1830 MIYOSHI T et al. Circ J 2018; 82: ORIGINAL ARTICLE doi: /circj.CJ
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1 1830 MIYOSHI T et al. Circ J 2018; 82: ORIGINAL ARTICLE doi: /circj.CJ Imaging Assessment of Second- and Third-Generation Drug-Eluting Stents on Chronic Coronary Angioscopy Multicenter Study on Intra-Coronary AngioScopy After Stent (MICASA) Prospective Data Analysis Toru Miyoshi, MD; Hiroshi Matsuoka, MD, PhD; Hideo Kawakami, MD, PhD; Kazuoki Dai, MD; Tetsuya Sato, MD, PhD; Kouki Watanabe, MD, PhD; Masaharu Ishihara, MD, PhD Background: The vascular response, in terms of quality and quantity, of the second- and third-generation drug-eluting stents (2G- and 3G-DES, respectively) was assessed prospectively on coronary angioscopy (CAS). Methods and Results: The Multicenter study on Intra-Coronary AngioScopy After Stent (MICASA) is a multicenter CAS registry. A total of 107 DES (71 2G- and 36 3G-DES) were prospectively observed on CAS 8.7±2.7 months after percutaneous coronary intervention. Neointimal coverage (NC) grade was evaluated using a 4-point grading scale, from 0 (no coverage) to 3 (complete coverage). Plaque yellow color (YC) was also assessed using a 4-point grading system, from 0 (white) to 3 (bright yellow). Max-NC (2G-DES vs. 3G-DES: 2.14±0.68 vs. 2.44±0.73, P=0.023); min-nc (1.07±0.48 vs. 1.39±0.60, P=0.002), and dominant-nc (1.57±0.69 vs. 2.08±0.84, P=0.002) were significantly higher and the YC grade (1.23±0.82 vs. 0.86±0.76, P=0.031) significantly lower in the 3G-DES group than in the 2G-DES group. There was no significant difference in the presence of thrombus (28.2% vs. 22.2%, P=0.51) between the 2G- and 3G-DES groups. Conclusions: The higher NC grade and lower YC grade in 3G-DES than in 2G-DES might be associated with better long-term clinical outcome, which remains to be determined in future studies. Key Words: Coronary angioscopy; Second-generation drug-eluting stent; Third-generation drug-eluting stent First-generation (1G) drug-eluting stents (DES) dramatically reduced the rate of in-stent restenosis and target lesion revascularization (TLR) compared with bare metal stents (BMS). 1,2 These stents, however, were also known to cause late and very late stent thrombosis, neoatherosclerosis 3 and peri-stent contrast staining 4 due to poor biocompatible polymer or prolonged drug elution. Thus, the 1G-DES was changed to the second-generation DES (2G-DES), and these problems were thought to be solved. Some problems, however, still existed: thin neointimal coverage (NC) of residual yellow plaque and neoatherosclerosis. 5 In the third-generation DES (3G-DES), the drugs are delivered over 3 months, and the polymers break down completely in 4 months. Although the neointima of 2G- and 3G-DES stent struts have been examined on optical coherence tomography (OCT), the assessment of vascular response of 2G-DES and 3G-DES, 6 in terms of quality and quantity, using coronary angioscopy (CAS), is still unclear. Methods Patients The Multicenter Study on Intra-Coronary Angioscopy after Stent (MICASA) is a prospective multicenter CAS registry conducted in 5 Japanese institutions. The DES of 185 patients were observed using CAS after percutaneous coronary intervention (PCI) between 1 August 2014 and 31 March From this group, 119 patients were observed after PCI for 4 18 months (mean, 8.7±2.7 months). Five BMS patients, 4 zotarolimus-eluting stent (ZES) patients, 1 patient with drug-coated balloon, 1 patient with covered stent, and 1 patient with missing data were excluded. A total of 71 lesions were treated with 2G-DES: 32 lesions were implanted with durable-polymer everolimus-eluting Received December 20, 2017; revised manuscript received February 13, 2018; accepted February 21, 2018; released online March 30, 2018 Time for primary review: 19 days Department of Cardiology, Ehime Prefectural Imabari Hospital, Imabari (T.M., H.M., H.K.); Department of Cardiology, Hiroshima City Hospital, Hiroshima (K.D.); Department of Cardiology, Okayama Red Cross Hospital, Okayama (T.S.); Department of Cardiology, Saiseikai Matsuyama Hospital, Matsuyama (K.W.); and Division of Coronary Heart Disease, Department of Internal Medicine, Hyogo College of Medicine, Nishinomiya (M.I.), Japan Mailing address: Toru Miyoshi, MD, Department of Cardiology, Ehime Prefectural Imabari Hospital, Ishiimachi, Imabari , Japan. mmyrb0807@gmail.com ISSN All rights are reserved to the Japanese Circulation Society. For permissions, please cj@j-circ.or.jp
2 CAS Assessment of DES 1831 Figure 1. Flow chart of patient inclusion. 2G-DES, 2nd-generatin drug-eluting stent; 3G-DES, 3rd-generation drug-eluting stent; BES, biolimus-eluting stent; BP, bioresorbable polymer; DP, durable polymer; EES, everolimus-eluting stent; MICASA, Multicenter Study of Intra-Coronary Angioscopy After Stent; PCI, percutaneous coronary intervention; R, slow-release; SES, sirolimus-eluting stent; ZES, zotarolimus-eluting stent. Figure 2. Definitions of (Upper) neointimal coverage (NC) grade and (Lower) yellow color (YC) grade. stents (DP-EES: Xience V, Abbott Vascular, Santa Clara, CA, USA, n=24; Promus Element TM, Boston Scientific, Natick, MA, USA, n=8); 31 lesions were implanted with slow-releasing ZES (R-ZES: Resolute Integrity TM, Medtronic, Minneapolis, MN, USA); 8 lesions with biolimuseluting stents (BES, Nobori ; Terumo, Tokyo, Japan); and 1 lesion with hybrid stents (DP-EES+R-ZES). A total of 36 lesions were treated with 3G-DES: 26 lesions were implanted with bioresorbable polymer sirolimus-eluting stents (BP-SES; Ultimaster Terumo), and 10 lesions were implanted with BP-EES (Synergy TM ; Boston Scientific). We did not enroll patients with in-stent restenosis (Figure 1). Informed consent was given by each patient and the study protocol was reviewed and approved by the ethics committee of each hospital. CAS Catheterization was performed with a radial, brachial or femoral approach using 6-F guiding catheters. CAS was performed with the FT-203F (FiberTech Co. Ltd., Tokyo,
3 1832 MIYOSHI T et al. Table. Clinical and Lesion Characteristics in the MICASA Study Variable 2G-DES 3G-DES (n=71) (n=36) P-value Time to angioscopy (months) 10.1± ± Age (years) 69.9± ± Men Hypertension DM Dyslipidemia Current smoking Etiology ACS 30 (42.3) 20 (55.6) 0.22 Stable angina 41 (57.8) 16 (44.4) Lesion location LAD LCX RCA ACS No. stents per lesion 1.14± ± Stent diameter (mm) 3.09± ± Stent length (mm) 23.3± ± Medication at follow-up DAPT Statin LDL-C (mg/dl) 84.4± ± Serum Cr (mg/dl) 0.85± ± HbA1c (%) 6.31± ± Data given as mean ± SD, % or n (%). 2G-DES, 2nd-generation drug-eluting stent; 3G-DES, 3rd-generation drug-eluting stent; ACS, acute coronary syndrome; Cr, creatinine; DAPT, dual antiplatelet therapy; DM, diabetes mellitus; HbA1c, hemoglobin A1c; LAD, left anterior descending artery; LCX, left circumflex artery; LDL-C, low-density lipoprotein cholesterol; MICASA, Multicenter Study of Intra-Coronary Angioscopy After Stent; RCA, right coronary artery. Japan) non-obstructive coronary angioscope system and the VISIBLE (FiberTech Co. Ltd.) optical fiber. Stented lesions were observed angioscopically, while blood was cleared from the field of view using an injection of 3% dextran, as previously reported. 7 Angioscopy was recorded using a digital recorder. Each CAS analysis was performed as agreed by 2 independent cardiologists. Evaluation NC grade was evaluated using a 4-point grading scale, from 0 (no coverage) to 3 (complete coverage). We determined maximum (max-) and minimum (min-) NC, dominant-nc grades, and heterogeneity index (HI: max-nc grade minus min-nc grade). Plaque yellow color (YC) was assessed using a 4-grade system, from 0 (white) to 3 (bright yellow). We recorded the maximum YC grade visible for each patient. The presence of thrombus was also assessed (Figure 2). 8 Statistical Analysis JMP version 12 (SAS Institute, Cary, NC, USA) was used to analyze the results. All continuous variables are given as mean ± SD. Comparisons between the 2G- and 3G-DES groups were analyzed using Student s t-test for continuous variables and chi-squared test for discrete variables. Wilcoxon s test was used to analyze the ordinal variables, in particular CAS findings (NC grade, YC grade). Multivariable logistic regression analysis was performed to identify the independent factors for YC grade (YC grades 2 and 3) and the presence of thrombus. P<0.05 was considered to be statistically significant. Results Baseline Characteristics The clinical characteristics of the 2G- and 3G-DES groups are listed in Table. Dual antiplatelet therapy (DAPT) was discontinued by the time of CAS more frequently in the 3G-DES group. There was no difference between the 2 groups in terms of etiology (acute coronary syndrome [ACS] or stable angina pectoris). The duration from PCI to CAS was shorter in the 3G-DES group than in the 2G-DES group (8.8±2.6 months vs. 10.1±2.9 months, P=0.026). The lesion in the left anterior descending artery was more frequently higher in the 2G-DES group than in the 3G-DES group (P=0.024). CAS The CAS findings regarding NC grade are shown in Figure 1. Max-NC (2G-DES vs. 3G-DES: 2.14±0.68 vs. 2.44±0.73, P=0.023), min-nc (1.07±0.48 vs. 1.39±0.60, P=0.002), and dominant-nc (1.57±0.69 vs. 2.08±0.84, P=0.002) grades were significantly higher in the 3G-DES group than in the 2G-DES group. There was no significant difference in HI (1.07±0.68 vs. 1.05±0.67, P=0.85). YC grade (1.23±0.82 vs. 0.86±0.76, P=0.031) was significantly lower in the 3G-DES group than in the 2G-DES group. There was no significant difference in incidence of thrombus (28.2% vs. 22.2%, P=0.51) between the 2 groups. On multivariate analysis, hemoglobin A1c (HbA1c; OR, 3.56; 95% CI: , P=0.028) and morbidity of diabetes
4 CAS Assessment of DES 1833 Figure 3. Maximum neointimal coverage (max-nc) grade, minimum (min)-nc grade and heterogeneity index vs. drug-eluting stent (DES) status. 2G-DES, 2nd-generation drug-eluting stent; 3G-DES, 3rd-generation drug-eluting stent. Figure 4. Yellow color (YC) grade of plaque and incidence of thrombus vs. drug-eluting stent (DES) status. 2G-DES, 2nd-generation drug-eluting stent; 3G-DES, 3rd-generation drugeluting stent. mellitus (DM; OR, 4.78; 95% CI: ) were independent factors for YC grade (YC grade 2 or 3), and dyslipidemia was an independent factor for thrombus (OR, 3.29; 95% CI: , P=0.017). In this study, ACS and 3G-DES were not associated with YC grade or thrombus (Figures 3,4). Discussion In this prospective study, we compared the CAS findings between 2G- and 3G-DES. The main findings were as follows: (1) max-nc, min-nc, and dominant-nc grade were higher in the 3G-DES group than in the 2G-DES group: (2) YC grade was lower in the 3G-DES group than in the 2G-DES group; (3) there was no significant difference between the 2G- and 3G-DES groups in terms of the presence of thrombus; and (4) DM morbidity and HbA1c were correlated with YC grade; and dyslipidemia was correlated with thrombus, on multivariate analysis. We conducted this study to evaluate the clinical efficacy of 3G-DES at mid-term follow-up using CAS. The 3G-DES group had lower YC grade than the 2G-DES group, which may be due to the lower level of neoatherosclerosis in 3G-DES than in 2G-DES or to the difference in baseline patient background between the 3G- and 2G-DES groups. Previously, Nakazawa et al reported the existence of a new atherosclerosis caused by inflammation of 1G-DES, known as neoatherosclerosis. 3 It was well-known that 1G-DES decreased in-stent restenosis, but late and very late stent thrombosis and the late-catch up phenomenon emerged as new problems. Use of a biocompatible polymer and improvement in the pharmacokinetics of drug elution were expected to resolve these problems, but neoatherosclerosis still occurred, even in 2G-DES. 5,8 11 The DESNOTE study showed that the presence of atherosclerosis at follow-up, with or without yellow plaque immediately after PCI, was responsible for the very late stent failure (VLSF). In the DESNOTE study, 360 patients underwent CAS 1 year after DES implantation (1G- and 2G-DES). Patients were classified according to the presence of yellow neointima within the stent, and the incidences of VLSF, cardiac death, myocardial infarction related to the target lesion, and TLR, were compared. During the follow-up interval of 4.3±2.4 years, VLSF occurred more frequently in patients with yellow plaque than in those without yellow plaque. 12 The DESNOTE study suggested that early detection of neoatherosclerosis using CAS can predict VLSF. The 3G-DES is able to elute drugs (sirolimus or everolimus)
5 1834 MIYOSHI T et al. after 3 months and resorb polymer after 4 months. The lower YC grade in the 3G-DES group than in the 2G-DES group may explain the lower rate of neoatherosclerosis. Dai et al compared BMS to 1G- and 2G-DES using CAS in a MICASA retrospective study. 7 Max-NC and min-nc grades were lower in the 1G- and 2G-DES groups than in the BMS group. Moreover, the max-nc grade for the 2G-DES was similar to that with the 1G-DES, but the min-nc grade was higher in the 2G-DES group; the HI, YC grade, and incidence of thrombus were all lower in the 2G-DES than in the 1G-DES group, which in turn was similar to the BMS group. The Dai et al study used both prospective and retrospective data, but in the present study we used only prospective data. From that retrospective study, 7 3G-DES that changes BMS in 4 months after PCI may be efficient to prevent stent failure. The CENTURY II trial demonstrated the non-inferiority of BP-SES to permanent polymer-ees (PP-EES) in terms of the target lesion failure (TLF) at mid-term follow-up (approximately 9 months). 13 Kuramitsu et al reported a substudy of the CENTURY II trial, on the vascular response of BP-SES vs. PP-EES using optical coherence tomography. 6 There were no significant differences between BP-SES and PP-EES in terms of strut coverage (BP-SES vs. PP-EES: 98.98% vs %, P=0.35) and mean neointimal thickness (BP-SES vs. PP-EES: 110±10 μm vs. 93±9 μm, P=0.22). The vascular response of BP-SES and DP-EES was similar. In the CENTURY II substudy, BP-SES was expected to have a good clinical outcome similar to PP-EES. That study, however, did not investigate whether thrombi, neointima and mural thrombus could be differentiated on OCT, therefore thrombi may appear as neointima on OCT. In this prospective study, DM and HbA1c were associated with YC grade and dyslipidemia was correlated with thrombus. The correlation between DM and YC grade has been previously reported. 14,15 This may be due to the level of high-sensitivity C-reactive protein, which was significantly higher in patients with DM than in those without. Vascular inflammation may be associated with YC grade. 14 In contrast, dyslipidemia was associated with thrombus; this is consistent with other investigations, and is due to the increase in platelet-dependent thrombin production in hyperlipidemic patients. 16 Also, platelet-dependent thrombin responds to statin treatment. 17 In addition, hematopoietic cell-derived tissue factor is expressed during activation of coagulation, and the expression is enhanced in thrombosis in hyperlipidemic patients. 18 Therefore, it seems reasonable to infer a correlation between dyslipidemia and in-stent thrombus. The present multivariate analysis yielded results contrary to expectations: stent generation did not affect plaque YC grade or in-stent thrombus formation. Plaque YC grade was, however, affected by DM morbidity and by control of DM and HbA1c. This suggests that prevention of neoatherosclerosis and stent thrombosis after 2G- and 3G-DES implantation primarily depends not on choice of stent but on risk factor control. In conclusion, the higher NC grade and lower YC grade in 3G-DES than in 2G-DES might be associated with better long-term clinical outcome, which remains to be demonstrated in future studies. Study Limitations It is possible that the thrombus formation and YC grade of the plaque in the stented lesions were underestimated because the blood was cleared from only part of the vessel wall in the field of vision using dextran injection during CAS assessment of the stent. Additionally, CAS was not performed immediately after stent implantation. The initial YC grade of the stented site was therefore unknown. Conclusions The higher NC grade and lower YC grade in 3G-DES than in 2G-DES might be associated with better long-term clinical outcome, which remains to be determined in future studies. Disclosures The authors declare no conflicts of interest. References 1. Moses JW, Leon MB, Popma JJ, Fitzgerald PJ, Holmes DR, O Shaughnessy C, et al. Sirolimus-eluting stents versus standard stents in patients with stenosis in a native coronary artery. N Engl J Med 2003; 349: Morice MC, Serruys PW, Barragan P, Bode C, Van Es GA, Stoll HP, et al. Long-term clinical outcomes with sirolimus-eluting coronary stents: Five-year results of the RAVEL trial. J Am Coll Cardiol 2007; 50: Nakazawa G, Otsuka F, Nakano M, Vorpahl M, Yazdani SK, Ladich E, et al. The pathology of neoatherosclerosis in human coronary implants bare-metal and drug-eluting stents. J Am Coll Cardiol 2011; 57: Tada T, Kadota K, Hosogi S, Kubo S, Ozaki M, Yoshino M, et al. Optical coherence tomography findings in lesions after sirolimus-eluting stent implantation with peri-stent contrast staining. Circ Cardiovasc Interv 2012; 5: Otsuka F, Vorpahl M, Nakano M, Foerst J, Newell JB, Sakakura K, et al. Pathology of second-generation everolimuseluting stents versus first-generation sirolimus- and paclitaxeleluting stents in humans. Circulation 2014; 129: Kuramitsu S, Kazuno Y, Sonoda S, Domei T, Jinnouchi H, Yamaji K, et al. Vascular response to bioresorbable polymer sirolimus-eluting stent vs. permanent polymer everolimus-eluting stent at 9-month follow-up: An optical coherence tomography sub-study from the CENTURY II trial. Eur Heart J Cardiovasc Imaging 2016; 17: Dai K, Matsuoka H, Kawakami H, Sato T, Watanabe K, Nakama Y, et al. Comparison of chronic angioscopic findings of bare metal stents, 1st-generation drug-eluting stents and 2ndgeneration drug-eluting stents: Multicenter Study of Intra- Coronary Angioscopy After Stent (MICASA). Circ J 2016; 80: Nishimoto Y, Ueda Y, Sugihara R, Murakami A, Ueno K, Takeda Y, et al. Comparison of angioscopic findings among second-generation drug-eluting stents. J Cardiol 2017; 70: Park SJ, Kang SJ, Virmani R, Nakano M, Ueda Y. In-stent neoatherosclerosis: A final common pathway of late stent failure. J Am Coll Cardiol 2012; 59: Miyoshi T, Kawakami H, Oshita A, Matsuoka H. A case of instent restenosis with pathologically proven chronic inflammation seven years after sirolimus-eluting stent implantation. J Cardiol Cases 2017; 15: Kawakami H, Matsuoka H, Oshita A, Kono T, Shigemi S. A case of a newly developed yellow neointima at stent implanted site 1 year after sirolimus-eluting stent placement: Angioscopic findings. J Cardiol 2009; 54: Ueda Y, Matsuo K, Nishimoto Y, Sugihara R, Hirata A, Nemoto T, et al. In-stent yellow plaque at 1 year after implantation is associated with future event of very late stent failure: The DESNOTE Study (Detect the Event of Very late Stent Failure From the Drug-Eluting Stent Not Well Covered by Neointima Determined by Angioscopy). JACC Cardiovasc Interv 2015; 8: Saito S, Valdes-Chavarri M, Richardt G, Moreno R, Iniguez Romo A, Barbato E, et al. A randomized, prospective, intercontinental evaluation of a bioresorbable polymer sirolimus-eluting coronary stent system: The CENTURY II (Clinical Evaluation
6 CAS Assessment of DES 1835 of New Terumo Drug-Eluting Coronary Stent System in the Treatment of Patients with Coronary Artery Disease) trial. Eur Heart J 2014; 35: Takayama T, Hiro T, Ueda Y, Honye J, Komatsu S, Yamaguchi O, et al. Plaque stabilization by intensive LDL-cholesterol lowering therapy with atorvastatin is delayed in type 2 diabetic patients with coronary artery disease: Serial angioscopic and intravascular ultrasound analysis. J Cardiol 2013; 61: Kurihara O, Takano M, Yamamoto M, Shirakabe A, Kimata N, Inami T, et al. Impact of prediabetic status on coronary atherosclerosis: A multivessel angioscopic study. Diabetes Care 2013; 36: Aoki I, Aoki N, Kawano K, Shimoyama K, Maki A, Homori M, et al. Platelet-dependent thrombin generation in patients with hyperlipidemia. J Am Coll Cardiol 1997; 30: Puccetti L, Bruni F, Bova G, Cercignani M, Palazzuoli A, Console E, et al. Effect of diet and treatment with statins on platelet-dependent thrombin generation in hypercholesterolemic subjects: Nutrition, metabolism, and cardiovascular diseases. Nutr Metab Cardiovasc Dis 2001; 11: Owens AP 3rd, Byrnes JR, Mackman N. Hyperlipidemia, tissue factor, coagulation, and simvastatin. Trends Cardiovasc Med 2014; 24:
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