(Circulation. 1999;100:1872-1878.)
© 1999 American Heart Association, Inc.
Clinical Investigation and Reports |
Angiographic Patterns of In-Stent Restenosis
Classification and Implications for Long-Term Outcome
From the Angiographic Core Laboratory and Intravascular Ultrasound Imaging and Cardiac Catheterization Laboratories, Washington Hospital Center, Washington, DC.
Correspondence to Roxana Mehran, MD, Cardiovascular Research Foundation, Washington Hospital Center, 110 Irving St NW, Suite 4B-1, Washington, DC 20010.
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Abstract |
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Background—The angiographic presentation of in-stent restenosis (ISR) may convey prognostic information on subsequent target vessel revascularizations (TLR).
Methods and Results—We developed an angiographic classification
of ISR according to the geographic distribution of intimal hyperplasia
in reference to the implanted stent. Pattern I includes focal
(
10 mm in length) lesions, pattern II is ISR>10 mm within
the stent, pattern III includes ISR>10 mm extending outside the
stent, and pattern IV is totally occluded ISR. We classified a total of
288 ISR lesions in 245 patients and verified the angiographic accuracy
of the classification by intravascular ultrasound. Pattern I was found
in 42% of patients, pattern II in 21%, pattern III in 30%, and
pattern IV in 7%. Previously recurrent ISR was more frequent with
increasing grades of classification (9%, 20%, 34%, and 50% for
classes I to IV, respectively; P=0.0001), as was
diabetes (28%, 32%, 39%, and 48% in classes I to IV, respectively;
P<0.01). Angioplasty and stenting were used
predominantly in classes I and II, whereas classes III and IV were
treated with atheroablation. Final diameter stenosis ranged
between 21% and 28% (P=NS among ISR patterns). TLR
increased with increasing ISR class; it was 19%, 35%, 50%, and 83%
in classes I to IV, respectively (P<0.001).
Multivariate analysis showed that diabetes
(odds ratio, 2.8), previously recurrent ISR (odds ratio, 2.7), and ISR
class (odds ratio, 1.7) were independent predictors of TLR.
Conclusions—The introduced angiographic classification is prognostically important, and it may be used for appropriate and early patient triage for clinical and investigational purposes.
Key Words: restenosis • angioplasty • stents • angiography
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Introduction |
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Stents reduce angiographic restenosis in comparison with balloon angioplasty.1 2 The rate of in-stent restenosis (ISR), although less frequent than postangioplasty restenosis, is becoming increasingly prevalent due to the recent exponential increase in the use of intracoronary stents. Prior studies showed that tubular slotted stents do not recoil and do not allow geometric arterial constriction, which may account for up to 55% of lumen loss in the restenotic process after angioplasty or atherectomy.3 4 5 Therefore, ISR is due to neointimal hyperplasia.6 7 8 The patterns of in-stent restenosis have been described before as either diffuse (lesion>10 mm in length) or focal (lesion<10 mm in length). Previous studies showed a high recurrence rate after treating diffuse ISR with conventional balloon angioplasty.9 10 11 Atheroablative devices (ie, excimer laser coronary angioplasty [ELCA] and rotational atherectomy [RA]) have been used in an attempt to improve results.12 13 However, thus far, no devices have significantly improved outcomes after the treatment of diffuse ISR.
Aside from lesion length, other morphological ISR patterns have not been described or related to prognosis. We developed an angiographic classification for ISR, which was verified by using intravascular ultrasound (IVUS), and assessed long-term clinical follow-up to determine whether this classification schema conveyed important prognostic information.
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Methods |
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Patient Population and Treatment of ISR
A total of 325 ISR patients were treated at the Washington Hospital Center from January 1, 1995 through July 31, 1997. We excluded patients if they were treated with nontubular slotted stents (n=40), did not undergo IVUS-guided therapy because of operator preference (n=26), or were lost to follow-up (n=14). The remaining 245 patients were included in this study. Devices to treat ISR were chosen by the operators; they included balloon angioplasty/percutaneous transluminal coronary angioplasty (PTCA), RA, ELCA, and stenting. All devices were applied with standard methods and followed by high-pressure (
12 atm) balloon
dilation within the stented area.
Demographics and Follow-Up
The hospital charts of all patients were reviewed to obtain
clinical demographics and laboratory results. Risk factors for
coronary artery disease that were tabulated included diabetes
mellitus (only if treated medically), hypertension (only if treated
medically), and hyperlipidemia (only if treated
medically or if serum cholesterol was >240 mg/dL).
Clinical follow-up was performed with telephone contacts or office
visits at 1, 3, 6, and 12 months after the procedure. The occurrence of
major late clinical events was recorded; these included death,
Q-wave myocardial infarction, and target lesion site
revascularization (percutaneous or
surgical).
Classification of ISR
Angiograms were reviewed off-line by 2 independent observers who
classified the lesions on separate occasions as follows (Figure
).
- Class I: Focal ISR group. Lesions are
10 mm in length and are
positioned at the unscaffolded segment (ie, articulation or gap), the
body of the stent, the proximal or distal margin (but not both), or a
combination of these sites (multifocal ISR)
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Class II: "Diffuse intrastent" ISR. Lesions are >10 mm in
length and are confined to the stent(s), without extending outside the
margins of the stent(s).
Class III: "Diffuse proliferative" ISR. Lesions are >10 mm in
length and extend beyond the margin(s) of the stent(s).
Class IV: ISR with "total occlusion." Lesions have a TIMI flow
grade of 0.
Angiographic Analysis
An independent core angiographic laboratory performed
qualitative and quantitative angiographic analyses. All
cineangiograms were analyzed using a
computer-assisted, automated, edge-detection algorithm (ARTREK,
Quantitative Cardiac Systems). Using the outer diameter of the
contrast-filled catheter as the calibration, the minimal lumen diameter
(MLD) in diastole before intervention was measured from
multiple projections; the results from the single "worst" view
were recorded. The reference segment diameter was averaged from
user-defined, 5-mm-long, angiographically normal segments proximal and
distal to the lesion but between any major side branches. Lesion length
was measured as the distance (in millimeters) from the proximal
shoulder to the distal shoulder in the projection with the least
amount of foreshortening. Ostial lesions were within 3 mm of the
coronary ostia or <3 mm distal to a major proximal side
branch. These are standard qualitative and quantitative
analyses and definitions, and they have been validated and
published previously.14
IVUS Imaging
A total of 293 lesions in 245 patients were considered for
inclusion in the present analysis. Five lesions were
excluded because they had a poorly visualized stent in the preprocedure
angiogram and IVUS assessment was discordant with the angiographic
class. Preintervention IVUS imaging was available for all patients, and
lesion classification was confirmed qualitatively by IVUS in all 288
lesions included in this study. All IVUS imaging studies were performed
before intervention and only after intracoronary administration
of 200 µg of nitroglycerin. The IVUS studies were
performed using 1 of 2 commercially available systems. The first
(InterTherapy/Cardiovascular Imaging Systems Inc)
incorporated a single-element, 25-MHz transducer and an angled mirror
mounted on the tip of a flexible shaft that was rotated at 1800 RPM
within a 3.9F short monorail polyethylene imaging sheath to form planar
cross-sectional images in real time. The second
(Cardiovascular Imaging Systems Inc.) incorporated a
single-element, 30-MHz, beveled transducer within either a 2.9F long
monorail imaging catheter having a common distal lumen design (the
distal lumen alternatively accommodates the imaging core or the
guidewire but not both) or a 3.2F short monorail imaging catheter. With
both systems, the transducer was withdrawn automatically at 0.5
mm/s to perform the imaging sequence. The IVUS catheter was advanced at
least 10 mm distal to the lesion, the video recorder was
turned on, the transducer pullback device was activated, and
the entire artery was imaged to the aorto-ostial junction. IVUS studies
were recorded on 1/2-inch high-resolution s-VHS tapes for
off-line analysis. Images were evaluated off-line by an
independent, blinded, core IVUS laboratory to verify the accuracy of
the angiographic classification, given the limited radiopacity of the
stents. The classification schema used was the same used with
angiographic criteria.
Quantitative IVUS Measurements
In-stent restenosis lesion length was measured from
number of seconds on videotape. At a pullback speed of 0.5 mm/s,
2 s of videotape playback equals 1 mm of axial stent length.
This has been validated in vivo.15 In-stent
restenosis length was defined as the axial length of a stented
or nonstented segment (in millimeters) in which 75% of intimal
hyperplasia (for stented segment) or plaque+media (for nonstented
segment) was seen in a cross-sectional area (CSA).
CSA measurements by IVUS have been previously validated.16 17 18 19 20 21 22 23 Area measurements were performed with a commercially available program for computerized planimetry (TapeMeasure, Indec Systems). The smallest lumen and stent cross sections were identified before and after intervention within the stented segments and traced. The intimal hyperplasia CSA was calculated as stent CSA minus lumen CSA. When the plaque encompassed the catheter, the lumen was assumed to be the physical size of the imaging catheter.
Statistics
Statistical analysis was performed using StatView 4.02
(Abacus Concepts) or SAS (Statistical Analysis Systems,
SAS Institute Inc). Categorical data are presented as
frequencies. Data are presented as mean±1SD. Categorical data
were compared using Fisher's exact test. Continuous variables were
compared using factorial ANOVA or ANOVA for repeated measures with post
hoc analysis. P<0.01 was considered significant.
The primary end point was the association of lesion classification with
target lesion revascularization (TLR).
Univariate variables with P<0.2 were
entered into the multivariate model; forward stepping
was used to determine the independent predictors of TLR.
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Results |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Of the 288 lesions analyzed, 42% (n=121) were focal (class I), 21% (n=61) diffuse intrastent (class II), 30% (n=86) diffuse proliferative (class III), and 7% (n=20) total occlusions. Baseline patient characteristics are presented in Table 1
. All groups were well-matched with
respect to age and sex. Increasing levels of ISR classification were
associated with an increasing prevalence of diabetes mellitus (28%,
32%, 39%, and 48% for classes I to IV, respectively;
P<0.01) and the number of prior episodes of ISR (9%, 20%,
34%, and 50% for classes I to IV, respectively;
P<0.01).
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Lesion location, including aorto-ostial position, was comparable in all
ISR classes, as indicated in Table 2.
Device selection was significantly different among the ISR classes.
Lesions were treated predominantly with PTCA and stent alone in classes
I and II, whereas classes III and IV were exclusively treated with an
atheroablative device (RA, ELCA), used either alone or in combination
with stenting (Table 3). Procedural
success was achieved in all cases, without evidence of any abrupt
vessel closure.
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Angiographic Results
By classification definition, lesion length increased with
increasing levels of ISR classification (Table 4). Class I ISR lesions were associated
with larger vessels, and the final MLD achieved was also larger
compared with the other classes. Class IV ISR lesions were associated
with the smallest vessels, and the MLD achieved was the smallest
compared with the other ISR classes. However, all classes achieved
similar percent diameter stenosis after
transcatheter therapy, despite the different
revascularization strategies.
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IVUS Results
Qualitative IVUS analysis completely verified the accuracy
of the angiographic classification of ISR. Quantitative IVUS
measurements (Table 5) verified the
angiographic observations that patterns III and IV occurred in vessels
with smaller reference dimensions that had a smaller postintervention
luminal area. However, the final intimal hyperplasia area was similar
among all groups.
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Long-Term Results
One-year clinical event rates were uniformly high, without
significant differences among the groups with respect to death or
myocardial infarction (Table 6). However,
a significant increase occurred in TLR with increasing levels of ISR
classification (class I, 19%; class II, 35%; class III, 50%; and
class IV, 83%; P<0.0001). This was due to significantly
increasing rates in both percutaneous (15%, 26%,
36%, and 67% in classes I through IV, respectively;
P<0.0001) and surgical (4%, 8%, 14%, and 17% in classes
I through IV, respectively; P<0.0001)
revascularization procedures.
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Multivariate Analysis
We introduced diabetes, reference diameter, final MLD, left
anterior descending artery location, number of implanted stents,
recurrent ISR, stent type and length, lesion length, and the pattern of
ISR according to the introduced angiographic classification in a
multivariable model to identify predictors of TLR. The only
parameters that independently predicted TLR after treatment
of ISR were the pattern of ISR according to the angiographic
classification (odds ratio, 1.7; P=0.0380), occurrence of
previous ISR (odds ratio, 2.7; P=0.0006), and presence of
diabetes mellitus (odds ratio, 2.8; P=0.0003). Final MLD and
reference vessel size were eliminated in this model.
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Discussion |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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ISR presents in various angiographic patterns, which can be classified angiographically. The method of classification we describe relates not only to lesion length but, as introduced in this article for the first time, also to the geographic position of the neointimal proliferative response relative to the initially implanted stent. Angiographic definition of these patterns had an excellent correlation with IVUS assessment, demonstrating that even minimal stent radiopacity was adequate for appropriate recognition of the ISR class angiographically.
The results of the present investigation demonstrate that the classification system we used to characterize the pattern of ISR independently predicted the long-term need for repeat revascularization. The only other 2 predictors were diabetes mellitus and prior episodes of recurrent ISR. In a previous report, we specifically identified diabetes as a powerful determinant of neointimal hyperplasia.24 Furthermore, this finding has been reported by others.25
Characteristics of ISR
The above 3 factors reflect the intrinsic biological property of
the vessel wall to have a tendency to mount an exaggerated
neointimal response to injury. The initial proliferative
stimulus was initial stent implantation. This resulted in
neointimal hyperplasia, and the magnitude of the response
was captured by our classification scheme. Accordingly, this response
was profound in patients who presented with the highest levels
of the classification, ie, proliferative ISR or total occlusion.
Indeed, increasing levels of ISR classification
were characterized by increased plaque burden at the lesion site and
increasing lesion length (Tables 4
and 5). Despite
optimal interventional treatment and achievement of similar final
diameter stenosis, the minimal luminal dimensions were less
favorable in the highest ISR classes. However,
multivariate analysis determined that the
independent predictor of future target vessel failure was the
preintervention ISR pattern (Figure), whereas the final
postprocedure MLD was eliminated. This is a novel paradigm in which a
preintervention variable prevails over the conventional results of
transcatheter therapy with respect to long-term
results.
In addition to the magnitude of intimal hyperplasia, the second characteristic component of this biological phenomenon was the evidence for repeated recurrences after transcatheter therapy. This unique response to vascular injury seen in the highest ISR classes is highly reproducible after repeat vascular injury, with or without a new stent, suggesting a possible genetic basis. We previously reported that intimal hyperplasia thickness is independent of stent size, which implies that ISR disproportionately affects smaller arteries.26 Other groups have also reported on the importance of previous recurrent ISR as a powerful determinant of future target vessel failure.27 Moreover, the time to initial ISR has been reported to correlate with future recurrences.28 These are specific features for ISR that suggest the involvement of a unique response to stent injury in certain individuals that does not conform to the rules identified for post-PTCA restenosis. This response occurs early, is profound, and does not correlate with inadequate device therapy.
The reason for this exaggerated initial neointimal hyperplasia occurring in response to stenting and, subsequently, to any intervention at the target lesion site is unknown. Recent studies have implicated genetic factors in the pathogenesis of ISR (ie, polymorphism of the gene encoding for the angiotensin-converting enzyme correlated with diffuse ISR).29 Although these results are preliminary, they support the theory of an inherent, intrinsic factor as the main driving force of this process, especially in the higher levels of the classification (ie, proliferative ISR or total occlusion).
Treatment of ISR
Percutaneous intervention for ISR is safe and
yields good angiographic results. Previous studies showed similarly
disappointing long-term results after the treatment of diffuse
ISR.
An initial hypothesis was that the tissue within the stent may never be completely ablated and, therefore, it acts a stimulus for further tissue proliferation. The luminal result obtained after the treatment of ISR is never as large as at the time of original stent implantation, and acute tissue recoil may occur.30 The use of stents to treat ISR abolishes the remaining tissue within the original stent, as shown by IVUS. However, despite the full recovery of the original lumen, stents may also have poor long-term results, thereby contributing to the inadequacy of conventional interventional therapies for the treatment of ISR. However, long-term outcome is heavily influenced by preprocedure patient-related (diabetes) and ISR-related (pattern, previous early recurrence) characteristics.
Our study documents the very high rate of subsequent revascularization after interventional therapy with currently available treatment modalities in patients presenting with the higher ISR classes. Because the assignment of an ISR class can be performed angiographically, early triage of these patients to appropriate therapy is feasible. With respect to current research directions, our study provides the means for proper identification of patients who may benefit most from the use of adjunct therapy (ie, radiation, molecular, or medical). Intracoronary radiation was recently reported as an effective treatment for the high-risk ISR population, and it may complement the deficiency of conventional interventional therapies.31
Early and appropriate allocation of healthcare resources for high-risk ISR patients using our angiographic classification may improve cost-effective patient management and help conceptualize newer revascularization strategies.
Limitations
This is a retrospective analysis and is, therefore,
subject to the limitations pertinent to this type of clinical
investigation. Data were retrieved from our Quality Assurance Database.
The database is updated by an independent coordinating center, which
collects and enters the same data for all patients undergoing
percutaneous interventions, regardless of clinical
indications or disease. We needed to verify the accuracy of the
angiographic classification by IVUS and, therefore, excluded patients
without IVUS imaging. Because IVUS is routinely available at our
institution, only a small number of patients were excluded for this
reason. Patients were not excluded because of an inability to cross the
lesion with the IVUS catheter. Patients with total occlusions were also
included.
Conclusions
ISR presents with various angiographic patterns that provide
important prognostic information. Diffuse intrastent, proliferative,
and totally occluded ISRs represent a spectrum of increasing
disease severity (exaggerated neointimal response), which
determines, along with diabetes and previous episodes of recurrent ISR,
long-term outcome. In contrast, luminal dimensions after interventional
therapy are less important determinants of late clinical results after
treatment of ISR. An intrinsic patient-related process seems to be
responsible for the high ISR classes, which suggests that such clinical
presentations may be due to a distinct biological process.
The angiographic classification of ISR provides the means for
appropriate and early patient triage for clinical and investigational
purposes.
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Acknowledgments |
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This study was supported in part by an educational grant from the Cardiovascular Research Foundation, Washington, DC.
Received February 26, 1999; revision received June 25, 1999; accepted July 2, 1999.
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D. Greenberg, A. Bakhai, and D. J. Cohen Can we afford to eliminate restenosis?: Can we afford not to? J. Am. Coll. Cardiol., February 18, 2004; 43(4): 513 - 518. [Abstract] [Full Text] [PDF]
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Y. S. Do, E. Y. Kao, F. Ganaha, H. Minamiguchi, K. Sugimoto, J. Lee, C. J. Elkins, P. G. Amabile, M. D. Kuo, D. S. Wang, et al. In-Stent Restenosis Limitation with Stent-based Controlled-Release Nitric Oxide: Initial Results in Rabbits Radiology, February 1, 2004; 230(2): 377 - 382. [Abstract] [Full Text] [PDF]
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G. W. Stone, S. G. Ellis, D. A. Cox, J. Hermiller, C. O'Shaughnessy, J. T. Mann, M. Turco, R. Caputo, P. Bergin, J. Greenberg, et al. A Polymer-Based, Paclitaxel-Eluting Stent in Patients with Coronary Artery Disease N. Engl. J. Med., January 15, 2004; 350(3): 221 - 231. [Abstract] [Full Text] [PDF]
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M. Degertekin, P. A. Lemos, C. H. Lee, K. Tanabe, J.E. Sousa, A. Abizaid, E. Regar, G. Sianos, W. J. van der Giessen, P. J. de Feyter, et al. Intravascular ultrasound evaluation after sirolimus eluting stent implantation for de novo and in-stent restenosis lesions Eur. Heart J., January 1, 2004; 25(1): 32 - 38. [Abstract] [Full Text] [PDF]
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M. Sahara, H. Kirigaya, Y. Oikawa, J. Yajima, K. Ogasawara, H. Satoh, K. Nagashima, H. Hara, Y. Nakatsu, and T. Aizawa Arterial remodeling patterns before intervention predict diffuse in-stent restenosis: An intravascular ultrasound study J. Am. Coll. Cardiol., November 19, 2003; 42(10): 1731 - 1738. [Abstract] [Full Text] [PDF]
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J. W. Moses, M. B. Leon, J. J. Popma, P. J. Fitzgerald, D. R. Holmes, C. O'Shaughnessy, R. P. Caputo, D. J. Kereiakes, D. O. Williams, P. S. Teirstein, et al. Sirolimus-Eluting Stents versus Standard Stents in Patients with Stenosis in a Native Coronary Artery N. Engl. J. Med., October 2, 2003; 349(14): 1315 - 1323. [Abstract] [Full Text] [PDF]
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F. Alfonso, J. Zueco, A. Cequier, R. Mantilla, A. Bethencourt, J. R. Lopez-Minguez, J. Angel, J. M. Auge, M. Gomez-Recio, C. Moris, et al. A randomized comparison ofrepeat stenting with balloon angioplasty in patients with in-stent restenosis J. Am. Coll. Cardiol., September 3, 2003; 42(5): 796 - 805. [Abstract] [Full Text] [PDF]
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P. A. Lemos, F. Saia, J. M.R. Ligthart, C. A. Arampatzis, G. Sianos, K. Tanabe, A. Hoye, M. Degertekin, J. Daemen, E. McFadden, et al. Coronary Restenosis After Sirolimus-Eluting Stent Implantation: Morphological Description and Mechanistic Analysis From a Consecutive Series of Cases Circulation, July 22, 2003; 108(3): 257 - 260. [Abstract] [Full Text] [PDF]
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C. O. Costantini, A. J. Lansky, G. S. Mintz, K. Shirai, G. Dangas, R. Mehran, M. Fahy, S. Slack, M. Coral, P. S. Teirstein, et al. Intravascular brachytherapy for native coronary ostial in-stent restenotic lesions J. Am. Coll. Cardiol., May 21, 2003; 41(10): 1725 - 1731. [Abstract] [Full Text] [PDF]
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A. Colombo, D. Orlic, G. Stankovic, N. Corvaja, V. Spanos, M. Montorfano, F. Liistro, M. Carlino, F. Airoldi, A. Chieffo, et al. Preliminary Observations Regarding Angiographic Pattern of Restenosis After Rapamycin-Eluting Stent Implantation Circulation, May 6, 2003; 107(17): 2178 - 2180. [Abstract] [Full Text] [PDF]
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R. Waksman, E. Cheneau, A. E. Ajani, R. L. White, E. Pinnow, R. Torguson, R. Deible, L. F. Satler, A. D. Pichard, K. M. Kent, et al. Intracoronary Radiation Therapy Improves the Clinical and Angiographic Outcomes of Diffuse In-Stent Restenotic Lesions: Results of the Washington Radiation for In-Stent Restenosis Trial for Long Lesions (Long WRIST) Studies Circulation, April 8, 2003; 107(13): 1744 - 1749. [Abstract] [Full Text] [PDF]
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R Seabra-Gomes In-stent restenosis: intracoronary {beta}-radiation at the crossroads Eur. Heart J., April 1, 2003; 24(7): 583 - 585. [Full Text] [PDF]
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P. Urban, P. Serruys, D. Baumgart, A. Colombo, S. Silber, E. Eeckhout, A. Gershlick, K. Wegscheider, L. Verhees, R. Bonan, et al. A multicentre European registry of intraluminal coronary beta brachytherapy Eur. Heart J., April 1, 2003; 24(7): 604 - 612. [Abstract] [Full Text] [PDF]
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D. T. Ashby, G. Dangas, E. A. Aymong, I. Iakovou, F. Kuepper, R. Mehran, G. W. Stone, M. B. Leon, and J. W. Moses Effect of percutaneous coronary interventions for in-stent restenosis in degenerated saphenous vein grafts without distal embolic protection J. Am. Coll. Cardiol., March 5, 2003; 41(5): 749 - 752. [Abstract] [Full Text] [PDF]
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N Mercado and P.W Serruys A meta-analytical approach for the treatment of in-stent restenosis Eur. Heart J., February 1, 2003; 24(3): 217 - 218. [Full Text] [PDF]
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A. C. Ferreira, A. A. Peter, T. A. Salerno, H. Bolooki, and E. de Marchena Clinical impact of drug-eluting stents in changing referral practices for coronary surgical revascularization in a tertiary care center Ann. Thorac. Surg., February 1, 2003; 75(2): 485 - 489. [Abstract] [Full Text] [PDF]
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