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Novel electronic-ionic hybrid conductive composites for multifunctional flexible bioelectrode based on in situ synthesis of polydopamine on bacterial cellulose Yajie Xie, Yudong Zheng, Jinsheng Fan, Yansen Wang, Lina Yue, and Nannan Zhang ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.8b05345 • Publication Date (Web): 13 Jun 2018 Downloaded from http://pubs.acs.org on June 14, 2018

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ACS Applied Materials & Interfaces

Novel electronic-ionic hybrid conductive composites for multifunctional flexible bioelectrode based on in situ synthesis of polydopamine on bacterial cellulose Yajie Xie†, Yudong Zheng

†

†

, Jinsheng Fan†, Yansen Wang†, Lina Yue‡, Nannan Zhang§

School of Materials Science and Engineering, University of Science and Technology Beijing,

Beijing 100083, PR China ‡

School of Environmental Engineering, North China Institute of Science and Technology,

Yanjiao Beijing 101601, PR China §

Shenzhen Institues of Adavanced Technology, Chinese Academy of Science, Shenzhen 518055,

PR China KEYWORDS: Poly(dopamine), bacterial cellulose, hybrid conductive property, flexible biological electrode, in-situ composite

ABSTRACT: With the rapid development of the wearable detector and medical devices, flexible bio-sensing materials have received more and more attention. In this work, a novel flexible and conductive biocompatible composite with electronic and ionic bio-conductive ability

ACS Paragon Plus Environment

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was demonstrated to fabricate a new flexible bioelectrode used for the electrophysiological signal detection. This composite was prepared by the in situ self-polymerization of dopamine on the nanofiber of bacterial cellulose(BC) under the neutral pH condition. By using this method, polydopamine(PDA) could form a uniform and continuous wrapped-layer on the BC nanofiber that can prevent the aggregation of PDA caused by rapid polymerization under the conventional alkaline condition. And the fabricated film with this special structure is suitable for the transportation of electron and ionic existed in it. Moreover, the flexible conductive film(FCF) reveals an extremely tensile strength which is two times higher than the pure BC in addition to a high electric conductivity which reaches a value of 10-3 S/cm with a high PDA content. Furthermore, the result of electrocardio signal(ECG) testing shows that the antibacterial property of the FCF bioelectrode has an excellent stability, which is comparable to or better than the commercial available electrode. The BC/PDA flexible conductive film(BC/PDA-FCF) provides a platform for the creation of flexible conductive biomaterials for wearable response devices.

1. INTRODUCTION Recently, the FCF has exhibited significant potentials for a wide range of applications such as bio-sensing technique, artificial electronic skins, implantation instruments, wearable medical devices and novel biomedical materials. Soft and flexible conductors are important materials for bioelectronics that are particularly true to a broad range of biomedical applications. Among them, conductive polymer is a kind of polymer materials that has electrical conductivity. And the biomedical conductive polymer which include polyaniline(PANI)1, 2, polypyrrole(PPy)3 and polythiophene(PTh) that have intrinsic electronic conductivities have attracted great interest


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since they have been discovered. However, the unsatisfactory workability of these polymer materials limited their applications in the fields of biomedical materials where suitable mechanical property is required. In order to solve this problem, a lot of researchers have focused on the study of conductive polymer composites together with other sort of materials in the last decade, such as membrane materials4, electrolyte materials5 and fiber materials6. Of all the materials employed to produce conductive polymer composites, bacterial cellulose(BC) has become one of the natural polymer that could be used as the matrix to fabricate the composites due to its developed three-dimensional network structure and abundant chemical reactive groups made possible mainly by the function of hydroxyl. Up to now, BC has been used to prepare biological conductive polymer films, such as BC/PANI gel composite membrane1 and BC/PPy composite materials7. Although the application of BC could solve the problem associated with workability partly, some problems still exist. Firstly, during the fabrication process the mechanical properties of the composite materials would reduce sharply especially in the physical and chemical compound process. Secondly, some of the conducting polymers are not suitable for the biomedical application due to the cytotoxicity of these polymers. So the biocompatibility of the composite materials still needs to be improved. Since the discovery of electrical properties of eumelanin in the 1970s, melanin has been widely suggested to be a naturally organic semiconductor.8 The electrical conductivity of eumelanin was observed to be strongly influenced by the temperature, physical forms, and the humidity of the measurement conditions.9 The practical usage of eumelanin is a condition of many aspects. As a major pigment of naturally occurring melanin, Poly(dopamine)(PDA) displays many striking properties of naturally occurring melanin in electricity, optics and magnetism and, most importantly, it processes excellent biocompatibility10. Another valuable


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feature of PDA lies in its chemical structure that incorporates many functional groups such as catechol, amine and imine. These functional groups can serve as the starting points for covalent modification with molecules. With these benefits, PDA has been used as a coating material and rapidly incorporated into a wide range of applications across the chemical, biological, and materials sciences, as well as in applied science engineering, and the technology fields10. Recently, the research on PDA mainly focused on the adhesion performance11,

12, 13

,

reducibility14, 15, 16, and biocompatibility17, 18, 19. To be specific, the PDA is usually used to the material adhesion layer, reductive agent and bioactivity coating. Recent work from Sureshkumar et al.20 adopted a more physiological approach to acquire favorable antibacterial property by gluing magnetic particles on the surface of BC fiber by PDA and using the nano-silver as an antibacterial agent that were then successfully prepared a kind of magnetic composite materials with antibacterial property. For bioactivity coating, Wang et al.18 investigated the performance of PDA as a bioactive coating by compositing the PDA on the intravascular stent with complex shape which improved the biocompatibility of intravascular stent. As mentioned, PDA as a major pigment of naturally occurring melanin not only has been provided with electronic conductivity but also has ionic conductivity, because of its excellent ion affinity. It is assumed that the PDA can be used for electronic-ionic hybrid conductive materials, and some researchers21 have explored the electrical properties of PDA and related composite materials. For example, Xu22 prepared a kind of composite film which was made from PDA and other natural fiber materials, and the research related the use of the film as separation films of lithium battery indicated that the composite film could transport ions. Moreover, one of the advantages brought by the good electronic accept ability of PDA is the possibility to made PDA as an electron acceptor in the artificial photosynthesis as has been explored by Kim’s group23. From research works mentioned


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above, most of the researchers have paid close attention to the PDA used as adhesive and biological activity coating in the surface modification of materials24, composite materials field25. But the electrical properties of PDA do not attract enough attention. Besides, almost no researchers noticed the distribution of PDA in the composite materials and the factors to influence its distribution so far. So it is necessary and meaningful to research these properties and the effect of PDA when it is used as conductive materials rather than a biological coating and adhesive. In this study, a kind of naval flexible and conductive film was prepared by the in situ oxidative polymerization of dopamine with the use of BC as a three-dimensional flexibility template. All of the processes were conducted at a neutral pH condition instead of conventional alkaline condition26, enabling the uniformity of the PDA distribution on BC fibers. Conductivity is the most important properties of electrical signal sensor materials and it can be well controlled through this method. To demonstrate the electrophysiological signal collection performance produced by the application of BC/PDA, the BC/PDA-FCF was made of disposable ECG electrodes. Moreover, the microstructure, surface topography, mechanical properties and cytocompatibility were also studied by SEM, FTIR, LSCM and stress strain curve test respectively. For the further application, when it was used to measure the electrocardiogram, the BC/PDA-FCF also showed significant potential in applications for electronic skins, conductive materials, tissue adhesives, implantable or wearable biosensors for human health monitoring and other biomedical applications. 2. EXPERIMENTAL SECTION


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2.1. Materials. Bacterial cellulose(BC) with a thickness of 2.0 mm were provided by Hainan Yida Food Co., Ltd (Hainan, China). Dopamine hydrochloride, Hydrochloric acid(HCl), Sodium hydroxide(NaOH) were purchased from Sinopharm Chemical Reagent Co., Ltd (China). Deionized water was produced from our lab building. Other regents used in the experiments were all of analytical level. 2.2.

Preparation

of

bacterial

cellulose/Poly(dopamine)

flexible

and

conductive

film(BC/PDA-FCF). The preprocessing method of bacterial cellulose is the same one as Wu’s27. This process can exclude the influence of bacterial cellulose impurities caused by bacterial cell debris, impurities of cultures and so on. The solution of dopamine has a concentration of 1.0 g/L. For the complete permeability of dopamine monomer into the network of BC, some BC discs (d=15 mm, δ=2.0 mm) which has been cut by the circular blade were soaked into those dopamine solution and kept in dark and closed environment for 12 hours. After that the samples were emerged into dopamine solution with a content of 2.0g/L. Then, the solution was placed in ventilation and lighting environment. We took a sample every 24 hours. The samples were named BC/PDA-1, BC/PDA2, BC/PDA-3 and BC/PDA-4 respectively and the content of PDA (BC/PDA-1(11.22% ± 1.02%), BC/PDA-2(14.71% ± 0.98%), BC/PDA-3(22.32% ± 1.87%), BC/PDA-4(26.27% ± 2.62%)) was tested by weight method(the calculation formula is shown as follow) with a precision electronic balance. Take 3 samples at random for each group for measurement, then take the average value. ߱௉஽஺ % =

௠೛ ି௠ಳ಴ ௠೛

× 100%

(1)


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Where mp represents the weight of composite films and mBC represents the weight of BC. 2.3. Characterization of chemical structures(ATR-FTIR). The composite bacterial cellulose film was prepared through a freeze drying technique. The chemical analysis of the composite bacterial cellulose film was carried out by fourier transform infrared spectroscopy with the aid of BRUKER TENSOR Ⅱ Fourier Transform Infrared Spectrometer. The wavelength range was from 600 cm-1 to 4000 cm-1. 2.4. Morphology of the composite materials. The morphology of the composite bacterial cellulose films were imaged with a scanning electron microscope(SEM) from Carl Zeiss Jena Company and the microscope, working in a high vacuum mode with an acceleration voltage of 5 kV, was used. These samples were prepared by using a freeze drying technique before spraying carbon. 2.5. Electrochemical characterization. The conductivity of the samples was measured with a conventional four-point probe technique(RTS-8, Probes Tech., China) at ambient temperature. For electrochemical impedance spectroscopy(EIS) measurements, an alternating potential with amplitude of 5 mV was applied to the two steel electrodes at open circuit potential and the frequency range was from 0.01 Hz to 100 kHz. 2.6. Mechanical property. Tensile stress-strain properties of the BC/PDA-FCF were determined by using a Stable Micro Systems TA-HD plus Texture Analyzer with a loading rate kept at a strain rate of 50 mm min-1 at room temperature. The mechanical testing specimens whose dimensions following ISO standards were casted directly in the mold through the casting procedures described above. Each of the tensile specimens was cut into a geometric shape of dumb-bell with 4 mm wide, 1 mm thick and a gauge length of 20 mm [ISO37:2005(E)]. In each


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case, three samples were tested from which the mean and standard deviation were calculated respectively. 2.7. The surface physical property. When a drop of water drops on the surface of the material, the solid-liquid-gas three-phase junction reaches an equilibrium. The angle between the tangent of gas-liquid interface and the tangent of solid-liquid interface is called water contact angle which can be used to characterize the hydrophily of materials. The water contact angle was tested with the aid of an optical contact angle meter(OCA20, Dataphysics Inc.) at ambient temperature in this study. The volumes of each drops of water were 2 µL. Samples placed on glass slides were dried at room temperature to ensure the complete spreading of them ahead of the test so that the accurate data of contact angle of BC and BC/PDA could be measured. The roughness also reflects one aspect of the surface physical properties. In particular, the cell attachment may be concerned with the levels of roughness of materials. The roughness was tested with laser scanning confocal microscopy(LSCM). The samples were dried on the surface of glass before testing. 2.8. In Vitro Biocompatibility Test. The biocompatibility of BC/PDA-FCF was assessed by the fluorescence microscopic observation of mesenchymal stem cells(MSCs). The mesenchymal stem cells were cocultured with composite films as described above in vitro for 7 days, with pure BC as control. After specified cell culture time periods, cells were fixed for 10 min in 4% paraformaldehyde, followed by staining with two vital dyes for 15 min, the red fluorescent cell membranes marker PKH26 and the cell nuclei vital blue fluorescent marker Hoechst 33342. The fluorescent microscopy images of the cells were acquired with the aid of an laser scanning confocal microscope(FV1200, Olympus, Japan).


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2.9. The test of electrocardiograms and antibacterial activities. This BC/PDA-FCF selfadhered on the author’s chest used as a surface electrode to record the electrocardiograms(ECG), which can be used to record activity from sets of heart motions. ECG data during systole processes of heart was detected by measuring electromyographic signal through adhered composites electrodes using a BIOPAC Acquisition Systems, Inc.(Goleta, CA, USA). The commercial electrode was the control group. The antimicrobial activities of BC/PDA-FCF investigated against Escherichia coli(E. coli ATCC 25922) as the model Gram negative bacteria and Staphylococcus aureus(S. aureus ATCC 25923) as the model Gram-positive bacteria by the disc diffusion method28 and colony counting method29. 3. RESULTS AND DISCUSSION 3.1. Analysis of microstructure. Researchers made a lot of study on the adhesion behavior of PDA which was very easy to stick on the metals. The most important factor to influence the conglutination character considered was that the catechol and amino functional groups were able to combine with metal surface by non-covalent. Otherwise, PDA could also combine with organic surface by covalent which has been proved by the report that the PDA could have the Michael addition reaction with amino or thiol groups. However, there are not any sorts of groups exist on BC except hydroxy. Thus the fibers and PDA could combined together by a large number of hydrogen bonds and this kind of non-covalent interactions may be the chief interaction between BC and PDA. Figure 1a shows the schematic diagram of the polymerization process of dopamine and PDA aggregated on the surface of BC.


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Figure 1. (a) the schematic diagram of the polymerization process of dopamine and PDA aggregation on the surface of BC (b)SEM photographs showing surface morphology of different BC/PDA-FCF The speed of the polymerization reaction in this experiment was lower, because the reaction condition was under neutral pH, than that carried out by the classic method through which the reaction occurred in the Tris buffer solution under pH 8.5 so that the aggregation process of PDA in BC network could be observed from the SEM images easily. We found that the PDA which had a granular distribution in the three dimensional network of BC adhered to the surface of nanofibers. When the BC was soaked in the dopamine solution, the dopamine monomers were found to have infiltrated into the BC and distributed on the surface of nanofibers due to the influence of the hydrogen bond and Van der Waals' force. In the initial stage of the selfpolymerization reaction, the reaction was happened on the surface of nanofibers. The PDA could infiltrate into the 3-D network of BC, because the size of the PDA particles was enough small. With the increasing of the concentration of PDA, more and more PDA particles tended to cover the nano-fibers of BC gradually. From the Figure 1b, the PDA covered BC fibers completely and formed a coating layer when the PDA concentration reached a value of over 20%. In this stage, the 3-D network of BC still existed. Then the subsequent PDA particles tended to adhere to the


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polymer particles which have already generated above the BC. Therefore, a large number of particles filled in the BC network and jammed the meshes of the BC. Many PDA particles cohered to form a polymer aggregation. Finally, the fibers and the meshes were covered with the paste completely so that the 3-D network structures of BC disappeared which could be observed clearly in the last sample which has the highest concentration of PDA. It’s worth noting that porous in the network of BC were filled up thoroughly when the contents of PDA merely reached 3.95%. The reason is that the newly produced PDA particles tend to combine with the PDA which have already covered the surface of BC and this rapid process enable the precipitation of PDA particles advanced at a tremendous speed to cover the surface of BC network completely. From the photo of BC/PDA-FCF(Figure 1b), the color of the sample became deeper and deeper with the increasing of PDA contents meanwhile the transparency turned bad(Figure S1). The transformation of the color apparently corresponded to the increasing of contents of dark brown PDA. 3.2. Analysis of ATR-FTIR. Figure 2a compares the FTIR spectra of each sample which obtained from the sample of BC and BC/PDA-FCF respectively. The spectra of the sample of BC have shown strong signals at 3347 cm-1, 2908 cm-1 and 1050 cm-1 respectively. These signals correspond to the characteristic absorption peak of BC. The absorption peak at 3347 cm-1 attributed to the intermolecular hydrogen bond stretching vibration caused by O-H. The peak at 1050 cm-1 was caused by the stretching vibration of carbon-oxygen bonds. Otherwise, the absorption peak at 2908 cm-1 was produced by the stretching vibration of CH2-CH which was the characteristic absorption peak of sugar. The BC/PDA-FCF has shown a unique absorption peak compared to that of BC located at 3288 cm-1. It was noticed that the band at 3288 cm-1 arose due


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to the amino stretching vibration of PDA. The typical absorption bands at 1583 cm-1 and a shoulder at 1616 cm-1 which caused by the backbone ring vibrations of PDA were depicted in the magnified area respectively. The curved vibration peak of C-H which was shown in the benzene ring also could be found in the infrared spectra of BC/PDA-FCF at 789 cm-1 and the little peak at 1507 cm-1 could be produced by the C-N. In conclusion, the above presentation indicates that the polymerization of dopamine could happen in the deionized water and the PDA has been composited on the BC successfully.

Figure 2. (a) The ATR-FTIR spectra of BC membranes and BC/PDA-FCF. FTIR spectra (KBr) of the different reaction time of (b) dopamine(PDA-1:24 h, PDA-2:48 h, PDA-3:72 h, PDA-4:96 h) and (c) poly(dopamine) The infrared spectrums of PDA with different reaction time were also shown in the Figure 2. Comparing the spectrum of dopamine and PDA(Figure 2c), lots of the absorption peaks of


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dopamine disappeared in the spectrum of PDA which means that the change of chemical bonds was predestined to happen in the processes of polymerization. But this inference was not conformity with some literature reports which considered that PDA was an aggregation of monomers, whose structures were cross-linked primarily via strong, noncovalent forces including hydrogen bonding, charge transfer, and π-stacking, similar to other synthetic or biological supramolecular polymers. This spectrum in this study demonstrates that the change of covalent bonds occurred in the process of the polymerization of dopamine rather than the noncovalent self-assembly. 3.3. The mechanical properties of composite. The tensile curves of PDA/BC-FCF were shown in the Figure 3. The result of pure BC was also listed here. The tensile strength of BC was 0.38± 0.1 MPa and the elongation at break was 20.56±2.1%. By comparison, all of tensile curves of the BC/PDA-FCF exhibited a substantial increasing. The highest tensile strength of BC/PDAFCF reached a maximum of 0.87±0.22 MPa and the elongation reached 48.71±8.6%. Along with the time extension of the polymerization reaction, there was a gradual increasing in the elongation at the break of BC/PDA-FCF. The significant improvement of mechanical properties improves the flexibility and conformability of BC/PDA-FCF as a biosensor.


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Figure 3. The schematic diagram of BC/PDA-FCF mechanical property(2.0 g/L) (a)The tensile stress-strain cures of BC and BC/PDA-FCF, (b)the tensile strength histogram of BC, BC/PDAFCF, (c)the elongation histogram of BC and BC/PDA-FCF, (d)the mechanical data table of BC, BC/PDA-FCF, (e)the schematic diagram of mechanical properties increasing of BC/PDA-FCF. The improvement of mechanical properties may relate to the appearance of PDA. Firstly, the substantial increasing of mechanical properties of BC/PDA-FCF had some connection with the excellent adhesion properties of the PDA. Figure 3e was the schematic diagram of the mechanical property of BC/PDA-FCF. We found that some BC fibers closely attached to the PDA particles and the PDA was in the nature of adhesion, so the fibers around the particles would strongly combine with the PDA which exerted an extremely powerful function on enhancing mechanical properties. The PDA acting as connection center increased the numbers of interaction sites of nanofibers results in the improvement of mechanical property of BC.22 Otherwise, the adhesion function of PDA increased the interaction among nanofibers which simply rely on the interaction of hydrogen bonds before the use of PDA, which lead to the improvement of the ability of BC to resist tensile force from the outside and of the elastic limit.


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Furthermore, this situation that the PDA filled in the blanks of BC network could also enhance the mechanical properties. Secondly, the construction features of BC also contributed to the mechanical properties of BC/PDA-FCF, especially the rich chemical groups of BC which could provide a strong combined point for PDA particles so that the PDA particles could stick to the BC fibers easily. 3.4. The analysis of surface properties. The surface structures and properties play an important role to the conductivity and cytocompatibility. Herein, the surface roughness and the hydrophilicity of these materials were tested and the results were shown in the Figure 4. The results indicated that the BC/PDA-FCF with low PDA content had a smooth surface which had a close resemblance with the pure BC, because of the existence of PDA and the distribution of which filled the hole of the BC network. The flattening surface tended to have a good effect on reducing the contact resistance. But when PDA content was sufficient to fill the holes, a large number of PDA formed a "ridge" prominence on the BC surface. The roughness improved sharply and reached 1.448 µm, which was beneficial to the adhesion of cells.


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Figure 4. The analysis of surface properties. (a) the 3-D pictures and the histogram of different samples surface roughness, (b) the picture and histogram of BC/PDA-FCFs’ contact angle, (c) the histogram of different samples contact angle, (d) the data statistics of the surface roughness and contact angle. The 3D images are measured by laser confocal microscopy and the pictures in the bottom left corner of the 3D images are the optical photographs.(the scale was 400µm)


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The hydrophilia was a crucial factor to achieve remarkable cells adhesion which was usually characterized through the water drop angle meter(Figure 4b, c). Obviously, the porous were abundant in the structure of BC saturated with water and the existence of water together with the porous structure has a bad effect on the measurement of contact angle. Before testing, the samples were attached on the glass slide and dried at room temperature in order to measure the contact angle. After that the network of BC collapsed completely and the influence associated with the existence of water was excluded with the disappearance of the network. The test results and photographs were shown in the Figure 4c and Figure 4b. The contact angle of BC/PDA-FCF with different PDA content were 73.5±5°(BC/PDA-1), 67.2±2°(BC/PDA-2), 62.2 ± 10°(BC/PDA-3), 41.2 ± 4°(BC/PDA-4), respectively. With the growth of the PDA content, the degree gradually reduced. But the contact angle of pure BC, only 35.7°, was lower than the value of BC/PDA-FCF. Some studies30 have proved that the BC was too smooth to facilitate cell attachment, but the surface properties of BC/PDA-FCF turned out to be suitable for the cell adhesion after the modification. In addition, a large amount of positive groups(amino, imino) which came from the PDA molecule were beneficial to the cell attachment. 3.5. Electrical performance analysis. The uncertainty of knowledge in the electrochemical properties of PDA still exists, but some researchers used PDA composite films as separation films for lithium ion batteries. To be specific, dopamine was also used as electron acceptor materials in the artificial photoelectric effect. Further observation revealed that the electrical conductivity of PDA was strongly influenced by the temperature, the physical form, and the humidity of the measurement conditions. In our works, the electrical conductivity of BC/PDAFCF was tested by the four point probe tester. We have found that the electrical conductivity also had some connection with the content of PDA. The result of the conductivity of composite


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materials with different content of PDA was shown in Figure 5. Obviously, the electrical conductivity of composite materials rose with the rising of the PDA content. But the relation was not completely described as a direct proportion. The conductivity value of BC/PDA-3 reached 6.3×10-3 S/cm which was the maximum value among all samples was closed to the electrical conductivity of polyaniline composite films. Another, it was difficult for the PDA to interact with each other caused by their sporadical distribution on the matrix result in the transportation of electrons been blocked, so that the electrical conductivity of PDA/BC could hardly been measured. When the content of PDA was so high that a continuous structure or network formed, electrons could transport due to the conductive network, and eventually the electrical conductivity of composite materials could be measured. Furthermore, the electrical conductivity of BC/PDA-FCF was measured under the condition of stretching and relaxing respectively and results were shown in Figure S2. The results indicate that the electrical conductivity were 1.98×10-4 S/cm(BC/PDA-1), 1.91×10-3 S/cm(BC/PDA-2), 6.18×10-3 S/cm(BC/PDA-3), 4.37×103

S/cm(BC/PDA-4) and 2.24×10-4 S/cm(BC/PDA-1), 1.74×10-3 S/cm(BC/PDA-2), 5.62×10-3

S/cm(BC/PDA-3), 4.16×10-3 S/cm(BC/PDA-4) under the condition of relaxing and stretching respectively. After the cycle of stretching and relaxing for 10 times, the electrical conductivities under different conditions were also measured and the result is also shown in Figure S2. These results could be employed to prove that the electrical conductivity was steady.


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Figure 5. (a)The diagram of the conductivity of composite materials, (b)the ultraviolet spectrogram of DA and PDA, (c)the diagram of the interaction between PDA molecule by p-p interaction At present, the molecular structure of the PDA has yet to be determined. But some researchers31 indicated that PDA was an excellent electron acceptor as well as a versatile adhesive. Researchers suggested that dopamine oxidation state by different ratio without lead, and dopamine combination according to certain proportion by benzene groups formed between C-C bands in parallel or anti-parallel polymerization32,

33

. Up to now, there weren’t any

explanations established to explain the mechanism of the electronic conductivity of PDA, but some theories postulated that the phenomenon(shown in Figure 5c), which would happen during the self-polymerization of PDA34, was responsible. First, the dopamine molecules can be stacked by π bond interaction. Then, the PDA molecules were mounted layer upon layer in the same way. Therefore, the reason why the PDA had electronic conductivity could attribute to the π bond interaction structure was similar to the mechanism of graphite.


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From the ultraviolet spectrum of dopamine and PDA(Figure 5b), we found that the ultraviolet absorption peak of PDA shifted to the long wave direction which was the so called red shift and which indicated the molecular structure was changed during the process of polymerization. With the increasing of conjugated chains, the conjugated system energy was decreased and the maximal absorption wavelength showed the bathochromic effect. This result conformed to the speculation shown in Figure 5c. All of the analysis could be employed as evidence which indicated that the electronic conductivity of PDA has some connection with π-π interaction between molecules. As we all know, the movement of charge carriers through the πsystems would lead to conductivity in eumelanin. Polydopamine as a kind of eumelanin has the same electrical conduction mechanism as them, and this suggestion was proved by the result in this study. Some researchers, however, suggest that eumelanin as an electronic−ionic hybrid conductor rather than an amorphous organic semiconductor.35 Therefore, the dc electrical conductivity was measured in order to study the electrical conductivity of BC/PDA-FCF. Known as a sensitive and effective method EIS which was used for probing the resistance properties of the polymer functionalized composite membrane was employed in this study to investigate the changes of the interfacial resistance over the period of the polymerization. The device of EIS test was shown in Figure 6e. EIS spectra in the form of Nyquist plot were usually composed of a geometric pattern of depressed semicircle in the high-frequency region and a straight line in the low-frequency region. But EIS’s spectra in Figure 6a indicated that the spectra which transited from a geometric pattern of straight line to a semicircle(from 4 days to 10 days) were not completely in conformity with the description. These results can be attributed to the high surface area of the macroporous of BC/PDA-FCF networks and the nanostructure of PDA in swollen BC networks. The Nyquist plot of BC/PDA-1 was a line which indicated that the


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transportation of ion was controlled by the process of diffusion. By comparison, the BC/PDA-4 curve revealed a geometric pattern of semicircle in the high-frequency region and a straight line in the low-frequency region. Therefore, it was evident that this was a mixed controlled electrode process including the process of charge transfer and diffusion. The structure of BC/PDA-FCF with a low PDA content had a close resemblance with the structure of BC network. As we know the electrode process depends on the diffusion process. Once the network disappeared when the PDA filled up the holes, the diffusion process was blocked which led the charge transfer process to dominate the resistance property. The diameter of the semicircle pattern in the Nyquist plot attributed to the charge-transfer resistance(Rct) of the probe at the electrode/electrolyte interface, and the value of which depended on the dielectric and insulating characteristics of the surface layer. The analysis of the EIS spectra by fitting to a Randles equivalent circuit as described previously31 revealed that the charge-transfer resistances of the BC/PDA-FCF with different PDA contents were 1.49×104 Ω ， 1.07×104 Ω(BC/PDA-3, BC/PDA-4), respectively. The coordinates of the Nyquist plot which intersected with the X-axis indicated the contact resistances between the stainless steel electrode and the BC/PDA-FCF. All of the contact resistances were under 200 Ω(Figure 6c).


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Figure 6. The Nyquist plot of BC/PDA-FCF, (a)the full Nyquist plot of BC/PDA-FCF, (b)the high frequency region Nyquist plot of BC/PDA-FCF, (c)the histogram of the coordinates of the Nyquist plot intersect with the X- axis, (d)the diagram of diffusion process and charge transfer, (e) the installation drawing of the device for alternating-current impedance test 3.6. The cell compatibility. As the BC and PDA have a good capacity of cell adhesion, it is necessary to estimate the cytocompatibility of BC/PDA-FCF, which is significant for the biomedical application. To explore the cytocompatibility of the BC/PDA-FCF, we used the MSCs for cell proliferation analysis and demonstrated the biocompatibility of BC/PDA-FCF to MSCs by means of fluorescence microscopic observation analysis. To clearly observe whether cells could survive after contacting with composite materials, phalloidin(as the red fluorescence dye links to cell cytoskeleton) and DAPI(4',6-diamidino-2-phenylindole, as the blue fluorescence dye that bonding strength to DNA) were employed. As shown in Figure 7a, fluorochromelabeled cells(merged images) exhibited substantial increasing with the continuous increasing of


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the PDA content, and this conclusion could also be proved by the result of the statistical analysis of cell proliferation. Compared with the pure BC, the BC/PDA-FCF facilitated MSCs’ adhesion and proliferation(shown in Figure 7), because the free catechol groups on the PDA chains interacted with the amine or thiol groups and formed cation-π or π-π interactions on cell membrane.36 Furthermore, this result could also ascribed to the high surface roughness and good hydrophilia of the BC/PDA-FCF. To be sure, the excellent cytocompatibility of BC/PDA-FCF benefited from the natural property of PDA and the distribution of the PDA on the BC.


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Figure 7. (a) Apoptosis of MSCs cultured in BC and BC/PDA-FCF samples at 7 days, (DAPI staining (blue), phalloidin (red) and merged nuclei and intact cytoskeleton), (b) the statistical analysis of cell proliferation

3.7. The test of electrocardiograms. According to the research work carried out by former researches, the flexible and conductive composite materials have had excellent mechanical properties, cytocompatibility and electronic-ionic hybrid conductive properties. Thus, the BC/PDA-FCF can be used for testing the biological electro cardiac signal. In this work, the BC/PDA-FCF were fabricated into a ECG electrode. The human body test data and antibacterial test results using the BC/PDA-FCF as a disposable ECG electrode were shown in Figure 8, and the Ag/AgCl commercial disposable electrode was the control group(shown in Figure 8c). The test results of the BC/PDA composite electrode with different PDA contents showed that with the increasing of PDA content, the ECG signal became stabilized gradually while the amplitude of the signal enhanced, because with the increasing of the PDA content the conductivity of BC/PDA composite electrode increased which led to the decline of the contact resistance, so that the contact between the electrode and the skin of the human body gradually became stable, and the ECG signal test was more and more obvious. Figure 8 showed a contrast of the ECG signal between the BC/PDA composite electrode and the general commercial product, both of them were employed to make a circuit with the Ag/AgCl electrode respectively, and the results showed that the ECG signals measured by the composite film electrode with a high PDA content were consistent to that of the common use commercial electrode. It was also suggested that the signal stability and strength reached the standard that the commercial electrode required. As the traditional commercial electrode that choose conductive gel as electrode materials(shown in Figure 8c) was generally devoid of the antibacterial properties, it can easily cause bacterial


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infections when it was used as materials that directly contact with the human skin for a long time. By comparison, the BC/PDA composite electrode has excellent antibacterial properties(shown in Figure 8d) and its antibacterial properties could be proved by experiments with the usage of both gram-negative bacteria (Escherichia coli) and gram-positive bacteria (Staphylococcus aureus). All of the inhibition zone diameter were greater than 20 mm and the inhibitory rate was more than 98%. These results indicated that the BC/PDA-FCF has excellent antibacterial properties that may relate to the rich amino content on the PDA molecule. The BC/PDA composite electrode also has excellent flexibility so it can contact closely with the skin, which was significant to ensure the stability of testing. Therefore, the electrodemade from BC/PDA-FCF can be used as a new type electrocardio-electrode with antibacterial properties.


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Figure 8. Electrocardiogram (ECG) signals detected by BC/PDA-FCF. (a) The ECG signals tested by different BC/PDA composite electrode. (b) The contrast of the BC/PDA composite electrode signals and commercial electrode signals. (c) The BC/PDA composite electrode can be well adhered on the author’s chest. (d) The antibacterial property of the BC/PDA-FCF. This data include the inhibition zone and the bacteriostatic rates. 4. CONCLUSIONS In conclusion, a novel flexible and conductive biocompatible composite BC/PDA-FCF with electronic and ionic bio-conductive ability were prepared by the in situ self-polymerization of


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dopamine on the nanofiber of bacterial cellulose under the neutral pH condition, which can be used as a new flexible bioelectrode for the electrophysiological signal detection. By controlling the reaction conditions, polydopamine could form a uniform and continuous wrapped-layer on the BC nanofiber that can prevent the aggregation of PDA caused by rapid polymerization under the conventional alkaline condition. The resultant PDA uptake on the fiber surface was strongly dependent on the covalent interaction. The BC/PDA-FCF with this special structure possesses higher electronic and ionic conductivity, and excellent mechanical properties. Meanwhile, it possesses a better cytocompatibility and antibacterial property. It is proved that the PDA plays an important role in improving the cytocompatibility and antibacterial property. The highest electrical conductivity reaches 10-3 S/cm, and the highest ionic conductivity reaches 1.51×10-5 S/cm. The value of tensile strength is double the pure BC value, and up to a maximum of 0.87 MPa. All above properties of the BC/PDA-FCF could be controlled by the PDA content and reaction time. Furthermore, the BC/PDA-FCF as a disposable ECG electrode shows outstanding signal stability and antibacterial properties. In summary BC/PDA-FCF with great comprehensive performance have great potential to be used for biological electrodes and flexible biosensor for wearable medical device. ASSOCIATED CONTENT Supporting Information Details of the result of the transparency test, the conductivity testing photograph under different conditions(relaxed and stretched conditions) and the test results. AUTHOR INFORMATION Corresponding Author


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*E-mail: [email protected]. Tel: +86-10-62330802. Fax: +86-10-62332336. Author Contribution The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. Notes The authors declare no competing financial interest. ACKNOWLEDGMENT This work is supported by National Natural Science Foundation of China (Nos. 51473019, 51773018), Key Research and Development Projects of People's Liberation Army(BWS17J036) and the Fundamental Research Funds for the Central Universities(3142017099). REFERENCES (1) Yue, L.; Xie, Y.; Zheng, Y.; He, W.; Guo, S.; Sun, Y.; Zhang, T.; Liu, S. Sulfonated Bacterial Cellulose/Polyaniline Composite Membrane for Use as Gel Polymer Electrolyte. Composites Science and Technology 2017, 145, 122-131. (2) Zhang, S.; Sun, G.; He, Y.; Fu, R.; Gu, Y.; Chen, S. Preparation, Characterization, and Electrochromic Properties of Nanocellulose-Based Polyaniline Nanocomposite Films. Acs Appl Mater Inter 2017, 9, 16426-16434. (3) Lay, M.; González, I.; Tarrés, J. A.; Pellicer, N.; Bun, K. N.; Vilaseca, F. High Electrical and Electrochemical Properties in Bacterial Cellulose/Polypyrrole Bembranes. Eur Polym J 2017, 91, 1-9. (4) Vijayakumar, V.; Khastgir, D. Hybrid Composite Membranes of Chitosan/Sulfonated Polyaniline/Silica as Polymer Electrolyte Membrane for Fuel Cells. Carbohyd Polym 2018, 179, 152-163. (5) Liu, D.; Du, P. C.; Wei, W. L.; Wang, H. X.; Wang, Q.; Liu, P. Flexible and Robust


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Graphical abstract


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Novel ElectronicâIonic Hybrid Conductive ... - ACS Publications

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