ARTICLE pubs.acs.org/Biomac
Electrospun Fullerenol-Cellulose Biocompatible Actuators Jia Li,† Sridhar Vadahanambi,‡ Chang-Doo Kee,† and Il-Kwon Oh*,‡ † ‡
Department of Mechanical Systems Engineering, Chonnam National University, Gwangju, Republic of Korea Division of Ocean Systems Engineering, School of Mechanical, Aerospace and Systems Engineering, Korea Advanced Institute of Science and Technology, 335 Gwahak-ro, Yuseong-gu, Daejeon 305-701, Republic of Korea
bS Supporting Information ABSTRACT: Though there are many stimuli-responsive polymer actuators based on synthetic polymers, electroactive natural biopolymer actuators are very rare. We developed an electrospun fullernolcellulose biocompatible actuator with much lower power consumption and larger electromechanical displacement in comparison with a pure cellulose acetate actuator. Morphology of the electrospun membranes resembles the nanoporous structure of extracellular matrix in natural muscles. Presence of minute concentrations of fullerenol leads to sharp increase in the degree of crystallinity and substantial increase in tensile strength of membranes. Chemical interactions between cellulose acetate and fullerenols are confirmed by three shifts in carboxylate, carboxy, and carbonyl linkages from the Fourier-transform infrared spectrometry. Much larger tip displacement, nearly 3-fold even at 0.5 wt % fullerenol content, was observed with much lower power consumption under both alternating and direct current conditions.
’ INTRODUCTION Stimuli-responsive polymer actuators are one of smart materials that have the ability to respond to external stimuli and exert mechanical work showing large deformation. Many synthetic polymers like Nafion,13 Flemion,4 and other ionic polymers57 have traditionally been the source materials to fabricate polymer actuators. There are some reports on electroactive actuators based on natural polymers like bacterial cellulose,8 plant cellulose,9 and chitosan,10 but the degree of actuation was less than desirable. However, until date, these actuators were fabricated by traditional solvent recasting technique and the membranes are nonporous in nature and do not mimick the basic fibrous structure of natural muscles. Additionally, natural polymer actuators are usually tested in fully hydrated conditions or under water, thus, limiting the scope and applications of the actuators. We recently showed actuation behavior of bacterial cellulose, however, it has certain disadvantages like low strength, difficulty in handling, and very low degree of actuation.8 Though there are some reports on actuation of natural polymers, it involves usage of expensive ionic liquids as the electrolyte buffer, and also, the degree of actuation is less than satisfactory.11 These abovementioned drawbacks can be overcome by fabricating electrospun natural polymers like cellulose acetate with fullerenols. Electrospinning is a simple and efficient technique to fabricate highly interconnected, nonwoven fibers with diameters in the micro- and nanometer range.12 Due to their extraordinary properties, such as porosity, large specific surface area, and ability to physically resemble natural extracellular matrix (ECM) protein structure,13 electrospun polysaccharide fibers had been widely r 2011 American Chemical Society
used in biomedical applications such as tissue engineering,14 wound healing, drug carrier,15 antimicrobial medical implants,16 dental applications, and biosensors.17 However, until date, there are no reports on electrospun natural polymer actuators. In this study, we report novel electrospun fullerenol-cellulose acetate actuators, which can be actuated under electrical input signals. Polyhydroxy fullerenols are known to be water-soluble, biodegradable, and are reported in a wide range of biomedical applications like cancer imaging,18 cancer therapy,19 and tumorinhibitory effects,20 whereas cellulose acetate is a biocompatible natural polymer. The aim here is to combine the excellent biocompatibility of fullerenols and cellulose acetate to fabricate novel electroactive actuators that can be used in biomedical applications. Addition of minute quantities (0.1 and 0.5 wt %) of fullerenols (hydroxyl-terminated fullerenes, C60-(OH)n) improved the electrochemical properties of the electrospun nanofibers. This manuscript is also the first report on the electrospun fullerenol-cellulose acetate nanofibrous composite actuators. Consequently, indepth studies of structureproperty characteristics including stressstrain tests and thermal characterization by DSC are also reported. FTIR and XRD analyses are also carried out to quantify the chemical interactions between hydroxyl moieties of fullerenols and cellulose acetate. The actuation performance of electrospun fullernol-cellulose acetate actuators was evaluated under several electrical input signals in wet condition. Received: December 8, 2010 Revised: April 21, 2011 Published: April 25, 2011 2048
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Figure 1. Photographs of electrospun cellulose acetate-fullerenol membranes before (a) and after electrode deposition (b).
Figure 3. TEM morphology of electrospun cellulose acetate-fullerenol nanofibrous membranes: (a, b) Morphology of fibers at 0.1 wt % of fullerenol (c) and (d) morphology of fibers at 0.5 wt % of fullerenol. grown in LuriaBertani (LB) liquid medium at 37 °C. 13C NMR spectra were recorded on a Bruker AVANCE 400 spectrometer with tetramethylsilane as an internal reference. The cross-sectional images and chemical analyses were performed using a 300 kV JEOL JEM 3010 with 0.17 nm point resolution at low temperature. Figure 2. SEM morphology of electrospun cellulose acetate-fullerene nanofibrous membranes.
’ EXPERIMENTAL SECTION Cellulose acetate (CA; white powder; Mn ∼ 30000 by GPC, 39.8 wt % acetyl groups), N,N-dimethylacetamide (DMAc; assay: 99.0%), and fullerenol C60-(OH)n were purchased from Sigma-Aldrich and were used as received. Cellulose acetate was dissolved in mixed solvents of DMAc/acetone (2:1 v/v)21 and stirred vigorously until a transparent solution was obtained at the room temperature (20 wt/v %). To this, 0.1 and 0.5 wt % fullerenols were added, respectively, followed by homogenizing the solution in an ultrasonic bath. A syringe pump was used to squeeze out the solution at speed of 2 mL/h through a needle with an inner diameter of 0.21 mm. The distance between the needle and collector is 15 cm and the applied voltage was 25 kV to obtain electrospun membranes with a thickness of 100 μm. Digital images of the obtained membranes are shown in Figure 1a. The membranes were immersed overnight in 1.5 N aqueous solution of lithium chloride. The electrospun actuators were fabricated by depositing very thin gold electrodes on both sides of the electrospun membranes using a physical deposition system (108 auto sputter coater, Cressington). The size of the actuator was tailored with dimensions of 10 40 0.1 mm and a representative photograph of the actuator is shown in Figure 1b. X-ray diffraction (XRD) of the composites was measured using DMAX-Ultima III X-ray diffractometer in the range of 20 to 90°. SEM (scanning electron microscopy) images were recorded using a cold field emission scanning electron microscope (S-4700, Hitachi, Japan). The ionic exchange capacity was calculated using the titration method with NaOH. ATR-FTIR (attenuated total reflection-Fourier transform infrared spectroscopy) of the membranes was tested using a Shimadzu IR Prestige-21 spectroscope. The experimental setup for the measurement of actuation consists of a charged couple device camera (XC-HR50, Sony), a laser displacement sensor (LK-031, Keyence), a NI-PXI system (1042Q, NI), and a current amplifier (UPM1503, Quanser). The biocompatibility of the electrospun nanoporous cellulose acetate membranes is tested in Escherichia coli K-12 bacteria cultures
’ RESULTS AND DISCUSSION Figure 2 shows the SEM images of the electrospun cellulose acetate nonwoven mats. Though many solvent solutions were used, the best results were obtained in a mixed solvent of DMAc/ acetone in 2:1 volume ratio. Scanning electron microscopy images reveal that electrospun CA nanofibrous membranes are composed of randomly oriented fibers with well interconnected three-dimensional pores. At lower concentrations of fullerenols, fibers in the size range of 400800 nm are formed with minimal degree of bead instabilities. Additional SEM micrographs and their size distribution can be found in the Supporting Information. However, at higher concentrations of fullerenols (1 wt %), the size of the nanofibers reduced to a considerable extent, accompanied by extensive bead formation, which can be attributed to cellulose-induced agglomeration of fullerenol particles, as shown schematically. Additionally, fullerenols are known to be electrostrictive and, at higher concentrations, more charges are carried along the jet in the electrospinning process, resulting in strong elongational forces due to mutual charge repulsion within the jet.22 As a result, the jet is stretched further, forming thinner fibers, whereas the beads are due to accumulation of the charges around fullernol agglomerates. In both the cases, a high degree of porosity is observed, which can be advantageous for actuator applications. The high porosity observed in the electrospun nanofibrous mats allows efficient diffusion of ions, and the high surface area provided by the well-separated nanofibers in the bundles is helpful for the higher electrochemical actuation.23 Moreover, the majority of nanofibers are tubular form that facilitate effective ion diffusion, which also contributes toward higher actuation. TEM pictures of electrospun nanofibers were taken in an in situ TEM operating at 300 kV and low temperatures (100 °C) to minimize beam damage due to thermal heating. Figure 3a and b show the images of 0.1 wt % fullerenolCA nanofibers. Nanofibers show the presence of a skin-core type 2049
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Figure 4. FTIR spectra of electropsun cellulose acetate and fullerenol reinforced cellulose acetate nanofibrous membranes.
of structure with an inner core compromised of well-dispersed but localized fullerenols (Figure 3b), whereas at the outer core there is the presence of very small quantities of fullernols. The skin-core microstructure of the electrospun fibers suggests that the fibers could have experienced a two-stage solvent evaporation during electrospinning, in which the skin precipitates faster than the core and, thus, has a different microstructure from the core. However, well dispersion of fullernols throughout the fibers is observed at 0.5 wt % of fullernol-CA membrane without the skincore structure in Figure 3c,d. Chemical interactions between CA and fullerenols are monitored by the shifts in the FTIR spectra shown in Figure 4. Shifts in three absorption bands at 1755 cm1 assigned to CdO ester stretching, the 1237 cm1 band assigned to stretching of CO of the acetyl groups, and the large OCC bond stretching at 1049 cm1 have been monitored.24 Low concentrations of fullerenol in CA membrane cause no apparent shift in any of these bands, whereas at 0.5 wt % significant shifts to the tune of 20 cm1 in all these three major bands indicate considerable chemical interactions between the hydroxyl moieties of fullerenol and carbonyl groups of cellulose acetate. The strong electrophilic properties of fullerenols are extremely reactive and are capable of selective nucleophilic addition reactions to carbonyl moieties in alkaline medium. Besides these, changes in minor bands like the COC antisymmetric bridge stretching at 1167 cm1 and symmetric stretching of methyl groups at 1370 cm1 is also noticeable. It is known that fullerenes are capable of Michael addition reaction with carbonyl peaks causing minor shifts at 896 cm1 β-glucosidic linkages between the glycosidic units, indicating changes in crystallinity.25 More information about the extent and type of interactions between the dispersed fullernols and cellulose acetate was studied by using NMR. Figure 5 shows the cross-polarization magic angle spinning (CP/MAS) 13C solid state NMR spectrum of electrospun pure cellulose acetate (a) and fullernol reinforced cellulose acetate nanofibers (b) at room temperature. The signals at 169, 100.94, 95.2, 72.6, and 62.53 can be attributed to CdO, C1, C4, C2C5 cluster, C6 and C-methyl at 37.782 and 34.93. A minimal shift in peak locations without any appreciable decrease in intensities of all carbon resonance spectral lines can be observed. However, there is a considerable decrease in intensities of the C-methyl spectral lines at 37.782 and 34.933, which indicates preferential attachment of fullerenols to these moieties.
Figure 5. Solid state 13C CPMAS NMR spectra of electrospun pristine cellulose acetate (a) and fullerenol reinforced cellulose acetate (b).
Figure 6. XRD spectra of electrospun cellulose acetate and fullerenol reinforced cellulose acetate nanofibrous membranes.
The variations in crystallinity of nanoporous electrospun cellulose acetate membrane are investigated with XRD data as shown in Figure 6. The main peak located at approximately 8° is associated with the principal characteristic of semicrystalline acetylated structure of cellulose acetate. At low concentration of fullerenol, no apparent change in this peak is seen, whereas at 0.5 wt % the position of this peak changed drastically indicating generation of a disorder caused by the projection of the substituting fullerenols along the axes and is associated with an increase in the interfibrillar distance and is also related to the breakdown of microfibrillar structures. This reduction of crystallinity when compared to the original cellulose acetate occurs due to the adherence of fullerenols to the acetyl groups of cellulose acetate. Minor changes in the overlapped 1R and 1β phase broad peak spanning from 15 to 25° are also observed in membranes with 0.5 wt % fullerenols with clear distinction in peaks of 1101R and 2001β becoming more apparent. Fullerenes are also known to be strong electron acceptors, the electron affinity of C60-(OH)n is 2.689 eV, therefore. the polar groups of cellulose acetate will provide cites for polymerfullerenol interactions via π-orbital mixing, which seems to start within the amorphous region, and reaction progresses sequentially into the crystallites. FTIR and XRD studies, in conjunction with the rigid-rod model 2050
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Figure 8. DSC curves of electrospun cellulose acetate and cellulose acetate-fullerene nanofibrous membranes. Figure 7. Stressstrain curves of electrospun cellulose acetate-fullerenol nanofibrous membranes.
of semicrystalline polymers, indicates that three distinct phases consist of a crystalline fraction due to the inherent crystallinity of CA, the mobile amorphous fraction, the fraction of CA chains adhering to the dispersed fullerenols, the rigid amorphous fraction, and the fraction of CA which are at the outer skin of the electrospun nanofibrous membrane.26 This enhanced crystallinity and strong chemical interactions between the CA chains and hydroxyl moieties of fullerenols makes the membranes rigid and is reflected as substantial increase in mechanical properties of the membranes. The stressstrain curves of the electrospun membranes are shown in Figure 7. Pristine cellulose acetate fibers showed tensile strength of 1.6 MPa, whereas in 0.5 wt % fullerenol, the value increased to 2.75 MPa an increase of more than 75%. The magnitude of increase in tensile strength reflects the degree of chemical and physical interactions between the fullerenols and the cellulose acetate moieties, as extensively discussed in earlier sections. Fullerenol is a zero-dimensional nanosized filler whose size is lower than the length scale of the cellulose acetate polymer chain. So, some fullerenols may be physically entrapped in the free volume leading to labile bonding of cellulose acetate chains to the fullerenol surface, resulting in substantial increase in tensile strength. The increase in tensile strength is also accompanied by drastic reduction of elongation at break of nearly 100%, indicating that the addition of fullerenols increases the stiffness of the membranes. Figure 8 shows the DSC spectra of all the three membranes. Three distinct peaks, the glass transition (Tg), melting (Tm), and degradation (Td) temperatures of cellulose acetate are known to be around 190, 224, and 350 °C, respectively.27,28 The glass transition temperature of the electrospun pure CA membrane occurs around 182 °C, whereas, in 0.1 and 0.5 wt % fullerenol reinforced membranes, it is observed at 206 and 221 °C, respectively, an increase of 24 and 39 °C. The increase in Tg with the incorporation of fullerenols may be attributed qualitatively to the confinement of the polymer chain mobility as a result of strong fullerenepolymer interactions.29 A similar 2030 °C increase in melting temperature also indicates that the polymer chains in the immediate vicinity of the fullerenols are constrained exhibiting substantially reduced mobility of the polymer chains.30 Electromechanical actuation tests including step responses, harmonic responses, and currentvoltage tests were conducted
under deionized water. The tip displacements of the actuators actuated under deionized water were measured with a laser displacement sensor (LK031, Keyence) and a National Instruments data acquisition system (PXI 6252). The LabVIEW program was used with an industrial computer to acquire and control the data. Also, motion image was obtained with a general machine vision camera (Sony XC-HR50) with a resolution of 640 480 and frame rate of 60 frames/s. The harmonic responses of the tip displacement for three electrospun actuators responding to sinusoidal electrical inputs with excitation frequency of 0.1 and 0.2 Hz and the voltage amplitude of 3.0 V are shown in Figure 9a,b, respectively. In both cases, the tip displacement of the 0.5 wt % fullerenol-cellulose acetate actuator is three times larger than that of the pure cellulose acetate based actuator. Also, 0.5 wt % fullerenol-cellulose acetate actuator shows larger tip displacement than the 0.1 wt % fullerenolcellulose acetate actuator at all tested frequencies. Present results show that an improvement in the electromechanical bending actuation performance can be achieved by the addition of minute quantities of fullerenols. Natural biopolymers like wood, cellulose, and its derivatives like cellulose acetate are known to exhibit piezo-electric behavior due to their dipole structures.31 A combination of the following processes, orientation of permanent dipoles under applied electric current, polarization due to displacement of ions and charge injection from electrodes, are generally responsible for this phenomenon.32 In our case, though the applied voltage is low 3 V, piezoelectric behavior due to charge injection from gold electrodes seems to induce polarization. The orientation of dipoles can also be induced by drawing and stretching in wet cellulose as recently reported.33 Electrospinning is a variant of drawing in which an electrostatic force acts on the Taylor cone at the tip of needle which pulls the fibers from needle to collector. This force aligns the polymer chains along the length of fibers, which increases the orientation of dipoles to a preferable direction. Addition of fullerenol acts as nucleating agents for the formation of crystallites and increases the overall degree of crystallization, leading to increased dipoles in the nanofibrous nonwoven membranes. The other reason for the enhanced actuation in electrospun fullerenol-cellulose acetate membranes is due to increased ion conductivity of the membranes with the addition of fullerenols. The ionic conductivity of the membranes was tested by impedance analyzer and found to be 8.2 104 in pristine cellulose acetate and 11.47 104 and 18.12 104 S/cm in 0.1 and 0.5 wt % fullerenol samples, indicating more than 100% increase in value due to enhanced electron-hopping phenomenon.34 Another reason for 2051
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Figure 9. Harmonic (a and b) and step (c) responses of tip displacement of electrospun cellulose acetate actuators under wet condition; Digital photograph of the time responses (d).
Figure 10. Currentvoltage plots as a function of fullerenol concentration (a) and 0.5 wt % fullerenol reinforced cellulose acetate at increasing frequencies (b).
the enhanced bending actuation can be attributed to the electrostrictive behavior of fullerenols. Under the application of external electric field, the electrons are localized near the fullerenols, whereas the Liþ cations move toward the cathode thereby
increasing the actuation. Fullerenes are known for their excellent electron conducting property due to their small size, which allows a higher degree of solvated cation diffusion, induced by greater degree of differential swelling and 2052
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Figure 11. Biocompatibility tests in E. coli medium after 24 h incubation: (a) blank, (b) electrospun cellulose acetate membrane, and (c) electrospun fullerenol reinforced cellulose acetate membrane.
corresponding to much larger bending deformation. A similar result was reported in fullerene reinforced actuators.35,38 The DC induced tip-displacement of actuators shown in Figure 9c and also increase in displacement is achieved to the extent of 400%. Not only the degree of actuation but also the response time is also shortened by the addition of fullerenes shown by digital photographs in Figure 9d. In the case of pristine cellulose nanofibrous actuators, there is no actuation even until 60 s, whereas in 0.1 wt % fullerenol, actuation starts instantaneously and by 9 s attains maximum displacement. But at the highest concentration of fullerenols, the potential difference between the electrodes increases with addition of fullerenes, increasing the cation flux and bending of the tip. The fullerenol molecule is not “super aromatic” as it tends to avoid double bonds in the pentagonal rings, behaving like an electron-deficient alkene,36 and reacts readily with lithium ions forming metal-fullerene ion complexes that act as electron buffer.37 Capacitive hysteresis behavior was also studied to characterize the effect of fullerenes on power consumption and energy dissipation of the fullerenol-cellulose acetate actuators. Figure 10a shows the hysteresis behaviors of a electrospun cellulose acetate and 0.1 wt % and 0.5 wt % fullerenols reinforced nanoporous actuators in the range of 3 to þ3 V at a constant resistance of 1.3 Ω and the excitation frequency of 3.0 Hz. The maximum current density of the electrospun actuators increases up to three times in comparison with a pure CAbased actuator. Also, the elliptical area of hysteresis means the electrical input power, so-called power consumption. The fullerenol-cellulose acetate actuators show much lower power consumption in comparison with the pure cellulose acetate actuator. The elliptical area increases with the increase in the applied frequency, as shown in Figure 10b, and the maximum value of the measured current density is around 0.017 mA/mm2 at 3.0 Hz with 3.0 V amplitude. This increase in power consumption results in larger energy dissipation which results in much larger tip displacements. In this study, the biocompatibility of the electrospun nanoporous cellulose acetate membranes was tested in Escherichia coli K-12 bacteria cultures grown in LuriaBertani (LB) liquid medium at 37 °C. After 4 h of growth, E. coli, at a concentration of 106 cells/mL, was inoculated on the surface of MacConkey agar plates. Subsequently, the membranes with a diameter of 2 mm and weighing 0.47 g were placed on surface of each inoculated plate. The plates were incubated at 37 °C for 24 h and digital photographs are shown in Figure 11. Both electrospun nanofibrous pure cellulose acetate and fullerenol reinforced cellulose acetate membranes does not show any inhibitions of E.coli in agar plates, indicating good biocompatibility of the membranes.
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’ CONCLUSIONS In conclusion, we have developed novel electrospun cellulose acetate-fullerenol nanofibrous actuators. Morphology of the membranes showed porous structure mimicking extracellular matrix of natural muscles. Chemical interactions between the hydroxyl moieties of fullernols and carboxylate groups were observed from FTIR. XRD and DSC results indicate substantial increase in crystallinity and labile bonding of polymer chains to the fullerenol surface resulting in the formation of novel crystalline structures. Actuation results show more than a 3-fold increase in the tip displacement even at minute concentrations of fullernol under both DC and AC conditions. A combination of three factors, namely, increases in crystallization, piezoelectric effect of cellulose acetate, and electrostrictive behavior of fullernols, are responsible for the improved actuation performance. Present results show beneficial effects of minute concentrations of fullernols on structural and electroactive performance of cellulose acetate nanoporous biocompatible actuators. ’ ASSOCIATED CONTENT
bS
Supporting Information. Additional SEM micrographs and their size distribution. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*E-mail:
[email protected].
’ ACKNOWLEDGMENT This work was supported by Midcareer Researcher Program through a NRF grant funded by the MEST (Nos. 2010-0018423 and 2009-1459). Authors are thankful to Dr. G. Gnanasekaran of the Department of Chemistry, Chonnam National University, Gwangju, for his help in conducting biocompatibility tests. ’ REFERENCES (1) Shahinpoor, M.; Kim, K. J. Smart Mater. Struct. 2001, 10, 819–833. (2) Oguro, K.; Kawami, Y.; Takenaka, H. Trans. J. Micromech. Soc. 1992, 5, 27–30. (3) Abe, Y.; Mochizuki, A.; Kawashima, T.; Yamashita, S.; Asaka, K.; Oguro, K. Polym. Adv. Technol. 1998, 9, 520–526. (4) Wang, J.; Xu, C.; Taya, M.; Kuga, Y. J. Mater. Res. 2006, 21, 2018–2022. (5) Lu, J.; Kim, S. G.; Lee, S.; Oh, I. K. Adv. Funct. Mater. 2008, 18, 1290–1298. (6) Wang, X. L.; Oh, I. K.; Kim, J. B. Compos. Sci. Technol. 2009, 69, 2098–2101. (7) Wang, X. L.; Oh, I. K.; Lee, S. Sens. Actuators, B 2010, 150, 57–64. (8) Jeon, J. H.; Oh, I. K.; Kee, C. D.; Kim, S. J. Sens. Actuators, B 2010, 146, 307–313. (9) Kim, J.; Yun, S.; Ounaies, Z. Macromolecules 2006, 39, 4202–4206. (10) Wang, N.; Chen, Y.; Kim, J. Macromol. Mater. Eng. 2007, 292, 748–753. (11) Terasawa, N.; Takeuchi, I.; Mukai, K.; Asaka, K. Polymer 2010, 51, 3372–3376. (12) Formhals, A. U.S. Patent 1975504, 1934. (13) Suwantong, O.; Ruktanonchai, U.; Supaphol, P. J. Biomed. Mater. Res., Part A 2010, 94, 1216–1225. 2053
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