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Mechanical Thrombectomy in Acute Ischemic Stroke: Angiographic Predictors of Outcome
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.355085
Keywords: Acute ischemic stroke, clot burden score, endovascular treatment, mechanical thrombectomy, stent retrievers, TICI
The outcome following mechanical thrombectomy (MT) depends on various clinical and imaging factors. Keeping the time to groin puncture and recanalization time to a lowest level is really challenging in resource-poor developing countries, which necessitates various workflow modifications. Computed tomography (CT) and CT angiography or magnetic resonance (MR) angiography features are important in patient selection, device selection, and prognostication. Several studies have separately evaluated angiographic features like collaterals, clot burden, recanalization, number of device passes, and the presence of intracranial atherosclerotic disease (ICAD) in predicting the outcome after MT. Clot burden and collateral status have shown their direct relationship with the recanalization and outcome.[1],[2],[3],[4] Adequate recanalization, less number of device passes, and absence of ICAD are considered indicators of a favorable outcome.[5],[6],[7] In this study, we analyzed all of these angiographic factors in patients who underwent MT in a comprehensive stroke care center.
Study design A retrospective analysis of prospectively collected data was performed for all patients who presented to our comprehensive stroke care center with acute ischemic stroke and large vessel occlusion (from October 2012 to December 2019). The institutional ethics committee approval was received. Patient selection Patients who presented with acute ischemic stroke and underwent MT for an anterior or posterior circulation large vessel occlusion were included for analysis. CT and CT angiography (CTA) was used for decision-making in all acute ischemic strokes. However, magnetic resonance imaging (MRI) was done for patients with posterior circulation strokes, stroke mimics, borderline CT Alberta Stroke Programme Early CT Score (ASPECTS) and clinico-radiological mismatch in CT. The decision for MT was primarily based on the National Institutes of Health Stroke Scale (NIHSS) score, CT/MRI ASPECTS score, site of occlusion, and consent of patients and/or their family. Patients were considered for MT if their clinical presentation was within 24 hours of the onset of ictus and ASPECTS was favorable (≥4) and a large vessel occlusion was demonstrated on CTA or MR angiography (MRA). CT perfusion was done for patients with anterior circulation stroke if their presentation was more than 6 hours of the onset of ictus, wakeup or unwitnessed stroke, and in a clinico-radiological mismatch. Intravenous recombinant tissue plasminogen activator was initiated if the ictus was less than 4.5 hours. Endovascular intervention technique Endovascular interventions were usually performed under local anesthesia or with conscious sedation, and general anesthesia was reserved only for uncooperative, obtunded, or comatose patients as in posterior circulation stroke. An 8F balloon guide catheter (BGC; Cello, Covidien, Irvine, CA, USA or Merci, Stryker Neurovascular, USA) or 6 F Neuron (Penumbra, CA, USA) in cases of posterior circulation was used as a guide catheter. MT was done either using stent retriever or contact aspiration (CA) technique. Two types of stent retrievers (Solitaire FR, ev3 Irvine, CA, USA or Trevo Proview, Stryker, CA, USA) were used for MT and the Penumbra System (Penumbra, Alameda, CA, USA) was used predominantly for CA thrombectomy. As an institutional protocol, we used stent retriever (stentriever) MT as the first-line modality. The number of attempts of the first-line modality, rescue contact aspiration depended on the discretion of the neuro interventionist after taking into consideration of the assumptive occlusion pathomechanism, the patient's clinical status, and window period. Baseline characteristics Baseline demographic, clinical (time from symptom onset), risk factor profile, stroke severity- National Institutes of Health Stroke Scale (NIHSS score), blood pressure, blood sugar at admission, baseline imaging characteristics (Alberta Stroke Program Early CT Score (ASPECTS), clot burden score (CBS),[1] collateral status, and procedural technique (device used, number of passages), procedure efficiency (thrombolysis in cerebral infarction - TICI grade)[5] and intracranial atherosclerosis (ICAD) status were analyzed. Imaging analysis was done by two neuro interventionists blinded to the outcome. Various process times like stroke onset to hospital arrival, door to needle time (hospital arrival to start of bridging therapy), door to groin puncture (hospital arrival to securing arterial access), groin puncture to recanalization (arterial access till achievement of recanalization or abandonment of procedure) were collected and analyzed. Clot burden score[1] and collateral grading were assessed from baseline CTA. The number of passes and TICI grading[5] were derived from the selective bilateral internal carotid artery (ICA) or vertebral artery angiograms following MT. For ICAD assessment, post-procedure angiograms were also used. From CTA, clot burden score was assessed using the method described by Puetz et al.[8] and Miteff[9] system was followed for collateral grading into good, moderate, and poor grades. The patient group was dichotomized with a threshold of ≥7 and ≥2b for CBS and TICI, respectively. Outcomes The primary outcome was 90-day functional independence, defined as modified Rankin Scale (mRS) score of 0–2. Other outcome measures included NIHSS score at 24 hours and symptomatic intracranial hemorrhage (sICH) as defined by ECASS II criteria.[10] Statistical analysis All analyses were performed among the patients with anterior/posterior circulation large vessel occlusion and recanalization by a mechanical device. Categorical variables were expressed as frequencies and percentages, and continuous variables as means (SD) or medians (interquartile range, IQR) for non-normal distribution. Normality of distributions was assessed graphically and by using the Shapiro–Wilk test. Baseline characteristics were described and compared according to the 90-day functional outcome mRS scale (≤2 versus >2) using the Chi-squared or Fisher's exact tests for categorical variables, and Student's t or Mann–Whitney U tests for continuous variables, as appropriate. The relation of clinical endpoint (mRS ≤2 versus >2) and its potential predictors was analyzed using binary logistic regression. The observed effects are described in terms of odds ratios and 95% confidence intervals. Statistically, null hypotheses were rejected at P values of <0.05. Variables significant at the bivariate level were included in a multivariate analysis simultaneously using the ENTER model. Statistical analyses were performed using Statistical Package for the Social Sciences (SPSS) software version 25 for Windows (SPSS, Armonk, NY, IBM Corp, USA).
A total of 163 patients with acute ischemic stroke were included in the study. Of them, 5 patients were lost during the 3-month follow-up period and 1 patient underwent only extra-cranial ICA stenting. Remaining 157 patients were included for final analysis. Demographic and clinical characteristics are detailed in [Table 1]. The median age was 60 years (IQR 51–68) and 34.4% were female. Median NIHSS score at hospital admission was 17 (IQR 12–21). Median CT/MRI ASPECTS was 6 (IQR 6–8). Of them, 56.4% of patients were known hypertensive and 40.5% were diabetic.
Intracranial T or L type of occlusion was found in 12 patients, M1 occlusion alone in 103 patients, and extra-cranial ICA with intracranial M1 tandem occlusion was observed in 12 patients. Favorable collateral grades (including good and moderate grades) were observed in 82% of patients. The mean CBS value observed was 7 (SD 1.31), lower values (<7) were detected in 47 patients. TICI score of 2b or more was attained in 126 (80%) patients. Recanalization rate of ≥2b was achieved in 48% during the first attempt of the device passage, but the recanalization had reduced to 25%, 5%, and 0.6% on 2nd, 3rd, and 4th attempts, respectively. A good functional outcome at 90 days was observed in 65 (41.4%) patients and 11 (7%) patients had symptomatic intracranial hamorrhage. Bivariate analysis [Table 2] showed age >60 years, presence of diabetes mellitus, NIHSS at admission >15, ASPECTS <6, CBS of <7, and presence of ICAD and TICI <2b were associated with poor functional outcome at 90 days. On multivariate logistic regression analysis [Table 3], CBS of <7 (odds ratio [OR] 0.32) and TICI of <2b (OR 5.51) were independent predictors of poor outcome at 90 days.
On subgroup bivariate analysis, the good outcome was observed in patients with symptom onset to arrival time below 135 minutes (P = 0.017) and time from groin puncture to recanalization below 45 minutes (P = 0.012). Of the 41 (26%) patients with ICAD, 70% showed poor outcome, poor recanalization (23%) of 2b or above. Among patients with ICAD, 53% required multiple passes for achieving recanalization.
Studies have shown that MT with appropriate case selection will improve the outcome and reduce long-term disability in acute ischemic stroke with large vessel occlusion.[11],[12] This study was aimed at the evaluation of the angiographic features which predicted outcome after MT. Clot burden score and the degree of angiographic recanalization were identified as independent predictors of outcome at 90 days. Location of the occlusive thrombus and its length have a direct positive influence on recanalization, ASPECTS, final infarct size, and neurological outcome.[1],[3] Higher rate of recanalization and good functional outcome were observed in patients with CBS of 7 or more.[3] For the CBS, threshold values of ≥7 came as an independent predictor of the final outcome in our study. There are conflicting reports about the CBS and angiographic recanalization.[13],[14] We found a relatively higher percentage of recanalization of ≥2b in patients with CBS of >7; however, this association was not statistically significant. This indicates that other factors like nature of the occluding clot, collaterals, vascular tortuosity, interaction between device, clot, and vessel wall may be also important in achieving good recanalization. Robust collateral is very important in the sustenance of penumbra for a longer period. The collateral status is mainly determined by age, comorbidities like diabetes mellitus, hypertension, ICAD status, and completeness of circle of Willis.[4],[15] In our cohort, good and intermediate collaterals were noticed in 82% and 66.4% of patients with CBS ≥7. But collaterals were not an independent predictor of a good outcome. This may be due the presence of ICAD in a significant number of patients. The latest randomized trials showed 4%–8% symptomatic hemorrhages, and it is as high as 16% in non-randomized studies.[2] The reported association of sICH and CBS[2] was not observed in this study probably due to the relatively low number (11 patients, 7%) with symptomatic intracerebral hemorrhages. As observed in all MT studies,[5],[16],[17],[18] TICI was an independent predictor of outcome in this study. Good recanalization of TICI ≥2b was achieved in 80% of the patients. Even with this good recanalization rate, relatively lesser rate (41.4%) of functional outcome was observed, possibly due to the presence of ICAD in significant number of patients. Patients with ICAD even after good recanalization had shown evidence of partial or complete re-occlusion after successful MT. Similar to other studies,[18] we observed a substantially better outcome with higher grades of recanalization of 3 compared to 2b (45.7% vs. 53.3%). The final clinical outcome following the mechanical thrombectomy is directly related to the faster and complete recanalization. Single passage of single device can lead to good outcome.[6] In some situations, multiple attempts of device passage are necessary to achieve adequate recanalization. Studies have shown that an increase in the number of passes, especially those above 4, is more associated with poor outcome.[19],[20] In nearly half of the patients (48%), recanalization of ≥2b was achieved during the first attempt itself. As the number of passes increased, there was a significant decrease in the recanalization rate (P = 0.0001). The observed recanalization rate (≥2b) was 25% for the second attempt, 5% for the third attempt, and 0.6% for the fourth attempt. Other factors like the nature of clot, arterial tortuosity, and ICAD might have influenced poor recanalization rate and increased the number of device passes. It has also been shown that the incidence of parenchymal hematoma is more when there is a higher number of passes.[21] No such association was demonstrated in our cohort. This finding is probably due to fewer number of patients (two in number) with ≥4 attempts. It's also observed that a higher number of passes (3 or more passes) was required in cases with ICAD and those with poor collaterals. Even though the recanalization rate of mechanical thrombectomy was high, it did not always translate to good outcome. Various factors have been identified as contributing to the poor outcome. Intracranial atherosclerosis is found to be one factor contributing to this poor outcome.[7] Among Asians, ICAD is one of the major causes of ischemic stroke.[22] Since the occlusion of the vessel is due to the rupture of underlying atherosclerotic plaque, mechanical removal of the clot usually leaves significant stenosis compromising antegrade blood flow. About one-third of our patients (30.5%) showed angiographic evidence of intracranial atherosclerotic disease. Involvement of anterior circulation was higher than posterior circulation. Poor outcome was observed in cases with ICAD, especially those involving the anterior circulation. Mechanical thrombectomy without angioplasty/stenting might have also contributed to this poor outcome in patients with ICAD. There is no significant correlation noted with the posterior circulation ICAD, possibly due to a lesser number of cases and relatively good collaterals in the posterior circulation. From our study, we have observed that CBS and TICI are the independent predictors of outcome at 90 days. Presence of ICAD also showed a direct positive correlation with poor outcome. The number of passes and collateral status were not predictive of the final outcome. These findings reiterate the importance of achieving complete recanalization even with multiple device passes. The relatively high incidence of ICAD in our cohort suggests the need of additional rescue treatments like angioplasty/stenting and early initiation of antiplatelet therapy to avoid re-occlusion and worse outcome.
The relatively small sample size and the use of the older generation of penumbra catheters during the initial cases are the main limitations of our study. We have used stentriever as the primary device for the mechanical thrombectomy, making the aspiration thrombectomy group relatively small in number. The prospective collection of the data, meticulous 3-month follow-up, and evaluation of all angiograms by the interventional radiologist are the strengths of our study. Financial support and sponsorship Nil. Conflicts of interest There are no conflicts of interest.
[Table 1], [Table 2], [Table 3]
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