Conductive Hydrogels: Mechanically Robust Hybrids for Use as Biomaterials

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Conductive Hydrogels: Mechanically RobustHybrids for Use as Biomaterials

Rylie A. Green,* Rachelle T. Hassarati, Josef A. Goding, Sungchul Baek,Nigel H. Lovell, Penny J. Martens, Laura A. Poole-Warren

A hybrid system for producing conducting polymers within a doping hydrogel mesh ispresented. These conductive hydrogels demonstrate comparable electroactivity to conven-tional conducting polymers without requiring the need for mobile doping ions which aretypically used in literature. These hybrids have superior mech-anical stability and a modulus significantly closer to neuraltissue than materials which are commonly used for medicalelectrodes. Additionally they are shown to support the attach-ment and differentiation of neural like cells, with improvedinteraction when compared to homogeneous hydrogels. Thesystem provides flexibility such that biologic incorporation canbe tailored for application.

1. Introduction

With the advent of more sophisticated electronics, con-

ductive polymers (CPs)[1] have enormous potential for a

wide range of uses. CPs have significant promise inmedical

electrodeapplicationsdueto their lowimpedance,[2] butare

limited by their poor mechanical performance, charac-

terised by brittle failure[3] and poor cohesion,[4] which

results in material loss and delamination.[5] This research

presents a new hybrid CP system, termed a conductive

hydrogel (Figure 1), which is both mechanically stable and

retains the electrical property of the homogeneous CP.

For biomedical applications, it has been recognised that

incorporation of biological molecules into CPs, such as

laminin peptides and growth factors, enhances their

capacity to interact with cells and tissues. However, it is

clear from recent studies that the physical and mechanical

properties can be significantly altered after incorporation

Dr. R. A. Green, R. T. Hassarati, J. A. Goding, S. Baek, Prof. N. H. Lovell,Dr. P. J. Martens, Prof. L. A. Poole-WarrenGraduate School of Biomedical Engineering, University of NewSouth Wales, Sydney 2052, AustraliaE-mail: [email protected]

Macromol. Biosci. 2012, 12, 494–501

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of biological molecules.[6,7] Modulation of mechanical

properties may be achieved via alternate synthesis and

processing approaches,[8] through composite or nano-

composite approaches[9,10] or by blending or producing

layered CPs with other polymer types.[11–13] The latter

approach is the focus of this research as it provides a

means for not only improving mechanical properties, but

maintaining electrical properties and introducing capacity

for improved incorporation of biological molecules.

Several groups have focused on using a second polymer

that is softer and more elastic than the CP component to

form a hybrid CP. Typically, this second polymer has no

inherent conductivity. The key challenges in forming an

appropriate hybrid, is in combining the CP and non-CP

component to preserve the overall electroactivity while

imparting the desired mechanical softness and elasti-

city.[14] Although variants of silicone rubber,[15,16] poly-

urethanes,[17,18] polystyrenes[19–21] and polyvinyls[11] have

been explored, hydrogels present the most promising

option for producing hybrid CPs with physico-chemical

andmechanicalpropertieswhichcanbe tailored for specific

applications.[14,22–24]

library.com DOI: 10.1002/mabi.201100490

Figure 1. Schematic of ideal hybrid configuration (left) and photo comparison of hybridmaterial created from using a bound dopant, compared to stratified compositeproduced from using a free dopant (right). Both material samples are hydrated.

Conductive Hydrogels: Mechanically Robust Hybrids . . .

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Hydrogels are fabricated from hydrophilic polymer

chains via chemical or physical crosslinking processes that

convert the soluble polymer chains into insoluble, polymer

networks with a mesh-like structure.[14] The resulting

crosslinked network typically has a high water content

that has the advantage of being able to act as a ‘‘space’’ for

formation of the CP around the hydrogel backbone.

The mechanical properties of a hydrogel can be easily

controlled viamodification of the crosslink densitymaking

this material a versatile component for creating CP

hybrids.[25,26]

While several CP/hydrogel copolymers and composites

have been reported,[22,23,27–30] the synthetic approaches

used tend to result in a phase separated material in which

the CP forms within the hydrogel but is concentrated on or

near the electrode surface. A clear illustration of this is

demonstrated in recentwork by Sekine et al.[30] inwhichCP

was deposited within an agarose gel to form flexible moist

electrodes immediately adjacent to the electrode. The CP in

thesecasesappears tooccupyahydratedvolumewithin the

hydrogel with negligible integration.[31–34] The reason for

this poor integration between the CP and hydrogel is their

minimal interaction during electropolymerisation, the

dominant method used for producing composites. Fabrica-

tion approaches for CP/hydrogels typically uses a freely

mobile dopant for balancing the charge across the CP

backbone and maximising electrical conductivity.[28,31,35]

However, this method of fabrication encourages the CP

to move through the hydrogel toward the underlying

electrode where the free radicals are generated and

nucleation occurs. As a result, the oxidation potential for

polymerisation is lowest at the electrode surface. This not

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only encourages the CP to form on the

underlying substrate but also may result

in displacement of the hydrogel (as

shown in Figure 1, bottom).

To address themechanical shortfalls of

CPs while retaining overall electroactiv-

ity, a true hybrid or interpenetrating

network (IPN) of the component materi-

als is required. In short, the CP and

hydrogels must occupy the same space.

It is important to note that an IPN can

only be formed with two crosslinked

networks, and CPs are not considered

crosslinked, but rather linear polymers

which crosslink only when defects occur

during polymerisation.[36,37] Despite

efforts to control chain formation and

produce ideal CP chains without cross-

linking,[38,39] the electrochemical poly-

merisation of CPs is a minimally con-

trolled process that inevitably forms

polymers with defective couplings (a-b

or b-b couplings), which do in fact crosslink all CPs. This

defect crosslinking property creates a CP network that can

forman IPNwithothernetworks. In this studywedetail the

formation of an IPN by employing an anionic hydrogel

component to dope the CP component, and effectively form

a conducting hydrogel. This approach differs from those in

the literature as the material produced is not a stratified

composite or copolymer but rather a true hybrid, where

both component polymers occupy the same space as

depicted in Figure 1.

2. Experimental Section

2.1. Sample Preparation

Hybridmaterials were produced by photopolymerising a thin film

of 18wt% poly(vinyl alcohol) (PVA)/2wt% heparin methacrylate

(Hep-MA) or 30wt% Hep-MA using methods previously described

by Martens[26] on a platinum disc electrode which had been pre-

coated with poly(3,4-ethylenedioxythiophene) doped with para-

toluenesulfonate (PEDOT/pTS), then electrodepositing the PEDOT

throughout the hydrogel network.

The pre-coat was electropolymerised for 1min at 1mA � cm�2

from a 1:1 solution of deionised (DI) water and acetonitrile with

0.1M EDOT (Sigma-Aldrich, Aust) and 0.05M pTS (Sigma-Aldrich,

Aust). After crosslinking the hydrogel film with ultra-violet (UV)

light (70mW � cm�2, 366nm) for 180 s the disc was immersed in

water overnight to extract unreacted Hep-MA. PEDOT was then

polymerised through the gel by electrodeposition from a 0.01M

EDOT aqueous solution for 30min at 0.05mA � cm�2.

Control samples of PEDOTdopedwith either pTS or poly(styrene

sulfonate) (PSS) were produced by galvanostatic electrodeposition

from0.1MEDOTand0.05Mofdopant ina1:1solutionofacetonitrile

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R. A. Green et al.

and DI water. Films were fabricated to be of comparable thickness

(6mm) to hybrids by application of 2mA � cm�2 for 7.5min. All

samples were washed in DI water post-fabrication, air dried and

stored at room temperature prior to use.

2.2. X-Ray Photoelectron Spectroscopy (XPS)

XPS (Kratos XSAM800) results were used to analyse the chemistry

of hybrids. XPS peaks were analysed to determine the presence of

both the CP and doping hydrogel. Multiple measurements were

made across the film in linear tests to determine the presence of

non-uniformities. Spectra were analysed using the peak fitting

functions to allow calculation of the area beneath the curve

obtained from the raw data. Four linear spectra were analysed in

three different sectors of the film.

2.3. Scanning Electron Microscopy (SEM)

SEMwas performed on air-dried samples in a JEOL bench-top SEM

(Coherent Scientific Aust) under vacuum with an accelerating

potential of 15 kV. Images were captured at 1000� and 3000�magnification.

2.4. Electrical Conductivity

Direct conductivity measurements were made by attaching

planar electrodes to the upper and lower surface of the samples

in the dry state. DC currentwas applied at 50, 100, 500 and1000mA

using an eDAQ galvanostat (eDAQ Pty Ltd., Australia). Voltage

between the plates was used to calculate conductivity. Three

samples were tested for each material type and reported with

standard deviation.

2.5. Cyclic Voltammetry (CV)

CV was performed on an eDAQ potentiostat and eCorder unit

(eDAQ Pty Ltd., Australia). The cycling voltage chosen was�700 to

þ700mV to prevent hydrolysis of the electrolyte solution by

remaining within the water window. Cycling was performed at

120mV � s�1 for 850 continuous cycles in 0.9% saline. Recordings

were made via an isolated Ag/AgCl reference electrode with a

Pt counter electrode. The charge storage capacity (CSC) was

determined by integration of the current (I) response with respect

to the time base, and results were presented as themean total CSC

versus cycle number with standard deviation for six repeats.

2.6. Impedance Spectroscopy

Impedance response of hybrids was assessed by application of

small amplitude sinusoids (30mV) across the frequency range of

0.1Hz–1MHz using an impedance spectrometer (InPhaze Pty. Ltd.,

Sydney, Australia). The average of three full scans (a full scan

consists of both a forward and backward scan to eliminate

hysteresis) was taken for each of three samples. The mean

impedance magnitude and phase angle were plotted for each

material type with standard deviation.

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2.7. Peak-Force Nanomechanical Mapping

Mechanical stiffness of the hybrids was analysed by peak-force

nanomechanical mapping (PF-QNM) using an atomic force

microscope (Bruker, MM8 AFM) to attain data on the force-

deformation response. Scans were taken at 1Hz across 25mm2

sectionsof10mmdiameterdiscs. Threescansweretakenoneachof

three samples for all material types. The mean Derjaguin–Muller–

Toporov (DMT) modelled of 512 data points per line was recorded

and presented with standard deviation.

2.8. Adhesion Testing

The ASTM tape adhesion test[26] was performed using modified

parameters to account for small areas of films. Testing was carried

out with low-medium adhesion Scotch 3M Blue masking tape for

delicate surfaces (3M2080). Two incisionsweremade inanXacross

the film, exposing the substrate. Tape was placed over each X and

left for 5min before removal as described by ASTM D3359.[26]

NIH software Image J was used to calculate loss of coating. Six

independently prepared sampleswere prepared and analysed. The

results are presented as the mean with standard deviation.

2.9. Neural Cell Culture

PC12 cells were cultured in RPMI-1640 cell growth media

supplemented with 1% horse serum on substrates coated with

5mg �mL�1 laminin (from murine engelbreth sarcoma, L2020,

Sigma-Aldrich, Australia). Cells were plated at 20 000 cells � cm�2

and nerve growth factor (NGF 2.5S, Jomar, Israel) was used to

stimulate neurite outgrowth at 50ng �mL�1. Cells were fed with

the nerve growth factor (NGF) supplementedmedia at 48h and the

experimentwas analysedat 96hpost-plating. NIH software Image

J with the Neuron J plug-in was used to measure neurite length.

ANOVA with student t-test was used to determine the statistical

significance of material responses.

3. Results and Discussion

In this hybrid material the hydrogel component not only

provides covalently bound anions to dope the CP, but also

sites of lower oxidation potential throughout the hydrogel

for the nucleation of CP growth during fabrication. These

areas provide a localised low energy state for the formation

of the CP by balancing the charge across the inherently

unstable CP backbone as the chain length increases and the

CP precipitates out of the monomer solution within the

hydrogel space. In short, the dopants distributed through-

out the hydrogel will guide the CP backbone formation

within the hydrogel space.

Twohydrogel variantswere used for this study, one a co-

polymer of 18% PVA with a 2% HepMA component

crosslinked into the polymer mesh, and one a 30% HepMA

homogeneous hydrogel. The HepMA bound into the

hydrogel structure provides a covalently bound dopant

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0

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824

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Coun

ts

Binding Energy (eV)

PVA-HepMA PEDOT/PVA-HepMA

Element eV PVA-HepMA

PEDOT/PVA-HepMA

30HepMA

PEDOT/ 30HepMA

S2p3 A 163.84 - 4.27 1.91 3.71

S2p3 B 168.07 0.21 1.51 4.71 3.00

Figure 2. XPS spectra and sulfur peak analysis for homogeneoushydrogel compared to hybrid with PEDOT deposited through theanionic hydrogel. The resulting hybrid hydrogel has a spectraconsistent with both components, demonstrated through thepresence of the sulfur peak at 163.8 eV, which is the aromaticallybound S in the EDOT monomer.

Figure 3. SEM of typical surface topography obtained for the hybrid cgel, with (A) PEDOT/PVA-HepMA; (B) PEDOT/30HepMA and (C) PEDOcross-section; compared to (D) conventional PEDOT/pTS. Images are tB, D) and 3000� (C) magnification.





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via its highly sulfated backbone. In this case we demon-

strate the electrodeposition of PEDOT through the hydrogel

mesh. The result is a PEDOT/hydrogel hybrid which has

been confirmed by XPS. The spectral wide signal in Figure 2

shows that hybrids produced with the CP polymerised

through the hydrogel have sulfur peaks consistentwith the

formation of PEDOT.

In the accompanying table of Figure 2 the sulfur peak at

163.8 eV is specific to the EDOT monomer units which

comprise theCP component.[6] The sulfurpeakat168.1 eV is

consistent with sulfonate ions which are found in the

dopingheparinunits covalently boundwithin thehydrogel

component.[40] Similar analysis for the hybrids formed

within 30% HepMA hydrogels also exhibited shifts in the

sulfur peaks consistent with PEDOT formation, but

quantification is less specific due to the presence of excess

heparin molecules which form not only the doping

component but also the bulk hydrogel mesh.

Hybrid materials have a distinctive surface morphology

in comparison to conventional CPs as shown in Figure 3.

Both hybrids have larger, but more uniform nodular

aggregations than the homogeneous PEDOT which has a

flatter appearance, with outcrops of non-uniform surface

features. An additional image of the hybrid in cross-section

(Figure3C) shows that thePEDOThasdeposited throughout

the hydrogel to create an integrated material. This is a

onducting hydro-T/PVA-HepMA inaken at 1000� (A,

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significant improvement on interpene-

tration compared to other composite

hydrogel/CP materials pictured in the

literature,[41–43] which are accurately

described as ‘‘semi-interpenetrating’’.[41]

Direct conductivity in the dry state

was used to confirm that PEDOT was

distributed throughout the hydrogel and

produced an electrically active path from

the material surface to the underlying Pt

substrate. The conventional PEDOT/pTS

was shown to have a conductivity of

1.4� 0.3 S � cm�1, which was not signifi-

cantly different to PEDOT/PVA-HepMA

which had a conductivity of 1.1� 0.2

S � cm�1. As a control the hydrogel PVA-

HepMA, without PEDOT deposited

throughout was shown to have only

minor conductivity of 0.1� 0.01 S � cm�1,

thought to be primarily due to the

proximity of the Pt electrodes (25mm)

and the underlying PEDOT/pTS pre-coat

layer. In literatureCPshavebeenreported

to have a conductivity ranging from

14 to 150 S � cm�1.[9] Although these

values are lower than other reported CP

conductivities, this is likely to be the

result of the testing set up. Typically a

im497

Figure 4. Characterisation of hybrid conductive hydrogels: (A) CSC of hybrids calculated from CV performed versus Ag/AgCl at 120mV � s�1

from �700 to þ700mV over 850 cycles; (B) electrochemical frequency dependent impedance data, showing reduction in impedance andphase lag generated from hybrid coating; (C) elastic moduli (calculated from DMT model) under hydrated conditions, compared to Pt,homogeneous CPs and neural tissue (latter value is published by Lippert and Grimm [50]); (D) PC12 cell density and neurite outgrowth areshown with standard deviation (N¼ 3, � p<0.05).

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four-point probe is required which penetrates the material

surface or contacts across a small defined point; however,

in this study surface electrodes were required. Imperfect

contact between the planar electrodes of 10mm diameter

and the roughened polymeric materials will result in

increasedresistancewherecontact isnotmaintainedacross

the entire area. The results clearly show that a conductive

path has been formed by the PEDOT when deposited

throughout thehydrogelmaterial fromtheupper surface to

underlying electrode.

The CSC measured by means of CV in Figure 4A,

demonstrates that the crosslinking of anionic HepMA

within the PVA hydrogel was successful in introducing

doping ions to the hybrid system. This is shownby a sixfold

increase in CSC at Cycle 1 from 2.4 mC (12.2 mC � cm�2) for

the undoped PEDOT/PVA (thought to be primarily due to

the underlying pre-coat) to 13.4 mC (68.4 mC � cm�2) for

the doped PEDOT/PVA-HepMA. The covalently bound 2%

HepMAwithin the PVA co-polymer hydrogel does not dope

the PEDOT as fully as the conventional sulfonate ion, pTS.

The 30% HepMA hydrogels were created in an attempt to

impart better doping andagreater charge carrying capacity

to the hybrid system. The CSC determined from CV

indicated that the highly anionic homogeneous heparin

hydrogelprovidedbetterdoping, increasing thefinalCSCby



37% from 46 up to 73 mC � cm�2. This charge transfer

capacity is similar to PEDOT films in the literature which

have been functionalised with the highly ballistic carbon

nanotubes.[44] The continual cycling demonstrates that the

hybrid CP hydrogels were able to maintain their electro-

activity across this extended period (850 repetitions) of

oxidation and reduction cycling with improved stability

compared to PEDOT/pTS controls. The PEDOT/pTS under-

went a loss of 49% from the original electroactivity

(established from the CSC at Cycle 1) compared to a loss

of only 28% for both hybrid variants. This is due to the

HepMA ions being covalently bound within the hybrid

system, preventing their diffusion away from the electrode

interface during cycling. Despite the charge carrying

capacity of these materials being significantly reduced

compared to the PEDOT/pTS, it is important to note that the

hybrids still have a CSC with an order of magnitude higher

than Pt, and comparable to values reported in the literature

for many other CP variants.[45,46]

The average impedance magnitude of the hybrids was

slightlybutnot significantlyhigher than that of PEDOT/pTS

(see Figure 4B), the most commonly investigated CP.

However, the effect of the increased surface area provided

by the PEDOT component was evidenced by the lower

impedance magnitude and smaller phase angle of the

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hybrids than that of thePt at lowfrequency. The impedance

for the undoped PEDOT/PVA control was significantly

higher than that of both the PEDOT/PVA-HepMA and

PEDOT/30HepMA, concurring with the findings of the CV.

In the biologically significant frequency range for both

neural stimulation and recording of neural activity, 10–

1000Hz,[47,48] the hybrids were able to decrease the

impedance of the Pt electrodes (diameter 5mm) from 500

to 75V and decrease phase lag from 70 to 78 (example

values taken at 100Hz, a common stimulation frequency

for neuroprostheses).

Mechanically the hybrids have a significantly reduced

stiffness compared to conventional PEDOT as measured by

hydrated atomic force microscopy (AFM) with PF-QNM.

Values are presented in Figure 4C for both of the hybrid

conductive hydrogels, two conventional PEDOT variants,

PEDOT/pTS and PEDOT/PSS, and Pt. A literature value for

cortical neural tissue is also included for comparison. No

significant difference was observed in the elastic modulus

between samples of the same class, that is, both homo-

geneous hydrogels had a similar modulus of �0.5 kPa,

compared to both homogeneous CPs, which had amodulus

of around 40MPa. Similarly the hybridswhichwere tested,

PEDOT/PVA-HepMA and PEDOT/30HepMA, demonstrated

a modulus close to 2MPa, significantly lower than the CP

modulus and two orders of magnitude lower than the

Pt. It is clear that the hydrogel component imparts the

required mechanical softness and elasticity required

to dampen the effects of the metallic electrodes. This

reduction in interface stiffness should improve interactions

at the implant interface by reducing damage to neural

tissue.[49]

Adhesion of both CPs and hydrogels can be problematic,

and it is absolutely necessary that coatings on implantable

materials remain intact in the long-term. As such the

hybrid system employs a pre-coat layer, designed to

increase interactions between the hybrid material and

the underlying substrate. A thin film of the PEDOT doped

with pTS,which is known to have good adherence to Ptwas

used for the pre-coat.[7] By fabricating the hybrid with a

very thin pre-layer the PEDOT deposited through the

hydrogel matrix will integrate with the initial PEDOT/pTS

and bond the hybrid to the underlying metallic substrate.

When sampleswere producedwithout this pre-layer a 24h

soak in DI water caused the hybrid to delaminate.

To quantify the adhesive behaviour of the conducting

hydrogel an ASTM defined x-cut test was carried out. The

fully fabricated hybridwas tested in comparison to PEDOT/

pTS, which is known to have good adherence, but can be

brittle and non-cohesive, resulting a limited usable life-

time.[7,51] This is one of the CPmechanical issues which the

hybrid system was designed to address.[14] The x-cut test

was able to confirm that not only was the pre-layer

successful in adhering the hybrid to the underlying




substrate, but the hydrogel component was also able to

decrease the loss of bulk material from the upper surface.

The totalmaterial loss for thehybrids, PEDOT/PVA-Hepwas

1.5� 0.5% and the PEDOT/30Hepwas 2.1� 0.5%, compared

to the PEDOT/pTS which lost 16.0� 7.1% of its bulk

material.

As a potential material for neural prosthetic and other

implant applications, the hybrid system must also have

suitable interactions with neural tissue. In vitro studies

using the model neural clone PC12 cell line have yielded

positive results which demonstrate the hydrogels are

compatible with biological tissues. PC12 cells were chosen

as a neural model which not only differentiates when

exposed toNGF,but thedegreeof cell adherenceandneurite

outgrowth is known to be strongly influenced by physico-

mechanical cues and surface chemistry.[2,6,7]

Cell density was comparable to PEDOT/PSS, one of the

most commonly implanted synthetic CPs which has been

shown to be biocompatible,[52,53] but neurite growth was

halved. It is expected that this is a result of reduced cell

interaction with the substrate. The cells were observed to

have a more rounded appearance with finer neurites,

indicating a lower communication with the material. This

reduced interaction property is thought to be due to the

lower fouling and protein interactions commonly experi-

enced by hydrogels,[54,55] and also responsible for the poor

cell response on the homogeneous PVA-Hep hydrogel.

However, as demonstrated in Figure 4D, the cell growth

response on the hybrid PEDOT/PVA-Hep was significantly

improved compared to both Pt and the homogeneous gel

PVA-Hep, indicating that the CP component has improved

cell interactions.

The hydrogel chosen for these hybrids is biosynthetic.

The synthetic component, PVA, provides robust, tunable

mechanical properties,[25] but the biological component

provides not only anionic tails for doping the CP, but also

sequences with bioactivity. This hybrid system has been

designed such that the biological component can be

appropriately substituted to give specific cell interactions

for a given application. Although this functionality is still

under investigation, it is believed that cell interactions can

be significantly improved through the addition of peptide

sequences or other bioactive factors which have been

shown to have neural cell attachment and growth

activity.[6,7,56,57]

4. Conclusion

In summary, we have developed a conducting hydrogel by

hybridising the conducting polymer PEDOT with anionic

hydrogels. Two hydrogel variants were explored, the

biosynthetic 18wt% PVA/2wt% heparin and a pure

30wt% heparin hydrogel. It was shown that the hybrid

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material produced addresses the problem of poor

mechanics seen in conventional CPs while retaining

superior electroactivity compared to metal electrodes. This

class of materials has been termed conducting hydrogels

and has potential application not only in medical electro-

des, but also in nerve guides, wound healing products, drug

delivery and gene therapies.

Acknowledgements: The authors acknowledge funding fromUniversity of New South Wales, Silver Star grant scheme,PS24596 and New South Innovations Proof of Concept funding,L002317. The authors would like to thank Naomi Staples forproducing the conceptual artwork.

Received: November 30, 2011; Revised: December 15, 2011;Published online: February 17, 2012; DOI: 10.1002/mabi.201100490

Keywords: conducting polymers; hybrids; hydrogels; mechanicalproperties

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