Development of Antimicrobial and Antifouling Universal Coating via

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Interface-Rich Materials and Assemblies

Development of Antimicrobial and Antifouling Universal Coating via Rapid Deposition of Polydopamine and Zwitterionization Yu-Jhen Fan, Minh Tan Pham, and Chun-Jen Huang Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b01730 • Publication Date (Web): 16 Aug 2018 Downloaded from http://pubs.acs.org on August 19, 2018

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ABSTRACT Biomaterials-associated infections (BAIs) are related to bacterial colonization on medical devices, which lead to a serious medical burden, such as increased healthcare cost, prolonged hospital stays, high mortality and morbidity. To reduce the risk of infections, in this work, a new approach which make use of a bio-inspired coating with dual antimicrobial and antifouling functions was developed through rapid deposition of functional polydopamine (pDA) and antimicrobial copper ions, and subsequent conjugation of zwitterionic antifouling sulfobetaine (SB) moieties by the aza-Michael addition reaction. pDA permits surfaces-independent versatile functionalization on a variety of substrates, such as TiO2, SiO2, gold, plastics and Nitinol alloy. The characterizations for chemical elemental compositions and hydrophilicity by X-ray photoelectron spectroscopy and contact angle goniometer, respectively, indicating the successful grafting of SB moieties and the presence of copper ions in the pDA adlayers. Ellipsometric thicknesses of the thin films were followed to monitor the formation of pDA films and the changes after the post conjugation. UV-Vis spectroscopy and inductively coupled plasma-mass spectrometry revealed the coordination structure of catechol-Cu, and release profile of Cu2+ from the constructed functional coatings. Superhydrophilic and charge-balanced SB interface allowed effective resistance of bacterial adsorption. Intriguingly, we scrutinized that the release of bactericidal copper ions enables killing the residual amount of adsorbed bacteria. Moreover, viability tests for fibroblast cells indicate the excellent biocompatibility of the developed medical coatings. For the real-world implementation, the antifouling and antimicrobial coatings were applied on the commercially available silicone-based urinary catheters and evaluated the existence of bacteria by using the plate-counting assay. The results showed an undetectable level

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of living bacteria. Consequently, the dual functional medical coating offers a promising approach to eliminate BAIs for practical applications.

Keywords: Antifouling property, antimicrobial coating, zwitterionic materials, aza-Michael addition reaction, dopamine.


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INTRODUCTION Bacteria non-specifically adhere to a surface and settle to build a source of contamination. A large community of bacteria on surface produce an extracellular polymeric matrix, leading to development of biofilms.1 Bacteria in biofilms enable concealing from immune defences and endangering the efficacy of antibiotics.2, 3, 4, 5 In the modern society, the non-specific adsorption of bacteria on medical devices has become a crucial issue that can result in biomaterialsassociated infections (BAIs) and malfunction of medical devices.6, 7 Therefore, development of an effective antimicrobial coating on medical devices is of importance for clinical practices. Solutions to combat BAIs rely on either disrupting interactions between bacteria and surface, or killing adsorbed bacteria.8, 9 By far, a wide range of antimicrobial coatings have been developed and, however, these technologies have limited applicability due to cumbersome preparation process, needs of special instruments, and material dependence.8, 9, 10 In 2007, Messersmith et al. reported a multifunctional coating through simple dip-coating of objects in an aqueous solution of dopamine (DA) onto a wide range of inorganic and organic materials.11 The formed polydopamine (pDA) adlayers allow post-conjugation of amine- and thiol-containing organic species via Schiff base reaction and Michael-type addition. The evolutionary bio-inspired coating technology has provoked the rapid advance in polydopaminebased materials for environmental, energy, and biomedical applications.12, 13 Very recently, our group developed a new route for the post functionalization of pDA films by formation of βamino carbonyl linkages via aza-Michael reaction.14 Acrylate- or acrylamide-based molecules with antifouling oligo(ethylene glycol) (OEG) and zwitterionic sulfobetaine moieties were brought to react with pDA. The reaction occurs when the nucleophilic amine groups in pDA attach α,β-unsaturated carbonyl compounds. The results indicated the excellent resistance of the


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functionalized pDA films against bacterial adsorption, particularly for the samples with grafting of sulfobetaine acrylamide (SBAA). Nevertheless, the slow polymerization of DA with a deposition rate of 2.1 nm/h is a major challenge.15 Very recently, Xu et al. conducted a CuSO4/H2O2–triggered rapid deposition of pDA films onto universal surfaces.16 Reactive oxygen species (ROS) and Cu2+ produced by reactions of H2O2 and CuSO4 extremely enhance the polymerization rate of DA. Herein, a new approach to the development of a dual functional coating for antimicrobial and antifouling properties on various materials has been established based on the pDA chemistry. The functional basal layer of pDA was formed by CuSO4/H2O2-triggered rapid deposition, followed by grafting of zwitterionic SBAA via aza-Michael addition reaction. The chelated copper ions in the pDA films offer an antibacterial property against Gram-negative Escherichia coli (E. coli) and Gram-positive Staphylococcus epidermidis (S. epidermidis).17, 18 Meanwhile, the conjugated zwitterionic sulfobetaine (SB) moieties were responsible for prevention of bacterial adsorption due to the superhydrophilicity and charge balance.14 The contact angle and X-ray photoelectron spectroscopy (XPS) measurements were conducted for the wettability and interfacial elemental composition of coatings, as well as the chemical states of copper ions. Atomic force microscopy (AFM) and ellipsometry were applied to monitor the changes in the morphology and thickness during the film construction. The release profile of the copper ions was characterized by inductively coupled plasma mass spectroscopy (ICP-MS). The universal coating feature was confirmed by developing the films on various substrates. More importantly, the functional coatings were applied onto the commercially available silicone-based urinary catheter to determine the antibacterial efficiency. Consequently, the potent bio-inspired medical


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coating technology provides not only an effective and applicable route to address the BAIs, but also a versatile platform for developing multifunctional interfaces.


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EXPERIMENTAL SECTION Materials Dopamine hydrochloride, triethylamine (TEA), Trizma hydrochloride (Tris), HPLC grade ethanol, and copper sulfate pentahydrate (CuSO4·5H2O) were from Sigma-Aldrich. The protocol for the synthesis of sulfobetaine acrylamide (SBAA) was cited from the reference of Lee et al.19, 20, 21

Phosphate buffer saline (PBS) were acquired from Acros Organic. LIVE/DEAD BacLight

bacterial viability kit, MTT assay kit, and sodium dodecyl sulfate (SDS) were all purchased from Thermo Scientific. Luria-Bertani (LB) agar was obtained from BD Biosciences. Dulbecco’s modified Eagle’s medium (DMEM), fetal bovine serum (FBS), and tissue culture polystyrene (TCPS) were purchased from Gibco. Luria-Bertani broth (LB broth) was obtained from BD. All water used was purified to a resistivity of 18 MΩ·cm using the Academic Milli-Q Water System (Millipore Corporation) and filtered using a 0.22 µm filter. NIH 3T3 fibroblasts, S. epidermidis, and E. coli were provided by the Bioresource Collection and Research Center of Taiwan.

Deposition of pDA on Substrates Before coating pDA, substrates of TiO2, SiO2 (glass slide), Au, silicon wafer and Nitinol alloy (Jp&J Technic) were cleaned in a sonication bath of 1% SDS aqueous solution, acetone, and deionized (DI) water for 10 min of each, followed by drying in a stream of nitrogen. For polystyrene (PS) substrate, acetone was avoided to use in the cleaning process. The surface substrates, then, were cleaned to remove organic contaminants on surfaces by O2 plasma in a plasma cleaner (PDC-32G, Harrick Plasma, NY) for 10 min. The clean substrates were immediately immersed into a dopamine hydrochloride solution at a concentration of 2 mg/mL in a 50 mM Tris buffer at pH 8.5, containing CuSO4 (5 mM)/H2O2 (19.6 mM). The coating solution was stood at rt for different time (20 min, 40 min, 60 min, 120 min), followed by washing with DI water and drying in a stream of nitrogen.

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The coating prepared from the CuSO4/H2O2-

triggered rapid deposition was denoted as r-pDA, and the coatings with different deposition times from 20 to 120 min were denoted as r-pDA-20, r-pDA-40, r-pDA-60, and r-pDA-120.

Conjugation of SBAA


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The pDA-deposited substrates were soaked in the freshly prepared conjugation solution containing 100 mM SBAA and 30 µL of TEA in DI water (4 mL)/ethanol (0.8 mL) mixture. The reaction solutions were stirred by a magnetic bar at 55 °C for 24 h. Then, the substrates were removed, copiously rinsed with DI water and dried in a gentle stream of nitrogen.

Contact Angle Measurements Static water contact angles were measured via the sessile drop method using a contact angle goniometer (Phoenix mini, Surface Electro Optics). 5 µL water drops were placed on substrates by a microsyringe, and the measurements were carried out four times at random positions on substrates. The surfaceware9 software (Surface Electro Optics) was used to analyze the contact angle.

Thickness Measurements of Thin Films The air-dried thicknesses of r-pDA and r-pDA with conjugation of SBAA (r-pDA-SBAA) thin films on a silicon wafer were measured using an ellipsometer (Lse-Traveler, Gaertner) with a light source at a wavelength of 633 nm and a fixed incident angle of 70°. The refractive index of polymer thin films on the substrates was fixed to around 1.45. The thickness measurements were taken on four random spots on each sample.

Release Profile of Copper Ion The presence of copper ions on the pDA films were confirmed through UV-vis spectroscopy analysis. The samples of r-pDA-20, r-pDA-40, r-pDA-60, and r-pDA-120 on quartz slides were prepared as described above, and the pDA sample deposited via the conventional approach was used as a control sample. The absorbance of samples was scanned from a wavelength of 200 to 800 nm with 1 nm increments was recorded by an UV−vis spectrophotometer (V-600, JASCO, MD). ICP-MS (Agilent 7500ce, Japan) was used to monitor a release profile of copper ions from the r-pDA coatings. Coated substrate (1 cm X 1 cm) was placed into a 10 mL tube containing 5 mL of 0.85 wt% NaCl solution. The tubes were incubated in a water bath at 37 °C to release copper ions. The substrates were moved daily to new tubes containing 5 mL of fresh


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saline solution. The ICP-MS testing solution was prepared from 800 µL of the used saline solution from each tube, 160 mg of 70% nitric acid, 40 µL of 1 ppm internal standard, and 8 mL of DI water. The accumulative amount of released-copper ions over 8 days was recorded.23

Surface Characterization using XPS and AFM XPS measurements for the coatings on TiO2 substrates were conducted by using a microfocused and monochromatic Al Kα X-ray source (power = 25 W, energy of photons = 1486.6 eV, and beam spot = 100 µm; Sigma Probe, Thermo Scientific). The takeoff angle (with respect to the surface) of the photoelectron was set at 45°. The pressure of the system was controlled below 10−8 Pa using an oil-less ultrahigh vacuum pumping system. A dual beam charge neutralizer (7 V Ar+ and flooding 3 kV, 1 µA electron beam) was employed to compensate the charge-up effects. Spectra were collected with a pass energy set to 58.7 eV, while the binding energy measured was calibrated against the Ti2p peaks for TiO2 at 458.5 eV. An elemental ratio was analysed using a software of the PHI SUMMITT XPS for VersaProbe. AFM (Bruker, Dimension Edge, CA) was used to measure the surface SiO2 substrate coating roughness and morphology. A cantilever with a resonance frequency of 160 kHz and force constant of 7.4 N/m (NanoWorld AG) was used. The AFM was operated in a tapping mode. Three representative areas (5 µm X 5 µm) from each sample were randomly selected and scanned to obtain the topographic images. The images were then analyzed using the AFM Nanoscope Analysis 1.40 Bruker Corporation program.

Cell Viability Assays The viability of NIH 3T3 fibroblasts was assessed after the exposure to the coated substrates by MTT assay. The viable cells can metabolize soluble yellow-colored MTT (Merck) in their mitochondria into insoluble purple colored formazan.24 Fibroblasts in 24-well plates at an initial seeding amount of 1 × 104 cells/well were cultured in DMEM containing 10% of FBS at 37 °C in an incubator with 5% CO2 content for 24 h, followed by changing fresh serum-free DMEM. The TiO2 substrates modified with organic adlayers were soaked into culture wells containing fibroblasts and incubated for another 24 h. Afterward, fresh medium containing the MTT reagent (0.5 mg/mL) was added into wells. After incubation for 3 h at 37 °C, cells were solubilized by adding an equal volume of sterile DMSO. Multimode plate spectroscopic reader


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(Synergy HT, BioTek) was used to measure the absorbance of the samples at 540 nm. Samples without treatment were used as a positive control and set as 100 % viable cells. The average values were obtained from the triplicate.

Bacterial Attachment Test E. coli, S.epidermidis were used to assess the antimicrobial properties of the modified substrates. Bacteria were inoculated into 25 mL of LB Broth media. After 16 h incubation at 37 °C in an incubator with 5% CO2 content, the bacteria culture was diluted with PBS to an optical density OD670 of 0.1, corresponding to around 8 × 107 cells/mL. Then, the bacteria were collected by centrifugation at 5000 rpm for 1 min, followed by washing with sterile PBS, and resuspended in PBS in three replicates. The substrates were respectively immersed in the bacterial cell suspension solution at 37 °C for 3 h to allow bacterial absorption, followed by shaking at 100 rpm in fresh sterile PBS for 5 min. The attached bacterial cells on the substrate surfaces were observed by staining with 50 µL of LIVE/DEAD BacLight and covered with paraffin for 15 min at rt. Afterward, the substrates were rinsed with PBS for three times. The relative viable attached bacterial cells were evaluated by placing the cell-attached substrate under a fluorescence microscope (ZEISS Microscope Axio Obserber A1, Germany) with a magnification of 200× and an excitation wavelength of 488 nm. The bacterial fluorescence images were acquired at five random locations on each sample, and the number of the adsorbed bacteria was analyzed using an ImageJ software package (developed at National Institutes of Health, MA).

Antimicrobial Coating on Catheter Fortune urological silicone-based catheter (Catheter, Fortune Medical) device was bought for testing the antimicrobial effectiveness of the developed medical coatings. The bacterial solution containing S. epidermidis was prepared at an optical density OD670 of 0.1. The coated catheters fabricated as described above were immersed in the bacterial solutions. After incubation for 3 h at 37 °C, the catheters were rinsed gently three times with DI water to remove unattached bacteria. The catheters were then sonicated in a sonication bath for 7 min at 25 °C in 10 mL PBS to detach the adsorbed bacteria. The bacterial suspension was serially diluted 100-fold. 100 µL of the diluted-bacterial solution was plated on LB agar petri dish. Then bacteria colonies were


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counted after overnight incubation. The antibacterial efficiency (Eb) was measured using the following equation: ‫ܧ‬௕ =

ܰ௣ − ܰ௠ × 100% ܰ௣

Np and Nm are the numbers of colonies collected from the unmodified and modified catheter, respectively.


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RESULTS and DISCUSSION Preparation of Dual Functional Coatings The deposition of pDA on various materials has been widely exploited for the universal functional modification. The functional groups of pDA coatings allow subsequently grafting amine-, vinyl- and thiol-containing molecules, as well as chelating metal ions coatings.11, 14, 23, 25 For rapid deposition of pDA coatings, a mixture of CuSO4 and H2O2 was used as an activator for generating reactive oxygen species (ROS) of O2·-, OH· and HO2·, which play a key role in the polymerization of dopamine.22, 26 In this work, the versatile pDA coatings were prepared on TiO2 substrates by immersing them in a Tris buffer containing DA and CuSO4/H2O2 mixture for reaction times of 20, 40, 60, and 120 min, referred to r-pDA-20, r-pDA-40, r-pDA-60, and rpDA-120, whereas pDA-18h was prepared in Tris buffer without addition of CuSO4/H2O2. Zwitterionic acrylamide-based molecules (SBAA) were brought to react with amine groups in pDA basal adlayers via the aza-Michael addition for the formation of β-amino carbonyl linkage, and zwitterionized samples were referred to r-pDA-20-SBAA, r-pDA-40-SBAA, r-pDA-60SBAA, r-pDA-120-SBAA, and pDA-18h-SBAA (Scheme 1).

SO3

Substrate

SO3

N

H2N

O3S N

CuSO4 H2O2

NH N

O NH

HO

OH

O

Rapid deposition N

NH2

NH HN O

HN

N

N

aza-Michael addition O

O

O

O

O

pDA + Cu pDA

O

O

O

O

O

O

O

pDA + Cu

Substrate

Substrate

Antifouling and Antimicrobial Coating

Scheme 1. Schematic illustration of preparation of coatings for dual antifouling and antimicrobial properties.


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Characterization of Bio-inspired Coatings As shown in Figure 1, the static water contact angle on bare TiO2 was measured to be 70°, while that of pDA-18h, r-pDA-20, r-pDA-40, r-pDA-60, and r-pDA-120 varied from 33.7° to 39.9°, consistent with previous studies.11, 23, 27 For samples with the post-conjugation with SBAA, the contact angle values of pDA-18h-SBAA, r-pDA-20-SBAA, r-pDA-40-SBAA, r-pDA-60SBAA and r-pDA-120-SBAA were remarkably lower than 5°. The low contact angles present the superhydrophilic nature of zwitterionic SB moieties, ascribing to the strong ionic solvation with water molecules.28, 29, 30, 31, 32 Moreover, the newly discovered grafting chemistry via aza-Michael addition can be readily applied to the pDA films prepared both from conventional and rapid deposition approaches.

80 70 Contact angle [deg.]

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60 50 40 30 20 10 0 Ba

re

TiO 2 -18h A-20 -40 A-60 -120 BAA AA BAA AA AA B A D B B S D A pD r-p r-pD r-p r-pDA-18h- -20-S -40-S -60-S120-S A A A A pD r-pD r-pD r-pD r-pDA

Figure 1. Static water contact angle measurements for the substrates with and without modifications.

The time-dependent UV-vis absorbance of the pDA films on quartz substrates was followed to monitor the film formation. For the pDA-18h sample, an absorbance peak atλmax = 285 nm was found (Figure 2a). When the deposition process was triggered by a mixture of CuSO4/H2O2, a bathochromic shift to λ max = 298 nm was observed, and intensities of


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absorbance increased with the deposition time. The peak at λ max = 285 nm should be a combination of the characteristic peaks of leukochrome, dopachrome, and unreacted DA.33, 34 The absorbance at higher wavelength refers to more internally cyclized DA derivatives, suggesting a higher degree of oxidation of DA molecules. Moreover, a broad peak in a range of 500-700 nm appeared in r-pDA samples should indicate the presence of the coordination structure of catechol-Cu2+ in the films.35, 36 Collectively, DA molecules subjected oxidation to form quinone structures and rapidly transform into leukochrome and other cyclized derivatives.34 The mixture of CuSO4/H2O2 in the solution generates radicals to accelerate the oxidation process, leading to the abundant amount of cyclized products. In addition, the co-deposition of Cu2+ was suggested by UV-vis spectra and, thus, the CuSO4/H2O2-triggered rapid deposition can serve as a method for preparation of antimicrobial coatings. The thicknesses of r-pDA and r-pDA-SBAA thin films as a function of time were measured by ellipsometry (Figure 2b). The DA molecules were deposited onto the silicon wafer for 20, 40, 60, and 120 min, followed by the conjugation of SBAA. For the r-pDA thin films, the deposition rate is 16.4 nm/h, which is much faster than 2.1 nm/h with the conventional pDA deposition method.11 However, after post-modification with SBAA, the film thicknesses considerably decreased, likely due to replacement of pDA by grafted SBAA and release of loosely bound pDA macromolecules during the treatment.37, 38 Currently, the stability of pDA coatings was examined using surface-plasmon resonance imaging system in different solutions.38 The results reveal that the coating stability was mostly dependent on pH of aqueous solutions, giving detachment ratios up to 66% and 80% at pH 1.0 and pH 14.0. In this work, the conjugation of SBAA was carried out in an alkaline condition at 55 °C for 24 h, which very likely causes the reduction in the film thickness of pDA. Nevertheless, the interfacial properties of the pDA films are considerably moderated by the surface chemistry, which will be characterized in the following tests.


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Figure 2. UV-vis spectra of pDA films on quartz substrates prepared from the CuSO4/H2O2triggered rapid deposition and conventional approaches (a). Ellipsometric thicknesses of r-pDA and r-pDA-SBAA as a function of pDA deposition time (b).

The surface morphology and roughness of r-pDA-40 and r-pDA-40-SBAA on SiO2 substrates were accessed by AFM in Figure 3. The roughnesses, Rq, of bare SiO2 and r-pDA-40 were Rq = 1.20 and 4.08 nm, respectively. The increased Rq could be attributed to deposition of the large pDA aggregates on the film. After the conjugation of SBAA, the Rq of r-pDA-40SBAA decreased to 0.45 nm, which may reflect the detachment and replacement of the pDA aggregates from the films. The data can explain the findings in the ellipsometric measurements and previous work, where the reduced thickness of pDA films was observed after the further treatments.38


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Figure 3. AFM images of coatings of bare (a), r-pDA-40 (b) and r-pDA-40-SBAA (c) on SiO2.

Chemical Compositions of Functional pDA Coatings XPS measurements were carried out to verify chemical compositions and coordination structures of copper ions in pDA films. The CuSO4/H2O2-triggered pDA coatings were deposited on TiO2 substrates for 40 min, followed by the chemical attachment of SBAA via the azaMichael addition reaction. Ti2p spectra for samples of bare TiO2, r-pDA-40 and r-pDA-40SBAA were shown in Figure 4a. The peaks centered at binding energies (BEs) of 458.5 and 464.3 eV for bare TiO2 samples are attributed to Ti2p1/2 and Ti2p3/2, respectively, of O-Ti-O, while no peak was observed in r-pDA-40 and r-pDA-40-SBAA, which can be explained by large thicknesses of coatings beyond the limited probing distance of XPS (~10 nm).14, 39 In Figure 4b, the N1s core level spectrum of r-pDA-40 appears characteristic signals of tertiary (=N−C, BE = 398.6 eV), secondary (C−NH−C, BE = 399.9 eV), and primary amines (C−NH2, BE = 401.9 eV). 40, 41

After the conjugation of SBAA, r-pDA-40-SBAA coatings showed a peak component at BE

= 402.5 eV, corresponding to the presence of quaternary ammonium (-NMe3+) in the SB moieties. Moreover, in Figure 4c, a spin-orbit doublet at BEs = 167.0 and 168.2 eV in the S2p spectrum of r-pDA-40-SBAA is attributed to the presence of -SO3-. The atomic ratio of –NMe3+/-SO3- form the XPS measurements was 1.09, which is approximate to the stoichiometric value of SB


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moieties. Therefore, from the evidence of XPS results, we can confirm the successful conjugation of SBAA on the rapidly deposited pDA films via the aza-Michael addition.

Figure 4. XPS spectra of Ti2p (a), N1s (b), and S2p (c) for samples of bare TiO2, r-pDA-40 and r-pDA-40-SBAA.


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In order to investigate the chemical state of immobilized copper, we further to analyze the spectra of Cu2p3/2 and Auger Cu LMM in Figure 5. The peak component at BE = 934.4 eV contributed to Cu2+.

42, 43

The lower peak component at BE = 932.7 eV can be assigned to Cu+

and Cuo, which is unable to be discerned by XPS. Thus, the auger electron spectroscopy (AES) was used to detect the copper species (Figure 5c, d). The Auger Cu LMM spectra for both samples of r-pDA-40 and r-pDA-40-SBAA show that the peaks were centered at BE = 570 eV, corresponding to Cu+, whereas the characteristic peak (BE = 568 eV) for Cu0 was not found. Therefore, compared with the results from the UV-Vis spectroscopy, Cu2+ and Cu+ were both deposited in the pDA films. The Cu2+ ions were chelated by catechol groups of pDA, and Cu+ ions reducing from the oxidant of Cu2+ should present in a form of Cu2O in the oxidation and polymerization process of DA.44, 45 Herein, the compositions of the zwitterionic SB moieties and antimicrobial agent of copper ions in the pDA films prepared from rapid pDA deposition and facile post-conjugation approaches were confirmed by XPS. The potential of the coatings in medical applications will be examined in bacterial tests.


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Figure 5. Cu2p3/2 spectra for samples of r-pDA-40 (a) and r-pDA-40-SBAA (b). XAES spectra of Auger Cu LMM for samples of r-pDA-40 (c) and r-pDA-40-SBAA (d).

Release Profile of Cu Ions and Cytotoxicity of Functional pDA Coatings The accumulative release profile of copper ions from the pDA films was followed by using ICP-MS in Figure 6a. The linear release profiles of copper ions were witnessed over 8 days from the

samples

of

r-pDA-40

and

r-pDA-40-SBAA.

It was calculated that the release rates from r-pDA-40 and r-pDA-40-SBAA coatings on glass substrates with 1 x 1 cm were 19.42 ppb/day and 12.48 ppb/day, respectively, corresponding to 9.71 x 10-7 and 6.24 x 10-7 mg/day. The lower release rate of r-pDA-40-SBAA should be attributed to the thinner pDA film as measured by ellipsometry. Moreover, the results also illustrate that the grafted SBAA adlayer does not hamper the release of copper ions into exterior environment. The toxicity of copper ions released from the films needs to be clarified before applying the coatings for medical uses. NIH-3T3 fibroblast cells were co-incubated with modified TiO2 substrates in culture medium for 24 h, followed by the MTT test. As shown in Figure 6b, the cell viability values of all testing samples were all higher than that of the control sample of bare TiO2 substrate. According to Dietary Reference Intakes, set by the U.S. Food and Nutrition Board of the Institute of Medicine, the reference daily intake and the tolerable upper intake for copper ions are 0.9 and 10 mg/day, respectively,46 which are much higher than that from r-pDA-40 and rpDA-40-SBAA coatings. In addition, it was reported that pDA coatings attenuated the toxicity effect of semiconductor quantum dots in blood

47

and

enhanced blood compatibility of

48

materials. SB-related materials have been applied for the medical applications due to their high biocompatibility.49, 50 Accordingly, the released copper ions from the coatings cause negligible cytotoxicity, and the coatings can be regarded as biocompatible materials for medical applications.


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Figure 6. The accumulative Cu release profiles of r-pDA-40 and r-pDA-40-SBAA coatings by ICP-MS measurements (a). Viability tests for co-incubation of NIH-3T3 fibroblast cells and coated substrates with respective to the control sample of bare TiO2 (b).

Antimicrobial Property of Functional pDA Coatings The medical campaigns have seriously emerged from bacterial infections and drug resistance in hospitals. Metal ions, such as gold, zinc, silver, titanium, and copper, have been reported to serve as alternative antimicrobial agents to minimize or overcome the alarming risk of infections.51 Among the antimicrobial metal ions, copper ions have widely used against a wide range of bacterial species due to high accessibility and powerful biocidal potency. In addition, copper and many of its alloys were registered as antimicrobial materials at the U.S. Environmental Protection Agency (EPA) in 2008. Copper ions undergo redox reactions between Cu+ and Cu2+, leading to transmitting electrons to hydrogen peroxide, and consequently producing hydroxyl radicals impairing intracellular bacteria.52, 53 Herein, the catechol functional groups of the pDA films were used for chelating copper ions to provide sustainable biocidal coatings.15, 16, 54, 55 Meanwhile, the subsequently conjugated SBAA allows repellence of bacterial adsorption.56 The dual antifouling and antimicrobial properties of the coatings toward E. coli and S. epidermidis were verified by observing the numbers of adherent bacteria and the fraction dead. In Figure 7a, the live/dead images for E. coli on bare TiO2, pDA and SBAA functionalized coatings was shown. The quantitative data for the total number of adherent bacteria and their fraction dead are present in Figure 7b and S1 for E. coli and S. epidermidis, respectively. The


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amounts of adsorbed bacteria seem to decrease with the deposition time of pDA and zwitterionized pDA films enable to resist the bacterial adsorption by 96% with respect to that on bare TiO2 surfaces, in agreement with previous works.8, 14, 57 The features of superhydrophilicity and charge balance of SB moieties at interfaces permit the formation of highly structured bound water layers to avoid the interaction between foulants and surfaces. Interestingly, the thick pDA films prepared from the CuSO4/H2O2-triggered rapid deposition reduced the numbers of bacteria, which should be associated with the release of adsorbed bacteria during the washing step owing to the low stability of the r-pDA films. Additionally, the r-pDA films exhibited antimicrobial property as indicated by the high fraction dead. However, the fractions did not correlate with the thickness of the r-pDA films. We hypothesized that the as-prepared r-pDA films with higher thickness should contain more copper ions and exhibit the faster release rate than that of SBAA-conjugated r-pDA films. Nevertheless, the envelope structure of the bacteria adhered on the zwitterionized r-pDA films may be destructed due to the surface wetting property and textures to permit better antimicrobial effectiveness of copper ions.58, 59 Herein, the antifouling and antimicrobial SBAA grafted r-pDA coatings were exploited to potentially restrain BAIs.


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Figure 7. Live/dead fluorescent images of adherent E. coli on bare and modified TiO2 substrates with a scale bar of 10 μm (a). The quantitative analysis for the number of adsorbed E. coli and fraction dead on bare and modified TiO2 substrates (b).

Universal Antifouling and Antimicrobial Coatings The capability of the substrate-independent coating was accessed by depositing r-pDA films on substrates of TiO2, SiO2, polystyrene (PS), silicon wafer, gold, and Nitinol, followed by covalent conjugation of SBAA. As shown in Figure 8a, the modification of SBAA afforded highly hydrophilic surfaces on all types of substrates, demonstrating the unique universal bioadhesive property of DA molecules to facilitate subsequent functionalization. Moreover, the antifouling and antimicrobial properties of r-pDA-40-SBAA on various materials were tested and compared to the bare substrates by observing the adhesion and viability of E. coli (Figure 8b and c). Obviously, the numbers of adsorbed bacteria were greatly reduced


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on the coated substrates by more than 95% with respect to that on their bare substrates. As a result, the antifouling and antimicrobial properties of functional coatings were well displayed on all substrates as a potential universal coating for different medical devices to harness the infection issues.

Figure 8. The wetting property of the modified substrates of TiO2, SiO2, polystyrene (PS), silicon wafer, gold, and Nitinol for comparison with their bare surfaces (a). The numbers (b) and fraction dead (c) of adsorbed E. coli on bare and r-pDA-40-SBAA modified substrates.

Antifouling and Antimicrobial Coatings on Silicone-based Urinary Catheters The adhesion of bacteria onto implants causes threatening infections in clinical practice.60, 61

S. epidermidis is commonly found in catheter-based infections and the biofilms show

insusceptible to antibiotic agents.62, 63, 64, 65 In this work, the capability of dual functional coatings on the urinary catheters for avoiding infection of S. epidermidis was evaluated by using the platecounting assay. In Figure 9a, the appearance of the modified silicone-based catheters was different due to the deposition of pDA and SBAA modification. The r-pDA-40 coating displays


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darker than that of r-pDA-40-SBAA, ascribed to the depletion of the pDA adlayer after the SBAA conjugation. In bacterial tests, the adsorbed bacteria were removed from the catheters in a sonication bath, and the solutions were diluted and applied on LB agar plates for the bacterial colony formation. The results in Figure 9b-d showed that the r-pDA-40 coating enables reduction of the bacterial growth. Moreover, the viability of bacteria can totally be suppressed on the rpDA-40-SBAA coating, indicating its effective and practical antimicrobial and antifouling properties on medical devices.

Figure 9. Photograph of silicone-based urinary catheters with and without surface modification (a). The plate-counting assays for S. epidermidis released from catheters without modification (b) and modification of r-pDA-40 (c) and r-pDA-40-SBAA (d).


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CONCLUSIONS In the present work, we have designed and prepared a new medical coating with dual antifouling and antimicrobial properties by rapid CuSO4/H2O2-triggered deposition of composite pDA films, followed by covalent conjugation of SBAA via aza-Michael addition. The azaMichael addition is a reaction in which the nucleophilic amine groups attach α,β-unsaturated carbonyl compounds. The acrylate- or acrylamide-based molecules, such as SBAA, react with amine groups in pDA to form β-amino carbonyl linkage. The chelated copper ions permitted sustainable release profiles to suppress bacterial growth. The zwitterionic conjugated SBAA exhibited excellent repellence against bacterial adsorption. The promising fouling resistance and antimicrobial properties of r-pDA-SBAA coatings were confirmed by low adherent bacterial numbers and high fraction dead. Although the deposition method allowed a high deposition rate, the film thickness and roughness decreased after zwitterionization, likely due to depletion of rpDA films in an alkaline condition. Moreover, the universal and superhydrophilic characteristic of SBAA grafted r-pDA films were clearly demonstrated on various substrates. A proof-ofconcept demonstration of the functional r-pDA coatings on silicone-based urinary catheters for inhibition of bacterial growth was declared to approach real-world applications.


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ACKNOWLEDGMENT The authors acknowledge the Ministry of Science and Technology (MOST 105-2628-E-008 -007 -MY3; 106-2119-M-194 -002) for financial support of this project.

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Development of Antimicrobial and Antifouling Universal Coating via

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