Letter Cite This: Nano Lett. XXXX, XXX, XXX−XXX
pubs.acs.org/NanoLett
Stretchable Fiber Biofuel Cell by Rewrapping Multiwalled Carbon Nanotube Sheets Hyeon Jun Sim,† Dong Yeop Lee,† Hyunsoo Kim,† Young-Bong Choi,‡ Hyug-Han Kim,‡ Ray H. Baughman,§ and Seon Jeong Kim*,† †
Center for Self-Powered Actuation, Department of Biomedical Engineering, Hanyang University, Seoul 04763, Korea Department of Chemistry, Dankook University, Cheonan 31116, Korea § The Alan G. MacDiarmid NanoTech Institute, University of Texas at Dallas, Richardson, Texas 75083, United States Downloaded via UNIV OF WINNIPEG on July 17, 2018 at 09:24:53 (UTC). See https://pubs.acs.org/sharingguidelines for options on how to legitimately share published articles.
‡
S Supporting Information *
ABSTRACT: The fiber-type biofuel cell is attractive as an implantable energy source because the fiber can modify various structures and the wound can be stitched like a suture. In addition, in daily life, the biofuel cell is forced by human motion, and stretchability is a critical requirement for real applications. Therefore, we introduce a new type of highly stretchable, stable, soft fiber biofuel cell with microdiameter dimensions as an energy harvester. The completed biofuel cell operated well in fluids similar to human fluids, such as 20 mM phosphate-buffered 0.14 M NaCl solution (39.5 mW/cm2) and human serum (36.6 μW/cm2). The fiber-type biofuel cell can be reversibly stretched up to 100% in tensile direction while producing sustainable electrical power. In addition, the unique rewrapping structure, which traps the enzyme between multiwalled carbon nanotube sheets, enormously enhanced the stability of the biofuel cell when the biofuel cell was repeatedly stretched (the power density retention increased from 63 to 99%) and operated in human serum (the power density retention increased from 29 to 86%). The fiber can be easily woven into various structures, such as McKibben braid yarn, and scaled up by series and parallel connections. KEYWORDS: Stretchable, stable, soft, fiber, biofuel cell the smart fiber has mechanical degrees of freedom and can modify various structures, such as building blocks and knotting for weaving textiles. In addition, the wound can be stitched with the implantable fiber device like a suture.29 Currently, the stretchable fiber devices have been actively studied because they are necessary for human motion in daily life.30−32 Our group demonstrated a fiber-type high-power biofuel cell for energy harvesting from subcutaneous glucose from artificial human fluid.13 The fiber is highly flexible and easily woven as an electrode into a textile. However, in real applications in daily life, stretchable movement can cause deformation to wearable and implantable devices, leading to one of the crucial factors for performance decrease. When the biofuel cell was
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he ubiquitous health-care system has been attracted to wearable smart cloth and implantable devices. 1−5 Sustainable electric energy sources without replacement are required to achieve this goal.6−9 For the energy source of implantable devices, enzymatic biofuel cells, which convert biochemical energy from humans, such as glucose, into electric energy, have been studied as a promising next-generation energy source.10−19 Recently, a flexible and microsize energy harvester has been applied to a real application. Therefore, recent research on energy harvesters has focused on the dimension conversion from three- or two-dimensional (3-D, 2-D) structures to onedimensional (1-D) fiber structures.20−28 Previous brittle and bulky energy harvesters can be limited in implantation because the device takes up a large space in the body and can restrict the movement of tissue and organs in daily life. The fiber-type device has high potential to apply in real applications because © XXXX American Chemical Society
Received: June 4, 2018 Revised: July 2, 2018 Published: July 11, 2018 A
DOI: 10.1021/acs.nanolett.8b02256 Nano Lett. XXXX, XXX, XXX−XXX
Letter
Nano Letters
Figure 1. Fabrication and structure of biofuel cell fiber. (a) Fabrication process for stretchable biofuel cell fiber. For a stretchable biofuel cell fiber, the stretchable electrode was fabricated by MWNT sheet-wrapped rubber fiber. After the wrapping process, the stretchable electrode was coated with an active enzyme layer that is blended with an enzyme, redox mediator, and cross-linker. Finally, the active enzyme layer-coated electrode was rewrapped with MWNT sheets. The rewrapped structure was used to enhance electrode performance and stability of the biofuel cell fiber. (b) Schematic illustration of the structure and function of biofuel cell fiber, which indicates associated electron-transfer processes and chemical transformations. The anode enzyme and redox mediator polymer used were glucose oxidase (GOx) and mediator I, respectively. The cathode enzyme and redox mediator polymer used were bilirubin oxidase (BOx) and mediator II, respectively.
was formed as a multilayered core−shell structure, which traps the enzyme between MWNT sheets. First, the process starts with the prestretched rubber fiber. Commercially available rubber was stretched ∼100%, and the two ends of the rubber fiber were tethered to prevent release during subsequent fabrication processes. The stretched rubber fiber was wrapped with MWNT sheets that were drawn from MWNT forests.29 The MWNT sheet-wrapped rubber fiber was used as a stretchable electrode. Second, after the wrapping process, the stretchable electrode was coated with the active enzyme layer, which is blended with an enzyme, redox mediator, and cross-linker. To make the anode and cathode, we used different enzymes and redox mediators, where oxidation and reduction occurs (Figure 1b). The glucose oxidase (GOx) and poly(N-vinylimidazole)[Os(4,40-dimethoxy-2,20-bipyridine)2Cl])+/2+ (redox mediator I) was used as enzyme and redox polymer of the anode, respectively. Bilirubin oxidase (BOx) and poly(acrylamide)poly(N-vinylimidazole)-[Os(4,40-dichloro-2,20-bipyridine)2Cl])+/2+ were used as enzyme and redox polymer of cathode, respectively. Each enzyme was cross-linked by poly(ethylene glycol) diglycidyl ether. Osmium-based conducting polymers were selected as redox mediators to produce rapid electron transfer between the enzymes and the MWNT sheets. Biofuel cell fiber was simply produced using dry-coating methods and integrated in proximity to the MWNT sheet. The linear structure can eliminate the requirement of a separator and has the advantage of a single-compartment biofuel cell structure. Finally, the active enzyme layer-coated electrode was rewrapped with MWNT sheets. The rewrapped structure has two significant advantages. First, the rewrapped structure
deformed, the active enzyme layer was deformed by mechanical property mismatch compared with a stretchable electrode, leading to gradual lamination, leaching, and performance decrease. Here we introduce a new type of highly stretchable, stable, soft fiber biofuel cell with microdiameter dimensions for energy harvesting. The fiber-type biofuel cell could be reversibly stretched up to 100% in the tensile direction, producing sustainable electrical power in fluids similar to human fluids. In addition, the unique rewrapping structure, which traps the enzyme between multiwalled carbon nanotube (MWNT) sheets, is the key component for highly stable performance with reversible stretching cycles and time. The stability of the biofuel cell with mechanical deformation and time was enhanced by rewrapping the MWNT sheet over the active enzyme layer (the power density retentions after 100 stretching cycles and 10 h in human serum were 99 and 86%, respectively) compared with nonrewrapped biofuel cell, which is not rewrapped with the MWNT sheet on the active enzyme layer-coated electrode (the power density retentions after 100 stretching cycles and 10 h in human serum were 63 and 29%, respectively). The stretchable inner electrode, which was formed as a microwrinkled structure, is prepared by wrapping a MWNT sheet on the commercial rubber fiber. The enzyme mixtures, which are blended with an enzyme, enzyme mediator, and cross-linker, were coated on the inner electrode, and the MWNT sheet was rewrapped on the enzyme-coated fiber. Because MWNT sheets are highly porous and conductive, mass transport and electron transport in oxidation and reduction will readily occur. The fabrication process of an enzymatic biofuel cell electrode is shown in Figure 1a. The biofuel cell electrode B
DOI: 10.1021/acs.nanolett.8b02256 Nano Lett. XXXX, XXX, XXX−XXX
Letter
Nano Letters
Figure 2. Stretchable electrode performance of MWNT sheet-wrapped rubber fiber. (a,b) SEM image showing the surface of a 500 μm diameter carbon nanotube (CNT) sheet-wrapped rubber fiber at the initial state. The scale bars are 200 and 20 μm, respectively. (c,d) SEM micrographs showing the stretched CNT wrapped rubber fiber with ∼100% strain. The scale bars are 200 and 20 μm, respectively. (e) Linear resistance with strain after 100 cycles and (f) the stress−strain curve of finally fabricated biofuel cell fiber.
enhances the stability of the biofuel cell fiber. Recent research has attempted to develop stretchable biofuel cells. These studies have shown that only the electrodes have elasticity and the active enzyme layer is inelastic. When the biofuel cell was deformed, the active enzyme layer was broken down by mechanical property mismatch compared with a stretchable electrode, leading to gradual lamination, leaching, and performance decrease. The rewrapped structure can overcome this problem. The MWNT sheet tightly adhered to the active
enzyme layer and prevented leakage of the active enzyme layer from the electrode when the active enzyme layer was cracked during deformations such as bending, twisting, and stretching. Second, rewrapping the MWNT sheet supports the electron transportation compared with the nonrewrapped structure, which is only an active enzyme layer-coated electrode without the rewrapped MWNT sheet. The MWNT sheet has a highly conductive and porous structure, which allows fast electron transport generated from glucose and oxygen for oxidation and C
DOI: 10.1021/acs.nanolett.8b02256 Nano Lett. XXXX, XXX, XXX−XXX
Letter
Nano Letters
Figure 3. Stretchability of the completed biofuel cell fiber. (a) Photonic image of the stretchable biofuel cell fiber in the initial and stretching states. (b) Polarization curves for the biofuel cell fiber anode in 7 mM glucose concentration and air-saturated electrolyte. (c) Polarization curve for the biofuel cell fiber cathode in 7 mM glucose concentration and air-saturated electrolyte. (d) Areal power density as a function of potential for the completed biofuel cell system in 7 mM glucose concentration and air-saturated electrolyte. The experiment was carried out under 20 mM PBS solution (temperature: 37 °C) when stretched about 0% (black symbols) and 100% (red symbols).
reduction. In addition, mass transport of glucose and oxygen occur well because of the highly porous structure of the MWNT sheet. The diameter of the finally fabricated biofuel cell fiber, the coating thickness of active enzyme layer, and thickness of rewrapping MWNT sheets were about 380, 20, and 2 μm, respectively (Figure S1). Scanning electron microscope (SEM; Hitachi S4700) images show the initial morphology of the MWNT sheetcoated rubber fiber for a stretchable electrode (Figure 2a,b). This fiber has a uniform diameter of ∼340 μm. In a magnified SEM image of the electrode surface, microscopic MWNT wrinkles that are 1.2 μm wide and 2.2 μm height were observed along the entire fiber. MWNT wrinkles were spontaneously formed along the fiber during relaxation from the fabrication strain, resulting in the wrinkled electrode. Figure 2c,d shows the process that occurs during the elongation of the electrode at 100% strain. These uniform wrinkles became flat at a high strain (100%), providing high stretchability in the tensile direction of the electrode. Concurrently, the core-rubber fiber diameter was decreased by Poisson’s ratio, and MWNT wrinkles also were formed along the circumference. In addition, the wrinkles were unfolded in stretching cycles and reversibly folded in releasing cycles.
To evaluate the electrical stability of the stretchable biofuel cell electrode, the electrical performance with strain was examined. The linear resistance of the fiber (normalized to unstretched fiber length) versus percent stretching is plotted in Figure 2e. The linear resistance slightly increased in the initial stage and then became flat according to the strain. The linear resistance increased from 510 to 600 Ω/cm on stretching this to 100% strain, but the original resistance was reversibly recovered after the releasing cycle. Because MWNT sheets tightly adhere to the core rubber fiber as a result of ethanolbased MWNT densification, no noticeable delamination of MWNT was observed during the stretching and releasing cycles. The MWNT wrinkles were reversibly changed with strain, and the resistance was constant at overall strain during the stretching and releasing cycles (Figure S2). The result indicated that the stretchable electrode can be used as a strain sensor because the resistance value is fixed at strain regardless of the change in the strain direction. In addition, the electrical resistance stability during repeated cycles is an important issue for practical applications. The linear resistance after 100 cycles is similar to the linear resistance of the initial state without distortion, and we expect that the finally fabricated stretchable biofuel cell was electrically stable and sustained its performance during stretching cycles. D
DOI: 10.1021/acs.nanolett.8b02256 Nano Lett. XXXX, XXX, XXX−XXX
Letter
Nano Letters
Figure 4. Stability of the completed biofuel cell fiber with stretching and time. (a) Areal power density with reversible 100% stretching for the completed biofuel cell system at 7 mM glucose concentration and air-saturated electrolyte (inset: the power density ratio (P/P0) with reversible stretching cycles). (b) Areal power density with time during 10 h for the completed biofuel cell system in human serum solution (inset: the power density ratio (P/P0) with time).
potential for the onset of catalytic oxidation of glucose at the anode (−0.3 V versus Ag/AgCl) and catalytic oxygen reduction at the cathode (0.5 V versus Ag/AgCl). The maximum areal power density was 42 μW/cm2 (based on the external surface area of the yarn electrode and corresponding to a volumetric power density of 2.1 mW/cm3). The performance of the biofuel cell to generate electric power is negligibly interrupted after extreme stretching of 100% strain, and the result indicated that mechanical deformation abruptly affects the electrochemical properties of biofuel cell fibers. It is noted that the stretchable biofuel cell is capable of performing desirably under daily life because the maximum strain of human motion was ∼27%.17 The biofuel cell can play a pivotal role in various health-care and environmental applications in the presence of mechanical deformation; therefore, the performance stability during mechanical deformation should be confirmed. The power density of biofuel cell fiber was recorded after every 10 cycles of 100% strain at 7 mM glucose solution (Figure 4a). After 100 stretch−release cycles, the power density of rewrapped biofuel cell fiber slightly decreased from 39.5 mW/cm2 in the initial state to 39.1 mW/cm2 (the performance retained ∼99% compared with the initial power density). After 1000 stretching cycles, the performance retained ∼95% compared with the initial power density, and there was a negligible impact of such repeated strain (Figure S5). The biofuel cell has excellent stability during repeated stretching cycles, and we expect that the unique rewrapped structure enhanced the stability of the biofuel cell. To investigate the effect of the rewrapped structure, the power density of the rewrapped biofuel cell was compared with a nonrewrapped biofuel cell, which is not rewrapped with MWNT sheet on the active enzyme layer-coated electrode. In the nonrewrapped biofuel cell fiber, the performance greatly decreased from 38.4 mW/cm2 in the initial state to 24.2 mW/ cm2, and the performance retained ∼63% compared with the initial power density. The rewrapped biofuel cell fiber was more stable than the nonrewrapped structure, and the reason is that the rewrapping MWNT sheets are retaining the active enzyme layer. Because the active enzyme layer is brittle, the layer was easily cracked and delaminated from the electrode during mechanical
The elastic property of the stretchable electrode is shown in Figure 2f. From the stress−strain curve, a tensile stress of 0.3 MPa can be applied to the fiber without causing irreversible fiber deformation. The stretching and releasing cycles showed elastic recovery resulting in
