of directly weakening the bacteria−surface interfacial interactions, the bacteria can be removed from the surface by breaking the linkers between the bacteria and surface. For example, host−guest interactions based on supramolecular chemistry provide a facile and flexible way to incorporate specific molecules on surfaces by forming host−guest inclusion complexes.100−103 The host− guest interaction is a relatively weak, noncovalent interaction, providing the possibility to dissociate the complexes on demand, which might favor bacterial detachment.104−107 Exploiting these characteristics, a supramolecular carbohydrate-functionalized graphene derivative was developed for bacterial capture, release, and disinfection.108 In this system, heptamannosylated β-CD (CD-Mannose) was incorporated on thermally reduced graphene oxide (TRGO) functionalized with Ada groups via the host−guest interaction between β-CD and Ada. The resulting platform could effectively agglutinate E. coli due to the specific affinity of the mannose ligands on CD-Mannose for the lectin proteins on bacterial surfaces. Moreover, 99% of the captured E. coli were eliminated upon exposure to near-infrared (NIR) laser irradiation due to the unique photothermal property of TRGO. The killed bacteria were partially released by dissociation of the Ada/ CD-mannose complexes through the addition of a competitive guest sodium adamantine carboxylate (AdCNa). In addition to competitive guests, the Ada/β-CD complexes could also be dissociated by the introduction of a surfactant, sodium dodecyl sulfate (SDS).109−111 Considering this property and our previous work, we designed a universal strategy to fabricate antibacterial surfaces with broad applicability, bacterial release capability, regenerability, and multifunctionality.112 In this design, various substrates were deposited on multilayered films containing Ada groups as guest moieties using LBL assembly. The Ada groups served as binding sites for the incorporation of biocidal “host” molecules, CD-QAS, via the host−guest interactions. The entire preparation process of LBL deposition and host−guest inclusion was conducted in a mild aqueous medium at room temperature and could be applied to diverse substrates with different surface chemistries and structures. The resulting surfaces exhibited excellent broad-spectrum biocidal activity and bacterial release achieved by dissociation of the Ada/CD-QAS complexes using SDS. Specifically, the regenerated surface could be reincorporated with fresh CD-QAS for further antibacterial application (Figure 13). When another functional β-CD derivative molecule was “co-incorporated” with CD-QAS, the surfaces performed both functions simultaneously, and neither the specific biofunction nor the antibacterial

Similarly, Wu and co-workers reported a counterion-responsive antibacterial surface with a switchable function based on poly(ionic liquid) (PIL) brushes.97 An imidazolium-type PIL showed different hydrophobicity with different counteranions, Br− and Tf2N−. The exchange between these two anions caused changes in the wettability of the grafted surface and in the grafted polymer chain conformation, leading to a switch of the surface function between killing and releasing bacteria. In addition to a counterion solution, salt solution could also be used as a releasing reagent to induce the detachment of bacteria from solid surfaces.98 For example, surfaces grafted with a polyzwitterionic brush, poly(3-(dimethyl (4-vinylbenzyl) ammonium) propyl sulfonate) (PDVBAPS) reversibly switched between a bioadhesive state and a biorepellent state in response to the salt concentration.66 Based on this finding, a smallmolecule, antibacterial agent, triclosan (TCS), was covalently conjugated to the PDVBAPS brushes to achieve a salt-responsive antibacterial surface, which could kill more than 95% of attached bacteria and, subsequently, rapidly detach ∼97% of the killed bacteria after gentle shaking in 1.0 M sodium chloride (NaCl) for 10 min (Figure 12). More importantly, no deterioration of the

Figure 12. Schematic illustration of a salt-induced regenerative surface based on polyzwitterionic PDVBAPS brushes and a biocide TSC for bacteria killing and release. Reprinted with permission from ref 99. Copyright 2017, American Chemical Society.

killing effectiveness or release rate occurred after four severe killing-release cycles, indicating that this surface has great potential in reusable medical devices.99 Compared to the counterion exchange of polyelectrolytes, which is complicated and time-consuming, using NaCl provides a simple and rapid way to trigger the release of bacteria. 37519


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Figure 13. Schematic illustration of a universal antibacterial surface prepared by the combination of the LBL deposition of multilayers containing guest moieties (Ada) and the incorporation of biocidal host molecules (CD-QAS) for the killing and releasing of bacteria. Adapted with permission from ref 112. Copyright 2016, American Chemical Society.

researchers in the fields of surface chemistry, materials science, biomedical engineering, and biotechnology to make remarkable progress, but this research should provide plenty of opportunities for innovation beyond antibacterial surfaces.

activity was compromised by the presence of the other, suggesting great potential in applications requiring synthetic surfaces that exhibit specific properties in addition to antibacterial activity.

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5. SUMMARY AND PERSPECTIVES Smart antibacterial surfaces based on the “kill−release” strategy have undergone rapid development in the last 5 years. Compared with conventional antibacterial surfaces with a single function (killing bacteria or repelling bacteria) or a simple combination of dual functions (killing and repelling bacteria), these new surfaces provide a more-promising solution for the prevention of initial bacterial attachment and subsequent biofilm formation. In particular, the self-cleaning property and repeated function switching make these surfaces more suitable for applications in which longterm antibacterial activity is required. Despite the considerable progress that has been made, many challenges in both the science and the technology of this field remain and will be the directions of future research. The core of “kill−release” smart antibacterial surfaces is the function switching, which usually needs to be triggered by stimuli such as temperature, pH, salinity, or other external factors, as discussed previously. Importantly, some factors compromise the surface biocompatibility, and some are not suitable for applications in the human body. Using endogenous factors such as enzymes and sugars may provide a promising solution. Another important consideration for antibacterial surfaces is long-term stability and capability of a surface to maintain its property over time, which is crucial for clinical applications such as medical devices and implant materials. However, the long-term storage stability and surface performance are always ignored. Despite the successful killing and release of initially attached bacteria over short periods, whether the same strategy is applicable to biofilms formed over long-term periods remains unknown. Finally, many of the reports to date are proofs of concept, and some model surfaces could only be fabricated under laboratory conditions using sophisticated instruments and relatively complex procedures, which are not suitable for practical applications. Simple, cost-effective, environmentally friendly, and reproducible fabrication method are needed, and these important design criteria should be considered in future study. Tackling these important challenges may require collaborative efforts from

AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Qian Yu: 0000-0003-3612-6951 Hong Chen: 0000-0001-7799-4961 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by the National Key Research and Development Program of China (grant no. 2016YFC1100402), the National Natural Science Foundation of China (grant nos. 21774086, 21404076, and 21334004), and the Jiangsu Clinical Research Center for Cardiovascular Surgery.

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ACS Applied Materials & Interfaces Switchable Chitosan Wound Dressing through a ’Click’-Type Interfacial Reaction. Colloids Surf., B 2015, 136, 7−13. (92) Yuan, S.; Li, Y.; Luan, S.; Shi, H.; Yan, S.; Yin, J. InfectionResistant Styrenic Thermoplastic Elastomers That Can Switch from Bactericidal Capability to Anti-Adhesion. J. Mater. Chem. B 2016, 4, 1081−1089. (93) Sobolčiak, P.; Špírek, M.; Katrlík, J.; Gemeiner, P.; Lacík, I.; Kasák, P. Light-Switchable Polymer from Cationic to Zwitterionic Form: Synthesis, Characterization, and Interactions with DNA and Bacterial Cells. Macromol. Rapid Commun. 2013, 34, 635−639. (94) Cao, B.; Lee, C.-J.; Zeng, Z.; Cheng, F.; Xu, F.; Cong, H.; Cheng, G. Electroactive Poly(sulfobetaine-3,4-ethylenedioxythiophene) (PSBEDOT) with Controllable Antifouling and Antimicrobial Properties. Chem. Sci. 2016, 7, 1976−1981. (95) Kaur, R.; Liu, S. Antibacterial Surface Design − Contact Kill. Prog. Surf. Sci. 2016, 91, 136−153. (96) Huang, C. J.; Chen, Y. S.; Chang, Y. Counterion-Activated Nanoactuator: Reversibly Switchable Killing/Releasing Bacteria on Polycation Brushes. ACS Appl. Mater. Interfaces 2015, 7, 2415−2423. (97) Dong, Y.; Xiong, X.; Lu, X.; Wu, Z.; Chen, H. Antibacterial Surfaces Based on Poly(cationic liquid) Brushes: Switchability between Killing and Releasing via Anion Counterion Switching. J. Mater. Chem. B 2016, 4, 6111−6116. (98) Tan, M.; Wang, H.; Wang, Y.; Chen, G.; Yuan, L.; Chen, H. Recyclable Antibacterial Material: Silicon Grafted with 3,6-O-Sulfated Chitosan and Specifically Bound by Lysozyme. J. Mater. Chem. B 2014, 2, 569−576. (99) Wu, B.; Zhang, L.; Huang, L.; Xiao, S.; Yang, Y.; Zhong, M.; Yang, J. Salt-Induced Regenerative Surface for Bacteria Killing and Release. Langmuir 2017, 33, 7160−7168. (100) Cabanas-Danes, J.; Rodrigues, E. D.; Landman, E.; van Weerd, J.; van Blitterswijk, C.; Verrips, T.; Huskens, J.; Karperien, M.; Jonkheijm, P. A Supramolecular Host-Guest Carrier System for Growth Factors Employing VHH Fragments. J. Am. Chem. Soc. 2014, 136, 12675−12681. (101) Dubacheva, G. V.; Curk, T.; Mognetti, B. M.; Auzély-Velty, R.; Frenkel, D.; Richter, R. P. Superselective Targeting Using Multivalent Polymers. J. Am. Chem. Soc. 2014, 136, 1722−1725. (102) Neirynck, P.; Schimer, J.; Jonkheijm, P.; Milroy, L. G.; Cigler, P.; Brunsveld, L. Carborane-β-Cyclodextrin Complexes as a Supramolecular Connector for Bioactive Surfaces. J. Mater. Chem. B 2015, 3, 539−545. (103) Zhan, W.; Shi, X.; Yu, Q.; Lyu, Z.; Cao, L.; Du, H.; Liu, Q.; Wang, X.; Chen, G.; Li, D.; Brash, J. L.; Chen, H. Bioinspired Blood Compatible Surface Having Combined Fibrinolytic and Vascular Endothelium-Like Properties via a Sequential Coimmobilization Strategy. Adv. Funct. Mater. 2015, 25, 5206−5213. (104) Boekhoven, J.; Rubert Perez, C. M.; Sur, S.; Worthy, A.; Stupp, S. I. Dynamic Display of Bioactivity through Host-Guest Chemistry. Angew. Chem., Int. Ed. 2013, 52, 12077−12080. (105) Brinkmann, J.; Cavatorta, E.; Sankaran, S.; Schmidt, B.; van Weerd, J.; Jonkheijm, P. About Supramolecular Systems for Dynamically Probing Cells. Chem. Soc. Rev. 2014, 43, 4449−4469. (106) Bian, Q.; Wang, W.; Wang, S.; Wang, G. Light-Triggered Specific Cancer Cell Release from Cyclodextrin/Azobenzene and AptamerModified Substrate. ACS Appl. Mater. Interfaces 2016, 8, 27360−27367. (107) Zhan, W.; Wei, T.; Cao, L.; Hu, C.; Qu, Y.; Yu, Q.; Chen, H. Supramolecular Platform with Switchable Multivalent Affinity: PhotoReversible Capture and Release of Bacteria. ACS Appl. Mater. Interfaces 2017, 9, 3505−3513. (108) Qi, Z.; Bharate, P.; Lai, C.-H.; Ziem, B.; Böttcher, C.; Schulz, A.; Beckert, F.; Hatting, B.; Mülhaupt, R.; Seeberger, P. H.; Haag, R. Multivalency at Interfaces: Supramolecular Carbohydrate-Functionalized Graphene Derivatives for Bacterial Capture, Release, and Disinfection. Nano Lett. 2015, 15, 6051−6057. (109) Cao, L.; Qu, Y.; Hu, C.; Wei, T.; Zhan, W.; Yu, Q.; Chen, H. A Universal and Versatile Approach for Surface Bio-Functionalization: Layer-by-Layer Assembly Meets Host-Guest Chemistry. Adv. Mater. Interfaces 2016, 3, 1600600.

(110) Hu, C.; Qu, Y.; Zhan, W.; Wei, T.; Cao, L.; Yu, Q.; Chen, H. A Supramolecular Bioactive Surface for Specific Binding of Protein. Colloids Surf., B 2017, 152, 192−198. (111) Qu, Y.; Wei, T.; Zhan, W.; Hu, C.; Cao, L.; Yu, Q.; Chen, H. A Reusable Supramolecular Platform for the Specific Capture and Release of Proteins and Bacteria. J. Mater. Chem. B 2017, 5, 444−453. (112) Wei, T.; Zhan, W.; Cao, L.; Hu, C.; Qu, Y.; Yu, Q.; Chen, H. Multifunctional and Regenerable Antibacterial Surfaces Fabricated Using a Universal Strategy. ACS Appl. Mater. Interfaces 2016, 8, 30048− 30057.

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Smart Antibacterial Surfaces with Switchable ... - ACS Publications

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