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Ischemic Stroke
Original research
Endovascular recanalization of chronically occluded internal carotid artery
  1. Federico Cagnazzo,
  2. Pierre-Henri Lefevre,
  3. Imad Derraz,
  4. Cyril Dargazanli,
  5. Gregory Gascou,
  6. Carlos Riquelme,
  7. Raed Ahmed,
  8. Alain Bonafe,
  9. Vincent Costalat
  1. Neuroradiology Department, CHRU Gui de Chauliac, Montpellier, France
  1. Correspondence to Dr Federico Cagnazzo, Neuroradiology Department, CHRU Gui de Chauliac, Montpellier 34000, France; f.cagnazzo86{at}gmail.com

Abstract

Background It is debated whether endovascular treatment is indicated for a symptomatic chronically occluded internal carotid artery (COICA).

Objective To assess outcomes after endovascular treatment of COICA.

Methods We performed a systematic search of three databases (PRISMA guidelines), including endovascular series of COICA. Outcomes were analyzed with random-effects models.

Results We included 13 studies and 528 endovascularly treated patients with COICA. Successful recanalization was 72.6% (347/528, 95% CI 65.4% to 79.9%, I2=68.9%). Complications were 18% (88/516, 95% CI 12.1% to 23.8%, I2=65%), with 5% (25/480, 95% CI 2% to 7%, I2=0%) of permanent events, and 9% (43/516, 95% CI 6% to 13%, I2=34%) of thromboembolisms. Treatment-related mortality was 2% (11/516, 95% CI 0.5% to 2.6%, I2=0%). Shorter duration of the occlusion was associated with higher recanalization: 80% (11/516, 95% CI 54% to 89%, I2=0%), 63% (33/52, 95% CI 49% to 76%, I2=0%), and 51% (18/35, 95% CI to 37% to 88%, I2=40%) recanalization rates for 1, 3, and >3 months occlusions, respectively. Complications were 6% (3/50, 95% CI 3% to 21%, I2=0%), 14% (4/27, 95% CI 5% to 26%, I2=0%), and 25% (13/47, 95% CI 10% to 30%, I2=0%) for 1, 3, and >3 months occlusions, respectively. Patient aged <70 years presented higher revascularization rates (OR=3.1, 95% CI 1.2 to 10, I2=0%, p=0.05). Successful reperfusion was higher (OR=5.7, 95% CI 1.2 to 26, I2=60%, p=0.02) and complications were lower (OR=0.2, 95% CI 0.6 to 0.8, I2=0%, p=0.03) for lesions limited to the cervical internal carotid artery compared with the petrocavernous segment. Successful recanalization significantly lowered the rate of thromboembolisms (OR=0.2, 95% CI 0.8 to 0.6, I2=0%, p=0.01) and mortality (OR=0.5, 95% CI 0.1 to 0.9, I2=0%, p=0.04), compared with conservative treatment.

Conclusions Endovascular treatment of COICA gives a 70% rate of successful recanalization, with 5% morbidity. Patients aged <70 years, lesions limited to the cervical internal carotid artery, and a shorter duration of the occlusion decreased the risk of complications. Successful recanalization of symptomatic lesions lowered by about 80% the likelihood of thromboembolisms, compared with medical management.

  • dissection
  • stenosis
  • stent
  • stroke

https://doi.org/10.1136/neurintsurg-2019-015701

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    Introduction

    Natural history and optimal management of a chronically occluded internal carotid artery (COICA) continue to be debated. Despite studies in the literature, which reported a rate of recurrent stroke of between 5% and 6% per year,1 evidence that treatment may reduce the ischemic risk compared with the medical management is lacking.2 Treatment of these lesions is difficult, as both carotid endarterectomy and extracranial/intracranial bypass have been shown to have a limited benefit in symptomatic patients.3 Recently, endovascular recanalization of a COICA has been proposed and has been associated with heterogeneous rates of technical success and neurological improvement.4 However, whether endovascular treatment should be evaluated for selected symptomatic patients with a COICA is undetermined, because the related success rate and complications have not been well investigated. This study is a large systematic review and meta-analysis of the literature, reporting technical and clinical outcomes related to the endovascular treatment of a COICA. Our aim was to define if endovascular revascularization of a COICA is safe and effective, and if selected patients may benefit from endovascular treatment when medical therapy has failed to prevent symptomatic ischemic events.

    Materials and methods

    Literature search

    A comprehensive literature search of PubMed, Ovid EMBASE, and SCOPUS was performed for studies published between January, 1990 and November, 2019. PRISMA guidelines (Preferred Reporting Items for Systematic Reviews and Meta-Analyses)5 were followed. The key words and the search strategy are reported in online supplementary table 1. Studies included in our review are described in online supplementary table 2. COICA was defined as a 100% cross-sectional stenosis of the vessel lumen as documented on CT angiography, MR angiography, and confirmed by DSA. Chronicity was defined as ≥1 month of known occlusion of the cervical internal carotid artery (ICA) documented on imaging studies.4 The inclusion criteria were the following: (1) studies reporting series of patients with COICA who underwent endovascular carotid recanalization; and (2) studies comparing the outcome between endovascular treatment versus medical treatment. Exclusion criteria were the following: (1) case reports; (2) review articles; (3) studies published in languages other than English; (4) in vitro and/or animal studies; (5) studies reporting patients with COICA treated with surgical or hybrid (surgical and endovascular) approaches; and (6) acute carotid artery occlusions. When patient populations overlapped, the series with the largest number of patients or most detailed data was selected. Eligibility for inclusion was determined by two independent readers, while a third author resolving discrepancies.

    Data collection

    The following data were extracted: (1) rate of successful recanalization of the ICA; (2) rate of carotid reocclusion or sever stenosis during follow-up; and (3) treatment-related complications and clinical outcomes. The rate of successful recanalization and complications was analyzed based on the patient age (<70 years vs ≥70 years), and on the duration of the occlusion (30 days vs 30–90 days vs >90 days). When reported in the study, the occlusion period was, in general, defined as the time between the radiologically confirmed ICA occlusion date and treatment. In addition, outcomes were analyzed based on the type of ICA occlusion classified as limited to the cervical ICA, and occlusion of the cervical and intracranial ICA (up to the petrocavernous segments).6 7 Complications were also compared between successfully recanalized ICA versus failed recanalization, and successfully recanalized ICA versus medical management.

    Outcomes

    The primary objective of this study was to analyze the safety (complication rate) and the efficacy (recanalization rate) of the endovascular treatment of COICA. The secondary objectives were to define the effect of age, and duration and type of occlusion on the studied outcomes, as well as the impact of successful recanalization compared with medical treatment or unsuccessful revascularization.

    Quality scoring

    The Newcastle-Ottawa Scale8 was used the quality assessment of the included studies (online supplementary table 3). The quality assessment was performed by two authors independently, and a third author resolved discrepancies.

    Statistical analysis

    We estimated, from each cohort, the cumulative prevalence (percentage) and 95% CI for each outcome. Heterogeneity of the data was assessed by the Higgins index (I2 and, subsequently, the DerSimonian and Laird random-effects model was applied. The graphical representation was provided by a forest plot. To evaluate the heterogeneity and bias, a subgroup analysis and funnel plot, followed by Egger’s linear regression test, were performed, respectively. Meta-regression was used to test the relationship between the period of the intervention (expressed in years) and the outcomes. Results were analyzed by meta-analysis of proportion (prevalence) or odds ratio meta-analysis (odds ratio), when appropriate. Statistical significance was set at p<0.05. Meta-analysis was performed with ProMeta-2 (Internovi-Cesena-Italy) and OpenMeta (Analyst).

    Results

    Literature review and quality of studies

    Studies included in our meta-analysis are summarized in (online supplementary figure 1) . The search flow diagram is shown in figure 1.

    Figure 1
    Figure 1

    (A,B) Forest plots with random-effects model demonstrating the overall rate of complication (A) and the rate of successful recanalization (B) after endovascular treatment of chronically occluded internal carotid artery. COICA, chronicallyoccluded internal carotid artery.

    A total of 13 studies and 528 patients with COICA, treated with an endovascular approach, were included in our meta-analysis.

    Eleven studies were retrospective series,6 7 9–17 one study had a prospective design,18 and one was done from a prospective registry.4 Overall, 10 articles4 7 9 10 12–16 18 were rated as high-quality studies based on the Newcastle-Ottawa quality assessment criteria (online supplementary table 3). Seven studies (54%) clearly stated that their series represented consecutive cases of endovascularly treated COICA, including failed attempts.

    Patient population

    Mean age, sex, and vascular risk factors are reported in online supplementary table 4.

    Most commonly, patients presented motor deficits due to ischemic events (63%), followed by aphasia (15.6%), and cognitive impairment related to cerebral hypoperfusion (11%). Cranial nerve palsy (4.6%) and amaurosis (5.5%) were less common presenting symptoms.

    Indication for endovascular treatment of COICA, when specified by the authors, was done for symptomatic patients after failure of medical management.

    The mean radiological and clinical follow-up were 14.4 months (median 12, IQR 10–19), and 17 months (median 14, IQR 12–23), respectively.

    Technical and clinical outcomes after endovascular revascularization of COICA

    Proportion meta-analysis

    The investigated outcomes were analyzed by a random-effects meta-analysis because this model incorporates heterogeneity among studies. Overall, the rate of successful ICA recanalization was 72.6% (347/528, 95% CI 65.4% to 79.9%, I2=68.9%) (table 1 and figure 1). The funnel plot, followed by Egger’s linear regression test, reasonably excluded publication bias (p=0.5) (online supplementary figure 2A). Meta-regression showed a non-significant variation of the effect size (p=0.09) over the investigated period (online supplementary figure 2B).

    View this table:
    Table 1

    Outcomes after endovascular treatment of chronically occluded internal carotid artery (COICA)

    During a mean radiological follow-up of 5 months (median 3.5, IQR 2–8), 13% (26/205, 95% CI 4% to 21%, I2=62%) of the treated ICA presented a sever stenosis or reocclusion. The percentage of patients requiring a second treatment after diagnosis of severe stenosis/reocclusion was not reported in the available literature.

    The overall rate of complications was 18% (88/516, 95% CI 12.1% to 23.8%, I2=65%), with 12% (63/480, 95% CI 5% to 15%, I2=61%) and 5% (25/480, 95% CI 2% to 7%, I2=0%) of transient and permanent events. The Egger linear regression test excluded publication bias (p=0.6) (online supplementary figure 3A)(online supplementary figure 2A). Meta-regression showed a non-significant variation of the effect size (p=0.2) over the investigated period ((online supplementary figure 3B)).

    Periprocedural/early complications (within 30 days from treatment) were more common (12.6% (65/516, 95% CI 5% to 15%, I2=66%) than delayed adverse events (after 30 days) (23/516=4.5%, 95% CI 1% to 5.6%, I2=38%). Most of the complications were ischemic events (43/516=9%, 95% CI 6% to 13%, I2=34%), whereas hemorrhagic events (cerebral hematoma) were 5% (26/516, 95% CI 2% to 8%, I2=0%). Carotid cavernous fistula, carotid pseudoaneurysm, bradycardia during angioplasty, and hyperperfusion syndrome represented less than 1% of the adverse events, respectively.

    Treatment-related mortality was 2% (11/516, 95% CI 0.5% to 2.6%, I2=0%). The rate of good outcome (defined as modified Rankin Scale score 0–2 or improved neurological status after revascularization) during the clinical follow-up was 87% (69/89, 95% CI 71% to 89%, I2=35%).

    Influence of the duration of the occlusion

    Successful recanalization was higher among cases with 1 month of known occlusion (11/516=80%, 95% CI 54% to 89%, I2=0%), compared with 3 months (33/52=63%, 95% CI 49% to 76%, I2=0%), and more than 3 months occlusion (18/35=51%, 95% CI 37% to 88%, I2=40%). Contrariwise, complications were proportional to the duration of the occlusion: 6% (3/50, 95% CI 3% to 21%, I2=0%), 14% (4/27, 95% CI 5% to 26%, I2=0%), and 25% (13/47, 95% CI 10% to 30%, I2=0%) for 1 month, 3 months, and more than 3 months' duration of the occlusion, respectively (table 2).

    View this table:
    Table 2

    Treatment-related outcomes analyzed by subgroups of age, type, and duration of the occlusion

    Odds ratio meta-analysis

    Patients aged <70 years presented a higher rate of successful revascularization (OR=3.1, 95% CI 1.2 to 10, I2=0%, p=0.05), compared with ≥70 years. Complications were not significantly different between <70 and ≥70 year-old patients (OR=1.8, 95% CI 0.7 to 8.1, I2=0%, p=0.2) (table 2).

    Successful recanalization was higher (OR=5.7, 95% CI 1.2 to 26, I2=60%, p=0.02), and the complication rate was lower (OR=0.2, 95% CI 0.6 to 0.8, I2=0%, p=0.03) after treatment of occlusions limited to the cervical ICA, compared with lesions involving the intracranial (petrocavernous segments) portion.

    Impact of the successful revascularization

    The likelihood of ischemic complications (OR=0.2, 95% CI 0.8 to 0.6, I2=0%, p=0.01) and mortality (OR=0.5, 95% CI 0.1 to 0.9, I2=0%, p=0.04) were significantly lower when successful revascularization of a COICA was achieved, compared with conservative treatment (best medical management).

    Perioperative and early complications were significantly higher in cases of endovascular treatment with failed reperfusion (vs successful reperfusion) (OR=3.3, 95% CI 1.3 to 8.5, I2=7%, p=0.01). Delayed adverse events were not significantly different between successful and unsuccessful recanalization (OR=2, 95% CI 1.1 to 4.3, I2=0%, p=0.07). Finally, mortality was lower for successful carotid artery reperfusion (OR=0.4, 95% CI 0.1 to 0.9, I2=0%, p=0.04) (table 3).

    View this table:
    Table 3

    Subgroup analysis of treatment-related outcomes comparing successfully revascularized chronically occluded internal carotid artery versus medical treatment, and successful versus unsuccessful recanalization

    Heterogeneity

    Heterogeneity was moderately raised for the overall rate of successful ICA recanalization and the overall rate of complications, as well as for the incidence of sever stenosis or reocclusion during follow-up. All other outcomes from subgroup analysis showed a low heterogeneity.

    Discussion

    Pooling 13 studies with more than 500 patients, our meta-analysis provides important insights into endovascular management of COICA. Revascularization appeared technically feasible with a rate of success close to 70%. Endovascular successful reperfusion gave 80% reduction of ischemic events in comparison with conservative treatment, whereas failed recanalization presented a likelihood of new ischemic events three times higher than successful reperfusion. However, age (≥70 years), occlusions older than 3 months, and lesions extended to the intracranial ICA were important prognosticators of treatment failure. Nevertheless, despite the technical feasibility, an 18% rate of complications was not negligible, although most were transient ischemic events.

    Angiographic and clinical outcomes

    In our review, successful revascularization of COICA ranged between 58% and 91%, depicting heterogeneous angiographic outcomes among studies (figure 1). This variability is probably multifactorial. First, it is important to consider that the reported recanalization rate in a single center retrospective and uncontrolled series may exclude limited attempts, overestimating the real successful rate. In addition, endovascular revascularization techniques for COICA are different and not standardized. In a recent technical note, Cagnazzo et al 19 described the reconstruction of a chronic occlusion of the ICA among five patients deploying balloon-mounted stents (coronary stents) in a telescopic fashion into the distal segment (petrocavernous), and Xact stents for the cervical part, under a flow reversal technique, inflating a 9 F balloon catheter at the common carotid artery. The authors gently dissected the occluded carotid with a 0.014" microwire, checking the lumen by microcatheter injections. Shojima et al 14 reported eight cases of COICA treated with angioplasty and a self-expanding Wallstent (Boston Scientific) or Precise (Cordis) under proximal (inflation of two balloons at the common and external carotid artery) and distal protection (filter), using intravascular sonography to confirm that the guide wire was in the true lumen.

    However, the characteristics of the occlusion are probably the first factor influencing the feasibility of the revascularization. Compared with occlusions involving the petrocavernous segment, we showed that successful reperfusion was five times higher if the lesion was limited to the cervical ICA (table 2). In addition, cervical occlusions presented an odds of complication 80% lower than those of distal occlusions. Hasan et al 7 identified four types of radiographic COICA, reported as the ICA with occlusion involving the cavernous or supraclinoid portions, presenting 25% cases of successful recanalization and 25% cases of complications, compared with an 80% success rate and 15% of complications of more proximal lesions. Similarly, Lee et11 reported a 52% success rate and 22% of adverse events for chronic occlusion at (or distal to) the clinoid segment, and an 89% success without major complications for occlusions proximal to the clinoid portion.

    However, it is important to point out that etiology may play an important role in the successful treatment of COICA. Owing to the scant published data, we were unable to analyze outcomes in relation to etiology. Nevertheless, it has been reported that, among younger patients, occlusion is often due to chronic dissection of the ICA, whereas in older subjects, the occlusion is often caused by atherosclerosis, with harder or calcified plaques presenting difficulties for recanalization.20

    We found that a longer duration of the occlusion was associated with a lower probability of achieving recanalization: technical success decreased from 80% to 50% when the duration of the occlusion was 30 days and >3 months, respectively. A reflection of the technical difficulties during revascularization of older ICA occlusions is also the higher rate of complications (almost four times higher) for occlusions older than 3 months. Namba et al 13 reported 11 patients with COICA treated endovascularly: difficulties during wire advancement and successful revascularization were 50% and 65% for occlusions >3 months, compared with 16% for occlusions with a duration of 1 month. In a recent series of 36 patients with COICA,9 complications after endovascular treatment were 24% among the group of patients with a mean duration of the occlusion of 5 months, while no adverse events were reported among patients with a duration of the occlusion of ≤1 month.

    Finally, age <70 years appeared to be a predictor of technical success, increasing the likelihood of revascularization three times compared with older patients. This is probably related to a more complex and tortuous anatomy of the supra-aortic trunks among older patients, potentially increasing the technical difficulties of the procedure.

    Outcomes after successful revascularization

    The risk of stroke from a COICA is reported to be close to 7% a year, despite the best medical management.2 This risk may be as high as 12% a year if perfusion imaging shows that flow to the brain is compromised.21 22 Persoon et al,23 in a randomized pilot study, showed that patients with a symptomatic ICA occlusion and compromised cerebral perfusion had a trend toward significant increase in cerebral blood flow after intervention, compared with medical management.

    In a retrospective series, improvement of hypoperfusion after endovascular treatment of COICA is reported to be between 70% and 100%.4 18 19

    Nowadays, the natural history of an occluded ICA is still not completely understood, and indication for treatment should be defined.1 The extracranial–intracranial bypass surgery trial, despite being associated with initial improvement of the National Institutes of Health Stroke Scale scores, failed to demonstrate a reduction of the ischemic stroke rate, largely owing to the increased risk of periprocedural neurological events among patients who underwent surgery compared with those given medical therapy.3

    Our meta-analysis, although derived from a retrospective series, showed that ischemic complications and mortality decreased by about 80% (OR=0.2, 95% CI 0.8 to 0.6, p=0.01) and 50% (OR=0.5, 95% CI 0.1 to 0.9, p=0.04) among symptomatic patients having endovascular treatment with successful recanalization, compared with medical management. It is likely that revascularization via an endovascular approach leads to improvement of the cerebral hypoperfusion due to the full anatomical restoration of blood flow to all ICA branches.4 Accordingly, recent series have also shown improvement of cognitive function after stenting COICA as measured with different neurocognitive scales.4 24

    In addition, it is interesting to underline that failed recanalization increased the risk of periprocedural ischemic events by three times (OR=3.3, 95% CI 1.3 to 8.5, p=0.01) in comparison with successful reperfusion.

    Limitations

    Our study has some limitations. First, available studies were retrospective series, and most of the data was derived from studies without control groups. Indication for endovascular treatment and the techniques used were not standardized: accordingly, the analyzed outcomes were heterogeneous.

    Data for antiplatelet treatment before and after stenting were not always available. The etiology was not investigated. A definition of the duration of the occlusion was inconstantly reported among the analyzed series. Accordingly, because most of the studies presented a retrospective deign, the occlusion period may be underestimated or overestimated in this meta-analysis.

    However, publication bias was reasonably excluded from this meta-analysis, and our study is the largest to date investigating the treatment-related outcomes of endovascular recanalization of COICA.

    Conclusions

    Knowledge on the appropriate treatment and management of COICA is still limited. Our meta-analysis emphasized that endovascular treatment of these lesions is feasible, with a 70% rate of successful recanalization. The procedure is technically demanding, with a morbidity rate close to 5%. Symptomatic patients requiring revascularization should be carefully selected. Age <70 years, lesions limited to the cervical ICA, and a shorter duration of the occlusion potentially decreased the risk of complications. Finally, successful recanalization lowered the likelihood of ischemic events by about 80% in comparison with medical management alone or failed reperfusion.

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    Supplementary materials

    Footnotes

    • Contributors Substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data for the work: FC, P-HL, CD, ID, GG, CR, RA, AB, VC. Drafting the work or revising it critically for important intellectual content: FC, P-HL, VC. Final approval of the version to be published: FC, P-HL, CD, ID, RA, GG, CR, AB, VC. Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: FC, P-HL, CD, ID, GG, RA, CR, AB, VC.

    • 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 None declared.

    • Patient consent for publication Not required.

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

    • Data availability statement Data sharing not applicable as no datasets generated and/or analysed for this study. Data from a meta-analysis of the literature.