Transparent, Adhesive, and Conductive Hydrogel for Soft

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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 Chem. Mater., Just Accepted Manuscript • DOI: 10.1021/acs.chemmater.8b01446 • Publication Date (Web): 23 Jul 2018 Downloaded from http://pubs.acs.org on July 25, 2018

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Chemistry of Materials

Transparent, adhesive and conductive hydrogel for soft bioelectronics based on light transmitting polydopamine-doped polypyrrole nanofibrils Lu Han1#, Liwei Yan1#, Menghao Wang1, Kefeng Wang2, Liming Fang3, Jie Zhou1, Ju Fang4, Fuzeng Ren4, Xiong Lu1* 1

Key Lab of Advanced Technologies of Materials, Ministry of Education, School of Materials Science and Engineering, Southwest Jiaotong University, Chengdu 610031, Sichuan, China 2

National Engineering Research Center for Biomaterials, Genome Research Center for Biomaterials, Sichuan University, Chengdu 610064, Sichuan, China 3

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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, Guangdong 518055, China #

The two authors contributed equally.

* Corresponding Author Tel.: +86-28-87634023 Fax: +86-28-87601371 Email address: [email protected]

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Chemistry of Materials 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Abstract. Conductive hydrogels are promising materials for soft electronic devices. To satisfy the diverse requirement of bioelectronic devices, especially those for human-machine interfaces, the hydrogels are required to be transparent, conductive, highly stretchable, and skin-adhesive. However, fabrication of a conductive-polymer-incorporated hydrogel with high-performance is a challenge because of the hydrophobic nature of conductive polymers making difficulties in processability. Here, we report a transparent, conductive, stretchable, and self-adhesive hydrogel by in situ formation of polydopamine-doped polypyrrole nanofibrils inner 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. The 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 promising in a range of applications, such as transparent electronic skins, wound dressings, and bioelectrodes for seeing-through body-adhered signal detection.

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INTRODUCTION 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 reported conductive hydrogels are opaque because they contain high concentrations of non-transparent conductive nanofillers, such as metal (Au, Ag, Ni) based nanowires or nanoparticles7-9 and carbon-based nanomaterials.2 Another route for realizing transparent and conductive hydrogel is to produce ionogels comprising of 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, there continues to be a need for intrinsically conductive hydrogels with good stability and high transparency.

Conductive

polymers

(CPs),

such

as

polypyrrole,

polyaniline,

and

poly(3,4-ethylenedioxythiophene), have good electrical characteristics and softer mechanical properties than metals for flexible electronic devices, and are also potential candidate fillers in fabrication of transparent conductive hydrogels.15-18 However, CP-based bulk hydrogels are generally opaque, such as pure polypyrrole and polyaniline based hydrogels by directly 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 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

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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 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 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 4


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promote cell adhesion, proliferation, and differentiation.31,

32

Thus, PDA can improve the

biocompatibility of CP on the cellular level.

Recently, mussel-inspired hydrogels were developed by introducing catechol groups to the polymer networks.25, 33 These hydrogels showed great potential for use in various biomedical applications, including tissue adhesives, drug-delivery systems, and cell culture platforms by utilizing different DOPA chemistries.33 Based on 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 non-transparent carbon nanomaterials inside the hydrogel network, and the hydrogels cannot satisfy the requirement the 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. Owing to the light transmittability of the nanomesh with interwoven nanofibrils, the hydrogel exhibited high transmittance of 70% across the visible spectrum even it was thicker than 1 mm. In addition to transparency in 5



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 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 non-adhesive, 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.

EXPERIMENTAL SECTION Materials: Dopamine (DA), pyrrole (Py), ammonium persulfate (APS), N, N’-Methylene bisacrylamide (BIS), tetramethylethylenediamine (TMEDA), and polyvinyl alcohol (PVA, MW=2000 Da) were purchased from Sigma-Aldrich (USA). Acrylamide (AM), sodium hydroxide (NaOH) and ferric chloride (FeCl3·6H2O) were purchased from Kelong, Chengdu. All chemicals were reagent grade.

Synthesis of PDA-PPy nanoparticles. The polydopamine-polypyrrole nanoparticles (PDA-PPy NPs) were synthesized by a modified aqueous dispersion polymerization method. First, Polyvinyl alcohol (PVA, 1.5 g) were first dissolved into the deionized water (20 ml) at 90 °C under magnetically 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, pyrrole (Py) monomer (2 mmol, 140 µl) and dopamine (DA) monomer (0.05 g) were added into the above solution, and the mixed 6


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solution was continually stirred in ice-water bath for 9 hours to allow Py and DA monomers complete polymerization, with the color of resulted solution changing to fully black. Fourth, the resulted solution was then went through three cycles of centrifugation and washing with hot water to remove impurities. Finally, the PDA-PPy NPs was obtained and was stored in refrigerator at 4 °C for further use. Pure PPy nanoparticles (PPy NPs) without DA addition were also prepared using the same procedure.

Preparation of PDA-PPy-PAM hydrogel. In a typical hydrogel synthesis process, PDA-PPy NPs (15.6 mg) were well dispersed in the deionized water (8 ml) under magnetic stirring. Then 2.6 g of acrylamide (AM) monomers were dissolved in the PDA-PPy dispersion, forming homogeneous dark dispersion. Subsequently, ammonium persulphate (APS), N, N-methylenebisacrylamide (BIS) and tetramethylethylenediamine (TMEDA) were added in the above mixture under stirring. After 5 min stirring, the stirrer was removed and the AM monomers were polymerized to form a pre-gel. The pre-gel was sealed and stored under ambient environment for 3 days of aging until the transparent PDA-PPy-PAM hydrogel was obtained. For comparison, the PDA-PPy-PAM hydrogels with different contents of PDA-PPy NPs were prepared, and the 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 PDA-PPy NPs was confirmed by molecular dynamic simulation. The morphologies of NPs were investigated by using a scanning electron microscopy (JSM 6390, JEOL, Japan). The mean particle size and 7



polydispersity index of the NPs were determined by dynamic light scattering with a laser particle analyzer (ZETA-AIZER, Malvern, UK). For detailed methods, please refer to SI Materials and Methods.

Molecular dynamic simulation on the hydrophilicity of PDA-PPy complex. The trimer dopamine (PDA) was built according to previous reported possible structure of polydopamine, as shown in Figure S5a.38 The model of PPy system (Figure S5c) contained 720 of PPy chains, and each PPy chain comprised 10 of Py monomers (Figure S5b). PDA-PPy complex contained 720 of PPy chains and 260 of PDA trimer (Figure S5d). The size of the cluster was 60 × 52 × 98 Å3 and the density of cluster for PPy and PDA-PPy complex was set to 1.47 g/cm3 according to previous investigations.39 Charmm GENeral Force Field (CGENFF) parameters for pyrrole were assigned to PPy.40 The force field for PDA was calculated by Force Field Toolkit (FFTk) developed by Mayne et al41 based on first principle calculation. All the parameters were adopted into CHARMM force field for the system simulation. The molecular dynamics (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 for van der Waals interactions and electrostatic interactions in real space. Particle-Mesh-Ewald summation (PME) was employed to describe long range electrostatics. SHAKE algorithm was enabled and a time step of 1 fs was set to the system. The details are provided in the Supporting Information.

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Characterization of PDA-PPy-PAM hydrogel. The microstructures of the hydrogels were examined using the SEM (JSM 6390). The transmission spectra of the hydrogel were measured on a UV-visible spectrometer (TU-1901, Puxi, China) equipped with a deuterium lamp 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-visible spectrometer (TU-1901) 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 5 individual samples. For detailed methods, please refer to Figure S1 and Equation 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 hydrogels, were tested. The content of PDA-PPy complex and PPy nanoparticles in the hydrogel was 0.6 wt.%, as listed in Table S1. Before experiments, the hydrogels were firstly 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 9



marrow stem cells (BMSCs) were used for cytotoxicity test. BMSC 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 PAM hydrogel were used. Before cell culture, the hydrogels were purified by immersing them in sterilized PBS and swelled to the equilibrium state for 2 days in a CO2 incubator at 37 ºC. BMSC (passage 4) were seeded on the hydrogels with a density of 5×104 cells/hydrogel. After 3, 7 days of culture, a 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay was used to evaluate the proliferation of BMSC. The morphology of cells grown on hydrogels was observed by confocal laser scanning microscope (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 animal experiment. Before testing, the dorsal skin surface was shaved and cleaned prior to experiment. Then the back skin was irradiated by UV light (30 mW/cm2, 365 nm) for 20 min with different treatments: (1) covered by 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 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 10


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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 was prepared in a simple two-step process, as schematically shown in Figure 1. First, hydrophilic PDA doped PPy nanoparticles (PDA-PPy NPs) was synthesized by Fe3+-induced aqueous dispersion copolymerization of dopamine and pyrrole monomers through non-covalent 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 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 dopamine, as well as convert 5,6-dihydrox-yindole into the corresponding quinone via hydrogen abstraction.25 Thus, during the formation of the PDA-PPy complex, DA oligomers with low molecular weight were formed, as analyzed by mass spectroscopy (Figure S3). There were still un-oxidized catechol groups in the PDA-PPy complex, which were essential to the adhesiveness of the hydrogel.35 In the second step, acrylamide (AM) monomers were mixed in the dispersion of the PDA-PPy NPs, and then polymerized into a pre-gel with the presence of ammonium persulfate (APS) as initiator via free-radical polymerization. After gelation, the pre-gel was stored in an ambient environment for 3 days of aging to allow the in situ formation of PDA-PPy nanofibrils from PDA-PPy 11



NPs, which was critical for the fabrication of a conductive and transparent PDA-PPy–PAM hydrogel, as discussed in the following sections.

The design of hydrogel with multiple unique properties was based on two key points. One point was the production of the hydrophilic and conductive PDA-PPy NPs. 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 monomers,25 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 molecular dynamics simulation to investigate the hydrophilicity of the PDA-PPy complex. To quantify the hydrophilicity of these two materials, we used penetration depth of water in PPy and PDA-PPy models to evaluate the 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, which improved the hydrophilicity of PPy, making the polymer-water interaction is more favorable, according to the previous study.39 The MD simulation results were consistent with results 12


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from 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 polymer chains. First, the APS generated radicals that continuously broke down the PDA-PPy NPs into nanodots through reduction of π-π stacking interaction between the oligomeric units in PDA-PPy complex.47 Next, guided by the PAM chains as template in the hydrogel, the PDA-PPy nanodots were self-assembled 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 Fourier transform infrared (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 hydroxyl radical-induced degradation of pure PDA-NPs.47

The in situ evolution of the PDA-PPy from nanoparticles to nanofibrils can be directly visualized in a series of SEM images under three different conditions, including immediately 13



polymerized pre-gel, hydrogels stored after 1 and 3 days (Figure S9b). Before incorporated into hydrogel, the PDA-PPy NPs were spherical with the particle size of around 500 nm (Figure S7c). In the freshly formed pre-gel via APS induced 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). 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, similar structural change from particles to nanofibrils was also observed at different aging time (Figure S9a). However, due to 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 PAM chain to interweave a highly interconnected network in the hydrogel, leading to a combination of high transparency, good conductivity, and super mechanical 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 light-absorbing nanoparticles, the PDA-PPy nanofibrils allowed visible light to pass through with negligible scattering.48 Third, the in-situ formed PDA-PPy nanofibrils integrated well with the polymer chains via various forms of 14


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non-covalent bonds to reduce the susceptibility to crack formation 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 PDA-PPy complex in the hydrogel (Figure S9b). As shown in Figure 3a, the freshly prepared pre-gel 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 of 400-800 nm for the PDA-PPy-PAM hydrogel at different stages. The average transmittance per mm thickness of the hydrogel with at wavelength of 660 nm increased from 10% for the pre-gel to 50% after 1 day, and finally reached 70% after 3 days. It is well documented that PDA and PPy nanoparticles are black because of their light absorbability in a wide range of wavelengths,50-54 and therefore the pre-gel with embedded nanoparticles was non-transparent. 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 15



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 PDA-PPy NPs. As shown in Figure 3c, the PDA-PPy–PAM hydrogel became opaque with increasing content of PDA-PPy NPs. The UV-visible (UV-vis) spectra indicated that the transmittance of the PDA-PPy–PAM hydrogel per mm thickness measured at a wavelength of 660 nm decreased from 80% to 40% when the PDA-PPy content was increased from 0.3 to 1.8 wt.% (Figure 3d). The percentage transmittance of hydrogels with different thickness is also plotted in Figure S10, and the results indicated that the transmittance decreased with 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 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 16


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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 skin covered by 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 contrast, the naked skin and PAM hydrogel covered skin 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 be 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 twist 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 conductivity of the hydrogel measured at different stages, including the freshly prepared pre-gel, the hydrogel after stored 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 17



conductivity increased from 7 S/m for the pre-gel to 12 S/m for the hydrogel after 3 days. The improvement in conductivity was accompanied by the structural change of nanoparticles 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 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 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 well dispersed in the hydrogel matrix and became entangled with 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 non-connected nanoparticles.

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 18


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tensile-adhesion 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 the intimate contact between the devices and the curved biological surfaces without hurting substrates or skins and incurring pains.2, 64, 65

Super mechanical properties of the PDA-PPy-PAM hydrogels. The in situ formed PDA-PPy nanofibrils showed 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 to 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 second after stretched to six times of its initial length. After compressed to 80% of its original height, hydrogel was able to recover to its original height in 5 seconds. The mechanical properties of the hydrogels were strongly affected by the weight ratio of the PDA-PPy NPs. All 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 PDA-PPy content, and the hydrogel containing 1.8 wt.% of PDA-PPy showed the highest stretchability, with strains exceeding 2000% and tensile strength of 130 KPa (Figure 5c,d). The fracture energy had a maximum 19



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 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 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 (Figure 5g, 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 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, 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 be comparable to the natural soft collagenous tissues such as cartilage and skin, with tensile strength around 0.1-10 MPa, the failure strain in the range of 40-70%, and the fracture toughness in the range of 1-10 kJ/m2.66-69 20


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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 a hydrogel-based sensors for seeing-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 hydrogel (0.6 wt.% of PDA-PPy NPs) was 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 the movements even they went through large deformations. The corresponding time-dependent responses (measured as the relative change in the resistance, ∆R/R0) of the hydrogels during body movement were recorded. The highest value of ∆R/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 health of the patient (Figure 6b). The signals obtained by the hydrogel electrode were as accurate as those obtained by commercial electrodes (Figure S16). 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 21



was clearly observed. In addition, the hydrogel was biocompatible and non-irritating 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 bone marrow stem cells (BMSCs) on the surfaces of the as-prepared hydrogels. After 3 days of incubation, the numbers of cells on the PDA-PPy–PAM hydrogels were 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 the PDA.

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 UV-protective 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.

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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 works. In our previous works, the conductivity of hydrogels was attributed to the incorporation of the 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 conductive-polymer nanofibrils inside the elastic polyacrylamide matrix. The in situ formed nanofibrils with good hydrophilicity is the key factor for determining the super properties of the PDA-PPy-PAM hydrogel. These in situ formed nanofibrils created 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 have balanced transparence and conductivity, which cannot be offered by non-transparent conductive nanofillers-incorporated hydrogels prepared in our previous studies.

To authors’ knowledge, this is the first report on in situ formation of nanofillers of hydrophobic conductive polymers in hydrophilic matrix, which opens a new route to incorporate hydrophobic and undissolvable conductive polymers into hydrogels. Compared with previous simple blending and mixing, this strategy of in situ forming conductive nanofillers is more attractive because of effectively avoiding the aggregation of nanofillers that is frequently encountered during processing of the nanocomposite hydrogels, and overcomes the intrinsic shortcomings of conductive polymers, such as hydrophobicity and brittleness. Ultimately, we hope to extend this in situ strategy to develop new conductive 23



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polymer-based hydrogels, and consequently broadens the applications of conductive polymer-based hydrogels in future like transparent electronic skin, bionic robots, and wearable or implantable smart devices.

ASSOCIATED CONTENTS Supporting Information: 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; FTIR spectra of pure PPy and PDA-PPy NPs; water contact angle of PPy and PDA-PPy coated film; SEM images and DLS results of PDA-PPy complex; SEM morphology of PDA-PPy-PAM and PPy-PAM hydrogels; compressive

behaviors

of

PDA-PPy-PAM

hydrogels;

transmittance

spectra

of

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 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. Movie S1. The recoverability of the hydrogel after stretched. Movie S2. The recoverability of the hydrogel after compressed.

AUTHOR INFORMATION Corresponding Author 24


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*Tel.: +86-28-87634023. Fax: +86-28-87601371. E-mail: [email protected]. Author Contributions L.H. and L. W. Y. contributed equally to this work. Notes There are no conflicts of interest to declare.

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 China Postdoctoral Science Foundation (2017M622997). The authors wish to acknowledge the assistance on materials characterization received from Analytical & Testing Center of the Southwest Jiaotong University.

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Figure 1. Transparent, conductive, stretchable, and adhesive hydrogel by in situ formation of polydopaminedoped polypyrrole (PDA-PPy) nanofibrils. (a-i) The formation of hydrophilic PDA-PPy nanoparticles. (a-ii) PDA-PPy NPs with highly hydrophilic properties. (b) An opaque pre-gel was formed after acrylamide (AM) monomers polymerized in the suspension of PDA-PPy NPs. 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 PAM chains. (d) SEM image of PDA-PPy NPs embedded opaque pre-gel, which absorbed light. (e) SEM image of nanofibrils in the transparent hydrogel, which allowed visible light to pass through while blocking UV irradiation. (f) A representative photo of the transparent hydrogel covering on a leaf. (g) The hydrogel was stretchable and conductive. 175x171mm (300 x 300 DPI)



Figure 2. Molecular dynamic simulation on the hydrophilicity of PDA-PPy complex. (a-b) Snapshot of the PPy system, which contained 720 of PPy chains and 3921 water molecules. (a) Initial configuration, (b) final configuration. (c-d) Snapshot of the PDA-PPy system, which contained 720 of PPy chains, 260 of 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. The blue curve represented all the atomistic distributions of the system. The red curve represented the atomistic distributions of O atoms in water. (e) PPy system and (f) PDA-PPy system. 154x148mm (300 x 300 DPI)


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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 freshly prepared pre-gel 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 skin dressing for UV-shielding. (g) H&E staining showed that the naked skin and skin tissue covered by PAM hydrogel was damaged after UV irradiation, whereas the skin tissue protected by the PDA-PPy-PAM hydrogel remained intact. 196x214mm (300 x 300 DPI)



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) The hydrogel (0.6 wt.%) exhibited stable conductivity under cyclic stretching. The y axis represents resistance change ratio (∆R/R0) under an applied strain. R0 and ∆R represent the initial resistance without deformation and the resistance change at the applied strain of 40%, respectively. (c) The structural change of the PDA-PPy complex from the nanoparticles to nanofibrils led to the increase in conductivity. (d) Comparison of the conductivity of PDAPPy-PAM hydrogel and PPy-PAM hydrogel, demonstrating that PDA doping greatly improved the conductivity. (e) Adhesion strength of the hydrogels with different compositions. (f) Adhesion strength after different storage periods. The error bars represent the standard deviation from the mean of five samples. 168x179mm (300 x 300 DPI)


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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. (i) Photo of the hydrogel that was stretched to 6 times of its initial length. (ii) Photo of the hydrogel that was compressed to 1/5 of its initial height and recovered in 5 seconds 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 PDA-PPy-PAM hydrogel (0.6 wt.% PDA-PPy) for up to three cycles. (g) Structural change of the PDA-PPy complex from the nanoparticles 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. 161x145mm (300 x 300 DPI)



Figure 6. Conductive, adhesive, stretchable and biocompatible hydrogels used as wearable devices. The content of PDA-PPy in the hydrogel was 0.6 wt.%. (a) The hydrogel was adhered on an author’s wrist (1) and knee joint (2), serving as strain sensors to detect the motion of the human body. (b) The hydrogel acted as the self-adhesive electrode to detect signals for the electromyographic (EMG) (1) and electrocardiogram (ECG) (2). The transparent hydrogel allowed operators to see vein underneath the electrode (inset in b1). (c) CLSM images of bone marrow stem cells (BMSCs) adhered on pure PAM and PDAPPy-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. 172x164mm (300 x 300 DPI)


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Transparent, Adhesive, and Conductive Hydrogel for Soft

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