In Vivo Evaluation of a Fluorine-
Acryl-Stylene-Urethane-Silicone
From the 1Department of Radiology, Tohoku Uni-
versity School of Medicine, Sendai City, Japan; and
2Cyclotron Radio Isotope Center, Tohoku Universi-
ty, Sendai City, Japan.
Address reprint requests to T. Matsuhashi, MD, De-
partment of Radiology, Tohoku University School of
Medicine, 1-1 Seiryo-cho, Aobaku, Sendai City,
980 Japan.
Received January 16, 1996, and accepted for pub-
lication after revision March 22, 1996.
Acad Radiol 1996;3:581-588
© 1996, Association of University Radiologists
Antithrombogenic Coating
Material Copolymer for
Intravascular Stents
Toshio Matsuhashi, MD 1, Hideo Miyachi 1 Tadashi Ishibashi, MD 1,
Kiyohiko Sakamoto, MD 1, Akira Yamadera, ScD 2
Rationale and Objectives. We evaluated the effectiveness of a fluorine-
acryl-styrene-urethane-silicone (FASUS) copolymer as an antithrombogenic
coating material for intravascular stents in dogs.
Methods. FASUS copolymer-coated stents were placed in the right iliac
veins, and uncoated 304 stainless steel stents were placed in the left iliac
veins. We examined platelet deposition, microthrombus formation, and
neointimal hyperplasia 4 w e e k s after stent placement by measuring the
activity of lllIn-labeled platelets, by using scanning electron microscopy,
and by measuring neointimal thickness.
Results. Platelet deposition was significantly decreased on coated than
on uncoated stems (p < .05). A less p r o n o u n c e d increase in red blood cell
deposition was observed at the sites of the coated than uncoated stents (p
< .05). Neointimal thickness 4 w e e k s after stent placement also was signifi-
cantly less at the sites of the coated stents (0.27 -+ 0.08 m m versus 0.48 +
0.23 mm, p < .05).
C o n c l u s i o n . FASUS copolymer coating over the vascular stent is effec-
tive for preventing thrombus formation and neointimal hyperplasia.
K e y W o r d s . Antithrombogenicity; stent coating material; fluorine-acryl-
styrene-urethane-silicone copolymer; vascular stent.
he concept of vascular stenting for vascular stenosis was first intro-
T duced in 1969 by Dotter [1], w h o attempted to k e e p vessels o p e n by
scaffolding the inner surface with a tubular metal structure. Since then,
m a n y types of stents have b e e n studied in animals and even have b e e n
experimentally used in h u m a n vessels [2-5]. Vascular stents are n o w being
used in the treatment of arterial stenosis and venous stenosis in the supe-
rior vena cava and inferior vena cava, as well as in transjugular intrahepatic
portosystemic shunts [6, 7].
Because stent placement is an irreversible procedure, stent biocompati-
bility, biomechanics, and thrombogenicity are important considerations.
Biocompatibility and biomechanics have b e e n studied extensively [8, 9].
Severe problems associated with vascular stents include acute thrombosis
581
MATSUHASHI ET AL. Vol. 3, No. 7, July 1996

and delayed intimal h y ~ r p l a s i a . The risk of acute uncoated and coated stents. For each animal, we con-
thrombosis is greater in venous than in arterial stents. firmed that the right and left iliac veins had similar flow
Other researchers recently have recognized the clinical patterns. Therefore, the differences detected b e t w e e n
importance of early thrombotic stent closure. Acute veins having coated and uncoated stents were unlikely
thrombosis has b e e n reported in 13-40% of cases with to be attributable to initial flow patterns.
the use of self-expanding stents [5]. The risk of stent-
related thrombosis appears to be an acute problem that Stent Design
is temporally related to stent placement and probably The stents used in this study were self-expandable Z
attributable to the stent's thrombogenicity. Palmaz et al. stents, which were constructed of 0.3-ram, 304 stainless
[10] and Johnston et al. [11] demonstrated that the steel wire in a cylindrical, zigzag configuration of six bends.
effects of aggressive anticoagulation can decrease the Stents were 10 m m in diameter when fully expanded and
amount of thrombus deposition on a vascular stent. 15 m m long. Coated and uncoated stents apparently have
However, a disadvantage of this method is h e m a t o m a the same configuration (Figs. 1 and 2).
formation at the puncture site. It would be better to
place a vascular stent without using aggressive antico- C o a t i n g Material: F A S U S C o p o l y m e r
agulation measures, a procedure that might prevent
The FASUS copolymer has an alternate hydrophilic
hemorrhagic complications.
and hydrophobic lamellar structure and a segregated
To avoid acute thrombosis, researchers [12-14] have
microdomain structure (Fig. 3). This graft-block copoly-
used several types of coating materials for vascular
mer is c o m p o s e d of a perfluoroalkyl compound, a
stents. Kawahito et al. [15] reported the use of a fluo-
methacrylic acid/styrene copolymer, urethane, and
rine-acryl-styrene-urethane-silicone (FASUS) copolymer
siloxane (Fig. 4). The hydrophilic perfluoroalkyl com-
as an antithrombogenic coating material for a circula-
p o u n d and the hydrophobic methacrylic acid/styrene
tow-assist device in 1993. They evaluated the anti-
c o m p o n e n t may be responsible for the lamella-type
thrombogenicity of the FASUS copolymer in a
venoarterial bypass circuit in dogs. This material has a
hydrophilic lamella with a segregated microdomain
structure, which is expected to suppress the adhesion
of platelets. The advantages of the FASUS copolymer
over other coating materials are as follows: (1) It is easy
to coat the surface of metallic structures and macromol-
ecule resin, except for T e f o n , silicone, and olefin; (2)
coating by FASUS copolymer is rigid and stable; and (3)
the cost of coating is inexpensive. The purpose of the
current study was to investigate the effectiveness of a
FASUS copolymer-coated vascular stent without the use
of systemic anticoagulation in dogs. FIGURE 1. Uncoated self-expandable Z stent constructed of 0.3-mm, 304
stainless steel wire in a cylindrical, zigzag configuration of six bends.

MATERIALS AND METHODS

Animals

Twenty-two adult dogs (weight = 10.2-14.8 kg, M =

12.9 kg) were used in our studies. We complied with
the National Institutes of Health's guidelines for the use
and care of laboratory animals. We used dogs because
their circulatory systems are relatively resistant to
thrombosis in arteries and large veins. Because of their
small diameter (6-8 m m ) and slow blood flow, we used
bilateral c o m m o n iliac veins or external iliac veins for FIGURE 2. Coated stent, which appears to have the same structure as the un-
stent placement to compare the thrombogenicity of coated stent.

582
Vol. 3, No. 7, July 1996 COATING MATERIAL FOR INTRAVASCULAR STENTS

gous blood (50 ml) was obtained from each dog's vas-
cular sheath and was used to label platelets. The
platelets from these samples were isolated and labeled
with indium-I 11 oxine (1111n-oxine; Amersham, Tokyo,
Japan) and reinfused.
Thirty minutes after reinfusion, each coated stent was
compressed until it fit inside the distal end of the
">'-. ' - % > :7\ sheath and was advanced to the right external iliac vein
> >{,>< >..;2a: ,..
using an inner sheath. The outer sheath was withdrawn
while the inner sheath was held immobile, and the
stent was placed into the right external iliac vein. In the
same way, each uncoated stent was placed into the left
external iliac vein.
Anticoagulant or platelet anti-aggregating agents were
FIGURE 3. Scanning electron microscopic image shows lamella-shaped mi- not used during this phase of the study. The dynamic
crodomain structure of the fluorine-acryl-styrene-urethane-silicone copolymer
(original magnification, x5,000). deposition of 1111n-oxine-labeled platelets was deter-
mined by measuring the radioactivity of regions of inter-
est (ROIs) in the confined areas of stent placement
every 10 min using a bismuth germanite oxide counter
(10 m m in diameter, 3 cm long). Radioactivity was mea-
Perfluoroalkyl compound )
sured for 180 min.
I
Si (OR)3
I
Si (OR)3
Scanning Electron Microscopy
I I
( Methacrylic acid / styrene copolymer ) Twelve adult dogs (average weight = 13.5 kg) were
Si (OR)3 Si (OR)3 given general anesthesia using pentobarbital (25 m g / k g

(
I
Urethane
' )
I
Si (OR)3
FIGURE 4. Chemical structure of the fluorine-acryl-styrene-urethane-silicone
copolymer.
microdomain structure of FASUS. Urethane is a copoly-
mer that improves adhesiveness to substructures, forming a
pendant structure with the perfluoroalkyl compound and
methacrylic acid/styrene copolymers. These polymers form
a bridge with siloxane. The FASUS copolymer is easily
applied to the metallic structure.
Platelet Studies
Five adult dogs (average weight = 12.5 kg) were
given general anesthesia with pentobarbital (30 m g / k g
intravenously [IV]). Under sterile conditions, 7-French-
long sheaths (Medikit, Tokyo, Japan) were introduced
percutaneously into the bilateral femoral veins using
the Seldinger method and were advanced into each
external iliac vein under fluoroscopic guidance. Autolo-
IV). Under sterile conditions, 7-French-long sheaths
were introduced percutaneously into bilateral femoral
veins using the Seldinger method and were advanced
into each c o m m o n iliac vein. Coated and uncoated
stents were inserted into the right and left c o m m o n iliac
veins, respectively (as described earlier). Anticoagulant
or platelet anti-aggregating agents were not used dur-
ing this phase of the study.
The animals were euthanized in groups of four 30
rain, 2 hr, and 4 hr after stent placement. Euthanasia was
performed under general anesthesia using fluid volume
replacement with 5% glucose in water. Immediately after
cardiac arrest, 35-mm stented segments (as well as seg-
ments proximal and distal to the stent) were resected
and flushed with saline. The veins with stents were fixed
overnight under 2.5% glutaraldehyde solution in a 0.1-
mol/1 phosphate buffer (pH = 7.4). After being dehydrated
in graded ethanol to 100% and critically point-dried, the
stents were sputter-coated with platinum. The specimens
were observed using a Hitachi S-450 scanning electron
microscope (Hitachi Medical, Chiyoda-ku, Tokyo,
Japan). Detailed documentation of cellular and subcellu-
lar morphology was obtained. We evaluated thromboge-
nicity by counting the number of red blood ceils that

583
MATSUHASHI ET AL. vol. 3, No. 7, July 1996

adhered to the stent surface (five random points) per 100

x 100 btm square.

Neointimal Hyperplasia

Five adult dogs (average weight = 12.0 kg) were given

general anesthesia with pentobarbital (25 mg/kg IV).
Under sterile conditions, 7-French-long sheaths were
introduced percutaneously into the bilateral femoral veins
using the Seldinger method and were advanced into each
common iliac vein under fluoroscopic guidance.
Coated and uncoated stents were placed into the right
and left common iliac veins, respectively, in the manner
described earlier (Fig. 5). Anticoagulant or platelet anti-
aggregating agents were not used during this phase of the
study. Four weeks after stent placement, general anesthe-
sia (via pentobarbital) was administered IV and 5-French
vascular sheaths (Medikit) were placed into the bilateral
femoral veins. Bilateral iliac venography was performed
(Fig. 6), and the animals were euthanized using fluid vol-
ume replacement with 5% glucose in water. Immediately
FIGURE 6. Bilateral iliac venography from the vascular sheath 4 weeks after
after cardiac arrest, 35-mm stented segments (as well as stent placement. A partial defect (probably indicative of intimal thickness) can
be seen at the left common lilac vein.
segments proximal and distal to the stent) were resected
and flushed with saline. The veins with stents were fixed
under formaldehyde solution for at least 2 days. The spec-
imens were opened longitudinally and photographed. unsuspected complications were conducted. The stent
Gross inspections for thrombus, intimal coverage, and struts then were removed carefully and the veins stained
with elastica-Masson's trichrome. Morphometric measure-
ment of the formed neointima at the stented segment (five
random points of intermediate neointima between the
stent struts) of the vein was performed with a Nikon
ocular micrometer (Nikon, Tokyo, Japan) at a magnifi-
cation of xl0.

Statistical Analyses

We analyzed the radioactivity of ROIs at the stented

FIGURE 5. A coated stent in the right common iliac vein and an uncoated stent
in the left common iliac vein.
site (relative count), the average number of red blood
cells that adhered to the stent struts per 100 × 100 ~m
square, and the mean thickness of neointimal hyperpla-
sia at the stent site.
Statistical analysis was performed on a Macintosh
computer using StatView software (Abacus Concepts,
Berkeley, CA). A repeated measures analysis of variance
was used to compare the radioactiviW of the ROIs and the
average number of red blood cells that adhered to the
stent struts. Paired t tests were used to compare the mean
thickness of neointimal hyperplasia at the stent site. Data
are reported as mean _+ standard deviation. Significance
was set at the .05 level.

584
Vol. 3, No. 7, July 1996 COATING MATERIAL FOR INTRAVASCULAR STENTS

RESULTS : .... , 30 rain. 2 hour's + 4 hours

lii
Platelet Studies
Platelets w e r e labeled with 30.5 + 3.6 MBq 111In-
oxine; the labeling efficacy w a s 77.2 + 9.0%. The plate- i:+ +
let c o u n t a v e r a g e d 118.7 + 22.3 × 1 0 3 / m m 3. Platelet
deposition at the stent sites w a s time d e p e n d e n t (Fig.
7); a m a x i m u m increase w a s f o u n d within the first 120
min and plateaued thereafter. A less p r o n o u n c e d
increase was o b s e r v e d at the c o a t e d stent site than at
the u n c o a t e d stent site (p < .05).

Scanning Electron Microscopy

Qualitative results are s h o w n in Figures 8 and 9. Little
thrombus formation can be seen o n the surface of the
coated stent 30 min after placement. Figure 8 shows
dense thrombus formation o n the surface of the
u n c o a t e d stent versus rare, scattered thrombus formation
o n the surface of the coated stent 2 hr after placement.
There w e r e extensive fibrin deposits b e t w e e n the red
b l o o d cells o n the surface of the u n c o a t e d stent 4 hr after
placement (Fig. 10). There w e r e considerably fewer red
b l o o d cells o n coated stents than o n u n c o a t e d stents.
Thirty minutes after stent placement, there w e r e 15.5 +
5.8 red b l o o d cells per 1.0 x 104 btm 2 o n coated stents
c o m p a r e d with 64.5 _+ 19.9 red b l o o d ceils per 1.0 x 104
g m 2 o n u n c o a t e d stents (p < .05). T w o hours after stent
placement, there w e r e 48.0 _+ 8.6 red b l o o d cells per 1.0
× 104 btm 2 o n coated stents c o m p a r e d with 244.3 _+ 26.4
red b l o o d cells per 1.0 _+ 104 btm 2 o n u n c o a t e d stents (p
< .05). Four hours after stent placement, there were 49.5
FIGURE 8. Scanning electron microscopic images of coated and uncoated
stents analyzed 30 min, 2 hr, and 4 hr after stent placement (original magnifi-
cation, ×150).
-+ 11.3 red b l o o d cells per 1.0 + 10 4 btm 2 o n coated stents
c o m p a r e d with 239.5 + 41.8 red blood ceils per 1.0 x 104
t,tm 2 o n u n c o a t e d stents (p < .05).
Neointimal Hyperplasia
Gross examination. On the uncoated stents, exami-
nation of the interior of the vessels s h o w e d a variable
but unusually thick layer of neointima, with essentially
100% stent coverage (Fig. 11), w h e r e a s o n the coated
stents a thin layer of neointima w a s o b s e r v e d in the
interior o f the vessels (Fig. 12). Gross examination of

+1+l++O ~mt~ ~mnt

"~ 120
115
.03 I t I Illlixll
105
<

O 30 60 90 120 150 180

Time ( min. )
FIGURE 9. Scanning electron microscopic images of coated and uncoated
FIGURE 7. Time-activity curves for coated and uncoated stents after reinfu- stents analyzed 30 min, 2 hr, and 4 hr after stent placement (original magnifi-
sion of platelets labeled with indium-111 oxine. cation, ×500).

585
MATSUHASHI ET AL. vol. 3, No. 7, July 1996

stent. Histopathologic examination of the veins with

300
coated stents showed thinner intimal hyperplasia than
~D 250 veins with uncoated stents.
X Morphometric analysis revealed a mean neointimal
q 200 thickness of 0.48 +_0.23 mm in the veins where uncoated
,,--t
stents were placed. This neointima was significantly
150 coated ] thicker than in the veins where coated stents were
uncoatedJ placed; the mean neointimal thickness was 0.27 _+ 0.08
100
mm (p < .05; Fig. 15).
50
DISCUSSION
0
30 min 2 hours 4 hours The implantation of intravascular stents into arteries or
veins is a simple and safe procedure. Recently, various
FIGURE 10. Number of red blood cells (RBCs) that deposited on the surface
of the stent (mean _+standard deviation). types of metallic filaments such as stainless steel alloys
(304 and 316 L), tantalum, and nitinol have been used in
intravascular stents. 304 stainless steel is an alloy of chro-
mium and nickel (18:8). This type of stainless steel is
used widely in vascular stents such as the Z stent, the
Bird's Nest filter, the Gunter filter, and Gianturco coils.

FIGURE 11. Gross inspection of the left common lilac vein. Note the thick
neointima covering the uncoated stent.

FIGURE 13. Light microscopic specimen of the left common lilac vein. Stent
struts are surrounded by some foreign bodies. The holes were caused by re-
moval of the stent struts from the tissue (elastica-Masson's stain, x40),

FIGURE 12. Gross inspection of the right common iliac vein. Note the thin
neointima covering the coated stent compared with the left common lilac vein.

both types of stents showed no thrombus and no evi-

dence of vascular injury related to stent compression.
Neointimal thickness. Figure 13 shows the typical histo-
logic appearance of a vessel with an uncoated stent. His-
topathologic examination of the veins with uncoated
stents showed variable intimal thickening. The intimal
proliferation was composed mainly of fibroblasts, smooth-
muscle cells, and connective tissue. Figure 14 shows the
FIGURE 14. Light microscopic specimen of the right common iliac vein. Stent
typical histologic appearance of a vessel with a coated struts are surrounded by some foreign bodies (elastica-Masson's stain, ×40).

586
Vol. 3, No. 7, July 1996
.8 ¸
g.7
.6
.5
.4
-~ .3
Z .2
uncoated coated
FIGURE 15, Neointimal thickness (mean _+standard deviation) associated with
uncoated and coated stents 4 weeks after stent placement (p < .05).
However, in clinical studies, thrombus formation remains
a serious problem associated with stent placement
despite aggressive antithrombotic therapy [11]. In large
vessels with fast blood flow rates, thrombotic occlusion
of the stent is unlikely. However, in smaller vessels, par-
ticularly veins, the thrombogenicity of stents can result in
a high failure rate.
To avoid acute thrombosis, anticoagulative agents are
given IV or orally before, during, and after stent inser-
tion. Palmaz et al. [10] analyzed the thrombogenicity of
vascular stents with respect to various anticoagulants
and determined that acute thrombogenicity decreased
as anticoagulation regimens were intensified. Aggressive
anticoagulation is useful, but it increases the frequency
of complications such as hemorrhage or h e m a t o m a at
the puncture site.
Several approaches to improving the antithromboge-
nicity of blood-exposed surfaces in cardiovascular pros-
theses currently are being explored [16, 17]. The
development of some types of antithrombogenic coating
materials for intravascular stents recently has been
reported [12-14]. Okano et al. [18] proposed that the
microdomain-structured polymer surface, constructed of
hydrophilic and hydrophobic sites on the level of assem-
bled macromolecutes, is an important parameter. Kawa-
hito et al. [15] reported a FASUS copolymer as an
antithrombogenic coating material for a circulatory-assist
device in 1993. They evaluated the effectiveness of the
FASUS copolymer in a venoarterial bypass circuit in dogs.
The assessment of platelet deposition in vivo using scin-
tigraphy with 111In-oxine-labeled platelets provides a mea-
sure of quantifying thrombus formation [19]. In the current
study, continuous recording of the activity allowed the
study of thrombus deposition on the stent surface. An
immediate reaction was observed that involved a rapid
C O A T I N G MATERIAL FOR I N T R A V A S C U L A R S T E N T S
increase in platelet deposition during the first 90 min at
the uncoated stent site. Deposition was less pronounced
at the coated stent site during the first 180 rain.
The FASUS copolymer has an alternate hydrophilic
and hydrophobic lamellar structure, with a segregated
microdomain structure. The structure has the ability to
suppress platelet adhesion and the morphologic changes
of the adhering platelets [18].
When a foreign-body surface is in contact with blood,
the surface immediately is covered with plasma protein
before it interacts with the platelets. Therefore, platelets
adhere to the surface of the blood protein layer that is
formed on the foreign-body surface. The protein layer on
the surface affects platelet adhesion and aggregation. It
has been found that albumin selectively adsorbed on the
hydrophilic microdomains and T-globulin and that fibrino-
gen adsorbed on the hydrophobic microdomains [20].
Therefore, an organized protein layer was formed on the
microdomain surface and was assumed to regulate the
distribution of different binding sites on a molecular level
at the platelet-block copolymer interface. Although re-
versible adhesion of platelets was influenced by tile
strength and number of binding sites at the platelet-poly-
met interface, suppression of irreversible platelet adhesion
was influenced more by the distribution of binding sites
than by the strength of the binding [20]. Alternate lamellar
microdomain structures appear to exhibit a remarkable
suppressive effect on platelet adhesion and morphologic
changes of adhered platelets.
In this way, the lamellar structure of this material was
expected to suppress contact-induced platelet adhesion
and aggregation. Once platelet adhesion and morpho-
logic changes are suppressed, deposition of red blood
cells induced by the platelets also is thought to be inhib-
ited. Scanning electron microscopic results showed that
deposition of red blood cells on the surface of the stent
also was significantly inhibited by the FASUS copolymer.
Clinical vascular stent placement has b e e n compli-
cated by both early thrombosis and subsequent neoint-
imal hyperplasia leading to restenosis. Although our
study was limited, we found that neointimal thickness 4
w e e k s after stent placement was significantly less than
on the site of the uncoated stent. Salam et al. [21] found
that stents were associated with the development of a
significant degree of neointimal hyperplasia during the
blood vessel's healing process. Angelini et al. [22] found
that late restenosis appears to be the result of both ind-
real thickening caused by migration and proliferation of
smooth-muscle ceils.
587
MATSUHASHI ET AL.
Palmaz [231 found that t~e l:hickness of the formed
neointima after stent placement was increased signifi-
cantly by the presence of prior platelets on the surface of
the vascular stent. This relationship between platelet
deposition and neointimal hyperplasia may be explained
partly by the release of platelet-derived growth factor
from the alpha granules of the deposited platelets. Plate-
let-derived growth factor is one of many growth factors
involved in intimal thickening. In arteries, when some
growth factors are released, the thrombotic layer cove>
ing the stent struts is replaced slowly by fibromuscular
tissue in 3-4 weeks. This tissue then is replaced by col-
lagen, which decreases luminal diameter 8-12 weeks
after stent placement. In veins, when some growth fac-
tors are released, the thrombotic layer covering the stent
struts is replaced progressively by fibromuscutar tissue in
a few days to weeks. This tissue then is progressively
replaced by collagen 4-8 weeks after stent placement.
Many researchers have argued the importance of inhibit-
ing acute thrombosis in order to regulate late intimal
proliferation, especially in veins. In our research, acute
thrombus deposition was inhibited by the FASUS copoly-
mer. We assumed that the release of some growth factors
such as platelet-derived growth factor also was probably
inhibited and that it led to thin neointimal thickness
compared with the site of uncoated stents.
In summary, our research shows that the FASUS copoly-
mer coating for the vascular stent was effective in preventing
acute thrombus deposition under anticoagulant, agent-
free conditions and that it also inhibits the formation of
neointimal hyperplasia during the blood vessel's healing
process. More research is needed to determine the indica-
tions for this coating material for vascular stents.
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