Enokitake Mushroom-like Standing Gold Nanowires toward Wearable

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Cite This: ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

Enokitake Mushroom-like Standing Gold Nanowires toward Wearable Noninvasive Bimodal Glucose and Strain Sensing Qingfeng Zhai,†,‡ Shu Gong,†,‡ Yan Wang,†,‡ Quanxia Lyu,†,‡ Yiyi Liu,†,‡ Yunzhi Ling,†,‡ Joseph Wang,§ George. P. Simon,‡,∥ and Wenlong Cheng*,†,‡,⊥

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Department of Chemical Engineering, ‡New Horizon Research Centre, and ∥Department of Materials Science and Engineering, Monash University, Clayton, Victoria 3800, Australia § Department of Nanoengineering, University of California, San Diego, La Jolla, California 92093, United States ⊥ The Melbourne Centre for Nanofabrication, Clayton, Victoria 3800, Australia S Supporting Information *

ABSTRACT: We have recently demonstrated that Enokitake mushroom-like gold with nanoparticles as the “head” and nanowires as the “tail” could grow directly on elastomeric substrates, which are extremely stretchable electrodes that can be used as wearable sensors for detecting strain and pressure. In this work, we show that such electrodes can also be used as intrinsically stretchable glucose biosensors. By modifying the vertical gold nanowire electrodes with glucose oxidase and Prussian blue nanoparticles, a limit of detection of 10 μM, sensitivity of 23.72 μA·mM−1·cm−2, and high selectivity can be achieved. The as-obtained glucose biosensors were able to maintain a high sensing performance under various mechanical deformations. Even for 30% strain, a sensitivity of 4.55 μA·mM−1·cm−2 toward glucose detection in the artificial sweat was possible. Furthermore, it was found that strains could be simultaneously detected with a gauge factor of 2.30 (strain 0−10%) and 22.64 (strain 10−20%), demonstrating the potential of such bimodal sensors to allow simultaneous monitoring of physical and biological signals. KEYWORDS: Enokitake mushroom-like gold nanowires, wearable and stretchable, bimodal sensor, glucose sensing, strain detection

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INTRODUCTION In recent years, soft and stretchable electronics have gained rapidly increasing attention because of their potential to be worn on body for noninvasive continuously monitoring of vital signs related to health, anytime and anywhere.1−3 To date, most of the current success has been limited to physical parameters, such as blood pressure,4,5 heart rate,6,7 and body motion.8 Nevertheless, past several years have witnessed encouraging progress in wearable electrochemical sensors for monitoring chemical and biological markers related to human health.9−12 Body fluids such as sweat come from eccrine glands and contain a wealth of chemical information that can indicate the health status of the body at the molecular level.13,14 Among various chemical biomarkers, glucose level in the sweat has been the focus because of its direct relevance to diabetes, and some studies have shown the correlation between perspiration glucose and blood glucose.14,15 Thus, wearable glucose sensors are highly desirable because they can avoid the pain and accompanying intense stress for invasive blood collection in the conventional “finger pricking” monitoring system.16−18 To date, a number of methods have been reported for glucose biosensors,19 among which enzyme-based electrochemical detection is important due to its high © XXXX American Chemical Society

selectivity, sensitivity, and simplicity for integration into wearable devices.20−22 It has been shown that it is possible to monitor glucose level in a noninvasive manner.16,23−26 However, these biosensors are largely based on rigid bulk metals with limited stretchability.27 One-dimensional (1D) nanomaterials possess a great advantage in the designing of stretchable electrodes for soft electronics.28 Such types of electrodes can be used for electrochemical biosensors.24,25 To achieve stretchability, electrodes can be designed extrinsically via structural design or intrinsically with nanomaterials.1 For the former, prestrain29 and serpentine pattern30,31 represent common design strategies; for the latter, metal nanowires32−36 or carbon nanotubes37 are viable materials of choice. Although each type of 1D nanomaterials may possess their own advantages and disadvantages for the applications in fabricating stretchable biomedical sensors, gold nanowires shows merit, including high chemical inertness, great biocompatibility, wide electrochemical window, high electrical Received: November 5, 2018 Accepted: February 11, 2019

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DOI: 10.1021/acsami.8b19383 ACS Appl. Mater. Interfaces XXXX, XXX, XXX−XXX

Research Article

ACS Applied Materials & Interfaces

Figure 1. (A) Fabrication process of the v-Au NW-based stretchable electrodes on flexible substrates with the assistance of a specially designed mask. (B) SEM characterization of the obtained v-Au NW film electrode. combining a specially designed mask39,40(Figure 1 A). Briefly, the EcoFlex substrate was pretreated with O2 plasma for 12 min, followed by immersion in APTES/ethanol solution and citrate-stabilized Au seeds solution for 2 h, respectively. After being washed with H2O and dried by N2, the specially designed pattern (Figure S1) was attached on the surface of Au seeds absorbed EcoFlex substrate. Finally, v-Au NW-based patterned stretchable electrodes were obtained after immersing the mask-attached EcoFlex substrate into ethanol solutions containing 12 mM HAuCl4, 980 μM MBA, and 29 mM L-AA for 3 min; the obtained v-Au NW-based stretchable electrode was used for characterization and fabrication of biosensors. Preparation of Glucose Biosensor. The above-obtained v-Au NWs were used as the three-electrode systems for the detection of glucose. All the three electrodes were based on the use of v-Au NWs with nonmodified v-Au NWs used as the counter electrode and Ag/ AgCl paste deposited on the v-Au NWs acted as the reference electrode. The working electrode was v-Au NWs that modified with GOx and PB particles.11,16 First, a thin layer of PB was deposited onto the v-Au NWs electrod through cyclic voltammetry (CV) scanning from 0 to 0.5 V for two cycles, with a scan rate of 20 mV/s in the PB deposition solution. Following this step, 3 μL of the mixture containing GOx (40 mg/mL in PBS, pH = 7.4) and SWCNTs (1 mg/mL) in the ratio of 2:1 (volume to volume) was drop-cast on to the PB-modified v-Au NW electrode. After drying at room temperature, 3 μL of 1% chitosan solution in 2% acetic acid was drop-coated on the surface of the electrode in order to maintain the GOx activity. The resultant biosensing electrodes were stored at 4 °C prior to electrochemical testing. Electrochemical Detection. PBS solution (pH = 7.4) was used as the supporting electrolyte. For CV scanning, the typical electrochemical window is −0.3 to 0.5 V with a scan rate of 0.05 V/s; for chronoamperometry, the applied voltage was −0.1 V. Such electrochemical tests were done for different stretched states of the sensor in artificial sweat (0, 10, 20, and 30%).

conductivity, and facile surface modification based on thiol− Au chemistry.38 Recently, we have shown that vertically aligned Enokitake-like gold nanowires (v-Au NWs) that bonded to EcoFlex elastomers can be stretched up to 800% strain without losing conductivity.39−41 Compared with the Au NWs percolated networks, such three-dimensional (3D) standing nanowires may simultaneously offer very high surface areas and high conductivity for electrochemical reactions, which provides the impetus to explore novel stretchable electrodes for glucose biosensing applications.42 To demonstrate this, we modified v-Au NW electrodes with glucose oxidase (GOx) and Prussian blue (PB) nanoparticles. Such chemically modified electrodes were used in a standard threeelectrode system, in which nonmodified v-Au NW electrodes and Ag/AgCl served as counter and reference electrodes, respectively. We systematically investigated glucose-sensing performance including the detection limit, sensitivity, and selectivity of the as-prepared biosensors. For artificial sweat samples, the detection results for glucose sensing under different stretched states were also performed, which can achieve a sensitivity of 4.55 μA·mM−1·cm−2 with a linear range of 0−800 μM under 30% strain. During the electrochemical reaction, strain could be detected simultaneously with a gauge factor of 2.30 (strain from 0 to 10%) and 22.64 (strain from 10 to 20%) via chronoamperometry. Such a unique sensing capability demonstrates the potential of our system as bimodal physical and biological sensors applicable to comprehensive human health monitoring.

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EXPERIMENTAL SECTION

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Chemicals and Reagents. (3-Aminopropyl)triethoxysilane (APTES), HAuCl4, NaBH4, sodium citrate, L-ascorbic acid (L-AA), 4-mercaptobenzoic acid (MBA), K3Fe(CN)6, K4Fe(CN)6, KCl, NaCl, FeCl3, and glucose, GOx were purchased from Aspergillus niger, and chitosan, urea, lactic sodium, uric acid (UA), NaH2PO4, and Na2HPO4 were purchased from Sigma-Aldrich. EcoFlex (00−30) was purchased from Smooth-On, Inc. Single-walled carbon nanotubes (SWCNTs) were purchased from Jiangsu XFNANO Materials Tech Co., Ltd (China). PB deposition solution was freshly prepared containing 2.5 mM FeCl3, 2.5 mM K3Fe(CN)6, 0.1 M KCl, and 0.1 M HCl. Artificial sweat was prepared according to the published literature11 containing 22 mM urea, 5.5 mM lactic acid, 25 μM UA, 10 mM KCl, and 100 mM NaCl (pH = 5.5). Phosphate-buffered solution (10 mM, PBS) containing 0.1 M KCl (pH = 7.4) was used. All of the chemicals were of at least analytical grade and the water used throughout all experiments was purified by a Milli-Q system (resistivity > 18 MΩ·cm−1). Fabrication of a v-Au NW-Based Stretchable Electrode. The patterned v-Au NW-based stretchable electrode on an EcoFlex substrate was fabricated according to our published protocol

RESULTS AND DISCUSSION V-Au NWs that tethered to an elastic EcoFlex substrate were obtained using our previously published protocol39,40 that combines the specially designed shadow mask, as shown in Figure 1A. After growth, the morphology and structure of vertical standing Au NWs were characterized by scanning electron microscopy (SEM), as shown in Figures 1B and S2, and the electrode was composed of 1D gold nanowires with a vertically aligned structure and which leads to a 3D nanowire system. In addition, the orientation of dense v-Au NWs can be confirmed with nanoparticles on one side and nanowires on the opposite side, corresponding to our previous report.39,41 The diameter and the length of v-Au NWs were about 10.5 nm and 5.6 μm, respectively. The as-obtained patterned three-electrode system could bear arbitrary mechanical deformations including strain, bending, and twisting without observable cracks and delamination B


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Figure 2. (A) Modification process of the v-Au NW-based stretchable glucose biosensor. (B) CV curves of the fabricated stretchable biosensor before and after addition of glucose. (C) Chronoamperometric response of the fabricated stretchable biosensor upon successive addition of glucose at −0.1 V (inset: the linear calibration curves between the current and the concentration of glucose); (D) selectivity study of the stretchable biosensor using amperometric current responses at −0.1 V with successive addition of glucose (300 μM), followed by other electroactive interfering species, lactate (3 mM), KCl (10 mM), AA (50 μM), and UA (50 μM).

properties of excellent electricity and good biocompatibility were used as a suitable carrier for incubating the enzyme and enhancing the stability of the biosensor;11 the SEM micrograph of the stretchable electrode after coating SWCNTs is shown in Figure S6. Lastly, chitosan was used to prevent immobilized species from desorbing, as well as to maintain the bioactivity of GOx. It is well-known that PB is an effective artificial peroxidase that can significantly improve the sensitivity toward glucose detection at a relatively low potential.11 Figure 2B shows the CV curves generated by the fabricated biosensor before and after addition of glucose. It can be seen that both show the pair of characteristic redox peaks of PB at about 0.15 and 0.1 V. After the addition of glucose, the oxidation current decreased and the reduction current increased, indicating the good catalytic response of the fabricated biosensor to glucose.43 Chronoamperometry was further applied to evaluate the sensitivity of the biosensor for glucose detection, and the current response upon the successive addition of glucose under stirring is shown in Figure 2C. A “staircase” curve was obtained, demonstrating a clear, quantitative response to glucose concentration. Further numerical fitting (insert in Figure 2C) yielded a linear response range for glucose from 0 to 1.4 mM (R2 = 0.9951). The sensitivity and limit of detection are 23.72 μA·mM−1·cm−2 and 10 μM (S/N = 3), respectively. The results are comparable to other kinds of sensing electrodes (Table S1). The selectivity of our v-Au NW-based biosensor was further studied. It is known that sweat comes from eccrine glands composed of very complex chemicals, including ions, metabolites, acids, small proteins, and peptides.13 In human sweat, electrochemically active molecules, including lactate, UA, and AA as well as KCl were chosen to test if they influenced the sensing response toward glucose (Figure 2D). It can be seen that the current increases remarkably after

(Supporting Information, Video S1). We further evaluated the electrochemical performances after stretching the electrodes by differing amounts, while using Fe(CN)63−/4− as redox probes (Figure S3). The redox peak currents increased slightly on extension, which is likely due to increased electroactive surface after stretching by exposing inner v-Au NWs to the solution. The peak-to-peak separation also increased slightly as the applied strain for many times because of the increase in resistance. Nevertheless, both changes were not significant, even after 100% strain for 50 times. In addition, the conductivity and resistance changes of the electrode were also investigated, as seen in Figure S4A; the conductivity of the stretchable electrode was slightly decreased along with the increase of strain and then reached stability, which was caused by the increase of the resistance of the electrode along with increasing strain (Figure S4B). The patterned three-electrode system for glucose detection was further extended, where the v-Au NW electrode modified with GOx and PB served as the working electrode; nonmodified v-Au NWs acted as the counter electrode and Ag/AgCl-modified v-Au NWs were used as the reference electrode. As a working electrode, the electrode was pretreated in H2SO4 solution under CV scanning prior to chemical modification (Figure S5). It can be seen that the v-Au NW electrode shows features typical of a gold electrode that Au was first oxidized (commencing at about 0.9 V) and then electrochemically reduced in the negative potential sweep at a potential of about 0.4 V. The electrochemical surface area of the fabricated electrode can be calculated through integrating the charge required for reducing the gold oxide formed in the positive sweep,42 it is about 1.2 cm2, which is much larger than its geometric area (≈0.07 cm2). In addition, the electrochemical sweep step resulted in a clean electrode surface, which was followed by electrodeposition of PB and immobilization of GOx (Figure 2A). Here, SWCNTs with C


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We further show that our patterned three-electrode system based on v-Au NWs may serve as a bimodal sensor for simultaneous detection of physical signals (strains in this study) and chemical signals (glucose in this study). To prove this concept, the current changes of the working electrode were recorded upon the addition of glucose and the application of strains (Figure 4A). Clearly, the addition of glucose leads to

injection of glucose. In contrast, the addition of other interfering species did not induce much change in current. This clearly demonstrates the high selectivity of the fabricated biosensor for glucose detection. More importantly, the high electrochemical sensing performances could be maintained, even after multiple stretching cycles at various strains (Figure S7). Such a high durability encouraged further for glucose detection tests in artificial sweat at different stretched states, which is important for wearable biodiagnostics. Consistent with our recent studies,39,40 v-Au NWs film surfaces experienced tiny cracks under low level of strains, which are difficult to see, even under an optical microscope (Figure 3A) and show little change for different

Figure 4. Proposed bimodal stretchable sensor based on the threeelectrode system for glucose and strain detection. (A) Original chronoamperometric response of the stretchable biosensor upon the successive addition of glucose and application of strains. (B) Extractive current response upon the successive addition of glucose (B) and application of strains (C) (insets are the relationship between the current and the concentration of glucose and the applied strains, respectively).

Figure 3. Detection performances of the fabricated stretchable biosensor toward glucose at different stretched states from 0 to 30% strain in artificial sweat. (A) Optical microscope images of the stretchable sensor (scale bar: 100 μm). (B−E) Chronoamperometric response of the stretchable biosensor upon the successive additions of glucose at −0.1 V (inset: the photographs of the electrodes). (F) Linear calibration curves are between the current and the concentration of glucose.

an increase in the absolute currents, whereas the strain would lead to the decrease in the absolute currents. The change of faradic current response to glucose and strains has been extracted (Table S2) and replotted in Figure 4B,C, respectively. The relationship between the current and the concentration of glucose shows good linearity in the range of 0−1.15 mM (R2 = 0.9763) and yields a sensitivity of 27.32 μA· mM−1·cm−2 (inset in Figure 4B). In addition, the current signal response to strain could also be determined and is shown in a percentage-based plot (inset in Figure 4C), demonstrating a gauge factor of 2.30 (strain 0−10%) and 22.64 (strain 10−20%). These proof-of-concept results indicate that our v-Au NWs-based systems allow the fabrication of multimodal sensors for identification of both

degrees of extension. Under such deformed conditions, the quantitative detection of glucose was investigated for the concentration range of 0−800 μM (Figure 3B−E). For all three strain levels (10, 20, and 30%), staircase-like chronoamperometry curves were observed. Further regression fitting showed that all the three stretched electrodes exhibited linear relationships between the current and the concentration of glucose, as shown in Figure 3F. The sensitivities at 0, 10, 20, and 30% were 25.45, 19.45, 11.79, and 4.55 μA·mM−1·cm−2, respectively. The reduced sensitivity with the increased strain may be due to the decreased conductivity and increased resistance of v-Au NW-based electrode as a result of cracks formed under such stretched conditions. D


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(5) Pan, L.; Chortos, A.; Yu, G.; Wang, Y.; Isaacson, S.; Allen, R.; Shi, Y.; Dauskardt, R.; Bao, Z. An Ultra-Sensitive Resistive Pressure Sensor Based on Hollow-Sphere Microstructure Induced Elasticity in Conducting Polymer Film. Nat. Commun. 2014, 5, 3002. (6) Shin, K.-Y.; Lee, J. S.; Jang, J. Highly Sensitive, Wearable and Wireless Pressure Sensor Using Free-Standing ZnO Nanoneedle/ PVDF Hybrid Thin Film for Heart Rate Monitoring. Nano Energy 2016, 22, 95−104. (7) Shao, Q.; Niu, Z.; Hirtz, M.; Jiang, L.; Liu, Y.; Wang, Z.; Chen, X. High-Performance and Tailorable Pressure Sensor Based on Ultrathin Conductive Polymer Film. Small 2014, 10, 1466−1472. (8) Wang, Y.; Gong, S.; Wang, S. J.; Simon, G. P.; Cheng, W. Volume-Invariant Ionic Liquid Microbands as Highly Durable Wearable Biomedical Sensors. Mater. Horiz. 2016, 3, 208−213. (9) Windmiller, J. R.; Wang, J. Wearable Electrochemical Sensors and Biosensors: A Review. Electroanalysis 2012, 25, 29−46. (10) Yang, Y.; Gao, W. Wearable and flexible electronics for continuous molecular monitoring. Chem. Soc. Rev. 2018, DOI: 10.1039/C7CS00730B. (11) Gao, W.; Emaminejad, S.; Nyein, H. Y. Y.; Challa, S.; Chen, K.; Peck, A.; Fahad, H. M.; Ota, H.; Shiraki, H.; Kiriya, D.; Lien, D.-H.; Brooks, G. A.; Davis, R. W.; Javey, A. Fully Integrated Wearable Sensor Arrays for Multiplexed in Situ Perspiration Analysis. Nature 2016, 529, 509. (12) Imani, S.; Bandodkar, A. J.; Mohan, A. V.; Kumar, R.; Yu, S.; Wang, J.; Mercier, P. P. A Wearable Chemical−Electrophysiological Hybrid Biosensing System for Real-Time Health and Fitness Monitoring. Nat. Commun. 2016, 7, 11650. (13) Bariya, M.; Nyein, H. Y. Y.; Javey, A. Wearable Sweat Sensors. Nat. Electron. 2018, 1, 160−171. (14) Nyein, H. Y. Y.; Tai, L.-C.; Ngo, Q. P.; Chao, M.; Zhang, G. B.; Gao, W.; Bariya, M.; Bullock, J.; Kim, H.; Fahad, H. M.; Javey, A. A Wearable Microfluidic Sensing Patch for Dynamic Sweat Secretion Analysis. ACS Sens. 2018, 3, 944−952. (15) Lee, H.; Choi, T. K.; Lee, Y. B.; Cho, H. R.; Ghaffari, R.; Wang, L.; Choi, H. J.; Chung, T. D.; Lu, N.; Hyeon, T.; Choi, S. H.; Kim, D.H. A Graphene-Based Electrochemical Device with Thermoresponsive Microneedles for Diabetes Monitoring and Therapy. Nat. Nanotechnol. 2016, 11, 566. (16) Bandodkar, A. J.; Jia, W.; Yardımcı, C.; Wang, X.; Ramirez, J.; Wang, J. Tattoo-Based Noninvasive Glucose Monitoring: A Proof-ofConcept Study. Anal. Chem. 2014, 87, 394−398. (17) Jia, W.; Bandodkar, A. J.; Valdés-Ramírez, G.; Windmiller, J. R.; Yang, Z.; Ramírez, J.; Chan, G.; Wang, J. Electrochemical Tattoo Biosensors for Real-Time Noninvasive Lactate Monitoring in Human Perspiration. Anal. Chem. 2013, 85, 6553−6560. (18) Liu, Q.; Liu, Y.; Wu, F.; Cao, X.; Li, Z.; Alharbi, M.; Abbas, A. N.; Amer, M. R.; Zhou, C. Highly Sensitive and Wearable In2O3 Nanoribbon Transistor Biosensors with Integrated On-Chip Gate for Glucose Monitoring in Body Fluids. ACS Nano 2018, 12, 1170−1178. (19) Chen, C.; Xie, Q.; Yang, D.; Xiao, H.; Fu, Y.; Tan, Y.; Yao, S. Recent Advances in Electrochemical Glucose Biosensors: A Review. RSC Adv. 2013, 3, 4473−4491. (20) Wang, J. Electrochemical Glucose Biosensors. Chem. Rev. 2008, 108, 814. (21) Vashist, S. K. Non-Invasive Glucose Monitoring Technology in Diabetes Management: A Review. Anal. Chim. Acta 2012, 750, 16− 27. (22) Zhang, X.; Jing, Y.; Zhai, Q.; Yu, Y.; Xing, H.; Li, J.; Wang, E. Point-of-Care Diagnoses: Flexible Patterning Technique for SelfPowered Wearable Sensors. Anal. Chem. 2018, 90, 11780−11784. (23) Kim, J.; Campbell, A. S.; Wang, J. Wearable Non-Invasive Epidermal Glucose Sensors: A Review. Talanta 2018, 177, 163−170. (24) Xuan, X.; Yoon, H. S.; Park, J. Y. A Wearable Electrochemical Glucose Sensor Based on Simple and Low-Cost Fabrication Supported Micro-Patterned Reduced Graphene Oxide Nanocomposite Electrode on Flexible Substrate. Biosens. Bioelectron. 2018, 109, 75−82.

physical and chemical signals with appropriate algorithm methods.

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CONCLUSIONS We have shown that Enokitake-like v-Au NW films are new electrochemical electrodes that allow the detection of glucose with the detection limit, linear range, sensitivity, and selectivity matching commonly used bulk gold and glassy carbon electrodes. Unlike these traditional electrochemical electrodes, our v-Au NW-based electrodes are intrinsically stretchable without significant reduction in their conductivity for low strains. This attribute allowed for detection of glucose when stretched, with adequate sensitivity and selectivity toward wearable sensing applications. Moreover, our three-electrode biosensing platform could identify strains while detecting glucose through chronoamperometry. This indicates the potential of our system to serve as a bimodal sensor for comprehensive monitoring of physical and chemical biometric signals and is thus promising for future biointegratable, remote biodiagnostics.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.8b19383. Additional information about the mechanical deformation study of the fabricated v-Au NW-based stretchable electrode, CV curve characterizations in H2SO4 and Fe(CN)63−/4−, obtained biosensor for glucose detection after multiple stretching cycles at various strains, and comparison results of the obtained glucose sensor with other reported GOx-based electrochemical sensors (PDF) Obtained v-Au NW-based electrode undergoing arbitrary mechanical deformation (AVI)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Joseph Wang: 0000-0002-4921-9674 Wenlong Cheng: 0000-0002-2346-4970 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work is financially supported by the ARC discovery projects DP170102208 and DP180101715. This work was performed in part at the Melbourne Centre for Nanofabrication (MCN) in the Victorian Node of the Australian National Fabrication Facility (ANFF).

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REFERENCES

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Enokitake Mushroom-like Standing Gold Nanowires toward Wearable

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