Diamond & Related Materials 15 (2006) 1941 – 1948
www.elsevier.com/locate/diamond
Hemocompatibility of diamondlike carbon–metal composite thin films
Melanie Andara a , Arvind Agarwal a , Dirk Scholvin b , Rosario A. Gerhardt b , Anand Doraiswamy c ,
Chunming Jin c , Roger J. Narayan c,⁎, Chun-Che Shih d,e,f , Chun-Ming Shih g ,
Shing-Jong Lin d,f,h , Yea-Yang Su d
a
Department of Mechanical and Materials Engineering, Florida International University, Miami, FL, 33199, USA
b
School of Materials Science and Engineering, Georgia Institute of Technology, Atlanta, GA, 30332, USA
c
Joint Department of Biomedical Engineering, University of North Carolina, Chapel Hill, NC 27599-7575, USA
d
Institute of Clinical Medicine, School of Medicine, National Yang-Ming University, Taipei 112, Taiwan
e
Division of Cardiovascular Surgery, Taipei Veterans General Hospital, Taipei 112, Taiwan
f
Cardiovascular Research Center, National Yang-Ming University, Taipei 112, Taiwan
g
Graduate Institute of Medical Sciences, School of Medicine, Taipei Medical University, Taipei 110, Taiwan
h
Division of Cardiology, Taipei Veterans General Hospital, Taipei 112, Taiwan
Available online 30 June 2006
Abstract
We have investigated the hemocompatibility of diamondlike carbon–silver composite and diamondlike carbon–titanium composite thin films
prepared using a multicomponent target pulsed laser deposition process. These materials were examined using transmission electron microscopy,
Raman spectroscopy, nanoindentation, electrochemical charge transfer testing, and platelet adhesion testing. Cross-sectional transmission electron
microscopy revealed that silver self-assembles into nanoparticle arrays within the diamondlike carbon matrix in the diamondlike carbon–silver
composite film. On the other hand, titanium self-assembles into alternating nanometer-thick titanium carbide layers within the diamondlike carbon
matrix in the diamondlike carbon–titanium composite film. The hemocompatibility of these materials was examined using electrochemical charge
transfer testing and platelet adhesion testing. A few small, widely scattered crystals were observed on the surface of the unalloyed diamondlike
carbon film exposed to platelet rich plasma. On the other hand, dense fibrin networks with densely aggregated platelets were observed on the
surfaces of diamondlike carbon–silver and diamondlike carbon–titanium composite thin films exposed to platelet rich plasma. Electrochemical
testing revealed that the time constant for the diamondlike carbon thin film (λ = 1) was significantly higher than those for the diamondlike carbon–
silver and diamondlike carbon–titanium composite thin films. These results suggest possible uses for diamondlike carbon thin films and
diamondlike carbon–metal composite thin films as coatings in next generation cardiovascular implants.
© 2006 Elsevier B.V. All rights reserved.
Keywords: Diamondlike carbon; Hemocompatibility; Pulsed laser deposition
1. Introduction
A common problem with cardiovascular medical devices,
including artificial heart valves and cardiac stents, is thrombus
formation [1–6]. Thrombus formation is a multiple step process, which involves plasma protein adsorption, platelet
adhesion, platelet activation, and clotting factor activation
[7,8]. These thrombi can embolize (break loose) and cause
damage to the brain, kidneys, lungs, or other internal organs.
Carbon biomaterials have been used for over thirty years to
⁎ Corresponding author. Tel.: +1 919 513 8102; fax: +1 919 513 3814.
0925-9635/$ - see front matter © 2006 Elsevier B.V. All rights reserved.
doi:10.1016/j.diamond.2006.05.013
prevent thrombus formation on cardiovascular device surfaces.
Pyrolytic carbons, which are prepared from hydrocarbon gas in
a fluidized bed reactor, are commonly used in heart valve
prostheses. In 1969, De Bakey introduced a pyrolytic carboncoated aortic valve prosthesis, which incorporated a carboncoated hollow ball and carbon-coated metal struts [9]. These
valves have demonstrated exceptional biocompatibility, inertness, and immunity to fatigue. More recently, diamondlike
carbon has been considered for use in cardiovascular medical
devices. The term diamondlike carbon (DLC) is used to describe amorphous carbon thin films that contain a high fraction
of sp3-hybridized atoms [10–12]. Diamondlike carbon thin
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M. Andara et al. / Diamond & Related Materials 15 (2006) 1941–1948
films exhibit atomic number densities greater than 3.19 g atom/
cm3, and may possess atomic number densities closer to that of
diamond (3.51 g/cm3) than that of graphite (2.26 g/cm3).
Microcrystalline or nanocrystalline graphite domains may be
observed in this amorphous material. Films that contain predominantly sp3-hybridized atoms and tetrahedral local carbon
configurations are often referred to as tetrahedral amorphous
carbon (ta-C) films. The terms amorphous diamond and amorphic diamond are also used to describe this material [13].
Diamondlike carbon thin films have been prepared using
several deposition techniques. Deposition of diamondlike carbon thin films requires a carbon source, and an energy source to
create excited carbon species. Excited carbon species may be
generated by (a) bombardment with energetic species (ion assisted deposition), (b) collision with energetic species (sputtering), (c) acceleration of carbon ions, or (d) energy transfer (laser
ablation). Carbon species with kinetic energies on the order of
100–1000 kT (2.5–25 eV) are produced using these processes
[14]. These high energies are necessary to promote 2s electrons
to 2p orbitals and create sp3-hybridized carbon bonds. Pulsed
laser deposition of diamondlike carbon thin films involves
ablation of a sp2 bonded carbon target at room temperature,
resulting in the formation of sp3-hybridized diamondlike carbon
thin film. Other target materials have included pressed diamond
powder, glassy carbon, and various polymers [15–17]. Deposition using hydrogen-free carbon sources provides hydrogenfree diamondlike carbon films, and deposition using hydrocarbon sources provides diamondlike carbon films with significant
hydrogen and/or hydrocarbon incorporation. The growth rate of
diamondlike carbon films using a krypton fluoride excimer laser
(λ = 248 nm) is ∼ 0.01 nm/pulse [18].
Diamondlike carbon has been considered for use in several
cardiovascular devices [19–21], including coronary artery
stents [22,23], heart valves [24–26], left ventricular assist devices [27], and heart prostheses [28]. Diamondlike carbon thin
films exhibit decreased platelet activation, and reduced thrombus formation [29]. In addition, diamondlike carbon possesses
an extremely low coefficient of friction, which may increase the
blood flow rate and enhance other hemodynamic properties.
Diamondlike carbon-coated biomaterials have demonstrated
exceptional hemocompatibility in several studies. In vitro studies have shown that platelet activation and platelet adhesion
occur less often on diamondlike carbon-coated surfaces than on
Fig. 1. Schematic of the pulsed laser deposition (PLD) system.
Fig. 2. Schematic of the composite target used in pulsed laser deposition of
diamondlike carbon–metal composite films.
titanium, titanium carbide, titanium nitride, and stainless steel
surfaces [2,3,26,30–32]. For example, 125I-labelled platelet
adhesion measurements demonstrate that a smaller number of
platelets adhere to diamondlike carbon-coated titanium surfaces
than to titanium surfaces [30]. In fact, diamondlike carbon thin
films may resist platelet adhesion and thrombus formation better
than pyrolytic carbon [33]. Cui et al. have suggested that ratio
between albumin adhesion and fibrinogen adhesion is an important factor that determines the amount of platelet adhesion on
a biomaterial surface, and have shown that albumin adhesion/
fibrinogen adhesion ratios for diamondlike carbon-coated surfaces are higher than those for polymethylmethacrylate surfaces
[32]. Chen et al. have demonstrated a correlation between the
fraction of sp3-hybridized carbon atoms, the surface energy of the
diamondlike carbon film, and the number of adherent platelets
[22].
One major limitation preventing the practical application of
diamondlike carbon films is large compressive stresses. Stresses
as high as 10 GPa have been observed within as-deposited
diamondlike carbon thin films [34–36]. These very high stress
values limit maximum film thickness to ∼0.1–0.2 μm. Delamination of diamondlike carbon films can occur when internal
stresses exceed a critical value. Diamondlike carbon film adhesion can be improved through incorporation of modifying
elements. Numerous modifying elements, including gold, chromium, copper, silicon, oxygen, tungsten, titanium, iron, platinum, niobium, nickel, silicon, tin, and tantalum, have been
incorporated within diamondlike carbon thin films [37–44].
Narayan et al. have developed a modification of the conventional pulsed laser deposition process in order to incorporate
modifying elements within growing diamondlike carbon thin
films [43–47]. In this process, a multicomponent target (pure
graphite covered by a piece of the desired modifying element
target) is loaded into the pulsed laser deposition chamber. A
focused excimer laser beam sequentially ablates the graphite
target component and the modifying element target component
to form composite films. Adherent, 1 μm thick diamondlike
carbon–titanium and diamondlike carbon–silver films have
been demonstrated using this technique [47].
In this paper, the structural, mechanical, and hemocompatibility properties of diamondlike carbon–silver and diamondlike carbon–titanium composite films were examined. The
M. Andara et al. / Diamond & Related Materials 15 (2006) 1941–1948
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useful biomedical properties. Schroeder et al. examined diamondlike carbon–titanium films, and demonstrated that the
titanium within these films had a positive effect on protein
adsorption, cell attachment, and cell proliferation [51]. Visible
spectrum Raman spectroscopy and transmission electron
microscopy were used to assess carbon bonding characteristics.
Nanoindentation testing was performed in order to determine
the mechanical properties of these films. The hemocompatibility of the diamondlike carbon and diamondlike carbon–
metal composite films was examined using platelet adhesion
testing and electrochemical testing. Our results suggest that
diamondlike carbon–metal composite films, particularly functionally gradient diamondlike carbon–metal composite thin
films, may play unique roles in cardiovascular implants.
2. Experimental
Several 1 cm2 pieces of 2.5 Ω/cm2 (p-type), 525 μm thick,
silicon (100) wafers (Silicon Quest International, Santa Clara,
California) were cleaned with acetone and methanol in an
ultraonic cleaner. The silicon pieces were then dipped in
hydrofluoric acid to remove silicon oxide and produce a
hydrogen-terminated surface. The target used for processing
diamondlike carbon films was high purity graphite. Diamondlike carbon–silver or diamondlike carbon–titanium composite
films were prepared by placing pieces of silver or titanium over
the graphite target such that 90° of the ablation circle was
covered by the metal piece (Fig. 1). The cleaned substrates and
targets were loaded into a pulsed laser deposition chamber,
which was evacuated to a pressure of ∼ 5 × 10− 6 Torr (Fig. 2). A
Compex 205 KrF excimer laser (Lambda Physik, Goettingen,
Germany) operating at a frequency of 248 nm was used for
ablation of the multicomponent target. The laser was operated at
a pulse duration of 25 ns and a frequency of 10 Hz. The laser
Fig. 3. a. Cross-sectional Z-contrast dark field transmission electron micrograph
of diamondlike carbon–silver composite film. b. Cross-sectional Z-contrast dark
field transmission electron micrograph of diamondlike carbon–titanium
composite film. This film was prepared according to a procedure described in
[52].
metal component in these diamondlike carbon composite films
was chosen to promote specific biological responses [48–50].
For example, silver is highly toxic to microorganisms, and
demonstrates biocidal effects against Staphylococcus aureus,
Escherichia coli, Pseudomonas aeruginosa, Listeria monocytogenes, and other species of bacteria. The exact mechanism
of action is unknown, but it is believed that silver ions act by
binding to deoxyribonucleic acid, interfering with electron
transport within cells, and/or injuring bacterial enzymes.
Diamondlike carbon–titanium composite films may also have
Fig. 4. Visible Raman spectra of (a) diamondlike carbon and (b) diamondlike
carbon–silver composite thin films. Diamondlike carbon–metal composite films
exhibit greater asymmetry in the G-band and a slight increase in the D-band
height.
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M. Andara et al. / Diamond & Related Materials 15 (2006) 1941–1948
pulses provided average energy densities of ∼ 5 J/cm2 to the
targets. The targets were rotated at 5 rpm during the deposition
process, and the total time for each deposition was 10 min. The
target–substrate distance was maintained at 4.5 cm. Previous
profilometry studies have shown that diamondlike carbon and
diamondlike carbon–metal composite films prepared using
these deposition conditions exhibit film thicknesses in the range
of ∼60 nm.
High-resolution Z-contrast images were obtained using a
JEOL 2010 F scanning transmission electron microscope equipped with field emission gun and Gatan Image Filter (GIF). In Zcontrast imaging, an image is formed by collecting large-angle
scattered electrons using an annular detector. The resulting
contrast is proportional to the atomic number squared. Raman
spectra of the diamondlike carbon layer were obtained using a
SPEX 1704 spectrometer with argon ion laser source
(λ = 514.5 nm) (Horiba Jobin Yvon Inc., Edison NJ). Peak
positions were obtained from Gaussian interpolation of the
Raman data.
A Nanoindenter XP® system (MTS Instruments, Oak Ridge,
TN) was used to determine hardness and Young's modulus
values for the diamondlike carbon and diamondlike carbon–
silver films. The samples were examined using an ultra-low
load DCM indentation head and a three-sided diamond pyramid
(Berkovitch) tip. Indentations were performed using a trapezoidal loading curve. The maximum load was varied between
150 and 600 mN. A constant loading rate of 30 mN/s was
applied. Hardness and Young's modulus values were measured
as a function of indentation depth, and were determined using a
modified Oliver–Pharr model [49]. The tip was calibrated
following the partial unloading method, and was cleaned with
isopropanol between indentations.
Platelet adhesion testing was performed to investigate the
morphology, quantity and aggregation of the adherent platelets
in the film. Fresh whole blood was drawn from a healthy adult
volunteer. The blood was tested for anticoagulants and other
pharmacologic agents that could alter the results. The blood was
treated with sodium citrate to prevent coagulation. It was then
centrifuged at 25 °C for ten minutes, at 25 °C for ten minutes,
and at 4 °C for one hour. The platelet rich plasma was separated
from red blood cells by admixing 1:50 volume of avin (50 U/ml)
and incubating the resulting solution at 37 °C for 10 min. The
platelet rich plasma was frozen for storage prior to testing. The
diamondlike carbon film, diamondlike carbon–silver composite
Fig. 5. a. Scanning electron micrograph of the platelet adhesion testing result for the diamondlike carbon–silver composite film. A dense fibrin network containing
aggregated platelets was observed on the film surface. b. Energy dispersive X-ray microanalysis spectrum of the diamondlike carbon–silver composite film after
platelet adhesion testing. Elements gold, silver, sodium, chlorine, and carbon are present.
M. Andara et al. / Diamond & Related Materials 15 (2006) 1941–1948
film, and diamondlike carbon–titanium composite film were
immersed in platelet rich plasma solution and incubated at 37 °C
for ten minutes. The samples were then rinsed with 0.9% saline
solution to remove weakly adherent platelets. The adhered
platelets were fixed in 4% glutaraldehyde and critical point
dried. The platelet rich plasma-exposed films were then examined for thrombus formation and platelet adhesion using a S-800
field emission scanning electron microscope (Hitachi, Tokyo,
Japan). Films were sputtered with a thin layer of gold in a G5000 sputter coater (Electron Beam Services, Agawam, MA) to
enhance imaging. Energy dispersive X-ray analysis was used to
examine the chemical composition of the film surface.
Electrochemical tests were performed using a standard threeelectrode, temperature controlled cell and a microprocessorcontrolled potentiostat. A saturated calomel electrode (SCE)
was used as the reference and a platinum wire was used as the
counterelectrode. An alternating current impedance measurement technique was used to investigate the electrochemical
kinetics at the composite–electrolyte interface. The measurement was performed at an open-circuit potential. The frequency
was varied from 105 Hz to 10− 5 Hz. A voltage of 5 mV
(alternating current) was used in these studies. The surface of
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the film acted as a capacitor when it was placed in contact with
platelet rich plasma, and the time necessary for the reaction to
take place (time constant (λ)) was calculated by multiplying the
values of capacitance and resistance obtained from impedance
measurements.
3. Results and discussion
In Z-contrast scanning transmission electron microscopy,
contrast is proportional to the atomic number (Z) squared. For
example, the silver:carbon contrast is over 60:1. Silver does not
chemically bond with carbon, and forms self-assembled arrays
of nearly spherical metal clusters within the diamondlike carbon
matrix. Fig. 3(a) demonstrates the atomically sharp boundaries
between the 4 nm silver nanoparticles and the hard carbon
matrix. The reduction in surface energy is the driving force for
the clustering of silver within the diamondlike carbon–silver
composite film. The large random particles that are observed in
this micrograph are artifacts of the ion milling process used in
sample preparation. Previous studies have shown that atoms
that form chemical bonds with carbon, including titanium, form
nanolayered composite films containing alternating ∼2 nm
Fig. 6. a. Scanning electron micrograph of the platelet adhesion testing result for the diamondlike carbon–titanium composite film. A dense fibrin network containing
aggregated platelets was observed on the film surface. b. Energy dispersive X-ray microanalysis spectrum of the diamondlike carbon–titanium composite film after
platelet adhesion testing. Elements gold, titanium, sodium, chlorine, silicon, and carbon are present.
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M. Andara et al. / Diamond & Related Materials 15 (2006) 1941–1948
layers of metal carbide and diamondlike carbon (Fig. 3(b))
[47,52].
The Raman spectra of the diamondlike carbon and diamondlike carbon–silver composite films (Fig. 4) contain two prominent features. The G-band is a broad hump centered at 1510–
1557 cm− 1; this feature reflects the optically allowed E2g zone
center mode of crystalline graphite. The D-band is a small
shoulder at 1350 cm− 1; this feature reflects the A1g zone edge
mode of graphite. The Raman spectrum of the diamondlike
carbon–silver composite film exhibits a reduction in the G-band
full-width half maximum, a shift in the G-band to lower wavenumbers, and an increase in the D-band height. The reduction of
G-band width may be attributed to a decrease in compressive
stresses within the film, the G-band position shift may be related
a decrease in the concentration of sp3-hybridized carbon atoms
or an increase in graphitic cluster size, and the increase in Dband height may also be related to a decrease in the concentration of sp3-hybridized carbon atoms [53,54]. These
features taken together suggest that diamondlike carbon–silver
composite film possesses lower amounts of tetrahedrally
hybridized atoms and/or lower compressive stresses than the
unalloyed diamondlike carbon film. Similar features were also
observed in diamondlike carbon–titanium composite films
examined using ultraviolet spectrum Raman spectroscopy [55].
The hardness and Young's modulus values for the diamondlike carbon–silver composite film on silicon (100) substrate
were 25.7 +/− 7.4 GPa and 267.0 +/− 61.6 GPa, respectively.
The hardness and Young's modulus values for the diamondlike
carbon–titanium composite film were 15.5 +/− 1.1 GPa and
201.0 +/− 12.4 GPa, respectively. The hardness and Young's
modulus values for the diamondlike carbon film on silicon
(100) substrate were 42.1 +/− 1.4 GPa and 379.0 +/− 42.9 GPa,
respectively. The hardness and Young's modulus values for the
silicon (100) substrate itself were 21.1 +/− 1.4 GPa and
237.0 GPa +/− 29.7 GPa, respectively. These hardness values
observed in the diamondlike carbon–metal composite films
were higher than those observed in nanostructured copper/
amorphous hydrogenated carbon (a-C:H) composite films
prepared using a hybrid sputter-deposition/microwave plasmaenhanced chemical vapor deposition process (2.0–2.5 GPa), but
were significantly lower than those observed in tetrahedral
amorphous carbon films prepared using a filtered cathodic
vacuum arc technique with substrate pulse bias (85 GPa)
[56,57].
Fig. 7. a. Scanning electron micrograph of the platelet adhesion testing result for the diamondlike carbon film. A few scattered sodium chloride crystals were observed
on the film surface. b. Energy dispersive X-ray microanalysis spectrum of the diamondlike carbon film after platelet adhesion testing. Elements gold, sodium, chlorine,
silicon, and carbon are present.
M. Andara et al. / Diamond & Related Materials 15 (2006) 1941–1948
Table 1
Time constants for diamondlike carbon and diamondlike carbon–metal
composite films
Sample
Time constant
Diamondlike carbon thin film
Diamondlike carbon–silver thin film
Diamondlike carbon–titanium thin film
1.0
3.3 × 10− 3
4.2 × 10− 7
Adhesion of platelets to the diamondlike carbon and diamondlike carbon–metal composite films was observed with scanning
electron microscopy. Fig. 5(a) contains a scanning electron
micrograph of a diamondlike carbon–silver composite film after
the platelet adhesion testing. A dense fibrin network with densely
aggregated platelets is observed, indicating significant thrombosis
on the surface of the thin film. Fig. 6(a) contains a scanning
electron micrograph of a diamondlike carbon–titanium composite
film after the platelet adhesion testing. A dense fibrin network
containing randomly distributed platelets is also observed on the
surface of this diamondlike carbon–metal composite film. Fig. 7
(a) contains a scanning electron micrograph of a diamondlike
carbon film after platelet adhesion testing. No fibrin networks or
platelet aggregation was observed on the surface of the platelet
rich plasma-exposed diamondlike carbon thin film. A few small,
widely scattered crystals were observed on the film surface. The
energy dispersive X-ray analysis spectra for the diamondlike
carbon–silver, diamondlike carbon–titanium, and diamondlike
carbon films are shown in Figs. 5(b), 6(b), and 7(b), respectively.
The presence of sodium and chlorine in the energy dispersive Xray analysis spectra for diamondlike carbon–silver, diamondlike
carbon–titanium, and diamondlike carbon films suggests that the
sodium chloride crystals precipitate from the platelet rich plasma.
It appears that this process is independent from the blood coagulation process.
The clotting process has been attributed to electrochemical
activity that results from the release of fibrinopeptides from
fibrinogen [58]. A charge transfer theory for blood clotting
proteins was proposed by Srinivasan et al., in which an exchange of electrons between blood proteins and the surface of a
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semiconducting material triggers the release of fibrinopeptides
that precipitate thrombosis of blood [59]. The rate of charge
transfer during the interaction of platelet rich plasma and the
film surface is a function of the time constant of the film. The
value can be determined using the following equation:
q ¼ kð1−e−t=k Þ
ð1Þ
in which q is the rate of charge transfer, λ is the time constant,
and k is a constant [55]. Films with higher time constant values
exhibit lower transfer current densities. The time constants of
the diamondlike carbon and diamondlike carbon–metal composite films were obtained by multiplying the values of electric
resistance and capacitance, and are listed in Table 1. Fig. 8 contains
an imaginary vs. real impedance Nyquist plot for the charge
transfer during the interaction between the platelet rich plasma and
the diamondlike carbon films. The slope for the diamondlike
carbon film is steeper than those for the diamondlike carbon–
silver and diamondlike–titanium composite films. In addition, the
time constant for the diamondlike carbon thin film (λ = 1) is
significantly higher than those for the diamondlike carbon–silver
and diamondlike carbon–titanium composite thin films. As a
result, the diamondlike carbon film exhibits a lower amount of
charge transfer. The time constant for the diamondlike carbon–
titanium composite film is four orders of magnitude smaller than
that for the diamondlike carbon–silver composite film. The time
constant for the diamondlike carbon–silver composite film is in
turn is three orders of magnitude smaller than that for the
unalloyed diamondlike carbon film. Liberation of metal ions from
the diamondlike carbon–metal composite film surface may also
play a significant role in activation of platelets and initiation of
thrombosis [60].
4. Conclusions
We have deposited diamondlike carbon–silver composite
and diamondlike carbon–titanium composite thin films using a
novel multicomponent target pulsed laser deposition process.
Fig. 8. Nyquist impedance plots for diamondlike carbon and diamondlike carbon–metal composite films.
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M. Andara et al. / Diamond & Related Materials 15 (2006) 1941–1948
Cross-sectional transmission electron microscopy of the
diamondlike carbon–metal composite films revealed that silver
and titanium self-assemble into nanoparticle arrays and alternating nanometer-thick layers within the diamondlike carbon
matrices, respectively. Unalloyed diamondlike carbon thin films
did not exhibit fibrin or platelet aggregation during in vitro
platelet rich plasma testing. On the other hand, diamondlike
carbon–metal composite films exhibited low time constants and
significant in vitro thrombosis. These results suggest that a
functionally gradient diamondlike carbon–metal composite
film design, in which there is a reduction in metal atom concentration from the substrate/film interface to the film surface,
may provide the positive attributes of unalloyed and alloyed
films. The high metal atom concentration at the film–substrate
interface may allow for improved adhesion. The low metal atom
concentration at the film surface may allow for improved
hemocompatibility as well as maximum hardness and Young's
modulus values at the load bearing interface. Diamondlike
carbon thin films, diamondlike carbon–metal composite films,
and functionally gradient diamondlike carbon–metal composite
thin films may each play unique roles in next generation cardiovascular implants.
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