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Ischemic Stroke
Original research
Acute carotid stenting in patients undergoing thrombectomy: a systematic review and meta-analysis
  1. Gabrielle Dufort1,2,
  2. Bing Yu Chen3,
  3. Grégory Jacquin1,2,4,
  4. Mark Keezer1,2,4,
  5. Marilyn Labrie1,
  6. Bastien Rioux1,2,
  7. Christian Stapf1,2,4,
  8. Daniela Ziegler5,
  9. Alexandre Y Poppe1,2,4
  1. 1 Neurosciences, Universite de Montreal, Montreal, Quebec, Canada
  2. 2 Neurology, Centre Hospitalier de L'Universite de Montreal, Montreal, Quebec, Canada
  3. 3 Medicine, McGill University, Montreal, Quebec, Canada
  4. 4 Axe Neurosciences, Centre de Recherche du CHUM (CRCHUM), Montreal, Quebec, Canada
  5. 5 Bibliothèque du Centre Hospitalier de l'Université de Montréal, Montreal, Quebec, Canada
  1. Correspondence to Dr Alexandre Y Poppe, Neurosciences, Centre Hospitalier de L'Universite de Montreal, Montreal, QC H2X 0C1, Canada; alexandre.poppe.chum{at}ssss.gouv.qc.ca

Abstract

Background The benefit of acute carotid stenting compared with no acute stenting on clinical outcomes among patients with tandem lesions (TL) undergoing endovascular thrombectomy (EVT) remains unknown.

Methods We conducted a a systematic review and meta-analysis of studies comparing acute carotid stenting versus no stenting among TL patients undergoing EVT with regards to 90 day modified Rankin Scale (mRS) score, symptomatic intracerebral hemorrhage (sICH), and mortality. Four reviewers screened citations for eligibility and two assessed retained studies for risk of bias and data extraction. A random effects model was used for the synthesis of aggregated data.

Results 21 studies (n=1635 patients) were identified for the systematic review; 19 were cohort studies, 1 was a post-hoc analysis of an EVT trial, and 1 was a pilot randomized controlled trial. 16 studies were included in the meta-analysis. Acute stenting was associated with a favorable 90 day mRS score: OR 1.43 (95% CI 1.07, 1.91). No significant heterogeneity between studies was found for this outcome (I2=17.0%; χ2=18.07, p=0.26). There were no statistically significant differences for 3 month mortality (OR 0.80 (95% CI 0.50, 1.28)) or sICH (OR 1.41 (95% CI 0.91, 2.19)).

Conclusions This meta-analysis suggests that among TL patients undergoing EVT, acute carotid stenting is associated with a greater likelihood of favorable outcome at 90 days compared with no stenting.

  • stroke
  • thrombectomy
  • stent
  • stenosis

https://doi.org/10.1136/neurintsurg-2020-015817

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    Patients with tandem lesions (TL)—that is, stroke with an acute intracranial anterior circulation occlusion and an ipsilateral cervical internal carotid artery (c-ICA) high grade stenosis or occlusion— constitute about 15% of patients undergoing endovascular thrombectomy (EVT).1 Patients with TL present a unique therapeutic challenge and tend to have worse outcomes than patients with isolated intracranial occlusions.2 In these patients, intravenous (IV) thrombolysis is less effective, presumably owing to a larger clot burden and low anterograde flow impeding thrombolytic drug access to the intracranial thrombus.2 When EVT is performed in TL patients, treatment strategies vary according to clinical, anatomical, and technical considerations, as well as physician preference.

    Two main approaches exist: the first is to traverse the c-ICA lesion, perform intracranial clot retrieval, and leave the c-ICA largely untreated for possible endarterectomy or stenting in the ensuing days or weeks. The second is to recanalize the c-ICA more definitively using stenting during the EVT procedure, either prior to or following intracranial thrombectomy. These two treatment strategies exemplify the competing risks that must be balanced in TL patients—that is, ischemic stroke progression or recurrence on the one hand, and intracranial hemorrhage on the other. Without randomized controlled trial data to guide therapeutic decisions, both approaches are widely used in clinical practice.3 Thus while we do not know which is superior, neither approach can truly be considered either the standard of care or experimental therapy.

    To determine if existing data might support the superiority of one approach over the other with regards to functional outcomes, we conducted a systematic review and meta-analysis of the literature.

    Methods

    Protocol and eligibility criteria

    This systematic review is reported according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.4 All published randomized controlled trials, cohort studies, case control studies. and case series evaluating endovascular treatment of adults with acute anterior circulation strokes due to TL were eligible for inclusion. Abstracts, case reports, or case series with fewer than six participants, comments, reviews, and meta-analyses were excluded. Tandem lesions were defined as high grade stenosis (70–99%) or occlusion of the c-ICA with ipsilateral occlusion of the distal ICA and/or middle cerebral artery. Only studies published between 2000 and 2018 that reported outcomes both for patients undergoing acute c-ICA stenting and patients undergoing intracranial thrombectomy alone were included. There were no initial restrictions concerning country or language of publication. The primary outcome was a favorable modified Rankin Scale (mRS) score of 0–2 at 3 months. Secondary outcomes were symptomatic intracranial hemorrhage (sICH) and mortality at 3 months.

    Search strategy

    The search strategy was designed in collaboration with a medical librarian having expertise in systematic reviews (DZ). The following electronic databases were searched: Ovid EMBASE, EBSCO CINAHL Complete, Ovid MEDLINE, Web of Science, Google Scholar, and Open Grey. The following search keywords were used to target selected studies: Carotid, Thrombectomy, thrombectomy, thrombolysis, thromboendarterectomy, stent, angioplasty (see online supplementary appendix e-1 for detailed search strategy). Additionally, we searched the bibliographies of all of the included studies to find additional studies. The most recent literature search was completed on February 19, 2020.

    Study selection

    Reviewers (GJ, ML, AYP, CS) independently screened each title/abstract using a free online systematic review application (https://rayyan.qcri.org/).5 Full text articles were obtained when identified by any reviewer as potentially relevant to the research question. Full text articles were then independently screened by two reviewers and the reasons for any exclusions were recorded. Disagreements about eligibility were resolved by consensus.

    Protocol approval

    No ethics approval was required for this systematic review and meta-analysis.

    Data collection and risk of bias

    Data collection was completed by one author (GD) and reviewed by a second (AYP) using a data extraction instrument designed specifically for this review. Demographic data for each included study were collected when available, including number of participants, age, sex, initial National Institutes of Health Stroke Scale score, Alberta Stroke Program Early CT Score (ASPECTS), key vascular comorbidities (hypertension, diabetes, smoking, dyslipidemia, atrial fibrillation), etiology of the ICA lesion (atherosclerosis, embolism, dissection), site of intracranial occlusion, use of IV thrombolysis, use of antiplatelet agents or anticoagulation, and the thrombectomy device used. For stented patients, the order of stenting relative to intracranial thrombectomy (before, or anterograde vs after, or retrograde) was also documented when specified. Corresponding authors were contacted when data relevant to the primary and secondary outcomes were not included in the original publication (four of seven authors responded).

    Risk of bias was evaluated for the individual studies using a customized quality assessment tool designed based on recommendations from the Ottawa Non-Randomized Studies Workshop and Cochrane Handbook for Systematic Reviews of Interventions.6 Each quality criterion was rated as having a low, high, or unclear risk of bias.

    Data synthesis and analysis

    A random effects model was chosen for the synthesis of aggregated data. In order to compare acceptably homogeneous data, studies were included in the meta-analysis only when outcome data respected our prespecified time frame (mRS score and mortality at 90 days). Summary effect measures (ORs) were calculated using data extracted from primary studies and were compared using 95% CIs.

    Heterogeneity between studies was evaluated with visual assessment of forest plots, as well as I2 and χ2 tests. We defined important inter-study heterogeneity as an I2 test result of >50% and a χ2 test result of <0.1. Reporting bias was assessed using funnel plots for each outcome of interest. Analyses were performed with R Studio (V.1.2) using the meta package (V. 4.9–5; https://www.rdocumentation.org/packages/meta).

    Subgroup analyses

    Subgroup analyses were conducted when at least three studies were available for each variable of interest. Studies were divided according to year of publication (before or after 2017 to capture studies conducted before and after the era of modern thrombectomy devices), total number of participants included (<50 or ≥50), order of stenting relative to thrombectomy among stented patients (≥50% of stented patients in study stented before thrombectomy vs ˃50% of patients stented after thrombectomy), and study design (observational study vs randomized controlled study).

    Data availability

    Data are available on reasonable requests by qualified investigators to the corresponding author.

    Results

    Study selection

    Study selection and reasons for study exclusion are detailed in the PRISMA flow diagram (figure 1). A total of 1715 articles were identified through database searching, and one was identified through other sources (bibliographic hand search); 1556 records were screened after removal of duplicates, of which 204 full texts were assessed for eligibility. A total of 21 studies, including 1635 patients (974 with acute stenting and 661 without), were included in our systematic review (online supplementary table e–1).

    Figure 1
    Figure 1

    Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow diagram for literature search and study selection. mRS, modified Rankin Scale.

    Two studies were prospective cohort studies,7 8 eight were retrospective cohort studies,1 9–15 nine were retrospective cohort studies from prospectively collected databases,16–24 one was a post hoc analysis of a randomized controlled trial,25 and one was a pilot randomized controlled trial.26 Data regarding study population, management, and follow-up duration are summarized in online supplementary table e–1. One study included patients with posterior circulation TL which were excluded from our analysis.10 Stenting was compared with angioplasty or no acute treatment of the c-ICA in 13/21 studies and with multiple different treatment regimens in 6/21 studies. Management of the c-ICA lesion in patients without acute stenting was not specified in 2/16 studies.9 19 Most (14/21) studies1 7 9 10 14–17 19 20 22–24 26 specifically compared reported outcomes in patients with and without acute c-ICA stenting. However, four studies described outcomes for each patient without direct comparison between the patient groups,11–13 18 one compared patients according to c-ICA patency at 24 hours regardless of treatment regimen,8 one divided patients according to acute intervention on c-ICA regardless of type of intervention,25 and one conducted a multivariate analysis of predictors of functional independence without direct comparison between patients undergoing acute c-ICA stenting or not.21 In three studies, intracranial lesions were treated with intra-arterial tissue plasminogen activator alone11–13 while the others used a combination of thrombolysis and thrombectomy. ASPECTS score was inconsistently reported in the included studies. However, apart from one study where ASPECTS was significantly higher in participants in the stenting subgroup compared with the no stenting group,15 the scores were comparable between treatment groups when reported. Antiplatelet and anticoagulation treatment regimens were widely variable and inconsistently reported in the included studies, precluding meaningful analysis of this component of patient management.

    Risk of bias assessment is summarized in online supplementary table e–1. Allocation of intervention was performed in most studies (20/21) according to the treating physicians, making the risk of selection bias high. One study26 was randomized but crossover of two patients from the stenting group to the no stenting group make the risk of selection bias uncertain. Performance bias risk was considered high in retrospective studies (17/21) where concealment of intervention allocation was unlikely, and in two open label studies.25 26 Most studies were at low risk of detection bias for mortality and sICH (17/21),1 7–10 14–23 25 26 and of unclear risk for mRS score (13/21).1 10 15 18–20 22 23 However, evaluation of outcome at differing time points between patients made 4/2111–13 24 studies at high risk of detection bias for these outcomes. Only 3/217 14 25 studies mentioned blinding of staff assessing mRS at follow-up. Risk of attrition bias was high in 3/217 20 23 studies excluding patients without outcome data at 3 months but was otherwise of low or unclear risk. Selective reporting bias risk was unclear in most studies (20/21), but likely to be high as in most observational studies, and high in one25 that was a post hoc analysis of previously published data.

    Narrative synthesis of included studies

    Narrative examination was completed for all studies included in our systematic review. Two studies1 23 reported statistically significant favorable mRS scores at 90 days and one of these also reported significantly lower mortality23 for patients with acute c-ICA stenting compared with no stenting. Statistically significant favorable mRS scores at 90 days were found in one study8 for participants with c-ICA patency at 24 hours compared with no patency at 24 hours and in another study15 comparing patients with acute c-ICA stenting with antithrombotic medication compared with no stenting. Sample size was too small for statistical analysis in 5/15 studies.9 11–13 18

    Meta-analysis of included studies

    Sixteen studies were included in the meta-analysis of the primary outcome (mRS score 0–2 at 3 months). Four studies were excluded because of mRS data outside our prespecified time frame11–13 24 and one because of unavailable data.18 Stenting was associated with a favorable mRS score at 3 months (OR 1.43 (95% CI 1.07, 1.91)) (figure 2). No significant heterogeneity between studies was found for this outcome (I2=17.0%; χ2=18.07, p=0.26). There were no statistically significant differences for 3 month mortality (OR 0.80 (95% CI 0.50, 1.28)) or for sICH (OR 1.41 (95% CI 0.91, 2.19)), although the direction of the association suggested lower odds of death and higher odds of sICH with stenting (figure 3).

    Figure 2
    Figure 2

    Meta-analysis of functional independence at 90 days (modified Rankin Scale (mRS) score of 0–2) with respect to acute stenting versus no stenting.

    Figure 3
    Figure 3

    Meta-analysis of (A) symptomatic intracerebral hemorrhage (sICH) and (B) mortality at 90 days with respect to acute stenting versus no stenting.

    Sensitivity analyses

    Subgroup analyses for year of publication, number of patients, timing of stenting relative to thrombectomy, and study design had no significant effect on the results (data not shown). Funnel plot inspection did not reveal any asymmetry for mRS or sICH (online supplementary figure e-1). For mortality, funnel plot asymmetry indicated possible reporting bias (online supplementary figure e-2).

    Discussion

    This systematic review and meta-analysis suggests an association between acute c-ICA stenting and better 3 month functional outcome in patients with TL undergoing EVT for acute stroke. To date, no large randomized controlled trials have been completed addressing the question of optimal c-ICA management in acute stroke patients with TL. While the current meta-analysis is limited almost exclusively to prospective and retrospective observational studies, contrary to previously published meta-analyses, we included only studies comparing stented and non-stented patients and also captured more recent, larger cohorts. Four main meta-analyses of smaller case series have been published,19 27–29 most with relatively few patients not having undergone acute stenting and only two28 29 reporting whether acute ICA stenting was associated with different clinical outcomes than no stenting.

    Data from the HERMES collaboration provides clear evidence that patients with TL benefit from EVT, without regard to how the c-ICA lesion is addressed.30 As EVT becomes ever more widespread, it is necessary to further refine its use in specific subpopulations, including patients with TL. There are putative advantages for both acutely stenting the c-ICA and for foregoing acute stenting during EVT. Acute c-ICA stenting may more effectively treat the cause of stroke, favor intracranial clot lysis, and decrease the risk of recurrence while improving overall cerebral perfusion.27 However, foregoing acute c-ICA stenting can avoid early administration of antiplatelet agents which may increase the risk of intracranial hemorrhage in the immediate post-recanalization phase, particularly in patients having received IV thrombolysis or having a large core of infarction.31 32 Furthermore, stent placement carries an inherent risk of in-stent thrombosis which may confer a worse prognosis.33 An international survey of stroke experts highlighted this therapeutic uncertainty, with 75% of respondents having equipoise regarding optimal acute management of c-ICA stenosis in TL patients.3

    Our meta-analysis is the first to demonstrate a statistically significant difference in functional outcome at 90 days favoring acute c-ICA stenting in TL patients undergoing EVT. This result is likely driven by the inclusion of two large and more recent multicenter series that both suggested better outcomes with acute stenting.1 15 A cumulative funnel plot analyzing studies according to year of publication suggested progressively better mRS outcomes over time. This may reflect improvements in techniques for both intracranial recanalization and c-ICA stenting as well as the higher quality of more recently published series.

    Although not statistically significant, there was a trend suggesting lower mortality in patients undergoing acute stenting, possibly related to lower stroke recurrence and better functional outcomes or perhaps reflecting a selection bias favoring more aggressive acute c-ICA lesion treatment of patients felt by the treating team to have a better prognosis. Conversely, there appeared to a trend towards higher rates of sICH among stented patients, likely explained by earlier and more aggressive use of antithrombotic agents as well as the possibility of an increased risk of reperfusion injury. Similar to a previous meta-analysis,29 the order of stenting relative to thrombectomy was not associated with functional outcome in our study. There are, however, theoretical advantages to c-ICA stenting after thrombectomy, including shorter intracranial recanalization times and avoidance of potential snagging of the retrievable stent in the struts of an already deployed carotid ICA stent. Stenting of the c-ICA earlier in the procedure also subjects the patient to potential hemodynamic instability due to baroreceptor activation while cerebral perfusion is still impaired by the presence of intracranial occlusion. Furthermore, in some cases, merely traversing the c-ICA lesion with catheters to access the intracranial thrombus is sufficient to dilate the stenosis or occlusion and potentially obviate a clear indication for stenting. However, sometimes specific technical circumstances dictate that access to the intracranial circulation requires anterograde stenting.

    The current meta-analysis has limitations, the most important of which is that primarily uncontrolled observational, often retrospective, studies were included, all of which had at least a moderate risk of bias while only one small randomized trial was identified. Furthermore, older studies included may not reflect contemporary EVT techniques and may thus be less applicable to current practice. Factors that may have influenced both the decision to stent and overall outcomes, including baseline ASPECTS, type of antiplatelet agents used, and etiology of c-ICA lesions (athersclerosis vs dissection) were not systemically reported in the included series. Nevertheless, unlike previous reviews, our meta-analysis is strengthened by the inclusion of recent, large multicenter prospective cohorts and only studies that explicitly compared acute stenting with no acute stenting.

    While this large meta-analysis of observational data suggests an advantage of acute c-ICA stenting during EVT for TL patients, only randomized trials comparing acute stenting with no acute stenting will provide more definitive evidence to guide optimal management for these patients. Two forthcoming trials (TITAN (NCT03978988) and EASI-TOC (NCT04261478)) are expected to address this important clinical question.

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    Footnotes

    • Correction notice Since the online publication of this article, Figure 3 has been replaced as it was incorrectly linked to this paper and affiliation 5 was updated to remove 'Centre de documentation'.

    • Contributors GD: data acquisition, data analysis, and interpretation, and writing and revising the manuscript. BYC: data acquisition, data analysis, and interpretation. GJ: design and conceptualization of the study, data acquisition, data analysis, and interpretation, and revising the manuscript. MK: statistical analysis and data interpretation, and writing and revising the manuscript. ML: data acquisition, data analysis, and interpretation. BR: statistical analysis and interpretation. CS: design and conceptualization of the study, data acquisition, data analysis, and interpretation, and revising the manuscript. DZ: study design and data acquisition. AYP: design and conceptualization of the study, data acquisition, data analysis, and interpretation, and revising the manuscript.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial, or not-for-profit sectors.

    • Competing interests AYP is the principal investigator for a forthcoming trial of patients with tandem lesions, Endovascular Acute Stroke Intervention–Tandem OClusion study (EASI-TOC), for which he has received a networking grant from the Canadian Stroke Trials for Optimized Results (CaSTOR) initiative.

    • Patient consent for publication Not required.

    • Provenance and peer review Not commissioned; externally peer reviewed.

    • Data availability statement Data are available on reasonable requests by qualified investigators to the corresponding author.