DOI: 10.1002/adma.

200800757
Mechanically Strong, Electrically Conductive, and
Biocompatible Graphene Paper**
By Haiqun Chen, Marc B. Mu ller, Kerry J. Gilmore, Gordon G. Wallace,
*
and Dan Li*
Research on graphene was originally motivated by its
peculiar electrical transport properties and the promise of
future applications in nanoelectronics.
[1,2]
Graphene sheets,
owing to their exceptional thermal and mechanical properties
and high electrical conductivity, are also of great interest to
serve as new nanoscale building blocks to create unique
macroscopic materials.
[35]
Recent studies have shown that
graphene sheets can be prepared in large quantity through
chemical conversion from graphite,
[612]
which has facilitated
the fabrication of graphene-based electronic devices
[13,14]
and
has also made it possible to create new bulk materials
comprising graphene sheets for a broader range of applica-
tions.
[35,15,16]
For example, it has been recently demonstrated
that chemically modied graphene sheets can be dispersed
throughout a polymeric
[3]
or inorganic matrix
[15]
to make
electrically conducting composites with a percolation threshold
as low as 0.1 vol %. Thin graphene lms have also been used as
potential transparent electrodes for solar cells.
[16]
More
recently, Ruoff and co-workers have demonstrated that graph-
ene oxide (GO) sheets dispersed in water can be assembled into
a well-ordered structure under a directional ow, yielding
ultrastrong GO paper.
[4]
GO paper is superior to many other
paperlike materials in stiffness and strength, however, a lack of
electrical conductivity limits its use. Although GO paper can
be rendered conductive by thermal annealing, the structure
and mechanical properties seriously deteriorate after this
treatment (see below for further discussion).
We have recently demonstrated that aqueous dispersions of
graphene sheets can be readily produced without the need for
polymeric or surfactant stabilizers.
[12]
This has enabled us to
prepare electrically conductive graphene paper directly, using
the same strategy that has been used to make carbon nanotube
buckypaper and GO papers.
[4,17,18]
Here, we demonstrate that
the resulting graphene paper displays a remarkable combina-
tion of thermal, mechanical, and electrical properties, whilst
preliminary cytotoxicity tests suggest biocompatibility, making
this new material attractive for many potential applications.
Graphene dispersions were prepared by controlled reduc-
tion of GO dispersions with hydrazine using the procedure
reported in one of our recent publications.
[12]
Graphene paper
was then fabricated by ltration of a measured amount of
graphene dispersion through an Anodisc membrane lter,
followed by air drying and peeling from the lter. The samples
of graphene paper were annealed at different temperatures
before being cooled to room temperature for various
measurements (see the Experimental section for details).
We observe that as-prepared graphene paper displays a
shiny metallic luster on both sides (Fig. 1A). Scanning electron
microscopy (SEM) analysis reveals that the surface of the
graphene paper is quite smooth (Fig. 1B) and the fracture
edges of the papers exhibit a layered structure through the
entire cross-section (Fig. 1C and D), which looks similar to the
microstructure obtained for GO paper prepared using the
same method.
[4]
These results indicate that, similar to
hydrophilic GO sheets,
[4]
chemically reduced graphene sheets
can also be assembled to form highly ordered macroscopic
structures under vacuum ltration-induced directional ow.
The thickness of the graphene paper can be varied from tens of
nanometers to around 10 mm by adjusting the volume of the
colloidal dispersion. Nevertheless, only stable and agglomer-
ate-free graphene colloids can produce uniform, smooth, and
shiny paper. In contrast to GOpaper,
[4]
graphene paper cannot
be redispersed into water by ultrasonication, exhibiting an
excellent water-resistance behavior.
Another remarkable property of graphene paper is its high
thermal stability, especially when compared with GO using
thermogravimetric analysis (TGA) (Fig. 2A). The mass loss
below 200 8C can be attributed to the evaporation of adsorbed
water. A slight mass loss appears between 200 and 500 8C,
presumably owing to the decomposition of some residual
oxygen-containing groups. In contrast to GO paper (Fig. S1A
of the Supporting Information), there is no sharp weight loss at
around 200 8C for graphene paper, indicating that most
oxygen-containing groups have been removed by the hydra-
zine reduction. The total weight loss (<10%) of graphene
paper between 200 and 500 8C is much lower than that of GO
paper (ca. 30% loss, as shown in Figure S1A of the Supporting
Information). When graphene paper is annealed between 200
C
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[*] Dr. D. Li, Prof. G. G. Wallace, Dr. H. Chen, M. B. Muller,
Dr. K. J. Gilmore
ARC Centre of Excellence for Electromaterials Science
Intelligent Polymer Research Institute
University of Wollongong
Northfields Avenue, Wollongong, NSW 2522 (Australia)
E-mail: gwallace@uow.edu.au; danli@uow.edu.au
Dr. H. Chen
Department of Safety and Environment Engineering
Jiangsu Polytechnic University
Changzhou 213016 (PR China)
[**] D.L. and G.G.W. acknowledge the support from the Australian
Research Council. H.C. acknowledges the support from the Jiangsu
Province Studying-Abroad Foundation. Supporting Information is
available online from Wiley InterScience or from the authors.
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and 500 8C, the mechanical integrity of the paper as well as the
physical appearance (smooth shiny surface) are retained. In
fact, the lustrous appearance is enhanced by thermal annealing.
In contrast, when GO paper is treated above 200 8C, the paper
becomes crumpled (Fig. S1B and C of Supporting Informa-
tion), presumably as a result of vigorous gas release caused by
thermal decomposition.
[6]
These results clearly indicate that
paper composed of chemically reduced graphene is much more
thermally stable than unreduced GO paper.
We have further studied the effect of thermal annealing on
the microstructural ordering of graphene sheets in the resulting
paper using X-ray diffraction. As shown in Figure 2B,
as-ltrated graphene paper, when dried at room temperature,
displays a weak and broad X-ray diffraction peak at around
238, corresponding to a layer-to-layer distance (d-spacing) of
about 0.387 nm. As the annealing temperature is increased, the
peak at around 238 becomes more pronounced and sharper.
The d-spacing is slightly reduced, approaching 0.341 nm when
treated at 500 8C. The XRD results clearly indicate that
thermal annealing enables a better ordering of the two-
dimensional sheets. Note that the d-spacing of the resulting
graphene paper is slightly greater than,
but quite close to, that of graphene layers
in pristine natural graphite, indicating that
chemically prepared graphene sheets are
similar to the pristine sheets. The slightly
increased d-spacing of chemically pre-
pared graphene paper can be ascribed to
the presence of a small amount of residual
oxygen-containing functional groups or
other structural defects.
As a consequence of better ordering
and additional deoxygenation by thermal
annealing, the electrical conductivity of
graphene paper is found to increase with
treatment temperature (Fig. 2C). It is
noteworthy that although GO can be con-
verted to conductive graphene by thermal
deoxygenation, the electrical conductivity
of thermally treated GO paper is found to
be lower than that of our graphene paper,
most likely owing to the disrupted struc-
ture of heat-treated GO (Fig. S1C and D
of the Supporting Information). For
example, the conductivity of GO paper
heat-treated at 220 and 500 8C is around
0.8 and 59 S cm
1
, respectively, while the
graphene paper treated at the same
temperatures exhibits a conductivity of
118 and 351 Scm
1
, respectively. The
conductivity of the graphene paper sam-
ple treated at 500 8C is an order of
magnitude higher than that reported for
compressed pristine graphite powder,
again indicative of a strong intersheet
interaction in the graphene paper.
[6]
Similar to GO prepared using the same method,
[4]
graphene
paper is supposed to be formed by stacking and interlocking of
individual sheets under a ltration-induced directional ow.
Given that individual graphene sheets are predicted to have a
tensile modulus of up to 1.01 TPa
[9]
and the sheets are
well-packed in graphene paper, we surmised that similar to GO
paper, graphene paper should have excellent mechanical
properties. Mechanical analysis of the graphene paper reveals
that the stiffness and tensile strength are comparable to or, if
properly annealed, higher than those of GO paper. Figure 3A
presents typical stressstrain curves of graphene paper
annealed at various temperatures. The results obtained using
the samples dried at room temperature show an elastic and a
plastic deformation region as well as an initial straightening
region similar to those observed for GO paper.
[4]
When the
samples are annealed at temperatures above 100 8C, the plastic
deformation is difcult to observe (Fig. 3A). The stiffness and
strength of graphene paper samples are found to be dependent
on the thermal annealing temperature used. As shown in
Figure 2B and C, both stiffness and strength increase with
increasing annealing temperature up to about 220 8C. The
Figure 1. A) Photograph of two pieces of free-standing graphene paper fabricated by vacuum
ltration of chemically prepared graphene dispersions, followed by air drying and peeling off the
membrane. Front and back surfaces shown. B) Top-view SEM image of a graphene paper sample
showing the smooth surface. C,D) Side-view SEM images of a ca. 6 mm thick sample at increasing
magnication.
3558 www.advmat.de 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim Adv. Mater. 2008, 20, 35573561
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enhancement of mechanical properties is attributed to the
better ordering of graphene stacks brought about by thermal
annealing, which results in enhanced interlayer contact and
interactions of graphene sheets. This is consistent with the
XRD and electrical conductivity measurement results. The
sample annealed at 220 8C yields the greatest mean Youngs
modulus at 41.8 GPa, and the greatest mean tensile strength at
293.3 MPa. Although the values are still much lower than those
of individual sheets (likely owing to the weaker bonding
between sheets), they are both higher than those of GO paper
and over 10 times higher than the corresponding values for
exible graphite foils.
[4,19,20]
To our knowledge, these values
are the highest yet reported for electrically conducting
carbon-based paperlike materials. When the heat treatment
is performed at temperatures above 220 8C, the graphene paper
becomes more brittle and the measured stiffness and strength
tend to decrease with annealing temperature. Further studies
are required to understand this phenomenon.
Note that for GO paper samples, the mechanical properties
are comparable to those of graphene paper when thermally
annealed below 150 8C. However, both stiffness and strength
Figure 2. A) Normalized remaining mass of graphene paper as a function
of temperature in air and argon gas, respectively. B) XRD patterns of
graphene paper samples that have been heat treated at various tempera-
tures. For comparison, the XRD pattern of the pristine graphite powder is
included. All the XRD patterns were recorded at room temperature.
C) Room-temperature electrical conductivity of graphene samples that
have been thermally annealed at various temperatures.
Figure 3. A) Typical stressstrain curves, B) Youngs modulus, and
C) tensile strength of graphene paper strips that have been heat-treated
at various temperatures. The mechanical properties of GO paper are also
presented in (B) and (C) for comparison. The data shown in (B) and (C) are
averages of six measurements.
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are signicantly reduced when treated at 220 8C(Fig. 2Band C)
as a sequence of structural destruction caused by thermal
decomposition (Fig. S1 of the Supporting Information).
Carbon materials have proven to be promising for
biomedical applications such as tissue engineering and
implants, in part because of their inherent biocompatibil-
ity.
[2126]
To our knowledge, there have been no reports
regarding the biocompatibility of chemically prepared gra-
phene-based materials. Graphene paper offers an ideal
platform for cell culture experiments owing to the ease of
handling. Initial biocompatibility assessment of the graphene
papers was addressed by culture of the mouse broblast cell
line (L-929), which is commonly used to assess cytotoxicity of
potential substrates for cell growth, and has been used
previously in biocompatibility testing of carbon nanotubes.
[25]
L-929 cells were found to adhere to and proliferate on the
graphene papers, such that by 48 h of culture time a
subconuent layer of metabolically active cells could be
visualized (Fig. 4). The doubling time for the cells was the same
on graphene papers as on commercial polystyrene tissue
culture plastic (data not shown), indicating normal prolifera-
tion rates on these materials. Thus, graphene paper provides a
good substrate for the adhesion and proliferation of L-929
cells, suggesting that chemically prepared graphene may be a
biocompatible material.
In summary, we have demonstrated that highly ordered
graphene paper can be prepared by directional ow-induced
assembly of graphene sheets that are well dispersed in solution.
Moderate thermal annealing can enhance its mechanical
stiffness and strength as well as electrical conductivity. We
have also presented the results of cell culture experiments,
which indicate that graphene paper may be biocompatible and
therefore suitable for biomedical applications. The combina-
tion of the exceptional mechanical strength, thermal stability,
high electrical conductivity, and biocompatibility makes
graphene paper a promising material for many technological
applications, from electrodes for exible batteries to biome-
dical applications, such as inclusion in heart valves.
Experimental
Fabrication of Graphene Paper: Graphene paper was fabricated by
vacuum ltration of graphene dispersions. In a typical procedure,
graphite oxide was synthesized from natural graphite powder (SP-1,
Bay Carbon, Bay City, MI, USA) using a modied Hummers method
[27, 28]. After being puried by ltration and subsequent dialysis or by
several runs of centrifugation/washing, graphite oxide was exfoliated
into water by ultrasonication for 30 min using a Branson Digital
Sonier (S450D, 500 W, 30% amplitude). The obtained GO was
diluted to 0.25 mg mL
1
. With the pH of the dispersion adjusted to 10
using ammonia and the solution surface covered with a thin layer of
mineral oil, the dispersion was then subjected to reduction by
hydrazine at ca. 95 8C for 1 h. Graphene paper was prepared by
ltration of a measured amount of the resulting colloid through an
Anodisc membrane lter (47 mm in diameter, 0.2 mm pore size,
Whatman), followed by air drying and peeling from the lter. Unless
specically stated, graphene paper with a thickness of around 6 mm was
used for all measurements reported in this work. These samples of
graphene paper were annealed at different temperatures in air
(<220 8C) or argon (>220 8C) for 1 h before being cooled to room
temperature for various measurements. For comparison, GO paper was
also prepared, using a similar ltration method, as reported in Ref. [4].
Structural and Properties Characterization: The thermal properties
of the graphene papers were characterized by TGA (Q500, TA
Instruments). All measurements were conducted under air or nitrogen
gas at a owrate of 40 mLmin
1
over a temperature range of 30800 8C
with a ramp rate of 5 8Cmin
1
. The XRD patterns of graphene paper
samples annealed at different temperatures were recorded on an
Australia GBC Scientic X-ray diffractometer (40 kV, 20 mA, Cu Ka
radiation, l 1.5418 A

) at room temperature. Static uniaxial in-plane

tensile tests were conducted with a dynamic mechanical analyzer
(DMA Q800, TA Instruments). The samples were cut with a razor into
rectangular strips of approximately 3 15 mm
2
for mechanical testing
and were gripped using a lmtension clamp with a clamp compliance of
about 0.2 mmN
1
. All tensile tests were conducted in controlled strain
rate mode with a preload of 0.01 N and a strain ramp rate of
0.05%min
1
. Conductivity measurements were carried out on a Jandel
RM3 Conductivity Meter using a four-point probe head. SEM images
were obtained using a Hitachi S-900 eld-emission scanning electron
microscope operated at an accelerating voltage of 4 kV.
Biocompatibility Test: Graphene paper that was thermally annealed
at 1008C was screened for biocompatibility by monitoring the growth of
L-929 (mouse broblast) cells. The graphene paper samples were placed
into wells of a 96-well polystyrene cell culture plate and soaked overnight
in two changes of culture media, then rinsed with water to remove soluble
impurities. The samples were sterilized by rinsing with 70% ethanol,
followed by air-drying and placing under UV light for 20min. Samples
were seeded with 510
3
L-929 mouse broblast cells per well, and
cultured in DMEM/F12 media supplemented with 5% FBS for 48 h.
Finally the cells were stained with Calcein AM, which is cleaved to yield
a green uorescent product by metabolically active cells. Images were
obtained using a Leica DMIL inverted uorescence microscope
equipped with a Leica DC500 camera.
Received: March 18, 2008
Revised: May 14, 2008
Published online: July 23, 2008
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