Transparent, adhesive and conductive hydrogel for soft bioelectronics

Conductive hydrogels are promising materials for soft electronic devices. .... visible light, the hydrogel had UV-shielding ability, which is useful a...
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Article Cite This: Chem. Mater. 2018, 30, 5561−5572

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Transparent, Adhesive, and Conductive Hydrogel for Soft Bioelectronics Based on Light-Transmitting Polydopamine-Doped Polypyrrole Nanofibrils Lu Han,†,⊥ Liwei Yan,†,⊥ Menghao Wang,† Kefeng Wang,‡ Liming Fang,§ Jie Zhou,† Ju Fang,∥ Fuzeng Ren,∥ and Xiong Lu*,†

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†

Key Lab of Advanced Technologies of Materials, Ministry of Education, School of Materials Science and Engineering, Southwest Jiaotong University, Chengdu 610031, Sichuan, China ‡ National Engineering Research Center for Biomaterials, Genome Research Center for Biomaterials, Sichuan University, Chengdu 610064, Sichuan China § Department of Polymer Science and Engineering, School of Materials Science and Engineering, South China University of Technology, Guangzhou 510641, China ∥ Department of Materials Science and Engineering, Southern University of Science and Technology, Shenzhen 518055, Guangdong China S Supporting Information *

ABSTRACT: Conductive hydrogels are promising materials for soft electronic devices. To satisfy the diverse requirement of bioelectronic devices, especially those for human−machine interfaces, hydrogels are required to be transparent, conductive, highly stretchable, and skin-adhesive. However, fabrication of a conductive-polymerincorporated hydrogel with high performance is a challenge because of the hydrophobic nature of conductive polymers making processing difficult. Here, we report a transparent, conductive, stretchable, and self-adhesive hydrogel by in situ formation of polydopamine (PDA)doped polypyrrole (PPy) nanofibrils in the polymer network. The in situ formed nanofibrils with good hydrophilicity were well-integrated with the hydrophilic polymer phase and interwoven into a nanomesh, which created a complete conductive path and allowed visible light to pass through for transparency. Catechol groups from the PDA−PPy nanofibrils imparted the hydrogel with self-adhesiveness. Reinforcement by the nanofibrils made the hydrogel tough and stretchable. The proposed simple and smart strategy of in situ formation of conductive nanofillers opens a new route to incorporate hydrophobic and undissolvable conductive polymers into hydrogels. The fabricated multifunctional hydrogel shows promise in a range of applications, such as transparent electronic skins, wound dressings, and bioelectrodes for see-through body-adhered signal detection.

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INTRODUCTION

there continues to be a need for intrinsically conductive hydrogels with good stability and high transparency. Conductive polymers (CPs), such as polypyrrole (PPy), polyaniline, and poly(3,4-ethylenedioxythiophene), have good electrical characteristics and softer mechanical properties than metals for flexible electronic devices, and CPs are also potential candidate fillers in the fabrication of transparent conductive hydrogels.15−18 However, CP-based bulk hydrogels are generally opaque, such as pure PPy- and polyaniline-based hydrogels by a direct oxidation process.19,20 One approach to obtain a transparent CP hydrogel is to produce nanostructured CP fillers and incorporate them into the transparent matrix. If

Conductive hydrogels for biomedical applications, especially wearable devices, require flexibility and tissue-adhesiveness to allow integration with the human body.1−4 Transparency is also an important requirement for biomedical electronics when applied in see-through surgical operations.2,5,6 However, most of the reported conductive hydrogels are opaque because they contain high concentrations of nontransparent conductive nanofillers, such as metal-based (Au, Ag, Ni) nanowires or nanoparticles7−9 and carbon-based nanomaterials.2 Another route for realizing a transparent and conductive hydrogel is to produce ionogels comprising an ionic liquid hosted with a three-dimensional polymer network;10−12 however, the stability of those ionogels is uncertain because of the leakage of ions,13,14 especially in physiological environments. Thus, © 2018 American Chemical Society

Received: April 9, 2018 Revised: July 21, 2018 Published: July 23, 2018 5561

DOI: 10.1021/acs.chemmater.8b01446 Chem. Mater. 2018, 30, 5561−5572

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Chemistry of Materials

visible spectrum even if it was thicker than 1 mm. In addition to transparency in visible light, the hydrogel had UV-shielding ability, which is useful as dressing for protection against UV irradiation. The hydrogel was also flexible and stretchable, allowing it to tolerate a large strain exceeding 2000%. The hydrogel retained the strong adhesiveness of PDA and therefore can freely adhere to the human body without any external aid. Compared with previously reported CP hydrogels that are generally opaque and nonadhesive, the current conductive hydrogel can be used as self-adhesive and transparent bioelectrodes that can be directly adhered to the human body to accurately detect biosignals.

the average diameters of the CP nanofillers are less than half of the shortest wavelength of visible light, the CP hydrogel can be rendered transparent. However, these nanoscale fillers are prone to aggregate, leading to decreased conductivity because the hydrophobic nature of CPs makes them insoluble and incompatible with the hydrophilic polymer phase during hydrogel preparation.17,21,22 Thus, the transparency and conductivity are contradicting attributes of CP hydrogels, and the optimization of transparency and conductivity thus remains a big challenge in the preparation of CP hydrogels for biomedical applications.23 Recently, small molecules were added to endow the CP with high conductivity, transparency, and stretchability.16 However, the use of CP components to fabricate hydrogels is still limited by the hydrophobicity of CPs, which precludes complete integration of CP with the hydrophilic hydrogel matrix. Mussel-inspired polydopamine (PDA) is a promising material for improving the hydrophilicity of hydrophobic substrates, which sheds light on functionalizing hydrophobic CPs to overcome their poor dispersibility in water.24 PDA has many advantages that can be exploited to functionalize CPs and consequently to modify the physiochemical properties of CP. First, PDA has high hydrophilicity because of its functional groups, such as the carboxyl, amino, imine, and phenol groups.25 Second, the reactive catechol groups on the hydrophilic PDA can form a complex with the CP through many types of interactions.25,26 Third, through its functional groups, PDA can react with a wide range of molecules and can therefore enhance the interactions between the CP and the polymer matrix.25,27 Fourth, PDA shows robust and strong adhesiveness to a variety of surfaces, particularly wet mucosal surfaces and tissues, which has been demonstrated to be beneficial for wound healing, surgical tissue adhesives, and tissue engineering.28−30 Finally, PDA is also biocompatible and cell affinitive, which can promote cell adhesion, proliferation, and differentiation.31,32 Thus, PDA can improve the biocompatibility of the CP on the cellular level. Recently, mussel-inspired hydrogels were developed by introducing catechol groups into the polymer networks.25,33 These hydrogels showed great potential for use in various biomedical applications, including tissue adhesives, drugdelivery systems, and cell-culture platforms by utilizing different DOPA chemistries.33 On the basis of mussel adhesion chemistry, our group designed tough and self-adhesive hydrogels that can be used for tissue repairing.34,35 We had also previously employed PDA to functionalize carbon nanomaterials, which is a critical step in the formation of hydrogels with well-dispersed carbon nanomaterials, and to endow the hydrogel with conductive and adhesive properties.36,37 However, those conductive hydrogels are black and opaque because of the high content of nontransparent carbon nanomaterials inside the hydrogel network, and the hydrogels cannot satisfy the requirement of wearable conductive devices. In particular, both transparent and conductive properties are highly required for electronic skins and stretchable displays.2,6 In this study, we prepared a transparent, stretchable, adhesive, and conductive hydrogel realized by the in situ formation of polydopamine-doped polypyrrole (PDA−PPy) nanofibrils, which were interwoven in an elastic and transparent polyacrylamide (PAM) network. The hydrogel features a high intrinsic conductivity of 12 S/m. Due to the light transmittability of the nanomesh with interwoven nanofibrils, the hydrogel exhibited a high transmittance of 70% across the

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EXPERIMENTAL SECTION

Materials. Dopamine (DA), pyrrole (Py), ammonium persulfate (APS), N,N′-methylene bis(acrylamide) (BIS), tetramethylethylenediamine (TMEDA), and poly(vinyl alcohol) (PVA, Mr = 2000 Da) were purchased from Sigma-Aldrich (USA). Acrylamide (AM), sodium hydroxide (NaOH), and ferric chloride (FeCl3·6H2O) were purchased from Chengdu Kelong (China). All chemicals were reagent grade. Synthesis of PDA−PPy Nanoparticles. The PDA−PPy nanoparticles (NPs) were synthesized by a modified aqueous dispersion polymerization method. First, PVA (1.5 g) was dissolved into deionized water (20 mL) at 90 °C with magnetic stirring, and then, the solution was cooled to room temperature. Second, FeCl3·6H2O (4.6 mmol, 1.2 g) was dissolved into the PVA solution, and the mixture was transferred to an ice−water bath. Third, Py monomer (2 mmol, 140 μL) and DA monomer (0.05 g) were added into the above solution, and the mixed solution was continually stirred in an ice− water bath for 9 h to allow the Py and DA monomers to completely polymerize, with the color of the resulted solution changing to fully black. Fourth, the resulted solution went through three cycles of centrifugation and washing with hot water to remove impurities. Finally, the PDA−PPy NPs were obtained and were stored at 4 °C for further use. Pure PPy NPs without DA addition were also prepared using the same procedure. Preparation of the PDA−PPy−PAM Hydrogel. In a typical hydrogel synthesis process, PDA−PPy NPs (15.6 mg) were welldispersed in deionized water (8 mL) with magnetic stirring. Then, 2.6 g of AM monomers were dissolved in the PDA−PPy dispersion, forming a homogeneous dark dispersion. Subsequently, APS, BIS, and TMEDA were added to the above mixture with stirring. After 5 min of stirring, the stirrer was removed, and the AM monomers were polymerized to form a pregel. The pregel was sealed and stored under an ambient environment for 3 days of aging until the transparent PDA−PPy−PAM hydrogel was obtained. For comparison, PDA− PPy−PAM hydrogels with different contents of PDA−PPy NPs were prepared, and PPy−PAM hydrogels incorporating pure PPy NPs without PDA were also prepared. The contents of the hydrogels are listed in Table S1. Characterization of PDA−PPy NPs. The hydrophilicity of the PDA−PPy NPs was confirmed by molecular dynamics (MD) simulation. The morphologies of the NPs were investigated by using scanning electron microscopy (SEM; JSM 6390, JEOL, Japan). The mean particle size and the polydispersity index of the NPs were determined by dynamic light scattering (DLS) with a laser particle analyzer (ZETA-AIZER, Malvern, UK). For detailed methods, please refer to the Materials and Methods section of the Supporting Information. MD Simulation on the Hydrophilicity of the PDA−PPy Complex. The trimer dopamine (PDA) was built according to a previously reported possible structure of polydopamine, as shown in Figure S5a.38 The model of the PPy system (Figure S5c) contained 720 PPy chains, and each PPy chain comprised 10 Py monomers (Figure S5b). The PDA−PPy complex contained 720 PPy chains and 260 PDA trimers (Figure S5d). The size of the cluster was 60 × 52 × 98 Å3, and the density of the cluster for PPy and the PDA−PPy 5562

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Figure 1. Transparent, conductive, stretchable, and adhesive hydrogel by in situ formation of PDA−PPy nanofibrils. (a-i) Formation of hydrophilic PDA−PPy NPs. (a-ii) PDA−PPy NPs with highly hydrophilic properties. (b) Opaque pregel was formed after AM monomers polymerized in the suspension of the PDA−PPy NPs, and a transparent hydrogel was obtained after 3 days of aging. (c) In situ formation of PDA−PPy nanofibrils. During the aging process, APS generated radicals that continuously broke down the PDA−PPy NPs into nanodots, which self-assembled to form nanofibrils under the templating effect of the PAM chains. (d) SEM image of PDA−PPy NP-embedded opaque pregel, which absorbed light. (e) SEM image of nanofibrils in the transparent hydrogel, which allowed visible light to pass through while blocking UV irradiation. (f) Representative photo of the transparent hydrogel covering on a leaf. (g) Hydrogel was stretchable and conductive. complex was set to 1.47 g/cm3 according to previous investigations.39 CHARMM GENeral Force Field (CGENFF) parameters for Py were assigned to PPy.40 The force field for PDA was calculated by the Force Field Toolkit (FFTk) developed by Mayne et al.41 based on a first-principle calculation. All the parameters were adopted into the CHARMM force field for the system simulation. The MD calculations were performed using NAMD 2.12 code.42 Periodic boundary conditions in explicit TIP3P water environment were applied to both systems, and a cutoff of 12 Å was applied for van der Waals interactions and electrostatic interactions in real space. The Particle− Mesh−Ewald summation (PME) was employed to describe the longrange electrostatics. The SHAKE algorithm was enabled, and a time step of 1 fs was set to the system. The details are provided in the Supporting Information. Characterization of the PDA−PPy−PAM Hydrogel. The microstructures of the hydrogels were examined using SEM. The transmission spectra of the hydrogels were measured on a UV−visible (UV−vis) spectrometer (TU-1901, Puxi, China) equipped with deuterium and tungsten lamps from 400 to 900 nm. To evaluate the UV-shielding performance, the transmittance spectra of the hydrogels were measured on the UV−vis spectrometer from 200 to 350 nm. The electrical conductivity of the hydrogels was tested by a two-probe method using a potential state (CHI 660, USA). The tissue-adhesive strength of the hydrogels was tested by the universal test machine

(UTM, Instron 5567, USA). The mechanical properties were performed on the UTM with a 100 N load cell. Each mechanical test was repeated with five individual samples. For detailed methods, please refer to Figure S1 and Eq S1 in the Supporting Information. Swelling Characterization. In order to evaluate the water uptake capacity of the hydrogels, the swelling behaviors of three kinds of hydrogels, including PDA−PPy−PAM, PPy−PAM, and PAM, were tested. The content of the PDA−PPy complex and the PPy NPs in the hydrogel was 0.6 wt %, as listed in Table S1. Before the experiments, the hydrogels were first dried with a critical point dryer, and the weight of the initial dried hydrogel (W0) was recorded. Then, the hydrogels were soaked in deionized water. At different time intervals, the weight of the hydrogels was recorded, denoted as Ws. Three parallel samples were used for the tests. The water uptake was calculated using the following equation:

water uptake (W %) = (Ws − W0)/W0 × 100% Cell Culture. In order to evaluate the biocompatibility of PDA− PPy−PAM hydrogels, bone marrow stem cells (BMSCs) were used for a cytotoxicity test. BMSCs were extracted from 7 day old Sprague−Dawley rats as described in our previous studies.43 The PDA−PPy−PAM hydrogels with 0.6 wt % of PDA−PPy NPs and the PAM hydrogel were used. Before the cell culture, the hydrogels were purified by immersing them in sterilized phosphate-buffered saline 5563

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Figure 2. MD simulation on the hydrophilicity of the PDA−PPy complex. (a, b) Snapshot of the PPy system, which contained 720 PPy chains and 3921 water molecules: (a) initial configuration; (b) final configuration. (c, d) Snapshot of the PDA−PPy system, which contained 720 PPy chains, 260 PDA trimers, and 3921 water molecules: (c) initial configuration; (d) final configuration. (e, f) Atomistic distribution along the normal axis (z) to the polymer−water interface: (e) PPy system; (f) PDA−PPy system. Blue curve represented all the atomistic distributions of the system, and red curve represented the atomistic distributions of O atoms in water.

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and swelled to the equilibrium state for 2 days in a CO2 incubator at 37 °C. BMSCs (passage 4) were seeded on the hydrogels with a density of 5 × 104 cells/hydrogel. After 3 and 7 days of culture, a 3(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay was used to evaluate the proliferation of the BMSCs. The morphology of the cells grown on the hydrogels was observed by confocal laser scanning microscopy (CLSM; TCSSP5, Leica, Germany) after the cells were stained by calcein AM (A017, USA). The experimental details are provided in the Supporting Information. In Vivo Demonstration of the Hydrogel as UV-Shielding Dressing. Three mice (6−8 weeks, weighing 20−25 g) were used for the animal experiment. Before testing, the dorsal skin surface was shaved and cleaned. Then, the back skin was irradiated by UV light (30 mW/cm2, 365 nm) for 20 min with different treatments: (1) covered by the PAM hydrogel; (2) covered by the PDA−PPy−PAM hydrogel (0.6 wt % PDA−PPy NPs); (3) naked skin area without hydrogel protection (Figure S18a). The rat was anaesthetized by receiving an intraperitoneal injection of pentobarbital (2 wt %, 2 mL/ kg). Then, all of the groups were irradiated. After UV irradiation, the animals were euthanized by cervical dislocation, and the skin at the irradiated site was collected and fixed in 10% formalin. The skin surface tissue was cut into 4 μm thick vertical slices for cross-sectional observation. Histological observations were performed after hematoxylin−eosin (H&E) and Masson trichrome staining. The experiments were performed in accordance with protocols approved by the local ethical committee and laboratory animal administration rules of China. The details are provided in the Supporting Information.

RESULTS AND DISCUSSION

Design Strategy for the PDA−PPy−PAM Hydrogels. The hydrogels were prepared in a simple two-step process, as schematically shown in Figure 1. First, hydrophilic PDA−PPy NPs were synthesized by Fe3+-induced aqueous dispersion copolymerization of the DA and Py monomers through noncovalent interactions between the PPy and PDA chains (Figure S2), such as π−π stacking and hydrogen bonding.23,24 Note that DA would be not oxidized to PDA with a higher molecular weight in a FeCl3 solution with low pH value. However, FeCl3 is a strong oxidant and can participate in the initial oxidation of DA as well as convert 5,6-dihydroxyindole into the corresponding quinone via hydrogen abstraction.25 Thus, during the formation of the PDA−PPy complex, DA oligomers with a low molecular weight were formed, as analyzed by mass spectrometry (Figure S3). There were still unoxidized catechol groups in the PDA−PPy complex, which were essential to the adhesiveness of the hydrogel.35 In the second step, AM monomers were mixed in the dispersion of the PDA−PPy NPs and then polymerized into a pregel with the presence of APS as the initiator via a free-radical polymerization. After gelation, the pregel was stored in an ambient environment for 3 days of aging to allow the in situ formation of PDA−PPy nanofibrils from PDA−PPy NPs, which was critical for the fabrication of a conductive and 5564

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Figure 3. Transparency and UV-shielding performance of the hydrogel. (a) Photos of the color changes of the hydrogel correlating with the process of nanofibrils formation. (b) UV−vis transmittance spectra of a freshly prepared pregel and the same gel after 1 and 3 days of aging. (c) Digital photos of the hydrogels containing different PDA−PPy contents. (d) UV−vis transmittance spectra of hydrogels with different PDA−PPy contents after 3 days of aging. (e) UV−vis absorption spectra of the hydrogels with different PDA−PPy contents. (f) Photo of the hydrogels covering on the back skin of a rat, and schematic demonstration of the hydrogel used as a skin dressing for UV-shielding. (g) H&E staining showed that the naked skin and the skin tissue covered by the PAM hydrogel were damaged after UV irradiation, whereas the skin tissue protected by the PDA−PPy− PAM hydrogel remained intact.

transparent PDA−PPy−PAM hydrogel, as discussed in the following sections. The design of the hydrogel with multiple unique properties was based on two key points. One point was the production of the hydrophilic and conductive PDA−PPy NPs. By owing to its organic nature, PPy is hydrophobic and does not merge well with the hydrophilic polymer networks in a hydrogel.44−46 In the current study, we employed highly reactive and hydrophilic PDA to hybridize and dope PPy to produce PDA−PPy NPs. PDA showed high affinity for both hydrophobic PPy and hydrophilic monomers25 and therefore ensured the effective integration of PPy into the hydrophilic polymer phase in the hydrogel. The results of a water-contact-angle experiment showed that the PDA−PPy NPs were more hydrophilic than pure PPy NPs (Figure S4). We also performed a MD simulation to investigate the hydrophilicity of the PDA−PPy complex. To quantify the hydrophilicity of these two materials, we used the penetration depth of water in the PPy and PDA− PPy models to evaluate their hydrophilicity. The penetration

depth is defined as the distance between the point where water emerges in the complex to the point at which the complex extinguishes in water, as indicated by the arrow in the density profiles depicting the atomistic distributions of polymers and water (Figure 2e,f). The penetration depth of water in the PPy−PDA model was 46.8 Å, which was higher than that in the PPy model (30.0 Å). This can be explained by the existence of hydrophilic PDA in PDA−PPy NPs that improved the hydrophilicity of PPy making the polymer−water interaction more favorable, according to the previous study.39 The MD simulation results were consistent with results from the water-contact-angle experiment. The second key point of the hydrogel design was the surprising in situ generation of PDA−PPy nanofibrils from PDA−PPy NPs inside the hydrogel network with the presence of excessive APS. We hypothesized the following mechanism for the in situ formation of nanofibrils with the aid of APS under the templating effect of the polymer chains. First, the APS generated radicals that continuously broke down the 5565

DOI: 10.1021/acs.chemmater.8b01446 Chem. Mater. 2018, 30, 5561−5572

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Chemistry of Materials PDA−PPy NPs into nanodots through reduction of π−π stacking interactions between the oligomeric units in the PDA−PPy complex.47 Next, guided by the PAM chains as a template in the hydrogel, the PDA−PPy nanodots were selfassembled to form nanofibrils (Figure 1c). To prove that APS could induce the generation of PDA−PPy nanodots, we directly added APS to a suspension of PDA−PPy NPs, and the color of the suspension immediately changed from dark green to light pink and subsequently to pale yellow (Figure S6). SEM images and DLS analysis showed that these NPs degraded into nanodots after APS was added (Figure S7). No obvious shift was observed from the Fourier transform IR (FT-IR) spectrum of the PDA−PPy NPs before and after APS-induced degradation (Figure S8a), which demonstrated that only the morphology of the PDA−PPy complex was changed during this degradation process. Actually, this mechanism has also been demonstrated to create PDA nanodots from hydroxylradical-induced degradation of pure PDA NPs.47 The in situ evolution of PDA−PPy from nanoparticles to nanofibrils can be directly visualized in a series of SEM images under three different conditions, including the immediately polymerized pregel and hydrogels stored after 1 and 3 days (Figure S9b). Before incorporation into the hydrogel, the PDA−PPy NPs were spherical with the particle size of around 500 nm (Figure S7c). In the freshly formed pregel via APSinduced polymerization, the PDA−PPy NPs still can be observed in the matrix (Figure 1d). After aging with an extended period from 1 to 3 days, the NPs in the hydrogel gradually disappeared, and nanofibrils filled the area (Figure 1e). A high-magnification image showed that the hydrophilic PDA−PPy nanofibrils were well-dispersed and integrated with the hydrophilic polymer without phase separation (Figure S9b). For the PPy−PAM hydrogels, a similar structural change from particles to nanofibrils was also observed at a different aging time (Figure S9a). However, because of the hydrophobicity, the PPy nanofibrils separated from the matrix. It can thus be concluded that the PDA hybridization not only improved the hydrophilicity of PPy but also facilitated the interactions between the in-situ-formed PDA−PPy nanofibrils and the PAM chain to interweave a highly interconnected network in the hydrogel, leading to a combination of high transparency, good conductivity, and supermechanical properties of the PPy−PDA−PAM hydrogel. The in-situ-formed hydrophilic PDA−PPy nanofibrils endowed the hydrogel with remarkable multifunctions. First, compared with directly blended nanofillers in a hydrogel, the in-situ-formed nanofibrils were uniformly distributed and integrated with the hydrophilic polymer phase to form a highly interconnected conductive path in the hydrogel, which therefore led to high conductivity. Second, unlike lightabsorbing NPs, the PDA−PPy nanofibrils allowed visible light to pass through with negligible scattering.48 Third, the insitu-formed PDA−PPy nanofibrils integrated well with the polymer chains via various forms of noncovalent bonds to reduce the susceptibility to form cracks during the deformation of the hydrogels, which effectively improved the overall mechanical properties of the hydrogels. Thus, the in situ formation of PPy nanofibrils was critical for the hydrogel synthesis, which has not been demonstrated in previous reports on the CP-based hydrogels.49,50 Transparency and UV-Shielding Performance of the PDA−PPy−PAM Hydrogels. To understand the contribution of the PDA−PPy nanofibrils to transparency, we

investigated the transmittance of hydrogels in different stages, in accordance with the different formats of the PDA−PPy complex in the hydrogel (Figure S9b). As shown in Figure 3a, the freshly prepared pregel with PDA−PPy NPs was black. The hydrogel turned to pale yellow after 1 day and finally became transparent after 3 days, accompanied by a gradual in situ transition of the PDA−PPy NPs to nanofibrils in the hydrogel matrix (Figure S9b). Figure 3b shows the plots of the transmittance of light in the wavelength range 400−800 nm for the PDA−PPy−PAM hydrogel at different stages. The average transmittance per millimeter of thickness of the hydrogel at 660 nm wavelength increased from 10% for the pregel to 50% after 1 day and finally reached 70% after 3 days. It is welldocumented that PDA and PPy NPs are black because of their light absorptivity in a wide range of wavelengths,50−54 and therefore, the pregel with the embedded NPs was nontransparent. After the in situ formation of PDA−PPy nanofibrils, a highly transparent hydrogel was obtained, because the nanofibrils interwove to form a nanomesh, thus allowing light to pass through and resulting in a transparent hydrogel. In short, the enhancement in transparency was attributed to the in-situ-formed conductive nanofibrils that were well-dispersed in the hydrogel to form light-passible nanoscale networks, which is a big breakthrough in the development of CP-based conductive hydrogels. The optical transmittance of the PDA−PPy−PAM hydrogel was also dependent on the content of the PDA−PPy NPs. As shown in Figure 3c, the PDA−PPy−PAM hydrogel became opaque with an increasing content of PDA−PPy NPs. The UV−vis spectra indicated that the transmittance of the PDA− PPy−PAM hydrogel per millimeter of thickness measured at 660 nm wavelength decreased from 80% to 40% when the PDA−PPy content was increased from 0.3 to 1.8 wt % (Figure 3d). The percentage transmittances of hydrogels with different thicknesses are also plotted in Figure S10, and the results indicated that the transmittance decreased with an increase in thickness. Remarkably, the transparency drop of our hydrogel against thickness was significantly small in comparison. The PDA−PPy−PAM hydrogel still showed high optical transmittance even at a thickness of 3 mm, which surpassed the performance of previously reported conductive and transparent materials with directly blended CP nanofillers because they only allowed light to pass through when their thickness was on the nanometer or micrometer scale.16,18,55−57 Interestingly, the transparent hydrogel only transmitted visible light but cut off UV light owing to the ability of PDA− PPy to absorb UV light (Figure S11). As shown in Figure 3e, the UV absorbance of the hydrogel increased with increasing PDA−PPy content in the hydrogel. The PDA−PPy−PAM hydrogel with both high transparency and good UV-shielding performance has great potential to be used as sun-protective dressing, as demonstrated in an in vivo animal experiment. The PDA−PPy−PAM hydrogels were adhered on the back skin of a rat, and then, the rat was irradiated by a UV lamp (365 nm, 30 mW/cm2), as illustrated in Figure 3f, g. The PAM hydrogel was also tested as the control. After exposure to UV light for 20 min, the skin protected by the PDA−PPy−PAM hydrogel was intact and appeared similar to the normal skin as observed by the naked eye, whereas the naked skin and the skin covered by the PAM hydrogel immediately developed a white eschar (Figure S18). Histological analysis further indicated that the morphological appearance of the skin protected by the PDA− PPy−PAM hydrogel was well-preserved (Figure 3g). In 5566

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Figure 4. Conductivity and self-adhesiveness of the PDA−PPy−PAM hydrogel. (a) Photos illustrating the good conductivity of the hydrogel (0.6 wt %) under large deformation. (b) Hydrogel (0.6 wt %) exhibited stable conductivity under cyclic stretching with the y axis representing the resistance change ratio (ΔR/R0) under an applied strain. R0 and ΔR represent the initial resistance without deformation and the resistance change at the applied strain of 40%, respectively. (c) Structural change of the PDA−PPy complex from the NPs to nanofibrils led to the increase in conductivity. (d) Comparison of the conductivity of the PDA−PPy−PAM and PPy−PAM hydrogels, demonstrating that PDA doping greatly improved the conductivity. (e) Adhesion strength of the hydrogels with different compositions. (f) Adhesion strength after different storage periods. Error bars represent the standard deviation from the mean of five samples.

for the pregel to 12 S/m for the hydrogel after 3 days. The improvement in conductivity was accompanied by the structural change of NPs to nanofibrils in the hydrogel, as observed by SEM (Figure S9). Furthermore, the conductivity of the hydrogels was greatly improved by employing PDA hybridization and doping (Figure 4d). To demonstrate this, the conductivity of the PDA−PPy−PAM hydrogel was compared to that of the PPy−PAM hydrogel after 3 days of aging. When only PPy was incorporated, the conductivity of the PPy−PAM hydrogel was only 5 S/m. When the PDA−PPy NPs were incorporated into the hydrogel, the conductivity of the PDA−PPy−PAM hydrogels jumped sharply to the maximum value of 12 S/m with 0.6 wt % of PDA−PPy NPs, which was much higher than that of the PPy−PAM hydrogel with the same amount of PPy NPs. The high conductivity of the PDA−PPy−PAM hydrogel can be explained from two perspectives. First, the PDA hybridization promoted the integration of hydrophobic PPy with the PAM network, and the conductive PDA-doped PPy nanofibrils were thus welldispersed in the hydrogel matrix and became entangled with

contrast, the naked skin and the skin covered by the PAM hydrogel showed significant injury with ruptured collagen fibers and subcutaneously visible congestion (Figures 3g and S18). Together with the reasonable water uptake capacity (Figure S17), the PDA−PPy−PAM hydrogel can be potentially used as UV-shielding dressing. Electrical Conductivity of the PDA−PPy−PAM Hydrogels. The in situ formation of PDA−PPy nanofibrils resulted in high electrical conductivity of the hydrogel. Figure 4a shows typical photos of the PDA−PPy−PAM hydrogel that maintained high conductivity and transparency even when it was stretched, bent, or twisted to a large deformation. The conductivity was stable during cyclic stretching and compressing (Figures 4b and S12), which is a crucial requirement for flexible electronic devices.57 The conductivities of the hydrogel measured at different stages, including the freshly prepared pregel and the hydrogel after storage for 1 and 3 days, are shown in Figure 4c. The PDA−PPy−PAM hydrogel containing 0.6 wt % of the PDA−PPy NPs was taken as a representative sample. The conductivity increased from 7 S/m 5567

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Figure 5. Mechanical properties of the PDA−PPy−PAM hydrogels. (a) Stretchability and recoverability of the hydrogel containing 0.6 wt % PDA− PPy. (a-i) Photo of the hydrogel that was stretched to six times its initial length. (a-ii) Photo of the hydrogel that was compressed to one-fifth of its initial height and recovered in 5 s after removal of the load. (b) Typical tensile stress−strain curves of various hydrogels. (c−e) Extension ratio, tensile strength, and fracture energy of the hydrogels containing different contents of PDA−PPy. (f) Representative cyclic loading−unloading curves of the PDA−PPy−PAM hydrogel (0.6 wt % PDA−PPy) for up to three cycles. (g) Structural change of the PDA−PPy complex from NPs to nanofibrils increasing the fracture energy of the PDA−PPy−PAM hydrogel (0.6 wt % PDA−PPy). The error bars represent the standard deviation from the mean of five samples.

enhancement on the mechanical properties of the PDA−PPy− PAM hydrogel. As shown in Figure 5a, the hydrogel was highly stretchable and fully recoverable. It could be stretched to six times its original length. It could also be compressed and recovered immediately. As shown in Movies S1 and S2, the hydrogel was able to recover to its original length in 1 s after being stretched to six times its initial length. After compressed to 80% of its original height, the hydrogel was able to recover to its original height in 5 s. The mechanical properties of the hydrogels were strongly affected by the weight ratio of the PDA−PPy NPs. All the hydrogels with different compositions showed good stretchability, as demonstrated by the tensile tests (Figure 5b). The tensile strength and extension ratio of the hydrogels increased with the PDA−PPy content, and the hydrogel containing 1.8 wt % of PDA−PPy showed the highest stretchability, with strains exceeding 2000% and a tensile strength of 130 kPa (Figure 5c, d). The fracture energy had a maximum value of 3000 J/m2 (Figure 5e) when the hydrogel contained 1.8 wt % of PDA−PPy. However, the compressive strength of the hydrogels decreased with increasing PDA−PPy content (Figure S13), which might be attributed to the increased amount of the PDA component. As demonstrated in our previous study,35 PDA addition resulted in the increase in viscosity of the hydrogels, as demonstrated by dynamic rheological tests, in which the loss tangent increased with increasing DA content. Cyclic compression tests demonstrated

the PAM chains. Second, the nanofibrils became interwoven to form a nanomesh in the hydrogel matrix, which provided a more complete conductive path than that offered by the separated and nonconnected NPs. Self-Adhesiveness of the PDA−PPy−PAM Hydrogels. In addition to enhancing conductivity, a distinctive and advantageous feature of utilizing PDA to hybridize PPy was that PDA imparted the PDA−PPy−PAM hydrogel with high self-adhesiveness through a mechanism similar to that employed by mussels to adhere to substrates.58−63 The adhesive strength of the hydrogels was quantified by using porcine skin to represent tissue surfaces during a tensileadhesion test. The results demonstrated that the adhesive strength of the PDA−PPy−PAM hydrogel reached the maximum value of 30 kPa (Figure 4e). The structural change of the PDA−PPy NPs did not affect the adhesiveness of the hydrogel (Figure 4f). In particular, our PDA−PPy−PAM hydrogels did not require any external agents and preloadings to enhance the state of adhesion, in contrast to previous adhesive hydrogels. The high tissue adhesiveness enabled the hydrogel to be applied as a part of epidermal electronics, or implantable sensors, which require intimate contact between the devices and the curved biological surfaces without hurting substrates or skins and incurring pain.2,64,65 Supermechanical Properties of the PDA−PPy−PAM Hydrogels. The in-situ-formed PDA−PPy nanofibrils showed 5568

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Figure 6. Conductive, adhesive, stretchable, and biocompatible hydrogels used as wearable devices. PDA−PPy content in the hydrogel was 0.6 wt %. (a) Hydrogel was adhered on an author’s (1) wrist and (2) knee joint, serving as strain sensors to detect the motion of the human body. (b) Hydrogel acted as the self-adhesive electrode to detect signals for the (1) EMG and (2) ECG. Transparent hydrogel allowed operators to see the vein underneath the electrode (inset in b-1). (c) CLSM images of BMSCs adhered on the pure PAM and PDA−PPy−PAM hydrogels after 3 days of culture. Scale bar: 500 μm. (d) Quantification of the total cell number after 3 and 7 days of culture. The error bars represent the standard deviation from the mean of five samples.

Transparent, Conductive, and Adhesive Hydrogels as Sensors and Bioelectrodes. To demonstrate the practical applications of the conductive PDA−PPy−PAM hydrogel with the integration of high tissue adhesiveness, optical transparency, and good mechanical properties, we fabricated hydrogel-based sensors for see-through human body signal detection. These self-adhesive electrodes can be easily adhered onto various stretchable substrates or curved surfaces, especially those on the human body, giving sensor functions. For demonstration, the hydrogels (0.6 wt % of PDA−PPy NPs) were used as strain sensors and directly adhered to the skin without extra aids to detect the bending and stretching of the human body, such as movements at the wrist and knee joint (Figure 6a). The hydrogels were stably attached to the body, and they repeatedly detected movements even they went through large deformations. The corresponding time-dependent responses (measured as the relative change in the resistance, ΔR/R0) of the hydrogels during body movement were recorded. The highest value of ΔR/R0 from the sensor on the wrist was 90%, while that from the sensor on the knee joint was 80% (Figure 6a). Moreover, the PDA−PPy−PAM hydrogel was also used as a self-adhesive electrode to detect biosignals, such as electrocardiograph (ECG) and magnetocardiography (EMG) signals, to obtain information about the

that the hydrogel had stable and recoverable mechanical properties under large deformation (80% strain) (Figure 5f). Remarkably, the in-situ-formed PDA−PPy nanofibrils had a major impact on the stretchability and toughness of the hydrogel (Figures 5g and S14). This phenomenon can be explained by the reinforcement provided by the nanofibrils, which led to the uniform stress distribution and load sharing in the hydrogel during deformation. The PPy−PAM hydrogels with different PPy contents were also tested as controls. As shown in Figure S15, the extension ratio and fracture energy of the PPy−PAM hydrogels were much lower than those of the PDA−PPy−PAM hydrogels. Comparison of the results of the PDA−PPy−PAM and PPy−PAM hydrogels demonstrated that the incorporation of PPy NPs alone did not effectively impart the hydrogels with good mechanical properties and PDA−PPy incorporation was necessary to form tough and resilient hydrogels. In short, by owing to the PDA complexion of PPy, the elaborately designed conductive and transparent PDA− PPy−PAM hydrogels exhibited mechanical behavior of softness, stretchability, and elasticity, which make them comparable to the natural soft collagenous tissues such as cartilage and skin, with the tensile strength around 0.1−10 MPa, the failure strain in the range 40−70%, and the fracture toughness in the range 1−10 kJ/m2.66−69 5569

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composite hydrogels and it overcomes the intrinsic shortcomings of CPs, such as hydrophobicity and brittleness. Ultimately, we hope to extend this in situ strategy to develop new CP-based hydrogels and consequently broaden the applications of CP-based hydrogels in the future such as transparent electronic skin, bionic robots, and wearable or implantable smart devices.

health of the patient (Figure 6b). The signals obtained by the hydrogel electrode were as accurate as those obtained by commercial electrodes (Figure S16). By owing to its adhesiveness and transparency, this conductive hydrogel was superior to its opaque counterparts because the high transparency allowed medical personnel to observe the tissue response under the hydrogel during detection. As shown in the inset in Figure 6b, the vein under the hydrogel was clearly observed. In addition, the hydrogel was biocompatible and nonirritating when adhered to human skin, and the strong tissue adhesiveness of the hydrogel electrodes would avoid the use of extra bandages during operation. More importantly, the PDA−PPy−PAM hydrogels showed excellent biocompatibility and cell affinity as confirmed by the culturing of BMSCs on the surfaces of the as-prepared hydrogels. After 3 days of incubation, the number of cells on the PDA−PPy−PAM hydrogels was higher than that of cells on the PAM hydrogels (Figure 6c). The cell proliferation was further quantified by MTT, which followed the same trend (Figure 6d). The good biocompatibility of the hydrogel was attributed to the high cell affinity of catechol groups in PDA.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.chemmater.8b01446. Experimental details for preparation of the hydrogels; compositions of various hydrogels; details of mechanical tests of hydrogels; details of electrical conductivity measurement of the hydrogels; details of adhesive tests of hydrogels; FT-IR spectra of the pure PPy and PDA− PPy NPs; water contact angle of the PPy- and PDA− PPy-coated films; mass spectrometry analysis; details for MD simulations; SEM images and DLS results of the PDA−PPy complex; SEM morphology of the PDA− PPy−PAM and PPy−PAM hydrogels; compressive behaviors of the PDA−PPy−PAM hydrogels; transmittance spectra of the PDA−PPy−PAM hydrogel with different thickness; relative resistance change of the hydrogel under compression; UV−vis spectra of the PDA−PPy NPs; mechanical properties of the PPy− PAM hydrogels; summarized properties of the PDA− PPy−PAM hydrogels with various properties; water uptake capacity of the hydrogels; details of in vitro cell culture and in vivo experiments (PDF) Movie S1: the recoverability of the hydrogel after stretching (AVI) Movie S2: the recoverability of the hydrogel after compression (AVI)

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CONCLUSIONS The current study developed a new family of conductive hydrogels with integration of optical transparency and conductivity as well as good mechanical properties, adhesive properties, and biocompatibility. In addition, the hydrogel has UV-shielding ability, which enables it to be used as an UVprotective dressing. Finally, the hydrogel with biocompatible and self-adhesive properties can directly adhere to flexible and dynamic biological surfaces for see-through body signal detection, which is an indispensable property for applying transparent and conductive hydrogels at the electrical− biological interface. Thus, the PDA−PPy−PAM hydrogels can provide promising versatile applications, such as those in soft bioelectrodes and optoelectronic devices. Moreover, we would like to stress that the strategy of conductive hydrogel formation in the current study is conceptually different from that adopted in our previous work. In our previous work, the conductivity of the hydrogels was attributed to the incorporation of PDA-reduced graphene oxide or PDA-decorated carbon nanotubes into the polymer network, while the current PDA−PPy−PAM hydrogel was obtained by in situ formation of CP nanofibrils inside the elastic PAM matrix. The in-situ-formed nanofibrils with good hydrophilicity are the key factor for determining the superproperties of the PDA−PPy−PAM hydrogel. These in-situformed nanofibrils created a complete conductive path and endowed the hydrogel with high conductivity. In particular, the nanofibrils interwove to form a nanomesh that allowed light to pass through, thus making the hydrogel optically transparent. Thus, this hydrogel has balanced transparence and conductivity, which cannot be offered by nontransparent conductive nanofiller-incorporated hydrogels prepared in our previous studies. To the authors’ knowledge, this is the first report on in situ formation of nanofillers of hydrophobic CPs in a hydrophilic matrix, which opens a new route to incorporate hydrophobic and undissolvable CPs into hydrogels. Compared with previous simple blending and mixing, this strategy of in situ forming conductive nanofillers is more attractive because it effectively avoiding the aggregation of nanofillers that is frequently encountered during processing of the nano-

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AUTHOR INFORMATION

Corresponding Author

*Phone: +86-28-87634023; fax: +86-28-87601371; e-mail: [email protected]. ORCID

Xiong Lu: 0000-0001-6367-430X Author Contributions ⊥

Authors L.H. and L.W.Y. contributed equally to this work.

Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was financially supported by the National Key Research and Development Program of China (2016YFB0700800), NSFC (81671824), Fundamental Research Funds for the Central Universities (2682016CX075, 2682018QY02), and the China Postdoctoral Science Foundation (2017M622997). The authors wish to acknowledge the Analytical & Testing Center of the Southwest Jiaotong University for assistance with characterization of the materials. 5570

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