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Role of surface-electrical properties on the cell-viability of carbon thin films grown in

nanodomain morphology

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2016 J. Phys. D: Appl. Phys. 49 264001
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Journal of Physics D: Applied Physics

J. Phys. D: Appl. Phys. 49 (2016) 264001 (7pp)

doi:10.1088/0022-3727/49/26/264001

Role of surface-electrical properties on the

cell-viability of carbon thin films grown
in nanodomain morphology
AmjedJavid1,2, ManishKumar1, SeokyoungYoon3, JungHeonLee4,
SatomiTajima5, MasaruHori5 and JeonGeonHan1
1

Center for Advanced Plasma Surface Technology (CAPST), NU-SKKU Joint Institute for Plasma
Nano-Materials (IPNM), Advanced Materials Science and Engineering, Sungkyunkwan University,
Suwon 440-746, Korea
2
Department of Textile Processing, National Textile University, Faisalabad 37610, Pakistan
3
SKKU Advanced Institute of Nanotechnology (SAINT), Sungkyunkwan University, Suwon 440-746,
Korea
4
Biological & Nanoscale Materials Lab, Advanced Materials Science and Engineering, Sungkyunkwan
University, Suwon 440-746, Korea
5
Plasma Nanotechnology Research Center, Nagoya University, Furo-cho, Chikusa-ku 464-8603, Japan
E-mail: manishk@skku.edu and hanjg@skku.edu
Received 8 February 2016, revised 8 April 2016
Accepted for publication 14 April 2016
Published 31 May 2016
Abstract

Carbon thin films, having a combination of unique physical and chemical properties, exhibit
an interesting biocompatibility and biological response to living entities. Here, the carbon
films are developed in the morphology form of nano-domains with nanoscale inter-domain
separations, tuned by plasma conditions in the facing target magnetron sputtering process.
The wettability and surface energy are found to have a close relation to the inter-domain
separations. The chemical structure of carbon films exhibited the relative enhancement of sp3
in comparison to sp2 with the increase of domain separations. The cell-viability of these
films shows promising results for L929 mouse fibroblast and Saos-2 bone cells, when
inter-domain separation is increased. Electrical conductivity and surface energy are identified
to play the key role in different time-scales during the cell-proliferation process. The
contribution from electrical conductivity is dominant in the beginning of the cultivation,
whereas with the passage of time (~35 d) the surface energy takes control over conductivity
to enhance the cell proliferation.
Keywords: carbon films, cell viability, surface energy, photoelectron spectroscopy,
conductivity
(Some figuresmay appear in colour only in the online journal)

1.Introduction

tissue regeneration and implant coatings [57]. Recently,

ultra-light weight graphite is reported for potential application in electrodes and supercapacitors [8]. The quantum dots
of carbon and graphene exhibit interesting applications in the
area of biology, optoelectronics and energy materials [9]. The
physical, chemical, and electrical properties of carbon films
are mainly correlated to the ratio of sp2 to sp3 bond configurations and are controlled by various process parameters [10].

Carbon materials with nanoscale dimensions (nanotubes,

graphene, fullerene) have been the focus of research and
development over the last 25 years because of their novel physicochemical properties [14]. Owing to their physicochemical
and tribological properties, carbon films have found industrial
applications as wear and corrosion resistant coatings, sensors,
0022-3727/16/264001+7$33.00

2016 IOP Publishing Ltd Printed in the UK

A Javid etal

J. Phys. D: Appl. Phys. 49 (2016) 264001

The cell-adhesion to biomaterials is a primary step

affecting their subsequent physiological functions (spreading,
proliferation, differentiation, cell communication and regulation) [11, 12]. The process is mediated through the adhesion
receptors (integrins) on the cell surface that bind to the extracellular matrix (ECM) [13, 14]. The ECM, constituting the
cellular environment, is a source of binding sites for the other
proteins. For the cells to function properly, there must be cell
cell and/or cellECM contacts [15, 16]. The adhesion of cells
to ECM takes place in different phases such as cell attachment, flattening, spreading and organizing the actin skeleton
to generate the focal adhesion between cells and biomaterials
[11]. In biological applications e.g. tissue engineering, it is
very important to develop cellbiomaterial and inter-cellular
interface interactions [17]. The cellbiomaterial interactions
are reported to depend upon the materials physicochemical
characteristics, i.e. surface charge [18], wettability [19], surface morphology [20], chemical composition [21] and surface
pH [22]. Carbon films are promising candidates as biomat
erials, since with/without functional modifications, their surfaces are capable of being used in the biomedical field owing
to their inert nature and excellent biocompatibility.
Despite frequent reports on the biocompatibility of carbon
films [23, 24], the deciding property for the cell-proliferation
of carbon films is still not established, and hampered due to
the contradictory reports. For example, a few groups have
shown sp3 content as favourable for cell-proliferation [25],
others reported cell growth enhancement with an increase
of sp2 content [26]. Miksovsky etal observed the increase in
cell proliferation with the increase in film wettability and surface energy [27]. It is also known that in sputtering induced
carbon thin films, variation in surface properties (morphology,
porosity) also changes the electrical properties [28]. Hence,
identification of the decisive role of material properties for
cell-proliferation, whether it is surface features or the electrical
parameters, remains a mystery and needs to be addressed. To
the best knowledge of the authors, no study is available to
differentiate the role of electrical conductivity and surface
energy on the cell-proliferation of carbon thin films.
The present work attempts to identify the key material
property of carbon thin films in cell-proliferation. Details
of plasma diagnostics during the synthesis of films are presented along with the different film properties as a function of
working pressure. After the cell-viability testing for L929 and
Saos-2 cells, the obtained results are correlated to distinguish
the role of material properties.

where, R represents the sheet resistance (/) and t stands

for the thickness (cm) of films. The wettability of the films
was measured by contact angle goniometry using a sessile drop method. The deionized water drop with controlled
volume (4 l) was put on the film surface to capture the drop
image by an adjacent camera. The diiodomethane was used
to measure the contact angle with the nonpolar component.
X-ray photoelectron spectroscopy (XPS) was performed by
an ESCA 2000 Instrument (VG Microtech, UK) with an Al
K x-ray source. Core level spectra were deconvoluted using
the XPSPEAK4.1 software. The surface morphology of the
thin films was observed through FESEM technique (FESEM,
JEOL JSM-6500F).
For L929 cell viability observation, the culture medium
having 89% RPMI-1640 (Nutritious solution), 10% fetal
bovine serum (FBS- RM Bio, USA) and 1% antibiotics (penicillin and streptomycin) was incubated at 37 C for 24h in
standard atmosphere (95% air and 5% CO2) for normalization.
The carbon films deposited on round glass cover slips (15mm
diameter) after UV sterilization (15min) were cultured with
the medium in 24 well plates having the cell density 5103
per well for in vitro investigation. After 1, 3 and 5 d, the culture medium was extracted and MTT (Calbiochem Germany,
3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide)
solution (serum free media) was added in the wells and incubated for 3h. The MTT was exchanged with dimethyl sulfoxide (DMSO). After 30min shaking (to absorb formazan)
the DMSO was transferred to 96 well plates to measure the
absorbance. The complete procedure for Saos-2 cell cultivation is discussed somewhere else [29].

2. Experimental details

3. Results and discussions

Si wafer and round glass cover slips are used as substrates and
these were cleaned via ultrasonication in acetone and ethyl
alcohol (separately for 15min) before the deposition. The
carbon films with 200nm (10nm) thickness were deposited by facing target magnetron sputtering using a graphite
target (99.99%, 4 inch diameter). The plasma chamber was
evacuated to the base pressure of 1105 Torr through high
vacuum pump along with the rotary pump. The discharge was

The characteristics of plasma, being dependent upon the

synthesis conditions, affect the properties of deposited
films. The properties of plasma during magnetron sputtering of the graphite target were studied by OES as a function of working pressure. The emission spectra, as shown in
figure 1(a), were obtained in the wavelength range of 350
550nm. The important spectral lines are indexed at 419.83,
426.7 and 488.1nm corresponding to Ar I, C II and Ar II,

generated in the working pressure range of 2.58.5 mTorr

using Ar (99.99%) gas and using fixed pulse DC power conditions (power density: 20W cm2, pulse frequency: 150kHz
and pulse reversal time: 2.9 s).
The film thickness was measured by surface profiler
(KLA-Tencor, Alpha-Step IQ). The plasma discharge characteristics were analyzed by optical emission spectroscopy
(OES) using an Acton spectra 500i spectrometer connected to
a CCD camera (PRIMAX Princeton Instrument). The spectra
were obtained using WinSpec32 software. The sheet resist
ance was observed by 4-point probe technique (Chang Min
Co. Ltd). The electrical conductivity was calculated by the
following equation:
1
=
(1)
R t

A Javid etal

J. Phys. D: Appl. Phys. 49 (2016) 264001

pressure and smaller at lower pressure. At lower pressure, the

bombardment of energetic ions on the growing film surface
gives rise to a compact structure with smaller gaps between
NDs. However, at higher pressure the energy of the deposited
atoms decreases and the resulting structures are grown with
relatively higher gaps between NDs. The growth of the films
in the columnar structure is attributed to the nucleation and
growth mechanism. The atoms approaching the substrate have
sufficient energy to adsorb into the surface of the substrate to
give rise to the islands of carbon atoms. These islands provide
the nucleation centers to further incoming atoms to grow in
columnar structures during the process of energy relaxation
on adsorption. Since, the atoms within the column are closely
packed, they grow in the z-axis perpendicular to the substrate.
The variation in chemical structure of carbon films is
presented as a function of working pressure, as shown in
figure3. Figure3(a) shows the XPS survey spectra of films
in the binding energy range of 11000eV. From the assigned
prominent peaks, it is clearly visible that apart from O there
is no impurity in the deposited films. Figure 3(b) represents the deconvolution of C-1s core level spectra into three
components. The components, centered at 284.4, 285.4 and
287.6eV correspond to CC (sp3 hybridization), C=C
(sp2 hybridization) and CO, respectively. The high resolution
O-1s spectra is also shown in figure3(c), by deconvoluting the
recorded peak into two components corresponding to physioadsorbed oxygen (at 532.2eV) and chemically bonded oxygen
(at 533.49eV), respectively. The relative hybridization of sp2,
sp3 and ratio of sp3 to sp2 are calculated using the area under
deconvoluted components of C-1s, and shown in figure3(d).
It is observed that the intensity of the CC increases and C=C
decreases with the increase in pressure. It is clear that the
increase in pressure generates the film structure with higher
sp3 and relatively lower sp2 hybridized carbon atoms. Further,
it is noted that the intensity of the peak at 533.49eV increases
with the increase in pressure due the relatively higher oxidation of films on exposure to air. This can be attributed to the
higher porosity of the films at higher pressure. Moreover, the
films are free from any heavy metal contents which can have
harmful effect on the cell viability which shows that the films
are quite safe for bioapplications.
Figure 4 represents the variation of electrical conductivity
of carbon thin films as a function of working pressure. The electrical conductivity was observed to decrease from 0.196 S cm1
to 1.850104 S cm1 with the increase in pressure from
2.5 mTorr to 8.5 mTorr. These results can be justified by the
fact that the carbon films are a combination of mixed sp2 and
sp3 bonds. The sp2 bonds, having electrons, are the origin
of charge transportation in carbon films. The electrons give
rise to the conjugation phenomenon to induce an ability in
the films to conduct charge. The higher concentration of sp2
bonds at lower pressure as compared to the higher pressure, as
evidenced by the XPS results, increases the electrical conductivity of the films. The higher electron temperature at lower
pressure, as revealed by the OES results, causes the orientation of carbon atoms to be bonded in sp2 configurations. In
such a configuration, electrons can generate higher delocalization causing an increase in electrical conductivity. Moreover,

Figure 1. (a) Optical emission spectra of plasma discharge at

various working pressure. (b) Intensity ratio of Ar II to Ar I,
calculated from OES data.

respectively. It is observed that the intensity of all these species tends to decline on increasing the pressure. It reveals
that the highly excited plasma species are generated at the
lower pressure. Furthermore, the intensity ratio of Ar II
(at 488.1nm) to Ar I (at 419.83nm) is calculated and shown
in figure1(b). This ratio is associated to the electron temper
ature. On increasing the pressure, the increase in density of Ar
enhances the electronneutral collision frequency due to lowering the mean free path. This will reduce the electron temper
ature and excitation of the present species as well. Hence, the
lower energy species approaching the substrate will generate
the film structure with lower density.
The surface morphology, studied by FESEM, is shown in
figures2(a) and (b), for the representative samples prepared at
2.5 mTorr and 6.5 mTorr, respectively. The top view clearly
depicts the growth of films in the form of nano-domains (NDs)
separated by nanoscale dimensions. Similar morphology has
been reported by Kumar et al in carbon films deposited as
a function of power density and pulsed frequency [29]. The
cross sectional image represents the film growth in columnar
structures. The separations between NDs correspond to
the nano-channels between the columns. The observations
depict that the spacing between the columns is large at higher
3

A Javid etal

J. Phys. D: Appl. Phys. 49 (2016) 264001

Figure 2. FESEM images of carbon film deposited at: (a) 2.5 mTorr, (b) 6.5 mTorr with magnification200000. The nano-domains and
the separations in columnar structure are pointed out by arrows.

Figure 3. XPS spectra of carbon films: (a) survey spectra, (b) high resolution C-1s spectra, (c) high resolution O-1s spectra. (d) Relative
hybridization of sp2, sp3 and ratio of sp3 to sp2 calculated from the area of C-1s components.

the films, deposited at lower pressure, have higher density

(lower spaces between NDs) which ultimately enhances the
electron density to decrease the sheet resistance.
The variation in water contact angle as a function of
pressure is shown in figure 5. The contact angle, using diiodomethane as a non polar liquid, was also measured to calculate the surface energy (s) of the carbon films. The Fowkes
model is used to calculate the surface energy using the following equation[30]:

where, dl and lp represent the dispersive and polar components

of liquid respectively, whereas sd and sp are the dispersive and
polar components of solid respectively. First, sd is calculated
from equation(2) by putting lp=0 for non polar aprotic liquid
(diiodomethane). Second, the films are tested for water and sp
is computed from equation(2). Here, , dl and lp are taken as
50.8, 50.8 and 0 respectively for diiodomethane and , dl and
lp for water are taken as 72.8, 51.0 and 21.8 respectively [31].
The total surface energy is equal to the sum of dispersive and
polar components as given in equation(3).

l(cos + 1) = 2 ( dl )( sd) + ( lp)( sp)

(2)

A Javid etal

J. Phys. D: Appl. Phys. 49 (2016) 264001

Figure 4. Electrical conductivity of carbon films deposited as a

function of working pressure.

Figure 6. The viability of carbon films for: (a) L 929 cells as a function
of working pressure. (b) Saos-2 at fixed 4.5 mTorr working pressure.
Figure 5. Water contact angle and surface energy of carbon films
deposited as a function of working pressure.

diameter of nano-capillaries induces higher housing of water

molecules, subsequently showing higher wettability and
higher surface energy. From a surface chemistry point of view,
higher chemically bonded O in XPS results (O-1s spectra at
533.49eV) in the films deposited at higher pressure can introduce the hydrogen bonding with water molecules. Thus, the
higher wettability and surface energy can be justified at higher
working pressure.
The biological response of carbon films was investigated
in vitro using L929 mouse fibroblast and Saos-2 cells, shown
as (a) and (b), respectively in figure6. The films deposited under
various pressure conditions were exposed to the culture media
to observe the cell viability. The bar diagram in figure 6(a)
exhibits all the films having sufficient biocompatibility and
significant increase in cell viability with time. The films prepared in extreme pressure conditions (2.5 and 8.5 mTorr)
show higher viability as compared to the other films (deposited at 4.5 and 6.5 mTorr). After one day of cell culturing, the
higher viability exhibited by the films (deposited at 2.5 mTorr)
is attributed to its higher electrical conductivity. The higher
conductivity films provide the higher electrically conductive
interface to the cells to alter its functions (signal transduction
process) for cell adhesion and regulation using the electrical
cues. Kim et al reported the higher cell growth on lower
resistivity carbon films [26]. With increase in pressure values

s = sd + sp.
(3)

The observations depict the higher water contact angle at

lower pressure and show a decreasing trend with the increase
in pressure. Subsequently, the surface energy increases with
the increase in pressure. It should be noted here that the wettability of the materials is mostly affected by surface roughness,
surface chemistry and porosity. In the present case, the surface roughness varies in a very narrow range (data not shown
here) and thus should have a negligible effect on the surface
wettability. Thus, the porosity and surface chemistry can be
regarded as the main parameters affecting the surface wettability and surface energy.
The porosity of carbon films increases on increasing the
pressure during plasma sputtering [26]. It should be noted
that the carbon films are grown in the form of NDs and the
dimensions of separation between the NDs are tailored due
to working pressure variation as revealed by SEM results.
These separations work as nano-capillaries to accommodate
water molecules. At lower pressure, the capacity of the nanocapillaries to house water molecules is less due to compact
structure (smaller gaps between NDs) and water contact angle
is higher. On the other hand, when porosity is increased at
higher pressure, the resulting increase in surface area and
5

A Javid etal

J. Phys. D: Appl. Phys. 49 (2016) 264001

role to enhance the cell growth. In previous works, Liao etal

observed the carbon films to have sufficient potential for L929
cell growth that is enhanced by nitrogen doping [23]. An
enhancement of cell growth on carbon films containing TiO2
nanoparticles was also reported in the literature [32]. The
increase in the proliferation of human osteoblast Saos-2 cells
upon O-terminated nanocrystalline diamond was observed by
Kalbacova etal [33]. These films have sufficient potential to
be used in regenerative medicine and medical implants where
the tissue regeneration is the prime requirement to repair the
damaged organs. Plasma induced biomaterials present an
effective and safe approach for tissue engineering applications
as the films are contamination free and can be deposited irrespective of substrate type.
Figure 7. Comparison of carbon films having the same electrical
conductivity and different surface energy deposited at 2.5 mTorr
working pressure.

4.Conclusion
The deposition of carbon films having nanodomain morph
ology with tunable inter-domain separation is successfully
achieved through a facing target magnetron sputtering plasma
process. The process facilitates control over the energy of species in the plasma by variable working pressure. The chemical
structure as analyzed by XPS shows the formation of higher
sp2 bonds in the films at lower pressure which controls the surface electrical properties of carbon films. The nano-separations
in the nanodomains structure work as nano-capillaries to
accommodate the water molecules. The films exhibit higher
wettability and surface energy at higher working pressure
because of the larger separations between columns. The time
dependent cell growth study for L929 cells reveals the dominance of electrical conductivity in the beginning of the cell
cultivation, followed by surface energy playing a leading role
in cell population enhancement after the passage of time.

(at 4.5 and 6.5 mTorr), the observed decrease in viability is

controlled by the decrease in the surface conductivity (as
shown in figure4). However, the higher viability for the films
deposited at 8.5 mTorr can not be justified only on the grounds
of conductivity. The results in figure6(a) shows that the cellviability of the films prepared in extreme working pressure
conditions are very similar (at a fixed duration of time). For
justification of such an observation, it is important to also
consider parameters other than just conductivity. Another,
equally important, parameter is porosity, which plays a key
role in cell interaction owing to its linear correlation with
surface energy. We anticipate that in the present case, as the
time passes, the surface conductivity of carbon films reduces
due to the adsorption of atmospheric hydocarbons. As a
result, porous films have competition between surface energy
(decreasing with time) and surface resistivity (increasing with
time) to govern the cell-viability behaviour with time. After
three and five days, the contribution from surface energy
becomes dominant over the conductivity. The carbon films
also exhibit good viability for Saos-2 bone cells. The films
show significantly higher viability as compared to control
after five days as shown in figure6(b). The findings provide
the broader perspective of carbon films in bioapplications.
In films of higher surface energy, the cells can spread easily
to perform the subsequent processes more comfortably. The
films, with similar electrical conductivity to the films deposited at 2.5 mTorr pressure but having lower surface energy
were compared to explore the effect of surface energy. For
this, additional films were prepared using deposition from a
single target on the facing and rotating substrate. The comparison of the viabilities of these two films is shown in figure7.
The higher surface energy films show less viability after one
day of cell cultivation. After three days, the viabilities of both
the films are comparable and after five days, the viability of
higher surface energy films is higher than the lower wettability films. One can conclude from the results of figures6(a)
and 7, that the role of higher conductivity and relatively lower
surface energy of carbon films is important regarding adhesion of L929 cells in the beginning of cell cultivation. During
the proliferation phase, the surface energy plays an important

Acknowledgments
This study was supported by the National Fusion Research
Institute of Korea (NFRI) through the R&D Program of
Plasma Advanced Technology for Agriculture and Food
(Plasma Farming) and the Global Development Research
Center (GRDC), under the program of the Ministry of Science,
ICT and Future Planning (MSIP, Grant No. 20120006672,
2nd stage 3rd year). Authors also acknowledge the help from
Chikage Yamada during the cell viability experiments.
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