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Abstract

Background:

Management of extracranial internal carotid artery steno-occlusive lesion during endovascular therapy remains debated. Stent occlusion within 24 hours of endovascular therapy is a frequent event after acute carotid artery stenting, and we currently lack large population results. We investigated the incidence, predictors, and clinical impact of stent occlusion after acute carotid artery stenting in current clinical practice.

Methods:

Patients treated by endovascular therapy with acute carotid artery stenting between 2015 and 2019 in 5 large-volume endovascular-capable centers were retrospectively analyzed. Patients were separated in 2 groups according to the stent patency at 24 hours after carotid artery stenting. We compared baseline characteristics, treatment modalities, and clinical outcome depending on 24-hour stent patency. Primary end point was favorable outcome, defined as a modified Rankin Scale score 0–2 at 3 months.

Results:

A stent occlusion was observed in 47/225 patients (20.9%). Patients with stent patency had a lower baseline National Institutes of Health Stroke Scale (median [interquartile range]: 13 [7–17] versus 18 [12–21]) and had more often stroke of atherothrombotic origin (77.0% versus 53.2%). A higher stent patency rate was found for patients treated with P2Y12 antagonists at the acute phase (odds ratio [OR]‚ 2.95 [95% CI‚ 1.10–7.91]; P=0.026) and treated with angioplasty (OR‚ 2.42 [95% CI‚ 1.24–4.67]; P=0.008). A better intracranial angiographic reperfusion was observed in patients with 24-hour stent patency compared with patients without stent patency (OR‚ 8.38 [95% CI‚ 3.07–22.78]; P<0.001). Patients with a stent patency at 24 hours had a higher chance of favorable outcome (OR‚ 3.29 [95% CI, 1.66–6.52]; P<0.001) and a lower risk of death (OR‚ 0.32 [95% CI, 0.13–0.76]; P=0.009).

Conclusions:

One out of 5 patients treated with carotid artery stenting during endovascular therapy presented a stent occlusion within 24 hours. This event was associated with worse functional outcome. Stroke etiology, P2Y12 antagonist administration, quality of intracranial reperfusion, and angioplasty were associated with 24-hour stent patency.

Graphical Abstract

See related article, p 132
An estimated 10% to 30% of acute ischemic stroke (AIS) patients with a large vessel occlusion present with a concomitant cervical internal carotid artery (ICA) lesion,1–3 that may benefit from endovascular therapy (EVT).4 The results of ongoing randomized trials being pending, the best strategy for ICA lesion management during EVT remains unclear. Although carotid artery stenting (CAS) seems associated with better rates of reperfusion and clinical outcomes,5 an early stent thrombosis may occur in 5% to 30% of reported cases and was associated with a poor clinical outcome.6,7 Several aspects of early stent occlusion occurrence remain unknown because we lack large sample data. Recent studies reported that diabetes, limited perioperative antiplatelet therapy, residual poststenting stenosis, and insufficient intra-stent angioplasty were associated with early stent occlusion.6–8 Patient’s selection, technical modalities, and the antithrombotic regimen for CAS during EVT have been studied in few retrospective small sample size studies with conflicting results. Therefore, the aim of our study was to evaluate the incidence, predictors, and clinical impact of early stent thrombosis in large registry-based cohort of patients treated with CAS during EVT for AIS.

Methods

Data for this study are available upon a reasonable request from the corresponding author. All patients gave written informed consent for inclusion in the Endovascular Treatment In Stroke (ETIS) registry (NCT03776877).9 When the patient was unable to give an informed consent, a patient’s guardian consent was considered. The local ethics committee approved the use of patient data for this research protocol (comite de protection des personnes sud-est I, 2017-EudraCT number: A03457-46).

Population

Five French comprehensive stroke centers (Rothschild Foundation Hospital‚ Nancy Hospital‚ Strasbourg Hospital‚ Bordeaux Hospital‚ and Bicêtre Hospital) gathered clinical and radiological data of patients treated for AIS with acute cervical CAS during EVT from January 2015 to December 2019. In these 5 centers, acute CAS was performed routinely during EVT in current clinical practice. Data were extracted from local prospectively updated endovascular database in each center. In the present analysis, patients were eligible if they had: (1) an anterior AIS treated by EVT within 8 hours of stroke onset; (2) an acute cervical CAS was performed during EVT for either an ICA occlusion or an ICA severe stenosis. Patients were excluded from the study if: (1) they had an ICA lesion of other cause than atheroma or dissection; (2) no carotid stent patency imaging was performed at 24 (±12) hours after CAS; (3) they had no primary outcome assessment at 3 months (lost to follow-up). This study followed the STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) guidelines.10

Collected Data

We recorded baseline characteristics of the patient’s stroke event and previous medical history. ICA lesion etiologies (atheroma or dissection) were defined on initial imaging and first ICA angiogram during EVT. Technical details of EVT procedure were collected: recanalization strategy, stent characteristics, use of balloon angioplasty, and antithrombotic agents during procedure. Single-layered stents are distinguished from the new generation dual-layered stent in that the latter have higher metallic coverage. Cerebral imaging data, including initial computed tomography or magnetic resonance imaging, EVT procedure, and 24 (±12) hours cerebral imaging, were retrospectively reviewed by each center investigators.
Patients were separated in 2 groups according to the stent patency at 24 (±12) hours after CAS. Stent patency imaging was performed by following each center protocol, using magnetic resonance angiogram or computed tomography angiogram. Stent patency was defined as a full opacification of the carotid lumen.

Outcomes

The primary outcome was the 90-day modified Rankin Scale (mRS) score of 0 to 2, which was termed favorable outcome. Approximately 90 days after the acute event, functional outcome was assessed by board-certified vascular neurologists during a routinely scheduled clinical visit or by a study nurse certified in administering the mRS during a standardized telephone interview if the patient was unable to attend. The secondary outcomes were excellent outcome (90-day mRS score, 0–1), technical outcomes, safety outcomes, infarct extension, and National Institutes of Health Stroke Scale (NIHSS) shift. Technical outcomes included successful reperfusion, which was defined as a modified Thrombolysis in Cerebral Ischemia score of 2b-3, and complete reperfusion (modified Thrombolysis in Cerebral Ischemia score 3). Safety outcomes included any intracerebral hemorrhage, parenchymal hemorrhage type 2 (PH2), and symptomatic intracerebral hemorrhage. Parenchymal hemorrhage and symptomatic intracerebral hemorrhage were defined according to the European Collaborative Acute Stroke Study classifications. To assess infarct extension, we calculated the Alberta Stroke Program Early CT Score (ASPECTS) 24 (±12)-hour shift.

Statistical Analysis

Categorical variables were expressed as frequencies and percentages. Quantitative variables were expressed as the mean (standard deviation) or median (interquartile range) according to the normality of distribution, which was assessed using histograms and the Shapiro-Wilk test. Patients were divided in 2 groups according to presence or not of stent patency at 24 (±12) hours of stenting. Main pretreatment’s characteristics were described according to the 2 study groups without formal statistical comparison. We compared the stent patency rate according to treatment characteristics by using χ2 tests or Fisher exact tests in cases of expected cell frequency of <5 patients. The magnitudes of differences were expressed in term of odds ratios (ORs) of stent patency; regarding the use of Fisher exact test, OR and its CI were estimated using a penalized logistic regression model. Angiographic and clinical outcomes were compared between patients with and without stent patency in univariate analyses. Binary outcomes were compared using logistic regression models, overall distribution of mRS at 3 months was compared using an ordinal logistic regression model, and quantitative outcomes (groin puncture to successful reperfusion time, NIHSS, and ASPECTS changes at 24 [±12] hours) were compared using a linear regression model (after applying a log-transformation for groin puncture to successful reperfusion time to stratify the normality of model residuals and after adjustment for baseline values for NIHSS and ASPECTS changes). Using patients without stent patency as reference, we derived from these regression models, ORs, common OR (for 1-point improvement in 3-month mRS), and mean difference as effect size measures, with their 95% CIs. Statistical testing was done at the 2-tailed α level of 0.05. The data were analyzed using SAS, release 9.4 (SAS Institute, Cary, NC).

Results

During the study period, 5015 patients with AIS were consecutively treated by EVT in the 5 participating centers. Among them, 272 patients with cervical ICA occlusion (isolated cervical occlusion or tandem with intracranial occlusion) were treated with emergent CAS. In total, 47 patients were excluded from the analysis (Figure S1): 8 patients with an etiology of carotid lesion other than atheroma or dissection, 35 patients without available stent patency imaging, and 4 patients lost to follow-up.
Among the 225 patients included, the 24 (±12) hours follow-up imaging was performed using computed tomography angiogram for 170 patients (75.6%) and magnetic resonance angiogram for 55 patients (24.4%). Stent occlusion within 24 (±12) hours was detected in 47 patients (20.9%). Baseline characteristics are reported in Table 1 according to the stent patency within 24 (±12) hours. Compared with the patients with stent occlusion, patients with stent patency had a lower stroke severity assessed by pre-treatment NIHSS score (median [interquartile range]: 13 [7–17] versus 18 [12–21]) and had more often a stroke of atherothrombotic origin (77.0% versus 53.2%).
Table 1. Baseline Characteristics According to the Stent Patency at 24 (±12) Hours
CharacteristicsStent patency
No (n=47)Yes (n=178)
Age, y59 (51–64)64 (56–73)
Men34/47 (72.3)128/178 (71.9)
Medical history
 Hypertension23/47 (48.9)97/178 (54.5)
 Hypercholesterolemia17/47 (36.2)62/178 (34.8)
 Diabetes12/47 (25.5)23/178 (12.9)
 Current smoking16/47 (34.0)72/178 (40.4)
 Pre-stroke mRS ≥16/47 (12.8)13/178 (7.3)
Previous antithrombotic use
 None37/47 (78.7)120/176 (68.2)
 Antiplatelets9/47 (19.1)47/176 (26.7)
 Anticoagulant0/47 (0.0)8/176 (4.5)
 Antiplatelets and anticoagulants1/47 (2.1)1/176 (0.6)
Current stroke events
 Initial imaging
 MRI37/47 (78.7)151/178 (84.8)
 CT10/47 (21.3)27/178 (15.2)
 NIHSS18 (12–21)13 (7–17)
 ASPECTS*7 (5–8)8 (6–9)
 Infarct side
  Right23/47 (48.9)91/177 (51.4)
  Left24/47 (51.1)85/177 (48.0)
  Bilateral0/47 (0.0)1/177 (0.6)
 Intracranial occlusion (tandem)41/47 (87.2)155/178 (87.1)
 ICA disease
 Dissection22/47 (46.8)41/178 (23.0)
 Atheroma25/47 (53.2)137/178 (77.0)
Values are no./total no. or median (interquartile range).
ASPECTS indicates Alberta Stroke Program Early CT Score; CT, computed tomography; ICA, internal carotid artery; MRI, magnetic resonance imaging; mRS, modified Rankin Scale; and NIHSS, National Institutes of Health Stroke Scale.
*
Eight missing values (5 in patent stent group).
Table 2 reports the univariate associations of treatment characteristics with stent patency. During endovascular procedures, the use of a second stent was required for 12/47 (25.5%) and 23/178 (12.9%) cases in the occluded and patent stent groups respectively. The ICA treatment with 2 stents was associated with less frequent stent patency (OR‚ 0.43 [95% CI‚ 0.19–0.96]). A dual-layered stent type was used in 22/225 (9.7%) of cases, and it was associated with a lower rate of stent patency at 24 (±12) hours (OR‚ 0.22 [95% CI‚ 0.08–0.54]) in comparison with single-layered stents. After CAS, a balloon angioplasty was performed for 24/47 (51.1%) and 126/176 (71.6%) patients in the occluded and patent stent groups, respectively. Stent patency at 24 (±12) hours was more often achieved when balloon angioplasty was performed after CAS (OR‚ 2.42 [95% CI‚ 1.24–4.67]). Antiplatelet agents used in association with CAS were aspirin in 185/225 (82.2%) of cases, P2Y12 antagonists in 51/225 (22.6%) of cases, and gpIIb/IIIa inhibitors in 9/225 (0.04%) of cases. A higher stent patency rate was found in patients treated with P2Y12 antagonists during the procedure compared with patients that were not (OR‚ 2.95 [95% CI‚ 1.10–7.91]). The use of a dual antiplatelet therapy was more frequent in the patent stent group (30.5% versus 14.9%) but without significant difference on stent patency rates when compared with monotherapy or no antiplatelet treatment. There was no statistical difference between groups for the use of intravenous thrombolysis, other antiplatelet drugs or heparin during procedures. There were no significant differences in intracerebral hemorrhage rates with a combination of antiplatelet agents or intravenous thrombolysis (Table S6). Stent patency was less frequent in patients with stent thrombosis at the end of the procedure.
Table 2. Univariate Association of Treatment Characteristics With 24 (±12)-Hour Stent Patency
CharacteristicsStent patencyP valueOR (95% CI)
No (n=47)Yes (n=178)
Number of stents
 135/47 (74.5)155/178 (87.1)0.0341.00 (ref.)
 212/47 (25.5)23/178 (12.9) 0.43 (0.19–0.96)
Stent types
 Single layer36/47 (76.6)167/178 (93.8)0.001*1.00 (ref.)
 Dual layer11/47 (23.4)11/178 (6.2) 0.22 (0.08–0.54)
Balloon angioplasty24/47 (51.1)126/176 (71.6)0.0082.42 (1.24–4.67)
Intravenous thrombolysis22/47 (46.8)85/178 (47.8)0.911.04 (0.54–1.98)
Antiplatelet during procedure
 None5/47 (10.6)19/177 (10.7)0.0911.00 (ref.)
 Single35/47 (74.5)104/177 (58.8) 0.78 (0.27–2.25)
 Dual7/47 (14.9)54/177 (30.5) 2.03 (0.57–7.17)
Type
 Aspirin37/47 (78.7)150/177 (84.7)0.321.50 (0.66–3.28)
P2Y12 antagonists5/47 (10.6)46/177 (26.0)0.0262.95 (1.10–7.91)
 gpIIb/IIIa antagonists4/47 (8.5)5/177 (2.8)0.095*0.31 (0.08–1.20)
Heparin during procedure10/47 (21.3)35/177 (19.8)0.820.91 (0.41–2.01)
Stent thrombosis at the end of procedure8/47 (17.0)7/177 (4.0)0.0040.20 (0.06–0.59)
Values are no./total no. unless otherwise as indicated. OR indicates odds ratio for stent patency to be associated with each treatment characteristics.
*
Fisher exact test.
OR and its CIs are calculated using penalized logistic regression model.
As shown in Table 3, patients with stent patency at 24 (±12) hours had a faster and better successful intracranial reperfusion at the end of EVT (OR‚ 8.38 [95% CI‚ 3.07–22.78]) in comparison with patient with stent occlusion. Patients with stent patency also experienced less frequent periprocedural complications, including new intracranial emboli, iatrogenic arterial dissection, and arterial perforation (6.8% versus 23.4%; P=0.002). At 3-month follow-up, stent patency was significantly associated with favorable outcome (OR, 3.29 [95% CI, 1.66–6.52]) and lower risk of death (OR, 0.32 [95% CI, 0.13–0.76]; P=0.009). As reported in the Figure, stent patency was significantly associated with a shift toward better functional outcome at 3 months (OR‚ 3.26 [95% CI, 1.84–5.99]).
Table 3. Outcomes According to the Stent Patency at 24 (±12) Hours
OutcomesStent patencyEffect size (95% CI)P
No (n=47)Yes (n=178)
mTICI 2b-335/47 (74.5)171/178 (96.1)8.38 (3.07 to 22.78)<0.001
mTICI 2c-326/47 (55.3)144/178 (80.9)3.42 (1.72–6.80)<0.001
mTICI 314/47 (29.8)91/178 (51.1)2.47 (1.23–4.92)0.011
Delay from puncture to mTICI 2b-3, min79 (55–110)*65 (44–92)*−0.27 (−0.46 to −0.07)0.007
Procedural complications11/47 (23.4)12/177 (6.8)0.24 (0.09–0.59)0.002
Any ICH23/47 (48.9)76/177 (42.9)0.79 (0.41–1.50)0.46
Parenchymal hematoma10/47 (21.3)20/177 (11.3)0.47 (0.20–1.10)0.079
24 (±12) h NIHSS improvement−3.0 (−5.2 to −0.7)3.9 (2.7–5.0)6.9 (4.3–9.4)§<0.001
24 (±12) h ASPECTS improvement2.8 (2.1–3.6)0.6 (0.3–1.0)−2.2 (−3.0 to −1.4)§<0.001
Early neurological improvement6/46 (13.0)60/173 (34.7)3.54 (1.42–8.83)0.007
3-mo favorable outcome15/47 (31.9)108/178 (60.7)3.29 (1.66–6.52)<0.001
3-mo all-cause mortality11/47 (23.4)16/178 (9.0)0.32 (0.13–0.76)0.009
Values are no./total no. unless otherwise as indicated. Effect size are odds ratio unless otherwise as indicated.
ASPECTS indicates Alberta Stroke Program Early CT Score; CT, computed tomography; ICH, intracerebral hemorrhage; mTICI, modified Thrombolysis in Cerebral Infarction; and NIHSS, National Institutes of Health Stroke Scale.
*
Median (interquartile range values).
Mean difference in log-transformed values.
Mean (95% CI) adjusted on baseline values.
§
Mean difference (95% CI) adjusted on baseline values.
Figure. Distribution of the 3-mo modified Rankin Scale score according to the stent patency at 24 (±12) h.
Detailed subgroup analyses of patients with ICA dissection and ICA atheroma are available in the Supplemental Material (Tables S1 through S4 and Figure S2). Stent occlusion occurred for 22/63 (34.9%) patients in the dissection subgroup, and 25/162 (15.4%) in the atheroma group. In patients with ICA dissection, the use of balloon angioplasty after stent placement was associated with a lower chance of stent occlusion (OR‚ 4.13 [95% CI‚ 1.36–12.48]). The use of P2Y12 antagonists was associated with more frequent stent patency in the atheroma subgroup (OR‚ 4.46 [95% CI‚ 1.00–19.84]). In both dissection and atheroma subgroups, the stent occlusion at 24 (±12) hours was associated with a significant shift toward worse clinical outcome (cOR‚ 3.81 [95% CI‚ 1.45–10.00] and cOR‚ 3.88 [95% CI‚ 1.75–8.54]‚ respectively).

Discussion

In the current multicenter study, around 20% of AIS patients treated with acute CAS presented an occluded stent within 24 to 36 hours, which was associated with a lower likelihood of good functional outcome and higher likelihood of death at 3 months. Stent patency was less frequent in patients with ICA dissection, insufficient intracranial reperfusion (Thrombolysis in Cerebral Infarction <2b), treatment with 2 stents, dual-layered stents, and more often achieved when balloon angioplasty was performed after CAS or in patients treated with P2Y12 antagonists.
In the present study, stent occlusion was not a negligible event and was associated with a poor clinical outcome. Taken into account these findings, it is crucial to maintain stent patency. We identified predictors of carotid stent patency that were previously reported in small single center series,6,7,11 but also the impact of P2Y12 antagonists which has never been reported. In our study, the use of P2Y12 antagonists was significantly associated with more frequent stent patency, especially for patients with an ICA atherosclerotic lesion. The use of at least 1 antiplatelet agent during EVT for tandem occlusion has been associated with a better reperfusion and a lower 3-month mortality.8 Furthermore, an aggressive strategy based on dual antiplatelet therapy with Aspirin and Clopidogrel has been associated with less stent thrombosis, as well as better clinical outcomes in comparison with Aspirin monotherapy.6,12 In our series, patients with stent patency had less severe stroke, suggesting that physicians used P2Y12 antagonists more often in patients with lower hemorrhagic risk. This may explain why the use of P2Y12 antagonists was not associated with difference in hemorrhagic event rates. Of note, intravenous thrombolysis and heparin during procedures were not associated with 24 (±12)-hour stent patency which suggest that it might not protect against carotid stent occlusion. However, it likely increases the risk of hemorrhagic event. Our results suggest the use of P2Y12 antagonists as an effective and safe strategy to reduce the risk of early stent occlusion. With further studies pending, physicians should remain cautious about an aggressive antiplatelet strategy especially in patients who are treated with intravenous thrombolysis.
In our cohort, the choice of P2Y12 antagonist administration was heterogenous between centers. Currently, the antiplatelet strategy surrounding emergent CAS during EVT is without consensus and is at the discretion of the local stroke team. This heterogeneity was recently highlighted in a French nationwide survey.13 Trials are needed to evaluate the optimal antiplatelet strategy. Small series reported a good safety profile of Cangrelor used during emergent CAS,14–17 especially when compared with GpIIb/IIIa inhibitors.18 The intravenous use, rapid time-to-effect, and short half-life profile (eg, platelet function restoration within 1 hour after drug interruption) of Cangrelor seems ideal in the context of EVT. Moreover, a recent meta-analysis of stroke patients reported promising safety and efficacy profiles of Cangrelor during complex EVT procedures.19 Still a dedicated randomized control study remains necessary to address the benefit of cangrelor, if any.
ICA dissection led to more stent occlusion, which is consistent with other published series.6,7,11 It may be explained by the difficult catheterization of the true lumen and the risk of false lumen stenting, as well as a higher risk of intracranial emboli, which are the main challenges when performing emergent CAS for ICA dissection. These observations may correlate with the increased proportion of use of a second stent to cover a long-dissected segment and with longer procedures in our series. In the current literature, CAS for ICA dissection was found to be safe but without significant benefit on patient disability,20 whereas it was suggested to be effective for patients with athero-thrombosis.21 A higher stent occlusion frequency in patients with ICA dissection could have been involved in the observed differences in outcome in these series. Further studies are needed to evaluate the benefit of CAS for patients with ICA dissection.
In our cohort, successful intracranial reperfusion (Thrombolysis in Cerebral Infarction ≥2b) was associated with increased stent patency rate. Our hypothesis is that insufficient intracranial reperfusion might be responsible for reduced in-stent blood flow, enhancing the risk of early stent thrombosis. Physicians should consider this factor for the decision of CAS after the intracranial reperfusion. For CAS technical considerations, the use of a second stent and dual-layer–type stent led to more stent occlusion at 24 (±12) hours. Also, the use of poststenting angioplasty was associated with more frequent stent patency, especially for patients with ICA dissection. These results are consistent with previous reports7,22 and support the use of a single-layer stent followed by balloon angioplasty of the residual stenosis, as the preferred strategy. The residual stenosis threshold for a benefit of poststenting angioplasty is unclear. Excessive use of balloon angioplasty may expose increased risk of intracranial emboli, whereas insufficient use may incur early stent occlusion. Recently, Renú et al also reported the benefit of poststenting angioplasty for a residual stenosis >30% of the distal reference vessel.7 In our cohort, a balloon angioplasty was performed for a residual stenosis with an expected hemodynamic impact but without stenosis measurements. Precise indication for poststenting angioplasty needs further evaluation, as it may lead to significant improvement in ICA lesion management during EVT.
Our study provides interesting new features that could be further analyzed in the future; however, it has some limitations. First, it is a retrospective analysis with its inherent shortcomings. Second, 81 patients treated in Strasbourg Hospital have already been reported in another study focusing on early stent occlusion.6 This could have contributed to the results of this study. Third, indication criteria for CAS decision were not recorded, and there was no distinction between ICA occlusion and severe stenosis. Without clinical trials data, the indication criteria for CAS remain unclear, and the decision is made according to physician’s preference. Finally, patients with stent occlusion had worse intracranial reperfusion and more frequent periprocedural complications, which could explain the difference in outcome at 3 months follow-up.
With the rapid development of EVT in the setting of AIS, dedicated clinical trials are needed to guide recommendations for extracranial ICA lesions management during EVT. CAS provides better reperfusion rates but exposes to the risk of stent occlusion, which is associated with a poor prognosis. The use of antithrombotic treatments in association with CAS seems to be a key point to be studied in the future. More definitive results on emergent CAS during EVT should be provided by the ongoing TITAN (Thrombectomy in Tandem Occlusion; NCT03978988) and EASI-TOC (Endovascular Acute Stroke Intervention-Tandem Occlusion Trial; NCT04261478) randomized multicenter trials.23,24

Conclusions

Early stent occlusion after acute CAS is not a negligible event and negatively impacts clinical outcome at 3 months. Avoiding a carotid stent occlusion is crucial. Stroke etiology, P2Y12 antagonist administration, quality of intracranial reperfusion, and poststenting angioplasty were the main factors associated with 24 (±12)-hour stent patency. Patients with an ICA dissection seem to benefit from poststenting balloon angioplasty, and patients with atherosclerotic lesions from more potent antiplatelet therapy (ie, P2Y12 antagonists). The optimal endovascular strategy and antiplatelet therapy should be evaluated in large studies and ideally in randomized controlled trials.

Article Information

Supplemental Material

Figures S1–S2
Tables S1–S6

Footnote

Nonstandard Abbreviations and Acronyms

AIS
acute ischemic stroke
ASPECTS
Alberta Stroke Program Early CT Score
CAS
carotid artery stenting
EVT
endovascular therapy
ICA
internal carotid artery
NIHSS
National Institutes of Health Stroke Scale
OR
odds ratio

Supplemental Material

File (str_stroke-2022-039797_supp1.pdf)
File (str_stroke-2022-039797_supp2.pdf)

APPENDIX

On Behalf of the Endovascular Treatment in Stroke (ETIS) Investigators

Raphael Blanc, Hocine Redjem, Simon Escalard, Jean-Philippe Dessilles, François Delvoye, Stanislas Smajda, Benjamin Maier, Hebert Solène, Mikael Mazighi, Mikael Obadia, Candice Sabben, Seners Pierre, Raynouard Igor, Ovide Corabianu, Thomas de Broucker, Eric Manchon, Guillaume Taylor, Malek Ben Maacha, Laurie-Anne Thion, Lecler Augustin, Savatovsjy Julien, Adrien Wang, Serge Evrard, Maya Tchikviladze, Nadia Ajili, David WeisenburgerLile, Lucas Gorza, Géraldine Buard, Oguzhan Coskun, Federico Di Maria, Georges Rodesh, Sergio Zimatore, Morgan Leguen, Julie Gratieux, Fernando Pico, Haja Rakotoharinandrasana, Philippe Tassan, Roxanna Poll, Sylvie Marinier, Xavier Barreau, Jérôme Berge, Patrice Menegon, Ludovic Lucas, Stéphane Olindo, Pauline Renou, Sharmila Sagnier, Mathilde Poli, Sabrina Debruxelles, François Rouanet, Thomas Tourdias, Jean-Sebastien Liegey, Pierre Briau, Nicolas Pangon, Alexis Coussy, Lisa Papillon, Jean Papaxanthos, Lili Detraz, Benjamin Daumas-Duport, Pierre-Louis Alexandre, Monica Roy, Cédric Lenoble, Hubert Desal, Benoît Guillon, Solène de Gaalon, Cécile Preterre, Serge Bracard, René Anxionnat, Marc Braun, Anne-Laure Derelle, Romain Tonnelet, Liang Liao, François Zhu, Emmanuelle Schmitt, Sophie Planel, Lisa Humbertjean, Jean-Christophe Lacour, Nolwenn Riou-Comte, Marcela Voicu, Lionel Alb, Marie Reitter, Madalina Brezeanu, Agnès Masson, Adriana Tabarna, Iona Podar, Francisco Macian-Montoro, Suzanna Saleme, Charbel Mounayer, Aymeric Rouchaud, Vincent Costalat, Caroline Arquizan, Cyril Dargazanli, Grégory Gascou, Pierre-Henri Lefèvre, Imad Derraz, Carlos Riquelme, Nicolas Gaillard, Isabelle Mourand, Lucas Corti, Federico Cagnazzo, Adrien Ter Schiphorst, Jean-Christophe Ferre, Hélène Raoult, Thomas Ronziere, Maria Lassale, Christophe Paya, Jean-Yves Gauvrit, Clément Tracol, Sophie Langnier-Lemercier

References

1.
Fransen PSS, Beumer D, Berkhemer OA, van den Berg LA, Lingsma H, van der Lugt A, van Zwam WH, van Oostenbrugge RJ, Roos YB, Majoie CB, et al; MR CLEAN Investigators. MR CLEAN, a multicenter randomized clinical trial of endovascular treatment for acute ischemic stroke in the Netherlands: study protocol for a randomized controlled trial. Trials. 2014;15:343. doi: 10.1186/1745-6215-15-343
2.
Goyal M, Demchuk AM, Menon BK, Eesa M, Rempel JL, Thornton J, Roy D, Jovin TG, Willinsky RA, Sapkota BL, et al. Randomized assessment of rapid endovascular treatment of ischemic stroke. N Engl J Med. 2015;372:1019–1030. doi: 10.1056/nejmoa1414905
3.
Molina CA, Chamorro A, Rovira A, de Miquel A, Serena J, Roman LS, Jovin TG, Davalos A, Cobo E. REVASCAT: a randomized trial of revascularization with SOLITAIRE FR device vs. best medical therapy in the treatment of acute stroke due to anterior circulation large vessel occlusion presenting within eight-hours of symptom onset. Int J Stroke. 2015;10:619–626. doi: 10.1111/ijs.12157
4.
Goyal M, Menon BK, van Zwam WH, Dippel DW, Mitchell PJ, Demchuk AM, Dávalos A, Majoie CB, van der Lugt A, de Miquel MA, et al; HERMES Collaborators. Endovascular thrombectomy after large-vessel ischaemic stroke: a meta-analysis of individual patient data from five randomised trials. Lancet. 2016;387:1723–1731. doi: 10.1016/S0140-6736(16)00163-X
5.
Papanagiotou P, Haussen DC, Turjman F, Labreuche J, Piotin M, Kastrup A, Steglich-Arnholm H, Holtmannspötter M, Taschner C, Eiden S, et al; TITAN Investigators. Carotid stenting with antithrombotic agents and intracranial thrombectomy leads to the highest recanalization rate in patients with acute stroke with tandem lesions. JACC Cardiovasc Interv. 2018;11:1290–1299. doi: 10.1016/j.jcin.2018.05.036
6.
Pop R, Zinchenko I, Quenardelle V, Mihoc D, Manisor M, Richter JS, Severac F, Simu M, Chibbaro S, Rouyer O, et al. Predictors and clinical impact of delayed stent thrombosis after thrombectomy for acute stroke with tandem lesions. AJNR Am J Neuroradiol. 2019;40:533–539. doi: 10.3174/ajnr.A5976
7.
Renú A, Blasco J, Laredo C, Llull L, Urra X, Obach V, López-Rueda A, Rudilosso S, Zarco F, González E, et al. Carotid stent occlusion after emergent stenting in acute ischemic stroke: Incidence, predictors and clinical relevance. Atherosclerosis. 2020;313:8–13. doi: 10.1016/j.atherosclerosis.2020.09.002
8.
Zhu F, Anadani M, Labreuche J, Spiotta A, Turjman F, Piotin M, Steglich-Arnholm H, Holtmannspötter M, Taschner C, Eiden S, et al; TITAN Investigators. Impact of antiplatelet therapy during endovascular therapy for tandem occlusions: a collaborative pooled analysis. Stroke. 2020;51:1522–1529. doi: 10.1161/STROKEAHA.119.028231
9.
Endovascular Treatment in Ischemic Stroke Follow-up Evaluation. https://ClinicalTrials.gov/show/NCT03776877.
10.
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP; STROBE Initiative. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet. 2007;370:1453–1457. doi: 10.1016/S0140-6736(07)61602-X
11.
Moulakakis KG, Kakisis J, Tsivgoulis G, Zymvragoudakis V, Spiliopoulos S, Lazaris A, Sfyroeras GS, Mylonas SN, Vasdekis SN, Geroulakos G, et al. Acute early carotid stent thrombosis: a case series. Ann Vasc Surg. 2017;45:69–78. doi: 10.1016/j.avsg.2017.04.039
12.
Pop R, Severac F, Hasiu A, Mihoc D, Mangin PH, Chibbaro S, Simu M, Tudor R, Gheoca R, Quenardelle V, et al. Conservative versus aggressive antiplatelet strategy for emergent carotid stenting during stroke thrombectomy. Interv Neuroradiol. 2022:15910199221083112. doi: 10.1177/15910199221083112
13.
Caroff J, Aubert L, Lavenu-Bombled C, Figueiredo S, Habchi K, Cortese J, Eugene F, Ognard J, Tahon F, Forestier G, et al. Antithrombotic therapies for neurointerventional surgery: a 2021 French comprehensive national survey [published online March 28, 2022]. J Neurointerv Surg. 2022. doi: 10.1136/neurintsurg-2021-018601
14.
Cervo A, Ferrari F, Barchetti G, Quilici L, Piano M, Boccardi E, Pero G. Use of cangrelor in cervical and intracranial stenting for the treatment of acute ischemic stroke: a “real life” single-center experience. AJNR Am J Neuroradiol. 2020;41:2094–2099. doi: 10.3174/ajnr.A6785
15.
Aguilar-Salinas P, Agnoletto GJ, Brasiliense LBC, Santos R, Granja MF, Gonsales D, Aghaebrahim A, Sauvageau E, Hanel RA. Safety and efficacy of cangrelor in acute stenting for the treatment of cerebrovascular pathology: preliminary experience in a single-center pilot study. J Neurointerv Surg. 2019;11:347–351. doi: 10.1136/neurintsurg-2018-014396
16.
Marnat G, Delvoye F, Finitsis S, Lapergue B, Gariel F, Consoli A, Desilles JP, Mazighi M, Dargazanli C, Bourcier R, et al; ETIS Investigators. A multicenter preliminary study of cangrelor following thrombectomy failure for refractory proximal intracranial occlusions. AJNR Am J Neuroradiol. 2021;42:1452–1457. doi: 10.3174/ajnr.A7180
17.
Elhorany M, Lenck S, Degos V, Sourour NA, Frasca Polara G, Shotar E, Godier A, Drir M, Mahtout J, Premat K, et al. Cangrelor and stenting in acute ischemic stroke: monocentric case series. Clin Neuroradiol. 2021;31:439–448. doi: 10.1007/s00062-020-00907-0
18.
Delvoye F, Maier B, Escalard S, Labreuche J, Thion LA, Aknouche S, Hebert S, Redjem H, Smajda S, Ciccio G, et al. Antiplatelet therapy during emergent extracranial internal carotid artery stenting: comparison of three intravenous antiplatelet perioperative strategies. J Stroke Cerebrovasc Dis. 2021;30:105521. doi: 10.1016/j.jstrokecerebrovasdis.2020.105521
19.
Marnat G, Finistis S, Delvoye F, Sibon I, Desilles JP, Mazighi M, Gariel F, Consoli A, Rosso C, Clarençon F, et al. Safety and efficacy of cangrelor in acute stroke treated with mechanical thrombectomy: endovascular treatment of ischemic stroke registry and meta-analysis. AJNR Am J Neuroradiol. 2022;43:410–415. doi: 10.3174/ajnr.A7430
20.
Marnat G, Lapergue B, Sibon I, Gariel F, Bourcier R, Kyheng M, Labreuche J, Dargazanli C, Consoli A, Blanc R, et al; TITAN and ETIS Investigators. Safety and outcome of carotid dissection stenting during the treatment of tandem occlusions: a pooled analysis of TITAN and ETIS. Stroke. 2020;51:3713–3718. doi: 10.1161/STROKEAHA.120.030038
21.
Gory B, Piotin M, Haussen DC, Steglich-Arnholm H, Holtmannspötter M, Labreuche J, Taschner C, Eiden S, Nogueira RG, Papanagiotou P, et al; TITAN Investigators. Thrombectomy in acute stroke with tandem occlusions from dissection versus atherosclerotic cause. Stroke. 2017;48:3145–3148. doi: 10.1161/STROKEAHA.117.018264
22.
Yilmaz U, Körner H, Mühl-Benninghaus R, Simgen A, Kraus C, Walter S, Behnke S, Faßbender K, Reith W, Unger MM. Acute occlusions of dual-layer carotid stents after endovascular emergency treatment of tandem lesions. Stroke. 2017;48:2171–2175. doi: 10.1161/strokeaha.116.015965
23.
Endovascular Acute Stroke Intervention - Tandem OCclusion Trial. In: https://ClinicalTrials.gov/show/NCT04261478.
24.

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History

Received: 21 April 2022
Revision received: 29 September 2022
Accepted: 7 October 2022
Published online: 21 December 2022
Published in print: January 2023

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Keywords

  1. carotid artery stenting
  2. stent occlusion
  3. stroke
  4. thrombectomy

Subjects

Authors

Affiliations

Department of Interventional Neuroradiology, Rothschild Foundation, Paris, France (J.A., F.D., B.M., MP, M.M.).
University of Paris‚ France (J.A., M.M.).
Department of Interventional Neuroradiology, Rothschild Foundation, Paris, France (J.A., F.D., B.M., MP, M.M.).
Department of Neuroradiolology, CHU Strasbourg, France (R.P.).
Institut de Chirurgie Minime Invasive Guidée par l’Image, Strasbourg, France (R.P.).
University of Strasbourg, INSERM UMR-S1255, France (R.P.).
Department of Biostatistics, CHU Lille, University of Lille, France (J.L.).
Department of Interventional Neuroradiology, Rothschild Foundation, Paris, France (J.A., F.D., B.M., MP, M.M.).
LVTS, INSERM U1148, University of Paris, France (BM., M.M.).
Department of Diagnostic and Interventional Neuroradiology, University Hospital of Bordeaux, France (G.M.).
Department of Neurology, Stroke Center, University Hospital of Bordeaux, France (I.S.).
Department of Diagnostic and Therapeutic Neuroradiology, CHRU-Nancy, Université de Lorraine, France (B.G., F.Z.).
Bertrand Lapergue, MD, PhD https://orcid.org/0000-0002-8993-2175
Department of Neurology, Foch Hospital, Versailles Saint-Quentin en Yvelines University, Suresnes, France (B.L.).
Diagnostic and Interventional Neuroradiology, Foch Hospital, Versailles Saint-Quentin en Yvelines University, Suresnes, France (A.C.).
Department of Neuroradiolology, CHU Kremlin-Bicêtre, Le Kremlin Bicêtre, France (L.S.).
Christian Denier, MD, PhD https://orcid.org/0000-0002-2087-5563
Department of Neurology, CHU Kremlin-Bicêtre, Le Kremlin Bicêtre, France (C.D.).
Sébastien Richard, MD, PhD https://orcid.org/0000-0002-0945-5656
Department of Neurology, Stroke Unit, Université de Lorraine, CHRU-Nancy, France (S.R.).
CIC-P 1433, INSERM U1116, CHRU-Nancy, France (S.R.).
Department of Interventional Neuroradiology, Rothschild Foundation, Paris, France (J.A., F.D., B.M., MP, M.M.).
Department of Diagnostic and Therapeutic Neuroradiology, CHRU-Nancy, Université de Lorraine, France (B.G., F.Z.).
IADI, INSERM U1254, Université de Lorraine, Nancy, France (B.G.).
Department of Interventional Neuroradiology, Rothschild Foundation, Paris, France (J.A., F.D., B.M., MP, M.M.).
LVTS, INSERM U1148, University of Paris, France (BM., M.M.).
University of Paris‚ France (J.A., M.M.).
ETIS Investigators

Notes

A list of ETIS Investigators is available in the Appendix.
Supplemental Material is available at Supplemental Material.
For Sources of Funding and Disclosures, see page 124.
Correspondence to: Julien Allard, MD, Interventional Neuroradiology Department, Rothschild Foundation Hospital, Paris, France. Email [email protected]

Disclosures

Disclosures Dr Mazighi provides consulting for Acticor Biotech, Air liquid, Amgen, Boerhinger-ingelheim, and Novo Nordisk. Dr Spelle provides consulting for Balt, Medtronic, Microvention, Philips, and Striker.

Sources of Funding

None.

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  1. 7 Identifying Patients for Stroke Thrombectomy Stroke thrombectomy, identifying patients for, Hemorrhagic and Ischemic Stroke, (2025).https://doi.org/10.1055/b-0044-205908
    Crossref
  2. Outcomes in acute carotid-related stroke eligible for mechanical reperfusion: SAFEGUARD-STROKE Registry, The Journal of Cardiovascular Surgery, 65, 3, (2024).https://doi.org/10.23736/S0021-9509.24.13093-5
    Crossref
  3. Outcome of tailored antiplatelet therapy in carotid stenting: a retrospective comparative study, CVIR Endovascular, 7, 1, (2024).https://doi.org/10.1186/s42155-024-00482-2
    Crossref
  4. Triple platelet inhibition in intracranial thrombectomy with additional acute cervical stent angioplasty due to tandem lesion: a retrospective single-center analysis, BMC Neurology, 24, 1, (2024).https://doi.org/10.1186/s12883-024-03597-0
    Crossref
  5. Cangrelor for emergent carotid stenting during stroke thrombectomy: a comparative analysis versus glycoprotein IIb/IIIa inhibitors or aspirin monotherapy, Journal of NeuroInterventional Surgery, (jnis-2024-022125), (2024).https://doi.org/10.1136/jnis-2024-022125
    Crossref
  6. Tirofiban versus aspirin to prevent in-stent thrombosis after emergent carotid artery stenting in acute ischemic stroke, Journal of NeuroInterventional Surgery, (jnis-2024-021845), (2024).https://doi.org/10.1136/jnis-2024-021845
    Crossref
  7. The Dual-layer CGuard Stent Is Safe and Effective in Emergent Carotid Artery Stenting and in Tandem Occlusions: a Multi-centric Study, Clinical Neuroradiology, (2024).https://doi.org/10.1007/s00062-024-01455-7
    Crossref
  8. Intravenous thrombolysis with tenecteplase versus alteplase combined with endovascular treatment of anterior circulation tandem occlusions: A pooled analysis of ETIS and TETRIS, European Stroke Journal, 9, 1, (124-134), (2023).https://doi.org/10.1177/23969873231206894
    Crossref
  9. Antithrombotic regimen in emergent carotid stenting for acute ischemic stroke due to tandem occlusion: a meta-analysis of aggregate data, Journal of NeuroInterventional Surgery, 16, 3, (243-247), (2023).https://doi.org/10.1136/jnis-2023-020204
    Crossref
  10. Comparison of three antithrombotic strategies for emergent carotid stenting during stroke thrombectomy: a multicenter study, Journal of NeuroInterventional Surgery, 15, e3, (e388-e395), (2023).https://doi.org/10.1136/jnis-2022-019875
    Crossref
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