Chronic Arterial Responses to Overlapping Paclitaxel-Eluting Stents
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1 JACC: CARDIOVASCULAR INTERVENTIONS VOL. 1, NO. 2, BY THE AMERICAN COLLEGE OF CARDIOLOGY FOUNDATION ISSN /08/$34.00 PUBLISHED BY ELSEVIER INC. DOI: /j.jcin Chronic Arterial Responses to Overlapping Paclitaxel-Eluting Stents Insights From Serial Intravascular Ultrasound Analyses in the TAXUS-V and -VI Trials Jiro Aoki, MD, PHD,* Gary S. Mintz, MD, FACC,* Neil J. Weissman, MD, FACC, J. Tift Mann, MD, FACC, Louis Cannon, MD, FACC, Joel Greenberg, MD, FACC, Eberhard Grube, MD, FACC, A. R. Zaki Masud, MD, FACC,# Joerg Koglin, MD,** Lazar Mandinov, MD, PHD,** Gregg W. Stone, MD, FACC* New York and Buffalo, New York; Washington, DC; Raleigh, North Carolina; Petoskey, Michigan; Orlando, Florida; Seigburg, Germany; and Natick, Massachusetts Objectives The purpose of this study was to use intravascular ultrasound (IVUS) to investigate chronic arterial responses at the site of and adjacent to overlapping paclitaxel-eluting TAXUS stents (PES) compared with overlapping bare-metal stents (BMS). Background Increased paclitaxel dose in the PES-overlap region might be associated with arterial toxicity expressed as excessive expansive remodeling, incomplete stent apposition, or aneurysm formation. Methods In the TAXUS-V and -VI trials, 51 patients with overlapping stents (27 PES and 24 BMS) were imaged with serial IVUS immediately after procedure and at 9 months. The IVUS measurements included intimal hyperplasia (IH), peri-stent plaque plus media (P&M), and external elastic membrane (EEM) areas. Vascular responses were assessed at the proximal and distal single stent strut regions and the central overlap region. Results Compared with BMS, all 3 PES stent regions showed: 1) significantly decreased IH (proximal: mm 2 vs mm 2, overlap: mm 2 vs mm 2, distal: mm 2 vs mm 2, all p 0.05); and 2) increased P&M and EEM areas (Delta P&M; proximal: mm 2 vs mm 2, overlap: mm 2 vs mm 2, distal: mm 2 vs mm 2, all p 0.05). The IH and changes in EEM and P&M areas were not significantly different in both the BMS and PES groups comparing the single stent strut and overlap regions. Incomplete stent apposition did not occur at the site of overlapping PES in any patient. Conclusions Nine months after stent implantation, neointimal tissue growth was reduced and expansive remodeling was greater with PES compared with BMS effects that were not exaggerated at the overlap region of PES. (J Am Coll Cardiol Intv 2008;1:161 7) 2008 by the American College of Cardiology Foundation From *Columbia University Medical Center and Cardiovascular Research Foundation, New York, New York; Cardiovascular Research Institute, Washington Hospital Center, Washington, DC; Wake Heart Research, Raleigh, North Carolina; Cardiac & Vascular Research Center of Northern Michigan, Petoskey, Michigan; Florida Heart Institute, Orlando, Florida; Helios Klinikum, Siegburg, Germany; #Buffalo General Hospital, Buffalo, New York; and **Boston Scientific Corp., Natick, Massachusetts. Drs. Mintz, Weissman, Mann, Cannon, Greenberg, Grube, and Stone have received research grants from Boston Scientific; Drs. Mintz, Weissman, and Cannon are on Boston Scientific Speaker s Bureau and have received honoraria; Drs. Mintz, Weissman, Cannon, Greenberg, and Stone are on the Boston Scientific Consultant/Advisory Boards; and Drs. Koglin and Mandinov are employed by Boston Scientific. Manuscript received October 12, 2007; revised manuscript received December 3, 2007, accepted December 10, 2007.
2 162 JACC: CARDIOVASCULAR INTERVENTIONS, VOL. 1, NO. 2, 2008 Growing evidence supports the clinical benefit of paclitaxeleluting stents (PES) across a broad range of patient and lesion types (1 4). However, stent overlap is associated with more frequent angiographic restenosis even with drugeluting stents (DES) (2). Whereas only 1 stent/lesion was implanted in the TAXUS-II and -IV trials, TAXUS-V and -VI permitted overlapping stents for longer lesions (1,2,5,6). An experimental study using balloon-injured rabbit iliac arteries showed that overlapping PES resulted in delayed healing compared with adjacent proximal and distal single PES-layer segments (7) and greater inflammation and fibrin deposition than overlapping sirolimus-eluting stents (SES). Conversely, studies in porcine coronary artery models have shown comparable healing for overlapping PES (8). Finally, clinical outcomes after overlapping PES compared with overlapping SES were similar in some real-world observational studies Abbreviations and Acronyms BMS bare-metal stent(s) CSA cross-sectional area DES drug-eluting stent(s) EEM external elastic membrane IH intimal hyperplasia (area) ISA incomplete stent apposition IVUS intravascular ultrasound system PES paclitaxel-eluting stent(s) P&M plaque and media (area) SES sirolimus-eluting stent(s) (9,10). Vascular responses after stent implantation may be assessed with serial angiographic and intravascular ultrasound (IVUS) measurements. Although percent in-stent obstruction in the overlap region based solely on follow-up IVUS analysis was performed in the TAXUS trials (11), peri-stent responses to DES (i.e., outside the stent or between the stent and the vessel wall) have been incompletely characterized (12). Early assessments of volumetric changes outside DES reported a dosedependent and partially reversible increase in arterial dimensions over time when compared with bare-metal stents (BMS) (13). These findings were hypothesized to reflect a controlled biologic response to the implantation of polymeric DES. Along with the comparison of different dose formulations, such as slow- versus moderate-release PES in the TAXUS-II trial (14), the implantation of overlapping stents represents another internally controlled model allowing examination of chronic vessel reactions to varying local paclitaxel doses by comparing the proximal and distal single stent strut regions with the central overlap region. The objective of the present analysis was to use serial (baseline and follow-up) IVUS studies from the randomized TAXUS-V and -VI multicenter studies to study chronic arterial responses to overlapping PES implantation. Methods Patient selection. The study designs and clinical and angiographic outcomes of the prospective, multicenter, doubleblind, controlled TAXUS-V and -VI trials have been described elsewhere (2,6). Briefly, TAXUS-V randomized 1,156 patients to either slow-release PES or visually indistinguishable Express 2 BMS (both Boston Scientific Corp., Natick, Massachusetts). The TAXUS-VI randomized 446 patients to either moderate-release PES or Express 2 BMS (both Boston Scientific Corp.). Patients with single de novo lesions, 10 to 46 mm in length, in a native coronary artery with reference vessel diameter between 2.25 and 4.0 mm were enrolled in TAXUS-V, whereas patients with single de novo lesions 18 to 40 mm long in a native coronary artery with reference vessel diameter between 2.5 and 3.75 mm were enrolled in TAXUS-VI. By protocol, multiple stents were required for lesions 26 mm in length, in which case 4 mm of stent overlap was specified in both studies to ensure the absence of gaps. Of 1,602 total patients, 80 who were treated with overlapping stents were assigned to a substudy that included baseline and follow-up IVUS imaging and analysis. However, among these 80 patients, 19 did not have IVUS at implantation; and the overlap region could not be differentiated from the adjacent single-pes layer in an additional 10 patients. The remaining 51 patients (27 PES and 24 BMS) were included in the present study. All patients provided written informed consent, and this investigation was approved at the local institutional review board or ethics committee of each participating center. Quantitative IVUS analysis. The IVUS imaging was performed after intracoronary administration of 0.1 to 0.2 mg nitroglycerin with motorized pullback (0.5 mm/s) and contemporary commercial scanners. Images were recorded onto s-vhs videotape or digitally onto CD or MO disc for offline core laboratory analysis. These images were analyzed according to published standards, with computerized planimetry (Tapemeasure, Indec Inc., Mountain View, California) by an independent core laboratory (Washington Hospital Center, Washington, DC) that remained blinded to treatment allocation (15). The stented lesion was divided into 3 regions according to location: 1) proximal single stent layer; 2) middle overlapping double stent layers; and 3) distal single stent layer (Fig. 1). External elastic membrane (EEM), stent, and lumen cross-sectional areas (CSA) were measured for each millimeter. Peri-stent plaque and media (P&M) CSA (P&M EEM stent) and intimal hyperplasia (IH) CSA (IH stent lumen) were calculated for each millimeter. The results are expressed as the average of the individual cross-sectional slices within each region. Although every attempt was made to analyze EEM CSA for each millimeter throughout the stented segment, it was not possible in all patients, because in come cases the stent artifact obscured
3 JACC: CARDIOVASCULAR INTERVENTIONS, VOL. 1, NO. 2, Figure 1. Three Regions in the Overlapping Stented Lesion The stented lesion was divided into 3 regions (proximal single stent layer, middle overlapping double stent layers, and distal single stent layer). the media-adventitia border. Therefore, for the purpose of the current analysis, we excluded segments in which 25% of the length of the EEM was not identifiable (16). Asa result, EEM analysis was possible in 26 patients (96.3%) in the PES group and in 21 patients (87.5%) in the BMS group. Incomplete stent apposition (ISA) was defined as 1 or more stent struts clearly separated from the vessel wall with evidence of blood flow behind the struts and not overlapping a side branch (13,17). Incomplete stent apposition was classified as 1 of 3 types. Resolved ISA was defined as ISA that was present at implantation but disappeared during follow-up. Persistent ISA was defined as ISA that was present both at implantation and at follow-up. Late acquired ISA was defined as ISA that was absent at implantation but present at follow-up. When ISA was detected, P&M area was calculated as EEM CSA stent CSA ISA CSA. Statistical analysis. Discrete variables are displayed as percentages and tested with Fisher exact test. Continuous variables are expressed as mean SD and compared with paired or unpaired Student t test or analysis of variance as appropriate. Linear regression was performed to assess the correlation between different IVUS outcomes. A value of p 0.05 was considered statistically significant. Results The PES and BMS groups were well-matched with respect to clinical and lesion characteristics (Table 1). Average implanted stent length, stent diameter, and overlap length Table 1. Baseline Characteristics PES (n 27) BMS (n 24) p Value Age, yrs (27) (24) 0.94 Gender male, % 70.4% (19/27) 66.7% (16/24) 1.00 Current smoking, % 11.1% (3/27) 25.0% (6/24) 0.28 Diabetes mellitus, % 40.7% (11/27) 37.5% (9/24) 1.00 Hypertension, % 66.7% (18/27) 58.3% (14/24) 0.57 Unstable angina, % 44.4% (12/27) 37.5% (9/24) 0.78 Prior myocardial infarction, % 22.2% (6/27) 33.3% (8/24) 0.53 Statin prescription at discharge, %* 85.0% (17/20) 72.2% (13/18) 0.44 Treated vessel Left anterior descending coronary artery, % 44.4% (12/27) 25.0% (6/24) 0.24 Left circumflex coronary artery, % 22.2% (6/27) 16.7% (4/24) 0.73 Right coronary artery, % 33.3% (9/27) 58.3% (14/24) 0.10 Reference vessel diameter, mm (27) (24) 0.20 Lesion length, mm (27) (24) 0.23 Total stent length, mm (27) (24) 0.66 Average stent diameter, mm (27) (24) 0.23 *TAXUS-V patients only. BMS bare-metal stent; PES paclitaxel-eluting stent.
4 164 JACC: CARDIOVASCULAR INTERVENTIONS, VOL. 1, NO. 2, 2008 Table 2. Intravascular Ultrasound Measurements at Post-Procedure and Follow-Up PES BMS Post-Procedure Follow-Up p Value Post-Procedure Follow-Up p Value Proximal region (single stent layer) EEM area, mm (26) (26) (21) (21) 0.89 Stent area, mm (27) (27) (24) (24) 0.84 Lumen area, mm (27) (27) (24) (24) IH area, mm (27) (24) Peri-stent P&M area, mm (26) (26) (21) (21) 0.94 Length, mm (27) (27) (24) (24) 0.35 Overlap region (double stent layers) EEM area, mm (26) (26) (21) (21) 0.93 Stent area, mm (27) (27) (24) (24) 0.27 Lumen area, mm (27) (27) (24) (24) IH area, mm (27) (24) Peri-stent P&M area, mm (26) (26) (21) (21) 0.48 Length, mm (27) (27) (24) (24) 0.92 Distal region (single stent layer) EEM area, mm (26) (26) (24) (24) 0.71 Stent area, mm (27) (27) (24) (24) 0.23 Lumen area, mm (27) (27) (24) (24) IH area, mm (27) (24) Peri-stent P&M area, mm (26) (26) (24) (24) 0.54 Length, mm (27) (27) (24) (24) 0.12 BMS bare-metal stent; EEM external elastic membrane; IH intimal hyperplasia; P&M plaque and media; PES paclitaxel-eluting stent. (PES: mm vs. BMS: mm, p 0.50) were also comparable between the 2 groups (Table 2). Overlapping BMS. In lesions treated with BMS, there were no statistically significant changes in serial (baseline vs. follow-up) measures of the EEM, stent, or peri-stent P&M CSA in the proximal, overlap, or distal stent regions. Lumen CSA significantly decreased in both the single stent and overlap regions during the 9-month follow-up period (Table 2). The IH CSA and serial changes in EEM, stent, and peri-stent P&M area were not significantly different among the proximal, overlap, and distal BMS regions (Table 3). At follow-up, ISA was found in 4.2% of the proximal regions but in none of the overlap or distal regions (p 0.36). Overlapping PES. Unlike BMS-treated lesions, there was an overall increase in EEM and peri-stent P&M areas in all 3 PES segments (proximal, overlap, and distal). Stent CSA did not change, but lumen CSA decreased during the Table 3. Comparison of Vessel Responses Among the 3 Regions Proximal Region Overlap Region Distal Region p ANOVA PES IH area, mm (27) (27) (27) 0.38 Peri-stent P&M area, mm (26) (26) (26) 0.21 % Peri-stent P&M area (26) (26) (26) 0.28 EEM area, mm (26) (26) (26) 0.38 % EEM area (26) (26) (26) 0.31 BMS IH area, mm (24) (24) (24) 0.85 Peri-stent P&M area, mm (21) (21) (24) 0.48 % Peri-stent P&M area (21) (21) (24) 0.40 EEM area, mm (21) (21) (24) 1.00 % EEM area (21) (21) (24) 0.95 Numbers in parenthesis indicate the number of segments available for serial intravascular ultrasound analysis. ANOVA analysis of variance; other abbreviations as in Table 2.
5 JACC: CARDIOVASCULAR INTERVENTIONS, VOL. 1, NO. 2, month follow-up period (Table 2). More than threequarters of PES-treated lesions showed an increase in peri-stent P&M area (proximal region: 73.1%; overlap region: 84.6%; and distal region: 80.8%). The increase in EEM CSA was similar to the increase in peri-stent P&M CSA, indicating that vessel remodeling outside the stent paralleled the increase in peri-stent plaque (Table 3). Similar to BMS-treated lesions, IH area and serial changes in peri-stent P&M and EEM CSA were not significantly different among the 3 regions (Table 3). When the vascular responses to the slow-release PES stents used in TAXUS-V were compared with the moderate-release PES stents in TAXUS-VI, there was a non-significant trend toward an increase in peri-stent P&M CSA in the moderate release PES-treated lesions in all 3 regions: proximal region, mm 2 versus mm 2 (p 0.39); central overlap region, mm 2 versus mm 2 (p 0.40); and distal region mm 2 versus mm 2 (p 0.51). At 9 months follow-up among PES-treated lesions, ISA was found in 11.1% of the proximal regions and in 7.4% of the distal regions but not in any of the overlap regions (p 0.22). BMS versus PES stents. Comparing the vascular responses between PES and BMS, PES-treated lesions had reduced IH CSA in the proximal, overlap, and distal stent regions (Table 4). Although the difference did not reach statistical significance, IH area tended to be less in the PES overlap region than in single strut PES regions ( mm 2 vs mm 2,p 0.27), whereas the opposite trend was noted with BMS ( mm 2 vs mm 2,p 0.34). Furthermore, a greater increase in EEM CSA and peri-stent P&M CSA was present with PES compared with BMS, consistent with a greater degree of expansive remodeling (Table 4). There were no significant differences in the frequency of ISA with PES and BMS in either the single stent or multiple overlapping stent regions. For lesions treated with BMS, significant correlations were found between the degree of neointimal growth (IH) and the degree of outward remodeling (delta EEM) in all 3 regions (R 0.67, p in the proximal; R 0.51, p 0.02 in the overlap; and R 0.50, p 0.01 in the distal region). However, these correlations were not observed in lesions treated with PES (R 0.12, p 0.54 in the proximal; R 0.15, p 0.46 in the overlap; and R 0.03, p 0.89 in the distal region). Discussion Several previous studies (angiographic [18,19], IVUS [20,21], angioscopic [22], and pathologic [7]) have addressed the issue of DES overlap. To our knowledge, there have been 2 published manuscripts in which IVUS analysis was performed after overlapping DES implantations Table 4. Comparison of Vessel Responses Between PES and BMS PES BMS p Value Peri-stent P&M area, mm 2 Proximal region (26) (21) 0.02 Overlap region (26) (21) 0.02 Distal region (26) (24) 0.03 EEM area, mm 2 Proximal region (26) (21) 0.07 Overlap region (26) (21) 0.04 Distal region (26) (24) 0.01 IH area, mm 2 Proximal region (27) (24) Overlap region (27) (24) Distal region (27) (24) Late acquired ISA, n (%) Proximal region 3.7% (1/27) 4.2% (1/24) 1.00 Overlap region 0.0% (0/27) 0.0% (0/24) Distal region 7.4% (2/27) 0.0% (0/24) 0.49 Persistent ISA, n (%) Proximal region 7.4% (2/27) 0.0% (0/24) 0.49 Overlap region 0.0% (0/27) 0.0% (0/24) Distal region 0.0% (0/27) 0.0% (0/24) Resolved ISA, %n(%) Proximal region 0.0% (0/27) 8.3% (2/24) 0.22 Overlap region 0.0% (0/27) 0.0% (0/24) Distal region 0.0% (0/27) 4.2% (1/24) 0.47 ISA incomplete stent apposition; other abbreviations as in Table 2. (20,21). Kang et al. (20) presented a comparison of IVUS outcomes after different-des overlap and same-des overlap. The IH and EEM CSA at the overlapping site were not significantly different between the 2 groups. However, there was no comparison between DES overlap and BMS overlap. In addition, this analysis was based only on follow-up IVUS analysis. Therefore, analyses of vessel remodeling and detailed ISA (late acquired, persistent resolved) were not possible. Kawaguchi et al. (21) presented angiographic and IVUS outcomes after BMS overlap and 3 different types of DES overlap implantation in patients with diabetes. Percent IH was less in the DES arms than the BMS arm in both overlap and non-overlap regions. The EEM area at postprocedure and follow-up was analyzed. However, there was no serial analysis. In addition, ISA was not observed at post-procedure and follow-up in all patients. Detailed serial ISA analysis was not possible. The present analysis represents the first manuscript to investigate vessel response inside and outside the overlapping stent region, including detailed ISA analysis. The major findings of this serial IVUS analysis of overlapping BMS and PES are as follows: 1) compared with BMS-treated lesions, neointimal growth in PES-treated lesions was significantly reduced in the central overlap region as well as the adjacent proximal and distal non-overlapped regions; 2) in all 3 regions the
6 166 JACC: CARDIOVASCULAR INTERVENTIONS, VOL. 1, NO. 2, 2008 increase in EEM and peri-stent P&M areas in PES-treated lesions was significantly greater than in BMS-treated lesions, and more than three quarters of PES-treated lesions showed an increase in peri-stent P&M area in both single strut and overlap regions; 3) among the 3 regions the relative changes in IH, EEM, and peri-stent P&M areas were not significantly different in the both BMS and PES groups; and 4) late acquired ISA was not observed in the PES overlap region. Vascular remodeling after BMS and PES. An increase in peri-stent P&M area after single PES implantation has been observed in several studies with both slow- and moderate-release PES in TAXUS-II and with slow-release PES in TAXUS-IV (13,14,23). Similarly, Petronio et al. (16) reported a slight increase in peri-stent P&M area after slow-release PES implantation in the left anterior descending coronary artery. The present study thus confirms that PES result in greater increases in EEM and peri-stent P&M areas than with BMS, at both the site of overlapping stent struts and adjacent proximal and distal single stent regions. Whereas swine studies have shown comparable endothelial cell coverage in the PES overlap zone (24), increased paclitaxel or sirolimus elution from overlapping stents results in delayed healing and arterial toxicity in the rabbit injured iliac model (7). Concern has thus been raised about the potential for drug toxicity at the site of overlapping PES, because of greater dose at this site (25). In TAXUS-II the degree of peri-stent P&M area increase was exaggerated with moderate-release PES compared with the slow-release formulation, potentially explained by the greater paclitaxel release during either the burst phase within hours after stent implantation or the 3- to 8-fold total increased paclitaxel dose eluted (in vitro). In the present study, however, exaggerated vascular responses were not seen at the PES overlap site, although a trend was present toward greater expansive remodeling with the moderate-release PES. High doses of paclitaxel might also be expected to result in an increased incidence of late acquired ISA. The antimetabolic effect of higher-dose paclitaxel theoretically might induce focal necrosis or apoptosis and generate a new empty space between the struts and the vessel wall (26). In the present study, however, ISA also did not occur at the site of overlapping PES. Thus it would seem that overlapping the commercially available slow-rate release PES does not result in excessive expansive remodeling or adverse vascular responses, either because doubling the paclitaxel dose remains below the toxic threshold or because the arterial drug concentration in the overlap region might not be twice as great as a single layer region (27). An additional reason why vascular toxicity might not have been seen in the present report in contrast to the aforementioned animal study was that the length of overlap was significantly shorter in the current study (mean 4 mm vs. 9.8 mm) (7). IH. In the current study, neointimal growth was significantly inhibited for PES compared with BMS in the overlap region and in the adjacent proximal and distal single strut regions. Although the difference did not reach statistical significance, the IH area was lowest in the overlap region of PES-treated lesions compared with non-overlap regions. Although overlapping BMS struts might induce more medial injury and a subsequent increase in IH (28,29), this effect seems to be counteracted by the increased drug density at the overlap site of PES. Considering that immature endothelial coverage of stent strut is a predictor of late stent thrombosis (30), a longer clinical follow-up of patients with overlapping stents should be reassuring in future studies. Study limitations. Several limitations of the present study should be noted. Factors unrelated to the stent might play a role in vessel remodeling (31). Drugs such as statins and antihypertensive agents influence the change in plaque volume (32 34). Although the prevalence of statin use was similar between PES and BMS groups, detailed lipid levels were not measured and this influence cannot be totally excluded. Not all patients in the substudy had baseline and follow-up IVUS. The entire length of the EEM could not be measured in each patient, because of stent shadowing or artifact. Finally, this study comprised a relatively modest number of patients. It might be possible that a larger sample size would have been able to show significantly different vessel remodeling among the 3 regions in the lesions treated with overlapping PES. In addition, the number of patients enrolled receiving the slow-release and moderate-release PES was insufficient to allow definitive conclusions to be drawn regarding differential vascular responses between the 2 PES types. Further IVUS investigation involving large numbers of patients after DES overlap implantation is warranted. Conclusions Nine months after implantation of overlapping stents, neointimal tissue growth inside PES was significantly reduced compared with BMS at the expense of greater expansive remodeling. In the PES group, exaggerated vascular responses were not present in the overlap region compared with the adjacent proximal or distal single stent regions, and ISA was not observed at the site of PES overlap. Reprint requests and correspondence: Dr. Gary S. Mintz, Cardiovascular Research Foundation, 111 East 59th Street, 11th Floor, New York, New York gmintz@crf.org.
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